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| [[file:Mark_Hill.jpg|90px|left]] This 1949 third edition textbook by McEwen describes embryonic development.
<br><br>
[https://archive.org/details/06031200R.nlm.nih.gov/page/n3 1923 Edition]
<br><br>
'''Modern Notes:''' [[Historic Textbooks]]
 
 
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{{Historic Disclaimer}}
{{Historic Disclaimer}}
=Vertebrate Embryology=
=Vertebrate Embryology=


Robert S. Mcewen
Robert S. McEwen


Professor Emeritus of Zoology, Oberlin College
Professor Emeritus of Zoology, Oberlin College
==Contents==
[[Book - Vertebrate Embryology (1949) 1|Part I The Germ Cells and Early Development of Amphioxus]]
* 1. Introduction
* 2. Fertilization and Early Stages in Development
* The Early Development of Amphioxus
[[Book - Vertebrate Embryology (1949) 2|Part II The Development of the Frog]]
* The Frog: from the Production of the Germ Cells through Gastrulation
* The Frog: Early or Embryonic Development Subsequent to Gastrulation
* The Frog: Later or Larval Development
[[Book - Vertebrate Embryology (1949) 3|Part III The Teleosts and Gymnophiona]]
* The Teleosts and Gymnophiona: their Segmentation and Gastrulation
[[Book - Vertebrate Embryology (1949) 3|Part IV The Development of the Chick]]
* The Chick: the Adult Reproductive Organs, and the Development of the Egg Previous to Gastrulation
* Gastrulation and Development through the First Day of Incubation
* The Chick: Development during the Second Day of Incubation
* The Chick: Development during the Third Day of Incubation
* The Chick: Development during the Fourth Day of Incubation
* The Chick: Development during the Fifth and Subsequent Days
[[Book - Vertebrate Embryology (1949) 3|Part V The Development of the Mammal]]
* The Early Development of the Mammal and its Embryonic Appenclages
* Development of the Pig to the Ten Millimeter Stage
* The Later Development of the Pig
* The Skeleton, Teeth, Hair, Hoofs and Horns
Index


==Preface to the Fourth Edition==
==Preface to the Fourth Edition==
Line 21: Line 65:


==Preface to the First Edition==
==Preface to the First Edition==
This book is designed as an introductory text in Vertebrate Embryology, a work which seems to be justified on the following grounds: The older texts upon this subject, though in many cases excellent, do not cover exactly the field which is now covered in many colleges; these texts, moreover, are becoming somewhat out of date in various details. Among the newer books the best ones tend to do one of two things. Either, in the interest of thoroughness, they confine their attention entirely tn one form, e.g., the Chick, or else, for the sake of a broader viewpoint, they deal with a considerable number of animals, but in doing so touch only upon the earlier developmental stages of each. Now it is obvious that there is great value for the student, both in the accuracy gained by the careful intensive study of a single type, and also in the possession of less detailed knowledge of the history of other forms which are nearly related to it. Hence, what has seemed to be needed was a book which would, so far as is possible, make available both these advantages. To meet this need, the major part of the present text comprises a mo-,leratcl}‘ complete account of the development of two typical forms. i.e., the Frog and the Chick, each of which, in the writer’s opinion, has special features which justify such treatment. These relatively detailed discussions are then supplemented by chapters which present brief comparisons, not only with the Mammal, but also with certain other significant members of the Vertebrate group. Furthermore, the essentially embryological portion of the book is preceded by an optional introductory chapter dealing with the elements of cytology. Upon this basis the effort throughout the work has been to produce something adapted to the requirements of the general student of Zoology. us well as to the individual particularly interested in premedical preparation.


This book is designed as an introductory text in Vertebrate Embryology, :1 work which seems to be justified on the following grounds:
The older texts upon this subject, though in many cases excellent, do
not cover exactly the field which is now covered in many colleges;
these texts, moreover, are becoming somewhat out of date in various details. Among the newer books the best ones tend to do one of two things.
Either, in the interest of thoroughness, they confine their attention entirely tn one form, e.g., the Chick, or else, for the sake of a broader
viewpoint, they deal with a considerable number of animals, but in doing so touch only upon the earlier developmental stages of each. Now
it is obvious that there is great value for the student, both in the accuracy gained by the careful intensive study of a single type, and also in
the possession of less detailed knowledge of the history of other forms
which are nearly related to it. Hence, what has seemed to be needed was
a book which would, so far as is possible, make available both these advantages. To meet this need, the major part of the present text comprises a mo-,leratcl}‘ complete account of the development of two typical
forms. i.c., the Frog and the Chick, each of which, in the writer’s opinion, has special features which justify such treatment. These relatively
detailed discussions are then supplemented by chapters which present
brief comparisons, not only with the Mammal, but also with certain
other significant members of the Vertebrate group. Furthermore, the
essentially embryological portion of the book is preceded by an optional introductory chapter dealing with the elements of cytology. Upon
this basis the effort throughout the work has been to produce something
(‘Sf)t‘t',i£1ll_\‘ adapted to the requirements of the general student of Zoolog}. us well as to the individual particularly interested in premedical
preparation.
As i'crgzvx'tls certain details concerning the method of handling the
topics involved, the following remains to be said. Because of the character of the book, the chapter upon cytology places special emphasis
upon the structure, development, and function of the germ cells, with
particular reference to nuclear phenomena and their genetic significance. The strictly cnibryological subject tn:-ttter is then introduced by
a short general discussion of the more lundaixiierxtal and universal proc of Vertebrate development from the comparative standpoint. This
includes a description of the various types of segmentation, gastrulation, and the formation of the rudiments of the nervous system and the
V“
viii PREFACE TO THE FIRST EDITION


main mesodermal structures. Following these introductory chapters,
As i'crgzvx'tls certain details concerning the method of handling the topics involved, the following remains to be said. Because of the character of the book, the chapter upon cytology places special emphasis upon the structure, development, and function of the germ cells, with particular reference to nuclear phenomena and their genetic significance. The strictly cnibryological subject tn:-ttter is then introduced by a short general discussion of the more lundaixiierxtal and universal proc of Vertebrate development from the comparative standpoint. This includes a description of the various types of segmentation, gastrulation, and the formation of the rudiments of the nervous system and the main mesodermal structures. Following these introductory chapters,


‘Amphioxus is the first particular type to be considered lI(’('£lUSt‘. of the
‘Amphioxus is the first particular type to be considered lI(’('£lUSt‘. of the


relatively primitive character of most of its early history. The later development of this animal, i.e,, that following the fnrnizuion of the mt'.s'ndermal somites. is, however, quite highly S])tT‘(‘l3li’!.t‘4‘l in I‘{‘sper_'l.~' uhi:-li
relatively primitive character of most of its early history. The later development of this animal, i.e,, that following the fnrnizuion of the mt'.s'ndermal somites. is, however, quite highly distinguish it from the vast majority of Clionlates are without great significance for the general student. tliey are mniuml.
distinguish it from the vast majority of Clionlates. .-\s tlwsu lzltcr .<ta;.u-.~
are without great significance for the general student. tliey are mniuml.


The Frog, as suggested above, is one of the two forms which have
The Frog, as suggested above, is one of the two forms which have been treated at some length. The reasons for suvli extencled mnsirl<~ration in this instance and in that of the Chick are presunmbly olwious to every Zoiilogist. For the sake of the student. however. the uzlim uf these animals as subjects of enibryologitral study is lt\[llt‘txil,’il in tinparagraphs of the text which introduce them. ln the case ui lhv "I":-u;_». its early history has been presented under the head of c-ertuin fairly. well recognized stages which lend themselves well to corre-l;1tion with work in the laboratory. In further pursuance of this method the-. internal changes have been noted in alternation with those or-currin;__r cxtc-rnall_\ . This was done in order that the reader might obtain. so far as pm-s_<il»le. a correct idea of the really simultaneous character of tliese processes. It did not seem feasible, however, in a work of this St'(}pt.' to continue this plan throughout the entire course of development in this animal. The later external changes. therefore, are included under one lieading. while the more advanced details of organogeny are described in terms of particular systems.
been treated at some length. The reasons for suvli extencled mnsirl<~ration in this instance and in that of the Chick are presunmbly olwious
to every Zoiilogist. For the sake of the student. however. the uzlim uf
these animals as subjects of enibryologitral study is lt\[llt‘txil,’il in tinparagraphs of the text which introduce them. ln the case ui lhv "I":-u;_».
its early history has been presented under the head of c-ertuin fairly.
well recognized stages which lend themselves well to corre-l;1tion with
work in the laboratory. In further pursuance of this method the-. internal
changes have been noted in alternation with those or-currin;__r cxtc-rnall_\ .
This was done in order that the reader might obtain. so far as pm-s_<il»le.
a correct idea of the really simultaneous character of tliese processes.
It did not seem feasible, however, in a work of this St'(}pt.' to continue
this plan throughout the entire course of development in this animal.
The later external changes. therefore, are included under one lieading.
while the more advanced details of organogeny are described in terms
of particular systems.


Following the treatment of the Frog, there has been introduced a very
Following the treatment of the Frog, there has been introduced a very brief account of segmentation and gastrulation in the Teleosts and the Gymnophiona. This has been done despite the realization that in the case of the latter group laboratory consideration will in most cziscs be impossible. The reason for this is the authors opinion that segnu-xi1;+ tion and gastrulation in these two classes of animals are extrem:-ly valuable in assisting the student to relate these processes in the Frog In those which he is about to study in the Bird. Experience, xnoremm‘, has seemed to indicate that the relation of avian and mammalian gztstrulzb tion to that in more primitive forms is always particularly clillicult for
brief account of segmentation and gastrulation in the Teleosts and the
Gymnophiona. This has been done despite the realization that in the
case of the latter group laboratory consideration will in most cziscs be
impossible. The reason for this is the authors opinion that segnu-xi1;+
tion and gastrulation in these two classes of animals are extrem:-ly
valuable in assisting the student to relate these processes in the Frog In
those which he is about to study in the Bird. Experience, xnoremm‘, has
seemed to indicate that the relation of avian and mammalian gztstrulzb
tion to that in more primitive forms is always particularly clillicult for


i the beginner to grasp, and it is believed, therefore. that any legitinmte
i the beginner to grasp, and it is believed, therefore. that any legitinmte aid to this end is worth while.


aid to this end is worth while.
In treating the early stages of the Chick a good deal of stress has been placed upon the method of segmentation and gastrulation. The latter especially has been emphasized because of its peculiar character, and the desirability of making clear its relationship to that in the forms already studied. The later history of this animal is then presented in daily periods, according to the well-known plan of Foster and Balfour. This has been done because it seems to the writer that at least in a beginning course, this method has certain marked advantages over that of stuclying the complete embryology of one system at a time. In the first place the Bird lends itself particularly well to treatment by periods, and secondly, the simultaneous development of all the systems is what is actually seen to occur in any animal. This latter fact it would seem well to impress upon the student when possible by the method of presentation. Finally it has appeared not only possible but easier to conduct the class work in correlation with the laboratory when development is studied by periods rather than by systems. It should be noted, nevertheless, that in this book the material has been so arranged that the student can readily follow through the complete growth of any one system if the instructor so desires.


In treating the early stages of the Chick a good deal of stress has
As regards the Mamxnals, it is felt that the detailed differences between the organogeny of this group and that of the Birds are not, on the. whole, of great general biological significance. Of very considerable significance, however, are those unique characteristics of both mother and embryo connected with mammalian gestation. For this reason the discussion in this portion of the text is confined chiefly to the earlier developinental stages, which are treated largely from the comparative standpoint. The subject is introduced by a description of the structure and functions of the adult reproduetige organs in the,same manner as in the case of preceding forms. This involves the process of ovulation, and in that connection it has seemed worth while to describe briefly the peculiar cyclic phenomena which accompany this process in the mammalian female. Following this, the comparative idea is pursued with particular reference to the development of the extra-embryonic z1ppt’ll(l£lgC.‘.‘~. This is believed to be especially important from an evolutionary viewpoint because it shows how these appendages, already observed in the Chick. have been modified in the various Mammals. This discussion is naturally accompanied by a description of the structure and probable evolution of the placenta. For the general plan of treatmom of these latter topics the author frankly acknowledges his indebtedness to Professor Jenl<inson’s excellent book, Vertebrate Embryology.
been placed upon the method of segmentation and gastrulation. The
latter especially has been emphasized because of its peculiar character,
and the desirability of making clear its relationship to that in the forms
PREFACE TO THE FIRST EDITION


already studied. The later history of this animal is then presented in
Concerning bibliographical material, references to the more important literature of each subject are appended to the chapter which concludes consideration of the topic in question. As intimated, it will be quite obvious that these references make no pretense of being exhaustive. Their object is rather merely to point the way to further study for the reader who desires it. This is done, first, because the present volume is intended primarily as a text rather than as a book of reference, and, secondly, because it is felt that the beginner’s interest may be more effectively aroused in this manner than by presenting to him at once every reference available. The latter, if desired, can be readily obtained in the more advanced books which are cited.
daily periods, according to the well-known plan of Foster and Balfour.
This has been done because it seems to the writer that at least in a beginning course, this method has certain marked advantages over that of
stuclying the complete embryology of one system at a time. In the first
place the Bird lends itself particularly well to treatment by periods,
and secondly, the simultaneous development of all the systems is what
is actually seen to occur in any animal. This latter fact it would seem
well to impress upon the student when possible by the method of presentation. Finally it has appeared not only possible but easier to conduct the class work in correlation with the laboratory when development is studied by periods rather than by systems. It should be noted,
nevertheless, that in this book the material has been so arranged that
the student can readily follow through the complete growth of any one
system if the instructor so desires.


As regards the Mamxnals, it is felt that the detailed differences between the organogeny of this group and that of the Birds are not, on
It is recognized that illustrations constitute an extremely important feature in a text of this character, and the writer has spared no pains in the attempt to make the figures adequate both in number and quality. It will be evident, however, that the majority of them are not original. This is due to the fact that through the kindness of the authors and publishers indicated below, there were made available a large number of excellent illustrations, which it seemed hardly worth while to attempt to improve upon. Nevertheless, in every instance where it was felt that such improvement was possible, or where it appeared that a new figure would be profitable, original drawings have been inserted. Lastly. it remains to be. stated in this connection that in the case of all borrowed illustrations, great care has been taken to have the illustration and the terms used in its legend agree with the respective description and terminology in the text. The desirability of this, especially in an clexnemarj.' book, is obvious; yet, according to the writer’s observation, it is a feature which is too frequently overlooked.
the. whole, of great general biological significance. Of very considerable
significance, however, are those unique characteristics of both mother
and embryo connected with mammalian gestation. For this reason the
discussion in this portion of the text is confined chiefly to the earlier
developinental stages, which are treated largely from the comparative
standpoint. The subject is introduced by a description of the structure
and functions of the adult reproduetige organs in the,same manner as
in the case of preceding forms. This involves the process of ovulation,
and in that connection it has seemed worth while to describe briefly
the peculiar cyclic phenomena which accompany this process in the
mammalian female. Following this, the comparative idea is pursued
with particular reference to the development of the extra-embryonic
z1ppt’ll(l£lgC.‘.‘~. This is believed to be especially important from an evolutionary viewpoint because it shows how these appendages, already observed in the Chick. have been modified in the various Mammals. This
discussion is naturally accompanied by a description of the structure
and probable evolution of the placenta. For the general plan of treatmom of these latter topics the author frankly acknowledges his indebtedness to Professor Jenl<inson’s excellent book, Vertebrate Embryology.


Concerning bibliographical material, references to the more important literature of each subject are appended to the chapter which concludes consideration of the topic in question. As intimated, it will be
In conclusion I desire to express my appreciation of the following favors. To Professor Frank R. Eillie and to Henry Holt and Co., I am indebted for their generous permission to use a large number of figures from Lillie’s Development of the Chick; to Professor T. H. Morgan. his co-authors, arid Henry Holt and Co., for certain illustrations from The Mechanism of Memlelian Heredity; to Henry Holt and Co., for numerous figures from Kellicott’s General Embryology and Chordate Development; and to the Delegates and Secretary of the Clarendon Press for a like favor as regards .lenkinson’s Vertebrate Embryology. It is also a pleasure to acknowledge a similar debt to Professor Morgan and The Columbia University Press fr;-2' figures from Heredity and Sex: to Professor J. Playfair McMurrich and P. Blakiston’s Son and Co. for cliches from McMurrich’s Development of the Human Body‘; to P. Blalcistozfs Son and Co. for further clichés from Minot’s Laboratory Text Book of Embryology; to Messrs. Longmans, Green and Co. for cliches from Quain’s Anatomy; to Messrs. G. P. Putnam and Co., for permission to use again certain figures from Marshall’s Vertebrate Embryology, copied and slightly modified by Kellicott; and to Professor 0. Van der Stricht and Dr. T. W. Todd for allowing the use of photomicrographs made in the Anatomical Department of Western Reserve University Medical School from preparations presented to that department by Professor Van der Stricht. In all cases the illustrations thus borrowed are acknowledged in the legends of the figures concerned.
quite obvious that these references make no pretense of being exhaus
IX
x _ PREFACE TO THE FIRST EDITION


tive. Their object is rather merely to point the way to further study for
I wish further to express particular gratitude to Professor T. H. Morgan for reading and criticizing the first half of the manuscript; to Professor J. H. McCregor for performing a similar service for the entire hook; to Professor M. M. Metcalf for suggestions regarding the earlier chapters: to my wife for assistance with the proof; and to Pro.fessor R. C. llarrison for the identification of the frog larvae used in niaking certain of my original drawings. Especial gratitude is also felt for the constant interest and helpfulness shown by my colleagues, Professors R. A. Budington and C. G. Rogers.
the reader who desires it. This is done, first, because the present volume is intended primarily as a text rather than as a book of reference,
and, secondly, because it is felt that the beginner’s interest may be more
effectively aroused in this manner than by presenting to him at once
every reference available. The latter, if desired, can be readily obtained
in the more advanced books which are cited.


It is recognized that illustrations constitute an extremely important
R. S. MCE.  
feature in a text of this character, and the writer has spared no pains in
the attempt to make the figures adequate both in number and quality.
It will be evident, however, that the majority of them are not original.
This is due to the fact that through the kindness of the authors and
publishers indicated below, there were made available a large number
of excellent illustrations, which it seemed hardly worth while to attempt
to improve upon. Nevertheless, in every instance where it was felt that
such improvement was possible, or where it appeared that a new figure
would be profitable, original drawings have been inserted. Lastly. it
remains to be. stated in this connection that in the case of all borrowed
illustrations, great care has been taken to have the illustration and the
terms used in its legend agree with the respective description and terminology in the text. The desirability of this, especially in an clexnemarj.'
book, is obvious; yet, according to the writer’s observation, it is a feature which is too frequently overlooked.


In conclusion I desire to express my appreciation of the following
Oberlin College, August 15, 1923.
favors. To Professor Frank R. Eillie and to Henry Holt and Co., I am
indebted for their generous permission to use a large number of figures
from Lillie’s Development of the Chick; to Professor T. H. Morgan. his
co-authors, arid Henry Holt and Co., for certain illustrations from The
Mechanism of Memlelian Heredity; to Henry Holt and Co., for numerous figures from Kellicott’s General Embryology and Chordate Development; and to the Delegates and Secretary of the Clarendon Press for
a like favor as regards .lenkinson’s Vertebrate Embryology. It is also a
pleasure to acknowledge a similar debt to Professor Morgan and The
Columbia University Press fr;-2' figures from Heredity and Sex: to Professor J. Playfair McMurrich and P. Blakiston’s Son and Co. for cliches
from McMurrich’s Development of the Human Body‘; to P. Blalcistozfs
Son and Co. for further clichés from Minot’s Laboratory Text Book of
Embryology; to Messrs. Longmans, Green and Co. for cliches from
Quain’s Anatomy; to Messrs. G. P. Putnam and Co., for permission to
use again certain figures from Marshall’s Vertebrate Embryology,
PREFACE TO THE FIRST EDITION x1


copied and slightly modified by Kellicott; and to Professor 0. Van der
Stricht and Dr. T. W. Todd for allowing the use of photomicrographs
made in the Anatomical Department of Western Reserve University
Medical School from preparations presented to that department by Professor Van der Stricht. In all cases the illustrations thus borrowed are
acknowledged in the legends of the figures concerned.


I wish further to express particular gratitude to Professor T. H.
Morgan for reading and criticizing the first half of the manuscript; to
Professor J. H. McCregor for performing a similar service for the entire hook; to Professor M. M. Metcalf for suggestions regarding the
earlier chapters: to my wife for assistance with the proof; and to Pro.fessor R. C. llarrison for the identification of the frog larvae used in
niaking certain of my original drawings. Especial gratitude is also
felt for the constant interest and helpfulness shown by my colleagues,
Professors R. A. Budington and C. G. Rogers.


R. S. MCE.
Oa1zm.r:~' Cm.x.scx-:,
August 15, 1923.
CONTENTS
PART I: THE GERM CELLS AND EARLY
CHAPTER DEVELOPMENT OF AMPHIOXU5
1. Introduction
2. Fertilization and Early Stages in Development
3.
9.
10.
13.
14.
15.
16.
17.
The Early Development of Amphioxus
PART II: THE DEVELOPMENT OF THE FROG
~. The Frog: from the Production of the Germ Cells through
Gastrulation
. The Frog: Early or Embryonic Development Subsequent to
Castrulation
The Frog: Later or Larval Development
PART lll: THE TELEOSTS AND GYMNOPHIONA
. The Teleosts and Gymnophiona: their Segmentation and Gas
trulation
PART IV: THE DEVELOPMENT OF THE CHICK
. The Chick: the Adult Reproductive Organs, and the Develop
ment of the Egg Previous to Gastrulation
Castrulation and Development through the First Day of Incubation
The Chick: Development during the Second Day of Incuba
tion
. The Chick: Development during the Third Day of Incubation
12.
The Chick: Development during the Fourth Day of Incubation
The Chick: Development during the Fifth and Subsequent
Days
PART V: THE DEVELOPMENT OF THE MAMMAL
The Early Development of the Mammal and its Embryonic
Appenclages
Development of the Pig to the Ten Millimeter Stage
The Later Development of the Pig
The Skeleton, Teeth, Hair, Hoofs and Horns
Index
xiii
39
10-1
147
169
262
280
300
332
370
395
433
561
655
673
PART 1
THE GERM CELLS AND EARLY
DEVELOPMENT OF AMPHIOXUS
NTRODUCTION
IT has long been an axiom with biologists that all organisms consist either of single cells or of cell aggregations. often with the addition
of various cellular products. It is also well known that even in the case
of multicellular animals or plants, each individual starts from a single
cell. This cell may be one that has recently fused with another in the
process called fertilization, or it may develop without such fusion by a
process called parthenogenesis. The latter is a natural prmi-mlure in
 
some instances and may be artificially induced in othgfi,
With the foregoing facts in mind it may then be stated that the dcvel~
opment of any multicellular animal or plant involves three fundamental
processes which go on more or less coincidentally. These processes are:
The increase in cell numbers b cell r d division (usually mi
totic‘ ; the i erentiation of the cells and sometimes their products ‘;Efi¢“’ "
..........._....—..........._.---n
e arran ement o t ese ce 5 an tissues to constitute
parts and organs. It is therefore the study 0 t ese processes which com»
prises embryology. Stated thus baldly and reduced, so to speak, to its
lowest terms, the subject may appear rather d _v and prosaic. Such,
however, is furthest from the truth for anyone with any real interest in
living things, and in the problems of existence in general. F or there is
no more astounding and fascinating drama which one may view than to
watch the development of certain eggs. This is particularly true of relatively srnall transparent ova which it is literally possible to see through
in the living state, such as those of many of the Invertebrates, like Sea
Urchins or Molluscs, and even some Vertebrates, like many Fish. Here
one may observe under the microscope the active division of the cells
and their gradual differentiation and rearrangement. Thus in certain
rapidly developing forms, there may be seen in a.few hours the transformation of an apparently structureless blob of jelly into a clearly recognizable and relatively complicated organism. Careful and accurate
descriptions of these and many other cases more dilficult to observe
have been recorded for a long time, and this constitutes descriptive embryology. It was inevitable, however, that after observing this veritably
magical performance man should begin to inquire how it was done, and
 
vari us tissues THE GONADS 3
this inquiry has led to the growing and very active field of experimental
embryology. Hence at first by relatively crude acts of interference with
normal development, and later by more cleverly planned procedures
it was and is being sought to analyze the fundamental processes involved. As in the analysis of all life phenomena the goal has constantly
been to reduce them to physico-chemical terms; and though this end is
by no means attained, workers everywhere are constantly pressing toward it. Hence, though the primary aim of this book is to present a description of normal embryological phenomena, opportunity will frequently be taken to indicate how experiment has helped to throw light
on many of the basic mechanisms concerned.
.lLhaLb;.en_§t§t§é-£!29!..,:1ev91Qprssnt starts from 3_9§l1.an.<lt_11at cells
c_o_nstitute the ‘units or building ':b_locks:of  living structures ar_e
mafie. Vileiimighlfthereforelspend some time in a discussion of cell structure and physiology. For the purposes of this book, however, it is assumed that the student is already familiar with this subject, and with
the phenomenon of normal cell division or mitosis. We shall therefore
omit further reference to this matter. It does, however, seem desirable
to make some comment as to the origin and history of the germ cells.
Let us then begin with this topic.
THE GONADS AND THE GERM CELLS
The germ cells or- gametes are certain cel_ls_in both cytpplasrn
andjnfileusgare speciéiliied:iv5_r:thelpill-pose‘ of reproduction. They are
thus distinguished ££oz'fi"'Is6d§% or somatic cells which are specialized for
other functions in the life of the organism. Before considering the detailed development of the germ cells it will first be necessary to give a
brief history and description of the organs in which they are finally
located.
THE GONADS
T_l_1_e__germ cells of__tl,_1eMadult occur in _orga<ns”_lcnqw_n_has_ _g9riq§s, the
f§¥D.§1P...§9l1a$l..bEl95..l9F'll¢dllllifilillfys and. Ihe_._rrn_s1s g9ns§,.-t1.1§.te:s_tisIn most true Verte_brates___these are paired structures,  same
iayéiriééiliiliétli m<.=z¥fl9e:s.é£ .:h_e" pair are aanmycai the §9m¢_..§2x- In
their earliest condition both ovarieswanidiitesties ap;’$飣aiiikej as a pair
of ridges (the genital ridges) consisting largely of thickened coelomic
epithelium (the germinal epithelium). Beneath this epithelium there
occur a mass of loose mesodermal cells known as mesenchyme. Pres4 INTRODUCTION
ently these cells give rise to real connective tissue which soon increases
and constitutes the supporting element of the organ, termed the medallary tissue or stroma. Each genital ridge lies along the back on either
side of the dorsal mesentery of the gut between it and the embryonic excretory organ. Within the germinal epithelium there presently appear
_5 :2 ,. ?¥«.s2.¥?~“°
J o u i
1'} ‘LIT
r ‘<4 Q3 _
‘” r‘-:«'2»::-at-.5:
pr. 0.
Fig. 1.—-Cross section of the ovary of a fledgling of Numenius arcurzrus 3-4 days
old. From Lillie after Hoilmarm. The region of the germinal epithelium is toward
the bottom of the figure. f. Follicle. o. A very young ovum around which the epithelial cells have formed a definite follicle. str. Stroma. pr.o. Primitive ovum within
a portion of the germinal epithelium.
certain cells which are often distinguishable from their fellows by their
larger size and also by their relatively larger nuclei. These are the primitive or primordial germ cells in which sex diiie1'entiation, at least as
regards the cytoplasm, is not yet apparent. The origin-and later development of these cells will he discussed after completing our descrip
tion of the gonads. ‘
The Ovary. --lt'l_l:~lt§_£§§§_M9f‘ltl'i§_pY§.}f}:, as the germinal epithelium
graduzilly _ing_r_§eses in thickness it is in someliiristances dividedlby the
4 '  iooigeurdus cords. In any
orinests of the epithelial
__  __»__  fllgecorriew scetteretl about
   
event, during
cells, each con aining a priini
-—-"---— .........__....
it e ourse of growth
.............._......____ __
 
“ "‘ —-.... .....————«
THE GONADS 5
thr u‘gh_gvutm_t_he connective tissue. Each germ cell then proceeds to de
as  the epithelial/celllslwhicli‘surround‘ it,’ known asfitsd
1), servhelto convey’ it iiiru‘i£n‘Erit.t ' '  l H K
-'-<.....,_._,. _. , we . . ...
Fig. 2.—-Cross section through the periphery of the testis of a just
hatched Chick. From Lillie (Development of the Chick). After Semon.
The sexual cords have acquired a lumen, and the walls of the canals
thus formed are lined within by the spermatogonia. Next to the latter
come a layer of supporting or Sertoli cells, and outside of these a thin
layer of connective tissue, the theca (not labeled). The remaining connective tissue (stroma) lying between the sexual cords (now seminiferous tubules) connects at the periphery of the testis with the special
layer of connective tissue (albuginea) which covers the entire organ
beneath the thin outermost layer of coelomic epithelium.
Alb. Albuginea. c.T. Connective tissue of the stroma, or septulae
testis. Ep. Remains of the germinal epithelium now forming the outermost or serous covering of the testis. l. Lumen of the sexual cords. pr.0.
Spermatogonia. s.C. Sexual cord, lined by supporting cells and spermatogonia.
The Testis. — __ ithin the_young gonad which is to become a testis
there develqp. .th£9P..s.h9yLth§ ,s,tr.€>iIrié; ‘sfiands o£..fiésfié it. this . case
té??7§3'ls§aey.zl eerie Th9y.sh._..thsi: 9_1ti.si.nin s°rr!9..i.n§t§p9es is 'd0’l“l1"btfl1l’
ih5Y..%ERaF9.¥!lX. %‘.5§¢= Tik.f9.F1}E=.v .9Y}s¢r.9t1.,s .9,91.1<1..s, trorx1.th¢_.g9rmi:1a1,ePi
thelium._Whatever their iorigin,Ahowever;theyapresently become filled
cords then
with the germ cells whi§ltL§eern,to migratejnt __t
6 I INTRODUCTION
become tubular, and the tubes are lined by the germ cellsteither arranged in layers oreinclosed in cysts (some Amphibia). Certain of the
cells constituting the walls of the cysts, or tubes, as the case may be, are
homologous in function to the follicle cells of the ovary, i.e., they bring:
nutriment to the growing germ cells. These nourishing cells in this case
are often termed supporting or Sertoli cells. Externally each tube is
covered with a thin layer of connective tissue termed the theca, and the
whole is known as ‘a seminiferous tubule ig. 2).
more detailed’ description of the development and structure of a
typical vertebrate ovary and testis will be found in our treatment of
this subject in connection with the Chick. Likewise short discussions
of these organs are included in the accounts of the other animals to he
studied. With this as an introduction the student is now prepared for a
description of the history of the actual germ cells.
THE GERM CELLS
The Origin of the Primordial Germ Ce11s.——There have been
two theories regarding the origin of the germ cells. lt was originally
believed that they arose through the modification of certain cells of the
germinal epithelium. In the earlier part of the century. however, it was
discovered that in some animals, at least, the primordial cells were not
first seen in the germinal epithelium at all, but were discernible as far
away as various parts of the gut wall. From thence they were seen by
some to migrate to the gonad through the mesentery of the gut. as in the
Turtle and Gar-pike (B. Allen, ’O6, Fig. 3), or to be moved thither by
shifting of parts due to growth as in the Amphibia (Humphrey, ’25l . or
to be carried by the blood stream as in the Chick (Goldsmith, ’28) .
While evidence for this sort of thing has continued to accumulate.
other observers have questioned the ultimate fate of these migrating
cells. In many cases it is claimed that such cells are not the ones which
form the actual or definitive germ cells. lt is asserted on the contrary
that the so-called primordial cells degenerate, and that the definitive
germ cells arise later by the transformation of indifferent epithelial
cells as was originally supposed. This is said to be the case for the Rat
by Hargitt (’25, ’30) , for the Cat by Sneider (’40) , for the Opossum by
Everett ("42), for the Guinea Pig by Boolchout (’45), and in various
other cases. Also in some instances, there are opposing views concerning the same animal as in the case of the Cat in which Kingsbury (’38)
claims, contrary to_ Sneider, that all definitive germ cells come from the
primordial ones.
THE GERM CELLS 7
It appears too that the situation may vary in different animals since
Everett (’43) thinks that in the Mouse, contrary to his View regarding
the Opossum, the primordial cells furnish all the definitive germ cells.
Thus it is evident that this question is still an open one, and hence subject to continued research. The reason for reference to it here is that
much of this interest in the origin of germ cells in Vertebrates stems
Lepi steus Lepidosteus
     
     
   
germ. End.‘
.. ....:..:-- \
anus-In-unuflglulhl
Periph. End. Vat. End.
Fig. 3.——-From Morgan (Heredity and Sex. Published and copyrighted
by the Columbia University Press). After Allen. Origin of germ-cells in
certain Vertebrates, viz., Turtle (Chrysemysl, Frog (Rana), Car-pike
(Lepidosteus), and Bow-fin (Amid). The germ-cells are seen migrating
from the digestive tract (endoclerm). End. Endoderm in various localities.
Int. Intestine. S.C. Sex (germ) cells. S.gl. Region of the gonads.
from certain well-known cases of apparently very early origin of these
cells in some of the Invertebrates, e.g., the Coelenterates (Weismann,
’83) and Ascaris (Boveri, ’l0). These cases in turn were long used to
bolster the famous Weismannian theory of the fundamental separateness
of the germ plasm and somatoplasm, and also the correlated theory by
that author concerning the mechanism of development. Modern genetical and experimental embryological research has pretty much outmoded
Weismann’s notions as to the nature of the germ cells and the mechanism of development in their original form. The actual source of the
germ cells, however, is still obviously a subject of considerable interest
to biologists. Let us now turn to a consideration of the structure and
development or maturation of a typical female and typical male germ
cell.
3 T INTRODUCTION
The Ovum. —The fully developed female germ cell is termed the
ovum. The ova of different Vertebrates vary widely in size, in the
amount and arrangement of their deutoplasm, and in their coverings.
They are uniform, however, in their relatively large size and inertncss
as compared with the male reproductive cell (Fig. --L). They also rosemhle both the latter and each other in one particular, i.e.. the behavior of their chromatin. This latter point involves a rather compli~
cated aspect of maturation termed meiosis which conipriscs two special
cell divisions, the meiotic divisions, sometimes known simply as the
maturation divisions.
Fig. 4. —GVeneralized diagram of a slightly telolecithal egg
ready for fertilization. The only membrane represented here
is the vitelline. :1. Animal pole. 2'2. The nucleus containing
a nucleolus and a linin network along the fibers of which
chromatin appears. 0. An oil vacuole. v. Vegetal pole. vt.
Vitelline membrane. yg. A yolk granule.
Inasmuch as these divisions are not only complicated, but also of great
significance, they will be considered later under a separate heading.
The other features of maturation in an ovum and then in a spermatozoon
will now be discussed.
It has already been noted that the primordial germ cells which migrate into the germinal epithelium are not readily distinguishable as
to sex, at least as regards their cytoplasmic morphology. Their male or
female character becomes apparent, however, as the gonad develops
THE GERM CELLS 9
and they become distributed through the stroma of the ovary, or take
their places in seminiferous tubules as the case may be.
In the former instance which is now under consideration the young
female germ cells in and near the epithelium proceed for a time to
multiply quite rapidly. They do this by means of typical mitotic divisions, and during the process are known as oiigonia. This stage of
Fig, 5.———Egg of the Teleost, Fundulus heteroclitus. From Kellicott
(General Embryology l. Total view, about an hour after fertilization.
c. Chorion. d. Protoplasmic germ disc or blastodisc. 0. Oil vacuoles.
p. Perivitelline space. 2;. Vitelline membrane. y. Yolk.
simple multiplication usually continues at least until the time of birth
or hatching of the animal in which they are contained. According to
most accounts the multiplication of cells then ceases, so that at this
time the animal in question contains as many——-though only partially
grown -— ova as it will ever have.
The next period is one of growth during which the cell becomes surrounded by its follicle, and is termed an oficyte.
The Nucleus. ———The nucleus during this second period enlarges
greatly, and is known as the germinal vesicle. It is relatively clear,
though it usually contains a line reticulum, and may possess one or
10 INTRODUCTION
more conspicuous nucleoli. The latter may he of either the plasmosome
or the karyosome type or both, and their significance is not well understood. It probably varies in dilierent cases. At the end, and also sometimes at the beginning of the growth period, certain changes occur in
the nucleus which are connected with meiosis. These will he described
below.
The Cyzopla.sm.——Meantime the cytoplasm is increasing considerably in bulk, chieilv as a result in many cases of the accumulation of
deutoplasm or yolk. This substance usually first appears in the shape of
granules and droplets. Later it assumes various forms and contains a
variety of chemical substances, consisting in general of proteids. nucleoalbumins, fats, carbohydrates, and certain salts. Not only does the composition of the yolk vary, but also its amount and distribution. Thus
where the amount of deutoplasm is large the oocyte becomes relatively
enormous as in the eggs of Birds and some Fish. In such forms the yolk
comes to be situated on one side of the ovum — the vegetal pole, whereas
the remaining cytoplasm containing the nucleus occupies a greater or
less part of the opposite side, or animal pole. Ova of this type are
said to be telolecithal, and in those instances where this arrangement
is most marked the relatively yolkless cytoplasmic cap at the animal
pole is called the blastodisc (Fig. 5). In other ova, such as those of the
Mammal, there is relatively little yolk and this is scattered throughout
the cytoplasm. An egg of this type is termed homolecithal.
The manner in which the yolk originates and grows is of some interest. The actual new material for its formation is of course supplied
from without, probably throughithe medium of the follicle cells. The
organization of this material into yolk, however, often seems to take
place in connection with a certain body known as a yolk-nucleus-Corr»
plex. The nature and even the exact origin of this body is rather uncertain, and indeed seems to vary iri different cases. Frequently, however,
it is seen near the true nucleus as a clear spheroidal mass, similar to if
not identical with an idiozome} containing a granule or granules (centrioles), and surrounded by a layer (pallial layer) consisting partly of
Golgi bodies and mitochondria. Whatever its nature when present it
seems to exercise some influence over the building up of the nutritive
material. T
The Central Body. — Concerning this body in the oiicyte there is considerable question. In some eggs, as just indicated, the oégonial divi
1 This is a special term applied to the centrosome during certain stages in the
development of the germ cells.
THE GERM CELLS 11
sion-center appears to persist for a time as a part of the yolk-nucleus
complex. Before the yolk has finished forming, however, this complex
generally disappears, and with it the division-center also usually vanishes. At the time of meiosis a new center forms, apparently in connection with a new (?) centriole, the origin of the latter in these cases being uncertain.
The Egg Membranes. —-— Following growth the oiicyte, or ovum, as it
may now be called, is often surrounded by as many as three different
types of coverings, whose character and development are as follows.
The first of these is a thin envelope immediately surrounding the egg,
termed the vizelline membrane. It is doubtful in the eggs of many
Vertebrates whether or not this covering is really present. When it is
present, however, it is characterized by the fact that it is a secretion
from the ovum itself. The second covering is the chorion, which is
secreted by the follicle cells. It varies much in structure and again may
be entirely lacking, as is probably the case in the Chick. Finally there
are frequently one or more tertiary coverings. These may be jelly-like
as in the Frog, or one soft and the other calcareous as in the Bird. When
present they are always secreted by some portion of the oviduct through
which the egg must pass on its way to the exterior.
The Spermatozc-5n.-—The mature male germ cell is called the
sperm.atozoiJ'n. In general it is characterized by its extremely minute
size, its lack of any nutrient material within itself, and its equipment
for active locomotion through a semi-fluid medium. More particularly
such a typical sperm consists of the following main parts (Fig. 6) :
I. The Head. —— This is chiefly composed of concentrated chromatin
enclosed in a thin envelope of cytoplasm. It varies greatly in shape in
different animals, but is often a more or less ovoid disc. To its anterior
end is attached a tip, usually rather pointed, but also subject to much
variation in form. It is the acrosome or perforatorium, apparently derived from a part of the centrosome or idiozome. Thus the head may be
said to consist essentially of the nucleus and a very little cytoplasm.
II. The Middle Piece. — This has long been a convenient descriptive
term rather than an accurate designation of a part which is truly homologous in different forms, and is in general the region immediately
posterior to the head. According to Bowen (’24), however, this part
may be more accurately described as that portion of the spermatozoiin
which is composed of the following materials:_cytoplasm, mitochondria,
the axial filament, and a centriole or centrioles, to one of which the
filament is attached. Of these items, moreover, the mitochondria and
ep. ep.
Fig. 6.——A diagrani of
a generalized flag:-llate
spermatozoiin based on
the Mammalian type,
showing the flat side of
the head and also its
edge.
H. Head. M. Middle
piece. T. Tail. a. Acrosome. af. Axial filament.
c. Centrosome. cy. Cytoplasm forming an envelope for the head and
middle piece. ep. End
piece. mi. Mitochondria
arranged in the form of
a spiral thread. s. Sheath
of unknown origin and
’ constitution covering the
axial filament of the
main piece of the tail,
and extending up inside
the cytoplasm of the
middle piece. :1. Neck.
INTRODUCTION
centrioles are supposed to be confined to the
middle piece, thus defining it. Sometimes at its
anterior end is 3 short clear region of the
middle piece attaching it to the head. It is
termed the neck, and when it exists one or niore
of the centrioles lies in it.
III. The Tail or Flagelhtm.-—Continuing
with the definitions of Bowen. this part of the
sperm extends posteriorly from the point win.-re
the cytoplasm and mitochondria of the middle
piece and. It thus consists of that mgiszni of the
axial filament which though lat.-1-ting these.» mv<,-.rings is nevertheless enveloped by a sheath, plus
a short final portion of naked iilaxrwiit. The
sheathed region is termed the main piece. and
the naked filament the end piece. The former,
along with the middle piece, may also possess
a fin-like membrane which is supposed to arise
from the axial filament. lt should be noted that
according to this description some sperm. e.g.,
those of the Urodeles, have no main piece, the
middle piece extending all the way to the end
piece.
It must now he added that though the chiei
features thus described may be regarded as
typical of spermatozoa in general, there are
numerous, and sometimes quite bizarre, variations. Indeed in certain cases even the characteristic flagellum is lacking, and the cell depends
upon amoeboid movements for its locomotion.
A suggestion of the varieties of forms which
occur is indicated in Figure 7.
With this idea of the general structure of a
sperm in mind, it is now possible to consider
the stages through which such a cell passes in
its development or maturation. The primordial
germ cells have already been described in the
study of the ovum, and it was noted that during this early period their
appearance is practically alike in both sexes. Thus no further account
of this stage is necessary in describing the history of the male cell.
64
Fig. 7.—-—Variou5 types of spermatozoa. From Kellicott ( General Embryology). A, B._ The Teleost, Leuciscus (Ballowitz). C. D. The Birds,
Phyllopncuste and Tadorna (Ballowitz). E, F. Two forms of the sperm
of the Snail, Paludina (Von Bmnn). C. The Nematode Ascaris (Van
Beneden). H. The Annulate, Myzostoma (Wheeler). 1. The Bat, Vesperugo (Ballowitz). J. The Opossum, Didelphys (Wilson). K. The Rat
(Wilson). L. The Urodele, Amphiuma (McGregor). M. The Crustacean,
Ethusa (Grobben). N. The Crustacean, Inuchus (G1-obben). O. The Crustacear;, Sicla (Weismann). P. The Crustacean, Bythotrephes (Weisrnann .
1:. End knob. m. Middle piece. n. Nucleus. p. Perforatorium. u. Undulatory membrane. Not drawn to same scale. A—F, I-K, from Wilson.
13
14 INTRODUCTION
By the time the male germ cells have become located in the seminiferous tubules, they have become clearly distinguishable as such.
They then enter upon a period of multiplication in which they are
known as spermatogonia. This stage corresponds in all essentials to
the similar period of multiplication of the young ova (oogonia) .
Following this stage is a time of growth which also corresponds to a
period of like change among the ova (oiicytes) . The cells at this time
are therefore called spermatocytes. In this case, however, the growth,
though noticeable, is naturally much less marked than was observed
in the oéicytes, and there is, of course, no accumulation of yolk. The
nucleus, nevertheless, goes through processes very similar to those
which characterize the ovum at this period, at the close of which it
undergoes meiotic divisions. Although these divisions are fundamentally the same as those of the oiicyte, they differ in certain important
details which will be considered more fully when that topic is discussed.
Other Difierences between the Development of the Sperm
and the Ovum. — It will be recalled that in the case of the ovum the
end of the growth period found it practically completed. This, how
ever, is one of the points in which the spermatocyte cliiiers strikingly
from the female cell. After meiosis the products of the second division
are called spermatids, and instead of being complete they are just ready
to enter upon their remarkable metamorphosis into the highly specialized spermatozoa. This process varies considerably in different animals as regards its details, particularly with respect to the exact method
of formation of the middle piece and tail. Indeed there is still so much
difference of opinion on the matter, that it seems inadvisable in a text
of this type to attempt a description beyond an indication of the general
constitution of each of the main parts as already stated. The student
interested in the details of metamorphosis as it has been described in
a particular form is referred to the account of the process in the seal
by .l. R. Oliver (’13).
Two further dilierences between the history of the egg and sperm may
finally be noted as follows: One of these is the fact that the multiplication of spermatogonia does not cease during the sexual life of the animal. This of course is correlated with the almost continuous production of vast numbers of spermatozoa in comparison with the relatively
much smaller production of eggs. As a result of this condition, all the
various stages of developing sperm are always to be found in the seminiferous tubules. Where there are no cysts, theyoungest cells occur next
THE GERM CELLS 15
to the epithelium, and the older
ones successively nearer the central
lumen. Where there are cysts, on the
other hand, any one, at a given
time, usually contains only cells of
one stage. In view of the very great
number of spermatozoa thus produced, there is perhaps even more
question in their case than in the
case of the ova, whether all are.derived from the original primordial
germ cells. Instead it seems probable that some at least arise directly
from the division of apparently indifferent epithelial cells.
The second dilierence is the arrangement of the developing sperm
relative to their source of nutriment.
it has already been indicated that
the cells iSertoli cells) which furnish this do not, except sometimes
in the earliest stages, surround each
spermatozoiin. Instead they form the
lining to either a tubule or’ cyst
containing many such germ cells.
Then as the development of these
Fig. 8.—-Diagrammatic outline. of the
spermatogenesis of the Rat in thirty-two
stages. From Kellicott (General Embryology). Aiter v. Ebner. Theca of tubule
toward the left. Lumen of the seminiferous tubule toward the right.
I-8. Period of multiplication (the number of cell generations is actually very
large). 9-18. Period of growth. I9-24.
Period of meiosis. 25-32. Period of metamorphosis. b. Basal cells or Sertoli cells.
I -I 6. Spermatogonia. 17, I 8. Primary spermatocytes preparing for division. 19. First
spermatocyte division. 20. Secondary spermatocytes. 21. Secondary spermatocyte division. 22-25. Spermatids. 26-31. Transformation of spermatids. 32. Fully formed
spermatozoa.
15 INTRODUCTION
cells proceeds, they become arranged in bundles, all the heads of one
bundle becoming imbedded in a single nutrient cell. When the sperm
are mature the cyst wall, if there be one, breaks so that their tails
project freely into the lumen of the tubule. At the same time the spermatozoa become loosened from the _Sertoli cells and are tlius ready to he
released into the above mentioned ‘lumen (Fin. 8).
MEIOSIS
It is now necessary to return to the consideration of a process whit,-h
is common to both ovum and sperm, i.e., meiosis. As has alrvmly i.tt"l*'.‘Il
indicated, the phenomenon is a rather complicated one. Furthcrrnme,
it varies somewhat in diilerent animals, and the exact i'ne.axiiii;:s of statue
of its stages are still in considerable doubt. For the sake of nec:e:ssary
brevity and clearness, therefore, it will be nece:-sary to limit rather
sharply the varieties described, and the possible interpretations of
which their stages are susceptible.” Also, inasmuch as there are differ‘ences in the behavior of the ovum and sperm, it will be necessary to
describe them separately. The male germ cell will he considered first.
Meiosis in the Spermatocyte.
I. The Leptotene Stage. —— Shortly after the last spermatogonial division, the chromatin of the enlarging nucleus arranges itself in spireme or
lepzotene threads (Fig. 9). These threads are relatively very fine, and
appear as a tangled maze in which it is difiicult or impossible to determine where any particular thread begins or ends. This often leads to the
impression that the threads consist of a continuous network, but this is
probably not so. Rather, the most favorable cases indicate that this network really is composed of the thread-like components of the chromosomes known as chromonemaza (singular chromonema) (Figs. 9 [2],
11, I). It is, of course, difficult to determine their exact number, but at
this stage there is probably one representing each chromosome, and the
number would be the same as that of the chromosomes in the somatic
nuclei of the organism concerned.
11. The Synaptene Stage.—At this point it should be recalled that
the somatic chromosomes of most organisms, with the exception of one
chromosome to be noted later, occur in pairs. The members of a given
pair appear alike, and were derived, respectively, one from each parent
of the organism in question. Such a pair of chromosomes are called
'~’ For a full discussion of this subject with references to the complete literature
the student is referred to The Cell in Development and Heredity by E. B. Wilson.
MEIOSIS 17
homologous chromosomes as contrasted with a’ pair produced by mitotic
division of a single chromosome, and known as sister chromosomes. It
then happens that during this stage the chromonemata come to lie side
by side in pairs ‘which are thought to represent pairs of homologous
chromosomes. Usually these chromonemata converge to the nuclear
membrane on the side nearest the centrosome, and extend thence toward
the other side of the nucleus (Fig. 9 [4]; Fig. 11, II). Presently the
members of the pairs begin to fuse or synapse. If this is the correct interpretation the number of pairs should be just half the somatic number of
chromosomes. Unfortunately, however, the threads or chromonemata in
this stage are still so fine and tangled that they give only the general
impression described above, and it is impossible to determine their number exactly.
Even so, in instances where the pairs of threads are well lined up with
their ends toward one pole, a fairly close count can be made; in such
cases the results confirm the interpretation indicated. Another type of
synaptene occurs in some animals and many plants which is termed
syrzizesis or contraction. Here the leptotene threads or chromonemata become drawn into a tangled mass, usually somewhat to one side of the
nucleus. In this type of synaptene the side by side pairing of the threads
is much less clear; yet even here there is some evidence that it is occurring as the contraction into the mass begins, and this is generally assumed to be the case. Sometimes, also, the contraction is not so complete as to obscure the fundamental nature of the process. Whichever
appearance this stage may have, there is plenty of indirect proof that
a close union of the homologous members of chromosomal pairs is occurring here, and hence the name synopsis or fusion (Fig. 9 [4—5] ; Fig.
11, 1 I, Ila).
III. The Pachytene Stage.——— In this stage the threads appear much
thicker and often somewhat fuzzy (Fig. 9 [6-7] ; Fig. 11, III). They are
also obviously fewer in number than in the leptotene, and though an accurate count is again difficult, the number at this time appears to be
about half that of the chromosomes in somatic cells. Indeed according to
the interpretation generally accepted and here given, this number is
exactly half, except for the possible presence of the one odd chromosome
to be mentioned later; this has been brought about by the more or less
complete fusion of the, paired threads of the synaptene. This half number of chromonemata, or of chromosomes, of which they are the equivalents, is known as the haploid number, as compared to the number
formed in the somatic cells and termed the diploid number. It should
18 INTRODUCTION
he noted, however, that the reduction here indicated is not really a
genuine reduction since all the threads are still present in a fused condition. The true reduction comes later. This is emphasized by the fact
that in some cases, as in the Orthoptera, for instance, there is always, in
,;f;;:.;:,. «
«I! I
Fig. 9.—Prophases of the heterotype division in the male Axolotl. From Jenkinson (Vertebrate Embryology).
’ 1. Nucleus of spermatogonium or young spermatocyte. 2. Early leptotene. 3. Transition to synaptene. 4. Synaptene with the double filaments converging toward the
centrosome. 5. Partial synizesis or contraction figure. 6, 7. Pachytene. 8. Early.
9. Later diplotene. I0. Heterotypic chromosomes with disappearing nuclear membrane and with one figure showing its quadripartite character.
properly stained preparations, a slight indication of the duality of the
fused threads.
TV. The Diplotene Stage. -——Following the pachytene stage the chromatin threads no longer converge toward one pole, and again appear
definitely double. Indeed, especially toward the latter part of this stage,
each pair of chromonemata may appear fairly clearly quadripartite, at
MEIOSIS V 19
which point each one of the four threads is called a chromatid, and the
group of four is called a tetrad (Fig. 9, [9—10] ; Fig. 11, IV, IVa). This
quadripartite condition is due to the fact that sometime during the
pachytene or early diplotene each chromonema of an homologous pair
has duplicated itself to form a sister thread. At the same time the four
chromatids in each tetrad have become twisted about one another in a
Fig. 10.—First meiotic division in the male. 2. Salamander, the remainder
Axolotl. From Jenkinson (Vertebrate Embryology). 1, 2. The heterotypic chromo
somes on the spindle (metaphase). 3. Anaphase. 4, 5. Telophase. 6. Resting nuclei.
4-6. Cell-division into two secondary spermatocytes.
peculiar way to be explained later, this twisted condition being called
strepsinema (Figs. 9 [9]; 11, IV). On the basis of the four-part situation just described one might ask why this stage is termed diplotene,
meaning double thread. It is because, though the groups may be quadripartite, one of the lines of separation is usually much more evident
than the other, and it is along this line that the first meiotic_ division
occurs. '
It used to be thought of considerable interest, whether this line represents a separation of the formerly synapsed homologues, or whether it
represents a new _line of separation between duplicated sister chromonemata, now chromatids. If it is the former, the first meiotic division
is said to be reduczional because it appears to separate the original homologous members of chromosomal pairs. The second division, then, must
20 INTRODUCTION
   
3 4
'3.’..“'..::~.. /‘~» ~ .
3:: ‘W
, s., -......
 
Fig. 11.———-Diagrams of possible prophases of meiosis, involving three pairs of
chromosomes; 1, barred, light, dark; 2, dots, rings; .3, szippled, white. I. Lepmrene.
Chromosomes in form of thread-like chromonernata. II. Synaprenc. limnnlngous
chromonemata fusing. Ila. Synizesis, another form of synapsis. III. Pzu-l:,we~ne.
Chromonemata fused, each one starting to duplicate itself, and also starting to ex~
change parts in 2 and 3. Only “ pre-reduction” situation shown in this stage (see
below). I V, I Va. Diplotene, shown enlarged in 1, la, etc. Members of pairs starting
to separate, each chromonema now definitely duplicated to form a chromatid of
a tetrad. In the barred pair pre-reduction is shown in IV and 1, post~rc-duction in
I Va and 1a. In the other two pairs exchanges have occurred between the members
of the pairs as indicated. Hence though the arrangement of parts varies, as shown
in 2, 2a and 3, 3a, each separation in these cases is partly reductional and partly
equational. In 4 and 411 two exchanges between a single pair of chromonemata is
shown, a case not represented above or in Fig. 12. There are other possibilities. V,
Va. Diakinesis, show possibilities of this stage following IV and I Va, respectively.
presumably separate the sister chromatids produced by duplication,
and hence like any ordinary mitosis is equational. This order of events
is called pre-reduction. If the sequence is reversed, it is post-reduction.
(Fig. 13). Actually, since all four chromatids of a group usually look
alike, and since the number of remaining chromatids is the same in
‘ either case, there is generally no way of telling which type of division
has occurred except in a few peculiar situations such as illustrated in
Figs. 20, 21, and 22. Here post-reduction, though probably the more
unusual‘ type, can clearly be seen to have taken place. Obviously, however, the final result following the second division will be the same in
either case. Also, because of certain further events, the terms “ pre- ”
and “ post-reduction ” often lose their significance. These events are as
follows:
MEIOSIS
21
 
 
 
   
\\\\\\V
(IIIII)
     
 
%
t.-.
I '-.' - ‘
// . 1' \ ‘I
\ l '. -i
C C’
;——"———\
a
Fig. 12.-— Continuation of diagram in Fig. 11, showing the I and II meiotic divisions. In I and II the barred tetrad, as in Fig. 11, is undergoing pre-reduction. In
la and [Ia the same tetrad is undergoing post-reduction, i.e., the II division is reductional (see text and Fig. 13). As indicated under Fig. 11, for the other two
tetrads each division is partly reductional and partly equational. The groups of
chromosomes bracketed under a given letter (A, A etc.) are those to be found in
each cell following the division immediately above. Each tetrad behaves independently of the others, e.g., in 1, cell A happens to receive the lightly barred pair of
chromatids (chromosomes), but this is a matter of chance, and is unrelated to which
pairs from the other sets of tetrads go to this cell. This is called independent assortment, and applies similarly to the single chromosomes of the II division. Hence
many more combinations are possible than are shown above.
 
\
oauouo D
At some point after the quadripartite condition has developed, apparently in the pachytene or early diplotene, it is believed that exchanges of parts (genetic cross-overs, see below) frequently occur between the homologous chromonemata (chromatids) of a tetrad. While
such exchanges may occur between one pair of homologues at one or
more places simultaneously, and possibly between one pair at one place
and the other pair elsewhere simultaneously, exchanges between members of both pairs seem never to occur simultaneously at the same
place (Fig. 11, [2, 3, 4]). It should now also be noted that following
such exchanges the initiation.of repulsion between corresponding parts
4‘lP..W,WK'Tt.’>s
A.
Pre - Reduction
First Division Second Division
Reductiona! EQU3t|°“3l
 
First Division P°st' Reducthn Second Division
Equational Reductional
.0 .0
 
Fig. 13.——-A stereoscopic diagram representing the two possible types of behavior
of one of the three pairs of chromosomes indicated in Fig. 12 during the first and
second meiotic divisions. The letter a designates one member of the pair and b the
other member. For the sake of clearness, the plane of the second division is indicated in both types before the first division has actually started, in this manner
producing a tctrad consisting of four chromatids. These chromatids are often
definitely separate at this stage, or even as early as the diplotene stage (see text
and Figs. 11, 12, 14).
In the upper set of four figures the first division (that on the left side) is reductional, i.e., a and b are separated from one another, while the second division
(that on the right side) is equational, i.e., a and b are each split in half (Prereduction). In the lower set, on the other hand, the first division (that on the left
side) is equationnl, i.e., a and b are each split in half, but in each instance the half
of it remains attached to the half of b. The second division (that on the right side)
then follows and in each half which resulted from the first division the a portion
is separated from the b portion (Post-reduction).
22
MEIOS-IS 23
of chromatids leads to a crossing of the chromatids as in Fig. 11. In the
case of “ pre-reduction,” the repulsion will be between the corresponding parts of the hornologues which attracted one another during synapsis, while in “ post-reduction ” it will be between corresponding parts of
Fig. 14.—Tetrad formation in the spermatogenesis of Ascaris megalov
cephala bit/alerts. From Kellicott (General Embryology). After Brauer.
x 795. A—'G. Stages in the division of the primary spermatocyte. A, B.
Splitting, and C, condensation of chromatin thread, seen in side view.
D. shows, in end view, that the splitting is double. Centrosome divided.
E. Migration of centrosomes and formation of spindle. F, G. Division
of the cell body and of the two tetrads. H.,Secondary spermatocyte
containing two dyads. I. Division of secondary spermatocyte. J. Two of
the spermatids, each with two “ monacls ” or single. univalent, chromosomes.
n
sister chromatids. In either case, crossing results, and the point of crossing is called a chiasma (pleural chiasmata) , the general situation being
termed chiasmazypy.
In some forms the diplotene is followed by a so-called confused or
diffuse condition in which the threads become less distinct, and approach
the state seen in a “ resting ” nucleus. Either with or without the interpolation of this diff use condition, there may _also ensue a second contraction stage in which the threads are again drawn into .a clump quite similar in appearance to that of the original synizesis in those cases where
the ‘latter occurs.
24 ‘ INTRODUCTION
V. The Diakinesis Stage. -In this stage the chromatid threads, as
in the case of any chromonemata approaching the metaphase stage of a
cell division, undergo great shortening and condensation of chromatin.
In the case of meiosis, however, the forming chromosomes difier from
those of a similar mitotic stage in that they assume peculiar shapes, e.g.,
crosses, rings, etc. (Fig. 9 [10]; 11, V; 15: D, E), and are hence Said
to be heterotypic. This is due partly to the quadripartite nature of the
chromatid groups, and partly to the twisting of the chromonema indicated above. The number of tetrad groups is of course haploid.
V I . The First Meiotic Division. —- The above chromatids are presently
arranged at the equator of an ordinary amphiaster, but, because of the
quadripartite character of the groups and the chiasmata involved, the
metaphase figures, like those of diakinesis, have a peculiar appearance
and are also termed heterotypic (Figs. 12, I, la; 15, A, B) . As has been
stated this division occurs along the more prominent of the diplotene
separations, and in the case of a tetrad where no exchanges of chromonemal sections have occurred, the division will be exclusively reductional or equational, depending upon whether the separation is between
homologous or sister chromatids. Even so, since all four chromatids of
a tetrad look alike, there is usually nothing to show which type of division has occurred. Also where exchanges have taken place between homologues, each division is inevitably partly reductional and partly equational. In any event the resultant number of double chromatids, like the
number of tetrads, will be haploid.
VII. The Second Meiotic Division.--Until the completion of the
first division, the spermatocyte is known as primary. After that it is
called secondary. The secondary spermatocyte generally enters upon a
brief period of rest preceding the next division (Fig. 12, II, Ila). During this time the nucleus is often reconstituted, and the chromatin assumes to varying degrees the typical resting condition. Presently. however, the haploid number of double chromatids emerges from this stage
in the usual manner, and becomes arranged on the spindle preparatory
to the second division. Upon this occasion they generally present a normal appearance, aside from the important fact that their number remains
haploid, and hence this division is termed homotypical.
From preceding discussion and reference to Figs. 11 and 12 it should
now be clear why the question of pre- and post-reduction, as stated, often
loses its meaning. Thus it may even be that the situation is different for
dilferent tetrads in the same nucleus. The only cases where pre- or postreduction applies to the entire nucleus would be in organisms like the
male of Drosophila where, for some unknown reason, there are no exMEIOSIS . 25
changes between any of the chromonemata. In instances where there are
exchanges, however, reference to Figs. 11 and 12 makes it evident that
in these cases two meiotic divisions are needed to effect complete separation of all homologous parts. Thus, considering parts 2, 2a and 3, 3a in
the above figures, it is evident that each division as diagramed is, as
noted, partly reductional and partly equational, and this is probably the
Fig. 15.-—Meiotic divisions in certain Insects, showing
forms of chromosomes and their relation to tetrads.
From Kellicott (General Embryology). After de Sinety.
x; 1125. A, B.'Two stages in anaphase of primary spermatocyte division in Stenobothrus parallelus. Rings
opening into Vs which diverge. C. Anaphase of spermatogonial division in Orphania denticauda, showing differentiated chromosome, x. D, E. Preparation for first
spermatocyte division in Orphania, showing “tetrads”
in various stages of formation from rings and crosses,
i.e., diakinesis figures.
situation in the majority of cases, not only with respect to particular
pairs of chromosomes, but with respect to all the pairs in a nucleus.
The above situation might be cited as a reason why two meiotic divisions are necessary, but this is not so. It is rather the duplication of
chromonemata, probably in the pachytene previous to the exchanges of
parts, which requires a subsequent second division in order to secure distribution of all homologous sections to separate nuclei. It is, therefore,
the original duplication which needs explaining, and it appears that
this phenomenon is simply inherent in all prophases. Hence a second division is inevitable whether needed to effect complete reduction or not. In
any event, regardless of when reduction occurs, it is now evident that the
25 INTRODUCTION
final result is the same; that is, there are produced four spermatids,
’ each containing one haploid set of chromosomes with unique parts.
This last statement, it should be added, is frequently not precisely
true. The exception is exceedingly important, but it has been omitted
for the time being for the sake of clearness. It can be better appreciated, furthermore, when described in connection with the condition
in the ovum. We shall reserve this point, therefore, until after the description of meiosis in the female.
Fig. 16.-—-From Kellicott (General Embryology). A. Chromatin extrusion from
the nucleus into the cytoplasm in the oiicyte of the Medusa, Pelagia noctiluca.
After Schaxel. B. Extrusion of chromatin into the cytoplasm during the maturation
of the oiicyte of Proteus anguineus. After Jiirgensen. x 1080.
Meiosis in the Ovum.——-Meiosis in the ovum is fundamentally
similar to that in the sperm, with certain variations in detail. lt will be
possible, therefore, to make clear the process in the oiicyte by simply
"indicating the points in which it differs from that just described. These
points"may be stated as follows:
1. Length of Early Sta,ges.———In some instances at least, the early
meiotic stages up to and including synizesis occur immediately after
the lastoiigonial division. As previously noted, however, these divisions are said in some cases to cease at the time of the hatching or birth
of the female containing the cells in question. As indicated this is now
denied with respect to Mammals, and is in doubt as regards all Vertebrates. In so far as it may occur, however, there follows the fact that
certain of the meiotic stages must, in the cases of the last ova to mature,
MEIOSIS 27
Fig. 17.—Meiosis and fertilization in the Nemertean, Cerebratulus.
From Kellicott (General Embryology). After Coe. C, D, x 375, others
3: 250. A. Primary oficyte. Part of the chromatin has been condensed into
chromosomes, only five of which are shown (the number present is sixteen) . The remainder of the chromatin is thrown out into the cytoplasm.
The centrosomes, each with a small aster, are diverging, and the nuclear
membrane is commencing to disappear. B. First polar spindle fully
formed and rotated into radial position. Chromosomes in equatorial plate.
The extra chromatin (vc) is seen scattering through the cytoplasm. C.
First oiicyte division; anaphase. D. First polar body nearly separated. E.
First polar body completely cut 0E; second polar spindle formed and
rotating into radial position. Spermatomiin within the egg. F. Second
polar body completely separated. Egg pronucleus forming, surrounded
by large aster. Sperm pronucleus, also with a large aster, enlarged and
approaching the egg pronucleus. These steps connected with the be
havior of the egg and sperm nuclei (pronuclei) will be fully explained
later on in the text.
c. Chromosomes. o. Nucleolus, vacuolated and commencing to disappear. 5. Spermatozotin just within the egg. v. Germinal vesicle. vc. Extra
chromosomal chromatin being scattered through the cytoplasm. I, II,
First and second polar bodies. 0” Sperm nucleus (pronucleus). 9? Egg
nucleus (pronucleus).
occupy very considerable periods of time. This is apparently not true of
these stages in any of the sperm.
II. Loss of Chromatin.—— In the oiicyte, a loss of chromatin into the
cytoplasm has been alleged in a few special cases during the growth period, particularly in the diplotene stage (Fig. 16, B). That this phenomenon actually involves a loss of parts of the diplotene threads, however, seems unlikely for these threads or chromonemata presumably
carry the genes, and any indiscriminate discarding of genes at any time
INTRODUCTION
Primordial germ cell
("Primitive Ovum")
Period of multiplication. s
chromosomes. The number
of cell generations is much
greater than indicated here _ Danni,
Period of growth, ending in
tetrad formation or its
equivalent
Primary Oocyte
Secondary Oocyte,
Period of maturation
divisions. the first in this
case being reductlooal
and first polar body
Mature ovum and
2 three polar bodies,
‘ each with ‘g’
chromosomes
Fig. 18. —~Diagram of the chief events of oogenesis. Modified from Kellicott after
Boveri. The chromosomes are assumed to consist of two pairs represented by letters. AA represents one pair and BB the other. It is to be noted that the members
of a chromosomal pair are not always dissimilar as the light and dark letters in
i this case suggest. They are so represented here in order to make apparent the ¢lis~
tinction between the equational and reductional divisions during meiosis. Also as
indicated in connection with Fig. 12, the dissimilarity of the members of one pair
has no necessary relation to the dissimilarity of those of the other. Finally, it should
be remembered that when dissimilarity between members of a pair of chromosomes
does exist, it can rarely be detected by observation of the bodies themselves, only
by the efiects they produce.
is highly improbable. It, therefore, seems more reasonable that whatever
loss there is in these cases concerns only the matrix material surrounding
the coiled chromonemata, storage karyosomes, or the like (Figs. 16, A;
17) . Such losses as these are not observed in spermatocytes.
III. Size of the Division Pratlucts.- Perhaps the most striking of
all the differences between meiosis in the ovum and that in the sperm is
the difference in the size and fate of the products of the two divisions.
In the sperm, as, has been noted, the two meiotic divisions are equal
MEIOSIS 29
Period of multiplication. s
chromosomes. The number
of cell generations is much
greater than indicated here
Period of growth, ending in
tetrae formation or its
 
equivalent Primary spermamma
Period of maturation
divisions, the first in this S°°°"d“" "’°'""‘°°’"
case being reductional
Spennatids
\ 1, ‘\ \ I \ I
Period of metamorphosis. ‘t I ‘. II ‘\ I ‘..'
spermatozoa
-§- chromosomes present ‘E’ E’ ‘E’ 3'
Fig. 19.—Diag_ram of the chief events of spermatogenesis. Modified from Kellicott after Boven. The chromosomes are represented in the same manner as in the
case of the ovum in Fig. 18. It will be noted that the light and dark members of
the pairs are differently arranged relative to one another in the primordial and
subsequent cells. This was done to indicate that this phase of the arrangement is
purely a matter of chance. It might be the same in the case of the ovum or as suggested in that case the A and B might both be light or both dark in all the cells.
Likewise starting with the combination shown in the primary oiicyte or the primary
spermatocyte the four final cells in either instance might have had AB in two and
AB in the other two instead of the combinations indicated. All that is required is
that there be one member of each pair in each mature cell or polar body.
and the resulting four cells are all alike and functional. In the ovum,
on the other hand, the cytoplasmic divisions in both cases are extremely
unequal and only one of the four final products is a functional egg cell.
The others are relatively minute and are known as polar bodies, the one
resulting from the first division being termed the first polar body and
that resulting from the second division the second polar body. This
condition of inequality is brought about by the fact that at each divi30 INTRODUCTION
sion the nucleus and division mechanism take up a position at the periphery of the cell instead of at its center. Thus one set of chromosomes
remains in the main cell, while the other set is pinched off in a very
small bit of cytoplasm (Fig. 17).
Although there is this great discrepancy in the distribution of the
cytoplasm, there is good reason to believe that the nuclear content is
thg same in every case, just as it is in the sperm. In other words, the
performance is in every
way homologous with
the two spermatocyte
divisions except for the
inequality in the distribution of the cytoplasm. This idea is
borne out by the fact
that in many cases, as
might be expected, the
first polar body divides again as does its
larger sister cell, thus
Fig 20 -—A diplotene nucleus in Lygaeus bicrucis. Producing one Olvum
After E. B. Wilson. Note the condensed condition of and three P013; bodies.
~ - X d Y. Th ' ' h - . . .
‘.lI}i(()3s:fr1xe‘5:,h‘:l1lnt‘llse‘):(l-Jltelltlir hzziiid, are stiallrfgigalilllrilgef oliile T]-115 behavlor 1“ the
of them, a, as well as the sex-chromosome X, show- case of the ovum is
ing the characteristic diplotene split. This split in h ah t b d
the case of the X is obviously equational. The plas- t ‘mo '3 ° 3 an 3 3P‘
mosome, 121., is only partly visible. tation to secure the
greatest amount of cytoplasm and nutriment in a single cell.
IV. The Time of the Meiotic Divisions. —— In the sperm, as has been
seen, meiosis is entirely completed within the testis and before the spermatid even enters upon its final period of development. In the ovum, on
the contrary, meiosis is the last thing to occur. Sometimes division takes
' place while the ovum is in the ovary. More frequently, however, espe
cially among the Vertebrates, at least one of the two divisions occurs
after the ovum has left the gonad. Indeed in many cases the second division does not take place until after the egg has been entered by a spermatozoiin (Fig. 17). A comparison of the chief processes involved in
the development of the sperm and ovum is presented diagrammatically
in Figures 18 and 19.
The _Sex-Chromosome-s.—-We are now prepared to return to a
consideration of the exception in chromosomal behavior which was
MEIOSIS ' 31
Fig. 21.—Meiosis during the spermatogenesis of the squash-bug,
Anasa tristis, showing the behavior of the X-chromosome or idiochro~
mosome. From Kellicott (General Embryology). A, After Wilson,
others after Paulmier. A. Spermatogonium. Polar view of equatorial
plate showing twenty-one chromosomes (ten pairs, plus one). The
X-chromosome is not distinguishable at this time. B. Primary spermatocyte. Tetrads formed. C. Equatorial plate of first spermatocyte
division. X-chromosome divided. D. Anaphase of same division. The
daughter X-chromosomes have also diverged. E. Equatorial plate of
second spermatocyte division. F. Anaphase of same division. The Xchromosome lies, undivided, between the two groups of daughter
chromosomes. G. Late anaphase of same division. The undivided
X-chromosome has passed to the upper pole, lagging behind the
others. H. Telophase of same division. X~chromosome still distinct.
noted but not described at the end of the account of meiosis in the
sperm.
In the somatic and germ cells of many animals, both male and fe- ‘
male, there are found one or more chromosomes which in many cases
behave quite differently from their fellows. They often stain more '
deeply, and are especially peculiar in that they frequently remain in the
condensed condition during the entire growth period of the germ cells.
32 INTRODUCTION
On this account they sometimes appear at this time like nucleoli with
various distinctive shapes (Fig. 20). A150, during the 3“aPha5e stage
of cell division, they are noted for a tendency to lag behind on the
spindle (Fig. 21). One of the most striking things about these chromo
6'
 
Protenor E
5 .O.2.o"'">'
0.0:.‘ ‘l ll l 1 ll
5?.  -> ®
13? __,l1ifill'] E,
‘ ' list ..f'. _,
on \  @
HHS: 5'
 
Fig. 22.—A diagram of the behavior of the chromosomes during the
meiotic divisions in the male of Protenor belfragei. From Morgan
(Heredity and Sex, published and copyrighted by the Columbia University Press). The sex-chromosome throughout is represented in outline, the others in solid black. A. The chromosomes in the somatic
cell of a male. B. The chromosomes united in synapsis prior to the
first meiotic division of a germ cell. The single sex-chromosome is
without a mate. C. The first meiotic division, which for the sex—chromosome is certainly equational. D. The second meiotic division, “ reductiona1” for the sex—chromosome, i.e., the latter goes to one pole or
the other. It is impossible to say, certainly in this case, which division
is really reductional for the ordinary chromosomes (autosomes). E,
E’. The distribution of the chromosomes in the four spermatids resulting from the two meiotic divisions.
somes, however, is the fact that in some animals in the male, each somatic cell, as well as each unmaturated germ cell, possesses only one of
them, while each cell of a similar type in the female has two. Under
such conditions the one or two eccentrically behaving chromosomes are
termed X-chromosomes. In such cases it follows of course that in the
male the total number of chromosomes in each cell of the types indi
cated is odd, whereas in the female the number in each cell of a similar
type is even. ’
MEIOSIS ' 33
Thus in the male of the insect Protenor the somatic cells and the unrnaturated germ cells each possess 13 chromosomes, while similar cells
in the female have 14 (Figs. 22 and 23). Under such circumstances it
is obvious that when the male germ cell undergoes meiosis, its X-chro
Q Protenor
:. °
0.9 0° 9 0 0
Fig. 23. —A diagram of the behavior of the chromosomes during the
meiotic divisions in the female of Protenbr belfragei. From Morgan
(Heredity and Sex, published and copyrighted by the Columbia University Press). The sex-chromosomes throughout are represented in
outline, the others in solid black. A. The chromosomes in a somatic
cell of the female. B. The chromosomes united in synapsis prior to the
< first meiotic division of a germ cell. Note that in this case the sexchromosome has a mate. C. The first meiotic division, probably
equational, at least for the sex-chromosomes. D. The second meiotic
division, which, if the first division was equational, is presumably reductional. E. The distribution of the chromosomes in the two polar
bodies and the egg. The first polar body is represented as just under
going the second division.
mosome will be without a mate. Apparently as a result of this fact the
odd chromosome in the male only divides at one of the meiotic divisions, e.g., in the instance in question the first; and since this chromosome has not had a mate, its division must presumably be equational
(Fig. 22, C). Following the second division, the final result, as usual,
is four male germ cells, but their content is obviouslynot quite equal.
Two of them possess six ordinary chromosomes (autosomes), while
each of the other two possesses a similar six autosomes, and in addition
an X chromosome, i.e., a total of seven (Fig. 22, D, E, D’. E’).
INTRODUCTION
<3‘
Lygaeus
A D  :
3&3  ///i\\/'
0006.00
. 052909 / 
\ ,»///“ii/' @
0000000
0lfi°OCi
\
Fig. 24.——A diagram of the behavior of the chromosomes during the
meiotic divisions in the male of Lygaeus bicrucis. From Mor an (Heredity and Sex, published and copyrighted by the 3:"§:l!lm1la University Press). A. The chromosomes in the somatic cell of at male.
Note the large X and the small Y sex-chromosomes. B. The chromosomes united in synapsis prior to the first meiotic division of a
germ cell. The X and Y do not usually unite at this time so that it
is not indicated in the diagram (see Fig. 261. C. The first meiotic
division in this case, so fat as the sex-chromosomes go, is evidently
equational. D. The second meiotic division, which for the Ee!-Cl’ll‘0mosomes is evidently reductional. E, E’. The distribution of the chromosomes in the four spermatids resulting from the two meiotic divisions, two receiving an X-chromosome and two a Y.
In the female since there aretwo X~cht-omosomes in the germ cells
previous to meiosis each egg after meiosis ‘will contain an X. This will
also be true of course of the three polar bodies, but these being nonfunctional may be disregarded. Obviously, then, whether a fertilized
egg is to contain one X or two will depend upon whether it is united
with an X~bearing sperm or with one without an X.
There are numerous variations of this basic situation, the most com~
man one being the type illustrated by the insect Lygaeus. Here the
X-chromosome in the male does have a mate called the Y-chromosome,
but it is different from the X, in this instance smaller, and can thus be
distinguished from it (Figs. 24., 2Q, $6). A similar situation as regards
MEIOSIS 35
an X and Y pair of chromosomes occurs in Man. A slight variant of
this arrangement is seen in Drosophila, the fruit fly, where the mate of
the X in the male differs from it in shape rather than size (Fig. 27).
There are still other situations where the X and Y are quite similar in
appearance to each other, and even to the autosomes, but can be distin
Q Lygaeus
Zsffs
Ԥoo/?
A
E
\
Fig. 25. —A diagram of the behavior of the sex-chromosomes in the
female of Lygaeus bicrucis. From Morgan (Heredity and Sex, published and copyrighted by the Columbia University Press). A. The
chromosomes in the somatic cell of a female. Note the two X-chro-i
mosomes. B. The chromosomes united in synopsis prior to the first
meiotic division of a germ cell. C. The first meiotic division, probably
equational. D. The second meiotic division, probably reductional. E.
The distribution of the chromosomes in the two polar bodies and the
egg. The first polar body is just undergoing the second division.
guished from the latter by their behavior, as already noted. ln this last
case, where the X and Y are not visibly distinguishable from one another, there is of course no obvious difference between the chromosomal
condition in the male cell with its X and Y and in the female cell with
a double X. There is good evidence from other sources, however, that
even here fundamental qualitative differences do exist between the presumed X and Y chromosomes.
A more fundamental and striking variation in the relationships of
these chromosomes occurs in Moths, Birds, and some Fishes. Here it is
the female which has the odd chromosome, while the male has two of a
kind. Since this arrangement was first observed in the moth Abraxas it
is known as the Abraxas type. Also to avoid confusion the peculiarly
behaving chromosomes are here termed Z and W instead of X and Y.
INTRODUCTION
Fig. 26.——Division figures from the meiosis of the germ cells in
the male of Lygaeus bicrucis. After E. B. Wilson. A. A polar View
of the first meiotic division. In this insect the synapsis of the Xand Y-chromosomes not only does not occur while they are in a
threadlike condition, but is postponed until almost the end of the
first meiotic division. Even then it is evidently very slight,  indicated lay the figure. B. A side View of the second meiotic division
in the same animal. The chromosomes in this case do not lose
their identity during interkinesis (i.e., the interval lwtweeii the
two divisions), and it therefore is possible to determine that the
X and Y which united in synapsis 81 the end of the first division.
as shown in A, are now being separated from one another. Thus
for these chromosomes in this instance the second division is
clearly reductional.
9 <3’
JJ..k\ ..
I,\,  It
Fig. 27. -— From the Mechanism of Mendelian Heredity, after
Brildges. The female and male groups of chromosomes in Drosophila
Re ¢z)SJ{gasi.:er,_ showing the four pairs of aiitosome chromosomes plus
e pair in the female and the XY pair in the male. In this ani
afighe members 0i 93°11 Pair are usually found together as indiTHE SIGNIFICANCE OF MEIOSIS 37
It is then the ZZ combination which is found in the males and ZW in
the females. Because of the evident relationship to sex which these XY
or ZW chromosomes have, they are also termed sex-chromosomes.
Something more concerning this important relationship will be said in
a subsequent paragraph, but first a word is required regarding the entire ‘meiotic phenomenon as so far described.
THE SIGNIFICANCE OF MEIOSIS
It is assumed that the student is aware of the evidences from his study
of heredity and cytology that chromosomes are qualitatively different
from one another with respect to chemical entities called genes or determiners. These genes, as is well known, are distributed from one end
of a chromosome to the other, and with the exception of the sex chromosome in the male they normally occur in pairs. One member of a pair
of genes is in one member of a pair of chromosomes, and the mate or
allelomorph of that gene is in a corresponding position on the other
chromosome of that pair. Thus‘ it happens that at the reductional
meiotic division one complete haploid set of chromosomes, and hence
of genes, goes into one cell and another set into the other. The only
normal exception to this is the case of the sex chromosome in the XY
male, and the genes it carries.‘They go to one cell only. The non-reductional meiotic division is then similar to ordinary mitosis, and merely
doubles the number of cells containing haploid sets. Fertilization of
course involves the fusion of two germ cells, an egg and a sperm, and
obviously the reduction of the chromosomes and genes at meiosis prevents them from being progressively multiplied at successive fertilizations. How this ingenious state of affairs came about is not known, and
the speculations concerning it would take us too far afield in this text.
A further very significant parallel between the behavior of the genes
and that of the chromosomes is as follows: It will be recalled that in the
discussion of the heterotypic chromosomal figures of late diplotene and
diakinesis it was suggested that part of the explanation for such figures
was the fact that an exchange of sections had occurred between the homologus chromonernata (chromatids) of tetrads during the pachytene or
early diplotene. It now remains to add that genetic evidence indicates
that exchanges of blocks of genes, technically termed cross-overs, take
place somewhere during the interval when the pachytene and diplotene
stages are visible. The exact time is uncertain, but that these gene exchanges are in some way definitely related to the exchanges between
homologous chromoneniata is generally admitted as beyond doubt.
3;; ' INTRODUCTION
’ ssx DETERMENATION
It is known that the XY chromosomes, more particularly the X, also
carry genes and some of them apparently concern sex. Genetic evidence
7
V N 81
Fig. 28.—~Diagrsm to illustrate crossing over. From
Morgan (Mechanism of Mendelian Heredity). The white
and the black rods (a) twist
and cross at two points (1)).
Where they cross they are
represented -as uniting (shown
in c). That an interchange
of pieces has taken place in
the region between genes W
and Br is demonstrated from
the standpoint of inheritance
by breeding experiments. The
results of these are most
readily explainable on the
assumption that the gene M
has gone over to the other
chromosome.
from normal and abnormal cases itidicatcs
that the sex genes in the X-chromosome
tend to produce female characteristics, or
at least to produce the initial impulse in
that direction, while those in the autosomes tend to produce male Cll3I‘i1(‘I£3i'S.
This of course applies only to the nonAbraxis type of sex inheritance wlicre the
male contains the single X. Tin: sitnaticm
is evidently reversed in the other types.
Thus the determination of sex is a matter
of balance between two types of gene influence. Normally a diploid set of autosomes balanced against a single X pru«
duces a male, while the addition of another X is enough to produce a female.
All genes, however, produce their eficcts
by interacting not only with each other,
but with their surroundings. Thus we
know that various inherited tendencies can
be modified by the proper environment.
' So it should not be surprising that sex also
is subject to environmental influences. In
some animals, like Birds and Mammals,
it is rather hard to alter the surroundirigs
of the developing organism very rnuclt. In
other animals like Amphibians, however.
this is easily possible, and in such crea
tures various environmental changes have been tried. It has thus been
found that proper temperatures at critical periods (Witschi, ’29, see
Chap. VI) , and other appropriate procedures are able to reverse the sex
which a particular chromosome complex would have produced in a more
normal situation. Also changes in the internal environment, such as
3 endocrine secretions, might be expected to alter the development of sex
characters, and experimental evidence shows that this is true, not only in
Amphibians, but In both Birds and Mammals.
ERTILIZATION AND EARLY STAGES IN "DEVELOPMENT
FERTILIZATION
B EFORE proceeding to an account of development in any par-'
ticular animal, it may be well to discuss certain processes which are always involved, and to note the chief methods of their occurrence.
rtilization in all hitvher forms consists of the union of
n; This union may occur within some cavity of the female
into which the sperm have been introduced, or it may occur outside.
The latter is the more common method among animals which live in the
water. In either case, thousands of the relatively minute sperm are required to insure the fertilization of each single egg by one spermatozoon. We shall now turn to a generalized account of the process.
PENETRATION
The Action of the Sperm. —— Both eggs and sperm contain certain
substances similar to hormones, hence called gamones. Those in the
sperm are androgamones, one which prevents premature excessive sperm
activity thus conserving their energy, and another which dissolves the
gelatinous membrane surrounding many eggs. Those in the egg, on the
other hand, are gynogamones, one of which, at an appropriate time,
counteracts the first androgamone, thus increasing sperm activity, and a
second which makes the sperm heads sticky, causing them to adhere to
the egg surface. In addition, some eggs may secrete something which attracts sperm. Penetration of the egg may take place at any point of the
surface, or the sperm may enter through a special orifice, the micropyle.
Usually only one sperm enters (monospermy), and in case more do so
development is generally abnormal. Sometimes, however, in relatively
large yolked eggs, several sperm normally enter, a phenomenon called
polyspermy. Even in such cases only one of the spermatozoa takes active
part in the further events of fertilization. The remainder eventually degenerate and disappear; previous to this they may divide several times,
and perhaps aid in breaking up the yolk to make it more assimilahle.
4o, FERTILIZATION, EARLY DEVELOPMENT
In such cases they are referred to as merocytes. The method by which
the extra sperm are excluded in the event of monospermy will be discussed presently.
As soon as the head of the sperm has punctured the surface of the
egg the swimming movements of its tail cease. In some cases the latter
, e is regularly drawn into the egg along with the head and middle piece,
while in others it is left outside. In either event it soon degenerates and
takes no more part in the fertilization process.
The Reaction of the Egg.
The Perivitelline Space and the Fertilization Membrane. —— Probably
the first and most characteristic reaction of almost all eggs to puncture
by a sperm is the formation of a space between the egg surface and its
innermost covering (i.e., in most instances the vitelline membrane) . lt
is called the perivitelline space and seems in some cases to be due to the
pushing away of the membrane by a secretion from the egg. In other
instances it may be due to shrinkage of the egg or to absorption of
water by some substance between the membrane and the egg surface.
In any event such a separation of the egg from its covering of course
makes the latter more conspicuous, and even in such eggs as have seemed
previously to lack a membrane, one now becomes visible. Because of
this increased visibility following fertilization, the membrane about the
perivitelline space, whether it be the original vitelline membrane, one
apparently newly formed, or a fusion of both of these, is frequently
called henceforth the fertilization membrane (Fig. 46, D). The significance of the phenomenon just noted is not well understood. It was
thought at one time to aid in preventing polyspermy. Since eggs from
which the membranes have all been entirely removed continue to be
impervious to further fertilization, however, it is evident that this condition is not the result of the existence or the location of any membrane. It has also been maintained that the obvious alteration in position of the membrane is accompanied by increase in its permeability to
gases and other substances. That‘ there is considerable basis for this
belief is indicated by the fact that in some instances there is a decided
increase in oxidative processes and other phenomena requiring such a
change.
The Changes in the Egg Cytoplasm. ——Aside from these phenomena
connected with the inner egg membrane, fertilization also initiates certain other changes in the egg proper. Almost simultaneous with the
appearance of the perivitelline space there is frequently evident an out. of the sperm which it contains are apparently drawn down into the
PENETRATION 41
Fig. 29.——Enu-ance of the spermatozoiin in the fertilization of the Annulate, Nereis limbata. From Kellicott (General Embryology). After
Lillie. A. Spermatozoon. B. Perforatorium has penetrated egg membrane;
entrance cone well developed. Fifteen minutes after insemination. C.
Thirty-seven minutes after insemination. D. Entrance cone sinking in
and drawing the head of the spermatozoiin after it. Forty-eight and onehalf minutes after insemination. E. Head drawn in still further. Fortyeight and one-half minutes after insemination. F. Entrance completed.
First meiotic division in anaphase. Fifty-four minutes after insemination.
The middle piece, as well as the tailnremains outside.
c. Head cap. e. Entrance cone. h. Head of spermatozoiin (nucleus). m.
Middle piece. p. Perforatorium. v. Vitelline membrane. 1. First polar division figure.
pushing of the cytoplasm at the point where a spermatozoéin has penetrated the fertilization membrane. This protuberance is then entered
by the sperm, and because of this fact it is often termed the entrance
cone (Fig. 29, B). Following these events both the cone and the parts
deeper egg substance ( Fig. 29, C, D, E). Besides this somewhat localized activity on the part of the cytoplasm, however, there are.alse—evidances of other efiects which seem to he more widespread. Thus, since
Fig. 30. -—Total views of the egg of Tunicate Cynthia partita, showing (‘l111!1§:f'fi in
arrangement of materials of egg subsequent to fertilization. From Kr-lli<-on Werneral Embryology). After Conklin.‘ x 200. A. Unfertilized egg, before fading out of
germinal vesicle. Centrally is gray yolk; peripherally is protoplasmic layer with
yellow pigment, and surrounding egg, the test cells and clmrirm. B. Almut lire
minutes after fertilization, showing streaming of superficial layer of prntuplo-em
toward lower pole where spermatozoon enters, and consequent exposure of gray
yolk of upper hemisphere. The test cells are also carried toward lower pnlt-. C.
Side view of eggs showing yellow protoplasm at lower pole: at upper pole at small
clear region where polar bodies are forming. The location of sperm prnnucleus
(nucleus) is also indicated. D. Side view of egg shortly before first cleavage, showing posterior collection of pigmented protoplasm (yellow crescent) and clearer area
above it. E. Posterior view of egg during first cleavage, showing its relation to the
symmetry of egg. ‘
a. Anterior. c. Clear protoplasm.
layer, with yellow pigment. g._u.&3 ' Jge
Polar bodies. t. Test cells. y. Ydk
0“ Sperm nucleus. "'4?
 
w crescent. e. Exoplasm or cortical
e. 1:. Chorion. p. Posterior. p.b.
0 terial). y.h. Yellow hentisplrerc.
‘D
FERTILIZATION: LATER STAGES 43
polyspermy is not prevented by the fertilization membrane, it is held
that such prevention may be due to a general alteration in the egg
cytoplasm.
More specifically, according to one theory the entrance of the sperm
is made possible by the interaction of a substance in or on its head with
another substance on or near the surface of the egg. This latter substance
is called fertilizin, and such part of it as is not used up in the interaction with the sperm is supposed to be immediately eliminated by interaction with another substance called antifertilizin. This latter material is thought to be located more deeply within the egg cytoplasm, and
is brought into contact with the fertilizin by a rearrangement of the egg
materials produced by the entrance of the sperm. All the fertilizin having thus been eliminated, no f_urther fertilization is possible (Lillie,
’19). Though this explanation of events is still theoretical there is considerable experimental evidence for it in certain organisms. Also,
whether or not this be true, evidence is not wanting that in some cases
at least, all of the egg cytoplasm is profoundly disturbed by the sperm
entrance. It seems likely indeed that this is more or less true of all egg
but the disturbance is particularly obvious in certain instances because
in these instances different regions of the egg cytoplasm are diflerently
colored and thus distinguishable. In such eggs it has therefore been
possible to observe that, following fertilization, a sudden and marked
rearrangement of these parts of the cytoplasm takes place. Such, for example, is the case with the egg of the Tunicate, Cynthia (Styela) partita
(Fig. 30), and also with that of Amphioxus (see below).
THE LATER STAGES
The later steps in the fertilization process which are now to be described are all more or less directly connected with the fusion of the
nuclei of the sperm and egg.
The Egg Nuc1eus.———The meiotic divisions of the egg are some-l
times entirely completed previous to’ fertilization. More usually. however. as in the case of most Vertebrates, only one of these divisions
occurs before the sperm entrance, and in some instances (e.g., Nereis)
both are delayed until after this event (Fig. 32, B, C ). In these cases
where meiosis has not begun, or is unfinished prior to the penetration
of the sperm, the latter event seems to act as a stimulus which causes
the meiosis to proceed. As soon as it is completed the egg nucleus is defi
nitely formed, and the centrosome which took part in .the second division disappears. ‘
44 FERTILIZATION, EARLY DEVELOPMENT
Fig. 31.-—A generalized diagram of the penetration of the sperm and the fusion
of the egg and sperm nuclei, the haploid number of chromosomes being assumed
in this case to be two. The trail of pigment marking the path of the sperm actually 7
occurs only in the case of the Frog’s egg. The egg membranes are not represented.
Compare the stages with those in Fig. 32 showing corresponding processes in the
egg of Nereis.
.-A. The first polar -body has been given off, and the second meiotic division is in
progress. The sperm head and middle piece have entered the egg, leaving the tail
outside. B. The first polar body has divided and the second has been given off,
while the completed egg nucleus has started to move toward the center of the ovum.
The sperm nucleus consisting of the sperm head has enlarged somewhat, has partially rotated, and is also moving toward the center of the egg. The new divisioncenter has appeared in the region of the middle piece. C. The two nuclei are enlarging and approaching one another. The sperm nucleus, having completed its
‘ rotation, has altered the direction of its movement somewhat (not always neces
sary), to hasten their meeting, and the division-center is dividing into two parts.
D. The nuclei, each containing the haploid number of chromosomes, have started
to fuse. The division-centers, each consisting of a centriole and centrosome and
stfirrfitinded by its aster, have taken up their places preparatory to the first division
o t e egg. ,
cp. Copulation path. ec: Entrance cone. en. Egg nucleus. ep. Entrance path. h.
Head of sperm. m. Middle piece of sperm. ms. Meiotic spindle of the second
meiotic division. pbi, pbz. First and second polar bodies. sn. Sperm nucleus. 1:.
Tail of sperm.
FERTILIZATION ‘ 45
Fig. 32.——Photomicrographs of sections of Nereis eggs, showing stages in fertilization meiosis and cleavage. The photographs were made in the Anatomical Department of Western Reserve University Medical School from specimens presented
to that department by Professor 0. Van der Stricht, and are reproduced by the
courtesy of Professor Van der Stricht and Dr. E. W. Todd.
A. At the top of the figure the spermatozoon is shown just entering the egg; The ,
egg membrane is broken, and separated from the egg‘ at various points. B. The first
meiotic division spindle. C. The first meiotic division has been completed, and the
first polar body lies outside the egg beneath the egg membrane. it appears at the
top of the figure and slightly to the right. Just within the egg in the same vicinity
is the second meiotic spindle, while at about the center of the egg is the sperm
head with its aster in front of it. D. The egg and sperm nuclei in the upper left
hand part of the egg are fusing, while just beneath the egg membrane is one of the
polar bodies. E. The division spindle for the first cleavage. F. The first cleavage is
completed and parts of the asters for the second cleavage are indistinctly visible
in the two daughter cells. ~
46 FERTILIZATION, EARLY DEVELOPMENT
The Sperm Nucleus and the Division-Center. —— While this
completion of the meiotic divisions is taking place, the head and the
middle piece of the sperm advance into the egg.‘ Also, as this u(:cux's
these parts rotate through an angle of 180° so that the middle piece is
in the lead (Fig. 31, A, B). The advance then continues along a course
whose first portion is called the entrance or penetration. path, and
which, in the case of the Frog, is marked by granules of pigment. Meanwhile the acrosome which etiected the entrance of the sperm has disappeared, while marked changes are also taking place in the nuclear pnl‘~
tion of the head and the middle piece. The former is cnlmgirig. and
within it the chromatin is forming a typical nuclear reticulum. in the
region of the middle piece, on the other hand, a rrentriole and u.-utmsome appear and are presently surrounded by a small astcr. it has lwvn,
claimed that this centriole is identical in whole or in part with the contriole (or one of the centrioles) which entered the middle piece during
the transformation of the spermatid. This is very doubtful, and in many
cases is certainly not true. It does seem, however, that in most instances
the new division—center at least arises under the influence of the middle
piece.
The Fusion of the Egg and Sperm Nuclei. — Previous to or during the above processes, the second meiotic division of the Pgg has been
concluded, and the egg nucleus has moved from the periphei _v of the
cell into approximately the midst of the active cytoplasm (Fig. 31, D;
Fig. 32, D). Of course in telolecithal eggs with a large yolk, this point
will be just below the surface of the animal pole. rather than at the
actual center of the egg. The new sperm division-center and nucleus,
which have meanwhile been advancing along the penetration path. now
move directly toward the egg nucleus. This in many instances may involve a slight change in the course of the sperm, and when such is the
case the latter portion of its course is termed the copulation pat}: as distinguished from the first portion or entrance path (Fig. 31, C ) .
As the nuclei meet each other their membranes disappear. Also there
has appeared in each the haploid number of chromosomes "' I'l’i,r_r,. 31,
C, D). Meanwhile the sperm division-center and aster divide, if indeed
they have not already done so, and form a typical division spindle.
Upon this spindle the restored number of chromosomes arrange the-.m~
1 In some instances; e.g., Nereis, the middle piece, as well as the tail, remains
outside.
3 In many cases the chromosomes are not actually visible as such until after the
fusion of the pronuclei. In these instances the number appearing in the single
fusion nucleus is then diploid as would be expected.
CONSEQUENCES . OF F ERTILIZATION 47
selves, and each is then divided in the usual manner preparatory to the
first cleavage of the egg (Fig. 32, E). It should be noted that in this
process there is no fusion of the chromosomes. On the contrary, this
event, presumably the actual climax of the entire phenomenon, does not
occur until the period of synapsis in the germ cells in the new individual, as described above.
THE CONSEQUENCES OF FERTILIZATION AND THEIR
IMPORTANCE
We may now consider briefly some of the apparent results of this
process and their possible importance. There have been three main
consequences of fertilization which have been held to be of vital signifi
cance, though as will appear, none of them has proved to be necessarily
dependent on this phenomenon. They are as follows:
I. Reproduction. —— It has been said that the chief result of fertilization is to bring about reproduction, (a) by restoring the diploid number of chromosomes, and (b) by furnishing or causing to develop a
new kinetic division-center. This argument is unsatisfactory for the following reasons:
1. Granting that these events take place in connection  reproduction, the answer is, nevertheless, superficial. For the question immediately arises, why should the egg lose half its chromosomes and its
division-center, thus making fertilization necessary before reproduction
can occur?
2. There are numerous cases of both artificial and natural parthenogenesis, showing that neither the extra chromosomes nor the new divi'sion-center is absolutely necessary.
3. Finally the fact that the union of two cells so frequently precedes
reproduction may be explained thus. Let us assume that there is some
reason, such as those indicated below, why a mixture of different strains
of protoplasm is beneficial. It then follows that in a Metazoan, the only
time such a mixture _can possibly occur is when the protoplasm of the
animals concerned is in the form of single cells, i.e., the germ cells.
Then since the animals are in fact Metazoa, the union of the germ cells
must eventually be followed by cell division in order that the Metazoan
condition may again be reached. Under such’ circumstances, the multiplication obviously is not proved the result of the fertilization.
II. Rejuvenescence.-—It has been widely held that the fusion of
different strains of protoplasm which occurs during fertilization is necessary to bring about a revivifying of any given race of animal or plant.
48 FERTILIZATION, EARLY DEVELOPMENT
Without this, it is held, cell division will gradually become less frequent, and will finally cease. The chief argument for this view has been
furnished by certain experiments on Protozoa. Thus, Calkins C19)
seemed to prove this by work with Paramecium, although earlier studies
by Woodruff (’14) had appeared to show that some strains could. be kept
going indefinitely by an internal reorganization called erzulonzrxzs. Later
work by Jennings (’4-44), Sonneborn ,('39), and others has shown the
situation to be even more complicated than had first appeared. Thus, con—
jugation sometimes prolongs the life of certain lines. and sometimes
not. At all events it is evident that the mixing of different strains of
protoplasm is at least not universally necessary for revitalization.
III. Variation.——Fundamentally, of course, variation depends
upon changes in the genes. As modern genetics has shown, however,
the actual appearance of these variations in an animal or plant may
sometimes depend upon the shuffling and recombinations of the genes
which meiosis and fertilization bring about. Also in some instances
significant variations may result from the abnormal behavior of whole
chromosomes or sets of chromosomes, which in a few instances is definitely known to have produced new species. Weismann was entirely
ignorant of the details of all these processes as now understood, but he
did have some rather elaborate theories concerning normal meiosis
and fertilization. He termed the recombinations of genetic determiners.
which he correctly believed came about through these latter events,
amphimixis, and he considered that variations so caused were an important source of material upon which natural selection might act.
Others, e.g., Hertwig, believed that the shuflling and recombining processes tended to cancel out the effects of gene mutants and thus helped to
keep the race constant. As a matter of fact it is now clear that both
points of view are correct in different‘ cases. It also appears that evolution could occur without the fertilization process, though probably not
so rapidly.
Conclusion. —— In view of the above facts, the general conclusion as
to the function of fertilization may perhaps be stated thus: While it
seems reasonable that the process is an important one in view of its
wide occurrence, we do not as yet understand its full significance. lt
does appear likely, however, that recombinations of genes favorable to
renewed vigor, and also to production of -variations, are involved. Advantages of this nature, while not essential for life, may well have been
great enough to have favored the evolution of sex and the correlated
phenomenonof fertilization.
GENETICS AND EMBRYOLOGY 49
EARLY STAGES IN DEVELOPMENT
RELATIVE INFLUENCE OF EGG AND SPERM ON. THESE
STAGES
In the above discussion of the germ cells it has been stated that despite the great disparity in the cytoplasmic content of the ovum and
sperm, their influence upon development is approximately equal. The
abundant egg cytoplasm is simply for the purpose of supplying food
and material for the nuclear factors to work upon, and varies according
to requirements in these respects. The sperm cytoplasm, on the other
hand, is only for the purpose of bringing its nucleus to that of the inert
egg, and possibly of initiating division. Indeed the very features which
characterize the cytoplasm of a particular egg or sperm are presumably
determined by genes within the chromosomes, just as are the features
which characterize the adult animal.
Nevertheless, it must now be n_oted that the character of the egg cytoplasm does determine in a rather obviously mechanical way, and apparently sometimes in more subtile ways, the nature of the early stages
in development which we are about to consider. The cytoplasm of the
sperm, however, though often strikingly variable in form, is apparently
without any such influence. Because of this fact, in the case of most of
the animals whose embryology is to be studied, it will be necessary to
give a rather full account of the ovum and its development. The various
kinds of spermatozoa, on the contrary, will need little further attention.
RELATION OF GENETICS AND EMBRYOLOGY
Before proceeding with a general description of the first steps in development, it is perhaps pertinent to say a few words at this point concerning the relationship between the field of genetics on the one hand
and that of embryology on the other. This text deals primarily with
the latter, yet the term gene or determiner has been frequently employed, and quite evidently these entities are supposed to be significant
controlling elements in development. As a matter of fact the subject
matter of these two disciplines, i.e., genetics and embryology, like that
of physics and chemistry, is becoming constantly more interrelated. In
the earlier days of these subjects the geneticists were more concerned
with showing how genes were distributed during the reproductive proc- -
ess. They also sought to prove that their occurrence in certain combinations always resulted in the appearance of certain;  the
. V .,
I  r""' ““‘ V?‘
A./, ‘--l /" -\ I‘
50
FERTILIZATION, EARLY DEVELOPMENT
Fig. 33.—Cleavage in the Sea-urchin, Strongylocentrozus lividus.
From Jenkinson, after Boveri. Animal pole uppermost in all cases.
a. Primary oiicyte surrounded by jelly, and containing large germinal
vesicle with nucleolus. Pigment uniformly distributed over surface. 1).
Ovum after formation of polar bodies. Pigment forms a band below the
equator. c, 41. First cleavage. e. Eight-cells. Pigment almost wholly in
lower quartet (vegetative blastomeres). f. Sixteen-cells. The lower
quartet has divided latitudinally and unequally, forming four micromeres at the vegetal pole; the upper quartet has divided meridionally
forming a plate of eight cells. g. Section through blastula. h. Later
blastula, showing formation of mesenchyme at lower pole. i, j, 1:. Three
etages in gastrulation, showing the infolding of the pigmented cells to
form the hypoblast (archenteron). In j the primary mesenchyme is
separated into two masses, in each of which a spicule is formed (k).
In k_ the secondary, or pigmented, mesenchyme is being hudded ofl from
the inner end of the archenteron.
GENETICS AND EMBRYOLOGY 51
Fig. 34.-—Meroblastic cleavage in the Squid, Laligo pealii. A, B. Egg
viewed obliquely, showing animal pole. x 45. From Kellicott (General Embryology).Jifter Watasé. C, D. Surface views of animal pole, more highly
magnified, to show bilateral arrangement of blastomeres. From Wilson,
“ Cell,” after Watasé. A. Four-cell stage. B. About sixty cells. Cells at the
animal pole very small, lowermost cells incomplete, cell walls extending
down toward the uncleaved lower pole. C. Eight-cell stage. D. The fifth
cleavage (sixteen to thirty-two cells).
a—p. Marks the plane of the first cleavage and the median plane of the
organism. l—-r. Marks the second cleavage, and the transverse plane of the
organism.
adult animal or plant.'The embryologists, on the other hand, were
occupied mainly with describing the steps in development. Presently,
however, both groups came to ask the question: How do the genes act
to produce their end results? This has led to a rapid rapprochement between the students of the two fields. The geneticists have tried to find
out how genes interact with each other and with their cytoplasmic environment to cause the development of the adult characters. Also, as
already suggested, the embryologists on their side have ceased to be
interested in merely describing what happens, and are now actively engaged in experiments to find out how it happens. Thus both groups are,
52 FERTILIZATION, EARLY DEVELOPMENT
so to speak, approaching the same goal from opposite sides. When they
meet, and we know how all the genes act to produce all the end results,
the problems of embryology will be solved. Meantime, enough remains
to be done from both directions to keep us all busy for a long time.
 
 
C
Fig. 35.--Cleavage in the Sea-bass, Serranus amzrius. From H. V. Wilson. A.
Surface view of blastoderm in two-cell stage. B. Vertical section through four-cell
stage. C. Surface view of blastoderm of sixteen cells. D. Vertical section through
sixteen-cell stage. E. Vertical section through late cleavage stage.
c.p. Central periblast. m.p. Marginal periblast. s.c. Segmentation cavity (blastecoel).
SEGMENTATION
Subsequent to the first division of the egg which has been indicated,
further divisions follow each other, often in relatively rapid succession.
The period of these early divisions is termed that of segmentation or
cleavage.
Types of Cleavage.—-As has been suggested above, the type of
cleavage is largely determined by the nature of the egg cytoplasm,
particularly as regards the amount and distribution of the yolk which
the latter contains. In a homolecithal egg with relatively little yolk, the
cleavage is total or holoblastic, and approximately equal (Fig. 33)
GASTRULATION 53
The equality in the size of the cells decreases, however, as the amount
of yolk increases. This follows from the fact that where there is much
yolk present, it is never equally distributed. Instead it gathers on one
side, i.e., the vegetal side, so that the ovum becomes telolecithal. Then
since yolk-filled cytoplasm divides with more difliculty than cytoplasm
that is free from ‘yolk, inequality of division necessarily results. It is
termed simply unequal cleavage (Fig. 61). Finally in cases where the
amount and density of the yolk is very great, as in many Fishes and
Birds, that part of the egg which contains it does not cleave at all, or
only very slightly. In such eggs, as already noted, the yolk-free cytoplasm exists only as a small accumulation at the animal pole of the
em called the blastodisc. It is then chiefly this disc which divides; after
DO’
division it is called the blastoderm. Cleavage of this type is known as
meroblastic, or discoidal (Figs. 34, 35).
The Blastula.-— After cleavage has continued for a time in an egg
of the homolecithal type a hollow sphere of cells results, with a cavity___
at or near its center (Figs. 33, g; 36, A). Such a sphere is called a blas- 7
tula, and the cavity at its center is termed the segmentation cavity, or
blastocoel. In eggs of the markedly telolecithal type there also exists at
' the completion of cleavage a sphere, but in this case, as has been noted,
the greater part of it consists of undivided yolk. It is nevertheless
termed a blastula, and the segmentation cavity will lie at the animal
pole between the largely unsegmented yolk mass and the blastoderm
(Figs. 35, D, E; 37, A). Although cell division continues the cleavage
stage may be said to end when the blastula condition has been reached.
GASTRULATI ON
Gastrulation, as the name implies, has to do with the formation of
the primordial gastric or gut cavity called the archenteron. In many
cases this cavity is entirely separate from the blastocoel from the beginning of its formation, but in others complete separation comes later. In
any event in addition to the formation of the gastrular cavity the process also usually involves the setting‘ apart of two of the three primordial
germ layers with which all higher animals start their differentiation.
These first two layers are sometimes referred to as the ectoderm and
enzloderm, the former being on the outside and the latter lining the
archenteron. This, however, is not quite correct because the thirdlayer,
called mesoderm, to be referred to presently, is necessarily derived from
one or the other or both of the two already formed. Hence at least one
of these is really ‘more than ectoderm or endoderm for it contains the
54 FERTILIZATION, EARLY DEVELOPMENT
elements of the mesoderm. Therefore the one from which the third is derived in cases where this origin is clear, is often temporarily termed
mesectoderm or mesentoderm as the case may be. Another pair of terms
frequently applied to these two layers are eptblast for the outer layer
and hypoblast for the inner one. These terms are noncommittal so far
as indicating which is to give rise to mesoderm, and it is therefore convenient to use them, up until the time that this last-named layer appears.
After that each of these layers can be referred to by its definitive name,
ectoderm, mesoderm, and endoderm. This is the procedure which will
be followed in this text. It should be further added that in some Invertebrates, like the earthworm, the mesoderm actually arises before gastrulation by the budding off of cells into the blastocoel. After this budding off of the mesoderm, the remaining wall of the hlastula might then
be called ectoendoderm, since it is this wall which later becomes differentiated into definitive ectoderm and endoderm during gastrulation.
Among Vertebrates, however, events appear to be always in the order
indicated. _
Gastrulation having been thus defined, it now becomes necessary to
indicate briefly and in a general way the processes through which it
may occur. For the sake of clearness and convenience these processes
will be described separately, though it should be noted that in the majority of actual cases two and often more of them take place together.
Invagination. — Probably the simplest method of gastrulation is by
invagination, a method which is sometimes spoken of as being typical.
As_a matter of fact, however, the accomplishment of gastrulation by
this means alone is rather exceptional even among the Invertebrates,
and among the Vertebrates it never occurs to the exclusion of other
methods. Indeed within the latter phylum it is found in a relatively unmodified form only among a few of the very lowest members of the
group. In all the higher animals it is very largely altered and aug
’mented by other means, and in many instances appears not to be present at all. In its simplest and most unmodified condition, however, it
may be described _thus:
Let the blastula be thought of as a hollow sphere, "one hemisphere of
which is to be regarded as the animal half and the other hemisphere as
the vegetal half, while the cavity within the sphere is the blastocoel
( Fig. 33, g; 36, A). Now, imagino the vegetal half.to be pushed in or
invaginated until it almost touches the animal half opposite to it. The
sphere has thus become a gastrula. The original blastocoel has been
virtually obliterated and a new cavity has been formed by the imaginaGASTRULATION M 55
tion. This is the archenteron, and it is lined by the original vegetal cells
which may now be termed hypoblast (Figs. 33, k; 36 B). The cells which
constitute the animal hemisphere, on the other hand, are now called
epiblast. The opening of the archenteric cavity to the exterior is then in
this case the blastopore, and the rim of this opening the lip of the
blastopore. It must be immediately stated, however, that only in, eggs
of a relatively yolkless character, is the blastopore thus a wide-open
orifice. As the amount of yolk increases it tends to fill both the archen
Fig. 36.—Diagrammatic representation of gastrulation by invagination.
A. Ideal meridional section of a blastula. B. Ideal meridional section of a
gastrula. (1. Animal pole. arrh. Archenteron. blast. Blastocoel. bl. Blastepore. ep. Epiblast. hyp. Hypoblast. lp.b. The lip of the blastopore or germ
ring. 21. Vegetal pole. The cells at the vegetal pole are usually larger because they contain more yolk.
teron and its opening more and more, until in eggs of the extremely tel- t
olecithal type there is very little left of the archenteron as a cavity or
of the hlastopore as an openinu. Thus in eggs of this sort the boundary
of the blastopore, i.e., the blastoporal lip, is really the edge of the
blastoderm. To cover all cases, therefore, it is perhaps better to describe
the lip of the blastopore as the line of undifferentiated tissue where
epiblast and hypoblast merge with oneanother. This description it will
be found applies to the edge of the hlastoderm asxwell as to the rim of
a blastopore which possesses a wide opening, It» may now be added that
the lip of the blastopore is also often called by another name, i.e., the
germ ring. The reason for this is the fact that it was once thought that
a very large portion of each side of the embryo always originated from
this ring in a manner to be described below (see concrescence). A further word will be said on this topic when the latter process is discussed.
56 FERTILIZATION, EARLY DEVELOPMENTT
Invc1ution.——A second process of gastrulation may be described
as involution or inflection. It is very common among the Vertebrates,
and, within this group at least, it probably always accompanies any invagination which may occur. In many cases also it appears to be the
chiefifactor involved, particularly among forms arising from a telolecithal egg. Therefore we shall study involution in a telolecithal egg.
blast. bld.
 
A B
Fig. 37.— Diagrammatic representation of gastrulation by involution in
the case of an egg with a large yolk mass which does not segment. A. Ideal
meridional section of a blastula. B. Ideal meridional section of a partially
completed gastrula, bisecting the dorsal blastoporal lip. arch. Archenteron.
blast. Blastocoel. bld. Blastoderm. ep. Epiblast. hyp. Hypoblast. lp.b. The
lip of the blastopore. The arrow points to the blastopore, and indicates the
movement of involution.
In such eggs it has been noted that the yolk usually does not segment
at all, and that in correlation with this the blastocoel will be greatly
reduced (Fig. 37, A). Under such conditions it is evident that gastrulation cannot occur by simple invagination because the mass of yolk
filling the center of the blastula will not permit it. What does happen, therefore, is this: At some point on the edge of the blastoderm (see
above), the dividing cells, instead of extending out over the unsegmented yolk, begin to be turned over the blastodermal rim, i.e., involzited into the segmentation cavity. These inturned cells then constitute the hypoblast, while those which remain without are epiblast ( Fig.
37, 3). According to definition, therefore, the edge of the rim, in this
case the edge of the blastoderm, is the blastoporal lip or germ ring,
while the movement over this lip is designated as involution. As suggested above, however, this process is not confined to animals with a
large yolk mass, and it is to be clearly understood, therefore, that the
GASTRULATION 57
only essential feature concerned is the passage of cells over the lip. It
is this movement, which, as stated, comprises involution, and this remains true whether the active cells be arranged in the form of a blasto
derm or otherwise. In some instances where the yolk mass is very great,
as in many Fishes, the movement is accompanied by no invagination. In
others (Amphioxus and Amphibians), the latter process also takes
place to a greater or less extent. In any event the inflecuon or involu4
eplblast archenzeron infiltrating
blasroderm hypobhfl
;,,-:m.+-rat-s:a._,,“
V .
     
A B
Fig. 38.———Diagrammatic representation of gastrulation by infiltration in
the case of an egg with a large yolk mass which does not segment. A. Ideal
meridional section of a blastula as in Fig. 37. B. Ideal meridional section
of a partially completed gastrula, showing some of the cells of the blaste
derm creeping inside the former blastocoel, and spreading out there to
form the hypoblast.
tion is most active in that portion of the blastoporal lip which eventually proves to be dorsal. The degree and character of its occurrence in
other parts of the lip vary considerably in different animals, and can
best be indicated later in specific cases. .
Mechanisms Concerned in Invagination and Involution. —— Before proceeding to a description of the next methods of gastrulation, it
seems well to pause here to consider the possible mechanisms involved
in the processes already described. As has been indicated the essential
feature in either invagination or involution is the movement of cells
over or around an edge or lip. This type of movement, moreover, is an
important aspect of various other cell rearrangements in embryology,
as for example in the enterocoelic formation of mesoderm and the de
velopment of neural folds to be described later. Hence an effort to discover the mechanism involved here has been one of the important points
of attack by the experimentalists. What makes a ball of cells invaginate?
What makes cells roll over a margin? The answer seems to be that it is
_.—r"
53 FERTILIZATION, EARLY DEVELOPMENT
\due to a change in the shape of the cells as suggested long ago by Rhum.
bler, Butschli, T. H. Morgan and others. This can be easily understood
if one imagines a hollow ball of cells such as depicted in Figure 36. If
one notes especially the bigger cells in this figure it is clear that they
are larger atutheir outer ends. It is also clear that so long as they retain this shape :'t will be very difiicult or impossible for them to roll inward. If. however, the cells at 0116 P013 °f the 883a 0’ in the case Of tel‘
troph. icm.
 
Fig. 39.—Diagrammatic representation of gastrulation by delamination.
A. Ideal meridional section of a blastula, or as it is called in Mammals,
the blastocyst. B. Ideal meridional section of a gastrula. arch. Arehenteron,
as yet only partially lined by endoderm and lacking a blastopore. blast.
Blastocoel. ep. Epiblast. hyp. Hypoblast. icm. lnner cell mass, virtually
homologous with the blastodenn of blastulas with much yolk. rroph.
Trophoblast, an embryonic layer peculiar to Mammals. t, See chapter XIV.)
olecithal eggs, at the blastoporal lip, should become smaller at their
outer ends, the case would be difierent. Then their tendency would be
to behave just as they actually do behave in invagination or involution,
l.e., to 1‘0'll inward around the margin of a lip. That this is what occurs,
seems now to be quite evident. The question remains, however, as to
what makes cells in such situations change their shape. Here experiment
is still seeking a complete answer. However, according to some investigators it is most probably due mainly to a higher alkalinity of the
blastocoelic fluid. This in turn causes a change in surface tension in
different regions of the cell membranes of the cells concerned (Holtfreter, ’44, Lewis, ’47). Thus if the tension at the inner ends of these
cells became relatively less than at their outer ends, the inner ends
would tend to become larger. One can and must of course then go still
further back and ask why the tension changes in these cells and not in
GASTRULATION I 59
others. This and related questions have not all been satisfactorily an
swered, but their asking points the way in which investigation must
proceed.
Infiltration. ——Heretofore this process has not been recognized as
.a method of gastrulation. Recent investigations on the Chick, however,
seem to indicate that possibly such a term is appropriate to describe
what takes place there and'perhaps also in the Mammal. In any case it
involves simply the inwandering or infiltration of cells from the blastederm, or its homologue, into the space beneath (the blastocoel). This
space may or may not be largely filled with yolk. In the Chick of course
it is so filled, while in the Mammal it is not. In either event the cells
thus originating soon spread out to form a continuous layer of» hypoblast, and the former blastocoel becomes the archenteron. The infiltration process, if and where it occurs, is, like invagination and involution,
probably -due to the change in shape of some of the cells of the original
layer. Each cell concerned, becoming larger at its inner end, tends to
form, as it were, a sort of pseudopodium, and crawl into the blastocoel
(Fig. 38).
Delamination. —= A fourth process by which gastrulation may occur
is that of delamination, and so far as Vertebrates are concerned it has
been supposed to take place most typically in Mammals. However, just _
as. infiltration may be involved to some extent in this group, so may
delamination occur to a certain degree in the Birds. According to
Brachet, delamination of a sort also plays a small part in a rather special manner in the gastrulation of the Amphibian. This "will be considered more fully when we come to the Frog. At any rate the process,
wherever it may occur, consists simply in the separation or splitting ofi'
of cells from a pre-existing layer or mass. These cells then become confluent, as in the case of those derived by infiltration, to form the hypoblast (Fig. 39).
It should be noted that where gastrulation occurs wholly, or almost
wholly, by either infiltration or delamination, or both, no real blastepore exists, at least at first, and hence apparently there can be no blasteporal lips. It will be recalled, however, that the blastoporal lips have
been defined in general as the region where the epiblast meets and
merges with theyhypoblast. Furthermore it may be stated that even in
the cases of gastrulation almost or wholly by infiltration or delamina- .
tion the epiblast and hypoblast do ultimately come_into cgntact around
the rim of the blastoderm, and also in another region to be noted later.
Hence the essential part of the definition of a blastoporal lip stillholds _
60 FERTILIZATION, EARIY DEVELOPMENT
for both the places referred to. This problem will be discussed at
greater length when the cases of the Chick and the Mammal are reached.
Accessory Processes. —-Two other processes are probably always
to some extent involved in gastrulation, and in most instances are of
considerable prominence. As will presently appear, however, these movements, at least among Chordates, are not strictly a part of gastrulation
1 1
Fig. 40.—Diagrams illustrating four stages in the formation of the Teleost embryo (having an extremely
teiolecithal egg), and the growth of the germ ring or lip
of the blastopore around the yolk mass (epiboly). From
Kellicott (General Embryology). After 0. Hertwig. e.
Embryo. gr. Posterior margin of the germ ring. y. Yolk
mass. 1, 2, 3, 4, successive positions occupied by the
germ ring as it advances over the yolk.
proper;'i.e., they do not actually differentiate hypoblast from epihlast,
though they aid in the extension and disposition of both these layers.
Hence they may be more correctly regarded as accompanying or accessory _ activities.
I. E piboly.——This is the first of these accessory movements, and
occurs most typically in the development of eggs possessing abundant
yolk, e.g., those of Fishes and Amphibians. It merely involves the grad
? ual growth of the blastoporal lip over the yolk, or the yolk-filled vege
tal cells. It pray be roughly pictured (Fig. 40) by imagining a solid
sphere, the yolk, over which a rubber cap, the blastoderm, is being
stretched, the rim of the cap representing of course the lip of the blastopore. The movement,
however, is not due ap
parently to any actual '
process of stretching, but
rather to active cell division in the overgrowing
layers, and this activity
is thought to be most intense in the region of the
lip itself, i.e., the germ
ring. It may be also that
in this case, too, the
movement is augmented by surface-tension
changes which produce
a creeping of the cellular rim over the yolk. At
all events the result of
such a process will obv1ously be eventually to
enclose the yolk as in a
sac (the yolk sac); the
completion of this process necessarily involves
also the closure of the
blastopore (Fig. 40).
II. Concrescence and
Convergence. The
process of concrescence
as contrasted with that
of convergence is one
whose
occurrence, - as
previously suggested, is
now seriously ques
tioned. At least this is
GASTRULATION 61
Fig. 41.——Diagram of the formation of an embryo
by confluence (concrescence). From Kellicon
(General Embryology). A. Germ ring before formation of the embryo is indicated. The letters a-e
represent symmetrical portions of the germ ring.
B. Beginning of confluence. C. Embryo forming.
AA, BB represent regions of the embryo formed
out of the materials of the germ ring at aa, bb. D,
E. Later stages in the formation of the embryo.
The germ ring regions cc and dd, have been differentiated into the embryonic regions, CC, DD.
true with the conception of it originally held. Nevertheless in order to
understand what is now believed it seems best to indicate the essentials of
the original theory. It may be described thus. As the process of epiboly
goes forward there always results, as noted, a gradual drawing together
of the blastoporal lips, so that the size of the blastopore itself is dimin62 FERTILIZATION, EARLY DEVELOPMENT
ished. Furthermore, in the course of this procedure there is not, contrary to what might be expected, any noticeable puckering or thickening
of the lips as their circumference decreases. This fact may be readily
accounted for by assuming that much of the material which they contain is required to furnish the layers which they are leaving behind
them. Aside from this, however, there was held to be another source for
the consumption of at least part of the surplus substance of the germ
Fig. 42.———-Diagrammatic representation of the process of convergence as contrasted with that of confluence or concrescence illustrated in Fig. 4-1. .4. Surface
view of the blastoderm at the beginning of the process. B. Asimilar view near the
completion of gastrulation. Note that here most of the originally marginal material indicated by the letters, has simply moved medially and slightly posteriorly,
i.e., has converged toward the median line of the future embryo and toward the
dorsal hlastoporal lip. Some of it represented by letters a and b has been involnted
over the dorsal blastoporal lip, and hence is no longer visible. “Invisible” letters
shown in dots.
ring. Thus as gastrulation proceeds it was thought that the two sides of
the germ ring were flowing together at a certain point upon the margin
of the blastoderm, this movement being aptly designated as confluence
or concrescence (Fig. 41). In this manner, as previously noted, it was
held that each side of the original ring actually came to form a lateral
half of the axial structures of the embryo. Thus the halves of the ring
or blastoporal lips could be thought of as the “ germ ” of the future
embryo, and hence the name germ ring. The theory was originally applied more especially to telolecithal eggs with a very large yolk as the
description and figures suggest. It was not, however, confined to these
types. ‘
The present View is that actual concrescence in the manner just described is very limited. Indeed in no case can the complete side of the
axial structures of an embryo be said to arise in this manner from a
half of the blastoporal rim. Actually what seems to happen in most
MESODERM AND CO‘-ELOM 63
cases‘ is more in the nature of a flow of material from each entire posterior half of the blastoderm toward the median line and to some extent
over the dorsal blastoporal lip (involution). In this manner, much of
the substance forming the axial structures of the embryo is brought into
its definitive position (Fig. 4-2) . This process of movement toward the
median line may perhaps he aptly described in part as convergence,
but hardly as concrescence in the original sense, and the latter term is
now seldom used. Also in correlation with this point of view it seems
scarcely appropriate any longer to speak of the blastoporal lips as the
germ ring. This is because, though materials destined for certain parts
do, as we have said, pass over the lips, these materials are not, to any
great extent, actually furnished by them. Nevertheless the term is still
employed by many embryologists especially in’ connection with telolecithal eggs.
FORMATION OF MESODERM AND COELOM
All animals whose tissues are formed from three fundamental cell
layers are said to be triblastic. The Chordates belong to this group and
therefore, as already indicated, possess a third embryonic layer, the
mesoderm, which eventually lies between the other two. The source of
this layer has also been mentioned, and it was stated that among Vertebrates it always arises from one or both of those previously differentiated by gastrulation. After its emergence as a separate layer the three
primary layers may then, as noted, he definitely referred to as ecto
derm, mesoderm and endoderm. It is now necessary to describe the ways '
in which mesoderm may arise. There are four chief methods, and the
first is rather intimatelyconnected with the origin of the coelom. The
’ remaining three, as we shall see, are not quite so closely correlated.
I. The Enterocoelic Method.——This method, though common
among certain Invertebrates, occurs in connection with only a few of
the lowest members of the Chordate phylum. In its general aspects it
may be described thus: Along each side of the archenteron in its dorsal
region there arises from the hypoblast a longitudinal outpushing or
fold lying between the epiblast, now ectoderm, and hypoblast, now endoderm. This is indicated diagrammatically in Figure 43, A. Later each
fold develops a space between its two layers as shown in the diagram.
Then, as a result of the downgrowth of the folds on either side, the two
spaces presently meet ventrally and fuse (Fig. 43, B"). The common
cavity thus formed is the coelom, and its lining is mesoderm. The lining next to the ectoderm is called somatic’ mesoderm, and this somatic
64 FERTILIZATION, EARLY DEVELOPMENT
Fig. 43.—A diagram of the origin and early differentiation of the mesoderm, and of the notochord and nerve cord
in a generalized Vertebrate.
A. The mesoderm is arising by means of enterocoelic
pouches which are pushing out from the archenteron and
are not yet separated from it. B. The enterocoelic pouches
have separated from the archenteron, their walls forming
the splanchnopleure and somatopleure, and their cavities
the coelom. The notochord is beginning to develop and the
meclullary folds are approaching each other. C. The regions
of the vertebral plates, which are divided transversely into
somites, the nephrotomes and the lateral plates are marked
out, and the various parts of the somites are distinguishable. D. The closing of the neural tube or nerve cord is
completed. The somites are further developed and the myocoel is nearly obliterated. The notochord is separated from
the archenteron, and the mesentery has formed. The pronephros or embryonic kidney is developing from the neph~
rotome.
coel. Coelom. dt. Dermatome. ect. Ectoderm. e.ca. Enterocoelic cavity. end. Endoderm. lp. Region of the lateral
plate. me. Myocoel. mf. Medullary folds. mg. Medullary
groove. mp. Medullary plate. mes. Mesoderm originating in
th1s case by the enterocoelic method. mest. Mesentery. mt.
Myotome. nc. Neural canal. neph. Region of the nephrotome. neph.c. Region of the nephrocoel. not. Notochord. nt.
Neural tube or nerve cord. prn. Rudiment of the pronephros or embryonic kidney. 5. Region of segmental or
vertebral plate (somites). scl. Sclerotome. s.mes. Somatic
mesoderm. spl._mes. Splanclmic mesoderm.
MESODERM AND COELOM 65
mesoderm with the adjacent ectoderm are sometimes referred to together as the somatopleure. The lining of the coelom next to the endoderm on the other hand is called splanchnic mesoderm, and it together
with the adjacent endoderm may be designated as splanchnopleure. In
this case it will be noted that it was the hypoblast which gave rise to the
mesoderm. Hence in this instance the hypoblast would be mesentoderm
if one were using that terminology. Meanwhile dorsally the splanchnic
mesoderm from either side has pressed in above the endoderm and has
fused to form a double sheet of tissue called the mesentery. Thus the enteric canal or enteron, formally the archenteron, is, so to speak, slung
from the dorsal wall of the coelomic cavity by this sheet.
It remains to be observed that, despite the rarity of this method of
mesoderm formation among the Chordates, it is regarded nevertheless
as of considerable zoological interest. The reason for this is the fact.
already suggested, that it is found abundantly in some of the large
Invertebrate groups (e.g., the Echinoderms and Prosopygia), and is
then repeated among the lowest Chordata. This is significant because
such repetition in these members of the Chordate phylum is suggestive
in helping to determine from which class of Invertebrates the Vertebrate group arose. a
II. The Method of Delamination.—The production of a cell
layer by a method whose essential feature was a splitting off or delamination of cells has already been noted in connection with the diiTerentiation of the first two layers. It now remains to be stated that a similar
process is quite frequent among Vertebrates with respect to the generation of mesoderm. Here again the layer from which the mesoderm arises
is the hypoblast, only in this case the origin is by splitting of? instead
of evagination (Fig. 44, A). Later the coelom forms by still another
split within the mesoderm itself, giving rise as before to a somatic and
splanchnic layer. The relations of these somatic and splanchnic layers
to the body wall and to the enteron and the subsequent development of
other parts are the same as in Method I.
III. The Method of Pro1iferation.—This method involves simply the budding OH of cells from the sides of a linear thickening in the
outer of the two primary layers (epiblast), along what will be the
longitudinal axis of the future embryo. This thickening in these cases
is termed the primitive streak, of which more will be said in connection
with specific forms, and the cells budded from its sides soon spread out
between the two primary layers, and constitute the mesoderm (Fig. 44-.
B). Presently as in the previous cases this mesoderm splits into two
66 FERTILIZAT ION, EARLY DEVELOPMENT
mesoderm
endoderm
ectoderm
I I ‘endodcrm
Fig. 44.--Diagrams illustrating three other methods of mesoderm origin. A.
Method II, delamination, shows mesoderm split ofi from the underlying hypoblast.
It is characteristic of the Frog and other Amphibians. 13. Method III. proliferation,
shows mesoderm budding off from a median longitudinal thickening of epiblast,
the primitive streak. This was formerly supposed to be characteristic of the higher
Vertebrates. C. Method IV, “invagination” or involution, shows mcsodernt being
involuled through the primitive streak from the overlying epiblast. This is now
thought to be the method in Birds, and probably in the other higher Vertebrates.
In all cases the single layer of mesoderm later splits into two with the coeiom between them.
sheets. As usual the one next to the outer layer, now ectoderm, is somatic mesoderm, and that next to the inner or endodermal layer is
splanchnic mesoderm with the coelom between them. It is to be noted
that it is only in this last instance that the epiblast rather than the
hypoblast gives rise to mesgderm. Hence on the basis of the older terminology the mesoderm in this case is mesectodermal in origin.
The method just described is one which has been supposed to prevail
generally among the highest Vertebrates, i.e., the Birds and Mammals.
According to the most recent evidence, however, it now seems probable
that it plays little if any part in the Birds, and quite possibly this is
SOURCES OF TISSUES 67
also true of the Mammals. Instead, considerable rather convincing evidence has been produced by Spratt, ’4-6, in the case of one bird, the
Chick, in support of a fourth process. This will be discussed in some
detail in our description of mesoderm formation in that form, but to
make the record complete it must be briefly indicated here.
IV. The Method of “ Invagination.”—This is a term which it
will be recalled was used in connection with gastmlation, and indeed
the process as envisaged here is essentially the same as that which is
sometimes employed to describe a similar activity in endoderm production. Again as in that case, however, the writer feels that involution
would be a better word to use. In fact in this case the process may be
even more accurately described as a sort of combination of involution
and infiltration. What is said to happen is simply this: The epiblast
cells from either side of the blastoderm which aggregate along a line
to form what we have designated as the primitive streak, do not remain
here. Instead many of them continually move ventrad through the
streak and spread out on either hand to become mescderm (Fig. 44, C).
Thus again this mesoderm might be called mesectodermal in origin.
THE SOURCES OF THE TISSUES
The three embryonic cell layers having thus been defined and their
origin described, the subject may be concluded by indicating in a gem
eral way the tissues to which each cell layer eventually gives rise.
1. The ectoderm produces the epidermal part of the skin, includ~
ing cutaneous glands, hair, feathers, nails, hoofs, and one type of horns
and scales. It also gives rise to parts of the eye and of the internal ear,
and the lining of the anus and oral cavities, including the enamel of
the teeth. It is the origin of the entire nervous system and a few muscles. .»
2. The mesoderrn gives rise to most muscles, as well as to adipose
tissue and all other varieties of connective tissue including the dermis,
certain types of scales and horns and the main portion (dentine) of the
teeth. It also produces the skeletal system, the blood vascular system,
and the greater part of the urinogenital system. It forms the coelomic
epithelium, mesenteries, the outer layers of the alimentary tract, the
Eustachian tube, and sometimes lines the middle ear.
3. The endoderm produces the lining of the alimentary tract and
the epithelial parts of all the organs which arise as outgrowths from,
it; i.e., the respiratory system, the thyroid and thymus glands, the liver,
and the pancreas. It also lines the middle ear in some cases, and forms a
small part of the urinogenital system
63 FERTILIZATION, EARLY DEVELOPMENT
THE NOTOCHORD
A characteristic feature of the embryos of all true Chordates is a rod
of vacuolated tissue lying along the mid-dorsal line just above the gut.
It is termed the notochord, and makes its appearance at about the
same time at which the mesoderm starts to develop, or in some instances
somewhat later. It is clearly derived in many cases from the dorsal wall
of the archenteron, i.e., it is hypoblastic (Fig. 43, B, C, Di . In some instances, however, e.g., in Birds and Mammals, the origin of the notochord is apparently partially or entirely epiblastic. The position which
the structure occupies is obviously that which is taken by the vertebrae
of the higher adult Chordates, i.e., the genuine Vertebrates. As will
appear, the bony structures which thus replace the notochord in the latter animals arise from certain of the mesodermal tissues which surround it, while the notochord itself is gradually absorbed.
Relation of Notochord to Germ Layers.—As has been indicated, in triblastic animals all tissues and structures are supposed to be
derived from one of the three primary layers. The question frequently
arises therefore as to just which layer the notochord belongs. As noted
it is, like the mesoderm, derived from either epiblast or hypoblast. Yet
it frequently originates, in some cases partly, and in other cases entirely, separately from the mesoderm. If one is to be consistent and stick
to the three-layer idea, it is probably most logical to regard the notochord as a sort of specially derived mesoderm. Otherwise it becomes a
kind of embryological orphan which no layer will own. A rather common method of avoiding this dilemma of nomenclature, however, is to
refer to the third layer and notochord together as chorda.-mesoderm.
Thus the intimate relation of notochord to mesoderm, as well as their
semi-independent status, are both suggested in one compound term.
THE LATERAL PLATES, THE SOMITES AND THE
NEPHROTOMESM
Among all the Chordates, except in the case of a few of the most
primitive members of the group, there accompanies or immediately
follows the development of the coelom, certain other fundamental differentiations of the mesoderm. These differentiations result in the formation of threemajor divisions of this substance, whose origin and
character may be described in a general way as follows:
I. The Lateral Plates.——It has already been suggested that the
main portion of the mesoderm upon each side of the animal gives origin
LATERAL PLATES, SOMITES, NEPHROTOMES 69
to the coelom and its lining. It remains to state that each of these portions is frequently known as a lateral plate.
II. The Vertebral Plates. — The mesoderm which is not involved
in the production of the lateral plates, nevertheless remains connected
with them for a time, lying dorsally along either side of the notochord
and nerve cord in the form of a relatively narrow band, a vertebral or
segmental plate (Fig. 43, C). The major portion of each band (i.e., all
of it, save a narrow strip connecting it ventrally with the respective
lateral plate) then thickens somewhat, and soon begins to be transversely divided into a series of block-like masses termed somites. The
more anterior members of the series usually appear first, and each one
as it is formed proceeds to give rise to three fundamental elements: the
dermatome, the myotome, and the sclerotome (Fig. 43, C, D). Of these
elements the relatively thin dermatomes lie next to the ectoderm, and
are concerned chiefly in‘ the production of the deeper layer of the skin,
i.e., the dermis. The thicker myotomes come beneath and median to the
dermatomes and give rise to the bulk of the voluntary muscles, While
the sclerotomes, arising as proliferations of scattered cells, are nearest
the notochord and produce the skeletogenous tissue of the axial skeleton.
It may be further remarked that in many instances at this period a
small portion of the coelomic space extends up into each somite between the dermatome and myotome, and is there known as a myocoel.
Like the connection between the somites and the lateral plates, however,
it is of only temporary duration.
In Amphioxus, one of the very primitive Chordates referred to above,
it should be noted that the term somite as used in the early history of
this animal is somewhat more inclusive than in the foregoing description. Thus in this instance these bodies when newly formed, comprise
not only the elements of the dermatomes, myotomes, and sclerotomes,
but likewise those of the lateral plates. It may finally be added that
since there are no bones in Amphioxus, the sclerotomes give rise only
to connective tissue.
III. The Nephrotomes. —— It will be recalled that of each band of
mesoderm lying between the lateral plate and the notochord, the major
dorsal portion goes to form the somites. The remaining narrow strip,
which for a time connects these bodies with the corresponding;-;lat)eral
plate, is then designated as the nephrotome or internzpg§‘£dt£,cellqnjqé§,
while its cavity, temporarily uniting the main coelomvanidghe myocoe"l~s,'L_,=,‘-\1
is the nephrocoel (Fig. 43, D). The nephrotomfisfsliter coptrihutej ca
. \,_ _ “.s.'5“"
chiefly to the formation of the excretory organs. ‘arr (K M... J  L
J ,"
'‘‘‘*hm-mv-''’‘
70 FERTILIZATION, EARLY DEVELOPMENT
In Amphioxus and the other primitive Chordata no nephrotome
exists, and the excretory organs are therefore of an entirely different
character and origin.
THE DORSAL NERVE CORD
The final fundamental feature of Chordate anatomy which appears
in connection with these very early embryonic stages is the dorsal nerve
cord or neural tube. The latter term is used not only because it indicates
a characteristic of this structure which is peculiar to Chordatcs, but
also because it suggests the method of its development, which is likewise peculiar to this group. This method is as follows.
Shortly following the processes of gastrulation, and more or less concurrent with the process of mesoderm formation. a broad strip of ectoderm along the future dorsal side of the animal becomes thickened. This
thickened area is termed the medullary or neural plate (Fig. 43, A).
The median portion of this plate then becomes depressed slightly to
form a groove, the medullary or neural groove, while the sides are correspondingly elevated as the medullary or neural folds (Fig. 43, B).
These folds gradually grow toward one another until their crests meet
and fuse, and there is thus developed a tube, which presently becomes
entirely separated from the ectoderm above it (Fig. 43, C, D) . This is
the rudiment of the nerve cord or neural tube, while the canal which
traverses its center is the neural canal or neurocoel.3 At its anterior end
this canal opens to the exterior for a time through a small aperture, the
neuropore. At the posterior end, on the contrary, the fusion of the medullary folds eliminates the external opening (except in some Sauropsids and Mammals) at an early stage, but preserves an internal passageway as follows. Instead of stopping dorsal or anterior to the nearly
closed blastopore, the above folds extend slightly downward or backward upon either side of it. They then fuse above the latter orifice in
such a way that through it, for a considerable time, the neurocoel communicates with the enteric cavity. The short bent portion of the neurocoel in this particular region, together with the remains of the blastepore, is then known as the neurenteric canal (Fig. 53) .
The process thus described has already been indicated as character
3 This method of nerve cord formation is, as noted, characteristic of most Vertebrates, but is modified somewhat in the case of the Lampreys and many of the
Teleost Fishes. Thus in these animals no grove is formed in the thickening medullary plate. Instead the latter simply presses downward beneath the surface as a
solid cord of tissue. The neural canal then arises later within this cord by the separation or disintegration of the cells along its axis (Fig. 144).
REFERENCES TO LITERATURE 71
istic of all true Chordates, and as regards all fundamental points this
is true. 11; should be stated, however, that once more in the case of
Amphioxus certain minor variations occur. These will be considered in
connection with the development of that animal.
REFERENCES TO LITERATURE
Abbreviations for the names of periodical publications referred to in the literature cited at the ends of chapters are as follows:
Am. Anat. Mern. = American Anatomical Memoirs, Philadelphia.
Am. _l011X'- Aflat = American Journal of Anatomy, Baltimore and Philadelphia.
Am. Jour. Obstet. and Gynec. = American Journal of Obstetrics and Gynecology, St. Louis.
Am. Jour. Physiol. = American Journal of Physiology, Boston.
Anat. Anz. == Anatarnischer Anzeiger, Jena.
Anat. Hefte = Anatomische He/te, Wiesbaden.
Anat. Rec. = Anatomical Record, Philadelphia.
Arbeit. zool. Inst. Wien. = Arbeiten aus dcm zoologischen Institute zu Wicn.
Arch. Anat. u. Entw. = Archiv fiir Anatomic und Entwickclungsgeschichtc,
Leipzig. { Same as Arch. Anat. u. Physiol.)
Arch. Anat. u. Physiol. = Archiv. filr Anatomic und Physiologic, Leipzig.
Arch. Biol. = Archives de Biologic, Leipzig and Paris.
Arch. d’Anat. Micr. = Archives d’Anatomie Microscopiquc, Paris.
Arch. Entw.—mech. = Archiv fiir Enzwickelungsmechanik der Organismen, Leipzig.
Arch. mikr. Anat. =Archiv fiir mikroskapischc Anatomic und Entwiclcelungsgeschichtc, Bonn.
Arch. Zellf. == Archiv fiir Zellforschung, Leipzig.
Arch. Z001. Exp. = Archives de Zoologic experimentalc ct gencrale, Paris.
Aust. J. Exp. and Med. Sci. = Australian Journal of Experimental Biology and
Medical Science, Sydney.
Biol. Bull. = Biological Bulletin, Woods Hole, Mass.
Biol. Centr. = Biologisches Centralblatt, Leipzig.
B. M. C. Z. Harvard = Bulletin of the Museum of Comparative Zoology at Harvard College, Cambridge, Mass.
Bull. Soc. Impér. Moscou-=Bulletins dc la Societe Impériale de Natural——
de Moscou.
Carnegie Cont. to Emb. = Carnegie Institution. Contributions to Embryology,
Washington.
Carnegie Inst. of Wash.=Carnegie Institution of Washington.
Cold Spring Harbor Symp. on Quant. Biol. Cold Spring Harbor Symposia
on Quantitative Biology, Cold Spring Harbor.
C. I‘. Soc. Biol. Paris = Comptes rendus des séances ct mémoires de la Société
de Biologic, Paris.
Deutsche Thieraerztliche Wochenschr.=Deutsche Thieraertzliche Wochenschrift, Karlsruhe.
Ergeb. Anat. u. Entw. = Ergebnisse cler Anatomic und Entwiclcelungsge
schichtc, Wiesbaden.
Festsch. f. Gcgenbaur = F estschrift fur Gegenbaur, Leipzig.
Intern. Monatsschr.=Intcrnationale Monazsschrifz fiir Anatomic and Physiologic, Leipzig.
72 FERTILIZATION, EARLY DEVELOPMENT
Jena Zeitschr. = Jenaisclze Zeitschrift fz'ir‘NaturIz;isse_ns§l,l1léf¢, 1:113-B If r
Johns Hopkins H°sp_ Rep_:]ahns Hopkins ospzta epor s, ‘a xmo_e.
A M d Assn. = Journal of the American Medical Association, Chicago.
J°“" m‘ e ' - ' ,4 1 Plzvsiolo r London
jour. Anat. Phys1o1.=JourII!I1 of 7"”0’"}’ ax’) -I ¥’i’5{_I'd 1 1:’
Joan Comp» New-=10“’"“’ "f 60"’-”""mzez ("lira ogii 1:11” E .p..1iid'Pi.z1ade1
Jour. Exp. Zo61.=Journal of Expenmenta oo 05)’. 3 H10“? 4
1' . .
J°ml.3.n1l1/[O,ph_= foumgz of Morphology or Journal of Jlorphology and Pll_}‘5l
1 ~, Ph'l dl l'a. _ . . _
Jamil 05'lniv_ l1?01:;on.—= journal of the College of Science, Imperial University of
Kg1T0S]:i::Ji1sk. Vet. Hand1.=Kongliga Svenska Vetenskapsokadenzie, Ablzantl»
lungen aus der Naturlehre, Leipzig: , ' ’ '
Mérn. Acad. Impér. St. P. =1lIémoLres cle l Acadernze Irrzperzale de St. PetersMenl.:ouAi‘ad_ 1.oy_ Be1g_ = Mémoires de l’Actzdemie royale tie Belgique.
Mem: Boston Soc. Nat. Hist. = Memoirs of the Boston Society of Natural HisMéI'llJ.r}l,‘l. Y. Acad. Sci. = Ménzoirs of the New York Academy of Science?’
Mitt, zool. Stat. Neapel = Mzttezlungen aus der zoologzschen Station zu 1 cape],
Berlin.
Morph. Arbeiten. = .-llorphologisclte Arbeiten, Jena.
Morph. Jahrb. = Morpholagisczes JahrBbui:h, Lexpzlg.
Nat.-wiss. = Die Naturwissensc a. ten, er in. _
Phil. Trans. Roy. Soc.=PhilosophicIzl Transactions of the Royal Soczety of
London.
Physiol. Rev. = Physiological Reviezvs, Baltimore. .
Physio}. Z061. =Physiological Zoology, Phllarlelphxa. ‘
Proc. Am. Acad. Arts and Sci. =Proceedzngs of the American Academy of
Arts and Sciences, Boston. _ I . _
Proc. Am. Phil. .Soc.=l’roceedings of the American Philosophical Society,
Philadelphia. d P d I I I _ 1
Proc. Internat. Cong. Z061. Camhri ge= rocee ings o (18 nternauona
Congress of Zoiilogists, Cambridge. S I 1
Proc. Soc. Exp. Biol. and Med. =Proceedings of the ociety or Experimenta
Biology and Medicine, New York.
Ptoc. Z061. Soc. = Proceedings of the Zoiilogical Society of London.
Q. J. M. S. = Quarterly Journal of Microscopical Science, London.
Quart. Rev. Biol. = Quarterly Review of Biology, Baltimore.
S. B. G. M. P. = Sitzungs-Berichte zler Gesellschaft fiir tllorphologie und Physiologie, Miinchen.
Sitzber. Ber. Akad. = Sitzungsberichte der Koeniglich Preussisclzen Alratlerizie
tier Wissenschaft, Berlin.
Tijd. Nederl. dierk. Ver. ==Netlerlandsclze dierlcumlige Vereeniging, 7'1’/(L
schrift, Leyden.
Trans. Am. Phil. Soc. = Transactions of the American Philosophical Society,
Pliilaclelpliia.
Univ. Cal. Press. = University of California Press, Berkeley.
Verh. d. Anat. Gesell. = V erhandlungen der Anatomisclzerz Gesellschaft. Jena.
Ver. kon. Akad. Wetensch. = Verhandelingen lconirtklijke Al.-mlemie van
Wetenscl-zappen, Amsterdam.
Verh. Phys.-Med. Ges. = Ferlzantlltzngen Physilmlisclze-Merlizinische Case!!schaft, Wurzburg.
REFERENCES‘ TO LITERATURE 73
Zeit. Anat. Entvv. = Zeitschrift fiir Anatomic und Entwickelungsgeschicltte,
Leipzig.
Zeit. ind. Abs. u. Vererb. = Zeitschrift fiir induktivc Abstammungs- und Vererbungslehre, Berlin. ‘
Zeit. Mikr.-Anat. Forsch.=Zeitschrifz fiir Mikroskopisch-Anaiomisc/1e F orschung, Leipzig.
Z001. Jahrb. = Zoologische Jahrbiicher, Jena.
CHAPTERS I AND II
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Allen, Edgar, “ Ovogenesis during Sexual Maturity,” Am. Jour. Anat., XXXI, 1923.
Allen, E., Kountz, W. B. and Francis, B. F., “ Selective Elimination of the Ova in
the Adult Ovary,” Am. Jour. Anat., XXXIV, 1925.
Babcock, E. B. and Clausen, R. E., Genetics in Relation 20 Agriculture, New York
and London, 1918.
Benda. C., “ Die Mitochondria,” Ergeb. Anat. u. Entw., XII, 1903 (1902) .
Bookhout, C. G., “ The Development of the Guinea Pig Ovary from Sexual Differentiation to Maturity," Jour. Morph., LXXVII, 1945.
Boveri, Th., “ Die Entstehung des Gegansatzes zwischen den Geschlechtszellen und
den somatischen Zellen bei Ascaris,” S.B.G.M.P., Miinchen, VIII, 1895.
Bowen, R. H., “ Studies on Insect Sperrnatogenesis,” VI, “ Notes on the Formation
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Biitschli, 0., Untersuchungen fiber mikroskopische Schaiime und das Protaplasma,
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Castle, W. E., Genetics and Eugenics, 2nd Ed., Harvard Univ. Press. 1920.
Everett, N. B., “The Origin of Ova in the Adult Opossum,” Anat. Rec., LXXXII,
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Flemming, W., Zellsubstanz, Kern und Zellteilung, Leipzig, 1882.
Geerts, J. M., “Cytologische Untersuchungen einiger Bastarde von Oenothera
gigas,” Berichte Deutsche Botanisehe Cesellschaft, XXIX, 1911.
I Goldsmith, J. B., “The History of the Germ Cells in the Domestic Fowl,” Jour.
Morph. and Physiol., XLVI, 1928. _
Goodrich, H. B., “ The Germ Cells in Ascaris,” Jour. Exp. Zo6l., XXI, 1, 1916.
Hargitt, G. T., “ The Formation of the Sex Glands and Germ Cells of Mammals.”
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Physz'ol., XL, l92S.—-II. “ The History of the Male Germ Cells in the Albino
Rat,” Iour. Morph. and Physiol., XLII, 1926.—-III. “ The History of the
Female Germ Cells in the Albino Rat to the Time of Sexual Maturity.” -—- IV.
“ Continuous Origin and Degeneration of Germ Cells in the Female Albino
Rat,” Jour. Morph. and Physial., XLIX, 1930.
Hertwig, A., Die Zelle und die Gewebe, Jena, I, 1893; II, 1898.
Holtfreter, 1., “ A Study of the Mechanics of Gastrulation,f' Part I, Jour. Exp. Zo6l.,
VIC, 1943.—-- Part II, Jour. Exp. Zool., VC, 1944.
Humphrey, R. R., “The Primordial Germ Cells of Hemidactylium and other Amphibia,” Jour. Morph. and Physiol., XLI, 1925. ~—“ Extirpation of the Primordial Germ Cells of Amblystoma: Its Effect_,,U_pg.n...the Development of the
Gonad,” Jour. Exp. Zob'l., XLIX, I927.——i‘ The Early Position of the Pri
mordial Germ Cells in_Urodeles: Evidence from Experimental Studies,” Anat.
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74 FERTILIZAT ION, EARLY DEVELOPMENT
Jenkinson, J. W., “ Observations on the Maturation and Fertilization of the Egg of
the Axolot ,” Q.J.M.S., XI, viii, 1904.-—Vertebrate Embryology, Oxford and
London, 1913. ,
Jennings, H. B., “Paramecium hursaria. Life History. V. Some Relations of External Conditions, Past or Present, to Aging and to Mortality of Ex-conjugants,
with Summary of Conclusions on Age and Death,” Jour. Exp. Zool., IC, 1945.
Kingsbury, B. F., “The Postpartum Formation of Egg Cells in the Cat,” Iour.
Morph., LXIII, 1938.
Lewis, W. H., “ Mechanics of Invagination,” Anat. Rec., IIIC, 1947.
Lillie, F. R., Problems of Fertilization, Chicago, 1919.
McC1ung, C. E., “The Accessory Chromosome-— Sex Determinant?” Biol. Bull.,
III, 1902.
Meves, F., “Ueber Struktur und Histogenese der Samenfiiden von Salamandra,”
Arch. milcr. Anat., I, 1897.
Moenkhaus, W. .l., “ The Development of the Hybrids between F tmdulus heterodirus
and Mendidia notata, with Special Reference to the Behavior of the Maternal
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Montgomery, T. H., In, “A Study of the Chromosomes of the Germ Cells of the
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Morgan, T. H., Heredity and Sex, New York, 1913. The Physical Basis of Heredity,
Philadelphia, 1919. The Physical Basis of Heredity, Philadelphia and London,
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Morgan, Sturtevant, Muller, and Bridges, The Mechanism of Mendelian Heredity,
New York, 1915.
Oliver, J. R., “ The Spermiogenesis of the Pribilof Fur Seal (Callorhinus alascanus
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Painter, T. S., “ Studies in Mammalian Spermatogenesis. II, The Spermatogenesis
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Riddle, 0., “The Theory of Sex as Stated in Terms of Results of Studies on Pigeons,” Science, XLVI, 1917.
Rosenberg, 0., “Cytologische und morphologische Studien an Drosera longifolin
X rotundifolia,” Kgl. Svenslc. Vet. Handl., 43, 1909.
Sharp, L. W., An Introduction to Cytology, New York, 1921.
Sinnott and Dunn, Principles of Genetics, New York, 1925.
Sneider, M. E., “Rhythms of Ovogenesis before Sexual Maturity in the Rat,” Am.
Jour. Anat., LXVII, 194-0.
Strassburger, E., Zellbilzlung und Zellteilung (3rd ed), Jena, 1880.
Sutton, W. S., “On the Morphology of the Chromosome Group in Brachystola
rnagna,” Biol. Bull., IV, 1902.
Van Beneden, E., “Recherches sur la Composition et la Signification de l’CEuf
etc-a M97fl- 4604- 707- Belg», XXXIV, 1370.-—“ Recherches sur la Maturation
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Weismann, A., “Entstehung der Sexualzellen bei den Hydrornedusen,” Fischer
Jena, 1885. '
Wilson, E. B., Atlas of Fertilization and Karyokinesis, New York. l895.——- The
Cell in Development and Heredity (Columbia University Biological Series, IV,
}3g%I,e:’¢‘i;)i9l1‘I2¢=:w York, 1925.—-“Studies on Chromosomes,” four. Exp. Zool.,
HE EARLY DEVELOPMENT OF AMPHIOXUS
T H E early stages in the development of Amphioxus ( Branc/ziostomu.
lanceolatum) are taken up because in this form these stages are thought
to be as nearly primitive as those occurring in any other Chordate.
This applies particularly to the method of segmentation, gastrulation,
and formation of the mesoderm and coelom. Indeed the general resemblance of these processes to what occurs among Invertebrates, such
as the Echinoderms, is so marked that their primitive character in Amphioxus can hardly be doubted. Also according to the most recent studies there is a marked and significant resemblance between the early
stages of this animal and those forms sometimes designated as Protochordates, i.e., the Ascidians.
There are numerous accounts of the development of this classic
form, some of the best known being those of Hatschek (1882, ’88),
Wilson (1893), Cerfontaine (’O6) and the most recent that of Conklin
(’32). The studies of the last named investigator, though agreeing in
many respects with those of his predecessors, differ rather fundamentally in some of the earlier details. Since the work of Conklin is not
only the most recent, but is supported both by elaborate observations
of normal development, and by experimental procedures, it is believed
to be the most accurate. It is therefore the one followed in this text
except where otherwise indicated. It is assumed that the student has in
mind a fair knowledge of the adult anatomy of the animal under discussion.
THE REPRODUCTIVE ORGANS
THE OVARY
Since the work of Conklin does not cover very completely the character of the ovary and the process of oogenesisdthe following brief statements on these subjects are based on the account of Cerfontaine.
The ovaries are developed in each myocoel (Fig. 45) on both sides of
the body from the tenth to the thirty-fifth or thirty-sixth sornite inclusive. Each originates as a proliferation of cells on the antero-ventral
5
{gs76 THE EARLY DEVELOPMENT OF AMPHIOXUS
Fig. 45.——Diagram of a section through
the gonad of Amphioxus. From Kellicott
(Chordate Development). After Cerfontaine. Right side adjacent to atrium.
b. Peribranchial (atrial) epithelium. c.
Cicatrix. f. True follicular epithelium. fe.
External layer of follicular epithelium. g.
Gonocoel. ge. Germinal epithelium. 0;. Primary ovarian cavity. 02. Secondary ovarian
cavity. pg. Parietal layer of gonocoel. v.
Cardlinal vein. vg. Visceral layer of gonocoe .
wall of the myocoel. This proliferation then pushes forward
as a small bud, covered by the
portion of the myocoelic wall
from which it arose. The bud
of germ cells with its covering
thus comes to project sac-like
into the myocoel anterior to the
one in which the proliferation
started. The neck of the sac
then forms a short stalk connecting it with the posterior myocoelic wall of the cavity into
which the evagination has occurred. Thus in these animals
each egg is not surrounded by
its individual follicle, but is attached to the wall of the above
sac, which acts as a general follicle for all the ova within it. As
development proceeds, the most
ventral part of each myocoel
which contains the gonad is cut
ofi” from the part above as the
gonocoel. By the time a batch
of ova is ripe, however, which
occurs for the first time in animals about two centimeters in
length, each ovary has grown
so that it virtually obliterates
all coelomic spaces surrounding it (Fig. 4-5) . These eggs are
then extruded (see below),
while the ovary during the process almost disappears. It then develops
anew in preparation for the next breeding season.
THE TESTIS
The development of the testes in Amphioxus is not so well known,
but it appears to be similar in a general way to that of the ovary. The
products are discharged to the outside as are the eggs.
THE OVARY
Fig. 46.—The egg of Amphioxus. From Kellicott (Chardate Development). C. After Cerfontaine, others after Sobotta. A. The ovarian egg showing cortical plasm. The first polar body ls being
pinched ofi, and the spindle for the second meiotic division is
formed. B. The cortical layer forming the perivitelline membrane
on the surface of the egg within the vitelline membrane. C. The
fusion of the vitelline membrane and perivitelline membrane to form
the fertilization membrane is complete, but the latter has not yet
left the surface of the egg. D. The extruded and fertilized egg. The
fertilization membrane is beginning to leave the surface of the egg.
c. Cortical layer. e. Endoplasm. m. Fused vitelline and perivitelline membranes, i.e., the fertilization membrane. p. Perivitelline
space. s. Spermatozoiin. v. Vitelline membrane. I. First polar body.
11. Second polar spindle.
77
78 THE EARLY DEVELOPMENT OF AMPHIOXUS
THE HISTORY or THE OVUM To GASTRULATION
OGGENESIS
Multiplication and Growth.———After passing through a typical
oogonial or multiplication stage the cells cease dividing and enter upon
a period of growth. During this period the nucleus passes through the
last processes prior to meiosis, while deutoplasm appears throughout
the greater part of the cytoplasm. Inasmuch as this is a comparatively
yolk-free egg the latter substance does not become very dense. It does
become just abundant enough, however, so that the yolkless portion is
clearly distinguishable. At the conclusion of growth and previous to
the maturation divisions this portion apparently consists mainly of a
thin vacuolated layer lying everywhere just beneath the Surface (Fig.
46, A). The germinal vesicle is in contact with this layer on one side,
the animal pole, while the remainder of the egg cytoplasm is relatively
full of yolk granules. Near the close of the growth period a thin vitelline membrane is formed.
MATURATION AND FERTILIZATION
The First Meiotic Division. —— When the egg has reached full size
the first meiotic division takes place at the animal pole. It is preceded
in this instance by the formation of tetrads (see page 20), and the
spindle of this and the ensuing division are without centrosomes or
asters. Immediately following this division, preparations for the second
one begin, and proceed as far as the metaphase (Fig. 4-6, A} . The proc~
ess pauses in this stage until after fertilization. Meanwhile as the first
polar body separates from the egg it pushes through the vitelline membrane, carrying a small portion of the latter with it. Hence it is entirely
free and is often lost (Fig. 46, D). At the same time the egg bursts out
into a portion of the gonocoel next to the atrium.
Spawning and Fertilization.———Spawning occurs throughout the
spring and summer, and always toward evening, while the animals are
swimming. At this time muscular contractions occur in the walls of
the above gonocoel cavities and thus cause the eggs to burst through
these walls, at certain points termed the cicatrices. The cutis wall of
the atrium is also ruptured in these regions and the eggs thus reach the
atrial cavity and from thence the exterior. As soon as the egg comes in
contact with the sea water a second membrane is formed inside the first.
It is called the perivitelline membrane, and is separated from the origiMATURATION AND FERTILIZATION 79
mil covering by a slight space} The new membrane seems to be formed
from the outer part of the vacuolated cytoplasm (cortical plasm) at the
surface of the ovum, with which for a short time it remains in close
contact. It is at first of a fluid consistency, but after a brief exposure to
the action of the water it begins to toughen. This process starts in the
dorsal
future endoderm
anterior <-—
 
animal pole
future ectoderm
ventral
Fig. 47.—A median sagittal section through the fertilized egg of Amphioxus,
viewed from the left side. After Conklin. The egg is oriented in terms of the position of its parts relative to the future embryo. Actually, according to Conklin, it
floats with the animal pole up at this time. The fertilization membrane is shown at
some distance from the egg, and beneath it at the animal pole is the second polar
body. The pronuclei are shown fusing in the midst of the clear hyaloplasm.
region of the animal pole, from where it soon spreads rapidly around
the egg. '
Meanwhile the latter has become surrounded by sperm which have
been shed into the water near the female. One or more of these sperm
now penetrate the outer or vitelline membrane, cross the intervening
space, pierce the inner membrane, and enter the egg. Such entrance is
generally effected near the vegetal pole where the perivitelline covering
remains longest in a fluid condition. As soon as the sperm have reached
the egg itself, however, the toughening of this membrane is rapidly com
1 This space is literally perivitelline, and is often referred to as such. It differs
from the space more usually so named, however, in that it exists previous to fertili
zation, and also in that it is, at this time, separated from the egg by a separate
covering, the pcrivllelline membrane.
ext
80  EARLY DEVELOPMENT OF AMPHIOXUS
pleted. Also it seems to fill the space between the egg and the original
vitellineimembrane with which it apparently becomes fused (Fig. 4-6,
B, C). The fused membranes thus form together what may be termed
a fertilization membrane, and this presently becomes separated from
the surface of the egg by the usual (“true”) perivitelline space (Fig.
46, D).
The Second Meiotic Division: Fusion of the Egg and Sperm
Nuc1ei.—-The entrance of the sperm is a stimulus which causes the
second meiotic division to become completed, and the second polar
body is cut off. In this case, however, the body is retained beneath the
fertilization membrane, thus helping to mark the animal pole, and so to
orient the egg.
Meanwhile the sperm head (i.e., the sperm nucleus) enlarges so that
it is equal in size to the egg nucleus. The two nuclei then meet and fuse
in the usual manner. The point of this fusion is generally a little above
the equator of the egg, and slightly toward the side which will eventually be the posterior of the embryo, as shown in Figure 4.7. As is indicated in this figure, the fused nuclei now lie within an area of clear
cytoplasm lhyaloplasm) which, though it is mainly toward the animal
pole, extends somewhat posteriorly. Cerfontaine represents it as a cone
as outlined in Figure 48, A, though Conklin ( Fig. 47) shows this shape .
less clearly. The source of this hyaloplasm is not quite clear, though
Conklin seems to suggest that it arises from the breakdown of the germinal vesicle, at the maturation divisions. Whatever its source this clear
material should be noted as the third differentiated substance in the unsegmented egg, the other two being the yolk filled cytoplasm, and the
peripheral vacuolated layer. The further fate of these substances will be
indicated presently. Any other sperm which may have gained entrance
degenerate without further activity and the process of fertilization may
be said to be complete.
EGG SYMMETRY AND SEGMENTATION
Symmetry and Orientation.-——-The polarity of the egg, i.e., the
establishment of the animal and vegetal poles, is traceable to its point
of attachment in the ovary; i.e., the vegetal pole is on the unattached
side. This is a matter of considerable interest because, as Conklin has
pointed out, in many Invertebrates it is the vegetal pole which is
attached in the ovary. This writer then very pertinently suggests that
this reversal may well mark the initiation of the later reversal in dorsaventral symmetry which places the nerve cord in Chordates on the dorEGG SYMMETRY AND SEGMENTATION 81
sal ‘instead of the ventral side. This seems reasonable, since such a
profound and early appearing diflerence as this must certainly have its
origin very far back in the ontological process.
VVhatever may be the conclusion with respect to this question, it is
evident that the entrance of the sperm slightly to one side of the vegetal
futu re
future endodcrm
ectoderm
       
Fig. 48.——Diagrarns illustrating the relations between the adult axes
and the axes of the egg and early stages based on the accounts by Cerfontaine and Conklin. A. Fertilized egg. B. Fully formed blastula. C.
Gastrulation begun. D. Fully formed gastrula. The arrow in each case
indicates the future anterior-posterior ax-is, while the polar body marks
the animal pole. In A the pronuclei are represented as fusing in the
midst of the cone of yolk-free cytoplasm. (See ‘Fig. 47.) According to
Conklin, the egg or embryo does not actually assume the position indicated until shortly after the closure of the blastopore (see text).
pole establishes a third point on the egg with reference to the two poles
already present, and so determines a median plane. Not only is this true
but, as later events prove, this median plane of the egg becomes the me‘diam plane of the future embryo, and the side toward which the sperm
enters becomes the posterior side of the embryo. This is well to bear
in mind since in the study of the Frog we shall find another case in
which the sperm entrance point is significant in determining embryonic
symmetry. , ‘
With respect to this matter of embryonic symmetry, a further word
82 THE EARLY DEVELOPMENT OF AMPHIOXUS
must now be said. Though the bilateral. and antero-posterior symme.
tries of the future embryo have now been determined in the egg as indicated, the question arises as to how soon the floating egg or developing embryo actually becomes oriented with the antero-posterior and
dorso-ventral parts in their definitive positions. It has been said that
this occurs at the time of, or immediately following, fertilization so
that the undivided egg actually assumes an orientation in the water such
as indicated in Figures 47 and 4-8, A. As a matter of fact. however. this
appears probably not true. Conklin does not refer to the point in his
paper, but has been kind enough to inform the writer that in his opinion this definitive orientation probably does not occur until “ shortly
after the closure of the blastopore.” In the meantime this investigator
believes that the dividing egg probably floats like most other floating
eggs, with the animal pole up. The lack of certainty in this connection
is due, Conklin says, to the fact that “the polar bodies are minute and
difficult to recognize,” while other means of orientation are also hard
to discern in the living egg. His opinion under these circumstances is
based on such observations as are possible, and on the fact that on the
centrifuge the yolk pole always goes to the centrifugal position. However, in spite of this probable actual orientation of the animal and vegetal poles of the egg, it is convenient in describing development to assume a constant orientation from the very beginning. Hence in the
ensuing description the terms dorsal, ventral, anterior, and posterior
are used throughout with reference to the definitive position of these
parts subsequent to gastrulation. This relation of the animal and vegetal poles of the egg to the orientation of the future embryo is indicated
in Figure 43. On this basis it is evident that the anterior end of the
future animal will lie about 30 degrees above the animal pole of the
egg as here shown and the posterior of the animal about 30 degrees below the vegetal pole. It is to be borne in mind, however, that according
to Conklin the developing ovum probably does not really assume this
position until about the stage represented by Figure 51, F , or shortly
thereafter.
In addition to the plane of symmetry‘ established by the mere entrance of thesperm and the position of the fusion nucleus, other significant reinforcements of the symmetry so initiated quickly ensue. As
the sperm passes into the egg there is, according to Conklin, a flow
of the superficial vacuolated layer of cytoplasm from the animal pole
to the region where the spermatozoon entered. Here it forms a crescent
of material across the future ‘posterior surface of the egg, as above deEGG SYMMETRY AND SEGMENTATION 83
fined, with the horns of the crescent extending somewhat anteriorly.
This, Conlclin emphasizes, is exactly comparable to the mesodermal
crescent similarly formed in the Ascidians, and it has exactly the same
fate, i.e., it gives rise to all the future mesoderm. This conclusion is
based on a study of sections of successive stages, the flow not being
actually observed in the case of Amphioxus. Aside from the potential
Fig. 49.—Prophase of first cleavage figure in Amphioxus.
From Kellicott (Chordate Development). After Sobotta.
Inner and outer membranes fused and separated from the
egg by a wide space called the perivitelline space.
mesodermal material which Conklin thus finds preformed in the egg,
this investigator also noted that the future endodermal substance consists of the yolk-filled cytoplasm now located dorso-anteriorly to that
destined to be mesoderm. The remaining yolk-free cytoplasm or hyaloplasm, containing the cleavage nucleus then lies, as noted, largely toward the antero-ventral side, and is destined to become ectoderm and
notochord (Figs. 4-7, 48) . We are now prepared to describe the process
of segmentation, keeping always in mind the sense in which dorsal,
ventral, anterior, and posterior are being used.
Segmentation.——Segmentation in Amphioxus is of the total or
holoblastic type, but is not quite equal. The first division occurs about
84 THE EARLY DEVELOPMENT OF AMPHIOXUS
an hour after fertilization, and the second about an hour after the first.
Subsequent divisions follow each other at intervals of fifteen or twenty
minutes. 4
First Cleavage. —- The first cleavage spindle becomes situated within
the cone of clear protoplasm, where its position is such that its center is
cut at right angles by the median plane of the egg. The line of cleavage,
therefore, coincides with that plane, and divides the ovum, including
its three preformed substances, into equal right and left halves (Fig.
49).
Second Cle¢wa.ge.—The second cleavage is at right angles to the
first, and is also approximately meridional. It is not exactly so, however, since its plane lies a little postero-ventral to the animal and vegetal poles, thus causing the antero-dorsal pair of blastomeres to be
slightly larger than the postero-ventral pair (Fig. 50, A). This is the
interpretation of Conklin, and is exactly the opposite of that of Cerfontaine and others. It is significant because it carries through the entire early development, and is necessary in order to locate the potential
mesoderm in the ventro-lateral lips of the early gastrula where Conklin
insists it is. We shall follow Conklin’s interpretation. This writer also
calls attention to a slight spiral tendency in this cleavage comparable
to what regularly occurs in Annelids and Gastropods. He maintains that
usually two of the four blastomeres are sufficiently in apposition so that
when viewed from the animal pole the line ofcontact at that pole appears as a short furrow turning to the left. From the same viewpoint
the furrow at the vegetal pole turns to the right. This feature, however,
does not have the constancy which is characteristic of the Invertebrate
forms referred to.
Third Cleavage. —The third cleavage plane is at right angles to the
first two; i.e., it is latitudinal with respect to the animal and vegetal
poles of the egg. It is not quite equatorial, however, since it is situated
slightly nearer the animal pole. The result is the production of four
pairs of cells, the two at the animal pole being termed micromeres, and
the two at the vegetal pole macromeres (Fig. 50, B, C }. As regards the
orientation of these cells relative to the future embryo, the upper pair
of micromeres are anterior, and the lower pair ventral, while the upper
pair of macromeres are dorsal and the lower pair posterior. From the
account of the preceding cleavage also it is evident that the anterior
pair of micromeres and the dorsal pair of ma_cromeres are respectively
slightly larger than the other pair of the same type. Likewise it is to
be noted that the potential mesodermal material is largely located in
EGG SYMMETRY AND SEGMENTATION 85
Fig. 50.———Cleavage in Amphioxus. After Conklin. A. Four-cell stage viewed from
the animal pole. B. Eight-cell stage viewed from the animal pole, showing the four
sizes of the cells. C. Eight-cell stage viewed from the left side. The arrow indicates
the anterior-posterior axis. Again note the relative sizes of the cells, the anterior
micromeres being slightly larger than the ventral ones, and the dorsal macromeres
slightly larger than the posterior ones which contain the mesodertnal substance. D.
Eight-cell stage going into sixteen viewed from the animal pole. E. Thirty-two cell
stage viewed from the left side with many of the cells about to divide again. The
arrow indicates the anterior-posterior axis. E. About the 128-cell stage, four hours
after fertilization, viewed from the left side. The arrow indicates the anterior-posterior axis. Note that at this time the largest of all the cells are at the future dorsal
blastoporal lip, and represent the endoderm. (See Fig. 51, A.)
86 THE EARLY DEVELOPMENT OF AMPHIOXUS
the two posterior (smaller) macromeres, the potential endodermal
material in the dorsal macromeres and the dorsal parts of the posterior
macromeires, and the potential ectodermal substance chiefly in the
micromeres (Fig. 50, C).
Fourth Cleavage.-——The planes of this cleavage are again approximately longitudinal or meridional with respect to the poles of the egg.
The cleavage is not precisely meridional, however, in all the blastemeres but very slightly bilateral. Thus in the four micromeres each of
the new planes runs not exactly toward the center of the egg, but a
little toward the plane of the first cleavage, while in the macromeres the
inclination of these fourth cleavage planes is a little toward the plane
of the second cleavage. This may be noted to some extent in Figure
50, D, although the incipient planes of the macromeres in this case appear to be essentially meridional.
Fifth Cleavage. —-—- This division is typically again latitudinal, so that
there result two layers of micromeres and two of macromeres. Thus, in
all, there are thirty-two cells arranged in eight meridional rows with
respect to the original animal and vegetal poles, the micromeres toward
the former and the macromeres toward the latter. It should be added,
however, that the arrangement of the cells following this cleavage is
seldom entirely regular so that a strictly meridional appearance such
as shown in Figure 50, E is not often seen.
The Blastula. — The sixth cleavage is more or less meridional, giving rise to sixty-four cells. The arrangement is even more irregular than
in the lastcase, however, and it is impossible to identify exactly the
various cells in terms of their origins. Although the seventh cleavage is
more irregular than the sixth, about one hundred twenty-eight cells are
produced, and by the eighth cleavage the synchronous character of the
divisions is also lost.‘ This dividing mass of cells may now be termed a
blaszula (Fig; 50, F). From the figure just referred to it will be evident
that this blastula is not round. Instead it is somewhat pear-shaped with
the small end of the pear posterior. Also, as might be assumed, it is
not a solid mass of cells, but as usual contains a cavity or blastocoel.
This indeed has existed from the four cell stage since the cells are
rounded and hence not in complete contact. The space in question is
filled with a gelatinous material which Conklin calls blastocoel jelly,
and at first communicates with the outside through spaces between the
rounded cells. As cleavage continues, however, the cells establish contacts except at their inner ends, and thus close the openings into the
blastocoel, the ones at the poles persisting longest. Meanwhile the jelly
GASTRULATION 37
in the hlastocoel is absorbing water, so that it greatly increases in volume, and becomes quite fluid. As a result of this increase in volume the
size of the completed blastula is about one third greater than that of
the unsegmented egg.
The fact that the cells of the blastula are somewhat irregularly arranged makes it, as noted, almost impossible to identify each one precisely in terms of its source. Nevertheless this relationship can be approximately determined by the positions of the cells with respect to
the polar body, and by their relative sizes. Thus it appears that the‘
smallest and most rapidly dividing cells of the blastula are located
posteriorly. Hence they are derived from the two posterior macromeres
of the eight cell stage, and represent potential mesoderm. The somewhat
larger and slightly more slowly dividing cells located in the anteroventral region are derived from the four micromeres of the eight cell
stage, and are potential ectoderm. Finally the largest and most slowly
dividing cells in the postero-dorsal region are derived mostly from the
dorsal pair of macromeres of the eight cell stage and are potential endoderm (Fig. 50, F).
GASTRULATION, FORMATION OF CENTRAL NERVOUS
SYSTEM, MESODERM, NOTOCHORD, AND COELOM
GASTRULATION
The exact nature of the process of gastrulation in Amphioxus has
been the subject of much dispute. This is owing partly at least to the
minute size of the larva at this time, and the consequent difliculty of
determining just what occurs. As before, the account which will be
followed here is that of Conklin, according to whom the main processes are invagination, involution and a kind of epiboly. It should be
stated, however, that Conklin does not himself employ the last named
term. Concrescence, which is said to occur hy Cerfontaine and other writers, is. according to this investigator entirely lacking. Conklin indeed
does not even refer to convergence.
Invagination and Involution. —-—As noted the completed hlastula
consists of a hollow pear-shaped mass of cells the wall of which is
everywhere a single cell layer in thickness. Antero-dorsally from the
smaller posterior end of this pear shaped structure, the hypohlastie wall,
consisting of potential endodermal cells, is already somewhat flattened
(Fig. 51, A), and this process soon involves the whole postero-dorsal
ventral
blastuporal
lip
notochordal primardium future
esoderm
blaxtopore
3
«E
E
C
"°X‘“"“‘I °l “'“"°P°" "mm Pl: E ucurcntern:
Fig. 51.-—~Gastrulation in Amphioxus. After Conklin. Arrows indicate anteriorposterior axis. A. Hemisected blastula from left (cut) side. Note flattened vegetal
pole preliminary to gastrulation, also position of future endoderm and mesotlernt.
B. Moderately early hemisected gastrula from left side with epiblast of right side
removed, permitting view through remains of blastocoel. C. Slightly later gastrula.
Same view and treatment as in B. Note position of future mesoderm. D. Still later
gastrula. Same view and treatment as in B and C. Note posterior movement of
dorsal lip and dorsal movement of ventral lip, thus bringing mesoderm nearer to
dorsal lip. E. Posterior view of total gastrula slightly later than D. Future mesoderm apparent in both lateral lips, but not in ventral lip, though it is there. (See
text) F. Much later hemisected gastrula, again viewed from left (cut) side. 0.
Completed hemisected gastrula from left side. Mesoderm, except at blastopore, is
in enterocoelic fold and mostly invisible. (See text.) H. Young hemisected embryo
from left side. Neural folds forming and covering blastopore to form netttenteric
canal. Only one layer in “fold” at this stage. (See text.)
88
' one choses to regard the angle where these last named lips meet as such.
as being the probable immediate cause of the process of involution.
[of the gastrulation of Amphioxus. This is probably because of the effort of this
GASTRULATION ' T I 39
side. Because of the general form of the blastula this flattening wall or
plate when viewed from the future posterior, has the shape of a triangle
with slightly curved sides. The widest side of this triangle is anterodorsal toward the larger end of the pear. The other two sides extend
postero-ventrally until they meet at the smaller end. As will presently
appear, the broad transverse antero-dorsal edge of the plate will constitute the dorsal lip of the blastopore. The other two edges will constitute the ventro-lateral lips, there being no strictly ventral lip unless
Hence the blastopore as it develops will, for a time at least, be triangular rather than round (Fig. 51, E).
The flattening of the hypoblastic plate is further accentuated, and
presently the cells so affected begin to move inward somewhat as in the
typical illustration of the invagination process." In this case, however,
the movement is not equal on all sides. Instead it is greatest at the broad
transverse dorsal lip, becoming less as one goes posteriorly along the
postero-lateral lips. It is somewhat as though the hypoblastic plate were
a door swinging inward, with the more posterior part of the postero-ivem
tral lips acting as the hinge. It is clear, however, that the swinging in
movement cannot occur to the exclusion of other processes. If it did a
break would necessarily take place between the plate and the part of the
lip from which it is moving away. That such a break does not occur is 2
apparently due in part to the involution or inflection of cells at these
regions of the lips, particularly at the dorsal lip. This in turn is made
possible by active cell division. It may also be noted in this connection
that the cells of the hypoblastic plate whose inner ends are distinctly
rounded have become more columnar in shape, while those of the epiblast have become less columnar and more cubical (Fig. 51, A). These
and other changes in shape of gastrular cells have already been noted
Another feature to be mentioned at this point is the fate of approximately six transverse rows of cells just at, and immediately anterior to,
the dorsal blastoporal lip. As involution proceeds three of these rows
9 The terms epiblast and hypoblast are not used by Conklin in his description
author to emphasize the fact that the materials for all three germ lay_¢;rs;;;arre,‘d;istinguishable, as noted, from the very beginning. However, it seems ber@fto‘be 'cjgg‘h-‘. V_
sistent in our use of these terms. Therefore, we shall apply the nz'rt‘§les,«ec”toderrr‘i’,*.:-'
endoderm and mesoderm to these layers only after they have actuall§'v'bo€n set aside ‘‘ -,,’t
as definitive cellular sheets. Previous to that we have referred to « " rfiaterials con-vi , ...."*
cerned as “ potentially” this or that. During gastrulation the ‘ unéy intierl"aii{'l“ -l
outer layers will be designated as usual as hypoblast and epiblas 7; K . ,7’ :~
«.4 . x.  V t;,:
90  EARLY DEVELOPMENT OF AMPHIOXUS
are turned over the edge of the lip and into the growing archenteric
roof. These turned-in rows thus become a part of the hypoblast, while
the other three remain outside as part of the dorsal epiblast. The former
cells will eventually be the source of the notochord, while the latter,
i.e., those not involuted, will furnish material for the neural tube. This
will be referred to again when the origin of these structures is described.
Epiboly.———This process is typically thought of in connection with
large yolked eggs in which a layer or layers of cells overgrow a mass
of yolk. There is of course ‘no such mass in the case of Amphioxus.
Nevertheless part of the gastrulation process here is essentially epibolic,
the gastrular cavity taking the place of solid nutrient material. This
epiboly is accomplished initially in the following manner: The ventrolateral lips tend to become continuous and begin to grow dorsally while
at the same time the dorsal lip becomes more arched. In this way the
originally triangular blastopore loses its angles and becomes more or
less of a transversely placed oval. The dorsal side of this oval now
constitutes the dorso-lateral lip of the blastopore, and the ventral side
the ventro-lateral lip. All parts of the oval then grow toward one another with the lateral parts moving relatively more rapidly than the
dorsal and ventral. As a result of these activities the oval blastopore
presently becomes a small circular opening. Thus an essentially epibolic process is responsible for covering over the gastrular cavity. At
the same time there is also occurring a gradual lengthening of the
entire gastrula owing to active cell division in the blastoporal lips and
elsewhere. In this manner what. might be described as a double walled
tube-shaped sac is formed, the outer layer of the wall being epiblast,
and the inner wall hypoblast (Fig. 51, D, F , G, H). Henceforth this
sac-like structure may be referred to as a larva or embryo. Accompanying these movements there has necessarily been a redistribution of
the material of the mesodermal crescent which Yaccording to Conklin lies
in the two original ventro-lateral lips. The details of this rearrangement
will be taken up in connection with the history of the definitive mesoderm.
Convergence. —— According to previous accounts gastrulation in this
animal has also involved a distinct process of concrescence or flowing
together of the material from the two sides of the dorsal lip along a
median line. Conklin, however, asserts very positively that nothing of
this sort occurs. Nevertheless, he does admit that regions in and about
the lip do contribute substances to the embryo by a process which is
THE CENTRAL NERVOUS SYSTEM 91
essentially convergence as described below. In correlation with this
view Conklin never refers to the lips as the germ ring.
During the above processes the ectoderm cells develop cilia which
vibrate and thus cause the embryo to rotate slowly within the egg mem
-brane.
THE CENTRAL NERVOUS SYSTEM
The early development of the nervous system occurs more or less
simultaneously with the differentiation of the notochord and the mesodermal somites. It is convenient, however, to describe these three proc
esses separately, and we shall therefore begin with the‘ nervous system. ..
The Neural Plate and the Neural Fo1ds.—As previously suggested there exist in the early gastrula about six rows of approximately
ten to twelve cells, each extending transversely across the embryo just
at, and anterior to, the dorsal lip of the blastopore. As indicated the
row immediately adjacent to the lip, and the two next anterior rows, are
presently involuted to the roof of the archenteron. Here they will be
referred to later in connection with the development of the notochord.
The three cell rows which remain outside, together with all the rest of
the epiblast, may henceforth be called ectoderm. These three rows (Fig.
51, E) then give rise to the nervous system in the following manner:
As the embryo increases in length the cells in these rows divide, along
with the others, and so continue to extend from the margin of the dorsal
blastoporal lip very nearly to the anterior end of the embryo. They thus
constitute an elongated‘ band of material about twelve cells in width. It
is the neural or medullary plate. At the same time the ectoderm along
each side of this plate becomes slightly elevated, and these elevations
then begin to grow toward one another above the plate. As this process
continues the ectoderm constituting the elevations becomes separated
from that at the margins of the plate, and the former gradually approach each other until they meet and fuse along the median line (Fig.
52, A, B, C). Thus the medullary plate itself is entirely roofed over,
and during the process it is customary to speak of the free edges of the
two approaching layers of ectoderm as the medullary or neural folds.
As a matter of fact, however, these layers obviously involve none of the
actual medullary plate, and constitute only the outer half of a true fold
(Fig. 52)‘. Hence the neural folds, as here indicated, are but partly homologous with the similarly named structures in most higher forms (see
below). It should now be added that the phenomena just described do
not occur everywhere’ simultaneously. The depression of the neural
/figs»:
92 THE EARLY DEVELOPMENT OF AMPHIOXUS
V .
aciauaq 933%
. Q
B‘?
‘MID
showing formation of nerve cord, notochord and mesoderm. From Kellicott
(Chordate Development). After Cerfontaine. A. Commencement of-the
growth of the superficial ectoderrn (neural folds) above the neural or
medullary plate. B. Continued growth of the ectoderm over the neural
plate. Dilferentiation of the notochord, and first indications of the mesoderm and enterocoelic cavities. C. Section through middle of larva with
two somites. Neural plate folding into a tube. D. Section through first pair
‘of mesodermal somites, now completely constricted oil. E. Section through
middle of larva with nine pairs of somites. Neural plate folded into a tube.
Notochord completely separated. In the inner cells of the somites, muscle
fibrillae are forming. ‘
c. Enterocoel. ch._ Notochord. ec. Ectoderm. en. Endoderm. f. Muscle
fihrillae. g. Gut cavity. m. Unsegrnented mesoderm fold. ms. Mesodermal
somite. nc. Neurocoel. nf. Neural fold. np. Neural plate. nt. Neural tube.
Fig. 52.———Transverse sections through young embryos of Amphioxus, ‘
THE CENTRAL NERVOUS SYSTEM 93
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Fig. 53.—-—Optical sections of young embryos of Amphioxus. From Kellicott
(Chordate Development). After’ Hatschek. The cilia are omitted. A. Two-somite
stage, approximately at the time of hatching, showing relation of neuropore and
neurenteric canal. B. Ninesomite stage, showing origin of anterior gut diverticula.
C. Fifteen-somite stage. End of the embryonic period. ‘
ap. Anterior process of first somite. According to Conklin the existence of this is
doubtful. c. Neurenteric canal. ch. Notochord (or its rudiment, in A). cg. Clubshaped gland (or its rudiment in 8?. ago. External opening of club-shaped gland.
co. Coelomic cavity of somite. cu. Cerebral vesicle. g. Gut cavity (enteron, mesenteron). gs. Rudiment of first gill slit. 1'. Intestine. ld. Left anterior gut diverticulum
(preoral pit in C). In. Mouth. mes. Unsegmented mesoderm. n. Nerve cord (or its
V rudiment, in A). no. Neurocoel. nip. Neuropore. p. Pigment spot in nerve cord. rd.
Right anterior gut diverticulum (preoral head cavity in C). st 52. First and second
mesodermal somites. spc. Splanchnocoel (body cavity).
94 THE EARLY DEVELOPMENT OF AMPHIOXUS
plate begins just in front of the blastopore, and extends anteriorly,
while the fusion of the neural folds begins slightly further forward and
extends both ways. The latter process is further augmented, according
to Conklin, by the continued upgrowth of the ventral lip of the blastopore over the dorsal side. Insofar as this occurs the layer so arising
simply fuses with that of the lateral neural folds as described above
(Fig. 51, H). As a result of these processes the blastopore is presently
entirely roofed over.
The Neuropore. —— Although the blastopore has been covered in the
manner just indicated, the archenteron still communicates with the exterior. This is accomplished by means of the space extending along the
back of the embryo between the neural folds above and the medullary
plate beneath. This space leads from the blastopore forward to the
point where the folds are still in the process of uniting, and here opens
to the outside. This opening is termed the neuropore, and is constantly
advancing as the meeting of the folds continues. At the time of hatching,
which occurs eight to fifteen hours after fertilization, this point is generally somewhat anterior to the middle of the embryo (Fig. 53) .
The Neurocoel and the Neurenteric Canal. —When in approximately this condition as regards the nervous system, the young embryo
breaks out of the egg membranes. Further development of this system
then proceeds as follows. The process of roofing over the medullary
plate is completed so that the neuropore is carried almost to the anterior end of the animal. The center of the neural plate is then some
_ what further depressed, while its edges 3 are bent upward and inward
until they meet (Fig. 52, C, D, E). There is thus formed within the old
space between the archenteric roof and the fused neural folds, a new
tube—- the neural tube, containing a canal, the neural canal or neurocoel (Fig. 53, B). The inner surface of this canal is evidently that of
the original neural plate, and hence as might be expected, is lined with
cilia. From the method of its formation also, it is clear that anteriorly
the neurocoel will open to the exterior at the neuropore and that posteriorly it will still communicate with the archenteron through the
blastopore. This posterior passageway through the blastopore into the
neurocoel is now termed the neurenteric canal. Both neurenteric canal
and neuropore remain open throughout the embryonic period, i.e., until
the mouth is formed.
Later, the anterior portion of the neural tube widens somewhat to
3 These edges are mostly homologous with the inner or nervous portion of the
neural folds as described in the Frog (see below).
DEVELOPMENT OF THE NOTOCHORD 95
form the rudiment of a brain while within the tube at this and other
points, pigment spots appear. These, or the tissues externally adjacent
to them, are probably light receptors.
This is as far as it is necessary to consider the development of 'the
nervous system in Amphioxus. In comparing this development with
that of most higher Chordates there will be found a fundamental similarity. There is one variation in detail, however, which, though it has
already. been indicated, deserves a further word of emphasis. In all
those cases where the neural tube is formed by so-called neural folds
it is only in Amphioxus that the completion of the real tube occurs later
than,..and hence separately from, the overgrowth and fusion of the folds.
Indeed, as will appear from reference to Fig. 43, in all true Vertebrates
in which the tube arises by fold formation, the edge of the plate remains
united to the edge of the outer layer of overgrowing ectoderm until the
folds from opposite sides meet. Thus in these latter cases the structures
so named are truly folds, instead of being only the outer half of a fold
as in Amphioxusf
THE DEVELOPMENT OF THE NOTOCHORD, MESODERMAL SOMITES AND COELOM
The Notochord. —-It will be recalled that in connection with the
development of the nervous system reference was made to the occurrence in the early gastrula of three transverse rows of cells immediately
adjacent to the dorsal lip of the" blastopore. It was indicated that these
cells are involuted into the roof of the archenteron. As the gastrula increases in length the hypoblast cells of these inturned rows multiply
along with the outer epiblastic cells which are to give rise to the neural
plate. Thus like those of the latter structure they produce a lengthening
band ten or twelve cells wide which forms the archenteric roof. As
in the case of the neural plate, this hand then begins to fold, but in this
instance the edges are directed downward instead of upward. Also as
the sides of the fold come together the cells tend to interdigitate (Fig-.
52, B, C, D, E). In this manner a solid rod of tissue is formed, the
notochord, lying immediately beneath the neural tube. Although at first
the notochordal cells are wedge shaped and interdigitated, they eventually become disc-shaped and in a cross sectional View appear, as Conic
4 The peculiar method by which the neural tube is formed in Amphioxus must
probably be regarded as specialized rather than primitive. Upon this same basis
some authorities do not hornologize the overgrowing ectoderm with any part of a
true neural fold.
96 THE EARLY DEVELOPMENT OF AMPHIOXUS_
lin says, to be piled like a stack of coins. Finally their nuclei and protoplasm disappear, leaving a clear substance, presumably possessing a
turgor which helps give rigidity to the entire structure. Posteriorly the
notochord ceases at the neurenteric canal, while anteriorly it eventually
reaches to the extreme anterior end of the embryo in front of the brain
(Fig. 53, C). In this last respect Amphioxus differs from other Chordates in which the notochord always stops beneath the mid-brain.
The Mesodermal Somites and Coelom. — It will be recalled that
according to Conklin the material destined to be mesoderm, like that
destined to form ectoderm and endoderm, is differentiated and visible
clear back in the fertilized egg. Here the potential mesodermal sub- —
stance is gathered in the form of a crescent across what will presently
be the posterior side of the larva. As segmentation occurs this crescent,
as was noted, retains its position, and thus in the early gastrula comes
to lie just inside the ventro-lateral lips of the triangular blastopore. Its
middle section is at the median and ventral-most region where the two
' lips may be said to meet one another, while the two horns of the cres
cent extend antero-dorsally to the angles made by the junction of the
ventro-lateral lips with the dorsal lip (Fig. 51, E, F). It will now be recalled that the two ventro-lateral lips presently become one, the angle
between them never having been a very acute one. Thus as previously
noted the entire‘ blastopore takes on the shape of a transversely placed
oval, the lower lip of which becomes identical with the posterior border
of the crescent. As already indicated, as this ventral lip then moves
upwiard, the middle part of the crescent is likewise raised, and the sides
or horns assume an almost horizontal antero-posterior position; Meanwhile the cells of this potential mesodermal region have become the
most actively dividing in the embryo, and hence the smallest. With the
ensuing drawing together of the blastoporal lips and the lengthening
of the embryo, the material in the former mesodermal crescent suffers
a, further redistribution as follows: The posterior part of this potential
mesodennal material, i.e., the part which has formed the middle of the
crescent, now passes around the ventral and lateral side of the contracted blastopore just within its margin. As a result of the lengthening
process, the former horns then proceed forward in two bands, each of
which is six to nine cells in width. Each band is immediately adjacent
to the edges of the rather flat archenteric roof which is about to fold
downward in the manner indicated to form the notochord. Thus the
hypoblastic bands of potential mesoderm occupy the angles uniting the _
roof of the archenteron with its sides. Before-proceeding further with
DEVELOPMENT OF THE NOTOCHORDE 97’
the fate of these bands it is necessary to pause a moment to consider one
or two theoretical matters.
It will be recalled that under the general discussion of the processes
of gastrulation in the preceding chapter it was indicated that the lip of
the blastopore is sometimes referred to as the germ ring. This is done,
it was said, on the ground that this lip or ring comprises the “ germ”
of the embryo in that each side of it contains half of the embryonic anlage which is then brought into contact with the other half by commacence of the blastoporal lips to form a whole. It was suggested, how-.
ever, that this is scarcely true in the sense originally conceived, and the
present case alfords a good instance of the ways in which the original
conception has had to be modified. First, it is quite evident that only
in the vaguest sense can a half embryonic anlage be said to lie in the
lateral blastoporal lips. All that can be said is that certain materials
for the embryo do pass into it from within or near the lips of the blastopore, the potential mesoderm from the ventro-lateral lips, and potential
neural and notochordal material from the dorsal lip. Secondly, as we
have seen, these materials do not assume their definitive positions by
a simple process of the concrescence of two sides, though the process
may be thought of as a kind of convergence or confluence. If the term
germ ring is to continue to be employed at all therefore it can only be
with a considerably modified significance as indicated in this instance.
Returning now to the further history of the potential mesoderm it
soon appears that the hypoblastic bands on either side of the notochordal region very shortly become folded so as to form grooves with
the grooved side of the fold facing the archenteron (Fig. 52, B, C). In
this manner this part of the hypoblast becomes cut olf from the archenteron, and thus becomes definitive mcsoderm. At the same time the
hypoblast to the lateral side of each groove is drawn toward the midline. Here, as the notochord is also becoming folded off, it is finally
drawn completely together so as entirely to line the archenteric cavity
as definitive endoderm. In both these situations it may be noted that the
folding process is accompanied by, and probably dependent upon, a
change in the shape of cells, causing them to roll over a lip. The gen~
eral significance and widespread occurrence of this mechanism for cell
rearrangement was pointed out in connection with the general discus?
sion of involution as a method of gastrulation.
Meanwhile as the folding process is taking place the mesoderm forming each lateral groove is becoming distinctly moniliform, i.e., transverse constrictions are developing in it particularly at the anterior end.
98 THE EARLY DEVELOPMENT OF AMPHIOXUS
In this way there are soon produced anteriorly definitely separate
mesodermal blocks, each with a small cavity within it. These blocks are
termed mesoclermal somites, and it is to be noted that they are formed
essentially as enterocoelic pouches by a process of folding off from the
archenteron in the presumablyaprimitive manner. Only the first two or
three somites thus formed, however, have actual cavities at this time.
Posteriorly the groove closes as it forms, and the cavities within the
constricted blocks of mesoderm form later. Whenever formed such
cavities represent the beginnings of the coelom, and certain other spaces
to be described presently. Eventually as many as sixty-one pairs of
somites are thus produced. In this connection it must be clearly noted
that the tem somite as used with respect to Amphioxus applies both to
the myotomal region (segmental plate in true Vertebrates), and to the
lateral plate, instead of only to the former. This will become apparent
from what follows. ,
Before proceeding with the further development of the somites a word
should be said concerning a certain classification of mesoderm which
is sometimes made on the basis of the method of its setting aside as
such. Thus it has been seen that the rnesoderm of the first eight or ten
somites arises by the folding off of material which just preceding this
' process lies within the archenteric wall. Later somites, however, arise
more directly from material which is paid into the dorso-lateral regions
from the lips of the blastopore as the embryo elongates. Hence the
somite material (mesoderm) which is set aside in the former manner
has been called gastral, while the "latter arising more directly from the
lips of the blastopore is called peristomial. In view of the fact, however,
as brought out by Conklin, that apparently all the mesoderm has its origin from material at first lying within the -blastoporal lips, such a distinction as the above largely breaks down. All of it is really peristomial.
THE FURTHER DEVELOPMENT OF SOMITES AND COELOM
By the time seven or eight pairs of somites have been formed, it becomes evident that only the members of the first pair and the upper
parts of the second are exactly opposite one another. Posterior to this
the somites of the left side are more and more in advance of their mates
on the right, until soon they alternate. This is a feature peculiarly
characteristic of Amphioxus.
The Lateral Plate.——At the stage of fourteen or fifteen somites
certain further changes begin to appear in the more anterior pairs. In
each somite the enterocoel becomes larger, while the walls of the venSOMITES AND COELOM 99
tral portion below the level of the notochord become thinner. At the
same time this portion begins to lengthen in a postero-ventral direction,
the region thus affected being known as the lateral plate.
The outer wall of this plate next to the ectoderm is called the somatic
or parietal mesoderm,
while the inner wall next
to the enteron is splanchnic or visceral mesoderm.
The part of the enterocoel
which lies between them
is the splanchnocoel or
true coelom. The lateral
plates on each side of the
embryo continue to grow
ventrally until they finally meet. Presently the
ventro-median wall which
at first separates the
splanchnocoels of the two
sides largely disappears,
as well as the walls sepa
rating the successive
splanchnocoels of the F_ 54 D, f tr _
. 1 . .— a
Sarne 5! ae. Thus the g 1 grams 0 KIISVCISG SCCUOTIS
through Amphioxus larvae. From Kellicott (Chor
splanchnocoel or coelom
becomes completely continuous throughout the entire lateral and ventral
region of the animal.
The Myotomal Region. ——While this is go
date Development). A. Through the body region
of a larva with five gill slits, showing separation
of mycococl and splanchnocoel (coelom). B.
Through the region between atriopore and anus
of young individual, shortly after metamorphosis,
showing relations of sclerotome. After Hatschek.
a. Dorsal aorta. c. Coelom (splanchnocoel). ch.
Notochord. d. Dermatome. df. Dorsal fin cavity. :3.
Epidermis. i. Intestine. mc. Myocoel. mp. Muscle
plate (myotome). n. Nerve cord. s. Sclerotomc. v.
Subintestinal vein. 1:)‘. Ventral fin cavity.
ing on in the lower portion
of each somite, the upper portion on a level with the notochord is assuming the < shape characteristic of the adult. It is also becoming thicker,
largely as a result of the horizontal flattening of its cells in the wall
adjacent to the notochord. These cells presently become differentiated
as muscle cells, extend throughout the length of the somite, and nearly
obliterate the enterocoel in this upper region. The thickened muscular
tissue of each somite is then called a myotome, while the slight entero
coelic space still remaining between the latter and the outer unthickened .
100‘ THE EARLY DEVELOPMENT OF AMPHIOXUS
 
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Fig. 5$.—-Sections through young Amphioxus embryos showing the origin of the anterior gut diverticula. From Kellicott (Chordate Development). After
Hatschek. The cilia are omitted. A. Frontal section
through embryo with nine pairs of somites. (See Fig.
53, B.) The dotted line marks the course of the gut
wall ventral to the level of the section. B. Optical
sagittal section through anterior end of embryo with
thirteen pairs of somites, showing position of right
anterior gut diverticulum. C. Same in ventral view.
c. Coelomié cavity of somite. ch. Notochord. csg.
' Rudiment of club-shaped gland. cl. Rudiment of an
terior gut diverticula. ec. Ectoderm. en. Endoderm. g.
'Gut cavity (enteron, znesenteron). gsl. Rudiment of
_iirst gill slit. ld. Left anterior gut diverticulum. n.
Nerve cord. np. Neuropore. rd. Right anterior gut
diverticulum. $15259, First, second and ninth mesodermal somites.
 
 
   
         
   
wall is termed a myocoel (Fig. 54). Later,
between the myotome
and the lateral plate
there develops a horizontal partition which
acts as a boundary between the two regions.
Eventually also there
grows out from the
ventral region of the
myotomal portion of
each somite a fold of
tissue which presently
becomes divided into
two parts. One part
then extends upward
between the myotome
and the noto_chord and
nerve cord as the sclerotome. The inner layer
of this sclerotomal part
finally forms the skeletogenous sheath for
the latter structures,
while its outer layer
forms the covering or
fasciae for the inner
sides of the myotomes
themselves; the latter
have no fasciae on their
outer sides, as they do
in the Craniates. The
other portion of the original fold meanwhile extends outward and downward between the somatic layer of the lateral plate and the ectoderm.
This fold, together with the outer unthickened wall of the upper or myo,-tomal region, is known as the dermatome. The upper myotomal portion
of the dermatome gives rise to the cutie layer of the integument in the
dorsal part of the animal, while the fused inner and outer sheets of the
I dermatomal fold constitute the same layer ventrally. These points should
I
1
1
SOMITES AND COELOM T H 101
be kept in mind, in connection with the development of homologous parts
in the higher Vertebrates.
The Anterior Gut Diverticula. ——Although it is not strictly connected with the formation of the somites, we may mention in closing
the appearance of certain diverticula of the archenteron, which in their
early stages are not unlike enterocoels.5 When about seven pairs of
somites have been formed, there develops from the dorsal wall of the
gut in front of the most anterior somites a transverse ridge. This ridge
thus produces a sort of dorsal bay or pouch at the anterior extremity of
the gut beneath the notochord (Fig. 53, B). The sides of this bay then
push upward on either side of the notochord, thus forming two dorsalateral pouches. The ventral edge of the transverse ridge now grows
anteriorly cutting off these two pouches ventrally from the anterior extremity of the gut beneath them. Each then develops in its own peculiar
fashion (Figs. 53, 55). The right one becomes greatly enlarged, assumes a median position, and occupies the whole of the space beneath
the chorda and in front of the enteron. The left remains smaller «and
finally acquires an opening to the outside of the head known as the preoral pit (Fig. 53, C).
The later development of Amphioxus is too highly specialized to help
us much in an understanding of the higher and more typical Chordates.
It will therefore be omitted. Those students who are interested in the
further history of this animal, however, will find a good brief account
with references to original papers in Kellicott’s Chordate Development.
They should also note the references at the conclusion of this chapter.
REFERENCES T0 LITERATURE
Cerfontaine, P., “'Recherches sur le développement de l’Amphioxus,” Arch. Biol.,
XXII, 1906.
Conklin, E. C., “ The Embryology of Amphioxus,” Jlaur. Morph, LIV, l932.—“The Development oi Isolated and Partially Separated Blastomeres of Amphioxus," Jour. Exp. Zob'l., LXIV, 1933.
Garbowski, T., “ Amphioxus als Grundlage der Mesodermtheorie,” Anat. Anz., XIV,
1898.
Hatschek, B., “ Studien iiber Entwickelung des Amphioxus,” Arbeit. zool. Inst.
Wien. IV, 1882. “Ueber den Schichtenbau von Amphioxus” (Verhand. d.
Anal. Gesell., II), Anat. Anz., Ill, 1888.
Klaatsch, H., “Bemerkung iiher die Gastrula des Amphioxus,” Morph. Jahrb.,
XXV, 1897.
Kowalewsky, A., “Entwickelungsgeschichte des Amphioxus lanceolatus,” Mém.
Acad. Impér. St. P., VII, 11, 1867.—“Weitere Studien fiber die Entwicl:e
5 By some authorities (Hatschek, MacBride) these structures are regarded as
actual, though modified, mesodermal soxnites.
102 THE EARLY DEVELOPMENT OF AMPHIOXUS
Iungsgeschichte des Amphioxus lanceolatus, nebst einem Beitrage zur Homologie des Nervensystems der Wiirmer und Wirbelthiere,” Arch. mikr. Anat.,
XIII, 1877.
Legros, R., “ Sur quelques cas d’asyntaxie blastoporale chez l’Amphioxus,” Mitt.
Zool. Stat. Neapel, XVIII, 1907.—-“Sur le développement des fentes branchiales et des canicules de Weiss-Boveri Chez l’Amphioxus,” Anat. Anz.,
XXXIV, 1909. — (Published anonymously.) “ Sur quelques points de l’anatomie
et du développement de l’Amphioxus: Notes préliminaires. 1. Sur le néphridium
de Hatschek,” Anat. Anz., XXXV, 1910.
Lwofi, B., “ Ueher einige wichtige Punkte in der Entwickelung des Amphioxus,”
Biol. Centr., XII, 1892.—“ Die Bildung der primiiren Keimbléitter und die
Entstehung der Chords. und des Mesoderms bei den Wirbelthieren,” Bull. Soc.
Impér. Mascou, II, 8, 1894. ‘,
MacBride, E. W., “The Early Development of Amphioxus,” Q. J’. M. S., XL,
1898.-——-“ Further Remarks on the Development of Amphioxus,” Q. J. M. S.,
XLIII, 1900.—“ The Formation of the Layers in Amphioxus and its Bearing
on the Interpretation of the Early Ontogenetic Processes in Other Vertebrates,”
Q. J. M. S., LIV, 1909.
Morgan, T. H. and Hazen, A. P., “ The Gastrulation of Amphioxus,” Jour. Morph.,
XVI, 1900.
Samassa, P., “ Studien fiber den Einfiuss des Dotters auf die Gastrulation und die
Bildung der primiiren Keimhléitter de Wirbelthiere, IV. Amphioxus,” Arch.
Entw.-mech., VII, I898.
Sobotta, .I., “ Die Reifung und Befruchtung des Eies yon Amphioxus lanceolatus,”
~ Arch. mikr. Aruzt., L, 1897.
Willey, A., “The Later Larval Development of Amphioxus,” Q. I. M. S., XXXII,
1891. -—Amphioxus and the Ancestry of the Vertebrates (Columbia University
Biological Series II), New York, 1894.
Wilson, E. B., “ Amphioxus and the Mosaic Theory of Development," four. Morph.,
VIII, 1893. I
PART II
THE DEVELOPMENT OF THE FROG
HE FROG: FROM THE PRODUCTION OF THE GERM
CELLS THROUGH GASTRULATION
T H E embryology of the Frog, Rana sp., will be taken up as the
first example of the development of a true Vertebrate, being a valuable object for such study for the following reasons: In the first place
its earlier history furnishes an excellent transition between the corre
sponding stages in Amphioxus and those in animals which are more
highly evolved. Second, the later development of the Frog is also very
suggestive from an evolutionary point of view. Thus it illustrates in a
striking manner the transformation of a purely aquatic gill-breathing
* Vertebrate into one which breathes largely by lungs, and is capable of
extended existence on land. Third, in the course of its development the
Frog shows the origin of practically all of the fundamental Vertebrate
systems. Yet in many cases these systems remain in a rather primitive
condition, and are thus helpful to an understanding of the complications which are met with in other types. Fourth. the development of
the Frog is important bothbecause of the thoroughness with which
it has been observed under normal conditions, and also because of the
active experimental work which has been and is being done upon it and
its near relatives. Lastly, there are also certain practical considerations.
The living material is usually available at an appropriate time of year,
it is easy to handle, and the young can be readily cared for under laboratory conditions.
THE REPRODUCTIVE ORGANS or THE ADULT, oc">eENE—
SIS, AND THE EXTRUSION or THE OVA
THE MALE ORGAN S
The Testes. —-There are two" testes in the Frog, each one lying in
the dorsal region of the coelom, close to the kidney (Fig. 56). Each is
enveloped by the peritoneal epithelium, which is fused above the organ
into a two-layered sheet of tissue, like a mesentery. This sheet attaches
the testis to the body wall and is termed the mesorchium. In appearance
,m
~ THE MALE ORGANS 105
each testis is a white ovoid body.
which may be a half inch or. so in
length. In some species in which _the
sperm are produced continuously,
the size of the organ remains fairly
' constant. In others, however, in which
‘ spermatogenesis is chiefly confined to
the breeding seasons, the dimensions
vary considerably. This variation is
‘nevertheless relatively small com
pared to what always occurs in the
ovary.
In structure each testis consists essentially of a mass of seminiferous
tubules. These are grouped into lobules and the latter again into lobes
separated by thin partitions of supporting or connective tissue. This tissue also covers the whole organ in a
coat called the tunica albuginea, outside of which is finally the peritoneum. The walls of the tubules are
lined internally with follicle or nutrient cells (Sertoli cells), while between the latter and the lumen of
each tubule come groups of germ
cells in various stages of development, those in any given group being
in approximately the same stage‘ As
the cells of a group reach the condition of spermatids their heads are
gathered together and the tips embedded in a Sertoli cell. Finally when
fully ripe the spermatozoa are liberated into the tubular lumen.
To the anterior end of each testis
Fig. 56.--The male urinogenital
system of the adult Frog (Rana
pipiens) viewed from the ventral
side. The testes in this case are
medium sized. The urinary bladder and rectum have been dissected out and reflected posteriorly. Otherwise in the ventral
View they would cover the lower
part of the reproductive organs.
Note the large fat bodies as compared with those in the’ female.
Also note'\ the rudimentary oviducts. In many species of Frogs
these ducts do not develop so far
in the male as in R. pipiens. They
have no known function in this
sex.
ad. Adrenals. bv. Blood vessel.
cl. Cloaca. fb. Fat bodies. 1:. Kidney '(mesonephros). od’. Rudimentary oviduct. ‘r. Rectum. sv.
Seminal vesicle. t. Testis. ub. Urinary bladder. ur. Ureter, in the
male serving also as a vas deferens. ut’. Rudimentary -uterus. ve.
Vasa eflerentia.
otobedrawnonatthistime.
is attached a fat body, composed of a mass of yellow streamers. Its function is uncertain. Inasmuch as the animals do not eat during the breeding season, however, it may serve as an extra supply of nutrient material
106 THE FROG: THROUGH GASTRULATION
The Sperm Ducts. —The tubules of each testis open into about a
dozen fine ducts, the vasa eflerentia. These connect with some of the
more anterior kidney tubules, which thus function as continuations of
the vase eiferentia as well as in excretion. These tubules in turn of
course empty into each kidney duct, which therefore
acts as both ureter and
sperm duct (vas deferens) .
The two vasa deferentia are
dilated just before entering
the cloaca to form the seminal vesicles. In these, the
sperm are stored previous
to discharge.
THE FEMALE ORCANS
The Ovaries. —— The
ovaries are also paired organs and occupy the same
relative position as the
testes (Fig. 57). As in the
case of the latter, each is
Fig. 57.—The female urinogenital system of
the adult Frog (Rana pipiens) viewed from the
ventral side. The left ovary has been removed,
showing the fat body, kidney and oviduct upon
that side. The right ovary full of nearly mature
eggs remains in place. Note that the fat body is
smaller than in the male, having presumably
suffered depletion during the development of
the eggs. The urinary bladder and rectum are
omitted from the figure, but occur in the same
position as in the male. .
inf. Infundibulum. o. Ovary. ad. Oviduct. ut.
Uterus. Other abbreviations as in Fig. 56.
suspended from the body
wall by a double sheet of
peritoneal tissue in this instance called the mesovarium. Unlike the testes,
however, the ovaries always
vary greatly in size and appearance, depending upon
the time of year. After ovulation in the spring they
appear as flattened cream colored organs, about three—quarters of an inch
long in Rana pipiens, with a few dark specks scattered through them. As
the oiigonia for the ensuing season multiply and presently grow into
oiicytes, however, the organs increase immensely in size, and by the end of
the summer they occupy a large share of the body cavity. They are now
lobulated in form, and exhibit a characteristic black and white speckling, due to the color of the ripe eggs. Under normal circumstances they
OOGENESIS 107
remain in this condition throughout the winter. As will be indicated later,
however, the eggs are completely developed, and by artificial means
such ovaries can be made to ovulate viable ova at any time.
In structure, the ovary consists of a number of compartments, whose
outer walls are formed of connective tissue or stroma. Within the compartments the oiigonia may be in the process of multiplication, as suggested above, or if this stage has passed the compartments will be filled
with oiicytes. Each of these oéicytes is surrounded by a single layer of
flattened cells which constitute its follicle. Outside of this is another
layer termed the theca, which serves to attach the ovum to the wall of
its compartmert. This theca in turn is divided into an outer layer containing chiefly blood vessels, the theca externa, and an inner layer of
smooth muscle fibers, the theca interna.
Attached to the anterior end of each ovary is a fat body similar in
appearance, and presumably in general function, to those connected
with the testes.
The Oviducts. ———These are long convoluted tubes whose size and
convolutions are somewhat increased during the breeding season. They
open anteriorly into the coelom by a ciliated funnel, the infundibulum.
Posteriorly they open into the cloaca. Throughout the greater part of
their length the walls are quite thick, especially during breeding time.
This thickening is due to the hyper-development of numerous simple
tubular glands which secrete the gelatinous covering of the eggs. The
lumen of the ducts is lined by ciliated epithelium. At the posterior end,
each duct widens and its walls become thinner and very elastic. These
dilated regions, known as the uteri, serve for storing the ova just prior to
extrusion. Each duct is covered by a layer of peritoneum and slung from
the dorsal body wall in the same manner as are the gonads.
OGGENESIS
The Ofigonia. —— The normal breeding season, as already suggested,
occurs in the spring or early summer. At this time the ovaries are emptied of ripe eggs, and the relatively few oiigonia which remain begin to
multiply to produce the eggs for the next season. These occur in nests,
and in each such nest only one cell is destined finally to become an
ovum, the others constituting its follicle. As soon as an ovum has become definitely differentiated as such, and its follicle formed, the period of growth and membrane formation sets in.
‘The Growth Period.-——When this period has been reached the
young ovum or oiicyte, as it may now be called, begins to accumulate
A  ..Tr..;..- -~
 
is 5
108
THE FROG: THROUGH GASTRULATION
Fig. 58.--Oogenesis in the Frog (R. temporaria). From Kellicott
(Chordate Development). A—E, after Lams. F—I, after Lebrun. A. Primary oocyte in synizesis. B. Primary oocyte with vitelline substance
(yolk) of mitochondrial (chromidial?) origin in the cytoplasm. C. Primary oocyte showing feathery chromosomes and chromatin nucleoli. D.
Primary oocyte with ring-like vitelline mass. E. Primary oocyte showing cytoplasm in two zones. F. Nuclear region of primary oocyte after
dissolution of the nuclear membrane showing the small chromosomes
and large chromatin nucleoli. Egg still in ovary. C. First polar spindle
in primary position. From egg in body cavity. H. First polar spindle in
metaphase. From egg in uterus. I. First polar body formed and second
polar spindle forming. From eggs in uterus.
c. Centrosorne. ch. Chromosomes. f. Follicle cells. g. Contents of germinal vesicle. n.'Chroznazin nucleoli. v. Vitelline substance of mito
bd "..Ylk]t.I.F' 1 ‘d1
«.01.. my in 1). zz.°sZc§.L‘f’,§‘o13. sp‘.-’..ai§" °‘ W ‘W “"" °
OOGENESIS 109
yolk. Before this starts nucleoli appear under the nuclear membrane.
Also hasophilic yolk-nuclei arise within the cytoplasm, and move first
to the cell periphery and second to the nuclear periphery. The yolk then
develops as granules just beneath the surface of the oocyte. Though the
source of these granules is uncertain, they may be derived from Golgi
apparatus, the ground substance of the cytoplasm and the nucleus (Hibbard, ’28) . This layer of granules gradually widens, and the granules or
platelets increase in size (Fig. 58, B, D, E). Eventually, the entire cytoplasm is filled with yolk (Kemp, ’53), but the platelets are larger and
more concentrated in what proves to be the vegetal half of the egg,
thus making the latter telolecithal. What causes this polarity is still
unknown. However, it is initiated very early by establishment of a
ribonucleoprotein gradient (Brachet, ’4~7b), a movement of the nucleus
toward the animal pole, and by the collection of pigment beneath the
surface of the animal hemisphere (Wittek, ’52). This pigment soon
spreads somewhat below the egg equator, shading in the vegetal hemisphere into a creamy white, thus giving the Frog ovary its speckled appearance. The ovum has meantime been acquiring two membranes. The
inner membrane is an extremely delicate and close-fitting envelope secreted by the egg itself. It is therefore a true vitelline membrane, but is
so thin that its actual existence is denied by some investigators. The
outer covering is thin, but tough, and is formed by the follicle. Hence
it is a secondary membrane or chorion.
While the ovum has been growing and acquiring its membranes, the
nucleus has been passing through the stages preliminary to the first
maturation division. In the female Frog these stages vary somewhat
from what has been described as typical. The chief difference consists
in the fact that after synizesis (Fig. 58, A), the chromatin threads are
less visible so that when the heterochromosomes for -the first maturation
division later appear they seem to come from the chromatin nucleoli, but
this is unlikely. They probably arise as usual from chromonema threads.
(Fig. 58, C, D, E, F).
Before these chromosomes actually form, however, certain other
events occur, as follows: The nucleus moves quite close to the animal
pole, and the latter becomes slightly flattened. It is also claimed by some
that the pigment of this pole withdraws to a certain extent just above
the nucleus to form a small light area termed the fovea. The writer has
never observed this in normal freshly spawned eggs, but this does not
preclude its existence in eggs at the proper stage within the ovary or
oviduct. Porter (’39) notes the existence of a small white spot at the
110 THE FROG: THROUGH GASTRULATION
animal pole, with a dark dot within it marking the location of the second maturation spindle. This, however, was in eggs outside the ovary,
and he makes no reference to the term “ fovea.” Likewise Rugh and
others have noted that a fading of pigment occurs at the animal pole of
aging eggs, but this again is in eggs outside the ovary, and probably
not in a normal condition. The fovea as originally described therefore
is, if it exists, apparently a separate phenomenon. The egg has now
reached a diameter of from 1.5 to 3 mm., depending upon the species
of Frog, and is ready for ovulation.
As noted, the series of processes leading to this result have taken
place during the summer, and are virtually completed before the time
of hibernating arrives. The eggs then normally remain in this condition
until the period of spawning in the following spring.
OVULATION TO F ERTILIZATION
Ovulation.—When spring arrives the ova are released from the
ovary by the process known as ovulation. It was originally thought that
the embrace of the male Frog known as amplexus, which occurs
throughout spawning, was a necessary stimulus for the ovulatory process. As Rugh (’37) has so ably shown, however, amplexus really has
nothing to do with it. This investigator clearly demonstrated that ovulation is brought about by an increase in the secretion of one of the
pituitary hormones. Thus by injecting a suliicient number of minced
pituitary glands into the body of a female Frog, ovulation can be artificially produced at any time when the ovary contains ripe eggs. Pituitaries from female frogs are more eflective than those from males.
However, any pituitary will probably do if properly prepared. The production of ovulation. by this technique has been a great boon to Frog
embryologists, since it is now possible to obtain fertiliiable eggs at least
nine months out of the year._ The process of ovulation itself may be described as follows: The ovarian follicle breaks, and the ripe ovum is
forced out through the epithelial covering of the ovary into the coelom.
No matter in what region of the body cavity this act may occur, ciliary
action on the peritoneum serves to convey the egg to the mouth or infundibulum of the oviduct. This is also ciliated and the ovum is drawn
into the duct.
The First Maturation Division.-—-Before following the progress
of the egg further it will be necessary to return for a moment to processes occurring within it. '
At about the time of ovulation the nuclear membrane dissolves, and
OVULATION TO FERTILIZATION A 111
shortly afterward the chromosomes of the first maturation figure arise
from the nucleoli, as indicated above. As this figure forms, another
peculiarity of maturation in the female Frog becomes evident, for
neither centrioles, centrosomes nor asters are visible. Out of the fibrillar
protoplasm, however, a spindle develops, division of the chromosomes
occurs, and the first polar body is pinched off while the egg is in the
upper part of the oviduct.
This body lies just beneath the
chorionic membrane. Immediately following this the
spindle for the second division develops, and the division proceeds to the metaphase. In this stage it remains
until after fertilization.
The Tertiary Egg Coverings.—As the egg passes
down the oviduct from the infundibulum to the uterus the
walls of the duct secrete about
it three or four layers of 3]. Fig. 59.—Egg of Frog a short time after
. . . laying and fertilization, showing the swollen
bummous mammal whlch c°n' egg membranes. From Ziegler (Lehrbuch,
stitute a tertiary covering. etc-ls after 0- 5°h“1tZe
. b. Th h ' bl 1
These layers are hardly d1s- m’é’ume r.fenfhf§£ZT"p."'§i‘;§';Znt§dppiiefii
finct as Such at this time, but tion path of the spermatozoon. r. Polar bod
. ' 1‘ ' ‘ ' Hi .1 2 ‘
as mu appear below they be :§§d.¥1’;‘i;3 §:i:¥“§u.?.if.§i.“::...;...1.f;,i§:‘§
come so after contact with the layers of “jelly.”
water.
Spawning. ——Within about two hours after entering the infundibulum the egg reaches the uterus where it may remain for a day or two
until this portion of the duct is full. The accumulated mass of ova are
then expelled into the water, and in the common American Wood Frog
a single such act of expulsion usually completes the process of spawning. In some varieties of Frog, however, the expulsive act is followed
by another accumulation of eggs, and the spawning period is thus prolonged. Hence, though in American Frogs its duration is usually not
more than a few days, in some,European species it may continue for
over a week, the process in any case being retarded by cold. As already
noted the male remains in amplexus throughout this time, although in
those instances where repeated expulsions are the rule, the actual extru112 THE FROG: THROUGH GASTRULATION
sion of eggs generally occurs only in the early mornings of successive
days. In this way he is always in a position to discharge sperm over the
ova as they emerge. Furthermore, although this act of amplexus has
been shown to have nothing whatever to do with ovulation, it is now
clear, as intimated above, that it does afford the stimulation for spawning. Without it “ stripping ” of the female is necessary in order to press
the accumulated eggs out of her uteri. The total number of eggs
spawned in a season varies in different species of Frogs and in different individuals. Thus in Rana Lemporaria it runs from 1000 to 2000,
while in Rana esculenm it may be anywhere from 5000 to 10,000.
It is of some interest in this connection to note the factor which is
the stimulus for amplexus on the part of the male. It might be assumed
to be the presence of the female, or at least of a female with eggs in her
uteri. Such, however, is not the case. As again clearly shown by Rugh
(’37) this action. on the part of the male Frog is, -like ovulation in the
female, entirely conditioned by a secretion of the anterior pituitary.
Indeed not only does the secretion of his pituitary cause him to go into
amplexus with a female Frog, or any other convenient object, but it
also brings about the release of ripe sperm from the Sertoli cells of his
testis. Without an adequate increase in this hormone on the other hand,
the male shows no interest in a female even though her uteri may be
filled with eggs.
The Effect of Water on the Tertiary Membrane. ——After
spawning the membrane indicated above of course comes in contact
with the water, and by absorbing it, begins immediately to swell. This
action progresses rather rapidly at first, so that within two or three minutes the jelly-like covering has increased from one sixth the diameter of
the egg to about one half that diameter. In fifteen minutes it generally
equals the egg diameter: thereafter the swelling becomes slower. At this
point, if fertilization has not occurred the absorption of water by the
jelly is said almost to cease. If fertilization has taken place, however,
the swelling process may continue for several hours until the thickness
of the jelly is as much as twice the width of the ovum.
This thickening reveals more clearly the three or four layers of which
the jelly membrane is really composed. The innermost is a thin dense
stratum applied closely to the chorion, and sometimes erroneously referred to as the chorion itself. Next comes a rather thick and watery
layer, and finally one which is both thick and firm. When a fourth is
present it is thin and fibrous; it does not occur outside, butijust beneath the thick firm layer which is always outermost.
FERTILIZATION 113
Although some species of Frogs have elaborate habits connected with
the care of the eggs, the common Frog does not. When fertilized, the
eggs are simply deposited and left to their fate. On this account the
thick envelope of jelly which they possess appears to exercise several
important functions. In the first place it serves to attach them to each
other and to debris, so that they are not readily washed abo.ut. It
protects them from mechanical injury, and also appears to be distasteful to water snails and perhaps other animals.
In addition to these functions it has long been claimed that the jelly
serves as a lens to concentrate the rays of the sun upon the eggs, and
thus to raise their temperature. This it was assumed would be of advantage because it would speed up the otherwise slow development in
the cold water of early spring. This particular claim and assumption,
however, is an excellent example of the way in which an untested assertion which seems superficially reasonable, may become widely accepted,
and yet be entirely without foundation in fact. "Thus to begin with,
Hugh (’33) showed that temperatures a little too high will injure the
eggs, and we know from other sources (see below) that such temperatures upset the sex ratio. Hence it would appear probable that the risk
accompanying such an effect as suggested would more than overbalance
any possible advantage. Bethat as it may, Rugh has further shown that
the water in which the eggs occur, plus the jelly, which is about 78 percent water, filters out most of -the radiant energy of a heat-producing
character. Consequently the light which the eggs receive, even though it
is absorbed by the black pigment on their surface, produces relatively
little heat. Lastly Cornman and Crier (’4-1) have demonstrated very
conclusively that even if there were any heat. in the light passing
through the jelly, the latter totally lacks the effect of a lens. Indeed its
refractive index is about that of the water in which it occurs, and hence
with the curvatures involved would bring the light to a focus far beyond the egg. Thus it would appear that far from raising the tempera
ture of Frog eggs the jelly may even act as an insulator to keep them
from getting too warm.
FERTILIZATION AND EGG SYMMETRY
FERTILIZATION
The Penetration of the Sperm. —— As the eggs are extruded by the
female, the male Frog immediately discharges over them the seminal
fluid. This fluid contains thousands of spermatozoa, and hence the eggs
114 THE FROG: THROUGH GASTRULATION
tend to be surrounded by them. Many of these pierce the outer jelly, I
but usually one of them is slightly in advance of its fellows and thus
arrives first at the surface of the egg itself. As soon as it has started to
enter some change is effected in the egg so that the remaining sperm are
unable to pass beyond the jelly. Polyspermy is thus abnormal in the
Frog and when it occurs the course of development is interfered with.
The entrance of the sperm always occurs in the animal hemisphere of
the egg, and usually, according to some authorities, about 40° from the
pole. Aside from these limitations, however, there is apparently nothing
which fixes the point of penetration; that is, this point may be located
on any one of the infinite number of meridians which may be imagined
to pass from one pole of the egg to the other.
The Perivitelline Space.——The penetration of the‘ ovum by the
sperm seems to cause the egg to give up a certain amount of its fluid.
In any case, whatever its source, fluid does collect at this time between
the chorion and the surface of the ovum. It is indeed presumably inside
the vitelline membrane if the latter exists, and hence the space containing this fluid is as usual termed the perivitelline space. Its formation
releases the egg from the grip of its coverings so that it is free to rotate
within them. Under these conditions if the lighter animal pole is not
already uppermost it presently becomes so. _
The Entrance Path.—— In the case of the Frog the whole spermatozoan enters the ovum, and it usually requires a minute or two for it
to get entirely inside. The tail then disintegrates, and the head and
middle piece travel steadily along a path which is generally approximately a radius of the egg, leaving a trail of pigment behind them (_ Fig.
60, A). This is the penetration or entrance path, and as the head and
middle piece move along it, the usual rotation of these parts occurs,
thus placing the latter structure in the lead. At the same time the head
is enlarging to form a typical nucleus.
The Second Maturation Division.—Meanwhile the stimulus of
the entrance of the sperm has incited the completion of the second maturation division of the egg nucleus which had paused in the metaphase.
After throwing off the second polar body, the egg nucleus withdraws
from the surface of the ovum, usually to a position in the egg axis. The
sperm nucleus then proceeds toward it.
The Copulation Path and the Fusion of the Egg and Sperm
Nuclei.—-—As suggested under the general topic of fertilization, the
course followed by the sperm immediately after its penetration of the
egg (i.e., the entrance path) may not be directed exactly toward the egg
. SYMMETRY or THE OVUM 115
nucleus. In those instances where it is not, therefore, the point where
the sperm does start to move directly toward this nucleus is marked by
a slight change in its course. The second portion of the sperm path
which thus arises, as has already been noted, is then called the copulation path, and like the first portion, in the case of the Frog, it is marked
by a trail of pigment (Fig. 60, A).
Proceeding along this second path the sperm nucleus presently meets
that of the ovum. Meanwhile the middle piece has initiated the formation of a division-center and aster, and before the meeting of the pronuclei occurs this new center and its aster have divided into two. The division has taken place at right angles to the copulation path, and hence
as the nuclei come together the axis joining the division-centers coincides with their plane of union (Fig. 60, A, B).
THE SYMMETRY OF THE OVUM AND ITS SIGNIFICANCE
The causes which determine the symmetry of any ovum and the relation which this symmetry bears to cleavage and to the symmetry of the
embryo are subjects of fundamental importance for the understanding
of development. They have therefore received considerable attention in
different groups of animals, and among Vertebrates the Frog’s egg has
seemed particularly well adapted for such study. Hence it appears desirable in the case of this animal to make some mention of the results
to which this study has led. It must be noted, however, that in spite of
the work which has been done, there still exists some disagreement as
to the exact facts, at least as regards certain details. In the interest of
clearness, therefore, it seems best merely to state the main features of
this phase of development in the Frog according to one view, the accounts followed being chiefly those of Roux and J enlcinson.
The First Plane of Symmetry.———Before the egg is fertilized it is
radially symmetrical about an axis passing through its poles. The
penetration of its surface by the sperm, however, confers upon it a bilateral symmetry. That is to say, the point of this penetration, together
with the polar axis, determines a plane which, save for the possible
eccentricity of the egg nucleus, divides the ovum into equal halves. It
may be termed, therefore, the sperm entrance point plane (Fig. 60, A).
The existence of this plane of symmetry,'determined solely by the egg
axis and the sperm entrance point, however, is brief. Other factors presently enter which determine a second plane, often, though not necessarily, closely correlated with the first (see below), and developed in
the following manner: ‘
116 THE FROG: THROUGH GASTRULATION
also cleavage plane
sperm entrance l
point.
sperm entrance deavagg
P°”“ \. / plane
entrance
   
 
 
 
   
 
 
 
 
entrance
path _
copulation
path COP’;
pat
mitotic
spindle
3'3Y
crescent
A W .n& embryonic
crescent axis
b d . _ C '3 / entrance point plane
em ryonic axis an entrancexpom p ne
5 erm entrance
sperm entrance P point
entrance
cleavage path
plane‘ _
8'3)’
crescent
\
cleavage
plane
gray
C"°5'5€""v embryonic
entrance point plane axis
embryonic axis and entrance
point plane, also cleavage
plane
Fig. 60. —— Diagram to illustrate some of the possible relations of the axes in a
fertilized Frog egg. In all cases the egg is assumed to be viewed from the animal
pole. The arrow indicates the longitudinal axis oi the future embryo, with the
head pointing anteriorly. The dash line indicates the first cleavage plane where
the latter does not coincide with the longitudinal axis of the future embryo. The
dotted line indicates the entrance point plane where this does not coincide with
the longitudinal axis of the future embryo. The dot in the center indicates the
center of the animal pole.
A. An egg in which the entrance point plane, the entrance and copulation paths,
the gray crescent plane, the first cleavage plane and the longitudinal axes of the
future embryo all coincide. B. An egg in which the entrance path and the copuIa~
tion path are not in the same straight line. Hence the gray crescent plane and the
longitudinal axis of the future embryo fail to coincide with either the entrance
point plane or the first cleavage plane. C. An egg distorted by pressure. Notethe
consequent orientation of the mitotic spindle as explained in text. This prevents
coincidence of the first cleavage plane with any of the others. D. The same situation with the added complication due to the fact that as in B the entrance path and
copulation path are not in the same straight line. Note that in all instances the gray
crescent plane and that of the longitudinal axis of the future embryo coincide.
EGG SYMMETRY OF THE OVUM
Fig. 61.—CIeavage stages and the beginning of gastrulation in the
Frog’s egg (Rana pipiens). The shading in this figure indicates the distribution of pigment, except along the lines of cleavage, where as usual
it denotes shadow. A. Fertilized egg viewed from the left side in terms
of the future embryo. Note the left half of the gray crescent at the
right side of the figure, i.e.. its dorsal side in terms of the embryo. B.
An egg in which the first cleavage has been almost completed. Since
the egg is again being viewed nearly from its left side in terms of the
future embryo, the cleavage furrow is virtually in the plane of the
paper and scarcely shows. The gray crescent is again to the right as in
A, but at this stage the region of the crescent has evidently become
whitened and so added to the original light area of the vegetal pole.
C. An incomplete four-cell stage, also viewed from the left side. The
second furrow has not quite reached the vegetal pole. D. A view of C
from the animal pole, with the region of the gray crescent toward
the right (dorsal). E. An eight-cell stage. The animal pole is again at
the top of the page, and the vegetal pole at the bottom, but the future
dorsal region is turned slightly toward the observer, thus showing art
of the first furrow. F. An approximate sixteen-cell stage directly mm
the left side. The cleavage is obviously somewhat irregular. G. Between
a 64- and 128-cell stage viewed from the left side. H. A virtually complete blastula‘ from the left side. Note that the pigmented area is tending to move downward somewhat. I. An early gastrula from the left
side. The cells in the animal hemisphere are too small and numerous to
indicate separately. The beginning of the blastopore lip is visible as a
slight notch in the lower right side of the figure.
117
118 THE FROG: THROUGH GASTRULATION
The Second Plane of Symrnetry'.——As the sperm travels along
the first part of its path within the egg, it seems to cause certain disturbances in the egg substance. The result is a more thorough separation between yolk and cytoplasm, and an apparent streaming of the
latter in the direction of the sperm. This flow seems to cause a withdrawal of pigment granules from along the border of the pigmented
animal hemisphere on the side of the egg from which the How is taking
place, i.e., the side approximately opposite to that upon which the
sperm entered. The result is the appearance upon that portion of the
pigmented border of a lighter strip termed the gray crescent. This crescent is usually quite clear shortly after fertilization and during the first
few cleavages. After a little time, however, its outlines become less distinct. Hence its existence is soon detectable only by the fact that the light
area extends somewhat higher up on the side of the egg where a definite
crescent originally occurred (Fig. 61). The new plane of symmetry,
therefore, is one which again passes through the egg axis and also bisects the gray crescent, or the increased area of white which replaces
it. It may be called the second or gray crescent plane, and by virtue of
its method of formation it will evidently have a decided tendency, as
suggested above, to-coincide with that of the sperm entrance point (i Fig.
60, A ). That this is a tendency rather than an inevitable condition, however is due to the following considerations:
It will be recalled that the path of a sperm toward the egg nucleus
is not necessarily a straight one. Presumably because of failure to enter
at quite he correct angle, the sperm may not at first be headed in the
right direction, and hence has to alter its course, thus producing the
initial or entrance path and the later copulation path. But, as suggested
above, ithtprns put phat tlhe infiuednce of the spelrm in causing the pigment wit rawa is arrve y exerte as it asses a on the entrance ath.
Therefore, if the entranoce path does not happen to Ii: in a vertical rilane
coinciding with the poles and a radius of the ear , it follows that in such
cases the entrance point plane and the gray crgsghent plane also will not
coincide (Fig. 60, B).
The Cleavage Plane. —Following the union of the egg and sperm
a third plane makes its appearance, i.e., that of the first cleavage. This
incidentally is of course an actual plane, not merely a hypothetical one
determined by three points. Under normal conditions this plane passes
approximately through the animal and vegetal poles, a condition resulting from the following facts:
In accordance with a generalization known as Hertwig’s law the
, .-.,___,.,_._. ,, ........
SYMMETRY OF THE OVUM 119
mitotic spindle always tends to lie so that its longitudinal axis coincides
with that of the yolk-free cytoplasm of the cell. Now in the Frog egg
this yolk-free cytoplasm ordinarily occupies about the upper third"of
the animal hemisphere, and hence has approximately the form of a
rather thick plano-convex lens. Therefore the long axis of the spindle
may fulfill Hertwig’s law by lying in any direction so long as it is parallel to the fiat surface of the lens-shaped disc of cytoplasm. This will
of course also make it at right angles to the polar axis of the egg. Furthermore, since the egg nucleus is in this axis the movement of the
sperm and spindle to that nucleus will presently cause the middle of the
spindle to coincide with the eggs polar axis. Finally because the plane
of cleavage is perpendicular to the length of the spindle at its middle,
this plane will also coincide with the eggs polar axis and so pass
through its poles (Fig. 60, A, B).
Though Hertwig’s law thus determines that the first cleavage must
pass through the egg poles, this law does not determine with which of
the infinite number of imaginary radii emanating from the polar axis
the cleavage must coincide. There is another consideration, however,
which does determine the radial direction of this cleavage. The sperm
division center, it will be recalled, divides so as to cause a new mitotic
spindle to form at right angles to the copulation path. Hence the cleavage plane should coincide with this path, as well as pass through the
poles of the ‘egg. Under most circumstances these are the only factors
involved, and such coincidence occurs (Fig. 60, A, B). It should be
noted, however, that pressure on the egg perpendicular to its polar axis
may distort the lens-shaped disc of cytoplasm so that its periphery is
no longer circular. Under such conditions the mitotic spindle, in accordance with Hertwig’s law, will be displaced so that the cleavage
plane may not be related to any other (Fig. 60, C, D).
The Plane of Embryonic Symmetry. —This plane is of course
the one which divides the future embryo into equal right and left halves.
In the Frog it always coincides with the gray crescent plane (Fig. 60),
i.e., except when the latter fails to exist (see below}. This coincidence‘
results from the fact that normally the dorsal blastoporal lip develops
at the middle of the lower border of the crescent. On this basis one
might assume that the median plane is determined by the gray crescent,
the latter having been in turn determined by the entrance path of the
sperm. Indeed this has been quite generally regarded as true. As parenthetically suggested above, however, it must now be stated that the
existence of a gray crescent is not inevitable. Thus the writer has ob120 THE FROG: THROUGH GASTRULATION
served fertilized eggs in which the pigment merely tapered 01? in
streamers more or less equally distributed on every side. Yet many of
these eggs appeared to develop quite normally. It should be added that
these were eggs which had been obtained by stripping pituitary injected
females, and which had then been artificially inseminated. Whether this
lack of a gray crescent ever occurs in eggs normally produced the author cannot say, but it seems not unlikely that it does. Indeed this seems
highly probable in view of the fact that in some Amphibian eggs there
is no pigment from which a crescent can be formed, and yet needless to
say, these eggs develop an embryonic symmetry.
_In view of these facts, then, the question arises as to what if any relation the gray crescent, when it exists, really does have to embryonic
symmetry, since, under some circumstances, the latter can quite evi
dently develop without it. The most probable explanation of the situa--_
tion seems to be this: The passage of the sperm along the entrance path
causes a rearrangement of materials within the egg with a certain reference to this path. Of this there seems little doubt. Normally, moreover,
this rearrangement involves the withdrawal of superficial pigment in the
eggs of those Amphibians which possess it, and thus produces the gray
crescent. However, the two phenomena, i.e., withdrawal of pigment and‘
rearrangement of internal ‘materials, are not inevitably connected, and
it is the latter which is fundamentally significant: Hence it would appear
that the entrance path of the sperm is the initially determining factor
of embryonic symmetry in fertilized Amphibian eggs. What this factor
may be in eggs artificially stimulated to parthenogenesis is at present
unknown. Also, what may happen to the initially determined symmetry
in eggs later abnormally oriented remains to be stated (see below).
Relationship of the Various Planes Summarized. ———There have
now been defined ‘four planes, the sperm entrance point plane, the gray
‘crescent plane, the first cleavage plane, and the plane of embryonic
symmetry. Of these four the one most frequently out of line with the
others is that of the sperm entrance point. This is because, as shown, the
other planes are all related in one way or another to the path, or paths
of the sperm, and not essentially to its point of entrance. Thus the gray
crescent plane is determined by the entrance path. The cleavage plane
in turn is fixed by the copulation path in conjunction with the shape
of the yolk-free cytoplasm and its relation to the egg poles. The plane
of embryonic symmetry normally coincides with that of the gray crescent, but this is probably not a causal relationship. The really fundamental determiner of embryonic symmetry under normal conditions is
CONCLUSIONS FROM EXPERIMENTS
121
probably the path of sperm entrance. In conclusion it may be stated
that there will be a considerable tendency for all four planes to coin
cide (Fig. 60, A).
CONCLUSIONS DERIVED FROM EXPERIMENTS
It is of interest in connection with the question of the relation of embryonic symmetry to the cleavage and gray crescent planes to note the
results of certain experiments which have been performed upon the two cell stage of the Frog and
other Amphibians. It is not possible to kill or re
._ move one blastomere of the egg of the common
Frog without killing the other. It has been found,
however, that if a hot needle is thrust into one of the
cells, this cell though not dead will fail to divide.
Under these circumstances it was long ago discovered by Roux (’88), Morgan (’O2, ’O4), Hertwig
(’93) , and others, that when this is done to eggs in
which the first cleavage plane has passed through
the middle of the gray crescent, the uninjured cell
may eontinue to develop. Under these conditions it
Fig. 62.——A half
embryo of the Frog
produced by thrusting a hot needle
into one of the first
two blastomeres.
After Roux.
then generally produces approximately the lateral half of an embryo,
with the undeveloped hemisphere of material comprising the other
blastomere adhering to it (Fig. 62). Another investigator, McClendon
(’10), then found that in the case of the tree frog,
Chorophilus, it is possible by the proper technique
to remove one of the first two blastomeres without
injuring the other. When this was done it was discovered that the remaining cell developed not into
a half embryo as in the preceding experiment, but
into a whole one. Taken together these results might
reasonably be interpreted to mean that the failure
Fig 63_ _ Two to develop a whole embryo in the first case was due
Frqg €mb1'Y0S simply to the inhibiting presence of the inert blasteEglétfid proléfgéd 12;). mere, and indeed McClendon himself did reach this
inverting the tW0- conclusion. Other facts exist, however, which render
gfilultifge‘ Aim another interpretation more probable. They are as
follows:
It was discovered by Schultze (’94) that if the egg of the Frog is
exactly inverted following the first cleavage, andheld in this position,
each blastomere will give rise to approximately a whole embryo, the
122 THE FROG: THROUGH GASTRULATION
two animals being united, however, in various degrees after the manner
of Siamese twins (Fig. 63). This interesting result was supplemented
by an experiment by Morgan (’95) in which he inverted the two cell
stage after the manner of Schultze, but in addition inyured one of the
blastomeres. Under these conditions the remaining blastomere instead
of developing into a half embryo as in the first experiment, formed a
virtually whole one, despite the presence of the injured hemisphere. The
latter, therefore, cannot be the cause of the half embryos. More detailed
observation of what takes place in the inverted cells, however, seems to
furnish a possible explanation of the results in all the above cases.
It has been noted by several observers that when the eggs are inverted the contents of the cell or cells becomes rearranged in response
to gravity. Thus the materials of the gray crescent can sometimes be
seen to become separated into two parts. At the same time the lighter
yolk free cytoplasm comes to what is now the top (the former vegetal
pole), and the heavier yolk sinks to the former animal pole. With such
profound changes going on there is every reason to believe that the
critical materials concerned with embryonic symmetry are also rearranged, and probably divided. If this is so it might be expected that
with their division two embryos would develop, as in fact they do. As
regards McClendon’s isolated, but uninverted blastomeres, it must of
course be supposed, according to this hypothesis that a similar reorientation takes place, though in these cases it must presumably occur either
as a result of the manipulation of the eggs, or on account of the change
in shape of the isolated cells. ’
CLEAVAGE, GASTRULATION, AND THE FORMATION OF
MESODERM, NOTOCHORD, AND MEDULLARY PLATE
It has already been suggested that in the Frog the character of the
processes indicated is transitional; it serves to bridge the gap between
the activities observed in the development of Amphioxus and those in
some of the forms which are to follow. Not only is this true, but the
character of the Frog’s egg as regards its yolk content is also transitional. The egg of Amphioxus was telolecithal, but the amount of yolk
was relatively slight. The egg of the Frog is telolecithal, but the
amount of yolk is much greater. Finally, as will be seen, this condition
is carried to its extreme in the Fish and Bird. As our study of these
forms proceeds it will become increasingly apparent that this parallel
ism between the character of early development and the yolk content is
CLEAVAGE . 123
not a coincidence. Rather, as intimated in the first chapter, the latter
very largely determines the former. The student then should keep this
clearly in mind in attempting to understand the stages which follow as
compared with corresponding stages in Amphioxus. V
CLEAVAGE
The Early Stages. ——In spite of the larger amount of yolk in the
Frog’s egg, segmentation is still holoblastic. Following the second
cleavage, however, it is less nearly equal than in Amphioxus (Fig. 61).
As has been stated the first division plane normally passes through the <
poles of the egg, and is thus perpendicular to the egg equator, and vertical if the egg is normally oriented. This means that it divides the ovum
into parts which are at least quantitatively similar. The particular meridian cut by the division is determined by factors noted above. The furrow which marks the beginning of this cleavage appears on the upper
surface of the ovum about two and one half hours after fertilization and
within an hour has extended around to the ventral pole. By the time it
has reached this pole, the internal substance of the egg is also divided.
A period of “ rest ” ensues, and then, about three quarters of an hour
after the appearance of the first divi.sion, the_furrows of the second become evident. This cleavage is also vertical and at right angles to the
first. The furrow in each of the two hemispheres again begins approximately at the animal pole, often exactly so. When the latter is the case
the upper ends of these furrows will evidently lie opposite each other
and form a continuous line across the pole (Fig. 61, D).
Following the completion of the second cleavage, the third soon
starts. It is horizontal, and in each of the four cells it lies about 60°
below the animal pole. Hence its furrows form a virtually continuous
line around the egg a little above the equator. This is the typical or at
least the ideal condition (Fig. 61, E). There-are, however, not infrequent variations.
The furrows of the fourth cleavage are in general vertical, and tend
ideally to meet one another at the poles. This tendency, however, is seldom perfectly realized, even in the animal hemisphere. Thus in the
latter half, the lines of division usually pass either to one side or the
other of the polar center, while in the vegetal hemisphere this and other
irregularities are even more marked. The ideal result, however, is sixteen cells, eight relatively small pigmented ones above, and eight larger
whitish ones below (Fig. 61, F).
The fifth cleavage, resulting in the formation of thirty-two cells, is
124 THE moo: THROUGH GASTRULATION
still more variable than the fourth. There is a tendency, however, for
the furrows to be horizontal, and to form four tiers of eight cells each.
In the most regular instances the cells of the two upper tiers are about
equal, and are all pigmented. The cells of the third tier are about mid
Fig. 64.—-Median vertical sections of four cleavage stages in the Frog’s egg. A.
An eight-cell stage. Note the small segmentation cavity or blastocoel. B. A later
stage (about 32 cells) which may be called an early blastula. C. A later blastula.
D. A still later blastula, showing marked increase in size of segmentation cavity.
way in size between those above and those below them. They are ap
proximately on the equator, and contain less pigment than the two upper
tiers. The lowest tier is formed of the largest cells, which are mostly
without pigment.
The Blastula. — By the time the thirty-two-cell stage is reached it
is hardly possible longer to refer to this dividing sphere as an egg. It
may now, therefore, be termed the blastula. Within this blastula is the
blastocoel or segmentation cavity, which arises as follows:
CLEAVAGE 125
From the first the cells into which the ovum has been divided are
pressed rather closely against one another so that their surfaces of contact are flattened. This, it will be recalled, is contrary to the rounded con
dition of the very early cleavage cells of Amphioxus. Even in the Frog,
however, the inner ends of the cells show some curvature, and by about
the eight to the sixteen cell stage these inner ends are sufficiently rounded
so that they are no longer in contact. Thus is produced the blastocoel,
which, because of the smaller size of the cells at the animal pole, is
somewhat above the equator of the blastula (Fig. 64). Also up to the
beginning of gastrulation the blastocoel is gradually increasing in size,
due partly perhaps to the closer packing of the cells, to the secretion of
albuminous fluid from them, and to the infiltration of water from without (Fig. 64, A, B). The latter two factors are probably the more important.
Besides this increase in size of the blastocoel, cleavage following the
thirty-two cell stage becomes quite irregular, and cells begin to be split
off internally. At the same time the relatively yolk-free cells of the animal hemisphere begin to divide _much faster than those of the vegetal
hemisphere, and some of the smaller ones tend to migrate toward the
equator, thus making the roof of the blastocoel thinner. Regarding the
matter of the cleavage rate in general, an interesting fact has been noted
by Ting, ’51. He found by crossing different species of Frogs, using
both normal and enucleated eggs, that the rate of division up to the time
of gastrulation is determined entirely by the egg cytoplasm, whose character was presumably previously determined by maternal genes.
Finally, at what may be termed the end of the blastula period, the
following conditions obtain: First the blastula is about one fifth larger
than the original egg, the increase in size being mainly due no doubt
to the absorption of water noted above. Secondly, the superficial pigment has everywhere extended downward somewhat, thus decreasing
the white area (Fig. 61, H). This extension having been approximately I
uniform, however, the latter region still reaches farther upward upon
the side where it was originally augmented by the addition of the gray
crescent. Thirdly, sections reveal the fact that on the side opposite to
that which was marked by the gray crescent, the wall of the blastocoel
is usually slightly thicker than it is elsewhere (Fig. 67, A). Lastly, it
may be noted that a split has occurred in the roof of the segmentation
cavity, so that this wall is composed of two sheets. The outer is the epi
dermal layer; the inner is called the nervous layer because parts of it '
help form the nervous system.
126 THE FROG: THROUGH GASTRULATION
   
Fig. 65. —Diagrams of the closure of the blastopore in
the egg of the common Frog (R. tenzportzria). From
Jenkinson (Vertebrate Embryology). In A—E the egg is
viewed from the vegetal pole, and in F, speaking in
terms of the future embryo, from its ventral side. The
dorsal lip is at the top of the figures. In D the ventral
lip has just been formed and the blastopore is circular.
.In E the rotation of the whole egg has begun, and in F
is complete.
GASTRULATION
External Processes.—Upon the side of the blastula where the
white area was increased by the addition of the region of the gray crescent, it has been noted that the pigment is still not quite so far down
as upon the side opposite. Nevertheless, even at the former point the
pigment extends markedly below the equator, the line between the light
GASTRULATION 127
and dark zones being everywhere marked by an area of intermediate
shading. It is then midway between the ends of the former crescent region, and toward the lighter and lower side of the shaded area in-this
region that the dorsal blastoporal lip first appears. It is thus probably
located at approximately the lower border of the original crescent,
though the exact relation is difiicult to determine because of changes
in pigmentation during cleavage. It is also somewhat below the level of
the floor of the hlastocoel. This lip has the appearance at first of a small
dent, which soon elongates into a groove following roughly the border
of the pigmented area (Fig. 61, I; Fig. 65, A, B; Figs. 67, B and 68, B).
As the process of elongation continues it is accompanied externally
by two phenomena. In the first place the groove gradually extends
around either side of the gastrula, and as it does so the pigment advances to its edge, i.e., to the lip of the blastopore. This lip thus comes
to constitute a sharp boundary between the dark and light areas (Fig.
65, A, B, C). In the second place the blastoporal lip everywhere moves
steadily nearer to the vegetal pole. This movement is greatest on the
side where the groove first appeared, i.e., at the dorsal lip, and becomes
progressively less toward either side. The first process, i.e., that of
lateral extension, causes the groove to become curved so that it has the
shape of a crescent, and eventually the horns of this crescent meet each
other so as to form a complete circle. A continuation of the second
process, i.e., the downgrowth of the lip, and hence also of the pigmented area, then results in a rapid diminution of the white region.
Thus the latter is soon in the form of a circular spot which is being
encroached upon from all directions (Fig. 65, D, E, F).
Epiboly.-——The white region evidently occupies the position of the
blastopore. The first appearance of the groove marks the beginning of
overgrowth by the dorsal blastoporal lip, while the lateral extensions of
this groove indicate the same process on the part of the lateral lips.
Finally, as already noted, the ends of the grooves meet one another on
the future postero—ventral side of the gastrula, and thus show that there
also a slight downgrowth is taking place. This overgrowth of the yolk, or
epiboly, by the cells of the blastocoel roof necessarily involves the use
of material which can only be supplied by a thinning of this roof due to
a rearrangement of its cells (Fig. 67). _
C0n11ergenc.e.——-In correlation with epiboly certain other processes
are also occurring, for an understanding of some of which more than
mere external observations are required. There is one other, however,
128 THE FROG: THROUGH GASTRULATION
which can also be studied from the outside. Such a study has proven
especially fruitful in the case of some of the tailed Amphibians, like
Triton, in which the’ egg is relatively colorless. In these animals it is
thus possible to put stains upon the outside of the blastula, and so to
observe what movements occur there during the ensuing gastrulation.
This was done by Vogt (’22, ’25, ’26) and Goerttler (’25) who placed
pieces of agar saturated with stains upon the egg membranes. The stains
penetrated the membranes and colored the cream tinted surface of the
late blastula. The results are depicted in Figure 70, A, B, C, D. From
these it appears that there is a streaming of the materials of the dorsal
and lateral surfaces of the ea-rly gastrula toward the blastopore. At the
same time, as is especially indicated by the later stages (C and D of
Fig. 70), there is a shifting of the lateral regions toward the midline. It is this combined type of novement which is now generally described as convergence, and though it has some aspects of the old
alleged concrescence it is obviously not the same thing. Thus it is evident that in this case, as in Amphioxus, the lips of the blastopore do not
actually constitute the sides of the embryo, or even furnish much of the
material for it. However, a good deal of this material does as usual pass
over the lips, and for this, and perhaps merely historical reasons, they
are sometimes referred to in this animal as the germ ring.
More recently Schectman (’-4-2), Holtfreter (’4-3) and others have
made further studies of the movements thus described in an effort to
arrive at a more basic understanding of them. Schectman particularly
stresses the idea that none of the regions undergoing the movements
heretofore indicated act entirely independently. Each has certain autonomous capacities, such as the extension or self-stretching" capacity of the
presumptive chordal region of the dorsal blastoporal lip. This region,
however, lacks “invagination” (involution) capacity which is conferred oh it by the normally adjacent lateral lips. The combined movements resulting in these regions Schectman therefore calls “correlative.” Holtfreter has sought especially to reach physico-chemical
explanations of the gastrulation phenomena. Thus he has suggested that
an unfolding of denatured protein molecules is partly responsible. This
unfolding, it is thought, causes a spreading of the superficial cells over
a substrate with appropriate adsorption properties. The epiboly and
perhaps the convergence are hence due to this spreading tendency,
which is apparently augmented by a lowering of surfme tension in
parts of the spreading cells. It will-be recalled that such a change in
surface tension was also referred to in the general discussion of gastruGASTRULATION V 129
lation as a possible cause of involution and invagination. On the basis
of these conclusions it is further suggested that all these cell movements
may be essentially similar to the cell movements seen in wound healing
and in phagocytosis. Additional study is of course needed either to disprove or to confirm and amplify these ideas.
Rotation. — Returning -to more obvious and directly observable matters, we are confronted with a very definite change in the position of the
whole gastrula which accompanies the processes just described. The
Fig. 66.-Diagrams of the Frog’s gastruls showing the position of the blastopore at various ages. From Kellicott
(Chordate Development). A. Posterior view. B. Lateral view.
I-5 indicate the successive positions and forms of the blastepore. The change in position is due both to the actual growth
movements of the blastopore. and to the rotation of the entire
gastrula.
movement of epiboly continues until the dorsal lip has passed over an
arc somewhat greater than 90°, and the area of white, i.e., the blastepore, is reduced to a small circle. This area, therefore, will be situated
rather beyond the original vegetal pole. It is now to be noted, however,
that accompanying this downgrowth of the dorsal lip another and quite
different movement has also been going on. The entire gastrula has been
rotating about a horizontal axislying at right angles to the original
median plane of the egg. That is the direction of rotation is such that
the dorsal lip is in a sense carried backward in one direction as fast or
faster than epiboly moves it forward in the other. The result is that at
the completion of both processes the blastopore, formed at approximately the vegetal pole, is posterior, and the morphologically dorsal
and ventral lips are actually dorsal and ventral (Fig. 66). From this
it also follows that the original animal pole of the egg is to form the
antero-ventral. side of the future embryo, while the region formerly
marked by the gray crescent is to form the dorsal side.
As regards the events so far described it is evident that gastrulation
mes. V.
Fig. 67.—Sagittal sections through Frog’s egg during formation and closure of
hlastopore. From Jenkinson t.Vertebrate Enzbryology). A—D. Before rotation. E
During rotation. F. After rotation. The arrow marks the egg-axis. its head the
animal pole. arch. Archenteron. d.l. Dorsal lip. mes.v. Mesoderm originating
at ventral lip (i.e., a very small part of that which is classed as peristomial t. mes.2.
Mesoderm originating from the yolk cells pushed into segmentation cavity (i.e.,
gastral). s.c. Segmentation cavity. 1;.l. Ventral lip. y.p. Yolk plw.
130
“ I9-C
gin’
Fig. 68._—— Semi-diagrannnatir store-o,I__rrams of a l1exui.<e-t-ted Frog hlastula, A, and
sttvcessive stages of hcmisected gastrulae, with small curving arrows indicating the
directions of L't‘ll movements. Stages in alphabetical order.
.e\rr«_:w.»' an outer uncut surface of the gastrulae, to the right in each figure, show
movement of material toward blastoporal lip. Involution of material over lip shown
by arrow on cut surface of lip margin. Invagination, of a sort, shown by arrows on
cut surface of yolk mass and floor of archenteron. Epibaly, evident from decrease in
size of yolk plug. Delamination, in this case gastrular cleavage, shown by extent
of splits bracketed under letters g.c. Ingression, being most questionable, not shown.
but would be designated by arrows pointing directly from vegetal pole to floor of
l)la$I0('0E’l in early stages. Animal pole marked by head of arrow outside each
figure. Rotation of entire gastrula shown by changes in the positions of the poles in
E and F.
131
132 THE FROG: THROUGH GASTRULATION
in the Frog is not essentially dissimilar to the same process in Amphioxus. The main differences are due to the presence of the large yolk
cells. Thus, to cite one instance, if these were absent the blastoporal lip
would bound an opening just as in the former case. Here, however, this
opening, i.e., the blastopore, is filled by these cells, which at this point
are therefore termed the yolk-plug. As will presently appear, the phenomenon of rotation and various internal peculiarities are also due to
the presence of so much inert nutrient material.
Internal Processes. -— While the above changes are apparent from
the outside of the gastrula, sections through it at various stages will reveal important accompanying developments within. They are as follows:
Invagination. —- As the external processes of gastrulation begin,
meridional sections of the blastula (or early gastrula) bisecting the
future dorsal blastoporal lip reveal the fact that the floor of the blastocoel is beginning to move upward. Usually this movement begins on the
dorsal side nearest the dorsal lip, and spreads part way around the
margins of the blastocoel in company with the external extension of
the lateral lips (Figs. 67, B; 68, B). Sometimes, however, the up-pushing is more central, and thus causes the blastocoel to become crescent
shaped. In either case the movement is essentially one of invagination, albeit an invagination which is considerably hindered and modified by the mass of material to be moved. This mass of course is the
yolk which occupied the vegetal half of the egg, and now occupies the
relatively large and numerous vegetal cells. This modified invagina~
tion continues until the blastocoel cavity has been virtually eliminated,
except for the narrow slit separating the outer layer of cells, now epi
blast from the inner yolk-filled cells, now /zypoblast (Fig. 67; Fig. 68,
C, D, E, F ) .2
2 It seems pertinent to mention at this point an observation made upon one of
the tailed Amphibians by Schectman (’34l. This investigator stained the vegetal
pole of a fertilized Triturus egg and found that by the midblastula stage the stain
occupied cells some distance from the surface, and near to the floor of the blastocoel. He did not follow the material in later stages, and refers to its inward movement as “unipolar ingression.” This he properly enough indicates as occurring
during “ blastulation ” (cleavage), and does not suggest that it has anything to do
with gastrulation. However, he does note that it seems to be involved in the upward
movement of the blastocoel floor, in this case at its middle, and this movement, it
may be recalled, is one which we have designated as a part of modified imagination. Whcther, therefore, this movement in Triturus is really to be regarded as a
kind of premature and greatly modified invagination, and hence a precocious aspect
ofgastrulation, is a question for further study. At least it is a possibility to be borne
in mind. Finally it may be added that the pfocess in question acquires additional
GASTRULATION . 133
As has been suggested this internal process is going on simultaneously with the externally observable process of epiboly. As a result
of both a new cavity is being formed which replaces the blastocoel. It
is the archenteron, and is lined by hypoblast, a relatively thin layer
forming the roof and the main mass of yolk-filled cells constituting the
floor. ' ,
Involution.—~It now remains to point out that in addition to the
processes so far described there is also a distinct process of involution.
This is most active at the median dorsal lip and progressively less so
as one passes around either side, until at the ventral lip there is almost
none at all. The immediate cause of this movement, as well as of such
invagination as occurs, is apparently a change in shape of the cells adjacent to the lips and in the yolk plug.
From this account, the roof and sides of the archenteric interior consist of material originally outside, dorsal and lateral to the blastoporal
lip, while the floor is composed of cells originally on the outside of
the vegetal region. The latter seem to have moved into their definitive position by an inpushing and inturning of the yolk cells called
modified invagination (Fig. 68) . Any inwandering of individual vegetal
cells (ingression) , as implied by Sc-hectman and others (see footnote) is
denied by Ballard, ’55, who says that only the stain moves in, no cells.
Delamination.—In the general account of gastrulation in Chapter
II, it will be recalled that the origin of endoderm by the process of
splitting off was said to occur to a slight extent among the Amphibia.
It should here be stated, however, that its occurrence is not universally
admitted. Those who do describe it (Brachet, for instance) say it takes
place in the following manner: _
Reference to the figures will indicate that, as the process of invagination begins, one of the results is as follows: As the yolk cells (hypoblast) about the margins of the blastocoel are pushed upward, they tend,
as previously noted, to obliterate the portions of this cavity between
themselves and the epiblast. The obliteration, however, is not quite complete, so that between the uprising hypoblast and the epiblast there
remains a slight crevice. The upward extent of this crevice is then obviously increased by the continuance of the above processes. By those
who maintain the existence of delamination, however, it is held that
interest in the light of Peter’s observations on the inwandering of cells in the gastrulation of the Chick (see gastrulation in the Chick). In that case, however, the
movement is into the blastocoel from a layer over it instead of from the yolk be
neath it. Perhaps, however, in, view of the changed relationships in the Bird, due
to excess yolk, this difference is not significant.
134 THE FROG: THROUGH GASTRULATION
besides this upward extension there is also a well marked downward
extension. i.e., in the direction of the blastoporal lips. This appears to
occur first, but least extensively, in the margin of the blastocoel nearest
the dorsal lip, whence it presently extends entirely around the circumference and becomes most extensive toward the ventral lip. Here it apparently serves throughout a considerable region to separate the yolkfilled cells from the epiblast on the definitive ventral side of the gastrula. The significant point, however, is the fact that wherever the process takes place it is due apparently to a splitting apart or delamination
of the cells at the bottom of the crevice (Fig. 68, go). But since at all
points this crevice serves to separate epiblast from hypoblast, its downward extension in the manner indicated is obviously setting apart these
layers by delamination. In this particular situation this separation has
also been given the name of gastrular cleavage.
Summary of the Processes. —— To sum up the processes involved in
the gastrulation of the Frog, it is found that there are four of them
which also occurred in Amphioxus, i.e., epiboly, involution, invagination and convergence or confluence. In addition there seems to be some
delamination which appears here for the first time. Though a common
method for setting aside mesoderm and notochord, it is not so commonly
thought of in connection with gastrulation. As we shall see, however, it
is perhaps the only methodin Mammals, and possibly also in Birds.
In connection with these gastrulation processes it may finally be
noted that there has been a considerable shifting of the yolk mass, and
hence of the center of gravity. It is to these shiftings, apparently, that
the rotation of the gastrula is due.
MESODERM, NOTOCHORD AND NEURAL PLATE
The Mesoderm and the Notochord. —— As the archenteron develops the layer which is invaginated, involuted, or delaminated to form
its roof has been referred to as hypoblast. It now appears that this
hypoblast contains the elements of a part of the endoderm, and all of
the mesoderm, including the notochord. The ‘setting aside of these layers
occurs as the result of a delamination from the hypoblast. The lower
layer of cells thus split off forms the endoderm of the archenteric roof
and sides. It is of course continuous ventrally with the yolk cells which
l3€t;.0!1‘I.C the endoderm of the floor. The upper layer resulting from this
split hes between the newly formed endoderm of the roof and sides and
the epiblast. This in between layerlis mesoderm, while the overlying
epiblast may now be called ectoderm.
MESODERM,_ NOTOCHORD, NEURAL PLATE 135
It should here be noted that the splitting off of the mesoderm does
not occur everywhere simultaneously, but begins on either side and proceeds toward the median line. Here for a time a narrow strip of cells
remains connected with the underlying layer. Presently it is separated
both from the endoderm beneath and from the mesoderm on either side.
It is the notochord (Fig.
69). The mesoderm of the
ventral part of the embryo
is formed later mainly by
a downgrowth of the lateral sheets between the endodermal yolk mass and
the ectoderm. Anteriorly
it occurs not as a definite layer, but rather as
loosely arranged cells, a
‘type of mesoderm generally referred to as mesenchyme.
Presently by the above
means the mesoderm
comes to exist throughout
the greater part of the
embryo, as a separate
layer between ectoderm
and endoderm. As noted,
it is interrupted dorsally Fig. 69.-—Three stages in the differentiation
~ of the roof of the archenteron in the Frog.
by fife notochord’ whlle From Jenkinson (Vertebrate Embryology).
anterlorly the cells are arch. Archenteron. n.ch. Notochord. mes. Dor
very loosely arranged. 5&1 Mewderm‘
Lastly in the region of the blastopore there persists for a time an undifferentiated mass of cells containing the elements of all three layers.
These gradually become defined, as the blastopore closes.
The Medullary or Neural Plate and Related Structures.—— It
has already been noted that at the end of segmentation the epiblast of the
animal hemisphere was split into an outer layer and an inner nervous
layer. During gastrulation this becomes true also in the vegetal hemisphere. Thus toward the latter part of that process, a  35?»; of
ectoderm exists everywhere except in the immediate,vi&iii;ity"of"tl1di§l‘astoporal lips. Throughout certain regions of the  'la the ner
( ;-t\r-h§‘=b’‘di }
K J
it ’ \-,_ _‘;/I
-.  "~..._......e'
’w._\5:£:h “§
136 THE FROG: THROUGH GASTRULATION
ectodermal layer then begins to thicken, the thickening being defined’
as the medullary or neural plate. This plate extends forward from the
dorsal blastoporal lips as a median band, widening rapidly as it approaches the anterior end of the gastrula. Here it terminates, the extremity having the form of a broad curve (Fig. 77, A).
The thickening process which has given rise to the plate presently
grows most marked around its margins, and these become slightly
elevated. The elevations which thus occur along the sides of the plate
are the beginnings of the lateral neural ridges or folds, while around
the anterior end they are continuous with one another as the transverse
neural ridge or fold (Fig. 77, B _). Accompanying or immediately following the thickening of the nervous ectoderm which produces the
ridges, there is a corresponding thinning of this layer along the midline of the plate. As a result there soon appears here a shallow depression. It is sometimes scarcely evident externally at this stage, but as
soon as it becomes so, it is termed the neural groove.
EXPERIMENTAL RESULTS
Some of the most significant work in modern experimental embryology has been done upon the early stages of Amphibian development.
There have been two main lines of investigation. One has interested itself in the movements and fate of materials during gastrulation, while
the other has sought information concerning the effect of these materials upon one another. Though the aims of these studies have thus been
somewhat different, the results, as will presently appear, have largely
tended to supplement each other.
Location and Movement of Materials During Gastrulation. —
One important method for discovering the movements and fate of materials during this process has been to stain the surface of very early
gastrulae with vital stains at certain significant points, and then observe the shifts in these stains in later development. This is possible in
some of the Urodeles, such as Triton, which possess unpigmented eggs,
and has been done by Vogt, Goerttler, and others, with the external results shown in Fig. 70. Other experiments, noted presently, help prove
the reality of the involution of part of this material, as already described, to form the hypoblast of the roof and sides of the archenteron.
On the basis of these results Vogt and Goerttler constructed more or less
idealized maps showing their views as to the location of this hypoblast
(potential endoderm, mesoderm and notochord) previous to gastrulation. Their conclusions are shown in Figure 71. l
3
EXPERIMENTAL RESULTS
137
More recently the matter has been reinvestigated by Pasteels C42)
in another Urodele, Axolotl. and in an Anuran, the primitive Frog,
Discoglossus, the results being indicated in Figure 72. It will be noted
that aside from differences between the older and newer maps of the
Urodeles there are
also some differences between those
of the Urodeles and
the Anurans. On
the whole, however,
these are matters of
detail, the fundamental patterns being similar in all of
them.
Aside from these
minor differences
show. in the pregastrula maps, there
is one alleged postgastrula difference
between the Urodeles and at least
most Anura which
the maps partly sug
gest but do not
really show, and
which is perhaps
worth mentioning.
It has to do with the
Fig. 70. ~— Four stages in the development of :1 Triton
egg which had been marked with dyes in the early
gastrula stage. The changes in shape and position of
the colored areas indicate the movements of the materials of the egg during gastrnlation and the formation
of the medullary folds. After Goerttler.
A. The early gastrula from the postero-dorsal side.
B. A slightly later stage from the same View point. C.
A much later stage viewed from the posterior. The
neural folds are in evidence, but the blastopore does
not show. D. About the same stage as C viewed from
the dorsal side.
actual setting aside of notochord and somitic and lateral-plate mesoderm from endoderm, and is as follows: We have already noted that in
the common Frog, Rana, the materials for the notochord, somites, dorso-,
ateral mesoderm and endoderm are involuted as a single sheet of hypoblast. This hypohlast is then later separated by delamination into notochordal, somitic and lateral-plate mesodermal material above, and the
endoderm of the archenteric roof beneath. In the Urodeles, however, this
is not true. The involuted hypoblastic roof of the archenteron turns out
to be composed exclusively of the definitive notochord and somites with
. perhaps even a little of the dorso~lateral mesoderm. This roof thus lacks
138 THE FROG: THROUGH GASTRULATION
temporarily any endoderm; the latter being presently supplied, not by
delamination, but by the upgrowth of endoderm lying lower down on
either side.
In concluding this topic there is this further point to note: The external area indicated by these maps as giving rise to the notochord and
at least parts of the mesoderm and endoderm is also approximately the
area of the gray crescent in those cases where there is one.
The Region of the Gray Crescent as the Center of Organization. ——Turning now to the problem of how the materials affect one
Dorsal
 
   
 
.1: ‘
   
Mesoblastic M Ventral Rim
somites Dom,
T ‘I Rim horda
3' 1 I esoblastic
mesoderm mlgoedrgrm somites
' Tail mesoderm Dorsal lip
Ventral
Fig. 71.~—Diagrams of a Triton egg previous to gastrulation, showing the supposed location of the materials which, with the exception of the neural plate, are
destined to be involuted to form various structures as indicated. A. View from the
vegetal pole. B. Side view. After Vogt.
Rim. The region which eventually becomes the lip of the blastopore at the end of
gastrulation.
another a long series of experiments might be cited. Only enough will
be mentioned, however, to indicate what the trend has been, and the
important conclusions which have at present been reached.
As has already been made clear, though the first cleavage in the Frog
tends to bisect the dorsal lip of the blastopore, it does not always do so.
In some cases indeed it may come as far as possible from this, and lie
parallel to this lip. Bracket (’05, ’06) took advantage of this fact to
find out what would happen when one of the blastomeres of such an
egg was killed, as had previously been done with the blastomeres of
more normal cleavages. In the latter case it will he recalled one side of
an embryo developed, unless the egg had been so treated as to rearrange
materials related to the gray crescent. In the latter event a whole, or
nearly a whole, embryo was formed. Now in Brachet’s eggs it is clear
that the crescent will be in only one of the two hemispheres, i.e., the
one containing the dorsal blastoporal lip. It is perhaps not surprising
therefore that when one blastomere of such an egg was killed, the reEXPERIMENTAL RESULTS 139
maining one would only develop when it was the one which contained
the crescent. These, moreover, formed better than half of the anterior
and dorsal part of an embryo. Thus once again the importance of mate
rials connected with the gray crescent region was demonstrated (Fiv.
73).
C V- P- DISCOGLOSSUS V- P- D
Fig. 72.~—Maps of young gastrulas of (A and B) Axolotl, a Uroclele, and (C and D) Discoglossus, an Anuran,
showing the location of materials destined for various
structures. After Pasteels. The figures to the left (A and
C) show ‘the gastrulas from the left side, while the figures
todthe right (B and D) show them from the future dorsal
si e.
D. Dorsal. V. Ventral. Lat. Lateral. bl. Blastopore. a.p.
Animal pole. L‘.P. Vegetal pole. Stippled areas, notochord.
Vertically-hatched areas, neural ectoderm. Diagonallycrossed hatched areas, mesoderm. Clear areas toward bottom of page from the mesoderm are endoderm. They contain bars representing material for the future gill slits.
The next step was taken by Spemann and Mangold (’24) . These men
took a small piece of material just anterior to the dorsal lip of a Triton
early gastrula and grafted it upon the surface of another gastrula.
Wherever it was placed, this material was soon covered over by surrounding cells, and the cells which covered it presently formed a medullary plate. Later this plate would give rise to a neural tube, or part of
one, as shown in Figures 74, 75. The same experiment was eventually
done with the Frog. Also Bautzmann (’26) -performed more detailed experiments to see how far from the blastoporal lip of an early gastrula
140 THE FROG:.THROUGH GASTRULATION
t_he material possessed this power to cause other ectoderm to become
neural plate. She found the region extended about 85 degrees anterior to
the middle of the lip, and about 80 degrees to either side, the anterior
extent decreasing as one proceeds laterally. The effective area thus had
the form of a crescent occupying a similar but somewhat wider zone
than that occupied by the gray crescent when the latter exists.
Now normally of course the material transplanted
in these experiments reaches a position beneath the
ectoderm by being involuted over the lip of the
blastopore. Hence involuted material (hypoblast)
taken from archenteric roof of a late gastrula should
also be expected to stimulate neural plate formation
in any ectoderm under which it occurs. Marx (’25)
and Geinitz (’25) tested this assumption by transplanting such involuted hypoblast beneath other
Fig. 73.———A Frog
embryo produced _
by injuring one Of ectoderm than that which normally produces neural
gllfirirstigwoabliigz plate. The assumption proved correct (Fig. 76) . In
where Hie first deed this fact is one of the proofs that involution
cleavage pane was
parallel to the gray occurs‘
grescent instiad of Though the action of potential chorda mesoderm
' g at ' I an- . . .
gig: to sag as is In mducmg neural tube formation has thus been
usual. The blasto- .proven, another question still remains. Is all the
mere injured was d f bl 1 I C t 1 H
the one which did ecto erm o a astu a or ear y gas ru a rea y ennot contain the tirely equivalent in its potentialities? Though
crescent, since oth- h d d -11- d 6 It 1) f temise no develop c or ameso erm W1 1n uce n ura u e orma ion
me}1t_ occurs. The in'any ectoderm is it not possible that some ectoéuélyélfziiledcelligfg derm, namely that of the normal neural plate resomewhat more gion, might form neural tube without any chorda
than half of the an« d t? A“ t t h.
M301, portion of an meso erm presen . emp s 0 answer t IS quesembryo. After Bra~ tion have been made by several workers, notably
Chet‘ Spemann (’I8, ’21) . This worker transplanted small
pieces of ectoderm from the prospective neural plate region of a young
gastrula to a different region in another gastrula. He also performed the
converse experiment of placing ordinary ectoderm in the position of part
of the prospective neural plate. In some of the cases, moreover, he made
the interchange between different species of Triton having ectoderm of
distinctly diflerent shades. Thus it was possible to follow accurately the
fate of the transplants in their new environments. The results in all cases
showed that at this stage of development the fate of the ectoderm has not
yet been determined. The prospective neural plate material when placed
EXPERIMENTAL RESULTS 141
elsewhere did not form neural plate, but ectoderm like that surrounding
it in its new location, while the latter when implanted in the midst of the
future neural plate became a normal part of the plate and future neural
tube. Later Work by Marx (’25), it is true, showed that just before the
neural plate appears the ectoderm has become determined, but previous
to that time the results are as indicated. These data
therefore would seem to prove that in very early
gastrulae the ectoderm of the prospective neural
plate region has not yet come under the influence
of the chorda mesoderm, and that under these circumstances it has the same, or nearly the same, potentialities as in any other location (see below).
The Principal of Induction.-—-The action of
a substance in thus causing cells to respond by forming some specific tissue or structure is known as induction or evocation. The tissue which responds, on
the other hand, is said to have a certain competence.
Although such a relationship has received its greatest emphasis in connection with the material in the
vicinity of the dorsal lip of the Amphibian blastepore, this particular instance is by no means unique.
Fig. 74.—An embryo of Triton on
whose left side an
extra neural tube
_has been induced.
‘This was done by
implanting in the
side of this embryo
at the gastrula
It occurs in many organisms, and in connection
with all sorts of tissues and stages of development,
some of the more striking examples of which will
be pointed out as we come to them. Because of the
stage a piece of external material from
the blastoporal lip
of another gastrula.
After Spemann and
Mangold.
early discovery and far reaching consequences of
the inducing material in the vicinity of the Amphibian blastoporal lip,
however, it was especially designated as the ‘organizer.
It must now further be added that the induction and response relationship in general is not always such a completely open and shut one
as so far indicated. Some tissues have different degrees of inducing
capacities, while the competence of other tissues to respond in a specific
way varies considerably as one proceeds away from the site where a
particular response normally occurs. Thus even in the original case of
neural plate induction, it now appears possible that, contrary to some
of the earlier results indicated, not all ectoderm is quite alike in its
ability to respond. Some areas of ectoderm form neural plate and tube
more easily than others, especially if properly oriented (Barth, ’4-1).
It should also be stated that when a tissue has once begun to respond in
a certain direction, it loses its competence to respond in any other.
142 THE FROG: THROUGH GASTRULATION
The Nature of the Inducing‘ Substance.-—It now remains to
add’ a word regarding more recent attempts to analyze the nature of inducing substances, particularly the original one designated as the organizer. The first steps in this direction involved eiiorts at discovering
how specific the inducing substance was, i.e., would anything other
than material related to the gray crescent region induce neural tube?
 
pr. neur.
Fig. 75.-—A cross section of the same embryo shown in Fig. 74, at a later stage,
showing the two neural tubes.~After Spemann and Marigold.
I. sec. ear. Left secondary ear vesicle. pc. Pericardial cavity. pr. neur. Primary
neural tube. sec. neur. Secondary or induced neural tube which because of the
orientation of the section appears on the right instead of the left side.
The answer was rather startling. It was found that a very wide variety
of materials would work, e.g., pieces of adult liver and kidney as well
as certain Invertebrate tissues like. ganglia of Lepidoptera. It has further been discovered that a tissue which normally lacks inductive capacity, such as neural plate, may acquire it by being in Contact with
one which normally possesses it, such as chorda-mesoderm. Indeed it is
now known that neural tube, having itself been induced, is then capable
for a time of inducing tube formation in undetermined ectoderm. It was
also shown that tissues need not be alive or recently killed. Tissues
would work even after being fixed and imbedded in paraffin as for sectioning. Not only this but in some instances material such as pieces of
blastula which normally have no inducing capacity will act as inductors after they have been boiled! Thus it is clear that the substance
EXPERIMENTAL RESULTS 143
concerned is non-living, and is fairly widespread. From this point it
would seem that with modern analytical methods it should not be too
difiicult to trace down the essential chemical involved. Such, however,
has proved far from the case. Many workers have attacked the problem, among the most prominent being Spemann in Europe, Needham
and Waddington in England and Holtfreter and Barth in the United
States. Spemann believed that glycogen might be the substance, but
Needham thinks that one of the sterols is responsible. Barth and Grail
Fig. 76.——A. Diagram of Bombinator (a Toad).
The small circle indicates the’ blastopore, and the
shaded square represents the region from beneath
which a piece of the archenteric roof was taken, and
transplanted to the blastocoel of a gastrula of Triton.
B. An older stage of the Triton to which the transplant from (A) was made. After Geinitz. M. The regular primary neural tube. In. The partial secondary
tube induced by the transplant.
(’38) , on the other hand, doubt the possibility of determining with certainty just what the normally acting material may be. The difficulty is
that various chemicals and treatments, some of which are probably
actually toxic, nevertheless have an inductive effect. It seems unlikely
that so many different substances are concerned under natural conditions, and it is certainly unlikely that any of them are toxic. It has
been said that these chemicals are not the inductors, but release the latter from the live tissue. Also it is possible that the process may consist
of the removal of a blocking substance which has inhibited various
developmental possibilities inherent in the cells acted upon. Finally, the '
reason for different reactions by like material, e.g., the formation from
the neural plate of brain in one place a_nd neural tube in another, may
be due either to a quantitative or qualitative difference in the inductor
produced by different regions of the archenteric roof (Barth, ’53) .
Significance of Developmental Concepts.— In concluding this
general topic it is well to emphasize first the very great importance of the
144 THE FROG: THROUGH GASTRULATION
fundamental concept of induction. As this concept becomes increasingly
established and elaborated we can see, at least theoretically, how a
complex structure like an embryo may develop from a specific physicochemical system like an egg. Thus, when the equilibrium of this system
is disturbed by fertilization or otherwise, an orderly chain of reactions is started, each one inducing others. Obviously this does not completely explain development. Yet it does reveal a significant aspect of
it which will be repeatedly demonstrated as we proceed.
Recently Townes and Holtfreter, ’55, have discovered something which
may help to establish another concept. By mixing ectoderm, mesoderm,
and endoderm cells from neuralae-gastrulae they have shown that these
cells possess certain “ directive movements and selective adhesiveness ”
characteristic of each cell type, causing some to move inward, while
others spread peripherally, arranging themselves in normal tissue patterns.
A COMPARISON OF GASTRULATION, MESODERM
AND MEDULLARY PLATE FORMATION IN
AMPHIOXUS AND THE FROG
A comparison of gastrulation, mesoderm and notochord formation,
and the development of the medullary plate in Amphioxus and the Frog
may now be presented in tabular form, as follows:
Gastrulation
AMPHIOXUS Fnoc
The processes involved are: in- The processes involved are:
vagination, involution, epiboly, modified invagination, involution,
and convergence.
epiboly, some convergence, and
clelamination.
Mesoderm Formation
1. Gastrulation is ‘virtually completed before definite setting aside
of mesoderm begins.
2. The potential mesodermal
material is identifiable in the fertilized egg. It can be traced into
the ventro-lateral blastoporal lip
of the early gastrula, whence it is
carried into its definitive position
1. Gastrulation is completed before mesoderm is set aside.
2. The potential mesodermal
material is not visually distin«
guishable until after gastrulation,
but evidence shows that it exists
lateral to the lips of the blastopore.
Thence it is brought into its definiCOMPARISON OF AMPHIOXUS AND FROG 145
AMPHIOXUS
by a kind of combined involution,
epiboly, and convergence.
3. The setting aside of the mesoderm in the form of somites occurs
by a process closely akin to enterocoelic evagination, especially in
the more anterior region.
Fxoc
tive position by processes of involution, epiboly, and convergence.
3. The dorsal and lateral mesoderm is set apart as such by delamination. Ventrally, however, it
arises to a considerable extent by
the proliferation of cells from that
already formed.
The N otoc/Lord
The potential notochordal material occurs at the dorsal lip of the
blastopore. Thence it is involuted
to the archenteric roof from which
it is set aside by evagination.
The potential notochordal material lies anterior to the dorsal lip
of the blastopore. Thence it is involuted to the archenteric roof.
From this roof and from the mesoderm on either side it is then separated by delamination.
The Medullary Plate and Folds
1. There is no split between
outer and nervous ectoderm. Dorsally a median strip of ectoderm
becomes slightly depressed to constitute the medullary plate. The
edges of the ectoderm on each side
of this plate presently become separated from the margins of the latter, and then grow together above
it. The overgrowing layers so
formed thus constitute only the
outer half of a true medullary
fold. Later, the margins of the
plate itself also bend toward one
another until they meet and fuse
beneath the overgrown ectoderm.
2. In Amphioxus no attempt has
been made to demonstrate induc
1. An inner or nervous layer of
ectoderm is formed by delamination over the entire gastrula. The
medullary plate arises by a thick
. ening of this layer in the mid
dorsal region. As will appear below, the margins of this plate then
come to constitute the crests of
true neural folds. This follows
from the fact that in this case the
sides of the plate are carried upward and together, not later than,
but in company with the ectoderm
around their edges. Thus no sepa-A
ration occurs between the ectoderm of the plate and that surrounding it until’ the crests of the
folds meet. _
2. In the Frog experimental
procedure has demonstrated that
146 THE FROG: THROUGH GASTRULATION
AMPHIOXUS Faoc
tive action. However, it very prob- the ectoderm is stimulated to form
ably occurs here as in the Amphib- neural plate and tube by the induc
ians and other forms. tive action of the underlying
chordo-mesoderm.
In concluding this comparison it is well once more to emphasize the
fact that the above differences, at least those of gastrulation and mesoderm formation, are chiefly due to differences in relative amount of
yolk. It may also be repeated that a further increase in this substance
in the Fish and Bird is apparently responsible for the still greater modifications of the above processes in those animals.
HE FROG: EARLY OR EMBRYONIC DEVELOPMENT
SUBSEQUENT TO GASTRULATION
T H E general condition of the embryo at the conclusion of gastrulation has already been indicated, and there was also noted the origin
of the notochord, the mesoderm, the medullary plate and neural folds.
Following this there occurs a period characterized by the beginning of
elongation and also by the appearance of the rudiments of the main
systems and organs. Thus at the end of the time in question, during
which the animal has reached a length of from 2:5 to 3 mm., virtually
all these rudiments are present. For this reason it will be convenient to
carry forward the description of both external and internal development to about this point. We shall then be prepared to describe more
clearly the remaining changes which lead to the formation of the adult.
In carrying out this plan it will not be possible to state with any
accuracy the age at which a particular size and degree of development
is reached, even in the same species of Frog. This is necessarily so on
account of the variableness of temperature to which the eggs are subjected. It will nevertheless be helpful occasionally to mention the average age of embryos of a given condition. The student must clearly bear
in mind, however, that this is never more than approximate. It is desirable to begin by considering the development of this early period in
its external aspects.
EXTERNAL CHANGES
As the embryo begins to elongate certain rather conspicuous features
arise as elevations or depressions of the surface. All of these structures
are at first more or less connected with the medullary plate, and all of
them appear at about the same time. It will be necessary, however, to
describe them separately.
External Development of the Neural Tube. —— The neural
groove whose beginning has been noted, now becomes much deeper and
more prominent (Fig. 77, C) . At the same time the lateral neural ridges
or folds begin to increase their elevation and to bend toward one an148 THE FROG: THE EARLY EMBRYO
Sp.
Inf.
Fig. 77.~—Drawings of preserved Frog embryos (Rana pipiens) showing successive stages in the development of the neural tube, the sense plate and the gill
plates. A. Antero-dorsal view of a stage shortly after the completion of gastrulatiou,
showing the neural or medullary plate. B. Same \-'l(‘W of the next stage, showing
the beginnings of the neural folds and the sense plate. C. Same view of somewhat
later stage, showing the beginnings of the gill plates. D. Antero-lateral view of same
specimen. E. Antero-dorsal view of still later stage, showing neural folds about to
fuse.’ The sense plate and gill plates are clearly marked. F. Lateral view of same
specimen.
gp. Gill plate. Inf. Lateral neural, or medullary folds. ng. Neural groove. np.
l_‘lt]a§ral, or medullary plate. sp. Sense plate. tn]. Transverse neural or medullary
o .
EXTERNAL CHANGES ,. i 149
other until eventually their crests meettand fuse; thus is formed the
neural tube. Further, as noted above, the neural plate in this case,
as in that of all true Vertebrates, is involved in the process from the
first. Hence no break occurs along the crests of the folds between their
outer and inner layers until after these crests have met (Fig. 80) 1 The
phenomenon thus indicated starts somewhat anterior to the middle of
the embryo in about the region of the future medulla, and from here
the fusion proceeds in both directions. Anteriorly, this lateral closure
is further augmented by the back growth of the transverse neural fold.
Nevertheless, as will be noted presently, the completion of the process
occurs later in the anterior region because of the greater space which
separates the folds in this vicinity. The tube which is thus formed soon
appears as a prominent ridge along the back.
The Sense Plate and the C-ill PIate.—— During the above process
there are also developed certain other structures as follows: Just as the
medullary ridges are preparing to fold in, a slight and rather narrow
elevation grows outward from the antero-lateral region of each of them,
and begins to extend in an antero-ventral direction. This continuesuntil
the two elevations meet one another on the front of the embryo some
distance below the anterior edge of the transverse neural fold (Fig. 77,
B). There is thus formed a relatively narrow band of slightly elevated
tissue which traverses the lower anterior region of the embryo in a
bro-ucl curve and then ascends on either side until it merges with the
edges of the neural folds. It is termed the sense plate. For a time the
median area between the inner edge of this semicircular band-like plate
and the edge of the transverse neural fold above it remains relatively
depressed; i.e., of no greater elevation than theregion outside the plate.
Presently, however, the distinction between this median area and the
plate which constitutes its ventral and lateral boundary gradually
lessens, the central region becoming almost as much elevated as its border. In this manner the sense plate comes to constitute a broad, some-.
what shield-shaped region extending across the front of the embryo
from side to side, while dorsally it is more or less continuous with the
anterior of the neural tube (Fig. 77, E, F).
During the course of these processes anotherevent is taking place
immediately posterior to those portions of the sense plate where it joins .
the neural folds upon either side. In each of these two regions there is
1 It is to be noted that these literal crests of the folds are not quite identical
with the “neural crests” referred to below in Fig. 80, the distinction becoming
clear as the tube is about to be completed.
150 THE FROG: THE EARLY EMBRYO
4b.cl. ’ 4b.et. g.p.
       
   
OS.
4 br. cl. 2 br. cl.
st. i.
Fig. 78.—-Drawings of preserved Frog embryos (Rana pipiens) from 2-2 to 2-5
mm. in length, showing particularly the changes in the sense and gill plates. A.
Right side of a 2.2 mm. embryo. The outpushing of the optic vesicle is just beginning to appear on the dorsal part of the sense plate. The latter is becoming more
clearly separated from the gill plate by the rudiment of the hyomandibular cleft,
while the posterior boundary of the gill plate, i.e., the rudiment of the fourth branchial cleft, is also becoming more evident. B. Right side of a slightly older embryo
than A. The invagination of the left oral “ sucker ” (mucous gland) is visible near
the ventral end of the sense plate. C. The same embryo viewed directly from the
anterior end. The stomadaeal invagination and the two parts of the developing mucous gland are clearly shown. D. A 2.5 mm. embryo from the right side. The rudiments of the first and second branchial clefts have appeared upon the gill plate.
Also, just posterior to the dorsal part of the gill plate the outpushing due to the
pronephros is visible, and the external indications of some of the myotomes are
beginning to appear.
Ibr. cl. 2br. cl. 4br. cl. Rudiments of the first, second, and fourth branchial (gill)
clefts. The arch anterior to each cleft is named in the text. gp. Gill plate. }zy.c[.
Rudiment of hyomandibular cleft. my. External indication of one of the myotomes.
op. External indication of the outpushing optic vesicle in the upper region of the
sense plate. as. Rudiment of oral “ sucker ” or mucous gland in the lower region of
the sense plate. prn. External indication of the pronephros. 511. The sense plate,
whose lower portion really represents the mandibular arch. sz.i. The stomodaeal invagmatton.
EXTERNAL CHANGES 151
developing another elevation which extends outward from the neural
folds approximately parallel with the posterior border of the sense
plate. Indeed, each of the new elevations is said by some authors to be
merely a part of the original plate separated from it‘ liy the development of a depression. In any event the new raised areas, because of
their future development, are termed gill plates (Fig. 77, C, D, E, F).
As the anterior portions of the neural ridges meet one another, a
slight protuberance arises upon either side of the dorsal region of the
sense plate (Fig. 78, A). These protuberances mark the outpushings of
the two optic vesicles (see below). Also at about this time there begins
to develop in the middle of the sense plate a rather wide vertical groove
extending from near its ventral margin dorsally to about the level of
the lower edges of the optic protuberances (Fig. 78, C). This is the
stomodaeal invagination, the stomodaeum proper, forming later at its
dorsal end. It is evident that the development of this groove results in
a division of the sense plate throughout the greater part of its length,
so that the raised portions exist only upon either side of the median
line. It may now be added that each of these raised areas constitutes
the rudiment of one side of the future lower aw or mandible, and hence
each such area is designated at this time as a mandibular arch. Lastly,
at the ventral end of each of these arches there now develops a small,
somewhat elongated, and slightly pigmented depression. These depressions then deepen, while their postero-ventral ends grow toward one
another and fuse, thus forming the characteristic V shaped “ sucker ”
or mucous gland of the early larva.
It has been noted that the sense plate (now represented by the man’dibular arches) is separated from each gill plate by a slight furrow; it
remains to be added that a similar indentation also bounds each of the
latter plates posteriorly (Fig. 78). Upon either side the more anterior
of these furrows, i.e., the-one between the mandibular arch and gill
plate, marks the location of the hyomandibular “ cleft” (in this case
‘never an actual cleft), while the posterior one indicates the approxi
mate position of the future fourth bronchial (gill) cleft. There next
appear upon the surface of each gill plate itself two more vertically
elongated depressions denoting the beginnings of the first and second
branchial clefts, the rudiment of the third branchial cleft not developing until somewhat later (Fig. 78, D).
It is now further obvious that, between the depressions just noted,
the surface of each gill plate will be relatively raised so as to form
ridges which are the external indications of the hyoid and branchial
152
   
THE FROG: THE EARLY EMBRYO
Inf
Fig. 79.——Posterior ends of a series of young Frog embryos,
showing the later history of the blastopore, and the relation of
the neural folds to it. The embryos are viewed obliquely from
the postero-lateral aspect. From Kellicott (Chordate Development). After F. Ziegler. A. Blastopore nearly closed, neural
folds just indicated. B. Blastopore becoming divided into neurenteric and proctodaeal portions, lips between fusing to form
primitive streak; neural folds becoming elevated. C. Neuronteric canal forming; neural folds"closi_ng together. D. Neural
folds in contact throughout. E. Neural folds completely fused;
tail commencing to grow out.
b. Blastopore, containing yolk plurr. b1. Rudiment of neurenteric canal (dorsal part of blastopore). be. Rudiment of proctodaeal pit (ventral part of hlastopore). brz. Branchial arches.
g. Neural groove. nf. Neural folds. np. Neural plate. p. Proctodaeal pit. 5. Rudiment of oral “sucker.” t. Rudiment of tail.
9:. Neural folds roofing the blastopore and establishing the
neurenteric canal. y. Primitive streak.
EXTERNAL CHAN GES 153
arches. The most anterior portion of the plate which lies between the
hyomandibular cleft and the fi1‘SlZ hranchial cleft is the hyoid arch, while
the portion lying between the first and second branchial clefts is the
first branchial (gill) arch. Since the third branchial cleft has not yet
appeared, the portion of the plate posterior to the second branchial
cleft really represents both the second and the third branchial arches.
The Closure of the Blastopore. ~—~As the above events are transpiring anteriorly, certain processes are also occurring posteriorly, as
follows: As the medullary folds begin to move toward one another, the
lateral lips of the blastopore also draw together, so that the latter is
no longer round. Instead it has the form of a short vertical slit (Figs.
79, B and 80). Presently, moreover, these lips fuse with one another
for a certain distance midway between their dorsal and ventral ends.
As a result there may appear in this region for a time a slight vertical
groove connecting the dorsal and ventral openings which temporarily
remain. In the present case this is the primitive streak. In it, ectoderm,
mesoderm, and endoderm meet in one mass, and from this mass, cells
for all three layers are budded as the embryo increases in length. It is
very important to note that this primitive streak is homologous with the
similarly named structures which are to be described in connection with
the next two forms. It is also probably comparable with the primitive
streak of Birds and Mammals, and with the structure similarly defined
in the general discussion in Chapter II.'Tl1is question will be discussed
more fully in connection with the Chick.
The opening which remained at the ventral lip closes presently, but
only the ectoderm and endoderm are involved. Hence the wall is thin
at this point, and a slight pit remains. It is the procIo(z'(m11.r7r (Figs. 79,
D and 80). The dorsal opening of the blastopore persists for a somewhat longer time. It disappears externally, however, because the neural
folds which extend on either side of it fuse at this point as elsewhere,
and thus roof i.t over. This process will be further noted in connection
with the nervous system.
Other Changes. —— Besides the features already mentioned there are
a few other external alterations which usually become apparent by the
time the embryo is from 2.5 to 3 mm. in length. In the first place, in con
nection with its slight elongation, the animal has begun to lose its spher- ‘
ical form, so that the convexly curved line of the back (Fig. 77, F) becomes first straight and then actually concave (Fig. 78). Secondly, just
posterior to the dorsal region of the gill plate there may often he noted
a slight swelling, the outward indication of the internal growth of the
154 THE FROG: THE EARLY EMBRYO
B medullary plate C
 
 
 
 
 
 
 
 
 
 
neural fold
   
notochord
blastoooral
part or future
neurenzenc .
- neural
- tube
rcgmnaf
future
neuranzernc
canal
fug:urc_
prumluve
streak region
{Iervcus
ayer of
eccodzrm
mesoderm
reeonscru - cl median sagitral section
lmfargln of oral
evaglnallon
mesoderm
blastcporal
part of future
neurcnteric canal
 
 
nervous layer
of ectoderm
neural tube
reglan of future
neurenteric canal ‘
proccodaeum
E
X section I22 F
X secuan I27
Fig. 80.———A median sagittal section reconstructed from serial cross sections, and
a stereogram of a hemisected total neural groove stage. A, B, C, D, E, F. Selected
cross sections as shown by serial numbers, at levels indicated by vertical lines on
the sagittal section. The neural folds have not yet closed posteriorly to- form the
neurenteric canal and the primitive streak.
THE NEURAL TUBE AND RELATED PARTS 155
pronephros or embryonic head‘ kidney (see below). Also along the
dorso-lateral region posterior to the gill arches and just above the level
of the pronephros, > shaped markings arise giving external evidence
of the myotomes. Lastly the embryo by this time is partially covered by
cilia whose motion causes it to rotate slowly within its membranes.
Under average outdoor conditions the stage thus described is generally reached at about the end of the second day after fertilization.
Let us now turn to a consideration of the internal processes which have
been going on during the same period..
INTERNAL CHANGES: THE NERVOUS SYSTEM
THE NEURAL TUBE AND RELATED PARTS
The Neural Tube. —- This structure, as its name suggests, possesses
an internal, laterally compressed canal termed the neurocoel or neural
canal. From the manner of its formation, the lining of this canal is obviously the former outer ectodermal layer of the medullary plate, while
the present outer wall of the tube was previously the inner or nervous
layer of that plate. Thus the floor of the tube is relatively thin, since it
occupies the position of the former medullary groove where the inner
or nervous layer was least developed. The lateral walls, on the contrary,
are thick because they are constituted of the well developed nervous
layer on either side of the groove. The roof is evidently formed as the
edges of the two folds meet one another and fuse, and, like the floor, it
is thin as compared with the sides. As will appear below, this is due to
the fact that not all of the nervous layer along the line of fusion becomes involved in that process. Finally it should be added that as the
tube is thus made complete, the meeting of the folds likewise makes
continuous the ectodermal wall above it.
The Neural Crests.»-—As just noted, not all of the nervous layer
of the medullary plate is used up in the formation of this tube. The
lateral edges of the plate, i.e., the neural ridges proper, although carried up to the region of dorsal fusion are not included in the walls of the
tube. Instead, these ridges of nervous tissue are partially constricted off
from the main part of the nervous layer. Each of the two ridges is thus
semi-independent, and occupies a position well up in the angle between
the sides of the tube and the ectoderm of the body wall (Fig. 80, no) .
These are the neural crests, which presently become out up into successive segments. In the head and branchial region the crests are quite
prominent, but more posteriorly they are obscure and difficult to detect.
156 THE FROG: THE EARLY EMBRYO
In general they are concerned with the development of the cranial and
spinal rranglia although those in the head and branchial regions have
n 7 _
been fdaund also to furnish material for some of the visceral arches.
Their respective fates will be discussed in more detail in connection
with the development of the nervous system.
THE BRAIN REGION AND SENSE ORGANS
The Brain Region.—In the anterior region the complete closure
of the neural tube is somewhat delayed because of the greater breadth
of the medullary plate at this point. Indeed, the process here might be
still slower were it not that the growing together of the lateral edges is
accompanied by the backgrowth of the transverse ridge. At the place
where this ridge and the lateral folds are about to fuse there exists for
a brief time a small opening; it is the neuropore, and is homologous
with the similar structure in Amphioxus.
At the time the medullary plate first appeared, the embryo was still
virtually in the form of a sphere, and the plate followed its curvature.
As the neural tube begins to form, however, the embryo, as already
noted, starts to lengthen out, the line of the back becoming straight,
and then slightly concave. During this pm;-cess, net-ertl‘.-eless, the original curvature in the foremost portion of both the neural tube and the
notochord not only ersists but even increases. it thus happens that
these parts are bent ldownward so that the anterior and sornewl‘zut expanded extremity of the tube has the aspect of the bulbous closed end
of a chemical retort. This bending‘ is termed the cranial flexure. Hence
it comes about that the roof of the tube in this region is actually
anterior, and in the midst of this anterior wall is the recently closed
neuropore. This point is marked by a slight iuvagination, both exterinally and in the brain wall, and by a small thickening in the nervou:-:
layer of ectoderm (Fig. 81). V
Elementary Divisions of the Brain. —The constrictions which divide
the brains of most vertebrate embryos into fore-brain, mid-brain, and
hind-brain have not become evident in a 2.5 mm. Frog larva. These
divisions of the brain may be roughly defined at this time, however,
by reference to the following landmarks: Just opposite the curved anterior region of the notdchord, the posterior wall of the brain, as suggested above, also curves, and the most anterior point on this curve may
be designated as the tuberculum posterius. Directly across from this on
the anterior brain wall is the invagination already noted as marking
the closed neuropore, and immediately dorsal to this is a distinct inTHE BRAIN REGION AND SENSE ORGANS 157
ward bulge formed by a mass of cells termed the dorsal thickening
(Fig. 81). Using these points as places of reference the brain may now_
be divided into its three fundamental regions:
I. The fore-brain or proscencephalon extends from the anterior ex
notothord
 
 
 
 
   
   
endoderm
neural plate
beginning of future
neurenterl: canal
pm‘mdaeum_ transverse neural ridge
rectal evagination
mesodermal layer
nervous layer of ectoderrn
pldermal layer
tuberculum potterlus
dorsal thickening
neurenteric canal
Iosed neurbpore
infundlbulum
1- primordium of
anterior pituitary
proczosiaeum
stamodaeum
mesoderm of
future pericardium
beginning of mucoux gland
pharyngeal reglon
nervous layer
0! ettoderm
 
\§
cm.-‘
liver evaginatlon
Fig. 81.—A. Sagittal section of neural groove stage. The remains of the blastecoel is not often seen so late as this. In this case the region between the beginning
neurenteric canal and the proctodaeum (primitive streak_l has been occluded by the
fusion of the sides of the blastopore. B. Sagittal section of neural tube stage. The
proctodaeum does not usually have so large a cavity connected with it, but did in
this case. The rectal evagihation which meets the proctodaeum is unlabeled.
tremity of the tube, i.e., the lowest part of the bent region, to a plane
joining the tuberculum posterius with a point between the dorsal thickening and the closed neuropore. »
II. The mid-brain or mesencephalon extends from the posterior
boundary of the proscencephalon to another plane which joins the
tuberculum posterius with a point slightly back of the dorsal thickeninv.
III. The hind-brain or rhombencephalon. extends from the posterior
boundary of the mesencephalon insensibly into the spinal cord.
158 THE FROG: THE EARLY EMBRYO
It is thus evident, as indicated above, that the fore-brain is chiefly
below and in front of the end of the notochord, the mid-brain is anterodorsal to the end of the notochord, while the hind~brain lies entirely
‘over the notochord.
Within the divisions of the brain thus defined there is very little
differentiation of any sort as yet. In the most ventral portion of the
forebrain, however, there does appear at about the end of the time we
are considering, a slight rather broad and vaguely delimited posterior
outpushing. It is the rudiment of the infundibulum, which will become
the posterior part of the hypophysis or pituitary body. The anterior
part of this important endocrine gland: also appears at this time, and
it is therefore convenient to describe it here, though unlike the posterior infundibular part it is not a brain derivative at all. At this stage
it is more clearly defined than the infundibulum, and arises as a tongue
of ectodermal cells of the nervous layer extending dorso-posteriorly
from the dorsal margin of the stomodael invagination. It lies therefore
just beneath the forebrain, and is growing backward in such a way as
eventually to meet the infundibulum (Fig. 81, B).
With the mention of these structures it becomes necessary to digress
for a moment in order to make clear the way in which we shall use the
terms applied to them and their parts. This is because the definitions
of these terms have been considerably confused by various writers,
especially as they have been employed in connection with some of the
lower animals. Strictly speaking the organ referred to as the hypophysis or pituitary in human and other mammalian anatomy includes two
main parts from the point of view of origin. One is derived from an ingrowth from the stomodaeum, and includes the pars distalis (anterior
lobe proper), pars intermedia and pars tuberalis. The other main part
is called the pars nervosa, which is derived from the larger portion of
the infundibulum, the smaller remainder forming the stalk of the hypophysis. The pars nervosa is also frequently referred to as the posterior
lobe (Gray’s Anatomy, 24th edition). Even here, however, there is confusion since the “posterior lobe” according to some authors (Maximow
and Bloom, 5th edition) seems to include not only the pars nervosa. indubitably of infundibular origin, but also the pars intermedia which is
indubitably from the stomodaeum (Hegre, ’46) . As a matter of simplification, and for the purposes of this text, the writer will term all parts of
the hypophysis derived from the stomodaeum simply the anterior part,
and all parts derived from the infundibulum, i.e., the pars nervosa, the
posterior part. Finally it should be understood that in the Amphibia
THE BRAIN RF:GION AND SENSE ORGANS 159
the position of the anterior part as here defined is really posterior to
the pars nervosa or posterior part. The parts are nevertheless designated in this way because in adult avian, human and other mammalian
anatomy the anatomically and embryologically homologous parts do
actually. occur in the anterior and posterior positions.
The Sense Organs.—Before the anterior or brain region of the
medullary plate has closed, there appears on either side a patch of
pigmented cells (Fifi. 82). As a result of the closing process, these
outpushtng
Pom“ of optic vesicle
neural crest
Fig. 8Z.—Cross section of a 2 mm. Frog embryo
through the anterior end of the neural groove, showing
optic vesicles starting to push out. Note the pigment
spot on the inner side of each vesicle. The epidermal
and nervous layers are thicker because they are cut
tangentially due to the curve of the embryo in this
region.
patches presently come to occupy positions on opposite sides of the
interior of the fore-brain. The area of the brain wall including and immediately surrounding each patch now begins to push out or evaginate
toward the external ectoderm of the head (Fin. 85, A). These evaginations are the optic vesicles. Presently each vesicle reaches the ectoderm
in the dorso-lateral region of the sense plate, and by its pressure here
soon causes a slight external protuberance noted above. Meanwhile the
regions of the vesicles nearest the brain begin to become slightly constricted to form the optic stalks (Fifi. 85, A).
The sensory portions of the ears, unlike the above parts of the eyes,
do not develop from any region of the brain itself. Instead they arise
from the dorso-lateral walls of the head. The rudiment of each appears
during this period as a thickened patch of the nervous‘ layer of ectoderm
opposite the hind-brain. These thickenings in part constitute the auditory placodes (see below under ear).
At about the same time in another region of the head two other thick160 - THE FROG: THE EARLY EMBRYO
enings of the nervous ectoderm develop. In this case each is within
the area of the sense plate a short space beneath, and, median to, the corresponding optic protuberance. These are the beginnings of the olfactory organs, and are termed the olfactory placodes (Fig. 83). Though
later each is indicated externally by a pit, these markings are usually
not in evidence at this stage (see below). Figure 83, however, is of a
slightly later stage (3.5 mm.), which accounts for their appearance in
that case.
 
olfactory placo
nervous layer
f d optic vesicle
O CCIO erm
         
 
‘tii:'LT?'9n
mandibular arch
' yomandibular cleft
(3 hyoid arch
‘em, lst branchtal cleft
’ H‘
infundibulum ' i‘
     
|Vth branchial cleft
undivided mesoderm
Fig. 83.—Frontal section of a 3.5 mm. Frog embryo through the olfactory pits,
optic vesicles, and visceral clefts and pouches.
Experimental Results. —— In connection with the discussion of gastrulation a good deal was said about the principle of induction, and it
was indicated that further illustrations of it would be noted as occasion
arose. Three excellent examples are afforded with respect to the origin
of the oral mucous glands, the nasal capsules and the optic vesicles.
In the Urodele, Amblystomaf it happens that in place of the mucous
glands there occur leglike projections called balancers on which the ani
2 The writeriis aware that the correct generic name for this animal is Ambystoma rather than Amblystoma. However, the latter has become so firmly fixed in the
literature, particularly the embryological literature, that it seems best to use it in
this text. This is made even more advisable in view of the fact that the latter spelling is the one used in all the articles cited.
THE N EURENTERIC CANAL 161
mal rests. Schotte and Edds (’40) found that Frog ectoder'm from regions which would not normally produce mucous glands, would do so
when transplanted to the head of Amblystoma at the site of, and in
place of, the latter animal’s balancer producing ectoderm. This shows
two things. It indicates first that the formation of either mucous glands
or balancers is apparently due to the inductive action of the underlying
mesoderm. Secondly, it shows that though the Frog ectoderm is thus
acted upon by the Amblystoma inductor, it can, nevertheless, only form
the kind of organ for which it has competence, namely, mucous gland,
not balancer.
In the case of the nasal placodes Zwilling (’4«O) has shown among
other things that apparently they may be induced in the nervous ectoderm by the roof of the‘ underlying archenteron. Also the olfactory pit
can be induced in the epidermal ectoderm by the layer of nervous olfactory ectoderm underlying it.
Finally in the case of the optic vesicles Adelmann (’30, ’37) and
others, by the usual transplantation experiments, have demonstrated
two points. First, the inherent capacity (competence) of the head ectoderm to form these vesicles at all is considerably reinforced by the inductive action of the underlying prechordal plate (potential notochord). Secondly, this inductive action causes two vesicles to form
where there would otherwise be only one (cyclopia) .
THE NEURENTERIC CANAL
While the above developments have been taking place in connection
with the anterior end of the nervous system there has also been a change
posteriorly. It was noted in describing the externals that as the neural
folds close in this region, they roof over the dorsal part of the blastepore. As stated, however, this portion of the blastopore, though no
longer communicating with the outside, still remains open. It thus constitutes a temporary connection between the enteron and the neurocoel.
As in Amphioxus, this connection is termed the neurenteric canal (Fig.
81). It should be noted in this case that the canal is seldom if ever
demonstrable as an actual open tube, and its existence has therefore
been denied by some. Usually in fact it appears merely as a line of pigment. In good specimeliis which the writer has examined, however, the
clean cut character of the cells bordering the path of the “ canal ” in all
probability indicates a definite line of cleavage. Indeed it seems clear
that what amounts to a “ probe patency ” certainly exists, were it possihle to use a probe on so small a structure.
162 THE_ FROG: THE EARLY EMBRYO
INTERNAL CHANGES: THE ENTERON
THE FORE—GUT
The anterior region of the archenteron is enlarged and lies in front
of the mass of yolk cells which form the floor -of the middle region.
This anterior portion is therefore termed the fore-gut, and a little later
will be differentiated into the pharynx, esophagus, stomach, and liver.
These parts are as yet scarcely distinguishable. Nevertheless, during the
period under discussion, the fore-gut as a whole gives rise to certain
rudiments as follows:
The Pharyngeal Region.——In the antero-ventral region beneath
the fore-brain there is an outpocketing in the direction of the invaginated ectoderm, though the two walls are not yet in contact. It is called
the oral evagination and may be considered as the extreme anterior end
of -the pharynx (Figs. 81; 85, B). Immediately posterior to this in the
region of the fore-gut which is destined to hecome the pharynx proper
there have already been noted the external rudiments of certain of the
visceral clefts; i.e., the hyomandibular, and the first, second, and fourth
branchials. Considering now the internal development of this region at
a corresponding stage, the following condition is to be observed. Opposite the invaginating ectoderm which marks externally the rudiments
of the above mentioned clefts the endoderm of the pharynx is beginning
to push outward upon either side to form the corresponding pairs of
' hyamandibular, and first and second branchzal or gill pouches. It
should further be added that although these vertically elongated pharyngeal evaginations are called pouches, they do not actually appear as
such. This is because the anterior and posterior walls of each outpushing are at this time fused together, so that no pouch cavity really exists.
Thus it may be noted that each pouch resembles rather a two layered
sheet of endoderm, extending from the fore-gut toward the ectoderm
(Figs. 33, 102).
The Liver.—In the extreme ventro-posterior part of the general
pharyngeal region there is evident a slight posteriorly directed pocket
beneath the anterior end of the yolk mass. This represents the rudiment
" of the liver (Fig. 81, B).
THE MID-GUT
The portion of the enteron following the fore-gut lies, as noted, above
the main mass of the yolk cells which thus form its floor. Its lumen is
THE VISCERAL ARCHES 163
, relatively small with a thin roof, and sides which thicken ventrally. It
is the mid-gut, and is destined later to develop into the intestine.
A peculiar and transitory structure developed in connection with this
region is the hypochorclal rod. It arises at about 2.5 mm. as a longitudinal string of cells constricted oil‘ from the dorsal wall of the mid-gut,
between it and the notochord. Appearing first slightly posterior to the
pharyngeal region it later extends even into the tail. It soon becomes
separated from the gut by the development of the dorsal aorta, and
shortly after hatching it disappears entirely.
THE HIND~GUT
Posterior to the mid-gut just in front of the neurenteric canal the en
teron enlarges slightly. This region is termed the hind-gut, and is destined to form the rectum.
THE MESODERM AND REIATED STRUCTURES
Shortly following gastrulation, the condition of the mesoderm is as
follows: Ventrally and laterally it exists as a continuous sheet extending up to the notochord on either side. In the head and most of the
pharyngeal region it is represented only by scattered cells, while posteriorly it reaches to the blastoporal region, which continues to bud it
oil. During the period we are now discussing the mesoderm thus indicated begins to give rise to various structures in the following manner:
THE VISCERAL ARCHES
It will be recalled that in the pharyngeal region at this time) the
hyomandibular and the first two pairs of branchial or gill pouches are
developing as solid vertically elongated evaginations of endoderm. As
these evaginations push out to the ectoderm, it is obvious that the
mesoderm in the way of each will be thrust to either side. In this manner such mesoderm becomes more or less concentrated in the regions of
the future visceral arches which are to alternate with the pouches. Indeed, it may at this time be said to represent their rudiments, whose
external appearance has already been described, as having the form of
raised areas between the incipient clefts. Thus in front of the first or
hyomandibular pouch is the mesodermal rudiment of the mandibular
arch (apparent externally as the lower portion of the sense plate upon
either side of the stomodaeum) , while between the hyomandibular and
first branchial pouch is the rudiment of the hyoid arch. The first bran» 164 THE FROG: THE EARLY EMBRYO
Fig. 84.—-Sections through Frog embryos (R. sylvatica) illustrating the formation of the pronephros. From Kellicott (Chordate Development). After Field. A.
Through the anterior body region of an embryo at the commencement of its elongation. B. Through the anterior end of the pronephric rudiment of an embryo in
which the neural folds are just closed together. C. Through the second nephrostome
of an embryo of about 3.5 mm.
c. Coelom. ca. Rudiment of pronephric capsule. cc. Communicating canal. ec.
Ectoderm. en. Endoderm. g. Gut cavity. mp. Medullary plate. my. Myotome. n. Notochord. nc. Rudiment of neural crest. ne. Nephrotome. 5. Pronephric nephrostome.
sc. Spinal cord. sn. Subnotochordal rod (hypochorda). so. Somatic layer of mesoderm (in A the reference line points to the rudiment of the pronephros). sp.
Splanchnic layer of mesoderm. t. Pronephric tubule. v. Vertebral plate of mesoderm.
chial arch then follows the first branchial pouch, and the second branchial arch follows the second branchial pouch. Since, however, the
third branchial pouch is scarcely formed as yet, the mesodermal ele
ment of the second branchial arch is not at this time very clearly distinguishable from the tissue posterior to it. '
THE SEGMENTAL PLATES AND THE LATERAL PLATES
Along either side of the notochord ‘posterior to the pharyngeal region, the mesodermal sheet thickens into a relatively narrow band which
THE SEGMENTAL AND LATERAL PLATES _ 165
is termed the segmental or vertebral plate. The remainder of each sheet
below this region is then called a lateral plate. Ventrally the two lateral
plates are continuous with one another (Fig. 85, D).
Formation of the Coelom. — In its dorsal region each lateral plate
now begins to become split into two sheets. The outer sheet next to the
 
beginning of auditory
vesicle llnd placode
beginning of perlcardial cavity
Fig. 85.——Four selected cross sections from a series of one 2 mm. (neural-tube
stage) Frog embryo. A. Through the optic vesicles and rudiment of anterior pituitary. B. Through auditory vesicles and oral evagingtion. C. Through pharynx in
region of III neural placodes and crests, and the future heart. D. Through anterior
part of mid-body region, showing liver evagination and nephrotomes.
ectoderm is the somatic mesoderm (somatopleure), while the inner
sheet next to the enteron is the splanchnic mesozlerm (splanchopleure)
(Fig. 85, D). Between them a space presently becomes evident which
is the rudiment of the coelom. Upon either side, this coelom then gradually extends downward through its respective lateral plate. During the
period we are describing, however, these two extensions do not reach
quite far enough to meet one another beneath the gut. Thus in this region the coelomic cavity in each plate is temporarily separated from
the one on the opposite side. Besides this downgrowth of these cavities
166 THE‘ moo: THE EARLY EMBRYO
Fig. 86.—Transverse section through the
sixth mesodermal somite of a 5 mm. larva of
R. temporaria, illustrating the arrangement
of the mesoderm. From Kellicott (Chordate
Development). From Maurer
Harulbuclz, etc.).
c. Cutis plate. ch. Notochord. D. Gut wall.
In. Myotome (muscle plate). me. Nerve cord.
p. Lateral plate. scl. Sclerotomal cells. 12.
Ventral process of myotome and cutis plate.
( I-lertwig’s
there is also an upgrowth into
the mesoderm of the segmental"
plates (Fig. 84). Here the
slight spaces which last but a
brief time are termed the
myocoels.
The Somites. —— Meanwhile the segmental plates are
also undergoing other changes.
Just back of the pharynx each
plate is being divided transversally into sections termed
somites. During the period
under consideration, about
four pairs of these. somites
are thus formed, development proceeding posteriorly.
Shortly after its formation
each somite loses its connection with the lateral plate,
and exists as a separate mass
of cells. Within each somite so
isolated the myocoel may persist for a brief time, not at the
center of the mass, but just
beneath the outer surface. Because of its previously supposed subsequent history (see
below) the thin layer of cells
forming this outer surface is
termed the cutis plate or dermatame. For the same reason
the remaining inner part of
the somite is called the myotome. The differentiation between these
parts is often indistinct at this time (Fig. 85, D), but is usually clearer
at a later stage (Fig. 86).
4 THE NEPHROTOMF
Along the dorsal border of each lateral plate, just at the line of sepa
ration between lateral plate and segmental plate, is a narrow strip of i
PERICARDIAL CAVITY AND THE HEART ‘I67
somatic mesoderm which is destined to form both the larval and adult
excretory systems. This strip is termed the nephrotome, and becomes
evident as such very early (Fig. 84, B; Fig. 85,’ D) . Indeed, even before
separation of the above plates this region begins to proliferate cells between itself and the ectoderm. In this way the nephrotome becomes a
thick band of tissue attached along its inner border to the dorsal edge
of the lateral plate, whose side it overhangs slightly, like the cave of a
roof. At the very first, as segmentation appears in the vertebral plate,
it also‘ extends slightly into the nephrotomal band. Thus the single
nephrotome tends to become divided into a series of nephrotomes. This
division, however, is very transitory in the Frog and disappears without
further significance. As the coelomic split ‘begins to appear in the
lateral and segmental plates, spaces also start to form in the nephrotome from about the second to the fourth somites (Fig. 84, C). This
marks the beginning of the pronephros, the evidence of -whose presence
has already been noted in the description of the exterior.
THE BEGINNING OF THE MPERICARDIAL CAVITY AND
THE HEART
In the region of the pharynx it has been indicated that laterally the
rather loosely arranged mesoderm is involved in the formation of the
gill arches. In the floor of this region, however, uniting the ventral ends
of these arches, there is a sheet of mesoderm coextensive posteriorly with
the fused lateral plates. It will be recalled that at this period the downpushing coelornic spaces in these plates have not reached to the ventral
side of the animal. Anteriorly, however, in the ventral portion of the
mesodermal sheet which lies beneath the pharyngeal floor, there may
now appear a. slightly indicated pair of independently developing
spaces (Fig. 85, C). Each space lies within the sheet upon either side
of the mid-line, the two spaces being separated from one another by a
narrow median strip of the mesoderm which remains undivided (Fig.
85, C). These spaces are the rudiments of the pericardial cavity, whose
walls are termed the pericardium. The outer or parietal wall is in
dicated at present by the lower of the two mesodermal sheets. It is cons —
tinuous, both now and in the completed organ, with the inner or visceral wall which arises from a portion of the upper sheet, and which
eventually forms a closely adherent covering for the heart muscle. (See
Fig. 85, C and D; cf. also Fig. 107.)
Just above the median strip, between it and the endodermal floor of
the pharynx, there may also appear at this time a few scattered cellsl
168 ‘THE FROG: THE EARLY EMBRYO
These cells have been regarded as having originated like the dorsal
mesoderm of the lateral plates, i.e., by a splitting off from the endodenn
which in this case lies above them. It now appears, however, that they
are derived entirely from mesoderm which, in Amblystoma at least, as
shown by staining experiments of Wilens, ’55, has migrated from between the ear anlage and the hind-brain. The scattered cells are destined
to form the endothelial lining of the heart, or endocardium, while the
remainder of this mesodenn forms other heart and pericardial tissue
to be described in the following chapter (Fig. 85, C). Though all parts
of the heart are thus apparently mesodermal in origin, there is evidence
that the overlying endoderm does have an organizing efl'ect on their
development (Bacon, ’45).
Before leaving the development of the heart at this early stage, it is
of interest to note what happens when these heart-forming elements are
manipulated in various ways as was done by Copenhaver (’26) on
Amblystoma. Thus if a moderate amount of the median region is removed, the lateral parts will grow down and replace it so that a single
complete heart develops. If, however, a piece of foreign mesoderm is
substituted for the removed part, the lateral parts will form two separate hearts with mirror image symmetry. Removal of an anterior or
posterior half does not prevent the formation of a complete heart if it
is done early enough, but the anterior and posterior parts are apparently irreversibly determined considerably sooner than are the lateral
' parts. Not only, however, is it true that parts may form whole hearts,
but two wholes if properly united may form single hearts. Thus if a
second layer of heart-forming mesoderm from one embryo is superimposed by transplantation upon the heart-forming mesoderm in another embryo, the two layers will fuse and a single normal heart develops. On the other hand, as might be anticipated from the previous
statement about anterior posterior determination, this only happens at
the stage in question if the second layer is normally orientated. If the
latter is reversed with respect to its antero-posterior axis, fusion is im
perfect. Also, since heart pulsation is initiated at what is at first the
posterior end of the organ, in this latter case disharmonic pulsation
results.
"HE FROG: LATER Oli LARVAL DEVELOPMENT
IN the last chapter the development of the embryo was discussed
up to the point where it had reached a length of about 2.5——3 mm., and
acquired the rudiments of most of the chief systems and organs. We
shall now continue the history of the animal from this point to the adult
condition, having regard to both the external and internal changes. The
former will be considered first, under the head of three rather obvious
stages which ‘will become apparent as the description proceeds.
EXTERNAL DEVELOPMENT
TWO AND ONE—HALF MILLIMETERS T 0 HATCHING
During the first week or two, depending on the temperature, elongation progresses to a considerable extent, largely as a consequence of
the outgrowth of the tail region posterior to the blastopore. Concurrent
with this process, the > shaped depressions marking the boundaries of
the myotomes not only -become evident throughout the body region, but
appear also upon the sides of the tail. At the same time just back of the
gill plates the pronephric swellings increase in size. In the head the outpushings due to the optic vesicles become somewhat more pronounced,
but in a slightly different position from the one which they first occupied, i.e., less upon the front of the head and more upon the side. This
last mentioned change is really due to the beginning of a forward
growth of the region anterior to them, which continues gradually for
some time, and results in the eventual location of the eyes some distance
from the tip of the snout. Meanwhile the stomodaeum proper forms at
the dorsal end of the elongated stomodaeal invagination, while upon
each sense plate, slightly dorsal and to one side of the stomodaeum, appears a small depression, the olfactory pit. Each gill plate, on the other
hand, now develops upon its surface another slight vertical groove lying between the rudiments of the second and fourth branchial clefts.
This new indentation is the beginning of the third bronchial cleft, so
that theypositions of all four branchial clefts are now indicated (Fig.
3br. cl.  2br.cl.
spr.
1 br.cl:
°PC
.cl.
- by sti.
Fig. 87.—-Drawings of preserved Frog embryos and larvae (Rana pipiens) from
4 mm. to 14.5 mm. in length. For the sake of keeping correct the relative size differences of the drawings in this figure it has been necessary to make them on a smaller
scale than those in figure 78. A. Right side of a 4- mm. embryo. It will be noted that
the tail has just begun to grow out, that the positions of all the visceral clefts are
apparent, and that the olfactory pits are present. The oral “suckers,” being now
entirely ventral, are not actually visible from this point of view. The myotomes in
this embryo and in B and C are very slightly indicated externally. B. Right side of
a 6 mm. embryo. The external gills of the first and second branchial arches have
begun to develop, concealing the second and third hranchial clefts. The stomodaeal
invagination is deepening, and is slightly visible from the side. C. Right side of a
9 mm. embryo. ‘The external gills have grown considerably, and developed several
lobes. From the posterior border of the lower portion of the hyoid arch, the operculum is just starting to develop, and thus covers slightly the region of the first
branchial cleft. The stomodaeal invagination, scarcely visible from the side, has
almost given rise to the mouth. D. Left side of a 14.5 mm. larva. The external gills
have been covered by the operculum, and the gill chamber opens to the outside only
through the spiracle. The eye is formed, the mouth is opened into the pharynx and
its‘ lips are covered with raspers. The hind limb buds have appeared, and the tail
has developed a finely veined memhraneous edge or fin.
a. Anus. I br.d. 2 br.cl. 3 br.cl. 4 br.cl. Rudiments of the first, second, third,
and fourth branchial clefts. The corresponding arches and their positions are indicated in the text._ e. Eye. 1 eg. 2 eg. First and second external gills. hl. Hind limb
buds. hy.c_l. iludiment of hyomandibular cleft. In. Mouth. ol.p. Olfactory pit. op.
External indication of optic vesicle. ope. Edge of operculum. as. Oral “sucker.”
pm. External indication of pronephi-os. spr. Spiracle. :t.i. Stomodaeal invagination.
170
ol. p.
FROM HATCHING TO METAMORPHOSIS . 171
87, /1). Lastly, a short time before hatching there appears upon the
upper part of the first and second branchial arches of each side a small
lobed outgrowth; the rudiments of two pairs of external gills (Fig.
87, B).
The embryo (6-7 mm.), which is now ready to hatch, presently
wriggles its way out of the surrounding jelly. From this time on it may
be referred to as the larva or tadpole.
FROM HATCHING TO METAMORPHOSISV
Early Larval Life. —- For a few days after hatching, the young tadpole. which is a dark brownish color, lies on its side or remains attached to some convenient object by its V-shaped mucous gland. During
the first part of this period the mouth is incompletely formed, and the
animal is still dependent on the yolk for its nourishment. Meanwhile
the two pairs of external gills develop rapidly, the original lobes of
each gill putting forth several longer minor lobes or filaments (Fig.
87, C). There furthermore arises upon each third branchial arch a rudimentary third gill. This gill, however, never develops far, and is overlapped and concealed by those anterior to it. Aside from these features
it will also be noted that the body and particularly the tail have increased in length, while the optic protuberances are still further back,
as a result of the continued outgrowth of the snout. Upon the center of
each of these protuberances, moreover, there frequently appears at this
time a slight depression marking the external beginnings of the actual
eyes which are soon clearly visible.
In another week or somewhat less (9-10 mm.),- certain further
changes occur as follows. The mouth is opened and appears as a small
round orifice armed with a pair of horny jaws and with lips covered
by horny rasping papillae. At the same time the above mentioned mucous gland begins to atrophy, and the larva giving. up its fixed existence
swims actively about in search of food. This consists of either animal or
vegetable debris which it can scrape loose with its horny aws and lips;
in captivity it will feed readily on any sort of cereal. In connection.with
this change of. nourishment, the digestive organs are rapidly developed
so as to give the body a full rounded appearance. This is particularly
due tothe great increase in the length of the intestine which can be seen
through the ventral body wall looking like a coiled spring.
As the above alterations occur in connection with the alimentary
tract, certain changes also take place in the respiratory system, of which
the following may be regardedas exterior. Posterior to the first and second branchial arches the incipient second and third branchial clefts be172 THE FROG: LATER on LARVAL. DEVELOPMENT
come opened into the pharynx by way of the corresponding pouches as
actual clefts or gill slits. The first and fourth branchial depressions then
presently become true clefts in a similar manner. Concurrent with these
events there is also developing from the posterior border of each hyoid
arch a fold of integument called the operculum. These opercula then
grow backward on each side, covering the gills as they progress. They
also grow toward one another ventrally until they meet and fuse. Thus
a closed bronchial or gill chamber is formed which opens externally on
the left side only, through a short funnel between the body wall and
operculum, known as the spiracle (Fig. 87, D). It should finally be
noted in this connection that as the closure of the branchial chamber is
completed, the external gills start to atrophy and are replaced by internal gills upon the edges of the gill slits. These new organs will be
' more fully described in the discussion of internal changes.
Later Larval Life.—-After the attainment of the above condition
during the first two or three weeks of larval life, development proceeds
somewhat more gradually to the time of metamorphosis. During this
- interval, which may last for two or three months or sometimes over the
following winter, the larva increases considerably in size.‘ It also loses
its brownish color and becomes more or less green dorsally, and white
ventrally. Perhaps the most striking external feature, however, is the
growth of the legs which begins at about the end of the first month. The
fore legs develop first, but are not visible because they are covered by
the operculum. The hind legs are easily seen as they arise at the base of
the tail, and by the end of the second month they begin to show joints.
Experimental Results.——In connection with leg development a
considerable amount of experimentation has been done to discover
when the antero-posterior and dorso-ventral axes are determined, and
what factors may be involved in the process. These experiments have
been made on Amblystoma rather than the Frog, but it seems likely
that results would be quite similar in the latter animal. The procedure
consisted in reorientating the forelimb rudiment either in the normal
(orthotopic) location or in some abnormal (heterotopic) location.
Thus Harrison (’21) found that if in an embryo with a small tail bud
(stage 29) this limb rudimentwere implanted dorsal side down in its
normal place it would develop a limb with the dorsal side up, but with
the antero-posterior axis reversed. Eventually of course a stage would
1 The larval condition is said to be prolonged by a cool season or a scarcity of
food. Also the larva of certain species, i.e., the Bull Frog, Rana catesbiana, normally
passes through the winter before metamorphosis.
,»__?_R:,.,,....
METAMORPHOSIS 173
he reached where the dorso-ventral axis also could no longer adjust
itself following inversion, but that obviously occurs at a later period.
Other workers have confirmed and amplified these conclusions. Thus
Swett (’37, ’39, ’4l) showed that subsequent reversal of the dorso
ventral axis of.a previously inverted limb is apparently due to factors
in "the flank region, since inverted rudiments implanted in the region
of the myotomes remain inverted. Also it appears that the effect of these
flank factors may be blocked if tissue dorsal to the limb rudiment is
included in the inverted implant.
It should be realized of course that all these cases are again simply
illustrations of special instances of the effect of one part upon another,
i.e., induction.
METAMORPHOSIS
Usually under normal conditions the tadpoles of most species begin
to frequent the surface of the water during the third month. Here they
expel bubbles and gulp in air to supply the developing lungs. This is
one of the signs that metamorphosis is near at hand, and at about the
end of this month the final changes to the form of the adult Frog generally occur with relative rapidity. .
These changes are both internal and external. The former will be
described more fully later. They involve, however, a complete development of the lungs accompanied by certain changes in the circulatory
system. There is'also an enlargement of the stomach and liver, and at
- the same time a great shortening of the intestine. This change is appar
ently correlated with the carnivorous habits assumed by the adult. Externally the alterations are no less fundamental,.and perhaps even more
striking. The larval skin is cast 0H, and with it the horny jaws. The
frilled lips likewise disappear and the mouth instead of being round
becomes very wide. The tongue enlarges, and the eyes grow more prominent. The fore legs become visible by being thrust through the operculum. The left appears first because.it extends through the respiratory
funnel on that side, while the right is forced to break through the opercular wall. At the same time, in company with the development of the
lungs, the gills dry up and the gill slits opening into the opercular
chamber are closed. The hind limbs, which have long been visible, increase greatly in length, and the tail is rapidly absorbed. Sexual differences both internal and external now become clearly evident. There are
other minor changes, but those cited comprise the more prominent and
important ones. .
174 THE FROG: LATER OR LARVAL DEVELOPMENT
The changes just described have of course been known for a very
long time. It is only within recent years, however, that some of the
activating factors have been uncovered by numerous experimenters.
By appropriate removal, transplantation, and injection operations it
has been pretty thoroughly demonstrated that as in the case of so many
other bodily functions the prime mover of metamorphosis, so to speak,
is the pituitary gland. This small, though extremely important, endocrine gland starts to hypertrophy as the time of change approaches. It,
or more specifically the anterior part of it, then secretes a hormone
which in turn activates the thyroid. The latter responds by secreting
the thyroxin whichin this case brings about the various metamorphic
changes characteristic of the particular tissue and the specific animal
concerned, B. M. Allen (’32), Atwell (’35), Atwell and Holley C36),
Etkin (’36), Etkin and Huth (’39), Figge and Uhlenhuth (’33) and
others.
In addition to this evidence as to the internal secretions involved
in metamorphosis there have also been numerous experiments indicating how different tissues respond to the change in general body environment brought about by the endocrines. Thus Helfi (’29, ’30) has shown
that tail muscle transplanted to the back atrophies at the time that the
rest of the tail disappears, and the same has been demonstrated for the
tail skin by Lindeman (’29). This might be anticipated, but it is more
significant that back muscle and skin transplanted to the tail does not
atrophy with the latter. Instead it simply moves up onto the back. An
even more striking example of this is the case of eyes transplanted to
the tails. In several successful operations the eye alsowmoved up at
metamorphosis, and appeared on the rear end of the Frog (Schwind,
’33, Fig. 88).” These are situations with respect to tissues occurring
within a single species. Another revealing result is obtained when Frog
tail buds are transplanted to Amblystoma larvae. At metamorphosis,
when the Amblystoma loses its tail fin, though not of course its tail, the
well-developed Frog tail entirely disappears (as reported by Goldsmith
at A. A. A. 5. meeting ’33) .
Thus in all these cases it seems clear that the fundamental bodily
condition brought about by the endocrine secretions is similar. What
differs is the kind of tissue. Indeed different tissues in the same animal
obviously must differ in this respect, else a general condition causing
2 Though not stated, it is scarcely possible that these eyes were functional, even
though pieces of brain were present in some cases. Hence these remarkable specimens were probably not blessed with both foresight and hindsight!
Fig..88.—Photographs of stages in the metamorphosis
of a Frog tadpole which had had an optic vesicle transplanted from another larvato the region of the tail at the
tail-bud stage. Both tail and vesicle developed normally.
Then when the tail was absorbed, the fully formed eye
persisted, and was moved forward to the posterior end of
the animal. Why was the eye not also absorbed? See text.
175
176 THE FROG: LATER OR LARVAL DEVELOPMENT
the atrophy of one would cause the atrophy of all. In that Went 110$
only would the tadpole tail disappear at metamorphosis, but the whole
tadpole would vanish like the famous cat in Alice in Wonderland. Evidently likewise the difference in the behavior of similar structures, e.g.,
the tails in the Frog and in Amblystoma, is due to specific tissue differences in these structures.
These activities, it may be noted, are in some sense different from
the inductive effects which have previously been cited as playing so
fundamental a part in development. The difference, however, is probably
not very significant. It must be assumed that in the case of endocrine
activities the effects are, or may be, produced on tissues at some distance
from the source of the inducing agent, in such instances called a hormone. In the cases of induction previously noted one must likewise
assume the production of some chemical substance which produces its
characteristic effects. Only in these latter instances the inducing agent
“hormone” is only active upon tissues in contact with or very close
to its source. There are further striking illustrations of the latter type
to be found in connection with metamorphosis. One of these is the case
of the histolysis of the opercular skin over the outpushing forelimb.
This skin is partly broken by the pressure of the limbs. However, Helfl
(’26) has shown that the histolytic action which aids this breakthrough
is produced by the atrophying gills in the immediate vicinity.
We have now finished our survey of the external changes in the embryonic development of the Frog. In the description of internal changes,
it will be most convenient, in so brief a discussion, to complete entirely
the history of one system before taking up the next. In the case of each,
however, as many references as possible will be made to the stages noted
in the account of the exterior. With this aid the student is urged to correlate as often as possible the condition reached by one group of organs
with that reached by another, as well as with external changes. Only in
this way is it possible to obtain a true conception of the growth of the
animal as a whole.
INTERNAL DEVELOPMENT: THE NERVOUS SYSTEM
THE BRAIN
When last mentioned, this organ had been somewhat artificially divided into fore-, mid-, and hind-brain, and within the fore-brain the rudi
ment of the infundibulum was vaguely outlined. Further development
in the three divisions now occurs as follows:
THE BRAIN 177
The Prosencephalon. —Somewhat previous to hatching, at about
4 mm., certain structures _,have developed which are characteristic of
Vertebrate brains at early stages, and which are clearly evident in
median sagittal sections as follows: To begin with the rudiment of the
infundibulum already noted has become somewhat more pronounced.
Proceeding anteriorly around the ventral side of the fore-brain, we encounter next a slight thickening, separated from another more anterior
thickening by a narrow region where the wall is thin, giving the -effect
posterior boundary of mid-brain
scomodaeum
 
anteflor pituitary
mmeus any-locus endadnellmn
Fig. 89.——Median sagittal section of the anterior end of a 4- mm. Frog
embryo. FB. Fore-brain. MB. Mid-brain. HB. Hind-brain.
of a depression. The posterior thickening next to the infundibulum is
the rudiment of the optic chiasma, though of course no nerve fibers are a
present in it at this time. The thin region anterior to it is the optic
recess, and the more anterior thickening is the torus transversus. Continuing up unto the anterior wall of the fore-brain, we see a distinct
thought-narrow outpushing slightly dorsal to the end of the notochord.
It is the epiphysis (Figs. 89, 90).
As regards other developments in this region of the brain we-find that
at about the time of hatching there grows out from the anterior end of
the fore-brain a thin-walled vesicle, which represents the rudiment of
the cerebrum. Presently its sides become thickened, and somewhat later
(12 mm.), it is partially divided in two by a median longitudinal invagination of the anterior and the dorsal wall. The laterally compressed
cavities of the resultant halves, or cerebral hemispheres, are then known
as the lateral ventricles. Posteriorly they communicate with the main
l '78
THE FROG: LATER OR LARVAL DEVELOPMENT
(1 Atrium. ao. Dorsal aorta. b Gall bladder. bk. Basihyal cartilage. c. Cavity of
rudimentary cerebrum. e. E ithelial plug closing the oesophagus. ep. Epiphysis. g.
Glottis. h. Hypoph sis. H. ind-brain. hr Cerebral hemisphere. ht. Horny “ teeth.”
i. Intestine. if. In undibulum. 1'. Lower jaw. 1. Liver. ly. Laryngeal chamber. m.
Mouth. M. Mid-brain. mb. Oral membrane (oral septum). n. Notochord. 0. Median
portion of opercular cavity. oe. Esophagus. p.~ Pharynx. pb. Pineal body. pc. Pei-i~
cardial cavity. pd. Pronephric (more posteriorly mesonephric) duct. pt. Pituit
body. 'pv. Pulmonary vein. pIIL Choroid plexus of third
plexus of fourth ventricle. r. Rostral cartilage. ro. Optic recess. s.
ventricle. pIV. Choroid
Stomodaeum. su.
Sinus venosus. t. Thyroid body. ta. Truncus arteriosus. tp. Tuberculum posterius.
v. Ventricle. vc. ‘Inferior (posterior) vena cava.
of this region becomes folded and hangs down into the cavity of the
THE BRAIN 179
cavity of the fore-brain, or third ventricle, by a pair of openings, the
foramina of Monro. During the remainder of larval life the hemispheres
continue to grow forward and their walls to thicken. Their anterior ends
become slightly constricted away from the main portion of the hemispheres as the olfactory lobes. At first these are separate, but later they
become fused. Thus at metamorphosis when the cerebrum is virtually
mature, it comprises half of the entire brain. Furthermore, on account
of this cerebral increase and the direction of the growth, the relative
proportion of the parts of the brain is so altered that the cranial flexure
appears to vanish. As a matter of fact, however, it is actually unchanged. I
Somewhat after the first appearance of the cerebral rudiment, i.e.,
at about 9 mm., a change occurs in the antero-dorsal wall of the third
ventricle just below and slightly in front of the epiphysis. The thin roof‘
ventricle. Later these folds become very vascular. and are known as the
anterior choroid plexus (Figs. 90; 91, B).
With the appearance of this final structure of the prosencephalon, it
is possible further to subdivide this region as follows. Suppose a plane
to be passed transversely through the third ventricle from the anterior
side of the choroid plexus, to the anterior side of the optic recess between it and the torus transversus. The portion of the ventricle anterior
to this plane is then termed the telencephalon, and the portion posterior
to it, the diencephalon. On this basis it is evident that the cerebral hemispheres arise from the telencephalon and the anterior choroid plexus
from the anterior part of the diencephalon.
Although the pituitary body, as already noted, is not strictly a part of
the brain, its further history may best be described at this point. The
backward growth of the anterior (stomodaeal) part of this organ continues, and at about the same time that the choroid plexus appears, it
loses its connection with the stomodaeal ectoderrn. At the same time it
acquires a cavity, and presently becomes united with the posterior (infundibular) part of the hypophysis, which retains its connection with
the brain through the hollow infundibular stalk. Later the posterior
portion of the anterior part of the hypophysis becomes convoluted and
tubular. As regards terminology, it is to be remembered that the actu__al=G ,_ ..
positions of the above mentioned “ parts ” are reversed in all adult_,§i!l§ ,- 4\ “*).
phibia so that the anterior or stomodaeal part is really behind tl;éfipqsterior or infundibular part. Lastly in this connection it is of -i erést
_ , a
to note that experiment has shown that neither the stomodaea gxlpu-"“"hb‘
i
180 E THE FROG. LATER OR LARVAL DEVELOPMENT
rm, I
Fig. 91.—Median sagittal sections through the brain of the Frog. From Von
Kupfier (Hertwig's Handbuch, etc.). A. Of a larva of R. fusca of 7 mm. in which
the mouth was open. B. R. esculenta at the end of metamorphosis.
c. Cerebellum. ca. Anterior commissure. cd. Notochord. ch. Hahenular commissure. cp. Posterior commissure. cpa. Anterior pallial commissure. cq. Posterior corpus quadrigeminum. ct. Tubercular commissure. cw. Optic chiasma. d. Diencephalon. dt. Tract of IV cranial nerve. e. Epiphysis. hm. Cerebral hemisphere. hy.
Hypophysis (pituitary body). .7. Infundihulum. M. Mesencephalon. Ml. Myelencephalon. Mt. Metencephalon. p. Antero-dorsal extension of diencephalon. pch. Choroid
plexus of third ventricle. R. Rhombencephalon. rm. Recessus mammillaris. ra. Optic
recess. :22. Roof diencephalon. t. Telencephalon. tp. Tuberculum posterius. tr. Torus
transversus (telencephali). vc. Valvula cerebelli. vi. Ventriculus impar (te1encephali) (third ventricle).
-,u—-n-gum-u~v———--—..-..._....._.......
THE BRAIN 181
fundibular part develops normally in the.absence of the other (Smith,
’20) . .
The Mesencepha1on.——The structures of the mesencephalon or
mid-brain are not so numerous as are those of the fore-brain. Its chief
features are the crum cerebri and the optic lobes. The former ‘arise
gradually as a pair of ventro-lateral thickenings composed of nerve
fibers connecting this portion of the brain with the fore-brain. The
latter, i.e., the optic lobes. appear at about 9 mm. as a pair of swellings
in the dorso-lateral regions of the roof. They attain their full size at
about the time of metamorphosis, and their complete development is
apparently dependent on the presence of normally developing eyes
(Kollros, ’53). The cavity of the mid-brain serves to connect the cavities of the fore- and hind-brains, and is termed the aqueduct of Sylvius.
The Rhombencepha1on.—The rhombencephalon or hind-brain
includes the metencephalon and the medulla oblongata. The principal
development of the metencephalon immediately behind the mid-brain is
quite limited in the Frog, the most prominent part being its roof which
at about 9 mm. gives rise to a thickened transverse ridge, the cerebellum
(Fig. 91). The medulla, on the other hand, is more extensive with a
thin roof. The latter always remains thin but at the same time that the .
cerebellum starts to develop it begins to become folded. Soon blood vessels extend down into these folds, and thus is formed the posterior
choroid plexus (Fig. 90, B). The floor and the ventro-lateral walls of
the hind-brain become thickened as nerve tracts. Its cavity connecting
anteriorly by way of the aqueduct of Sylvius with the third ventricle,
and posteriorly with the neural canal, is called the fourth ventricle.
The Spinal Cord. -——'-Posterior to the brain region the neural tube
gradually assumes the character of the adult spinal cord. The laterally
compressed neural canal is, as already noted, lined by cells which were
originally external. These are non-nervous and ciliated, and are known
as ependymal cells. The relatively thick nervous layer which constitutes the bulk of the lateral walls gives rise to both supporting or gl_ia
cells, and to neuroblasts or primitive nerve cells. The latter. lie relatively near the central canal, and comprise the so-called gray matter.
The fibers which arise from them, however, course up and down
through the more superficial parts of the cord, helping still further to .
thicken it, and constituting the white matter.
This thickening occurs first in the dorsal-lateral regions, thereby
causing the neural canal to lie temporarily very near to the ventral side
132 THE FROG: LATER OR LAEVAL DEVELOPMENT
(Fig. 92, A). Gradually, however, the growth of cells and fibers spreads
dowhward so that eventually the canal lies practically in the middle of
the cord..The ventro-lateral growth, moreover, is slightly greater than
Fig. 92.—Transverse sections through the spinal
cord of R. fusca. From Von Kupfier (Hertwig’s
Handbuch, etc.). A. Through the anal region of a
larva of 7 mm. B. Through the anterior body region
of a larva during metamorphosis.
a. Spinal artery. c. Central (neural) canal. d. Dorsal column (white matter). dw. Dorsal root of spinal
nerve. dz. Atrophied dorsal cells. g. Gray matter. oz.
Ventral cells. w. Dorso-lateral and ventro-lateral
column (white matter).
that exactly along the mid-ventral line. Thus a shallow depression occurs here in which runs the spinal artery (Fig. 92, B).
Posteriorly the neurenteric canal becomes severed even before hatching, and the nerve cord continues straight out into the tail. This portion
of the cord is of course lost at metamorphosis.
THE PERIPHERAL NERVOUS SYSTEM
The Cranial Nerves. — In discussing nerves in general, it is quite
customary to divide them into afierent or sensory nerves, and efierent‘
THE PERIPHERAL -NERVOUS SYSTEM
183
F
Fig. 93.-—Sections through young Frog embryos (R. fusca), illustrating the development of,the crest segments (“ ganglia”) and plaoodes. From Kellxcott (Chor~
date Development). After Brachet. A. Transverse secuon through the neural plate
of an embryo before elongation begins. B. Sagittal section to one slde of the mulline, through an embryo of the same age as A. C. Sagtttal sectmn, to one s1de_o{
the mid~line, through an embryo just beginning to elongate. D. Transverse section
througll; an emklirylorslightlfy older thanf that ocf‘ A 231.1:-ltd B. _ E. Friongal iafectfirri thrtglgh
an em ryo wit 1; ee or our pairs 0 meso erm somxtes. , , . ee usverse sections through an embryo just beginning to elongate (same age as C ),
showingl the) trigeminal, acustico-facial and glossopl1aryngeal~vagus crest segments
‘ gang ia .
af. Acustico-facialis crest segment (" ganglion ’’l. c. Notochord. en. Endoderm.
g. Gut cavity. gl. Glossopharyngeal crest segment (‘f gan_g11on”). gv. Glossophary1igeal-vagus crest segment (“ganglion”). l. Llver dxvernculum. m. Mesoderm. mp.
Primitive medullary plate. mpd. Definitive medullary plate. ’r’u:. Neural crest. s.
Mesodermal somites. tg. Trigeminal. crest segment (‘_‘ ganglion 3- mt. vagus (pneumogastric) crest segment (“ ganglion”).
mw».,.,_
Fig. 94.—Portions of sections through the head of the Frog (R. fusca), illustrating the formation of the placodes and the history of the crest segments (“ganglia ”). From Kellicott (Clzordate Development). After Brachet. A. Transverse section through the trigeminal crest segment (“ ganglion ”) of an embryo of 3 mm. B.
Transverse section through the trigemmal crest segment (“ ganglion ”) andplacode
of an embryo with three or four pairs of mesodermal somites. C. Transverse section
through the facial ganglion and auditory placode of an embryo of 2.8 mm.
ei. Inner or nervous layer of ectoderm. en. Endoderm. eo. Outer layer of ectoderm. m. Mesoderm. mpd. Definitive medullary plate. n.-Nerve cord. pa. Auditory
placode. pf. Facial placode. ptg. Trigeminal placode. r. Spinal prolongation of ganglion. tg. Trigeminal crest segment (“ ganglion ”).
Q
THE PERIPHERAL NERVOUS SYSTEM 185
or motor nerves. In describing both the cranial and spinal nerves, however, it is convenient to add a third category, i.e., mixed nerves, which
contain both afferent and efferent fibers. It is understood that all these
nerves occur in pairs, but it will be necessary to describe the development only on one side.
Purely A flerent Nerves. ——There are three cranial nerves which are
purely afferent; namely, the I or olfactory nerve, the II or optic nerve,
and the VIII or auditory nerve. The first two are of a rather special
nature, and are also very closely connected with the development of
the sense organs which they supply. It will therefore be more convenient to describe them later in connection with those organs. The VIII
nerve on the other hand arises in such close connection with the mixed
nerves that it will be described under that category.
Mixed Nerves and the Auditory Nerve.——The nature of the neural
crests has already been indicated, and ‘it was noted that each crest becomes divided into segments. In the brain region there are three such
segments on each side of the head. Considerably before hatching (3-4
mm.) , moreover, the nervous layer of ectoderm on the inside of the head
opposite the segments becomes thickened into patches termed placodes,
one opposite each of the first two segments, and two opposite the last.
It is then from certain nervous or ganglionic elements of these structures, i.e., the crest segments and placodes, that the ganglia of the V,
VII, VIII, IX, and X nerves (Fig. 93) and their afferent fibers develop
in the manner indicated below. The efferent fiber origins of all mixed
nerves will be noted separately. It remains to state that the strands of
cells attaching the crest segments to the brain merely contribute to the
sheaths of the nerves whose origins are being described.
The V or trigeminal nerve ganglion develops from dorsal and superficial cells (the ganglionic element) of the most anterior crest segment
along with cells derived from the inner or ganglionic portion of the corresponding placode (Fig. 94-, B). The anterior part of the ganglion arises
almost entirely from the anterior portion of the placode, and produces
the afferent fibers of the ophthalmic branch of the V nerve. The posterior
part consists of both crest and placode elements, and is sometimes distinguished as the trigeminal ganglion proper, or Gasserian ganglion.
This part produces the afferent fibers of the maxillary nerve which are
derived from the placodal element, and afferent fibers of the mandib
' ular nerve which seem to come from the crest element (Knoufi, ’27).
From both parts of the ganglion a common bundle of fibers also grows
inward to the medulla constituting the sensory element of the V nerve
   
.;.,;,,,.-.,..,.....,.,.‘..,._~;._._..; .,—.-Q_,... —,.o_-.
186 THE FROG: LATER OR LARVAL DEVELOPMENT
root. The ophthalmic branch of the nerve is destined for the skin of
the snout, while the mandibular and maxillary branches supply the
lower and upper jaw. As all of these branches start to develop previous
to hatching, in a 9 mm. tadpole they are well established. It may be
added that the non-nervous part of the crest segment, in this instance
the major part, grows ventrally and contributes to the mesenchyme of
the mandibular arch. The superficial (outer) non-nervous part of the
placode, on the other hand, disappears.
It is how believed that the sensory elements of the VII or facial gan
glion and nerve come exclusively from the second placode, while the
sheath cells are both crest and placodal in origin. At least this has been
proven for Amblystoma (Yntema, ’37) , and seems likely to be true also
in the Frog. As before, some of the fibers which issue from this ganglion proceed inward to the medulla, forming the sensory element of
the root, while others grow outward as the aiferent fibers of the nerve.
Before hatching, the latter have divided into the hyoid and palatine
branches. Here also the considerable non-nervous part of the crest contributes in this case to the mesenchyme of the hyoid arch. No part of
the placode in this instance, however, disappears. One portion is utilized as just described, while the remainder goes to form the ganglion of
the VIII nerve and the auditory apparatus, as indicated below.
The IX and X or glossopharyngeal and vagus (pneumogastric) ganglia arise from the ganglionic portion of the last cranial crest segment in conjunction with the inner, i.e., ganglionic part, of the third
and fourth placodes respectively. In these cases both crest and placode
contribute neurons as well as sheath cells. Fibers from these two ganglia enter the medulla as a single root. Peripheral outgrowths from the
IX ganglion supply the first branchial arch, While branches from the X
pass to the remaining branchial arches. The vagus ganglion also sends
branches to the viscera and to the lateral line organs (see below), the
nerves to these parts being entirely placodal in origin. At least this appears true for Amblystoma (Yntema, ’4-3) , the situation in the Frog not
having been so extensively investigated. Both of these ganglia with their
nerves develop quite early, and in a 9 mm. larva all the main branches
of the vagus nerve are present. In this case the non-nervous part of the
crest segment is not large, but, so far as itdexists, it goes to form mesenchyme. The superficial non-nervous portions of the placodes disappear.
It may now be added that the efferent fibers (axones) for each of
these four nerves (V, VII, IX, and X) grow out from neuroblasts in the
THE PERIPHERAL NERVOUS SYSTEM
walls of the medulla. They pass out of the
brain along with the sensory root fibers of
the respective ganglia, and having passed
through these ganglia they enter the outgoing branches of the mixed cranial
nerves.
The VIII or auditory nerve is, as already noted, entirely sensory, and its ganglion arises from the ganglionic portion
of that part of the second placode which is
not involved in the formation of the ganglion of the VII nerve. The more superficial portion of this placode as usual is
not included in either the VII or VIII
nerve ganglion, but nevertheless, as suggested above, it does not in this instance
disappear. Instead it remains in close contact with the latter ganglion, and develops later into the so-called inner ear, as
described below. Because of the prominent part which the major portion of this
second placode then plays in connection
with the auditory apparatus, it is frequently referred to as the auditory placode (Fig. 94, C l, already noted in the
account of an earlier stage (Camphenhout, ’35) . The roots of the VII and VIII
nerves are indistinguishable from one
another previous to the opening of the
mouth (9 mm.). '
Purely E flerent Nerves. — The III, IV,
and VI nerves are all motor ocular nerves
which innervate the muscles of the eye.
Their development is imperfectly known,
187
Fig. 95.—_-Transverse section
through 8.6 mm. larva of R.
escalenta, illustrating the relations of the sympathetic cord
and spinal nerve. From Kellicott (Chordate Development).
After Held.
a. Dorsal aorta, c. Spinal
cord. d. Dorsal (sensory, aEer
ent) root of spinal nerve. m.,
Myotorne. n. Notochord. r.
Ramus communicans. sc. Sympathetic cord. sg. Spinal ganglion. sn. Spinal nerve trunk. 11.’
Ventral (motor, efferent) root
of spinal nerve.
but they seem to arise from neuroblasts in the mid-brain and medulla.
.The III appears first, just before hatching, the others slightly later.
The Spinal Nerves.—The ganglia of the spinal nerves, unlike
those of the cranial nerves, arise entirely from the neural crests, no
placode elements in this case being involved. The division of the originally continuous crests of this region into the segments which eventu188 THE FROG: LATER OR LARVAL ‘DEVELOPMENT
ally become the ganglia is apparently conditioned, moreover, by the
previous segmentation of the myotomes (Lehman, ,2?! Detwilers ’37)Also if more or fewer myotomes are experimentally produced the related ganglia are correspondingly increased or decreased in number
(Detwiler, ’34-). From each crest segment, fibers grow inward and con
nect with the dorsal part of the cord. These are known as the dorsal
root: of the spinal nerves (Fig. 95). At the same time other fibers grow
outward to the skin, and other sensory organs; as in the head, all of
these ganglion fibers are afferent.
~ While this is occurring dorsally ventral nerve roots also arise (about 4mm.) . Each of these roots consists of a bundle of fibers (axones) originating from neuroblasts in the ventral part of the spinal cord. This has
. been confirmed experimentally by removing parts of the cord while leav
ing the crests, in which case the ventral roots are absent (Taylor, ’44) .
At or just beyond each dorsal root ganglion the fibers of the respec
tive ventral bundle mingle in a common sheath with the outgoing fibers
of the'ganglion. Thus, since the ventral root fibers are all efferent, each
'nerve sheath containing both sorts constitutes a mixed nerve (spinal
nerve trunk) as in the cases of a similar condition in the head. This
trunk soon divides into a dorsal and a ventral branch, each of which
now contains both afferent and eflerent fibers; the former pass to the
various sense organs and the latter to the muscles.
The problem of how these and other fibers are directed to their proper
destinations has long been of interest, and is not yet completely solved.
There does appear to be a tendency, however, for outgrowing nerves to
proceed toward certain kinds of tissue more than toward others. Thus
Detwiler (’36) has shown that whereas transplanted pieces of brain
failed to attract such nerves, transplanted limb, eye, and nasal placode
do so in the order indicated. Even so the attraction is apparently not
very specific, i.e., certain nerves are not inevitably attracted to their normal muscles, as shown by somewhat displacing the sources of the
nerves (Piatt on Amblystoma, ’4-0). The nature of such general attraction as there may be is not known, but may_ be tentatively assumed to be
both mechanical and chemical in character. Finally it may be noted
that there is also a question as to what causes more anterior parts of the
spinal cord to contain more nerve cells than the relatively caudal parts.
There has been some evidence that what a given segment contains is dependent to some extent on the character of the part anterior to it. Thus
if a piece of spinal cord were substituted for the medulla this might be
expected to lead to fewer cells and fibers in the cord posterior to the
ORGANS OF SPECIAL SENSE 189
implant. Such, however, seems not to be true in this case, thus suggesting, to a certain degree at least, an inherent developmental capacity in
various levels of the cord (Detwiler on Amblystoma, ’37).
The Sympathetic System. —- In the sympathetic system the neuroblasts have been shown to originate both from the neural crests and the
neural tube, while the sheath cells come entirely from the latter. At least
this has been demonstrated experimentally for Triton by replacing part '
of its neural tube by easily distinguishable material from Axolotl (Ra
audltory _ I
vesicle 4 Wm °
u‘.,;,‘|;, pigment layer < . “"4 <79“
of r ' ‘
lens _
rudiment P°"=l°|‘ 0'
 
oral "~ ~ ’ . : T
ev-«mm « 
Fig. 96.——Cross sections of 4 mm. stage of Frog embryo. A. Section through the
optic cups starting to form the vesicles. B. Section through the auditory vesicles and extreme anterior of the heart rudiment. This section also passes through
the pharyngeal region at the level of the third visceral or 1st hranchial arch.
ven, ’36), and it is probably true of other Amphihia. The cells of the
sympathetic system first appear, however, in small collections upon the
spinal nerves at about the level of the dorsal aorta, a position in which
they may be noted shortly before hatching. Presently they migrate to
the aorta, along each side of which they give rise to a sympathetic cord.
From these cords, nerve fibers later grow backto the spinal ganglia, as
the rami communicantes. Still other fibers proceed to the viscera, and
along these, cells migrate to form the various peripheral sympathetic
ganglia.
ORGANS OF SPECIAL SENSE
The Eye. —- When the rudiments of the eye were last considered the
optic stalks were just beginning to be defined as such, owing to a slight
constriction between the optic vesicles and the brain. This process is now
rapidly completed so that the stalks are clearly indicated. It is then evident that they do not join the vesicles exactly at the centers of the latter
but nearer to their ventral sides. There then begin certain changes ‘in
connection with the vesicles themselves as follows:
19o '_ THE FROG: LATER OR LARVAL DEVELOPMENT
The wall of each vesicle next to the ectoderm is flattened and then
pushed inward. By this process the cavity of the optic vesicle is obliterated, and at the same time a double-walled cup is formed, the optic
cup (Figs. 96, 97, 98). It must be noted, however, that the direction of
this imagination is not exactly horizontal. It begins rather in the ventrolateral region and proceeds obliquely upward. This fact, together with
T the original relation of the vesicle and
stalk, means that the latter will necessarily
be attached to the cup at its ventr-al edge.
The rim of the cup now grows outward,
particularly in its ventral and lateral regions, these being the regions which, as a
.result of the direction of invagination, are
further from the ectoderm. This outward
extension of the sides of the cup leaves between their ventral edges a slight fissure
extending inward to the optic stalk. This is
the choroid fissure, whose length is somewhat further increased by the continued
outgrowth of the sides of the cup. Furthermore, concurrent with this outgrowth the
entire rim begins to bend toward the center
of the cup’s aperture, thus obviously decreasing its diameter. This aperture,
Fig. 97.--Plastic figure of
hemiseoted optic vesicle, lens
and optic stalk of the Frog.
From Kellicott (Chardate
Development) .
f. Choroid—fissure. l. Lens.
pc. Posterior (Vitreous)
chamber of eye. pl. Outer or
pigmented layer of optic cup.
rl. Inner or retinal layer of optic cup. s. Optic stalk. v. Orig
which faces the ectoderm, is the pupil, from
whose ventral edge the choroid fissure runs
back to the optic stalk.
ma] cavity °f °Pfi° V‘i5i°1°' Meanwhile, about the time of hatching, a
thickened portion of the inner ectoderm on the wall of the head opposite the pupil becomes constricted off as a solid rounded mass of cells
(Fig. 98). This is sometimes, though erroneously, called the visual placode. It presently acquires a central cavity, which is soon obliterated,
however, by the thickening of the cells on the future retinal side. This
mass now moves in to the center of the pupil, and becomes the lens. The
invagination of the ectoderm to form the lens appears to be induced by
the adjacent optic vesicle (Beckwith, ’27), though the competence of
all ectoderm so to respond has been questioned. Thus, in this as in
some other cases, the ability of ectoderm to react specifically at a given
stage seems to depend upon its earlier subjection to another inductive
agent, e.g.,’ the mesentodenn (Liedke, ’51). On the other hand, under
ORGAN‘-5 OF SPECIAL SENSE 191
Fig. 98. — The development of the eye in the Urodele, Siredon pisciformis.
From Kellicott (Chordate Development). After Rab]. A. Of embryo with
about twenty-five pairs of somites, showing the thickening of the lens rudiment. B. Invagination of the lens and formation of the optic cup. C. Lens
separating from the superficial ectoderm in an embryo of about thirty-five
pairs of somites. D. Thickening of the inner wall of the lens. E. Shortly
before hatching; differentiation of the rods and cones in the retinal layer.
a. Anterior chamber of eye. c. Cavity of primary optic vesicle. co. Cornea. e. Ectoderm of head. f. Choroid fissure. i. Inner or retinal layer of
optic cup. ir. Rudiment of iris. Ic. Optic stalk. 1. Lens. 0. Outer or pigmented layer of optic cup. p. Posterior (vitreous) chamber of eye.
192 THE FROG: LATER OR LARVAL DEVELOPMENT
certain conditions it is known that if at the neural fold stage a lens has
been removed it can only be replaced by cells derived from the dorsal
rim of the iris (see below).
Shortly after hatching the cells in the walls of the optic cup begin to
differentiate. The inner wall thickens and develops into the retina, its
outermost. cells becoming the rods and cones. Its inner cells, i.e., those
toward its cavity, form neuroblasts which send axones over the inner
surface just beneath the thin internal limiting membrane, which is produced from fibers growing out from non-nervous cells deeper in the
retina. The axones, leaving the cup through the inner end of the choroid
fissure, grow within the substance of the ventral wall of the optic stalk
to the ‘brain, where those from opposite sides cross to form the optic
chiasma. The ventral wall of the stalk, thickened by its axones, soon
obliterates the stalk lumen, the other stalk cells disappear, and the
neural sheath is formed of connective tissue, the axones and sheath cells
together constituting the II or optic nerve. The outer wall of the cup
adjacent to the rods and cones develops pigment, and hence is called the
pigment layer of the retina.
Slightly before hatching the lips of the choroid fissure begin to fuse,
and shortly this fusion becomes complete everywhere except next to the
optic stalk, where the blood vessels and axones leave the cavity of the
cup. At the edge of the pupil the ‘closure is marked by a thickening,
the choroid knot, from which arise the cells of the iris. This closure of
the fissure is said not to occur in the absence of the lens (Beckwith, ’27) .
’The vitreous humor is formed in the cavity of the cup by cells budded
from the retinal wall and from the inner side of the lens. It is thus entirely ectodermal. The choroid coat of the eye is laid down outside the
pigmented layer, and outside of all is the tough sclerotic coat. Both the
choroid and sclerotic tissues are derived from mesenchyme. Opposite
the lens the ectoderm of the head becomes transparent, and, again with
the addition of mesenchyme, forms the cornea. The detailed development of the eye is not entirely completed until metamorphosis.
The Eat.
The Inner Ear or Membranous Labyrinth.-—Just before hatching
the superficial part of the auditory placode, i.e., the part not involved
in the formation of the VII and VIII nerve ganglia, moves in slightly
from the ectoderm. At the same time it invaginates to form a closed
membranous vesicle, the auditory sac or otocyst. By appropriate transplantations it was shown that the differentiation of this sac is induced
ORGANS OF SPECIAL SENSE
VIII‘
Fig. 99.—The development of the auditory organ in the Frog and
Toad. From Kellicott (Chordate Development). A, B, F. After
Krause. C, D, E. After Villy. A. Section through the auditory vesicle
of an embryo just beginning to elongate. B. Section through the
auditory vesicle that has very nearly separated from the superficial
ectoderm. C. Transverse section, somewhat oblique, through the
auditory organs of a 12 mm. R. temporaria. D. Slightly more advanced stage than C. E. Section through the auditory organs of a 25
mm. R. zemporaria. F. Membranous labyrinth of the Toad (Bufovulgaris).
a. Auditory sac. zztz. Anterior ampulla. ac. Anterior vertical semicircular canal. b. Pars basilaris. d. Dorsal outgrowth of primitive auditory vesicle (rudiment of endolymphatic duct). e. Endolymphatic
duct. g. Ganglion of auditory (VIII) nerve. hc. Horizontal semicircular canal. Z. Lagena or cochlea. pa. Posterior ampulla. pc. Posterior
vertical semicircular canal. 5. Saccule. ss. Sinus superior. u. Utricle.
VIII. Auditory nerve.
193
194 THE EROG: LATER OR LARVAL DEVELOPMENT
by the presence of the medulla, and also to some extent by the roof of
the archenteron. This seems to be true even when the medulla is from a
different species of Amphibian. As in the case of lens induction, however, it again appears that ectoderm near the normal site is more competent to respond in this manner than that from elsewhere (Albaum and
Nestler, ’37, and- Zwilling, ’4-1). From the dorsal wall of the otocyst a
small evagination now appears which is the rudiment of the endolymphatic duct (Fig. 99, A, B). An oblique partition then (10-12 mm.)
begins to grow across the cavity of the otocyst in such a way as to divide it into a lateral and ventral portion, the saccule, and an upper and
median portion, the utricle. These cavities remain connected by a small
poie in the membrane (Fig. 99, D). .
During the growth of the above partition there appear upon the inner surface of the wall of the utricular portion of the otocyst, two pairs
of ridges. One pair is vertical and anterior, the other horizontaland
lateral, upon the side nearest the ectoderm. Presently (15 ’mm.), there
is added another pair which is posterior and vertical. The edges of each
pair of ridges now fuse with one another along their entire length, thus
giving rise in each case to a tube open at each end into the cavity of the
utricle. The tubes thus formed are the rudiments of the three semi-circullzr canals. From the manner of their formation these tubes or canals
evidently lie upon the inside of the utricular wall. Shortly, however,
each canal pushes outward and presently becomes constricted away
from the wall of the utricle except at its ends. The canals which thus
come to lie outside of the utricle now continue to grow, and so reach the
adult condition. During this latter process, however, each canal acquires an enlargement at one of its ends termed an ampulla. These ampullae are not developed from the canals themselves, but are added to
them through a further constricting off of portions of the utricle
(Fig. 99, E, F). A
Meanwhile the saccule in the course of its separation from the utricle
has become the part of the otocyst which receives the endolymphatic
duct. The two ducts, one from each side of the head, then grow up over
the brain; during this process their ends become enlarged (at about 20
mm.) to form the endolymphatic sacs. By the time of metamorphosis,
these sacs have increased greatly in size, have become very vascular,
and fused with each other. In the adult they form a considerable vascular covering for the myelencephalon. It is also stated by Wilder
(’09) that in all the Anur-a an ‘outgrowth from each endolymphatic sac
extends down along the side of the dorsal nerve cord outside the dura
ORGANS OF SPECIAL SENSE 195
mater. Where each spinal nerve root emerges an extension from these
outgrowths also emerges, and forms asmall pocket partially wrapped
around the respective spinal ganglion. These pockets are filled with calcareous material, and it is this whitish substance seen through the pocket
wall that one observes when viewing the “ ganglia ” in a gross dissection
of the Frog.
In larvae of 15-20 mm. the saccule is also giving rise to two other
structures as follows: From its upper portion the lagena or cochlea
arises as a postero-ventral evagination, while a similar and slightly
more dorsal outpushing, in close connection with the first, constitutes
the basilar chamber (pars basilaris) (Fig. 99, F).
Sensory patches develop on the inside of the epithelial walls of the
utricle, saccule, cochlea, and ampullae, and these are connected with
branches of the auditory nerve which proceeds from its ganglion. The
. entire membranous labyrinth thus formed is eventually encased in car
tilage and bone arising from the surrounding mesenchyme. The casing
follows the contour of the membrane, and constitutes the auditory capsule. There is a slight space between the capsule and membrane, the
perilymphatic space, and this is filled with perilymphatic fluid.
At this point experimental procedures have again been applied which
show that not only is the membranous otocyst produced by induction,
but that it in turn induces the formation of the cartilaginous capsule
around it (Kaan, ’38). Apparently not quite any mesoderm is competent to react in this way, but at least that of the head region and some
of the somites will do so. Kaan also noted a reciprocal action in that a
normal capsule was necessary to induce the membranous otocyst to go on
and develop a normal membranous labyrinth. Thus we see a good illustration of the continuous actions and reactions in a developmental system that has once been set going. _
The Middle Ear. —This portion of the auditory organ develops
chiefly during and after metamorphosis, as follows: The vestigial visceral pouch between the mandibular and hyoid arches, i.e., the hyomantlibular, produces from its dorsal end a rod of cells with a terminal
knob. This rod grows out until the knob reaches a position between the
inner ear and the wall of the head. A cavity then develops in the knob
and in the rod of cells. The cavity in the knob is the tympanic cavity,
and that in the rod the Eustachian tube, which connects the cavity with
the pharynx. The tympanic cavity, or cavity of the middle ear, increases
in size until its outer wall fuses with the ectoderm. The membrane thus
formed is the tym panic membrane or ear drum, separating the tympanic
196 ‘THE FROG: LATER OR LARVAL DEVELOPMENT
cavity from the exterior. This membrane it may be noted has a special
histological character, and Hellf (’28) has proven that this Character is
induced by the presence of two pieces of cartilage. One is the annulus
tympanicus, a ring-shaped structure which surrounds the membrane at
-its periphery and supports it. The other will be indicated presently.
Hellf (’34)- has shown further that rings of cartilage cut from the supra
scapula have a slight tendency to produce changes in the ectoderm similar to those produced by the annulus tympanicus. He has also shown
that rings cut from the palato-quadrate cartilage (see account of skeleton) will act just as well as the annulus tympanicus itself. This last fact
is significant for the following reasons: In the lower Vertebrates the
palato-quadrate forms a part of the upper jaw, and it has long been suspected that a small part of it survives in the higher members of this
group as a bone of the middle ear. Such a hypothesis is obviously
strengthened by this observation of the similar peculiar inductive quali-
ties possessed by both palato-quadrate and annulus tympanicus.
Continuing with the history of the middle ear, we find that opposite
to the tympanic membrane the wall of the tympanic cavity contacts the
auditory capsule. Here there is an aperture in the latter, the fenestra
ovalis, opening into the perilymphatic space. In this aperture there develops a cartilaginous plug, -the operculum. Across the roof of the tympanic cavity there is also formed a cartilaginous rod connecting the
operculum with the tympanic membrane. It is the plectrum or columella,
and is thought to be a vestige of the upper part of the hyoid arch. It will
be recalled that the histological character of the tympanic membrane is
due to two pieces of cartilage one of which is the annulus tympanicus.
The other is the columella, without which the peculiar yellow fibers of
the membrane are not formed (Helff, ’31). Finally, at the close of metamorphosis, the columella separates from the dorsal wall of the tympanic
cavity, so that it stretches freely from the tympanic membrane to the
operculum. The columella and operculum then fuse, and the latter and
part of the former become ossiiied. Interestingly enough in the larvae of
some Frogs a temporary so-called bronchial columella connects the inner
ear and the lung (Witschi, ’55). This is suggestive of the ossicles connecting the air bladder and the inner ear in some Fish.
There is no outer ear, the tympanic membranes appearing on the outside of the F rog’s head. « _
The Olfactory Organ.—In the account of the external developments, we have already referred to the olfactory pits, which are evident,
»even in a 2.5 mm. larva. Each is situated slightly above and anterior to
ORGANS OF SPECIAL SENSE 197
Fig. 100.—-The development of the olfactory organ in R. fusca. From Kellicott
(Chordate Development). After Hinsberg. A, B, C. Sections through the olfactory
pit and organ of 5 mm., 6 mm., and 11 mm. larvae, respectively. D.” Medial View of
a model of the olfactory organ of a 31 mm. larva. The dotted line marks the limit
between the sensory and non-sensory portions of the epithelial lining of the olfactory
cavities.
c. Hypophysis. ch. Internal nares (choanae). d. Dorsal lumen. dc. Dorsal sac. en.
External nares. g. Olfactory pit. 1'. Cut edge of integument. in. Internal nares
(choanae). I. ‘Elongation toward the mouth. la. Lateral appendix. m. Mouth cavity.
n. Inner or nervous layer of ectoderm. ns. Part of chamber lined with non-sensory
epithelium. p. Olfactory placode. r. Ridge marking the limit between middle and
ventral chambers. s. Superficial layer of ectoderm. se. Part of the chamber lined
with sensory epithelium. st. Stomodaeum. t. Telencephalon. v. Thickened bands of
superficial ectoderm cells (possibly the vestige of a primitive sense organ). ,vc. Ventral sac. zig. Ventral nasal gland attached to Jacobson’s organ. x. Elevation~around
external nares. y. Canal leading to olfactory cavity. z. Fold around internal narial
opening.
I'_ 11 "
LA _
"y'TV'f  I r ..
1.5!’: . > _, !‘;"’)::
a. Auditory vesicle (in A, its rudiment). b. Basement membrane of epidermis. ch.
Notochord. g. Gut. gV. Trigeminal ganglion, of V cranial nerve. gVIIl. Acoustic
ganglion of VIII cranial nerve. gX. Vagus ganglion. gXl. Ganglion of lateral nerve
(branch of the vagus). i. Intersegmental thickenings of epidermis (ectoderrn). I.
Rudiment of lateral line nerve. lp. Lateral plate of mesoderm. my. Myotomes. 1:.
Inner or nervous layer of epidermis (ectoderm). nc. Nerve cord. 12. Pigment in epi
dermis. 5. Superficial layer of epidermis (ectoderm). si. Inner sheath cells of lateral
line organ. sn. Sensory cells of lateral line org'an. 50. Outer sheath cells, of lateral line
organ.
198
ORGANS OF SPECIAL SENSE 199
the side of the mouth. As these pits form, the superficial epithelium in
this case disappears, while the inner invaginating layer thickens. These
thickenings, which thus constitute the walls of the pits, are the olfactory
placodes already indicated (Figs. 83, 100). Compare with Figure 88 of
the exterior for general location.
A little after hatching there grows inward and downward from the
floor of each pit a solid rod of cells. These rods presently become connected with the buccal cavity just at the posterior limit of the stomodaeum, and in tadpoles of 12 mm., each has acquired a lumen. Their
openings into the cavity thus constitute the internal nares.
Somewhat later the olfactory lobes develop from the cerebrurn, as
indicated above. From each of these lobes, cells are then proliferated,
which mingle with other cells derived from the placodes. The two
strings of tissue thus constituted seem to become the sheaths of the I or
olfactory nerves. The actual fibers of these nerves, however, arise from
neuroblasts in the placodes, and grow backward to the lobes.
Meanwhile the pits are enlarging as the nasal cavities, and the remainder of the placode cells line them as the nasal epithelium. In the
course of growth the cavities are removed somewhat from the surface
' of the head, but remain connected with it by tubes whose outer open
ings form the external nares. Changes in the shape and the proportion
of the head alter from time to time the direction of the olfactory tracts.
Thus these tracts first become vertical rather than horizontal, and later
during metamorphosis develop a sharp flexure, due to the backward
movement of the internal nares. At this latter period, also, each of the
nasal cavities becomes greatly modified by complex evaginations and
foldings. Of the former the most prominent arises ventro-medially from
each cavity. The two bodies thus produced are the organs of Jacobson;
they later acquire glandular masses at their medial ends.
The Lateral Line Organs. —At about 4 mm., a small dorsolateral portion of the vagus ganglion of each side separates from the remainder and unites with a part of the most posterior or fourth placode.
The placode then grows backward through the epidermis until, just before hatching, it reaches the tip of the tail (Fig. 101). At intervals
along this cord there meanwhile arise groups of sensory cells which
push their way to the surface and develop hair-like processes. These
organs are innervated by a branch from the X nerve ganglion constituting the ramus lateralis (lateral line nerve). Other similar sensory organs develop in rows on the head,_and are innervated by branches of the
VII, IX, and X nerves. All these organs disappear at metamorphosis.
.4 7”"”'\
200 THE FROG: LATER on LARVAL DEVELOPMENT
INTERNAL DEVELOPMENT: THE ALIMENTARY CANAL
’ AND DERIVATIVES '
THE MOUTH
‘When last described, the endoderm in the antero-ventral part of the
pharyngeal region of the fore-gut had pushed out an evagination toward the ectoderm. The ectoderm had also “pitted in ” toward this
evagination to form the stomodaeum already noted. The stomodaeal
wall now meets and fuses with the endodermal wall in this region forming the oral plate or oral membrane (Fig. 90, A). A few days after
hatching (about 9 mm.), the oral plate becomes perforated, and henceforth the stomodaeal cavity or mouth communicates freely with the
pharynx. The margins of the small larval mouth are formed fundamentally of the mandibular ridges, i.e., the outer edges of the mandibular
arches. Outside of these ridges, however, the skin is drawn forward to
form the dorsal and ventral lips.
The dorsal lip of the larva soon develops three medially incomplete
rows of “teeth.” Each of these teeth is formed from a cornified ectodermal cell which is periodically replaced by a similar cell pushing up
from beneath. The ventral lip has four rows of such teeth; these rows,
however, are complete. At the base of each lip, parallel with the rows of
teeth, is a hardened ridge or jaw, also formed of cornified ectoderm.
At metamorphosis the horny teeth and jaws are lost, the adult jaws
being of course much wider than those of the larva and formed largely
of elements derived from the mandibular arch (Marshall). The permanent teeth occur only on the upper jaw, and are similar in their general
structure to mammalian teeth. The tongue develops at this time from a
proliferation of cells in the floor of the pharynx.
THE FORE-GUT AND ITS DERIVATIVES
The Visceral Arches and Pouches. —The beginnings of the first
three pairs of pouches arising as solid vertically elongated evaginations
of endoderm have already been indicated. The most anterior pair are
the rudiments of the hyomandibular pouches, whereas the second and
third pairs are the rudiments of the first and second branchial pouches.
There presently arise three more pairs of these solid rudiments, making
in all six pairs, one hyomandibular and five branchial, the last pair,
however, being mere vestiges. The condition of both pouches and arches
at hatching may be summed up in the following manner (Fig. 102):
THE FORE—GUT AND ITS DERIVATIVES
With the exception of the sixth and
last, the pbuch rudiments, as noted,
push out until they finally reach and
fuse with the ectoderm of the corresponding clefts. They thus divide the
mesoderm into the following bars or 3
visceral arches: (1) the mandibular
arch in front of the first or hyomandibular pouch; (2) the hyoid arch between
the hyomandibular pouch and the first
branchial pouch; (3) the first branchial
arch following the first branchial pouch;
(4) the second branchial arch following the second branchial pouch; (5) the
third branchial arch following the thirdbranchial pouch; (6) the fourth branchial arch, poorly defined, and following
the fourth branchial pouch. There are
thus six arches in all, beginning with
the mandibular arch in front of the hyomandibular pouch, and ending with the
fourth branchial arch in front of the
last vestigial fifth branchial pouch.
The further development of the gill
slits and gills has already been partially
described in the account of the exterior.
Nevertheless, it will be well at this point
to recall the main features indicated,
and to add certain details.
It will be remembered that, at about
the time the mouth opens, the pharynx
was said to be placed in communication
with the exterior by means of the. four
pairs of branchial clefts and pouches.
Fig. 102. — Diagram of a frontal
section of a Frog larva at the
time of hatching. From Kellicott
(Chordate Development). After
Marshall (modified). (Vertebrate
Embryology, courtesy of Putnam’s
Sons.)
c. Coelom. d.’ Pronephric duct.
F. Fore-brain. i. Infundibulum.
in. Intestine. n. Nephrostome. a.
Base of optic stalk. ol. Olfactory
pit (placocle). p. pharynx. t. Pronephric tubules. II. Hyoid arch.
III—VI. First to fourth branchial
arches. 1. Hyomandibular pouch.
2-6. First to fifth branchial
pouches.
The changes in the solid pouches which make this possible, however, remain -to be noted. Shortly after hatching, cavities appear in the first four
pairs of branchial pouches, and these cavities become continuous with
that of the pharynx. The cavities of the second and third pairs of branchial pouches then acquire openings to the outside by breaking through
the points of fusion between the invaginated ectoderm and the endoderm,
202 THE FROG: LATER OR LARVAL DEVELOPMENT
Fig. 103.—-Semi-diagrammatic sections through the branchial region of tadpoles
of R. esculenm, showing the development of the gills and the history of the aortic
arches. From Kellicott (Chordate Development). After Maurer. A. 4 mm. larva
showing the continuous first branchial aortic arch. B. 5 mm. larva showing the
anastomosis between the afferent and efferent portions of the aortic arch. C. 6
mm. larva with vascular loops in the external gills. D. 13 mm. larva. On the left
the opercular chamber is closed and the external gill is beginning to atrophy, while
on the right -this chamber is still open and the external gill well developed and
projecting through the opercular opening. E. 17 mm. larva. Vessels of the second
branchial arch. External gill represented only by a minute pigmented vestige.
a;. First branchial aortic arch. ab. Afferent branchial artery. ao. Root of lateral
dorsal aorta. au. Auditory organ. c. Conus arteriosus. e. Epithelioid body. eb. Efferent brarichial artery. eg. External gill. i. Internal (anterior) carotid artery. ig.
Internal gills. n. Nerve cord. 0. Operculum. p. Pharynx. pc. Pericardial cavity. r.
Gill rakers. 5. Oral “sucker.” v. Velar plate of floor, roof plates not visible here.
.1. Anastomosis between afierent and efferent branchial arteries.
and the cavities of the first and fourth presently do likewise. The two
hyomandibular pouches never develop any real cavities, however, and
the tissue which composes them later disappears. Since, likewise, there
are no cavities in the fifth vestigial branchial pouches, there are formed
altogether but four pairs of actual gill slits.
It has been noted that after the external gills are covered by the operTHE F ORE—GUT AND I'l‘S DERIVATIVES 203
culum they soon atrophy and are functionally replaced by the internal
gills. On the first three pairs of branchial arches these consist of a double row of filaments situated just ventral to those which are disappearing, but upon the posterior side of each arch, rather than upon its outer
face. There is also a single row of filaments upon the anterior side of
each of the fourth branchial arches. It is due to the fact that these new
gills are upon the sides of the arches instead of upon their outer faces
anterior pituitary "ab:
infundibulum
Vth nerve
internal carotid artery _ .  fragment of audimry capsule
‘ ' internal jugular vein
cular cartilage
endolymphatic lining
 
 
 
 
 
muscle
hypobranchial Plate palate-quadrate
velar plates
gill rakers
external
jugular vein  '~'
gill chamber
anterior fragment
of main coelom
Fig. 104. -— Cross section through the head of a late 10 mm. Frog larva in the region of parts of the 1st, 2nd, and 3rd hranchial arches. The arches are cut trans
versely because of their diagonal courses. Only the extreme anterior portions of the
auditory vesicles appear.
that they are termed internal. Nevertheless, they are still ectodermal
rather than endodermal, and project well into the branchial (opercular) chamber. Thus, save for the fact that they are covered by the operculurn, the term internal as applied to them is something of a misnomer.
Meanwhile during the development of these structures other changes
have been taking place, as follows: First, owing to the inequalities in
growth, there has been a considerable ventral shifting of the two branchial regions, accompanied by a marked dorso-ventral flattening of the
pharyngeal cavity, so that the extent of its strictly lateral walls is greatly
reduced. Thus instead of being situated on the sides of the pharynx the
gill arches soon come virtually to occupy its floor, upon_either side of
a median strip which is relatively wide anteriorly and narrow posteriorly. Hence the new gills do not project laterally, but tend to hang
204 THE FROG: LATER OR LARVAL DEVELOPMENT
Fig. 105.~———Diagrams of derivatives of visceral pouches
and arches in Frog. From
Kellicott (Chordate Develop
ment). After Maurer, with
Greil’s modification. A. Lateral view, Frog larva. B. Lateral view, after metamorphosis. C. Transverse section
through gill of Frog larva. D.
Transverse section through
gill region just after metamorphosis; gills still visible.‘
a. Afierent branchial arteries. c. Carotid gland. d. Dorsal gill remainder. e. Epithelioid bodies. pg. Internal gills.
In. Middle gill remainder. o.
Operculum. s. Suprapericardial body. t. Thyroid bod . th.
Thymus bodies. 11. Ventral gill
remainder. I—IV. Visceral
arches. I. Mandibular arch.
II. Hyoid arch. IIl~VI. 1st to
4th branchial arches. 1—.6. Visceral pouches. (1. Hyomandibular pouch. 2-6. 1st to 5th
branchial pouches).
downward into the opercular chamber
(Fig. 104). Furthermore, the direction of
the arches is not at right angles to the long
axis of the pharyngeal floor. Instead they
run diagonally backwards and outwards
from the somewhat triangularly shaped
median strip to the sides. From the borders
of this strip which run almost at right
angles to the gill arches, flaps of tissue now
grow postero-laterally so as to cover these
arches at their inner and more anterior
ends. The two flaps, moreover, become continuous with one another at their posterior
and median extremities, so that actually
only a single V shaped flap exists, whose
posteriorly directed apex is attached to,
and overlaps, the narrowest region of the
median strip-. At the same time on each side
a somewhat lesser flap develops from the
lateral and dorsal wall of the pharynx
along a diagonal line parallel with, but
slightly posterior to, the respective side of
the flap arising _from the floor. These dorsolateral flaps then grow anteriorly, medially
and slightly downward, and because of the
present close approximation of the pharyngeal floor and roof, they almost meet the
lateral portions of the outgrowth from the
former. The single ventral, and two dorsalateral flaps, thus. indicated are termed
velar plates, and their arrangement is obviously such that only a narrow slit on
either side leads from the pharynx to the
gill chamber. It is these plates, together
"with toothlike processes on the inner sides
of the gill arches, called gill rakers, which
tend to prevent the escape of food, while
allowing the free passage of water. Finally
at the time of metamorphosis the gill
pouches and the gill cavity are filled by
THE FORE——GUT AND ITS DERIVATIVES 205
proliferated cells, while the mass thus formed is later absorbed leaving
the gill slits closed.
Structures Derived from Vestiges
of the Gill Pouches.——Just before
hatching, proliferations of cells occur
from the dorsal ends of the hyomandibular and first branchial pouches. Those
from the hyomandibular pouch presently
disappear, but those from each of the first
branchial pouches form a cell mass. These
separate from the pouches (about 12
mm.), and eventually take up their position back of the auditory capsules near
the surface of the head. They are the thymus bodies (Figs. 105, 106).
From the ventral ends of the first pair
of branchial pouches there occurs, at
about the 9-10 mm. stage, a proliferation
of cells. These cells, together with the
anastomosis of the proximal ends of the
Fig. '106.—Diagram of the
branchial pouch derivatives in
afferent and efferent blood vessels of the
first branchial arch (see below) form the
so called carotid glands. Though long
usage has apparently firmly fixed the title
of gland upon these structures, they are
not glandular in histological appearance
or in function. They consist rather of a
spongy network which. performs an im
‘VI. First to
the Frog. From Kellicott (Chordate Development). After Maurer, with Greil’s modification.
cg. Carotid gland. e1, e2, ea.
Epithelioid bodies. th. Thyroid
body. lml, tmz, Thymus bodies.
ub. Ultimobranchial body. Isixth visceral
pouches (I. Hyomandihular II~
VI. First to fifth branchial
pouches).
portant service in helping to secure a rela
tively aerated blood supply for the internal carotid artery of the adult
Frog. While the ventral ends of the first branchial pouches thus help to
form the carotid glands, cells from the ventral ends of the second and
third branchial pouches give rise to what are known as the epithelioid
bodies.
The fifth pair of branchial pouches never actually develop as such but
become mere masses of tissue known as the ultimobranchial bodies
(suprapericardial) .
The Thyroid.-—This organ appears before hatching as a median
longitudinal evagination from the floor of the pharynx in the form of
a solid rod. Later (about 10 mm.), this separates entirely from the phar206 THE FROG: LATER 011 LARVAL DEVELOPMENT
ynx, and divides into two lateral parts which eventually become vascular.
The Lungs.——They appear just after hatching as a pair of solid
posteriorly directed proliferations from the ventral side of the pharynx
just back of the rudiment of the heart. The pharynx at this point is later
depressed, and partially constricted off from the part above it as the
larynx. The opening left between the pharynx and larynx is the gloztis
(Fig. 90). The lungs soon acquire cavities, and as they grow, become
spongy and vascular. Part of their tissue is derived from the splanchnic
mesoderm, only the inner lining being endodermal.
In connection with the origin of these organs it may be noted that
there have been two general theories concerning their phylogenetic
history. One school has regarded the lungs as coming from a modified
swim bladder, while the other has considered them as developments of
what were once a seventh pair of gill pouches. The latter notion at least
has the merit of preserving a continuity of function in the forerunner
of the respiratory organs of air breathing Vertebrates.
Further Development of Liver. —- The liver rudiment has already
' been noted as a small endodermal diverticulum extending back slightly,
beneath the yolk mass. The anterior wall of this diverticulum becomes
folded and thickened, partly by the addition of scattered mesoderm and
yolk cells (Fig. 90). This is the liver proper, the posterior part of the
original outgrowth becoming partially constricted away from it as the
gall bladder. The original connection with the fore-gut remains as
the bile duct. These organs become well developed during the larval
stage.
The Pancreas. —— At the posterior margin of the opening of the bile
duct into the fore-gut, a pair of outgrowths arise connected with the
gut by a single piece of tissue, the future pancreatic duct. The free ends
of these outgrowths then grow forward and fuse in front of the bile
duct. Later they are joined by a mass of tissue which originated from
the dorsal wall of the gut, and the three elements thus fused constitute
the pancreas. Eventually the pancreatic duct comes to open into the
bile duct very near to the point where the latter joins the gut, instead of
directly into the gut itself. _
With respect to the histogenesis of this organ, it appears that the
islets of Langerhans in many species of the Frog at least, arise first
from the endodermal cells of the primitive pancreatic anlage. Later
these are added to by cells from the ductules. During metamorphosis
some of the acinous cells degenerate, while the remainder persist as the
THE FORE—GUT AND ITS DERIVATIVES 207
cells of the pancreatic tubules. The islet cells, on the other hand, become
more aggregated, and develop two characteristic types with respect to
staining capacity (lanes, ’38) .
The Esophagus and Stomach. — Shortly subsequent to hatching,
the portion of the fore-gut between the future glottis and the opening of
the bile duct elongates, and the anterior part of it becomes the esophagus. For a brief time the aperture between the latter and the pharynx is
closed, but reappears at about the time the mouth opens. The posterior
part of the above fore-gut region dilates slightly and assumes a transverse position as the stomach. This organ remains inconspicuous, however, until the time of metamorphosis, when it enlarges somewhat.
THE MID-GUT
The mid—gut is that portion of the archenteron lying above the large
yolk mass at the time of hatching. After hatching, the yolk, and some of
the cells of its floor are rapidly absorbed, and it begins to elongate. The
front portion extends across the body in the form of a loop, the duodenum, which with the remainder is soon thrown into a double spiral.
The coils of this spiral have a total length about nine times that of
the body, but this is shortened about one third during metamorphosis.
THE HIND—GUT
The Rectum. ——This terminal part of the gut originates with a rela
tively slight amount of growth from the small portion of the archenteron remaining between the yolk mass and the posterior body wall. It
will be remembered that the endoderm of this region had come into
contact with the ectoderm which had become invaginated to form the
proctodaeum. About a week before hatching a perforation occurs at the
point- of contact forming the anus, while the rectum itself becomes
slightly dilated. In this connection it is of interest to note that the proctodaeal portion of the blastopore which in the Frog closes with the rest
of this orifice, and later reopens, in the Salamander always remains
open. Thus the temporary closure in the former animal is probably a
secondary or non-primitive characteristic.
The Postanal Gut.——As the tail region develops, the notochord
‘and nerve cord extend into it, but since the proctodaeal region does not
move backward, the neurenteric canal is drawn out into a small tube‘
beneath the posterior end of the notochord. Somewhat before hatching
it breaks away from the neural tube and persists for a brief period as
the postanal gut.
208‘ THE FROG: LATER OR LARVAL DEVELOPMENT
The Cloaca and Urinary B1adder.—The general region where
the endoderm of the rectum joins the ectoderm of the proctodaeum constitutes a chamber called the cloaca.‘It has been said that the cloaca. is
in fact all ectodermal and therefore proctodaeal, but this seems to the
writer highly doubtful and extremely difficult, if not impossible, to
prove. The reason for this doubt is that the pigment which at first marks
the ectodermal cells, later becomes rather diffused, and the exact boundary of the original fusion of rectum and proctodaeum is obliterated.
At all events the point at which the rectum may be judged to end, i.e.,
to open into the cloaca, is technically the anus. The dorsal walls of the
cloacal chamber also receive the urinogenital ducts. Finally at metamorphosis the ventral part of the cloaca gives rise to an anteriorly directed outgrowth within. the body cavity; this becomes the urinary
bladder. In the higher animals this bladder is endodermal, and although
as indicated above it is impossible to be certain, it seems highly probable that it is so here. One difference between Amphibians and some
of the higher forms which is evident, however, is the fact that in the
Frog and its relatives, as noted, the above ducts do not open into this
bladder, but into the dorsal wall of the cloaca.
INTERNAL DEVELOPMENT: THE FURTHER DEVELOPMENT
OF THE NOTOCHORD AND MESODERM
THE NOTOCHORD
When last indicated the notochord was merely a rod of undiHerentiated cells with a considerable curvature at its anterior end to conform
to the cranial flexure of the brain. By the 4« mm. stage, however, the
cells of this rod have become vacuolated, intercellular vacuoles have
also appeared, and the anterior curvature so far as the rod is concerned
has almost vanished (Fig. 89). At the same time around the notochord
there presently develop two sheaths. The outermost, known as the primary or elastic sheath, is formed from the most superficial chorda cells.
The secondary or fibrous sheath lies within the latter and is formed of
the chorda epithelium. ' '
THE SOMITES '
I When last considered, the segmental plates had divided into four
pairs of somltes. This process continues posteriorly until there are thirteen such pairs, extending from just back of the auditory capsules to the
THE SOMITES 209
base of the tail. Within the latter organ the number is much larger and
somewhat variable. Thus in a 5.5 mm. larva there may be all told as
many as forty-five. Sometime after hatching, however, the first two pairs
disappear, and those in the tail are of course all lost during metamorphosis; there thus remain eleven well-defined somites in the body region.
Meanwhile, as these somites are formed they have been undergoing certain changes, as follows:
Each somite it will be recalled consists of an outer layer of cells
called the cutis plate, and an inner larger mass, the myotome. From the
inner and ventral edges of the myotome‘. (about 5 mm.), loose sclerot0nzal cells are proliferated (Fig. 86). "these cells then migrate medially
and dorsally between the rows of myotomes on the one hand, and the
notochord and nerve cord on the other. Eventually they thus form a
layer about the latter structures known as the skeletogenous sheath.
This ultimately (see below) gives rise to the cartilage and finally the
bone which forms the centra of the vertebrae together with their transverse processes and neural arches. Thereaare nine vertebrae thus formed
in such a way that they alternate with the myotomal elements of the
somites. The skeletogenous elements of the last two of the eleven somites
have a somewhat dilierent history, as will be indicated later.
At about the same time that the sclerotomal tissue is being prolifer
, ated, there are developing, within the myotomes, muscle fibrillae, which
are to form the muscles of the back. Also from the outer ventral edges
of the myotomes and from the ventral edges of the cutis plates or dermatomes, outgrowths extend down next to the ectodermal wall. These are
to form the ventral body musculature, and in the region of the limbs,
their musculature as well. The main part of each cutis plate breaks up
and some of the cells from these plates form the dermal layer of the
dorsal region, while others migrate between the myotomes to form connective tissue. It would appear that the dermis of the ventral regions is
not derived from the dermatomes at all, but from part of the somatopleure, as has been demonstrated for the Chick (see below). Partial
continuation for this View has been furnished for the Amphibia by the
e:~;perime.nts of Detwiler ("37) already cited. He has shown that although absence of somites ( including the dermatome) prevents spinal
ganglion formation, the dermis of the operated side is present as usual.
It might also be noted here that virtually all, if not all, pigment in the
Amphibia is ectodermal in origin, that of the later stages coming mainly
from the neural crests. This is true not only for pigment in the epider
~mis, but for that in the dermis and viscera as well (Dushane, ’38).
210 THE FROG: LATER OR LARVAL DEVELOPMENT
Finally, as indicated above, the mesoderm in the region where the
segmental plate separates from the lateral plate constitutes the nephrotome, and is concerned with the formation of the excretory system. This
will be described later.
THE GENERAL COELOM
The beginning of the coelomic spaces in the two lateral plates has already been described. These spaces continue to extend downward, until
in a short time they meet one another beneath the gut and fuse. Thus in
the trunk region, the coelom or splanchnocoel becomes continuous ventrally from one side of the embryo to the other.
Dorsally, the lateral plates of mesoderm on each side press up and
in, between the dorsal wall of the gut and the notochord, until they
meet. The splits in these plates then follow, but never quite reach each
other, and hence the splanchnocoel never becomes continuous dorsally;
there is always a thin but double-walled sheet of cells separating the
right and left cavities. This is the dorsal mesentery. The gut as it develops is therefore slung from the dorsal wall by this mesentery, and completely encased in the splanchnic mesoderm.
INTERNAL DEVELOPMENT: THE CIRCULATORY SYSTEM
THE HEART AND PERICARDIAL CAVITY
The Primitive Cardiac Tube. —— It will be recalled that when last
mentioned the heart consisted merely of a few scattered endothelial
cells lying between the endodermal floor of the pharynx and the mesoderm. It will also be remembered that upon either side of the mid-line
this mesoderm had developed within itself a space which was designated
as a rudiment of the pericardial cavity (Fig. 85, C). These spaces now
enlarge, and the mesoderm forming their uppermost walls presses up
and around each side of the above mentioned endothelial cells so as to
separate them from the overlying pharynx. Meantime these cells have
become arranged in the form of two parallel tubes (Fig. 107, A) , which
very shortly become more or less completely fused into a single tube
(Fig. 107, B) extending throughout the region. Presently the in-pushing
mesoderm from either side meets and fuses above this tube, so as entirely to surround it (3-6 mm), (Fig. 107, B, C). The latter with its
covering now represents the complete rudiment of the heart. The endothelial portion, as noted, forms its lining, the en.docara'ium, while the
THE HEART AND PERICARDIAL CAVITY 211
mesodermal envelope gives rise to the muscular wall, or myocardium,
and the close fitting covering of the latter, the visceral pericardium.
From the method of its formation, it is evident that this tubular heart
will at first be attached to the walls of its pericardial cavity by both a
dorsal and ventral sheet of mesodermal epithelium, or mesocardium.
The dorsal sheet was formed like that which suspends the gut, by the fu
Fig. 107.—— Sections showing the formation of the heart in the Frog. From Kellicott (Chordate Development). A. Section through pharyngeal region of R. temporaria. After Brachet. B, C. Sections through the same region in older embryos of
the smaller Frog, R. sylvatica.‘ A. 3.2 mm. embryo. Endothelial cells becoming arranged in the form of a double tube. B. Embryo of about 3 mm. C. Embryo of 5—6
mm. The single heart tube established; dorsal mesocardium still present.
(1721. Dorsal rnesocardium. e. Cardiac endothelial cells. en. Endoderm. g. Wall of
gut (pharynx). p. Pericardial cavity. so. Somatic layer of mesoderm (future parietal wall of pericardial cavity). sp. Splanchnic layer of mesoderm (future myocardium plus visceral wall of pericardial cavity).
sion of the sheets of mesoderm pushing in from each side. The ventral
sheet, on the other hand, has existed from the start as the median strip
separating the two pericardial rudiments. Thus the pericardial space remains temporarily divided along this middle line. Meantime, as indicated above, the lateral coelomic spaces in the trunk region have
extended ventrally, and now each side of the pericardial cavity communicates posteriorly with these spaces. The next step involves the entire disappearance of the ventral mesocardium, followed very soon by the
disappearance of the dorsal mesocardium also, except at its anterior and
posterior ends.
At this point it is worth pointing out that all Vertebrate hearts develop in essentially the same manner, except for some of the later de-V
212 THE FROG: LATER OR LARVAL DEVELOPMENT
tails involving the development of septa and orifices. That is, they all
start with a pair of straight tubes which shortly fuse into one, as has
been described, and this tube then develops in the manner about to be
indicated to arrive at the adult condition. Since this is true it would he
 
 
   
 
 
'"  truncus arteriosus "umus
arteriosus
_ bulbus
ventricular
P°"tl°" ventricular
portion
   
snino-atrial
portion
.. SIl'lUS venosus . ii -Ventride
DORSAL DORSAL VENTRAL
A B C
sinus venosus atrium sinus venosus atrium truncus
ventricular portion  l l
 
   
 
.1 truncus  - - _
bulbus  bulbus
 
sino- atrial i truncus
. t ' l
portion an°"°s"s Egritirciiiu ar -  I ventricle
RIGHT SIDE RIGHT SIDE RIGHT SIDE
sinus venosus /anterior vena cava
   
atrium .
 
truncus
RtGHT SIDE VF-l§ITRAL
Fig. 108.—Stages in the development of a Ve1'tch1'ato heart. These figures are
primarily of the Frog heart, but would apply almost equally well to that of the
Chick or Mammal (see text). The earliest stage is /1, and that of an essentially
adult heart is D. There are two views of each stage as indicated on the figure.
well for the student to follow the ensuing
be sure that it is clearly understood.
As the already-mentioned mesocardia disappear, the tubular heart be
gins to increase in length, and hy so doing becomes twisted in the fol
lowing manner. The straight tube first develops a marked bend to the
right (Fig. 108, Al. The broad apex of th
posteriorly and slightly to the left. Up
description carefully, and
e bend then moves ventrally,
on completion of this movement
THE HEART AND PERICARDIAL CAVITY 213
we find that what amounts to a loop has been thrown into the originally
straight tube (Fig. 108, 1?). The posterior limb of this loop extends
ventrally and then curves outward to the right to form the wide apex,
From the latter the ascending limb proceeds dorsally, slightly anteriorly
and leftward into the median plane. Thus the two ends of the loop, an.
terior and posterior, are still in essentially the same straight line. An.
teriorly the ascending limb of the tube divides at its upper extremity
into certain vessels which pass dorsally into the visceral arches. These
will be described presently. At the posterior end, on the other hand, the
tube comes into immediate and close contact with the anterior surface
of the yolk mass which is in process of developing into the liver (Fig.
90, A). In connection with the latter certain vessels are forming which
will also be discussed more fully below.
It is now possible to indicate how the parts of this twisted tube give
rise to- the adult structures for which they are destined. As will imme~
diately become apparent, not all of them belong to the heart proper.
Nevertheless, because of their very close connection and simultaneous
development it is convenient to describe them together.
Sinus Venosus Vitelline Veins and Atria. ——Beginning at the
posterior end it has just been noted that the heart tube abuts against
the developing liver. Forming on the antero-ventral surface of the latter organ are two vessels, the vitelline veins, which become continuous
antero-dorsally with the posterior end of the heart tube. The fused region of their entrance to the tube later becomes dilated to form the
sinus venosus, while just anterior to this another enlargement occurs.
This latter enlargement is the atrial portion of the heart proper, and
presently there grows down from its roof :1 sheet of tissue dividing it
into right and left chambers.“ These chambers are the atria of the Frog
heart, and the sheet of tissue is the inter-atrial septum. It is further to be
There has been considerable confusion over the definition of the terms auricle
and atrium. According to the virtually universal usage of American medical men
in human anatomy the two upper chambers of the heart are “ atria” which have
earlike appendages or “ auricles ” attached to them. In many of the lower animals
including the Frog, however, there are no such appendages, i.e., there are in the
strict sense no auricles, only atria. It should be noted that among British medical
men the term auricle is frequently more loosely used to include all of each upper
chamber, though they do sometimes refer to the auricular appendages of the atria.
Also among zoologists the terms auricle and atrium are used as essentially synony
mous. Nevertheless, there is good historical and logical precedent for the strict definition of these terms adopted by American human anatomists. Hence, sincemany
students of embryology are sure to he premedics, the present writer intends to try
to save them future confusion by adherence to the more precise definition of
atrium and auricle throughout this text. ’
is this region which sets the pace for the
214 THE FROG: LATER OR LARVAL DEVELOPMENT
noted in this connection that the growth of this septum occurs in such a
manner that the sinus venosus comes to open into the right atrium. The
left atrium, on the other hand, eventually receives the pulmonary veins
(see below).
The Ventricles, Bulbus and Truncus Arteriosus. —— While
these events are taking place in the postero-dorsal extremity (atr
gion) of the looped tube, the curved apex of this tube connecti
descending limbs is expanding. As it does so, it incorporates into itself
the ventral part of the descending limb not involved in forming the
atria. This expanded portion of the tube constitutes the ventricle. In the
case of the Frog, of course, it contains no dividing septum. Its wall, nevertheless, becomes greatly thickened by the development of muscular
tissue, some fibers of which traverse the ventricular chamber itself forming partial partitions. These, in connection with other factors, are said
to help prevent the mixture of the two classes of blood received from
the respective atria (Fig. 108, C).
Later, as a result of a rotation of the whole structure about an axis
passing transversely between the atria and ventricle, the ventricle assumes its definitive posterior position. Finally the ascending limb of
the original tube, also as a consequence of this rotation, comes to run
more or less anteriorly from the ventricle across the ventral side of the
atria. It is not strictly part of the heart, but constitutes a thick walled
vessel with two enlargements in it. The one nearer the vent
bulbus, and the more distal less prominent one the truncu
(Fig. 108, D). Within the latter extendin
ial re
ricle is the
5 arteriosus
g throughout its length there
With respect to the initiation of functioning of the parts of the heart
tube the following may be said: pulsation in all Vertebrate hearts so
far as known begins long before any innervation, it being the nature of
this particular type of muscle to contract rhythmically.
ave moving from
This point is shifted backnd as might be expected it
rate of heat. This has been
the posterior point of initiation anteriorly.
ward as the length oflthe tube increases, a
-sq
BLOOD VESSELS AND CORPUSCLES 215
clearly demonstrated for Arnblystoma by Copenhaver (’39, ’45) by cut.
ting the tube at various places and times so as to show the inherent
rates of the separated parts. By such experiments he has made clear that
the posterior part of the tube, i.e., the region where the pulsation ultimately starts has a faster inherent rate than more anterior parts. Not
only is this true, but interchange of posterior parts between species having different heart rates causes the imposition of the rate of the transplanted posterior part upon the anterior part of the host heart with
which it has fused. In view of these facts it is not surprising to= find that
in the completed heart the beat is initiated and its rate determined in
the sinus, which arises from the posterior end of the original tube.
However, in the adult organ the situation is altered to this extent:
though the beat is always initiated in the sinus, its inherent rate is modified by nervous control to meet the demands of changing conditions.
Isolation of the Pericardial Cavity.—~l\/lost of the above processes take place in the deyeloprnent of the heart before or shortly after
the tadpole hatches (7-12 mm.). One step which remains until considerably later, however,  the separation of the pericardial cavity from
the general coelom which lies posterior to it. This is accomplished by
the outgrowth of folds of peritoneum (epithelial lining of the coelom)
from the lateral coeloznic walls, in company with the cluctus Cuvieri
(see below). The partial transverse wall thus formed is then augmented
medially by the splitting off of peritoneal tissue from the anterior face
of the liver. The entire partition is not completed until metamorphosis,
when it is known as the septum z‘.ran.sversum.
DEVELOPMENT OF BLOOD VESSELS AND CORPUSCLES
The blood vessels develop out of the rnescnchyme and the splanchnic
rnesoderm by a rearrangement and differentiation of the cells to form a
flat endotheliurn which constitutes the inner lining of all the vessels. It
is entirely similar to, and continuous with, the endothelial lining (endocardium) of the heart which has just been described (Figs. 89 and 107) .
The muscular and connective tissue coats are likewise differentiated
from mesoderm and added later, the muscle being much more abundant
in the arteries and the connective tissue in the veins. In connection with
these processes it should be emphasized that the early endothelial tubes
do not originate as such at some one place, e.g., the heart, and simply
grow outward from there as immediately continuous structures. They
rather appear as disconnected sections or vesicles which grow toward
each other until they are united. However, though it is true that the ves216 THE FROG: LATER OR LARVAL DEVELOPMENT
sels do not originate at one point, the procedures indicated do occur
first in the more proximal regions of the embryo, and particularly in
the vicinity of the heart. It is important to bear these facts in mind
whenever the development of blood vessels is referred to, not only in the
Frog, but also in any other Vertebrate for the method of formation is
the same in all.
The corpuscles are formed chiefly from patches of splanchnic mesoderm on the ventral side of the yolk mass, from whence they find their
way into the developing vessels. These patches are called blood islands.
It appears, however, that the corpuscles produced by the islands do not
last long, but are replaced by corpuscles from other blood-forming centers, particularly the spleen under stimulation by the liver (Goss, ’28;
Cameron, ’4-1; Copenhaver, ’43). In Salamanders a diffusible substance
from the endoderm seems to aid haemoglobin formation, at least in the
island corpuscles (Finnegan, ’53).
The Arterial System. —-A few days before hatching (4~5 111311.},
the dorsal aorta develops as stated, just above the gut, and in the pharyngeal region is divided into two lateral dorsal or suprabra/Iclzial aorzae.
The Visceral Arch and Gill Circulation. —— At about the same time the
blood vessels of the visceral arches also develop in the following manner:
dorsally with the corresponding suprabranchial aorta. Presently similar
connections are also established by the other two pairs. Thus complete
loops or aortic arc/Les are formed in all but the mandibular and hyoid
arches. Here no real aortic arches ever develop, though certain transitory vessels appear for a time.
As the external gills now begin to form, the following changes occur
in the first, second, and third hranchial arches: A second looped vessel
appears external to the primary aortic (branchial) vessel, the new vessel being attached to the primary vessel dorsally and ventrally (Figs.
103, C; 109, B). This new loop now extends out into the tissue of the
corresponding external gill, where the two sides of the loop are con
loop and its capillaries. The greater part of the blood, however, takes
the latter course. Hence it passes out from the truncus arteriosus along
the more ventral and external side of the gill loop, which is therefore
aflerent, and back along the dorsal side, which is therefore eflerent.
BLOOD VESSELS AND CORPUSCLES 217
When the external gills disappear, the ventral limb of the external
loop (i.e., the section ab) remains to form the afierent vessel of the in.
ternal gills (Figs. 103; 109). The efferent vessel, with which it then beComes connected by capillaries, is the more ventral part of the original
primary loop (section x) . iV'leanwhile, this primary loop breaks its
main ventral connection at the point where the external loop branched
off from it. Thus during the remainder of larval life all the blood in the
arches has to go through the internal gill capillaries. Since the fourth
Fig. 109. — Diagrams of the second aortic arch of the adult
Frog and tadpole. From Kellicott tChar(late Development).
After .\laurer. A. The continuous second (main systemic
aortic arch of the adult; showing the parts corresponding
with the larval vessels, 8. External gill and associated vessels in young tadpole. C. Internal gill and associated vessels
in the tadpole after the disappearance of the external gills.
ab. Afferent hranchial artery. e. Epithelioid body. eb. Efferent hranchial artery. eg. External gill. ig. Internal gill.
o. Operculum. .r. Direct connection hetween afferent and
efferent" hranchial arteries, i.e., ventral part of primary loop.
arch never develops external gills, the vessels related to these particular
structures never appear in it. Otherwise the history of the blood system
within this arch is essentially similar to that just described in those anterior to it.
Changes in. Gill Circulation at Metamorphosis. ———The gills and their
capillaries, including the major part of the afferent or external loops,
gradually degenerate. At the same time the original primary loop vessels re-establish their ventral connections with the proximal parts of the
afferent gill vessels. The primary vessels in the four pairs of branchial
arches then undergo the following changes.“ The vessels of the first pair
4 It is to be noted in this connection that at least in some Frogs, as indicated in
a preceding paragraph, no genuine aortic loops are formed in the mandibular and
hyoid arches (Marshall and Bles on R. temporaria). In many other Vertebrates or
their embryos, however (see the Chick), complete arteries do exist in these arches
at one time or another, as well as in the four branchial arches. Thus in such cases
the third aortic loop of the entire series is homologous with that in the first branchial arch referred to in the following account.
218 THE FROG: LATER OR LARVAL DEVELOPMENT
VI l
VI V‘ IV 111
     
Fig. 110.—Diagrams of the branchial blood vessels
in Frog larvae. From Kellicott (C/zorrlate Development) . After Marshall. ( Vertebrate Embryology, courtesy of Putuam’s Sons.) /1. A 7 mm. larva (shortly
after hatching). The vessels supplying the external
gills are removed, only their roots being indicated.
B. A 12 mm. tadpole. The vascular loops in the gills
are omitted.
rz. Atrium. ac. Anterior (internal) carotid artery.
am. Anterior commissural artery. eo. Dorsal aorta. (rp.
Anterior palatine artery. b. Basilar artery. c. Anterior
cerebral artery. cg. Carotid gland. cv. Posterior (inferior) vena cava. dC. Ductus Cuvieri. g. Pronephric
glomus. h. Hepatic veins. /Ly. Hyoidean vein. 1. Lingual artery. in. Mandibular vein. 1). Pulmonary artery.
ph. Pharyngeal artery. pm. Origin of posterior commissural artery. pp. Posterior palatine artery. pv. Pulmonary vein. s. Vein of oral sucker. t. Truncus arteriosus. u. Cutaneous artery. 1:. Ventricle. I~~4. First
to fourth afferent branchial arteries. 1, II. Efferent arteries of the mandibular and hyoid arches. II1'—VI.
First to fourth efferent brauchial arteries. VI I. Lacunar vessel of the fourth branchial arch.
BLOOD VESSELS AND CORPUSCLES 219
oi branchial arches retain their dorsal connections with the respective
dorsal aortae, and with them form the proximal ends of the internal
carotids which run forward into the head (Fig. 110). The vessels of the
same arches are joined at their ventral ends by the external carotids or
lingual arteries which have grown back from the floor of the mouth.
Almost at the junction of the external and internal carotids on each
side, the latter develops an enlargement
consisting of spongy tissue. This is the carotid gland already referred to. It arises
from a slight anastomosis between the
proximal ends of the afferent and efferent
aortic vessels of the first branchial arch,
with the addition of some epithelial cells
from the ventral end of the first branchial
pouch.
The vessels of the second pair of branchial arches also retain their dorsal connections with the lateral dorsal aortae,
while the latter disappear anteriorly be- Fig. 111.——Diagram of the
tween this point and the first branchial “mic ‘“°h°5 ‘md ‘heir Chief
arches (disappearance not shown in Fig. branches 1" an adult Frog110). Thus the vessels of the second branchial arches become the main 3 /slemic arteries. The vessels of the third branchial
arches disappear. The vessels of the fourth
From Kellicott (Chordate Development). Ventral view.
an. Dorsal aorta. c. Carotid
artery. cg. Carotid gland. cu.
Cutaneous artery. 1. Lingual
artery. p. Pulmonary artery. .9.
Systemic arch. sc. Subclavian
branchial arches; having already given off ‘m°"V' " T““‘°“5 ‘“‘e‘i°5“5'
_ v. Vertebral artery.
branches to the lungs and skin, become the
pulmocutaneous arteries. The portion of each of these vessels connecting
it with the respective lateral aorta disappears after metamorphosis. Thus
all the blood going to these aortic arches must henceforth pass to the
lungs or skin.
It may be noted that in most of the air-breathing Vertebrates not all
of the section of the fourth arch between the origin of the pulmo-cutaneous artery and the dorsal aorta, known as the ductus Botalli, completely
disappears. Instead it remains as a vestigial strand. Among the Amphib~
ians this is true of many of the Urodeles. but not of the Anura.
In conclusion the functions of certain of the rather special structures
of the Frog heart whose development has been described may be briefly
indicated. It will be recalled that muscle fibers in the undivided ventricle tend to act as partial partitions and to keep the kinds of blood in it
V 1,: - .t_._..._ ___.__....__..,a.-_....M.-..........._.
i T
l
220 THE FROG: LATER on LARVAL DEVELOPMENT
separated. The spiral valve in the truncus arteriosus then assists in
guiding these different kinds to the proper pairs of arches. Thus the
relatively unaerated blood leaves the heart first, and goes into the
fourth arch on the way to the lungs and skin. Then the mixed blood is
guided into the main systemic arches and external carotid. Lastly, the
relatively aerated blood is forced through the carotid “gland” and
into the internal carotid to the upper part of the head and brain (Fig.
111 .
0)ther Arteries.——The pharyngeal arteries develop at about 9 mm.‘
from outgrowths of the suprabranchial aortae, which at first connect
with transitory vessels in the mandibular arches. At about the middle of
each main systemic aortic arch a large branch is given off to the fore
limb; it is the subclavian. The suprabranchial or lateral aortae come together to form the single dorsal aorta at about thelevel of the pronephros (see below). Throughout the remainder of its course this artery
gives off several lumbar arteries to the body wall, as well as larger
branches which supply the viscera (mesenteric arteries), and the hind
limbs and adjacent regions (iliac arteries).
The Venous System.
The Hepatic and the Hepatic Portal Systems. —- In discussing the development of the heart, it was noted that almost from the first two veins
entered it posteriorly, i.e., the vitelline veins. Just at the point of entrance to the heart their fusion resulted in the formation of a common
chamber, the sinus venosus. Between this point and the liver a further
fusion of these veins occurs not long after hatching, and the result is for
the time being the hepatic vein. (F ig. 110) . Although first mentioned in
V connection with the heart, the vitelline veins actually appear first on
the ventro-lateral sides of the yolk mass, whence they pass along the
sidesof the yolk and liver to the heart. As noted, fusion early occurs an- i
terior to theliver, but posterior to it the vitelline veins remain separate.
The right vein within this region then disappears, and the left becomes
the hepatic portal vein. It remains connected with the anterior hepatic
vessel only through capillaries within the liver substance, while posteriorly it sends branches to the digestive tract. This vein with its branches
and liver capillaries constitutes the hepatic portal system.
BLOOD‘ VESSELS AND CORPUSCLES 221
each of these connections there presently develops a sinuslike vein, the
ductus Cuvieri. These veins do not run horizontally from the sinus ve
nosus to the body walls, but obliquely upward. At the points of union
with the respective wall each ductus then gives rise to an anterior and
a posterior branch within the wall itself. These are the anterior and pos
atr1o- ventricular aperture
 
 
 
   
 
external jugular
 
   
   
 
 
internal jugular anterior
smo
 
externai iugular atria. “"3 ‘"3
. Lj subscapular aP°m"°
“"31 . innominate
portion of internal
heart . lU8'-"3" . .
‘ ubclavian
sinus venosus ‘T lg‘ d,U=l_uS nth”;
, ‘ uviera
\_ , _muszulocutaneous
he zitics ,
P left posterior
anterior part ol cardinal sinus
posterior vcna cava spam
liver portals
r‘ ht oster' « ' .
cfidinpal '°r left posterior
- _ v osterior vena cava
cardinal vein hdney ' 7
(mesonephros
substance of forming ,
rnesonephros
Fig. 112. — Figure A is areconstrnction in ventral view of the chief veins of a 10
mm. Rana pipiens larva made from serial cross sections, and enlarged 22.5 times.
The ventricle of the heart is omitted, and _the mesoncphros is of course shown only
diagrammatically to indicate its relative position. Figure B is a semi-diagrammatic
representation in ventral view of the veins in an adult Frog which are derived from
those shown in A, with the addition of the abdominal vein, as described in the text.
The entire heart is omitted from this figure, and the dotted lines merely outline
where the posterior cardinal sinuses would be if, they were still present. It should
he noted, as indicated by the labels, that the aperture in figure A is a completely
difierent one from that represented in figure B. Also, it is to be emphasized that
since figure B is near natural size, the two figures are on nowhere near the same
scale. As usual, relative degrees of growth of parts account for many of the differ
- ences, especially in connection with the development of the anterior vena cavae.
terior cardinals. Presently there grows anteriorly from the base of each
ductus Cuvieri a vein which extends into the lloor of the mouth, the inferior (external) jugular. This situation is clearly in evidence at 10
mm. or earlier (Fig. 112, A). Later at about the point of origin of each
inferior jugular there also grows toward the region of the respective future shoulder another vein which becomes the subclavian. At approximately the same time, so far as is known, the base of each ductus Cuvieri
becomes extended somewhat, thus separating the place of origin of the
respective inferior jugular and. subclavian from the sinus venosus. The
222 THE FROG: LATER OR LARVAL DEVELOPMENT
short new section of vessel thus added to the proximal end of each duc~
tus is then known as an anterior vena cava. The remaining portion of
each ductus between the origin of the respective inferior jugular and
the origin of the respective anterior cardinal, the posterior cardinals having meanwhile disappeared (see below), is henceforth called an innominate. Thus each anterior cardinal itself now becomes a superior (internal) jugztlar. At about the junction of each innorninate vein and the
respective superior jugular a backward curving vessel arises which is a
subscapular (Fig. 112, B).5
Turning now to the posterior veins, each posterior cardinal will be
found proceeding from the junction of the ductus Cuvier and anterior
cardinal (superior jugular) backward through the pronephric region.
Here it has the form of a broad sinus which more or less surrounds the
pronephric tubules (see below). Posterior to this region, it turns sharply
toward the median line and continues along the median side of the respective pronephric (Wolffian) duct to the cloaca (Fig. 112, A) Along
its course, each of the cardinals receives branches from the body wall,
and at their posterior extremities the two veins unite and receive the
caudal vein which brings the blood from the tail.
At about the 10 mm. stage in Rana pipiens, modifications in this arrangement begin as follows: Along the median dorsal surface of the
liver a new vein forms which empties into the hepatic vein anteriorly,
and posteriorly unites with the right posterior cardinal just caudal to
the pronephros (Fig. 112, A). At approximately the same time, or
slightly later the posterior fusion of the posterior cardinals proceeds
anteriorly in an intermittent manner into the region of the developing
mesonephroi, and eventually it occurs throughout the extent of those
organs. Thus is produced a median cardinal vein which, due to the manner of its formation, is continuous anteriorly with the new vein connecting the right cardinal with the hepatic. With the disappearance of
the pronephros, the right cardinal, anterior to the point where the new
vein has joined it, and all of the left cardinal, also disappear. The single
median vein which results is called the posterior vena cava. It is to be
noted that its posterior portion is really simply the former median cardinal vein, while its extreme anterior part is merely the old hepatic
vein which receives branches from the liver. As the latter vein thus he
comes part of the posterior vena cava opening into the sinus venosus,
indicatecl as arising subsequent to 10 mm. actually develop, though the early larval
and the adult conditions are of course well known.
5 There is no very complete description of just how some of the branches just
-a.... . _.  , ,_ .  ..s.,,-r........ - ~/«<>~4 . . ............._..,..«,.,..e_a~...s.«a-.,.,.,,
BLOOD VESSELS AND coaPUscLEs' 223
the branches which it receives
from the liver substance become
the permanent hepatic veins
(Fig. 112, A).
Meanwhile it is to be noted
that as the posterior cardinals
fuse and the mesonephroi develop, there arises along the lateral border of each of these organs a new vein. Each of these
veins then becomes connected
with the rriedian vein (posterior
vena cava) by numerous channels through the mesonephric
substance (Fig. 112, A). Indeed
according to some accounts
(Shore, ’01) the cardinals simply fuse, and then are partially
divided by the mesonephroi into
three main parts, a median and
two lateral, the undivided remnants constituting the connecting
channels (Figs. 112, A; 113, A,
B). Though this is Shore’s description of the process, it seems
to the writer that three fairly
separate channels exist before
the mesonephros has developed
to any extent. The mesonephric
(pronephric) ducts are of course
present, however, and it appears
that they may help to split off a
lateral channel from each of the
fusing, more medially placed,
cardinals. It also appears to the
present author that in many, if
not in all, cases at the '10 mm.
stage the undilierentiated mesonephric primordium (nephrotomal tissue) extends across the
Fig. 113.——The development of the
posterior part of the venous system in
the Frog. From Kellicott (Chordate Development). After Shore. A. Portion of
a transverse section through the posterior mesonephric region of an 18 mm.
tadpole. B. Diagram of the veins of a
25—3O mm. tadpole. C. Diagram of the
veins of the adult Frog.
:2. Dorsal aorta. c. Vcna cava. e. Nuclei of the endothelial lining of the
mesonephric sinus, continuous with the
vascular endothelium. f. Femoral vein. 1'.
Iliac vein. lc. Lateral mesonephric channel of the posterior cardinal vein. in.
Mesentery. mn. Mesone-phros. n. Mesonephric tubules. p. Posterior cardinal
veins. (in C showing their original location). pv. Pelvic vein. rp. Renal-portal
vein. rr. Revehent renal veins. sc. Sciatic vein. st. Nephrostome. u. Caudal
vein. ucm. Median mesonephric channel
of the posterior cardinal vein. W Wolffian duct. x. Connection between caudal
vein and the lateral mesonephric channels. 1—1. Part of the renal-portal vein
formed from the lateral channel of the
posterior cardinal. 2-2. The posterior
part of the vena cava formed from the
median channel of the posterior cardinal vein.
224»! THE FROG: LATER OR LARVAL DEVELOPMENT
median line in many places as a single mass just above the fusing
cardinals. This mass then seems actually to be divided by the dorsally pushing median cardinal vein instead of the reverse process as usually described.,Perhaps the real procedure is one of mutual interpenetration of mesonephric substance and veins as suggested in Figure
‘ 112, A. The writer regards
this as most probable on
servations. Be this as it
may the ultimate result is
that the lateral vessels develop to become the renal
portal veins; and the channels connecting them with
the median posterior vena
cava are then the renal
veins. Later with the appearance of the legs each
renal portal vein is joined
by an iliac vein which. as
these appendages develop.
divides at its distal end
into the femoral and sciatic veins. Finally with
the loss of the tail the
Fig. 114..—-Ventral, lateral and dorsal views of P3” of the Poslerio" Vena
the lymphatics in a 26 mm. tadpole of R. tempo- -cava caudal to [he kidneys
raria. From Hoyer. For description see text. vanishes so that most of
the blood from the posterior region of the body must pass through the
renal portal vessels and the abdominal (see below) (Figs. 112; 113).
The Pulmonary Veins. — These begin to develop very early (6 mm.)
as a dorsal offshoot from the sinus venosus. Later this ofl"shoot opens
into the left atrium, while at the lungs the single pulmonary vein divides so as to receive blood from each.
bladder, making lateral connections with the femoral veins. Just anterior to the bladder the two vessels then fuse; while still further forward
the right one later disappears entirely. The remaining single vessel is
the abdominal vein, which finally loses its connection with the sinus
the basis of his own ob-'
THE PRONEPHROS AND SEGMENTAL DUCT 225
venosus; it then acquires a connection with the hepatic portal vein, and
also develops two branches opening into the capillaries of the liver (Fig.
112, B). ‘
The Lymphatic System. ~— Just before" hatching, the anterior
lymph hearts appear to arise from a superficial plexus of veins between
the third and fourth somites. They lie between the peritoneum and the
integument, and soon become incased in muscle fibers. In connection
with each “ heart ” there develop from other parts of the above venous
plexuses two vessels just beneath the skin. One proceeds anteriorly, and
the other posteriorly, while into these vessels drain numerous anastomos
ing capillaries; the latter eventually form the characteristic subcutane- ‘
ous lymph sacs of the Frog. Sometime after hatching (26 mm.), the
anterior vessels open downwards into large lymph sinuses in the branchial region (Fig. 114«) . The lateral posterior trunks unite at the root of
the tail, and divide into a dorsal and a ventral vessel, which pass into
it. The thoracic ducts seem to be outgrowths of the anterior lymph
hearts, which extend posteriorly between the dorsal aorta and the posterior cardinal veins. When the hind legs appear, posterior lymph hearts
develop from the segmental veins of that region also.
All the lymph hearts are guarded by valves between themselves and
the lymph channels on the one hand, and between the hearts and blood
vessels on the other. Thus the lymph always passes into the blood, never
in the reverse direction.
The Spleen. —— At about 10 mm. there appears in the mesentery, on
the anterior mesenteric artery, just dorsal and posterior to the stomach,
a collection of lymph cells. They multiply, and later (25 mm.) the cell
mass becomes very vascular. The body thus formed is the spleen.
INTERNAL DEVELOPMENT: THE LARVAL EXCRETORY
SYSTEM
Although both the ‘larval and adult systems are paired, we shall re
fer only to the development upon one side. This is done with theunderstanding that the processes on the opposite side are identical.
THE PRONEPHROS OR HEAD KIDNEY, AND THE
SEGMENTAL DUCT
The Pronephros.——When last described, the somatic wall of the
nephrotomal region had thickened until it slightly overhung the side
226 THE FROG: LATER on LARVAL DEVELOPMENT
Fig. 115.—-Sections through Frog larvae illustrating the later development of the pronephros.
From Kellicott (Chordate Development). A.
A section through the first nephrostome of a larva of Rana sylvatica of about 8 mm., with prominent external gills. After Field. B. A section
through the region of the second nephrostome of
a 12 mm. larva of Rana temporaria. After
bringer.
c. Coelom. ‘cu. Sinuses of posterior cardinal vein.
g. Gut cavity. gl. Glomus. gX. Ganglion nodosum
(part of the ganglion of the vagus nerve). l. Lung.
m. Mesencliyme. myz. Second myotome. p. Peritoneum. s1, 52. First and second pronephric neph
rostomes. tr.‘Common trunk. X. Root of vagus
nerve.
of the lateral plate between it and the ectoderm;
in the region of the second, third and fourth
somites, cavities were beginning to appear within the thickening, especially in its lateral portion
(Fig. 84) . These laterally
placed cavities now tend
to run together so as to
form in this region a continuous longitudinal lumen, the common trunk.
At the same time, other
spaces between this lumen
and the coelomic cavity
enlarge and unite with
one another to form three
separate tubules connecting the trunk with the
coelom. These are the pronephric tubules, and each
of them is opposite one of
the three somites referred
‘to. The opening of each
tubule into the coelom is
in the form of a funnel
named the nephrostome
(Fig. 115), which presently becomes lined with
long cilia. The tubules, together with the common
trunk, now become somewhat convoluted, and
these convolutions begin
to become imbedded in
the sinus-like cardinal
vein which partially surrounds them (Figs. 115,
,,,.,...,,4«-«a<.—«‘.,.er..‘«,»....-.,.r~«~,.. .. . .. .
THE PRONEPHROS AND SEGMENTAL DUCT 227
116). At the same time the mass which is thus formed becomes enclosed
on its dorsal and outer sides by connective tissue derived from the myotomes of this region and from the somatic mesoderm. This covering is
termed the pronephric capsule.
Although not directly connected with the pronephric tubules, there
develops with them another organ which because of its position and
structure is probably concerned with their function. It arises as an outpushing or fold of splanchnic mesoderm at the extreme dorsal limit of
the coelom in the region just opposite the nephrostomes. In this way a
Fig. 116.—Total views of the pronephros of the Frog (R. sylvatica). From Kellicott (Chordate Development). After Field. A. Right pronephros oi an embryo of
about 3.5 mm. The crosses mark the location of the nephrostomes. B. Right pronephros of a larva of about 6 mm. First tubule dotted; second white; third
obliquely ruled; pronephric (segmental) duct shaded with lines.
small mass of tissue becomes suspended directly opposite these openings. Presently numerous capillaries form within it and become connected with the nearby dorsal aorta. This vascular body is then called
the glomus, and it has been shown by transplants in Amblystoma that
the stimulus to its development depends upon the presence of the pronephric tubules (Fales, ’35), even though the latter have no direct connection with it. The pronephric tubules, together with the glomus, may
henceforth be referred to as the pronephros or head kidney (Figs. 116,
117).
The Segmental Duct. —-— So far as has yet been indicated, the larval
kidney has no external outlet. While the above changes are going on,
however, the lumen of the common trunk has extended backward
through the lateral border of the nephrotome until it has established a
connection with the cloaca. The outer ‘portion of the nephrotome containing this lumen is then called the pronephric or segmental duct.
Rosterior to the fourth sornite it gradually becomes more or less separated from the more median portion of the undifferentiated nephrotomal tissue which occurs in this region.
228 THE FROG: LATER OR LARVAL DEVELOPMENT.
Changes Subsequent to Hatching. - This is approximately the condition reached at the time of hatching, when the tadpole is from 6-7 mm.
long. The pronephros does not attain its maximum development, however, until. the animal is about 12 mm. in length. During this particular
period the pronephric tubules increase their convolutions to a considerable extent, and the coelomic
space into which the nephrostomes
open and in which the glomus is
suspended becomes cut off ventrally from the main coelomic cavity. This is accomplished by the
development of the lungs in this
region (see Fig. 115). These organs are covered by a fold of the
splanchnic mesoderm, and, as they
grow, this covering fold is eventually brought into contact with the
somatic mesoderm, with which it
fuses for a short distance. The cavity thus formed, though it is separated from the coelom beneath, remains open to it both anteriorly
Fig. 117.-—Transverse section of an
advanced Frog embryo. From J enkinson
(Vertebrate Embryology) .
m.!. Medullary tube. rz. Notochord.
s.n. Subnotochordal rod. my. Myotome.
a. Aorta. p.c.v. Posterior cardinal vein.
prn. Pronephric tubule. prn.f. Pronephric funnel (i.e., nephrostome). gl. Glomus. C. Coelom. so. Sornatopleure. spl.
Splanchnopleure. g. Gut. l. Liver. v.v.
Vitelline vein. ec. Ectoderm.
and posteriorly. It is termed the
pronephric chamber.
By the time the larva reaches a
length of 20 mm., the head kidney
begins to degenerate. Thus the
pronephric region of the segmental
duct becomes cut off from the part
posterior to it. The former portion
of the duct, together with the pro
nephric tubules and their nephrostomes, then gradually disappears; °
the glomus at the same time shrivels up, though remnants are visible
even after metamorphosis. As the larval kidney is thus eliminated, its
place is taken functionally by the mesonephros whose development is
now to be described.
5 Hall states that during the degeneration of the pronephros the three nephro
stomal openings, at least in R. sylvatica, always become fused into one, the common
nephrostome (Fig. 118 C ‘
THE MESONEPHRIC OR WOLFFIAN BODY 229
   
‘ - .g—..-ma"
 
Fig. 118.—Sections through the developing mesonephros and the degenerating
pronephros of R. sylvatzca. From Kellicott (Chordate Development). After Hall. A.
. Section through the eighth somite of an 8.5 mm. larva. B. Section through the meso
nephric rudiment of a 25 mm. larva. C. Section through the pronephric chamber
and the common nephrostome of the pronephros of a 25 mm. larva.
(I. Dorsal aorta. c. Coelom. en. Common nephrostome. g. Germ cell. 1'. Inner tubule. m. Mesonephric rudiment. my. Myotome. 0. Outer tubule. p. Remains of pronephros. pc. Posterior cardinal vein. s. Shelf cutting off the pronephric chamber
from the remainder of the coelom. so. Somatic rnesoderm. sp. Splanchnic mesoderm.
W. Wolffian duct. I. Primary mesonephric unit. II. Secondary mesonephric unit.
THE MESONEPHRIC OR WOLFFIAN BODY
Posterior to the pronephros the outer margin of the nephrotome went
to form the segmental duct. The inner portion medial to the duct appears meantime to have fused to some extent with that from the opposite side, thus forming a continuous mass ventral to the dorsal .aorta,
' and above the fusing, or fused, posterior cardinal veins. This inner por
tion now starts to form the adult kidney in the following manner.
The Mesonephric Vesic1e.——As indicated above, the inner part
is for a brief time divided into segmental nephrotomes. These, however,
230 THE FROG: LATER on LARVAL DEVELOPMENT
Fig. 119.—Series of diagrams illustrating the development of the
primary ymesonephric tubules in R. sylvatica. From Kellicott (Chordate Dewelopment). After Hall. The Wolflian duct is drawn in outline simply. The mesonephric vesicles are shaded; the somatic part
of the tubule is shaded by continuous lines, the splanchnic part by
dotted lines. A. Wolflian duct and simple mesonephric vesicle. B.
Mesonephric vesicle dividing into the large primary mesonephric
unit and the small dorsal chamber. The latter elongates anteroposteriorly and represents the rudiment of the secondary and later
mesonephric units. C. Formation of the rudiment of the inner tubule. D. Inner tubule extending upward and toward the mesonephric duct; formation of rudiment of outer tubule. E. Outer tubule
fused with peritoneum and rudiment of nephrostome thus established. Bowman’s capsule forming. Commencement of differentiation of secondary mesonephric unit. F. Separation of nephrostomal
rudiment from remainder of tubule. G. Connection of nephrostome
with branch of posterior cardinal vein; separation of secondary
unit.
a. Bowman’s capsule. 13. Inner tubule. n. Nephrostome. 0. Outer
tubule. p. Peritoneum. 1;. Branch ‘of posterior cardinal vein. 1.
Primary mesonephric unit. II. Secondary mesonephric unit. Tertiary mesonephric unit not yet developed.
M... 4.1;-.5
THE MESONEPHRIC OR WQLFFIAN BODY 231
disappear almost at once so that a single nephrotomal band extends
from the seventh to the twelfth somites. Within either side of this hand
there then arise a series of thickenings somewhat more numerous than
the somites, and in each thickening there soon appears a cavity (Figs.
118, 119). This cavity, which is called the mesonephric vesicle, eventually becomes divided into two parts, the second and smaller part still
later giving rise to a third. These parts are called primary, secondary,
and tertiary units, in the order of their appearance, and their further
development, though not simultaneous, is identical in character. lt will
be necessary, therefore, to describe the process in only one of the
primary units.
The Development of a Primary Vesicular Unit.—Upon the
dorsal side of the unit a small hollow outgrowth appears (Fig. 119, B).
This, as later events prove, represents the rudiment of the secondary
unit, but for the present does not develop further. Next (Fig. 119, C),
an evagination pushes out from the ventro-lateral side of the primary
unit in the direction of the segmental duct. This is the inner tubule,
which presently becomes connected with the segmental duct, the latter
being henceforth known as the mesonephric or Wolfiian duct. It is to be
noted, moreover, that, by virtue of the partial rotation of the primary
unit, this connection occurs dorsally rather than ventrally (Fig. 119,
D, E). A part of the inner tubule later becomes greatly convoluted and
the coils press down into the median cardinal vein (15 mm.), perhaps
helping to divide the latter, as indicated above. Meanwhile there has
grown out from what is now the ventral side of the unit, another evagination which presently become connected with the peritoneal (coelomic) cavity. This is the outer tubule, whose subsequent history in the
Frog is very peculiar." It soon (20 mm.) breaks away from the main
portion of the unit and acquires an opening into the lateral division of
the median cardinal vein, i.e., the future renal portal vein. At the same
time its opening into the coelomic cavity becomes ciliated as a typical
nephrostome, this curious connection between body cavity and blood
vessel persisting throughout life (Fig. 119, F, G).
The growth of these tubules has meanwhile been accompanied by a
loss of the round or ‘vesicular character of the region of the original
primary unit. Thus between the point of origin of the secondary unit
and that of the inner tubule, this region has become stretched out, and
at the same time invaginated in a ventro-medial direction (Fig. 119,
7 Some authorities assert that the outer tubule probably never actually opens
into the cavity of the primary unit from which it arises (Marshall Hall).
232 THE FROG: LATER OR LARVAL DEVELOPMENT
E, F, C). In this manner a cavity is produced which is later filled by a
mass of capillaries connected with the dorsal aorta and also with the
posterior vena cava. Such a capillary mass is called a glomerulus. The
occurrence of the venous connection and the location of the structure
within the kidney rather than in the coelom are two essential features in
which a glomerulus diifers from a glomus. The surrounding walls of the
Fig. 120.-——-Parts of sections through young R. temporaria, showing
the origin of the adrenal bodies. From Kellicott (Chordate Develop
m.en.r). After Srdinko. A. Through 30 mm. tadpole. B. Through 11
mm. Frog after metamorphosis.
a. Dorsal aorta. ac. Corticle cells of adrenal body. am. Medullary
cells of adrenal body. ct. Connective tissue. g. Gonad. gs. Sympa
thetic ganglion. m. Mesentery. n. Mesonephros. rv. Revehent renal
vein. v. Vena cava. x. Point where ganglion cells enter mesonephros
and adrenal bod_y.
invaginated unit in which the glomerulus thus lies embedded then constitute Bowman’s capsule, the capsule and capillaries together being
termed a renal corpuscle or Malpighian body. 7
The occurrence of similar processes in the other units finally results
in a mass of tubules, glomeruli, and nephrostomes, which constitute the
adult mesonephric organ or kidney. This organ is virtually complete by
the time metamorphosis is ended.
THE ADRENALS
Though in no sense a part of theexcretory system,
ways occur in such close connection w
to describe them at this point. Indeed,
ship of the adrenals and kidneys is
Vertebrates, so much so that it is difii
animal, the former organs appear 111
these organs alith the kidneys that it seems best
in the mature Frog the relationmore intimate than in the higher
cult to separate them. Thus in this
erely as an area of thin yellowish
ADRENALS AND GONODUCTS 233
tissue attached to the ventral side of the mesonephros. They are com
posed, however, of two kinds of cells, the so-called medullary su bszance,
and the cortical substance, which originate as follows:
The cortical substance is so named from the fact that in higher forms
it occurs on the outside of the organ, though this is not true of the
Frog. Here it consists of anastomosing cells apparently derived (at
about 12 mm.) from the rnesonephric blastema cells (Segal, ’53) near
the cardinal veins. These cells form a meshwork into which branches
from the veins soon penetrate. The medullary substance consists of pigmented cells which appear later. They are derived originally from sympathoblasts in the sympathetic ganglia of the mesonephric region, and
become scattered throughout the cortical tissue (Fig. 120).
INTERNAL DEVELOPMENT: THE GENITAL SYSTEM
THE GONODUCTS
In the Male. ———The vas deferens of the Frog is simply the meso-nephric or Wrolliian duct, which serves as both ureter and sperm duct.
Posteriorly, in the region of the cloaca, each duct develops a glandular
seminal vesicle. Anteriorly each vas deferens becomes connected with
the respective testis as follows: From the latter certain strands of tissue
known as rete cords (see below) develop into fine ducts which grow
into each rnesonephros along its median edge. Within the kidney these
fine ducts become connected with the Bowman’s capsules of some of the
kidney tubules. The fine ducts together with the tubules of the kidney
with which they thus connect then constitute the vase eflerentia, opening into each mesonephric duct (vas deferens) .
At about 20 mm., there appears on each side of the coelomic wall
just beneath‘ the pronephric region, a longitudinal thickening of the
peritoneum. Along the dorsal border of this thickening ‘there is then
proliferated a ridge of cells, whose edge grows downward and presently
fuses with the ventral border of the thickening. In this manner a tube is
formed, which, when completed, is held close to the body wall by a thin
covering of the general peritoneum (Fig. 121). This process continues
anteriorly to a point opposite the base of the lungs and posteriorly to
the cloaca, which it reaches subsequent to metamorphosis. In the male
this tube develops no further, and is very inconspicuous and without
function, but is the rudiment of a Miillerian duct ( see below) .
In the Female.——The mesonephric duct is of course present in the
female, but in this case acts only as a ureter. It possesses, nevertheless,
, ,.:.;..=.- . . ;_- .. .
234 THE FROG: LATER OR LARVAL DEVELOPMENT
extremely slight enlargements, representing rudimentary seminal vesicles.
Each Miillerian duct or oviduct, on the other hand, develops as described in the male, but does not stop at the point there indicated. Instead, the rudimentary duct moves away from the body wall somewhat,
though it still remains attached to that wall by its peritoneal covering.
Between the duct and the wall the two layers of the covering then fuse
   
Fig. 121.—Sections through the developing Miillerian duct of a 34 mm. tadpole
of R. syluatica, From Kellicott (Chordate Development). After Hall. A. Section
passing through the beginning of the Miillerian evagination. B. Section posterior
to A. Duct established but still connected with peritoneum. C. Section still farther
posterior, showing the separation of the duct from the peritoneum with which,
however, it is covered.
M. Miillerian duct. p. Peritoneum. 2:. Third pronephric tubule.
to form the mesentery-like sheet supporting the oviduct. Anteriorly the
duct turns down slightly, and its end becomes dilated as the infunclibulum, while posteriorly it acquires an opening into the cloaca; between
these points it gradually becomes greatly convoluted and thickened.
THE GONADS
The Indifferent Period. ——-As the early stages of these organs are
identical in the male and female, a single account will suflice for both.
At about the time of hatching, a slight median dorsal ridge appears
on the outside of the enteron (Fig. 122, A). It is composed of primordial germ cells, which, as in other cases, have apparently arisen from
among the cells of the gut. Indeed, at this time it is difficult to distinguish the cells of the ridge from the enter'
as noted above, the lateral plates of In
esoderm press in toward each
other in this region, and as they meet, t
hey separate the ridge of cells
THE GONADS V 235
Fig. 122.—Sections showing the origin of the sex-cells (germ
cells) in R. sylvatica. From Kellicott (Chardate Development).
After Allen. A, B. Sections of a 7.5 mm. larva showing (Al sexcell ridge of endoderm and (B) its separation as the sex-cell cord.
C. Part of a section of an 8.3 mm. larva showing the beginning of
the migration of the sex-cells, resulting shortly in the division of
the sex-cell cord into two parts.
a. Dorsal aorta. ch. Notochord. cv. Posterior cardinal vein. e.
Endoderm cells. g. Gut cavity. l. Lateral plate of mesoderm. m.
Mesentery. my. Myotome. n. Nerve cord. sc. Sex-cell cord (not to
be confused with sexual cords). sch. Subchordal rod (hypochorda).
sr. Sex-cell ridge. W. Wolifian duct.
(sex-cell ridge) from the enteron, so that the former lies just dorsal to
the newly formed mesentery (Fig. 122, B). This ridge, now the sex-cell
card (not to be confused with the sexual cords), soon divides in two
longitudinally andgeach part moves a short distance ventro-laterally,
taking up its position just beneath one of the cardinal veins. The two
parts covered by coelomic.epithelium (peritoneum) project slightly
into the coelom in these regions and are known as the genital ridges. As
each ridge increases in size it projects further into the body cavity in
236 THE FROG: EATER OR LARVAL DEVELOPMENT
which it is suspended by the peritoneal epithelium which covers it.
This epithelium gradually presses in above the organ, and thus forms
a double sheet of tissue similar to that which supports the oviduct. As
noted in the description of the adult organ, this sheet in thetcase of the
ovary is termed the mesovarium and in the case of the testis the mesorchium. At this stage sex is still indistinguishable, and the gonad
A
Fig. 122. ——./1. Section through the gonad of a 30 mm. tadpole of R. catesbeiana.
B. Section through a young ovary from a tadpole of the same species. The secondary genital cavity lined with rete cord cells is small, but the germ cell nests of
which the rest of the gonad ‘is composed are already beginning to break up. After
Swingle.
gc. Germ cell. gcn. Germ cell nest. pc. Primary genital cavity. rc. Rete cord cells.
sgc. Secondary genital cavity or ovarial sac.
whether male or female consists simply of an elongated sac in which the
germ cells are coming to be arranged about the periphery. Throughout
the interior there exists a space which is filled by a jelly-like substance containing a few nuclei, and though thus occupied by jelly this
region is termed the primary genital cavity (Fig. 123, A). The develop
strands, the ret'e cards, which grow ventrally into the primary genital
cavity, and dorsally into the mesonephros (Witschi, ’52) .3 At this point
in most Frogs the sexes begin to be differentiated as follows:
3 These strands are sometimes designated as the sexual cards, or sea; cords
(Swingle), but it seems preferable to reserve these terms for the strings of germ
cells coming from the germinal epithelium, and found in many of the higher vertebrates (see Chick).
THE GON ADS 237
The Period of Sexual DiFferentiation.——In the case of a gonad
destined to become an ovary the germ cells about the periphery begin
to multiply. Simultaneously the masses of rete cord material which at
certain points have grown down into the primary genital cavity begin to
develop spaces within themselves. These new spaces
within the rete cord material
are known as the secondary
genital cavities, and though
at first occurring at intervals
along the length of the organ
they presently become more
or less confluent. The larger
cavities formed by this confiuence are called ovarial
sacs, whose walls composed
of rete cord cells, are everywhere in contact with the innermost layer of germ cells.
These germ cells soon become arranged in groups or
nests’ each nest being sup Fig. 124.-—A. Section through a gonad of R.
catesbeiana showing the first signs of a begin
rounded by a layer of follicular cells apparently derived
from the peritoneum. Later
the nests break up, and each
growing oiicyte has its own
follicle (Fig. 123, B). As
this growth of the oocytes
and their follicles proceeds,
ning testis. Note the rete cord material extending out among the germ cells, and the absence
of any extensive secondary genital cavity. B.
A developing testis from the same species
showing nests of germ cells, the forerunners of
ampullae, and eventually tubules. Near the hilus or base of the organ note the rete cords
forming the distal parts of vasa efierentia,
which lower down branch out to connect with
the ampullae. After Swingle.
a. Ampullae. gc. Germ cell. pc. Primary genital cavity. rc. Rete cords.
their pressure upon the walls
of the ovarial sacs causes these walls to approximate one another until
the cavities of the sacs are virtually obliterated. According to most accounts there always remain in the Frog a few nests of oiigonia close
against the periphery of the ovary, and from these are derived the new
oiicytes for each breeding season.
In each gonad which is to form a testis on the other hand a different
procedure occurs. The multiplication of the germ cells is less at first,
while the proliferation of the rete cord material is greater. The latter
also does not develop extensive secondary genital cavities as in the case
it
i
3%
238 THE FROG: LATER OR LARVAL DEVELOPMENT
of the ovary, but instead remains relatively condensed. Into this, germ
cells from the periphery seem to migrate (R. sylvatica, ~Witschi, ’29),
or in some cases cords of rete material grow out and surround groups
of the germ cells (R. catesbeiana, Swingle, ’26, Fig. 124, A). In either
event cysts are thus formed lined partly by rete material, and partly
by connective tissue or stroma. These may at first be described as ampullae, but eventually they lengthen out to form the seminiferous tubules
of the adult. Within a given tubule most of the germ cells are usually
at the same stage of development, except that a few residual spermatogonia apparently always remain to furnish sperm for the next season.
As indicated above the seminiferous tubules are connected with the vas
deferens through the vasa efferentia, the latter being formed partly
from the rete cords and partly from mesonephric tubules (Fig. 124, B).
In both sexes the anterior third or half of each genital ridge fails to
develop as indicated above. Instead, some time previous to metamorphosis this portion of the organ starts to become converted into the fat
bodies.
It may also be noted that while this is the normal situation in Frogs,
in Toads an interesting modification occurs. In most species of the latter animal the male possesses a small ovary-like body lying between the
testis and fat body. It is called Bidder’s organ, and has long been an
object of interest. It is now believed by some (Witschi, ’33) to represent an incipient ovary. According to this view it is held that the undifferentiated gonad in this region is deficient in medullary substance,
thus allowing the cortex here to develop to a limited degree. Though as
indicated, it is most common in males, it also occurs in some female
Toads where it again appears, according to this interpretation, as an
undeveloped piece of the ovary (Witschi, ’33) .
SEX REVERSAL IN AMPHIBIA
The occurrence of hermaphroditism and of sex reversal is always of
interest in any animal which normally has two distinct sexes. Hence
since considerable experimental work in this connection has been done
upon the Amphibia it is appropriate to say a few words about it at this
point.
From the foregoing account of normal gonad development in the
Frog, it is obvious that the gonads of the two sexes start out from
common primordia. What then causes their differentiation? It will be
recalled from statements in the chapter on the germ cells that the initial
determination of sex in general is believed to depend on a balance beSEX REVERSAL IN AMPHIBIA 239
tween male and female determining genes. The female determining
genes in most animals occur in the X-chromosome and the male determining genes in the autosomes. It was also noted, however, that these
gene effects, like others, can be modified by the environment, and that
the Amphibia afford good examples of this fact. The complete story
here is not yet entirely clear, but experiments on both Frogs and
Urodeles by Burns, Humphrey, Witschi and others seem to have elucidated the more essential factors. These experiments involve transplanting gonad primordia of various stages between animals of opposite sex,
uniting at random many individuals to form pairs (parabiosis, Humphrey, ’36), injecting sex hormones, and altering the temperature at
critical stages. For example in the Frog the cortex of the partially differentiated gonads is apparently inhibited by excessive warmth (32
degrees C.) , causing prospective ovaries to become testes (Witschi, ’29) .
Or in various species of Amhlystoma it was shown that the implantation
of a gonad preprimordium of the opposite sex in a larval host of another stage shifts the sex of the implant or the host (Humphrey, ’53).
Also injection of male hormone, testosterone, during differentiation of
prospective female gonads in Amhlystoma, produces partial reversal to
males, while injection of oestrone in prospective males causes reversal
toward the female (Burns, ’38, ’39). Chang, ’53, however, thinks substances other than these hormones are involved. Lastly Bruner and
Witschi, ’54, showed that early use of testosterone actually causes the
pre-medullary component of the prospective male gonad to form mesonephric tubules instead of medulla, without which the cortex partly differentiates into ovary. _
Without going into detail the conclusions suggested by the results of
these procedures may be summarized as follows: The chromosome com
plex gives the first impetus to sex determination, apparently by affect-
ing the character of the mesoderm at the gonad site (gonad preprimordium) . The character of this preprimordium having been thus initially
influenced then determines whether, in the seemingly indifferent gonad
rudiment arising from it, the cortex or the medulla shall acquire the
ascendancy. As soon as one or the other of these tissues does gain a start
it begins to produce a substance with two effects. One effect is to stimulate still further the development of the favored tissue, cortex or medulla, and the other effect is to inhibit the development of the opposite
tissue. Thus when once initiated the general result is cumulative. Finally
when the mature gonad has formed, it produces the usual sex hormones, testosterone‘ or oesterone, and these tend, to control such secondary sex characters as may be characteristic of the species. With this
240 THE FROG: LATER OR LARVAL DEVELOPMENT
history in mind we may better understand various types of sex anomalies in ‘animals possessing a perfectly normal chromosome complex.
Thus it is possible to have complete sex reversal in both gonads and
gonoducts, or there may be partial reversal in these organs giving a sort
of nondescript neuter. Also there may be complete reversal on one side
only, resulting in real hermaphrodites. Lastly there may be reversal in
parts of both gonads producing a kind of sex mosaic.
INTERNAL DEVELOPMENT: THE SKELETON
Only a brief outline of the development of the specific parts of this
system as it occurs in the Frog, Chick and Pig will be given in this text.
For further details the reader is referred to more extended accounts
cited in the bibliography. However, since the general histogenesis of
the different types of bone is essentially similar in all true Vertebrates,
it seems desirable to give some details concerning the basicvprocesses
involved‘. This will therefore be done at this point, with the understanding that though the fundamental pattern is similar in all the forms studied there are some variations in detail. The more important of the latter will be indicated in connection with the forms concerned.
THE HISTOGENESIS OF BONE
Dermal or Membrane Bone.—This type of bone is peculiar in
that ossification (deposition of calcium salts) occurs directly within
membranous connective tissue without the intervention of a cartilaginous stage. It is a method of bone formation which occurs extensively,
though not exclusively, as we shall see, in certain bones of the skull,
and may be described as follows: .
Within a connective tissue layer where the bone is to form, certain
undifferentiated mesenchymal cells become arranged in isolated strands,
each strand being several cells in thickness. These cells then lose their
fine processes characteristic of the cells of mesenchyme, and begin to
secrete in their midst a delicate fiber, for which reason they are termed
fibroblasts. The fiber they secrete is called an ossein fiber, but is not
essentially different from other nonelastic or white connective tissue
fibers consisting of collagen. Soon numerous fibers thus formed in a
particular region come to constitute a thickened strand. In ‘the next step
the fibroblast cells which deposited the fibers become modified chemically, and about each fiber they begin to deposit calcium salts. ‘When
this stage has been reached the cells involved are called osteoblasts.
THE HISTOGENESIS or BONE 24.1
The fibroblasts and osteoblasts, continuing to form respectively both
ossein fibers and calcium salts about each original strand, add to its
thickness and length. As a consequence of the latter type of growth, .
these thickened and ossified strands, now termed trabeculae, are
brought into contact with each other, and thus a bony network is produced (Fig. 125) . Since, moreover, the deposition of fibers and calcium
(matrix) is more or less‘periodic we find any given trabecula consisting of layers of bone somewhat like the growth rings of a tree. It should
,1
bone trabecula connective tissue
,3 (membrane)
csteoblasu
Fig. 125.—Trabecu1ae of a piece of membranous jaw
bone from a Mammal in the process of being thickened by
fibroblasts and osteoblasts. Drawing from Turtox preparation.
also be obvious that as the osteoblasts deposit their matrix they must
keep moving away from the original center of deposition or else be‘ imprisoned in their own products. As a matter of fact different ones do
both these things. Those which move, and thus remain at the surface
continue to function as osteoblasts. Those which are trapped, so to
speak, cease deposition, but do not die. They remain as permanent bone
cells with delicate processes extending out into the matrix. These processes. Qonvey nutriment from the spaces containing blood vessels to the
cell bodies, which furnish it to the organic ossein fibers. When these
cells and the fibers deteriorate and finally disappear with senescence
only the calcium salts are left, and the bone becomes brittle.
The bone formed as described evidently contains many irregular
spaces, and so long as these exist it has a spongy texture. In the central
parts of membrane bones which are under discussion this condition is
permanent, and the bone is known as cancellous. The spaces in such
bone, however, are not empty. They are filled with blood vessels and
large thin walled sinusoids, surrounded and supported by reticulate
242 THE F ROG: LATER OR LARVAL DEVELOPMENT
connective tissue (stroma). The stroma contains all types of mature
blood corpuscles which are being constantly produced by its undifferentiated cells, and passed as needed into the sinusoids, which communicate with the blood vessels. This conglomeration of loose connective
tissue, blood spaces, vessels and cells is termed marrow. Sometimes it
is permeated with fat containing cells, and is then known as yellow marrow as compared with the corpuscle producing red marrow. The spaces
thus occupied by marrow of one sort or the other are lined by a more
dense flat connective tissue layer, now containing fibroblasts and osteoblasts, and known as the endosteum. It is not to be assumed of course
that marrow exists only in ‘dermal bones. It occurs as much or more in
the other type of bone as will presently be pointed out.
As so far described it might be supposed that dermal bone is entirely cancellous, but this is not the case. Surrounding the first formed
cancellous material is a layer of connective tissue similar to the endosteum which comes to line the marrow spaces. This being outside, how
I ever, is called periosteum, and it also contains fibroblasts and osteo
blasts. ‘These fibroblasts and osteoblasts, like those of the endosteum
covering the trabeculae, deposit fibers and bone, in this case in continuous layers completely surrounding the cancellous bone -and marrow.
Thus is formed one type of compact bone, between whose layers entrapped bone cells occur at intervals, just as in the case of the layers
deposited on the trabeculae. As implied, however, this is not the only
type of compact bone that may be formed. In some cases, as will be
described more in detail below, some of the more outer marrow spaces
are filled with concentric bone layers which thus make the region so involved compact. More will presently be said of this method of forming
compact bone. Also curiously enough some of the first continuous peripheral layers deposited may prove not to be permanent. Another type
of connective tissue cells, known as osteoclasts, may invade this peripheral bone and eat out cavities in it so that it in turn becomes cancellous.
Later, however, such secondary cavities will be filled in again in the
manner noted in the case of the other cancellous bone, thus making it
again compact. In any case a few of the continuous peripheral layers
are always finally Ieft surrounding the entire bone. The end result of
all these processes is that the completed dermal bone consists of a
cancellous and marrow filled central region surrounded by varying
thicknesses of compact layers of onersort or another. Bones of this type
it should be added are more or less flat in shape, occurring for the most
part, as noted, as covering bones of the skull. ’
THE HISTOGENESIS OF BONE 243
Cartilage or Endochondral Bone.— In the case of bone of this
type, which comprises the larger part of the skeleton, ossification does
not occur directly from membrane, but from an intervening cartilaginous stage. The process is as follows:
epiphysial
cartilage
cartilage
being
replaced
by bone
trabeculae
covered by
fibroblasts
and osceoblasts
dyiaphysls
Fig. 1Z6.—-—The epiphysis and a portion of the diaphysis of a developing mammalian long bone. The epiphysis is still entirely cartilaginous. At the boundary between the two regions, however, the cartilage is being ‘reduced to fine strands by
means of chondroclasts. Further down in the diaphysis these strands are being
built up into bony trabeculae by the fibroblasts and osteoblasts which cover their
surfaces. Photo of a Turtox preparation by the author.
As before the initial condition is that of a mass or layer of mesenchyme. The mesenchymal cells then lose their processes much as in the
preceding case. Now, however, instead of becoming aggregated in
strands they form a densely packed mass of multiplying cells which
gradually assumes the shape of the future bone. These cells, however,
do not form bone. Instead each cell begins to secrete a gelatinous
matrix of a substance called chondrin. This is at first quite elastic, and
thus the cells are able to move away from each other as they secrete.
244 THE FROG: LATER OR LARVAL DEVELOPMENT
Later the chondrin condenses to form the mature cartilage matrix.
When this stage is reached, the cells can no longer push each other
apart, or multiply much. Each cell may divide once or twice, and the
small group secretes just enough to cause the cartilage immediately
around it to become especially dense. Thus we have formed a mass of
cartilage the shape of the future bone. It consists of a dense chondrin
matrix containing numerous small groups of cells. Finally this mass of
cartilage has surrounding it a firm connective tissue layer called perichondrium, whose cells, like those of the periosteum, continue for a
time to add to the cartilage peripherally. The next step is the destruction of the cartilage and its replacement by bone.
The destruction of the cartilage is brought about by the same cells
which previously deposited it. Now, however, these cells behave like the
osteoclasts noted above, only in this case they act as chondroclasts, and
erode cartilage instead of bone. They proceed in such a way that soon
they have reduced the cartilage to delicate strands whose surfaces they
cover. Meanwhile certain cells of the perichondrium become active and,
along with blood vessels, start to invade the disappearing cartilage.
These cells turn out to be fibroblasts and osteoblasts which soon replace the cartilage eroding cells surrounding the cartilaginous strands.
These cartilaginous strands thus take the place of the fibrous strands
of cancellous membrane bone, and around them the new fibroblasts
and osteoblasts deposit fibers and calcium salts to form cancellous
endochondral bone ( Fig. 126). The resulting bony trabeculae surrounding marrow filled spaces are the same as before, only in this instance
the bone was preceded by cartilage. In View of its behavior the surrounding perichondrium is from now on termed periosteum. This endochondral cancellous bone may now become compact in the same way
that the cancellous bone ofmembranous origin does so. The details of
that process, which were merely suggested previously, are as follows:
The bone forming cells, fibroblasts and osteoblasts, covering the trabeculae gradually so arrange themselves while depositing bone that
the marrow spaces become tube shaped. Then as the osteoblasts and
fibroblasts continue to deposit layers of calcium salts and fibers, part
of the cells withdraw toward the center of the constantly decreasing
marrow space. Others, as previously described in another connection,
are trapped between the layers to form permanent bone cells. In this manner concentric layers of bone are produced surrounding a marrow space
which finally is reduced to a small canal containing only a couple of
blood vessels and a few cells. This is called an Haversian canal, and toTHE HISTOGENESIS OF BONE 245
gether with the concentric arrangement of the bone layers about it
constitutes an Haversian system (Fig. 127). Compact bone so formed
therefore would consist of many such systems filling completely the
spaces between the original trabeculae. The canals of the numerous
systems are, moreover, interconnecting, so that the blood vessels in them
ultimately reach the periosteum on the one hand or the central marrow
on the other.
It should again be emphasized that the actual process of bone depo
 
location of
V a bone cell
   
Haverslan canal P"l°“°3l
bone
Fig. 127. -——I-Iaversian systems from a section of adult ‘bone.
sition just indicated as occurring in compact endochondral bone is
exactly the same as that referred to in the case of one type of compact
membrane bone. The difference is entirely in the preceding processes.
In the former case the compact bone was preceded simply by cancellous
bone. In the present case the cancellous bone was itself preceded by
cartilage. In addition to this difference in the method of development
between membrane bones and the part of all endochondral bones thus
far described, there is one other feature characteristic of the final structure of most of the latter. A good deal, or all, of the central cancellous
material in mature endochondral bones is usually removed entirely by
osteoclasts, and the relatively large single space so produced occupied
by the marrow. Any other marrow in such bones will, as in membrane
bones, occupy the spaces of any cancellous bone which remains (Figs.
126, 128). l
' It must now be added that even so called endochondral bones are not
entirely so. This is because the endochondral compact bone formed in
246 THE FROG: LATER OR LARVAL DEVELOPMENT
the manner we have indicated is always ultimately surrounded by bone
formed directly from the periosteum, and hence entirely membranous
in origin. This may involve simply the laying down of the final circumferential layers. Usually, however, as in the case of completely membranous bone, some of the early surrounding layers are rendered can
 
marrow
’ bony
bone)
   
 
* 'ln,llu Hui | s\‘/
‘lu,'"lu.',"'l mmnum u$““I\}‘,‘
\‘gnuf,':g1_n_p-u:uuI_I_I_l_L‘}§“u-{‘:/
L
 
Fig. 128.— A semi-diagrammatic representation of a cross section of a mammalian
long bone (endochondral) , showing periosteum, periosteal bone lamellae, Haversian
systems and marrow.
cellous by osteoclasts, with the subsequent development of Haversian
systems. And in this case the latter were obviously not immediately preceded by cartilage. Thus it is to be remembered that when, in later discussions, we refer to certain bones as being endochondral in origin, it is
only a part of such bones which were really preformed in cartilage. Socalled “ membrane bones” are, however, entirely preformed in membrane. ’
Finally it should be noted -that in the case of any kind of bone the
later stages in its formation involve a very intimate connection with
the periosteum. This is because that, in; addition to blood vessels, innumerable white periosteal connective tissue fibers are surrounded by
THE VERTEBRAL COLUMN 247
the final calciferous deposits. Thus these fibers, known as the fibers of
Sharpey, are directly continuous from the periosteum right into the
compact bone forming an extremely tight union between connective tissue and the bone itself. It may also be noted that at certain points these
fibers are aggregated into bundles called tendons which are continuous in the opposite direction from the bone into the connective
tissue sheaths of its muscles. We are now prepared to turn to a brief consideration of the
formation of the various parts of the skeleton
of the-Frog.
THE VERTEBRAL COLUMN
At or a little before the time of hatching,
the skeletogenous sheath has already come to
surround the notochord and nerve cord, as in-.
dicated above. Some time after hatching
(about 15 mm.) , cartilage develops within
this sheath and presently becomes divided into
sections corresponding in position and num-'
ber to the future vertebrae. Within each such
Fig. 129. —-— Transverse
section through the vertebral column in the body
region of a larva of Xenopus capensis. From Kelli
cott (Chordate Develop
section, moreover, the cartilage about the
chorda soon forms a ring which completely
surrounds it (Fig. 129). Within these cartilaginous rings, ossification now starts and
gradually spreads inward until the notochord
at the core of every ring is entirely obliterated.
Thus is formed the centrum of each vertebra.
Meanwhile between these vertebral centra the
notochord is also obliterated by the ingrowth
of cartilage. Each intervertebral disc thus developed, later splits into an anterior and a
posterior part. Finally, during metamorphosis each of these parts he
ment) . After Schauinsland.
c. Notochord. d. Dorsal vertebral cartilaginous
arch. s. Sclerotomal (skel
etogenous) sheath. n.
Nerve cord. cs. Chorda
sheath (primary and secondary). t. Perichondral
connective tissue. 12. Ventral (hypochordal-) vertebral cartilage. The dorsal
and ventral cartilaginous
elements have not yet
come to surround the noto
chord.
\
comes ossified and fused with the end of the contiguous centrum.
In a like way the neural arches ossify from cartilage which extends
dorsad from the centra around the nerve cord, while the transverse
processes arise as bits of cartilage projecting laterally from each centrum, which also later ossify. Eventually minute cartilaginous ribs form
at the ends of the processes, but are soon fused with the latter. -Vertebra
formation is induced by nerve cord rather than notochord (Holtzer, ’52) .
1»
248 THE FROG: LATER OR LARVAL DEVELOPMENT
As already noted, the Frog possesses only nine real vertebrae, and
the above description applies only to them. The skeletogenous elements
of the last two somites, however, form a single tubular piece of cartilage
which surrounds the end of the notochord. Later it also becomes mostly
ossified, and is known as the urostyle.
Fig. 130. ——Dorsal views of the chondrocranium of the Frog larva. A. Cl1ondrocranium of a 7.5 mm. larva of R. temporaria. From Kellicott (Chardaze Development).
After Gaupp, from Stiihr-Ziegler model. B. Chondrocranium of a 14 mm. larva of R.
fusca. After Gaupp, from Ziegler model. .
a. Auditory capsule. bp. Basal plate. c. Notochord. ct. Trabecular cornu. f. Basicranial fontanelle. in. Internasal plate. ir. lnfrarostral cartilage. j. Jugular foramen
(for IX and X cranial nerves). m. Muscular process. M. Mecke1’s cartilage. mo.
Mesotic cartilage. o. Occipital process. pa. Anterior ascending process of palatequadrate cartilage. pl. Parachordal plate. pp. Posterior ascending process of palata
quadrate cartilage. pq. Palato-quadrate cartilage. sr. Suprarostral cartilage. t. Trabecular cartilage.
THE SKULL
The F1oor.—-«The posterior portion of the skull floor, i.e., that part
which lies beneath the hind brain, is formed medially by the notochord.
On each side of the notochord a cartilaginous rod develops which fuses
with the chorda or rather with the cartilage which soon takes its place,
thus completing the floor in this region. These rods are called the parachordals, and the fused mass is the parachordal plate (Fig. 130, A).
In front of each parachordal is another rod. These rods are curved
THE SKULL 249
I!’
Fig. 131.—/1. Anterior portion of chondrocranium of R. fusca during metamorphosis. Lateral view. From Kellicott (Chordate Development). After Gaupp, from
Ziegler. B. Skull of a 2 cm. R. fusca, after metamorphosis. Dorsal view. Membrane
bones removed from left side. After Gaupp, from Ziegler.
a. Auditory capsule. am. Anterior maxillary process. an. Annulus tympanicus.
art. Articular process of palato-quadrarte cartilage. ea. Exoccipital bone f. Frontaparietal bone. fpo. Proiitic foramen. mx. Maxillary hone. n. Nasal bone. 0. Olfactory cartilages. on. Orbitomasal foramen. pa. Anterior ascending process of palatequadrate. pg. Pterygoid bone. pl. Plectrum. pm. Posterior maxillary process. pp.
Posterior ascending process of palato~quadrate. pq. Palato-quadrate cartilage. pt.
Pterygoid process of palate-quadrate. px. Premaxillary bone. qj. Quadratojugal
bone. 11. Foramen for optic nerve. III. Foramen for ‘III cranial nerve. IV. Foramen
for IV cranial nerve.
250 THE FROG: LATER OR LARVAL DEVELOPMENT
somewhat, with their concave sides facing each other, and their posterior ends fused with the anterior ends of the parachordals. Their own
anterior ends grow toward each other and fuse between the olfactorv
organs; these rods are the trabeculae. The space between them in the
anterior floor of the skull is the basicranial fontanelle, which temporarily lodges the infundibulum. Later, as the trabeculae grow together,
this opening is closed. I
The Sides, End, and Roof.—The floor has reached the stage indicated only a short time after hatching. The other cartilaginous parts
of the skull then develop
as follows:
In the posterior region
the cartilaginous auditory
capsules appear at the sides
of the head (Fig. 130, B).
Ventrally they are presently united with the skull
floor by the mesotic and
occipital cartilages. The
capsules thus form the
sides of the posterior part
Fig. 132.——Hyoid and branchial arches of a29 of the skull’ while the 0c.
mm. larva of R. fusca. Ventral view. From Kelli- cipital cartilages grow up
cott (Chordate Development). After Gaupp, to form the Posterior walls
from Ziegler.
bb. Basibranchial (first), or copula. bh. Basi- and the l‘00f Of this region.
5‘32‘=F:f;. S:':;::::‘-.;:;,§::::%::;*:hfie‘  Between the eeeeveeele is e
‘ posterior opening, the fa
ramen magnum, through which the spinal cord passes into the brain.
Anteriorly the trabeculae grow up to form the sides of the skull in the
neighborhood of the orbits. Their more anterior portions then grow together dorsally forming the anterior roof. Between this anterior roof
and the posterior one formed by the occipitals is the supra-cranial fontanelle. The extreme anterior ends of the trabeculae go to form the
olfactory capsules, which are partly separated from the brain cavity by
a septum. All of these changes, both anterior and posterior, are virtually completed in larvae of 3 cms.
Dermal Elements in the Skul1.——The cartilaginous skull thus
formed later becomes ossified, in the usual way. Before this occurs,
however (about 20 mm.), many of the parts begin to be covered by
51:
ch
THE SKULL 251'
bony plates originating in the dermis (in the manner indicated above)
and hence called dermal bones (Fig. 131). Some of these plates, such as
the fronto-parietals, serve to cover open spaces left in the cartilage, e.g.,
the supra-cranial fontanelle. Most of the dermal bones as well as those
formed in the cartilage have appeared before metamorphosis is com
plete.
Fig. 133.—A. Hyobranchial apparatus of R. fusca, toward the end of metamorphosis. The left side is shown in a more advanced stage than the right, in that less
cartilage is present. The original cartilage is indicated by fine stipples. The coarse
stipples indicate the cartilage added during the early part of metamorphosis. From
Kellicott (Chordate Development). After Gaupp, from Ziegler. B. Hyobranchial apparatus of a 2 cm. R. fusca, after metamorphosis. After Gaupp, from Ziegler.
a. Alar process. ac. Anterior process of hyoid cornu. 17. Body of hypobranchial cartilage. bb. Basibranchial (first), or copula. ch. Ceratohyal (hyoid cornu in B). ho.
Hypobranchial plate. 1. Postero-lateral process of hypobranchial cartilage. m.'Manu
brium. 2. Remains of second ceratobranchial (postero-medial process of hypobrar.chial cartilage).
The Visceral Arches.—These arches at first consist merely of
concentrations of mesoderm, as indicated above. Shortly after the
mouth opens, however, all have developed skeletal elements of cartilage.
The cartilage of the mandibular arch early becomes divided into a dorsal portion, the palato-quadrate, ‘and a ventral portion, Meckel’s cartilage. The ‘former becomes fused anteriorly and posteriorly with the
trabeculae and at metamorphosis is considerably modified to form a
part of the upper jaw. As noted above, furthermore, a small outgrowth
becomes separated from the *posterior or quadrate portion of this cartilage and gives rise to the annulus tympanicus of the middle ear. Meek252 THE FROG: LATER OR LARVAL DEVELOPMENT
permanent
cartilaginous
'. epiphysls
erlosteum
cartilage
blood vessel
invading Eériiflng
blood vessel
forming
marrow
perlosteal bone
Iamellae of
diaphysls
marrow
Fig. 134-.-—-Semi-diagrammatic representations of medial longitudinal sections of growing long bones of Bullfrog tadpoles. A. A
young stage in which cartilage is still the dominant element in
both diaphysis and epiphysis. In the diaphysis, however, the periosteum has already replaced some of the cartilage with circumferential bony lamellae. Also a blood vessel along with chondrioclasts
has invaded the cartilage, and is beginning to form the marrow.
B. A later stage in which the diaphysial cartilage has all been replaced by marrow and circumferential bone lamellae laid down by
the periosteum. Note that in this case there are not, and never
would have been, any. I-Iaversian systems, all the bone of the diaphysis being formed from periosteal lamellae. The epiphyseal cartilages, at this and the preceding stages, contain a lozenge-shaped
growing zone characteristic of the Frog. The epiphyses remain
permanently cartilaginous in this animal. After studies by Marvin.
9
THE APPENDICULAR SKELETON 253
epiphysis
  .. __ _
l ’ lozenge
l shaped
«,3 region
. 4,
diaphysis
circumferential membrane
depositing bone lamellae
marrow
Fig. 135.—The epiphysis and part of the diaphysis of a developing
Bullfrog femur in a condition similar to that diagramed in Fig. 134, A.
Note the cap of epiphyseal cartilage extending down on either side of
the diaphysis. Also in this cap note the lozenge-shaped region of dividing cells. On each side of the diaphysis the heavy lines represent.
dense circumferential connective tissue within which the layers (lamellael of circumferential bone are about to form. A small region of
marrow which occupies the middle portion of the bone shows at the
lower edge of the picture. (Author’s photograph of preparation by
Marvin.)
el’s cartilage remains small throughout larval life, but constitutes the
core of the lower jaw in the adult-.
The hyoid arch (Ceratohyal) and the second branchial arch, together
with certain median elements, form the hypobranchial apparatus of
the adult. In the latter the hyoid arch becomes the so-called hyoid
(greater) cornu or horn, while the second branchial arch becomes the
lesser cornu. All of the other arches disappear entirely at metamorphosis (Figs. 132, 133). A \
254 THE FROG: LATER OR LARVAL DEVELOPMENT
THE APPENDICULAR SKELETON
Both the pectoral and pelvic girdles are said to be endochonclral in
origin, with the exception of the clavicle, which as in other animals is
a membrane bone. The long bones of the limbs are also usually thought
of as endochondral, but in the Frog, unpublished investigations by
R. W. Marvin (’47) in the author’s laboratory would seem to show that
in a strict sense they are not so at all. In the case of these bones in this
animal what appears to occur is this:
A cartilaginous core as usual first replaces the condensed mesoderm
or membrane, and around this the bone is later laid down exclusively by
the periosteum in circumferential layers (Fig. 134»). The cartilage is
then removed, as well as some of the first formed inner layers of bone.
This removed material, however, is all replaced by marrow, none of it
by bone. Hence if this account is correct there is no true endochondral
bone involved, i.e., none which replaces cartilage or bone preceded by
cartilage in the manner described above. The situation as so far indicated refers only to the bone shaft, i.e., the part defined in all such
bones as the diaphysis. The condition at the ends, whichare known as
the epiphyses, remains to be discussed. In the case of the Frog the ends
of the cartilaginous cores of the shaft of a long bone never become
ossified at all, even after all growth has ceased. Thus the ends or epiphysis in this case consist of permanent caps of cartilage whose borders extend down somewhat over the bony cylinders which constitute
the diaphysis (Fig.4 135) . These procedures in both diaphysis and epiphyses are at variance, as we shall see, with what occurs in both the Bird
and the Mammal, which also differ somewhat from each other.
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256 THE FROG: LATER OR LARVAL DEVELOPMENT
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Vogt, W., “Operativ bewirkte ‘ Exogastrulation’ bei Triton und ihre Bedeutnng
fiir die Theorie der Wirbeltiergastrulation,” Verh. d. Anat. Gesell., LV, 1922.
—“ Gestaltungsanalyse am Amphibienkeim mit iirtlicher Vitalflairbung,” Arch.
Entw.-mech., CVI, 1925.—“ Ueber Wachstun und Gestaltungsbewegungen am
hinteren Kfirperemde der Amphibian,” Verh. J. Anat. Gesell., LXI, 1926.
Weber, A., “ Etude de la torsion de Pébauche cardiaque chez Rana esculenta,” Bibliographic Anatomique, XVIII, 1908 (1909).
Wilder, H. H., History of the Human Body, New York, 1909.
Witschi, E., “Studies on Sex Differentiation and Sex Determination in Amphibians,” I. “Development and Sexual Differentiation of the Gonads of Rana
sylvatica.” Jour. Exp. Zoc'il., LII, 1929.——‘‘ Studies on Sex Differentiation and
Sex Determination in Amphibians. II. Sex Reversal in Female Tadpoles of
Rana sylvatica Following the Application of High Temperature,” Jour. Exp.
Zob'l., LII, 1929.—-“VI. The Nature of Bidder’s Organ in» the Toad,” Am.
Iour. Anat., LII, 1933.—“ VIII. Experiments on Inductive Inhibition of Sex
Differentiation in Parabiotic Twins of a Salamander,” Anat. Rec., LXVI, 1936.
-—“ IX. Quantitative Relationships in the Induction of Sex Differentiation, and
»
V.
260 THE FROG: LATER OR LARVAL DEVELOPMENT
the Problem of Sex Reversal in Parabiotic Sainruanders,” Iour. Exp. Zob'l.,
LXXV, 1937.——“ The bronchial columella of the ear of larval Ranidae,” Jour.
Morph., XCVI, 1955. .
Yntema, C. L., “An Experimental Study of the Origin of the Cells which Con.
stitute the Vllth and Vlllth Cranial Ganglia and Nerves in the Embryo of
Amhlystoma punctatum,” Jour. Exp. Zo6l., LXXV, 1937.—“An Experimental
Study on the Origin of the Sensory Neurones and Sheath Cells of the IXth and
Xth Cranial Nerves in Amblystoma punctatum,’ Jour. Exp. Zo5l., LXLII, 1943.
Zwilling, E., “An Experimental Analysis of the Development of the Anuran Olfactory Organ,” Iour. Exp. Zo6l., LXXXIV, 194-0.~—-“ The Determination of
the Otic Vesicle in Rana pipiens,” Jour. Exp. Zo6l., LXXXVI, 194-1.
APPENDIX To Face BIBLIOGRAPHY
, Ballard, W. W., “Cortical ingression during cleavage of Amphibian eggs, studied
by means of vital dyes,” Jour. Exp. Zoc'il., CXXIX, 1955.
Barth, L. G., Embryology, New York, 1953.
Brunet, J. A. and Witschi, E., “ Pluripotentiality of the mesonephric blastema and
the mechanism of feminization of male salamanders by androgenic hormones,”
Anat. Rcc., CXX, 1954.
Calkins, C. N., “ The restoration of vitality through conjugation,” Proc. Natl. Acarl.
Sci., V, 1919.
Chang, C. Y., “Parabiosis and gonad transplantation in Xenopus laevis daudin,”
Jour. Exp. Zob'l., CXXIII, 1953.
Finnegan, C. V., “Studies on erythropiesis in salamander embryos,” Jour. Exp.
Zob'l., CXXII-I, 1953.
Hibbard, H., “Contributions £1 l’étude de l’Ovogenese de la fecondation, et de
Yhistogenése chez Discoglossus pictus otth,” Arch. de Biol., XXXVIII, 1928.
Holtzer, H., “ An experimental analysis of the development of the spinal column.
I. The dispensability of the notochord,” Jour. Exp. Zo5l., CX'Xl, 1952.
Jennings, H. 5., “ Paramecium hursaria: Life History. Age and death of clones in
relation to the results of conjugation,” Jour. Exp. Zoi7'l., XCVI, 1944.
Kemp, N. E., “Synthesis of yolk in the oiicytes of Rana pipiens after induced
ovulation,” Jour. Morph., LXLII, 1953.
Kollros, J. .l., “The development of the optic lobes in the Frog. I. The efiects of
unilateral enucleation in embryonic stages.” Jour. Exp. Zot'il., CXXIII, 1953.
Liedke, K. B., “Lens competence in Amblystoma punctatum,” Jour. Exp. Zob'l.,
CXVII, 1951. V
Nicholas, J. S., “ Blastulation, its role in pregastrular-organization in Amblystoma
punctatum," Jour. Exp. Zo6l., C, 1945.
Nieuwkoop, P. D., “Experimental investigations on the origin and determination
of the germ cells and on the development of the lateral plates and germ ridges
in Urodeles,” Arch. Neerl. Zob'l., VIII, 1947.
Segal, S. J ., “ Morphogenesis of the oestrogen induced hyperplasia of the adrenals
in larval frogs,” Anat. Rec., CXV, 1953.
Sonneborn, T. M., “Mating types and groups, lethal interactions; determination
and inheritance,” Am. Na£., LXXIII, 1939. _
Ting, Han-po Paul, “ Diploid androgenetic and gynogenetic haploid development
in Anuran hybridization,” Jour. Exp. Zo6l., CXVI, 1951.
Townes, P. L. and Holtfreter, J., “ Directed movements and selective adhesion of
embryonic Amphibian cells,” Jour. Exp. Zo6I., CXXIX, 1955. ;
Wilens, S., “ The migration of heart mesoderm and associated areas in Amblystoma }
punctatum,” Jour. Exp. Zo5l., CXXIX, 1955. E
Wittek, M., “La vitellogenese chez les Amphibiens," Arch. de Biol., LXIII, 1952. '
Woodruil, L. A. and Erdmann, R., “ A normal periodic reorganization process without cell fusion in Paramecium,” Jour. Exp. Zob'l., XVlI, 1914.
1., .,..§.xs.c.z
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PART
THE TELEOSTS AND GYMNOPHIONA
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HE TELEOSTS AND GYMNOPHIONA: THEIR SEGMENTATIQN AND GASTRULATION
BE F 0 RE beginning the study of the Chick, it is desirable to give a
very brief account of the processes of segmentation and gastrulation in
the Teleosts (Bony Fishes) and the Gymnophiona. It is of advantage to
understand these processes in the forms mentioned because embryologicall-y they are intermediate between those found in the Frog and
those in the Reptile or Bird, i.e., the Sauropsids. This of course is not
meant to imply that modern Fishes, Amphibians, and Sauropsids form
a direct phylogenetic series. It is merely suggestive in a general way of
the manner in which the embryological conditions in the lower forms
have apparently been modified in the process of evolution.
THE TELEOSTS
SEGMENTATION
In the Frog the yolk is more or less concentrated in the vegetal half
of the egg, but is not sufliciently dense to prevent the whole egg from
segmenting. In the Teleosts, on the contrary, the concentration of yolk
is very marked, so that the protoplasm exists only as a thin plate upon
the animal pole. As noted in Chapter II, this plate is called the blastodisc, and from it the entire embryo arises, the remainder of the egg being purely nutritive. In these eggs, therefore, when segmentation begins,
the process is confined to this disc, and is said to be meroblastic or discoidal, as opposed to the holoblastic or total cleavage of Amphioxus
and the Frog (Fig. 136).
The first two planes of division pass entirely through the disc and "at
right angles to one another. Normally the third cleavage is at right angles to the second, so that at this point the pattern may be described as
bilateral with respect to the plane of the latter cleavage. This feature is
further emphasized in many Teleost eggs by the temporary lengthening
of the blastodisc along the axis of this second plane. Thus instead of
being circular at this stage the disc is an oval (almost an oblong), its
long axis commonly consisting of two rows of four cells each. The
r
THE TELEOSTS: SEGMENTATION 263
fourth cleavages then generally come in at right angles to the first so
that we have four rows of four cells each, two on either side of the second cleavage plane, i.e., on either side of the long axis of the oval (Fig.
137, C). However, shortly after this the dividing blastodisc ceases to be
Fig. 136. —— Egg of the Teleost, F undulus heteroclitus. From KelIicott (General Embryology). Total view, about an hour after let'tilization.
c. Chorion. d. Protoplasmic germ disc or blastodisc. 0. Oil vacuoles. p. Perivitelline space. 11. Vitelline membrane. 9'. Yolk.
an oval and again becomes circular. Further cleavages ensue, and the
disc is thus presently transformed into the blastoderm. This consists of
small cells whose original relationships are impossible to trace unless:
vital stains or other means of identification have been employed. Be
tween this blastoderm and the yolk, a space has meanwhile developed.
which is termed the segmentation cavity, and which corresponds to the
L cavity of the same name in the Frog (Fig. 137, D, E). Thus the egg has
become a blastula. ,
In the yolk around the margin of the blastoderm are a number of
nuclei (yolk nuclei) derived partly from the blastoderrnal edge, and
f’ partly perhaps from extra sperm (merocytes). These nuclei presently
I T begin to divide amitotically, and become amoeboid, in some cases mi264 THE TELEOSTS AND GYMNOP;HIONA
grating centrally beneath the blastoderm. Here they occupy the thin
layer of protoplasm forming the floor of the segmentation cavity, which
thus has the character of a syncytium. This syncytium or periblast, as
it is termed, presently spreads over the entire yolk, and is perhaps instrumental in making the latter assimilable by the cells of the blastederm. At all events, it finally disappears without taking any part in the
formation of the actual embryo; hence it need not be considered further.
Fig. 137.—Cleavage in the Sea-bass, Serranus atrarius. From H. V. Wilson. A.
Surface view of blastoderm in two-cell stage. B. Vertical section through four-cell
stage. C. Surface view of hlastoderm of sixteen cells. D. Vertical section through
sixteen-cell stage. E. Vertical section through late cleavage stage.
Central periblast. m.p. Marginal periblast. s.c. Segmentation cavity (blastecoe .
GASTRULATION
There have been several attempts to discover what determines the
antero-posterior axis in the Fish, but none in the writer’s opinion has
been very successful, including his own. It is a fact that in the forms
which have been studied this axis usually coincides with the second
plane of cleavage. But this is not always so, and what causes the variation no one really knows. Whatever the determining factor or factors
may be the axis becomes manifest with the advent of gastrulation.
THE TELEOSTS: GASTRULATION 255
Irlvolution.—In that region of the blastoderm which is destined
to form the posterior end of the animal, the blastodermal rim begins to
turn under, i.e., is involuted. Thus, in this region a lower layer of cells
begins to spread anteriorly into the segmentation cavity beneath the
blastoderm. It is the hypoblast, destined later to give rise to the endoderm, notochord and rnesoderm, while the remaining upper layer is the
epiblast. The margin of the blastoderm where the involution is occur
arche ceron
 
 
 
   
thickened epiblast
of head re ‘on
KupFfer's gl
vesicle hypoblasg
dorsal
blastoporal
Ilp
ventral
blastoporal
lip
periblast layer.
Fig. 138.—Diagram of a median sagittal section of a
Teleost gastrula shortly before the closure of the blastopore. From H. V. Wilson, slightly modified.
ring, constitutes the dorsal blastoporal lip, while the former segmentation cavity now lying between the spreading hypoblast and the yolk is
the archenteron, (Figs. 138, 139). The new cavity, like its predecessor,
is obviously extremely shallow, and though roofed by the hy poblast is
open below to the surface of the yolk, or more strictly speaking to the
thin syncytial layer of periblast. Lastly, it is to be noted that while the
process of involution is most active at the posterior edgeof the blastederm, it is also occurring to a much lesser degree all around the margin.
Epiboly. —-While involution is thus progressing chiefly at the posterior edge of the blastoderm, very active epiboly is taking place about
the remainder of the blastodermal margin, the result being to envelop
the entire yolk with an epiblastic covering of cells, the yolk-sac, and
concurrently to close the blastopore. In such cases, as suggested in
Chapter II, it is possible to regard the entire rim of the growing blastederm as the blastoporal lip. Thus while the posterior edge is recognized
Wo .
'?
l
",
-  WWW,‘-rear‘:
266 THE TELEOSTS AND GYMNOPHIONA
as the dorsal lip, the lateral edges must be regarded as the lateral lips
and the anterior edge as the ventral lip. It may be noted, furthermore,
that in some forms, e.g., Serranus, the Sea Bass, according to Wilson
(’89) , the epibolic process is most rapid‘ at the anterior edge (ventral
lip), and decreases along either side until at the posterior edge (dorsal
lip) it is comparatively slight. Under such circumstances the above
homology is particularly obvious because, owing to its relatively rapid
growth, the anterior edge passes clear around the vegetal pole and up
Fig. 139.—Sagittal sections through the blastoderm of Serranus during the formation of the germinal layers. From Jenkinson (Vertebrate Embryology). After
H. V. Wilson. A. Beginning of involution and slight epiboly at dorsal lip (d.l.) B.
Epiboly at anterior edge. C Further progress of involution at dorsal lip.
d.l. Dorsal lip. par. Parablast (periblast).
on to the posterior side, thus becoming actually a ventral lip in position
as well as in name (Figs. 138, 14-0) . How widespread among Fish
eggs this characteristic of the relatively excessive growth of the anterior edge of the blastoderm may be cannot be definitely stated,
because in most descriptions the point is not made clear. This is due
partly perhaps to difficulty in many cases of being sure of the constant orientation of the parts of the egg, which in the Sea Bass is said
to be fixed by the position of the oil globule. In at least one other instance, however, i.e., that of the oval egg of Hemichromis (McEwen
’30) , this orientation is equally well or better established by the shape
of the egg. In this case the blastoderm is at one end of the oval, and the
egg does not normally turn end over end within its chorionic membrane
because of the stiffness of the latter and its own viscosity. It is thus possible to observe that epiboly, unlike that in Serranus, is clearly equal on
all sides. Hence the blastopore obviously closes on exactly the opposite
side (end) of the egg from the original animal pole (Fig. 141).
Fig. 140. - Growth of the blastoderm over the yolk (epiboly) after the formation
of the material for the embryo in the Teleostan fish Serranus. From Jenkinson
(Vertebrate Embryology). After H. V. Wilson. A Lateral view of a very early stage
of gastrulation. B. Dorsal view of a much later stage. C. Lateral view of the same
stage as B. D. Lateral view of a late stage, gastrulation almost complete.
a’.l. Dorsal lip of the hlastopore (posterior edge of the blastoderm). a.e. Anterior
edge ofthe hlastoderm or ventral lip (v.l.) of the blastopore. s.c. Segmentation cavity. o.g. Oil globule.
Concrescence or Conve1'.gence.—The Fish, as previously stated,
is.the form in connection with which the theory of concrescence originated, and it may be that this process does occur here to a limited extent. However, as in other cases, it is now considered that the movement
which takes place in this form is more aptly designated as convergence _
(Oppenheimer, ’36). It goes on of course along with the epiboly, and
seems to involve two things. There is on the one hand some actual con
cresence or confluence of material in the germ ring on either side of
the dorsal lip of the blastopore. The greater part of this material, how268 THE TELEOSTS AND GYMNOPHIONA
ever, flows more directly, partly toward the lip and partly toward the
median line, i.e., it converges toward these regions (Fig. 14-2) . This and
the involution leads to a piling up of cells in a somewhat shield shaped
area anterior to the dorsal blastoporal lip, the base of the shield being
dorsal blastoporal lip
microp yle
   
 
ventral
blastoporal
lip
chorlon
embryonic
shield
ventral
blastoporal
lip
dorsal blastoporal lip
C D
Fig. 141.—/1 and B early stages, C and D, late stages in the gastrulation of the
Teleost. Hemichromis bimaculata. A and C are dorsal views, B and D are lateral
views. Note the equal epibolic growth of the blastoporal lips, unlike the condition
in Serranus.
adjacent to the lip. This area is in fact known as the embryonic shield,
and it is along its median longitudinal axis that the outline of the embryo presently appears as indicated in Fig. 141, C.
Meanwhile as the lips of the blastopore finally close posterior to the
shield they leave, at least in some embryos (Sea Bass, H. V. Wilson), a
short thickened line of cells. At the anterior end of this line is a slight
cavity extending upward from the shallow archenteron (Figs. 138, 143) .
MESODERM, NOTOCHORD, ENDODERM 269
It is called Kupfier’s vesicle, and seems to be an incipient neurenteric
canal. It cannot be a genuine neurenteric canal since the nerve cord, because of its peculiar method of formation in the Fish, does not yet itself
possess a lumen. At the posterior end of the thickened line is the place
of final blastoporal closure, and probably also the place where the future anus opens. However, since the Fish unlike the Frog does not have
Fig. 142.—A diagrammatic representation of the process of convergence, and incidentally a small amount of involution, essentially as they are thought to occur in
the Teleosts, as well as in some other forms. A. Surface view of the blastoderm at
the beginning of the processes. 3. A similar view near the completion of gastrulation. Changes in the positions of the letters and the directions of the arrows represent the movements which are supposed to have occurred. Dotted letters and arrows
indicate regions which have been involuted underneath the margin, and hence
would be invisible from above.
a proctodael invagination to mark this spot, the latter point is not certain. Assuming, nevertheless, the homology of Kuplfer’s vesicle with a
neurenteric canal, and the place of blastoporal closure with the anus,
the thickened line is evidently the homologue of the primitive streak of
the Amphibian. On this basis it may be so designated. The mass of cells
in and around the more posterior portion of it, however, because of their
character and future history, are often designated as the caudal knob.
Thus is produced, the Teleostean gastrula.
THE DIFFERENTIATION OF MESODERM, NOTOCHORD,
AND DEFINITIVE ENDQDERM
It has been stated that involution occurred chiefly at the dorsal lip of
the blastopore. The result is that in the region anterior to this lip, i.e.,
the region of the embryonic shield, the roof of the archenteron consists
of an extensive double layer of cells produced by this process. From the
dorsal side of the lower or involuted of these two layers (hypoblast),
270 THE TELEOSTS AND GYMNOPHIONA
between it and the overlying epiblast, the mesoderm is now delaminated
in two sheets situated upon either side of the middle line (Fig. 144).
Presently, also, the hypoblast along the middle line itself becomes separated from that upon either hand, and is aggregated into an axial rod,
the notochord, with the sheets of mesoderrn upon each side of it (Figs.
144, 145). What remains of the original hypoblast may now be spoken
of as endoderm, destined to form the lining of the gut. Since, however,
 
 
 
559 .
l§él§l?{
vatlxxrn \*—__
   
Fig. 143.— Sagittal section through the hinder end of a Fish ern—
bryo (Serranus), showing the undifferentiated primitive streak, an
terior to which the structures of the embryo are being differentiated.
From H. V. Wilson.
a.p. (v.l.). Anterior margin of the blastoderm or ventral lip of
blastopore, after having grown entirely around the yolk mass. bl.
Blastopore. ec. Ectoderm. en. Endoderm. g.r. Germ ring. k.v. Kupfer’s vesicle. nc. Notochord. nr. ch. Nerve cord. p. Periblast. pp.
(zl.l.). Posterior margin of blastoderm (dorsal lip of blastopore). pr.
str. Primitive streak.
the formation of the notochord consumed all of the primordial cells
along its line of origin, the definitive endoderm consists for a short time
of two separate lateral sheets. Shortly, these sheets unite with one another beneath the notochord, and the enteric roof is thus again complete.
The uppermost layer may now of course be designated as ectoderm.
CONSIDERATIONS CONCERNING THE ULTIMATE ORIGINS
OF THESE LAYERS
It remains to be noted that although the involution of the hypoblast
comprising potential endoderm, mesoderm and notochord, occurs chiefly
at the dorsal blastoporal lip, the material for these layers does not all
originate here. As in the case of the Frog we have seen that about this
region there exists a process of convergence whereby materials anterior
and lateral to the lip are carried toward it before they are involuted to
the interior. The pregastrular locations of the different components of
this hypoblast are indicated somewhat diagrammatically in Figure 146
ORIGINS OF THE LAYERS 271
taken from Oppenheimer’s studies on Fundulus. Her conclusions were
reached both by various grafting experiments and, as in the Amphibia,
by marking with vital stains. From them it appears that at least a considerable part of the mesoderm and endoderm of the Fish embryo is derived from the posterior third or so of the blastoderm and from its
margins.
Oppenheimer has also confirmed earlier work of a different sort by
Stockard to the effect that
the more anterior parts of
the blastoporal lip have
capacities which are not
normally realized. Thus
any part of the blastedermal margin if cut out
and implanted into the
embryonic shield may differentiate into a variety
of structures which it
would never form in its V
- - Fig. 144.——Transverse sections through the difusual location‘ This may ferentiating blastoderm of Serranus showing difsuggest an inductive effect ferentiation of the roof of the archenteron into
an the transplanted mm 3::‘;:*"z:‘3..z3'f°’:;;;.**;:::;*:1::: ‘z;::;:.a.::;‘% $233;
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the shield. It also may Wfl5°”'
mean that the material in various parts of the margin possesses inherent
potentialities which are normally inhibited as this material is involuted
over the dorsal blastoporal lip (Oppenheimer, ’38). To this limited extent therefore the blastodermal margin (entire lip of the blastopore)
may still be thought of as containing potentially the germ of any part, or
all, of an embryo. Hence in this highly modified sense the use of the
term germ ring as applied to this margin may still be justified. Finally,
in connection with matters pertaining to pregastrular materials, Oppenheimer (’36) finds that blastoderms removed from the yolk and periblast previous to the 16-cell stage fail to gastrulate. Instead they behave
somewhat like the upper quartet of cells from a Triton 8-cell stage which
have been isolated from the lower four cells containing the gray crescent. For this reason this investigator suggests that perhaps the periblast
of the 16-cell Fundulus contains a substance which influences the later
destinies of these cells, but which has not previously had time to act.
There is thus the implication that perhaps this periblastic substance has
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272
THE TELEOSTS AND GYMNOPHIONA
an organizing effect somewhat comparable to that which occurs in the
gray crescent region of the Amphibian.
EARLY FORMATION OF THE EMBRYO
As soon as the germ layers are formed in the embryonic region of
the blastoderm, and while the remainder of the latter is still in the process of enclosing the yolk, the outlines of the embryo begin to become
   
Z_.-.....__‘
\€?n’7E’E'v*E5
 
Fig. 145.--Formation of the gut (al.e.)
in Serranus by the bending down of the
sides of the roof of the archenteron. In A
note also the nerve cord forming by a solid invagination of ectoderm (characteristic of many Teleosts) instead of by folds.
From Jenkinson (Vertebrate Embryol
ogy). After H. V. Wilson.
s.n.ch. Sub-notochordal rod. end. Endo
derm.
 
clearly evident. This is the result
of a folding ofi7 process by which
the embryo is gradually raised
above the surface of the yolk. It
is to be noted that although these
procedures are fundamentally
similar to what will presently be
described in the Bird, there is one
important difference. In the lat—
ter, in spite of the constriction of
all three layers beneath the embryo due to the folding off, all
three nevertheless take part in
enclosing the yolk mass. In the
Fish on the other hand the folding ofi of the endoderm is
quickly completed to form a
closed tube, the primitive gut.
Hence only the ectoderm and
mesoderm constitute the rather
wide yolk stalk, and the covering
of the yolk, the yolk-sac (Figs. 144, 14-7). Aside from this difference
further early development of Fish and Bird is generally similar. By virtue of the folding, accompanied by rapid growth in all directions, the
embryo soon comes to extend outward above the yolk-sac which is attached like a bag to its ventral side. The tail in the Fish, it may be noted.
is largely formed by outgrowth from the caudal knob.
THE GYMNOPHIONA
SEGMENTATION
Segmentation in these somewhat aberrant Amphibians is again virtually meroblastic, and hence results in the formation of a blastula with
T,
THE GYMNOPHIONA: GASTRULATION 273
a blastoderm. and segmentation cavity very similar to that of the Teleost.
In this case, it is true, there is a slight superficial cleavage in the yolk
which forms the floor of the cavity, and this also extends out around
the periphery of the blastoderm. The burl: of the yolk nevertheless, remains undivided.
GASTRULATION
Involution and Epibo1y.——The advent of gastrulation becomes
evident by the occurrence of involution and epiboly at what proves to
be the posterior edge of the
blastoderm. i.e., the dorsal
blastoporal lip. As an obvious result of the involution
there are presently produced
the usual two layers of cells.
The outer is the epiblast beneath which the inner hypoblast spreads out within the
segmentation cavity above
the partially segmented yolk.
The method is made~evident
by reference to the median
longitudinal, sections of the Fig. 14-6.——A diagram of an early Teleost
blastoderm in Figure 148, A
and B. Up to this point, it
will be noted, the movements
observed are not essentially
(Fundulus) blastula. After Oppenheimer. The
cells have been numbered for identification
purposes in discussion of subsequent stages by
the author, but are not pertinent to the account in this text. The point to be noted here
is the location at this stage of the areas which
will later form nervous system (vertical hatch
diflerent from those which ing), notochord (heavy stipple), endoderm
took place at a correspond- (light stipple) and mesoderm (horizontal
ing stage in the Fish. The hatching) '
point in which the gastrulation of the Gymnophiona digresses from that
in the forms thus far studied and to a slightly greater degree resembles
that in the Birds, remains, therefore, to he noted.
The. Gymnophionian Blastopore. —- A surface view of the blastederm as gastrulation commences (Fig. 149, A), will reveal the fact that
the posterior portion of the rim where involution is occurring has the
shape of a wide crescent, whose ends or horns bend backward. As the
process goes on, moreover, these horns continue to grow posteriorly,
and presently turn toward one another until they meet (Fig. 149, B, C,
D). It is furthermore to he noted that this movement has occurred rela274 THE TELEOSTS AND GYMNOPHIONA
tively rapidly, whereas the epiholy of the anterior side of the hlastoderm, so rapid in the Fish, has scarcely started. The results of these
processes compared with those in the Teleosts, as well as with those in
forms with less yolk, may now be stated as follows:
If the entire blastodermal rim is still regarded as the lip of the blaste
somatic
   
splanchnic ;
mesoderm _i
Fig. i4'7.—A diagram to illustrate the method of gut formation
and yolk coverage in the Fish. Note that the endoderm has folded
in to form the gut without covering the yolk at all, i.e., there is no
endoderm in the yolk—sac. The latter is covered by the periblast
(not a permanent cell layer) and by the two layers of mesoderm
and the ectoderm. The extent of the coelom at this stage is exag
gerated in the diagram.
‘pore ( germ ring), it must be said that the movements ‘just noted have
divided this lip into two portions.‘One of these is quite limited; 'i.e.,
it merely furnishes the boundary for the small area of yolk (yolk plug)
enclosed by the fused horns of the crescent (Fig. 149, C ). The second
portion of the original lip, on the other hand, bounds the entire remaining expanse of uncovered yolk. Moreover, since epiboly has been slight,
this expanse comprises almost as much yolk surface as existed prior
to the beginning of gastrulation. Such is the situation thus far indicated.
Upon the basis of subsequent development, however, it may be stated
5
4
l
l
5
THE GYMNOPHIONA: GASTRULATION - 275
_‘__m,,,,u~nn!I\lIl’.tlll
yrs».-0
Fig. 148.———Formation of the germ layers in Hypogeophis (a Gymnophionian).
From Jenkinson (Vertebrate Embryology). After Brauer. A-—C. Sagittal sections of
three successive stages. D. Transverse section through the blastopore and yolk plug
()r.p.l.
s.c. Segmentation cavity into which in B and C the archenteron (arch.) opens.
d.l. Dorsal lip. l.l. Lateral-lip. v.l. Ventral lip.
that the small area enclosed by the horns of the crescent is the only part
which really corresponds to the blastopore in the forms previously
studied. Hence, as would be expected, its ultimate closure gives rise to
a line of tissue quite homologous with the typical primitive streak, the
neurenteric canal arising at its anterior end and the anus at the other.
From this it appears that in the Gymnophiona, the anterior and most of
the lateral parts of the blastodermal rim take no part in forming the
ventral and lateral lips of the region which must be homologized with
276 THE TELEOSTS AND GYMNOPHIONA
a true blastopore, these lips being formed by the horns of the crescent.
Instead, the outer (anterior and most of the lateral) portions of the rim
are occupied merely with the gradual covering of the main body of the
yolk, long after the true blastopore has been definitely delimited.
Whether any convergence takes place before or during this delimitation
has not been ascertained. Very possibly it does.
Fig. 1_49.——Formation and closure of the blastopore in the Gymnophione. From Jenkinson (V erlcbrate Embryologyl. A—D. Surface views of
the blastoderm of Hypogeophis. After Brauer. The lateral lips are seen to"
meet behind and so form the ventral lip. y.p. Yolk plug. E. Embryo of
Ichthyophis lying on the partially segmented yolk which is still uncovered
by the blastoderm. After the brothers Sarasin.
It may now be noted that it is with respect to the relation of gastrulation proper and the belated enclosure of the yolk that the Gymnophiona come a step nearer to the condition in the Bird. In the
latter also, as we shall see, gastrulation, so far as the embryo is concerned, is completed long before the mass of the yolk is covered by the
epiboly of the blastodermal rim. However, this is as far as the resemblance goes. The Bird. it now appears, has no true blastopore related
to the embryo itself, and the so-called primitive streak. if homologous
with a blastopore, is formed in a different manner from any of the
streaks so far described. ‘
oA  . A
MESODERM, N OTOCHORD, ENDODERM 27 71
THE DIFFERENTIATION OF MESODERM, NOTOCHORD,
AND DEF INITIVE ENDODERM
By means of the above processes of epiboly and involution, there is
presently developed a telolecithal gastrula, whose lower or endodermal
layer forms a roof for the former segmentation cavity (now the archanteron) in much the same way as in the Teleosts. In the present case,
also, this layer soon gives rise to the mesoderm and notochord. The lat
 
   
 
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\“%“
y %@'l*Il:tZ£l!!l?ilVH'llzz
 
 
   
 
nmrmmm7; , V wmrnmum.
5-e’4’,€3.=111:fix:d1llilx“uinit:t‘<\3&‘
 
 
Fig. 150. —Transverse sections of Hypogeophis showing the differentiation of the roof of the archenteron into notnchord (»n.ch.)
and mesoderm and the formation of the gut (al.c.) by upgrowth of
yolk-cells from the sides. From Jenkinson (Vertebrate Embryology). After Brauer.
ter originates quite as in the Fish, but the formation of the mesoderm
differs in the way previously noted as characteristic of other Urodeles.
Thus in the Teleost it will be recalled that, though the development of
the notochord involved all of the hypoblast in the median line of the
embryo, the mesoderm on either side was merely split oil‘, leaving a
layer of endoderm beneath it. In the Gymnophiona, on the other hand,
the entire central portion of the archenteric roof which did not go to
form the notochord becomes mesoderm (Fig. 150) . There is no delamination, and the result is that within the central area of the blastoderm,
the enteric cavity for the time being is roofed only by mesoderm and notochord. In other words, in this case the central portion of the mesoderm,
as well as the notochord, consumes in its formation all of the hypohlast
beneath it. Presently, however, the encloderm in this central region is
supplied by the ingrowth of lower layer cells from about the margin
(Fig. 150). The uppermost layer as usual is now termed ectoderm and,
278 ’ REFERENCES TO LITERATURE
as in the forms previously studied, all three layers are continuous with
one another about the lips of the blastopore.
As will presently appear the methods of mesoderm and notochord
formation in the Teleosts and Gymnophiona are not particularly significant as regards an understanding of these processes in the Bird. Yet,
because as usual, their occurrence somewhat overlaps gastrulation as
strictly defined, an account of their character has been included for
the sake of completeness.‘
REFERENCES TO LITERATURE
CHAPTER VII
B auer, A., “Beitriige zur Entwickelungsgeschichte der Gymnophionen,” Zoal.
’ Jahrb.,X, 1897.
Brummett, A. R., “The relationships of the germ ring to the formation of the
tail bud in Fundulus as demonstrated by the carbon marking technique,” Jour.
Exp. Zob'l., 1954-.
Hertwig, 0. (Editor), Handbuch der vergleichenden und experimentellen Entwicke
lugslehre der Wirbeltiere, I, 1, 1, “Die Lehre von den Keimhl$a'.ttern,” Jena,
1903 (1906).
Hertwig, O. and 11., “Studies on the Germ Layers,” Jena Zeitschn, XIII—XVI
(VI-IX), 1879-1883.
His, W., “ Untersuchungen iiber die Entwickelung von Knochenfischen, besonders
iiher diejenige des Salmens,” Zeit. Anat. Entw., I, 1876.—“Untersuchungen
iiber die Bildung des Knochenfischembryo,” Arch. Anat. u. Enzw., 1878.
Jenkinson, J. W., Vertebrate Embryology, Oxford and London, 1913.
Kopsch, F., Untersuc-Izungen. iiber Gastrulation und Embryobildung bei den Chordaten, “I. Die Morphologische Bedeutung des Keimhautrandes und die Embryobildung bei der Forelle,” Leipiz, 1904.
Korschelt und Heider, Lehrbuch der vergleichenden Entwickelungsgeschichte der
wirbellosen Thiere, I, “ Experimentelle Entwickelungsgeschichte,” Jena, 1902.
———Lehrbuch, etc., III, “ Furchung und Keimblatterbildungf’ Jena, 1909-1910.
McEwen, R. S., “ The Early Development of Hemichromis bimaculata with Special
Reference to Factors Determining the Embryonic Axis,” Jour. Morph. and’
Physiol., XLIX, 1930.
Oppenheimer, J. M., “Processes of localization in developing Fundulus,” Jour.
Exp. Zob'l., LXXIII, 1‘936.—“Potencies for differentiation in the teleostean
germ ring," Jour. Exp. Zo5l., LXXIX, 1938.
Sumner, F. B., “Kupfiefs Vesicle and its Relation to Gastrulation and Concrescence,” Mem. N. Y. Acad. Sci., II, 1900.——“A Study of Early Fish Development: Experimental and Morphological,” Arch. Entw.-mech., XVII, 1903.
Wilson, H. V., The Embryology of the Sea Bass (Sermnus atrarius), (Bull. U. S.
Fish Commission, IX), 1889.
1 Brummett ’54 has made a study of gastrulation in the fish, F unziulus, marking
the blastodermal margin (germ ring) with carbon particles instead of stain, and
concludes that, somewhat contrary to Oppenheimer and others, there is very little
confluence or convergence in this form. Only the regions of the ring at, and quite
near' (less than 90 degrees from) the incipient dorsal lip, are involved, and they
form only the extreme posterior of the embryo and tail bud.
PART IV
THE DEVELOPMENT OF THE CHICK
HE CHICK: THE ADULT REPRODUCTIVE ORGANS,
AND THE DEVELOPMENT OF THE EGG PREVIOUS
TO GASTRULATION
T H E Chick has long been an object of ernbryological interest, and
the study of its development has been connected with such classical
names as Malpighi (1672), Wolff (1759), and Von Baer (1828). In the
more modern era of science, moreover, workers in this field have continued to study it, until at the present time probably more details
regarding its development are known than in the case of any other animal. As will appear, however, certain points concerning the very early
stages are even yet in doubt, and are still under investigation.
Some of the reasons for the importance of this form and the study
which has been given it may be briefly indicated. In the first place the
material is usually easy to obtain and observe throughout most of the
developmental stages. Furthermore, unlike the Frog or Fish, the Chick
embryo, in common with those of other Birds as well as with those of
Reptiles, possesses certain very significant extra-embryonic membranes
and appendages. The significance of these structures lies not only in
their character and functions in the groups just cited, but also in the
fact that the same appendages and membranes occur also in the Mammals, though in a somewhat modified condition. Lastly, aside from the
features already indicated, the general development of the Chick is
more nearly mammalian than that of any of the forms previously considered.
In the following account we shall begin with a brief description of
the reproductive organs of the adult Bird.
REPRODUCTIVE ORGANS OF THE ADULT, OCDGENESIS
AND OVULATION
THE MALE
The male Bird, or Cock, possesses a pair of testes, each of which is
an ellipsoidal body about two inches long and one inch in diameter.
THE FEMALE 231
It is made up of seminiferous tubules and supporting tissue, and, as in
the case of the Frog, is rather closely attached to the dorsal wall of the
coelom by a fold of coelomic epithelium, the mesorchium. By way of
'the vase e flerentia, each testis discharges its products into its respective
Fig. 151. — Section of an ovarian ovum of the Pigeon, drawn from a preparation of
Mr. J. T. Patterson. From Lillie (Development of the Chick) . The actual dimensions of the ovum are 1.44 x 1.25 mm.
f.s. Stalk of follicle. G.V. Germinal vesicle. Gr. Granulosa. L. Latebra. p.P. Pe
ripheral protoplasm. pr.f. Primordial follicles. T h.ex. Theca externa. T hint. Theca
inter-na. Y.Y. Yellow yolk. Z.r. Zdna radiate.
vas deferens. The latter duct then leads to the cloaca, where its entrance
is marked by a papilla. There is some evidence that the sperm attain
their motility and functional capacity by the action of a testis hormone
during their passage through the vasa eflerentia (Munro, ’38).
THE FEMALE
The Ovary.—In the embryo Chick two ovaries are present, but
only the left develops. In the adult Fowl this is suspended from the
282 THE CHICK
Fig. 152.—-Reproductive organs of the Hen. (After Duval, based on a figure by
Coste). From Lillie (Development of the Chick). The figure is diagrammatic in
one respect, namely, that two ova are shown in the oviduct at different levels; normally but one ovum is found in the oviduct at a time.
1. Ovary; region of young follicles. 2 and 3. Successively larger follicles. 4. Stigmata (cicatrices), or non-vascular areas, along which the rupture of the follicles
takes place. 5. Empty follicle. 6. Cephalic lip of ostium. 7. Funnel of oviduct
.(ostium tubae abdominale‘ 5?. 0"-fin in the upper part of the oviduct. 9. The mag
num, where most, if not all, the albumen is actually secreted. 10. Albumen surrounding an ovum. 11. Ovum in portion of duct laid open to show it. 12. Germinal
disc. 13. The isthmus where the shell membrane is secreted, and possibly some thin
albumen. 14. The uterus where shell is secreted, and both layers of thin albumen
separated from remainder, producing thick albumen and chalazae (see text). 15.
Rectum. 16. Reflected wall of abdomen. 17. Anus, or external opening of cloaca.
THE FEMALE ‘ 233
body wall by the mesovarium in about the same position as the left
testis in the male. It consists of the usual vascular connective tissue
elements, or stroma, within which are imbedded ova in various stages
of growth. Each ovum is surrounded by a layer of follicle or granulosa
cells, and these in turn are encased in a sheath of the stroma called the
theca. It is sometimes customary to refer to such stages together with
their coverings as simply follicles (Fig. 151) . Normally only one ovum
matures at a time, though there may be several not many hours apart.
The Genital Tract.—-As in the case of the ovary, only the left
genital tract develops. This fact is apparently correlated with the production by Birds of fragile shelled eggs, such that the coming together
~ of two at the cloaca would be disastrous. In this connection it is of
some interest to note that although in certain species of Hawks there
are two fully developed ovaries, there is still only one genital tract
(Stanley and Witschi, ’4«0) . As regards this tract, we find that it opens
anteriorly adjacent to the ovary and posteriorly into the cloaca just
dorsal to the anus. Also it is suspended as usual from the dorsal body
wall by a mresentery-like fold of peritoneum, and in the Birds it may be
divided into three main parts as follows:
I . The Oviduct Proper. This is the anterior part and is itself divisible
into three sections:
(a) The Infundibulum or Ostium. This is a thin-walled muscular
funnel, the inner surface of which is lined by ciliated epithelium. It is
in the immediate neighborhood of the ovary, but does not directly connect with it. A '
(17) The Magnum. This is sometimes called the “ glandular portion,”
but since other parts are also glandular this is not a very good designation. The part in question is a long much convoluted tube following
immediately after the ostium. It leads into:
(c) The Isthmus. This is a shorter tube also glandular whose pos
terior end marks the termination of the oviduct proper.
II. The Uterus. This is a relatively short, dilated portion whose walls
are also glandular. It immediately follows the isthmus and leads into
the third and last main division: ‘
II I . The Vagina. This region is likewise short, but thin-walled, and
opens into the cloaca (Fig. 152).
The Ofigonia. ———The origin of the primordial germ cells and their
multiplication as oiigonia occur during the embryonic life of the Chick.
Thisearly history will therefore be dealt with later in connection with
the development of the gonadswkt the time of hatching, however, the
284 THE CHICK
oéigonia are said to have ceased to divide, and each is becoming surrounded by follicle cells preparatory to growth (Fig. 153). They may
now, therefore, be called oéicytes, or young ova, whose history from this
point onward will be taken up in more detail.
The Growth Period.
The Vitelline Membrane or Zona Radiata. — There now appears surrounding each ovum or oiicyte a membrane which is called the vitelline
membrane. Whether it is a true vitelline membrane arising entirely
from the surface of the egg itself, or whether it is secreted by the follicle cells and is therefore chorionic in character, is somewhat uncertain. As this membrane thickens slightly, it becomes pierced by minute
canals; for this reason it is also referred to sometimes as the zona radiata. Throughout these canals by way of the follicle cells the egg receives nourishment from the surrounding theca.
The Germinal Disc. —At first the nucleus occupies the center of the
oficyte, and the yolk granules are deposited in the cytoplasm around it.
This presently results in the existence of yolk-free cytoplasm only
around the periphery of the egg. This cytoplasm, however, is thicker
upon the side where the theca of the ovum is attached to the ovary; this
thickening is called the germinal disc (blastodisc) . Meanwhile the
ovum has been growing, and by the time it has become .6 mm. in diameter, the nucleus has migrated into this disc (Fig. 151).
The Deposition of Yolk. -——The growth of the ovum is largely due
to the deposits of yolk, which it appears occur in the following manner:
The nucleus, as noted, occupies at first a central position around which
the yolk begins to be formed. This‘ yolk is of a lightish color termed
white yolk, and the central mass of it which is thus deposited is known
as the latebra. Following this the peripheral layer of the protoplasm
starts to deposit around the latebra a darker colored substance, the yellow yolk. As the egg is thus enlarged, the nucleus, as indicated, leaves
its central location and takes a peripheral position, which it maintains
during subsequent growth. The result is that the yellow layer is everywhere interrupted along the path which the nucleus has taken. Along
this path there is thus left a continuous deposit of white yolk extending
from the latebra almost to the surface. It is known as the neck of the
latebra, and just beneath the blastodisc it spreads slightly to form a
plate, the nucleus of Pander (Fig. 154, B).
It should be noted that in some instances the deposit of yellow yolk
is interrupted by intermittent, usuallkthinner, layers of more white
THE FEMALE
E
Fig. 153. ——Growth stages in the oiigenesis of the Hen’s egg. From
Kellicott (Chordute Development). After Sonnenbrodt. A. Oiicyte
measuring 0.012 x 0.016 mm., the nucleus of which is 0.006 mm. in
diameter. B. Oiicyte measuring 0.018 x 0.028 mm., the nucleus of
which is 0.0105 x 0.014 mm., enclosed in follicle. C. Oiicyte measuring
0.040 x 0.045 mm., the nucleus of which is 0.020 x 0.022 mm. D. The
nucleus only, of an oiicyte measuring 5.84 x 6.16 mm., the nucleus
itself measuring 0.214 x 0.238 mm. Total view showing the small
chromosomes in the midst of a collection of chromatin nucleoli. E.
Vertical section of the nucleus only, of an oiicyte, the follicle of which
measured 37 mm. in diameter. The nucleus itself is 0.455 mm. in diameter and 0.072 mm. in greatest thickness.
c. Chromosomes. cr. Extra nuclear chromosome-like bodies. f. Follicle. m. Nuclear membrane. mf. Folds in nuclear membrane. 11. Nucleus. nu. Chromatin nucleolus. ps. Pseudo-chromosomes. .9. Centrosome. 1;. Yolk nucleus or vitellogenous body.
285
285 _ THE CHICK
Fig. 154. —— Semidiagrammatic illustration of the I-Ien’s
egg at the time of laying. From Kellicott (Chordate
Development). A. Entire “egg.” Modified from Mar»
shall. B. Vertical section through the vitellus or ovum
proper, showing the concentric layers of white and
yellow yolk. Actually there are seldom, if ever, as many
layers as this under normal conditions.
a. Air chamber. ac. Chalaziferous layer of albumen.
ad. Dense layer of albumen. af. Fluid layer of albumen.
b. Blastoderm. c. Chalaza. l. Latebra. nl. Neck of latebra. p. Nucleus f Ponder. pv. Perivitelline space. s.
Shell. smi. Innerelayer of shell membrane. Smo. Outer
layer of shell membrane. 1:. Vitellus or “yolk.” om.
Vitelline membrane. wy. Layers of white yolk. yy. Layers of yellow yolk.
yolk. This alternation was once thought to be universal, and to result
from the fact that yellow yolk was deposited during daylight and white
yolk at night (Fig. 154-, B). As indicated, however, many eggs can be
found in which no such alternation of layers exists, all the yolk aside
from the latehra and its neck being yellow. Experiment has now shown
that the diflerences in color of the layers, when they occur, are due entirely to alternating differences in the character of the food. The deeper
yellow is produced by xanthophyl, and appears in the yolk when grass
. , <3... .....
FERTILIZATION AND MEIOSIS 237
or yellow corn occurs in the diet; If this is fed periodically, it results in
an alternation of darker and lighter layers. Thus by proper feeding thick
or thin, few or numerous, layers can be produced at will. The white
yolk of the latebra and its neck, however, always occurs, and is evidently of a differentcharacter. It apparently‘ results from some influence of the nucleus, but its cause is unknown (Conrad and Warren, ’39) .
_ OVULATION, MEIOSIS, AND FERTILIZATION
During these processes the nucleus has greatly enlarged and as usual
in its enlarged form it is known as the germinal izesicle. The first maturation division is initiated about 4% hours previous to ovulation, and
is completed in about 2% hours, after which the spindle for the second
division is formed (Olsen, ’42, ’50) . At this point the large ovum still in
the ovary is grasped by the funnel shaped infundibulum or ostium. The
theca and follicle then rupture along a non-vascular line, the cicatrix,
and the egg is received into the oviduct. ’
Finally it may be noted that occasionally two eggs may mature and
be released together, in which case they are enclosed in a single shell
and form a “ double yolk egg.” While this is apparently the most usual
cause of this condition it is not the only one. Such eggs may also result either from the premature or the late ovulation of one of the
“ yolks ” (eggs), or from the picking up by the infundibulum of an
extra egg which has previously fallen into the body cavity.
FERTILIZATION AND MEIOSIS
When the egg is taken into the ostium, it is at once surrounded by
sperm which have been received from the male at a period from 24 hours
to two weeks previous to the ovulation of the ovum in question. Several
sperm enter the egg presumably, as in the Pigeon, in the neighborhood
of the hlastodisc, following which the second polar body is given off
and the egg pronucleus fuses with that of one of the sperm. Many of
the remaining sperm nuclei then degenerate, while others (supernamerary ‘nuclei or merocytes) persist for a time and produce certain phenomena to be described later in connection with segmentation.
THE HISTORY OF THE OVUM FROM FERTILIZATION
THROUGH GASTRULATION
The stages now to be described have not all been completely worked
out for the Chick. It is presumed, however, that they are somewhat
283 THE CHICK
similar to the corresponding stages in the Pigeon which have been fully
described by Patterson and Blount. Data concerning doubtful stages in
the Hen’s egg have therefore been partially supplied from the facts re:
garding the Pigeon. The points where this has been done will be noted
in passing.
v
THE APPLICATION or ALBUMEN, SHELL MEMBRANES
AND SHELL
Strictly speaking, the formation of the ovum proper is completed at
the time of ovulation, and it thus appears that what is ordinarily
spoken of as the “yolk” of the Hen’s egg is really the entire egg.
Nevertheless, in the case of the Bird, it is common usage to include
under the term egg not only the ovum proper (i.e., the “ yolk ”) but
also all its tertiary membranes, and this usage will be adhered to in the
following account:
As the yolk passes down the oviduct it takes a position such that a
line passing through the blastodisc and the center of the vegetal pole is
at right angles to the longitudinal axis of the duct at any particular
point. It then revolves slowly about the latter axis, and while so doing
receives its respective coverings from certain portions of the duct. In the
completed product these coverings of the egg or “ yolk ” are as follows:
Closely applied to the yolk comes a dense layer of albummous substance filled with fine mucin-like threads. This layer forms a thin but
firm covering, the chalaziferous membrane. At each side of the yolk opposite each end of the shell this membrane is twisted into cords, the
chalazae. Immediately outside of this chalaziferous membrane there is
said to occur a very narrow layer of thin watery albumen (Conrad and
Scott, ’38). There then comes a clear but relatively dense and wide
layer of albumen called simply dense albumen. Its density is apparently
also due to the presence of mucin. This layer in turn is surrounded by a
fairly wide layer of thin watery albumen called thin albumen which is
bounded externally by the so-called shell membrrme. The latter is a very
real and definite membrane in immediate contact with the outermost
coverings of all, the calcareous shell. The chalazae and the wide layers
of dense and of thin albumen are easily demonstrated by carefully
breaking an uncooked egg into a finger bowl. The innermost narrow
layer of thin albumen next to the chalaziferous membrane, however, is
not usually seen except by the use of more refined methods. The shell
membrane is readily detectable sticking to the inside of the shell. In a
hard-boiled egg the albumen can be more or less unwound in spiral
EGG MEMBRANES AND SHELL 289
sheets, apparently a result of the revolving of the egg in the duct during
its application. (Fig. 154, A).
The question now arises as to what parts of the genital tract listed
above are responsible for the different layers and membranes just indicated. This has been investigated by various workers, Asmundsen and
Burrnester (’36), Burmester C40), Cole (’38), Conrad and Phillips
(’38), Scott and Wai-Lan Huang (’4~l) and others. These men have
attacked the problem by removing parts of the duct to see what layers
were reduced or lacking, by studying the histology of parts of the tract
and in other ways. While the results of their investigations are not in
entire agreement on some details the following conclusions taken
largely from the discussion of Conrad and Scott (’38) are probably
very near to the truth.
Products of the Magnum. — The egg having taken about 18 minutes to pass the infundibulurn enters the magnum which it goes through
in a little short of three hours.‘ This latter region secretes all of the
thick or dense dlbumen which owes its character to numerous mucin
threads. Some (Asmundsen) claim that a little thin albumen (that of
the narrow layer?) is also secreted by the anterior part of the magnum,
but this seems to be one of the points on which there is disagreement
(see below).
Products of the Isthmus.———The egg passes through this part of
the duct in about 74 minutes, and receives here the shell membrane.
There may also be a little thin albumen secreted by this part of the
duct, though Conrad and Scott claim that almost all, if not all, of this
is produced, i.e., differentiated from other materials, while the egg, is
in the uterus. As will presently appear, however, not all the constituents
of this albumen are actually secreted in the latter organ.
Products of the Uterus.—-—The egg remains longest of all in this
region, about 20% hours, and as just suggested it is while the egg is
here that practically all of the thin albumen is -differentiated as such.
As noted, however, all of the material for this layer does not actually
originate in this part of the tract. Instead that portion of it which does
arise here consists largely of thin non-albuminous fluid and soluble
salts. This solution of salts then passes by osmosis through the already
existent shell membrane which is thereby distended. When the fluid in
question thus comes next to the dense albumen some of the protein
in the latter, other than the mucin, soon diffuses into the fluid. In this
1 Average time spent in Various parts of the duct was kindly furnished by
Dr. D. C. Warren.
290 THE CHICK
way the latter becomes albuininous, though still thin because it lacks
mucin threads.
While the egg is in the uterus there are also produced the chalazae,
chalaziferous membrane and the narrow layer of thin albumen. In this
case, however, none of the materials concerned are secreted here. The
substances for these structures are already present in the dense albumen
produced in the magnum. What happens is this: The muein fibers in the
part of the thick albumen immediately adjacent to the yolk are withdrawn from this albumen, and are concentrated against the yolk to
form the chalaziferous membrane. This concentration leaves the albumen next to the membrane without any fibers, and hence it becomes
thin, thus forming the very narrow thin layer noted as occurring in this
region. The chalazae are simply extensions of the concentration at the
two sides of the yolk. They are twisted apparently because the egg was
rotating at the time the albumen from which they are derived was laid
down, and possibly because rotation is still going on. The cause of the
separation of the mucin from the albumen is believed to ‘be mechanical,
but the process is not entirely clear. I
Finally the shell is entirely secreted by the uterus, and is known to be
substantially advanced, though not completed, after 8-10 hours within
that part of the genital tract. The source of the cuticle of the shell is uncertain, but it may be denatured protein. _
The Vagina. —- The egg probably remains only a few seconds in the
vagina before it is laid, and there is nothing added to it here.
THE PERIODICITY OF LAYING
The periodicity in the laying of eggs has been a subject of considerable investigation. Most chickens have an annual laying period of eight
or nine months, the commonest interval of rest being during the late
summer months. During the active period the Bird lays more or less
continuously at the rate of about an egg a day, if the eggs are constantly
removed. Otherwise when a suflicient number have been accumulated
the impulse to “ set ” may assert itself, and the laying ceases while a
brood is hatched and raised. From this it might be inferred that the impulse to set is dependent merely upon the accumulation of a certain
number of eggs, but the word “ may ” in the previous sentence is used
advisedly. Not every hen will set when enough eggs are accumulated.
On the other hand, the setting impulse, i.e., “ broodiness,” sometimes
asserts itself whether there are eggs or not. This is most likely to happen in the spring and early summer, i.e., during the time of year which
PERIODICITY OF LAYING 291
is the breeding season of many birds in temperate latitudes. Thus the
impulse to set is evidently due to more than the single factor of egg
accumulation. It is probably, like so many aspects of reproduction,
partly controlled by some of the endocrine glands, particularly the
pituitary, and this in turn may well be influenced by the length of day,
the temperature, or both. This irregularity in the advent of broodiness
in domestic hens is very likely the result of long selection with a View
to increasing the laying period. Even if the eggs are removed, however,
and the hen does not become broody, she does not lay one every day for
an indefinite period. Instead she lays a series of eggs on successive days,
and then skips a day, such an uninterrupted series being known as a
clutch. The eggs of a clutch, moreover, are not laid at the same time
each day. Rather the first one will be laid fairly early in the morning
of the first day, and each succeeding one about two hours later than its
predecessor on each of the following days. This continues until the last
egg of the clutch is laid around the middle of the afternoon, seldom
later. This means that after a_maximum of five or six eggs has been
laid, a day will ensue in which none is’ laid, and the hen will then begin
again in the morning of the day following.
It was formerly believed that this interruption in laying was due to
a delay in the act of laying itself. The theory was that if an egg was not
ready to be laid until late in the afternoon, the Bird would not lay it
then, but would retain it over night. Thus a day would pass with no egg
laid and the one laid the following morning would be a so-called
“ held egg.” This idea was made reasonable by the fact that there is
some difference in the degree of development of eggs, and this assumed
opportunity for prelaying incubation was supposed to account for it.
Further study, however, has rendered this theory untenable. In the first
place careful tracing of the history of eggs in the genital tract proves,
according to Scott and Warren (’36) that there are no held eggs. Instead it has been found that all eggs spend approximately 25 hours in
the genital tract with some minor variations. It is thought that these
minor variations are sufficient to account for such differences in embryonic development as are known to occur. Correlated with this near equality of time spent in the tract is the fact that each egg in a clutch is ovulated within a few minutesiof the laying of the previous one of that
clutch. These considerations would suggest that the explanation for’ the
omitted day must lie either in delay of ovulation of completely formed
eggs, or in a delay in the later growth stages of certain eggs in the
ovary.
292 THE CHICK‘
An effort to find which of the latter suppositions is true, and to deter‘mine the cause for whatever delay may occur, has been, made by subiccting the hens to variations in illumination. It has thus been found
that artificially reversing the time of illumination within the 24-hour
period will cause a corresponding reversal in the time of laying, but
this effect is delayed for about sixty hours. Also constant illumination
will cause the hens to distribute their laying more or less regularly
throughout the 24-hour period, and will make them lay more eggs to a
clutch. Clutches, however, do still occur, i.e.,. the laying is not continu»
ous. This and other data ‘led Warren and Scott (’36) to conclude that il
ilumination is responsible for normal periodicity in laying. Furthermore
since there are no held eggs the influence of the light could not be upon
the laying itself. It must be upon earlier stages in the entire process.
Finally because of the time lag before changed conditions produced
results these authors decided that the influence was also not upon ovulation, but, as intimated above, upon late stages in the growth of the
oocyte. Be this as it may, still later investigations by F raps, Neher and
Rothechild (’4-7) have shown that light is not the only environmental
factor involved. By giving or withholding food during continuous illumination it was clearly shown that this item and the accompanying
activity of obtaining it very definitely stimulate some step in the reproductive process, apparently ovulation. Also as was so thoroughly
demonstrated in the Frog, pituitary secretion seems to be the immediate
internal agent through which the external factors act.
SEGMENTATION
While the egg has been passing down the oviduct and receiving its
outer coverings, segmentation has been practically completed. As in the
Teleost and Gymnophiona eggs, this process involves only the germinal
disc (blastodisc) , which at the time of the first cleavage is about 3 mm.
in diameter and 0.5 mm. thick. It takes place in the following manner
and in the parts of the duct indicated:
The First C1eavage.~—The first cleavage furrow forms in about
the middle of the blastodisc, and extends only part way across it and
part way through it. It is completed during the passage of the magnum
(Fig. 155, A) .
The Second and Third Cleavagesp and the Accessory Cleavage. ——— As the egg enters the isthmus the second cleavage furrow begins
to form in the two existing cells; it is approximately perpendicular to
the middle of the first furrow, and is of about the same depth. There
Fig. 155.——Cleavage in the Hen’s egg. Surface views of the hlastoderm and the
inner part of the marginal periblast only. From Patterson. The anterior margin of
the blastodisc is toward the top of the page. A. Two cell stage about three hour:
after fertilization. B. Four cells, about three and one-fourth hours after fertilization.
C. Eight cells, about four hours after fertilization. D. Thirty-four cells, about four
and three-fourths hours after fertilization. E. One hundred and fifty-four cells upon
the surface; the blastoderm averages about three cells in thickness at this stage
(about seven hours after fertilization).
ac. Accessory cleavage furrows. m. Radial furrows. p. Inner part of marginal peniblaet. sac. Small cell formed by the accessory cleavage furrnra.
294 THE CHICK H N.
thus arise four cells, in each of which the furrow of the third cleavage
soon appears. These third cleavage furrows may be parallel with the
first, but their direction is quite frequently irregular. In this manner
 
inc. m _
york sc. "
CC.
, gggggnnp - uunnm: aaaaw
mp. mc. unuounn-noun using.» me. mp.
yolk sc.
cc.
.-ago. an
:2Z!’.......-. .=-..
....-.-on-...-uu.
Fig. 156.—Diagrams of vertical sections through the hlastoderm of a Hen’s egg
during cleavage stages. A. A section through an approximate 32 cell stage. B. A section through a slightly later stage where marginal cells are being added to the
original central cells. C. A section through a still later stage in which the marginal
cells have all been used up, and the extra (periblast) nuclei from some of them are
invading the periblast to form the germ wall. D. A stage just as gastrulation is
about to begin. The zones of junction and overgrowth are well marked, and the
germ wall is beginning to add cells to the original marginal cells.
ap. Approximate extent of the area pellucida, not yet marked, however, by the
thinning of the blastodermal roof. bld. Blastoderm. cc. Central cells. cp. Central
periblast. gw. Germ wall. j. Zone of junction. nmp. New marginal periblast. me.
Marginal cells. mp. Marginal periblast. acc. Original central cell region. omc.
Original marginal cell region. amp. Original marginal periblast region. sc. Seg
mentation cavity. sub. c. Subgerminal cavity. 9:. Line of separation between the
inner portion of the germ wall and the underlyingyolk. zo. Zone of overgrowth.
eight cells are formed, none of which are at first separated from the
deeper protoplasm of the disc or from that at the margin.
Before continuing the account of the regular cleavages it is now necessary to pause a moment to note certain so-called accessory cleavages.
These cleavages, which are extremely slight and transitory in the Hen’s
egg, seem to result from a few divisions of some of the supernumerary
sperm nuclei indicated above. They appear at about the four-cell stage
as faint radial furrows around the edge of the blastodisc, but by the
SEGMENTATION 295
time ten cells have formed they have completely vanished. Scattered
and degenerating sperm nuclei are sometimes observable as late as the
thirty-two-cell stage; these also, however, are presently lost sight of,
and apparently exercise no influence upon the ovum (Fig. 155) .
Fig. 157.—Vertical sections through the Chick blastoderm during the '
process of cleavage. From Kellicott (Chordate Development). After Pat- ‘
terson. A. Section through the two cell stage. B. Median section through
the thirty-two cell stage. C. Part of a longitudinal section through th
sixty-four cell stage.
b. Blastocoel or segmentation cavity. c. Central cells. i. Inner cell cut
oil by horizontal cleavage. 1. Neck of latebra. m. Marginal cells. mp.
Marginal periblast. n. Nucleus. p. First cleavage. v. Vitelline membrane.
The Central and Marginal Cells.—Subsequent to the eight-cell
condition, following the third cleavage, further furrows soon appear,
which result in the production of approximately sixteen cells. Some of
these furrows, moreover, are such as definitely to bound the outer edges
of those cells, whose protoplasm has heretofore been -continuous with
that which lay further out. Hence, there is thus created a central seg296 THE CHICK
mented area completely delineated from the unsegmented prqtoplasm
about it; the cells of this area are termed the central cells.
Cleavage then continues about the rim of this central area, producing new cells here which because of their position are called marginal
cells. These cells are for the time being unseparated both from the yolk
filled cytoplasm beneath, and from that lying still further toward the
periphery. This condition is characteristic of what is later known as the
zone of junction (see below) . As the process of cleavage goes on these
marginal cells are constantly being cut oil and added to the central
cells; meanwhile beyond them more marginal cells arise. In this manner the central segmented area is continually increasing in diameter
(Fig. 156, A; Fig. 157).
The Segmentation Cavity. —Furthermore, at the same time -that
the central cells are being defined as such by the furrows at their margins, horizontal cleavages are also taking place. These cleavages intersect the furrows which are visible from the surface, and thus cut off a
single superficial layer of the central cells from the protoplasm beneath
them. Fluid then begins to collect between this layer of cells and the
protoplasm, thus establishing a shallow space, the rudiment of the-segmenzatirm cavity.
As the egg leaves the isthmus, there have been formed in this manner approximately thirty-two cells; 9 it next enters the uterus, in which
cleavage is completed and gastrulation begun.
The Periblast and Its Segmentation.-—Further division both
horizontal and otherwise now takes place, so that the layer of central
cells, at first only one cell thick, soon acquires a thickness of several
cells; the area covered by the central and marginal cells has likewise
been increased. All the cleavage thus far indicated, however, has taken
place within the central region of the blastodisc (Fig. 156, B ) . About
the margin of this area, there remains a ring of the disc slightly darker
in color than the central portion, and about .5 mm. wide. It is still entirely unsegmented and is known as the pcriblast.
The Germ Wall and Subgerminal Cavity.” —— Presently the formation
of marginal cells about the edge of the central region reaches to the
inner margin of the ring, defined as periblast. At this point, although
the nuclei of the marginal cells continue to divide, the cytoplasmic
 
3 There are, according to Kiilliker, about forty-four cells in the blastoderm of
the Chick at this stage.
3 The ensuing description of the organization of the periblast and other later
phases of segmentation are from the accounts of Blount and Patterson, of homologous processes in the Pigeon.
SEGMENTATION 297
cleavages do not lceep pace with them. The extra nuclei (periblast
nuclei) thus produced then wander out into the region of the periblast
and convert. it into a syncytium. Some of these nuclei even move centrally for a short distance into the unsegmented protoplasm beneath
the rim of the segmentation cavity. The latter region of protoplasm thus
occupied by the extra nuclei is usually known as the central or subgenninal pcriblast (see below), to distinguish it from the strictly marginal periblast, the two regions, however, being.perfcctly continuous.
Following the above-mentioned penetration by the periblast nuclei,
what was periblast both central and marginal, is known as germ wall,
the peripheral non-nucleated cytoplasm in turn becoming periblast
(Fig. 156, D). Meanwhile, the last of the original marginal cells have
been cut off from the outlying periblast (now germ wall), and have
become continuous with, and similar in character to, the cells originally
defined as central. Vllithin the syncytial germ wall, cytoplasmic cleavage next begins to take place, and the cells which are thus produced are
added to the former marginal cells. Thus, partly by the multiplication of
the cells already in existence, and partly by the peripheral addition of
new cells arising within the wall, the central area of completely defined
cells spreads outward over the surface of the yolk‘ Upon this basis it
might be imagined that the germ wall would soon he used up, and as
regards the portion of it defined as central periblast this appears to be
true. The marginal part of the wall, however, is never exhausted during
this process of overgrowth. This is due to the fact that as fast as its inner
margin becomes nucleated and then converted into cells, a new germ
wall is created by the peripheral movement of more periblast nuclei into
the new periblast region which lies continually further out. Meanwhile,
as the cellular area is thus extended, the original segmentation cavity
likewise enlarges beneath it. This augmented central space is then often
referred to as the subgerminal cavity,‘ whose outward extension as such
ceases about the time gastrulation is completed.
The Zone of Junction and the Zone of Overgrowth.-——Beyond the
extent of the subgerminal cavity, however, the cellular area continues
to spread over the yolk. Although the actual cavity as such ceases to
expand subsequent to gastrulation, this outgrowth of the cellular region
is accompanied by an ever-widening zone, in which the newly formed
cells are nevertheless distinctly separated from the underlying yolk.
The separation is then continuous at its inner margin with the subger
4 The above distinction between segmentation cavity and subg-erxninal cavity
is frequently not adhered to, the two terms being considered synonymous.
298 THE CHICK
minal cairity. It should further be noted that at its outer edge this zone
of separation extends somewhat beyond the region where the germ
wall has been entirely organized, within its deeper portions, into cells.
in other words at the inner margin of the germ wall, the latter is already slightly separated from the yolk beneath it (Fig. 156, D, x) . In
its more peripheral part, on the other hand, the germ wall, as already
indicated, is quite continuous with the underlying yolk. Likewise, the
cells which, even in this outer zone, now cover the upper surface of the
wall as fast as it forms, are unseparated by cytoplasmic cleavage from
the unsegmented portion of the wall beneath them. Because of this lack
of separation between these superficial cells and the wall beneath them,
and also between the wall and the underlying yolk, this outer portion
of the germ wall is known as the zone of junction (Fig. 156, D). Lastly,
beyond the extreme limit of the zone of junction there exists a narrow
superficial rim of cells which extends out over the unsegmented yolk
lperihlast}, from which it is quite separate. This is called the zone of
0vergr0lL‘t/I, and, although arising from the outer edge of the zone of
junction, it seems to be maintained by the multiplication of its own
cells (Fig. 156, D).
The BZastoderm.——— It may now be added that with the appearance
of these zones the egg has become a blastula, while the entire cellular
and partially cellular area, including the zone of junction and the zone
of overgrowth, may henceforth be referred to as the blastoderm (Fig.
156, 1)). its establishment terminates the period of segmentation as
distinguished from that of gastrulation. Nevertheless, the outward extension of the blastoderm over the yolk continues for some time after
the latter process is completed. This is brought about by the steady
out-pushing of the zone of overgrowth and the germ wall, which not
only themselves increase somewhat in width (particularly the germ
wall ), but leave behind them an ever-widening area of extra-embryonic
ectoderm, mesoderm, and endoderm. The exact method by which these
cell layers are differentiated within the extra-embryonic blastoderm
will be discussed in detail later.
Before proceeding with a description of gastrulation, and the origin
of these layers, in the Bird, it is desirable to recall one point discussed in
connection with the Fish and Cymnophiona. It may he remembered
that in both the latter forms the rim of the blastoderm was homologized
with the lip of the blastopore. It was, nevertheless, indicated in the introduction that this homology is denied by some in the case of the Bird
because of the method of gastrulation in this form as about to be deTHE BLASTODERM 299
scribed. This problem will be mentioned again in that connection. One
point of functional similarity between the rim of the hlastoderm in the
Fish and Cymnophiona and that in the Bird is, however, already apparent. The process of overgrowth of the yolk, or epiboly, by the blastedermal rim, call this rim what one will, is the same in all.
ASTRULATION ‘ AND DEVELOPMENT THROUGH
THE FIRST DAY 2 OF INCUBANON
GASTRULATION
T H E problem of gastrulation in the Chick is one which has received considerable attention both by study of normal total hlastoderms
and sections, and more recently by experimental procedures. The latter
have involved removing living blastoderms and parts of blastoderms to
artificial locations, cutting them at various levels, and marking them
with vital dyes. The object has been to determine exactly what movements are taking place, where the primary layers are derived from, and
what parts of the early blastoderm give rise to specific features of the
early embryo. In spite of all this study investigators are still not in entire agreement on the answers to some of the above questions. At the risk
of satisfying no one, therefore, the writer is going to attempt to piece
together a more or less connected account. in doing so it will beneaessary to select conclusions regarding some of the moot points from different workers on the basis of what seems to us most reasonable and
likely. Statements over which there is especial disagreement will be indicated in order that the student may be aware of what is most generally accepted and what is not. It will be noted at once that the accepted
items largely concern the existence of successive stages of certain structures. Those matters under controversy, on the other hand, have mainly
to do with the interpretation of these structures, i.e., questions of their
homologies, of how they arise and what they produce. The investigators
whose accounts have been particularly consulted are Chen, Hunt,
Rawles, Ruclnick, Woodside, Pa.-steels, Peter and Spratt. The review of
the subject by Rudnick (’/-14) is especially valuable as a critical summary of the situation to that date, and the interested student is referred
to this and to articles by the other authors cited for further details.
1 Gastrulation is usually only slightly under way when the egg is layed (see
below).
1’ The term day as used in connection with the development of the Chick refers
to a period of 24- hours. ‘
i
3
FIRST DAY: GASTRULATION 301
 
.dark area within
area pel|ur.Ida=
embryonic shield
area opaca
area pellucida
primitive streak
Fig. 158. -——- Photographic surface views of early Chick
blastoderms. After Spratt. A. An unincubatcd blastoderin
of the pre-streak stage. The dark area opaca, and the lighter
area pellucida with a darker region within it, the embryonic
shield, are clearly shown. B. A blastoderm of eight hours
incubation showing the primitive streak at an early stage.
The darker embryonic shield lateral and anterior to the
streak shows clearly but is not labelled in this case.
The Area Pellucida and Area Opaca.—As gastrulation begins
the blastoderm above the subgerminal cavity becomes thinned somewhat by the outward movement of its cells. For this reason, the absence
of adhering yolk and the existence of the cavity, this central region
when viewed from above appears different from the surrounding parts.
Thus when observed upon the living egg it appears darker, while in a
stained blastoderm mounted upon a slide it is more translucent. Be302 THE CHICK
cause of this it is referred to as the area pellucida. The surrounding
parts comprising the zone of junction and zone of overgrowth on the
other hand are more whitish in the living egg, and more heavily stained
and opaque in preserved material. Therefore this surrounding region is
appropriately termed the area opaca (Fig. 158).
The Primordial. Hypoblast.—-The first step in actual gastrulation seems to he the appearance within the subgerminal cavity of a sec
A are: pellu: Na
r—-
eplblut
     
archenteron yolk
Z°"m W3“ . primordial hypoblasl: ]zg°;,r-'g°fi§',f~,
primitive streak
B
ectoderm
Fig. 159.—-«Diagrams of sections through the Chick blastoderm showing the origins of the primordial hypohlnst, the definitive endoderm and the mesoderm. A.
A median sagittal section through a very early Chick blastoderm such as is shown
in Fig. 158, A, in which the primitive streak has scarcely begun to form. The
hypohlast has just been delaminated (and, or, infiltrated) from the epiblast. The
area option at this stage consists only of the zone of junction and the zone of
overgrowth. At this stage the zone of junction is mostly, though not entirely,
identical with the germ wall. Thus it will be noted that the latter extends slightly
medially beneath the archenteric space. Later only a small part of the outer
periphery of the germ wall is thus identical with the zone of junction. B. A cross
section of the hlastoderm of a slightly later stage where the streak has formed,
and mesoderm, and perhaps definitive endoderm, is arising in connection with it
in the manner indicated in C.
ond cell layer which may be termed the primordial hypoblast. The space
between this layer and the underlying yolk then, as in the case of the
Fish, becomes the archenteron. The new layer is designated “ primordial” because it appears doubtful that it represents the final or defini.
tive hypoblast, or at least that it represents all of it. The method of its
origin is one of the disputed questions. It was formerly supposed to
originate by involution of marginal cells through a temporary interrupFIRST DAY: GASTRULATION 303
tion in the zone of junction along a small part of the hlastodermal rim.
The location of this activity if it occurred would of course represent, as
in the Fish, the dorsal blastoporal lip, and hence also as in the Fish the
future posterior region of the embryo. It has even been claimed by one
observer that an actual invagination occurs here, giving rise to a pocket
with both roof and floor, i.e., a complete archenteron (Jacobson. ’38) .
At present, however, the belief in either involution or invagination as
defined in this text is no longer entertained in the case of the Chick. Instead Peter (’38) and others seem to think that the process is rather
what we have designated as infiltration. That is to say, these workers
believe that individual cells wander in from the surface and detach
themselves within the subgerminal cavity where they eventually become
arranged to form a more or less continuous layer. lt should be noted incidentally that the sponsors of this View do not use the term infiltration,
preferring to call the inwandering of these individual cells “invagination." This, however, seems to the writer a misnomer—and confusing.-At
all events regardless of the terminology the activity is said to be as
designated.
It must further be stated that those who are agreed on the character of
the process as described are not entirely agreed on just where it takes
place. According to some (Pasteels, ’45) it occurs more or less all over
the pellucid area of the hlastoclerm. Peter, however, seems to think it
takes place mainly toward the future posterior side, especially near the
margin, with a subsequent forward movement. This would approach
more nearly the older idea of an involution from one side.
Finally it may be said that some workers (Spratt, ’46) describe the
process of hypoblast origin as one of splitting oil or delamination of
cells rather than their inwanclering (Fig. 159, A). Also at least one
investigator (Fraser, ’54«) has observed the infiltration of cells from the
epiblast at the anterior and posterior borders of the area pellucida, suggesting once more a sort of modified involution at these borders, but
without interruption of continuity in the epihlast. It is of interest to note
here that a similar problem regarding the nature of hypoblast origin
occurs in the Mammal where again some form of infiltration or delamination seems to occur. This matter will be referred to later in the
appropriate connection.
After the formation of the layer of primordial hypohlast it might be
assumed that gastrulation, as defined in this text, would be complete.
However, as noted, this hypoblast is.~prol3ably only part of the definitive
hypolalast (endoderm) , and in the Bird more than in the Frog and Fish
304 THE CHICK
it is difiicult to separate sharply the origin of the definitive hypoblast
from the origins of the mesoderm and notochord. Also the appearance
of the primitive streak, a structure previously related primarily to gastrulation, is, as we shall see, probably involved here both in the formation of definitive hypoblast, and in the origin of mesoderm and notochord. We shall therefore have to continue our discussion of these
activities more or less simultaneously as a later aspect of gastrulation.
Before proceeding with this it may be remarked that it is at about this
stage of development that the egg is usually laid. The diameter of the
entire blastoderm is approximately 3.36 mm., and that of the area pellucida about 2.16 mm. (Spratt, ’46). If unincubated it may remain in
this condition for some time. If incubation ensues before too long an interval has elapsed further development proceeds as follows:
The Primitive Streak.—The second step in gastrulation is the
development of the primitive streak whose history is as follows: Just
before the streak begins to form, about three fourths of the area pellucida_ as viewed from the surface, starts to become more darkly stain
ing and opaque toward what later proves to be its posterior side. This
is due both to a thickening of the epiblast in this region, and to the
presence of the underlying hypoblast. The part so affected is sometimes
designated as the embryonic shield, though not entirely homologous
with the region similarly named in the Fish as previously described
(Fig. 158, A ) . Presently the streak begins to appear at the posterior side
of this shield, as a still more darkly staining somewhat triangular structure with its base in Contact with the inner rim of the area opaca (Fig.
158, B). This appearance is produced by a further thickening of the
epihlast in the region concerned in a manner to be indicated below. At
first the thickened cpiblast reaches only a short distance cephalad, but
soon, as its growth is completed, its anterior end occurs at about the
middle of the pellucid area. As a result of this increase in length the
structure loses its triangular shape, and appears more as a broad band
or actual streak with a tapering and rounded anterior end. At the same
time sections reveal that from its first appearance the thickened epiblast of this band has been in intimate contact with the underlying hypoblast. A little later the hand (primitive streak) becomes still narrower, and a distinct groove develops down its middle with a little
twist or irregularity at its cephalic extremity where the groove terminatcs in a slight pit. The groove is termed the primitive groove,3 and
3 The term primitive streak is sometimes rather carelessly used to refer to both
streak and groove.
FIRST DAY: GASTRULATION 305
the pit is the primitive pic. The latter together with the surrounding
cells is called Hensen’s knot or Hensen’s node, also the primitive node
(Figs. 160, 161, 162) . The sides of the groove are sometimes designated
as the primitive folds, having nothing to do of course with the later neural folds. So far as the writer is aware no one questions the existence of
these structures as described. Again the real problem concerns the homology of the streak or groove, its origin and its functional relation to
the parts about it. Since the answer to the first of these queries depends
vnedullary told
ya vlrelllnu Intern:
   
Henna’:
knot
= blood islands at
the ma vnmlon
Fig. 160.-— Surface of the Chick hlastoderm and early embryo. A. A pre-incubation blastoderm showing the primitive streak, actually the primitive groove. B. An
18 hour blastoderm showing the beginning of the head process (notochord). C. A
24 hour blastoderm with embryo well started and the area vasculosa forming.
largely upon the answers to the last two, we shall take these latter up in
order. We shall then be prepared to return to the problem of homology.
The Origin of the Streak.--As a result of numerous marking
experiments it appears to be fairly clear that the streak originates by
the convergence of epiblast cells from the lateral regions toward the
place where the initial short “ streak” is first seen (Chen, ’32, Spratt,
’46), (Fig. 163) . This produces an aggregation of material here which
constitutes the thickening described as characteristic of this structure. It
should also be noted, as Spratt points out, that the cells thus aggregated do not pile up upon the surface of" the blastoderm, but pass inward, as he expresses it by “ invagination.” It is this process which almost at once, as previously indicated, brings them in contact with the
underlying hypoblast. After being started in this manner the lengthening of the streak occurs, according to Spratt, by the proliferation of its
cells as follows: At its front end these cells are so added as always to
be at or near the tip, as in the growing point of a plant. Posteriorly the
growth seems to be more by intussusception pushing this end backFig. 161. —— Five transverse sections through the head process and primitive streak
of a lCcIhick embryo. The head process is very short. From Lillie (Development of the
Chic’ ).
A. Through the head process, now fused to the entoderm. B. Through the primitive knot. C. Through the anterior end of the primitive groove. D. A little behind
the center of the primitive streak. E. Through the primitive plate. The total number
of sections through the head process and primitive streak of this series is 102. B is 4
sections behind A. C is 12 sections behind A. D is 59 sections behind A. E is 87
sections behind A.
Ect. Ectoderm. Enz. Entoderm. GJV. Germ wall. H.Pr. Head Process. med.pl.
Medullary plate. Mes. Mesoblast. pr.f. Primitive fold. pr.g . Primitive groove. pr.Im.
Primitive knot. pr.pl. Primitive piste.
306
.-.w
30?
Fig. 162. —— Three transverse sections of a late stage, through the head process and primitive streak of a
Chick embryo. From Lillie (Development of the Chick). A. Near the hind end of the head process. B.
Through the primitive pit. C. A short distance behind the center of the primitive streak.
BLI. Blood island. coel.Mes. Coelemic mesoblast. Ecl. Ectoderm. Ent. Entoderm. G.W. Germ-wall. med.
pl. Medullary plate. Mes. Mesoderm in area pellucida. N’ch. Notochord. pr.]. Primitive iold. pr.gr. Primitive
groove. pr.p. Primitive pit.
308 THE CHICK
ward, Accompanying, and perhaps partially caused by this movement,
the whole pellucid area changes its shape‘ from that of a circle to a pear
with the small end posterior. Finally it may be stated that this growth
of the primitive streak appears to be induced by the underlying primordial hypoblast. This is concluded from the fact that this hypoblast is at
Fig. 163.——A diagram to illustrate the movements occurring on a Chick blastedcrm during gastrulation and primitive streak formation. After Spratt. The movements are indicated by changes in the positions of carbon particles placed on the
hlastoderm at the start of the process. Horizontal rows A, B and C illustrate three
different plans of placing the particles. Vertical rows I, II and III indicate the
positions of the particles in each plan during successive stages in gastrulation.
The short horizontal lines outside the blastoderms are points of reference. Note
the general tendency of convergence toward the forming streak.
first chiefly toward the posterior of the bl-astoderm, and as it spreads
anteriorly the growth of the primitive streak follows it. There are also
other facts which support this hypothesis (Fig. 164) .
Functional Relations of the Primitive Streak.
Diflerentiation of Mesoderm, Endoderm and Ectoderm. —It is now
rather generally conceded that not only are materials moved into the
FIRST DAY: GASTRULATION 309
streak from the outlying epiblast, but they also pass through it to
specific destinations (Hunt, ’37, Spratt, ’4-6) . One of these is apparently
a layer of cells pushing out on either side of the streak between the
epiblast and the primordial hypoblast. This layer is the mesoderm. It is
also claimed that some of the cells moving through the streak pass into
and augment the previously existing primordial hypoblast (Hunt, ’37) ,
(Fig. 159, B, C). Thus this latter layer is converted into definitive hypoblast, or as it may now be called endoderm. The question as to just how
much of the endoderm owes its origin to this movement of cells through
epiblqsf A _prirnitive streak
 
 
 
pre-head prccess cells
germ wall
germ wall
3
primitive node primitive pit primitive streak (groove)
   
 
head process (notochord) endoderm 99"“ w°"
Fig. 164.——A diagram of a median sagittal section through the primitive streak,
A, and groove, B, and parts anterior to each, showing the origin of the head process
inotochord) according to Spratt and Fraser.
the streak, and how much to the spread of the primordial hypoblast is
one of the unanswered questions. As usual after the origin of these
layers the remaining epiblast may be called ectoderm.
Lastly, it may be noted that the process just indicated in connection
with the origin of the mesoderm and endoderm is again what we should
term a kind of infiltration. Nevertheless, as will be pointed out subsequently, it does bear some resemblance to the passage of cells around a
blastoporal lip, i.e., involution, and might help to account for the development of the groove. Also, as in the case of the inwandering of cells
from the surface into the primordial hypoblast, it has been referred to,
ambiguously the writer thinks, as “ invagination.”
The Head Process (Notochord). ——This leaves the origin of the
notochord still to be accounted for. Accompanying the above-mentioned
activities there also appears in front of the primitive streak or groove
another somewhat narrower line temporarily termed the head process
(Fig. 160, B). It begins at Hensen’s knot with which it maintains constant contact, and extends anteriorly. Sections reveal that it consists of
a line of cells somewhat like the streak, but in this case they have no
definite connection with the epihlast, now ectoderm, save at Hensen’s
310 THE CHICK
knot (Figs. 161, A; 162, .4). This head process rapidly increases in
length, and eventually undergoes histological changes to become the
notoclzord. Concerning the above statements there is no question. The
problem again arises, however, as to where the head process (notcchord) originates from, and by what method it develops. It has been
claimed that it arises by a splitting off of streak material from the epiblast in a posterior direction. Thus as the head process grows at its back
end the streak would shorten proportionally at the front end (Lillie,
’19). The streak does indeed shorten, but not proportionally. Hence it
has been claimed by others that the head process grows from cells budded off from the anterior end of the streak, and pushed forward.
Finally according to Spratt, ’47, and Fraser, ’54, the following occurs:
At first the streak, as noted, is quite short. As its substance grows anteriorly beneath the epiblast, the cells of the latter, originally just in
front of the streak, come to lie posterior to its anterior tip, i.e., somewhat behind the primitive node and pit. Some of these cells then pass
into the substance of the streak and forward within it to a point under
the node. Here they form a mass from which the head process is budded,
almost entirely posteriorly (Fig. 164, A). This means that the primitive
streak is forced to recede before it. However, according to Spratt’s evidence it does not shorten at its anterior end in the region where it is in
contact with the head process. Instead the substance of the streak is
“ pushed ” back, or at least it migrates backward. But though the streak
does not shorten at the front end, it does shorten at the back end. It
does this simply by “ dissolution ” into the ectoderm and mesoderm of
this region. As indicated in connection with one of the other theories,
however, this shortening is not quite at the same rate (i.e., proportional
to) the lengthening of the head process. Therefore Spratt suggests that
there must be some condensation of material in the shortened streak.
Eventually, nevertheless, the latter does entirely disappear, except in so
far as its remains may constitute the “ end bud ” (posterior tip) of the
embryo. Figures 164 and 165 illustrate diagrammatically the processes
supposed to be involved. This theory of head process (notochord) origin is supported by extremely careful studies based on a somewhat new
technique. Instead of the dyes previously used for marking points on
the living blastoderm, carbon particles were introduced into it, thereby
eliminating the spreading of the marks by mere dilfusion. Their movements were then kept track of in relation to certain fixed points outside
the area where the critical changes were occurring. The results seem
conclusive, but will of course have to be confirmed by other workers.
FIRST DAY: GASTRULATION 311'.
Distribution of Formative Materials in the Streak and Prestreak Blastoderrn.———In our consideration of gastrulation in the
Frog emphasis was laid on experiments indicating the distribution of
germ layer materials previous to the gastrulation process. The question
naturally arises therefore as to whether it has been 1: ssible to make
comparable pre-gastrular maps in the case of the Bird. The answer is
   
 
 
REEKREDK.
SNORTINIHG Of STRZAK
REGRE3$|DN
POST. BORDER
0? PSLLUCID AREA 0
n.————-———-n
00 GSIIK
Fig. 165. —- A diagram to illustrate the movements occurring in the primitive groove
(“ streak”) and parts connected with it during head process (“ chorda") formation. After Spratt. Three cells in the groove were marked by carbon particles just
before the head process started to appear as shown by the dots on the streak at the
left. As the head process forms, the location of the particles and the changes in the
parts are seen in successive stages as one passes to the right. Note what happens
to the groove as the head process lengthens.
that if one considers the existence of the primordial hypoblast as denoting the completion of gastrulation, such maps have not been made. This
is not surprising since this stage is reached prior to the laying of the
egg. However, in so far as the formation of the primitive streak is regarded as part of gastrulation, the answer is quite otherwise. Many
studies have been made of the potentialities of the various regions of the
blastoderm beginning with the late pre-streak stage, and extending on
to that of the head process. Wetzel, ’29, Rawles, ’36, Pasteels, ”37, Rudnick, ’38, most recently Spratt, ’42, and others have worked on this
problem largely by two techniques. (1) They have vitally stained or
otherwise marked the various regions of the hlastoderm in situ, and
noted the subsequent movements of the stained parts. (2) They have
isolated pieces of the blastoderm on various culture media, and observed what each piece is able to produce. Naturally, the later in de312 THE CHICK
velopment the experiments were performed, the more precise have been
the results, but also of course the further they are removed from the pregastrular situation. It is not feasible to go very deeply into this topic,
cartilage I bonemuscles»
mcaortephroa
Fig. 166. —-A diagram showing the sections into which a primitive
groove and head process stage of a Chick blastoderm was cut, and
the tissues and structures derived from the mesoderm of each isolated piece. After Rawles.
but we may present as an example of the conclusions of some of the
work on later stages one of the maps by Rawles (Fig. 166) . With reference to this map it should be stated that the results upon which it is
based were all obtained by the isolation method, and it must be admitted that this method has one weakness. Since the isolate is in a new environment the potentialities which it exhibits are not necessarily those
FIRST DAY: HOMOLOGY OF STREAK 313
it would have realized had it been left intact. In fact they are apt to be
greater, due perhaps to the removal of inhibition by neighboring parts,
or to lack of specific induction by those parts. It should be understood
that though the map selected is for mesoderm only this does not mean
that this was the only layer studied, or that the layers were transplanted
separately. The results for the different layers were merely recorded separately as a matter of convenience, and our choice of the map of this
particular layer has no special significance. As regards the conclusions,
in view of the results on earlier stages to be indicated presently, it is
perhaps noteworthy that for all layers the regions capable of producing
therhost structures were those near the center of the blastoderm, i.e.,
about Hensen’s node. It is of further interest that the left side showed
more potentialities than the right.
An example of a study of very early stages (early streak and late
pre-streak) is that of Spratt’s isolation work (742). Stated very briefly
his conclusions are essentially as follows: He finds, in substantial agreement with most others, that prospective neural plate material lies near
the center of the area pellucida. Notochord, on the other hand, is formed
from the region just behind this in about the third quarter of the pellucid area. Potential mesoderm, including heart forming material, appears to be somewhat more widely diffused both anteriorly and posteriorly. From this we see that although it has not been possible to map
prospective germ layer and organ-forming regions quite as early or as
accurately as in the case of the Amphibians, some progress has been
made. Thus it is at least evident that the materials for the nervous system, the mesoderm and notochord exist independently in more or less
separate, though overlapping, localities at the pre-streak stage, and that
they are subsequently moved into their definitive positions as the streak
develops. Whether the separation of these substances occurs still earlier, perhaps even in the unsegmented egg, as in Amphioxus and the
Arnphibia, we do not yet know.
THE HOMOLOGY OF THE PRIMITIVE STREAK
It will be recalled that the term primitive streak was used in connection with the Frog, Fish and Cymnophiona to denote the line formed
by the closed blastopore. The question now is whether the primitive
streak of the Chick is really homologous with this line, and hence represents a closed blastopore. ‘
314 THE CHICK
REASONS AGAINST HOMOLOGY OF PRIMITIVE STREAK
AND CLOSED BLASTOPORE
(1) The streak is not at any time an opening into the archenteron, as
a real blastopore is supposed to he.
(2) The origin of the primordial hypoblast at least is not related to
it, nor to its “ lips ” (sides of the groove) .
REASONS FAVORING HOMOLOGY or PRIMITIVE
STREAK AND CLOSED BIASTOPORE
(1) In the Frog and Fish it was shown that there is a convergence of
materials on the outside of the hlastula toward the forming blastopore.
Various marking experiments on the epiblast of the Chick blastoderm
show similar movements of material in its postero-lateral regions toward the forming primitive streak.
(2) In Amphioxus, the Frog, and Fish there was shown to be an involution of the materials just mentioned over the dorsal lip into the
roof and sides of the archentcron. In the Chick there is, strictly speaking, no blastopore in the region of the streak, and hence no blastoporal
lip. The streak, however, does have contact with the primordial hypohlast, and it does develop along either side of it, ridges which would
correspond to the lateral lips of a blastopore. Most important of all it
has been shown that there is a movement of material through these
ridges into the forming mesoderm, and possibly into the endoderm. In
other words as previously suggested there is a kind of “involution,” in
which the presumed homologues of the blastoporal lips are intimately
involved.
(3) In Amphioxus, the Frog, and Fish the notochord arises from
material involuted at the dorsal lip of the blastopore, and budded forward from that region. In the Chick we have seen that the notochord
originates from cells passing inward not, to be sure, through the pit,
whose anterior rim is the homologue of the dorsal blastoporal lip, but
posterior to it. Yet even here such movement is suggestive, even though
the material grows backward instead of forward to form the notochord.
(4) In Amphioxus and the Frog we have found the neurenteric canal
originating by the uniting of the neural folds over the anterior part of
the closing blastopore (primitive streak), while in the Fish Kupffer’s
vesicle, the homologue of that canal, occurs at the same location. Now
in the Chick, to be sure, there is no neurenteric canal at the anterior end
of the primitive streak. There is, however, a pit at this point which is
FIRST DAY: THE AREA OPACA 315
eventually covered by the neural folds, and in some Birds (Duck,
Goose and others) this pit does finally open to the archenteron. Thus in
these cases a neurenteric canal, incipient or actual, is formed in the
proper place if the streak be regarded as a closed blastopore.
( 5) In the Frog, certainly, and probably in the Fish, the anus forms
at the end of the closed blastopore opposite from the neurentcric canal,
the line between the two being designated as the primitive streak. We
have just seen that at least in some Birds what amounts to a neurenteric
canal forms at the anterior end of the streak. On this basis the anus
should arise at the posterior end of this structure, and apparently it does
so (Lillie, ’l9). V
( 6) In the Frog the material in and about the lip of the early blastepore is known to have remarkable inductive powers. In the Chick the
primitive streak is said by some (Woodside, ’37) to have similar powers
when transplanted beneath the epiblast of a very early primitive streak
host.
EXTENSION OF THE GERM LAYERS AND FORMATION
OF THE AREAS VASCULOSA AND VITELUNA
Up to this point the processes of gastrulation and germ layer formation have been considered only in relation to the area pellucida. It now
remains to consider what is happening in these connections in the area
opaca.
ORIGIN OF ENDODERM IN THE AREA OPACA
In connection with the origin of the primordial hypoblast before the
advent of the primitive streak, it was noted that this hypoblast arose by
the inwandering (infiltration) of cells from the surface of the blastederm, or by delamination from its under-surface. It was also said that
this probably occurs mostly about the posterior half of the blastoderm,
perhaps more especially around its margins. This hypoblast was then
supposed to be later augmented to form endoderm by infiltration of
cells through the streak. Upon this basis it is not surprising therefore
to learn that according to some accounts the endoderm of the area opaca
is derived as follows:
It is said that the nuclei from the zone of junction keep moving in toward the area pellucida. As they do so, the cytoplasm about each nucleus engulfs yolk granules, and becomes cut off from that about it to
form a definite cell. Thus the lower part of the germ wall becomes or316 THE CHICK
ganized so that toward its inner margin (the edge of the area pellucida) ,
it begins to form a cell layer. This layer is endoderm which becomes
continuous with the definitive endoderm of the area pellucida. If this
account be correct it would seem that a process which is essentially infiltration, in this case from the margins of the blastoderm, is still giving
rise to some of the endoderm, i.e., that of the area opaca. It may now be
stated that because of its subsequent history the endoderm of this area is
often referred to as yolk-sac endoderm.
THE BLOOD ISLANDS AND THETMESODERM IN THE
AREA OPACA
The Blood Islands.—Though the origin of the endoderm of the
area opaca has been described first, it actually follows slightly, both in
time and peripheral location, the formation of the mesoderm which comes
about somewhat indirectly as follows: It appears that cells from the
postero-lateral margins of the mesoderm in the area pellucida wander
into the upper part of the germ wall of the area opaca, where they also
engulf yolk granules. These cells become aggregated into small masses
in this region, and these masses presently anastomose to form a network. Throughout this network spaces or lacunae are then developed
which contain little groups of cells. Presently the walls of the lacunae
become differentiated into the flat endothelial cells characteristic of
the inner lining of blood vessels, while the cells within the lacunae be
come blood corpuscles. Because of the manner of their formation these
corpuscles are at first necessarily aggregated into groups, which appear
from the surface as darker splotches. These splotches of corpuscles, or
forming corpuscles and their surrounding endothelium, are known as
blood islands. Obviously they arise somewhat previous to the main parts
of the circulatory system with which they presently become connected
(see below).
The Mesoderm of the Area Opaca.—Coming now to the mesoderm of this region we find that it is produced by the budding off of
cells from the surface of the developing blood islands, between the islands and the overlying ectoderm. At its inner margin this mesoderm
like the endoderm becomes continuous with that occurring in the area
pellucida ( Fig. 162, C).
It remains to state that because of the indirect method of production
of this mesoderm its source as just described has been questioned by
some. Thus it has -been claimed that the blood islands, and hence the
mesoderm, come from cells originating in the zone of junction in the
FIRST DAY: THE AREA OPACA 317
same manner as the endoderm of this area. The account as we have previously given it, however, is afforded strong support by the following
fact: Patterson (’O9) has shown that where the mesoderm of the pellucid area fails to reach the germ wall no blood islands and no mesoderm develop in the area opaca. It may finally be noted that if the mesoderm of this area does arise from that in the area pellucida, as seems
most probable, then like the latter it also, though somewhat indirectly,
has its ultimate source in the primitive streak.
Though beginning in the postero-lateral regions as indicated the processes thus described are gradually working forward upon each side of
the area opaca, the proliferated mesoderm of the area pellucida keeping
pace with that which arises from the blood islands further out. Finally,
as the level of the anterior end of the head process is reached, the mesoderm of the pellucid area ceases to form. That in the area opaca, however, continues upon either side as a pair of anteriorly projecting wings,
which after proceeding somewhat beyond the future head region begin
to turn toward one another so that they eventually meet (see second
day). In the area pellucida, however, immediately in front of and
slightly to the sides of the head region, no mesoderm forms for some
time, the zone thus marked out being termed the proamnion (Fig.
160, C). Following the advent of the blood islands it soon becomes
possible to subdivide the blastoderm into further parts as follows:
The Area Vasculosa. ——-The blood vessels, having once become
formed in the area opaca, are not confined there. Very soon, especially
postero-laterally, they begin to extend into the, area pellucida, where
they unite with other vessels which have arisen in situ from the mesoderm; the entire region thus covered by them is then termed the area
vasculosa. Presently, around the outer edge of this area, its boundary begins to be clearly defined by an encircling blood vessel, the sinus ter
minalis (Fig. 160, C).
The Area Vitellina. — The remainder of the blastoderm peripheral
to the area vasculosa is termed the area vitellina, and is in turn subdivided as follows: The part at and near the blastodermal rim continues
to consist of the relatively narrow zone of overgrowth and zone of junction, and is known as the area vitellina externa. Between this area and
the area vasculosa there is then a. region which, with continued expansion of the blastoderm, soon becomes ‘rather extensive. Within it, although the germ wall is becoming occupied with yolk filled cells, these
cells have not yet become definitely organized into endoderm or blood
islands. Nevertheless this part of the wall is clearly separated from the
318 THE CHICK
epiblast above it, and is beginning to be more or less delimited from the
non-cellular yolk beneath it. The relatively broad region thus characterized is called the area vitellina interna (Figs. 167, 170, A, E ).
As has already been suggested, all of these areas, while retaining the
same relative position as regards each other, are constantly moving outward over the surface of the yolk by a process of epiboly (Fig. 167).
Fig. 167. - A. Hen’s egg at about the twenty-sixth hour of incubation, to show the
zones of the blastoderm and the orientation of the embryo with reference to the axis
of the shell. B. Yolk of hen’s egg incubated about 50 hours to show the extent of
overgrowth of the blastoderm. From Lillie (Development of the Chick). After
Duval.
a.c. Air chamber. a.p. Area pellucida. a.v. Area vasculosa. a.v.e. Area vitellina externa. a.v.i. Area vitellina interna. Y. Uncovered portion of yolk; i.e., the “yolk
blastopore" or yolk-sac umbilicus (see below, and page 362).
FURTHER HOMOLOGIES
The Margin of the Blastoderrn.——It was stated in connection
with the Fish that the margin of the blastoderm, or germ ring in that
form was entirely homologous with the blastoporal lips, and that it finally closed to form a primitive streak. It was then indicated that in the
Gymnophiona the margin of the blastopore is again the homologue of
the blastoporal lips. In this instance, however, these lips (germ ring)
become divided into two parts by the early contact of points on the lateral lips a short distance from the dorsal lip. In this manner a small
true blastopore (later a primitive streak) is formed immediately in
front of which the embryonic axis proceeds to develop. The remainder
of the blastodermal rim is then employed in covering the yolk. As it
completes this process there appears what amounts to a second or yolksac blastopore, with the closure of which the yolk is entirely enveloped.
>41! ._.......-,.-a.« W .. . .. ‘J
FIRST DAY: FURTHER HOMOLOGIES 319
The question now to be answered is what if any homologies exist between the avian primitive streak and blastodermal rim, and the blastopores of the Fish and Gymnophiona. We have already given reasons
for homologizing the primitive streak of the Chick with the streak of
less advanced forms such as the Fish and Frog in which this structure
represents the entire closed blastopore. What then of the remaining
blastodermal rim in the Bird?
In answering this let us first consider the character, and then the behavior of this rim. From what has been said it is clear that according to
present views there is no real involution at the blastodermal rim of the
Chick. Hence the epiblast and primordial hypoblast do not actually
unite along this line as at the typical lip of a blastopore. This is most
clearly true in the very early stages when the infiltration or the delamination of primordial hypoblast cells is said to occur more or less all
over the blastoderm. Even at this time, however, there is some evidence
that this process is more active about the postero-lateral margins. Later,
moreover, when the area vitellina externa has been established it has
been indicated that the origin of the cells for the endoderm of the yolk
sac, according to many, is mainly dependent upon, nuclei migrating from
the zone of junction. Thus it can be said that a kind of modified involution is after all occurring at essentially the margin of the blastoderm,
and that ectoderm and endoderm are ultimately in contact in that region. So much for the character of the margin. As to its behavior. it has
already been said that the blastoderm spreads over the yolk by the usual
process of epiboly, and this continues until finally the yolk is completely enveloped. By virtue of its method of formation the covering
thus developed consists of all three germ layers, and is called the
yolk-sac.
Upon the basis of both structure and function, therefore, it is evident
that the hlastodermal rim of the Chick bears a striking resemblance to
the blastoporal lips or germ ring of the Fish, and even more to that of
the Gymnophiona. Indeed there are only two essential differences between the rim of the blastoderm in the latter and that in the Bird. One
is the fact that in the Gymnophiona there is definite involution at one
point on the margin, while in the Bird there is not. The second difference is that in the Gymnophiona the blastoporal lips (blastodermal
rim) immediately adjacent to the region of involution soon fuse to form
a primitive streak. In the Bird, on the other hand, the primitive streak
is apparently formed by a convergence of material in the posterior part
of the blastoderm, but not from material actually in the blastodermal
320 THE CHICK
rim. In both cases the remainder of the yolk beyond the blastoderm is
temporarily uncovered, constituting the so-called yolk-sac blastopore
(Fig. 168). This is later enclosed by a yolk-sac in the Bird, and by
what virtually amounts to that in the Gymnophiona. In the Fish, of
course, the blastodermal rim is not thus divided into two parts, and
hence there is no question about the homology of all of it with a blasteporal lip. In the Fish, however, there is no endoderm in the yolk-sac.
Summary of Gastrulation Processes and Homologies in the
Chick.—We may conclude the discussion of gastrulation by summarizing the processes involved in the Chick as follows: According to
Fig. 168. —Median sagittal section. Stage of the first intersomitic groove. (Cf. Fig.
169). Owing to the bending of the primitive streak the section passes to one side of
the middle line posteriorly. From Lillie (Development of the Chick).
Ect. Ectoderm. F.G. Fore-gut. CJV. Germ-wall. H.F. Head~fold. med.pl. Anterior
end of medullary plate. Mes. Mesoderm. N’ch-l-Ent. Notochord and entoderm. Pr’a.
Proamnion. pr.kn. Primitive knot. pr.p. Primitive pit. pr.str. Primitive streak. Y.S.
Ent. Yolk-sac entoderm. '
the definitions adopted in this book they would include infiltration (i.e.,
a modified kind of involution), or (and) delamination, convergence and
epiboly. ‘
As to homologies, the primitive streak of the Bird is probably homologous with all other primitive streaks, including those in the Frog, Fish,
Gymnophiona, and, as we shall see, the Mammal. Furthermore, there is
good reason to homologize the blastodermal rim plus the primitive
streak of the Bird with the whole blastodermal rim of the Fish, though
the latter contains no endoderm. Likewise we may equally well homologize the rim of the blastoderm of the Bird minus the primitive streak
with the rim minus the streak in the Gymnophiona.
DETERMINATION OF THE EMBRYONIC AXIS
It is of course obvious that whatever fixes the position of the primitive streak determines the embryonic axis; The question therefore is
what fixes the position of the streak. We must immediately answer that,
as in the case of the Fish, we do not certainly know. However, there are
some reasonable hypotheses up to a certain point.
If a hen’s egg is allowed to rest on its side for a short time it' will he
FIRST DAY: THE EMBRYONIC AXIS
found upon opening it that
the yolk (ovum proper) has
turned so that the blastederm is uppermost. Furthermore, if the egg is fertile,
and has been incubated, the
long axis of the primitive
streak, and hence of the embryo, is sometimes exactly,
but more often roughly, at
right angles to that of the
egg shell. Lastly, it will also
be true that if the small end
of the shell is to the right
of the observer, the anterior
end of the streak, and hence
later the head end of the embryo, will usually be away
from him (Fig. 167). These
facts have long been known,
but in themselves only raise
further questions, to wit:
Why is the embryo transverse to the length of the
shell? Why is the head end
away from the observer and
why are there exceptions?
These are the crucial points.
It may be stated to begin
with that, granted one initial
321
u. r.
H. F.
\./'
Fig. 169.—Stage of first intersomitic groove
drawn from an entire mount in balsam by
transmitted light. From Lillie (Development of
the Chick).
a.c.v. Amnio-cardiac vesicle. a.o. Inner mar
gin of Area opaca. Ect. Ectoderm. Ent. Ento-_ ,
derm. H. F. Head-fold. i.s.f.l. First intersomitic
furrow. med.pl. Anterior end of medullary
plate. Mes. Mesoderm. n.g.r. Neural groove.
pr.gr. Primitive groove. Pr’a. Proamnion.
assumption, one group of known facts might account for the transverse
position, the direction of the head and the exceptions. The unproved assumption and the facts are as follows:
The assumption is that the egg passes from the ovary into the oviduct
in such a position that the blastoderm will rest against the wall of the
duct, not toward its lumen. It has been suggested by T. H. Morgan (’27)
that this might occur if the ovum is regularly more compressible in any
axis at right angles to the one vertical to the blastoderm. Granted this
initial assumption, it is then known that the blastoderm retains its position against the side of the duct as the ovum passes along it, revolving
Ent. spl. Mes. Coel. Nch. C09’
Somp.
$pl’p|.
Fig. 170.-—A. Transverse section across the axis of the embryo and the entire
blastoderm of one side. The section passes through the sixth somite of a 10s embryo,
and is intended to show the topography of the blastoderm. The regions B, C, D, E
are represented under higher magnification in the Figs. B, C, D, E. From Lillie (Development o/ the Chick).
A0. Dorsal aorta. a.u.e. Area vitellina exrerna. a.v.i. Area vitellina interna. Bl.i.
Blood island. Bl.v. Blood vessel. Cael. Coelom. GJV. Germ wall. M.0. Margin of
overgrowth. Nch. Notochord. N.F. Neural fold. Nph. Nephrotome. S. Somite. Somp.
Sammopleure. Spl’pl. Splanchnopleure. Som.Mes. Somatic layer of mesoblast. spl.
Mes. Splanchnic layer of the mesoblast. S.T. Sinus terminalis. Y.S.Em. Yolk-sac
cntoderm. ZJ. Zone of junction.
322
I
FIRST DAY: THE EMBRYONIC AXIS 323
as it goes. This means that the blastoderm traces an imaginary spiral
path around the wall of the duct. It is also known that the small end of
the shell is usually found at the leading end. Under such circumstances
Morgan further points out that the following conditions might then ensue. As the egg revolves, the two sides of the blastoderm might be under unequal pressure. This might then determine the transverse position
Fig. 171.—Median longitudinal section of the head, stage of 4 s. The section
passes through the length of one of the neural folds just behind the anterior end.
From Lillie (Development of the Chick).
a.i.p. Anterior intestinal portal. Ect. Ectoderm. Ent. Entoderm. F’ .0. Fore-gut.
H.F. Head-fold. Mes. Mesoderm. Mes.H.C. Mesohlastic head cavity. n.F. Neural
fold. or.pl. Oral plate.
of the primitive streak, its long axis lying parallel to the direction of
pressure. Furthermore, the pressure might presumably be greater on the
side toward which the egg was revolving. If so, and if the egg always
revolves in the same direction, this might determine that the anterior
end of the streak and embryo would always be on a certain side. Bartelmez (’18) has added the notion that the primitive streak axis is determined before the egg leaves the ovary. Then, if as suggested, it always passes into the duct in a certain way this might result in making
the primitive streak axis always transverse to the duct and shell. The
assumption of Bartelmez may be true, but there is no adequate proof
for it, and it seems only to push the ultimate solution further back.
ll
V
5:
it
324 THE CHICK
Morgan’s theory involves fewer unproved premises, and, due to slight
differences in direction of pressure, may account for the variations.
THE HEAD FOLD
A short distance in front of the anterior end of the head process, there
develops shortly a slight depression, and immediately posterior to this
depression a crescentic fold appears, involving both ectoderm and endoderm (Figs. 168, 169, 171). Its ends extend almost from one side of the
area pellucida to the other. The crest of this fold is not raised perpendicularly to the surface, but extends forward so that it overhangs the depression indicated above. It is the head fold, and its anterior edge
marks the anterior end of the embryo. The lateral and posterior limits
of the embryo are not distinguishable until much later. \
THE FORE—GUT
From the method of its formation, the cavity within the head fold is
necessarily lined by endoderm which is co-extensive with the endoderm
of the archenteric cavity posterior to it. It is the anterior portion of the
future fore-gut, the portion which may be said to represent the pharyngeal region. It is a broad, flattened cavity, and as suggested, opens posteriorly into the extensive archenteric space over~lying the yolk. The region of this wide opening is known as the anterior intestinal portal. The
endoderm on the antero-ventral side of the fore-gut soon fuses with the
ectoderm below it in a limited region to form the oral plate (Fig. 171) ;
elsewhere between the ectoderm and endoderm of this vicinity, there are
scattered mesoderm cells, i.e., mesenchyme.
DIFFERENTIATION DF THE EMBRYONIC MESODERM IN
THE AREA PELLUCIDA
THE SOMITES AND LATERAL PLATES
The lateral sheets of mesoderm of the area pellucida now become
thickened along either side of the head process and primitive streak
The ridges thus formed are known as the vertebral or segmental plates,
while the remaining lateral portions of the sheets are called the lateral ’
plates. Just in front of the anterior end of the primitive streak a transverse fissure now appears in each of the vertebral plates. The region of
the plates immediately anterior to these fissures then constitutes the first
pair of.sorr_zitcs; they remain continuous anteriorly with the mesoderm
FIRST DAY: SOMITES, LATERAL PLATES 325
of the head region (Fig. 172) . Slightly behind the first pair of fissures
a second pair develops, and the part of the vertebral plates between
the first and second pairs of fissures is the second pair of somites. The
exact number of somites, and correlated development, varies consider
€. 0.
F. G.
Fig. 172.—Chick embryo with three pairs of somites (about 23
hours). Dorsal view. From Lillie (Development of the Chick).
zz.c.v. Amnio-cardiac vesicle. a.a. Inner margin of area opaca. F .G.
Fore-gut. N’ch. Notochord. n.F. Neural fold. pr.gr. Primitive groove.
31, .92, 3;. First, second, and third somites. .
ably, especially in the early stages, due to the breed of hen, the condition of the egg at laying, the precise temperature and other factors.
At the end of 24- hours, however, there are usually from three to six
of them——often about four——lying anterior to the primitive streak
and hence upon either side of the head process, i.e., the rudiment of the
notochord. The first four pairs of these somites later disappear, being
included in the posterior part of the head.
326 THE CHICK
The Nephrotome. —A narrow strip of each lateral plate immediately adjacent to the somites serves, as it were, to unite them to the main
part of the plate. It is known as the nephrotome, and later gives rise to
the excretory organs.
THE COELOM
Within the lateral sheets, which for a time remain connected with the
somites by means of the nephrotomes, horizontal splits now develop.
They occur first in the anterior portions and gradually spread elsewhere. Of the two sheets thus formed, the one next to the ectoderm is the
somatic or parietal mesoderm (somazopleure) , and that next to the endoderm the splanchnic or visceral mesoderm (splanchnopleure) . The
space between them is the coelom (Fig. 170).
THE RUDIMENT OF THE PERICARDIAL CAVITY
In the region of the head fold, the coelomic spaces on each side push
toward each other. By so doing, they finally work their way in between
the ectoderm and endoderm just at the bend where these two layers pass
up from the depressed area under the fold on to its ventral surface. At
the end of 24 hours, the walls of the opposite spaces have met each other
and fused, so that the spaces themselves are separated only by a thin
layer of mesoderm. This process tends to separate the ectoderm and the
endoderm by pushing.the latter further back, and thus increasing the
length of the fore-gut. These in-pushing portions of the coelom are
the amnio-cardiac vesicles, and they represent the rudiment of the pericartlial cavity (Figs. 172, 183).
THE NERVOUS SYSTEM
Among the most conspicuous features of the early embryo is the rudiment of the central nervous system. This system first appears in the following manner:
THE MEDULLARY OR NEURAL PLATE
Beginning almost at the anterior limit of the head fold the ectoderm
above and along each side of the head process is thickened somewhat;
this thickening is the medullary plate. Posteriorly, the lateral portions
of the plate extend also along each side of the primitive streak (groove).
while the central portion merges with the ectoderm of the groove.
FIRST DAY: THE NEURAL TUBE 327
THE MEDULLARY GROOVE AND MEDULLARY FOLDS
Presently a depression appears running down the middle of the medullary plate above the head process, and on each side of this depression, the lateral portions of the plate rise up as two parallel ridges. The
depression is, of course, the medullary or neural groove, while the
ridges are the medullary or neural folds (Fig. 172). Approximately at
the anterior end of the plate, the ends of the folds meet one another.
However, because of the fact that they are already quite close together,
this meeting does not form an extensive transverse ridge as in the Frog.
Posteriorly, the folds do not at first reach quite to the region of the
first somite, but before the end of the day they have extended backward
to about the anterior end of the shortened primitive streak.
THE NEURAL TUBE
The parallel medullary folds now bend toward one another until
their crests meet and fuse a little distance posterior to the anterior limit
of the head fold, in the region of the future rnid-brain. As in the case of
the Frog, a continuation of this fusion results in the formation of a
thick-walled tube, whose roof, sides, and floor are derived from the inner walls of the medullary folds and from the groove; it is the neural
tube and its cavity of course is the neural canal. As in the Frog, also,
there occurs shortly after the fusion of the folds, a separation between
their inner (neural) and outer walls, the latter reconstituting above the
tube a continuous layer of ectoderm.
These processes continue both anteriorly and posteriorly until the
tube is entirely closed in. During the closure, however, the usual anterior and posterior openings into the neural canal persist. The former
is the neuropore, corresponding to the structure of that name in the
forms previously studied; this opening is closed during the first day. It
should also be noted that because of the protrusion of the folds in this
region, they extend forward slightly beyond the anterior limit of the
fore-gut (Fig. 172). Later, as growth proceeds, this region is actually
carried over the anterior end of the embryo on to the ventral side (see
below under flexures). Posteriorly fusion takes place more rapidly,
keeping pace with the extension of the medullary folds. Because of the
greater distance to be traversed, however, the process in this direction
is not completed until some time later. The completion at this end is
marked by the disappearance of the primitive streak (Fig. 173).
328
THE CHICK
8.0.8.
op. Ves.
ceph. Mes.
F. G.
V. o. m.
s. 2.
n. T.
s. T.
N'ch.
Fi . 173.—-Chick embryo with seven pairs of somites
(alxaout 26-27 hours). Dorsal view. From Lillie (Development of the Chick).
a.c.s. Anterigr cerebral suture; i.e., line of fusion of
neural folds ‘here. ceph.Mes. Cephalic mesoderm. F.G.
Fore-gut. N’ch. Notochord. n.T. Neural tube. op.Ves. Op
..tic vesicle. Pr’-a. Proamnion. pr.str. Primitive streak.
3.2,.-r.7. Second and seventh somitee. V.a.m. 0mphaIomesenteric (vitelline) vein.
Fig. 174.—Transverse section
Am.I". Amniotic fold. A0. Aorta. Coel. Coelom.
362). My. Myotome. My’c. Myocoel. N’ch. Nolochord.
somite. Scler. Sclerotome. V.c.p. Posterior cardinal vein.
W
n
D
through the twentieth somite of a 29 s embryo.
Derm. Dermalome. Gn.
N.Cr. Neural crest. Nep/z.T
Ganglion.
Wolfiian duct.
1
L5.
Nephrogenous tissue. 3.20.
From Lillie (Development of the Chick).
Lateral limiting sulcus (see page
Twentieth
FIRST DAY:
THE NEURAL TUBE 329
330 THE CHICK.
THE NEURAL CRESTS
At the same time that fusion of the folds is occurring, cells are proliferated between the outer and inner layers of each fold, just in the
region of its crest. Thus, as fusion takes place, these cells form a band
along either side of the dorsal part of the neural tube between it and
the surface ectoderm. These bands are the neural crests, which at this
time are united with one another across the dorsal surface of the tube
(Fig. 174).
THE OPTIC VESICLES
Anterior to the first point of fusion, the neural tube is broadened
somewhat. This is the region of the future optic vesicles.
SUMMARY OF THE CONDITION AT THE END OF THE
FIRST DAY OF INCUBATION ‘
I. THE MESODERMAL STRUCTURES
About four pairs of somites are present, lying in front of the primitive knot and connected with the mesoderm of the respective lateral
plates by the longitudinal nephrotomal bands.
The lateral mesoderm extends throughout the area pellucida except
in the region of the proamnion, and together with the endoderm is being differentiated in the area opaca. In the latter area, the formation of
this layer has progressed anteriorly until a pair of wing-like extensions
are level with the tip of the head fold. Also in the area pellucida this
mesoderm has been split into two sheets, the somatopleure and splendinopleure, with the coelomic space between them, and this process is
spreading into the area opaca. Beneath the fore-gut, the walls of the
amnio-cardiac portions of the coelorn have just met each other, and the
rudiment of the pericardial cavity is thus indicated in this region.
ln connection with the formation of the mesoderm, blood vessels and
corpuscles have started to appear in the area opaca and area pellucida,
transforming both into the area vasculosa. The latter is beginning to be
bounded by the sinus terminalis.
4 Degree of development, including somite number, as noted, varies considerably,
especially through 48 hours of incubation. and the hour or stage conditions designated in this text do not exactly agree with the carefully obtained results of Hamburger and Hamilton, 51. However, they are believed to correspond well with
those indicated on the slides sold by most of the Biological Supply companies.
FIRST DAY: SUMMARY 331
Outside the area vasculosa is an area consisting only of partially differentiated germ wall, the zone of junction, and the zone of over-xmwth
the area vitellina. 5 ’
II. THE HEAD FOLD AND THE FORE—GUT
The head fold has formed and in the process has given rise to the an.
terior or pharyngeal portion of the fore-gut.
III. THE RUDIMENTS OF THE NERVOUS SYSTEM
The medullary folds have appeared in the region in front of the primitive knot and have fused for a short space at their anterior ends_ The
neural crests have begun to appear, and the rudiments of the optic vesicles are also indicated.
10
HE CHICK: DEVELOPMENT DURING THE SECOND
DAY OF INCUBATION
GENERAL APPEARANCE
TH E embryos of the higher vertebrates, including Reptiles, Birds
and Mammals, all develop in a more or less confined space, i.e., either
within an egg shell or within the uterus. Also, in the early embryonic life,
almost the anterior half of the organism in these forms is occupied by the
brain which is growing very rapidly. Not only is this true, but the dorsal
part of the mid-brain is growing with disproportionate rapidity, and this,
combined with the confining space, causes a very marked bending of the
entire anterior region. This bending presently leads also to a turning of
the head end (torsion), and finally of the whole embryo, upon its side,
as described below. Thus though the bending and turning are basically
due to changes in the brain, and will be described in terms of that
structure, it is convenient to do it under the heading of general external
features.
FLEXURES AND TORSION
The Cranial Flexure. ——The first bend, and one previously noted
in connection with the brain of the Frog, is the cranial flexure. In the latter animal it was the only marked flexure of the brain, and had nothing
to do with development in a confined space. Indeed the curve of this region of the brain was rather in part the remains of a portion of the original curvature of the egg. In the Chick and other higher animals the
cranial flexure does not have this origin, but it does involve exactly the
same regions of the brain, and the front of the embryo; i.e. it involves
the fore-brain region which is bent down anterior to the notochord.
This flexure begins at about thirty hours, and by the end of the day the
bending is so great that the morphologically dorsal side of the midbrain is actually the most anterior part of the embryo. The morphologically anterior side of the fore-brain, on the other hand, faces posteriorly
so that this part of the embryo almost touches the heart (Figs. 175,
176). Finally, it should be noted that, as in the Frog, this flexure, in so
SECOND DAY: LIMB BUDS
far as it concerns the brain, is permanent, and is the only one of
those indicated at this time which
is so.
The Cervical F1exure.——By
the end of the day another broad
curvature is evident, extending
through the region of the hindbrain and back into the trunk. This
is the cervical flexure, and has no
counterpart in the Amphibian.
The Lateral Rotation or
Torsion. —— Finally as a result of
both these flexures the front of the
embryo would be thrust deep into
the yolk were it not for a lateral
twist which begins at the anterior
end. By 48 hours it has progressed
posteriorly about as far as the
back end of the cervical flexure,
i.e., approximately to the thirteenth somite. It is called the lateral ratation or torsion, and eventually results in turning the entire
embryo over so that it lies upon
its left side (Fig. 176) .1 It
should be clearly understood in
this connection that the terms dorsal, ventral and lateral in the present and following descriptions are
used in their morphological sense.
Thus dorsal will always refer to
the side of the embryo upon which
Fig. 175. —Chicl: embryo with twenty
pairs of somites (about 4-3 hours). Dorsal view. From Lillie (Development of
the Chick).
A.o.m. Vitelline artery. au.P. Auditory pit. Cr.Fl. Cranial flexure. D.C.
Ductus Cuvieri. Dienc. Diencephalon.
M esenc. Mesencephalon. M etenc. Metencephalon. Myelenc. I and 2. Anterior
and posterior divisions of the myelencephalon. 0p.Ves. Optic Vesicle. Ph.
Pharynx. pr.str. Primitive streak. s.2.s.5.,
etc. Second, fifth, etc., somites. Telenc.
Telencephalon. Vel.tr. Velum transversum. I/en. Ventricle.
the nerve cord and notochord occur, and ventral will refer to the opposite side regardless of how the embryo lies.
LIMB BUDS
No limb buds are ordinarily visible at 48 hours. Nevertheless, if tissue from the locations where they would later appear is transplanted to
1 Occasional embryos are found lying upon the right side. Apparently this does
not prevent subsequent normal development.
334 THE CHICK
Fig. 176. ——Chick embryo with twentyseven pairs of somites (about 48 hours).
From Kellicott (Chardatc Developmerm. After Lillie.
a. Auricle. am. Posterior margin of
amniotic folds. c. Carotid loop. cf. Cranial flexure (cervical flexure also shown,
see p. 333). d. Diencephalon. dC. Ductus Cuvieri. g1, g2, g3. Visceral clefts. i.
Isthmus. 1. Lens. ma. Mandibular arch.
ms. Mesencephalon. mt. Metencephalon.
a. Otocyst; to right of otocyst is ganglion of VII and VIII cranial nerves. r.
Retinal layer. S2, 510, 520. Second, tenth,
and twentieth somites. L. Tail-bud. 1;.
Vemricle. va. Vitelline artery. vv. Vite]line vein. 1, 2, 3. First, second, third aortic arches. V. Ganglion V cranial nerve.
other locations it will produce
there either a wing or a hind limb
depending upon its source. Furthermore, the dorso-ventral and
antero-posterior axes of these
transplanted tissues will not have
been altered, i.e., such potential
limb tissue (anlage) transplanted
in an inverted position will produce an inverted limb. Thus it appears that the destiny of this tissue has already been rather completely determined. It will not
only form a limb, but a limb of
a particular type which retains all
its original axes (Hamburger,
’38).
THE SOMITES
When last mentioned, the somites were described as masses of
mesoderm connected with the lateral plates by means of the nephrotomes. During the second 24
hours the connection between
nephrotome and somite is obliterated throughout the greater part
of the embryo; the number of
pairs of the latter increases to 27,
and beginning at the anterior end
the development of each of the
sornites proceeds in the following
manner:
THE MYOTOMES AND
THE CUTIS PLATES
Each somite is at first composed
of an outer layer of comparatively
dense cells surrounding an inner
mass of mesenchyme, the latter
SECOND DAY: THE FORE-GUT 335
comparable to a myocoel, so far as one exists (Fig. 170, B). Presently,
however, the denser layer of cells on the side of the somite next to the
nerve cord and notochord largely disappears, leaving the latter structures in direct contact with the mesenchymatous mass indicated above.
At the same time the dense layer upon the dorsal and outer side of the
somite becomes thicker. The dorsal portion of this outer layer is the rudiment of the myotome, while the more lateral and ventral portion is the
cutis plate or dermatome. Before the second day has passed, the dorsal
or myotomal portion of the above plate of cells begins to turn sharply
upon itself and grow downward between the mesenchyme and the cutis
plate. Thus a double layer of cells begins to be fonned consisting of the
cutis plate on the outside and the myotomal plate on the inside (Fig.
1 74) .
THE SCLEROTOME
The mesenchyme which now begins gradually to surround the notochord and the ventro-lateral region of the nerve cord is the rudiment of
the sol otome.
THE ALIMENTARY TRACT
THE F ORE—GUT
The Stomodaeum.—--During the first day it was noted that the
antero-ventral end of the fore-gut came in contact with the ectoderm at a
point on the ventral side of the head fold to form the oral plate. Now,
as the result of the downward flexure of the head and also of the pushing forward of the mandibular arches (see below), the central region of
the plate becomes relatively depressed to form a pit lined by ectoderm.
It is the beginning of the stomodaeum, and by a continuation of the
above process it presently acquires a considerable depth.
Rathke’s Pocket. — From the antero-dorsal wall of the stomodaeum
a small diverticulum now appears growing anteriorly along the morphologically ventral side of the posterior portion of the fore-brain
which has been bent down in front of it. It is called Rathke’s pocket,
and is destined to become the anterior part of the hypophysis or pituitary. (See the footnote on this under the Frog.)
The Visceral Pouches and Arches.
The Pouches. —— ln the anterior or pharyngeal portion of the fore-gut,
a series of vertical folds of the endodermal wall begin to push outtaward the ectoderm on each side of the head. These are the visceral
336 THE CHICK
pouches, and they develop in regular order, the most anterior pair appearing first. The first pair are known as the first visceral or hyomandibular pouches, and the remaining pairs, of which there are three, as
the second, third, and fourth visceral (“ branchial ”) pouches. They
decrease in size posteriorly, the last pair being relatively small. The
first pair of pouches, i.e., the hyomandibulars, fuse with the corresponding ectodermal invaginations (visceral furrows) only at their dorsal
ends, while the second and third pairs fuse with their respective furrows throughout their lengths, except for a slight interruption in their
upperhalves. The point of fusion of the first pouch now becomes perforated as the first or spiracular cleft. The fusion of the fourth pair of
pouches and furrows, and the perforation at the points of fusion of the
second and third pairs to form actual visceral clefts, occurs later (Figs.
176 and 194).?
The Arches. -—~ Anterior and posterior to each pouch the mesenchyme
becomes thickened to form the visceral arches. The arch in front of the
first or hyomandibular pouch is the first visceral or mandibular arch,
and the one between it and the second pouch is the second visceral_or
hyoid arch. The remainder are simply the third, fourth, and fifth visceral (“ branchial ”) arches, and they appear in the same order as the
pouches; the fifth and last arch is hardly more than a transitory vestige.
Presently, blood vessels and nerves pass into the arches, as will be indicated later.
It should be noted in passing, that though these pouches and arches
correspond to the similarly developed structures in the Frog, in this
case no gills ever appear in connection with any of them. The term visceral rather than branchial is therefore more aptly applied to them all.
The Thyroid. -—-This begins to develop near the end of the second
day as a small thickening in the middle of the floor of the pharynx, between the ventral ends of the second pair of visceral arches. Before the
end of the day it has become slightly evaginated so as to form a shallow depression in the pharyngeal floor (Fig. 184) .
2 According to a recent investigator (Dudley, ‘42) there are actually six visceral
pouches in the Chick embryo, but the last two are very early merged with the
fourth to form what this author calls the “fourth visceral complex,” the “sixth
pouch ” component later forming the post-branchial body (see below). As will he
noted later, others have regarded the primordial lung outgrowths as fifth visceral_
pouches. It appears to the present writer that these are all somewhat forced
attempts to make the situation in the Bird square more nearly with that in some.
of the lower Chordates. Whether either the lung outgrowths or the rudimentary
structures referred to by Dudley really represent any visceral pouches or not, is,
the writer believes, still open to considerable question.
SECOND DAY: THE HIND—GUT 337
The Respiratory Systems--Late the second day a longitudinal
groove, with a pair of slight posterior expansions, appears in the floor of
the pharynx caudal to the visceral pouches. lt is the beginning of the
larynx, the trachea, and the lungs, and thus represents the start of the
entire respiratory system. In this connection it may be recalled that according to one View the lung primordia of the Frog are to be homologized with a hypothetical seventh pair of gill pouches. It is therefore
of interest to find that in this case the above expansions which later develop into the lung primordia of the Chick are similarly homologized
by some with a fifth pair of visceral pouches. (See, however, preceding
footnote.) ”
The Liver. —Just at the posterior limit of the fore-gut behind the
pharyngeal region, there appear at this time two slight antero-ventrally
directed evaginations of the endoderm whose development is said to depend on Contact with the veins ( cardiac primordial in this region {W illier, and Rawles, ’3] T). The diverticula are not of course suspended in
space. but pushed forward into the mass of splanchnic mesoclerm (ventral nzesentery) which unites the gut and the ductus venosus in this vicinity. One of the diverticula is a little in advance of the other both in
position and in time of appearance. lt presently pushes forward so as to
lie just dorsal to the point of union of the vitelline veins (see below),
while the other, at this period, is barely distinguishable. These two
diverticula represent the rudiments of the liver.
THE MID—GUT
There is little indication of any real mid-gut during the secondday,
but rather merely a wide enteric space overlying the yolk. The beginning of folds along the sides of the embryo continuous with the lateral
margins of the head fold suggests, however, the manner in which this
portion of the gut will be formed.
THE HIND—GUT
The Posterior Intestinal Portal and Anal Plate. —— At the close
of the second day the hind-gut begins to develop in connection with a
tail fold very similar to the head fold. There is thus formed a posteriorly
directed cavity lined by endoderm, and lying beneath the remains of the
primitive streak. It is the hind-gut, and opens anteriorly into the wide
enteric space overlying the yolk (rudiment of the mid-gut). As in the
case of the fore-gut, the region of this opening is termed an intestinal
portal—in this instance, the posterior intestinal portal. There is li338 THE CHICK
nally one further resemblance between fore- and hind-guts in that at the
end of the latter the endoderm comes in contact with the ectoderm and
fuses with it. This point of fusion  at the posterior end of the primitive streak. and marks the location of the future anus. lt is termed the
anal plate or eloacal membrane. Besides these points of resemblance,
there are now to he noticed Certain important differences as follows
(Fig. 177):
T.B. tf
Eat. all. t.
Fig. 177.~—Median longitudinal section through the hind end of an embryo of
about 21 s. From Lillie (Development of the Chick}.
an.p[. Anal plate. an.!. Anal tube I’l1ixirl-grill. Ect. Ectoderm. Ent. Endoderm. files.
Mesoderm. p.IT.p. Posterior intestinal portal. T.B. Tail-bud. t.f.So’pl. Tail iold.in the
zomatopleurc and ectoderm. t.f.Sp‘pl. Tail fold in the splanchnopleure and endoem.
The Ventral Mesentery.—lt has been stated that the hind-gut
is formed in connection with a tail fold, just as the fore-gut is formed
in connection with the head fold, and in a general way this is true. In
the case of the tail fold, however, there is this difference. The endoderm
is folded in to form the hind-gut and the intestinal portal, but in this
case the ectoderm follows this infolding much more slowly than it did
in the case of the head fold. Thus it happens that the hind-gut arises
before there is any very marked indication of a tail fold on the surface
of the blastoderm. For this reason the anal plate, unlike the oral plate,
remains dorsal for some time, and is only gradually carried around onto
the ventral surface (Fig. 177) . ‘
Furthermore, this lagging behind of the ectodermal portion of the
fold necessarily means that there is a gap between the two cell layers;
this gap in the case of the tail fold is filled by mesoderm. Presently lateral extensions of the embryonic coelom press back into this region
upon either side, but for a time they do not meet one another. Thus
there is left a median mesodermal mass extending from the ventral side
   
l
SECOND DAY: THE HEART 339
of the hind-gut backward and upward to the underside of the lagging
ectoderm. That portion in contact Wiitll the gut may be referred to as
splanchnic, and that in contact with the ectoderm as 50ma;gc_ The two
portions are continuous, however, and together are known as the ventral
mesenteri-' of the hind-gut.
 
B
Fig. 178.—Ventral views of the head ends of Chick embryos. From Lillie (Development of the Chick). A. Embryo with five pairs of somitcs (about 23 hours). B.
Embryo with seven pairs of somites (about 25 hours).
a.c.v. Amnio-cardiac vesicle. a.i.p. Anterior intestinal portal. End’c.s. Endocardial
septum. F .0. Fore-gut. Ht. Heart. M }*’C. Myocardium. N’ch. Notochord. N’ch.T. Anterior tip of nomchord. n.F'. Neural fold. op.Ves. Optic vesicle. p.C. Pericardial cav
ity (amnio-cardiac vesicles). Pr’a. Proamnion. 32.54. Second and fourth mesodermal
somites. V .o.m. Omphalomesenteric vein.
THE CIRCULATORY SYSTEM
THE HEART
The Origin and the Formation of the Enclothelial Lining. —
While blood vessels and corpuscles have been developing from the germ
wall in the area opaca, vessels have also begun to form in the area pellucida. These latter vessels, which are in direct continuity with ‘chose already formed, also arise from blood islands, though these islands are
slightly different from those of the area opaca. They are merely aggregations of cells, apparently detached from the splanchnic mesoderm,
and the vessels into which they develop are temporarily entirely devoid
340 THE CHICK
of corpuscles. Erythrocytes, however, are soon supplied from the area
opaca, and also by cells buddecl from the posterior ends of the dorsal
aortae (Danchakoii, ’07). Thus from the cell aggregates, as indicated,
rudiments of two large vessels (the omphalomesenzeric or vitelline veins)
Fig. 179. ——~ Sections through Chick embryos showing particularly the formation of
the heart. pericardial cavity. and pharynx. From Kellieott (Chordate Developrmnzt).
After Lillie. A. Just posterior to the anterior intestinal portal of a Chick with seven
pairs of somitcs (about 25 hours). B. Section just anterior to A. C. Through the
heart of an embryo with ten pairs of somites (about 29 hours).
am. Axial mesodermal thickening. (:0. Lateral dorsal aorta. ebc. Exocoelom. cc.
Ectoderm. en. Endoderru. hb. Hind-brain. 17. Blood islands. 17]). Anterior intestinal
portal. my. Mayocardium (muscular layer of heart). n. Notochord. nc. Nerve cord.
p. Pharynx. pc. Pericardial cavity (atnnio-cardiac vesicles). 3. Endothelial septum.
so. Somatic mesorlerm. sp. Splanchnic mesoderm. th. Cardiac entlothelium. 11. Area
vasculosa. um. Ventral mesocardium. w. Germ wall. y. yolk~sac endodcrm.
soon appear in the area pellucida (Fig. 178) : Each rudiment rests upon
one of the ventro-lateral walls of the fore-gut, between it and the median-lateral wall of the respective amnio-cardiac vesicle from which it
has arisen (Fig. 179, A) .3 The anterior portions of these rudiments then
form the ehdothelial lining of the heart in the following manner:
It is to be recalled thatthe amnio-cardiac vesicles have already become fused beneath the fore—gut, just in front of the endodermal wall
3 The evidence of this figure would seem to indicate that the vessels are derived
from the walls of the gut rather than from those of the vesicles, and some authorities hold this to he the case. In view, however, of the origin of the other blood
vessels of this area from the mesoclerm, it seems more likely that the latter derivation is the true one.
i
a—u—an.m..._..,..
SECOND DAY: THE HEART 341
which marks its posterior limit (Fig. 178, A). The fusion now progresses posteriorly, as it does so pushing back and closing in the ventralateral gut walls against which the veins indicated in the preceding paragraph are resting. Thus as these walls come together the anterior ends
of the above mentioned vessels are likewise brought together side by
side beneath the newly formed gut, and as this occurs they fuse with one
another to form a single vessel with a median partition. This partition
soon disappears, and the single median tube which remains is t: e endothelial lining of the rudimentary heart (Figs. 178, B and 179, B, C).
The Myocardium of the Heart. — The median walls of the amniocardiac vesicles which now lie against each side of the endothelial tube
presently press in above and below it, and fuse with each other. Thus
the tube is completely surrounded by mesoderm which forms the myocardium or muscular element of the heart, and its covering the visceral
pericardium.
The Mesocardia.———The above fusion leaves the endothelial tube
and its myocardium suspended from the mesodermal covering of the
ventral wall of the fore-gut, or pharynx, by a double layered sheet of
mesoderm (ventral mesentery) here termed the dorsal mesocardium.
Ventrally also a similar sheet attaches the tube to the underlying
splanchnic mesoderm. The latter quickly disappears, and the former
does so later, except at the anterior and posterior ends of the heart (Fig.
179, C).
The Pericardial Cavity and Parietal Pericardium. —With the
fusion and disappearance of the median walls of the amnio-cardiac vesicles, it is clear that their cavities have become a single space which surrounds the heart. This space is the pericardial cavity, and its walls constitute the rudiments of the greater part of the parietal pericardium.
Postero-laterally, however, the pericardium is still incomplete, and
hence the above cavity continues to communicate in this direction with
the general coelom.
The Rudiments of the Atria, Ventricles, Bulbus and Truncus
Arteriosus. — In connection with the description of the development
of the Frog heart it was noted that the development of all Vertebrate
hearts is essentially similar. This similarity has already become apparent as between the Frog and Chick in that the hearts of both start with
the fusion of two vessels to form a tube. Further similarities will now
reveal themselves in the transformations of this tube in the Chick to
form the adult organ.
342 THE CHICK
As in the Frog, the straight tuhe first increases in length, and, its
‘ends being fixed, its middle hows laterally to the right (Figs. 180 and
181). The broad apex of the how is then drawn ventrally, and usually
slightly posteriorly, while the whole tube is at the same time thrown
into a loop. (These terms of direction it should here be recalled are being used in the morphological sense regardless of the rotation of the
embryo onto its side.) Again as in the Frog, the loop which has been
produced in the originally straight tube lies to the right of the median
line. This means that the posterior limb of the loop extends ventrally,
op. Ves.
VII -VIII
an. F.
V. o. rn.
5.4.
a. i. p.
Fig. 180. —— Ventral view of the anterior end of ti Chick embryo
with sixteen pairs of somites (about 38 hours). From Lillie
(Development of the Chick).
(I.i.p. Anterior intestinal portal. au.P. Auditory pit. B.a. Bulbus arteriosum F.B. Fore-brain. Inf. lnfundihulum. op.Ves. Optic vesicle. 0r.p1. Oral plate. Pr’am. Proamnion. 3.4-. Fourth
somite. Tr.a. Truncus arteriosus. v.Ao. Ventral aorta. Ven. Ven- '
tricle. V.o.m. Omphalomesenteric (vitelline) ‘vein. V II—-VIII.
Acustico-facialis ganglion.
and as suggested, usually slightly posteriorly. The middle part then
curves laterally toward the right, where it passes into the ascending limb
which extends dorsally, anteriorly and medially back into the median
plane (Figs. 108, 176) . It now remains to indicate the parts of the future
heart which the various regions of this loop are destined to form. Beginning at the posterior end the region where the posterior limb starts
to descend will comprise the atria. The apex of the loop and a small
portion of the descending and ascending limbs will become the ventricles. The larger part of the anterior ascending limb will become the
bulbu: and truncus arteriosua.
SECOND DAY: BLOOD VESSELS 343
As regards the functioning of the Chick heart, the first indications of
it have been found to occur about the twenty-ninth hour of incubation,
and as in the Frog, long before any innervation. T he contractions begin along the right side of the heart tube in the future ventricular region, and then spread to the left. As the atrial region forms behind the
ventricular, the contractions also extend to it, and finally to the sinus
venosus. As in the case of the Frog, experimental transections of the
heart tube show that the inherent rate of contraction increases as one
passes posteriorly. Also the most posterior region at any given stage
acts as the pacemaker, while the older anterior regions gradually lose
the power of automatic contraction. Thus the rate for the whole heart
is slowly stepped up and is finally set by the sinus, which is ultimately
incorporated into the right atrium ( Patten and Kramer, ’33, Barry,
’42). Later on following innervation the rate of heat is of course partially under nervous control.
THE BLOOD VESSELS OF THE EMBRYO
The Arteries.
The Dorsal Alarms and Their Branches. Along each side of the embryo, just at the inner margin of the pellucid area, two vessels now develop. These are the dorsal aortae (Fig. 181, A). Anteriorly each is
continued into a vessel differentiated in the mesenchynie on either side
of the head.l’osteriorly they give elf branches between the somites (segmental arteries) , and finally leave the sides of the embryo at about the
level of the seventeenth somite to pass out into the general vascular network as the vitellinc arteries. Near the end of the second day the two
dorsal aortae fuse with one another in the region above the heart, forming for a short distance a single dorsal vessel.
Development of the Aortic Arches. -——-The truncus arteriosus
at first runs anteriorly a short distance, this short relatively horizontal
extension being called a ventral aorta. It is. however, merely a continuation of the truncus, and is presently so incorporated with it that there
is no distinction. At its anterior end this short extension of the truncus
divides into two vessels which extend still further forward in the pharyngeal floor. They also are frequently called ventral aortae. As will
presently appear, however, their proximal portions really constitute the
proximal parts of the first pair of aortic arches (Figs. 180. 176). Somewhat anterior to the oral plate each of these vessels bends sharply upward to join the respective dorsal aorta, this bend being termed the
344 THE CHICK
Fig. 181.~—Chick embryo with 12 pairs of somites (about 33 hours). From Lillie
(Development of the (Jhiclr). A. Dorsal view of entire embryo. B. Ventral view of
anterior end.
A.C.S. Anterior cerebral suture. a.z'.p. Anterior intestinal portal. A0. Dorsal aorta.
F.C. Fore-gut. H.B. Hind-brain. Ht. Heart. M.B. Mid-brain. op.Ves. Optic vesicle
or.pl. Oral plate. pr.slr. Primitive streak. 82 S12. Second and twelfth somites. v.Ao.
Ventral aorta. V.o.m.. Omphalomesenteric vein.
carotid loop. Meanwhile, as previously indicated, the visceral pouches
and arches have been forming, and in the arches certain blood vessels
have been developing on each side as follows:
In the first place the single or common ventral aorta has, as pre-'
dicted, become incorporated into the truncus whose wide dorsal end
now terminates directly beneath the visceral arches. While this has been
SECOND DAY: BLOOD VESSELS 345
occurring each first or mandibular arch has pushed ventrad. As a result
of this the proximal part of each of the separate ventral aortae comes to
lie within about the ventral four-fifths of the respective mandibular
arch. Thus, as suggested above, this part of each ventral aorta comes
to form the proximal portion of each first aortic arch. The more distal
fifth of each first aortic arch which will lie within the corresponding
distal fifth of the mandibular arch, remains for the time being incomplete. The proximal four-fifths of this vessel is, however, still connected
with the dorsal aorta by way of the remaining anterior tip of the respective ventral aorta and carotid loop as previously indicated (Fig.
176). The actual completion of the distal portion of the first aortic arch
so that this artery lies entirely within the‘ mandibular arch apparently
does not occur until the third day, and wiil be described when that stage
is reached. The development of the remaining aortic arches is more
straightforward. The second aortic arches develop in the second visceral or hyoid arches, and the third aortic arches develop in the third visceral arches. These last pairs arise as buds from the dorsal aortae which
grow almost directly ventrad through the arches to -join the dorsal end
of the truncus.
The Veins and the Lateral Mesocardia. —— As has been indicated
above, the endothelial portion of the heart is formed by the growing together of two large vessels (omphalomescnteric veins) . It now remains
to state that this union continues for a short distance posterior to the
atrial rudiments. The most anterior part of this continuation is somewhat dilated and is known as the sinus venosus, while slightly further
back it receives the name of ductus venosus. The most anterior portion
of the sinus venosus is sometimes regarded as part of the heart proper,
because later it is involved in the development of the right atrium. At
this stage, however, it may best be considered as a part of the venous
system.
During the second day there develops in the mesenchyme on each
ventro-lateral side of the brain a vessel which runs posteriorly as far as
the level of the heart. These are the anterior cardinal veins. Meantime
there has occurred on each side of the embryo a fusion of the lateral
body wall with the posterior part of the sinus venosus. Thus a pair of
septa have been formed each of which passes somewhat diagonally laterally and dorsally from the posterior part of the sinus to the respective
body wall. These are called the lateral mesocarclia, and within each of
them develops a rather large vein, the ductus Cuvicri (Figs. 176; 182, C).
Each ductus Cuvieri connects ventrally with the sinus venosus and dorFig. 182.——Diagrams of the circulation in the Chick embryo and area vasculosa.
From Kellicott (Chordate Development). The vascular network of the area vasculosa is omitted for the most part. A. Anterior and central parts of the embryo and
vascular area at about thirty-eight hours (sixteen pairs of somites). Viewed from
beneath. After Popofi. B. Median and anterior parts of vascular area and embryo at
about seventy-two hours. (twenty-seven pairs of somizes; the number is usually
nearer to 36 at. this age). Viewed from beneath. After Popoff. C. The main vascular
trunks of the fourth day. After Lillie (modified).
a. Dorsal aorta. aa. Aortic arches (first and second in A, second, third, and fourth
in C) . ac. Anterior cardinal vein. al. Allantois. au. Atrium. b. Bulbus arteriosus. 11G.
Ductua Cuvieri. dv. Ductus venosus. cc. External carotid artery. 1:. Heart. ic. Internal
carotid artery. la. Lateral dorsal aorta. It). Left anterior vitelline vein. p. Anterior
intestinal portal. pc. Posterior cardinal vein. u. Posterior vitelline vein. ru. Right
anterior vitalline vein. t. Sinus terminalis. tr. enoue trunks oi the area vasculosa.
v. Venn-icle. va. Vitelline artery. w. Vitelline or omphalomesentcric vein (in this
region really lateral vitellinc vein) . .
546
SECOND DAY: CIRCULATION 347
sally with the posterior end of the respective anterior cardinal vein.
From this point of union still another Vein grows posteriorly along each
side of the body. These veins are known as the posterior cardz'.vzals tl7i;:.
182, C ).
THE‘ EXTRA:-EMBRYONIC BLOOD VESSELS
Extension of the Area Vasculosa and the Mesoderm. —~By
about the end of the second day the two anterior wings of the area vasculosa, and the extra-embryonic mesoderm and entoderm which accompany them, have bent toward one another and have fused in front of the
proaxnnion; The area vasculosa, therefore, now entirely surrounds the
latter region, and is itself completely encircled by the sinus terrninalis,
which has been referred to above (Fig. 182, A, B ) . Meanwhile, certain
veins and arteries have extended from the embryo into the vascular area,
as follows:
At the posterior end of the ductus venosus, the union of the vessels
which form it terminates, and each passes outward into the area pellucida. At this point the y are known as the vitelline or omphalomesenteric
veins. Upon coming into this region each of the veins turns e.nteriorly
and runs past the head around the inner boundaries of the approaching
wings of the area vasculosa. Hence these extensions are known as the
right and left anterior vizelline veins. First by a system of capillaries,
but presently directly, each of these veins then becomes connected with
the anterior extremities of the sinus terrninalis. It thus happens that as
the vascular wings meet one another, the sinus terminalis not only be
comes complete, but the ends of the two anterior vitelline veins also
' meet and form one vessel (Fig. 182). At the proximal ends of these
veins each gives rise during this period to a slight lateral outgrowth the beginnings of the lateral vizelline veins.
The vitelline arteries, already referred to, extend out into the lateral
portions of the area vasculosa some distance back of the vitelline veins,
i.e., by the end of the day at about the twentieth somite.
THE CIRCULATION AS ESTABLISHED ON SECOND DAY
It will now be seen that with the establishment of the capillary network within the area vasculosa, and the formation of the arches connecting the ventral and dorsal aortae within the embryo, a complete
system of circulation has been made possible. The further development
of this system will be described as it occurs.
348 THE CHECK
THE NERVOUS SYSTEM
THE MAIN DIVISIONS OF THE EARLY BRAIN
Early on the second day of incubation a slight constriction appears
just back of the optic vesicles, marking the posterior boundary of the
fore-brain or prosencephalon. Presently this is followed somewhat further back by another constriction which marks the posterior limit of
Fig. 183. ——-Median sagittal section through the head end of a Chick with 18 pairs
of somites labout 4-0 hours). From Lillie (Development of the Chick).
tt.i.p. Anterior intestinal portal. Aa. Dorsal aorta. At. Atrium. E.E.B.C. Exocoelom
(extra-ernliryonic body cavity). F.B. Fore-brain. H.B. Hinv.l~l)rain. H .F.Am. Head~fold
of amnion. Inf. lnfundibulum. Isth. Isthmus. M.B. Mid-brain. N’r:h. Notochord. or.pl.
Oral plate (oral membrane) . P.C. Pericardial cavity. Ph. Pharynx. Pr’a. Proamnion.
pr’n.g. Preoral gut. Retzopt. Optic recess. S.V. Sinus venosus. Tr.a. Trnncus arte
riosus. Vcn. Ventricle.
the mid-brain or mesencephalon. The part posterior to this is the hindbmin or rhombencephalon which passes insensibly into the region of the
spinal cord. The posterior limit of the hind-brain, however, may be fixed
in a general way at this time by the position of the fourth somite (Figs.
181, 183). lt should again be noted that the cranial and cervical flexurcs
are especially concerned with the brain. As suggested, however, because
that organ occupies so large a part of the anterior of the embryo at this
stage these flexures affect the whole organism in this region and were
therefore described under general appearances.
THE FORE—BRAIN OR PROSENCEPHALON
Its Extent.—-—0n the posterior wall, i.e., on the floor of that part
of the brain where the cranial flexure is most pronounced, at the end of
the slightly bent notochord, is an invagination. It is directed antero
..‘,,t-.-yw
SECOND DAY: THE‘ FORE—BRAIN 34.9
ventrally into the cavity of the brain, and is called the tuberculium. posterius (F ig. 184). On the opposite or anterior wall of the brain a little
below the level of this evagination is the slight, but broad, constriction
referred to above as marking the posterior boundary of the fore-brain.
This boundary may now be more accurately defined as a plane passing
from the tuberculum posterius on the posterior wall to the mid-point of
the broad constriction on the anterior wall. This mid-point marks also
the position of the future posterior commissure (see fourth day).
Fig. 184.——— Optical sagittal section of the head of an embryo of 22-23 s. The heart
is represented entire. From Lillie (Development of the Chick).
Atr. Atrium. B.a. Bulbus arteriosus. Cr.Fl. Cranial fiexure. Dienc. Diencephalon.
Hyp. Rathlce’s pocket, rudiment of anterior hypophysis. Inf. lnfundilmlum. Md.
Mantlilmlar arch. Melenc. Metencephalon. Myelenc. Myelencephalon. or.pl. Oral
plate. Pr’o.C. Preoral gut. Th. First indication of thyroid. Rec.opt. Optic recess.
Telcnc. Telencephalon. T.p. Tuherculum posterius. V.tr. Velum transversum.
Parts of the Fore—brain.
The Infundibulum.——Just ventral to the tuberculum posterius, a
small posteriorly directed evagination now appears lying slightly be
neath the anterior end of the notochord. It is the beginnirg of the in-
frmdibulum, the future posterior part of the pituitary (Fig. 184).
The Region of the Optic V esicles.——Ventral to the infundibulum,
but still on the posterior wall, is a thickening, the rudiment of the future
optic chiasma (not noticeable in Fig. 184) , while immediately ventral to
this thickening is a small evagination, the optic recess. From this recess
the hollow optic vesicles have grown out on either side, and as they have
grown their proximal parts have been constricted, as in the case of the
350 THE CHICK
Frog, to form the optic stalks. Below the optic recess, the posterior wall
begins to curve anteriorly onto the present ventral surface. This region
is relatively thin and is known as the lamina. zermirzaiis. Within it the
torus transversus is scarcely visible as yet.
The Cerebral Hem.ispheres.—Near the end of the second day the
sides of the fore-brain just dorsal to the lamina terminalis begin to push
out as the future cerebral hemispheres. Their cavities will be theylateral
ventricles opening into the cavity of the fore-brain or third ventricle,
through the foramina of Monro.
The Velum Transversum and Region of E piphysis. —— Beyond the region of the lamina terminalis on the antero—ventral side of the forehrain, we come to a portion of the wall which is slightly depressed. it is
known as the velum trcrnsversum. Further dorsal to this point on approx
imatcly the anterior surface may he found, also, the suggestion of an
outpushing; it marks the general region from which the epiphysis
(pineal gland) later (fourth day) arises. This brings us to the slight but
broad constriction mentioned above as indicating the location of the
future. posterior commissure, and the limit of the fore-brain.
The Divisions of the Fore—brain. ———As in the case of the Frog, it
is customary to divide the fore-brain into two parts, which with the aid
of the above lanclmarks may now be easily defined. That part of the
fore-brain which lies vcntro-anterior to a plane passing from the pos
,terior wall just ventral to the optic recess to the anterior wall slightly
anterior to the middle of the velum transversum is the telenceplzalon.
The remaining portion of the fore-brain, whose posterior limit is defined above, is then the diencephalon. The cerebral hemispheres arise
from the former.
THE MID—BRAIN OR MESENCEPHALON
The anterior boundary of the rnesencephalon ‘coincides with the posterior boundary of the diencephalon, marked by the broad constriction previously referred to. The posterior boundary may be defined as a
transverse plane passing from the postero-ventral wall or floor just
above and behind the tuberculum posterius, upward to about the middle
of another rather broad constriction on the antero-dorsal wall (Fig.
184). The roof of the mid-brain, moreover, is growing so rapidly in
connection with the cranial flexure, that it soon arches outward as the
most anterior region of the embryo. Other parts of the mesencephalon
have not appeared, and will, therefore, be described later as they
arise.
SECOND DAY: SPINAL CORD, NEURAL CRESTS 351
THE HIND-BRAIN OR RI-IOMBENCEPHALON
Its Extent. —The hind-brain lies entirely dorsal to the notochord,
and extends from the constriction marking the boundary of the midhrein posteriorly into the spinal cord. Its posterior boundary, as stated
above, can be defined only as that part opposite the fourth somite_ A5
in the case of the mid-brain, the parts of the hind-brain are not yet discernible, and will be indicated when they appear.
The Divisions of the Hind-brain.——The divisions of the hindbrain are also difficult to define at this early stage. We may say, however, that the anterior division is relatively short, and is known as the
nzretencephalon. The remainder of the brain constitutes the posterior di~
vision known as the myelencephalon. The cavity which extends through
both is called the fourth ventricle.
THE SPINAL CORD AND ETS NEIURAL CRESTS,
The Cord. —~As fast as the neural tube is formed by the fusion of
the neural folds, its central canal tends to become compressed laterally
and elongated dorso-ventrally. Its lateral walls also gradually thicken,
and at the end of the second day these walls consist chiefly of two sorts
of cells. First, there are elongated cells extending from the central canal out to its outer walls. These are the cells originally lining the canal,
now known as ependymal cells, and their function is that of support.
Secondly, among the ependymal cells and near the central canal are numerous rounded cells known as germinal cells. They later give rise to
neuroblasts or primitive nerve cells, and also probably to more supporting elements termed glia cells. It has recently been claimed (Barron,
’46) that some of the germinal (indifferent) cells are stimulated to become neuroblasts by contact with growing dendrites of other neuroblasts already partially differentiated.
The Neural Crests and Rudimentary Spinal Ganglia. — As indicated in the /previous chapter, the neural crests when first formed are
simply bands of cells which extend along the dorso-lateral walls of the
neural tube, on either side between it and the ectoderm. As was also
stated, these bands or crests are at first fused with one another dorsally.
By the end of the second day, however, in the older (i.e., anterior) portion of the tube, this dorsal fusion has been obliterated. In this region
there have also appeared in the crests successive enlargements, which
presently become separated from one another to form a series of rudimentary spindl ganglia. There is one of these ganglia for each somite,
352 THE CHICK
except for those of the head region, opposite whose somites the crests
disappear. The spinal ganglia at this time contain both neuroblasts and
indifferent cells.
THE CRANIAL GANGLIA
The neural crests of the head region anterior to the somites do not
disappear. but also form enlargements which separate and take part in
the formation of certain of the cranial ganglia. Parts of these ganglia,
however, are placodal in origin, and surprisingly, according to some
authors some of them even contain endodermal elements as indicated
below. By the end of the second day the ganglionic rudiments are visible, beginning at the anterior end, in the following positions:
The V Nerve Gang1ion.—~The ganglion for the V or trigeminal
nerve is somewhat anterior to the dorsal end of the first or mandibular
Ztl‘t".l1. At the end of the second day it usually appears merely as at Clark
patch in this region (Fig. 176), but later (see third day) it acquires
distimxtly the form of an inverted Y. Apparently most, or all, of this
ganglion is derived from crest material tYntema, 314-) .
The VII and VIII Nerve Ganglia. —-The ganglia for these
nerves form a single mass, the acustico-faciallis ganglion. It lies at this
time just antero-ventral to the auditory sac (see below) ; i.e._, it is above
and slightly in front of the dorsal end of the second or hyoid an-h.
Though unlabeled, it is shown in Figure 176 in the position indicated.
Jones, ’-42 has claimed that part of the VII ganglion is derived from the
dorsal wall of the first visceral pouch, an unusual source of nerve tissue
since the pouch is of course endoderm. Later study (Yntema, 7&4‘), however, seems to show that the origin is, as might be expected, partly crest
and partly placode. The geniculate portion is thought to come from the
placode, which, though closely associated with a pouch, is definitely not
part of it, while the remainder of the facial nerve ganglionic complex is
from the crest. The VIII ganglion appears to be entirely placodal.
The IX and X Nerve Gang1ia.—The IX and X nerve ganglia
arise together, but at the end of the second day they begin to become
separated. The former, or glossopharyngeal ganglion, is then situated
above the dorsal end of the third visceral arch while the latter, or vagus
ganglion, lies above the ends of the fourth and fifth visceral arches.
These ganglia are not visible in Figure 176. As to their sources, it appears that both contain some crest material, while it has again been
claimed by both Winiwarter, ’39 and Jones, ’42 that material for the
L
SECOND DAY: THE EYE 353
petrosal portion of IX and the jugulare part of X are from't'he second
and third visceral pouches respectively. It seems most probable, however, that, as in the case of the VII nerve ganglion, difficulty in separating the ectodermal and endodermal elements has led to error and that
only “ adjacent ectoderm,” i.e., placode, is involved. A diagram of the
location and form of the cranial gan- '
glia viewed from above early on the
second day is given in Figure 185.
ORGANS OF SPECIAL SENSE
THE EYE
The Optic Stalks, the Uptic Cup
and the Choroid Fissure. —The
optic vesicles, it will be recalled, are
hollow out-pushings from the forehrain with which they remain connected by constricted regions known
as the optic stalks (Fig. 186). These
stalks are the so-called “ optic nerves,”
though as will appear, the real optic
nerves develop later. It is to be noted
that the above constriction has occurred in such a manner that each
stalk connects with its vesicle near the
ventral side of the latter, rather than
at its center. Invagination of the outer
wall of the vesicle now occurs, oblit
Fig. 185. — Diagram of the cephal_ . ic neural crest of a chick of about
crating its original cavity, and con» 12 somiles From Lillie (Develop
ment of the Chick). After Wilhelm
vetting it into the two-layered optic His at Auditory Sm 3. 50mm,"
cup, with the optic stalk attached to
its ventral edge. The walls of the cup on either side of the point where the
stalk is attached now grow outward, i.e., toward the ectoderm, but their
ventral edges do not quite meet one another. Thus a fissure is left in the
ventral side of the cup extending from its edge inward to the optic
stalk. This, as in the Frog, is the choroid fissure. Meanwhile the rim of
the cup bounding its aperture, the pupil,’ becomes slightly constricted.
The invaginated or outer wall of the vesicle has now necessarily become
354 THE CHICK
the inner wall of the cup, and will, therefore, be referred to as the inner
wall in future discussion. It is the rudiment of the nervous layer of the
retina (see Chapter ll).
The Development of the Lens. —Before the above invagination
of each optic vesicle occurred, the vesicle had pushed out far enough to
‘touch the surface ectoderm. When this happened, the ectoderm at the
point of contact began to thicken, and when the invagination of the vesicle took place, this thickened ectodermal wall also invaginated. Thus
a hollow thick-walled sac was formed resting just within the rim of the
Fig. 186. — Diagrams of sections through the eye of the Chick embryo at the end
of the second day. From Kellicott (Chordate Development). After Lillie. The dorsal
margin is toward the top of the page in A and B. A. Eye as viewed directly. B. Vertical section through the line x—cf, in A. C. Horizontal section through the line y—y in A.
cf. Choroid fissure. co. Cavity of primary optic vesicle. ec. Superficial ectoderm
of head. i. Inner or nervous layer of the retina. l. Lens. 0. Outer or pigmented layer
of optic cup. 01. Opening of lens sac from surface of head. pc. Posterior (vitreous)
chamber of eye.-s. Optic stalk, continuous with the floor and lateral wall of the
diencephalon.
optic cup. This is, of course, the rudiment of the lens; at the end of the
second day it has not quite detached itself from the outer ectoderm.
As in the case of the Amphibian, it has been shown that the optic cup
has the power to induce lens formation in ectoderm which would not
otherwise form it. Thus optic vesicles or cups from embryos up to the
4.0-somite stage (fourth day) will induce lenses when transplanted to
young hosts (primitive streak to’ eight somites). In a host older than
four somites, however, the transplant will produce positive results only
when implanted as far anterior as the potential head or neck region. In
any case actual contact of the cup with the ectoderm seems necessary to
effect induction. Also as in the Amphibian, the new lens may come from '
cells of the optic cup itself as well as from the host ectoderm (Alexander, ’37) , and the inductive process is a gradual one (McKeehan, ’54).
3
3
l
5.
l
E
.oa.......« ~ e
.-
SECOND DAY: THE EXCRETORY SYSTEM 355
THE EAR
The sensory part of the ear begins as a thickening of the ectoderm on
the side of the head above and slightly posterior to the dorsal end of
the hyoid arch. This thickening presently starts to invaginate, thus forming a depression -— the auditory pit. During the second day the process
of invagination continues, and is soon accompanied by an approximation of the anterior and posterior lips of the pit. Near the end of the
second day the ventral lip also takes part in the closure by moving dorsally, and thus the pit is transformed into a small mouthed sac. It is the
auditory sac or otocyst (Fig. 176).
THE URINOGENITAL SYSTEM
Because of their close connection in the adult, the excretory and reproductive systems are, as usual, considered under a common heading.
Their development, however, is largely separate, and must, therefore,
he so treated. Of the two systems, only certain parts of the excretory
appear during the second day.
THE EXCRETORY SYSTEM
The excretory system of the Chick in common v",'.Li that of other Amniota consists of three separate parts, the pronephros, mesonephros, and
metanephros. These parts develop in the order named, and the first two
have largely disappeared by the close of embryonic life; only the last
remains functional as the permanent excretory organ of the adult. During the second day the pronephros develops, and near its close the mesonephros has just begun to appear.
The Pronephros.——The pronephros is vestigial in character, and
only appears typically from the tenth to the fifteenth somites. Rudiments of it, however, are sometimes found as far forward as the fifth
somite. In the more posterior region indicated, its development is as
follows:
The Pronephric Tubules. —— In the dorso-lateral portion of the nephrotome opposite the posterior end of each somite a thickening occurs,
and from it a cord of cells grows outward and upward for a short distance (Fig. 187, pr’n. 1). At the same time the nephrotome becomes
detached from the somite. These lateral outgrowths are termed the pronephric tubules, though they usually do not acquire any lumen. Some356 THE CHICK
times, however, a slight lumen is present in the proximal part of the
tubule (Fig. 187, pr’n. 2), and it opens into the coelom as a rudimentary nephrostome. It is also said that degenerate glonwrztli (or more
properly glomi) sometimes develop later on the coelomic wall opposite
the nephrostomal mouths (Lillie).
The Pronephric and W olfiian Ducts. — The distal part of each of the
above cell cards or “ tubules ” presently bends posteriorly and grows in
Fig. 187.-——A. Transverse section through the twelfth somite of a 16s embryo.
From Lillie (Development of the Chick). B. Three sections behind A to show the
nephmstoine of the same pronephric tubule.
A0. Aorta. CC. Central canal. Coel. Coelom. E.E.B.C'. Extra-emllryonic coelom
Iexocoelnm 1. .lIs'c/L. Mesenchyme. N’c}1. Notoclmrd. n.Cr. Neural crest. .’V’.st Nephrostome. n.T. Neural tube. pr'n. 1,2. Distal and proximal divisions of pronephric tubule.
$.12. Twelfth sornite. Sa’pl. Somatopleure. Spl’pl. Splanchnopleure. V.c.p. Posterior
cardinal vein.
this direction until it comes in contact with the tubule following it. In
this manner, a continuous backwardly directed cord of cells is formed
which connects with each successive tubule. Finally, the bent portion of
the last cell cord continues to grow posteriorly between the nephrotomal mass and the body wall. As will appear subsequently, the anterior
end of this backward growing rod of cells is the rudiment of the pronephric duct. and its more posterior portion, the rudiment of the mesonephric or Wolflian duct. Before the end of the second day, indeed, the
anterior or pronephric section of the rod has acquired a lumen, thus becoming a real duct.
SECOND DAY: THE AMNION 357
The Mesonephros. —— The mesonephros corresponds to the organ of
the same name which functions as the permanent excretory organ of the
Frog. In the Chick, however, as indicated above, this excretory function
continues only during a part of embryonic life. The antericr end of the
inesonephros slightly overlaps the posterior end_of the pronephric region, but its development here is rudimentary, the organ acquiring its
typical form only from the twentieth to the thirtieth somites. During the
close of the second day it begins to appear in the following manner,
development progressing posteriorly.
The Primary Mesonephric Tu‘ou1es.——The nephrotome in the
region indicated becomes separated both from the somites and the lateral plate. It then lies just ventro-medially to the rod of cells which is
to become the Woliiian duct. Above this duct the posterior cardinal vein
presently appears, while between the nephrotome and the median line
of the embryo runs the dorsal aorta. The nephrotorne is thus between
the aorta and the future Woliiian duct (Fig. 174«). Presently in the
neighborhood of each somite, there appear in this nephrotomal band
two or more spherical condensations. Then beginning at the anterior
end of the band each of these condensed spheres starts to acquire a cavity, each vesicle thus formed being the rudiment of a mesonephric tubule
and a Malpighian. body. The more ventral spheres in each somite are
the first thus to become vesicular, and they are the rudiments of the socalled primary mesonephric tubules as distinguished from the others.
(See next chapter, Fig. 207.)
T AMNION AND OTHER EXTRA-EMBRYONIC STRUCTURES
From the embryological point of view all Vertebrates belong to one
of two classes; i.e., the Anamniota or the Amniota. The former group
includes Amphibians and Fishes, while the latter includes Reptiles,
Birds, and Mammals. The Amniota. as the name implies. are those
which possess an amnion, while the Anamniota are those which lack it.
Amphioxus, the Frog, and Fish have been studied as representatives of
the latter class, and we are now studying the Chick as an example of
the former or Amniote group. The amnion begins to form on the second day of the Chick’s incubation, but is not completed until about the
fourth day. In order to make the structure of this organ more clear, however, it seems best to describe its entire development, together withthat
of certain other extra-embryonic organs and membranes.
358 . THE CHICK
THE AMNION IN PROCESS OF DEVELOPMENT
Development during the Second Day. —- During the second day
a fold in the blastoderm occurs just in front of the head of the embryo
in the region of the proamnion. Since there is as yet no mesoderm in
this region, the fold at first contains only ectoderm and endoderm. Presently, however, the mesoderm extends into this vicinity, and here, as
elsewhere, is split into the extra-embryonic extensions of the somatic
and splanchnic layers
with the extra-embryonic
coelomic space between
them; both these layers
then become involved in
the fold. The splanchnic
layer together with the
endoderm, however, is
soon withdrawn to the
surface of the yolk, while
t:,§t;§it:,2;?§;8t:;::‘:t..  ;;:a:::‘; the some layer  me
the yolk (,yolk-stilk uénbilicxislk in a ChicFlc of extra-embryonic ectoderm
3 -' ' ‘r. . ' . .
fi‘2‘;:,;:,:"zm;:,:;:e:,mi: 9.32:: winch  -r
a Dorsal aorta. c. Coelom. ebcxexocoelom. ig. In- the two permanent layers
testinal groove. la. Lateral folds of amnion. ‘UYJ.
Vitemne vein of the amniotic head fold.
The embryo has now begun to sink somewhat into the surface of the yolk, and as it does so the
amniotic fold gradually grows back over it. This backward growth is
also accompanied by the development of lateral amniotic folds extending posteriorly on either side. By the end of the second day the embryo
has been covered over in this manner almost as far back as the vitelline
arteries (Figs. 176 and 188). The latter figure shows a cross section
through a region where the folds have not yet quite covered the embryo.
Development during the Third Day. —— About the end of the
second day, or the beginning of the third, another fold appears at the
posterior end of the embryo, and grows forward toward the head fold.
This is the amniotic tail folcl, which soon becomes coextensive upon either side with the posterior ends of the lateral amniotic folds. It is similar to the corresponding head fold except that from the first it contains
only ectoderm and somatic mesoderm. Since the anterior portion of the
amnion starts earlier and grows rapidly, the point at which the converg
l
l
~ SECOND DAY: THE COMPLETED AMNION 359
e is quite near the posterior end of the
ing folds finally meet and {us
sting above the Chick previous to the
animal. The oval opening exi
is the amniotic umbilicus.
Fourth Day. —The end of the third,
or beginning of the fourth day, marks the meeting and fusion of the am
niotic folds at the center of the amniotic umbilicus. The embryo has by D
' ‘this time turned upon its left side throughout the greater part of its
closure
Development during the
ith 35 pairs of somites (about
-third somite. From Kellicott
ransverse section of Chick embryo w
hrough the region of the twenty
(Chordate Developm . .
Dorsal aorta. c. Embryonic coelom. ch. Chorion.
Fig. 189. —-T
72 hours), passing t
a. Amnion. ac. Amniotic cavity. ao.
d. Derrnatome. ebc. exocoelom. g. Rudiment of spinal ganglion. m. Mesonephric
tubule. my. Myotome. p. Posterior cardinal vein. 5. Sclerotome. sa. Sero-amniotic
connection. so. Subcardinal vein. so. Somatic mesoderm. sp. Splanchnic mesoderm.
12. Vitelline artery. W. Wolflian duct.
ds do not turn with it, the closure occurs
not above itsback, but above its right side. It also follows from this,
that the fold of the left side covers the hack of the embryo as well as a
part of the right side. The amnion may now be said to be complete.
_ THE COMPLETED AMNION AND RELATED PARTS
The Amnion and Amniotic Cavity. ——- It is obvious that the amniotic folds, like any other folds, must be composed of two main parts,
ther at the crest of the fold. It is
each part being continuous with the 0
also obvious that one of these parts, i.e., the inner or lower one, lies
everywhere next to the embryo. When fusion occurs, therefore, this inner
length, and inasmuch as the fol
360 THE CHICK .
part will become continuous, completely bounding a new cavity which
surrounds the embryo at every point except for a restricted region on its
ventral side (see below under somatic umbilicus). This continuous inner membrane is the amnion, and the cavity thus formed is the amniotic
cavity. Moreover, inasmuch as the folds involve both ectoderm and
mesoderm, the inner membrane or amnion must likewise consist of ectoderm and mesoderm, the former lining the amniotic cavity and the latter‘ '
forming a coat outside the lining (Figs. 189 and 190).
The Chorion.— At the fusion of the folds the outer part, like the
inner, necessarily becomes continuous. Likewise, it too consists of both
ectoderm and mesoderm, but in this case, the ectoderm will lie outside
and the mesoderm inside, i.e., toward the amnion. The outer membrane
thus formed is called the chorion, serosa or false amnion. Between it and
the inner membrane or true amnion, there is naturally the same space
which separated the inner and outer parts of the amniotic folds, i.e., the
extra-embryonic coelom or exocoelom. This relationship will be made
clear by reference to Figure 190. it may be mentioned incidentally in
this connection that this exocoelomic space eventually becomes filled by
an important sac-like organ (allantois) whose origin and structure will
be described below.
The Sero-Amniotic Connection.———It has been implied that the
extra-embryonic coelom, with whatever may occupy it, everywhere separates the amniotic membrane from the chorionic membrane. This is
true except at one point. At the point of final fusion of the amniotic
folds, i.e., the amniotic umbilicus, the coelomic space is interrupted by
a small area of mesoderm which persists, and serves to unite the above
membranes. It is called the sero-amniotic connection. (Figs. 189 and
190).
The Amniotic F luid.——Shortly after the completion of the amniotic cavity, fluid begins to accumulate within it. Thus the embryo is
soon practically surrounded by a liquid cushion which protects it from
pressure by its membranes and rigid shell. This is the amniotic
Presently, about the fifth day, muscle fibers develop in the mesoderm
of the amnion and begin to send waves of contraction over it. This
causes a gentle rocking of the embryo, and is apparently instrumental in
preventing its adhesion to the various embryonic membranes. It may
also help to obviate the stagnation of blood in the vessels, a condition
which might tend to occur on account of the pressure from the growing
organs.
SECOND DAY: THE COMPLETED AMNION 361
All. Am. char.
5. am. 7
   
Figs. 190, 191, 192.——Diagrams of the" relations of
the extra~embryonic membranes in the Chick. Figures
and description from Lillie (Development of the
Chick). The ectoderm and endoderm are represented
by plain lines; the mesoderm by a cross-hatched line
or band. The yolk-sac is represented by broken parallel lines. In Fig. 190 the allantois is represented as a
sac. In Figs. 191 and 192, where it is supposed Ito be
seen in section. its cavity is represented by unbroken
parallel lines. The stalk of the allantois is exaggerated
in all the diagrams to bring out its connection with
the embryo.
Fig. 190. —Fourth day of incubation. The embryo is
surrounded by the amnion which arises from the somatic umbilicus, Umb., in front and behind: the seroamniotic connection, S.am., is represented above the
tail of the embryo; it consists at this time of a fusion
of the ectoderm of the amnion and chorion. The allantois, AIL, is represented as a sac, the stalk of which
enters the umbilicus behind the yolk-stalk; the allantois lies in the extra-embryonic body-cavity (exocoelom) , and its mesodermal layer is fused with the
corresponding layer "of the chorion above the embryo.
The septa of the yolk-sac, Y.S.S., are represented at
an early stage. The splitting of the mesoderm has progressed beyond the equator of the yolk-sac, and the
undivided portion is slightly thickened to form the
beginning of the connective-tissue ring that'surrounds
the yolk-sac umbilicus. The ectoderm and endoderm
meet in the zone of junction, beyond which the ectoderm is continued a short distance. The vitelline membrane, V.M., is ruptured, but still covers the yolk in
the neighborhood of the yolk-sac umbilicus. The albumen is not represented in this figure. (For complete
explanation of lettering see Fig. 192.)
362 THE CHICK
THE SOMATIC UMBILICUS, THE YOLK—STALK, AND THE
YOLK——SAC
Though they are not a part of the amnion, it seems best to include in
connection with its description an account of these structures which, to
some extent, develop with it. 4
The Somatic Umbilicus. ——During the formation of the amnion,
the gradual separation of the embryo from the yolk has been progressing. This has been accomplished by the steady in-pushing of the ventral
portions of the head, tail, and lateral folds (limiting sulci} beneath the
body of the growing Chick. The result is that by the time the amnion
is completed, these folds have approached one another quite closely,
though without coming into contact. In this manner they give rise to a
short, thick, hollow stalk which connects the embryo with the yolk-sac
and its extra-embryonic membranes. The outermost wall of this stalk is
continuous with that of the amnion, and is, therefore, composed of ectoderm and somatic mesoderm: for this reason, this outer wall is referred
to as the somatic umbilicus (Fig. 190).
The Yolk-Stalk. —— Within this wall and surrounding the inner wall
of the stalk, is a space continuous externally with the extra-embryonic
coelom and internally with the coelom of the embryo itself. Finally, the
inner wall of the stalk consists of splanchnic mesoderm and endoderm.
It is known as the yolk-stalk, but is really merely an inner tube of the
somatic umbilicus separated from it by coelomic space.
The Yolk-Sac.——The wall of the yolk-stalk is coextensive within
the embryo with the wall of the gut, and externally with the layer of
endoderm and the splanchnic mesoderm which overlies the yolk. This
layer is continually growing out around the yolk, and at its outermost
border, i.e., the region of the zone of junction, the endodermal portion
of it becomes continuous with the chorion which overlies it. Thus by
means of the extension of these layers the yolk is gradually enclosed in
a covering, whose inner layer of splanchnic mesoderm and endoderm
constitutes the yolk-sac, attached to the embryo by means of the yolkstalk. Upon the ninth day of incubation this sac has become virtually
complete, save at a point on the side of the yolk postero-ventral to the
body of the Chick, where an opening remains, known as the yolk-sac
umbilicus. This opening, however, is finally closed about the seventeenth day by a solid mass of tissue. It may be recalled in this connection that the rim of the blastoderm, which has thus overgrown the yolk,
was previously homologized with the lip of a very extended blastopore,
4 .. .a_...m.,,.,,,_.,.j,
SECOND DAY: THE ALLANTOIS 353
the true blastopore (primil".Ve Streak) haVing been separated from the
remainder of the rim during gastrulation. Hence upon this basis it is
possible to consider the uncovered yolk mass as a sort of very large
secondary, or yolk-Lla.stopare, the latter term being really only another
name for the yolk-sac umbilicus. A somewhat similar separate blastepore, it may be noted, also occurs in the development of the Elasmobranchs (i.e., the cartilaginous or non-bony fishes) in which the term
yolk-blastopore is regularly applied to it.
On the basis of this description, it is clear that beyond the boundaries
of the amnion the chorion is really nothing more than the uppermost
layer of the blastoderm. It is to be noted, however, that this upper
layer consisting of ectoderm and somatic mesoderrn is soon separated
from the lower layer composed of splanchnic mesoderm and endoderm
by the extra-embryonic coelom. Furthermore, this space presently becomes occupied by another extra-embryonic organ (allantois) , to be described below. Finally it must also be mentioned that early in its development, the lower layer, just indicated, ie, the real yolk-sac layer,
consisting of endoderm and splanchnic mesoderm, becomes covered internally with deep folds, the yolk-sac septa, which gradually press downward into the yolk. These septa in common with the remainder of the
yolk-sac endoderm in the area vasculosa, contain glandular and absorbing cells which digest the yolk in situ before passing it into the
blood vessels. Thus though a slight lumen exists in the yolk-stalk connecting the inside of the yolk-sac with the enteric canal, no yolk appears to pass into the embryo through this lumen. Abnorrnally high or
low temperatures during incubation, e.g., 39.5° C and 3-15° C, appear
to slow up the process of absorption of both yolk and albumen (Romanofl', ’43) .
THE ALLANTOIS
Another extremely important extra-embryonic organ possessed in
some degree by all Amniota is the allantois, and it will be found convenient to consider its entire history also at this time.
Its Early Development. ——The allantois starts in the form of an
out-pushing from the ventral wall of the hind-gut (Fig. 193). This is
scarcely visible before the beginning of the third day, and was, therefore, not referred to in the foregoing description of the alimentary tract.
This out-pushing naturally involves the endoderm and the mesodermal
ventral mesentery which occurs in this region. Thus the sac which is '
presently formed possesses an inner endodermal and an outer mesoder364 THE CHICK
mal layer. By the fourth day the allantois has pushed out through the
coelomic space between the somatic umbilicus and the yolk-stalk, and
is beginning to spread out in the extra-embryonic coelom (Fig. 190}.
The narrow neck of the organ which then connects the outer sac-like
Fig. 191.—Ninth day of incubation. The yolk-sac um
, bilicus has become much narrowed; it is surrounded by
the mesodermal connective-tissue ring, C.T.R., and by the
free edges of the ectoderm and endoderm. The vitelline
membrarie still covers the yolk-sac umbilicus and is
folded into the albumen. The allantois has expanded
around the amnion and yolk-sac and its outer wall is
fused with the chorion. It has pushed a fold of the
chorion over the sero-amniotic connection, into which the
mesoderm has penetrated, and thus forms the upper fold
of the albumen-sac. The lower fold of the albumen-sac
is likewise formed by a duplication of the chorion and
allantois; it must be understood that lateral folds are
forming also. so that the albumen is being surrounded
from all sides. The stalk or neck of the allantois is exaggerated so as to show its connection with the embryo;
it is supposed to pass over the amnion, and not. of course,
through the cavity of the latter. (For explanation of lettering see Fig. 192.)
portion with the gut is known as the allantoic stalk or neck. Along this
stalk pass the two allantoic arteries (later only one), and the single allantoic vein, ‘to end in abundant ramifications over the surface of the
sac. The allantois now grows rapidly, and within a couple of days has
entirely covered the amnion, occupying the space between that organ
and the chorion. Presently the amniotic and chorionic mesoderm fuse,
forming the chorio-allantoic membrane (Figs. 191 and 192). In this
;
3
i
SECOND DAY: THE ALLANTOIS T 365
manner, the above ramifications of the blood vessels are brought very
near to the shell, through which an exchange of gases is possible. Thus
the allantois serves as an organ of respiration for the Chick during embryonic life. Its cavity also acts as a receptacle for the waste products of
gm. 3. Am.
   
All. 5. En:
5-"W AILC.
Chor. »(
Am.
Fig. 192.—Twelfth day of incubation. The conditions
are more advanced than those represented in Fig. 191.
The albumen-sac is closing; its connection with the cavity of the amnion by way of the sero-amniotic connection
will be obvious. The inner wall of the allantois has fused
extensively with the amnion. The umbilicus of the yolksac is much reduced, and some yolk protrudes into the
albumen (sac of the yolk-sac umbilicus, transitory structure soon drawn into the yoll-:-sac proper).
Alb. Albumen. Alb.S. Albumen-sac. .411. Allantois.
AIL]. Inner wall of allantois. /1ll.C. Allantoic cavity.
AZLS. Allantoic stalk or neck. All. + Am. Fusion of allantois and amnion. Am. Amnion. Am.C. Amniotic cavity. Chor. Chorion. C.T.R. Connective--ti.-rsue ring. Eat.
Ectoderm. E.E.B.C. Exococlom (extra-embryonic bodycavity). Ent. Endoderm. Mes. Mesoderm. S.-Am. Sero-amniotic connection. S.Y.S.U. Sac of the yolk-sac umbilicus. Umb. Umbilicus. (somatic). V./ll. Vitelline
membrane. Y.S. Yolk-sac. Y.S.S. Septa of yolk-sac.
metabolism, which are conveyed thither through the allantoic stalk from
the region of the cloaca. lt is thus to be noted that this organ is homologous not only in method of origin, but also partly in “function with the
urinary bladder of the Frog. The latter, however, of course never extends outside of the coelomic cavity, and though it may or may not
be endodermal, the allantois is certainly so.
366 THE CHICK
The Later Development of the Allantois and the Formation
of the A1bumen-Sac. — Meanwhile the albumen is becoming concentrated on the side of the egg next to the yolk-sac urnbilicus, and by the
ninth or tenth day has become very much condensed. Concurrently
the real yolk-sac layer, together with the chorion, has grown around the
yolk so that the edges of the over-growth have more than kept in con
tactfiwith the receding albumen. They have in fact thrust themselves in
between it and the yolk, so that the albumen is bounded upon its inner
side by a layer of chorion. At the same time, save postero-dorsally in
the region of the sero-amniotic connection, the allantois has been following this overgrowth of .the yolk-sac layer and chorion; it lies between
these two layers in the exocoelom, and its walls are fused respectively
with the chorionic layer and that of the yolk-sac. Thus as the latter layers push in between the yolk and the albumen to close the yolk-sac umbilicus, they are accompanied, except postero-dorsally, by the allantois.
Ventro-laterally a fold of the chorion presently pushes its way around
the outside of the albumen between it and the shell membrane. Here too,
moreover, between the two layers of the chorionic fold there follows an
outer fold of the allantois. Meanwhile in the postero-dorsal region, as already suggested, the expansion of this organ is obstructed by the seroamniotic connection. At this point, therefore, it pushes up over this connection, carrying the chorion before ‘it. Thus this dorsal fold, consisting
of a layer of chorion and allantoic wall, comes down between the albumen and shell membrane to meet the similarly constituted ventrolateral folds already described. Hence, at ten days the albumen at the
yolk-sac umbilicus is surrounded by a double layer of fused chorionic
and allantoic tissue, the albumen-sac. There is just one region in the
wall of the sac, however, where all of these layers are not present. This ,
is a small area on its internal dorsal side where the allantois could not
extend because of the sero-amniotic connection. There, therefore, the wall
consists only of chorion, and at one point of the connection itself (Figs.
191,192). A perforation appears in this connection, and on the twelfth ‘
day some albumen enters the amniotic cavity. The remainder of the
albumen is absorbed, and the albumen-sac together with the yolk-sac is
drawn within the embryo just previous to hatching. According to Randles A
and Romanoff, ’50, a periodic turning of the egg is necessary if all these
events are to be accomplished normally at the times indicated. Hatching
is apparently aided by the contraction of the muscular walls of the allantois and by the muscles of the somatic umbilicus (see also Fig. 193).
l
i
i
l
l
“"
SECOND DAY: SUMMARY . 367
SUMMARY OF THE CONDITION AT THE END OF THE
SECOND DAY OF INCUBATION '
I. GENERAL APPEARANCE
The cranial flexure has been initiated, and has brought the fore-brain
to a point where it almost touches the heart, and the mid-brain faces anteriorly. The cervical flexure is also evident in the region of hind-brain
and trunk. In correlation with these flexures lateral rotation has started
so that the embryo lies on its side as far back as the 13th somite.
II. THE SOMITES
There are approximately 27 somites, in which the myotomes and
cutis plates have begun to differentiate, together with the mesenchymatous rudiment of the selerotome.
III. THE FORE-GUT
In the fore-gut the stomodaeum is formed, and in connection with it
Rathke’s pocket, a part of the future hypophysis, is beginning to appear.
Four pairs of visceral pouches and five pairs of arches have begun to develop, and the first pair of pouches have acquired openings to the exterior. The -rudiments of the thyroid, the respiratory system, and the liver
are also present.
IV. THE MID—GUT
This is but slightly developed, although the lateral folds are beginning to mark it off from the extra-embryonic archenteron.
V. THE HIND—CUT
The hind-gut has begun to form and its posterior end has fused with
the ectoderm to form the anal plate or cloacal membrane. In connection
with it there has also arisen the ventral mesentery.
VI. THE CIRCULATORY SYSTEM
The Heart.—-A bent tubular heart has been developed, lined by
endothelium and covered with a myocardium. The regions of the atria,
the ventricles, and the bulbus and trztncus arteriosus are indicated, and
pulsation has been initiated.
368 THE CHICK
The Arteries. —The dorsal aortae are in evidence. Also the ventral
aorta has appeared and become incorporated into the truncus. The first
pair of aortic arches are in process of formation, and the second and
third aortic arches are completed. The vitelline arteries have appeared.
The Veins.——The anterior and posterior cardinals, the sinus venosus, the (luctus venosus, and the ducts of Cuvier have been developed.
In connection with the latter the septa known as the lateral mesocardia
Fig. 193.——Median sagittal section through posterior end of four-day chick. From Kellicott (Chordate Development). After Gasser (Maurer).
al. Allantois. am. Amnion (tail-fold). c. Cloaca.
rn. Cloacal membrane. 11. Notochord. r. Rectum. s.
Spinal cord. y. Wall of yolk-sac (endoderm and
splanchnic mesoderml.
have also been formed. Outside the embryo the anterior vitelline veins
have arisen, and with them the rudiments of the lateral vitelline veins.
The sinus terminalis has become complete.
VII. THE NERVOUS SYSTEM
The Brain and the Cranial Ganglia.-—As indicated under external appearance the cranial and cervical flexures have become well
marked. The fore-brain, mid-brain and hind-brain are now clearly indicated, and within the first main division certain parts are apparent, as
follows: The outgrowth of the optic stalks is well advanced, and there
may also be evident the rudiments of the optic chiasma, the optic recess,‘
the cerebral lzernispheres, the in fundibulum, and some other minor struc‘tunes. The roof of the mid-brain is becoming prominently arched.
SECOND DAY: SUMMARY 369
The cranial ganglionic rudiments of the V, VII and Vlll, and IX and
X nerves are visible, and the latter pair are beginning to separate.
The Spinal Cord and Ganglia. —— The spinal cord has become
thick-walled laterally, and has developed ependymal and germinal cells.
The neural crests are segmenting to form the spinal ganglia.
VIII. THE ORGANS OF SPECIALSENSE
The optic vesicles have become invaginated to form the optic cups,
and the external ectoderm opposite each cup has invaginated in the
process of forming a lens. In connection with the ear, the auditory portion of the ectoderm has become invaginated to form the auditory sac.
IX. THE URINOGENITAL SYSTEM
Only the embryonic parts of the excretory portion of this system appear during the second day. These are the pronephros, including the
Wolflian duct, and the rudiments of the mesonephros. These rudiments
consist of concentrations of nephrogenous tissue, some of which are beginning to become vesicular in the formation of the mesonephric tubules
and the Malpighian bodies.
X. THE AMNION
This extra-embryonic organ begins its development on the second day
with the appearance of the amniotic head fold, the amniotic lateral
folds, and sometimes an indication of the amniotic tail fold.
The complete development of the amnion, the chorion, the allantois,
and the yolk-sac is described in this chapter.
TI
HE CHICK: DEVELOPMENT DURING THE THIRD
DAY OF INCUBATION
GENERAL APPEARANCE
FLEXURES AND TORSION
THE embryo has of course increased somewhat in size, but the
most obvious changes concern the flexures. The cranial flexure is somewhat more marked, while the cervical flexure has greatly increased, so
that the region of the hind-brain, rather than the mid-brain is now the
most anterior part of the embryo. By the close of this day also a new
curvature has become evident at the posterior end. It involves mainly
the tail, and is called the caudal flexure. Between this flexure and the
cervical flexure the back of the embryo is temporarily somewhat bent
in a ventral direction, i.e., opposite to the other curvatures. This is because of the broad attachment to the yolk which still extends throughout
the middle region and tends to draw this part of the embryo ventrad
(Fig. 200). Accompanying these increases in flexure the lateral rotation has progressed posteriorly until by the end of the day the embryo
is on its side about as far back as the twenty-first somite.
LIMB 'RUDS
The limb buds become clearly visible by the end of the third day,
and appear as broad swellings on either side of the embryo. The anterior buds extend from about the fifteenth to the twentieth somite, and
the- posterior buds from about the twenty-seventh to the thirty-third
soniite.
THE SOMITES
During the third day the number of pairs of somites increases to about
36. The newer posterior somites when first formed are in the same condition as were those which are now anterior, and are destined to go
THIRD DAY: THE FORE—GUT 371
through the same process of development. Meanwhile, the more advanced anterior members of the series do not greatly change except for
further modifications along the lines already indicated on the second
day. These modifications are as follows:
Each myotome or muscle plate continues to grow down along the inside ot its respective cutis plate, until in the most mature somites it
reaches the ventral end of the cutis plate and fuses with it. In this manner a complete double layer of cells arises. In the inner layer or muscle
plate thus formed, the cells or rnyoblasts presently begin to become
spindle-shaped, reaching from the anterior to the posterior walls of each
myotome. These are mostly rudiments of dorsal voluntary muscles.
Somewhat later on the third day the outer or cutis plates of somites
which have reached this stage begin to break up into mesenchyme, which
wanders outward toward the ectodermal wall. There it eventually gives
rise to the dermis of the dorsal region, that of the lateral and ventral
parts being derived from the adjacent somatopleurc (Murray, ’28) .
The sclerotomal mesenchyme continues to collect about the notochord
and the sides of the nerve cord.
THE ALIMENTARY TRACT
THE FORE—GUT
The Oral Cavity.———During the third day, the oral plate breaks
through, placing the stomodaeum in direct communication with the
pharynx (Fig. 204-). The region in which the digestive tract opens to
the exterior anteriorly is thus partly stomodaeal and partly pharyngeal.
It is called the oral cavity.
The Hypophysis or Pituitary Body.——It will be recalled that
at 24 hours a hollow diverticulum called Rathke’s pocket was extending
forward from the roof of the stomodaeum toward the floor of the dien_cephalo_n in the vicinity of the infundibulum. At about the 30-somite
stage it has nearly reached the latter organ (Fig. 204), and shortly its
end begins to broaden out and become branched. Finally, near the end
of the incubation period, these branches have become a mass of tubular
tissue well supplied with blood vessels. This glandular mass then loses
all connection with the oral epithelium from which it arose, and be«
comesrfirmly attached to the infundibulum. In this manner the original
Rathl-:e’s pocket comes to constitute the anterior part of the hypophysis
or pituitary body, while the infundibulum becomes the posterior part
372 THE CHICK
and stalk of that organ. Experimental work has shown that the out.
growth of Rathl<e’s pocket is originally induced by the presence of the
infundibulum, and that both structures influence one another in the normal development of the completed organ (Hillemann, ’4-3). It may be
recalled that this same relationship is true in the Frog, except that there
the homologue of Rathke’s pocket is merely a strand of cells.
 
 
   
v.C.d.1 v,P...2, v.C.d.2
;-"v_’.;,~1_‘ M‘ __« v.P.3
:_prfo.G.
buss. ‘
     
     
 
 
tar. - tr. Gr. _
Ls  ,
Fig. 194.—Reconstruction of the fore-gut of a Chick of 72 hours. From
Lillie (Development of the Chick). After Kastschenko.
Hyp. Rathke’s pocket, rudiment of anterior hypophysis. Iar.-tr.Cr. Laryngotracheal groove._ Lg. Lung. Md.a. Mandibular arch. Oes. Oesopliagus.
pr’o.G. Preoral gut. Stom. Stomach. Th. Thyroid. v.C.d. 1, 2. Dorsal division of the first and second visceral clefts. v,C.i:.2. Ventral division of the
second visceral cleft. 1.2.1’. 1,2,3,4-. First, second, third, and fourth visceral
pouches.
The Visceral Pouches and Arches.
The P0uch.es.———lt will be remembered thatduring the second day
four pairs of visceral pouches had appeared; the first three had reached
the ectoderm, and each member of the first pair had acquired a cleft
opening ‘(O the outside. During the third day the first pair of pouches
retain their openings, while each member of the second pair develops
a short dorsal and a long ventral cleft, corresponding to the points of
fusion between ectoderm and endoderm described in the preceding chapter. The members of the fourth pair of pouches now acquire connections
with the ectoderm at their dorsal ends, but never develop any cleits
(Fig. 194).
The Arches. —-—— The visceral arches undergo no special change on the
third day, except the development in some of them of the aortic blood
vessels (arches) which will be described below.
The Thyroid. ~—~— During the third day, the rudiment of the thyroid
which was last described as a slight depression in the floor of the pharTHIRD DAY: THE FORE—GUT 373
ynx, continues to evaginate. By means of this process, the end of the
third day finds the above depression transformed into a wide-mouthed
sac. Figure 195 shows in cross section this and other structures indicated above.
The Laryngotracheal Groove and Lung Prirnordia.——At the
end of the second day a shallow longitudinal groove with a pair of
Fig. 195.—Frontal section through the pharynx of a 35 somite embryo. From
Lillie (Development of the Chick).
a.a. 1, 2, 3, 4. First, second, third, fourth aortic arches. Hyp. Rathkc’s pocket,
ru<iimr:nt of anterior hypophysis. J. J ugular vein. lar.-tr. Gr. Laryngotracheal groove
lpost branchial pharynx). or. Oral cavity. Ph. Pharynx. v./1. 1, 2, 3. First, second,
third visceral arches. L'.G. 1, First visceral cleft. v.F. 2, 3. Second and third visceral
furrows. v.P. 2, 3, 4. Second, third, fourth visceral pouches. III. Third cranial nerve.
postero-lateral expansions had appeared in the floor of the pharynx
just caudal to the visceral pouches, indicating the beginning of the
respiratory system. This groove now becomes much narrower and
deeper, and is called the laryngotracheal groove. Also its postero-lateral
expansions develop into tubelil-re outgrowths "which, as previously indicated, are then ordinarily termed the lung prirnordia. Strictly speaking, however, they really represent, not only the beginnings of the lungs,
but also of the bronchi, i.e., the entire respiratory system.
The Esophagus and the Stomach.—— By the end of thethird day
the esophagus is represented by an abrupt narrowing of the fore-gut
immediately posterior to the pharynx. The narrowed portion leads into
a slightly dilated region just anterior to the liver rudiment, and this di
lation is the beginning of the stomach, i.e., the proventriculus and gizzard (see the fifth day).
374 -THE CHICK
The Liver. —— At the end of the second day the liver was represented
by two anterior-ly directed diverticula from the region of the anterior
intestinal portal; the more anterior of these had extended far enough
forward to overlie slightly the point of union of» the vitelline veins.
During the third day, these diverticula grow somewhat further forward,
the anterior member of the pair along the left dorsal side of the ductus
venosus, and the posterior member along its right ventral side. Both
Fig. 195.--Rec-onstructions of the liver diverticula of the Chick.
From Lillie (Development of the Chick). After Hammar.
A. On the third day of incubation; from the left side; the diverticnlar arise from the anterior intestinal portal.
B. Beginning of the fourth day; from the left side.
a.z'.p. Anterior intestinal portal. D.V. Indicates position of ductus
vcnosus. g.b. Gall bladder. l.d.d'.(cr.). Dorsal or cranial liver diverticulum. l.d.v.(caud.). Ventral or caudal liver diverticulum. pad.
Dorsal pancreas. X. Marks the depression in the floor of the duodenum irom which the common bile duct is formed.
now also branch profusely, the branches spreading around the ductus
venosus and anastomosing freely with one another. At the same time
capillaries from the ductus venosiis begin to develop among the interstices of these anastomosing branches; this is the beginning of the main
body of the liver.
The Bile Ducts. ———- In the meantime, the intestinal portal has, of
course, moved backward beyond the point of origin of the diverticula.
This lengthens the gut and leaves these diverticula attached to its ventral side at their ‘points of origin. The parts of the diverticula between
the region of their anastomosis and the points of attachment to the gut
are at the nature of short tubes, the rudiments of the future bile ducts.
Presently the floor of the gut comprising the region where these ducts
enter it becomes depressed, and then drawn out so as to form a common
. , ,......l......>-yep "
THIRD DAY: THE HIND—GUT 375
duct into which the two original ducts empty. This common duct is
called the ductus choledochus, and is a temporary structure (Fig. 196).
The Gall Bladder. -—- While the above processes have been going on,
the gall bladder has arisen as a posterior evagination from the posterior
the gall bladder is drawn out to form the cystic bile duct.
All of these hepatic structures it should be noted are covered by the
splanchnic mesoderm of the ventral mesentery within which they have
developed. This rnesentery, here termed the gastro-hepatic ligament,
serves permanently to attach the whole mass to the gut and stomach.
The Panct'eas.——This organ first appears on the third day as a
thickening on the dorsal wall of the intestine within the dorsal mesontery about opposite the posterior liver diverticulum. The rudiment thus
indicated gives rise to only about a third of the entire organ whose further development will be described as it occurs (Fig. 196) .
THE MID—GUT
There is no great change in the mid-gut region during the third day
except that it becomes more clearly marked oil as the lateral folds continue to press in toward one another.
THE HIND—GUT
The Postanal Gut.——-It will be recalled that at the close of the
second day the ectoderm had taken so slight a part in the tail fold that
the anal plate retained a dorsal position. On the third day, however,
the fold becomes more marked, and soon takes on the character of a
posterior outgrowth, which is at first anterior to the anal plate. This
outgrowth is the tail bud. As its development progresses it becomes first
postero-dorsal, and then by turning downward postero-ventral, to the
anal plate, which itself becomes ventral instead of dorsal (Figs. 197.,
198). Also as a result of this process there is drawn out into the bud
an extension of the hind-gut, constituting a temporary structure known
as the postanal gut (Fig. 197).
The Allantois. -——The most important structure to appear in connection with the hind-gut during early embryonic life is the allantois.
The rudiment of this organ is usually indicated at about the beginning
of the third day. The method of its development and its final structure
have been described above (Figs. 190, 193) . In connection with the diagrams presented in Figure 198, however, a further word about its early
origin should be said. These diagrams represent the behavior of this re376 THE CHICK
gion as described in the text, and according to Gruenwald (°4«1). It must
he added, however, that in spite of the fact that there is apparent agreement regarding the movements which are taking place, Gruenwald puts
a somewhat different interpretation on them than do certain other an
s.A. Am. Am.cav. Ect. N'ch. n.1.
Fig. 197.-Sagittal section through the tail of an embryo of about 35 somites.
From Lillie (Development of the Clzic/:3.
All. Allantois. Am. Amnion. Am.cav. Amniotic cavity. An.pl. Anal plate. A0. Dorsal aorta. Bl.v. Blood-vessels in wall of allantois. c.C. Central canal of spinal cord.
Cl. Cloaca. Ect. Ectoderm. Ectam. Ectoderm of amnion. E.E.B.C. Exocoelom.
Mesrzm. Mesoderm of amnion. N’c}L. Notochord. n..T. Nerve cord. p’a.C. Post-anal
gut. p.i.p. Posterior intestinal portal. s.A. Segmental arteries, between the somites.
Spl’pl. Splanchnopleure and yolk-sac entoderm. T.B. Tail bud.
thors, e.g., Lillie and the present writer. Gruenwald, following an old interpretation presented by Duval in his atlas, chooses to regard the original “ hind-gut 7 as already “ allantois.” As can be seen from the
figures, it is true that a considerable portion of the original hind-gut is
eventually included in the allantoic outgrowth. It has also been shown
that the elimination of this region results in more or less complete elimination of this organ (Zwilling, ’46) . Nevertheless, it seems to the writer
confusing to identify this gut in its primary condition with the allantois,
THIRD DAY: THE HEART 377
involving as it= certainly does at that time the anal plate. It seems preferable to say that the allantois grows out from the part of this hind-gut
which, by the processes shown, eventually comes to lie anterior to the
anal plate.
an I plate
 
 
tall bud
anal plate
 
A
region of allantoic origln B
beginning of post anal gut
 
 
/Post anal gut
posterior Intestinal, portal——-“
can bud
beglnnlng of allantols
Fig. 198.——Diagrams representing changes in the tail and hind-gut region of the Chick during the third day. up to the 30 somite stage. After
Gruenwald with slight modifications. The successive stages are indicated
in the order of the letters.
THE CIRCULATORY SYSTEM
THE HEART
There are no very marked changes in the form of the heart during
the third day, though the atrium becomes slightly more prominent, and
the hendings and constrictions already described‘ are somewhat emphasized (Fig. 199). Internally toward the end of the (lay sections reveal
the appearance of a slight ingrowth from the atrial wall just to the left
of the sinus venosus. It is the beginning of the interatrial septum (Quiring, ’33) . In the ventricular region the myocardium is becoming thick378 THE CHICK
enecl and spongy, but in the bulbus arteriosus, on the other hand, endothelial thickening has occurred, while the myocardium remains thin
(Fig. 201).
THE EMBRYONIC BLOOD VESSELS
The Arteries. .
The Dorsal Aortae.—During the third day these vessels continue
their development by beginning to form posterior to the point at which
the vitelline arteries leave the body.
These latter arteries thus become
lateral branches of the dorsal
aortae, instead of their continuations, while the further posterior
growth of these aortae brings them
eventually to the extremity of the
tail bud. Meanwhile anteriorly
they have become fused, so that by
the end of the third day a single
aorta extends from just back of
the aortic arches almost to the origin of the vitelline arteries. Finally
during the fifth and sixth days the
fusion of these vessels progresses
Fig. 199.——Heart of 21 Chick embryo
of 72 hours, dissected out and drawn
from the dorsal surface. From Lillie
(Development of the Chick). _ _ , _
Aur.l. Left atrium. Aur.r. Right Into the tall region 3150, resulting
Elirggin-afii“-Igglgtiirgrfirlgfgéf in the formation of asinglé caudal
Ductus venosus. s.V. Sinus venosus. artery. It will not be necessary,
Tina. Truncus arteriosus. V.r. Right however, to trace these processes
limb of ventricle. , , _
of growth and fusion in detail.
The Aortic Arches.———During the third day each original carotid
loop plus the anterior part of each original ventral aorta disappears. At
the same time the part of each original ventral aorta which occupied
the ventral four-fifths of each mandibular arch becomes directly connected with its respective dorsal aorta through the upper fifth of each
of these arches (Fig. 200). In this way the actual first aortic arches are
completed.‘ However, before the end of the day the dorso-ventral con»
nections of these vessels in the mandibular arches have been broken,
1 This statement is based on figures from both Duval and Lillie. It should be
pointed out, however, that Lillie does not actually say that such a direct dorsal
connection occurs, and the writer has not been able. to verify the point at first
hand. If such a connection is established it is certainly for a very brief time, and
confirmation would require the study of closely graded embryos.
THIRD DAY: EMBRYONIC BLOOD VESSELS 379
‘~ :,'_/ L‘ h_' _— 3 I
s.2. V
i
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.7, /
7 {Ma .,
EXfl8E5':7Ial.fi.§‘£1V£'..:‘.1.‘
:§!"'!*"!’:.’.’.£%‘§‘,*.'£."‘e“‘\ \‘.
Fig. 200.—Chick embryo with adjacent portion of area vasculosa, with 35 pairs
of somites (about 72 hours). Dorsal view. From Lillie (Development of the Chick).
ma. 1, 2, 3, 4. First to fourth aortic arches. Am. Amnion. Ar. Branches of vitelline
arteries. Atr. Atrium (Auricle) . A.V. Vitelline artery. B./1. Bulbus arteriosns. cerv.
Fl. Cervical flexure. cr.F l. Cranial flexure. D.C. Ductus Cuvicri. D.V. Ductus venosus.
Ep. Epiphysis. Gn.V. Ganglion of V cranial nerve. Iszh. Isthmus. Jug. External jugular vein. Md. Mandibular arch. M.M. Maxillo-mandibular branch of V cranial
nerve. Myel. Myelencephalon. olf.P. Olfactory pit. Ophth. Ophthalmic branch of
V cranial nerve. 0t. Otocyst. 5.2, 5.10, 5.20, etc. Second, tenth, twentieth, etc., somites. V. Branches of the vitelline veins. V.c.p. Posterior cardinal vein. V.umb.
Umbilical vein. VJ’. Vitelline vein. V.V.p. Posterior vein. W.B. Wing-bud.
380 THE CHICK
and thus the first aortic arches vanish after a very brief existence. The
dorsal aortae in this region do not disappear, however, but extend anteriorly as the internal carotids. Ventrally the stump of each first aortic
arch persists, and presently produces an anteriorly growing twig which
becomes the primary external carotid. (See fifth day for final development.) Meanwhile a fourth aortic arch arises in each of the fourth visceral arches.
Chor. P_ c_ Lens p. Ch.
pl. gr. Am.
1
Fig. 201.—~Transverse section, passing tlirough the eyes and heart, of an embryo
with about 35 pairs of somites (about 72 hours). Compare with F ig. 200. From
Lillie (Development of the C/lick’) . V
Am. Amnion. A0. Dorsal aorta. Atr. Atrium. B.A. Bulbus artcriosus. cI'1..Fis. Choroid fissure. Chor. Chorion. D.C. Ductus Cuvieri. Dienc. Diencephalon. Lg. Rudiment of lung branches. P.C. Pericardial cavity. p.Ch. Posterior (vitreous) chamber.
pl.gr. Pleural groove. V.c. Posterior cardinal vein. Y.S. Yolk-sac.
The Pulmonary Arteries. — During the third ‘day, these arteries appear as rudiments within the walls of the lungs.
The Veins.
The Cardinals and Jugulars.——During the third day, the anterior
cardinals continue to branch considerably in the brain region and may
now be known as the internal jugulars. At the same time a vessel from
the floor of the pharynx joins each anterior cardinal (internal jugular)
just at its point of union with the duct of Cuvier. These new veins are
the external jugulars (Fig. 200). Late on the third day also a new pair
of cardinals begins to develop. They arise from a series of anastomosing
vessels on the ventral side of the mesonephros just lateral to the dorsal
aorta, and are known as the subcardinals. They are scarcely apparent
as definite vessels before the fourth day.
,
a
i
.
THIRD DAY: EMBRYONIC BLOOD VESSELS 381
The Vitelline Veins. —- Before leaving the body of the embryo, these
veins become united by a short transverse vessel which passes over the
intestine just posterior to the dorsal pancreatic rudiment. In this manner,
the intestine is surrounded by
a venous rinv. The anterior
ventral part of this ring is
formed by the posterior end
of the ductus venosus. The
lateral parts consist of the
portions of the vitelline veins
lying between the ductus venosus and the transverse vessel, and the posterior dorsal
part is constituted of the transverse vessel itself (Fig. 211,
A, B; see Chapter 12). Meanwhile, as indicated in the account of the liver, the portion
of -the ductus venosus which
lies within that organ is beginning to give of? capillaries
among the branches of the
liver diverticula.
The Untbilical Veins. —Early on the third day, a vein
develops in the body wall on
each side of the embryo, and
opens anteriorly into the respective duct of Cuvier. These
are the beginnings of the umbilical veins, although at this
Fig. 202.———Part of a transverse section
through the lateral mesocardia of a Chick
with 35 pairs of somites (about 72 hours).
From Kellicott
After Lillie.
a. Atrium. arm. Accessory mesentery. am.
Amnion. ac. Dorsal aorta. be. Bulbus arteriosus. ch. Chorion. cv. Posterior cardinal vein.
dC. Ductus Cuvieri. dm. Dorsal mesentery. 1.
Liver. lm. Lateral mesocardium. pc. Pericardial cavity. pe. Pulmoenteric recess. pg.
Pleural groove. 5. Stomach. sv. Sinus venosus.
um. Ventral mesentery.
(Chordate Development).
time they have no connection with the allantois (Fig. 203). Until such a
connection has been established the blood from this organ is conducted
to the lateral vitelline veins as follows: A transitory vessel, the subintestinal vein, develops upon the dorsal surface of the allantois, from
whence it proceeds up onto the ventral side of the gut, along which it
passes to the posterior intestinal portal. Here it divides into two parts
'which pass auteriorly around either side of the yolk-stalk to open into
the vitellines as these vessels run from the yolk-sac ‘along the margins of
the anterior intestinal portal to the ductus venosus.
382 THE CHICK
THE EXTRA—-EMBRYONIC BLOOD VESSELS
The Arteries.—The vitelline arteries reach further out into the
area vasculosa than during the second day, terminating near its border
in a network of capillaries which empty into the sinus terminalis.
Fig. 203.—Injected Chick embryo of the third day,
showing the arrangement of the cardinal veins and
the formation of the umbilical vein from capillary
networks. From Evans.
A.C. V. Anterior cardinal vein. P.C.V. Posterior cardinal vein. U.V. Umbilical vein.
The Veins.——Posterior to the point where the anterior vitelline
veins have fused, the right vein becomes greatly reduced. During this
period, also, the lateral vitelline veins passing backward and outward
along the margins of the anterior intestinal portal continue to form
from the vascular network lying close to either side of the embryo. In
this manner, they presently reach the region where the vitelline arteries
turn rather directly outward into the area vasculosa, and at this point
they also begin to pass outward just dorsal to the arteries. These veins
5
i
3
.
e
s
I
THIRD DAY: THE MESENCEPHALON 333
never extend all the we)’ t° the sinus terminalis, but branch widely in
the more central part of the vascular area. They receive blood from the
terminalis, however, through several intermediate veins (venous trunks),
which cross the outer network of arterial capillaries to reach them. Before the end of the third day, one other new extra-embryonic vessel
starts to appear, the posterior vitelline vein. At this time it is scarcely
more than a mass of capillaries, but very shortly begins to become distinct. It runs forward from the posterior side of the sinus terminalis,
and empties into the left lateral vitelline vein near its base (Fig. 182).
THE NERVOUS SYSTEM
THE FLEXURES
These have already been discussed under the description oi external
changes.
THE FORE—BRAIN OR PROSENCEPHALON
The Telencephalon. ——The indentation which marks the velum
transversum becomes much more prominent, while the rudiments of the
cerebral hemispheres grow in size and their walls increase in thickness.
In about the center of the lamina terminalis, a thickening appears called
the torus transversus. ltcorresponds to the similarly named structure in
the Frog, and as in that case it represents the rudiment of the future
anterior commissure.
The Di'encephalon.—The more anterior (ventral) portion of the
diencephalon is now sometimes distinguished as the parencepkalon, and
the posterior (dorsal) portion as the synencephalon (Fig. 204.-). Between them is a slight constriction, while the parencephalon is approximately boundcd below by the marked indentation of the velum transversum. Thus the roof of the parencephalic. region constitutes a
relatively raised area from which the epiphysis begins to develop at the
close of the day as a small out-pushing. Upon the floor of the diencephalon, the optic recess, the region of the optic chiasma, and the infundibulum all become more pronounced than they were at the end of
the second day.
THE MESENCEPHALON
The roof of the mid-brain grows rapidly and becomes prominently
arched, while its walls increase uniformly in thickness. This arching of
384 THE CHICK
the mid-brain causes the boundary between it and the roof of the diencephalon to appear gradually more constricted. Likewise posteriorly at
the connection between mid- and hind-brain, a slight constriction in the
roof and lateral walls, indicated during the second day, also becomes
very pronounced. This latter constricted region is henceforth known as
the isthmus.
Fig. 204. —— Optical longitudinal section of the head of an embryo of 30s. The heart
is represented entire. From Lillie (Development of the Chick).
Atr. Atrium. B.a. Bulbus arteriosus. D.v. Ductus venosus. Isth..Isthmus. Lg.
Laryngotracheal groove. Oes. Oesophagus. or.pI. Oral plate, which has begun to
rupture. Parenc. Parcncephalon. Ph. Pharynx. Stain. Stomach. Synenc. Synenceph
alon. Th. Thyroid. S.v. Sinus venosus. Ven.R. Right ventricle. Other abbreviations
as before.
THE RHOMBENCEPHALON
The Metencephalon. ——After the isthmus has become established
the thickening roof of the metencephalon consists largely of the wall
forming the posterior side of the constriction. By the end of the day, the
lateral walls of the metencephalon have also begun to thicken.
The Myelencephalon. —— The roof of the myelencephalon remains
thin, while its ventro-lateral walls have started to thicken somewhat.
The Spinal Cord. —— At the end of the second day, the wallsof the
spinal cord were seen to consist chiefly of ependymal supporting cells
and germinal cells. During the third day, the latter continue to multiply, and theirdescendants migrate out somewhat from their position
THIRD DAY: THE RHOMBENCEPHALON 385
near the central canal. In their new location, they presently become
transformed either into neuroblasts, i.e., primitive nerve cells, or into
primordial glia cells. The nerve cells even at this time have begun to
send out the axones and dendrites typical of the adult neurones. The
central parts of these neurones together 'with glia cells eventually come
to constitute the gray matter of the cord, while the axones form its
white matter.
Fig. 205. —Transverse section through the spinal cord
and ganglion of a Chick about the end of the third
day; prepared by the method of Golgi. From Lillie
(Development of the Chick). After Ramon y Cajal.
c. Cones of growth at the ends of growing nerve
fibers. Nbl. 1 and 2. Neuroblasts of the lateral wall.
Nbl. 3. Neuroblasts of the spinal ganglion. Nbl. 4.
Neuroblasts of the ventral horn (motor neurohlasts).
As regards the final condition of the cord, the following may be said:
Internally, the central canal is obliterated, save for a small ventral portion lined by the inner ciliated ends of the ependymai cells. Surrounding
this and filling the central part of the cord is the gray matter with
dorso-lateral and ventro-lateral extensions or horns reaching out into
the white substance. Externally, there develops along both the dorsal
and ventral sides a median longitudinal fissure. These fissures are
' formed mainly as a result of the enlargement of the lateral regions
through the accumulation of the nerve fibers within them.
The Spinal Nerves. -—The spinal nerves are sometimes described
as constituting parts of two systems, (1) the somatic, and (2) part of the
parasympathetic and the sympathetic; both systems start to develop on
the third day. We shall consider the somatic system. first.
I. The Somatic System. — From bipolar nerve cells within each
spinal ganglion one bundle of fibers (dorsal root) grows into the spinal
386 THE CHICK
cord, and another outward in a ventro-lateral direction. Together these
constitute the aflerent or sensory nerve fibers. At the same time from
the ventro-lateral side of the nerve cord beneath each spinal ganglion,
fibers (ventral root) are growing out from nerve cells located within
the cord. These are eflerent or motor fibers which mingle with those of
the respective outgrowing afferent bundle just at the point where the
latter leave their ganglion. The mixed fibers thus form the common
trunk of a somatic spinal nerve. This trunk then divides again into a
dorsal and ventral part, each part containing fibers of both the above
types. The condition thus indicated is approximately the stage reached
in the development of the somatic nerves at the end of the third day or
early on the fourth (Fig. 205; common trunk not shown).
Inasmuch as it will not be profitable in a work of this scope to follow
further the detailed development of the somatic spinal nerves from clay
to day, their future arrangement will be summed up at this time, as follows: The fibers of the divided trunks increase in number and at the
same time grow outward. Hence, they almost immediately come into
contact with the muscular and dermal plates, which are the rudiments
of the future voluntary musculature and dermis of the Chick. Thus nervous connections are early established with these elements, and as the
latter develop, the nerves (-motor and sensory) develop with them.
It should be noted that some of this musculature just indicated is destined for the limbs, and hence certain groups of the spinal nerves will
constitute the brachial and the sciatic plexuses. In this connection certain experimental results are of interest. Thus it has been shown that
when limb buds are transplanted to abnormal locations as described
above, spinal nerves nearby, which would normally have nothing to do
with limbs, are apparently “ attracted to them,” even forming a characteristic plexus before entering them (Hamburger, ’39). (However, see
conclusions of Detwiler and Piatt on this matter in the section on the
Frog). Hamburger (’39, ’44, ’49), Bueker (’45) and others have also
shown that the number of motor neurons in the cord may be respectively
decreased or increased by the extirpation of an adjacent limb bud or the
implantation of an extra one. Hamburger also showed that the variation
in number of motor neurons was apparently not caused by a difference
in the total number of cells, but rather by the differentiation of more or
less of this particular type of cell as compared with other types. These
results show the effect of developing limb buds on nerves. Lastly, however, Hunt (’32) and Eastlick (’4-3) have demonstrated that in transw_@afl >.
THIRD DAY: THE RHOMBENCEPHALON 387
planted limbs which for any reason fail to be innervated few muscle
fibers develop, and those that do, degenerate after about ten days. In
conclusion it thus appears that there are reciprocal influences between
a growing limb bud and its musculature on the one hand, and the devel.
opment of neurons and their fibers on the other.
11. The Sympathetic and Sacral Parasympathetic Systems. — As in the
Frog there has been much disagreement concerning certain details of the
origin of parts of these systems. For some time all postganglionic neurons at least were alleged to arise from neuroblasts in the dorsal root
ganglia, i.e., originally from the neural crests. Later Jones, ’37, ’39, ’4I
asserted that cells within the neural tube were the exclusive source for
these systems. Further experimental study by Hammond, ’49 and Yntema and Hammond, ’54 ’55 seem now to have resolved the problem as
follows: It appears that all postganglionic ne_urons and their fibers are
derived from the neural crest. All preganglionic fibers, both sacral
parasympathetic and thoraco-lumbar sympathetic arise from special aggregations of motor neurons within the spinal cord. The sheath cells of
all the fibers are from the crest and tube (Brizzee, ’49), and possibly
some mesoderm.
At the end of the third day or early on the fourth the postganglionic
cells derived from the crest collect just above and to either side of the
dorsal aorta. Here they send out fibers anteriorly and posteriorly, forming a pair of delicate longitudinal cords running from the cervical
region to the tail, with thickenings (ganglia) opposite each somatic
ganglion. These are the primary sympathetic and sacral parasympathetic
cords and ganglia, and each of these ganglia is connected with a somatic
ganglion by a strand of fibers, the primary rami communicantes. Lastly
there are a few cells in the dorsal mesentery, probably from the crest,
and destined to form Remak’s ganglion (Chap. 12, Fig. 216).
The Cranial Ganglia and Nerves.—-The ganglia of the V, VII,
VIII, IX and X nerves have already been described as appearing on the
second day. During the third day, the V ganglion shifts its position of
attachment to the brain somewhat, and its characteristic YM shape becomes more marked. The VII and VIII ganglionic mass also shifts to
a more dorsal position. Otherwise the cranial ganglia show no marked
alterations at this time (Fig. 200).
The Mixed Character of Certain Cranial Nerves.——In the Chick, as
in the Frog, it is possible to distinguish the V, VII, IX and X nerves as
mixed, i.e., as containing both sensory and motor elements. In this respect they are of course not different from the spinal nerves, except as
388 THE CHICK
regards the point at which the two types of fibers become mingled. Thus
in the region of the cord, the ventral or motor fibers of any nerve join
the dorsal or sensory fibers of that nerve slightly peripheral to the dorsal ganglion. In the mixed cranial nerves, on the other hand, the two
types of fibers issue from the brain very close together and mingle before entering the ganglion of the respective nerve. It may be further
noted that though the ganglion of the VIII nerve is very closely associated at this time with that of the VII, -its fibers are wholly sensory.
The III or Oculo-Motor Nerve. ——-Besides the mixed or wholly sensory nerves in the Chick, there are also, as in the Frog, certain cranial
nerves which are purely motor and without any connection with the
cranial ganglia. They take their origin from neuroblasts within the
brain itself, just as spinal motor fibers arise from neuroblasts within
the spinal cord. The III or oculo-motor nerve arises in this manner from
the median line of the ventral side of the mid-brain, at about sixty
hours. Its history will be traced a few steps further in connection with
the IV and VI nerves which arise on subsequent days.
THE ORGANS OF SPEClAL SENSE
THE EYE
The Optic Cup. -—— There are two main changes connected with the
optic cup during the third day. The first change is the rapid increase in
its size. Thus at the end of the second day the lens rudiment practically
filled the cavity of the cup, and came in contact with its inner wall. At
the end of seventy-two hours, on the other hand, the lens is entirely
separated from the wall of the cup, and simply rests within its rim.
The second change is the thickening of the inner wall, from whose
neuroblasts axones start to grow at the 30-somite stage (courtesy
Rogers, K. T.) . The optic stalk is still ventral at the point of attachment
to the cup, the region surrounding this point being called the fundus
(Fig. 201).
The Lens. ——The lens becomes detached from the superficial ectoderm during the third day, and forms a hollow ball, whose walls are
at flrst of almost uniform thickness. Presently, however, the cells of the
inner wall (i.e., the one next to the optic cup) begin to lengthen, in a
direction at right angles to this wall, so that the latter is thereby thickened. By the end of the day this thickening has progressed to a considerable extent, the elongated cells which cause it being destined to
form the lens fibers, which constitute the core of the lens.
THIRD DAY: THE EAR 339
THE EAR
At the end of the second day, the auditory pit had been transformed
into the auditory sac, whose mouth was still partly open to the exterior.
' By virtue of the method of the closure of the pit, described in the previ
ous chapter, the major part of the sac lies below the level of its external
Fig. 206.———Two stages in the development of the auditory organ of the Chick. From Kellicott (Chmrclare Development. A. Hemisected model of left auditory sac posterior
view, just before the separation from the head ectoderm,
at about 72 hours. After Krause. B. Median view of a
model of the left membranous labyrinth of an embryo of
7 days and 17 hours. After Riithig and Brugsch.
a. Anterior vertical semicircular canal. aa. Ampulla of
anterior vertical semicircular canal. up. Ampulla of posterior vertical semicircular canal. d. Ductus endolymphaticus. e. Superficial ectoderm of head. l. Lagena (cochlea). p. Rudiment of posterior vertical semicircular canal.
s. Rudiment of saccule. u. Utricle. 9:. Connection between
auditory. sac and superficial ectoderm.
orifice. The connection of this orifice with the dorsal portion of the sac
is then drawn out into a narrow tube, while the dorsal part of the sac
itself is at the same time slightly constricted away from the major ventral part. The former, or dorsal portion, is the rudiment of the endalymphatic duct, which presently ‘grows upward somewhat so that its
roof is slightly dorsal to the level at which the tube leading from it
opens to the exterior (Fig. 206, A).
THE OLFACTORY ORGANS
Early on the third day a small circular spot of ectoderm on each
ventrodateral side of the head somewhat in front of the eye becomes
thickened, in consequence of a lengthening of its cells. These patches
390 THE CHICK
Fig. 207.—Tlze development of the mesonephros. A.B. Transverse sections through the mesonephric tubules of the Duck embryo with 4-5 pairs of somites. From Kellicott (Chordate Development). After Schreiner. C. Transverse section through the middle
of the mesonephros of a Chick of 96 hours. From Lillie (Development of the Clzickt.
A0. Dorsal aorta. B. Rudiment of Bowman’s capsule. c. Conducting part of a primary tubule. coel. Coelom. Cal.T. Collecting tubule. cl. Dorsal outgrowth of the Wolfiian duct to form a collecting
tubule (see fourth day). Glam. Glomerulus. gcrm.Ep. Germinal
epithelium. M’s't. Mesentery. n.t. Nephrogenous tissue. rc. Rudiment of conducting portion of primary tubule. T. 1, 2, 3. Primary,
secondary, and tertiary mesonephric tubules. V.c.p. Posterior cardinal vein. W.D. Wolflian duct. '
then begin to invaginate, and thus form the olfactory pits (Fig. 200).
The thickened epithelium which lines them is the olfactory epithelium,
and is said to consist of two types of cells, simple epithelial cells and
germinal cells. The latter type later give rise to neuroblasts which eventually produce the sensory cells of the olfactory epithelium, while they
in turn give rise to axones which constitute the olfactory nerve. (See
next chapter.)
THIRD DAY: SUMMARY 391
THE URINOGENITAL SYSTEM
During the third day, the pronephros degenerates, while the mesonephros continues to develop, and soon becomes the primary excretory
organ during embryonic life in a manner about to be indicated. Neither
the metanephros nor the reproductive system appears during the third
day.
As regards the changes in the mesonephric region, it will be recalled
that at the end of the second day the Wolflian or mesonephric portion
of the pronephric duct was just beginning to acquire a lumen. Its backward-growmg end, however, was still solid, and had not yet reached
the cloaca. On the third day, this cellular rod connects with the cloaca,
and by the end of the day a lumen has formed throughout its length.
Concerning the mesonephros proper, at 4-8 hours the rudiments of the
mesonephric tubules were forming in the neighborhood of the twentieth
somite or segment, i.e., in the most anterior region of the future organ.
At that time, these rudiments, of which there were two or more to the
somite, consisted merely of spherical condensations of the nephrotome,
which were beginning to become vesicular. Now at the end of seventytwo hours, however, the vesicles opposite the most anterior mesonephric
somites are giving rise to small, hollow evaginafions in the direction of
the Wolfhan duct (Fig. 207, A). There is one evagination to each vesicle, and it is the part of the vesicle which is destined to form the actual
mesonephric tubule. Indeed, just anterior to the twentieth somite or
mesonephric region proper, some of the out-pushings have already become tubules and are connected through conducting portions with the
Wolflian duct (Fig. 207, B). In this region also Malpighian bodies have
appeared in connection with some of the tubules. These most anterior
tubules and glomeruli, however, never become functional.
SUMMARY OF THE CONDITION AT THE END OF THE
THIRD DAY OF INCUBATION
I. GENERAL APPEARANCE
The cranial and cervical flexures have increased, especially the latter. A small caudal flexure has appeared, and the region in between has
developed a slight ventral curvature. The lateral’ rotation has progressed
so that the embryo is on its side as far back as the twenty-first somite.
The four limb buds are clearly visible.
392 THE CHICK
II. THE SOMITES
The number of pairs of somites has increased to thirty-six and in the
more anterior pairs dermatomes and Inyotomes are completely developed. Sclerotomal tissue is still collecting about the notochord and the
sides of the nerve cord.
III. THE ALIMENTARY TRACT
The Fore-gut.-——The oral plate has broken through to complete
the oral cavity, and Rathke’s pocket reaches nearly to the infundibulum.
Subsequent development of these parts to form the pituitary is described
in this chapter. The second pair of visceral pouches has acquired clefts,
and the fourth pair has fused with the ectoderm. The thyroid depression
has become a sac. The depression indicating the respiratory system has
deepened in the laryngotracheal groove, and the rudiments of the
lungs have appeared. The esophagus and stomach are beginning to be
defined. Finally, the liver diverticula have grown forward and anastomosed about the posterior part of the ductus venosus; the rudiment
of the gall bladder is visible, and the dorsal portion of the pancreas has
appeared.
The Mid-gut. —— It has become more clearly defined.
The Hind-gut.~—The anal plate has been carried around to the
ventral side by the growth of the tail bud, and at the same time the
postanal gut has been formed. The rudiment of the allantois has appeared.
IV. THE CIRCULATORY SYSTEM
The Hea.rt.——There are no external changes aside from an emphasis of curvatures and constrictions already present. In the ventricular region myocardial thickening has occurred, and in the bulbus
arteriosus the same is true of the endothelium. The interatrial septum
has started to form.
Embryonic Arteries. —— Fusion of the aortae has progressed. The
first pair of aortic arches has been completed and then disappeared.
The dorsal aortae extend anteriorly as the internal carotids, while the
stumps of the first arches produce the external carotials. The fourth
pair of arches has developed, and the rudiments of the pulmonary
arteries have arisen in the lungs. '
Embryonic Veins. —— The anterior cardinals have branched considerably in the brain region and are now known as the internal jugulars
THIRD DAY: SUMMARY 393
which receive the external jugulars just at the union of the former with
the ducts of Cuvier. The ductus venosus is beginning to develop capillaries among the branching liver diverticula. A new vessel passes over
the intestine in the neighborhood of the pancreas and unites the vitelline veins to form a ring about the alimentary tract. A longitudinal vein
has developed in each body wall; they are the umbilical veins, though
at this time neither has acquired a connection with the allantois. The
rudiments of the subcardinal veins may be visible on the "ventral side
of the mesonephros. The transitory subintestinal vein is present.
Extra-embryonic Arteries.——The vitelline arteries have pushed
out into the area vasculosa until their branches nearly reach the sinus
terminalis.
Extra—embryonic Veins.~¥The right anterior oitelline vein has
almost disappeared; the posterior and intermediate vitelline veins have
started to arise, and the lateral vitelline veins have developed further.
V. THE NERVOUS SYSTEM
The Flexures and the Brain. —— As noted under external appear- '
ance the cranial and cervical flexures are both increased. The cerebral
hemispheres have grown somewhat, and the epiphysis has started to
develop. The optic chiasma, the optic recess. and the infundibulum
have all become more clearly marked. The roof of the mid-brain. is
more prominently arched and the isthmus has appeared. There has also
been thickening and thinning of the brain walls at various points.
The Spinal Cord and Spinal Nerves. ——The germinal cells have
changed their position and have begun to develop into neurones and
glia cells. The sensory and motor nerve fibers issue respectively from
the spinal ganglia and the ventral portion of the cord, the two types
uniting to form the common trunks of the somatic spinal nerves. The
primary sympathetic trunks, ganglia and communicating rami have appeared. The completion of the somatic portion of the spinal nervous
system is described in this chapter.
The Cranial Ganglia and Nerves.—-The ganglia have shifted
their position slightly, and the third or oculo-motor nerves have appeared.
VI. ORGANS OF SPECIAL SENSE
The Eye. —— The optic cup has increased in size and its inner wall
has thickened. The lens has become detached from the ectoderm, and
its inner wall is also thickening. 394 THE CHICK
The Eat. -——The rudiment of the endolymphatic duct has appeared
on the dorsal portion of the auditory sac.
The Olfactory 0rgans.~—The olfactory pits have been formed,
with walls consisting of epithelial and germinal cells. ’
VII. THE URINOGENITAL SYSTEM
The proneplzros has begun to degenerate, while the mesonephros has
started to develop tubules and glomeruli in its most anterior portion.
The Wolflian. duct has reached the cloaca and acquired a lumen throughout its length. °
VIII. THE AMNION AND ALLANTOIS
The folds of the amnion have approached one another above the posterior portion of the embryo and formed the amniotic umbilicus. The
allcmtois, by about the middle of the day, has the appearance of a
slight out-pushing from the hind-gut, and by the close of the day has
extended’ well into the somatic umbilicus.
12
HE CHICK: DEVELOPMENT DURING THE FOURTH
DAY OF INCUBATION
GENERAL APPEARANCE
FLEXURES AND TORSION
T H E cranial flexure remains about as on the previous day, but
the cervical flexure has increased so in degree and extent as to bring
the whole head further posterior. Also it brings the region of the dieti
1:. cephalon around so that it and the anterior part of the optic vesicles
face almost directly caudad. At the same time the mid-region of the
cervical flexure is now the most anterior part of the embryo. From the
anterior to the posterior limb buds the longitudinal axis has in most
cases lost its ventral curvature, and has become virtually straight. Caudad to the posterior limb bud the caudal flexure is more marked so that
the tip of the tail is curled around beneath the body. The lateral torsion
now extends throughout the whole embryo so that it lies entirely on its
side.
THE LIMB BUDS
All the limb buds have increased in prominence.
THE SOMITES
THE COMPLETION OF THEIR FORMATION
By the end of the fourth day the number of somites has reached 42,
and subsequent to this time ten more are added posteriorly. These last
ten, however, later disappear, together with the four most anterior ones
(head somites), which become fused with the skull. Thus at 96 hours
the Chick possesses all the somites which take any part in the development of the adult Bird. The development of the myotomal and derma
l tomal elements progresses posteriorly in the manner already described.
~ I». V
caud. Sci.
int's. F.
int'v. F.
caud. Sci.
X int's. F.
' ‘ Gn.
Derm.
ceph.ScL
snt{v§ 5.
My.
‘caud{ Sci.
4‘ im's. F.
perm. V
ceph. Sci.
My.
int'v. F, .
caud. Sci.
int’s.- F.
Derm.
«ceph. Sci.
. My_.
int'v. F.
caud. Sci.
int's. F.
ceph. sec.
Ep. M
Fig. 208. ——Frontal section through the base of the tail of a Chick embryo of 96 hours. The anterior end of the section (above in the figure)
is at a higher plane than the posterior end. From Lillie (Development
of the Chiclt).
caud.Scl. Caudal division of the sclerotome. ceph.Scl. Cephalic division of the sclerotome. Derm. Dermatome. Ep. Epidermis. Gn. Ganglion.
int’s.F. lntersomitic fissure. int’v.F. Intervertebral fissure. My. Myotome.
N’ch. Notochord. N.T. Neural tube. per’ch.Sh. Petichordal sheath. s.A.
Segmental artery.
THE CHICK
FOURTH DAY: THE SCLEROTOMES 397
THE ULTIMATE FATE OF MYOTOMES AND DERMATOMES
Although the ultimate disposition of these elements of the somites is
not accomplished until some time later, it is not desirable to follow
their development longer by one-day periods. Regarding the dermatomes, or cutis plates, it has already been stated that their substance
gradually moves out beneath the ectoderm, and ultimately forms the
dermis in the dorsal regions, the dermis in the more ventral parts being
derived from the underlying -somatopleure. Likewise Straus and Rawles,
’53 have now shown by carbon marking that the myotomes also are the
source of only about the upper one third of the voluntary body muscles
plus parts of three in the abdomen, the rest being somatopleural in origin.
Head musculature and involuntary muscles develop from mesenchyme.
THE SCLEROTOMES
During the third and fourth days the mesenchyme of the sclerotomes
comes to occupy all spaces about the notochord and between the latter
and the myotomes. Indeed, immediately around the notochord itself it
forms a thin continuous layer, the perichordal sheath. Further peripherally, however, a concentration of the mesenchyme in the cephalic and
caudal portion of each sclerotome, as well as a slight division between
these portions, has long made these parts distinguishable as such. Upon
the fourth day, moreover, it begins to appear that upon either side of I
the notochord the cephalic half of each sclerotome is beginning to become fused with the caudal half of the one anterior to it, thereby establishing a new segmental arrangement (Fig. 208). From the method of
their formation, it follows that the segments thus arising do not coincide with the myotomes; instead, they alternate with them just as they
did in the Frog. In this manner, blocks of mesenchyme are being
marked out on either side of the notochord; these are the rudiments of
the right and left halves of the future vertebrae. Lastly, from the cephalic and caudal portion of each sclerotome, mesenchymatous tissue
has new extended well upward around the sides of the nerve cord. This
forms the rudiments of the neural arches, the cephalic arch of one
sclerotome later fusing with the caudal. of the next to form single arches
corresponding to the vertebrae. The reason for the development of the
alternative arrangement between vertebrae and myotomes, i.e., muscles,
should be quite evident. In order to bend the back or neck it is apparent
that each set of muscles must be attached at each of its ends to a different vertebra.
398 THE CHICK
THE ALIMENTARY TRACT
THE REGION OF THE FORE—GUT
The Tongue. — The tongue appears on the fourth day as two papilliform outgrowths from the floor of the pharynx, one in front of and
one behind the thyroid. These two rudiments then grow forward and
fuse with one another. Eventually the structure thus constituted unites
with a pair of lateral folds to form the tongue of the adult.
The Visceral Pouches and Arches.
The Pouches.——During the fourth day, the third pair of pouches
acquire dorsal and ventral clefts like those of the second, while the
clefts of the latter pouches and of the first (hyomandibulars) become
closed. The second pouches then gradually disappear, whereas the dorsal portions of the first pair extend dorso-posteriorly toward the respective otocysts; here each eventually forms a part of the tubo-tympanic
cavity (see fifth day).
The Arches.—The five pairs of arches reach their maximum development as such during the fourth day, and certain changes in their
blood vessels take place; these changes will be described below.
The Thyroid.——The thyroid sac at this time completely separates
from the floor of the pharynx. Subsequently it becomes divided into
two massive lobes which move backward and take up'a position at the
junction of the subclavian and the common carotid arteries. The effect
of the pituitary upon the later development of this gland has been determined experimentally as follows:
Transplants have been made of thyroid glands from twelve-day old
Chicks to the chorio-allantoic membranes of Chicks with and without
pituitaries. It was found that only in Chicks possessing the pituitary
does either a transplanted thyroid‘ or that of the host develop beyond
the twelve-day stage (Martindale, ’4l).
The Respiratory Tract.——It will be recalled that at the end of
the third day, the posterior part of the pharynx had deepened and narrowed to form the laryngotracheal groove, with the lung primordia at
its posterior extremity. During the fourth day, the posterior portion of
this groove, including the lung diverticula, separates from the ventral
part of the alimentary tract. The anterior portion of the new tube thus
formed is the larynx which continues to open into the pharynx through
a slit-like aperture, the glottis. The remainder of the tube is the trachea,
FOURTH DAY: THE REGION OF THE FORE—_GUT 399
which divides into the lung primordia, really only the primary bronchi,
at its posterior end. This is the condition of the respiratory apparatus
at the end of 96 hours.
The Esophagus, the Stomach, and the Duodenum. —— At the end
of the third day, the fore-gut region posterior to the pharynx consisted of an elongated tube——the esophagus, a slight dilation——the
stomach, and finally another elongated region to which were attached
the rudiments of the liver and pancreas. This last section of the foregut may from now on be termed the duodenum. During the fourth day
the elongation of these parts continues, and also a certain curvature
becomes evident. This latter process extends from the posterior region
of the esophagus to the end of the duodenum, and the direction of the
bending is such that the convex side of the curve is toward the left.
The Liver.——It will be recalled that at the end of the third day
the main body of this organ had formed an anastornosing network
about the ductus venosus, and that it extended somewhat further forward on the left side than on the right. During the fourth day, this network increases, together with its interstitial blood vessels (Fig. 196, B).
As this enlargement proceeds, it will be found that the larger part of
the organ comes to lie more and more upon the right side of the body,
in the hollow made by the bend of the stomach.
The Pancreas. -——At the close of the third day, a thickening in the
dorsal wall of the intestine opposite the posterior liver diverticulum
was noted as the first rudiment of the pancreas. Upon the fourth day
this thickening becomes a solid outgrowth, somewhat hollowed at its
base. By the end of the day, two similar ventral rudiments may also
be visible as antero-lateral outgrowths from the common bile duct (the
ductus choledochus) . The subsequent union of these three elements will
be described in the following chapter.
The Spleen.--Although this organ is not really a part of the
digestive tract at all, it is convenient to describe its development at this
point. During the fourth day a proliferation of cells occurs in the
peritoneum at the base of the dorsal rnesentery just above" the dorsal
pancreatic element. These cells become mingled with the surrounding
mesenchymal tissue, thus forming the main substance of the spleen. Subsequent development results in the formation of a considerable mass,
filled with sinuses which communicate directly with the splenic veins.
Cells from the spleen are buddedyoff into these spaces and pass into the
circulation, where they apparently become transformed into blood corpuscles.
4.09 V THE CHICK
THE REGION OF THE MID—GUT
For purposes of definition, the fore-gut region may be said to terminate at the end of the duodenum, and this point is marked approximately by the opening of the bile duct. The mid~gut, therefore, is the
portion of the alimentary tract extending from the opening of this duct
to the point at which the gut contained in the tail fold begins. It is
difficult to define the latter point exactly at this time, except to say that
since the tail fold never becomes very deep, it is relatively near the
posterior end of the embryo, a short distance in front of the origin of
the allantois. This boundary between the mid- and hind-gut is marked
later by the intestinal caeca (see Chapter 13).
During the third and fourth days the folding-in process has been
going on rapidly in the region of the mid-gut, and due to this, and to
the growth of the entire body, the somatic umbilicus is so relatively constricted as to be called the umbilical stalk. Within it, as already noted,
are the allantoic stalk and the yolk-stalk. The former has always been
small, and the latter has necessarily shared in the constriction of the urnbilical walls. The result of these processes is obviously a mid-gut closed
in at every point save the relatively narrow opening into the yolk-stalk;
it is also a gut which still remains virtually straight. The section of
alimentary tract which has thus been defined is destined to become the
small intestine of the adult bird.
In concluding the discussion of this topic it is well for the student
to realize that there are two aspects to the umbilical constrictions just
indicated. There is, on the one hand, the absolute narrowing of the
umbilical opening. There is also in addition to this the immense growth
of the remainder of the embryo. The girth of the umbilicus is thus a
relative as well as an absolute matter, and the apparent reduction in its
size is due as much or more to the increase in size of the embryo as to
its own constriction.
THE REGION OF THE HIND—GUT
The remainder of the digestive tract posterior to the small intestine
is, by the above definition, the hind-gut, and constitutes the large intestine or rectum. This opens into a terminal chamber, the cloaca. There
is little to be said about the development of the rectum at this time,
since it remains short, uncoiled, and without appendages.
The cloaca at 96 hours consists of a chamber into whose anterodorsal wall there opens, as indicated, the rectum. Just back of the rectal
FOURTH DAY: THE HEART 401
orifice, the cloacal cavity also receives the Wolfiian ducts. Antero-ventrally below the rectal opening is the aperture of the allantois, while just
behind this on the ventral side of the chamber is the original anal plate,
or cloacal membrane (Fig. 193). It consists, as will be recalled, of a
fused plate of endoderm and ectoderm, and during embryonic life separates the cavity of the cloaca from the exterior. Posterior to these
apertures and the cloacal membrane, the cloacal chamber shows a
marked lateral compression.
THE CIRCULATORY SYSTEM
THE HEART
In order to understand the development of the heart during the
fourth and subsequent days, it will be necessary for the reader to refer
to the description of that organ at the end of the second day. Assuming
that this description is clearly in mind, we may then continue the account of the development on the fourth day, as follows:
Changes in the Proportion of the Parts. --The entire loop has
gradually been expanding so that its parts have tended to approach
one another. This has also resulted in a relative shortening of the two
ascending limbs, i.e., the posterior limb comprising the atrium and part
of the ventricle, and the anterior limb comprising another part of the
ventricle and the bulbus arteriosus. At the same time so great has been
the expansion of the transverse portion of the loop connecting these
two limbs that the limbs as such have almost disappeared. What remains of the posterior one is marked by what amounts to a constriction
just below the developing atrium. This apparent constriction, however,
is brought about not so much by an actual contracting of this region
as by the relative expansion of the parts above and below it. Since the‘
part above forms the atrium, and the part below is a portion of the
ventricle, the constriction between constitutes the atria-ventricular canal.
Changes in the Relative Position of the Parts.——At the same
time that these changes in shape and proportion have been occurring,
changes in the relative positions of the parts are also progressing. Of
these there are three principal ones which may be indicated thus:
(1) The bulbus arteriosus is swinging toward the median line beneath
the atrium (Fig. 209, D). (2) The ventricular region is moving backward behind the atrium and also somewhat toward the median line, the
region of the future apex pointing posteriorly. (3) To some degree as
402
THE CHICK
Fi . 209. —- The development of the heart of the Chick. From Kellicott
(C ordaze Development). A, F, after Hochstetter. B—E, after Greil.
A—E, ventral views of the heart. A. of a 40-hour embryo; B. of an embryo of 2.1 mm. head-length; C. of an embryo of 3.0 mm. head-length;
D. of an embryo of 5.0 mm. head-length; E. of an embryo of 6.5 mm.
head-length. F. Frontal section through the heart of an embryo of 9 mm.
head-length.
a. Atrium. b. Bulbus. d. Roots of dorsal aorta. e. Median endothelial
cushion (i.e., the cushion septum}. i. Interventricular groove. la. Left
atrium. le. Lateral endothelial cushion. to. Left ventricle. om. Vitelline
veins. p. Left pulmonary artery. ra. Right atrium. rv. Right ventricle. 5.
Intfrrventricular septum. sa. Interatrial septum. t. Roots of aortic arches.
entnc e.
E
1
»
FOURTH DAY: EMBRYONIC BLOOD VESSELS 403
a part of the latter movement, the posterior portion of the atrium into
which the sinus venosus opens is rotating forward. In this manner, it is
brought just over and then anterior to the atrio-ventricular canal, the
latter remaining at a comparatively fixed point between the ventricular
and atrial regions. Though not completed during the fourth day, these
movements are well under way at this time. Their progress, moreover,
is suflicient to show that their tendency is to place the parts of the heart
more nearly in their adult positions; i.e., the atrium anterior and dorsal,
and the ventricle posterior and ventral.
Interior Changes Involving the Growth of Septa.——Whi1e the
above external alterations in the form of the heart have been going on,
further internal changes are occurring as follows: (1) the interatrial
septum which started to form on the third day becomes more clearly
evident as, a sickle shaped membrane extending postero-ventrally from
the curved antero-dorsal wall, the back of the sickle being attached to
the wall. Eventually of course this septum, augmented by certain other
elements, completely divides the atrium into right and left chambers
(the atria). (2) At the apex of the ventricle, the interventricular septum
arises, and grows forward. Now since the ventricular apex has be</ome
posterior to both the atrio-ventricular canal and the bulbus arteriosus,
it is possible for the forward extension of this septum to meet them
both. This, it eventually does ( see Chapter 13). (3) At the same time
these septa are developing, a third one is beginning to arise within the
atrio-ventricular canal; it starts as two endothelial thickenings, one in
the floor, and the other in the roof of this canal. These are destined to
grow towards one another until they unite in the center of the atrioventricular aperture, thus dividing it into right and left parts. When
completed, this partition isknown as the cushion sept‘-tun (Fig. 209, F ) .
EMBRYONIC BLOOD VESSELS
The Arteries.
The Aortic Arches.-—— It will be recalled that during the third day,
the first pair of aortic arches disappeared, leaving the anterior extensions of the dorsal aortae as the internal carotids. In a similar manner,
extensions from the bases of the first arches continue anteriorly as the
external carotids. Upon the fourth day, the second aortic arches are
likewise obliterated, and the two pairs of oarotids continue posteriorly
to the dorsal and ventral ends of the third pair of arches. At the same
time two new pairs of aortic blood vessels develop in the vestigial fifth
visceral arches behind the fourth and last pair of visceral pouches.
£3
5
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404 THE CHICK
These are the fifth and sixth aortic arches (Fig. 210, A). The fifth pair
is small and quite transitory, being actually attached both dorsally and
ventrally to the anterior sides of the sixth pair. Shortly after the sixth
arches have thus arisen a small branch develops from about the middle
of each and connects with the rudiments of the pulmonary arteries
growing out from the lungs. In this manner the pulmonary arterial sysstem is completed, though throughout embryonic life the branches just
indicated remain small.
LEFT SIDE RIGHT SIDE
4} day 8 day
ductus Batallt subclavian artery
   
 
internal carotid
 
dorsal aorta
artery '  ‘ __:  carotid artery
h ‘ ' ';. 3 3rd aortic arch
5th BOFUC arches I ' j: 4th (systemic)
vitelline artery mm‘ arch
I ’d pulmonary artery th aortic arch
externa caroti
ITIGTY runcus arterlosus
A B
cruncus urtertosus '
Fig. 210.—Aortic arches of the Chick. Left side from a 45-day injected embryo.
Modified from Lillie, after Locy. Right side reconstructed from saggital sections of
an 8-day embryo. Modified from Lillie.
From this description, it is clear that only the ventral portions of the
sixth arches take part in the formation of the pulmonary arteries. The
dorsal portion of each arch, on the other hand, is known as the duct of
Botallo or ductus arteriosus, which, as will be noted below, atrophies
at the time of hatchinv.
The Subclavian Arteries. ——- As noted under the description of external features the primordia of the anterior and posterior limb buds appear by the end of the day as broad swellings on the sides of the body.
Correlated with this we find that on the fourth day the eighteenth segmental artery on each side gives rise to a branch which extends out toward the respective bud. It is the primary subclavian artery. From it,
at the point where it enters the limb, a branch also extends anteriorly
toward the third aortic arch. This is destined to form the permanent
subclavian (see fifth day).
The Sciatic Arteries.-—-Posteriorly, a pair of segmental arteries also
enlarge and grow out toward the hind limb buds. These vessels become
Fig. 211.——Diagrarns illustrating the formation of the
omphalomesenteric and umbilical veins, in the Chick, ventral view. From Kellicott (Chordate Development). Alter
Hochstetter. A. At about 58 hours. B. At about 65 hours
the veins are joined dorsal to the gut by a short transverse
vessel. C. At about 75 hours the anterior intestinal portal
has moved posteriorly somewhat so that the transverse vessel appears to be more anterior. At the same time, the left
side of the loop, which its development created. has disappeared. D. At 80 hours a second loop has been formed by
the fusion of the vitellineveins beneath the gut. E. At
about one hundred hours the right side of this new loop
has also disappeared. F. At about 130 hours, just before
the disappearance of the main portion of the ductus venosus within the liver. This figure is obviously on a much
smaller scale than E. A
c. Vena cava posterior (inferior). dC. Ductus Cuvieri.
dv. Ductus venosus. g. Gut. hl. Left hepatic vein. hr. Right
hepatic vein. 2. Liver. a. Omphalomesenteric or vitelline
vein (the posterior continuation of the ductus venmsus).
p. Anterior intestinal portal. pa. Rudiment of pancreas. ul.
Left umbilical vein. ur. Right umbilical vein. 1;. Vilelline
vein. I, II. Primary and secondary venous rings around
the gut.
406 THE CHICK
the sciatic arteries, and as the legs develop they grow with and supply
them.
The Umbilical Arteries. — During the fourth day, each sciatic artery
gives off at its base a branch which extends into the allantois. These are
the umbilical or allantoic arteries. Later {eighth day), the right member of this pair starts to disappear, while the left becomes a very important embryonic vessel, furnishing blood to the allantois. Indeed, so
large does it become that the left sciatic seems for a time to be merely
a branch from it.
The Renal Arteries and Those of the Conads. -—-Numerous branches
from the dorsal aorta supply the mesonephros at this time, and later on
a few of these persist as the renal arteries. Branches from the aorta also
supply the reproductive organs as these develop.
The Veins. _
The Vitelline Veirzs. —- It will be recalled that at the close of the third
day, the vitelline veins within the embryo had been united by a transverse vessel dorsal to the intestine, so that the latter was surrounded by
a venous ring. Between this time and the close of the fourth day, ‘inither changes have taken place in this region, as follows: Very shortly
after the transverse vessel has been formed the left side of the above
ring disappears (Fig: 211, C ). Later, as the anterior intestinal portal
moves backward, the vitelline veins between the poltal and the transverse vessel fuse with one another beneath the intestine. In this manner, a venous ring is again formed around the posterior extremity of
the fore-gut, and in this case the right side presently begins to grow
smaller. Anterior to the vitelline veins the ductus venosus continues to
receive capillaries from the surrounding liver (Flo: 211, D).
The Cardinal Veins. -— The anterior cardinals, as indicated -in the
previous chapter, have, by this time, reached a stage when they may be
known as jugulars, while the posterior cardinals continue as previously
described. The subcardinals which started to form on the third day become distinct vessels and presently acquire several direct connections
with the posterior cardinals lying on the dorso-lateral sides of the
mesonephros (Fig. 212).
The Inferior or Posterior Vena Cam. -~— This important vessel of the
adult Bird begins to develop at this time out of some of the capillaries
in the dorsal part of the liver on the right side. Slightly further back
it is also augmented by venous islands in a fold (the caval fold) of one
of the liver mesenteries. These capillaries and venous islands soon fuse
Fig. 212. -— Reconstruction of the venous system of a Chick, 90 hours, ventral view.
From Lillie (Development of the Chick). After Miller.
A.o.m. Omphalomesenteric. (vitelline) artery. a.sc.s. Left sciatic artery. A.u.s.
Left umbilical artery. 6. Vessels enclosed within ventral side of mesonephros c.
One of the direct connections of subcardinal with posterior cardinal. V.c.p.d.,s.
Right and left posterior cardinal veins. V.c.i. Venn cava inferior. V ..sc.d.,s. Right
and left subcardinal veins.
407
408 THE CHICK
together so as to form a definite vein which empties anteriorly into the
ductus venosus (Fig. 211, E), and posteriorly establishes a connection
with the right subcardinal (Fig. 212). Its subsequent development will
be described in the following chapter.
The Umbilical Veins. ——— Upon the fourth day, the veins of the lateral
body wall acquire connections with efferent vessels which have developed in the allantois, and at the same time, the right vein begins to disappear, along with the transitory subintestinal vein. The left vein on the
other hand persists, but presently loses its anterior outlet into the ductus
Cuvieri. At the same time, however, it develops new connections with
the anterior half of the ductus venosus (Fig. 211, D, E). Through these,
therefore, blood from the allantois flows quite directly into the latter
vessel, without taking any extensive part in the hepatic portal circulation. Later, these connections with the ductus venosus/fuse into one,
which thus constitutes _the anterior extremity of the single umbilical vein
(Fig. 211, F). Eventually this vein acquires a median position in the
embryo instead of its original lateral one. Subsequent to hatching, its
proximal portion persists as a vein of the ventral body wall.
The Pulmonary V eins.—-These vessels also develop at about this
period in connection with the rudiments of the lungs, and presently become connected with the heart in the region of its left atrium.
EXTRA-—EMBRYONIC BLOOD VESSELS
The Arteries.——-During the fourth day the proximal portions of
the vitelline arteries become fused with one another so as to leave the
dorsal aorta as a single vessel. This fusion, however, occurs for only a
relatively short distance, and never passes beyond the end of the umbilical stalk. From that point, the two main vessels continue to run out
laterally, branching as they go, and terminatingin a network of capillaries just inside the sinus terminalis. Subsequent development does
not fundamentally alter the arterial plan except that as the septa of the
splanchnopleure develop in the yolk-sac, the arterial capillaries come
to occupy the deeper portions of these septa.
The Veins.-—By the end of this "day the right anterior vitelline
vein has disappeared, while the left anterior vitelline vein and the
posterior vein, are well developed. The lateral vitelline veins have also
become larger and more definite at the point where they extend outward in company with the arteries. Furtherout in the area vasculosa,
they continue to branch extensively, the branches connecting with the
intermediate veins as already noted. By this time, however, these conFOURTH DAY: THE PROSENCEPHALON 409
motions are so pronounced that the intermediate vessels appear merely
as the finer endings of the lateral vitellines, uniting these veins with the
sinus terminalis (Fig. 182). Subsequent to the tenth day, the anterior
and posterior vitelline veins are gradually eliminated, the lateral veins
persisting as the main efferent vessels of the yolk-sac. After the tenth
day, the sinus terminalis is no longer distinct, becoming obliterated by
a mass of capillaries. These capillaries and the vessels with which they
are connected, forming the area vasculosa, then continue to spread over
the yolk in company with the yolk»sac mesoderm. Thus, like the latter,
they come at last virtually to surround it.
THE NERVOUS SYSTEM
This system, like the others, continues to develop through embryonic life. The differences observed in it between the fourth and fifth
days, however, are not, in most respects, very great. Therefore, since it
is not proposed to carry a detailed chronological description of any of
the organs beyond the fifth day, we shall conclude the account of the
nervous system in the present chapter.
THE FLEXURES
The cranial and cervical flexures of the brain and nervous system
have already been noted in the account of external changes through the
fourth day. As has been indicated in the general discussion of this matter, only one of the flexures just named, i.e., the cranial, is permanent,
the cervical gradually straightening out until it is entirely gone. Also,
though to a smaller extent than in the Frog, even the cranial flexure is
partly obscured in the adult brain by the development of the cerebral
hemispheres and other parts. There is now to be noted a third flexure,
which though barely visible on the fourth day, later becomes quite
marked. It, like the cranial, is permanent and also like the cranial is
never entirely obscured. This is the pontine flexure which consists of a
ventral bulge in the thickened floor of the myelencephalon (Fig. 214) .
THE PROSENCEPHALON
The Te1encepha1on.——-The cerebral hemispheres continue to increase in size during the fourth day, and their lateral walls in particular, are thickening to form the corpora striata, The other features already noted as characteristic of this portion of the brain have also
increased in prominence. As regards subsequent development the cere410 THE CHICK
bral hemispheres ultimately become one of the most noticeable portions
of the brain, their backward growth causing them to overlap, and to
conceal partially the large optic lobes. Their surface, however, never
attains the complicated convolutions so characteristic of the Mammal.
Anteriorly, beginning about the eighth day, small portions of these hem
Fig. 213.—-Optical longitudinal section of the head of an embryo of 395. From
Lillie (Development of the Chick).
Atr. Atrium. 8.1:. Bulbus arteriosus. D.v. Ductus venosus. Lg. Laryngotracheal
groove. Es. Oesophagus. or.pl. Oral plate, which has now ruptured; Parenc. Parencephalon. Plz. Pharynx. Slam. Stomach. Synenc. Synencephalon. Th. Thyroid. 5.12.
Sinus vcnosus. V en. Ventricle. Other abbreviations as before.
ispheres become partially constricted away from the main posterior
parts to form the olfactory lobes.
Concerning other parts of the telencephalon, as already indicated, the
anterior commissure appears in the midst of the torus transversus. On
the fifth day, also, an evagination develops at the antero-dorsal boundary of the lamina terminalis just between it and the velum transversum;
it is the paraphysis. This structure virtually marks the boundary between the telencephalon and diencephalon, Lillie placing it in the former. and some anatomists in the latter. Above this body occurs the inward bend of the wall which constitutes the velum transversum, whose
more dorsal half at least, according to most authorities, lies definitely
in the diencephalon.
FOURTH DAY: THE PROSENCEPHALON 411
i e
- Hyp. pant. Ft.
Com. ant. Rec. op.‘
<
' Fig. 214.—~Dissection of the brain of an 8-day Chick. From Lillie { Development
of the Chick). The arrows shown in the figure lie near the dorsal and ventral
boundaries of the foramen of Monro.
ch.Pl. Choroid plexus (anterior). Com.ant. Anterior commissurc Com.I’ost. Posterior commissure. C.str. Corpus striatum. Ep. Epiphysis. H. Hemisphere. Hyp.
Hypophysis (anterior stomodaeal, part). L.t. Lamina terminalis. Myel. Myelencephalon. olf. Olfactory nerve. ap.N. Optic chiasma. op.L. Optic lobe. Par. Paraphysis.
Ptzren. Parencephalon. pl.enc.v. Plica encephali ventralis. pon.t.Fl. Pontine flexure.
Recap. Recessus opticus. S.Inf. Saccus infundihuli. Tel.med. Telencephalon medium. Th. Thalamus. T.tr. Torus transversus. Tr. Commissura trochlearis.
hThe lines a-a, b-b, c-c, d-d, e-e, f-f, represent the planes of sections not figured in
t is text.
The wall of this portion of the fore-brain, therefore, gives rise to the
anterior comrnissure and the cerebral hemispheres. Its cavity forms the
anterior part of the third ventricle into which the lateral ventricles of
the hemispheres open through the foramina of Monro.
The Diencepha1on.~——The anterior part of the roof in this region
of the brain, as noted, apparently consists of the dorsal half of the
velum transversum which later becomes folded to form the anterior
choroid plexus. Eventually this plexus develops anterior branches extending forward into the lateral ventricles of the cerebral hemispheres.
Posterior to the plexus the epiphysis shows no great change on the
fourth day. Later, however, it grows out into a long narrow tube, whose
412 THE CHICK
end is dilated and possessed of numerous buds, the epiphysial or pineal
gland. Just posterior to this organ at the boundary between the fore- and
mid-brains, the posterior commissure eventually develops within the
broad constriction which has marked this point from the first.
During the fourth day no striking development occurs in the lateral
Fig. 215.——Median sagittal section through the brain of the Chick of 12_to 13
days. From Kupiier (He-rtwig's Handbuch; etc.).
c. Cerebellum. ca. Anterior commissure. cd. Notochord. ch. Habenular commissure. ci. Infundibular commissure. ck. Central canal of spinal cord. cp. Posterior
commissure. cpa. Anterior pallial commissure. cs. Spinal commissure. cu. Cavum
cerebelli. cw. Optic chiasma. dr. Epiphysial (Pineal) gland. dt. Decussation of the
trochlear (IV) nerve. e. Epiphysis. ex. Paraphysis. hm. Cerebral hemisphere. hy.
Hypophysis (anterior part). 1'. Infundibulum. le. Ependymal lamina of the roof of
the fourth ventricle. lo. Olfactory lobe. 1p. Posterior lobe of cerebral hemisphere.
M. Mesencephalon. opt. Optic chiasma. pch. Choroid plexus third ventricle. pl.
Choroid plexus of fourth ventricle. re. Epiphysial recess. ro. Optic recess. 5. Saccus
infundibuli. si. Posterior intracephalic furrow. tp. _Tuberculum posterius. lpi.
Tuberculum mammillare. tr. Torus transversus. wz. Velum medullare anterius. vi.
Median ventricle of telencephalon. up. Velum medullare posterius.
or ventral region of the diencephalon. Subsequently, however, the former region becomes greatly thickened to form the thalami. On the ventral side, the fate of the infundibulum has already been described (see
discussion of fore-gut, third day) while the optic chiasma comes to comprise a thick bundle of fibers from the optic nerves.
The floor of this posterior division of the fore-brain thus gives rise to
the optic stalks, the optic chiasma and the infundibulum, while the optic thalami develop within the lateral walls. The roof forms the anterior
choroid plexus and the epiphysis; the cavity constitutes the posterior
part of the third ventricle. C
FOURTH DAY: SPINAL CORD AND NERVES 413
THE MESENCEPHALON
There is nothing in particular to be said concerning the development
of this region on the fourth day. Later we find that the growth and thickening of the dorso—lateral parts of the mid-brain greatly exceed that of
a narrow dorso-median strip, thus producing the two large optic lobes,
which the median strip separates_ from one another by a fissure. Ventro.
laterally, the sides and floor of the mid-brain also become thickened,
constituting the crura cerebri. This thickening finally results in narrowing the central canal to form the aqueduct of Sylvius or iter, which con.
nects the cavities of the third and fourth ventricles.
THE RHOMBENCEPHALON
The Metencephalon. ~ The thickening which was noted in the roof
of this region on the third day continues to increase, resulting finally in
the production of a large median lobe, and two small lateral lobes
united with it. The body thus formed extends backward somewhat so
that it partially overhangs the myelencephalon. It is the cerebellum.
About the ninth day, transverse fissures appear on the surface of this organ, which deepen as development proceeds. The ventro-lateral walls of
the metencephal on, which have also been thickening, come eventually to
form the pans Varolii.
The Myelencephalon. —— It has already been stated that the roof
of this region of the brain remains thin; it eventually forms the choroid
plexus of the fourth ventricle. The ventral and ventro—latcral walls, however, showed signs of thickening on the third day. This tendency increases, and these walls finally constitute the medulla oblongata.
THE SPINAL CORD AND SPINAL NERVES
The description of the development. of the cord and of the somatic spinal nerves was completed in Chapter 11. The completion of the sympathetic. and parasympathetic systems, i.e., the autonomic, will now be noted.
The Sympathetic and Sacral Parasympathetic Systems.———It
will be recalled that at the end of the third day the primary sympathetic
and sacral parasympathetic systems had just been established. They consisted of two slender cords and their ganglia lying just dorso-lateral to
the dorsal aorta, and extending from the region of the vagus ganglion to
the tail. On the fourth and fifth days neuroblasts migrate from each
ganglion of the primary systems to positions above the primary cords
just median to where each somatic trunk divides (Fig. 216) . Each such
414 THE CHICK
aggregation of neuroblasts, or ganglion, forms neurons which again send
axones anteriorly and posteriorly to form the paravertebral or permanent sympathetic and sacral parasympathetic cords. For a time both
primary and secondary cords exist to some degree, but eventually the
primary cord is mostly eliminated. It
is generally thought that neuroblasts
from the ganglia ‘of the permanent
cords also migrate to the mesentery
and viscera to form the visceral plexuses, but, save for the sacral ganglia,
Yntema, ’55 denies this, and claims
that in the Chick at least, all these
visceral plexus neuroblasts are from
the vagus crest (see below). Though
unorthodox this view is supported by
extensive investigations.
It should be emphasized at this
point that all the neurons so far de
Fig. Z16.-—Diagram of the chief
elements of the sympathetic nervous system of the Chick, in trans
verse section: From Kellicott
(Chordate Development). After
His, Jr.
a. Dorsal aorta. op. Aortic plexus. J. Dorsal (afiercnt) root of spinal nerve. g. Spinal ganglion. i.
Intestine. m. Me-sentery. n. Notochord. R. Remak’s ganglion. s.
Splanchnic plexus. sg Sympathetic
elements in intestinal wall. 1!.
Mesonephric tubules. v. Ventral
(efferent) root of spinal nerve. I.
Primary sympatheticcord. 11. Secondary sympathetic cord. The rami
communicantes are only partially
scribed as originating from the neural
crests, constitute only the postganglionic elements of the systems under discussion. The preganglionic neurons on
the other hand are all derived from
neuroblasts in the neural tube. These
cells at first occupy the ventro-lateral
parts of the tube along with the somatic motor neurons. From here the
sympathetic and sacral parasympathetic neuroblasts separate from the somatic neuroblasts, and migrate dor
5l‘°‘””° sally taking up positions on either
nuclei of Term’. From these, cell fibers
grow out through the ventral somatic nerve roots to the points‘ where
these roots join their respective dorsal roots. The preganglionic sympathetic and sacral parasympathetic fibers then leave the somatic roots
and through short connections, the secondary or permanent rami commurzicantes, enter the ganglia of the permanent sympathetic and sacral
parasympathetic cords. Either in these ganglia (sympathetic) or in the
ganglia of the visceral plexuses (parasympathetic) they synapse with
the postganglionic fibers of these plexuses. '
side of the neural canal in the
FOURTH DAY: SPINAL com) AND NERVES 415
It should now be noted that all the nerves and fibers of the autonomic
system, i.e., the sympathetic and sacral parasympathetic already dis.
cussed, and the cranial parasympathetic described below, are strictly
motor. Nevertheless there are sensory fibers which convey sensations
from the viscera. These arise from neurons in the cranial and spinal
ganglia where all sensory neurons outside the nose, eye, and ear are
located. They leave the dorsal roots through the rami communicantes
and accompany the motor fibers of the autonomic system to the viscera,
though not part of that system.
The Cranial Ganglia, Mixed Nerves, and Cranial Parasyrnpathetics. Trigeminal Ganglion and Nerve.—-—It has been stated that
this ganglion has the form of an inverted Y. On the fourth day fibers
from the anterodorsal branch, i.e., the ophthalmic, pass anteriorly along
the dorsomedian wall of the optic vesicle. Eventually these ophthalmic
fibers, mostly sensory, reach the face and beak. The other branch of the
Y extends toward the angle of the mouth, where it also divides, one part,
the mandibular, is a mixed nerve, and supplies the lower jaw. The other
all sensory branch, the maxillary, supplies the upper jaw. As usual all
sensory fibers arise from neurons in the ganglion, while the motor fibers
are from neurons in the brain.
T he Acustico-facialis Ganglion and Nerves.-—As indicated above,
the ganglion which gives rise to the VII and VIII nerves is at first in a
single mass. During the fourth day, however, the antero-ventral portion
separates from the remainder, and gives rise to a nerve which extends
chiefly along the hyoid arch, though possessing also a small branch to
the mandibular. This is the rudiment of the future VII or facial nerve
with :1 motor component from the medulla. The remainder of the ganglion gives rise to the VIII or auditory nerve which is purely sensory,
and which communicates with the inner ear as described below.
The Glossopharyngeal Ganglion and Nerve. —-The origin of the IX
cranial ganglion was noted in the account of the second day, where it
was indicated as lying above the third arch. The IX nerve appears on
the fourth day and extends into this arch. Later another branch enters
the second arch, and together they eventually supply the tongue and
pharyngeal region. ,
The V agus and Cranial Parasympathetic S'ystem..——Neuroblasts in
the crest and an adjacent placode above the third branchial pouch, together with neuroblasts within the brain, produce the vagus complex as
follows: Upon‘ the fourth day the crest part of the X ganglion separates
from the placodal portion, and eventually produces the ganglion jagu~
416 THE CHICK
lare, the placodal part producing the ganglion nodosum. The exact
origin of all the neural elements of the X nerve complex in the Chick is
still uncertain, but the situation seems to be thus: Neuroblasts of the
ganglion jugulare produce the somatic sensory neurons, the somatic
motor neurons arising from within the medulla. The crest produces all
postganglionic neurons of the cranial parasympathetic system (Yntema
and Hammond, ’55) except possibly those of the ciliary ganglion, said
by Levi-Montalcini and Amprino, ’47, to be derived from mesenchyme;
the preganglionic neurons of this system arise within the medulla. From
the ganglion nodosum nerves pass into the fourth and fifth neural arches
and posteriorly to the heart, lungs, stomach, and intestine, while the
ganglion moves back into the thorax. Eventually a part of the nodosum
is detached as the ganglion cervical primum.
THE CRANIAL MOTOR NERVES
The Mo’cor—ocu1ar or III Nerve. — The early development of this
cranial motor nerve has already been described. During the fourth day,
it passes down beneath the optic stalk, and there enters a ganglion. This
receives a connection from the ophthalmic branch of the V nerve, and
is known as the ciliary ganglion. The III nerve ends by innervating the
superior, inferior, and internal rectus, and the inferior oblique muscles
of the eye when these develop.
The IV or Trochlearis Nerve.———This motor nerve does not appear until the fifth or sixth day, but will be described at this point. It is
peculiar as a motor nerve, in that it arises from the dorsal side of the
brain, at the bottom of the isthmus. It has no connection with any ganglion, and ultimately innervates the superior oblique eye muscles.
The VI or Abducent Nerve. —— This is a perfectly typical motor
nerve, appearing toward the end of the fourth day. It has no ganglion,
and arises from the ventral side of the medulla median to the point of
origin of the fifth nerve. It innervates the external rectus muscle of
the eye.
The XI or Spinal Accessory Nerve. ——There is no data on the
development of this nerve in the Chick (Lillie).
The XII or Hypoglossus Nerve. — This nerve develops during the
fourth day from two pairs of ventral roots on the medulla at the level
of the third and fourth somites. There are no ganglia, and the roots are
evidently serially homologous with the ventral roots of the spinal nerves.
The nerve to which they give rise eventually innervates the floor of the
pharynx. '
FOURTH DAY: THE EYE 417
THE ORGANS OF SPECIAL SENSE
THE EYE
At the end of the third day the inner wall of the optic cup had thickened, and the whole cup was in the process of enlarging. The lens, meanwhile, had separated from the external ectoderm, and the side of the
lens toward the cup had also begun to thicken. The further development
of the eye may be described as follows:
Parts Connected with the Optic Cup.—-During the fourth day,
pigment begins to appear in the wall of the optic cup nearest the brain,
i.e., its outer wall. At the same time, there is developing upon the innermost surface of the inner wall, the internal limiting membrane. Beneath
this membrane, but still toward the inner side of the inner wall, as noted
on the second day, neuroblasts near the fundus have sent out axones.
These have passed over the retinal elements just beneath the limiting
membrane, and have reached the optic stalk through the proximal part
of the choroid fissure. Here they proceed among cells of the ventral wall
of the stalk, and late on the fourth or early on the fifth day, reach the
brain and form the optic chiasma. Later many more-fibers grow through
the ventral part of the optic stalk, causing it to swell so that the original internal cavity is obliterated. It may then be termed the II or
optic nerve. In this connection it may further be noted that during the
fifth and sixth days the processes of growth occur in such a manner as
to alter the relative position of the point of attachment of the optic stalk
to the cup. The result is that at the completion of these processes the
point in question is no longer at the ventral edge of the cup, but approximately at its center, opposite to the lens.
Subsequent to the fourth day, other changes are also occurring in the
walls of the optic cup. As the various cell layers of the retina are formed
in the inner wall, this wall shows difierentiation into two zones. The
central and larger of these, which includes the fundus, is called the
retinal zone, i.e., the retina proper, and it is only within this zone that
the above retinal elements are developed. The remainder of the inner
wall consists merely of a band around the rim of the cup, and is known
as the lenticular zone. The line of separation between the two is known
as the cm serrata (Fig. 217). Within the retinal zone, the outer wall
forms the pigmented layer of the retina,'but never completely fuses
with it. In the lenticular zone, on the contrary, fusion between inner and
outer walls is complete, pigment penetrates them both, and both remain
418 THE CHICK
ant. ch. ‘ '
corn.
iris
Fig. 217. ——Frontal section of the eye of an eight-day Chick. From Lillie (Development of the Chick).
ant.ch. Anterior chamber of the eye. ch. Choroid coat. cil. Ciliary processes.
Corn. Cornea. l.e.l. Lower eyelid. n.m. Nictitating membrane. olf. Olfactory sac.
op.n.- Optic nerve. as. Ora serrate. p. Pigment layer of the optic cup. post.ch.. Posterior (vitreous) chamher oi the eye. ret. Retina. scl. Sclerotlc coat. scl.C. Sclerotic
cartilage. u.e.l. Upper eyelid‘
relatively thin. From this zone, in connection with certain mesenchymal
elements, are differentiated the iris and the ciliary processes. While these
parts are forming, the cavity of the optic cup is being filled with a gelatinous matrix containing fibers. Both elements are probably derived
from certain cells of the retinal and lenticular zones, and together are
known as the vitreous humor. Certain of the fibers of the humor are con
»
l
8
i
FOURTH DAY: THE EYE 419
nected with the ciliary processes, and help to support the lens. Finally,
the outside of the cup is gradually covered by two layers of mesenchymal origin. The inner is the choroid coat, and the outer the sclerotic
coat, the latter being partly cartilaginous.
The Pecten. -—This body is_also developed in connection with the
optic cup and choroid fissure, but is entirely peculiar to the Birds. It
Fig. 218. — Diagrammatic reconstruction of the pecten of the eye
of (Chick embryo of 71: days’ incubation. From Lillie (Development of the Chick). After Bernd.
Ch.fis.l. Lip of the choroid fissure. Ch./iss. Choroid fissure. Mes.
Mesenchyme. Mes.b. Upper edge of the rpesenchymal ridge covered by the lips of the choroid fissure. Mes.K. Thickening of the
edge of the mesenchyrnal ridge. op.C. Optic cup. 0.St. Optic stalk.
P. Pecten. P.B. Base of the pecten.
The arrow indicates the direction of growth of the lips of the
choroid fissure over the mesenchymal ridge. The line d shows the
plane of the section reproduced in Fig. 219.
has seemed well, therefore, to emphasize it by a separate description.
It arises during the fourth day in the form of a blood vessel embedded
in mesenchyme. This mesenchymal mass is in the shape of a ridge which
enters the cavity of the cup through the choroid fissure near its proximal
end. The distal end of the fissure between this mesenchyme and the rim
of the cup has, meanwhile, been closed. On subsequent days, the mesenchymal ridge pushes up into the cavity, while at the same time it is
being gradually covered over by the in-turning and up-growth of the
edges of the choroid fissure on either side of it. This covering soon becomes more prominent than the relatively thin ridge of mcsenchyme
420 THE CHICK
   
which it has overgrown, and presently (eighth day) the two parts he.
come indistinguishable. Though remaining constricted at its base, the
ridge of fused tissues inside the cavity of the cup continues to grow
somewhat, and later becomes folded, assuming the appearance of a fan,
though in most Birds it is more comb-like, and hence is named the
pecten. It is very vascular and probably helps to nourish the retina. The E
opening in the choroid fissure between pecten and optic stalk provides ‘
Fig. 219.-S£-ction in the plane of (1. of Fig. 218.
to show the histological structure. From Lillie (Development of the Chick). After Bernd. Bl.v. Blood
vessel in mesenchymal ridge. il. Retinal layer of op~
tic cup. Other abbreviations as in Fig. 218.
the exit for the optic nerve fibers from the retina. A few of these fibers
runrdirectly to this point, but the majority come to the base of the pecten,
and run along its sides to the place of exit (Figs. 218 and 219).
The Lens. — At the end of the third day, the inner wall of the lens
vesicle had thickened considerably by virtue of the lengthening of its
cells. This process continues for several days until the cavity of the vesicle is entirely obliterated. Moreover, inasmuch as the lengthening of
the central cells is greater than that of those at the periphery, the inner
surface of the lens becomes distinctly convex (Fio. 217). These lengthened cells of the inner wall form the core of the future lens, while the
cells of the outer layer toward the ectoderm form a simple flat epithelium. The lens now grows, largely by the production of cells at its equa- ‘V
tor where the inner and outer walls meet. These cells become fiber-like
. x
FOURTH DAY: THE EAR 4.21
and wrap themselves around the original elements which form the core,
thus increasing the size of the lens by the addition of concentric layers
of cells.
The Cornea, the Anterior Chamber, and the Lids. ——The
cornea at first consists merely of the external ectoderm opposite the
lens. On the fourth day, however, this layer is augmented internally by
a thin non-cellular layer of mesenchymal origin. On the fifth day, this
thickens slightly, and begins to be covered on the side toward the lens
by a third layer formed of mesenchymal cells. Later, the middle layer
becomes cellular by the migration into it of cells from the mesenchyme,
while the third and innermost layer forms a typical epithelium. The latter finally becomes continuous at its edges with the cells of the sclerotic
coat. The cornea thus constituted arches outward slightly, and thus a
chamber is formed between its inner layer and the front of the lens. This
is the anterior chamber, and it becomes filled with the aqueous humor.
The lids begin to develop about the seventh day as folds of the integument surrounding the cornea (Fig. 217).
THE EAR
The Internal Ear.—-At the end of the third day, the otocyst, or
future internal ear, was in the form of a sac. The uppermost portion of
the sac had been slightly constricted away from the lower major portion, and had started to grow upward somewhat as the rudiment of the
endolymphatic duct. This upper portion, furthermore, still retained its
narrow tubular connection with the exterior (Fig. 206). There is, in
these parts, no marked change characteristic of the fourth day. Upon the
fifth day, however, the connection of the endolymphatic duct with the
exterior is entirely lost. Moreover, the opening of the duct’ into the sac
is being gradually shifted ventrally along the median side of the latter.
At the same time, the dorsal part of the duct is continuing to grow upward, and expanding to form the means endolymphaticus. Eventually,
this becomes embedded in mesenchyme above the hind-brain.
While these events are taking place in connection with the formation
of the endolymphatic duct the remaining major portion of the otocyst is
developing further, as follows: Upon the early part of the fifth day,
there arises from its dorsal half a vertically elongated, hollow out-pushing in the direction of the ectoderm. Then a horizontal out-pushing appears just beneath the first, and therefore at about the equator of the
otocyst. Presently a vertical split develops in the ventral part of the
vertical out-pushing and soon extends dorsally, thus dividing it into an
..q,,,,,,.,/,,.,,a...,..~.,«._.. was 1—,.,~.«— <,..,..«
422 THE CHICK
anterior and a posterior ridge. The anterior, posterior, and horizontal
ridges which have thus arisen are the rudiments of the respective semicircular canals. These canals eventually develop by a gradual constricting away of the hollow ridges, so that they become separated from the
   
Fig. 220.——Model of the auditory labyrinth of the
the right side of a Chick embryo of 8 days and 17
hours; external view. From Lillie (Development of
the Chick). After Riithig and Brugsch.
A.zz. Ampulla of the anterior vertical semicircular
canal. A.l. Ampulla of the lateral horizontal semicircular canal. A.p. Ampulla of the posterior vertical
semicircular canal. C.a. Anterior vertical semicircular canal. C.l. Lateral horizontal semicircular canal.
C.p. Posterior vertical semicircular canal. D.c. Ductus cochlearis. D.e. Endolymphatic duct. La. Lagena.
Sa.c. Endolymphatic sac. U. Utriculus (utricle).
otocyst everywhere except at their ends. During this process a dilation
occurs" on each canal to form its ampulla. The remainder of the dorsal
portion of the otocyst into which the canals open is the utricle.
Meanwhile, most of the ventral part of the otocyst has grown downward and also turned backward and toward the median line of the head.
_,Itsi end forms the lagena, and the portion connecting this with the utricle ‘is the ductus cochlearis or cochlear duct. The sacculus arises about
the seventh day as a pouch on the median side of the uppermost portion
FOURTH DAY: ORGANS or SPECIAL SENSE 423
of the ventral part of the otocyst, i.e., just above the point where the latter receives the ductus cochlearis (Fig. 206, B).
The parts of the inner ear thus "far described constitute the membranous labyrinth (Fig. 220). The walls of this labyrinth are composed
of epithelium, and its cavity is soon filled with the endolymphatic fluid.
Except for small areas within the ampullae and at certain other points,
the above epithelium becomes flat. At these points, however, elongated
sensory cells end in hairs which project into the fluid, and among these
cells grow the endings of nerve fibers (axones) coming from the VIII
cranial ganglion.
On ‘the sixth day, the mesenchyme which immediately surrounds the
developing labyrinth begins to form a membrane (membrana propria)
in close contact with it. At the same time the more peripheral mesenchyme is forming a cartilaginous case, separated slightly from the labyrinth and its membrane, but following all its contours. The space between the two is called the perilymphatic space. It is bridged by tissue
which carries the nerves and blood vessels, and is filled by the perilymphatic fluid derived from loose mesenchyme tissue left within the
space. The cartilaginous case later becomes ossified, and is known as
the bony labyrinth. In it, on the side toward the middle ear, are two
small openings, the fenestra ovalis, and the fenestra rotunda.
The Middle Ear, or Tubo-tympanic Cavity. — As was stated in
connection with the alimentary tract, the first visceral clefts are closed
during the fourth day, and the ventral portion of the pouch of each disappears. The dorsal portion, however, grows up toward the respective
otocyst, and during the fifth and sixth days comes between it and the external epithelium. Each pouch then starts to enlarge, and the space
within it is the dorso-lateral portion of one of the two tuba-tympanic
cavities. Meanwhile," beginning on the fourth day, the ventro-median
portion of each cavity is developed, as follows. In the antero-dorsal region of the pharynx, a horizontal shelf has grown backward, so as to
produce a dorsal chamber virtually separate from the space beneath.
Laterally, the part of each tubo-tympanic cavity already developed
opens into this newly constituted dorso-median chamber. Then, as
growth proceeds, an increasing portion of this chamber becomes drawn
out into the respective cavities. Thus eventually the larger part of each
middle ear space is really developed in this manner, rather than directly from the original “ gill” pouch. When these processes axrgeorri-1 .’~.
plete the median part of the dorso-median chamber still $hains‘“as‘* *'
such. while its lateral parts constitute the Eustachian tubes e({ have a \‘f‘_
V S Q Alhlnbcd ) O
‘ O
4- K
“'r\""'/I lg‘
424 THE CHICK
common opening into the mouth by a single median slit-like aperture in
the horizontal shelf. With regard to the cavities themselves two other
points remain to be noted. First as in the case of the Frog, each tubotympanic cavity contains a bone, the columella. Its development can
best be described, however, in connection with the tympanum. Secondly
there is the peculiar relation which exists between the tubo-tympanic
cavities and certain of the other bones of the Bird’s skull. These bones
like bones in other parts of the Bird skeleton to be described later contain spaces which give lightness to the body. The case of the head bones
is noteworthy at this point, however, because in some of them the spaces
are formed and filled by outgrowths from the tubo-tympanic cavities
(Bremer, ’40). v
The External Auditory Meatus and the Tympanum. —-It will
be recalled that the temporary external opening of the first visceral
pouch occurs only at its dorsal end. Ventrally, however, there is a fusion
with the ectoderm which causes the latter to form a vertically elongated
pit. When the dorsal perforation closes, that point also is marked by a
pit. These pits presently disappear, and on the sixth day the point between them becomes marked by a new depression, the beginning of the
external auditory meatus. It gradually deepens until, except for a thin
layer of mesenchyme, the external ectoderm is in contact with the endoderm of the tympanic cavity. These thin layers of ectoderm, mesenchyme, and endoderm which thus separate the middle ear from the outside, constitute the tympanum or ear drum.
To the inside of the tympanum of an adult Bird is attached one end
of the columella. The other end is in contact with a membrane covering
the fenestra ovalis of the bony labyrinth, i.e., the bony case which finally surrounds the membranous labyrinth. The columella is, therefore,
like a bridge stretching across the tympanic cavity from the tympanum
to the inner ear. It is chiefly developed from mesenchyme which lies in
the dorsal wall of the enlarged tubo-tympanic portion of the gill pouch.
This mesenchymal rudiment, it may be noted, is thought to be derived
from the dorsal end of the second or hyoid arch. However that may be,
as the cavity increases in size, it extends upward on each side of the
above mesenchyrne until it has surrounded it except at its inner and
outer ends. Then as this mesenchyme becomes cartilaginous and finally
ossifies, it forms a bone (the columella), occupying the position already
described‘. Lastly, it should be added that the inner end of this bone in
contact with the membrane of the fenestra ovalis seems to arise, at least
in some_Birds, from an element (the stapes) which, though at first disFOURTH DAY: ORGANS or SPECIAL SENSE 425
Fig. 221.—Sagittal section through the head of a Chick embryo of 5 days, showing the floor of fore~brain, olfactory pit, and developing olfactory nerve between.
From Lillie (Development of the Chick). After Disse.
a. Unipolar neuroblasts near the olfactory epithelium. b. Bipolar cell in the olfactory nerve. c. Unipolar cell near the brain. F.B. Floor of fore-brain. N'bl. Neuro
blast in the olfactory epithelium. olf.Ep. Olfactory epithelium. alf.N. Olfactory
nerve. olf.P. Cavity of olfactory pit.
tinct, eventually fuses with the columella. This stapedial element in the
Bird would thus apparently correspond to the opercular element in the
ear of the Frog.‘
The Olfactory Organs.———lt will be recalled that, at the close of
the third day, the olfactory epithelium consisted of two types of cells:
1 Some writers recognize a third element, the stylohyal, which enters into the
formation of the columella of Birds. It must be stated. however. that the exact
origins, as well as the homologies of the bones of the middle ear in the various
groups of Vertebrates are not yet completely known.
426 THE CHICK
simple epithelial cells and germinal cells. It had also become depressed
to form the olfactory pits. During the fourth day this process of depres.
sion continues to a considerable extent, and thus the specialized olfactory epithelium lying at the bottom of the pits is carried in some dis.
tance from the surface. The epithelium forming the sides of the pits, on
the other hand, is unmodified and similar to that outside. The position
of the pits has also shifted somewhat with the growing of the head, so
that their months now lie just on the antero-lateral border of the oral
cavity.
At the same time that these processes are taking place, the germinal
cells referred to are transformed into neuroblasts, and the latter in turn
into typical neurones. On the external side, these neurones send short
processes to the surface of the olfactory epithelium. On the other side,
they produce axones which extend in toward the brain, the region of
whose future olfactory lobes they do not enter, however, until about the
sixth day. Along the course of these axones are a few bipolar neurones
and also numerous epithelial cells, the latter serving as supporting and
sheath cells for the fibers. Both types are said to migrate from the olfactory epithelium, to their final position during the growth of the axones. The axones, together with the other cells just indicated, constitute
the I cranial nerve (Fig. 221). _
On the fifth and succeeding days, the nasal cavities continue to
deepen somewhat, and become greatly modified in shape. This is partly
the result of the appearance of certain folds in the nasal wall; these
folds are the rudiments of the three nasal turbinals, only two of which
are finally covered by epithelium of the olfactory type.
While the internal development of the olfactory organ is thus progressing, certain external changes are also going on in connection with
the apertures. However, since these changes have more to do with the
development of the face than with that of the olfactory organs proper,
they will be discussed under the heading of general external changes in
Chapter 13.
THE URINOGENITAL SYSTEM
THE EXCRETORY SYSTEM
The Mesonephros.——At the end of the third dayithe pronephros
had virtually disappeared, while the typical mesonephros was beginning
to develop, posterior to the twentieth somite. During the fourth day, the
FOURTH DAY: THE REPRODUCTIVE SYSTEM 427
primary me5°“ePh1"iC tubules are developed from the most ventral vesicles thro11gh°ut_the greater part of the mesonephric region. The remaining vesicles which occur in every mesonephric segment are, moreover,
each giVi1'1g rise '50 a tubule. Thus besides the primary tubules, there are
formed eventually secondary and tertiary tubules and sometimes even
more, all of a similar nature, developing from the nephrotomal mass opposite each somite. As suggested in the previous chapter, the primary
tubules thus formed soon connect directly, through a non-secretory or
conducting portion, with the Wolflian duct. The others as they develop
empty into outgrowths from that duct, which receive the name of collecting tubules (Fig. 207).
At the time that these tubules are developing, the remaining portion
of each vesicle is forming a Malpighian body or corpuscle consisting of
a glomerulus and its capsule. These Malpighian corpuscles are similar
in essential respects to those found in the Frog, and need not be described further. Though its development is still incomplete, the mesonephros apparently starts to function as a kidney at this time (Boyden,
’24). In this connection it is of interest to note that in the Bird a few of
the more cephalic rnesonephric tubules also establish rudimentary nephrostomal relations with the coelom in the manner characteristic of all
these tubules in the Frog.
The Metanephros.—The rudiment of the ureter and collecting
tubules of the metanephros, or permanent kidney of the Chick appears
at the end of the fourth day as a diverticulum from the mesonephric
duct. It arises from the dorsal side of this duct just at the point where
the latter bends to enter the cloaca. During the fourth day, also, the
nephrotomal tissue, just posterior to the thirtieth somite or end of the
mesonephros, begins to degenerate for a short distance (see Chapter
13, Fig. 240). Thus anterior to this point, the mesonephros, and any
undifferentiated nephrogenous tissue overlying it, become entirely cut
off from the nephrotomal tissue posterior to this region. The latter tissue thus cut oi? accompanies the forward growth of the ureter and its
collecting tubules, and is destined to form the secreting portion of the
entire metanephros (see Chapter 13, Fig. 240).
THE REPRODUCTIVE SYSTEM
The Gonads.-—-The rudiments of the two gonads appear on the
fourth day as thickenings of the peritoneal epithelium on each side of
the dorsal mesentery, between it and the respective mesonephros. These
thickenings occur just posterior to the origin of the vitelline arteries
428 THE CHICK
and extend for seven or eight somites, i.e., through the posterior half or
third of the mesonephric region. Presently primordial germ cells appear
in this epithelial tissue, near to which they have been transported from
the anterior part of the germ wall, where they are said to be distinguishable as early as the primitive streak stage. According to the remarkable
observations of Swift (714) and Goldsmith (’28) they are conveyed to
their new location by the blood stream. No sex differentiation is apparent at this time.
The Gonoducts.——The future male gonoducts or vasa cleferentia
are the mesonephric ducts whose development has already been described.
‘The oviducts or Mzillerian ducts begin their development at this time
in both sexes in the form of two ridges, the tubal ridges. Each ridge is a
strip of thickened peritoneum which appears on the fourth day. It lies
on the dorso-lateral face of each mesonephros next to the body wall and
near to the Woliiian duct. It is first found at about the level of the twen
tieth somite; from this point it differentiates posteriorly (see Chapter
13, Fig. 246)
THE ADRENALS
These bodies, though not really a part of the renal system, are closely
connected with it, and their development may, therefore, best be described at this point.
As in the Frog, the adrenal organs are composed partly of cells de-,
rived from the peritoneum, and partly of cells from the sympathetic
nervous system. The former element, known as the cortical substance,
arises from the coelomic epithelium slightly anterior to the germinal
region, and proliferations of this substance presently penetrate the
mesenchyme between the Wolfiian body and the dorsal aorta. The element derived from the sympathetic nervous system (mainly the primary
sympathetic system) is known as the medullary substance, which comes
into contact with the cortical material by the end of the fourth day
(Willier, ’30).
SUMMARY OF THE CONDITION AT THE END OF THE
FOURTH DAY OF INCUBATION
I. GENERAL APPEARANCE
The cervical flexure has increased so that its mid-region is anterior
and the diencephalon faces posteriorly. The caudal flexure has also in
a..;..ys.u.e_.»....m.=»..-,..a»
FOURTH DAY: SUMMARY 429
creased, and the embryo between it and the end of the cervical flexure is
virtually straight. The entire embryo is on its side, and the limb buds
have increased in prominence.
II. THE SOMITES
The number of pairs of somites has increased to forty-two, including
all those which take part in the formation of adult structures, while the
myotomal, dermatomal, and sclerotonzal elements have been developed
in each pair. The last named element forms a nearly complete sheath
about the nerve cord and notochord, and shows slight indications of the
vertebral segments. The account of the further developnfint of the my
otomal and dermatornal elements is completed in this chapter.
III. THE ALIMENTARY TRACT
The Fore-gut. ——The rudiments of the tongue have appeared. The
first and second visceral clefts have closed, and the third opened; the
visceral arches reach their maximum development as such. The thyroid
has completely separated from the floor of the pharynx. Subsequent development of the tongue and thyroid are indicated in this chapter.
The posterior end of the laryngotracheal groove and the lung rudiments have separated from the alimentary tract.
The esophagus, the stomach, and the duodenum have increased in
length, and the two latter parts of the tract have developed a curve to
the left. The liver has increased in size and come to lie somewhat in the
curve of the stomach. The dorsal pancreatic rudiment has become a
solid outgrowth and a pair of ventral pancreatic rudiments have arisen
from the ductus choledochus. The spleen (not really a part of the alimentary tract) has started to develop.
The Mid-gut. —-—The mid-gut or region of the small intestine is now
a virtually straight tube open to the yolk only by the relatively con’
stricted aperture of the yolk-stalls.
The Hind—gut.—The anterior portion of the hind-gut constitutes
the rectum, while its terminal portion becomes the cloaca. The latter is
still separated from the exterior by the cloacal membrane, and its posterior part is laterally compressed.
IV. THE CIRCULATORY SYSTEM
The Heart. — The ventricular region, especially the transverse portion, has expanded and moved posteriorly. The bulbus arteriosus has
swung toward the median line, and the atrium has rotated forward. The
interventricular, the interatrial, and the cushion septa are developing.
430 THE CHICK
The Embryonic Arteries.———The second aortic arches have dis.
appeared, and the fifth and sixth pairs have developed. From the latter
have arisen the roots of the pulmonary arteries which grow out and connect with the rudiments coming from the lungs. The primary subclavian,
the rudiment of the permanent subclavian and the sciatic arteries have
appeared, while the last named have given rise to the umbilical or allantoic arteries. The history of the sciatic and allantoic vessels is concluded in this chapter.
The Embryonic Veins.——The ring about the alimentary tract,
which is formed in connection with the vitelline veins, has been broken
by the disappearance of its left half. A fusion of the above vessels has
occurred beneath the fore-gut, forming a second ring. The capillaries of
the ductus venosus among the branches of the liver diverticula are becoming more numerous. Posteriorly, on the ventral side of the mesonephros, the rudiments of the subcardinals have become distinct vessels
and have acquired direct connections with the posterior cardinals. The
inferior vena cava has begun to form in the liver and caval fold, and
posteriorly has connected with the right subcardinal. The longitudinal
vein in the right body wall is disappearing, along with the transitory
subirztestina.-l vein, and the left, having acquired a connection with the
allantoic vessels, has become the functional umbilical vein. The account of its development is completed. The pulmonary veins appear in
connection with the developing lungs.
The Extra-Embryonic Arteries. —The vitelline arteries have
‘ fused with one another for a short distance as they leave the aorta. Their
branches in the area vasculosa continue to develop in company with the
growth of that region, but are without features requiring further note.
The Extra-Embryonic Veins. -—The right anterior vitelline vein
has disappeared, but the left anterior, posterior, and lateral veins are
well developed. Subsequent development of the extra-embryonic veins is
included in this chapter.
V. THE NERVOUS SYSTEM
The Brain.——The cranial and cervical flexures have increased
slightly; the porztine fiexure may be in evidence. The cerebral hemispheres have increased in size, and their lateral walls are thicker. The
optic lobes are also becoming steadily more prominent. There are no
other marked changes evident at this time.
The Spinal Cord and Spinal Nerves.—-There is no special development on the fourth day.
FOURTH DAY: SUMMARY 431
The Cranial Ganglia and Mixed Nerves.—From the V nerve
ganglion a branch (ophthalmic) has extended toward the future beak
and another (mandibular) toward the angle of the mouth. The VII
nerve ganglion has become separated from the VIII, and has given rise
to the hyoial and mandibular branches. The IX ganglion has sent a nerve
into the third arch. The X ganglion has divided into the ganglion jugulare and ganglion nodosum, and the latter is giving rise to the vagus
nerve.
The Cranial Motor Nerves. —~ The III nerve has entered the ciliary
ganglion, and the VI nerve has just appeared. The XII nerve has also
begun to develop.
VI. THE ORGANS OF SPECIAL SENSE
The Eye. -— Pigment is presented in the outer wall of the optic cup.
On the inner wall the internal limiting membrane is developing and beneath this in the region of the fundus, axones of the retinal neuroblasts
are growing into the optic stalk. The choroid fissure has partly closed,
and its proximal end is filled with the ingrowing pecten. The inner wall
of the lens is continuing to thicken. The middle layer of the cornea has
begun to develop. '
The Ear. -—There is no characteristic change directly connected
with the ear at this time. Within the pharynx, however, the formation of
the tu-bo—tympanic cavities has begun.
The Olfactory Organs. —The depression of the pits has greatly
increased, and their openings now lie on the border of the oral cavity.
The olfactory epithelium is giving rise to the elements of the I nerve.
Besides describing the events of the fourth day, this chapter also in
cludes an account of the subsequent development of the nervous system
and the organs of special sense.
VII. THE URINOGENITAL SYSTEM
The Excretory System. -— Primary tubules have developed
throughout most of the mesonephros, while secondary and tertiary tubules are arising. Collecting tubules are springing from the Wolilian
duct to connect with the two latter types. The Malpighian bodies are
beginning to appear in the functional portion of the organ which starts
to act as a kidney at this time. Rudiments of the metanephros are evident as a divcrticulum from the posterior end of each mesonephric duct.
The nephrotomal tissue just behind the mesonephros is beginning to
degenerate.
432 THE CHICK
The Genital System. —— The Gonads are represented by thickenings
of the peritoneal epithelium on either side of the dorsal mesentery, and
contain primordial germ cells. The oviducts are present in both sexes
in the form of the tubal ridges.
VIII. THE ADRENALS
The cortical substance of the adrenal bodies appears on the peritoneal
wall near the mesonephros, and material from the primary sympathetic
nervous system which is to form the medullary substance comes in contact with it.
IX. THE AMNION AND ALLANTOIS
The amnion is completed upon the fourth day, while the allantois has
pushed out somewhat further into the extra~embryonic coelom.
13
HE CHICK: DEVELOPMENT DURING THE FIFTH
AND SUBSEQUENT DAYS
THE EXTERNAL APPEARANCE
GENERAL
DURING the fifth day, the cervical flexure reaches its maximum
curvature and from then on becomes less and less marked, while the protuberance caused hy the mid-brain also attains its greatest relative prominence at this time. The third and last visceral cleft closes during the
fifth day, and the future neck is slightly indicated; the first three visceral arches, however, are still somewhat in evidence in this region. The
limb buds which were merely rounded swellings on the fourth day are
beginning to give evidence of joints.
By the seventh day the second and third arches are no longer visible
externally, the heart has moved backward so that the neck is clearly
defined, and the external auditory meatus has appeared, as indicated in
the previous chapter. The limbs are distinctly jointed, and by the
eighth day, the fore limbs begin to appear winglike. Upon the eighth
day feather germs are also visible, the tail is relatively much shorter,
and the position of the abdominal viscera is quite clearly marked by an
external protrusion. From this time on, the embryo gradually assumes a
typical bircllike form, one of the most striking changes being the relative increase in the size of the body as compared with that of the head
due to mitosis and rearrangeinent of cells (Gaertner, ’49} (Fig. 222).
THE FACE
In connection with the development of the nose and mouth, the face
undergoes so great a change between the fourth and eighth days, that it
seems best to treat the subject separately.
At four days the openings of the olfactory pits are separated by a
median projection overhanging the mouth. It is the naso-frontal process.
Dorso-laterally each pit is further bounded by the lateral nasal process
lying between the pit and the antero-dorsal part of the eye. Just below
each lateral process there is also another slight out-pushing adjacent to
434 THE CHICK
the antero-ventral side of the eye, termed the maxillary process (Fi«_
223). During the fifth day the lateral nasal process of either side hecomes more closely united with the maxillary process heneath it. the
two being separated only by the shallow lac/Lrymal groove. At the same
time an extension of these
united processes crosses each
nasal pit and fuses with the
frontal process, thus dividing the pits into antacdorsal and postero-verma?
halves. Thereafter as detet.
opment proceeds the f0I:‘:‘;t:’.‘
are carried forward as: ti-to
external hares while the Hiter are drawn back ~-.{t:~.'I;;
the mouth as the z';.::.r»~,;.-1,."
nares (Fig. ‘724«). It is _
evident that the midriic: ;.zs;~:‘—
tion of the upper jaw  to
be derived from the nascfrontal process, and the lateral parts chiefly from the
maxillary process. The lower
jaw is molded upon the ventral and main part of the
mandibular arches (see he
Fig. 222.-—Embryo of 7 days’ and 7 hours‘ low)‘ By Virtue of tiles"
incubation 3:5. From Lillie (Development of changes the eighth day finds
the Chick). After Keihel and Abraham.
 
the nares and rudimentary
beak quite clearly defined, the latter being developed by the co1‘niiication of epidermal cells about the margins of the jaws. Further growth
of these parts, accompanied by a relative diminution in the size of the
eye and the development of the eyelids, brings the face to the condition
found’ at the time of hatchinrr.
FEATHERS
In a preceding paragraph feather germs were mentioned, and because of the peculiarly characteristic nature of these structures in the
whole class of Birds, it seems desirable to indicate very briefly the essentials of their development.
«.... ..»..:
FIFTH DAY: FEATHERS
Feathers, like hair, which
we shall consider briefly in
connection with the Mammal, are epidermal structures. That is to say, the
feather consists of hardened
tightly pacl-zed epidermal
(er.-toclermal) cells, not of
secretion by cells. Initially
:1 point on the skin where the
feather is to appear develops
a slight depression, in the
midst of which rises. 51 small
tipgroxrtli or papilla. The
apex ml the papillzi at iirst is
at about the level of the rim
of the surrounding depression, or sli_s;l1t'i§.* shove it. It
consists of 21 C3iT.' of dermis
(inesoilerm) covered by the
Fig. 22-t.—~Head of an embryo of about 5 days
from the oral surface. (N.L. 8 mm.) From Lillie
(Development of the Chielc).
ch.F. Choroid fissure. E.L. Eye-lid (nictitating;
membrane’). cx.mzr. External nares. l.Gr. Lachrymal groove. Other abbreviations as in Fig. 223.
435
Fig. 223. -—-Head of an emhryo of 4 days’ incubation. from the oral surface (‘N.L. 6 mm.).
From Lillie iflarclopnzent of the Chick).
E12. Epipliysis. H0111. Cerebral hemisphere.
Hy. llyoid arch. I.nas.pr. Lateral nasal process. Id. i\l:tmlihulur arch. flfx. Maxillary
procx.-ss. nas.fr. Nusu-f-rontal process. Olf. Olfactory pit. Or. Oral cavity. Ph. Pharynx.
1).A.3. Third visceral arch.
   
usual Malpighian layer of
the epidermis, and a thin
layer of stratified and
cornified epithelium cells,
the corrzeum. In other
words it possesses the
same cell layers which
constitute the
other regions.
Very shortly this papilla grows outward so
that it protrudes definitely above the Ievel of
the rim of the depression,
at which stage it is known
as a feather germ. Within
this germ the vascular
dermal core is now known
as the feather pulp. At
skin in
436 THE CHICK
the same time the Malpighian layer of the epidermis at the distal end ‘of
the germ forms folds whose cells are modified to make the barbs. More
proximally the folds arise from a nonfolded part of the Malpighian layer
whose cells produce a single axis, the quill. The latter structure pushes
upward and soon throws off its sheath of coreum, emerging as a down
feather, i.e., a short quill with many short, soft barbs. At the base of
the down feather the dermis produces the pulp of the permanent feather,
while the Malpighian layer here forms two main folds opposite each
other, the rachis, other lesser folds again producing the barbs. It is interesting to note that transplantation experiments by Cairns, ’54, have
shown that the underlying dermis determines the special type of epidermal structure which will be formed, i.e., wing feather, leg feather,
claw, or scale. '
THE SKELETON
As in the case of the Frog, only a brief description of the development
of the skeletal system will be given. For a more extended study, the
reader is referred to LilIie’s Development of the Chick, and the books of
reference cited therein.
THE VERTEBRAE, THE RIBS, AND THE STERNUM
At the end of the fourth day the cephalic portion of each sclerotome
was beginning to fuse with the caudal portion of the one anterior to it
to form the rudiment of the right or left half of a vertebra. The occurrence of these vertebral rudiments thus necessarily alternated with the
myotomes. An extension of mesenchyme had also grown up on either
‘side of the nerve cord above both the cephalic and the caudal divisions
of every sclerotome, forming in each case the respective posterior and
anterior rudiment of a future neural arch. This reversed cephalic and
caudal relationship between the original sclerotome on the one hand,
and the future vertebrae and their arches on the other, is of course a
corollary to the alternative arrangement between the vertebrae and myotomes just indicated.
Upon the fifth day, the fusion of the cephalic portion of each sclerotome with the caudal portion of the next anterior to it is completed. The
sclerotomes upon one side of the notochord also have become fused
above and beneath it with the corresponding sclerotomes upon the other.
Furthermore, as a result of concentration, all of the sclerotomal tissue
is beginning to become membranous, and ire; the region of each future
vertebra certain portions of this membrane appear especially condensed.
FIFTH DAY: VERTEBRAE, RIBS, HSTERNUM 437
One such condensation surrounds the notochord as a ring, constituting
the rudiment of a vertebral cenzrzmz. Another occurs in each of the upgrowing primordia of the neural arches, and still another arises in the
membranous mesenchyme extending outward between the myotomes on
either side of the notochord. Each of the latter extensions represents a
transverse or costal process.
During the sixth to the eighth days these eostal processes develop
Iurther, and in the thoracic region give rise to the membranous primordia of the dorsal two thirds of the upper parts of the true ribs, i.e.,
Fig. 225. —The right side of four bisected vertebrae of the trunk
of an 8-day Chick. From Lillie (Development of the Chick). After
Schauinsland.
caud.v.A. Caudal division of vertebral arch. ceph.v.A. Cephalic
division of vertebral arch. N’ch. Notochord.
those movably articulated to the vertebrae. The cervical costal processes
which are not movably articulated are often called cervical ribs.‘ The
first true rib primordlia are those of the fifteenth vertebra, which are followed by six other pairs. The third to the seventh pair of these ribs
possess ventral parts which develop from separate centers, and like the
ventral one third of the dorsal parts come from lateral plate mesoderm,
not sclerotome (Straus and Rawls, ’53). The third to the sixth of these
parts later fuse to the sternum. Further ventrally, the sternum itself develops from bilateral membranous plates also arising within the lateral
plate mesoderm. Presently the membrane of the neural arch primordia
unites above the nerve cord, and their normal development seems to be
. conditioned by both nerve cord and notochord (Waterson, ’54-) . Carti
lagepformation now starts in all of the regions indicated, and in the last
five pairs of ribs the dorsal and ventral part of each has its own center of
chondrification. The sternum or breast bone of the chick, including
1 Since there is no clear cut distinction between cervical and thoracic vertebrae
in the Bird, the writer is arbitrarily defining as thoracic all vetebrae with freely
articulating or true ribs.
438 THE CHICK
heel likewise has two cartilage forming centers, one in each of the lateral membranous plates; these, however, soon fuse. Following chondrification the cartilage is in turn replaced by actual bone; during this procedure the remains of the notochord are completely eliminated. Such
ossification is well advanced by the sixteenth day.
Subsequent to this time several of the thoracic and lumbar vertebrae
become rather firmly united with one another, and these in turn are
fused to the coalesced vertebrae of the sacral region. To this mass there
is also added posteriorly a number of the caudal vertebrae, so that a
considerable portion of the spinal column is virtually inflexible, a condition peculiar to the Birds. Lastly, the extreme terminal vertebrae are
likewise fused into a single piece termed the pygostyle.
C THE APPENDICULAR SKELETON
The Fore-limb. ——- On the fourth day a concentrated mesenchymal
mass—probably of sclerotomal origin appears in the base of each forelimb bud, and on the fifth day there grow out from this membranous
mass four processes. One, the primordium of the limb bones, grows out
into the lengthening wing bud; a second, the scapula, grows backward
and dorsally above the ribs; a third, the coracoid, grows down posteriorly toward the region of the sternum; and a fourth, the clavicle, grows
in front of the coracoid toward the median line. The last three elements
represent the rudiments of the pectoral girdle. Centers of chondrification occur’ in the membranous primordia of the scapula and coracoid
on the sixth day, followed later by ossification. The clavicle, on the
other hand, ossifies directly from membrane, about the eighth day. Like
the coracoid and scapula, all the bones of the fore-limb pass through
both a membranous and cartilaginous stage previous to ossification. It is
interesting to note that in the wrist there are 13 membranous elements
which as a result of fusions produce only two definitive carpals. Likewise in the hand five digits are represented in the membrane, but the
first and fifth soon disappear.
The Hind—1irnb. —-Like the fore-limb, the parts of the pelvic girdle
and hind-limb bones arise about the fifth day as four processes from a
common mass of mesenchyme in the region of each hind-limb bud. The
membranous process representing the limb bones grows out into the
bud; another process, the ilium, which is elongated in an anterior posterior direction, grows dorsally; a third, the pubis, grows anteroventrally, and a fourth, the ischium, grows postero-ventrally. By the
FIFTH DAY: APPENDICULAR 439
eighth day, the distal ends of the pubis and ischium have both rotated
posteriorly so that they are parallel with one another, and with the
ilium. Chondrification and ossification follow the membranous stage,
and the limb develops in a manner fundamentally similar to that of
the fore-limb. There are three tarsal elements and five digits present in
cartilage, but the rudiment of the fifth digit soon disappears. Later the
two proximal tarsals fuse with the tibia, and the distal one with the
three long metatarsals; subsequent to ossification the latter become
united, thus forming with
the distal tarsal element
the single tarso-nzetatan
sus.
As regards the details
of ossification in the long
bones of the Chick, we I , _ ., endochondng
find that the situation dif- , _ -  ‘‘ b°"°
remains of :‘ - — ‘ ‘
_ diaphysial
that 111 the Frog, and ca.-mag:
from what we shall. later
see in the Mammal. As
noted the membranous
stage is as usual followed
by cartilage, and as in the Fig 226__The head of a long bane (femur, in
Frog in the region of the the Chiizk. From Lillie, aftc; Br:11chet.1Thed.sifilua
_ - _  -- lion wit I respect to the epip ysia rarti age i ers
Shaft or d1al’h)“”i"'” ll“: from that in the Ft‘H,[_‘. but the -nizuation in the
cartilage is overlaid by «Iiapi; Z: i» :-in:El'ir to the extent that, save at the
uncjs, horn is little or no bone except that produced by the p:,'rin$t+"um.
 
 
   
fers somewhat, both from
marrow
perlosteum cavity
 
periosteal bone. In this
case, however, the cartilage is presently destroyed, and partly replaced by true endochondral
bone, though of a cancellcus character. Throughout the shaft this cancellous endochondral bone is then likewise removed to be replaced to a
considerable extent by marrow. Thus in respect to having most of each
long bone ultimately of periosteal and membranous origin the Bird approaches, but does not quite equal the condition in the Frog. There is
in the Chick some endo«::honrlral ossification of a permanent nature in
these bones which comes about because of their method of longitudinal
growth which takes place as follows:
The epiphyses or ends in the Chick bones, unlike those in the Frog,
only remain cartilaginous during the increase in length of the diaphysis.
440 THE CHICK
This increase occurs through ossification of the cartilaginous ends on
their diaphyseal sides, with simultaneous addition of more cartilage distally (Fig. 226). Finally as growth is completed the cartilage of the
epiphyses is entirely replaced by cancellous bone. In this manner it
happens that a little spongy bone at the ends of the diaphysis, and all
of that in the completely ossified epiphyses is of endochondral origin.
In concluding this topic it should be noted that among the long bones
of the Bird the humerus is peculiar in one respect. In this bone there is
relatively little marrow, the extensive cavity therein being largely occupied, as will presently be noted, by one of the lung outgrowths called
air sacs. (See below.)
THE SKULL
The Primordial Craniu~m.——The primordial or cartilaginous cranium of the Chick is first indicated by concentrations of mesenchyme
during the fourth and fifth days. Then, during the sixth, seventh, and
eighth days, these mesenchymal concentrations develop into the following fused elements of cartilage. Along either side of and encasing the
anterior end of the notochord, appear the parachordal plates. In the
Chick these elements develop from the first as a single piece, and are often known, therefore, as the basilar plate. Anterior to it are developed
simultaneously upon either side another pair of plates — the trabeculae.
Posteriorly, these are continuous with the parachordals, with which they
form an angle corresponding to the cranial flexure, while anteriorly,
their ends meet and fuse with one another. This fusion then extends
somewhat, so that eventually the central space is closed, except for a
small opening containing the pituitary body. Thus the trabeculae and
parachordals together form the entire cartilaginous floor of the skull.
At the same time that these plates are forming, cartilage also develops around the auditory sacs and the olfactory organs, forming respectively the auditory and olfactory capsules. These are in direct continuity eventually with the plates. From the postero-dorsal part of each
auditory capsule, processes now grow toward one another and fuse
above the hind-brain. Thus is constituted the only portion of the roof of
the cranium which is preformed in cartilage. Posterior to each auditory
capsule, a dorso-lateral plate of cartilage develops, while anterior to
and in contact with the capsule, a transverse partition arises between it
and the orbit. This partition extends medially somewhat, so as partially
to bound the brain cavity in front. Anterior to the cranial cavity, midFIFTH DAY: THE SKULL 441
way between the two orbits, and between the nasal capsules, a continuous longitudinal partition appears and fuses ventrally with the trabeculae. It is the interorbital and internasal septum.
The remaining part of the skull which is preformed in cartilage is
known as the visceral skeleton or cartilaginous splanc/mocralziunz, and
arises from the first three pairs of visceral arches. During the fifth day,
these arches are chiefly membranous. and the antero-ventral or distal
ends of the first mandibular pair have fused with one another in the
middle line. Subsequent to the fifth day, the ventral or main parts of
each mandibular arch become chondrified, and are known as Mec-kel’s
cartilages; they form the core of each side of the lower jaw. From the
proximal (i.e., hinder and upper) end of each of these arches, there develops a tri-radiate piece of cartilage, the palate-quadrate, which eventually ossifies as a separate bone. It is termed simply the quadrate, and
constitutes the articulation between the lower and upper jaws. The second (hyoid) and third visceral pairs of arches later‘ form the hyoid apparatus, consisting respectively of the paired lesser and greater cornuae
and the two median copulae. Moreover, the upper ends of the second
arches are thought to give rise to parts of the colurnellae, as noted in
the account of the ear (Chapter 12) .
Altogether, the final bones of the Bird’s skull which have been preformed in cartilage are the following: the basi-occipital, exoccipztals,
and supra-occipitals about the foramen magnum; the proiitic, epiotic,
and opisthotic about each auditory capsule; the basisp/zenoid, orbitasphenoids. alisphenoids, and interorbital and internasal septum about
the eyes and nasal capsules; the quadrate, and Meckel’s cartilages in
connection with the lower jaw; and the hyozd apparatus in the region
of the throat.
The Membrane Bones. ——These are bones which are not preformed
in cartilage, but ossify directly from the condensed mesenchymc or
membrane. They constitute a good share of the Bird’s skull, and begin
to develop about the ninth day. The bones thus formed are as follows:
the parietals, jrontals, and squamosals, forming together the main part
of the cranium proper; the lachrymals, nasals, and premaxillae, form
ing the face and part of the upper jaw; the maxillae, jugals, quadratojugals, pterygoids, palatines, parasphenoids, and vomer, forming the
rest of the upper jaw and the base of the cranium; and the angulars,
supra-angulars, operculars, and dentals, forming the coveringbones for
the lower jaw.
442 THE CHICK
THE ALIMENTARY TRACT
THE FORE—GUT REGION
The development of the mouth proper has already been suliiciently
described in connection with the discussions of the alimentary tract and
the middle ear in Chapter 12, and of the skull in the preceding paragraph. We shall proceed, therefore, to an account of the further development of the remainder of this tract and its appendages.
Fig. 227.-—— Derivatives of the visceral pouches and associated organs, in the Chick.
From Lillie (Development of the Chick). After Verdun (Maurer). Combined from
frontal sections. A. In embryo of 7 days. B. In embryo of 8 days.
Ep. 3,Ep.4-. Epithelial vestiges derived from ventral portions of the third ancl=fourth
visceral pouches. J. Jugular vein. p’br.,p’br.(V). Postbranchial bodies derived from
fifth visceral pouch. Ph. Pharynx. T h.3.,TH.4. Thymus bodies derived from dorsal
portions of the third and fourth visceral pouches. T’r. Thyroid body. 111, IV. Remains of third visceral cleft and position of fourth which never becomes a real cleft.
The Visceral Pouches and Arches.
The Pouc-hes.——At the end of the fourth day, the first and second
visceral clefts had closed, and the third had opened; during the fifth
day, this latter cleft also closes, whereas the fourth pouch, it will be recalled, has never developed an outer opening. About the seventh or
eighth day, the third and fourth pouches sever their connections with the
pharynx, and thus remain as patches of epithelium in the mesenchyme
of the neck, adjacent to the jugular vein. The dorsal portion of the epi
thelium from the third pouch then fuses with the dorsal portion from
the fourth to form a thymus body on each side of the throat of the
FIFTH DAY: THE FORE—GUT REGION 443
young Chick. Though thus apparently endoderrnal, I-lamrnond, ‘S4, states
that the clefts rather than the pouches may be the source of the thymus
and hence that it is ectodermal. Epithelial vestiges of the third and fourth
pouches are gener:.il.ly thought to produce the para:/iyroirls, while each
fourth pouch also produces a posterior outpushing sometimes regarded
as a vestigial fifth pouch. These separate from the pouches, and the left
one becomes the pose‘-bram:/zial body, somewhat like a small parathyroid.
while the right one clegenerates (Fifi. 227). Dudley, 7112, thinks these outpushings may be rudimentary sixth pouches, the filth having {used with
the fourth.
The Arches. —-The fate of the first three pairs of Visceral arches has
already been suiiiciently described above in ('0I1IlB('li()]] with the visceral
chondrocranium. The fourth pair of arches never develop beyond a
inesenchymal state and eventually disappear. The lifth pair are vestigial
and even more transitory.
The Respiratory Tract. —— At the end of the fourth day, the respiratory tract consisted of the glottis, the larynx, the trachea, and a pair of
posterior outgrowths from the latter. the rudiments of the bronchi and
lungs. All these parts, having arisen from the fore-gut, are necessarily
lined by encloderm. Upon the fifth day, however, the mesenchyme about
them begins to condense to form true mesoderm. through which the
lung rudiments continue to grow posteriorl_v as a pair of tubes. Upon
the sixth day, these tubes begin to branch, and thus it appears that the
original rudiments really represented the lining of only the two main
or primary bronchi. Their branches then constitute the linings of the
secondary bronchi’, and the intercommunicating terticlry or parnbronclzi,
together with the finer ramifications from the latter known as air capillaries. This network of air capillaries, it is to he noted. takes the place
of the blind terminal sacs or alveoli found in the Marnmals. Thus there
are no pockets of residual air in the lungs of the Bird, but continuous
passages which make possible a. complete circulation. The mesoderm
indicated above eventually gives rise in the region of the larynx and
trachea to the cartilages and muscles of these organs. Further hack it
surrounds the endodermal lining of the various bronchi and air capillaries, and ultimately forms the connective tissue substance of the lung.
Through this tissue the blood vessels later rarnify among the tubes
and capillaries.
In the case of the Bird, besides these tubes and respiratory capillaries,.there are also connectgd with the lungs the various air sacs. These
arise, with one exception, as outgrowths from the secondary bronchi,
the exceptional case being the abdominal sacs which originate directly
l
i
r
3
444 THE CHICK
from the posterior ends of the primary bronchi. The rudiments of the
abdominal and cervical sacs are said by some to be distinguishable as
early as the fifth day, while the others appear somewhat later (Fio.
228). In the course of development these peculiar sacs which have thus
originated, gradually push their way to their respective positions among
M°5»'"9‘-‘"' -1  '  ‘ -—  -Lat.moi.
Rec.Br.-:=.'  ‘  .  . ___Me5.mOi_
 
Rec. Br.
Abd. Sc.--""“'
Fig. 228. —A. Lateral view of the left lung of a 9-day embryo, showing branches
of the bronchi within it. B. Ventral View of the lungs and air-sacs of a 12day embryo, with internal branches of the bronchi not shown. After Locy and
Larsell.
Abd. Sc. Abdominal air-sac. A. Int. Sc. Anterior Intermediate air-sac. Br. Extrapulmonary bronchus. Cerv. Sc. Cervical air-sac. Ect. 1. An ectobronchus. Ent. 1.
An entobronchus. Lat. I, 2, 3. Laterobronchi. The ecto. ento. and laterobronchi are
all classed as secondary bronchi in the text description. Lat. moi., Mes. mai. Lateral and mesial moieties of interclavicular air-sac. 0e. Oesophagus. Par. Parabronchi. P. Int. Sc. Posterior Intermediate air-sac. Rec. Br. Recurrent bronchi.
the viscera. Here they come to occupy considerable space, while a branch
of the interclavicular sac extends eventually even into the upper bone
(humerus) of each wing.“ Besides being connected with the respiratory
passages by the bronchi from which they arose, each sac, with the exception of the cervicals, also develops secondary connections with the
parabronchi. In the adult these connections always convey air from the
3 In the latter case the bone is said to undergo a kind of dissolution to make
way for the ingrowing sac, and the dissolution is thought to depend on parathy-K
mid activity which in turn is due to oestrogens derived from the yolk-sac
* (Bremer, ’40) .
FIFTH DAY: THE FORE—GUT REGION 44.-5
sacs to the lungs, and are, therefore, termed recurrent bronchi. The cervical sacs, though possessing no recurrent bronchi, are indirectly connected with branches of the most anterior pair of secondary bronchi,
and these branches probably act as recurrents. The functions of the sacs
are apparently to lighten the Bird’s body, to help maintain air currents and, in the case of the abdominal sacs, to cool the testes.
Fig. 229.—Partially dissected viscera of the Chick, from the right
side. From Kellicott (Chordate Development). After Duval. A. Of a
6-day Chick, enlarged slightly less than six times. B. of a 13-day
Chick, enlarged two and one half times, showing the elongated intestine and its extension into the umbilical stalk. _
zz. Right atrium. al. Allantois. as. Abdominal air-sac. b. Bulbus
arteriosus. c. Caecal processes. zl. Loop of duodenum. dj. Duodenaljejunal flexure (a relatively fixed point during the elongation of the
intestine). f. Fore-limb bud (cut through}. g. Gizzard. go. Gonacl. h.
Hind-limb bud (cut through _). i. Loops of small intestine. l. Liver. lg.
Lung: ll. Left lobe of liver. lv. Left ventricle. M. Rudiment of Mullerian duct (tubal ridge). p. Pancreas. r. Rectum. rl. Right lobe of
liver. To. Right ventricle. s. Yoll-:-stalk. U. Umbilical stalk. W. Wolffian body or mesonephros.
Finally, in connection with the development of the respiratory system, it is to be noted that about the fifth day, the glottis begins to close.
Both larynx and glottis later become entirely shut, but subsequent to
the eleventh day, the opening is gradually re-established.
The Esophagus, the Stomach, and the Duodenum.-—At the
end of the fourth day, the esophagus was a straight tube, while the region of the stomach and duodenum was indicated by a slight curvature
to the left. The esophagus does not alter much on the fifth day, except
to continue to elongate. The stomach, however, is becoming distinguished from the duodenum by its greater dilation. Also, at the extreme left of the gastric duodenal curve, a slight pouch is forming. This
446 THE CHICK
marks the end of the gastric region. Later this pouch enlarges to form
the muscular gizzard. while the part between it and the esophagus develops the gastric glands and comprises the proventriculus. The crop is
evident by the eighth day as a dilation of the esophagus at the base
of the neck. Anterior to the crop at that time, the lumen of the esophagus is temporarily closed. ‘
The duodenum is not very clearly defined on the fifth day, but shortly
afterward it begins to develop as a loop in the tract just beyond the
gizzard. From the gizzard, the proximal limb of the loop descends a
short distance, and then bends upward to form the ascending branch.
Ultimately the pancreas comes to lie in between the limbs of this loop.
The end of the ascending branch marks the termination of the original
fore-gut region and the beginning of" the small intestine (Fig. 229).
The Liver.~——On the fifth and subsequent days, as on the fourth
day, development of the liver consists chiefly in further growth in size.
This is accomplished as already indicated by continuous branching and
anastomosing of the original diverticula together with the accompanying blood capillaries. These diverticular branches are at first solid, but
on the fifth day many of them have acquired a lumen, and this process
continues as growth proceeds. '
As regards the bile ducts, it is to be noted that on the sixth day the
common duct disappears, and the two bile ducts which emptied into it
again empty directly into the duodenum.
The Pancreas.——The pancreas at four days, it will be recalled,
consisted of three separate outgrowths: a dorsal one from the wall of
the duodenum opposite the common bile duct, and the beginnings of
two ventral ones from the duct itself. During the fifth day all three
diverticula continue to grow and branch (Fig. 230). On the sixth day,
the right ventral pancreatic mass becomes united with the dorsal, whose
duct shifts ventrally on to the left side of the duodenum. As noted
above, the common bile duct disappears at this time, and thus the two
ventral pancreatic ducts come to open directly into the intestine. Later,
the left pancreas becomes fused with the other two, and there remains
a single glandular mass lying in the mesentery within the loop of the
duodenum. lts three ducts continue to remain separate, however, and
they open into the distal limb of the duodenal loop near the bile ducts.
THE MID-GUT REGION
It has been indicated that the mid-gut or rudimentary small intestine’
begins at the end of the duodenum. At the close of the fourth day, it
n
F IFTH. DAY: THE MID—GUT REGION 44?
was noted that it extended from this point as a virtually straight tube
across the region of the umbilicus to the beginning of the tail fold and
hind-gut. In zibout the middle, it gave off the yolk-stalk. During the
fifth day a very slight downward bend (the duodeno-jejunal flexure)
Fig. 230.—-Reconstruction of gizzard; duodenum,
and liepato-pancreatic ducts of a Chiclc embryo of
124 hours. From Lillie (_Development of {he Clzz'c'/.15.
Alter Broulia.
D.clI. Duclus (:l10le(lOCllllS. D,r‘y. Ductus cystivus.
DJ1.cy. Duutus hepato-cysticus. 11.11.11. Do1'.~:ul or hepato-enteriv duct. Du. Duodenum. G.bl. Gall bladder.
Ciz. Gizzard. }’u.rI. Dorsal pancreas. Pa.2'.u’. Right
ventral pancreas. Pa.-v.5. Left \‘entr:il pancreas.
appears just at the point where the duodenum ends and the mid-gut
begins. From this bend, the latter extends postero-ventrally for about
half its length; at this point, as noted, it connects with the yolk-stalk. lt
then ascends again to its termination, which is now marked by a small
bilateral swelling, the rudiment of the intestinal caeca. The entire midgut region thus indicated is still quite short, and its dip down into the
umbilical stalk very slight. t
On the sixth day, however, the ventral dip of the small intestine
reaches well down into the above stalk, thus forming in the intestine
448 THE CHICK
as a whole a second distinct loop (Fig. 229, A). The latter soon becomes much more pronounced than the duodenal loop, and during later
development acquires numerous convolutions (Fig. 229, B). These
convolutions lie within the umbilical stalk until about the eighteenth
clay and are then drawn into the body. They are soon followed. by the
EVIL ._. W. D.
An. PL 
Fig. 231.—Chick embryo of 11 days, sagittal section through
the region of the cloaca. Reconstructed from several sections.
(After Minot.) From Lillie (Development of the Chick). Anterior end toward the reader’s left.
All’. Ascending limb of the allantois. Al ". Descending limb of
the allantois. An. Anal invagination, or proctodaeum. An.pl.
Anal plate or cloacal membrane. Art. Umbilical artery. B.F.
Bursa Fabricii. b.f. Duct of the bursa. Clo. Cloaca, i.e., the urodaeal portion. Eb. Ectoderm. Ent. Entoderm of the rectum. Ly.
Nodules of crowded cells, probably primordia of lymphoid structures in the wall of the large intestine. W.D. Wolfiian duct.
remains of the yolk-sac. The intestinal caeca which were barely indicated on the fifth day ultimately grow out into two fingerlike processes.
THE HIND—GUT REGION
On the fifth day, as on the fourth, there is no particular change in
the rectum. On the seventh and eighth days, however, its cavity becomes
occluded. Later, the lumen is restored except for a small plug separating it from the cloaca, and just anterior to this plug a slight dilation
develops. This dilation is the coprodaeum. The plug persists until about
the time of hatching.
The chief change in the cloaca during the fifth day is the fusion of
FIFTH DAY: THE HIND—-GUT REGION 449
the laterally compressed walls of the posterior part. During subsequent
development, a cavity is re-established in the postero-dorsal part of this
closed portion; it constitutes the bursa F abricii of the adult. This is a
sac which remains separate from the original cloaca, but which opens
into another cavity, communicating directly with the exterior. This
mesonephric duct
mecanephrlc duct
 
 
coprodaeu m
allantoic stalk
urodaeum
proctodaeum
Fig. 232.—A diagram of a sagittal section of the posterior end
of an approximately eleven-day embryo to indicate better the relations of the parts partially shown in Fig. 231. The metanephric
duct opening separately into the urodaeum (a condition attained
on the sixth day) is shown, though for some reason it does not
appear in Fig. 231. The anal plate separating urodaeum from
proctodaeum is shown in the diagram, but is unlabelled.
latter cavity is the proctodaeum, and has arisen by an outpushing of
the ectodermal _walls around the edges of the anal plate or cloacal membrane (Figs. 231, 232; compare Fig. 193, Chapter 10). At hatching the
latter disappears and thus the proctodaeum is finally placed in communication with the original embryonic cloaca minus the posterior portion of the latter which went to form the bursa Fabricii. At. about the
same time the plug which closes the rectum disappears. Thus, theadult
cloaca consists of three parts, the coprodaeum, a part of the original
cloacal chamber now called the urodaeum, and the proctodaeum. The
latter opens to the outside through the anus.
450 ‘THE CHICK
THE CIIRCULATORY svsrsm
THE HEART
During the fourth day a series of changes in the position of the various parts of the heart in relation to each other were indicated. During
the fifth day these changes progress rapidly, and upon the sixth day are
virtually completed.
Besides these movements, there were also noticed on the fourth day
the beginnings of certain partitions within the heart. These were the
interatrial, the interventricular, and the cushion septa. During the fifth
and part of the sixth days, all these are practically completed. This
process involves, first, the meeting of the two parts of the cushion septum so as entirely to divide the atrio-ventricular canal into right and
left channels. The interatrial septuin then unites with the cushion septum
on the antero-dorsal side of the latter, while the ventricular septum joins
it postero-ventrally. These fusions, though described separately, occur
more or less simultaneously (Fig. 209, F
In connection with these processes there remain to be added certain
details as follows: As the division of the originally single atrium into
two atria occurs communication between them is preserved by the concomitant development of perforations in the newly formed septum.
These perforations correspond functionally to the foramen ovale in the
heart of the Mammal, and their physiological significance is described
below. It must also be noted that the interatrial septum as thus far described is augmented in the adult Bird by the addition of another part
as follows: Upon the seventh day the proximal portions of the left precava and the pulmonary vein start to be incorporated into the atria,
and as this occurs the tissue between them is added to the septum. This
new part is called the pars cauo-pulmonalis (Quirring, ’33). Lastly,
there is also a small ventricular foramen whose final closure will be
described presently in connection with the development of . the aortic
division of the bulbus.
This completes the description of the septa within the heart proper.
Upon the fifth day, however, another septum develops within the truncus arteriosus. It appears first at the anterior end of this vessel in such
a position as to separate the orifice leading to the sixth aortic arches and
hence to the pulmonary arteries, from that which leads to the third and
fourth "aortic arches. This partition then grows backward through the
FIFTH DAY: THE HEART 451
distal portion of the bulbus, and on the sixth and seventh days it connects with a septum which has formed within the proximal portion of
that vessel. Thus a continuous somewhat spirally twisted partition has
been produced extending through the truncns .-md hullaus clear In to the
interventricular septum of the heart. It is to he noterl that the entire bul
bus, though now ventral,
still lies somewhat to the ca;,¢om_ l\
right of this latter septum. ;'
Nevertheless, the fusion of p 6 xi 3
the hulbus septum and inter- Au 4
ventricular septum is eiiectetl ' "  ,4»
in such a way that in cmmec- ‘pp  .1?‘ S_ GL5.
     
tion with subsequent changes
in the cushion septum the
aortic division (i.e., the division from the third and
fourth arches) of the bulbus
comes to open through the
foramen in the ventricular
septum directly into the left
ventricle. The pulmonary division, on the other hand,
continues to open into the
right ventricle (Fig. 233).
Subsequent to the fifth day
also, certain other changes
are Completed as f°u°w5'The Fig. 233.——The heart and aortic arches of a
semilunar valves develop in Chick embryo the latter part of the sixth day.
both the aortic and pulmo- Efogeacgézfifitiggiefrgfiiyllie (Development
nary divisions of the bulbus, Au. Atria. Car.com. Common carotid ar
and the parts of that vessel Zi§’$ia§°’;'§§'fé?‘ §'i'2'?’ls.“"i’h?f§°"€ii.-‘fulfil:
proximal to these valves are fourth (systemic) and sixth (pulmonary)
incorporated into the ventri- acme arches’
cles. The two divisions of the bulbus and truncus arteriosus distal to
this point are gradually separated so as to form distinct vessels, i.e., the
proximal portions of the aortic and pulmonary arteries. As noted in a
previous chapter, the sinus venosus becomes a part of the right atrium
into which empty all the systemic veins, and finally both atria acquire
small auricular appendages or auricles.
L2
452 THE CHICK
THE EMBRYONIC BLOOD VESSELS
The Arteries.
The Aortic Arches.——At the end of the fourth day, the pairs of
aortic arches which remained fully developed were the third, fourth,
and sixth. The third pair, it will be recalled, ran upward from the ventral aorta. and continued anteriorly as the internal carotids, while pos
teriorly the dorsal end of each of these arches was still connected with
the dorsal end of each fourth arch. From the base of each of the third
LEFT SIDE RIGHT SIDE
6th day 6th day
   
Internal carotid
 
 
 
 
 
i 3 r
aortlcv3rches{-‘i-th : ‘ systemic arch ’  4 h} “me h
gh < . '  r are es
‘ ' ' 6th
external carotid — ' ‘ .
external carotid
common carotid
. \tfUn€US 3l’t¢l‘lOSl.|S
Fig, 234.——Reconstruction of the aortic arches of a 6-day Chick embryo from a.
series of sagittal sections. Modified from Lillie. '
arches, on the other hand, another vessel ran forward as an external
carotid.
Upon the fifth day three further changes are initiated as follows.
First, on each side, the portion of each dorsal aorta between the third
and fourth arches begins to disappear. Secondly, the fourth arch on the
left side diminishes in size (Fig. 234-). Thirdly, there occurs anteriorly
an anastomosis between the internal and external carotids, while the
portion of the latter between this point and the base of the third arch
(primary external carotid in Fig. 235) begins to atrophy.
By the eighth day the changes thus begun have been completed. so
that the condition then obtaining is as follows: First as regards the systemic and pulmonary arches, it is to be noted that on the left side,
the entire fourth arch together with the dorsal aorta between the third
and the sixth arch has vanished. On the right side the dorsal connection between the third and fourth arches is gone, but the fourth arch
itself is well developed It persists as the main systemic arch of the
FIFTH DAY: EMBRYONIC BLOOD VESSELS 4153
adult (Fig. 210, B). It is to be noted that the Bird differs from the
Mammal in that in the latter, it is the left arch which remains. The
immediate cause of this interesting difference between Bird and Mammal according to Bremer (’28) is as follows: In the first place in the
Bird the torsion of the heart tube is somewhat greater than in the Mammal. Secondly this is cor
related Witll 3 greater . Eiigggim
backward movement of ‘°'°“d
the heart in the  in intemolcorotid '
connection with the great- _ 7
er length of the neck. This comm“ €°'°*‘d' . ‘°"""‘°" ‘°'°"d
last ‘feature results in
lengthening the aortic ves- NGHT
 
 
 
 
" internal carotid
LEFT
sels and in involving them
in the increased torsion of §f,;;‘,‘;'v‘f§,', _ §’:§,:{2C;°."..'
the cardiac tube. Thus the
left fourth arch is drawn dums \ [ mm;
into a disadvantageous Borulh ‘ W Soto"!
position on the ventral §?'r'§'.‘,‘,’"°'Y ‘ . °"“ °"°'Y
side of the truncus, while p,i,m,y V primary
the right assumes a dorsal ‘“""°"‘°" ‘”b°'°"'°"
position with a much systemic artery \ 1  p
more direct connection ‘3'*\5¢9'“°"‘°‘°'*°'Y '3'“ “"9'“""°‘”'"'V
with the dorsal aorta Fig. 235.—-Diagram ca; tgi ionic archvés fand
- connecting vesse s in t e ic as viewe rozn
(F1g' 236)‘ In the Mam‘ the ventral side. The vessels in outline indicate
mal on the other hand, the situation existing at one time or_ another in
not only is this not true the embryo. Those shown in black indicate the
1
permanent arrangement. “
but according to Congdon
and Wang (’26) the blood as it comes from the truncus on the right is
necessarily directed toward the left. Hence the left arch receives the
larger stream and so becomes the dominant vessel.
All parts of the sixth arches continue to be well developed on both
sides throughout embryonic life. At the time of hatching, however, the
upper portion of each vessel between the origin of the pulmonary
arteries and the dorsal aorta (i.e., the duct of Botallo or ductus arteriosus, indicated above) becomes atrophied and remains only as an occasional vestige in the adult.‘ In the second place with respect to the carotids it appears that since the atrophy of each external carotid between
i the base of the respective third arch and the point of its anastomosie
3 In the Mammal a remnant of the left duct of Botallo always persists.
454 THE CHICK
with the internal carotid has been completed, each external and internal
vessel now takes its origin and continues anteriorly from this point of
fusion. Posterior to this point certain remaining parts constitute on
either side a newly named vessel, the common carotid. Each common
carotid consists of what was previously the postero-dorsal portion of
the respective internal carotid, the respective third arch, and the part
dorsal aorta
aortlc arch
Fig. 236.——Diagrammatic ventral view of the truncus and the
third and fourth aortic arches in A, the Mammal, and B, the
Chick. After Bremer. Note that in the Chick the fourth arches
are involved in the twist of the truncus, thus bringing the right
fourth arch dorsal, and hence nearer to the dorsal aorta. The
left fourth arch on the other hand is brought ventrad, and hence
further from the dorsal aorta, thus leading to its elimination in
this form.
of each ventral aorta proximal to the base of this arch and the point of
union with the systemic vessel (Fig. 235). It is to be noted in this connection that the point of anastomosis between each external and internal carotid is not shown in Fig. 234. Hence each vessel there indicated
as an internal carotid eventually becomes part of a_ common carotid.
Finally, it must be remembered that while these changes are occurring,
the head of the Bird is being separated from the body by the development of the neck. This process results in the backward movement of the
heart and all its arches, so that by the time they have reached the stage
indicated on the eighth day, they lie entirely within the thorax. The
carotids, on the other hand, are elongated into vessels which pass forward into the head.
The Physiological Significance of the Embryological Structure of the
Heart and Aortic /1rches.—Before considering the remainder of the
FIFTH DAY: EMBRYONIC BLOOD VESSELS 455
blood vessels, it seems well to digress at this time in order to point out
the physiological significance of the heart and its arches as they have
just been described.
The heart, as has been seen, becomes virtually four chambered. It
fails to become entirely so during embryonic life, however, because of
the persistence of the foramina in the interatrial septum. This fact, as
well as the existence of the dorsal portions of the sixth arches, i.e., the
ducts of Botallo, is correlated with the embryonic method of aerating
the blood. This becomes clear upon a consideration of what this method
involves, as follows:
It is obvious that previous to the hatching of a Bird or birth of a
Mammal the lungs cannot act. Instead the allantois of the Bird, or as
will later be explained, the partially homologous placenta of the Mammal, performs the function of blood aeration. There now remains to be
described the relationship which the interatrial foramina and the ducts
of Botallo bear to the distribution of the different classes of blood. The
fully aerated blood from the allantois, the nutrient laden blood from
the yolk-sac, and a relatively small amount of strictly venous blood
from the posterior part of the body become mixed in the ductus venosus,
and from thence are poured together into the right auricle. At the same
time that this occurs the right auricle is also receiving blood through
the ducts of Cuvier or anterior venae cavae (see below). This blood is
returning from the head, and hence, save perhaps in the very early
stages, is relatively depleted of oxygen and nutriment. Up to this point
there is no question about the facts. From here on, however, there have
been two distinct theories as to the fate of the two classes of blood just
indicated. Both have been developed as a result of observations and
experiments upon Mammals, but probably apply equally well in their
essential points to Birds. 1
The first theory was somewhat obscurely outlined by Harvey in connection with his original discussion of the circulation of the blood in
1628. It can be very briefly stated as follows: It holds simply that the
two types of blood are completely mixed as they enter the right atrium,
and hence that there. is no separation of aerated and unaerated blood in
the embryo. This has been accounted for on the ground that the organism is sufliciently small and inactive and the circulation sufliciently swift
so that such separation is unnecessary. The second theory was developed
in 1798 by Sabatier, and may be described thus:
It is supposed that the structure of the right atrium is such that the
blood entering it from the posterior part of the body through the ductus
456 _ THE CHICK
venosus (aerated blood) is turned away from the right ventricle and
guided through the aperture or apertures in the interatrial septum into
the left atrium. From here it passes into the left ventricle, and thence
through the aortic division of the bulbus and truncus arteriosus into
the third and fourth aortic arches. The third arches, as has been seen,
convey this blood newly oxygenated and full of nutriment straight to the
head; the rest passes through the fourth arches (later only one, the
right or left) and backward along the dorsal aorta. On its way, however,
it becomes mixed with the depleted blood which has returned from the
head; this occurs as follows: It was noted above that this blood from
the head also passes into the right atrium. According to the present theory, however, its direction of entrance, together with the structure of the
cavity, is such that it is diverted from the openings into the left atrium,
and emptied directly into the right ventricle. From here it passes out
through the pulmonary division of the bulbus and truncus arteriosus,
and thence a slight part of it flows through the small pulmonary arteries into the rudimentary lungs. The larger part, however, continues
through the dorsal portions of the sixth arches, i.e., the ducts (later
only one duct) of Botallo, into the dorsal aortae; here, as indicated
above, it inevitably mixes with the aerated blood from the fourth arches
(later arch). Some of this mixture then supplies the body posterior to
the head. The larger share of it, however, eventually reaches again the
walls of either the allantois or the yolk-sac, where it receives respectively oxygen or food material, and is returned‘ to the heart in the manner already noted. Thus the posterior part of the body should get blood
poorer in oxygen and nutriment, at least during later stages when the
above arrangement would be in operation (Fig. 236X). Hence some
think there may be a relation between this and the faster growth of the
anterior end, if indeed that end is still growing faster at this time.
However, despite the theoretical considerations in favor of this second theory, all evidence until recently has supported the earlier view.
Thus to begin with, in the human embryonic heart near term at least, it
was shown anatomically that the interatrial aperture is not large enough
to pass all of the blood delivered by the postcaval vein. Hence it would
appear that some mixture of blood from the anterior and posterior veins
must occur in the right atrium. Then Pohlman, in 1909, apparently settled
the matter experimentally by injecting cornstarch into the vessels leading
from -the "placenta of the Pig embryo into the right atrium. He then
withdrew equal amounts of blood from each ventricle and found them to
contain equal numbers of grains. This type of experiment with certain
FIFTH DAY: EMBRYONIC BLOOD VESSELS 457
5 ‘nternal carotid artery
’ xternal carotid artery
internal carotid artery
external carotid artery
 
 
 
 
 
 
 
 
     
           
common carotid artery common carotid artery
~ subclavion artery (3rd arch)
subclavian artery (3rd arch)
main aortic (4th arch)
duct of Botollo (arteriosus
pulmonary artery (6th arch‘
anterior caval vein
ulrnonory artery (6th arch)
uct of Botallo (arteriosusl
- ulmonory veins
trunc us arteriasus
RIGHT LEFT
posterior vena cav
entrances of _
fight at,-.;um anterior cavol veins
entrances of
pulmonary veins
eft atrium
atria-ventricular
(mirrol) valves
hepatic vein
liver
 
entrance of
posterior vena cov
epotic portal vein
atrio-ventricular vaive
‘ oeliac artery ‘
‘ esenteric vein
right ventricle
 
ductus venosu
 
posterior vena covo "
 
       
 
eft ventricle
As. . .
.-,3! posterior mesenteric artery
.«
mbilical (ollantoic) vein
‘ caudal artery
A
umbilical (allantoic) arteries
Fig. 236X.—— Diagrams to illustrate the circulation in the Chick embryo according
to Lillie, and indicating at least a partial separation of aerated from unacrated
blood. Solid arrows represent aerated blood and broken arrows unaerated blood, the
relative amounts of each type being suggested by the size and heaviness of the
respective arrows. A, the complete circulation. B; the heart alone. Note the numerous small foramina in the interatrial septum as compared with the one larger
foramen ovale in the Mammal. The right atrio-ventricular valve is also different
from either of the mammalian valves (Fig. 336). With the substitution of the
placenta for the allantois, essentially the same type of circulation with the separation of the two classes of blood has been alternately denied and claimed in the case
of the Mammal ever since Harvey. For a complete discussion of this controversy
see the text. It seems now to be settled as shown.
Because this is an embryonic stage the sixth arches are connected with the
aorta. Being ‘a Bird the right sixth unites with the aortic extension of the right
fourth arch through the right ductus Botalli. In the Mammal it would be the left.
At hatching both ducts of Bot-allo will close and later atrophy (Coughlin and
Walker, ’53) .
458 THE CHICK
refinements was repeated by Kellogg on both the Pig and the Dog in
1923, and later by others with similar results. Therefore, it was reasonably concluded by both investigators that there had been a thorough
mixture of the two classes of blood in the right atrium. And so the question seemed to be finally answered.
Regardless of all this seemingly overwhelming evidence in favor of
the theory of mixture, however, many embryologists were still intrigued
by the hypothetical desirability of a separation if it could only be
proven. Consequently they have once more returned to the attack with
both similar and improved techniques, and with most interesting results. In the first place Windle and Becker (’40) using the Cat and
Guinea Pig, injected india ink instead of cornstarch. This probably did
not reduce the velocity of flow as did cornstarch, thus providing more
normal conditions, and their results supported the separation theory
of Sabatier. Next, in 194-1, Barclay, Barcroft, Barron, Franklin, and
Prichard performed the most ingenious experiment yet devised. They injected inert material, opaque to X-rays, into the blood stream of living
Sheep fetuses. Then by means of X-ray moving pictures they showed
that there is a fairly complete separation of the anterior and posterior
streams in the right atrium. This brilliant experiment, especially if confirmed, would seem to be conclusive. Finally, Whitehead (’42) has made
a model of an embryo Cat heart in neoprene by the reconstruction
method. With it he has demonstrated that the key to the separation of the
streams entering its right atrium is the pressure at which each stream enters. He, moreover, believes that the pressures with which the blood
streams do enter the actual Cat heart are such as to separate them. Thus
the matter rests at the date this book is written, and we are back once
more to the purely hypothetical conclusions of 1798.
However this may be in the embryo, it is of course certain that in the
adult Bird or Mammal the completely aerated blood from the lungs
(arterial blood) is normally entirely separated in the heart and arterial
circulation from the venous blood. To achieve this at, or shortly after,
the hatching of the Bird or the birth of the Mammal, all that is necessary' is the closure of the interatrial openings, or opening, in the septum and the occlusion of the ducts of Botallo (one duct in the Mammal).
Considering the matter of the septum first, it will be recalled that by
the end of the sixth day in the Chick this structure was closed except
for the existence of numerous foramina. During the embryonic life of
the Bird these foramina are kept open according to current theory in the
FIFTH DAY: EMBRYONIC BLOOD VESSELS 459
following manner: The pressure on the septum from the side of the
right atrium greatly exceeds that from the left side because of the relatively small amount of blood being returned to the left atrium from the
non-functioning lungs. Hence the septum tends to belly out to the left,
and to remain in a stretched condition with the foramina wide open. In
the Bird, as indicated below, the lungs start functioning to some degree
two or three days before hatching takes place. Hence the vessels of
these developing organs receive more and more blood, and the pressure
on the two sides of the septum is gradually equalized. This causes it to
straighten out, the stretch is taken out of it, and as a consequence its
wall thickens and the foramina are functionally closed. Later the tissue
about the former openings presumably becomes entirely fused. The
mechanism in the Mammal is somewhat different, but is supposed also
to depend on an equalization of pressure in the two atria, and a functional closure of the single interatrial opening. The details of the process in this class will be discussed further in connection with the Pig.‘
The closure of the duct of Botallo (arteriosus), at least in the Mammal where it has been most studied, is apparently brought about by the
contraction of muscle fibers within its walls. This has been rather cleverly demonstrated in the Guinea Pig by Kennedy and Clark (111) . Under anesthesia living, almost full term, fetuses were removed from the
uterus while leaving the umbilical cords attached. The fetuses themselves were then opened. so that the heart could be observed. When such
a fetus was in the air it would breathe. and the duct of Botallo could
be seen to close. When it was immersed in normal saline the embryonic
respiratory situation was restored, and the duct of Botallo would
promptly reopen. This could be repeated several times. Thus the closure
would appear to be a result of the stimulus of breathing. Within a
month or so after normal birth. however, the walls of the duct have
grown together, and the structure is reduced to a cord.
In conclusion of this topic it may be noted that in man either a defect
in the interatrial septum or a persistently patent duct of Botallo are
among the causes of infantile cyanosis, “blue babies.” Where a patent
4 The sudden functioning of the lungs as a factor in increasing the blood flow
from them to the heart in the case of the Mammal has been questioned for the
Cat and Guinea Pig by Abel and Windle (’39l. These authors claim that there is
already a good deal of circulation here at term, and that subsequent increase is
gradual. A similar situation is also claimed for other Mammals, including Man
(Patten, ’46). As noted the condition in the Bird is such that in that case gradual
initiation of lung function, and hence of change in the course of the blood, must
always occur.
460 THE CHICK
duct is the primary defect, it may be remedied by tying oii this vessel.
A failure in septal closure, however, is more diflicult to cope with. Yet
now even this may be greatly helped by a clever operation which involves rerouting part of the aortic blood to the lungs.
The Subclavian Arteries. -—-The primary subclavian arteries arise as
outgrowths from the. eighteenth segmental arteries. On the fifth day,
however, an anteriorly growing branch of each primary artery connects
with the respective third aortic arch, which as indicated eventually becomes a part of the common carotid (Bakst and Chaise, ’28; Figs. 233
and Q35) . These new branches then develop, while the original connections with the dorsal aorta through the segmental arteries become atrophied. Thus the permanent subclavians eventuallyarise from the carotids in the Bird. These arteries, of course, supply the wings, and in so
doing, develop various branches. It will not be advisable, however, to
follow them further in detail.
The Remaining Arteries. —— The only other major arteries whose development has not already been indicated in the account of the fourth
day, are the coeliac, the anterior mesenteric and the posterior mesenteric. The coeliac arises from the anterior part of the dorsal aorta, and
supplies the stomach, gizzard and part of the intestine. The anterior
mesenteric originates as an outgrowth from the single vitelline artery
close to the place where the latter leaves the aorta, and supplies the intestine. Lastly the posterior mesenteric develops from the aorta slightly
caudal to the kidneys, and supplies the rectum and cloaca. These three
arteries appear during the fifth and subsequent days (Fig. 237).
The Veins.
The Vitelline Veins. --- At the end of the fourth day, a second venous
ring had been formed about the intestine by a fusion of the vitelline
veins for a short distance beneath it. This second ring was beginning to
be destroyed by the disappearance of its right side, and during the fifth
day, this side is completely obliterated. From a review of the previous
development of this region, it will be evident that the condition of the
vitelline veins at this point has now become as follows. The two veins
unite just in front of the anterior intestinal portal, and ventral to the intestine, to form a single trunk, which is really a posterior continuation
of the ductus venosus. This trunk runs forward beneath the intestine for
a short distance, and then curves upward and to the ‘left. It next turns
sharply to the right and crosses over the intestine dorsally; finally it
bends immediately downward and again runs anteriorly to pass into the
FIFTH DAY: EMBRYONIC BLOOD VESSELS 461
liver (Fig 211, E). During subsequent stages as the anterior intestinal
portal continues to move backward, it is closely followed by the fusion
of the vitelline vessels. Indeed before very long this fusion passes beyond the region of the intestinal portal, and thus the single ductus venosus, or vitelline trunk, comes to extend a considerable distance into the
umbilicus before dividing into its two branches.
Fig. 237. —Diagrammatic lateral view of the chief embryonic blood vessels of the Chick, during the sixth day. From Kellicott (Chordate Development). After Lillie.
a. Atrium. al. Allantoic stalk. ao. Dorsal aorta. c. Coeliac artery. ca.
Caudal artery. cl. Cloaca. cv. Caudal vein. da. Ductus arteriosus. dv. Ducurs venosus. ec. External carotid artery. e]. External jugular vein. i. Intestine. ic. Internal carotid artery. ij. Internal jugular vein. 1. Liver. m.
Mesone‘phros. ma. Mesenteric artery. mv. Mesenreric vein. p. Pulmonary
artery. ,pc. Posterior cardinal vein. pv. Pulmonary vein. 5. Sciatic artery.
31:. Sulfclavian artery. scv. Subclavian vein. st. Yolk-stalk. sv. Subcardinal
vein. ul. Left umbilical artery. ur. Right umbilical artery. 1112. Left umbilical vein. 1;. Ventricle. va. Vitelline artery. vca. Anterior vena cava (anterior cardinal vein). vp. Posterior vena cava. vv. Vitelline vein. y. Yolksac. 3, 4, 6. Third, fourth, and sixth aortic arches.
The Hepatic Portal System. -—— It will be recalled that within the liver
the ductus venosus receives numerous capillaries. These capillaries increase during the fifth day, while at the same time the main channel of
the vein within the liver begins to disappear. This is brought about
through the gradual occlusion of this channel by means of strands of
the hepatic substance which grow into and across it. On the fifth day
also, a vessel starts to develop in the dorsal mesentery of the gut; it is
the mesenteric vein, and~presently acquires a connection with the vitelline trunk at about the region of the pancreas. By the seventh day the
462 THE CHICK
occlusion of the main part of the cluctus venosus within the hepatic sub
stance has been completed. From now on, therefore, the blood enters the
liver by the remaining posterior half of this vein, is distributed through
the hepatic capillaries, and is finally collected again to enter the now
separate anterior half of the same vessel through two main branches.
When development has reached this stage the posterior half of the ductus
venosus may be termed the hepatic portal vein, which receives the mesenteric vessel as its chief tributary. The two branches entering the anterior half of the ductus vencsus, upon the other hand, constitute the
Izepagic veins (Fig. 211, F).
Upon the fifth and immediately subsequent days the blood which enters the liver circulation is largely from the yolk-sac. Before long, however, the mesenteric vein has begun to send out branches which develop
simultaneously with the various digestive organs and spleen. Thus these
organs send an ever-increasing supply of blood through the hepatic portal rein to the liver. When the yolk-sac finally disappears they become
the sole source of the blood which passes through the hepatic capillaries.
The complete system of circulation which is developed in this manner is
then called the hepatic portal system.
The Fate of the Cardinals and Development of the Caval and Renal
Veins. -— On the fourth day, the subcardinals lying ventral to the mesonephros have direct connections with the posterior cardinals lying dorsolateral to it. Upon the fifth day, however, these connections are severed
and new ones established through capillaries within the mesonephric
-substance. At the same time, the subcardinals fuse with one another near
their anterior ends, and the connection of the right one with the posterior end of the vena cava inferior (established on the fourth day) becomes larger (Fig. 238). Thus a part of the blood in the posterior
cardinals now passes through the mesonephros and by way of the subcardinals and vena cava inferior to the heart. In other words, there is in
the embryo of the Bird a typical renal portal circulation. On the fifth
day also, or late upon the fourth, the subclavian veins begin to develop
in connection with the fore-limb buds. They arise as branches of the
posterior cardinal veins, a short distance behind the junction of the latter with the Cuvierian ducts.
Upon the sixth day, the section of each posterior cardinal between the
entrance of the respective subclavian vein and the anterior end of the
mesonephros disappears, thus forcing all the blood from the posterior
part of the body to traverse the renal portal channels. In this manner
also that portion of each posterior cardinal anterior to the entrance of
wag-ea
2;:;.5.~,a....~,..»s,~.._,.~ .. ,.
FIFTH DAY: EMBRYONIC BLOOD VESSELS 463
c. /V. sc. d. V. sc. s.
Fig. 238.--Reconstruction of the venous system of a
Chick of 5 days. Ventral view. From Lillie (Development
of the Chick). After Miller.
a. i\-Iesonephric veins. A0. Aorta. A.o.m. Omphalomesem
teric artery. A.u.s. Left umbilical artery. A.sc.s. Left sciatic artery. V.c.p.d.s. Right and left posterior cardinal
veins. v.c.i. Vena cava inferior. V..sc.d.,s. Right and left
subcardinal veins.
the subciavian becomes simply the proximal part of the latter vessel.
From this time on, the ducts of Cuvier, which now receive the jugulars
(anterior cardinals) and subclavians, may be termed the anterior or
superior caval veins. At about this stage also, the anterior portion of the
ductus venosus, which receives the two hepatic veins and the posterior
vena cava (vena cava inferior), may be said to have become merely the
anterior end of the latter vessel. Thus the posterior caval vein, like the
464 THE CHICK
two anterior cavals, now opens directly into the right atrium (Fig. 237).
While the above changes are occurring subsequent to the fifth day,
there are a pair of new veins arising in connection with the metanephros
Fig. 239. -o- Reconstruction of the venous system of‘ a sparrow embryo, corresponding to a chick of about 14- days. From Lillie (Development of the Chick). After
Miller.
V .c.i.H. Intra-hepatic part of the vena cava inferior. V.c.i.SC. Part of the venecava inferior derived from the suhcardinal vein. V.v.g. Genital veins. V.i.e.d.,s.
Right and left vena iliaca externa. V.i.i. Vena iliaca interna, (or V.c.p.s. Posterior
part of the left cardinal). V.i.l.d.,s. Right and left vena intervertehralis lumhalis.
V.r.m.d.,s. Right and left great renal veins.
or permanent kidney. These are the renal veins which presently take
blood from the permanent kidney to the anterior fused portion of the
subcardinals (now really the posterior part of the posterior vena cava) .
Just anterior to the kidney these renal veins also later establish direct
connections with the ‘posterior cardinals. Thus a new channel is formed
for the blood from the posterior part of the body via the cardinals and
the anterior portion of the new renal veins to the posterior vena cava
(Fig. 239). At the same time that this is occurring, the mesonephros toFIFTH DAY: SEPARATIO1'_V' OF BODY CAVITIES 465
gather with the renal portal system is disappearing. While the latter exists, however, it is essentially similar to the permanent system of the
same name in the Frog and other more primitive Vertebrates, thus affording an excellent example of recapitulation. It remains to note that
the hinder portions of the posterior cardinal veins persist in the adult
Bird as the iliac veins, receiving branches from the hind-limbs. Also in
subsequent stages, branches from the cardinals fuse with one another
medially at the posterior end of the body and give rise to the caudal
vein.
THE BODY CAVITIES
From previous discussion, it will be recalled that the space surrounding the heart has been designated as the pericardial cavity. Up to this
time, however, there has been no mention made of any separation of this
cavity from the peritoneal or general body cavity behind it. It now remains to describe how this separation is effected, together with the simultaneous closing 03 of 51 third space, the pleural cavity (see below). It
will then be possible in conclusion to show also how the walls of the
pericardial cavity come to form the independent pericardial sac of the
adult bird.
THE SEPARATION OF THE PERICARDIAL, PERITONEAL
AND PLEURAL CAVITIES
The separation of the peritoneal and pericardial cavities is chiefly
brought about by the development of a partition known as the septum
transversum. This so-called septum in turn is composed of three parts,
two of which have already been mentioned. The entire septum then is
made up as follows: First, there is a median mass consisting of the liver
and the sinus and ductus venosus, together with the dorsal and ventral
ligaments which unite the liver to the gut and for a time to the ventral
body wall. Second, there are the lateral mesocardia extending obliquely
in an anterior and lateral direction from the median mass to the body
walls. Above and below the lateral mesocardia, the pericardial cavity
still communicates posteriorly with the peritoneal or general body cavity. About the fifth day, however,'the ventral communication begins to
be closed. This is accomplished by the development of the third part of
the septum transversum, i.e., the lateral closing fold, extending from
the mesocardia to the ventro-lateral body wall. By the eighth day, this
closure is complete. In the meantime, the lungs have been developing in
466 THE CHICK
the portion of the peritoneal space which extends forward above the pericardial cavity. This space may be termed pleural cavity, and at this time
(fifth day) the oblique lateral mesocardia have not yet entirely separated it anteriorly from the pericardial cavity beneath it; posteriorly
also it still communicates with the general body cavity. Presently, however, with the further development of the lateral mesocardia and other
parts, the opening between the pleural and pericardial cavities is closed,
and a closure of that between the pleural and body cavities soon follows
(tenth day). This latter is effected by the pleuro-peritoneal septum,
which arises as an outgrowth from the sides of the esophagus. The median pericardial cavity is thus bounded dorsally largely by the mesocardia, laterally and ventrally by the peritoneum of the body wall, and
posteriorly chiefly by the median mass of the septum transversum.
THE ESTABLISHMENT OF THE DEFINITIVE PERlCAR—
DIUM
Eventually, however, the tissue upon the front of the median mass beu
comes thickened and splits into two sheets. The anterior sheet then becomes the posterior wall of the pericardium, the posterior sheet covers
the face of the liver, and the general body cavity extends between them.
At the same time, the latter cavity is also pushing forward beneath and
at the sides of the present pericardium, and as it does so, it apparently
splits the peritoneum of the body wall into two layers. The outer layer
forms the peritoneum of the general body cavity in this region, and the
inner layer constitutes the ventral and lateral wall of the pericardium
proper. In this manner, the final pericardial wall or definitive pericardium of the adult bird comes to surround the heart as a relatively
independent sac with a portion of the liver extending beneath it.
THE URINOGENITAL SYSTEM
THE EXCRETORY SYSTEM
The Mesonephrcs. — During the fifth day, the increase in the numher of the mesonephric tubules ceases, while the organ becomes more
active as a kidney. For a couple of days subsequent to this, however, the
tubules continue to grow in length, thus greatly increasing the bulk of
the organ. Degeneration begins about the eleventh day, and from then
on, the metanephros aids in performing the excretory functions which it
later entirely takes over.
FIFTH DAY: THE EXCRETORY SYSTEM 467
The Metanephros. ——
At the end of the fourth
day, the diverticulum
(ureterl from the posterior end of the W/olfiian
duct had just appeared,
and the nephrogenous tissue immediately behind
the mesonephros had degenerated. During the fifth
day, the above diverticulum, accompanied by the
nephrogenous tissue posterior to the region of
degeneration, grows forward somewhat, and begins to branch dichotomously ( Fig. 240, representing a slightly later
stage). Its position in this
region is adjacent to the
posterior cardinal vein,
upon the median side of
the latter and above the
Wolllian duct. The accompanying nephrogenous tissue lies. in turn, adjacent
to ‘the median side of the
diverticulum, so that the
latter, i.e., the diverticulum, lies between the vein
and the tissue. The nephrogenous tissue, which
is in immediate contact
with the diverticulum and
its branches, is called the
inner zone. Lastly this inner zone is covered on its
median sidelby a layer of
dense mesenchyme which
Fig. 240.——Profile reconstruction of the Wolffian duct and primordium of the metanephrns of
a Chick embryo of 6 days and 8 hours. From
Lillie (Development of the Chick). After Schrei~
ner.
XXV to XXXUI, thetwemy-fifth to thirty-third
somites. ALN. The neck of the allantois. CI. The
cloaca. Int. The intestine. M’s’n. The mesonephros.
71.7‘. The nephrogenous tissue of the metanephros
included within the dotted lines. W.D. The Wolffian duct. Ur. The ureter.
468 THE CHIGK
differentiates in advance of the growing nephrogenous element and diverticulum. It is called the outer zone (Fig. 241).
During subsequent days, the posterior end of the mesonephric duct
bearing the rnetanephric diverticulum (ureter) is drawn into the cloaca,
and thus the ureter acquires an opening separate from that of the mesonephros (Fig. 24-0}; The other end of the rnetanephric duct, with its
’ inner and outer zones,
meanwhile, grows still
further forward till it
reaches the region of the
mesonephros, and then
continues on dorsal to
that organ, nearly to its
anterior extremity. The
inner zone of this tissue
everywhere gives rise to
the secreting tubules and
glorneruli of the permanent kidney in a manner
very similar to that dethe scribed for the mesoneplr
ros. These tubules then
Fig. 241.—Transverse section through ‘
ureter and metanephrogenous tissue of a live
tziygdghick. From Lillie (Dez1elopmen.t of the Connect with the diCh0tO_
A.umb. Umbilical artery. Coal. Coclom. M’s’t.
Mesentery. n.(..i.z. Inner zone of the nephrogenous tissue. n.!.o.z. Outer zone of the nephrogenous tissue. Ur. UI‘€'l€!‘. V .c.p. Posterior cardinal vein. W13. Wolflian duct.
mous branches of the
metanephric duct, which
thus function as collecting
tubules, while the duct itself becomes the ureter of the adult. Eventually the outer zone helps
to form a connective tissue covering for the entire organ.
THE REPRODUCTIVE SYSTEM
The Gonads in the Male. ——~ During the fourth day, it is impossible
to distinguish sex. Occasionally on the fifth day, but more generally
and definitely on the sixth, the distinction becomes possible by the fact
that in the female the left gonad is slightly larger than the right.
This is apparently due to the fact that the right gonad usually possesses
relatively little cortex, and fewer germ cells. These latter facts according to Witschi (’35) are correlated. The left gonad in the female possesses more cortex because of the female chromosomal complex and the
excess cortex this worker thinks acts as an inductor to attract more germ
LY’).
FIFTH DAY: THE REPRODUCTIVE SYSTEM 469
cells. Be this as it may, in the male, which is to be considered first, there
is virtually no difference between the gonads, and therefore the description of one will suffice for both.
It has been indicated in the introductory discussion of germ cells in
general that the primordial germ cells of the Chick are said to be first
Fig. 242.—Section through the gonad of a Chick, the middle
of the fifth day, showing the sexual cords growing inward from
the germinal epithelium. The connections of many of the cords
with the epithelium have been cut across. From Kellicott (Chordate Derelopnzent). After Semen.
g. Germinal epithelium. m. Epithelium of the mesentery (peritoneum). o. Primordial germ cells. 5. Sexual cords. t. Connective-tissue stroma.
discernible well outside the embryo. Indeed, according to Swift (’l4)
and Goldsmith (’28, ’35), these cells are first found at the primitive
streak stage in the zone of junction lateral to the proanmion. From
here they are carried by the blood stream to the vicinity of the germinal
epithelium, whence by amoeboid movements they enter this epithelium
during the fourth and fifth days.
More recently, so far as the representatives of these cells which actually reach the germinal epithelium are concerned, their initial transfer
by means of the blood stream has been denied (Stanley and Witschi,
’40). These authors admit that primordial germ cells are indeed found
470 THE CHICK
I
l
l
l
l
Fig. 243. —-Cross-section through the genital primordium of Limosa aegocephalzz.
From Lillie (Development of the Chick). After I-ioffxnann, from Felix and Buhler.
The stage is about similar to that of a Chick embryo of 4; days, and shows the rote
cords extending from the Malpighian tubules to the germinal epithelium. The lat
ter appears in the figure as a dark mass on the right ventral side of the nn:soneph
ros next to the mesentery. Three primordial germ cells (light colored) are visible
in it. ;
Germ. Germinal epithelium. Ms.t. Mesentery. S.C. Rete cord. V. Posterior cardi-
nal vein. W.D. Wolflian duct. j
in the blood in early stages, but claim that they are only cast offs, never
destined to enter the gonads. According to them all movement of such
cells really on their way to the germinal epithelium is by passive shifting accompanying growth and rearrangement of parts, and later by
active migration as indicated? Be this as it may, by the fifth day the germinal epithelium with the primordial germ cells in it is being drawn
~" It must be further noted that according to Firket (’20) and others all, or most, ‘
of these so-called primordial germ cells in the Chick, as in the Albino Rat, ulti-
mately degenerate and are replaced by definitive germ cells derived from the germinal epithelium itself. ‘
FIFTH DAY: THE REPRODUCTIVE SYSTEM 471
Fig. 244. —Cross-section through the periphery of the testis of a just
hatched Chick. From Lillie (Development of the Chick). After Semen.
The sexual cords have acquired a lumen, and the walls of the canals
thus formed are lined within by the spermatogonia. Next to the latter
come a layer of supporting or Sertoli cells. The connective tissue
(stroma) lying between the sexual cords (now seminiferous tubules‘!
connects at the periphery of the testis with the special layer of connective tissue (albuginea) which covers the entire organ beneath the thin
outermost layer of coelomic epithelium.
Alb. Albuginea. c.T. Connective tissue of the stroma, or septulae
testis. Ep. Remains of the germinal epithelium now forming the outermost or serous covering of the testis. L Lumen of the sexual cords. pr.o.
Spermatogonia. s.C. Sexual cord, lined by supporting cells and spermatogoma.
somewhat on to the ventro-median surface of the mesonephros. Meanwhile from the capsules of the Malpighian bodies of that organ, strands
of cells begin to grow out through the loose mesenchyme to the germinal
epithelium. These strands are the rete cords, and are destined to form
the vasa eflerentia which help to connect the future tubules of the testis
with the vas deferens (see below). At about this period also the germinal epithelium begins to send processes inward among the mesenchyme
cells and the rete cords. These new strands of tissue of epithelial origin
are the sexual cards, which contain primordial germ cells (Figs. 24-2,
243) . Up to this point the condition of the male gonad is virtually iden472 THE CHICK
tical with that of the female. From now on, however, the former begins
to be differentiated to form the adult testis in the following manner:
The sexual cords become separated from the epithelium, and increase
in number so as to constitute the bulk of the organ (seventh day) , while
the rete cords are pressed to the side nearest the mesonephros. Presently also (eleventh day) the mesenchyme, which has been scanty, begins to increase among the sexual cords, forming the connective tissue
or stroma. Eventually it gives rise further to a layer, the albuginea, lying between these cords and the reduced sheet of epithelium which remains as the outer covering of the gonad. Meanwhile the sexual cords
themselves (twentieth day) begin to acquire a lumen, and are thus
transformed into the seminiferous tubules. The walls of the latter are
composed of supporting cells which are lined internally by the multiplying primordial germ cells. The latter may now be termed spermatogonia, from which arise in turn the sperrnatocytes and sperm (Fig.
244) . It is to be noted in this connection that the spermatogonia, unlike
the oiigonia in the Bird, continue to divide throughout the sexual life of
the individual. The ends of the seminiferous tubules eventually become
connected with the rete cords which, as indicated above, become tlt:
vasa efferentia. These in turn connect with the modified mesonephric tuhules in the anterior or sexual half of that organ, which thus becomes
the epididymis. The posterior and non-sexual portion of the mesonephros which remains becomes a vestige known as the paradidymis.
The Gonads in the Female. —Although differences in sex may be
indicated by the disparity in the size of the gonads as early as the fifth
day, there is little else to distinguish male from female at this time.
The description of the testes up to this point will, therefore, suffice
also for the ovaries. The right and left ovary, however, are different in
the Bird, and this difference appears at an early stage.
ln.the left ovary, following; the sixth day, a secondary set of sexual
cords, the ovigeraus cords, grow inward from the germinal epithelium,
and again carry primordial germ cells. The new cords press the original or
primary cords into the medullary region, and the germinal cells in the latter cords degenerate. In the right’ ovary no such secondary growth occurs,
and under normal conditions the primary cords develop only slightly,
the whole structure remaining rudimentary unless artificially stimulated
by injected male hormone to form a testis. In the left ovary, however,
the secondary or ovigerous cords soon break up into nests, each containing at least one germ, surrounded by remaining epithelial cells which
form its follicle. From this point on, the young egg cell begins to grow,
FIFTH DAY: THE REPRODUCTIVE SYSTEM 473
and it may, therefore, be termed an oiicyte (Fifi. 245) . This growth period is reached earlier by some ova than by others, but the oogonial or
multiplication stage ceases for all about the time of hatching. The anterior portion of the mesonephros, which in the male forms the epicli(ly
Fig. 245. -Cross-section of the ovary of a fledgling of Numenius arouatus 3-4 days old. The germinal epithelium is below. From Lillie (1)0velopment of the Chick). After Hoflmann. Note numerous oiicytes surrounded by a single layer of follicle cells.
s.c. Sexual cords degenerating. Germ. Ep. Gerrninal epithelium pruducing ovigerous cords.
mis, remains as a minute rudiment, the epoophoron. The paradidymis of
the male is sometimes evident in the hen as a still smaller vestige, the
pa/'o6p/Loron.
The Gonoducts in the Male. — It has already been stated that in
the male, the Wolffian ducts become the vasa deferentia or sperm ducts
of the adult. They connect with the testes through the vasa eflerentia and
epididymis. Late in ‘development, they become muscular and somewhat
convoluted, with a dilation at their posterior extremities.
474 I THE CHICK
The Gonoducts in.the Female. —— As has been stated, the oviduct:
begin development on the fourth day as the tubal ridges, one on the lat
eral side of each mesonephros adjacent to the respective Wolfiian duct
During the fifth day, a groove-like invagination develops along the an
mttz
   
Fig. 246.——Trans\ erse section through the metanephros, rnesonephros, gonads and
neighboring parts of an 8-day Chick. From Lillie (Development of the Chick).
A0. Aorta. bl.v. Blood vessels. BJ7. Body-wall. Coel. Coelom. COLT. Collecting
tubule of the mesonephros. col.T.M’t’n. Collecting tubules of the metanephros.
Glam. Glomerulus. Gon.l. Left gonad. Gon..r. Right gonad. M.D. Miillerian duct.
M’s’t. Mesentery. n.t.i.z. Inner zone of nephrogenous tissue (metanephric). n.t.o.z.
Outer zone of the nephrogenous tissue. Symp.Gn. Sympathetic ganglion of the
twenty-first spinal ganglion. V.C. Centrum of vertebra. V.s’c.l. Left subcardinal
vein. W.D. Wolfiian duct.
terior portion of each ridge, and the lips of the groove fuse with one
another to make a tube open at its anterior end. This tube which is quite
short, then grows backward independently between the remaining tissue of the ridge and the Wolfiian duct (Fig. 24.6) .
Subsequent development is as follows: By the eighth day each duct
has reached the cloaca, but does not open into it. At this time, there begins the atrophy of both ducts in the male and of the right duct in the
FIFTH DAY: THE ADRENALS - 475
female, accompanied in both sexes by the disappearance of the remains
of the tubal ridges. The left duct in the female, however, gradually enlarges and dillerentiates the infundibulum and glandular portions charaeteristi(- of the adult. It does not, however, effect. an entrance into the
cloaca until the hen is about six months old (Lillie alter Casserl. It always remains attachetl to the body wall and the rudiments of the meso
'nephros by a ligament or mesentery-like fold.
THE ADRENALS
During the fifth day, the cortical substarree, noted as arising on the
fourth day, increases in amount, and cornea into relation with the Malpighian capsules. On the sixth day it begins to be zirrzmged in definite
cords. \'\'l'tlC‘.ll during subsequent days increase in size and number. while
at the same time innervation of the organ begins. On the eighth day
this mass of cords is becoming penetrated by blood sinuses and by the
medullary material previously l!tLll(‘al€d. Within the latter, “ chromaffine ” cells are being differentiated, and eventually this medullary material also acquires a cord-like arrangement.
HATCHING
lt will be recalled that originally the embryo was orientated with its
long axis transverse to that of the shell. and with the head away from
the observer when the large end of the shell is to the obser\‘er’s left. Between the fifth and ninth days the position of the embryo varies considerably, and changes from time to time due to active contractions of the
amnion. By the tenth day, however, a normal embryo agrain assumes the
original position relative to the shell. But at this stage it is nearer to
the large end of the latter, and lies with its back against the yolk-sac in
‘ stead of either its ventral parts or its side. In this position of course its
legs are pressed against the shell. Next, aided by contractions of the amnion, the ‘yolk-sac is moved first toward the small end of the shell, and
then up over the ventral side of the embryo. This movement is usually
completed by the thirteenth or fourteenth day. During the next three or
four days the yolk-sac moves on over the ventral side of the embryo
until the now partially emptied and flabby sac occupies the large end of
the shell. As this is occurring the embryo by means of vigorous wriggling turns itself so that when the process is completed its tail is at the
small end of the shell, i.e., the long axis of the embryo and shell have
476 THE CHICK
now become parallel. According to the schedule indicated this condition is finally achieved on the seventeenth or eighteenth day.‘ The next
step involves the piercing of the egg membrane by the beak so that
breathing of air from the air chamber can begin. Some respiratory
movements may occur, however, even before this, there being by this
time small amounts of air in other parts of the egg. As respiration starts
the amnion and allantois dry up and become detached, while movements of the abdomen draw the remains of the yolk-sac within the body.
At the same time the necessary circulatory changes are occurring within
the embryo as already described. About the last hour before hatching
on the twenty-first day the Chick starts a vigorous counter clock-wise
rotation within the shell aided by strong thrusting movements of the
legs. Presently as a result of the thrusting of the legs and the stretching
of the neck the shell is broken into two parts and the Chick is hatched.
The foregoing description of later positional changes and hatching is
taken from the detailed account by Kuo (’32). One interesting feature
which is not mentioned by this author, however, is the so-called egg
tooth. This is a sharp cone shaped point of horny material developed on
the dorsal side of the beak, and is said by other writers to function in
chipping the shell. At all events it is a transitory structure lost soon
after hatching.
SUMMARY or THE CONDlT!ON AT THE END or THE
FIFTH DAY or INCUBATION C
I. THE EXTERNAL APPEARANCE
The cervical flexure has reached its rnaicimum development, the third
visceral cleft has closed, and the future neck is slightly indicated. The
limb buds are beginning to appear jointed. The nasal apertures are sep
arated into internal and external nares and the beak and mandible are
just startingto form.
II. THE FEATHERS
A depression develops in the skin. At its bottom a slight outgrowth
arises consisting of_a core of mesoderm, the pulp, with a covering of the
Malpighian layer and a thin outer layer of cornified epithelium. This
outgrowth is the papilla. The papilla emerges above the depression, and '
is known as the feather germ. With further growth and the throwing off
“Waters (’35) says usually not until the nineteenth or twentieth day.
FIFTH DAY: SUMMARY 4??
of the cornified cells the Malpighian layer becomes folded and modified
to form the quill and barbs of a feather. Feather germs appear in the
Chick on about the eighth day.
III. THE SKELETON
The definitive or vertebral segmentation of the mesencliymal slzeatlz,
about the notochord and nerve cord has become more marked, while all
the sclerotomal tissue is becoming membranous. These membranous condensations are especially evident in certain regions, representing parts
of the future vertebrae neural arches and costal processes. Mesenchymal
concentrations representing the limb bones and the parts of the pectoral
and pelvic girdles are also visible. The various parts of the primordial
cartilaginous cranium and visceral skeleton. are discernible at this time
as concentrations of mesenchyme about the head
IV. THE ALIMENTARY TRACT
The Fore-gut Region.———The third visceral cleft closes, the lung
rudiments have grown posteriorly somewhat through a mass of developing mesoderm, and faint indications of the abclomirzal and cervical air
sacs may be present. The glottis is partly closed.
The esophagus has continued to elongate, the stomach is slightly dilated, and a pouch representing the rudiment of the gizzard has appeared in connection with it. The duodenal loop is barely defined. The
liver has continued to branch, and some of the branches have acquired
lumens. The three pancreatic diverticula have also branched somewhat.
The Mid-Gut Region. The end of the duodenum is marked by a
ventral bend, the duodeno-jejurzal flexnre. From here the midgut or
small intestine descends to connect with the yolk-sac, and passes dorsally
again to its posterior end, marked by rudiments of the intestinal caecae.
The Hind—gut Region. —-The hind-gut or rectuniis not materially
altered, but the laterally compressed walls of the posterior part of the
cloaca have become fused.
V. THE CIRCULATORY SYSTEM
The Heart.———The alterations in the relative positions of the parts
are nearly completed, as are also the septa within the heart. The septum
of the truncus arteriosus has formed and that of the ‘bulbus has started
to develop.
The Arteries. —-— The portions of the dorsal aortae between the third
and fourth arches have begun to disappear, and the left fourth arch has
478 » THE CHICK
also diminished in size. The subclavian, arteries have become connected
with the carotids and the anterior mesenteric and coeliac arteries are
developed.
The Veins. —-—The right side of the second venous ring about the intestine has disappeared, so that in this region there is only a single vitelline trunk. Within the liver, the capillaries of the ductus venosus are
continuing to develop, while the main channel is atrophying. The mesenteric vein has started to form.
The subcardinals have lost their original direct connections with the
posterior cardinals, and have developed new ones through capillaries
within each mesonephros. At the same time the subcardinals have ‘fused.
with one another anteriorly, and by means of the previous connection
with the vena cava inferior, have thus established a renal portal system. The subclavian veins have started to develop from the posterior
cardinals.
VI. THE BODY CAVITIES
The ventral communication between the pericardial and peritoneal
cavities has begun to he closed by the development of the lateral closing
folds beneath the lateral mesocarzlia.
VII. THE NERVOUS SYSTEM
In connection with the description of this system in the preceding
chapter, it was noted that there are few important developments occurring in it on the fifth day. The following events, however, may be mentioned as having taken place during this period.,The fourth cranial
nerves have originated, and in connection with the ear the rudiments of
the semicircular canals have appeared. In the eye the mesenchymal
part of the pecten. is increasing, while the lips of the choroid fissure are
beginning to overgrow it.
VIII. THE URINOGENITAL SYSTEM
The Excfetory System. —— The mesonephric tubules have ceased to
increase in number, but are continuing to grow in length as the organ
becomes more active. The metanephric diverticulum, accompanied by its
nephrogenous tissues or inner zone, has grown forward and begun to
branch, while about the latter the outer zone is developing from mesonchyme.
The Genital System.——The primordial germ cells have begun-to
pass into the germinal epithelium and the rete and sexual cords have
9 REFERENCES TO LITERATURE » 479
started to develop. The male and female gonads are similar except for
occasional differences in size between the right and left organs in the
female. In both sexes, the oviducts are present as small tubes growing
toward the cloaca.
IX. THE ADRENALS
The cortical substance of the adrenals increases in amount, and comes
into relation with the Malpighian capsules.
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480 THE CHECK
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482 THE CHICK
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of the Chalaza in the Hen's Egg,” Poultry Science, XX, 1941.
Scott, H. M. and Warren, D. C., “Influence of Ovulation Rate on the Tendency of
the Fowl to Produce Eggs in Clutches.” Poultry Science, XV, 1936.
Spratt, N.‘T., “ Location of Organ Specific Regions and Their Relationship to the
Development of the Primitive Streak in the Early Chick Blastoderm,” Jour.
Exp. Za6l., LXXXIX, 194-2.—-“ Formation of the Primitive Streak in the Explanted Chick Blastoderm Marked with Carbon Particles,” four. Exp. Zo6l.,
CIII, 1946.—“ Regression and Shortening of the Primitive Streak in the
Explanted Chick Blastoderm," Jour. Exp. Zo5l., CIV, 1947.
Stanley, A. J. and Witschi, E., “ Germ Cell Migration in Relation to Asymmetry in
the Sex Glands of Hawks,” Anat. Rec., LXXVI, 1940.
Swift, C. H., “Origin and Early History of the Primordial Germ Cells in the
Chick,” Am. Jaur. Anat., XV, 1914.
Verdun, M. P., “ Sur les dérivés branchiaux du Poulet,” C. R. Soc. Biol. Paris, V,
1898.
Warren, D. C. and Scott, H. M., “Influence of Light on Ovulation in the Fowl,”
. Jour. Exp. Zob'l., LXXIV, 1936.
Waters, N. F., “ Changes in the Position of Chick Embryos after the Eighteenth
Day of Incubation,” Science, LXXXII, July 19th, 1935.
Wetzel, R., “ Untersuchungen am Hiihnchen. Die Entwickelung des Keims wfihrend
der erste beiden Bruttage,” Arch. Entw.-meck., CXIX, 1929.
Whitehead, W. H., “ A Working Model of the Crossing Caval Blobd Streams in the
Fetal Right Atrium,” Anat. Rec., LXXXII, 1942.
Williams, L. W., “ The Somites of the Chick,” Am. Jour. Amzt., XI, 1910.
Willier, B. H., “ A Study of the Origin and Differentiation of the Suprarenal Gland
in the Chick Embryo by Chorio-Allantoic Grafting,” Physiol. Zo6l., III, 1930.
-——, and Rawles, M. E., “Developmental Relations of the Heart and Liver in
Chorio-Allantoic Grafts of Whole Chick Blastoderms," Anat. Rec., XLVIII,
‘ 1931.
Windle W. F. and Becker, R. F., “The Course of the Blood through the Fetal
Heart. An Experimental Study in the Cat and Guinea Pig," Anat. Rec.,
LXXVII, 194-0.
Winiwarter, H. de, “ Origine et Développement du Ganglion Carotidien. Appendice:
Participation dc Phypoblaste 5. la Constitution des Ganglions Craniens," Arch.
Biol., L, 1939.
Witschi, E., “ Origin of Asymmetry in the Reproductive System of Birds,” Am.
Jour. Anat., LVI, 1935.
Woodside, G. L., “The Influence of the Host Age on Induction in the Chick
Blastoderm," Jour. Exp. Zoo'l., LXXV, 1937.
, Young, R. T., “ Origin of the Notochord in Chordates,” Anat. Rec., XXV. 1923.
i Yntema, C. L., “ Experiments on the Origin of the Sensory Ganglia of the Facial
Nerve in the Chick,” Jam’. Comp. Neur., LXXXI, 1944. * ‘
Zwilling, E., “Regulation in the Chick Allantois,” Jour. Exp. Zo5l., C1, 1946.
i””""’
E
APPENDIX TO CHICK BIBLIOGRAPHY
Brizaee, K. R., “ Histogenesis of the supporting tissue in the spinal and the sympathetic trunk ganglia in the chick,” Jour. Comp. Neur., XCI, 1949.
Cairns, J. ‘M., “ The influence of embryonic mesoderm on the regional specification
of epidermal derivatives of the chick,” Jour. Exp. Zo6l., CXXVII, 1954-.
Coughlin, F. E., Jr. and Walker, R., “Ductus arteriosi and their closure in the
chick,” Anat. Rec. Absts, CXVII, 1953.
Fraser, R. C., “ Studies on the hypoblast of the young chick embryo,” Jour. Exp.
Zob'l., CXXVI, 1954.
Gaertner, R. A., “ Development of the posterior trunk and tail of the chick embryo,”
four. Exp. Zo5l., CXI, I949.
Hamburger, V. and Hamilton, H. L., “ A series of normal stages in the development
of the chick embryo,” Jour. Morph., LXXXVIII, 1951.
Hammond, W. S., “ Origin of the thymus in the chick embryo,” Jour. Morph., XCV,
1954-.
Levi-Montalcini, R. and Amprino, R., “ Recherches experimentales sur l’origin du
ganglion ciliaire dans l’embryon de poulet,” Arch. de Biol., LVIII, 194-7.
Levi-Montalcini, R., “The origin and development of the visceral system in the
spinal cord of the chick embryo,” Jour. Morph., LXXXVI, 1950.
McKeehan, M. S., “A quantitative study of self differentiation of transplanted lens
primordia in the chick,” Jour. Exp. Zob'l., CXXVI, 1954.
Olsen, M. W. and Fraps, R. M. “ Maturation changes in the hen’s ovum," Jour. Exp.
Zob'l., CXIV, 1950.
Randles, C. A., Jr. and liomanolf, A. L., “ Some physical aspects of the amnion and
allantois of the developing chick embryo,” Jour. Exp. Zo6l., CXVI, 1950.
Straus, W. L., Jr. and Rawles, M. E., “ An experimental study of the origin of the
trunk musculature and ribs in the chick,” Am. Jaur. Anat., XCII, 1953.
— Waterson, R. L., Fowler, I. and Fowler, B. 1., “The role of the neural tube and
notochord in development of the axial skeleton of the chick,” Am. Jour. Anat.,
XCV, 1954-.
Yntema, C. L. and Hammond, W. S., “The origin of intrinsic ganglia of trunk
viscera from vagal neural crest in the chick embryo,” Jour. Comp. Neur., CI,
1954.-~ “ Experiments on the origin and development of the sacral autonomic
nerves in the chick embryo,” four. Exp. Zo6l., CXXIX, 1955.
PART V
L
A
M
M
A
M
E
H
T
’|-4
HE EARLY DEVELOPMENT OF THE MAMMAL AND
ITS EMBRYONIC APPENDAGES
INTRODUCTION
IN taking up the development of the Mammal in a book of this
type, intended primarily for college undergraduates, the writer faces a
dilemma in the choice of material. For those interested chiefly in Zoology the comparative aspects of early stages in several selected Mammals, suggesting as they do evolutionary trends, are highly significant.
On the other hand for those mainly intent upon the study of medicine
the emphasis of interest is likely to be different. Such students, and
many of their teachers, though willing to admit that the study of early
comparative mammalian development is of some value, feel that for
practical purposes they must begin to concentrate. Hence they prefer to
consider chiefly the embryology, both early and later, of a single form.
Preferably this would be Man, but since that is usually not practical,
the next best thing is to select for study some readily available Mammal whose history is nearly akin to that of Man. That Mammal is generally the Pig. If space allowed, there is of course no reason why both
these lines could not be followed in considerable detail. Unfortunately,
however, in a book already dealing at some length with the Frog and
Chick, space does not permit an extensive treatment of both topics. Consequently the following compromise way of treating the Mammals becomes necessary.
To begin with, it will be found desirable as in previous cases to go
back of the start of the embryo itself, and consider somewhat the reproductive organs of the adults. This will be especially necessary in the
mammalian females because of the special relation of certain of their
organs to the reproductive process and to the developing young.
We shall then proceed with the comparisons of the early embryos of
selected orders of Mammals with special emphasis upon the develop* INTRODUCTION 487
ment and character of their extra-embryonic membranes and structures.
This special emphasis is pertinent because we shall find that these membranes and organs are fundamentally similar to those already familiar
in the Chick, and found in all Sauropsids, i.e., Birds and Reptiles. They
are of present interest because of the manner in which both their origin
and structure has been modified in the different mammalian groups to
serve essentially their old functions. The modifications have resulted
from the different environment in which the embryo and fetus of the
Mammal occurs, and from the very special relations with the mother
which this environment makes necessary. That there should be similarities in these structures as between the Mammals and the Sauropsids is
of course natural in view of the known derivation of the Mammals from
the Reptiles. The modifications in the mammalian orders selected then
help to suggest the lines along which evolution has perhaps moved
within that class.
Having thus compared the early stages of certain representative mammalian fonns, we shall finally concentrate upon one of them, i.e., the
development of the Pig. The Pig, however, is an Ungulate, and the
Ungulates are one of the groups whose earliest stages and extra-embryonic membranes have been chosen for comparative study. In this latter
study, moreover, the Pig will be especially emphasized as an example
of the group. Hence when we come to the detailed consideration of this
animal it will not be necessary to start quite at the beginning. We shall
simply pick up where the comparative account left olf.
Lastly, another device by which we shall endeavor to save space and
time is the following: In the embryology of the Frog and Chick we
have already twice gone over in some detail the development of all the
main vertebrate systems. In the Chick, moreover, the processes in many
cases are, as has already been suggested, very similar indeed to those
found in the Mammal. Hence in the Pig we shall not repeat again in detail the development of each system. Instead we shall outline such development rather briefly, emphasizing only those points in which the
process or structure in this animal significantly difiers from that in the
Chick. Such treatment will of course be accompanied by as many illustrations as possible. This should be sufiicient, and will be so if the student of the Pig has reasonably well in mind the corresponding situations in the Chick. Anyone who does not have the Chick development
clearly in mind will find it necessary to refresh the memory by reference back to the appropriate account in that form.
488 EARLY MAMMALIAN DEVELOPMENT
THE ‘REPRODUCTIVE ORGANS OF THE ADULT
, THE MALE
The Testes and Their Ducts. —— In the adult male Mammal there
are normally two testes. These organs may be retained permanently
within the body of the animal, as in the case of the Elephant; more commonly, however, they pass out of the body during development, and are
contained either in two sacs, or in two chambers of a single one, the
scrotal sac or scrotum. This is the case in the Pig. In some cases, however, as among Rodents, an intermediate condition occurs in which the
testes descend into the scrotum only during intervals of sexual activity.
Each testis consists of the usual seminiferous tubules, embedded in connective tissue and leading by way of vasa eilerentia to the respective
vas deferens.
Accessory Organs.—— ln the Mammal there are, in addition to the
testes and other parts just noted, certain accessory organs connected with
the more distal parts of the genital tract. These are the prostate glands,
Cowper’s glands, and, in some animals (e.g., in the Pig and in Man).
the seminal vesicles. The function of the glands is to furnish a suitable
medium for the existence of the sperm after it leaves the organs of the
male. The vesicles presumably assist both in the secretion of additional
fluids and in storing the combined" sexual products or semen previous
to its ejaculation. Finally, there is in the male Mammal a penis. This
has a single duct, the urethra, which serves to discharge urine, and also
to introduce the semen into the genital tract of the female.
_ THE FEMALE
The Ovary.——In the female Mammal there is a single pair of
ovaries, and, as in the other forms studied, these organs are contained
within the body cavity and suspended from its wall by a mesovarium.
The ovaries are whitish ovoid objects, varying in size in different animals, but always relatively small. Thus in the Human Being, for example, each ovary is about 3-4 cm. long, and from 2-3 cm. wide, and they
are about the same in the Pig. Fundamentally, their internal structure is
similar to that already described in the Bird.
The Genital Tract.
The 0viducts.—As in the Bird, the ovaries are not directly connected with the Miillerian ducts or oviducts. The latter, sometimes
OOGENESIS" 439
known as the Fallopian tubes, are, however, provided as usual with a
typical fimbriated funnel, or infur.-dibulum, which serves to embrace the
ovary when an ovum is discharged. The walls of the oviducts are made
up as follows: On the outside is the serous membrane, next to that a
layer of more or less mingled longitudinal and circular muscles, then
a sheet of vascular connective tissue covered by ciliated epithelium. the
connective tissue with its epithelium being known as the mucous layer.
From each infundibulum the respective duct proceeds to join the one
from the opposite side. Between the infundibulum and the point of
junction, however, there is usually more or less bending, and in many
cases the duct actually starts anteriorly before curving backward and
medially to unite with its fellow.
The Uterus and Vagina. —— At some point distal to the infundibula ei
ther above or below the region of junction, or in some cases both above
and below, the character of the tract or tracts changes. The muscular
wall becomes thicker as does also the mucous layer which now contains
lymph spaces and many glands. The part or‘ parts of the genital tract
thus characterized are then known as the uterus or uteri, and the thick»
ened mucous layer plus its epithelium are referred to together as the
uterine endometrium. When these changes occur entirely proximal to
the point of union of the tubes so that there are two distinct uteri (Rodents) the condition is-known as uterus duplex. On the other hand when
they occur both above and below the region of union (Carnivores and
Ungulates) the situation is described as uterus bicornis. Finally, when
the uterine character exists only in the fused part of the tract the-condition is called uterus simplex.
_ Beyond the uterus, or uteri, as the case may be, there is a single passage leading to the exterior, known as the vagina. At the external end of
the latter there are certain rudiments homologous with the penis of the
male.
THE DEVELOPMENT OF THE OVUM UP TO 5EGMENTA—
TION, AND THE SEXUAL CYCLE
OOGENESIS ,
The O6gonia.——-The embryonic ovary of the Mammal contains the
usual primordial germ cells which, as in the lower Vertebrates, have
probably migrated thither from the walls of the gut. At first these cells
lie chiefly in the outer epithelium or cortex of the ovary. According to
490 EARLY MAMMALIAN DEVELOPMENT
Fig. 247. —— Section through part of the ovary of a Dog. From Kellicott (Chordate
Development). After Waldeyer.
a. “ Germinal epithelium.” b. Ovigerous cords. c. Small ovarian follicles. :1. Older
ovarian follicle. e. Ovum surrounded and attached to wall of follicle by cells of
discus proligerus (cumulus oiiphorus), including those of the future corona radiata.
f. Second ovum in follicle with e. (Only rarely are two ova thus found in a single
follicle.) g. Outer layer of follicular capsule. h. Inner layer of follicular capsule. i.
Membrana granulosa. k. Collapsed, degenerating follicle. L Blood-vessels. In. Sections through tubes of the parovarium. y. Involuted portion of superficial epithelium. z. Transition to peritoneal epithelium.
most accounts this cortical epithelium thickens and then produces out-l
growths which push into the deeper mesenchyme. These outgrowths are
the ovigerous cords similar to those described in the Chick, hut in this
instance often called the cords of Pfliiger.1 As in the Bird, they contain
both the female germ cells, or oiigonia, and numerous epithelial cells as
1 Also according to some recent studies by Gruenwald ('42) the development
of the cords is somewhat more involved than this, and varies to some extent in different Mammals. The end result, however, is essentially as indicated.
OOGENESIS 491
well. In the Mammal, however, the two types of cells are not easily distinguishable from one another, and it is quite possible that some germ
cells may arise in situ. from indiilerent cells of Pfliiger. During this period multiplication of all the cells goes on rapidly.
At some time before the birth of the animal in which the ovary is
contained the multiplication of the oiigonia is said to cease. As has been
previously noted, however, this assertion is now seriously questioned,
some workers (E. Allen, ’23, G. I. Hargitt, ’30, and others) maintaining
that in certain cases at least the ova derived from the primordial germ
cells all, or nearly all, disappear. These are then said to be replaced by
new oiigonia arising from the peritoneal (germinal?) epithelium at intervals during the sexual life of the individual. In any event the cells are
eventually arranged in nests or groups, each of which contains a single
oogonium, the remaining epithelial cells in the group being destined to
form the fo1licle.'The young ovum now enters upon the growth period
as an oiicyte.
The Oocyte and the Graafian Follicle. —At about this time, the,
epithelial cells referred to begin to become arranged about the young
ovum to form the highly characteristic mammalian or Graafian follicle.
At first they constitute a thin flat layer only one cell thick, but soon
multiply so as to form a mass of cells about the growing oiicyte. In one
side of this mass there then appears a space, the follicular cavity, which
gradually enlarges and extends around the sides of the oiicyte. These
extensions, however, never quite meet. Thus the oiicyte, still closely surrounded by several layers of cells, is suspended within the follicular
cavity, which becomes filled by a fluid, the liquor folliculi. Meantime,
the outside of the entire follicle has become covered by a capsule (follicular capsule or theca) , formed externally of connective tissue (theca
externa) and internally of cells, blood vessels, and nerves (theca
interna).
The various layers and parts of the entire Graafian follicle may now
be named, as follows: Beginning on the outside there is the follicular
capsule (theca) with its inner and outer layer. Just within this, and
bounding the follicular cavity, there are a few layers of the follicular
cells forming the basement membrane, or membrana granulosa. Upon
the side of the ovum where the cavity has not extended, a neck of cells
reaches from this membrane to those cells which immediately surround
the oiicyte. Thus the latter is attached to the inner wall of the follicle
by this neck, which, together with the more peripheral of the cells immediately surrounding the ovum, is termed the discus proligerus or
492 EARLY MAMMALIAN DEVELOPMENT
cumulus oophorus. Those of the immediately surrounding cells which
have remained closest about the egg are now gradually elongated at
right angles to the surface of the latter. Many of these cells remain attached to this surface for a time following ovulation when they become
known as the corona radiata (Figs. 24-7, 248) . This brings us to the actual egg and its membrane.
Fig. 248.—F'ully grown Human oiicyte just removed from the
ovary. Outside the oiicyte are the clear zona pellucida and the follicular epithelium (_ corona radiate) . The perivitelline space in this
instance is not apparent. The central part of the oiicyte contains
deutoplasmic bodies and the excentric nucleus (germinal vesicle).
Superficially there is a well-marked exoplasm, or cortical layer.
From Waldeyer (Hertwig‘s Handbuch, etc.).
THE MATURE OVUM AND OVULATIONI
The Mature Ovurn. — The mature ovum in all placental Mam~
mals 2 is relatively minute, though naturally varying in size in different
animals. Thus that of the Mouse measures about .075 mm. in diameter,
'-’ It will suflice to state at this point that the term placental Mammal includes
the vast majority of the group. Its exact significance will be fully described in the
section on the yolk-sac, allantois and placenta (see below).
THE FEMALE SEXUAL CYCLE 493 A
that of the Dog about 0.14 mm., that of Man 0.135 mm., and that of the
Whale 0.14 mm. (Hartman, ’29, ’30) . The reason for this minute size is
the fact that mammalian eggs are virtually without yolk (alecithal).
They consist of a central region of opaque endoplasm surrounded by a
thin layer of exoplasm, and within the former is a relatively large nudens (germinal vesicle), somewhat excentrically placed.
The ovum apparently does not possess any true vitelline membrane.
It is surrounded, however, by a thick transparent substance which is
presumably chorionic, i.e., is secreted by the cells of the follicle. This
layer, though clear, frequently appears to be perforated by minute canals through which processes of the follicular cells reach the egg to
nourish it. It is, therefore, known either as the zona pellucida or the
zona radiata. There is usually a slight space between this zone and the
iprotoplasm of the egg, and though there may be no vitelline membrane
this space is known as the perivitelline space (Fig. 24-8) .
Ovuiation.——-As a Graafian follicle and its ovum matures, it is
gradually brought to the surface of the ovary. At the same time one side
of the follicle becomes thin in connection with the formation of a cicatrix, as in the Chick. As complete maturity is reached, the discus proligerus is broken and the ovum floats freely in the liquor folliculi. In
most animals rupture of the follicle then occurs spontaneously, and its
contents is received by the infundibulum of the oviduct. In a few forms,
e.g., the Rabbit and Cat, the breaking of the ripe follicle does not usually occur spontaneously, but only following copulation with the male
(coitus). The liberation of an ovum may or may not take place in both
ovaries at once, and there may or may not be more than one follicle
ready for discharge in the same ovary at approximately the same time.
These variations, moreover, may occur normally in the same species of
animal. In Mammals which ordinarily produce a litter of young, however, the discharge of several ova at once is of course the usual thing.
THE SEXUAL CYCLE IN THE FEMALE
lt is well known that like many other animals, Mammals are capable
of breeding only during certain periods or seasons. Among this group,
moreover, these periods are far more marked in the female than in the
male. In the former sex they are also very definitely related to the process of ovulation so that it seems desirable to discuss the subject at this
point. In all placental Mammals which have been carefully studied, it is
known that during sexual life the walls of the uterus suffer a series of
periodic changes, interrupted only by pregnancy. The placentals, more494 EARLY MAMMALIAN DEVELOPMENT
over, may be divided into two main groups with respect to these uterine
changes, i.e., the Primates and the non-Primates.
The N on—Primate Cycle. —— Among this group the stages involved
are fundamentally similar, and these stages are well represented in the
Pig‘, whose embryology will later be considered. We shall begin therefore by a description of the sexual cycle in the female of this animal. In
the sow each sexual or oestrus cycle, as it is called, occupies twentyone days and in the absence of pregnancy, the cycles are continuous
throughout the year. As regards the behavior of the animal, the activity
of the ovary, and the condition of the uterine endometrium, the periods
or phases of a cycle are characterized as-follows:
I. The Dioestrum.-—-During this period lasting about two and one
half weeks the sow occupies herself with eating and sleeping, and shows
no interest in the opposite sex. A study of her ovaries, however, shows
that within this interval an important event takes place. The empty follicles which remain from the immediately preceding ovulation become
filled with a specialized type of fatty cell. In some cases (Man) these
cells are yellow in color, which has caused each body so formed to be
known as a corpus luteum. In the Pig, however, these bodies are pinkish. They quickly develop to a maximum extent, and persist in this condition for about the first thirteen to fourteen days of the period, at
which time they begin to regress. Correlated with the time of development and persistence of the corpora lutea in the ovary, the uterine mucosa, which was already quite thick at the beginning of this period,
becomes even more hypertrophied, especially the glands. This is a con-_
dition known as pseudopregnancy, because, as we shall see, the state of
the mucosa at this time resembles to a considerable degree its character
during true pregnancy, and due to the stimulus of the same hormone,
progesterone (see below). Finally as the corpora lutea regress the uterine mucosa likewise regresses, and within two or three days has become
relatively thin (F 249, A ). Thus during the last day or so of the dioestrum there is virtually nothing going on in the uterus so that this
brief interval may be thought of as a time of more or less complete
“ rest ” for that organ.
II. The Pro-oestrum.———Following the dioestrum there is a short interval of a day or,so generally known as the pro-oestrum, within which
the behavior of the animal remains about as before. Studies of her ovaries, however, reveal that undeveloped Graafian follicles are starting a
rapid growth, while the uterine mucosa also has again begun to hypertrophy (Fig. 249, A)
THE FEMALE SEXUAL CYCLE 495
III. The Oestrus. —— This period, lasting approximately three days, is
known as the time of “ heat,” and during it the sow becomes extremely
restless and will accept mating at any time. Examination of the ovaries
shows that the Graafian follicles come to maturity at about the middle
 
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Fig. 249.—Diagrams comparing the events of the oestrus cycles of the Pig and
.Dog with those of the ovulatory and non-ovulatory menstrual cycle in Man. The
line vertical rulings in the cycle of the Dog and in those of Man indicate the time
of occurrence and the approximate relative degree of bleeding in each case. There
is no normal obvious bleeding in the Pig. The rise and fall of the curved lines
indicates the relative degree of hypertrophy or degeneration of the tissues or
bodies designated.
of this period, and at that point ovulation occurs. The corpora lutea, already referred to, immediately start development which, in the absence
of pregnancy, continues into the succeeding dioestruxp as already described. The hypertrophy of the mucosa, well under way at the end of
the pro-oestrum, also continues on through oestrus and into the succeeding dioestrum, during most of which periods it remains at a high level
as indicated (Fig. 249, A) .
496 EARLY MAMMALIAN DEVELOPMENT
Variations in the Non-Primate _Cyc1e.—-The non-Primate cycle
as thus described for the Pig may be considered typical for the nonPrimate group of animals so far as its fundamental aspects are concerned. As already suggested, however, there are numerous variations in
detail, some of the more striking of which will now be noted. Probably
the most outstanding is that which occurs in animals like the Dog and
Cat. In these animals there are only two or three oestrus periods a year,
with a long inactive interval, known as an anoestrum between each period of “ heat.” In such cases the corpora lutea, and the uterine hypertrophy in the absence of pregnancy, only persist for a relatively short
time, the uterine mucosa being comparatively thin during most of the
long anoestrum. Breeding of course can only occur during the oestrus
periods which are hence referred to as the breeding seasons. The Dog
and Cow are further peculiar in that at the end of the pro-oestrum the
blood vessels of the hypertrophied mucosa are so gorged that some superficial bleeding occurs. This quirk‘ led to much discussion and misapprehension of the relations between the non-Primate and Primate cycles as we shall presently see. Another peculiarity of a few animals such
as the Cat and also the Rabbit, as already noted, is the fact that ovulation in these forms is not spontaneous during oestrus, even though the
mature ova are present. It only occurs at this time if copulation, or some
form of stimulation which simulates copulation, takes place. Otherwise
the ripe follicles simply degenerate, no corpora lutea are formed, and
hence no pseudopregnancy occurs (see below).
Not only do animals vary as between those with a succession of relatively short dioestrus cycles like the Pig, and those with long anoestrus
intervals like the Dog (Fig. 249, B), but in the latter type some forms
have several short dioestrus cycles between each anoestrum. That is
they have a breeding season perhaps once a year like some sheep, and
during that season they come into “ heat ” several times. Animals with
only one oestrus period at a breeding season are said to be monoestrus,
while those with several at each season, or with continuous short cycles,
are polyoeszrus. Lastly the length of the dioestrus cycles varies greatly
among different anmials. Thus, while it is twenty-one days in the Pig, it
is only five days in the Rat and Mouse, and fifteen in the Guinea-Pig. It
should be emphasized also that these are average times. There is commonly some variation in cycle length even in the same individual, depending upon temperature, food and other unknown conditions.
The Primate Cyc1e.——-In discussing this group it should at once
he pointed out that the peculiarities about to be described do not actuTHE FEMALE SEXUAL CYCLE ‘ 497
any apply to all Primates, e.g., to Lemurs and to the New World Monkeys. They do, however, apply to the Anthropoid Apes, the Old World
Monkeys and to Man. ‘The most complete studies have been made on
Man and Rhesus, an Old World Monkey, and we shall therefore consider the situation particularly as it applies to these forms, and first especially as it applies to Man.
The Menstrual Cycle. — The peculiar characteristic of the sex cycle
as it occurs in the Human female is the inclusion within it of the phenomenon of menstruation, from which the whole cycle takes its name.
The nature of this phenomenon, and its relation to the parts of the nonPrimate cycle, in so far as it can at present be related to them, is as
follows:
Keeping the Pig in mind as presenting a typical example of the situation in the non-Primates, we find that the first but least important
difierence between that animal and Man is in the length of the entire
cycle. Thus in the Pig, as just noted, it is about twenty-one days, while
in both Women and the Rhesus monkey it is normally twenty-eight days,
with numerous more or less minor variations. Proceeding next to a com
parison of the periods within the cycle, and starting with the one in Man
presumably homologous with the dioestrum in the lower animals, we
find conditions at that stage in the Human subject about the same as in
the sow. That is to say there is no sexual urge at this time, the ovary
contains a corpus luteum, and at the beginning the uterine mucosa is
hypertrophied. This phase, comparable with the first and major (pseudopregnant) part of the dioestrum, lasts for about two weeks. At the end
of this time, as in the lower forms, the corpus luteum disappears, and
accompanying this the uterine epithelium regresses. In this instance,
however, this regression instead of being relatively quiet and uneventful,
is a rather violent affair involving a serious breakdown of the endometrium, both mucosa and epithelium. This is accompanied by a sloughing of? of cells and considerable bleeding, and it is this process which
comprises menstruation. Following this as in the Pig, comes a “ rest ”
interval, in this instance, however, lasting four to five days and involving repair of the preceding damage, though the mucosa remains relatively thin. Menstruation plus this interval would therefore correspond
to the end of the dioestrum in the Pig, except that in that animal the
process of regression is much less violent. Hence the menstrual features
are lacking, and no “ repair ” is required during the “ rest ” interval.
The next period should be that of the pro-oestrum, and apparently
‘something essentially similar to this in the lower animals exists in
P 498 EARLY MAMMALIAN DEVELOPMENT
Man. As in the former case it apparently involves no accentuation of
sex interest, the ovary contains a maturing Graafian follicle, and the
uterine mucosa begins again to hyper-trophy. This lasts five to six days.
Following the “pro-oestrum” the next period should be that of
oestrus, but this is another respect in which the Primate cycle difiers
from that of the non-Primates. There is no oestrus. This means that
there is no time in the cycle of greatly heightened sexual activity. Ovulation, which "should occur sometime during oestrus, occurs at the end of
what we are calling the “ pro-oestrum,” though the use of this and other
"terms relating to the oestrus cycle is obviously questionable in a cycle
in which there is no oestrus. This is why the Primate cycle is commonly
referred to as the menstrual cycle in correlation with its most outstanding characteristic. Following ovulation a corpus luteum of course exists, and in the absence of pregnancy a new “ dioestrum ” begins, culminating in another menstruation and “ rest” interval (Fig. 249, C).
From this account it will be evident that ovulation occurs about midway between menstruations, i.e., from the twelfth to the sixteenth day
following the beginning of the last menstrual period (Corner, "43)
From this it is clear that menstrual bleeding has nothing whatever to
do, either in relative time of occurrence, or in character, with the minor
‘bleeding of the pro-oestrum in an animal like the Dog, a phenomenon
with which it was once confused. In this connection it should he noted
that a slight pro-oestral bleeding also. occurs in the Rhesus Monkey and
occasionally in Women, in which cases -it is known as intermenstrual
bleeding or Hartman’s sign, i.e., a sign of imminent ovulation.
To summarize a comparison of the two cycles, then, we may say this:
In both there is what amounts to a “ dioestrum” during which sexual
activity is not evident. The ovary contains a corpus luteum during the
first part of this period, and during this part the uterine mucosa is hypertrophied. Near the end in both cases the mucosa regresses, but in
the Primate cycle the regression is much more thoroughgoing, and is
termed menstruation,_ Finally a short quiescent interval ensues which in
E the Primates is occupied with uterinerepair. In both cycles a “proM 5 oestrum ” follows the “ dioestrum ” involving no change in sex activity,
but the growth of a new Graafian follicle and renewed uterine hyperI trophy. In the norn-Primate cycle this is followed by oestrus or “ heat ”
1 in the midst of which ovulation occurs. In the Primate cycle ovulation
occurs at the end of what we have called, for the sake of comparison,
the “ pro-oestrum,” and there is no oestrus. Instead the “ dioestrum”
immediately follows, and the cycle is complete.
i
I
THE FEMALE SEXUAL CYCLE 499
Having thus described the oestrus and the menstrual cycles there remain the problems of their causes and functions. Much work has been
done in this connection over a long period, but it is only within recent
years that the pieces of the puzzle have begun to fall into some semblance of order. As will presently appear, however, there are even yet
some pieces which are missing.
Causes qf the Oestrus and Menstrual Cyc1es.——It is already
evident that certain events in both the oestrus and menstrual cycles are
closely correlated. Thus we have seen that when a follicle is developing
in the ovary the uterine mucosa in either cycle is undergoing its prooestral hypertrophy. As the corpora lutea form it undergoes still further
hypertrophy, and when these latter bodies start to disappear this mucosa
regresses, either with or without extensive breakdown. Why is this? The
answer is found in the fact that the developing follicle produces a hormone called oestrone (theelin) which causes the initial pro~oestral hypertrophy. It also of course causes the behavioral phenomenon of
“ heat” in most “ lower ” animals?‘ As the corpora lutea form following ovulation they also produce orie or more hormones, including some
oestrone. The most prominent of these, however, is called progesterone,
and this causes the still further uterine hypertrophy of the first part of
the dioestrum. Both these hormones are sterols, have been obtained in
pure crystalline form, and their action repeatedly demonstrated experimentally. The withdrawal of the progesterone as the corpora lutea begin
to disappear would then explain both the dioestral regression and the
menstrual breakdown of the mucosa previously built up. The follicular
and luteal hormones produced in the proper order and then withdrawn
would therefore seem to account satisfactorily and completely for both
types of cycle. This would be true were it not for one curious fact. It
was discovered (Corner, ’23) that Rhesus monkeys, and probably more
rarely Women, experience menstruation without ovulation, and hence in
the absence of corpora lutea. The monkeys, it should be noted, have a
breeding season (the winter months), and it is at the beginning and end
of this season that these so-called anovulatory cycles occur. Women of
course have no such season, and in them cycles of this character have
been thought to occur most commonly in girls beginning to menstruate.
It is now known, however, that such anovulatory cycles, Otllu ». xse apparently normal, occur in a certain percentage of women during their
active sexual life. Indeed it has been proven that such women may only
3 Just what parts of the follicle are responsible for this hormone is not alto»
gather certain, but probably either the theca interns. or the granulosa or both.
500 EARLY MAMMALIAN DEVELOPMENT
actually ovulate two or three times a year in spite of seemingly normal
menstrual periods, causing serious interference with lertility. In any
event such cycles obviously upset theforegoing neat explanation of the
entire phenomenon. Much work has been done in an effort to solve this
problem, but no completely satisfactory answer has yet been arrived at.
It is known for instance that in castrate animals an apparently normal
cycle can be produced by the injection and sudden withdrawal, after a '
suitable interval, of oestrone alone. Yet in non-castrate animals extra
doses of oestrone will not prevent the uterine breakdown. A little progestrone, however, will do so. Hence the latter substance seems clearly
to have some important part in the cycles of normal ovulating animals,
probably in the manner already described.
With these facts in mind two possible explanations of the anovulatory
cycle may be briefly noted. One, considered by many the most probable,
is that a certain amount of oestrone is necessary, first to build up, and
then to maintain, the uterine endometrium in a state of preovulatory hypertrophy. This hypertrophy is of course not quite like that produced
by progesterone, but is nevertheless considerable. The necessary oestrone for this is furnished by the partially developed follicle, which instead of going on to ovulate, persists for a time, periodically regresses,
and is replaced by another. The regression of course produces a temporary lack of oestrone, and an anovulatory endometrial breakdown very
similar to menstruation occurs (Fig. 249, D). The second possibility,
suggested by Hisaw, is that the partially developed Graafian follicle produces not only oestrone, but a little progesterone as well. Then if, in the
anovulatory cycle, the production of the progesterone for some reason,
such as the-regression of the follicle, declines, this may be enough to produce menstruation even in the absence of ovulation and the ensuing
corpus luteum. There is a little suggestive evidence for this, but it is
diflicult to prove. So much for this part of the oestral cycle and menstrual mechanism.‘ '
4 It may be added that these hormones also have several other significant’ effects
not directly pertinent to the present discussion. Thus oestrone not only starts the
hypertrophy of the mucosa in each cycle, but is necessary to bring the infantile
uterus to a stage of development where progesterone can act on it. Also it controls
the growth of the muscles of the pregnant uterus, first stimulating, and then checking, and causes corfiification of the vagina of the Guinea Pig, thus revealing its
presence in this animal. Lastly it stimulates development of the breasts to a condition where they can be acted on by the pituitary hormone, prolactin, but at the
' same time prevents milk flow until birth. Progesterone in addition to its elfect on
the uterine mucosa has a decidedly quieting action on the normal rhythmic contractions of the uterine muscles, and is said by some to cause relaxation of the pelvic,
THE FEMALE SEXUAL CYCLE‘ 501
There still remains the question as to what sets ofl" these cycles, i.e.,
what starts the follicles to developing, and what stops them. The answer
to this appears to be found in that gland-of-all-work, the pituitary. The
anterior lobe of this gland is known to produce, among other things, a
follicle stimulating hormone (F.S.H.) which causes Craafian follicles
to begin their growth. What then seems to happen is that when the
growing follicle achieves a certain output of oestrone this acts in turn
to suppress secretion by the pituitary. (There is some experimental evidence for this.) The follicle then ovulates, and its extensive oestrone
production ceases, thus allowing the pituitary secretion to rise again,
and so the cycle repeats itself.
Here again, however, a problem arises which has not been entirely
satisfactorily answered. The scheme just presented works well enough
for animals like the Pig or Man with continuous cycles, but what of
those with an anoestrum? What causes the cycles to stop? We do not
know. It has been suggested that during the anoestrum in such animals
as the Dog or Cat the secretion of the pituitary and the ovarian follicle,
exactly balance each other so that nothing happens. Perhaps so, but
< there is no proof of it. Also if this is true, what produces an unbalance.
and starts off a new cycle?
Functions of the Female Cycle. —- Thus far the oestrus and menstrual cycles have been considered without reference to the possible occurrence of pregnancy. As might be suspected, however, each cycle is in
fact an invitation to, and a preparation for, this important event. In
cases where oestrus occurs the behavior of the female is such as to permit and encourage mating at this time, and it is of course at just this
point also that a ripe egg is released into the oviduct ready to be fertilized. In the menstrual cycle the same thing is true, except that here
I there appears to be no special sexual urge at the time of ovulation. Fol’ lowing this event in either case the egg is subject to fertilization in the
upper end of the oviduct. If this occurs the egg becomes what amounts
to a blastula in a manner to be described below, and after 3-4 days finds
its way into the uterus. Here meanwhile the climax in the hypertrophy
of the uterine mucosa is coming about. It now appears that this hypertrophy is just what is needed to insure the firm attachment of the developing egg to the uterine wall by a process known as implantation. This
i
A
1
»
ligaments of the Guinea Pig. Hisaw, however, has claimed a separate luteal hor) mane, relaxm, to be responsible for this. In some cases progesterone also acts as an.
acciassory in aiding the oestrogens to prepare the breasts for final stimulation by
pro actin.
-n.7<ma.t:..a
502 EARLY MAMMALIAN DEVELOPMENT
process varies considerably in different animals, and will be discussed
at some length later on. The point to be noted at the moment is that apparently the hypertrophy of the mucosa is a necessary preparation for it.
As has been noted, if fertilization and implantation fail to occur, the
hypertrophy regresses and a new cycle is initiated, with, as M.- 3. Gilbert
so cleverly suggests in her book, Biography of the Unborn, “ hope for
better luck next time.” On the other hand, if implantation does occur,
the hypertrophy persists and in fact increases. Because of the similarity
of this hypertrophy to that of the dioestrum, the latter, as previously
noted, is frequently termed pseudopregnancy. This persistence of the
hypertrophy when it is needed, and its disappearance when it is not
needed leads to some further questions to which we have at present only
partial answers. Some of these questions and the tentative answers are
as follows: .
What for instance makes the hypertrophy of the mucosa persist in
pregnancy and not at other times? In this connection it is of interest to
find that in many animals the corpora lutea also persist throughout
pregnancy instead of disappearing as in the non pregnant cycle. Is
there a causal connection here? It would appear that in those cases
where both corpora lutea and mucosal hypertrophy persist together
there is. Thus in the Rat and the Cow removal of the corpora lutea of
pregnancy causes regression of the mucosa and abortion, though in
other cases, like that of Man, this is not true. The answer as to what
makes the hypertrophied uterine mucosa continue in the former animals
then seems to be fairly clear. It will be recalled that one of the chief
hormones of the corpus luteum is progesterone. This hormone, however,
was so named because of the very fact that it maintains an ‘hypertrophied
condition of the mucosa not only during most of the dioestrum, but especially during pregnancy. Thus the corpora lutea apparently rather obviously persist during pregnancy in these cases in order to secrete the
progesterone which maintains this condition. There is also, as noted, evidence that the corpora lutea produce some oestrone, or something
closely akin to it. This and the progesterone appear to assist in causing
the hypertrophy of the muscles of the uterus as well as that of the mu~
cosa during pregnancy.
The next question is, how do the corpora lutea know, so to speak,
when to persist and when not to? The answer to this appears to be that
the organ which attaches the embryo to the uterine wall, termed the
placenta, itself secretes several hormones, one of which is luteinizing, i.e.,
helps to keep the corpus luteum developed. There is also a pituitary horTHE FEMALE SEXUAL CYCLE 503
nlone which has a luteinizing efi'ect, but this is apparently not the one
chiefly involved during pregnancy. _As just suggested the placenta pro
" duces other hormones, i.e., oestrogens (oestrone like hormones), and also
quite definitely progesterone. This source of these substances, it is now
generally agreed, soon becomes the main one in cases like Man where
the corpus luteum functions for only about the first four months of pregnancy, being operatively removable after the first few weeks without
harm.
Also, in Man at least, certain other gonad stimulating hormones, similar in action to the F.S.H. of the pituitary, are produced by the placenta.
They are called Prolan A and B, and are used in the Aschheim-Zondek or
Friedman tests for pregnancy. Thus so much of these hormones is produced under this condition, even within the first month, that they are
excreted in the urine. Advantage is taken of this fact to make a test for
their presence, and hence for pregnancy, by injecting a specified amount
of the suspected urine into a female rabbit (Friedman test). If the hormones are present they will cause the animal to ovulate within ten
hours.5 The particular tissue of the placenta from which these various
sterol substances appear to be derived in Man and Monkeys is a special
material called trophoblast to be described below (Wislocki and Bennett, ’43; Baker, Hook and Severinghaus, ’4-4) .
Finally, in this connection, what if any function has menstruation as
such? It would indeed be comforting to be able to assign it one, but to
date no adequate explanation for this excessive breakdown of the uterine
endometrium exists. It seems to be merely an overenthusiastic expression in some Primates of the regression following luteal hypertrophy
and withdrawal which occurs in a more restrained manner in other more
humble Mammals.
Parturition. —This is a process which might naturally be considered at the conclusion of development rather than here. However, possible dependence upon the hormonal substances which we have been discussing makes this an appropriate point to mention the factors which
may be involved. As a matter of fact there is not a great deal to say, because comparatively little is really known as to just what factors are
actually concerned in this phenomenon. It may be that among others a
- reduction of progesterone, which quiets uterine contraction, and an in
crease in oestrogens, which are known to stimulate it: play a part. This,
5 Another peculiar effect of these hormones is to cause the release ‘at sperm
from the testes of the Frog when so-called pregnancy urine is injected into a lymph
sac of one of these animals. This fact furnishes another pregnancy test which
promises to be of value ( Miller and Wiltberger, ’48).
504 EARLY MAMMALIAN DEVELOPMENT
however, is only a guess, and according to Corner many other elements
such as the balance of still other hormones, the rate of blood flow
through the placenta, the state of nutrition in the fetus, and probably
various other conditions are concerned. Indeed some have claimed that
the mere size and weight of its tenant finally irritates the uterus into
initiating the contractions of labor. Some evidence for this latter notion
is perhaps furnished by certain cases in the Cat studied by Markee and
Hinsey (’35) . In an abnormal situation in this animal one horn of the
uterus contained embryos differing considerably in age from those in
the other, a condition known as superfetation. In this case the born with
the older fetuses delivered itself thirteen days ahead of the other, the
normal full term in this animal being from sixty-three to sixty-five days.
This would thus seem to indicate that the conditions responsible for delivery are not entirely hormonal, and hence general, but are at least
partly quite local. These investigators also showed that thickness of
endometrium and muscle depends on the number and weight of fetuses
present in the horn in question. This again emphasizes the effect of local
factors on conditions which may "affect delivery. In concluding this
topic it is pertinent to note the normal term of gestation in the animal
we are about to consider in some detail, i.e., the Pig. As usual this period varies slightly with breed and other factors, the range being from
112-115 days, or just under four months (Asdell, ’46) .
THE SEXUAL CYCLE IN THE MALE
As regards the male among Mammals, it is found that here also there
is a tendency toward cycles of sexual activity. This phenomenon, however, is not so common as among the females, or among the males of
lower forms. In thosespecies of Mammals in which the male does experience special periods of heightened sexual desire, however, these normally coincide with the breeding season of the female, and are known
as the rutting periods. At such times the males may develop very special
secondary sexual characters, such as the antlers of the buck deer, as
well as great irritability and desire for combat with other males. On the
other hand, the males of many Mammals have no such special periods
of sex activity. Instead, they are apparently able to breed at any time,
even though the females of their kind will only receive them at certain
seasons.
With this understanding concerning the nature of the sexual cycle and
its relation to ovulation and sexual activity, we are now prepared to
return to the history of the ovum.’
MATURATION AND F ERTILIZATION 505
MATURATION AND FERTILIZATION
Although in Mammals the first maturation division often occurs before ovulation and fertilization, the second, with apparently only a few
exceptions (e.g., the Mole, Rabbit, and probably Man) occurs after
Fig. 250.——Reconstruction of four sections through the fertilized
ovum of the Cat. From Longley (combined from two figures). No
zona pellucida is visible in these sections. The corona radiata is
disintegrating.
s. Remains of second polar spindle. I. First polar body. II. Second polar hody. o”. Sperm nucleus. 9 . Egg nucleus.
ward. Hence it has seemed best to mention both divisions in connection
with the latter phenomenon.
The First Maturation Division.—At some time during the
growth of the oocyte, the preliminary stages of maturation are completed without any peculiarity of note. The first polar, spindle is then
formed, and usually a short time before ovulation the first polar body
is given off. In the latter connection the only feature to be noted as pe
‘culiar to Mammalsis the fact that this polar body is normally relatively
large, i_.e., often as much as one fourth the diameter of the ovum itself,
506 EARLY MAMMALIAN DEVELOPMENT
and in abnormal cases sometimes equal to .the latter. The fate of these
exceptionally large bodies is not known. After the extrusion of the first
polar body, the spindle for the second is formed and moves into position for division. The completion of the process may then take place in
the ovary (e.g., in the Mole and Rabbit) or it may be inhibited while
ovulation and fertilization occur.
Fertilization. —— Sperm introduced into the vagina of the Mammal
rapidly make their way into the uterus and up the oviducts. A few hours
0
Fig. 251. — Cleavage of the ovum of the Rabbit. From Kellioott (Chordate Development). After Assheton. A. Two-cell stage, 24- hours after coitus, showing the two
polar bodies separated. B. Four-cell stage, 25% hours after coitus. C. Eight-cell
stage.
a. Albumenous layer derived from the wall of the oviduct. z. Zona radiata.
or even less suiiices for them to reach the upper ends of these ducts
where the actual process of fertilization usually takes place.
Considerable work has been done on the rate and method of progress
of the sperm up the oviducts of different animals. Thus Parker (’31)
showed that in the Rabbit the sperm are transported up, both by contractions of the tube and by cilia, despite the fact that the latter beat in
an abovaxian direction. By contractions the tube is divided into small
compartments, and as soon as sperm get into the first of these they are
spread throughout it by ciliary currents which move down the walls and
up the middle of the compartment. Then the location of the contractions
shifts, and new compartments are formed. Sperm do of course swim, but
as just suggested, this auto-motility is not the only, or even the main
factor, involved in getting them to the upper end of the oviduct. In the
Sheep, Schott (’4l) found the sperm to reach the upper ends of the ducts
in about twenty minutes, and to travel at the rate of 4- cm. (40 mm.) per
minute. He does not, however, state that they swim at that rate. Phillips
and Andrews (’37) claim an average swimming speed in vitro of only
4.83 mm. per minute over a distance equal to the length of the ewe’:
MATURATION AND FERTILI7ATION 507
genital tract, though they do much better at first. In the ewe, however,
they travel, according to these authors, by swimming or otherwise, at a
rate of at least 12.4 mm. per minute. In the Rat, Blandau and Money
(’44.} say that in twenty-six out of thirty cases sperm reached the infundibulum in forty-five minutes. They do not say just how, but Rossman (’37) suggests a peristaltic activity of the uterus as responsible for
mnvement through that region. In this connection Asdell (’46) also
notes that contractions of the uterus probably aid in the transport of
the sperm, but gives the “ average” time required to reach the infundibulum “in all animals studied ” as about four hours. This, it will be
noted, is considerably longer than any of the times indicated above, and
he does not say what animals were involved. This author further states
that none of the first few sperm to reach an egg fertilize it, but they do
secrete an enzyme, hyaluronidase, which disperses the cells of the corona radiata, thus making the egg accessible to one of the sperm which
follow. He states that about one million sperm at an insemination are
necessary to insure fertilization by the one sperm required per egg
This is obviously only a rough estimate, since the kinds of animals, and
the numbers of eggs are not given.
Most recently some interesting data have been acquired concerning
these matters in relation to Man. These data were presented at the Washington meeting of the American Society of Zoologists (’-48) by Dr.
E. J. Farris under the title, “ Motile Spermatozoa as an Index of Fertility in Man,” and the results are ‘quoted with the author’s permission. According to this investigator Human sperm swim in vitro at the rate of
3 mm. per minute, a rate not so different for one of those claimed for
the Sheep. This author admits, however, that other factors, such as those
indicated above, are also active in the movement of the sperm in the fe«’
male genital tract, and claims that actually they reach the ovum at the
upper end in about an hour. This is much better than the “ average time
in all animals studied ” given by Asdell. Farris also notes that at least
130 million motile sperm per c.c. of semen, and preferably more, are
necessary to insure fertilization. ‘
Aside from such studies there are others indicating the time which
sperm retain their fertilizing capacity. In the Rat, Soderwall and Blandau (’41) say it is at the most fourteen hours, and that it falls off considerably after ten hours. In the Guinea Pig, on the other hand, Soderwall and Young (’4«O) place the maximum time at twenty-two hours,
while in Man, Farris places it at twelve hours, even though the sperm
may remain motile much longer than this. An extreme survivaltime is
508 EARLY MAMMALIAN DEVELOPMENT
found in the Bat where insemination occurs in the fall, and the sperm
apparently survive and retain fertilizing capacity in the hibernating females all winter (Wimsatt, ’44) . '
The functional survival of the egg previous to fertilization has also
been studied, ‘though not so extensively as in the case of the sperm. It is
said, however, to be able to retain its fertilizability for ten hours in the
future inner cell mass
   
 
«. _‘ ' A
future trophoblast
Inner cell mass
Fig. 252.—Semi-diagrammatic sections through stages of
early cleavage, blastula tblastocystt and early gastrula of the
Pig. After Heuser and Streeter. A. Early cleavage. B, C and D
formation of biastocyst with inner cell mass. E. S:art of epihlast and hypohlast differentiation (gastrnlation), probably by
delamination. or possibly some infiltration. of cells from the
inner cell mass. Trophoblast, often first called subzonal layer.
Rat (Blandau and Jordan, ’41), and for twenty hours in the Guinea Pig
(Blandau and Young, ’39) .
From these data it will be evident that even though ovulation may
not occur so that an egg is present at the moment sperm reach the upper end of the oviduct there is still good opportunity for fertilization to
occur there over a reasonable period. When a viable sperm does reach
an egg it malies its way through any remaining cells of the corona radiata and through the zona pellucida which still cover it. Usually only
one actually enters the egg, presumably due to mechanisms similar to
those previously described. In many cases, only the head and middle
piece of the sperm enter, but in others (Mouse), the entire spermatozoon is taken in; when this does occur, however, the tail soon degenerates. The head of the sperm next forms the sperm nucleus (male pronucleus) in the usual manner.
SEGMENTATION 509
The Second Maturation Division. — If this has not already been
completed its completion occurs following the entrance of the sperm
and while the nucleus of the latter is forming; it results in a second
polar body, usually smaller than the first. This division is soon followed
by the union of the sperm and egg nuclei, and the process of fertilization
is complete (Fig. 250).
SEGMENTATION, GASTRULATION, AMNION FORMATION, AND THE PRIMITIVE STREAK
SEGMENTATI ON
The Type of Cleavage. — Segmentation in the placental Mammals
is total, as might be expected from the virtual absence of yolk. The arrangement and behavior of the cells, however, is quite different from
that observed in the first yolkless form which was studied, i.e., Amphioxus. The reason for this is apparently due to the fact that the egg of a
Mammal is almost certainly only secondarily without yolk. The evidence
for this assumption will become more and more obvious in the course of
this chapter, but a couple of the more striking proofs may be indicated
here. Thus as will appear, the embryos of the primitive non-placental
Mammals known as Monotremes possess both yolk-sac and yolk, while
all the placental Mammals retain the sac, though it is empty. Secondly,
there are the origin of the embryo from what amounts to a blastoderm.
the method of gastrulation, and other features all characteristics of
large-yolked forms. We may now proceed to the actual method of segmentation. _
The Blastocyst.——Cleavage, though total, is irregular from the
start (Fig. 251) . The result is the formation of a spherical mass of cells
known as the morula in which the cells are of two types. On the outside
they are at first cubical, but soon assume the form of a flattened epithelium, which being covered temporarily by the zona radiata is called
the subzonal layer, later the trophoblast. The cells on the inside, on the
other hand, are spherical and are called the inner cell mass. Presently,
vacuoles appear on one side of this mass, beneath it and the subzonal
layer. These run together and increase until more than half of the
morula is occupied by a fluid-filled cavity. On the other side, the inner
mass hangs from the wall like a suspended drop (Fig. 252). The morula
has now become a ‘blastodermic vesicle or bldstocyst, which corresponds
in a general way to the blastula of lower forms. Hence the cavity may
510 EARLY MAMMALIAN DEVELOPMENT
be termed the blastocoel or subgerminal cavity, while the fluid within it
occupies the place of the yolk. Finally, as subsequent development
shows, the inner cell mass lying above the fluid virtually plays the part
of a blastoderm (Fig. 253).
Cleavage occurs while the ovum is passing down the oviduct, and in
some instances it may even have reached the blastocyst condition by "the
time it arrives in the uterus. The time required for this passage varies
‘ much in different animals, but is
ordinarily considerable, e.g., about
four days in the Rabbit, and eight
or ten days in the Dog. The movement down the duct is apparently
accomplished mainly by peristaltic
action, though in the Rabbit,
Parker claims that the cilia heating in-an abovarian direction are
involved.
Within the uterus the cleaving
egg, or morula, soon becomes a
blastocyst, if it is not already one,
and this begins to enlarge through
Fig. 253.—-Section through the fully
formed blastodermic vesicle of the Rabbit,’ From Quain’s Anatomy, after Van
Beneden.
f.c.m. Granular cells of the inner cell
mass. troph. Trophoblast. zp. Zona pellucida.
the multiplication and flattening
of the cells of the subzonal layer
(Fig. 253). There is considerable
variation in the size and shape
_ which is reached in this manner.
Thus in the Rabbit, the vesicle after three days in the uterus becomes
ovoidal, measuring about 4.5 x 3.5 mm. In Ungulates, on the other
hand, it becomes very long and tapering, that of a nine day Pig measuring about 8am. in length and .5 mm. in diameter, while in a day or two
more the length has reached about a meter, and the diameter a few millimeters. In all cases, however, the inner cell mass remains very small,
and in instances where the vesicle is elongated, as in the Pig or Sheep,
the mass is attached about midway between its ends (Fig. 254) .
' .< GASTRULQTION
As in the other forms studied, this term is here used to denote the formation of an archenteric cavity, and the setting aside of epiblast and
kypoblast. In most Mammals the latter appears to arise either by a splitting off (delamination) of cells from the ventral side of the inner cell
GASTRULATION 511
Fig. 254.——Photographs of Pig blastocyst by Heuser and
Streeter showing the transition from an oval to an elongated
form. In group A the long axis of the smallest specimen was
approximately 7.5 mm., while in the largest it was about 13.8
mm. In group B the magnification is less so that the smallest
specimen on the extreme left actually measured about 15 mm. in
length, and the greatly elongated specimen at the top of the
group measured about 150 mm.
mass, or by an infiltration of cells from this area. It will be recalled
that both these possibilities are identical with some of those recently suggested as occurring in the origin of the primordial hypoblast of the
Chick. At all events the cells so ‘produced then multiply and spread
around the inside of the vesicle until in many forms they eventually
completely line» it, just ‘as they line the archenteron ‘and yolk-sac of
the Bird. This extension of the hypoblast and later mesoderm around
the inside of the blastocyst is of course essentially epibolic, though the
overgrowth covers only a cavity. The cavity so lined constitutes the
archenteron, while part of it presently becomes the yolk-sac in a man512 EARLY MAMMALIAN DEVELOPMENT
Fig. 255.—Sections through four stages in the early development of
the lnsectivore Tupaia jauanica. From Hubrecht. A. Blastodermic
vesicle completely closed; hypoblast still continuous with the embryonic epiblast. B, C. Embryonic epiblast split and folding out upon the
surface of the vesicle, pushing away the trophoblast cells. D. Embry> oniclepiblast forming a Hat disc on the surface of the blastodermic
‘. vesic e.
E. Inner cells mass, now embryonic knob. ec. Embryonic epiblast. en.
Hypohlast. tr. Trophoblast.
ner to be indicated, despite the absence of yolk. Thus the situation differs from that found in previous forms, and particularly in the Bird, as
follows: In the latter case the original archenteron consisted only of a
shallow space between the hypoblastic roof and the underlying yolk.
i The central region of the roof, later augmented by mesoderm, then
folded off to form the gut, while the borders grew out and around the
yolk to form the sac. In most Mammals, on the other hand, there is of
IMPLANTATION i513
course no yolk at all, so that the cavity of the blastocoel beneath the
hypoblast may all, at first, be called archenteron. Later on the hypoblastic roof of this cavity now accompanied by mesoderm, and hence
termed endoderm, folds of? as in the Bird to form a gut. Meanwhile the
remainder of the cavity may or may not have become completely lined
with endoderm. In the Guinea Pig for example only the roof is ever so
constituted. In any event the part of this cavity not eventually occupied
by the allantois, amnion and extra-embryonic coelom becomes the yolksac, with or without a ventral wall. In many cases, as in the Rabbit,
Cat and Pig, this sac is fairly extensive, especially at first. In others,
like most Primates, it is very insignificant. Certain special details and
peculiarities of. these extra-embryonic structures will be considered later.
Meanwhile it is to be noted that with the origin of the hypoblast the remainder of the inner cell mass together with the original subzonal layer
may now be termed the epiblast. This epiblast is then further divided
into that which composes the inner cell mass proper, now termed the
embryonic knob, and that which composes the subzonal layer, now
termed the trophoblast. It is to be noted that the latter completely encloses, for a time at least, the embryonic knob and the yolk-sac. Hence
though originating differently, it occupies the same position as the chorionic ectoderm of the Chick (Fig. 255, A). In fact, with the mesoderm
which in some cases later comes to line it, this layer constitutes the
clwrion of the Mammal.
It is to be clearly understood that the process of gastrulation which
has just been described is entirely one of delamination or infiltration,
and proliferation; there is apparently no involution, invagination, nor
epiboly, and hence also no concrescence. Consequently, it is not surprising that there is no well marked blastopore, at least in connection
with the actual process of hypoblast formation. Later, as in the Chick, a
primitive streak arises as a thickening in the epiblast, and again as in
the Bird, parts of this streak are interpreted by many as the homologue
of a blastopore. This will be discussed further when the origin of the
primitive streak is described.
IMPLANTATION
By the time the stage described above has been reached, and some
' times somewhat earlier, the blastocyst has become attached to the uter
ine wall. This process is known as implantation, and there are several
methods by which it is brought about. It will be best, however, to postpone their detailed discussion until the description of the placenta is
514 EARLY MAMMALIAN DEVELOPMENT
taken up. Sufiice it to say at this point that it is brought about largely by
the activity of the trophoblast, aided by certain changes in the uterine
wall itself.
THE AMNION
There are two chief methods by which the amnion is formed in the
Mammal: ‘
I. The First Method of Amnion Formation.——-This method
may be defined briefly as the method of amnion formation by folds. The
Fig. 256.-—Formation of the amnion in the Rabbit (Lepus). From Jenkinson
(Vertebrate Embryology). After Assheton.
i.m. Inner cell. mass. Ll. Lower layer (i.e., hypoblast) . e.p. Embryonic plate (i.e..
blastoderxnal epiblast). R. Cells of Rauber. tr. Trophoblast.
first step in this method involves the transformation of the epiblast of
the embryonic knob into a flattened plate overlying the hypoblast, the
two layers being virtually homologous with the similar ones of the avian
blastoderm. This flattening is accomplished, however, by two different
processes. Thus though subsequent development of the amnion itself is
similar, it is convenient upon the basis of the above differences in the
initial stages to describe Method I under two headings, Type (a) and
Type (b). «
Method 1, Type (a) .-—-This type is illustrated by one of the Insectivores, T upaia (Fig. 255) ; in this animal a depression appears in the top
of the embrvonic knob, and extends well down into it. The bottom of the
depression then rises to the surface, and the edges are at the same time
pushed apart. As this occurs the trophoblast cells above are broken and
scattered. Thus the epiblastic plate of the blastoderm so formed comes to
lie directly on the surface of the blastocyst.
THE AMNION 515
Fig. 257.—DiEerentiation of the early Pig blastoderm.
After Heuser and Streeter. A, B and C are from blastocysts
measuring .6 mm. in diameter, and show clear differentiation
of the inner cell mass (chiefly epiblast), and a thin layer of
hypoblast, the whole being covered by a layer of trophoblast.
D measured .8 mm., but does not show the hypoblast. The
trophoblast over the inner cell mass is scattered, only two
cells (cells of Rauber) remaining. '
‘ Method I, Type (b). —-— In this type, of which the Rabbit or the Pig
form equally good examples (Figs. 256, 257), the process‘ is simpler,
for here the knob merely flattens without the occurrence of any previous depression. In such cases after the flattening is completed, scattered
trophoblast cells may remain for a time over the blastoderm, and are
known as the cells of Rauber; these, however, soon disappeux.
Subsequent Stages of Method 1, Types (a) and (b). —— As. suggested
above it will now appear that the later stages of types (a)" and (b) are
virtually alike. Before they are described, however, it should be noted
that during or soon after the above processes, mesoderm has been proliferated between the epiblast and the underlying hypoblast in a man516
EARLY MAMMALIAN DEVELOPMENT
Fig. 258.—Diagrams of the formation of the embryonic membranes and appendages in the Rabbit. From Kellicott (Chardate
Development). After Van Beneden and Julin (partly after Marshall). Sagittal sections. A. At the end of the ninth day, after
coitus. B. Early the tenth day. C. At the end of the tenth day.
Ectoclerm black; endoderm dotted; mesoderm gray.
al. Allantois. as. Allantoic stalk. b. Tail-bud. c. Heart. d. Allantoidean trophoderm (see page 543). e. Endoderm. ex. Exocoelom. f. Fore-gut. h. Hind-gut. m. Mesoderm. N. Central nervous system. p. Pericardial cavity. pa. Proamnion. s. Marginal
sinus (sinus terminalis). t. Trophoblast. ta. Tail fold of amnion.
v. Trophodermal villi. vb. Trophoblastic villi. y. Cavity of yolksac. ys. Yolk-stalk.
THE AMNION 517
ner to be described below. The two first layers may henceforth therefore
be referred to as ectoderm and endoderm. Moreover, there has arisen
within this mesoderm the usual coelomic split, separating it into the
somatic and splanchnic layers. In either type (a) or (b), the amnion is
then formed by folds of ectoderm and somatic mesoderm, which arise
about the rim of the flattened embryonic knob (i.e., the blastodermal
-ectoderm), in essentially the same manner as in the Chick (Fig. 258).
Thus as the amnion is completed by the meeting of the folds at the seroamniotir: connection, the chorion is at the same time re-established above
it. This portion of re-established chorion now consists as usual therefore
not only of an outer layer of ectoderm, but also of an inner layer of
somatic mesoderm. Between the latter and the somatic mesoderm of the
amnion is of course the extra-embryonic coelom.
There are, however, certain minor points of difference to be noted
between the case of the Bird and that of the placental Mammal. In the
first place there is the origin of the chorionic ectoderm. In the Bird this
arises entirely from ectoderm of the extra-embryonic blastoderm which
has grown out over the yolk. In the Mammal, on the other hand, since
the folds arise just at the border between blastodermal ectoderm (embryonic knob) and trophoblast, a large portion of the ectoderm in the
folds, i.e., that of the outer layer, seems to be formed from the latter
substance. Thus_while the lining of the amnion may be chiefly blastedermal, the ectodermal part of the chorion which covers it is apparently
entirely of trophoblast, a tissue which seems to have no real homologue
in the Bird. A second but rather less important diflerence between Bird
and Mammal is the fact that in the latter the tail fold often appears
earlier than the head fold, and is therefore the longer of the two. In the
Pig, on the other hand, head and tail folds are virtually equal, and are
continuous with the lateral folds which arise coincidentally (Fig. 300).
II. The Second Method of Amnion Formation.-—In the second method of amnion formation, the trophoblast above the embryonic
knob is never interrupted, a condition known as entypy. In contrast to
Method I, the amniotic cavity then arises merely as a space within the
embryonic knob or in connection with the knob and the trophoblast
above it. Here again, however, there are variations in the process, so
that it may best be described under the headings, Type “(a) , Type (12) ,
and Type (c). '
Method II, Type (a).——This type is illustrated by the Hedgehog
(Erinaceus, Fig. 259) in which the rudimentary amniotic cavity appears,
not in the knob itself, but as a space between the center of its dorsal side
518 EARLY MAMMALIAN DEVELOPMENT
and the trophoblast. The edges of the knob, however, remain adherent
to the trophoblast, and these edges now turn and grow toward one another between the trophoblast and the cavity. Thus when they meet and
fuse, the epiblastic (future ectodermal) layer of the amnion is completed. Later, the extra-embryonic coelom lined by mesoderm forces its
way in between the trophoblast (now chorionic ectoderm) and the epiblast, now ectoderm, of the amnion, so that in this manner the latter receives its mesodermal covering and the former its mesodermal lining. It
am.c.
C.
Fig. 259. -—Formation of the amnion in the Hedgehog (Erinaceus) . From Jenkinson (Vertebrate Embryology) . After Hubrecht. A. Early. B. Later stage.
am. Amnion. c. Extra-embryonic coelom. ec. Ectoderm. e.k. Embryonic knob.
l. Lacuna. m. Mesoderrn. n. Notochord. tr. Trophoblast. y.s. Yolk-sac.
may be noted that the type of amnion formation thus exemplified by the
Hedgehog is quite similar in many respects to that just described under
Method I, and may, therefore, represent a transitional stage between
Methods I and II. Later, as the embryo develops, the edges of the flat
blastoderm are folded downward in the usual manner, and portions of
the mesodermal layers are of course involved in this process. The layer
lying next to the endoderm is then splanchnic mesoderm, and the one
next to the ectoderm (either trophoblastic or embryonic) is somati;
mesoderm.
Method II, Type (b). — The second type of Method II is typically illustrated in the development of the Guinea Pig (Cavia), in which the
process is as follows: _
Shortly after gastrulation is completed, the embryonic knob becomes
separated from the trophoblast above it, and moves down near the opposite side of the blastocyst.‘’ In so doing, it pushes the central portion
5 In this case and that of the Mouse and Rat the blastocyst, presumably be
cause of its shape, has been termed by some the “egg cylinder,” though it is of
course neither an egg nor a cylinder.
THE AMNION ‘ 519
of the hypoblast layer before it; the edges of this central portion, nevertheless, remain attached to the dorsal trophohlast. This process presently results in the production of a clear space between the knob and
the trophoblast, bounded on its sides by the upstretching hypoblast. A
cavity now develops in the middle of the embryonic knob; this is the
rudiment of the amniotic cavity (Fig. 260, A, B). On the floor of this
cavity, the cells remain columnar, and are homologous with the upper
Fig. 260.—Fo1-mation of the amnion in the Guinea Pig (Cauia).
From Jenkinson (Vertebrate Embryology). After Selenka. A. Early.
B. Later. C. Latest stage.
a.tr. Allantoidesn trophoderm. o.tr. Omphaloidean trophohlast (see
page 543) . l. Lacuna. e.k_. Embryonic knob. am.c. Amniotic cavity. y.s.
Yo1k~sac hypoblast in A and B, endoderm in C.
or epiblastic layer of the embryonic portion of the blastoderm in previous forms. The cells of the roof and sides, on the other hand, soon flatten and form the epiblastic layer of the amnion. The latter now begins
to expand, filling the space above it (Fig. 260, C). In the meantime mesoderm begins to arise between the epiblast of the hlastoderm ‘and the
hypoblast beneath it. Thus the former becomes ectoderm and the latter
endoderrn, while within the mesoderm the coelomic split occurs, producing two layers. These layers then spread out upon either side, the
lower layer extending over the endoderm as the splanchnic mesoderm,
and the upper layer extending up over the ectoderm of the amnion as
the somatic mesoderm. The amnion is now completely formed, and consists, as in previous cases, of an" outer layer of mesoderm and an inner
one of ectoderm. Further development merely involves an increase in
size and a gradual folding in about the embryo to form thenumbilical
stalk.
Fig. 261.—Formation of the amnion in the Mouse (Mus). From Jenkinson. ( Vertebrate Embryology). A.—E. Successiye stages. am. Amnion. am.c. Amniotic cavity. a.tr. Allantoidean nophoderm. c. Extra-embryonic coelom. e.k. Embryonic knob. l. Lacuna. l.l. Lower layer, L6.
hypoblast. m. Mesoderm. m.g. Medullary groove. n. Notochord. a.tr. Omphaloidean trophoblast. py. dy. Proximal or upper, and distal or
lower walls of yolk-sac. tr. Trophoblast. tr.c. Temporary trophoblastic or false amniotic cavity. y.s. Yolk-sac.
THE AMNION 521
In anticipation of the method which is next to be described under
type (c), however, it may finally be added that besides the amniotic
cavity thus formed, there has also arisen a cavity in the dorsal trophoblast from which the knob was separated. This second space is often referred to as the false amniotic cavity, but in the type under discussion it
never has any connection with the true cavity. It presently disappears
and has no further significance.
Method 11 Type (c).—This last type of amnion formation is well
shown in the Mouse (Mus, Fig. 261). In this form the embryonic knob
moves down as in the Guinea Pig, pushing the endoderm before it, but
does not become separated from the trophoblast. Instead, the latter simply thickens, thus filling up the space which would otherwise result. A
cavity now appears in the upper part of the knob, and at once comes into
communication with a cavity in the lower part of the thickened trophoblast, i.e., the false amniotic cavity. The mesoderm next arises between
the hypoblast, now endoderm, and the epiblast, now ectoderm, of the
knob, whence it spreads upward between the endoderrn and the thickened trophoblast. Within this mesoderm the coelomic split next develops
upon either side, and the two coelomic spaces then press toward each
other and finally unite. In this manner the mass of ectoderm and trophoblast, including the cavity, is cut in two in approximately the region
where the ectodermal and trophoblastic elements were in contact. This
process is such as to leave one closed cavity in the trophoblast and
another closed cavity in the embryonic knob, with the extra-embryonic
coelom lined by mesoderm between them. The cavity in the knob is,
of course, the amniotic cavity with its usual layers, while the one in
the trophoblast is the false cavity already referred to. The latter. it will
be noted, is in no wise different from its homologue in type (b), except
that in this case it temporarily communicates with the true cavity. Later,
as in the former case, it disappears.
The Inversion of the Germ Layers. —— Before passing on to a discussion of the relative primitiveness of Methods I and ll, it is worth
while to note a peculiar misconception which arose in the minds of early
students of forms like Cavia and Mus. These are cases, it will be recalled, where the embryonic knob moves far down into the blastocyst.
The obvious result is that the endoderm extends well up on either side,
considerably above the level of the blastoderrn. Hence, if in examining
the blastocyst of such a form, the investigator overlooked the outer layer
of trophoblast, the first layer he would come to would be endoderm. He
would thus get the impression that in some mysterious manner the endo-“rm
522 EARLY MAMMALIAN DEVELOPMENT
derm had gotten on the outside of the blastocyst. This oversight was exactly what occurred, and the phenomenon was, therefore, referred to as
an “inversion of the germ layers.” As a matter of fact, it is now clear
that no such inversion really exists, and hence the phrase is of only historical interest.
 
beginning
primitive streak P”'“m"° 3'9"‘
substance
   
Fig. 262.—Graphic reconstructions of the Pig hlastoderm in the prestreak and early streak stages. After Streeter. A. Pre-streak stage. B.
Early primitive streak, showing beginning mesoblast formation. C and
D. Later stages in primitive streak development with greater extension
of the mesoblast. As in the Chick, the mesoblast can be seen spreading
out from the sides of the streak.
The Relative Primitiveness of Methods I and II. ——There has
been some discussion as to which of these two main methods of amnion
formation is the more primitive among placental Mammals, one view —
that of Hubrecht— being strongly in favor of Method II. The reasons
. for this attitude are based chiefly upon the characteristics of the mam
malian chorion indicated in connection with Method I, and are as follows: In the Bird or Reptile (i.e., the Sauropsids) , there is, as suggested,
no chorion (the layer corresponding in relative position to the mammalian trophoblast) until it is formed by the outer walls of the amniotic
folds. In all the Mammals whose early development is known, on the
~‘ other hand, the blastocyst is entirely enclosed in trophoblast, or chtfiifi
[, onic epiblast, before any amnion has been formed, either by folds or
...~..._.,_..m.. . . .,._.—...._t,...__.......,._t_
THE AMNION 523
otherwise. It is true that in those cases where the process of folding occurs (e.g., in the Rabbit), the original trophoblastic chorion above the
embryo virtually disappears, and the new one in this region is formed
from the outer walls of the folds. Nevertheless, even in these cases there
is no denying that there was a trophoblastic chorion previous to the
C
Fig. 263.--Later primitive streak and mesoblast formation in the Pig. After
Streeter.
folding, and further that most of the (chorionic) portion of the folds is
still really trophohlastic. Hence, as indicated above, it is said that the
original trophoblastic chorion of Mammals cannot be regarded as homologous with the layer of the same name in the Sauropsids. From this
statement it then follows, according to proponents, of this idea, that the
cases of the formation of the mammalian amnion and chorion by folds
could not have been derived from this process in the Reptiles; it must
rather represent a reversion to the reptilian condition, or else a piece of
independent evolution.
524 EARLY MAMMALIAN DEVELOPMENT
Fig. 264.——Surface view of two stages of the Pig blastoderm with parts of the
adjacent blaslocyst. After Streeter. A. Primitive groove stage, length of blastederm about 1 mm. B. Blastoderm showing primitive groove and also beginning
neural groove. length 1.7 mm. Crest of chorio-amniotic fold shows around margin
of blastoderm.
H.n. Hensen’s node (knot). N.gr. Neural groove. P.gr. Primitive groove.
There are, however, many zoologists who do not subscribe to the theory just presented. Instead they regard Method I as the more primitive,
for the following reasons: In the first place it is known that Mammals as
a class sprang from Reptiles, in which group the method of amnion formation is by folds as in the Birds. Furthermore, among those Mammals
which are in other respects most primitive, i.e., the Monotremes and
Marsupials, the formation of the amnion by folds (according to the evidence of those stages which are known in these animals) in all probability prevails. Lastly, as admitted by the opponents of the view now being
presented, the trophoblastic ‘chorion of the Mammal is not really homologous with the true chorion of the Bird; it is rather a secondary developTHE PRIMITIVE S'l‘REAK 525
ment, whose early and complete enclosure of the blastocyst is made possible by the absence of yolk. Consequently, though the trophoblast
usually takes a large part in the formation of the mammalian chorion,
it has not, contrary to the
argument stated in the foregoing paragraph, necessarily anything to do with the
formation of the amnion.
Indeed, as has been seen,
the latter frequently forms
by’ folds in spite of the
presence of the precocious 3"; owpnajsgmue
trophoblastic chorion, and
those cases where it does
not (Method II) are mere
ly another secondary devel
opment" In_ conclusion’ it Fig. 265.——Reconstruction of a surface view of
may be Sald that 01’! the a Pig blastoderm, length 1.56 mm. After Streeter.
Heavy dotted line anterior to Hensen’s node is
whole the lfrgurllents for the notochord. Cross hatched region is mesothe conception Just p1‘6- derm. Darkly lined area posterior to Hensen’s
sented appear to be rather node is remains of primitive streak.
more cogent and reasonable than those opposed to it and it is the one
which is more widely held.
THE PRIMITIVE STREAK AND RELATED STRUCTURES
It will have been noted that during the process of amnion formation
(in Method I, slightly preceding it) there arises in one way or another
from the embryonic knob a flat plate of epiblast. This area of epiblast
together with the hypoblast directly beneath it is the area from which
the embryo proper is now to develop. As has been suggested, in the
Chick it is termed the embryonic blastoderm; in the Mammal it is the
embryonic disc.
The Primitive Streak and Groove. ——The primitive streak arises
along the mid-line of the embryonic disc in what later proves to be the
longitudinal axis of the embryo. The questions as to its source are very
much the same as they were in the case of the Chick, but not so much
experimental work has been done in an eiiort to answer them. The reasons for this are fairly obvious in view of the conditions under which
the Mammalian embryo develops. However, careful study of fixed material has been made by Streeter and others in the case of the Pig, and
 
' Henserrs node
526 EARLY MAMMALIAN DEVELOPMENT
Fig. 266.-—A. Sagittal section through the embryonic shield of the Hedgehog,
showing the transitory blastopore. From Kellicott (Chordate Development). After
Hubrecht. B. Posterior part of a sagittal section through the embryonic disc of
the Mole. C. Diagram of a sagittal section through the embryonic disc of the Mole.
From McMurrich (Development of the Human Body). After Heape.
ant. Amnion. b. or bl. Blastopore. ce. Chorda endoderm. ec. Ectoderm. en. Endoderm. nc. Neurenteric canal. prm. Peristomial mesoderm. ps. Primitive streak.
t. Trophoderm.
the following conclusions seem justified. There first.appears a thickened crescent of epiblast about what proves to be the posterior margin
of the disc (Fig. 262, A). This crescent then assumes the form of an
oval (Fig. 262, B, C ), and this gradually elongatesy into the primitive
streak (Fig. 262, D; Fig. 263). Presently, as in the Bird, a primitive
groove forms along the middle of the streak and at its anterior end there
develops a thickened spot, Hensen’s knot (Figs. 264, 265) . It is to be particularly noted that in this knot there is likewise a pit which in some
Mammals, e.g., the Hedgehog, as in some Birds, temporarily opens into.
the archenteron (Fig. 266). In some others the pit merely pushes into
THE PRIMITIVE STREAK 527
the notochord where it is known as the notochordal canal. In either case
its possible homology with the part of the blastopore which in other
cases forms a neurenteric canal is obvious, even though it disappears before the neural folds arise. Just what is going on during these changes of
shape from a crescent, to a streak with a groove and knot, is not certain.
It seems highly probable, however, that the process is again one of convergence of material toward the mid-line, and perhaps even some concrescence. Also as in the
Chick, there is apparently
rapid proliferation of cells
in this region. The meanings
of the groove and knot are
no more or less clear than
in the case of the Chick, and
whatever their significance
in that form they probably
have the same significance
in the Mammal (see below).
Origin of Mesoderm
and Notochord. —-As in
the Chick, so in the Pig, and
presumably in other Mam
primitive streak
     
ectoderm
mesoderm
x section pig blastoderm
mals, the streak is again the Fig. 267.—-‘Transverse section of one side of v
d a Pig blastoderm similar to one from which
5°urce Of the meso erm’ surface reconstruction in Fig. 262, C, was
which is proliferated from made. After Streeter. Long axis measurement
. . of the blastoderm from which this section was
its sides, and spreads out on
taken was .5 mm.
either hand and posteriorly
(Figs. 267, 268). Indeed as shown in Figure 262, this proliferation actually begins even before the streak primordium has assumed its definitive elongated form. Whether there is later any actual movement of
cells through the streak from the upper surface, i.e., anything like infiltration (involution), as was suggested in the case of the Bird is not
known, but it seems quite possible. If this were true it might help, again
as in the Bird, to account for the development of the groove. Be that as
it may the mesoderm having thus originated as a single sheet, very early
begins to split into the usual somatic and splanchnic layers. This splitting starts in random isolated areas, thus producing small vesicles,
which presently coalesce, to form more extenisve coelomic spaces (Figs.
262, 263). It willebe noted incidentally that the coelom first formed in
this manner actually lies outside the definitely embryonic area, i.e., ap528 EARLY MAMMALIAN DEVELOPMENT
proximately the region comparable to the area pellucida of the Chick.
Hence this first coelornic space is extra-embryonic, but very shortly it
spreads within the embryonic region. Finally the notochord (headprocess) of the Pig arises according to Streeter (’27) as a rod of cells
 
 
 
“-‘9..3'.~‘4‘:-"W
,
Fig. 268.—A. Transverse section through the primitive streak of
the Mole. B. Transverse section through a Human embryo of 1.54
mm. (Graf von Spee’s Embryo Gle.) From Minot (Laboratory
Zfggt-Book of Embryology), after Heape (A), and Graf von Spee
ch. Notochord. ct. Somatic mesoderm of amnion. df. Splanchnic
mesoderm. Ec. or ek. Ectoderm. en. or En. Endoderm. df. Dorsal
furrow. g. Junction of extra-embryonic somatic and splanchnic mesvoderm. me. or mes. Mesoderm. p. Rudiment of embryonic coelom.
p.gr. Primitive groove. Pr. Primitive streak.
proliferated at the primitive knot and pushed anteriorly. This it will be
recalled is identical with one of the theories of notochord origin in the
Chick. According to one of the most recent theories, however (Spratt,
’47) , the notochord in the Bird lengthens by growing posteriorly rather
than anteriorly, as the primitive streak shortens. It is quite probable that
whatever the true process proves to be in that case it will be found to
hold also for the Mammal. However that may be, it should be noted
that there is an interesting difference between the relation of the mesoderm and notochord in the Pig from that observed in the Chick. Thus it
YOLK-SAC, ALLANTOIS, AND PLACENTA 529
will be seen that in the Pig the notochqrd has no mesoderm free area
(proamnion) anterior to it as was true in the Bird (Fig. 265). The only
suggestion of this occurs much earlier in front of the beginning primitive
streak sometime before the notochord has begun to develop (Fig. 262).
The Nature of the Mammalian Primitive St-reak.——From the
above ‘description it is very evident that the parts here indicated are
virtually homologous with the similarly named structures in the Bird.
Consequently if the primitive streak of the latter can be further homologizecl with the remains of an elongated closed hlastopore, it would
appear that this homology holds equally well for the primitive streak
of the Mammal. As previously suggested, however, because of practical
difliculties experimental observations on the behavior of materials dur-.
ing and immediately after the formation of the primitive streak are not
as yet available in this instance as they were in the Chick. The chief
evidence therefore arises from observation of the relations of the streak
to the formation of the notochord and mesoderm already noted, and to
parts of the future embryo. Thus in the latter connection it may be
stated that the anus forms at the posterior end of the streak, and a. very
marked pit, amounting in some cases to a virtual neurenteric canal, at
its anterior end. '
In the case of the preceding topic as in others to follow the student
who does not recall the comparable situation in the Chick is again
urged to refresh his memory on the points in question, since we shall
not repeat identical material. '
THE YOLK-SAC, THE ALLANTOIS, AND THE PLACENTA:
THEIR STRUCTURE AND FUNCTIONS IN THE MAMMAL
Among the Amniotes of which the Chick is a type, i.e., the Birds, the.
chief organs through which the embryo receives its nutriment and
effects respiration have been seen to be respectively the yolk-sac and the
allantois. Among the vast majority of the Amniote group known as
Mammals, however, these organs are very largely, and in many cases
completely, supplanted in these functions by a new structure, typically
associated with the allantois and termed the placenta. The large group
of Mammals among whose members this organ is most fully developed
is therefore known as that of the placental Mammals, a group which
hastalready been frequently referred to. It will presently appear, however, that within this group there are certain types of placentas which
vary from one another, ‘both in their structure, and in the degree to
530 EARLY MAMMALIAN DEVELOPMENT
Fig. 269.—Fetal membranes of A, Monotremata; B, C, D. Marsupials. B. Phalangista, Aepyprymnus, Didelphys, Bettongid; C. Dasyurus; D. Perameles and
Halmaturus. (In Didelphys the proamnion persists as in Dasyrus.) From Jenkinson (Vertebrate Embryology). (A, B, D, after Semon; C, after Hill.)
In this diagram of Mammalian fetal membranes the trophoblast (ectoderm of
mammalian chorion) is stippled, the ectoderm oi the amnion represented by a
continuous line, the endoderm by a broken line, and the mesodertn (somatopleure
and splanchnoplenre) by a thick line swollen at intervals.
all. Allantols. am.c. Amniotic cavity. pr. Proamnion, i.e., portion of amnion without mesoderm. y.s. Yolk-sac. s.t. Sinus terminalis of area vasculosa.
which they have assumed the place and functions of the allantois and
the yolk-sac‘. There exist also two relatively small mammalian groups,
the Monotremes and the Marsupials, whose members possess either no
placenta at all or only a very rudimentary one. Under these circumV or F‘ stances, therefore, it appears most convenient to treat the subject by
i taking up the conditions of the above organs in one group at a time.
The Monotremes and the Marsupials will be considered first, since they
are most primitive, and exhibit a condition most nearly akin to that in
the Reptiles and Birds. After these there will be discussed certain orders of truly placental Mammals which best illustrate the various types
noes-2 ax:
‘ma.
THE MARSUPIALS 531
of allantoic placenta, and perhaps suggest its method of evolution. The
orders to be thus considered are the Ungulazes, the Carnivores, the
Rodents, and the Primates. Finally before passing to a study of the first
group, it may be mentioned incidentally that the discussion of this subject also necessarily involves in each case a more extended reference
to the matter of implantation referred to above.
THE MONOTREMES
These curious mammalian forms comprise the Spiny Ant Eater
(Echidna) , and the Duck Bill (0rnithorhynchus) . They are remarkable
as Mammals in that they lay hard-shelled eggs like Birds. As might
be expected in such a case, the yolk—sac is well developed and illed
with yolk, while the allantois is also prominent. The placenta, on the
other hand, because of its peculiar nature and functions, which its study
will presently reveal, is naturally entirely lacking. In short, in eggs of
this sort the embryonic parts under discussion are in all respects characteristically reptilian or avian (Fig. 269, /1)-.
THE MARSUPIALS
This group comprises the Kangaroos (Macropodidae), the Opossums
(Didelphyidae), the Marsupial Cats (Dasyuridae) and the Bandicoots
(Peramelidae). These animals are all characterized by the fact that
their young are born in a comparatively undeveloped condition. They
then crawl inside of the Marsupial pouch of the mother and become
attached to her teats, where they remain for some time. As might be
expected under such circumstances, the means for obtaining nourishment and aerating the blood previous to birth are very primitive. In
fact, among the various members of the group there occur some very
excellent examples of graded transition from the condition in the Monotremes to that in the real placental Mammals. The Opossum is per»
haps as primitive a form as any in this respect, and will therefore be
considered first.
The Most Rudimentary Type of Placenta. -—ln Didelphys, or
the Opossum (Fig. 269, B), the yolk-sac, as in all the Marsupials, is
well developed though it contains no yolk. Nevertheless, upon its upper
surface there is a clearly defined area vasculosa, bounded by a sinus
terminalis. Since there is no yolk, however, the nutriment which the
above area is to convey into the embryo must be obtained from some
other source; this is accomplished in the following manner: Although
532 EARLY MAMMALIAN DEVELOPMENT
the mesoderm, and consequently the area vasculosa, do not reach to the
opposite side of the yolk-sac, the endoderm on that side comes into contact with the trophoblast of the blastocyst. During implantation this
trophoblast becomes thrown into folds (not shown in the figure) which
fit into depressions in the uterine wall. The latter then secretes a viscid
fluid, the uterine milk, which is absorbed via the trophoblast and endoderm, and finally reaches the embryo, partly at least by way of the area
va.sculosa.- This contact of the embryonic trophoblast and the uterine
tissue may be regarded as a very primitive beginning of what will later
berecognized as a placenta. The allantois is very small in this case, as
in most other Marsupials, and has no contact with the trophoblast. The
exact means by which the embryonic blood is aerated, therefore, is a '
little uncertain. Very possibly, however, it also is accomplished through
the contact of yolk-sac and maternal tissues.
A “ Yolk-Sac Placenta.” —-— Dasyurus is the second form to be considered, because it exemplifies the next step in the development of a
true placenta (Fig. 269, C). The allantois, however, is still small, and
the placenta-like structure which occurs is, therefore, again associated
entirely with the yolk-sac. Furthermore, the trophoblast in contact with
the non-vascular area of the sac once more forms the connection with
the uterine wall. In this instance, however, this implantation is more
thoroughgoing, and there appears for the first time that process ‘of
uterine erosion so noteworthy among some of the higher forms. This
erosion is accomplished by the trophoblast which, after becoming
thickened and syncytial (i.e., trophodermal) in certain regions, eats
into the uterine epithelium and engulfs some of the maternal blood vessels. The blood so obtained passes in between the trophoblast and yolksac, secretions from one or both of which digest it so that it can be absorbed. Presumably also such an arrangement makes possible respiratory
exchange of gases between embryonic and maternal blood. The type of
contact which is here illustrated is so intimate that the area in which it
occurs is sometimes referred to as a yplk-sac placenta.
A Primitive “ Allantoic Placenta.” —-— Finally, the most advanced
condition in this Marsupial series is illustrated in Perameles, where
the following situation occurs (Fig. 269, D) : Here the yolk-sac is again
large, and possesses an area vasculosa which is probably functional
in absorbing some nourishment by way of the trophoblast. In this case,
however, the allantois also is well developed,vand comes into contact
with the mesoderm of the chorion. Implantation then occurs and the
trophoblast in the area of this contact becomes attached to the uterine
—
‘-,
i
THE PLACENT-ALIA 533
wall, whose epithelium in this region is transformed into a vascular
syncytium. The trophoblast finally disappears, and the maternal blood
vessels come into intimate contact with those which have grown out
through the mesoderm of the allantois (Fig. 270). Thus there is established a true allantoic placenta. As will presently appear, however, the
exact relationship of its embryonic and its maternal parts is different
from that described in any of the subsequent types.
4/
 
f. b. v.
:73. mt.
Fig. 270.——Section through the placenta of Perameles. From Jenlcinson (Vertebrate Embryology). After Hill.
all. Allantoic epithelium. m. Mesoderm of allantois together with xnesoderm of
chorion. f.b.v. Fetal blood-vessel. ep.s. Syncytium of uterine epithelium. m.b.v.
Maternal blood-vessels. c.t. Sub-epithelial connective tissue of uterus.
In connection with this, the first real placenta to be noted, there is
one very important fact to be pointed out. Neither in this placenta nor
in those of any other type does the fetal and the maternal blood actually mix. It is always completely separated by one or more membranes.
Through these membranes, however, it is easily possible for an exchange of nutritive and waste materials, as well as gases, to take place.
This-completes the account of the Marsupials, and we are now prepared to pass on to the orders of the genuine placental Mammals. As
has been indicated, the latter are so named because here an allantoic
placenta of one sort or another becomes the usual and chief means of
embryonic nutrition and respiration. In the Marsupials, on the other
hand, such a condition occurs only in the single instance last cited. '
THE PLACENTALIA OR TRUE PLACENTAL MAMMALS
Within this large group, the embryonic appendages whose condition
is being considered are probably in their-most primitive form among
534 EARLY MAMMALIAN DEVELOPMENT
the Ungulates, and this ‘order, therefore, will be treated first with special reference to the Mammal; we have selected for later detailed study,
the Pig.
The Ungulates (the Pig).
The Early Means of Nutrition and the Yolk-Sac. —- Before the blaste
cysts enter the horns of the bicornate uterus, the latter have been prepared for their reception during the pro-oestrum, oestrus and early
Fig. 271.—Diagram of a fetal and maternal cotyledon of the Cow.
From Jenkinson (Vertebrate Embryology).
all. Allantoic epithelium. tr. Trophoblast. 11. Villus. ep. Uterine epithelium continued into crypt. c.w. Wall of crypt. The maternal conneco
live tissue is shaded.
dioestrum periods as explained in cohnection with the oestrus cycle. As
a result of this the uterine walls are thickened, and their glands hypertrophied to produce the secretion (uterine milk) which helps to supply
the embryos with nutriment and is eagerly absorbed by the trophoblast
of the blastocysts. Meanwhile gastrulation has occurred, the endoderm
(hypoblast) has grown around the inside of each blastocyst, and thus
with the advent of mesoderm and the folding off of the gut, an empty
yolk-sac is established in each. It is relatively large, and in the early
stages possesses a well developed area vasculosa. Thus it is able to function actively in passing nutriment from the uterine cavity into the embryo. Later, however, the yolk-sac becomes insignificant, its function
being entirely taken over by the allantois and the placenta, whose development will now be described. '
The Placenta arid the Allantois.—The blastocyst of this group, it
will be remembered, soon becomes greatly elongated, reaching a length
1
1
i
I
I
I
THE PLACENTALIA 535
of as much as a meter. It is not, however, to be understood from this
that it is actually extended to this extent, for if it were it would be
longer than the uterine horn in which it and several of its fellows are
contained. Instead, as the threadlike blastocyst of the Pig grows, it becomes greatly folded, the folds fitting into corresponding folds of the
blastodermic vesicle
amnion ¢mb")'°
   
l‘  I horlonlc crophoblast
diagrammatic x section r
of blastodermlc vesicle _.- '
 
Fig. 272.—-Drawing of a Pig blastodermic vesicle measuring about 350 mm. in
length and 4-0 mm. in diameter, and a diagrammatic :ransverse section of same.
The contained embryo measured about 40 mm. in length. Note the folds which
replace the villi of many Ungulates.
uterine walls. Later when the embryo develops and the blastocyst expands, the latter is very much dilated and shortened, after which the
term blastodermic vesicle is more commonly applied to it. As the vesicles reach their maximum length on about the thirteenth day. their
trophoblast has become relatively adherent to the uterine epithelium,
and implantation is said to have occurred.’ In the case of the Pig the
surface of the endometrium remains folded as does ,the surface of the
7 The implantation time varies in difierent animals, but in most of them it
occurs within a few days, often about seven, after the blastocysts reach the uterus.
In a few cases, however, implantation may be markedly dela'yed. Thus in the Long
Tailed Weasel and the Martin the blastocysts are said to lie dormant in the uterus
for many weeks (Wright, '42).
- 536 - EARLY MAMMALIAN DEVELOPMENT
blastocyst, though not to the extent that it was at its greatest length.
This arrangement of course increases the area of trophoblastic and uterine contact through which the exchange of nutriment and excretory
products can occur. This capacity for exchange is still further augmented
by the fact that in certain spots (areolae) microscopic projections
(villi) push out from the chorion into small spaces between the latter
and the uterine epithelium. These spaces are filled with the uterine secretion referred to above. In some Ungulates such as the Cow, the villi
atrial part posterior ardinti vein
 
 
 
ventricular area .
temporary viteiime and intcstlnai arteries
 
Fig. 273.——A 6.2 mm. Pig embryo (23 somites), injected, showing the circulatory system and beginning allantois. After Sabin.
are larger, and arranged in bunches or cotyledons, while the corresponding areas in the uterine wall with which the cotyledons come into
contact are called caruncles. These latter are permanently located, and
are said to exist as raised areas even in the uterus of the unborn calf.
Thus in these instances the locations of the embryonic cotyledons are
secondary, being determined by the positions of the maternal caruncles.
Meanwhile, to return to the Pig, by the time the embryo has reached
a length of 4-6 mm. the allantois has begun to outstrip the yolk-sac,
and soon comes to occupy the major part of the extra-embryonic space.
It appears first as a rather conspicuous crescent-shaped outgrowth encircling the posterior of the embryo, with its -horns extending anteriorly
(Fig. 273). In this respect it difl'ers considerably from the Chick allantois which it will be recalled is first noted as a roundish bladder pushing anteriorly and upward to the right from beneath the curled tail.
The crescentic allahtoic outgrowth of the Pig rapidly works its way
around the amnion, pushes aside the now useless yolk-sac, and eventuTHE PLACENTALIA 537
ally extends everywhere throughout the extra-embryonic space of the
vesicle except in the extreme ends (Fig. 272). The mesoderm which covers the allantois carries the umbilical blood vessels, and this mesoderm
together with the capillaries of the vessels becomes closely adherent to
the mesoderrn of the chorion into which these capillaries penetrate. In
this manner the fetal vessels come close enough to those of the uterine
mucosa for the necessary exchanges to occur. Thus is constituted the
Ungulate (in this case Pig) placenta, which as will be noted, comprises
almost the whole surface of the blastodermic vesicle.
It is to be especially noted that in the processes just described there
is absolutely no erosion of the uterine epithelium.‘ Instead the chorionic folds simply fit in between those of the endometrium from which
they may be easily stripped away at any time. Indeed during gestation
the endometriumicontinues to secrete nutritive substances between itself
and the chorion. This is absorbed by the latter and taken up by the
embryonic vessels, so that in this case, as in some others, the embryonic nutriment is not all obtained directly from that which is carried
in the maternal blood. A placenta in which the contact. between fetaland maternal tissue is such as indicated is often defined as indeciduate.
This term implies that at the time of parturition, the wall of the uterus
is literally not deciduous. That is, there is no tearing away of maternal
tissue when the fetal part of the placenta separates from that of the
mother.
In concluding this discussion of implantation in the Pig a curious
fact may be noted which apparently applies also to other Mammals
which have two horned uteri and produce litters. Thus it is well known
that the number of eggs ovulated by the two ovaries may be quite unequal as indicated by the corpora lutea present. Yet Corner has demonstrated that the number qf embryos developing in each uterine horn
is practically the same. This can only mean that enough of the embryos
from the side which produced more eggs have migrated to the opposite
side to equalize the numbers in the two horns. How this is brought
about no one knows, but in the case of the Pig it apparently occurs
previous to the elongation of the blastocysts.
The Carnivores.
The Yolk-Sac. —As in the Ungulates, the period of the pro-oestrum
results in the accumulation within the uterine hornsof a nutritive mix
3 According to some authorities there is erosion of the inaternal epithelium in
the Ruminants.
538 EARLY MAMMALIAN DEVELOPMENT
ture somewhat similar to that already described. In some cases, however (e.g., the Cat), it appears to be less abundant than in the Ungulates, and of a more watery consistency. The uterine mucosa is of course
also hypertrophied in the usual way, and everything is ready for the
Fig. 274.-——Fetal membranes and placenta of the Dog. From Jenkinson (Vertebrate Embryology). After Duval. '
all. Allantois. am.c. Amniotic cavity. In. Mesometrium, or sheet of connective
tissue attaching the uterus to the body wall. pl. Zonary placenta. (See text under
description of the placenta of the Carnivores for the definition of this term.) y.s.
Yolk-sac. The fetal mesoderm, connective tissue and blood-vessels are in black.
reception of the blastocyst, which in this instance is oval, never at any
time threadlike. Again the latter begins its development by absorption
of the nutrient fluid. A yolk-sac has meanwhile developed, in_ the usual
Mammalian manner, and apparently it plays about the same part in
this process as was noted in the Ungulates. As in that order, also, this
appendage later becomes relatively insignificant (Fig. 274) .
The Placenta and the Allantois. —— While these events are occurring,
3. change is taking place in the uterine wall. In a band which completely encircles this wall the epithelium disappears. Likewise, in the
THE PLACENTALIA 539
‘7‘;'';-~;-‘'7‘/=‘7‘-—--— 8"’:/’ %g___,.
tr.
rn.b.c.
f. c. t.
f. b. c.
In .b.v.
Fig. 275.—Section through the placenta and uterine
wall of the Cat. From Jenkinson (Vertebrate Embryology).
all. Epithelium of allantois. f.b.v. Large fetal bloodvessels. f.b.c. Fetal capillaries. f.c.t. Fetal connective
tissue. tr. Trophoblast (finely shaded). m.b.c. Maternal
blood capillaries; these are immediately surrounded by
maternal connective tissue (coarsely stippled). m.b.v.
Maternal blood-vessels passing through the maternal
glandular tissue (d). cp. Compacta (necks of glands).
sp. Spongiosa (dilutions of glands).
region of a corresponding band about the equator of the oval blastecysts, the latter begins to adhere to the prepared uterine wall. During
this process of implantation, trophoblastic villi similar to those of
some of the Ungulates begin to develop from the wall of the blastocyst
in the region of its adherence. Because of the obvious band or zone-like
shape of this region, the type of placenta which develops in this order A
is called zonary. The villi of the chorion, which may contain a core of
540 EARLY MAMMALIAN DEVELOPMENT
mesoderm, now push their way directly iillio the mucous tissue of the
uterus. As they do so, they absorb any remaining epithelial debris
which comes in their way. In this manner, they soon.become firmly embedded in the maternal tissue and surrounded by maternal blood vessels. While this is going on, the allantois has grown out, and as in the
Ungulates, soon becomes the chief appendage of the embryo. When the
allantoic mesoderm comes into contact with the chorionic mesoderm in
the zone of implantation, the allantoiccapillaries penetrate the villi,
and the placenta is virtually complete. During subsequent development,
however, it becomes thickened somewhat by growth and branching of
the villi and capillaries, and also of the maternal connective tissue in
which they are embedded. The glands of the latter continue to supply
debris and fat, which is absorbed by the chorionic villi up to the end
of gestation. The main source of embryonic nutrition, however, is presumably material contained in the maternal blood (Fig. 275).
It will be noted that the attachment of the fetal and the maternal
parts of the placenta is much more intimate in this case than it was in
the Ungulates. This has resulted from the disappearance of the uterine
epithelium, which allows the capillaries in the fetal villi to come that
much nearer to those of the mother. Because of this very close attach-.
ment, it also happens that at birth a large portion of the maternal tissue
is torn away with the fetal portion of the placenta. For this reason, this
type of placenta may be regarded as deciduate. Indeed, as will appear
from a study of the remaining groups, the Carnivores are probably the
only animals possessing a placenta of which this is true in any large
degree.
The Rodents.—-As in the forms previously studied, the uterine
epithelium of the horns is in, a hypertrophied condition following the
proioestrum and oestrus, and is thus ready to receive the blastocysts
(“ egg cylinders ”) when they reach the uteri. The method of attachment and of placenta formation which now follows varies somewhat
in different Rodents, although it is fundamentally similar in all of them,
and leads to practically the same results. It will further be found that
in this case, the former process, i.e., attachment or implantation, is
somewhat elaborate, and therefore requires more detailed attention than
has hitherto been necessary. The chief conditions with respect to this
process as well aslto the general character of the yolk-sac, may be illustrated by reference to two forms, the Mouse and the Rabbit. _
Implantation and the Development 0/ the Yolk-Sac. —— In the case of
the Mouse, each elongated uterine horn becomes lined with pits upon its
anti-mesometric side. This is the side opposite its point of attachment to
r_
THE PLACENTALIA 54.1
the coelomic wall, the latter region being termed the mesometric side.
Each of the ovoid blastocysts, of which there are several in the -Mouse,
becomes embedded in one of these pits with the embryonic knob facing
the narrow lumen of the uterus (Fig. 276, B). That this anti-mesometric
Fig. 276.—-Five stages in the formation of the placenta in the Mouse. From Jen»
kinson (Vertebrate Embryology). A. The blastocyst free in the uterus. B. The
blastocyst attached and the placental thickening of the developed allantoidean
trophoblast (trophoderm) (a.t.r.). C. Later stage, after closure of the amniotic cavity (am.c.) and the obliteration of the uterine lumen. D. Placenta becoming established, and reappearance of uterine lumen (l’u-.). E. Elaboration of the placenta.
l()isap)pearance of the distal wall of the yolk-sac and omphaloidean trophoblast
0.tf. .
c. Extra-embryonic coelom. l'u. New uterine lumen on the anti-mesometric si .
lu. Original lumen of the uterus. y.s. Yolk-sac. ;v.st. Yolk-stalk. u.c. Umbilical cor
m.. Mesometrium.
 
 
   
 
 
implantation is not the result of gravity has been clearly demonstraf
in the Rat by Alden (’45). He cut out the middle portion of a uter '‘
horn, leaving blood vessels intact, and replaced it in an inverted « .
tion. Implantation in this section was still on the anti-mesometric,‘;
now dorsal, side. Continuing with the case of the Mouse the furth
tory of a single blastocyst will suflice. ’ ..
As soon as the embedding has occurred, the trophoblast imm N
starts to erode the epithelium of the pit, and to devour the debris '
542 EARLY MAMMALIAN DEVELOPMENT
results. Meantime the blastocyst enlarges sufliciently so that the side containing the embryonic knob crosses the uterine lumen and comes in contact with the opposite wall (Fig. 276, B, C). In this way, each blastocyst
obtains attachment at every point, and completely obliterates the cavity
of the‘ ‘uterus where it is situated. At every place where contact is thus
97- am.
Fig. 277.--Fetal membranes and placenta of the Rabbit. From Jenlrinson (Vertebrate Embryology). After Duval and Van Beneden.
pr.am. Proamnion. Other letters as in Fig. 276.
established, i.e., on the bottom and sides of the original pit, and also
upon the uterine wall opposite to it, erosion of the uterine epithelium
is carried on. The placenta, which will presently he described, is established on the mesometric side of the uterus at the second point of
contact, and therefore next to the embryo. Then, owing to the intimate
relation of trophoblast and allantois in this region, the thickened trophohlast (trophoderm) on this side of the blastocyst is called allantoideon.
On the opposite side, i.e., at the original bottom of the pit, the uterine
lumen is later again established. Here for a while epithelium once more
develops, and covers both the wall of the uterus and the blastocyst (Fig.
F______ _. .. .Hhm_a_
THE PLACENTALIA 543
, 276, D). Inside the latter, the yolk-sac has meanwhile formed, and on its
3 upper surface has acquired an area vasculosa. Its lower wall, on the
other hand, which is in contact with the trophoblast of the blastocyst, finally degenerates. The trophoblast (in this region termed omphaloidgun) and the newly formed epithelium at this point then also vanish,
and thus the interior of the yolk-sac is placed in immediate communication with the re-established uterine cavity (Fig. 276, E) .9
Tufning now to the method of implantation in the Rabbit, it is found
to be somewhat less complicated. Here a pair of folds arise upon the
mesometric side of the uterus, and the blastocysts become attached to
these. Each blastocyst in this case lies between the folds and becomes
i attached by the trophoblast on either side of the embryonic disc. In
3 these regions, the uterine epithelium is eroded, and two placentas are
established which later merge into one (Fig. 277). The opposite side of
the blastocyst forms no intimate contact with the uterine wall and presently disappears. Concurrently the ventral wall of the yolk-sac also disappears, so that again, as in the case of the Mouse, the cavity of the sac
x is directly continuous with that of the uterus (this stage not shown in
the figure).
Having thus described the two chief types of implantation among the
Rodents, we are now in a position to discuss the nature of the placenta
and other means of nutrition common to all this group.
The Placenta and the Allantoi.s.———During the erosion of the uterine
epithelium indicated above, the allantoidean or placental trophoblast
becomes greatly thickened, to form trophoderm. This trophoderrnthen
continues to eat down into the mucous layer of the uterine wall, engulfing, as it does so, maternal blood vessels, together with glycogen from
the glycogen-filled cells (maternal glycogen tissue). There next appear
in the trophoclerm numerous lacunae, and into these is emptied the maternal blood from the vessels whose walls have been destroyed (Fig.
278, A). Meantime an allantois has arisen. In the Rodents, the endodermal portion of this organ containing the cavity is usually small,
although in the Rabbit, which in this as in most other respects is more
primitive, the allantoic cavity attains a considerable size (Fig. 277).
The mesodermal part, however, is always well developed, and soon
reaches the trophoderm of the placental region, bringing with it the umbilical blood vessels (Fig. 278, B). The capillaries of these vessels then
” The assumption has been that in this as in other cases the vascularized wall
of the empty yolk-sac functions in obtaining nutrimc.-nt for the early embnyo. Recent
experiments on the Rat. however, involving the tying 03 of‘ the vitelline vessels.
seem to indicate that such a function is negligible, at least in this animal
(Noer’47).
544_._ EARLY MAMMALIAN DEVELOPMENT
a. m. f. b. v.
 
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\\\\ ( ‘
.t\\\ r ‘~" ‘L
Fig. 278.—Placentation of the Mouse. Details of the five stages of
Fig. 276. From Jenkinson (Vertebrate Embryology».
A. Strip of a section through the allantoidean trophoblast (trophoderm) and overlying maternal tissues in stage C, Fig. 276.
a.t.r. Allantoidean trophoderm. mu. Muscularis. m.v. Maternal bloodvessel, opening below into I. lacunae of the trophoderm. Lu. Original
lumen of the uterus. m.g.c. Maternal glycogen tissue.
B. Similar strip of the same parts in stage D, Fig. 276.
_ fjmv. Fetal blood-vessel. a.m. Allantoic mesoderm. Other letters as
in .
C. Similar strip of the last stage, Fig. 276.
tr.g.c. Trophodermal glycogen tissue. Other letters as in 3.
Note that ,ultimately this placenta is very largely composed of
trophoderm, which is a non-maternal tissue. Hence, since at parturition the line of separation passes through the placenta (the trophodermal glycogen tissue), little or no maternal tissue is lost, and the
placenta is essentially indeciduate. (See text.)
l
THE PLACENTALIA 545
penetrate the trophoderm so as to come near to the cavities containing
the extravasated maternal blood. This blood is being constantly poured
into the central space of the placental region, and withdrawn at the
periphery through the maternal veins. Gradually, toward the maternal
side, the trophoderm surrounding the lacunae becomes further vacuolated through the secretion of glycogen, thus establishing a trophoder.
mal glycogen tissue (Fig. 278, C). Eventually through the increase of
the latter, the layer of original maternal glycogen tissue is entirely eliminated.” Such is the character of the completed placenta of the Rodents,
which, because of its development upon only one side of the blastocyst,
has the general shape of a disc or button. It is, therefore, termed discoidal, as distinguished from the zonary form found in the Carnivores.
Comparing the placenta in this case with that noted in the Carnivores,
the chief difference will be found to be that, in the completed organ of
the Rodents, maternal tissue plays very little part. The placenta indeed
is principally composed of the fetal trophoderm with its capillaries,
lacunae, and glycogen tissue. This difference seems to be achieved by
the fact that the trophoderm erodes not only the uterine epithelium, but
a large part of the mucosa and its blood vessels as well. Because of this
peculiar structure, it happens at parturition that, aside from the blood
in the lacunae, very little real maternal tissue is lost. This follows from
the fact that the actual line of separation runs through the region of
vacuolated cells which have now lost their glycogen and collapsed, and
this region, as noted, is held to be entirely trophodermal. On account
of this lack of maternal tissue to be torn away, many authorities regard
the term deciduate as a misnomer when applied to placentas of this
type. If the above description be correct, it apparently is a misnomer.
Nevertheless, such placentas are still commonly classified under this
head.
As regards the method of nutrition in this order, it is apparent that,
aside from the glycogen, nutriment is chiefly obtained, so far as the placenta is concerned, from the maternal blood. It will be remembered,
however, that among the Rodents, the yolk-sac is always eventually open
to the uterine cavity. Thus, for instance in the Mouse and the Rabbit,
the lower epithelial wall of this organ was found to disappear com- ‘
pletely, while in the Guinea Pig it is never even formed. This being the
case, the upper wall of the sac may, in’ some cases at least, function
throughout gestation in the absorption of uterine secretions. To the ex
1° The maternal glycogen tissue is said to be more abundant and persistent in
the Rabbit.
546 EARLY MAMMALIAN DEVELOPMENT
Fig. 279.——Diagrams illustrating the formation of the umbilical
cord and the relations of the allantois and yolk-sac in the Human embryo. From McMurric_h (Development of the Human Body). The
heavy black line represents the embryonic ectoderm; the dotted line
marks the line of the transition of the body (embryonic) ectoderm
into that of the amnion. Shaded areas, mesoderm.
Ac. Amniotic cavity. Al. Allantois. Bc. Exocoelom. Bs. Body-stalk.
Ch. Chorion. P. Placenta. Uc. Umbilical cord. V. Chorionic (tropho
dermal) villi. Ys. Yolk-sac.
tent that this is true, therefore, the Rodent yolk-sac, both in its form and
in its activity, differs markedly from the types previously studied within
the strictly placental group.
The Primates.“
The Allantois and the Yolk-Sac. —— In the order of Primates, the nature of the yolk-sac and allantois is somewhat unique, while the latter
11 The characteristics of the embryonic appendages which are ascribed to this
order apply to only'une of the family of Lemurs, i.e., Tarsius. This animal, in
respect to these organs, may be classed with the lower Monkeys. So far as is known,
however, all other Lemurs are similar to the Ungulates as regards the yolk-sac and
allantois, and also even in the possession of a difluse indecidiiate placenta. This
exception must be home in mind with reference to all statements concerning the
Primates as a whole.
THE PLACENTALIA 547
 
 
 
 
Fig. 280.——Diagrams of sagittal sections through the Human blastoderrnic vesicle, showing the formation of the amnion and trophoderm. From Kellicott
(Chardate Development). /1-D, after Keibel and Elze. E. From McMurrich (Development of the Human Body), after Graf von Spec. In all the figures the anterior
end is toward the left, and in all the figures except E the following conventions.
are used: Black, embryonic ectoderm: heavy stipples, trophoblast and trophoderm;
light stipples, endoderm. Ohlique ruling, mesoderm except in A. A. Hypothetical
early stage; oblique ruling represents magma reticulare (see text). 8. Amniotic
cavity and wide exocoelom established; endoderm limited to a small vesicle beneath the embryonic ectoderm. The exocoelom in reality contains scattered mesenchyme cells. C. Blastodermic vesicle enlarged and covered with trophedermal villi,
into which’ the mesoderm is extending. Endodermic vesicle (yolk-sac) very small
(stage of Peter’s ovum). D. Embryonic portion only, of an older vesicle showing
the neurenteric canal, primitive streak (in the plane of the section posterior to
canal), and body-stalk. The mesoderm of the yolk-sac is becoming vascular. E.
%;a;gi)ttal section through a Human embryo of 1.54 mm. (Graf von Spec’: embryo
C
a. Amniotic cavity. at. Allantois. am. Amnion. B. Body-stalk‘ (umbilical cord).
ch. Chorion. e. Exocoelorn. nc. Neurenteric canal. V. Chorionic villi. Y. Yolk-sac.
y 548 EARLY MAMMALIAN DEVELOPMENT
organ is also peculiar in its method of development. An account of these
structures will be given, therefore, before proceeding to the matter of
implantation and placenta formation within this group.
First, as regards the allantois, it will be found that the endodermal
sac is even more limited than it was in the majority of the Rodents. Furthermore, the mesoderm of that organ does not comprise, as in most
   
Trophcblosl‘
.. Ex traembryonic
mesoblusi
Pfimmve Exccoelo "c
cndodmn ,,,,,,,,,,;“,;
Extrcemrycmc mdoderm Uterus
ring,“ 5"," db“ Trophoblufl mesoblast Amnion Gerrfldigk
xh-cembryonic
‘"‘l°d"’"‘ mesobtast
   
E 1 A Primitive
",:.::ni,:::. endodtrm
Fig. 281.—Mid-sagittal sections through four Human blastocysts
(“ ova") and surrounding uterine wall. After Hertig and Rock. A and B
are estimated as 11 days old plus, while C and D are estimated as 12
‘days old plus. B is the Miller “ovum,” while D is the Werner (Stieve)
previous cases, a mere covering for the sac; instead, it forms a thick
stalk, the body-stalk, or umbilical cord, which attaches the embryo to
the chorion or wall of the blastocyst. Into the proximal end of the mesoclermal cord, the hollow endodermal element then projects for only a
short distance (Figs. 279 and 280). This condition is brought about as
follows:
From what is known of the earliest human embryos (7-15 days, see
i ‘ below I} the blastocyst, following cleavage and gastrulation, contains the
§ _ following structures and materials. First there is the blastoderm, con” E ‘ sisting of a layer of ectoderm and endoderm with a small amniotic cav;  ity derived appariantly from a split in the embryonic knob (Method II,
Type b, seeahove): Second, the greater part of the blastocoelic space is
,Ԥ
THE PLACENTALIA 54,9
occupied by a reticulate material, the magma reticulare, which probably
consists of coagulated protein containing fluid. Scattered through this
reticulate substance, and lining parts of the trophoblast, are a few mesoderm cells ':(extraembryonic mesoblast) presumably derived from the
blastoderm L,‘( Fig. 281, A, B). At about the center of the blastocyst in
these human specimens there occurs a particularly definite space
bou_nded laterally and ventrally by an especially clearly defined layer
of the reticulum, termed the exocoelomic membrane or Heu.ser’s mem
Remnant
exocoelamic membrane
Fig. 282,-Mid-sagittal section of a Human blastocyst and
surrounding uterine wall with an estimated age of 15 days, the
Edwards-.lones-Brewer “ovum.” After Hertig and Rock.
brane (Fig. 281). Dorsally this space is lined by the endoderm of the
blastoderm, and it has therefore been interpreted by some as the yolk— '
sac. Others maintain that the true yolk-sac does not appear until slightly
later, about the 13th day. It is difiicult, however, to distinguish the
_ “endoderm” of this later yolk-sac from the exocoelomic membrane
bounding the central “ exocoelomic space ” of the earlier embryos. At
all events in these later stages the magma reticulare has mostly disappeared and the trophoblast is lined by a definite layer of mesoderm.
This also extends around what is now termed the yolk-sac, up over the
amnion, and at what proves to be the posterior end of the embryo, serves
to attach the blastoderm to the trophoblast (Figs. 280, D; 281, D; 282).
This mesodermal attachment later comes to constitute the umbilical
stalk already referred to, and into it there presently grows a small outpushing from one side of the sac where the latter joins the blastoderm.
It is the beginning of the very small allantois (Figs. 279, 280, D, E).
550 EARLY MAMMALIAN DEVELOPMENT
Although at first located somewhat dorsally, the embryonic end of the
stalk soon moves around so as to be attached to the embryo on its ventral side. It retains, however, its original point of attachment to the
chorion since it is here that the placenta is to be formed.” From this
description it is evident that in the Primates, the allantois, or more
strictly in this case, the umbilical cord, does not grow out from the embryo to the trophoblast. It is there from the first.”
As concerns the yolk-sac, it is only necessary to state that it is very
rudimentary, having little or no function. The space which might otherwise be occupied by these appendages, however, is eventually filled in
this order by a very large amnion.“
Implantation and Placenta Formations-—According to previous accounts ovulation occurs following what amounts to a pro-oestral uterine
hypertrophy, and the blastocyst reaches the uterus while the latter is
under the influence of the progesterone of the succeeding corpus luteum.
Here implantation takes place through the erosion of the hypertrophied
endometrium by the newly arrived blastocyst between one or ‘two weeks
following ovulation. This is of course previous to the time of the menstruation which would have occurred had pregnancy not intervened.
As in the case of the Rodents the details of the implantation process
vary somewhat. In this instance, the chief variation occurs. so far as is
known, between two groups, i.e., Tarsius, together with the other lower
Monkeys, and the higher Apes, together with Man.
As regards the first group, i.e., that of Tarsius and the Monkeys, the
description may be brief. The region of implantation may occur on the
dorsal or ventral wall of the uterus, depending upon the form in question, and is not marked by either pits or folds, as in the Rodents. When
" In Tarsius the placenta is’ formed on the opposite side of the blastocyst, and
the stalk shifts its point of attachment to the trophoblast accordingly. V
‘3 In a more recent human specimen. the Martin-Falkiner blastocyst C38),
estimated at seventeen days of age, a somewhat different theory is expressed concerning the development of these structures. These investigators seem to think that
both the yolk-sac and allantois may arise as vesicles developing in the inner cell
mass itself, and that they may later all run together. If this is true it involves a
somewhat novel method of gastrulation, and a peculiar fate for the allantois. Since
there is some question about the normality of this embryo, theories based on it
should await confirmation from the study of more specimens.
“ Though not (iertainly known, it appears that the amnion in the Primates (excepting the Lemurs, in this instance including Tarsius) is formed in a manner
similar to that described under method II, i.e., by the development of a cavity in
the embryonic knob!" The process in this group differs from that described under
types I) or c of the second method, however, in that in this case the embryonic
knob does not move down to the opposite side of the blastocyst.
THE PLACENTALIA 551
the trophoblast of the blastocyst comes into contact with the hypertrophied uterine endometrium it promptly erodes the epithelium. A discoidal placenta which is very similar, if not identical, with that described for the Rodent, then develops at the place in question. Later, a
Fig. 283. —— Development of the fetal membranes in Tarsius. From Jenkinson (Vertebrate Embryology). After I-lubrecht.
a. Blastocyst before Rauber’s cells have disappeared. I). The embryonic knob
(e.k.) is being folded out to the surface; the yolk-sac is complete. c. The embryonic
plate (c.p.) is at the surface, the extra-embryonic coelom (c) is formed. (1. The
tail fold of the amnion is growing forward (t.am.), the allantois (all.) has pcnc-'
trated the mesoderm of the bodystalk, a placental thickening has been developed
at the anti-embryonic pole. e. The amnion is closed and the body-stalk or umbilical
cord (u.c.) is shifting its position, to be attached to the placenta (pl.).
second similarly shaped placenta may form where the blastocyst comes
in contact with the opposite side of the uterus. The umbilical cord, of
course, reaches only one of these, but the two are connected by blood
vessels (Fig. 283, only one placenta in this case). ‘
Considering now the second group, i.e., the higher Apes and Man, it
unfortunately happens that as regards the earliest ‘stages relatively little
is definitely known, chiefly because of the scarcity of material. Some of
552 EARLY MAMMALIAN DEVELOPMENT
the earlier classic cases which have been studied comprise the Miller
blastocyst Streeter (’26) with an estimated age of ll days and a diameter of 0.4 mm., the Bryce-Teacher blastocyst, estimated age 12—14 days,
diameter 0.64 mm., and the Peters blastocyst, estimated age 14-15 days.
diameter 1.1 min.” Somewhat more recently others have been added to
m. b.v. _ d. b. tr.
d. r. ep.
Fig. 284.——Early Human embryo with its membranes. From Jenkinson (Vertebrate Embryology). After Peters. "
am.c. Amniotic cavity. c. Extra-embryonic coelom. d.b. Decidua basalis (serotina). d.r.ep. Uterine epithelium covering the decidua reflexa or capsularis. l. Lacuna in trophoblast (tn). gl. Uterine gland. m.b.v. Maternal blood-vessels opening
here and there into lacunae. cl. Clot marking (probably) the point of entrance of
theblastocyst; here the uterine epithelium is interrupted. y.s. Yolk-sac.
the list, all of about the same or slightly greater estimated age. Thus
there is the Werner (Stieve) blastoeyst at 12 days, and the EdwardJones-Brewer blastocyst (Brewer, ’37) at 15 days with internal dimensions of 1.85 x 1.71 x . 1.01 mm., and the previously mentioned
Martin-Falkner hlastocyst, estimated age 17 days with possible abnormalities. Latest of all, are the Hertig-Rock blastocysts, one of which (not
shown in the figures) is estimated at about 7 days, the youngest yet dis
15 Whether some of these specimens have quite reached the blastocyst stage is
perhaps open to question: but they are certainly not “ ova ” as they have sometimes
been designated. ' '
v
»
__ .... _,.,, A,.,._
THE PLACENTALIA 553
covered (Hertig and Rock, ’4l; Figs. 281, 282). The additional data
from all the clearly normal sources, however, has not substantially modified the conclusions previously held concerning the early stages already
described, and the processes about to be discussed. From information
obtained from these early specimens, and from conditions which are
known to exist later on, implantation and development both in Man and
the higher Apes is thought to be as follows:
The blastocyst usually becomes attached to the dorsal (i.e., posterior)
wall of the uterus in Man, and to the ventral (i.e., anterior) wall in the
Apes; here the trophoblast promptly starts its work of erosion. In this
case, however, the process goes much further than in the instances so far
noted. In fact, it is thought that by this means the blastocyst becomes
completely buried in the mucous layer of the uterus, while the epithelium closes behind it. It thus virtually occupies the position of an
internal parasite within the uterine tissue (Fig. 284). As growth now
proceeds, the blastocyst, covered by a layer of uterine mucosa and some
epithelium, begins to project into the cavity of the uterus. Meanwhile, it
appears that changes are taking place in the trophoblast, or chorion, as
it may be called, quite similar to those which occurred in the Rodent,
i.e., a thickening, and the formation of lacunae. In this case, these processes by which the trophoblast is thus converted into the trophoderm at
first occur on every side of the blastocyst. Presently, however, the trophodermal development becomes much more marked on the inner side,
i.e., that side away from the cavity of the uterus, and it is here that the
permanent discoidal placenta is soon formed.
Throughout the trophoblast or chorion (now trophoderm) but especially on the placental side, the embryonic blood vessels, surrounded by
a sheet of connective tissue (chorionic mesoderm), are working their
way among the lacunae, into some of which they project. These vessels
and their connective tissue are covered with a’ thin trophodermal cell
layer known in human embryology as the cell layer of Langhans. Outside of this, there is an added layer of the trophoderm which is syncytial,
and is apparently derived from the cells of Langhans, the latter being
gradually used up. Thus, where the blood vessels, pushing their trophodermal and mesodermal layers before them, project into the lacunae,
they have something like the appearance of villi, and are often so referred to (Fig. 285). It should be clearly understodd, however, that
these “ villi” are in no sense homologous with the true villi described
in connection with the indeciduate placenta of the Ungulates. They are
not indeed essentially different from the capillaries‘ which push into,
554 EARLY MAMMALIAN DEVELOPMENT
Fig. 235.~— Diagrams illustrating the development of the “villi” in the Human
placenta. From Kellicott (Chonlate Development). A, B. After Peters. C. After
Bryce. A. Chorionic mesodetm just beginning to extend into the villi. B. Mesoderm
invading the villi which are now branched. Layer oi Langhans cells forming beneath the syncytintrophoderm. C. Continued branching of the villi, all now covered
only by the syncytiotrophoderm and the single layer of Langhans cells.
_ b. Decidua basalfs. cb. Capillaries of the decidua basalis. cv. Capillaries of the
villi. e. Endothelium of the maternal capillaries. f. Fibrin deposited at the junction of the trophoderm and decidua basalis. i. lntervillous cavity (i.e., lacuna or
sinus) filled with maternal blood. L. Langhans ‘cells. In. Chorionic mesoderm. s.
Syncytiotrophoderm. t. Trophoderm. 1:. Villi. vf. Fixation villi, i.e., those which extend clear across a sinus.
THE PLACENTALIA 555
Fig. 286. —A. A diagram of an idealized section through the inner portion of the
wall of the non-pregnant uterus a short time previous to the beginning of menstruation. The muscular layer is very thick, and only a small portion of it is shown.
Beyond this layer on the outside of the uterus would come the peritoneal covering
or serous membrane which here as elsewhere is quite thin. B. A diagram of a similar section through the Human placenta at a slightly later stage than that shown
in Fig. 2§S {according to Jenkinson). The trophoderm, it will  mired, has pen.
etrated slightly into the compacta in this stage, so that the_ villi are more firmly
attached. Note that these “ villi ” are quite different in their relation to the niaternal tissue from that observed in the Ungulates, (Compare Fig. 271). No attempt
has been made to distinguish between affereiit and efierent hlood vessels, although
itdis to be understood that both types exist on both the embryonic and maternal
si es.
.bc. Blood capillaries in the mucosa. c.l.L. Cell layer of Langlians, still clearly in
evidence. Chr. Chorion consisting of trophoderm plus extra-embryonic imz.-tvoderm.
co. Compacta. d. Decidua; for explanation of terms see further in text. f.bz-. Fetal
blood vessels. m. Muscular layer of uterus, or muscularis, ,only a small portion of
which is shown. mbv. Maternal blood vessels. n.ugl. Necks of uterine glands in the
compacts. s. Sinus lined by syncytial trophoderm, and filled with maternal blood.
That the syncytial layer and cells of Langhans line the sinuses on the side of the
decidua is questioned by some authors. sp. Spongiosa. str. Syncytial trophoaerm.
tunes. Tgophodelrrlrlial ”(chorionic) rnesoderm. u.ep. Uterine epithelium. u.gl. Uterine g an s. v. i us.
1
556 EARLY MAMMALIAN DEVELOPMENT
and are hence covered by, the trophodermal material in the Mouse or
Rabbit. As regards the lacunae, they are again filled with maternal
blood, and are often termed “ sinuses.” They also are lined by a syncytial layer of the trophoderm augmented to some extent by a layer of the
cells of Langhans, similar to, and continuous with, that which covers the
connective tissue of the fetal
capillaries (J enkinson) .
Outside of the discoidal placental region, the whole blastocyst is growing out so as to
fill the"cavity of the uterus
(Figs. 287 and 288) . Its wall
in this area consists internally
of extra-embryonic mesoderm,
and externally of the trophoderm, the two together as
usual constituting‘ the chorion,
while within this chorionic
trophoderm the “ villi ” and
lacunae are only slightly developed. Lastly, tightly adherent to, and covering this
trophoderm, comes the uterine mucosa and epithelium
which covered the blastocyst
after its embedding in the
Fig. 287.——-Human embryo of the fourth uterine wall‘ A5 growth con’
month in ulero, showing the arrangement of tinugs, this epithelium is even.
the membranes and placenta. From Kellicott
(Chonlate Development). After Strahl. many bound to come in con‘
c. Chorion and amnion. p. Placenta. LL. tact with that which lines the
Umbilical Cord‘ walls of the uterus at other
points. By the time this occurs; however, the uterine epithelium and
mucosa covering the growing blastocyst has become distended and is
disappearing. Thus the trophoderm of this region is brought into direct
relations with the epithelium which elsewhere still remains on the walls
of the uterus, and this epithelium too presently disappears. Concurrent
with the complete filing of the uterus and the disappearance of all its
epithelium the chorionic layer of the blastocyst is everywhere united to .
the sul)-epithelial mucosa of the uterine wall. It is only in the region
THE PLACENTALIA 557
I.-u.
d. v.
Fig. 288.—Diagrammatic section through the pregnant human uterus and embryo at the seventh or eighth week. From Jenltinson (Vertebrate Embryology).
After Balfour, after Longet.
am. Amnion. a.m.c. Amniotic cavity. The latter has enlarged until it occupies
nearly all of the extra-embryonic coelom (c), the amnion being reflected over the
umbilical cord (u..c.) and yolk-sac (y.s.). The yolk-sac, it will be noted, is very
small. d.b. Decidua basalis (serotinal, in connection with which the trophoderm or
chorion, represented everywhere by fine stippling, gives rise to the placenta. Thus
the chorion in this region is the chorion frondosum. d.r. Decidua capsularis (refiexa), consisting of a thin layer of. uterine epithelium and mucosa. It soon disappears, exposing the vacuolated trophoderm (chorion) beneath, which in this region
becomes the chorion laeve. d.v. Decidua vera, whose epithelium also disappears
when the trophoderm beneath the capsularis (chorion laeve) comes in contact with
it. Lu. Lumen of uterus, presently obliterated. o.d. Oviduct whose direction in the
non-pregnant uterus would be nearly horizontal. pl. Placenta; for details see Fig.
of the placenta, however, that the chorion normally continues to be
vascularized and to thicken by the growth of villi.
The placenta, as so far described, consists then essentially of a greatly
thickened layer of trophoderm containing lacunae or sinuses filled with
maternal blood, while into and across these sinuses extend chorionic
processes or “ villi” containing fetal connective tissue and capillaries.
The layer thus indicated is obviously essentially tissue of embryonic
origin, and is sometimes known as the “ placenta proper.” Between it
and the muscular wall of the uterus there still exists a certain amount of
558
EARLY MAMMALIAN ‘DEVELOPMENT
the uterine mucosa, i.e., that part of the mucosa which the trophoderm
has not destroyed. It now remains to state that in some of the higher
Apes and Man (as well as in certain of the lower animals already discussed, e.g., the Cat) this portion of the ‘mucosa is itself differentiated
Fig. 289. —— Reconstruction of a human embryo of 2.6 mm. From Minot
(Laboratory Text-Book of Embryology). After His.
/1. Aortic limb of heart. All. Bodystalk. A0. Dorsal aorta. Au. Umbilical arteries. Car. Posterior cardinal
vein. Jg. Anterior cardinal vein
(internal jugular). Om. 0mphalomesenteric vein. op. Optic vesicle.
or. Otocyst. V It. Right umbilical vein.
This completes the description
into two main layers. The outermost
of these layers adjacent to the muscularis is filled with glands, and is
known as the spongiosa. The second
layer, to which the trophoderm is
firmly adherent, and in which it is in
fact slightly embedded, is occupied
by the straighter smaller portions of
these glands, i.e., their necks, and is
called the compacta (Fig. 286).
Moreover, the compacta and spongiosa not only exist in the region of
the placenta, but likewise at all other
points around the uterine wall.“
Thus, when the non-placental trophoderm of the enlarging blastocyst
eventually comes into contact with
this wall from which the epithelium
soon disappears as indicated in the
preceding paragraph, it becomes here
also adherent to the compacta. During the later stages of pregnancy,
both the compacta and spongiosa
tend to degenerate and to become
stretched and thin. It is then through
the region of either one or both of
these layers that the tissue breaks at
the time of parturition.
of the placenta and the adjacent re
gions in Man and the Apes. It remains, however, to indicate the names
by which the various parts are known in human embryology. To understand the significance of this nomenclature, the student must bear in
mind the older idea that placentas of this type were truly deciduate.
16 The spongiosa and compacts indeed occur not only in the pregnant Primate
uterus, but in the non-pregnant uterus as well, particularly just previous to men
struation.
THE PLACENTALIA V p . 559
That is, it was thought that a large part of the uterine wall was deciduous, i.e., torn away or shed at parturition. Hence those layers of the wall
(i.e., the mucosa) which were supposed so to behave were termed the
decidua. Also in correlation with this idea, most of the placenta and the
covering of the blastocyst was supposed to be formed out of this decidua,
rather than out of trophoderm. With this in mind, the reasons for the
following names are fairly
evident:
That part of the uterine
wall to which the placenta is
attached is known as the decidua serotina, or decidua
basalis (Fig. 288). The portion of uterine mucosa and
epithelium which, during the
earlier development, covers
the blastocyst on the side opposite the placenta, is called
the decidua reflexa or decidua
capsularis. That is, this portion is, as it were, reflected
Fig. 290.—Human embryo of about 23 days
(4.0 mm.). From Minot (Laboratory Text
over the blastocyst, forming 300/t of Embfyolvgfb After His ‘Emb1‘:v'0 0)
. dl. Fore-limb bud. BS. Body-stalk. Op. Op31 cover or capsule for It‘ tic vesicle. pl. Hind-limb bud. IV. Fourth ven
L t1 the 1-emainin art of tricle of brain. 1. Mandibular process. 2. Hythaes uiérine wan witghpwhich oid arch. 3, 4. Third and fourth visceral
arches.
the thin chorion, now lack
ing the overlying decidua reflexa, finally comes in contact, is known as
the decidua vera, and as this contact occurs the decidua Vera disappears down to the compacta. Not only are the parts of the uterus thus
named, but the parts of the chorion are also defined. That part which
forms the placenta and adheres to the decidua serotina is termed the
chorion frondosum. The remainder, at least after its loss of the first
slightly developed “ villi,” is the chorion laeve.
Comparing the means of embryonic nourishment in the Primates with
those in the Rodents, there appears at least one notable difference. In
the Rodents the yolk-sac probably plays at least some part in obtaining
nutriment for the embryo throughout development; in“the Primates (except the Lemurs), on the other hand, this function, as well as that of
respiration, is entirely subser-ved by the placenta. Coming to the actual
structure of this organ itself, there exists a striking similarity between
560 EARLY MAMMALIAN DEVELOPMENT
the two orders. There is also, however, a slight difference here, which is
perhaps worth noting. At the time of parturition in the Rodents scarcely
any maternal tissue, save blood, is lost, and hence the placenta is not at
all deciduate in the strict sense of the word. In the Primates, on the
other hand, there is a certain amount of the compacta and perhaps of
the spongiosa lost at birth, and this is maternal tissue. Hence the Primate placenta, at least to this slight extent, may be said to be truly deciduate. The body—stalk in the two groups is in general similar in lack
ing any extensive endothelial element. As has been noted, however, its
method of formation is different.
15
EVELOPMENT OF THE PIG TO THE TEN MILLIMETER STAGE
I N the preceding comparative discussion of the early stages of various representative groups of Mammals we have carried the history of
the Pig in particular to about the thirteenth day of its development.
This means of course thirteen days from the time of fertilization in the
upper part of the oviduct. During this time, as we have seen, the egg has
reached the uterus, developed into an elongated blastocyst, and the
blastocyst is becoming implanted. The embryo itself is represented by a
blastoderm in which a primitive groove and notochord are evident, and
in which the three primary germ layers have already been diHerentiated as previously described. The nature of the archenteron, and its re
lation to the blastocoel has also been indicated.
Having reached this point, we are now prepared to proceed with a
description of the further development of this animal. In doing so we
are once more faced with the problem of whether to describe the complete development of one system at a time, or to carry all systems along
together as it were, in a series of stages. For fairly obvious reasons it is
not practical in the case of the Mammal to proceed very far by daily
periods. Furthermore, through study of the Frog and Chick we are now
familiar enough with the vertebrate plan of development so that we are
aware in a general way of what other systems are doing while we concentrate our attention upon one. For these reasons a sort of compromise
between the system plan and the stage plan becomes possible. Beginning
at the present point therefore we shall carry each system of the Pig to
completion in two main steps. The first step will take us to the condition which exists at the 10 mm. stage (20-21 days), a condition more
or less comparable with that of a 4-5 day Chick. The second step will
then bring the system in question to completion, or as near to it as it is
necessary to go. As we proceed with these steps, however, it is desirable
from time to time to mention the number of somites present, and also
the approximate length of the embryo. In the latter connection certain
facts concerning the general form of the animal need to be mentioned,
562 THE PIG TO TEN MILLIMETERS
and we shall take those up at this point, together with a few comments
on other external features.
Embryonic Flexions and Rotation. — As in other Vertebrates, so
in the Pig, the very early stages pose no question as to what line constitutes the longitudinal embryonic axis. This is obviously indicated by
the line of the primitive groove and notochord, and presently also by
the line of the fused neural folds, and the contours defined by the folding oil of the embryo. This simple condition persists up to about the
ten somite stage, when the
embryo is approximately
fifteen days old and measures from 3 to 4.5 mm.
in length (Fig. 291).
Shortly after this, how="¢U"3' §"°°V° ever, as in the Bird, vari
 
 
     
 
T‘ eural fold
Cgtedgfi “ ous curvatures begin to
o ammon .
:- r , , develop, and certain flex
; smus rhomboldahs . _ d
pmnmve streak: ures are again recognize .
The cranial and cervical
flexures are the same as
in the Chick, and in addi
Fig. 291. — Surfacfi View of a Pigf ernbrylp fofd7 {ion two others are named
somites (3 mm.), 5 owing c osing o neura 0 s. . . .
Amnion removed. After Keibel. whlch mlght 3150 be de5‘g'
nated in the Bird, but usually are not. These are the dorsal and lumbo-sacral flexures which refer
simply to the successively more posterior parts of the continuous curvature. The caudal flexure mentioned in the account of the Chick also
exists in the Mammal as a continuation of the lumbo-sacral flexure, but
is not generally especially designated (Fig. 294-). It should also be
noted thatlfor a brief interval before the caudal and lumbo-sacral flexures develop there is, as was also true of the Chick, a slight ventral bend
in the m_id—body region due again apparently to the pull of the yolkstalk (Fig. 292). This, however, is quite transitory. As soon as these
curvatures develop the question at once arises as to which of the infinite
number of straight lines which might be drawn through the embryo is
to be designated as its length. In Mammalian embryos, including Man,
there are two such lines which are quite commonly used. One is a line
passing from the most anterior point of the cranial flexure (mid-brain)
posteriorly through the “ rump.” The latter may be defined as a point
at about the middle of the convexity of the lumbo-sacral flexure, i.e.,
3
EXTERNAL FEATURES 563
somewhat posterior to a point dorsal to the origin of the hind-limbs.
This line of measurement is the crown rump axis. The other is a line.
from the posterior side of the cervical flexure, i.e., just over the ear,
anteriorly, and again terminating at the rump posteriorly. Because of
the position of the anterior point above the ear this may be called the
auricular rum p axis. All measurements referred to in this account will
be those of the straight embryo previous to the development of its flexures, and
later those of approximately the crown rump
axis.
In this general connection one further matter pertaining to the curvatures of cut edge
Mammalian embryos may ‘a’:‘3':h";‘:i';n;.
be mentioned, though it i»
has no reference to the E
problem of measurement.
It will be recalled that
when the Chick developed
its various flexures it also _ 1
acquired a lateral rotation .  under chorion
or torsion. In that case this i " ‘
rotation prevented the
burying of the anterior end Fig. 292. -— Surface view of a Pig embryo with
. about 16 somites (4.5 mm.), showing outpush“1 the yolk‘ In the Mam‘ ing of allantois beneath chorion. After Keibel.
cut edge
of yolk sac
 
mal of course there is no
yolk, but it is an interesting fact that the lateral torsion still takes place
to some degree (Figs. 292, 293). It is quite variable, as all vestigial structures and activities are apt to be, and soon vanishes entirely.
Other External Features.—Finally before proceeding to a dis-.
cussion of the specific systems a few further remarks are pertinent with
regard to general external features, aside from the various curvatures.
As will be apparent from Figure 294, four visceral arches and four
“ clefts ” are in evidence, while about the two posterior clefts is a general depression termed the cervical sinus. As sections‘ reveal, however,
these are not true cleft's since they do not normally actually open
through into the corresponding visceral pouches, but- it is convenient to
refer to them as such. Also from the figure itmight at first be supposed"
564 THE PIC TO TEN MILLIMETERS
that there are five-clefts and five arches rather than four. The apparent
first cleft, however, is really the space between the maxillary process
and mandibular arch, and is therefore not counted as a cleft, nor is the
maxillary process an arch. Immediately anterior to the maxillary process is still another depression separating this process from the front
parts of the face (see below). This depression is the lachrymal groove.
At its dorsal end is the eye, and at its ventral end the nasal pit. In this
connection it may be appropriately noted that one of the few rather
striking difierences between the appearance of the head of a 4-5 day
Chick and that of a 10
 
hyomndibuhr def‘. ':- mm. Pig is the much
auditory Pit Jolt ,3; greater size of the eye in
2nd  optic vgfldg the Bird.
"l“°"l‘l°f“ 3rd 0" i Viewing the embryo
somites'  llnmd‘ from the front it will fur.
amnion;
ther be seen (Fig. 295i
_‘ that antero-ventral_t.o,the
; eyes, between them and
‘ the olfactory pits, lie the
naso-lateral processes,
which as in the Bird
bound the pits laterally.
Medially the pits in the Pig are bounded by the naso-medial processes,
structures not indicated in the Bird. A comparison of these forms, however, reveals that these last named processes are really only special differentiations (prominences) of the lateral parts of the naso-frontal
process, which in the Chick is shown bounding the pits on their medial
sides. In the Pig the region between the naso-medial processes, i.e., the
middle of the “ naso-frontal process ” is sometimes termed simply the
frontal process. However, this region is soon (10 mm.) merged with
the naso-medial processes which may then be said to join each other in
the mid-line. The oral cavity of the Pig soon appears therefore as an
opening immediately beneath the fused naso-medial processes. This cavity as usual is bounded ventrally by the mandibular arches, while the
maxillary processes are pushing into it from either. side. The latter are
separated from the naso-lateral processes by-the lacrymal groove.
Finally, among external features of the 10 mm. Pig, are the prominent paddle-like fore and hind limb buds and the numerous well-marked
somites. Both of course are highly reminiscent of the appearance of
these structures in the Chick in a corresponding stage.
 
Fig. 293.-—Surface view of a 3.5 mm. Fig embryo
with chorion removed to show allantois. After
Keibel.
NERVOUS SYSTEM: EARLY DIFFERENTIATION 565
THE NERVOUS SYSTEM
As in the case of the Chick, much of the general form of the early
mammalian embryo, as well as various prominences appearing upon it,
are determined by the developing nervous system. It is therefore convenient to consider this system first.
Illrd viscera! arch
h 'd
Nth visceral arch yo. arch
 
 
 
 
'mandibu|ar arch
cervical sinus
forblimb bud - maxillary process‘
33% 5. :2 6””
7 mm. erribryo
Fig. 294.—Lateml View ‘of a 7 mm. Pig embryo with amnion and
chorion removed.
EARLY DIFFERENTIATION
The System as a Who1e.—The nervous system first appears in
embryos of about 2 mm. as the usual groove in an ectodermal medullary plate immediately anterior to the primitive streak (Fig. 264).
Slightly later definite folds arise upon either side of this groove in essentially the same way as in the Bird (Fig. 291). The location where
the folds most closely approach each other represents the future hindbrain region, while the wide open part immediately anterior to this is
the future fore-brain. The neural tube proper is obviously not yet repre566 THE PIG TO TEN MILLIMETERS
sented, which means that the anterior parts of the system are as usual
the first to form, and as in other cases maintain their advantage in precocity till very late in development. It will be noted that the chief difference between the situation in the Chick and the Pig at this stage is the
wider flare of the folds in the anterior region of the latter. Slightly later,
 
   
 
frontal PTOCCSS
olfactory plt
naso-lateral process _ '
- naso~medlaI process
maxillary process
mandibular arch
hyomandibular clef:
hyoid arch
lllrd viscera! arch 1
from 7 mm. embryo
Fig. 295.——Antero-ventral view of the head of a 7 mm. Pig embryo
showing parts constituting jaws and face.
at about 10 somites, another difference becomes evident in that, as previously stated, the optic vesicles of the Pig are much less prominent than
were those of the Chick at a comparable stage, and this remains true
throughout the earlier periods of development. As will be apparent from
the figures, these vesicles, at their earlier stages, are also somewhat differently shaped from those of the Bird.
DIFFERENTIATION TO TEN MILLIMETERS
The Brain. —— Following this early condition the cranial flexure
makes its appearance (13 somites), and shortly thereafter the cervical
and caudal flexuresiare also under way. Thus by the 25 somite stage the
anterior extremity is almost touching the heart in about the manner of
NERVOUS SYSTEM: TO TEN MILLIMETERS 567
a 48-hour Chick with the mid-brain at approximately the most anterior
point of the embryo. By this time also the various divisions of the brain
are evident, and are the same as those in the Bird, i.e., the prosence phalon, mesencephalon and rhombencephalon. As will presently be noted
these main parts are soon further subdivided, and give rise to the same
structures as enumerated in the previous form. Thus at 10 mm. (Figs.
296, 297) about the same degree of development of the brain exists,
with the same parts in evidence as in a 4-5 day Chick. The proscncephalon is divided into telencephalon and diencephalon, and the former is
giving rise to outgrowths (telencephalic vesicles) which will become the
cerebral hemispheres. The diencephalon, which is separated from the
telencephalon by the same features as characterized the Bird, has, as
before, given rise to the optic vesicles and the infundibulum. The chief
difference between this part of the Pig brain at this time, and that of the
4-5 day Chick, is the lack of an epiphysis in the Pig, in which it does
not appear until considerably later. The mesencephalon is as usual 3.
very prominent region whose protruding anterior side marks the apex
of the cranial flexure. It is, however, not so well developed as that of the
Chick at a corresponding stage. This is correlated with the fact that this
region is the site of the future optic lobes of the Bird, which are more
prominently developed than the partially comparable ‘corpora quadrigemina of the Mammal. A sharp fold, the isthmus, separates the mesencephalon from the following rhombencephalon, and the division of ‘the
latter into metencephalon and myelencephalon is now distinguishable
by the thickened sloping roof which characterizes the former (Fig. 297).
The Neural Tube and Crests. —- Passing posteriorly we find that,
as in the Frog and Chick, the neural tube has been formed by the closing neural folds so that its dorsal and ventral walls are thin and its lateral walls relatively thick. By the 10 mm. stage the cells in these walls
are becoming differentiated into several different types, some of which
have already been mentioned in the case of the Chick. Near the delicate
internal limiting membrane lining the neural canal the original germinal cells have given rise to spongioblasts and the latter to supporting
cells with long fibers running toward the outer periphery of the cord.
Again as in the Bird these supporting elements are called ependymal
cells. The larger part of the cord, however, is occupied at 10 mm. by
the mantle layer, consisting of other germinal cells in process of further
division and differentiation as follows: Some of the germinal cells become spongioblasts which in this layer eventually form other types of
supporting cells known as short and long-rayed astrocytes. The remain568 THE PIG TO TEN MILLIMETERS
tier of the germinal cells in the mantle layer are neuroblasts which later
differentiate into actual nerve cells. Finally outside the ependymal and
mantle layers, beneath a thin outer" limiting membrane, there occurs a
non-nucleated region termed the marginal layer. Because of the lack of
myelencephalon Vlllth and Vllzh (genleulate) ganglia
 
   
 
 
lX“(‘ 8‘"8l:)°" audkor), “Sid, metencephalon
Xth gangllon jugula . '¢ Vth(Gasserian) ganglion
' A lVth nerve
Xlth spina'laccess_ory nerve '5ml°'::;";‘°:;:l°"
Fig.1” Frorlep sgangluo . F3’. 2”
xnth-he.-.,¢.,-00;; - ophthalmic nerve
petrosal ganglion
. maxillar nerve
ganglion nodosum  Y
‘ 'diencephalon
Fig. 302 ' F?s- 302
xth nu,” / Rathke's pocket
esophagus ‘ Seesell‘s pocket
' OptIC cup
Fis_ 3°“ ‘ ' Fig. 301
_mng telencephalon
F‘ 305 W c:narndIib‘ular n rveF;'_ 305
---?{7;--— ° 3 0 Y P yuzel Inelyolldstalk
533.306 Fin» 306
t ch " - _
*a:t":..a 3» 3;;
d°rsa s allantoie stalk
, Fig. 3l0
FIg.3l0
l ncreas .
ventrzamabladder postncloacal gut.
Fig. an “9~ 3"
:a,.:m “-9- 313
l
spinal ganglion C mm
mesonephros
nephrogenous tissue of metancphr
mcsonephricvduct
Fig. 296.——Reconstruction of a 10 mm. Pig embryo, designed to show primarily
the main features of the nervous, digestive, respiratory and excretory systems at
this stage. Drawing made chiefly from a study of sections, with aid from a wax
reconstruction produced under the author’s direction in the Oberlin College Zoological Laboratory. Lines at the sides with figure numbers over them indicate where
the sections represented in these figures pass through the embryo. By laying a
ruler along any pair of lines the structures cut by the respective section may be
seen. *
nuclei, it stains very lightly compared to the darker more central regions. It will further be noted in sections of the 10 mm. Pig that portions of the mantle layer extend ventro—laterally somewhat, causing the
lower sides of the cord to bulge slightly. These extensions are the beginnings of the ventral horns (Fig. 298).
Aside from the cord itself it will be found, as in the case of the Frog
NERVOUS SYSTEM: TO TEN MILLIMETERS 569
and Chick, that as the neural folds come together a hand of cells is
pinched off between the tube and the overlying ectoderm. The cells of
this band soon become concentrated on either side to form the continuops neural crests. The latter are then further concentrated segmentally
pharynx metencephalon
 
 
 
 
   
 
 
 
notochord
mesencephalon
Ra:h$<e's pocket
v Seesell’s pocket
./ optic chiasma
, Optic recess
lamina terminalis
um bi Iical
artery
vltelline vein
posterio
vena cava
mesoneph ros
dorsal root ganglion
Fig. 297.-—Mid-sagittal section of a 10 mm. Fig embryo.
to form the groups of neuroblasts which develop into the spinal ganglia.
By the 10 mm. stage each such ganglion is clearly defined, and has
given rise to the dorsal roots of the spinal nerves which are definitely
connected with the cord. y
The Cranial Nerves. —— In the 10 mm. Pig all the cranial ganglia
-and nerves are represented except the I or oljactorf, and the II or optic,
the optic stalk not yet containing any actual nerve fibers (Fig. 296).
570 THE PIG TO TEN MILLIMETERS
The III or oculomotor nerves can be plainly seen emerging from the
ventral side_ of the mesencephalon, while the IV or trochelar nerves are
just starting from the dorsal side of the fissure (isthmus) between midand hind-brain. The V or trigeminal nerve ganglion of each side appears on the ventro-lateral side of the myelencephalon near its anterior
end. It is united to the brain by a large root, and from it emerges anteriorly the ophthalmic nerve, while more posteriorly and ventrally arise
 
 
 
       
 
external llmltlng membrane
lumen of
neural tube
mantle layer
prlmordlum of
ventral horn
blood vessel
K
I .- 1.1‘
»‘3 ventralnerve root
~:
internal Ilmltlng Vf
membrane
   
   
Fig. 298.———-Transverse section of the center and right side of the nerve
cord and a spinal ganglion of a 10 mm. Pig embryo.
-the maxillary and mandibular nerves. The entire complex lacks the distinct V shape which it had in the Chick due to the large mass of the ganglion proper which obscures the base of the V. More ventral than the V
nerve ganglion, at about the middle of the myelencephalon the VI or
abducens nerve of either side takes its origin, while above it at about
the level of the V ganglion occur the ganglia of the VII and VIII nerves.
These latter ganglia are somewhat dorso-ventrally elongated structures
much less massive than the V. The VII or geniculate ganglion is very
close to the VIII pr acoustic, but is slightly anterior to it, and the
branches of the VII or facial nerve are little developed at this time. The
acoustic or auditory ganglion in turn is in contact with the auditory
vesicle which lies posterior to it, the short branches of the auditory
nerve not being in evidence as yet. There is no single glossopharyngeal
NERVOUS SYSTEM: TO TEN MILLIMETERS 571
ganglion in the Pig. Instead the erve cells which would constitute this
ganglion are divided into two groups, a dorsal and a ventral. The dorsal
group is in close contact with the posterior side of the auditory vesicle,
and is called the superior ganglion of the IX or glosso pharyngeal nerve.
The ventral group occurs both ventral and slightly posterior to the superior ganglion, and is known as the petrosal ganglion of the same nerve.
As in the Chick, the X or vagus ganglion occurring just behind the IX is
also divided into two parts, the ganglion jugulare and the ganglion
lXth
Xth
   
 
}cranlal nerve ganglion
hind-brain (metencephalon)
1.3-‘
branches of anterior cardinal velni
mid—brain (mesencephalon)
Xlth cranial nerve (spinal accessory)
cndolymphatic duct
Fig. 299.—Transverse section through the brain region, including some of the
spinal ganglia, of a 10 mm. Fig embryo. See reconstruction Fig. 296.
nodosum. The former is so closely in contact with the superior ganglion
of the IX at this time as to be scarcely distinguishable as a separate ganglion (Fig. 299). From it there arise two thick strands of nerve fibers.
The more dorsal of these proceeds posteriorly to meet the XI nerve,
along whose posterior part it extends for a way, as the elongated commissural or accessory ganglion. The second strand passes postero-ventrally, and shortly enlarges to form the ganglion nodosum indicated
above. From the latter the vagus nerve containing both afferent and efferent fibers is evident at this stage proceeding toward the viscera. The
fibers of the XI or spinal accessory nerve, already referred to, also pass
antero-dorsally from the nodosum toward the ganglion jugulare along
with those of the X nerve. Before reaching this ganglion, however, these
fibers branch off in a well-defined strand which curves dorsad, and proceeds along the side of the myelencephalon until it ends in F r0riep’s
ganglion. This latter ganglion later disappears, and the nerve is entirely motor. The XII or hypoglossal nerve is also entirely motor, and
J‘:
572 THE PIG TO TEN MILLIMETERS
hence has no ganglion. It arises as a g oup of fibers ventral to the spinal
accessory, and these shortly unite to form a single trunk (Fig. 296).
The Spinal Nerves. — We have already noted the origin of the dorsal root ganglia and the fibers connecting them with the dorsal part of
the spinalicord. These are of course sensory nerves. The ventral root
motor nervefibers originate in the ventro-lateral portions of the mantle
layer of the cord, whence they emerge opposite each dorsal root (Fig.
298). As in the Chick, they then very shortly join the sensory fibers running outward from the dorsal root ganglion, and from near the point of
union three branches arise. The most dorsal branch of each spinal nerve
is a dorsalsomatic ramus, and the middle one a ventral somatic ramus,
both containing mixed sensory and motor fibers just as they did in the
Bird. The third and most ventral branc-h, also as in the Bird, is a ramus
conzmunicans of the sympathetic system, except in the sacral region
whose communicating rami belong to a part of the parasynz pathetic
system. The cell bodies which give rise to the fibers of all these rami lie,
as in previous cases, within the nerve cord, and are known as preganglionic Izeufanes. On the other hand the neurones ( postganglionic) which
constitute the chain ganglia of the sympathetic and parasympathetic systems to which the fibers of the rami run, have as usual migrated thence
from the nerve cord, the dorsal root ganglia, or both. This is also of
course true of the neurones in the various visceral plexuses. In the case
of the Pig, however, it has not been possible to analyze the exact sources
of these postganglionic and visceral neurones as carefully as in the Frog
and Bird. This is because of obvious limitations on experimental procedure. Also there seems to be no data as to whether the permanent system is preceded by a temporary primary one as in the Chick-. Lastly, in
connection with the parasympathetic system referred to above, it may
be noted that the preganglionic neurones of this system not located in the
sacral region, occur in the brain. The parasympathetic and sympathetic
systems together are often referred to as the autonomic system.
One interesting point concerning the spinal nerves which is true of all
the vertebrate embryos with appendages, comes out especially clearly
inrthe 10 mm. Pig. This is the modification in the original strictly segmental arrangement of the spinal nerves. Though this arrangement is
still marked, the fusing of several branches in their respective regions
to form the brachial and sacral plexuses is very evident. Also the caudal
migration of the appendages is indicated by the fact that the branches
which form the respective plexuses arise from regions of the cord considerably anterior to the limbs which they supply. The caudal movement
DIGESTIVE SY STEM: EARLY STAGES 573
of the diaphragm is likewise evidenced by the anterior origin and backward extension of the phrenic nerve it this stage. In later stages this
nerve continues to follow the diaphragm as it moves posteriorly.
The Organs of Special Sense. — As inthe case of the parts of the
nervous system just described, the organs of special sense in the 10
mm. Fig are also developed to about the same extent as those of a 4-5
day Chick. Thus the olfactory pits already noted in the account of the
exterior, are present opposite the prosencephalon. Further back the optic vesicles have formed cups in the usual manner, and each cup is oc} cupied by a hollow sphere of cells destined to become the lens. As in] dicated above, these forerunners of the eye are definitely much smaller
1 relatively than they were in the Bird, but they have formed in the same
; fashion from the same parts. Likewise the auditory vesicles have arisen
on either side of the hind-brain by invagination from the surface ectoderm in a way already familiar. They are about the same shape as those
of a 5-day Chick with the endolympliatic ducts extending dorsalward in
the usual manner. As in previous cases these parts are in close proxim- .
ity to the hyomanclihular pouch which will form the middle ear and
Eustachian tube (Figs. 296, 299, 302).
THE DIGESTIVE SYSTEM
‘ EARLY STAGES
The Primitive Gut and Related Parts. —— We have already noted
, that in the Pig. as in the Chick. the embryo forms from a fiat plate of
cells by a folding off process. Also by the time this occurs the germ lay‘ ers have arisen and the. mesoderm has been more or less completely split
into the somatic and splanchnic sheets. Hence the innermost layers of
the folds which form the gut will consist as usual of the splanchnic mesoderm and the endoderm (splanchnopleure) . As in the Bird, the folding '
off is accompanied by the outgrowth of the distal rim of the fold, especially anteriorly and posteriorly. Thus the fore-gut and hind-gut are
lengthened (Fig. 300). As in the Bird the proximal rim of the fold, on
the other hand, either remains stationary or actually draws together
i somewhat. Insofar as this latter movement involves the splanchnopleure
Q it produces a great relative narrowing of the yolk-stalk or yolk-sac um‘ bilicus (see Chick, Fig. 190), so that the gut cavity is more and more
I
1
sharply separated from the remainder of the extra-embryonic portion of
the archenteron. The folds of the somatopleure of course follow, thus
narrowing also the somatic umbilicus, or as it is called in the Mammal,
the body stalk, or later the umbilical cord.
574 THE PIG TO TEN MILLIMETERS
In connection with this process there are, however, certain differences
to be noted between the Chick an l Pig. In the first place it appears that
the folding off is somewhat more nearly simultaneous anteriorly, laterally and posteriorly in the Pig than it was in the Chick, though even in
the former the head fold is a little precocious. A second difference is perhaps more striking, and has already been referred to. It is the fact that
at a very early stage the mesoderm develops anteriorly as well as lat
amniotic heiad told
,7
"method Mung PI“: amniotic tail fold
' anal plate
   
 
   
A °"3lPlfl€ periczrdtal coelorn Ik mflodflm
yo 5“ endoderm
chcfionk uaphabhn amniotic head fold neural tube amniotic nail fold amnion
 
eczoder  chorionic trophohlasl
,,,,m°n  notochord  . Fla“ cmdum
\ mesoderm
mesoderm ‘_  ‘O \‘
hind-gut
   
yolk sac mesoderm
yolk sac endod:rm/
perlardial coelom
B
Fig. 300. —-— Diagrammatic mid-sagittal sections through early Pig embryos to
show primarily the method of origin of the allantois which is slightly difierent from
that in the Chick. See Fig. 198. Note also the relatively equal growth of the head
and tail amniotic folds as compared with their unequal growth in the Bird.
erally and posteriorly, so that there is no proamnion region which is
free of it. Hence the mesoderm is involved in the head fold of the Pig
from the first, the same as everywhere else. Still a third dilierence between Bird and Mammal has to do with the behavior of the mesoderm
beneath the forming gut. In both organisms it will be noted that as the
lateral folds of the splanchnopleure press toward each other the layers
of endoderm are the first to meet. Wliereupon they fuse and at once close
off to form the completed endodermal tube, save for the opening of the
yolk-stalk. The splanchnic mesodermal layers of the splanchnopleure
meet next and fuse, but do not close off. Instead they remain as a double
sheet, the ventral mesentery, which unites the gutto the ventral body
wall formed by the subsequent fusion of the somatic mesoderm and
ectoderm. In both Bird and Mammal the dorsal part of this mesentery
persists to help support the heart and liver. In the Bird, however, the
most ventral part, i.e., the part which makes contact with the body wall,
DIGESTIVE SYSTEM: EARLY STAGES 575
it may be recalled, almost immediately disappears. In the Mammal, on
the other hand, this part persists much longer. Indeed in the latter, as
we shall see, some of it exists permanently, and we shall have occasion
to return to it later on.
The Yolk—Sac. — While the folding of the splanchnopleure is forming the gut‘ and yolk-stalk, what remains ventrally of the original archenteric space becomes the yolk-sac. The endodermal lining of this sac
mcdullary plate
 
 
splanchnlc _
mesoderm ‘
somatic mesoderm
chorlonlc trophoblast
Fig. 301.——-Transverse section through a Pig blastocyst cutting the blastoderm
and embryo at the level of the second somite. After Streeter, modified to complete
the blastocyst ventrally. The embryo is the same as that reconstructed in Fig. 265.
and measures 1.56 mm. in length.
has of coursebeen completed ventrally by the growth of this layer clear
around the inside of the original blastocoel. The downgrowth of the
mesoderm followed by its split into two layers, however, proceeds more
slowly. Thus there is a time when this split mesoderm is pushing its
way ventrad and medially from both sides, but has not yet met ventrally (Fig. 301). Shortly, however, it does meet, thus everywhere separating the endoderm of the yolk-sac from the trophoblast by a layer
of extra-embryonic splanchnic mesoderm, the extra-embryonic coelom
and a layer of extra-embryonic somatic mesoderm.
The Allantois. — As the above events are taking place (2—4.5
mm.) , it should be noted that at the posterior end of -the embryo a condition exists which at first seems very similar to that which prevailed in
the Bird. Thus as in that case there is the same fold of the splanchnopleure which in the Bird we have called hind-gut, but which some have
576 THE BIG TO TEN MILLIMETERS
chosen to interpret as allantois. So far as the detailed events in this region have been described for the Pig, however, the subsequent differentiation of the actual allantois and the definitive hind-gut appear to dif~
fer somewhat from the history of these parts in the Chick. Thus in the
latter the original fold constituting the primordial hind-gut (by some
labeled allantois) is, according to our previously stated position, only
partly allantoic. This was on the ground that it is not until after the
tail-bud has swung around to the ventral side that a portion of this re
lnrq visceral‘ arch
Xth cranial nerve
end of 4th visceral pouch
 
 
 
mandibular arch
maxillary process
Pl‘3")’"* _/ i « _ -.  , ' i ‘ portion of
' ' ' ' ‘ ' « cerebral hemisphert,
nerve I'O0C
dorsal spinal ,
nerve root ganglia ‘
cervical nerve
 
anterlor cardinal veln
3rd vlsceral clef: hyommdl I "I" dd‘
Fig. 302.—Transverse section through the eye and visceral arch region of a 10
mm. Pig. See reconstruction Figs. 296, 318, 320.
gion gives rise to an anterior outgrowth which is entirely allantoic. In
the Pig, on the other hand, all of the original posterior fold continues
its backward growth to form allantois. Shortly afterward another fold
develops in the dorsal splanchnopleure slightly anterior to the allantoic
outpushing, and grows posteriorly above the latter to form the definitive
hind-gut (Fig. 300). '
FURTHER DEVELOPMENT OF THE GUT
The Stomodaeum. — As in the Chick the fore-gut does not at first
open to the outside. Soon, however, the ectoderm becomes invaginated
to meet the endoderm at a point slightly posterior to the extreme end of
the gut. This invaginated ectoderm is as usual the stomodaeum, and the
double membrane formed by its fusion with the endoderm is the oral
plate. Sometime between the 15 and 25 somite (4.5—-6.5 mm.) stage, this
plate breaks through, and puts the stomodaeal cavity in communication
with the future pharynx. The short portion of gut extending anterior to
the stomodaeum isii temporary structure known as the pré-oral gut, or
FURTHER DEVELOPMENT OF THE GUT 577
in the Mammal as Seesel’s pocket (Figs. 296, 297) .’ The stomodaeum itself later gives rise to the oral region involving the nasal, maxillary and
mandibular processes. At 10 mm., however, the only structure which it
has produced is an anterior outgrowth in the direction of the infundibulum of the brain. This diverticulum, as in the Chick, is Rathke’s pocket,
Fig. 303.——Reconstructions of the developing bronchi of a Pig’s lung at the
stages indicated. After Flint. The arteries and veins, though only labeled in one
figure, are represented in the same manner in each.
and is of course, the primordium of the anterior part of the pituitary.
(See footnote on this topic in the section on the Frog.)
The Pharynx.——This region of the gut is rather shallow dorsaventrally, and at an early stage begins to show the lateral outpocketings
which form the visceral pouches. There are usually four pairs of these
in the Pig, the hyomandibular and three posterior to that pair, though
, the last (fourth) pair aresmall and sometimes entirely lacking (Fig.
302). In a 10 mm. specimen all the pairs destined to appear are well
developed, and have come in contact with the corresponding ectodermal
“ clefts ” (Figs. 294, 296). As already indicated, in the case of the Pig,
it is to be noted that, as in most other Mammals, these regions of con578 THE PIG TO TEN MILLIMETERS
Xth cranial nerve endocardi! cushion
ductus Cuvier valvulae venosae
Fig. 304.—~Transverse section through the heart and trachael region of a 10 mm. Pig. See reconstruction Figs. 296, 318, 320.
esophagus
   
mesonephros
“mg posterior vena cava
subcardinal vein
Fig. 305. ——Transverse section through posterior of heart and the
lung region of a 10 mm. Pig. Umbilical stalk not included in figure. See reconstruction Figs. 296, 318, 320.
FURTHER DEVELOPMENT or THE GUT 579
tact seldom become perforated, so that no real visceral slits are formed.
In occasional instances, however, such perforations do occur even in
Man, as reminiscent anomalies, while in the Cow the second pair regularly develop slits for a brief period (Anderson, ’22).
The Trachea and Bronchi. — Just posterior to the visceral
pouches the pharynx develops a deep ventral groove which, as in the
stomach
fore- limb bud
     
left umbilical vein(ductus venosu§
coelom
ericardial cavity
ventricle
ventral vein of mesonephros
Fig. 306.———Transverse section through the region of the stomach, liver, and posterior tip of heart of a 10 mm. Pig. See reconstruction Figs. 296, 318, 320.
Bird, is the laryngo-tracheal groove. As in that case also it shortly hecomes converted into a separate tube the trachea, which at the 7.5 mm.
stage has already produced a couple of outgrowths at its posterior end.
These of course are the primordia of the main bronchi, though they are
commonly referred to as lung buds. At 10 mm. they in turn are just
starting to give rise to stubby outpushings, the beginnings of the branchial tubes (Figs. 296, 303, 304, 305).
The Esophagus and Stomach. —— Above the trachea the part
which remains after the former structure has been pinched off beneath
it, is the esophagus. Between the 5-10 mm. stages a dilation develops
in the enteric tube at the posterior end of the esophagus just behind
the limb buds. It is the beginning of the stomach (F igs.296, 306).
580 THE  TO TEN MILLIMETERS
The Liver and Related Parts. ——- In the Pig the liver primordium
arises as a single rather wide diverticulum from the ventral side of the
gut immediately caudal to the stomach region (duodenum) at about the
4 mm. stage. In the Bird, it will be recalled, there were two original
hepatic outgrowths. The single outgrowth of the Pig, however, very
shortly gives rise to several anteriorly directed buds which grow out ,
into numerous hepatic ducts. The posterior part of the same outgrowth
becomes extended as the cystic duct while its end enlarges as the gall
Fig. 307.—Reconstruction of the stomach, dorsal
and ventral pancreas and gall bladder of a 10 mm.
Pig, enlarged from Fig. 296.
bladder. The anteriorly growing hepatic ducts and the posterior cystic
duct remain connected with the gut by the original single outgrowth
which becomes extended as the common bile duct or ductus cholcdochus (Figs. 296, 307, 308, 309). All these structures, it should be
noted, do not just lie freely in the coelom, but are, as in the Chicl-:, embedded within the ventral mesentery whose existence in this region has
_ beenipreviously explained. Their development to the pointindicated
occurs between the 5-10 mm. stages.
The Pancreas. -— At about the same time that the liver diverticulum
first appears (4 mm.) a dorsal evagination occurs, in this case within
the‘ dorsal mesentery, and slightly posterior to the liver outgrowth. It is
the dorsal part of the pancreas. At 5 mm. a single ventro-lateral pancreatic rudiment has grown out from the ductus choledochus near the point
of union of the latter with the gut. It may be recalled that in the Chick
there were two of these ventro-lateral. pancreatic primordia from the
common bile duct,'as well as the single dorsal one. At 10 mm. each
single dorsal and ventral pancreatic primordium in the Pig consists of
numerous -budding cords of cells, and the two parts are almost fusing
(Figs. 296, 307, 308, 309).
FURTHER DEVELOPMENT OF THE GUT 581i
The Mid-gut Region.——Immediately posterior to the liver and
pancreatic diverticula the intestine of the Pig, like that of the Chick,
turns ventrad. It proceeds in this direction as far as the origin of the
yolk-stalk, and then passes dorsad again to the region of the rectum. By
the 10 mm. stage the gut in this region has become a rather small tube,
. and its ventral bending has become a very clear cut loop whose sides
are quite closely‘ approximated. At the most ventral point of this loop,
30,53‘ Pancreas ventral vein of mesonephros
Pegterior cardinal v
 
posterior vena ca
8l°m hepatic portal vein
Fig. 308.——Transverse section through the region of the
anterior and of the mesonephros, the bile duct and liver of
a 10 mm. Fig. Umbilical stalk not included in figure. See
reconstruction Figs. 296, 318, 320.
from its rather sharp apex, the yolk-stalk still takes its origin. By this
time, however, this stalk is extremely constricted to form an even
smaller tube than the intestine, and the yolk-sac at its extremity exists
merely as a shriveled vestigial diverticulum within the body-stalk (Figs.
296, 297, 309, 310). In some instances at this time a small enlargement
appears on the posterior ascending limb of the loop. It is the beginning
of the caecum.
The Hind-gut Regi0n.——_,-Continuing posteriorly it has already
been noted that an evagination or fold has arisen in the dorsal wall of
the splanchnopleure of this region just anterior to the allantoic outgrowth to form the hind-gut (Fig. 300) . The crest of this fold is almost
from the first in contact with the ectoderm above it, the fusion constituting the anal plate. Thus this plate is at first dorsal.just as in the Chick.
With the outgrowth of the tail bud the caudal portion of the hind-gut
region is. drawn posteriorly and ventrad. The result is that the anal
582 THE‘ PIG TO TEN LMILLIMETERS
genital ridge dorm Pancreas
posterior mrdinzl vein
 
 
 
I
for
ventral pancreas
ventral vein of mesonephros
Fig. 309.--Transverse section through the region of mesonephros, pancreas and
posterior of liver of a 10 mm. Pig. Only a part of the umbilical stalk included in
the figure. See reconstruction Figs. 296, 318, 320.
vltelline vein
subcardinal veins left umbilical vein
vitclline vein
’ ‘ K gut loop
 
umbilical arteries
ventral vcln ofmesonephros
right umbilical vein
Fig. 310.——Transverse section through the region of mesonephros, gut loop, um
bilical and vitelline argeries and veins, allantoic stalk and ti
p of embryo of a. 10
mm. Pig. See reconstruction Figs. 296, 313, 320.
FURTHER DEVELOPMENT OF THE GUT 583
plate, as in the Bird, is presently swung clear around to the ventral
side. With the further outgrowth of the tail bud a small portion of the
hind-gut is pulled out into this bud a short distance beyond the anal
plate. As in the Chick this extension is the postanal gut, but unlike the
case of the Chick it is entirely a temporary structure with no future
function, and so need not be referred to again. Both it and the anal
plate, it should be noted, are nowcaudal and ventral to the allantoic
stalk. Thus with the shift in these parts the latter no longer extends pos
ventral vein of mesonephros
fused subcardinal veins
7 ’ ‘- \ umbilical veim
 
posterior cardinal vet
 
mesonephros 'w-- i’ - T " ‘ ’
T \. — —* ut umbilical arteries
mesonephric duct
Eig. 311.— Transverse section through the region of rnesonephros, gut, umbilical
veins, allantoic stalk and cloaca of a 10 mm. Pig. See reconstruction Figs. 296, 318,
320.
teriorly, but rather proceeds at first dorsad before curving antero-ventrally into the body-stalk (Figs. 296, 311). Just within the embryo
postero-dorsal to the anal plate, the slightly enlarged end of the gut constitutes the cloaca, and the anal plate may now be termed the cloacal
membrane. This enlarged region of the gut is called the cloaca because
as in the Chick it presently receives not only the gut opening (anus),
but those of the urinogenital ducts and the allantois. The opening of
the anus is furthest postero-dorsal, those of the urinogenital ducts,
slightly more cephalad and ventro-lateral, and that of the allantois more
antero-ventral (Fig. 296). By the time this situation has developed, e.g.,
in a 6 mm. embryo, there has also occurred, according to some, the
usual depression in the ectoderm surrounding the cloacal membrane to
form the proctodaeum. The latter, though, seems not to be much in evidence at 10 mm. Thus we have a condition essentially similar to that in
forms previously studied. From this point onward, however, the situation in the Mammal begins.to diverge from that previously observed.
584 THE PIG TO TEN MILLIMETER_S
The divergences just suggested, though not far advanced in the 10
mm. stage, are definitely underway, as a result chiefly of one process.
Within the cloaca a crescentic sheet of tissue, the urorectal fold, is
growing from the postero-dorsal wall toward the cloacal membrane and
from the lateral walls toward the median line. When completed the result will be to divide the cloacal chamber into two parts. One, the
postero-dorsal into which opens the large intestine, will constitute the
rectum. The other, antero-ventral, part is called the urinogenital sinus,
and constitutes essentially an extension of the neck of the allantois
which now receives the urinogenital ducts (Figs. 311, 337). Although
this change has been initiated in the 10 mm. embryo, the cloacal division is not yet complete, nor is the cloacal membrane yet ruptured as is
the case with the oral plate.
MESODERMAL STRUCTURES
Under the headings of systems, we have thus far considered the nervous system, which of course is exclusively ectodermal, and the digestive
system. The latter because of its lining is often thought of as primarily
endodermal, though of course much of its walls are derived from mesoderm. Now, however, we are about to consider systems which are exclusively mesodermal in origin, e.g., the circulatory system, and the urinegenital system. Before embarking upon our discussion of these definite
systems, however, it is also necessary to make a few further comments
regarding the condition of the mesoderm in general.
The Sornites.-—— We have already discussed the origin of the lateral
plate mesoderm, but there has been no occasion to refer to the somites
except in a general way as criteria of development. It may now be
noted that these structures develop in the Pig in almost exactly the same
manner already made familiar in the Chick. As in that case the first ones
formed turn out to be the most anterior, each new. one being added between the most anterior old one and Hensen’s knot. Not only is the order of their origin similar but their character and method of development is the same. Thus the original ridges of mesoderm adjacent to the
notochord and nerve cord flrst become segmented. Then each segment
(somite) becomes a roundish mass with the cells radiating from its
slightly hollow center. Next the cells adjacent to the notochord and
nerve cord become loosely arranged about these structures as sclerotome. At the same time the cells of the dorsal part of the remaining
outer wall grow ventrad between this wall and the sclerotome. Thus is
formed a new dorso-ventrally elongated double layered structure with
THE CIRCULATORY SYSTEM 585
a space between the layers. The outer layer as before is called dermatome, and the inner wall myotome, the space between them being myocoel. The question of what these layers eventually give rise to, is still
uncertain in the case of the Mammal as it was in the Bird. The inner
layer certainly goes largely to form skeletal muscle, but to what extent
the outer layer or dermatome really forms dermis is not so clear. Probably only part of it so behaves. The sclerotome, however, again unequivocally gives rise to the parts of the vertebrae. By the 10 mm. stage the
parts of the original somites indicated above are no longer evident, except to a slight extent toward the posterior (Fig. 310).
The Intermediate Mesoderm. ——Though this term was not used
in the case of the Frog and Chick its equivalent was present. It is merely
the mesoderm between the somites and each lateral plate, i.e., it is the
part previously designated as nephrotome. The latter term indicated its
fate in the previous cases, and it is the same here. The details of this
will of course be taken up in connection with the urinogenital system.
The Somatic and Splanchnic Mesoderm.——The origin of the
somatic and splanchnic mesoderm, has already been discussed, and
need not be gone into here. However, it is pertinent to note that by the
10 mm. stage the intermediate mesoderm on each side no longer connects the lateral sheet of that side with the disappearing somites, but
throughout much of its length forms a discrete mass, the developing
mesonephros (Figs. 305, 309) . As the latter pushes out into the coelom
it ofqcourse carries a layer of mesoderm before it as its covering of
coelomic epithelium. It thus comes about that on the median side of
each mesonephros this covering passes dorso-medially until the two
sheets of epithelium are separated only by the mesentery of the gut.
With this arrangement the division between somatic and splanchnic
mesoderm might now seem to be somewhat confused. It is customary,
however, to designate only the mesodermal covering of the outer body
wall as somatic. The remainder covering the mesonephros (and later
the metanephros), the mesentery and the viscera is then splanchnic.
THE CIRCULATORY SYSTEM
The Blood Islands. -——- It will be recalled that in the Bird one of the
first manifestations of the beginning of the circulatory system is the _
formation of blood islands in the area vasculosa, which is of course
extra-embryonic. Virtually the same situation obtains in the Pig where
the blood islands also appear on the surface of the empty yolk-sac corresponding to the area vasculosa of the Chick. It will be recalled that
586 THE PIG.TO TEN MILLIMETERS
in the Bird, however, the mesoderm from which they arise in this region
is supposed to have migrated out from the area pellucida. It then forms
blood islands, and these in turn bud 0H mesoderm cells between them
and the ectoderm. No such indirect method seems to occur in the Pig.
The mesoderm is already in this area, and is divided into somatic and
splanchnic layers. The blood islands are then organized out of cells
from the splanchnic layer between it and the endoderm. As before, these
cells become aggregated into clum-ps, and while those around the periphery of each clump become flattened to form blood vessel endotlzelium, the more central ones 'transform into blood corpuscles. It
should be noted also that in the Mammal this activity is not confined to
the mesoderm of the yolk-sac. The allantois, which is somewhat more
precociously developed than in the Bird, likewise produces blood islands in a similar manner. It has recently been demonstrated, moreover,
that in certain Monkeys red blood corpuscles continue to be formed
from the endothelial walls of the blood sinuses of the chorionic villi
during early pregnancy (Wislocki, ’4-3). It is further claimed that in
the Baboon even the amnion produces red blood cells (Noback, ’46).
While early genesis of blood cells occurs in these various extra-embry
. onic locations their later formation is relegated to special organs such
as the mesonephros, liver, spleen and finally the bone marrow. Meanwhile the differentiation of the endothelium of numerous vessels goes
on constantly throughout the embryo. As the circulatory system thus
develops it is quickly supplied with both corpuscles and fluid from the
various blood islands, and later from the other sources just indicated.
Whether these later centers possess their capacity as a result of the migration to them of blood forming mother cells from the original blood
islands is still an open question. Some hold this view, while others maintain that the later centers give rise to their own blood-forming cells from
local mesoderm. Possibly both methods occur. In any event there are of
course many kinds of blood cells produced from the original mother
cells, and their varied diiferentiations make a complicated subject which
we shall not go into. '
The Heart. — One of the first parts of the intra-embryonic circulatory system to develop is the heart, and the method of its early formation
is virtually identical with what we have already described in the Chick.
On either side of tlie pharyngeal region, before this part has been closed
in ventrally, the endothelium of a blood vessel forms between the
splanchnic mesoderm and the endoderm in the manner described above.
As the closure occurs these two blood tubes fuse beneath the pharynx to
THE CIRCULATORY SYSTEM 587
4
t
t
6
dorsal acme
truncus arterloxus somlte posterior cardinal veln
 
   
 
vitelline (omphalomesenteric) veins
amum duct of Cuvier
1 anterior cardinat vein
i truncus arteriosus
_' . - g”
dorsal aortae
 
 
vitelline(omphalomesenteric)veins, arteries
Fig. 312.—A. Partial injection of the vessels of a Pig embryo of 14- somites, 4‘ mm. in length. After Sabin. B. Partial injection of the vessels of a Pig embryo of
1 27 somites, 6 mm. in length. After Sabin.
588 THE PIG TO TEN MILLIMETERS
form the usual single heart tube. The splanchnic mesoderm follows the
endothelium and while the latter constitutes the endocardium, the mesoderm covers it to form the epicardium, and the dorsal and ventral mesocardia. Because of the latter the two coelomic spaces on either side (_in
the Bird called the amnio-cardiac vesicles), as in that case, do not at
first communicate. Presently, however, the ventral mesocardium disappears, and the two parts of the pericardial space are united. The dorsal
mesocardium, as in the Chick, persists somewhat longer. This condition
septum ll
 
l I
J «I 4/
2 «._.,%2«:d? mcerventrlcular
. ,,
trabcculae I? T‘
Ca Ynea e
Fig. 313.—Frontal section through the heart of a 10 mm. Pig.
is reached at about the 4.5-5 mm., or 13 somite stage. (See Chick, Fig.
l 79.)
The next steps in cardiac development in the Pig are again very familiar. The dorsal mesocardium in its middle region disappears, leaving
the double-walled tube free to bend. Then as the latter increases in
length it becomes thrown into the usual curve to the right, and this
shortly becomes a loop whose apex is rotated backward. As in the Chick,
the postero-dorsal part of the loop becomes the atrium, the apex of the
loop and a portion of each limb the ventricle, and the antero-dorsal end
of the more anterior limb the truncus arteriosus. These parts then rotate so that the atrial region becomes antero-dorsal, and the apex of the
ventricle postero-ventral with the truncus running cephalad along the
antero-ventral face of the ventricle. From a comparison of this description and of the figures of the heart of the Frog and Chick at similar
stages the essential Ilikeness will be apparent (Figs. 108, 184-, 312).
By 10 mm. the befidings and shiftings indicated above are complete,
and the heart presents externally almost the adult appearance. Interl
i
!
THE CIRCULATORY SYSTEM 539
nally a crescentic septum, the septum primum (I) has grown from the
antero-dorsal wall of the atrium, and has partially divided it into right
and left chambers. Postero-ventrally, i.e., toward the ventricle, however, the growth is not quite complete, and the very small opening
briefly remaining is all that is left of the originally wide-open orifice
between the atria, the interatrial foramen primum (Figs. 313, 314).
Meanwhile dorso-anteriorly a new opening has developed in the septum
called the interatrial foramen secundum. Also another septum, the sep
 
 
 
 
 
 
P°5t"'°' °°'d'"°' M" anterior cardinal vein
duct of Cuvier
sinus venosus—«\
posterior vena cava ' interatrial foramenll
valvulae venosae - septum i(primum)
hepatic vein interatrial foramenl
bulbo-conus
septum Ii (secundum)
cushion septum
interventricular foramen
interventricular septum
Fig. 314.-—Reconstruction_of the heart of a 7.9 mm. Fig
with the right atrium and right ventricle opened from the
right side. After Morrill.
tum secunclum (II), is sometimes slightly in evidence to the right of the
septum primum (Fig. 313). The further fate of these septa, their openings and their functions will be fully discussed in the section on ‘later
development. Another conspicuous structure apparent within the right
atrium at 10 mm. is a pair of flaps guarding the orifice from the sinus
venosus to this atrium, the valvulae venosae (Fig. 304). Later on one
of these valves forms a minor ridge, the septum spurium, which soon
disappears.
Between the atrium and the ventricular region the heart is somewhat
constricted to form the atria-ventricular canal, and this also has become almost or quite divided by growths proceeding from its dorsal
and ventral walls. When complete these growths, as in the Bird, will
form the so-called cushion septum (Fig. 304). At the same time a third
septum, the interventricular, is growing from the apex of the ventricle
toward the atrio-ventricular canal (Fig. 304). All these septa will
shortly meet to divide the entire organ into completely separated right
and left chambers, save for the existence of one of the interauricular
foramina which persists until birth and even after. Finally the walls of
.._ .......__...._.. _. . . . ..s......,
590 THE PIG TO TEN MILLIMETERS '
 
V: /e-///ne vem
   
 
Dorsal rpm nan! a/I?/1‘ 1'1-'aor/Ic arch
/‘rt /mzry .‘1eaa’re/‘.1
Lell 4 §"aor}/‘c arch Pflmmy head mm Le/7 I '3-’aor//c are/t
V ‘ L7//c vesicle '
 
 
Le/I an):-rior cardinal Van
Luff dorsadaorla
 
Left dorsal not-la.
5egmenlaIar/er/es
 
Fig. 315.—St_ages in the development of the aortic arches and other anterior ar
. 4.4 mm., 10 somites. B. 4.15 mm., 19 somites. C.
3.8 mm., 26 sornites. D. 4.57 mm? 28 somites. E. 4.46 mm., 30 somites. F. 6 mm.,
stages of development
as indicated by the number of somites are not always exactly correlated with the
relative lengths of the embryos. The former is usually the more accurate criterion of
degree of general development in the earlier stages. Hence both items are given.
‘.s .4 4 . A
THE CIRCULATORY SYSTEM 591
   
     
       
 
 
 
 
     
/Ior//c /run/<
.3 ‘Paar!/c arc/7
E3-—i. eff dorsal aar/a
/f/gh/dorsa.’ aorla
 
/"/
4_"'ao.'/Ic arch
_:‘L
 
E »/’u/manar} arc/7 '
‘«\\\\\\'«\\‘\““““.“_‘T'“‘m"” ’ ' M‘
\\“\ .  . ‘. .
uuwlw/" """'“‘
Ex/erna/carom/ar/cry
Cxfernal camlrd arfery
4 " aor//c arch
Pu/mamzryarc/1
Pu/marlaly ar/cry
2/2’ dorsal aarla E
Pulmonary vein Ssgmrnlal ar/cries
 
   
Fig. 316.—Stages in the dgvelopment of the aortic arches" and other anterior
arteries of the Pig. After Heuser. A. 24 somites. B. 4.3 mm., 26 son-mites. C. 6 mm.,
36 somites. D. 8 mm. E. 12 mm. '
m
——
592 THE PIC TO TEN MILLIMETERS
 
   
   
M Tivigemrz-up
/ ,
vary/zeadvein /’
 
   
 
   
(Sr/ema/s arn- “
ht! arlery
florsalrerrmaninf  IA‘  “ I I
z#‘7°’A"5”"}’ ~~\\\\V§m\ ‘.  J5'aarIicarc}2
4"’aur1icarc}i 2;" V  , E  §g,ra‘a’r”J:"'}
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Fig. 317.—-Stages in the development of the aortic arches and other anterior arteries in the Pi . After Heuser. A. 12 mm. B. 14 mm. C. 17 mm. D. 19.3 mm.
THE CIRCULATORY SYSTEM 593
the ventricles become definitely thickened, and muscular bands, the
trabeculae carneae project into the ventricular lumen.
The T runcus and Aortic Arches. ——.The truncus arteriosus has
already been mentioned as it comes up underneath the pharynx. As in
iind visceral pouch
is: visceral pouch
   
   
 
internal carotid artery
external carotid artery
3rd aortic arch
?
II
.5:
‘<
F‘-s-299
     
   
 
 
F:g.3oz I RF?th|<e's pockeg
pulmonary artery I  9"”:
vertebralarter Ii:
Interatrigfomcn  V
subciaviaingdrtery  ’  fi"3°“
intervcntricular foramen
n,.3o5  “M05 »
. FI'g.3O6 ’
cociiac art:  3 u -in I
macs ' ,;,_ °‘ °' 9‘
E33.-L-'2
53%
d°"3' ‘°"‘ aliantolc stalk
F'»g.3lO '
3.3:‘:
Fig.323 ‘
superior mesenteric artery '
Fig. 318. —-—Reconstruction of a 10 mm. Pig embryo designed to show primarily
the main features of the arterial system at this stage. Drawing made by same
methods as used for Fig. 296. As before the lines at the sides indicate where the
sections denoted by the figure numbers above the lines, pass through the embryo.
the case of the Chick this large vessel does not, contrary to what most
diagrams suggest, really extend any distance cephalad in a horizontal
position before giving off the aortic arches. Instead it extends dorsally
and only ‘slightly cephalad directly into the -midst of the pharyngeal region (Fig. 318). Here it gives rise to the six aortic arches, but again as
in the Bird, not all at one time. The mandibular aortic ‘arch appears first,
then the hyoid, and by the time the other four pairs have developed in
the remaining visceral arches (10 mm.) the first two aortic vessels have _
disappeared (Figs. 315, 316). Also again as in the Chick, the‘ fifth pair
594 THE PIG TO TEN MILLIMETERS
are vestigial, sometimes appearing briefly as loops on -the front sides of
the sixth arches, and sometimes on the posterior sides of the fourth.
With respect to the sixth arches themselves it must be noted that as early
as 7.5 mm. each has given rise to a small posterior outgrowth which
 
 
 
 
 
 
   
   
circle of Wlllls
nternal
left carotid artery
lnterna xmlml
right carotid artery
external
lntersegmennl arterl 3", mm: "ch
_. common carotld artery
3rd , ' l l _ _ brachlo-cephalic artery
aortic arches-[4th I l . . <' I 4th aortic arch
Gil‘! ' ‘ -' l ' duct of Botallo
*:'::.:::'z,:.':r.:::: «me»
pulmonary arteries
trun_eus
arterlosus
left vertebral artery
dorsalaorta  ‘
Internal mammary arcerl
A B
Fi . 319.——Semi-diagrammatic representation of the development of the aortic
arc es and other anterior arteries of the Pig. A. Arteries at the 10 mm. stage. B.
Arteries of a specimen near term.
left subclavlan
artery
reaches the developing lung buds. These outgrowths, together with the
proximal parts of the arches, constitute at the 10 mm. stage the pulmonary arteries (Fig. 316, E). It may be noted that in other Mammals
studied the proximal parts of both the sixth arches continue to form a
part of these arteries. In the Pig, however, as we shall see, only the
proximal part of the left sixth arch persists as a part of the pulmonary
system (Figs. 317, A, B; 319). Anteriorly, the first two pairs of arches
THE CIRCULATORY SYSTEM 595
have disappeared, and each member of the third pair has given rise near
its base to a new vessel. These vessels are the external carotids, and appear at lffmm. as very tenuous strands extending cephalad toward the
ventral part of the head (Fig. 318). Both fourth arches at this time remain well developed.
The Dorsal Aortae. —— At their dorsal ends the arches of each side
are connected anteriorly and posteriorly by the two dorsal aortae. Cephalad these aortae remain separate, and extend into the head as the internal carotids. Posteriorly they also continue separately at first (Fig.
312, B), but at about 6.5 _mm. (17 somites) they become united at ap
proximately the middle of the embryo to form the single dorsal aorta. '
By the 10 mm. stage this fusion has progressed to the tail, and as far
forward as the anterior appendages (Figs. 316, 318).
Other Arteries Anterior to the Heart.——ln the Pig and other
Mammals the internal carotids are not the only dorsal arteries extending into the head. There early arise from the aorta throughout most of
its length small branches between each pair of somites, the inter segmental (or segmental) arteries. These were also noted in the Chick. In
the Pig, however, these arteries soon form antero-posterior anastomoses
in the region extending from the seventh cervical somite into the head,‘
and at the same time lose their connections with the dorsal aorta. As a
result of this process there are established in the neck region anterior to
the seventh cervical intersegrnental arteries, a pair of longitudinal vessels called the vertebral arteries (Fig. 317). These arteries, however, do
not continue separately clear into the head. Beneath the myelencephalon
they fuse into a single median vessel termed the basilar aitery. As re
- gards the seventh cervical intersegmentals, it may be noted that they are
starting to enlarge slightly to take part in the formation of the subclavian arteries, whose development will be described further in the
next stage. The fate of the intersegmentals posterior to the seventh cervical will also be noted at that time. Meantime by the 10 mm. stage the internal carotids have each sent a branch medially to unite with the basilar, thus producing a part of the future circle of Willis about the
hypophysis (Figs. 317, 318, 319).
Arteries Posterior to the Heart.—To complete the history of
the arteries at this stage we find that somewhat caudad from the middle
of the embryo, the two omphalomesenteric or vitelline arteries are
among the first to‘ arise from the dorsal aortae. These arteries connect
the aortae with the vessels formed in the wall of the yolk-sac, and since
the vitellines arise before the dorsal aortae have fused, they are at first
a
596 THE PIG T0 TEN MILLIMETERS
double (Fig. 312, B). Their function of course is to take blood from
the embryo to the yolk-sac, where it receives nutriment absorbed by
this organ from the uterine walls prior to the development of the allantoic placenta. At 10 mm. the aortae in the region of the origin of the
vitelline arteries have fused and with them the arteries, so that a single
 
 
 
 
   
 
 
fig. 299
j H9299
anterior cardinal vein
external jugular vein
Fig-302 F:‘g.302
right duct of Cuvier
valvulae venosae
I-75.304 Fig. 301!
“CW5 V¢"°‘"‘ omphalornescnteric vein
Fig-305 Fig.305
posterior vena cava
Fi .306 Fig. 306
right hepatic vein _
p;s_3o8 Fig. 303
fis.309 .F_li'_§2?.
hepatic portal vein 3"3|'|§°l€ 5'-ilk
I-'Ig.3lO Fi§.3IO
imemml am left umbilical vein
Fig.3" Fig.3l|
5* 3” right ugfiialu zcgl vein
' cloaca
esonephros
ventral vein of mesoncphro:
Fig. 320.——Reconstruction of a 10 mm. Pig embryo designed to show primarily
the main features of the venous system at this stage. Drawing made by the same
methods as used for Figs. 296 and 318. As in these figures the lines at the sides
indicate where the sections denoted by the figure numbers above the lines, pass
‘throughthe embryo.
vitelline artery extends along the mesentery into the body-stalk (Fig.
318). With the disappearance of the yolk-sac this vessel persists within
the body as the anterior mesenteric artery. A short distance anterior to
it the coeliac artery has developed at~10 mm., and extends toward the
stomach region, but the posterior mesenteric artery has not yet appeared.
In addition to the segmental arteries already mentioned the aorta also
gives off numerous small’ branches at the level of the mesbnephros to
the glomeruli and tubules of that organ, the renal arteries. Lastly, so far
as branches from the aorta are concerned, are the umbilical arteries to
2 . THE CIRCULATORY SYSTEM 597
the allantois. These arise quite early before the two aortae have fused
in this region, and even after their fusion at 10 mm. the umbilicals rernain separate. By this stage also each has produced a small branch in
ugh: duct of Cuvier let‘: duct of Cutler
   
 
sinus venosus mt! duct of Cums: Id: due: at Crmer
mad" anterior cardinal vein i
‘ cu-dinalveln ' "mm"
W . ' ——Post.erior ardlnll vctn “"“"" "l"
E P°“¢'l°|'  - poxzerlor
3; liver
‘inhumane: vein left umbllica! van
Ugh! umbmal veln aft umblllul vein
umphalemestntcrlc(virelline) veins
A ‘ omplulomesenreriz (vizemne) um!
i
4
I
5
left‘ due: of Cuvler
 
4 I umbilical vein
- hlombflid vein
Intestinal vein
oenptualomesenxerlc (yi::IIing)vgm
Fig. 321.—Reconstructions of stages in the development of the veins of the liver
and immediate vicinity. A. The veins in a. 5-6 mm. embryo, semi-diagrammatic.
Veins in the liver according to Butler, with the omphalomesenteric (vitelline)
veins extended posteriorly to show their relation to the gut. B. Veins in a 6 mm.
Pig embryo, semi-diagrammatic. Again the vessels within the liver are according
to Butler, with the omphalomesenterics posterior to it added. C. Veins in the liver
of a 10 mm. Pig embryo viewed from the right side (enlarged from Fig. 320). D.
Veins in the liver of a Pig at the same stage as C, but viewed ventrally.
connection with the developing hind limb bud, the external iliac. The
aorta itself continues on as a single vessel into the tail (Fiv. 318).
, The Omphalomesenteric Veins.—As in the Bird, among the
i earliest, if not the earliest, veins to develop in the Pig are the am phalaA mesenteric or vitelline veins. They. arise just as they did in the Chick
coincidentally with the formation of the cardiac tubes which fuse an-_
teriorly to form the heart. Posterior to the region of fusion these tubes
extend caudad and laterally out onto the yolk-sac where _theyi’become
continuous with the capillaries and blood islands which we have noted
593 ' THE PIG TO TEN MILLIMETERS
     
   
. Illllll VEVIOSUI '
   
ventral vein 0! mesonephrot
posterior ardlnnl veln
-right subcardlnal vein
Early stage in any young 5-6 mm. Fig embryo.
mammalian embryo.
sinus venesus
anterior ardlnal vein
duct of Cuvler
subclavian Vein
posterior ardlnal vein
I I
rlghl umbilical vcln e E umbmal "In
hepatic portal vein
3-7 mm. Fig embryo. 12-14 mm. Pig embryo.
Fig. 322.--Diagrams of developing venous system posterior to heart in: A. Any
very young mammal; B, C, E, F, H, I, J, in Pig at stages indicated. D. Transverse
section of C at level shown by arrow.
as originating there. As development proceeds the fusion of the vitellines continues for a very short distance posterior .to the atrial region of
the heart to form a thin walled sac, the sinus venosus (Figs. 312, A; 322,
A, B); At about this time also (3.5—4 mni.) the previously noted interatria  prirrium begins to develop, and in such a way that the sinus
l ._ 'j‘,e*‘6pa1-in\to"“l:Z1e right atrium (Fig. 304).
K.
‘t
2»~
I
posterior vena_u:va
(right mpnudlnafi
owunulllhc — " /\ /1 ’\
30-35 mm. Pig embryo; - Adult Pig.
Fig. 322 cont.—F, H, I, J, as noted ahove. G. Transverse section of F at level
shown by arrow. All stages after Butler. Princeton Embryological Collection.
At this point a difference may be noted between the further development of the vitelline veins in the Chick and that in the'Pig. The two
veins in the Pig do not continue their fusion to form may large part of
the ductus venosus as in the Bird, the major portion of that trunk arising from a different source in a way to be described be '
remain mostly separate,  the liver and pre ' fl t9-fie
600 THE PIG TO TEN MILLIMETERS
stage their middle portions have broken up into a capillary network.
Their anteriorstumps, however, remain as the two hepatic veins, while
their posterior parts persist for a time in the caudal half of the liver as
two distinctuvessels (Fig. 322, A, B). From there these vessels issue to
pass along either side of the gut to the regressing yolk-sac. As the latter
disappears they become simply two veins bringing blood from the intes
tine, and by the 10 mm. stage a further change has occurred, resulting
in the reduction of these two vessels to the one hepatic portal vein. The
method by which this takes place, producing the peculiar spiral course
of this single vessel about the gut, is illustrated in figure 321. It involves essentially the same process as in the Chick, i.e., a fusion of the
vitelline vessels first above the intestine, and then below it, with the
subsequent disappearance of the left and right sides of the loops thus
formed. The chief diiierence between the Chick and the Pig in this connection is that in the latter both sides of the loop are formed before ei
' ther disappears, but as indicated the end result is the same.
The Allantoic (Umbilical) Veins. —— Another pair of veins which
develop very early in the Mammal are the allantoic or umbilical veins.
In the Bird these are somewhat slower in forming, and it will also be
recalled that at first the allantois is drained by a transitory vessel, the
subintestinal vein, which opens anteriorly into the vitellines. This preliminary arrangement does not occur in the Pig. Instead the umbilical
veins develop at once in essentially the same way that they ultimately
do in the Bird. They arise as vessels in the lateral body wall which
open anteriorly directly into the sinus venosus (Fig. 322, A). Posteriorly they extend around the sides of the wall, and thence via the bodystalk onto the neck of theallantois (Fig. 273). This is the situation at
first, but by 10 mm. certain changes have developedas follows:
Anteriorly the two veins no longer empty directly into the sinus venosus. Instead as the liver comes into contact with the body wall, the umbilicals in that wall develop new channels connected with the hepatic
capillaries (6 mm.) (Fig. 322, B). By the 10 mm. stage some of these
capillaries in line with the flow of blood from the two umbilicals have
developed into well marked channels which soon become definite vessels
within the liver. The left one even at this stage is larger than the right,
which soon disappears in this region. Hence the part of the left umbilical within the liver now forms the major part of the ductus -venogms,
the short anterior section which opens into the sinus, being derived from
the very limited fusion of the vitellines indicated above (Figs. 320, 321,
322, C). Thus, as noted, the ductus has for the most part a quite difl'erTHE CIRCULATORY SYSTEM 601
ent origin from the similarly named vessel in the Chick where it arose
entirely from the posterior fusion of the vitelline veins. Caudad to the
liver the two allantoic or umbilical veins continue at this time to exist
as separate vessels as far as the umbilical stalk, but within this stalk
they have become fused into one. Thus there is but one umbilical vein
in the stalk, but two umbilical arteries. Even at this stage, however, the
right umbilical vein within the body wall is becoming smaller.
The Anterior and Posterior Cardinal Veins. —— So far we have
considered venous systems which are both intra- and extra—embryonic.
It now remains to indicate the development of those veins which are entirely within the embryo. Among these the most prominent up to the 10
mm. stage are the various cardinals, whose development very closely
parallels that in the Bird. Thus the anterior cardinals arise anteriorly
on either side of the neck and headregion slightly dorso-lateral to the
aortae, and soon develop a capillary network connecting with the latter
vessels. The posterior cardinals likewise develop in the same relative
position to‘ the aorta posterior to the heart. Dorso-lateral to that organ
the anterior and posterior vessels of each side dip.downward slightly,
and join one another to form the wide, short ducts of Cuvier which
slope ventrally and medially to enter the sinus venosus. A short distance cephalad to the point where the anterior cardinals enter the ducts
each cardinal is joined by a ventral branch coming from the region of
the mandibular arch. It is of course the future external jugular. Very
slightly posterior to, or at its junction with, the respective duct of Cuvier
each posterior cardinal receives the subclavian from the adjacent forelimb bud. This vein, as was the case with the corresponding arteries,
results simply from the enlargement of one of the numerous intersegmental veins which drain into the posterior cardinals (Fig. 321, 304).
The Subcardinals and Posterior Vena Cava. ——Again as in the
Chick, with the development of the mesenephros the original cardinal
circulation is supplemented by certain new vessels which in a 10 mm.
embryo are well established. Indeed by this time the posterior cardinals
have actually begun _to degenerate, and their functions to be taken over
by these new vessels as follows:
Along the ventro-medial border of each mesonephros a plexus of
capillaries is formed (5-6 mm.) , and soon these have anastomosed so as
to constitute continuous vessels running the length ‘of each mesonephros.
These are the subcardinals, and through further mesonephric capillaries
they are soon more or less connected with the posterior cardinals‘ (Fig.
322, B). In fact anteriorly these connections presently become quite
602 THE PIG T0 TEN MILLIMETERS
definite and direct. Now as the mesonephroi grow the suhcardinals are
crowded still nearer the mid-line, and at about the middle antero-posteriorly, ofthe mesonephroi they fuse into a single large sinus (Figs.
311, 322, C, D, E). Into this drain all the surrounding capillaries. This
comes about because, as this sinus is formed, the posterior cardinals at
this level disappear entirely, though they persist for a time both anteriorly and posteriorly. Thus it happens at 10 mm. that among the capillaries draining their blood into the median subcardinal sinus through
the mesonephros are many from the posterior parts of the posterior cardinals (Figs. 320, 322, C, E). At the same time anterior to the subcatdinal sinus, the left subcardinal begins to become smaller, and to lose
its connection with the anterior part of the left posterior cardinal,
though this is still functioning at 10 mm. (Fig. 322, C, E). The right
subcardinal, however, just as in the Bird, becomes more prominent, and
at 10 mm. has affected a connection with still another new vessel. This
vessel has formed from capillaries within the liver mesentery, and also
from some of those within the liver itself. It is the mesenteric and
hepatic part of the posterior vena ctwa, the subcardinal sinus and the
anterior portion of the right subcardinal, being the other parts developed at this time (Figs. 320, 322, C, E). Anteriorly the part of the new
vessel developing in the liver opens into the ductus venosus near its anterior end, where it also receives the two hepatic veins. As the caval
vein grows, the anterior part of the ductus between this vein and_ the
sinus becomes the anterior end of the vein (Fig. 321). The complete
development of its posterior end will be explained in our discussion of
the next stage.
In connection with the description of this vessel up to the present
point, however, there is, already one feature concerned with its posterior
part which is becoming evident, and which merits attention. This
feature is the development of a renal portal system in essentially the
same way that it was formed in the Bird (Fig. 322, E). When fully developed, these systems function more or less like that of the Frog,
though they arise somewhat difierently, there being no subcardinals in
the Frog.‘ It is interesting of course that this system exists in all these
forms, yet in the Bird and Mammal is only temporary. It is perhaps
even more remarkable that it is always the right side (in the Bird and
1 It appears that in the Pig,‘ and very probably the Bird, not so much of the
blood coming from the posterior of the embryo is actually supplied to the mesenpheric tubules as in the Frog. Instead more of it seems to be routed more directly
through the organ, while the tubules, as well as the glomeruli, are supplied more
from arterial sources.
THE EXCRETORY SYSTEM 603
Mammal the right subcardinal (in the Frog the right posterior cardinal)
which enters into the formation of the posterior vena cava. Such facts
can scarcely be entirely coincidental.
One minor feature regarding the cardinals in the 10 mm. Fig which
differs from that in the Chick should be mentioned to avoid confusion.
In the Chick there are no other vessels than those just described. In the
Pig, on the other hand, some of the capillaries along the ventro-latera-I
side of each mesonephros also anastomose to form a small vessel extending antero-posteriorly along this region. It is called the ventral
vein. of the mesonephros, and since it also connects through capillaries
with the respective posterior cardinal, it might be mistaken for a subcardinal. Its smaller size and superficial ventral position, however, distinguishes it and it soon disappears (Figs. 320, 322, C, D, E).
The Pulmonary Veins.-—0ne other important intra-embryonic
venous system which has no relation to the cardinals, but which also
starts to develop at an early. period is the pulmonary. Since the pulmonary arteries have been seen to arise as early as the 7.5 mm. stage,
the development of the veins at about that time might be anticipated,
and they have in fact arisen. There is some question, however, as to just
how these vessels have been formed, e.g., whether as an outgrowth from
the atrium, or as in so many other cases, by an anastomosing of plexuses along their course. In any event they exist at this stage as small
i veins which proceed from each lung bud, and unite in a common trunk
which enters theleft atrium. Later as in the case of the arteries the pulmonary veins also suffer certain alterations which will be noted in due
course.
THE URINOGENITAL SYSTEM
Although these systems are ordinarily considered together because of
the close association of some of their parts both embryologically and
anatomically, it is convenient as previously, to describe their development separately. We shall begin with the excretory systemsince it is the
first to become clearly evident.
E THE EXCRETORY SYSTEM
I The Pronephros. —— In the Pig, as in the Bird, there is a gesture
made toward the development of a pronephros. On-each side its rudimentary tubules arise as usual from the intermediate mesoderm, and occur in the cephalic region from about the sixth to the fourteenth somites.
These vestigial organs are of course without functional significance, but
I
. ‘T
604 THE PIG TO TEN MILLIMETERS
the tubules turn and grow caudad to give rise to the pronephric ducts,
in the way with which we are already familiar. By 10 mm. all parts of
this system, save the ducts, have virtually disappeared. ,
_ The Mesonephros.—The mesonephros arises in the intermediate ‘
mesoderm from about the fourteenth to the thirty-second somite of the I
Pig.‘ As usual it first appears as spherical concentrations in this meso- ' ii
derm, three or four such concentrations being developed opposite each
somite. These form vesicles, and the vesicles produce tubular outgrowths
which become coiled, and open into the old pronephric, now mesonephric, duct. The vesiculariportion of each tubule is invaginated by
the usual knot of capillaries forming a glomerulus, supplied with blood
by branches from the aorta, and draining into tributaries to the subcardinal veins. The invaginated part of the tubule of course constitutes
Bowman’s capsule.
Anteriorly the mesonephric duct is often difficult to distinguish in
cross section from the numerous mesonephric tubules, but more caudally
it can generally be located along the ventral border of the organ. Poste
rior to the mesonephros this duct continues to the cloaca, and by the 6
mm. stage has entered it. By 10 mm. the antero-ventral region, into the
sides of which this entrance was affected, is beginning to be separated
from the postero~dorsal part by the urorectal fold in the manner already described (Fig. 337). Thus the ducts are coming to open into the
part of the cloaca termed the urinogenital sinus which is in the process
of being added to the neck of the bladder (allantois). These arrange—
ments in the cloacal region are the beginnings of changes which will
ultimately bring about fundamental diflerences between conditions in
these parts in the Bird and the Mammal. These dilierences will be discussed in detail later in connection with the development of the external
genitalia. At this time, however, the most striking peculiarity of the
mammalian excretory system lies in the remarkable relative size of the
mesonephroi themselves. Thus in a 10 mm. Pig these organs are far
larger than at any period in the Chick, being in fact much the largest structures in the embryo (Figs. 296, 310, 311).-The functional significance of this difference is not known.
The Metanephros and Ureter. ——As the student is already aware,
the mesonephric kidney in all Amniotes is ultimately replaced by a
third or metanephric kidney. This kidney starts to appear at the 5-6
mm. stage as a very smalldiverticulum growing out from the posterodorsal side of each mesonephric duct just dorsal to the point where
if these ducts enter thelcloaca. By 10 mm. the diverticula still issue from
THE GENITAL SYSTEM 605
the mesonephric ducts rather than the neck of the bladder, but have
grown anteriorly somewhat, and the cephalic portion of each is enlarged slightly. The enlarged portion represents the lining of the future
pelvis of the kidney, and is already surrounded by a concentration
of intermediate nephrogenic mesoderm (Figs. 296, 323). This meso
mesonephros mesonephric duct
subcardinai veins hind-limb bud
Tm
_ \\ posterior cardinal vein
£“v
   
posterior cardinal vein
\_> .vI’
ventral vein of mesonephros ""“b""3 3'"‘°"Y
Fig. 323. —Transverse section through the region of the mesonephros, umbilical
arteries, mesonephric and metanephric ducts and hind limb buds of a 10 mm. Pig.
See reconstruction Figs. 296, 318, 320.
derm is carried forward with the pelvic portion, and later furnishes
the material from which the kidney tubules are made. The remainder
of_ the outgrowth of course becomes the future metanephric duct or
ureter.
THE GENITAL SYSTEM
The Gonads.——These are barely in evidence at the 10 mm. stage.
They may sometimes be detected, however, as very slight thickenings on
the medial sides of the mesonephroi, somewhat anterior to the middle.
16
HE LATER DEVELOPMENT OF THE PIG
HA V I N G completed our descriptions of the Pig embryo as a whole,
and of the various systems at the 10 mm. stage (20—21 days), we are
now prepared to indicate the further development of this animal as far
as it is profitable to carry it. This means in most instances, either to the
adult condition, or to a condition near enough to it so that the ‘steps required to attain the adult state are quite obvious. As in the discussion of
the earlier development we shall begin by a consideration of external
features. E ' '
The F lexures. —— Following the 10 mm. stage the Pig embryo grad
ually straightens to some extent. "This pr'ocess first involves mainly the _
dorsal flexure (15-20 mm., Fig. 324), and later the cervical and lumbesacral flexures. As in other vertebrates the cranial flexure is permanent,
but since it concerns chiefly the brain it also ‘becomes less obvious externally as development proceeds.
External Features Posterior to the Head and Neck Region. —At 15 mm. the boundaries of the somites are still clearly visible, and
the milk ridge has become evident. By 20 mm. the ,somite markings have
pretty much disappeared, while along the lower border of the milk ridge
fiveior six mammary anlagen are present. Ventral to these anlagen in
both these stages the abdomen protrudes greatly, due to the developing
mass of viscera within it. By the 50 mm. stage, however, these have been
drawn up, and the ventral contour is about _that of a well-fed adult.
Throughout all these periods there has been relatively little growth of
the umbilical cord. Its diameter does ultimately increase, however, due
to growth of the contained blood vessels and connective tissue, so that
at term it measures from 8-10 -mm., while the length of the whole animal may be as much as 25-30 cm. The paddle-like appearance of the
feet at 10 mm. has been referred to, and this condition still prevails at
20 mm. By that time, however, the existence of five toes in each foot is
clearly in evidence, and the limb joints are slightly suggested. In the
Pig and other Artiodactyls, as is well known, the first digit (homologue
of the thumb or great toe in Man) soon vanishes entirely. The third and
fourth digits develop evenly to form the cloven hoof, while the second
,;
EXTERNAL FEATURES 607
and fifth digits remain short and more or less vestigial. This condition
is well advanced in an embryo of 40-50 mm.
The Head and Neck Regions. —— Probably the most striking
changes of all in any mammalian embryo are those connected with the
head and neck, especially with relation to the face, and we shall now
indicate these changes in their main outlines.
 
 
   
' hair follicles
ear plnna
hear: area
milk ridge .
nipples
umbilical stalk
genital tubercle
20 mm. embryo
Fig. 324. +A 20 mm. Pig embryo viewed from the right side.
When last described at 10 mm. it will be recalled that there were
four visceral clefts and four arches visible in a side view, the first arch
being the mandibular (Fig. 294). Also apparent were the maxillary
processes and nasal pits. Each pit was bounded laterally by a nasclateral process which was separated from the adjacent maxillary process by'a groove running from oral cavity to eye, the lachrymal groove.
Viewed anteriorly (Fig. 295) the frontal process separated the nasal
pits, and adjacent to each pit this process was thickened to form the
naso-medial processes. Reference to the appropriate figures makes evident the great similarity of these facial anlagen in a 4-5 day Chick and
608 THE LATER DEVELOPMENT OF THE PIG
a 10 mm. Pig. It may now be added that the resemblance between Pig
and Man at comparable stages is even closer. Indeed the latter are so
much alike not only with regard to facial features, but in other respects,
that to a casual observer the differences between a 10 mm. Pig embryo
and a 10 mm. Human embryo would be scarcely noticeable. The
changes which gradually ensue to produce the condition in the head of
the adult Pig will now be indicated.
   
naso-lateral process
naso-lacrymal groove
naso-medlal process
eye
external naris
maxillary process
mandibular arch tdngue
auditory opening
Pl"“3 °f °a" (hyomandibular cleft)
Fig. 325.-—-A view of the face of a 17 mm. Pig embryo from the
antero-ventral side. '
The lower jaw, it may at once be noted, is derived entirely from the
mandibular arches which grow antero-medially until they meet. Posteriorly they form an angle with the maxillary processes which constitute
the larger part of the upper jaw. However, these latter processes do not
meet one another anteriorly, and hence do not form the antero-median
part of this jaw. Instead this part is comprised of the naso-medial processes whose forward extremities grow together. In so doing they crowd
the original median region, i.e., the frontal process, backward (Figs.
295, 325). Thus the naso-medial processes come to form the pre-maxillary part of the upper jaw, and the nasal septum, while the frontal process forms only the nasal bridge. While this fusion between the naso~
EXTERNAL FEATURES 609
medial processes is occurring in tlie mid-line, each of these processes is
also fusing postero-laterally with the respective maxillary process, and
also with the respective naso-lateral process. These fusions serve to
bound the nasal pits antero-laterally, and cut them off from the edge of
the oral cavity, thus producing the external nares (Fig. 325). Posteriorly these pits breakthrough into the oral cavity, and so give rise to."
the temporary internal nares, of which more will be said in connection with the development of the mouth proper. While the bridge of the
nose is formed as noted from the frontal process, its sides (alae) are
constituted by the naso-lateral processes. Also the lachrymal groove separating these processes from the maxillary processes is closed over so
as to form a tube, the lachrymal duct connecting eye and nose.
Further development of the Pig’s face consists largely of the outgrowth of all these parts. Indeed the whole procedure from 10 mm. onward may be roughly pictured thus: It is much as though all the above
processes were approached from the front by invisible fingers which
grasp these processes, squeeze them together, and then draw them out
anteriorly to make the Pig’s snout. Essentially these same changes occur in the development of the human face from the same original parts,
except that, fortunately from our point of view, the “ drawing out ” procedure is not carried to such an extreme. It is of some interest to note
in this connection that a failure in the fusion of the naso-median processes with the respective maxillary processeson one side or both results in the formation of the defect known as “ harelip.” An inspection
of Figure 325 will show why this is true.
On the sides of the head the almond shaped eyes do not possess lids,
even at 20 mm., though the follicles of the coarse bristles constituting
the Pig’s eyebrow _a_re,, clearly visible. Both upper and lower lids appear
very shortly, however, ‘at about 24 mm., as folds of skin. Eventually
these folds meet and fuse so that the eye is completely covered for a
time, and in some animals this condition even persists for a while-after
birth, e.g., in the Cat, in which case the animal is said to be born
“ blind.” As regards the eye itself, it has previously been indicated that
one prominent difference between the Chick and the Mammal is the
fact that in the earlier stages the eyes of all mammalian embryos are
definitely smaller than those of comparable Bird embryos. This is still
true at the stage of the latter corresponding to that of the 20 mm. Pig,
and it may be further remarked that the Pig eye is even smaller relatively than that of many other _Mammals, e.g., Man pr Rat.
610 THE LATER DEVELOPMENT OF THE PIG
THE NERVOUS SYSTEM
In the preceding chapter the development of the nervous system was
carried to the point characteristic of a 10 mm. Pig, and in so doing it
was found convenient to treat it by parts. These involved the brain, the
c°,.p°,., qu,d,..:¢m|m cerebral hemisphere
     
   
cerebellum
olctory bulb
   
 
   
A from 81 mm. embryo
cerebral hemisphere
parietal lobe
Sylvlan fissure
I frontal lobe
sulcus rhlnalis
   
pyriform lob
was hypophysls
spinal cord
 
olfactor tract
7 olfactory bulb
B from 230 mm. embryo
Fig. 326.—Lateral views of two stages in the development of the Pig brain. In B
the corpora quadrigemina are entirely covered by the cerebrum and cerebellum.
neural tube, the cranial nerves, the spinal nerves and the organs of special sense. We shall now proceed with the further development of these
parts so far as seems profitable. ‘
THE BRAIN
The Telencephalon. —' This structure is of course the anterior part
of the prosenoepharlon which is separated from the posterior part (diencephalon) by the same boundaries already familiar in the Chick. As
previously noted it has already started to give rise to its most important
and conspicuous products, the cerebral hemispheres. As in the Chick
THE BRAIN 611
these antero-lateral outgrowths contain cavities, the lateral ventricles,
which communicate with the small remaining space within the telencephalon by the foramina of Monro. This latter space as usual constitutes a small part of the anterior portion of the third oentricle.
It was noted in the discussion of this region in the Chick, that although the cerebral hemispheres are relatively prominent structures in
that form, they never attain the size and complexity characteristic of
the Mammal. In the latter animal their size eventually causes them to
constitute by far the larger part of the brain, and to cover entirely
the mammalian homologues of the Bird’s conspicuous optic lobes. In
addition to their mere size, in the Pig and most other higher Mammals,
their surface area (cortex) is increased by complex foldings, the narrow depressions or fissures between the folds being known as sulci. It
should now he noted that one of the more conspicuous of these sulci
extends horizontally along the ventro—lateral region of each hemisphere,
serving to separate the upper portion, or neopallium, from t.he lower
portion or rhinencephalon. It is therefore called the sulcus rhinalis.
Other sulci within the neopallium serve to divide it into the frontal,
parietal, temporal and occipital lobes or regions, which in turn are still
further subdivided (Fig. 326). The rhinencephalon does not contain
conspicuous sulci, but does give rise at its anterior extremity to the
olfactory lobes or bulbs, while its lateral walls constitute chiefly the
pyriform lobes. Quite evidently the.rhinencephalon is phylogenetically
the older part of the telencephalon, while the neopallium is a recent addition reaching its most conspicuous development in Man.
The Diencepha1on.——This posterior portion of the prosencephalon, whose laterally compressed cavity comprises most of the third ventricle, has already been noted as giving rise to the optic vesicles and infundihulum. The connection of the optic stalks with this part of the
brain is marked as usual by the optic recess which really constitutes the
ventral boundary between telencephalon and diencephalon. Immedi
p ately posterior to this recess and hence definitely in the wall of the di
encephalon, is a thickening which, as in the Bird, is the optic chiasma,
within which eventually the fibers of the optic. nerves cross each other.
Adjacent to the chiasma on the posterior side (i.e., the floor) occurs a
thin region of wall termed the lamina post optica, and immediately beyond that the pouch-like infunklibulum presently makes contact with
Rathke’s pocket growing antero-dorsally from the stomodaeum. As
previously indicated these two latter structures together produce the
adult pituitary or_ hypophysis. The anterior part of this organ, compris612 THE LATER DEVELOPMENT  THE PIG
ing the pars distalis, pars intermedia and pars tuberalis, is derived entirely from Rathke’s pocket, while the posterior part forming the pars
nervosa. and the stalk are derived entirely from the infundibulum.
Upon the anterior side, i.e., the roof of the diencephalon, two structures appear. The more posterior, or really dorsal, is an outpushing
whose lumen later becomes occluded, and which develops into the epiphysis. Anterior to this the rather thin roof of the third ventricle becomes
invaginated, and this invagination divides into two parts which extend
forward into each lateral ventricle. These invaginations or folds are
partially produced and augmented by the development of blood capillaries within their walls, and they thus come to constitute the anterior
‘choroid plexus or plexuses.
The sides of the diencephalon. are eventually thickened to form the
optic thalami, the thalami of each side being connected by a median
fusion of the walls. The transverse band of tissue formed by this fusion
is called the massa intermediu.
The Mesencepha1on.——As previously indicated, the roof of this
region, which in the Bird forms mainly the optic lobes, in the Mammal
gives rise to the corpora quadrigemina. As the name suggests, these consist of four, instead of two, thickened outpushings which, as already
noted, are well covered in the adult by the large cerebral hemispheres.
The more anterior pair are apparently more or less homologous in function with the avian optic lobes, and might be so named, but are not. Instead they are called the superior colliculi. The posterior pair are cen
s ters for auditory reflexes, and hence might be referred to as auditory
lobes, but again their actual names are the inferior colliculi. The sides
and floor of the mesencephalon become greatly thickened by fiber tracts
connecting the anterior andposterior parts of the brain. In the Bird
they were designated as the crura cerebri, though this term is not so
commonly employed ‘in the Mammal. Here these regions are often referred to as peduncles. At all events the growth of these parts com-4
presses the lumen of this region of the brain into a narrow canal connecting the third and fourth ventricles, and universally termed the
aqueduct of Sylvius.
The Rhombencephalon. — It will be recalled that in the Mammal,
as in the Bird, thenposterior part of the brain, i.e., the rhombencephalon,
is early divided into two parts, the anterior metencephalon and the posterior myelencephalon. The former is the shorter region, and indeed consists primarily in itsdorsal aspect of the thickened ‘sloping roof of the
posterior side of the isthmus fold (Fig. 297). As in the Chick this dorTHE NEURAL TUBE 613
' sal region presently undergoes extensive growth to form the cerebellum,
a part of the brain especially concerned with muscular coordination.
The division of this organ into a median lobe, the vermis, and lateral
lobes, which appeared to some extent in the Bird, is still further emphasized in the Mammal, and in addition each lobe develops, extensive foldings (Fig. 326). Ventro-laterally beneath the cerebellum the walls of
the metencephalon are greatly thickened by fiber tracts, partly from
fibers originating in the cerebellum itself, and partly from fibers
passing through these walls to and from anterior parts of the brain.
In this region, as in the mid-brain, the thickenings so caused are
often designated as peduncles. The ventral thickening becomes so pronounced eventually as almost to comprise a sort of reversed flexure. It
is called the pans, and because of the eflect just indicated is sometimes
referred to as the pontine flexure (see the Chick). Beside the thickenings caused by the fiber tracts there is also at deeper levels the development of numerous neurones connected with the cranial nerves which arise
from the sides of this part of the brain. The lumen of the metencephalon remains fairly large, and is considered a part of the fourth ventricle.
Posterior to the metencephalon the myelencephalon becomesa tube
which tapers off into the spinal cord, and is designated as the medulla.
In most respects the medulla resembles the cord except that it is wider,
especially anteriorly, and its extensive roof consists of a thin membrane
into which blood capillaries soon press. This produces a vascular ‘infolding similar to that described in connection with the diencephalon,
and in this case termed the posterior choroid plexus. The broad shallow cavity of this region into which these folds push is also quite extensive, and constitutes the larger part of the fourth ventricle. The ventralateral walls of the medulla are essentially similar to what has already
been described with respect to the walls of the neural tube. They consist
internally of a lining of ependymal cells, a middle mantle layer of neuroblasts which become nerve cells, and an outer marginal layer of iibers. It may be further noted that dissection, or cross sections, show
that a groove runs along either side of the internal wall of this region,
termed the sulcus limitans, dividing it into a dorsal and ventral part.
THE NEURAL TUBE
When last noted at 10 mm. the essential layers and types of cells in
the tube were already beginning to differentiate. Further development
consists mainly in the continued production and difierentiation of these
cells, so that the cord not only becomes larger, but assumes its charac614 THE LATER DEVELOPMENT OF THE PIG
teristic shape. Thus in cross section we find the ependymal cells lining
the now relatively small central canal, and sending their supporting
processes transversely through the substance of the cord. Within the
mantle layer the spongioblasts ultimately all become supporting cells
of other types, while the neuroblasts all finally become transformed into
nerve cells. As a result of growth this layer finally assumes in cross section a somewhat butterfly shape (i.e., with wings extended), constituting
the so-called gray matter of the cord. The dorsal andrventral extensions
(horns) of the “ butterfly wings ” serve to divide the outer marginal
layer into four tracts of relatively white material. These tracts or columns consist of bundles of medulated fibers, the myelin substance in
the fiber sheaves giving the tracts their white appearance. The dorsal
column consists mainly of sensory fibers conducting impulses to the
brain, while the two lateral columns and the ventral column are motor '
paths from the brain to the various spinal nerves.
THE CRANIAL NERVES
The origins of all cranial nerves, save the I and II, have already been
indicated, and there is little more that need be said about them except
to note briefly the parts which they ultimately innervate in the Pig. In
general the relationships of nerves and parts are the same as in the
Chick in so far as comparablestructures exist. Thus the III or oculamotor nerve as usual supplies the inferior oblique, and the superior,
inferior and internal (anterior) rectus muscles of the eye. The IV or
trochlear nerve innervates the superior oblique eye muscle, while the
external (posterior) eye muscle is innervated by the VI or abducens
nerve. Passing to the most anterior of the mixed neigves we find that the
ophthalmic branch of the V or trigeminal nerve comes to supply the
snout, eyeball, and upper eyelid; the maxillary branch supplies the upper lip, jaw, palate, face and lower eyelid; the mandibular branch supplies the tongue, lips, muscles of the jaw, the lower jaw itself, and the
external ear. The VII or facial’ nerve was but slightly developed at 10
mm. As its name suggests, it supplies the face, and is primarily motor,
though the existence upon it of the geniculate ganglion shows that it
contains some sensory fibers. These fibers come eventually to join the
mandibular branch of the V nerve and evidence indicates that they concern the sense of tiiste. The VIII is of course" the auditory nerve, and is
‘entirely sensory, being concerned with both hearing and the sense of
equilibrium. Though at first closely associated with the VII its ganglion
later becomes more distinct, and eventually divides into two parts the
THE SPINAL NERVES 615,
vestibular ganglion and the spiral ganglion. The branch from the former supplies the semicircular canals, is termed the vestibular nerve,
and is concerned with equilibrium. The cochlear nerve from the spiral
ganglion innervates the cochlea, and is concerned with hearing. The IX
or glossopharyngeal nerve fibers are mainly sensory, and come to sup-V
ply the pharynx and tongue. Such motor fibers as there are pass to the
pharynx. The X or vagus nerve develops further as follows: Sensory fibers from the ganglion jugulare come to innervate the external ear,
while sensory fibers from the ganglion nodosum eventually reach the
pharynx, larynx, trachea, esophagus and thoracic and ‘abdominal viscera. Motor fibers of the X nerve innervate the pharynx and larynx,
while other motor fibers connect with the sympathetic ganglia, and supply the visceral musculature. The XI or spinal accessory nerve, as previously noted, loses Froriep’s ganglion (which disappears), and thus
this nerve becomes entirely motor, and its fibers are very closely associated with the motor fibers of the vagus. Many of them also run to sympathetic ganglia, and thence to the viscera. Other motor fibers of this
nerve help to. innervate the pharynx and larynx, while still others originating along the cervical region of the cord proceed to the trapezius
and sterno-cleido-mastoid inuscles. The XII or hypoglossal nerve is the
motor nerve oflthe tongue. The muscles which it innervates originate
further back and migrate anteriorly as the tongue develops, carrying the
branches of the XII nerve along with them. Indeed phylogenetically the
tongue muscles are probably derived from the occipital myotomes, and
the XII nerve was -originally a spinal nerve which has recently become
cranial. '
The origin and development of the I and II cranial nerves will be
taken up in connection with the organs of special sense along with
which they develop.
SPINAL NERVES
The Somatic Nerves. —— As regards the further development of the
somatic spinal nerves, it may be said that their afierent and efferent fibers grow until they come in contact respectively with skin or muscle.
Then as the latter parts develop and move further away the. fibers grow
so as to maintain their contact. The sheaths of these fibers have two.
sources. The neurilemma is formed of cells of ectodemial origin which
accompany the fibers as they grow out. The myelin sheath. on the other
hand is not itself cellular; but is a cell product which accumulates at
numerous points between the neurilemma and the nerve fibers. These
616 V THE LATER DEVELOPMENT OF THE PIG
accumulations then spread until they meet, the meeting points forming
the nodes of Ranvier.
The Autonomic Nerves. ——The origins of the autonomic nervous
system have already been stated, and the fact that it involves both parasympathetic and sympathetic parts. Each part of course has to do with
controlling the involuntary movements of the viscera, and as in the case
of the somatic nerves, when the fibers make contact with the organs
which they are to innervate they grow with them. It is of interest that
the two parts of the system largely overlap with respect to the structures
which they reach, and that they have opposing functions. Thus the symp_athetic fibers reaching the heart from certain postganglionic neurones
carry accelerating nerve impulses. On the other hand, impulses in the
parasympathetic fibers from the brain via the vagus nerve to postganglionic neurones on the organ itself, have a retarding influence.
THE ORGANS OF SPECIAL SENSE
THE OLFACTORY ORGAN AND I NERVE
Following the formation of the olfactory pits, and the establishment
posteriorly of their communications with the oral cavity, the further
development of the olfactory organs proceeds as follows: In the lateral
walls of each nasal chamber folds develop known as conchae or nasaturbinals, these folds being more numerous in many lower animals and
in the human fetus than in the human adult. Meanwhile the epithelium,
at first simple cuboidal, soon becomes more or less stratified columnar
throughout a large part of its extent, with the occurrence of many ciliated and goblet cells. On the more dorsal conchae, and on the median
septum formed by the fusion of the naso-median processes, however, the
original cuboidal epithelium becomes transformed into that of the specifically olfactory type. In these regions no goblet cells are formed, and
the tall columnar cells which develop here lack cilia.‘Also just beneath
the surface certain of the cells turn out _to be neuroblastic. From each
of these a fine bristle-like process projects through the epithelium to
the surface. At the same time from its opposite pole each of these cells
sends an axone to the olfactory bulb or lobe of the brain. The bundle of
axones from each of the two olfactory areas then come to constitute the I
or olfactory nerves’. Eventually the various nasal sinuses, i.e., the'ethmoid, maxillary and frontal are developed by the invasion of the bone
by the non-olfactorys nasal mucosa which gradually excavates the bone
‘substance, and then lines the spaces so formed. The further development
THE AUDITORY ORGAN -617
of the posterior nasal passages and the internal nares will be referred to
in connection with the account of the oral cavity.
THE EYE AND ‘OPTIC NERVE
Except for one feature the development of this important organ is essentially the same in the Mammal as in the Bird, where it was described
in some detail. The vascular pecten, presumably an organ aiding in the
nutrition of the inner parts of the Bird eye, does not exist in the eye of
the Mammal. There are, however, blood vessels of course which supply
the mammalian retina and lens. These are capillaries arising from a
branch of the ophthalmic artery. This branch enters the optic cup along
t the groove on the ventral side of the optic stalk by way of the proximal
part of the choroid fissure. It is atfirst called the Ityaloid artery because it supplies only the developing lens, but later it supplies the retina also, and is then called the central artery of the retina. Shortly after
it appears, axones from the cells of the neuroblasts (future ganglionic)
layer of the retina start growing back along the artery which they soon
come to surround. As the number of these fibers increases they encroach on the tissue of the original stalk. Finally they become medullated and surrounded by a connective tissue sheath, while the old stalk
cells are virtually eliminated. Thus are produced the I or optic nerves.
As is well known, in the case of the mammalian eye the fibers from the
median sides of the two retinas cross in the optic chiasma, while those
from the lateral sides do not.
As suggested the development of the eye proper, aside from the
points noted, is so similar to that of the Chick that no further comment
on it is deemed necessary.
THE AUDITORY ORGAN
The Membranous Labyrinth. -—- In the 10mm. Pig the only indication of the auditory organ was the occurrence of the usual otic vesicle with its upgrowing endolymphatic duct. It now remains to state
that from this vesicle the membranous labyrinth of the inner ear develops essentially as in the Bird, except that 'n the Mammal one feature of
it develops considerably further. Thus it wi 1 be recalled that in the former case the semicircular canals arise from the upper part of the otocyst
‘termed the utricle. Then the lower portion of the otocyst partly con- _
stricts away, and produces an outpocketing called the sacculus. Up to '
this point the situations in the Bird and Mammal are similar. In the
Bird, however, it will be remembered that the larger part of the ventral
618 THE LATER DEVELOPMENT OF THE PIG
 
 
 
posterior
semi cir;ulu
~ canal
endolymphatk duct
endolymphatlt duet “Perm.
semicircular canal _-_ ‘
posterior
 
 
superior semicircular canal
endoiymphatic duct
' posterior}
 
_._..——_cochiur duct
(ductus eociilearls)
A rgan oi‘Corti
'‘ cochlear duct
3
E
n
3
In
S
U‘
E
:
 
 
ienestra rotunda ‘
zochlear duct
Euxuehian tube
. auditory nerve
seal: vestibuli
scaia tympani
 
Fig. 327.--A,'B, C and D, stages in the development of the membranous labyrinth of the Human ear. After Sireeten Although this is the Human ear and not
that of the Pig, the latter is presumably very similar, as are those of all Mammals
so far as known. All views are of the left ear from the left, i.e., lateral, side. A.
The otic vesicle from a 6.6 mm. embryo, showing rudiments of the membranous
semicircular canals» starting to form, also the beginning of the endolymphatic duct.
B. Membranous labyrinth from a 13 mm. embryo. C. Membranous labyrinth from
a 20 mm. embryo. D. Membranous labyrinth from a 30 mm. embryo. E. A semidiagrammatic representation of the middle and inner ear opened from the side.
Modified from various sources. F. A diagrammatic section through one side of the
cochlea, including of course the scala tympani kind vestibuli and the cochlear duct,
showing the organ of Corti.
portion of the otocyst is not involved in the sacculus, but grows out into
a relatively short tube termed the lagena. In the Mammal these same
parts exist, but here'the whole “ lagena ” is called the ductus cochlearis
or cochlear duct, and its connection to the utricle becomes narrowed to a
slender tube, the ductw -reuniens. Furthermore the remainder of the
mammalian ductus cochlearis continue: to grow until it has produced
i
I
i
1
i
fE5¢a.
THE AUDITORY ORGAN 619
an extensive spiral tube on whose floor the cells eventually become re.
arranged and differentiated to form the organ of Corti, and the tectorial
membrane. These last named structures, the most elaborate parts of the
organ of hearing, have no counterpart in the Bird. This, it may be suggested, is a somewhat remarkable fact in view of the auditory stimuli
which some members of this latter group can produce, and hence presumably appreciate. Surely the song of the Nightingale should require a
more complicated organ of reception than the Pigs grunt! Finally it remains to state that, as in the Chick, the whole membranous structure
derived from ectoderm is closely covered by a mesenchymal layer, the
membrana propria (Fig. 327).
The Bony Labyrinth.—Again as in the Bird, there has been developed around the membranous labyrinth and its mesenchymal membrana propria a bony labyrinth, the two labyrinths being separated by
the perilymphatic space. Naturally, however, in this case the bony capsule or labyrinth has also to be more elaborately formed in order to encase the spiral ductus cochlearis. Not only does it also become spiral in
order thus to encase this region, but in doing so it becomes divided into
two channels. One, dorsal to the ductus cochlearis, is the scala vestibuli,
while the other ventral to it is the scala tympani. At the apex of the
spiral, at the end of the ductus cochlearis these channels communicate.
At the other end surrounding the sacculus and the utricle the wall of
the scala vestibuli contains the fenestra ovalis to whose membranous
covering is attached a bone of the middle ear. The wall of the scala
tympani in this region contains the fenestra rotunda also covered by a
membrane.
The Middle Ear. —— Considering next the middle car we find again i
the same parts involved as in the Chick, but once more with a slightly
‘ dilierent outcome in certain respects. The first or hyomandibular pouch.
grows out-until it makes contact with the ventral part of the corresponding visceral furrow. This initial contact, however, does not long continue. The upper part of the pouch enlarges, but at the same time withdraws somewhat from the ectoderm of the furrow, while between them
mesenchyme develops. Presently within this mesenchyme cartilaginous
concentrations arise, representing the developing ear bones or ossicles.
In this case, however, instead of there finally developing only one such
bone, the columella, three of them appear——-—the‘ malleus, incus and‘
stapes ( Fig. .327). At the same time that the cartilaginous anlagen are
becoming ossified to form these bones, the mesenchyme surrounding
them is being absorbed. As this occurs, the upper end of the visceral
620 THE LATER DEVELOPMENT OF THE PIG
pouch once more extends so that it surrounds the developing ossicles,
including a little of the disappearing mesenchyme. It also again almost
reaches the outer ectoderrn, being separated from it only by a thin sheet
of mesenchyme. Thus there is formed the permanent cavity of the
‘ middle ear, or tympanic cavity. The part of the visceral pouch between
this cavity and the pharynx remains, of course, as the Eustachian tube.
It thus also comes about that the tym panic membrane or tympanum consists, as in previous cases, of tissue derived from each of the germ layers, the outer lining being ectodermal, the middle layer mesodermal,
and the inner lining endodermal. On its median side the lining of the
tympanic cavity is in contact with the bony capsule of the inner ear, and
so forms a membrane over each of its two fenestra. To the membrane
covering one of these, the fenestra ovalis, the stapes is attached, while
at the other end of the bony chain the malleus of course is fastened to
the tympanum. Though most of the mesenchyme about the ear bones is
ultimately absorbed, some of it becomes dilferentiated into the small‘
muscles attaching the ossicles to the wall of the tympanic cavity. It is
also interesting to note that in Man this mesenchyme does not entirely
disappear until a few months after birth. This apparently serves to prevent free movement of the ossicles, and thus to protect the ear of the infant from too strong stimulus by loud noises.
Homologies.——Turning now to the possible homologies of the
mammalian ear bones, it will be well to recall the situations which were
described in the Frog and Chick. Thus in the former animal, though
only one bone, the columella, finally existed as a separate entity within
the completed middle ear, there were originally two elements concerned.
For, fused to the inner end of the columella, there was also the operculum, lying within the fenestra ovalis. At its outer end, moreover, the
columella connected with a ring of cartilage around the tympanic membrane called the annulus tympanicus. In the Chick there was again a
columella which fused with an opercular element, in that case called
the stapes, but the -annulus tympanicus was lacking. In these cases it
was suggested that the columella was possibly the homologue of the
hyomandibular element ofthe hyoid arch of the primitive fishes, and
that the annulus tympanicus might be the homologue of the pa1atoquadrate cartilage of such forms. In the Mammal, where there are three
separate ossicles, the question of possible homologies again arises. It
has been suggested that the mammalian stapes corresponds to the columella, and hence ultimately to the hyornandibular, the incus to the
palato-quadrate (primitive upper jaw) and the malleus to Meckel’s carnuxzw-—-.—. .....‘,ws.,..._........._..., C,»
THE ORAL CAVITY 621
tilage (primitive lower jaw). This obviously leaves the opercular element of the Frog and the stapes of the Chick quite out of the picture.
As stated in connection with the Frog, there is good evidence, experimental and otherwise, to support these suggested homologies, and they
are, therefore, quite generally accepted. Thus the intriguing notion that
parts once connected with the coarse work of seizing food have finally
been promoted to the delicate “ white collar ” task of transmitting sound ‘
waves, seems to be well established. It probably affords an example of
functional adaptation correlated with a changing environment.
THE DIGESTIVE AND RESPIRATORY SYSTEMS
The Oral Cavity.-——0riginally the anlage of the oral cavity existed merely as the stomodaeum, a relatively shallow pocket lined with
ectoderm. By the 10 mm. stage, the oral plate which constituted the
stomodaeal union with the fore-gut had broken through, and the roof
of the stomodaeal cavity had given rise to Rathke’s pocket. Subsequent
to 10 mm. the stomodaeum becomes greatly deepened to form the ac~
tual oral cavity, while Rathke’s pocket becomes separated from it, and
as already noted, gives rise to the anterior part of the pituitary. The
deepening of the cavity as just suggested is extensive; so much so in
fact, that eventually we find the tonsils occurring "at about the original
site of the oral plate. This enlargement is brought about chiefly by the _
outgrowth of the mandible, and the various processes giving rise to the
face, nose and upper jaws. The external aspects of this procedure have
already been described, but it remains to indicate some of the details
more especially concerned with the mouth itself. Thus it will be recalled
that the maxillary processes formed the sides of the upper jaw (maxillae) , while the anterior tip was derived from the fused naso-medial processes. This tip is the premaxillaryt region, and from it there grows backward a small median plate constituting the more anterior portion of the
palate, and termed the median palatine process (Fig. 328). By far the
larger part of the permanent roof of the mouth, however, is formed by
the two lateral plates, the lateral palatine processes. These are simply
median extensions of the maxillary processes which soon meet and fuse
in the middle line. The more posterior plate so formed then unites with
the median palatine process and thus together these parts constitute the
complete hard palate. It is now to be recalled that ‘the temporary internal nares open into the oral cavity through its original roof fairly near
the front.,The formation of this new roof beneath the first one, however,
creates a new chamber between the two roofs into which the nares open."
622 THE LATER DEVELOPMENT OF THE PTG
2: mm. D 29 mm.
 
 
median ‘palatine process _
     
   
 
 
 
 
cerebral hemispheres
nasal cartilage
\
.§:_
nasal chamber
 
   
 
 
$3
'5'‘.**?-’*%
..~.\
 
 
 
nasal septum
\\
lateral palatine process '
tongue
nasal cartilage
   
 
nasal septum
fused lateral palatlne process
tongue ,. _
' mandibular cartilage
Fig. 328.——Illustrations to show the development of the roof of the mouth and
the nares of the Pig. A and B. The roofs of the mouths of specimens of the sizes
indicated, the lower jaw having been removed. C and D. Transverse sections of the
snouts of the same specimens at the levels indicated by the lines at each side of A
and of B. E. A transverse” section, made with a microtome, of a snout of a somewhat
older embryo than D at about the same level. This section appears somewhat
smaller than D because it does not show the surrounding parts of the head, and
because it was apparent1y.somewhat compressed laterally in cutting.
THE ORAL CAVITY 623
The further development of the nasal septum to fuse with the new or
1 lower roof then divides this chamber into two lateral parts. In this way
' there is produced essentially a posterior extension of the nasal cavities
 
 
 
 
 
 
tongue
ameloblast layer
5 enamel
- entine
' odontoblast layer
enamel pulp of
enamel organ
dental sac
dental papilla (pulp)
‘ 9--‘iosteum
bone crabesulae of mandible
Fig. 329.—-A. Transverse section through the right side of the
lower jaw and tongue of a Pig embryo somewhat older than the
oldest in Fig. 328, showing the beginning of tooth development. BThe same section shown in A, but at a much lower magnification soas to show the whole jaw, with an indication of the part from which
A was taken. Connection of enamel organ with dental ledge has
gone.
so that the definitive internal nares eventually open well back toward the
throat.
' While this is going on in the roof of the month, the tongue is being
formed in the-floor. As in the Chick it is made up of three thickenings,
a median one called the tuberculum impar, and a pair of lateral ones.
These lateral primordia soon overgrow the median one to form a single
mass which for a time lies between the lateral palatine processes. As
these come together, however, the tongue drops down to its adult posi
tion (Fig. 328).
624 THE LATER DEVELOPMENT OF THE PIG
Finally by the 23-30 mm. stage a thickening of the oral epithelium
(ectoderm) has developed around the border of both jaws. This thickening, termed the labio-clental ledge or lamina, pushes into the underlying mesenchyrne, and presently its inner and outer edges become particularly developed. The outer edge or part is called the labia-gingival
lamina (later a groove), and serves to separate the lip from the inner
part of the originally single thickening (Fig. 329). This inner part is
called the dental ledge or lamina, and within it the teeth eventually develop. Since these latter structures do not occur at all in modern Birds,
and were not mentioned in the Frog where they are not highly evolved,
we shall consider their formation separately along with that peculiarly
mammalian product, hair. _
The Pharynx.—~The pharynx begins at approximately the line
where the oral plate disappears, and thus is the most anterior part of
the alimentary and respiratory tracts to be lined by endoderm. It is also
the part which is flanked laterally by the remains of the visceral arches
posterior to the mandibular, and by the pouches. These arches and
pouches very shortly disappear as such, but as will be apparent, their
remains give rise to Various adult structures as follows:
Thus the second or hyoid pair definitely produce the styloid processes and lesser horns of the hyoid. There is also the possibility, as
noted, that the columella (mammalian stapes) of the car may be derived from it. The third pair of arches give rise to the greater horns of
the hyoid, while from the fourth pair of arches is derived the thyroid
cartilage of the larynx. No distinct fifth arches are ever visible, in the
Pig, but from the region where they should lie come the cricoicl and
arytenoid cartilages. All of these parts are of course involved in the
formation of the larynx, and immediately adjacent structures.
Turning to the products of the visceral pouches we find that, as we
have already noted, the first or hyomandibular pouches take part in the
formation of the Eustachian tubes and tympanic cavities. The second
pair in connection with ingrowths of lymphoidtissue produce the main
or palatine tonsils. The third pair give rise to the main or definitive
thymus bodies (thymus III), which migrate posteriorly until they are
eventually located in the upper part -of the thorax. It is interesting to
note that in the Guinea Pig the thymus bodies are permanently in the
neck instead of the thorax. This is apparently because the third pouches
in this case are so firmly fused to the ectoderm that they cannot be carried backward (Klapper, ’46). In addition to becoming transformed
into thymus tissue this third pouches also produce outgrowthswhich beaun:¢».». %. ._.- -
THE PHARYNX 625
come the chief pair of parathyroids (parathyroid III). These are located in the neck where they are ultimately associated closely with the
posterior parts of the thyroid. With respect to the fourth pair of visceral
pouch derivatives there has been some disagreement. So far as the Pig
is concerned Godwin ( ’4~0) concludes that, as noted, this pair of pouches
are not always present. When they are, he thinks that the remains of the
pouches proper become incipient thymus bodies (thymus IV) which
later disappear. In addition there are produced in this animal two distinct outgrowths either from the pouches if they are present, or if they
llnd visceral pouch
 
 
lst visceral pouch
lllrd visceral pouch Rathke 5 pocket
 
Nth visceral pouch
Fig. 330.—The pharyngeal region of a 10 mm. Pig embryo, showing diagrammatically the regions iroin which the thyroid, thymus and parathyroid bodies either
have been, or will be, derived.
are not, from the region of the pharynx where they would be. One of
these outgrowths is an additional pair of parathyroids (parathyroid
IV), each of which, according to ‘Godwin, soon divides into two parts
which persist. Others, however, have claimed that they disappear. The
other outgrowths are the pair of post-branchial bodies. Each of these
bodies eventually becomes embedded in the thyroid gland. According to
Godwin, however, there is nothing to indicate that they ever become actual thyroid tissue as believed by some (Fig. 330).
The thyroid gland as in other forms arises as an evagination from the
‘ floor of the pharynx between the first and second visceral pouches. It
soon loses its connection with the pharyngeal floor and becomes almost,
though not quite, completely divided into two lobes (Fig. 296). These
lobes then migrate posteriorly somewhat to lie eventually at the base of
the neck. As noted the parathyroids are closely associated with the thyroid, and the ultimo-branchial body becomes imbedded in it, whether a
part of it or not. Though the thyroid becomes separated from its point
of origin this point at the future root of the tongue“ is marked, in Man»
626 THE LATER DEVELOPMENT OF THE PIG
   
 
     
   
 
—-—dorsal mesentery
(rnesogastrium)
line of stomac
h attachment of
“°'““ dorsal mesentery
(mesogutflum) ventral mesentery
“var g3St|’0—hep:ttlc omcntum
n —-—ventral rnesentery
‘,5 B (falciform ligament)
d I stomach dorsal mesentery
0'53 m¢$¢“‘¢"Y meso astrium
(mesogutflum) \’ stomach J ( 3 )
liver
D falclform ligament
eplplol: foreman --——§u
gastric-hepatic omencum 5°33‘ mew“?-=77
(mesogastrlum)
dorsal mesentery
(mesogastrlum) “°"‘3Ch
eplplolc foramen ‘ spiem
falciform ligament
dorsal mcsogasrrlurn
spleen
Fig. 331.———A, .C and E are semi-diagrammatic representations of the developing
stomach and mesenteries of the Pig, as viewed from the ventral side. The dash
lines in C and E represent the part of the mesogastrium on the dorsal side which is‘
covered by the stomach in this view. The liver and ventral mesenteries (gastro
hepatic otnentum and falciform ligament) are not shown in these figures as they
would obscure the stomach. B, D and F are diagrams of transverse sections through
A, C and E viewed from the anterior. G is a diagram of a transverse section of
liver, stomach and colon in Man at a later stage when the stomach and colon have
become transverse to the body. Hence this section is mid-sagittal for the body as a
whole» The great ofnenturn, which does not occur in the Pig, is obviously an extension of the fall}. of the original dorsal mesentery down across the anterior (ventral)
wall of the abdomen. It,is largely this fold which accumulates fat in older persons.
THE ESOPHAGUS 627
at least, by a permanent depression, the foramen caecum. The histological differentiation of the thyroid is fairly simple. The endodermal derivatives become broken up into nests of cells which form the secreting
follicles, surrounded by mesodermal connective tissue ‘and blood capillaries.
One other structure of the pharynx remains to he mentioned, the epiglottis. It arises as a thickening in the floor of the pharynx just posterior
   
 
esophagus
 
 
 
 
 
stomach
yolh stalk future duodenum
future ileum
   
bulbus coli
future colon
I2 mm. 24mm.
stomach
caecum
30mm. i 35 mm.
Fig. 332.— Stages in the development of the intestine of the Pig from
the gut loop stage to that in a 35 mm. embryo. After Linehack.
to the lower ends of the third pair of visceral arches. It grows posteriorly, and eventually overhangs the slit-like opening to the larynx, i.e.,
the glottis.
The Esophagus.—At the back of the pharynx the original gut
canal had become separated at 10 mm. into a dorsal and ventral division, and the latter was starting to become differentiated into the respiratory system. The dorsal part, on the other hand, was already becoming
narrowed to constitute the esophagus. In carrying on the description of
these parts it will be convenient to discuss the digestive portion of the
originally undivided gut separately from its respiratory derivatives. In
so doing we shall consider the former first.
628 THE LATER DEVELOPMENT OF THE PIG
The esophageal part of the digestive tract posterior to the pharynx is,
as previously indicated, already relatively constricted. Its inner endodermal lining becomes differentiated into a smooth non-ciliated epithelial layer, and into mucous glands which extend into the connective
tissue (submucosa) beneath the epithelium. The connective tissue and
muscular coats are of course derived from»-mesoderm. ~
The Stomach and Its Mesenteries. — At 10 mm. the stomach was
represented by an enlargement in the primitive gut posterior to the
esophagus. As elsewhere this part of the gut was attached to the dorsal
body wall by its dorsal mesentery (dorsal mesogastrium). This en
 
descending colon
50mm. 95mm
Fig. 333. ——-A continuation of the development of the Pig intestine shown in Fig.
332 with special reference to the region of the colon. After Lineback. .
larged region is already slightly bent with the convex side dorsal, and
very shortly three things happen to it. (1) The bend increases, (2) the
anterior end shifts to the left, and (3) the whole structure rotates on its
longitudinal axis in a clockwise direction when viewed from the
esophageal end. As these movements take place it is obvious that some
adjustment must be made by the attached mesenteries. What occurs is
that the dorsal mesogastrium is extended to accommodate the bending
and rotation of the stomach. Furthermore, since the line of attachment
of mesentery to stomach does not change as the stomach rotates, ‘this line
necessarily rotates with it. Thus in the new position the line of mesenteric attachment simply follows the curve around the left convex side of
the organ. As these changes occur with respect to the dorsal mesentery,
the ventral mesentery has likewise had to shift its position so that it
now leaves the stomach on the concave side of the latter (Fig. 331).
In connection with these alterations certain further facts need now
to be noted as foliows. We have seen how, as the stomach changes its
THE INTESTINE 629
position, the dorsal and ventral mesenteries change to accommodate it.
In the course of this accommodation it is clear that the dorsal mesentery must increase in extent. It remains to add, however, that this mesontery increases more than would be required by the shift of the stomach.
As a result a fold of the mesentery comes to extend out beyond the
stomach so as to form a sort of wide pocket. This fold and pocket are
called the omental bursa, the spleen later developing within the walls
of the fold. Inspection of Figure 331 will show that an opening from the
general coelom into this more restricted pocket area occurs from one
side. This opening, at first quite wide, becomes much narrowed later on,
and is known as the epiploic foramen. In Man the fold itself also develops further to form still another structure which will be noted in
connection with the development of the intestine.
The Intestine. -—The intestine at 10 mm. consisted anteriorly of a
short region to which the liver and pancreas were attached, the duodenum, followed by a loop whose limbs passed into and out of the umbilical stalk. At the ventral apex of this loop a very narrow tube still
represented the yolk-stalk, while the upper end of the posterior limb
bent around caudally to the rectum (Fig. 332, 12 mm.). The whole
structure was of course supported by a mesentery. By the 24« mm. stage
the anterior limb of the former simple loop has become very markedly
coiled, and it is this region which forms the main part of the small intestine. Upon the posterior limb of the loop a short distance from the
apex, a slight outpocketing or caecum was evident at 10 mm., and
shortly thereafter it becomes a distinct diverticulum (Fig. 332, 24 mm.) .
In Man this caecum gives rise to a finger-like extension, the vermiform
appendix. From the point where the caecum grows out the distal part of
the original posterior loop becomes the large intestine or colon. Eventually this part bends so that the small intestine enters it at a right
angle. Also it too becomes coiled, forming a loop, a condition not found
in Man (Fig. 333). In correlation with all this bending and coiling the
dorsal mesentery of these parts of the intestine also becomes thrown
into somewhat involved configurations which it is not necessary to go
into. It is of interest, however, to note a further development of the
mesentery in the region of the stomach which occurs in the case of Man,
but not in the Pig. It occurs as follows:
The fold of the bursa, as previously described for the Pig continues
subsequently to increase in extent in the human embryo, and to grow
caudad, until eventually it comes into contact with the‘ parts of the colon
occupying a transverse position in Man. When this condition is reached
630 THE LATER DE/"EL -0P"MENT OF THE PIG
the bursal fold fuses with theepaetitczmeal covering of the colon, and
later, after birth, continues ‘to grocsw still further in a caudal direction.
At the same time the two liimlitsctftltie fold beyond the line of fusion
with the colon unite with ome antotlzflier no form a double sheet. This sheet,
the great omenlum, thus co-nstiitutmesa. sort of apron covering the lower
abdominal viscera on their veentrz-3 al( anterior) side between them and
the ventral body wall (Fig. 3311]." This is possible because in this region
the ventral mesentery haslnng‘; sithnce disappeared. Later this part of the
omentum usually becoxrnesastoontgeptt lace for fat, a feature which is frequently all too obvious in caldeerirz:-en .and women.
The Recturn.—At the 1(1) Ir::-.1111. stage the cloaca, into which the
large intestine opens, vtras in garoczess of being divided by the urorectal
fold to form the rectum arid tjhe urimogenital sinus. The cloacal membrane also had not yet rutptumerl I. Tlte completion of these processes,
however, is more readilydescr"ihoo din. connection with the description of
the development of the exte» rnulg<=_=2nitalia. and related parts. It will therefore be deferred until that subojeci-tis discussed.
The Liver and Its Nfesantaerie-s.——We are now prepared to return to the develop‘me1:1‘o‘E th:-istx_)utg:roWth of the duodenum. It will be
recalled that in the Pig th_ere is only one hepatic diverticulum insteadof two. This single outgr owtth 0 (ductus choledochus), moreover, had
produced several anter iorl ytllireoctecl buds, the anlagen of the liver tubules, while the remainso ftlneo outgrowth was extending posteriorly as
the anlage of the cystic duct zantllgall bladder (Fig. 307). This anlage
rapidly elongates to form theieefiuiiive duct while its end. enlarges to
produce a bladder. Me anwhiloethaeamteriorly directed tubules grow out
into the ventral mesentery’ wlr:1ete-ethey soon come into contact with the
Vll"‘lliI16 (oniphalozmesenteric ]v-veins; into which they push. They thus
break these vessels up in to finnr umeerable sinusoidal capillaries which
ramify amongst the liv’ert:uh1..t1les.a.ln this manner the tubules and capil
laries come .to constitute the manin mass of the hepatic substance with
i only a relatively small arnountttcifstupporting connective tissue. Having
completed our description-_ of ties dervelopment of the organ itself it remains to say a few words zregs arrli ing its mesenteries.
It has been repeatécllyslatecdthliat the liver develops within the ventral
mesentery of the Stomach ancfiitnodeanum. It may now be ‘added that the
part of this mesentery which .at ztachnes the hepatic mass to the intestine
and stomach is known as the: lesaser orrrentum, or sometimes the gastrohepatic omentum (gastro—lie1::patio cligarnent in the Chick). Beneath the
liver, i.e., between it amdtzlto ' van-ntral body wall, a small portion of mesLIVER AND ITS MESENTERIES 631
entery also permanently persists in the Mammal, where it is termed the
falciform ligament, connecting liver and body wall. This ligament is
absent in the Bird as previously noted (Figs; 331, 335).
The Pancreas. ——~Even as the liver in the Pig has only one origin
instead of two, so the Pig pancreas has only two origins instead of three.
The two primordia in question were already in evidence at 10 mm. One
consisted of an outgrowth from the dorsal side of the intestine of a mass
   
 
—-ductus choledochus
pancreatic ducts
d uodenai
diverciculum
ventral pancreas
Fig. 334.—-Later development of ‘the dorsal and ventral pancreas. Slightly modified from Thyng.
of cords at a level slightly caudad to the origin of the ductus choledochus. The other arose from the ventro-lateral side of the duct itself
(Fig. 307). The two growing masses soon fuse, and the cords of which
they consist become tubular. These in turn produce numerous buds
which develop into one of two things. Part of the buds remain connected
with the tubules, and form the pancreatic acini which produce digestive
secretions. The remaining buds become segregated, and constitute
among the tubules little aggregations of highly vascularized tissue, the
islets of Langerhans. Although the pancreas in the Pig has two origins
as indicated, the adult organ has only one duct. This is derived from the
dorsal outgrowth, and hence connects directly with the duodenum. The
ventral connection with the ductus choledochus in this case disappears
(Fig. 334). ~ , ‘
It is of interest to note at this point that in the Mammals generally
632 THE LATER DEVELOPMENT OF, THE PIG
this double, rather than triple, origin of the pancreas is the common procedure. Whether one or both primordia are to persist as ducts, however,
and if only one, which one, varies in different animals. Thus in the
Horse and Dog there are two permanent pancreatic ducts. In the Sheep
and Man on the other hand there is only one, and in these cases the ventral one opening into the base of the common bile duct. In the Ox, and
in the Pig (as already indicated), however, the dorsal duct is the persistent one, opening as noted into the duodenum.
Lastly, it should be recalled that as the liver outgrowths occur into
the ventral mesentery, so the pancreatic outgrowths push into the dorsal
mesentery. Furthermore, though they start into this mesentery at the
level of the duodenum, the fused pancreatic elements soon extend anteriorly into that part of the mesenterylsupporting the stomach, i.e., the
rnesogastrium. Then later as this forms the omental bursa we find the
pancreas in the more dorsal limb of the bursal fold, which eventually
becomes adherent to the dorsal wall of the coelom (Fig. 331).
The Respiratory System.——— The cartilages of the larynx have already been noted in connection with the fate of the visceral arches.
Also the initial development of the trachea and bronchial outgrowths
were indicated as present at 10 mm. Following this period the main
bronchial tubes and their branches continue to push out into the coelomic spaces (pleural cavities) beneath the esophagus and above the
heart‘( Fig. 303). The lining of the tubules is columnar or cuboidal, but
at their terminals the tubules produce little sacs, the lung alveoli, and
here the epithelium becomes thin and flat. ,
It must now be pointed out that when these endodermal outgrowths
first occur they do not really lie in the pleural cavities. Rather they lie
in a thick sheet of mesoderm which hangs from the dorsal body wall
like a rnesentery, and which, in addition to the trachea and lung buds,
also contains the esophagus. It is the dorsal part of the mediastinum.
Though within this structure at the start, the branching bronchi, as indicated, soon push out of it into the antero-lateral extensions of the
coelom termed the pleural canals or cavities. As they do so they carry,
reflected over them, a layer of mesoderm. This produces the mesothelium of the visceral pleura, the connective tissue about the alveoli
and bronchi, and the cartilaginous rings of the bronchi.‘ At the roots
of the lungs the mésothelium is of course reflected laterally onto the
1 It has been claimed (Clements, '38) that the endoderrnal epithelium of the
alveoli in the Pig (and probably other Mammals) later disappears entirely, leaving
the blood capillaries covered only by a very thin sheet of connective tissue.
~c,.a_..
DIVISION OF BODY CAVITY COMPLETED 633
outer wall of each pleural canal to form the parietal pleura. Finally it
remains to note that the pleural (coelomic) spaces within which the
lungs lie are not at first separated posteriorly from the rest of the
coelom. This and the completion of the pericardium comes about in a
manner which will now be described.
 
   
 
pleural cavity
> leuro-perlcardlal septum
aorta
ventral mesogastrium '_ -r
lT'|CS€|'1E¢I'y ..
Fig. 335. ——Diagrams to illustrate the separation of the pleural, pericardial and
abdominal cavities, and the formation of the diaphragm in the Pig and other Mammals. A. Transverse section of the body just behind the septum transversum. B.
Transverse section of the body through the lung region. C. Lateral view of median
region showing forming septa in relation to heart, liver, lungs and gut.
COMPLETION OF THE DIVISION OF THE BODY CAVITY
The Diaphragm. ——The development of the pericardium and diaphragm has already been described somewhat in the case of the Bird
where, however, the strictly diaphragmal parts are incompletely formed.
Also the structures involved are somewhat different in their origin. We
shall therefore start from the beginning in the Pig.
The first part of the diaphragm to appear is the septum transversum.
In this case it consists of a layer of tissue growing dorsad from the ven634.« THE LATER DEVELOPMENT OF THE PIG
tral body wall just anterior to the liver to whose face the septum is
fused. The median part of this septum also forms the posterior wall of
the pericardial cavity, i.e., the part of the parietal pericardium separating the cavity from the coelom posterior to it. The sides of the septum, however, form the ventro-lateral parts of the diaphragm separating
the ventral portions of the pleural cavities from the coelom posterior to
them. The dorso-lateral parts of the diaphragm completing this separation are formed by a pair of membranes, the pleura-peritoneal folds,
growing out from the body walls-(Fig. 335, A). In the middle they meet
the dorsal mediastinum and complete the diaphragm. These folds also
extend anteriorly in such a way as to bound the pleural cavities (canals) ventrally and the pericardial cavity dorsally. The ventral and
caudal growth of the lungs then occurs, causing these organs to lie
more on either side of the heart than above it. As this takes place the
lungs split off more and more of the pleural-peritoneal folds from the
body walls, and push these augmented folds before them._As this occurs
on the median side next to the heart, the folds come to constitute the _
lateral and ventral as well as the dorsal pericardial wall, and likewise
the medial pleural walls. Hence these parts of the pleural-peritoneal
folds (septum) are called the pleura-pericardial septum (Fig. 335, B, C ) .
The posterior pericardial wall formed by the median part of the septum transversum has already been noted. Anteriorly where the vessels
of the heart emerge, the parts of the parietal pericardium come together, and are reflected over the heart muscle as the visceral pericardium. Here also these parts fuse to form the dorsal mesocardium,
attached to what was the ventral edge of the dorsal part of the mediastinum. It is to be noted, however, that though the pleuro-pericardial
folds meet and fuse ventrally, the pleural cavities never become coextensive. Hence the ventral wall of the parietal pericardium is attached
to the ventral body wall. Thus the pericardium and heart now form a
central mass connecting the former ventral edge of the dorsal part of
the mediastinum with the body wall. This mass might then be referred
to as the ventral part of the mediastinum. Actually because of shifts dur
ing development the various parts of the mediastinum are difierently
named, but the details of this need not be gone into here.
THE CIRCULATORY SYSTEM
When this system was previously discussed we began with a description of the blood islands, and followed with the development of the
heart, leaving the intra-embryonic blood vessels until last. Nothing furTHE ARTERIES 635
th_er need be said of course about the blood islands which soon disappear, and for various reasons it is more convenient to begin with the
blood vessels rather than the heart. We shall therefore start with the
arteries.
THE ARTERIES
The Aortic Arches and Related Vessels. -—It will be recalled
that at 10 mm. the first pair of aortic arches had disappeared, while the
third, fourth and sixth remained, the fifth being vestigial. From the base
of the third pair the external carotids were just beginning to develop,
while the sixth pair had produced rudimentary pulmonary arteries. Dorsally the arches on each side were still connected by the dorsal» aortae
which continued anteriorly as the internal carotids. Posteriorly the aortae had fused as far forward as the anterior appendages, and posteriorly
to the tail.
Subsequent to 10 mm. we find that the base of each third arch between the origin of the respective external carotid and the point of origin of the fourth arch becomes lengthened somewhat. These lengthened
bases thus come to constitute the two common carotids (Fig. 317, B, C).
Conti.r..1ing posteriorly the part of each dorsal vessel between the third
and fourth arches as usual disappears, while on the left side the fourth
arch and the dorsal aorta posterior to it enlarge and persist as the main
or great aortic arch of the adult (Fig. 319, B). At this point two important differences between Bird and Mammal are to be noted. One of
course is the fact that in the former it was the right arch which so persisted. A second difference is that whereas in the Bird the fourth arch
opposite the great aorta entirely disappeared, in the Mammal it does
not. Thus in the Mammal this arch, in this case the right, remains to
form two things. Its proximal part constitutes the brachioceplzalic artery (innominate) while its more distal parts, together with a portion of
the right dorsal aorta, comprise the proximal part of the right subclcwian artery. The rest of the right dorsal aorta disappears. The left
subclavian, it may be noted, arises directly from the distal part of what
was the left dorsal aorta, but which later becomes simply a part of the
main aortic arch. The genesis of the right subclavian distal to its aortic
portion will be referred to presently. It now remains to add in connection with the carotids that in the Pig the left common carotid usually
shifts its point of attachment so that eventually it does not arise directly
from the left (main) aortic arch. Instead it emerges from the brachiocephalic close to the right common carotid (Fig. 319).
636 THE LATER DEVELOPMENT OF THE PIG
Passing now to the sixth aortic arches we are familiar with the manner in which they take part in the formation of the pulmonary arteries
in the Frog and Chick. It has been indicated also that this same situation occurs at first in the Pig (Fig. 316, E). Subsequent to 10 mm., however, certain changes occur which are a little different from events in
the Chick, or in other Mammals. Thus in the case of the Pig the two
pulmonary branches which proceed from the upper parts of the sixth
arches to the lungs, fuse with one another in their proximal regions.
This single branch then retains the connection with the left sixth arch,
but loses the connection with the right sixth which disappears completely. In this fashion it comes about in this animal that only the left
sixth arch is involved in the permanent pulmonary circulation (Figs.
317, 319). Meanwhile there develops within the truncus arteriosus a septum dividing it into two channels. One as usual leads from the left ventricle to the systemic aorta, and the other from the right ventricle to the
single pulmonary artery. In the Bird it will be recalled.that the portion
of each sixth (pulmonary) aortic arch between it and the respective main
aorta persists until hatching as a duct of Botallo or ductus arteriosus.
In the Pig and other Mammals, however, only the left so persists. Its
embryonic function and ultimate fate are similar in the Mammal to
what they were in the Chick, and will be referred to again in connection
with the development of the heart.
The Intersegmental Aortic Branches and Their Derivatives.
—- It may he recalled that the Pig like the Chick has intersegmental arteries, and that anterior to the seventh cervical they have fused to form
the vertebral and basilar arteries. It remains to note their further development as follows:
Posterior to the seventh cervical, the intersegmentals in the anterior
part of the thorax also become fused antero-posteriorly, and disconnected from the aorta. Thus independent longitudinal vessels are produced in this region also (Fig. 317). Here, however, they come to supply the breasts, and are known as the mammary arteries. Returning now
to the seventh cervical intersegmentals, it will be recalled that at 10
mm. these vessels have started to enlarge slightly in connection with the
development of the subclavians. In fact the left one, continuing to enlarge, comes to constitute the entire left subclavian, which as noted,
thus takes its permanent origin from the dorsal aorta. The right seventh
cervical also enlarges, but only forms the distal part of the right sub
clavian. This is l)ecause’the proximal part on this side is formed from
the right fourth aortic arch, and a short portion of the right dorsal aorta
THE VEINS 637
between the arch and the origin of the right seventh cervical. The part of
the right dorsal aorta posterior to its junction with the seventh cervical
of course disappears. Reference to figure 319 will make it clear how
these developments result in the origin of both the vertebral and the
mammary arteries on either side from the subclavians.
It is of some interest in connection with this origin of the subclavians
to recall that in the Chick the so-called primary subclavians arise as
branches of the eighteenth segmental arteries. Then a shift later occurs
so that the permanent subclavians arise from the common carotids. In
the Pig, as we have seen, it is the seventh cervical intersegmentals that
are involved in the development of the subclavians, both originally and
finally.
The Aorta and Its Branches Posterior to the I-Ieart.—The
origins of the coeliac and anterior mesenteric arteries have already been
noted as occurring at 10 mm. The more anterior of these, the coeliac,
eventually comes to supply the stomach, liver, pancreas and spleen,
while the anterior mesenteric passes mainly to the anterior and middle
intestine. Posterior to the anterior mesenteric the renal arteries grew
from the aorta at 10 mm. in connection with the mesonephros. Eventu
ally when the metanephros develops, other arteries in close association
with the original mesonephric vessels supply the new organs. The posterior or inferior m.e.senteric artery had not arisen at the 10 mm. stage,
but develops at about 12 mm., and sends branches to the posterior part
of the intestine at approximately the point where the latter emerges
from the body-stalk. It continues to supply this part of the alimentary
tract.
The largest branches of the aorta during fetal life in the Mammal
are the large umbilicals whose origin has already been mentioned. It
was also noted that even at 10 mm. each of them had given rise to a
small branch, the external iliacs. These increase in size as the hind limbs
develop, and finally at birth they become the main arteries supplying
the hind legs. At the same time parts of the former umbilicals within
the body, but distal to the point of origin of the external iliacs, persist
as small branches, the internal iliacs. The parts of the umbilicals proximal to the external and internal iliacs remain as the common iliacs.
THE VEINS
Derivatives of the Omphalomesenterics. -—-"By 10 mm. the yolksac had virtually disappeared, and with it the omphalomesenteric veins
leading to it. However, as was noted, the parts of these vessels within
638 THE LATER DEVELOPMENT OF THE PIG
the body proper altered to produce the hepatic portal system. This consisted of the two hepatic veins, the liver capillaries, and a single hepatic
portal vein, with branches draining blood from the intestine. This is essentially the adult situation.
The Umbilical Veins. ———When last noted there were two of these
within the body, though the right one was becoming smaller (Fig. 321).
Presently this latter vessel disappears anteriorly, while its caudal part
persists for a time as a small vein draining the body wall posteriorly
into the left umbilical. The latter vein increases its size within the liver
where, as noted, it forms the posterior major portion of the ductus
venosus. Also, as this occurs, it comes to lie nearer the mid-line, and
thus to pass between the two hepatic veins, which enter it at about the
same point as the hepatic section of the developing posterior vena cava.
As previously noted, the short anterior section of the ductus which empties into the sinus venosus, and was formed from the fused vitelline
veins, now receives the hepatic-s, the major part of the ductus, and the
hepatic portion of the posterior vena cava. Thus this short section becomes the 3'-'lt6I‘.l0I‘ extremity of that vessel. Therefore since the anterior
remains of the posterior cardinals empty into the ducts of Cuvier, it
comes about that the posterior vena cava is the sole vein entering the
sinus from the back part of the body. The further development of the
posterior parts of this important vessel will be considered presently.
As to the fate of the left umbilical, its function of course ceases entirely
at birth, the anterior portion of its path (the duptus venosus) being
marked by a fibrous strand, the round ligament of the liver.
The Anterior Cardinal System and Anterior Vena Cava. ———- As
described at 10 mm. the anterior cardinal system consisted of the anterior cardinal veins and their capillaries, and the external jugulars
which joined the cardinals just anterior to the ducts of Cuvier. It was
also noted that each subclavian, consisting of an enlarged intersegrnental vein, entered the posterior cardinal virtually at the point where anterior and posterior cardinals passed into the respective Cuvierian ducts
(Fig. 322, E). Continuing with the subsequent story it may now be
stated that with the caudal shift of the heart and ducts of Cuvier, these
‘parts soon come to lie posterior to the limb buds. As a result of this the
entrance of the subclavians shifts forward so that presently they definitely empty into the anterior cardinals (Fig. 322, F).
The next steps consist in the shifting of the previously symmetrically
arranged veins so that they enter the right side of the heart. This is
brought about mainly by the development of a diagonally transverse
THE POSTERIOR CARDINAL SYSTEM 639
vessel. This vessel runs from the junction of the left subclavian with the
left anterior cardinal, across to the right anterior cardinal, slightly pos-'
terior to the point where that vessel receives the right subclavian. In the
meantime the left anterior cardinal posterior to the origin of the new
vessel disappears (Fig. 322, H, I). Hence all the blood from the left anterior region, along with that from the right, now has to enter the sinus
venosus through the right anterior cardinal and duct of Cuvier. With
these changes the vessels concerned have their adult arrangement, and
may be given their adult names. The new transverse vessel is the left
innominate vein. The section of the former anterior cardinal between the
junction of the left innominate with this cardinal and the entrance of the
right subclavian, is now the right innominate vein (Fig. 322, I). The
posterior or proximal portion of the right anterior cardinal between the
entrance of the left innominate and the right duct of Cuvier, plus that
duct, is now the anterior vena cava. As will presently appear both posterior cardinals have by this time disappeared as such, though certain
remnants persist which will be described below. Finally the distal parts
of both anterior cardinals cephalad to the points of entrance of the respective subclavians and external jugulars are now termed the int-:-rnal
jugulars.
The Posterior Cardinal System, Posterior Vena Cava and Related Vessels. — It will be recalled that at about 10 mm. the posterior
cardinals had practically disappeared at the mesonephric level. Their
posterior remains, however, drained into the newly formed median anastomosis of the subcardinal sinuses through numerous capillaries. Anteriorly the left subcardinal had almost lost its connection with the anterior
part of the left posterior cardinal‘. At the same time the right subcardinal had established a connection with the newly formed median vessel
passing through the liver to the sinus venosus. This vessel, together with
the subcardinal sinus and remains of the right subcardinal then constituted the anterior part of the posterior vena cava. Its establishment, as
noted, has thus produced the essentials ‘of a renal portal system. The
final step in this process is the complete severance of the connection of
the left subcardinal vein with the posterior cardinal which occurs very
shortly after the 10 mm. stage (Figs. 320, 322, C, D, E). The further development of the posterior venous system then proceeds as follows:
The posterior parts of the posterior cardinals have from an early period received the external and internal iliac veins which form in con
nection with the posterior limb buds. These cardinals, however, are
gradually replaced by a new pair of cardinals close to the dorsal body
640 THE LATER DEVELOPMENT OF THE PIG
wall, and hence called the supracardinals (Fig. 322, F). The external
and internal iliacs then become attached to these new supracardinals
(Fig. 322, F, H) through the stumps of the old posterior cardinals, now
termed the common iliacs. In the region of the subcardinal sinus_ (the
present end of the posterior vena cava) the supracardinals become connected, at first through capillaries, and then by larger channels, with
this sinus. Just anterior to this region the supracardinals are ‘slightly
developed and presently disappear, though still further forward they
continue to exist and to connect with the anterior remains of the old posterior cardinals (Fig. 322, I ). We shall return to this situation presently. Continuing with the account of the more caudal region, however,
we find that the final steps here are: (1) the degeneration of the left
supracardinal, (2) the connection of the left common iliac with the end
of the right supracardinal, and (3) the shift of the latter to the median
line. The result of this is to make the surviving supracardinal the posterior extension of the posterior vena cava, thus completing that vessel in
its caudal extent (Fig. 322, H, I, I) . Anteriorly the portion of it within
the liver finally works its way to the dorsal surface where it becomes
quite conspicuous before opening into the right atrium of the heart in a
manner to be indicated presently.
Returning now to the more anterior parts of the supracardinals, and
the remnants of the posterior cardinals into which they drain, we find
that these vessels persist somewhat irregularly as the azygos veins. Generally the latter are united transversely, one or the other loses its anterior connection, and both drain into the anterior vena cava through
the remains of a posterior cardinal, now termed the cervico thoracic,
though in the Pig this may not occur (Fig. 322, J) . Hence it may happen
that the left duct of Cuvier is left with no (or in the Pig, few) tributaries. In any event it does not disappear, but instead becomes imbedded
in the heart muscle as the coronary sinus.
In conclusion of this discussion it remains to state that while these
changes have been going on both anteriorly and posteriorly the sinus
Venosus has been absorbed into the right atrium of the heart. Hence,
since the sinus previously received the anterior and posterior vena
cavae and the coronary sinus, this final change means that these three
vessels ultimately open separately into the right atrium.
The Pulmonary Veins.——It will be recalled that at 10 mm. the
‘pulmonary veins ehtered the left atrium of the heart by a common
trunk. It now remains to state that eventually this trunk is incorporated
into the atrium, and its two or more branches achieve separate openings.
THE ‘HEART 641
The Heart. —--When last described at 10 mm. this organ consisted
of a ventro-posteriorly directed ventricle and antero-dorsally directed
atrium. The walls of the former were lined by spongy tissue, the trabeculae carneae, and the chamber was partly divided by a septum growing
toward the atrio-ventricular canal. In the latter the fusion of the
 
   
   
   
anterior vena cava
septum secundum(Il)
' ena cava ‘
P°“"'°r V pulmonary vein
right atrium _ I (I)
septum pr mum
septum secundum (ll)
. left atrium
//2%
f 5; mitralvalves
_ i left ventricle
tricuspid valves
chordae tendineae
right ventricle
foramen ovale
septum II V
Fig. 336. ——-Drawing of fetal Pig heart at nearly full term, opened from the ventral side. B. Semidiagrammatic view of the foramen ovale and septa I and II from
the right side. C. Same from the left side. Arrows in all cases represent directions
of blood flow according to the most recent conclusions. In B and C the dashed
parts of the arrows indicate that a membrane lies between the arrow and _the ob»
server. For a complete discussion of the flow of blood in the embryo of the Chick
and the Mammal see the text on this topic in the account of the Chick, and Fig.
235X.
cushion septa had almost, or quite, completed the division of this orifice
into right and left channels. At the same time the atrium had been
nearly divided by the septum primum growing from -its antero-dorsal
wall. As was indicated, however, this septum had already developed an
opening in its antero-dorsal region called the interatrial foramen secundum. The right atrium received the sinus venosus, and the left the
single pulmonary vein. Further development may now be described as
follows: _
The completion of the cushion septum if not accoinplished at 10mm.
642 . THE LATER DEVELOPMENT OF THE PIG
soon takes place, This is then quickly followed by the completion of the
interventricular septum, and also that of the interatrial septum primum.
This latter event closes the interatrial foramen primum, but leaves wide
open the recently developed interatrial foramen secundum. The heart
therefore is now completely divided into right and left parts except for
this latter opening. Meanwhile there has developed another atrial septum just to the right of the first, called the septum secundum, the beginning of which was shown at 10 mm. (Fig. 313). It too is a crescentshapecl sheet extending from the antero-dorsal wall of the atrium along
its dorsal and ventral walls. Presently it extends all around these walls
and fuses with the septum primum near the atrio-ventricular cushion septum. The new septum secundum, however, fails to become complete in its central region just ventral to the interatrial foramen secundum of the septum primum. This opening in the new septum is called
simply the foramen ovale. As reference to Figure 336 will show its position is such that the middle part of the septum primum acts as a valve
which can functionally close the foramen ovale. Such closure would obviously occur if pressure were applied to the valve from the left side.
We shall return to this matter presently.
Meanwhile as the septa have been thus completed certain further
events have taken place. On the sides of the atrio-ventricular canals flaps
of tissue have developed, two on the left side and three on the right.
These form the atria-ventricular valves (tricuspid right, and mitral left)
which hang downward into the respective ventricles. Here their edges
have remained attached to some of the traheculae carneae, which in these
particular instances become drawn out into strands, the chordae. tendineae, continuous ventrally with the papillary muscles. These, however,
are not all the valves of the heart. As previously noted, the truncus arteriosus also becomes divided by a septum into two channels, the systemic and pulmonary, whifli lead respectively from the left and right
ventricles. It now remains to state that at its union with the heart the
truncus, previous to its division, develops upon its walls two thickenings. Then with the growth of the dividing septum these thickenings are
transformed into six semilunar valves, three in each channel.
Finally in the atrial region it has already been remarked that the sinus venosus has been incorporated into the heart on- the right side, and
the single pulmonary trunk on the left. This of course causes the separate veins previously opening respectively into the sinus and pulmonary
trunk to open directly into the right and left atria. In connection with
this it remains to state that as this occurs portions of the right valvula
THE EXCRETORY SYSTEM 643
venosa of the sinus are retained as valves of the caval and coronary’
openings. Also in the later stages of development the atria of the Pig
and other Mammals acquire the more or less earlike appendages which
have given rise to the name auricle. These it may be recalled occur in
the Bird, but only to a slight extent, and not at all in the Frog.
The Fetal and Adult Circulation.—This topic was discussed
at considerable length in the case of the Chick, and since essentially the
same situation is involved in the Mammal we shall not repeat it here.
The student is urged to reread that section at this point. If this advice is
followed it will be noted that the chief item of difference cited between
the Bird and the Mammal concerned the character of the interatrial
opening and its method of closure. There was only one septum in the
Bird, corresponding to the mammalian septum primum, and instead of
a single opening it contained several. These were closed at hatching by
the equalization of pressure on the two sides of the septum which took
the stretch out of it, and allowed the perforations to close by contraction. In the Mammal there is the same equalization of pressure at birth.
In this case, however, the result is to press the valvelike part of the
septum primum against the foramen ovale in the septum secundum, and
thus functionally to close that opening. The actual fusion of the parts
of the two septa does not occur for several weeks and sometimes several
months post partum. Indeed a probe patency may exist permanently,
but so long as equal pressure in the atria is maintained, this is of no
consequence. The closure of the duct of Botallo was also noted in the
discussion of this topic in the section on the Chick, and it was indicated
that its permanent closure in the Mammal might occur in about a
month. As a matter of fact the time varies in different animals, being
3-4 weeks in the Pig and 6-7 weeks in Man. The relation of the failure
of the closure of the septum or of the duct to infantile cyanosis in Man
was indicated in the discussion of this topic in the Chick (Figs. 236X,
- 336).
THE URINOGENITAL SYSTEM
THE EXCRETORY SYSTEM
The Mesonephros. —— When the excretory system was last discussed
the pronephros had entirely disappeared, and the .mesonephros was
well developed and functional. Indeed it is relatively larger at this and
immediately subsequent stages than when it reaches its peak in absolute
size and activity. Thus it continues to grow and funhtion for some time
644 THE LATER DEVELOPMENT OF THE PIG
beyond the 60 mm. stage, when it is replaced by the metanephros. In the
male of course certain parts of the mesonephros persist permanently in
connection with the reproductive system as will be indicated presently.
The Metanephros. —The origin of the permanent kidney or metanephros has already been indicated. Thus at 10 mm. each of these organs consists of a short tubular outgrowth from the postero-dorsal side
of the respective mesonephric duct just short of the point where the latter enters the cloaca. At its anterior end this outgrowth, the future ureter, has an enlargement, the anlage of the future pelvis of the kidney.
Surrounding this is a concentration of nephrogenic mesoderm (Figs.
296, 323). ‘ '
Further development consists in the forward growth of the ureter and
its pelvic enlargement, which carries with it the nephrogenic mesoderm
to a position dorso-lateral to the middle of the mesonephros. Meanwhile
from the pelvic enlargement there have grown out into the surrounding
nephrogenic substance numerous outgrowths which soon become hollow, and which represent the collecting ducts. At the same time concentrations within the nephrogenic mesoderm have become vesicular, and
the vesicles send forth outgrowths which become tubular and connect
with the collecting tubules. Later these outgrowing secreting tubules become even more convoluted than in the case of those of the mesonephros. Finally, each vesicle becomes invaginated by a glomerulus,
and thus is transformed into a Bowman’s capsule. The blood supply to
both glomeruli and tubules is entirely arterial in the metanephros. This
supply also differs from that to the mesonephros in that it is furnished
to each permanent kidney by one main renal artery instead of by several
smaller branches.‘
The details of development of the caudal outlets of the ureters and
mesonephric ducts can best be described in connection with related parts
of the reproductive systems, and will be taken up presently. Before proceeding to that topic, however, there remains a word to say about certain other organs closely connected with the kidneys, though not excretory.
* The Adrenals.—As we have seen in the case of the Frog and
Chick-, these structures vary considerably in form, but always consist of
two parts having specific origins. The medullary substance develops
from cells which: have their origin in the neural crests. These cells migrate from the crests along with some of the cells which are to form the
sympathetic ganglia, and many of them, after acquiring a special staining capacity, become associated with these ganglia. Others, now called
I
I
i
THE REPRODUCTIVE SYSTEM‘ 645
8'“ 10°?
mesoneph ros
 
 
 
   
yolk stalk .- V
. Hantolc suIkl""b"'°' "I"
mesonephros
2 urinary bladder
 
urinary bladder
Fig. 337. —Semi-diagrammatic illustrations of the development of the 1netanephros, the adult ureters and gonoducts, and the separation of the cloaca into anal and
urino-genital regions in the Pig. A. Unseparated cloaca with no indication of sex
differentiation (about a 10 mm. embryo). B and D. Progressive separations of the
cloaca. and development of the urino-genital ducts of the male. C and E. The same
process in the female.
chromafiin. cells, come to lie beneath the mesoderm of the coelom. The
larger number of these chromafiin cells, however, form a mass adjacent
to the cephalic end of the kidneys, where they form the adrenal medulla.
Around this medullary substance which becomes arranged in cords,
there then accumulate mesodermal cells which constitute the adrenal
cortex.
THE REPRODUCTIVE SYSTEM
The Gonads.—The later development of both, testes and ovaries
has been previously described at some length in general and in connec646 THE LATER DEVELOPMENT OF THE PIG
tion with specific forms. It is essentially similar in all these cases, except in regard to certain aspects of the mammalian ovary, which were
also considered previously when mammalian oiigenesis was discussed.
diaphragmatic ligament
metaneph ric kidney
 
       
 
 
 
inguinal ligament
portion of gubernaculum
..‘.'»».' ’"“" — —.‘\._L__ _ inguinal ligament
scrotal ligament
scrotal sac
tunita vaginalis
vas deleren: uh‘
   
 
 
scrotal ligament
processus vaginalls
inguinal canal
rectum
K “ ejaculatory duct
" , -1
seminal vesicle _.l,'§4~ g prostate
V35 d°f°l‘¢“‘,r/ a\  bulbo-urethral
‘ pubis
         
   
tunica vaginalis
, inguinal canal
   
Fig. 338.-— Diagrams representing the descent of a Pig testis. A. Before the testis
has started to move. B. The testis about to enter the scrotum. C. The testis in the
scrotum.
We shall not therefore go into this subject again in connection with the
Pig.
The Male Urinogenital Ducts. — As we have seen in the case of
the Bird, so in the Mammal, the mesonephric duct when no longer
needed as a ureter is pressed into service as a sperm duct, 'or 12:15 deferens. Anteriorly the connection between this duct and the respective testis
is made through certain mesonephric tubules which are retained for this
purpose. They, together with the immediately. adjacent portion of the
THE REPRODUCTIVE SYSTEM 647
 
   
   
 
 
I‘
. . _  '\y‘\‘\>\\‘“ \\
kidney metanephros mm, id
ov uct
urinary bladder n  "nth...
 
   
broad ligament ‘ix ‘
- .1. ureter r
UIETUS
§\\\
;- , ll
‘ - "‘.“'.‘—“.”W.*‘!'i\. ' "‘  ectum
kidney oviduct  §;..i~\ *~..a‘ vagina
x...-. . i  '*-"Pr-.'~'-' ~95
,u:erus —- - th y-,’/4r,‘r:...,~:~§-g vestibule
'°”"‘.i “83m¢"‘ °f\ ovary U e I.’.( T ‘fig: labium minus
ovary us .
 
 
lobium moius
clitoris
   
Fig. 339. — Diagrams representing the partial descent of a Pig ovary.
A. Before the ovary has started to move. B. After it has reached its
definitive position.
mesonephric duct become the e piclidymis. The extreme anterior remnant of the mesonephros may persist as the appendix to the epididymis,
while the vestigial caudal remainder occurs as the paradidymis. '
At its caudal end the mesonephric duct when last noted was emptying into the antero-ventral part of the cloaca, which was being separated ofl' as the urinogenital sinus. This division of the cloaca into urinogenital and rectal portions by the urorectal fold is presently completed,
and shortly thereafter the cloacal membrane is ruptured. This of course
648 THE LATER DEVELOPMENT OF THE PIG
puts both cloacal parts in communication with the proctodaeum, the
opening of the urinogenital sinus being termed the ostium urogenitale,
and that of the rectum, the anus (Figs. 337, 340) At the same time that
this has been going on the part of the allantois inside the body has been
dilating to form the urinary bladder. Presently when the urinogenital sinus, into which the allantois opens, becomes completely separated from
the rectum, the cephalic part of the sinus also expands somewhat. Thus
this part is in efiect simply added to the posterior end of the bladder,
forming its proximal portion. The more caudal portion of the sinus,
however, is narrowed instead of dilated, and becomes the urethra.
While this has been taking place the end of the mesonephric duct into
which the metanephric duct opened has been drawn into the urinogenital
sinus, so that these ducts now open separately. Furthermore, the cephalic
growth of the metanephros seems to have pulled its duct forward somewhat. The result is that when the separate openings are achieved, that of
the metanepliric duct is into the antero-lateral part of the old urinogenital sinus, now forming the base of the bladder. The opening of the old
mesonephric duct, however, now the vas deferens, is further posterior
into the part of the sinus whichgnow forms the urethra (Figs. 337, 338).
' It remains to add that slightly anterior to the point where the vas
deferentia enter the urethra each becomes dilated, and the dilation
drawn out slightly to form a small sac, the seminal vesicle. The short
remaining part of the vas deferens between the vesicle and its entrance
into the urethra is termed the ejaculatory duct. Finally the urethral
epithelium gives rise to two glands on the outside of the urethral lumen.
but with openings into it, the prostate and the bulbo-urethral or Cowper’.s gland (Figs. 337, 338). This concludes the part of the male urinogenital duct system which is, so to speak, within the body. The remain‘ing portion, together with a description of the ultimate disposition of
the testes, will be taken up presently. Before doing that, however, we
must return for a moment to the development of the ducts of the female,
and certain other considerations.
The Female Urinogenital Ducts. -—- The oviduct originates in_the
Mammal, .as it has been seen to in the Frog and Chick, from a thickened
ridge of mesoderm lying along each side of the mesonephric duct. This
_ ridge becomes tubular and pulls away from the body wall, to which it
‘ remains attached by’ a fold of peritoneum supporting both ovary and
duct. This fold or double sheet of tissue, homologue of the Chick mesovarium, is called‘ the broad ligament, of which more will be said later
(Fig. 339). There are of course two oviducts, one on either side, and they
THE REPRODUCTIVE SYSTEM 649
at first open separately into the urinogenital sinus. Very shortly, however.
their caudal ends fuse to form the vagina. Anterior to this each duct becomes differentiated histologically into a part called the uterus, and still
further forward into the definitive oviduct or Fallopian tube. As has already‘ been indicated in our introductory discussion of the Mammal, the
degree to which the uterine portions of each duct later fuse to form a single uterus varies in different kinds of animals. In all but the most primitive, however, a slight fusion always occurs to form a region known as the
cervix opening into the vagina by a single orifice. In the Sow and other
Ungulates this fusion continues a short distance anterior to the cervix to
produce a typical uterus bicornis; in Man, of course, the fusion of the uterine parts is complete, giving a uterus simplex. At their anterior ends each
oviduct, as has been seen, develops a funnel or infundibulum which
may or may not embrace the ovary. In the Sow it does, but in Man it
does not. In any event it is of interest to find that this anterior opening
develops. not quite at the anterior tip of the original tube, but slightly
caudal to it. I
So far as the excretory ducts of the female are concerned the ureter
comes to open into the base of the bladder following the division of the
cloaca, just as it does in the male. The mesonephric duct naturally has
no function in the female, but does persist, along with parts of the mesonephros as a vestige. There are asa matter of fact several of these vestiges in both sexes in addition to those already indicated. Some of these
are outside the body, and will be referred to later. Confining ourselves
for the moment, however, to those within, it will be well at this point to
make some further reference to these remnants.
Internal Vestiges of the Reproductive Systems.——The vestigial appendix of the epididymis and the paradidymis respectively have
already been noted. In addition to these in the male, a vestige of the
oviduct may be found in the tissue investing the testis, where it is called
the appendix of the testis. Posteriorly also a further vestige of the fused
parts of -the oviducts may occur as the uterus masculinus. In the female
the.undi~fferentiated anterior tip of the oviduct often remains as a small
vesicle attached to the duct. Also a vestige of the mesonephros is usually
embedded in the broad ligament (mesovariurn) as the epoiiphoron, a
structure previously mentioned as occurring in the Chick. Finally ves
"tiges of the mesonephric duct. or parts of it, may renriain near the uterus
and vagina as the» canals of Gdrtner.
We are now prepared to return to a consideration of the migration of
the gonads, and to the development of external features connected with
650 THE LATER DEVELOPMENT OF THE PIG
both male and female systems. We shall consider the movement of the
gonads first, and we shall begin with the testes.
The Descent of the Testes. -— The student is well aware of course
that in the lower animals, such as the Fishes, Amphibia and Reptiles
the testes remain within the body at their places of origin. Indeed this
is even true in the Birds, which in their way are quite as “ high ” or
specialized as the Mammals. It is only within the latter group, however, that the testes radically alter their position so that in most cases
they are actually outside the original body cavity all or part of the
time. How this comes about is now to be considered.
Both the mesonephros and adjacent testes’ are held against the body
wall by a covering of peritoneum. As they grow they push this covering out into the coelom, but the covering does not cut in above them to
form a mesentery-like sheet. Instead they simply remain beneath it, such
a position being described as retroperitoneal. As development goes on
the testis becomes relatively larger and the mesonephros relatively, and
finally absolutely smaller, so that the former occupies more and more
of the retroperitoneal space. Meanwhile, though the peritoneum (mesodermal epithelium plus connective tissue) does not cut in above the
testis and mesonephros, anterior and posterior to them it is drawn out
into a longitudinal fold within whose layers runs a bundle of connective tissue fibers. Anteriorly the fold and its bundle of fibers extends
from the mesonephros to the diaphragm, and is known as the diaphragmatic ligament (Fig. 338, A). The posterior section of the fold and
fibers reaches to the extreme caudal end of the coelom, this section being
termed the inguinal ligament of the mesonephros. Here a pair of coelomic
evaginations occur, the scrotal sacs or pouches, the cavity in each being termed the processus vaginalis. From the distal wall of each pouch
a fibrous strand, the scrotal ligament, proceeds beneath the epithelium
to the coelom prop,er. There each scrotal ligament becomes united to the
caudal end of the respective inguinal ligament of the mesonephros (Fig.
338). Here it should be incidentally noted that this inguinal ligament
has nothing at all to do in origin or function with the inguinal ligament
of the adult, known in Man as Poupart’s ligament.
While this is occurring posteriorly the testis is outstripping the mesonephros in growth, and as it does so the attachments of the diaphragmatic and inguinal ligaments of the latter organ become transferred to
the former. When this has taken place the united inguinal and scrotal
ligaments are given a single name, the gubernaculum. Thus it comes
about that a gubernaculum extends from the caudal end of each testis
THE REPRODUCTIVE SYSTEM 651
and adjacent epididymis to the bottom of each scrotal sac. We might
now briefly complete the story by simply saying that while the diaphragmatic ligament stretches the gubernaculum contracts, thus pulling
the testis and epididymis back and down into the scrotal sac. Essentially
this is what happens, but as a matter of fact the gubernaculum does not
contract. It merely fails to grow, while the other parts do, so that the
effect is the same as if it did contract. (It is like the case of the boy holding the cat’s tail. He does not pull it. The cat does that.) In the course
of this movement the vas deferens is bent into a loop which passes
across the permanent ureter.
It must now be pointed out that since the testis is retroperitoneal it
does not actually lie in the coelomic space of the scrotal pouch (processus vaginalis) any more than it lay in the general body coelom. Instead it is pulled down all the way beneath the peritoneal covering
which within the pouch is, reflected over it as the tunica vaginalis. Of
course in this process the coelomic space within the scrotal sac is elimil
nated. While this space existed, however, it was connected with the general coelom by the inguinal canal. From what has just been said it must
also be clear that the testes do not really pass into the pouches through
the canals, though the existence of the canals permits the movement.
They pass back of the canals underneath the peritoneum. After the testes
have thus gone into the scrotal sacs the inguinal canals fuse completely
shut, except in a few animals to be indicated presently. Nevertheless, it
is of interest that this spot evidently comprises a point of weakness
which accounts for the occurrence of inguinal hernia in Man. The fact
that it occurs in this case, but seldom if at all in the lower animals is
probably the result of Man’s erect position. There seem still to be certain advantages in walking on all fours.
It remains to state that the movement of the testes just described does
not occur in all Mammals. Thus in the Elephant the testes remain permanently within the body, while in the Rat they pass back and forth,
descending during sexual activity. In this connection it is significant
that the temperature of the scrotum has been shown to be lower than
that of the body cavity. Furthermore, experiment has proven that in
animals in which the testes normally remain permanently in the scrotum
the retention of the testes within the body results in sterility. Lastly, if
in such animals the temperature of the scrotum is‘ artificially raised to
that of the body, sterility also results. Thus it appears that in these
cases the temperature conducive to spermatogenesis and (or) sperm
survival is lower than the normal body temperature.
umbilical stalk
 
   
   
pl'£'pfLlC¢
Iabium mains
 
_ _ ; .,, “ lcbium moius
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90 mm. 0
Fig. 340.——Drawings of ‘stages in the development of the Pig external genitalia.
A and B. The same indifferent stage preceding sexual differentiation. In A the
genital tubercle and related parts are turned posteriorly. In B these parts are reflected anteriorly to show their ventral aspects. C’, E and G represent the progressive development of the genitalia of the male at the stages indicated, while D. F
and H represent corresponding development in the female.
652
THE REPRODUCTIVE SYSTEM 653
The DESCEINC Of the Ovary. — In the case of the ovary and oviduct
we have noted that these organs are attached to the coelomic wall by a
fold of mesothelium and connective tissue called in the Mammal the
broad ligament. Within this fold is enclosed the fibrous inguinal liga~
merit of the mesonephros along with the vestiges of the epididymis
(epoiiphoron) and vas deferens (canals of Giirtner) . In this instance as
development proceeds the inguinal ligament (anterior part of the guber-naculum of the male) apparently exerts no traction. Rather the ovary
and oviduct, pulled downward by their weight, stretch both the broad
ligament and inguinal ligament within it. Shortly the ovary has moved
so far posteriorly that both the oviduct and the ligament are bent
around at a considerable angle. When this has occurred the part of the
inguinal ligament between the ovary and the bend is called the round
ligament of the ovary, and that part between. the bend and the uterus the
round ligament of the uterus. In this manner the ovaries come to lie
much further back in the body than their point of origin, but unlike the
testes they never pass outside (Fig. 339). 3.
The External Genitalia, Indifferent Stage. ——As in the case of
the very early stages of the gonads themselves so also in this case an in»
dilferent stage exists during which sex is indistinguishable. Also, as will
presently appear, we find that the same fundamental structures occur in
both sexes. It is only with later development beyond the 25 mm. stage
that they begin to become differentiated to form the external urinogenital parts of the adult male and female. The parts concerned and
their locations are as follows:
As the urorectal fold is dividing the cloaca into the urinogenital sinus
and the rectum, the proctodaeum surrounding the original common orifice essentially disappears as such (Fig. 337). Thus the orifice of the
urinogenital sinus (the ostium. urogenitale), the edge of the urorectal
fold (the rudiment of the perineum) and the anus are brought virtually
to the surface in this region. Just anterior to the ostium urogenitale
there meanwhile appears a slight elevation known as the genital eminence, which shortly becomes more prominent, and is then called the
genital tubercle. Immediately on either side of this tubercle lie a pair
of folds called the genital folds. These folds lie not only at the sides of
the tubercle, but also extend caudad enough to flank the ostium urogenitale causing the latter to become slit-like. Somewhat further to ei~
ther side of the genital folds are another pair of elevations, the genital
swellings (Fig. 340, A, B).
The External Genitalia, Male.—-—The genital tubercle becomes
elongated, and grows forward toform the penis. The genital folds from
654 THE LATER DEVELOPMENT OF THE PIG
either side then grow around the penis to form the prepuce, while more
posteriorly and to the sides the genital swellings are pushed out by the
coelomic evaginations to form the coverings of the scrotal sacs. These
presently fuse in the mid-line to produce the single scrotum, the line of
fusion constituting a ridge called the scrotal raphe. Up to this point it
will be noted that the penis lacks a canal. This is formed by a groove
developing along its ventral side, the edges of which soon fuse, and thus
is formed the penile urethra, extending from the tip of the penis to the
urinogenital sinus. The part of this sinus between this point and the bladder then comprises the prostatic urethra. The line of fusion of the edges
of the ostium urogenitale and those of the groove along the ventral or
caudal side of the penis forms an extension of the scrotal raphe called
the penile raphe (Fig. 340, C, E, G).
The External Genitalia, Female. — The situation in the female is
considerably simpler. Starting from the same structures in the indifferent stage we find the tubercle forming a vestigial part; at the anterior
border of the ostium urogenitale. It is called the clitoris, and is obviously the homologue of the male penis. The urinogenital sinus itself becomes the vestibule which leads into the vagina formed from the fused
ends of the uteri. Upon either side the ostium urogenitale of the vestibule is flanked by the genital folds which have become the labia minora,
and slightly more laterally by the genital swellings which have become
the labia majora. The former are of course the homologues of the male
prepuce and the latter of the scrotal sac coverings. The term vulva includes all the parts just mentioned (Fig. 340, D, F, [17 ).
’l7
HE SKELETON, TEETH, HAIR, HOOFS AND HORNS
THE SKELETON
I T is not the intention to undertake for the Pig, anymore than we
have done for previous forms, a detailed description of skeletal development. It does seem worthwhile, however, to point out a few of the outstanding similarities and differences in this development as it occurs in
this animal and in the Frog and Chick.
The Skull. —As in the case of the Frog and Chick the bones of the
Pig skeleton may be divided into membrane or dermal bones and cartilaginous bones. On this basis we find in the cranial part of the skull
of this animal the same embryonic cartilaginous foundation which we
have previously noted, i.e., the basilar plate (fused parachordals and
notochord) and the trabeculae. Later of course these develop ossification centers giving rise to the ethmoid and certain of the sphenoid bones.
Also added to the cranium from cartilage are the occipitals and the
various bones forming the otic and nasal capsules such respectively as
the periotics and the naso-turbinals. It will be recalled, however, that
the primitive cartilaginous element of the upper jaw, the palato quadrate, still represented in the Bird by the quadrate, has in the Mammal
apparently moved into the middle car as the incus. Likewise in the
lower jaw a portion of Meckel’s cartilage, in the Mammal is thought to
constitute the malleus. All the dermal bones, i.e., those ossifying directly from membrane which occurred in the Bird, exist also in the Pig,
with the exception of the quadrato-jugals and parasphenoids. In the
lower jaw dermal elements replacing the main remnants of Meckel’s
cartilage become ossified and fused together to form the single mandible.
The Vertebrae, Ribs and Sternum.——The concentrations of
mesenchyme which are to form the vertebrae alternate with the original
_ somites just as they did in the Frog and Chick, and surround the noto
chord. Cartilage forming centers then develop, one about the remains
of the notochord, i.e., the future centrum, one in each neural arch and
one in each costal process. The cartilage soon spreads from these centers to form a continuous cartilaginous structure for each future vertebra. Then ossification begins in the same centers ivhere cartilage forma656 OTHER MAMMALIAN STRUCTURES
tion began, and spreads until each vertebra consists entirely of bone.
The rib cartilage is at first continuous with that of the costal processes,
but when ossification begins, the cartilage of the ribs becomes separated from that of the vertebrae, and each rib has its own ossification
center. It is of interest that in correlation with the adult condition the
cartilage in each rib of the Pig consists of a single piece, instead of two
as in some. of the ribs of the Bird. Although the cartilage of each rib is
in this case in a single piece, this cartilage ultimately contains more
than one ossification center. Thus the ribs in the Pig and other Mammals are like the long bones of the appendages in this class, in that the
ends ossify separately from the shafts, forming the so-called epiphyses.
As in the Bird the sternum has two cartilage centers attached to the rib
cartilage on either side. Later these fuse in the median line.
The Appendicular Skeleton.———Considering the fore limbs first,
we find the Pig shoulder girdle differing from that of the Bird in lacking both clavicle and coracoid. The only member of the girdle bones it
does possess is the scapula, and this of course is a bone ossified from
cartilage.
As regards the long bones of the fore limb (humerus, radius and
ulna) we find that in the Mammal the method of ossification in all such
bones differs somewhat from that in either the Frog or the Chick. Development begins as usual by the differentiation of cartilage from membrane. Around the middle (diaphyseal region) of this cartilaginous core
the former perichondrium, now periosteum, starts to erode the cartilage
and to deposit a band of bone. Sincethis band is soon thicker at its middie than at its ends, the remaining central cartilage presently becomes
hour-glass shaped. Almost simultaneous with this outer deposit by the
periosteum, the cartilage in the middle of the diaphyseal core also begins to be eroded by invading chondrioblasts, and its place is taken by
bone deposited by osteoblasts. Soon this endochondral bone and that
produced peripherally by the periosteum meet, and the diaphysis is entirely ossified. This bone, however, is all cancellous, and within it three
changes occur. First, in the central axis of the diaphysis or shaft the
bone is shortly removed and replaced by marrow. Second, about the
periphery the original cancellous bone of both central and periosteal
origin is also constantly removed and replaced as the diaphysis grows in
diameter. Finally, as growth is completed the inner cancellous bone remaining at that time is remade by processes previously described, into
compact Haversian systems. Likewise the outer cancellous periosteal
bone is replaced by layers of compact periosteal bone. On the basis of
THE SKELETON V 657
thisdescription it might be questioned whether any of the ultimate diaphyseal bone is really endochondral, and it would appear probable
that at least what occurs near the mid-region of the diaphysis is not.
Nearer the ends, however, the case is different, and for the same reason
that this was true in the Chick, i.e., because of the method of longitudinal growth. This method, though fundamentally similar to that in
the Bird, differs in certain significant details, and is as follows:
While the processes described above are occurring toward the midregion of the diaphysis each cartilaginous epiphysis is also undergoing
ossification in one and sometimes two centers. In this manner there is
presently produced in it a single disc of cancellous endochondral bone.
At either end of the diaphysis, however, between the bone earlier formed
in that location and the respective epiphyseal bony disc, there persists
during growth a plate of cartilage known as the epiphyseal plate. These
plates correspond in function to the cartilaginous ends of the growing
bones of the Chick, i.e., they continue to produce cartilage distally and
endochondral bone proximally on the side of each adjacent to the marrow cavity of the diaphysis. Finally, when growth ceases, the epiphyseal
plate becomes entirely ossified, and thus joins the already formed bony
epiphyses to the ends of the diaphysis. Hence it comes about that, as in
the Bird, all of every epiphysis is endochondral. Also somewhat more
of the mammalian diaphysis is endochondral because not so much of its
interior is ultimately removed as is true in the Bird. For further de
tails of bone histogenesis the reader is referred to the account of this
process under the Frog, and to the accompanying figures. .
The behavior of the digits has already been referred to in the Pig
and we have noted that, as in the Bird, five digits are present in mem
brane. In the Pig, of course, the third and fourth are well developed
while the first disappears and the second and fifth remain vestigial. The
ossification of the znetacarpals and phalanges occurs in these cases from
cartilage in the same manner as in other mammalian long bones.
Posteriorly the pelvic girdle is ossified from three cartilages representing the ilium, ischium and pubis. As in the Bird they extend respectively
anteriorly, posteriorly'and antero-ventrally. In the Pig, however, the
antero-ventrally extending pubic cartilages remain in this position, instead of rotating caudad to lie parallel with the ischia, as in the Chick.
Thus when ossification occurs the pubic bones meet one another in the
median ventral line, and are held firmly together by ligaments in the
manner characteristic of Mammals. The long bones of the Pig hind
limb are ossified in the same way as the long bones of the fore limb,
658 OTHER MAMMALIAN STRUCTURES
and consist of course of the femur, tibia and fibula. The four digits, two
vestigial, are also formed as in the anterior appendages.
THE TEETH
As previously noted, although the Frog does develop teeth, they are
small and late in forming so that nothing was said about them, while
modern Birds have no teeth at all. It therefore seemed best to postpone
stellate cells of dental papilla ameloblascs
4 enamel epithelium ofenamel organ
A.-. ,5. ‘ pp . _.‘
   
 
tcmmnn
odontoblast Tomes’ processes
dentine enamel pulp of enamel organ
Fig. 341.——A sagittal section through a developing tooth, showing
the cells responsible for the secretion of enamel and dentine, and
the relations of these cells to those products.
an account of the origin of these structures until we came to the Mammal in which class they attain their fullest development. We shall not
attempt to describe the development of any particular tooth since what
is true for one is true for all in forms like the Pig or Man, save for variations in shape. '
The Enamel Organs.———As has been previously indicated, at 30
mm. or shortly thereafter the originally single epithelial thickening
termed the labio-dental ledge, has divided into two parts. The outer
part presently forms the labio-gingival lamina or groove, and the inner
one the dental ledge (Fig. 329). This ledge runs along the surface of an
elevation which represents the gum, and at intervals along it the formation of the teeth occurs as follows: ‘
_ At each point in the gum region where a tooth is to develop, there occurs a special ingrowth from the dental ledge which penetrates further
into the mesenchymé than the non-tooth-forming part of the ledge. The
THE TEETH 659
lower part of this ingrowth is expanded into a double-walled inverted
cup, known as the enamel organ, which remains connected with the
dental ledge for a time by a fairly stout neck (_ Fig. 329). The ledge in
turn is also temporarily connected with the oral epithelium by a considerably narrower neck. The cells on the inner wall of the cup are co
llumnar in shape, and are destined to secrete the enamel of the tooth.
Hence they are called ameloblasts. Those in the outer wall are at first
polyhedral, but soon become flattened, and are known as the epithelium.
of the enamel organ. The rather extensive space between the inner and
outer walls of the cup is filled with a loose reticulate tissue termed the
enamel pulp. Though all enamel organs start out with the relatively
simple cap shape that has been indicated, each later assumes the contours characteristic of the crown of the tooth whose enamel it is to form
(Five. 329, 341) . .
The Dental Papiila. — As the enamel organ pushes into the mesenchyme the latter necessarily comes to occupy the cup which the organ
forms, by which process this mesenchyrne comes to constitute the dental
papilla. Of course where the tooth is to have several cusps and roots the
enamel organ develops more than one cup, and therefore gives rise to
more than one dental papilla and parts subsequently related to it. Presently through multiplication the cells constituting the bulk of a papilla
form a rather dense aggregation. At the same time those at its surface
adjacent to the ameloblasts of the enamel organ. become columnar like
the ameloblasts. These columnar cells of the papilla are then ready for
the secretion of their special product, the dentine, and are termed odontoblasts. It thus presently comes about that while the ameloblasts of the
enamel organ secrete enamel to form the surface of the tooth, the odontoblasts secrete dentine beneath and adjacent to the enamel. As this activity begins to get under way the enamel pulp lying between the outer
epithelium of the enamel organ and its ameloblasts, largely disappears,
thus placing these two layers almost in contact. Probably this is significant in bringing the now active ameloblasts that much closer to their
external blood supply. At the same time nerves and blood vessels penetrate the central tissue of the dental papilla, which gradually becomes
transformed into the pulp cavity of the completed tooth. By the time
these processes are under way, the enamel organ has lost all connection
with the dental ledge. V A 1
Formation of Dentine.~———The formation of the dentine by the
odontoblasts is in some respects similar to the formation of circumferential bone by periosteum. In both cases it involves the deposition of
660 OTHER MAMMALIAN STRUCTURES
calcium salts about organic fibers (ossein fibers). In the case of-the
dentine, however, the product is not laminated, i.e., in layers, but is
continuous. Also no cells are left entrapped within the calcareous substance, and the organic material is less abundant, about 28 percent in
dentine as compared with 45 percent in bone. Hence the dentine is
harder even than compact bone. Otherwise the materials are similar in
that the calcium salts are permeated with ossein fibers, both fibers and
salts being produced by the odontoblasts. Likewise there are processes
of the odontoblasts which extend into the hard matrix just as the living
processes of osteoblasts extend into bone. In this instance, however, the
processes all come from the layer of odontoblasts at the inner surface
of the dentine, since none are embedded within it, and they are known
‘as the fibers of Tomes (shown but not labeled in Fig. 341,) . They are in
general at right angles to the secreted ossein fibers. Obviously the continued production of dentine forces the odontoblasts away from’ the
enamel, and also reduces the size of the original pulp cavity, until it becomes not much more than a canal. This canal continues to contain
blood vessels and nerve fibers in intimate contact with the odontoblast
layer which ultimately becomes inactive and simply lines the pulp
canal. Since these inactive odontoblasts send the living fibers of Tomes~
clear through the dentine, it is easy to understand why this substance is
sensitive when injured by decay or bored into by a‘dental drill.
The Formation of Enamel.-The enamel, as already indicated.
is produced by the ameloblasts of the enamel organ. Because of the relation of these cells to the odontoblasts, moreover, the layer of enamel
will necessarily lie adjacent to, and on the outside of, the dentine, or
rather a part of it. As will shortly appear, and as reference to Figure 329
will show, the enamel organ, and hence the enamel, only covers the future crown of the tooth, not its roots These are covered by other material whose origin will be described presently. In the region of the crown
where the ameloblasts are at work we find that the layer they produce
consists of microscopic prisms of very hard calcium salt crystals called
dahlite. These are held together by small amounts of a different substance called cement. It seems to be clear that each prism of the enamel
is produced by a single ameloblast, and therefore extends all the way
from one side of the layer to the other. Since the prisms are not straight,
or precisely parallel to one another, however, this is difficult to demonstrate in section. Organic matter is present, but in even smaller amounts
than in the dentine, about 5 percent of the total substance being so constituted. It apparenlly consists mainly of fine protoplasmic processes
THE TEETH 661
from the ameloblasts which are often called the processes of Tomes
(Fig. 341). They evidently correspond to the similarly named processes or fibers put out into the dentine by the odontoblasts. Finally it is
obvious that as the tooth grows outward due to the formation of more
dentine underneath, the crown will presently be forced through the surface of the gum with the concomitant destruction of the enamel organ.
When this has occurred it is evident that no more enamel can ever be
formed, and that what has formed will extend only to the gum line.
Hence if this hard covering of the exposed surface is later destroyed in
any way it is gone forever. Dentine, on the other hand can be, and
often is, added to from within, if in later life some of it is removed, as
is the case when a tooth is filled. From what has just been said it also
follows that unlike the processes of Tomes in the dentine, those of the
enamel must disappear when the ameloblasts cease to exist.
The Formation of Cementum.— It has already been noted that
only the crown of the tooth is covered by enamel, and that a different
material covers the dentine of the root. This material is called cementum, and is produced by the mesenchyme which surrounds the entire
tooth and enamel organ previous to eruption. This rnesenchyme is said
to constitute the dental sac (Fig. 329). It is only in the neighborhood
of the root, however, that the tissue of the sac produces cementum. Here
its cells behave almost exactly like the osteoblasts of any periosteum,
and the cementum with which they cover the root is essentially the same
as periosteal bone. Indeed on its outer side where the cells of the sac
are in contact with the jaw bone instead of the teeth, they do in fact add
to that bone in the manner of any periosteum. As will be recalled ossein
fibers are produced by the cells of such periosteum, and such is the case
here, both on the side of the jaw bone, and on that of the cementum. It
thus comes about that these fibers actually extend out of the cementum
right into the bone of the jaw. In this manner therefore the tooth is very
firmly anchored in its socket.
The Permanent Teeth. —- Thus far no mention has been made of
more than one type of dentition. As everyone is aware, however, the
first set of so-called milk teeth is later replaced by the permanent teeth.
This process, however, need not detain us long. The enamel organ for
each second or permanent looth arises from the dental ledge near that
of the milk tooth. When the ledge disappears, the organ in question lies
in a depression of the alveolar socket on the lingual side of the growing
milk tooth, but develops no further at this time. Later this “tooth
germ ” goes through the same processes as occurred in the case of the
662 OTHER MAMMALIAN STRUCTURES
milk tooth. Meantime the root of the latter is absorbed, and the crown
is pushed off by the growing permanent tooth beneath it.
Teeth with Open Roots.— It is of some interest to note that in
some animals, notably the Rodents, the incisor teeth continue to grow
throughout life. This is made possible by the persistence of a wide root
canal and the constant addition of more dentine. To compensate for
this the outer end of these teeth is continually worn down by the gnaw
   
dermal (connective
outer mo, Sheath tissue) root ‘sheath
glassy membrane of -_
outer root sheath
' inner root sheath
V ——cortex
hairpapma  ~’ V V  N p ‘_ at 'V;~—-hair matrix
Fig. 342.—Photomicrograph of a mid-sagittal section through a hair
root and papilla under high magnification.
ing activities of these animals. This furthermore is made possible by the
fact that only the front side of the tooth is covered with enamel. The
back side is dentine. Hence since enamel is much harder than dentine
the wear is uneven, which gives the end of the tooth a constantly renewed chisel edge. Of course this process makes a continuance of enamel
formation also necessary on the front surface of the teeth by the perina
nent existence of ameloblasts within the gum in this region, not ‘found
in other cases.
HAIR
Since hair idevelflops long before the Mammal is born, and is one of
the most characteristic features of the class, occurring nowhere else, it
seems appropriate tci refer at least briefly to its development.
THE HAIR 663
As previously noted, hair like feathers is an epidermal structure, and
again it actually consists of cells, not of a secretion by them like teeth.
In this case the cellular character of hair is evident if it is examined
under the microscope. Under these conditions its surface lcuticle) reveals transverse rows of wavy lines, which represent the edges of flat
cells which overlap one another like the shingles of a roof. Beneath this
cuticle are cornified layers of spindle shaped cells and their products,
including pigment, which are termed the cortex (Fig. 3452). In many
types of hair, including that on the human head, the cuticle and the cortex constitute the entire substance of the shaft. In others, e.g., those of
the heard, there is a restricted central region, the medulla, occupied by
a few shrunken cells and numerous air spaces. The latter rfive such hairs
a more silvery appearance when the pigment disappears with age. The
base of each completed hair is contained in a tubular invagination of
the epidermis. This invagination is called the hair follicle, and all of
the parts which lie beneath the surface of the skin together comprise the
root. The walls of this follicle consist oi modified cells of the Malpighian layer of the epidermis, those next to the dermis constituting the
ouzer root sheath, and those next to the hair the inner rooi. sheath. The
latter is itself usually divided into three separate cell layers, but these
need not concern us here. At the base of the root these sheaths merge
into dividing cells which are producing the substance of the hair, and
pushing it upward through the lumen of the follicle. This mass of dividing cells is itself invaginated by an up-pushing bulblike portion of
the dermis containing a blood vessel and known as the hrzir papilla. It
is quite similar to the dermal invagination at the base of a leather called
the feather pulp, and the function in both cases is to nourish the growing structure (Fig. 342).
Again, as in the case of the feather, the hair originates as a downgrowth of the Malpighian layer termed the hair gernz. A small upgrowth
of the dermis invaginates the base or proximal part of this hair germ
and constitutes the beginning of 'the hair papilla. Presently the central
cells of the germ distal to the base become cornifiecl and thus form the
hair. The more peripheral cells of the distal part of the germ soon differentiate into the inner and outer root sheaths of the follicle indicated
above. As growth continues the hair presently comes to extend beyond
the surface of the skin, until much more of it is outside the follicle than
in it. At a point on the follicle near the surface certiain cells of the Malpighian layer constituting the sheaths bu‘d off groups of cells in which
fat droplets accumulate, and which constitute the sebaceous glands (Fig.
, ._.o_...-.......¢.....
l
4
l
l
l
664 OTHER MAMMALIAN STRUCTURES
343) . Just proximal to these there also develop, within the dermis, muscle cells which are attached at one end to the outer root sheath and at the
other to the under surface of the adjacent epidermis. They are called
the erectile muscles of the hair, and serve to ruflle it. This helps to keep
the animal warm, or probably in other cases to frighten its enemies by
making it appear larger, as in the Cat (Fig. 343).
Although not essentially
is of interest to note that all
types of hairs have relatively
fixed periods of life. At the
end of this period the hair is
shed, and its place taken by
a new one. As the time for
shedding approaches the epidermal cells at the base of
the hair shaft and inner root
sheath cease dividing. At the
same time those constituting
the base of the hair become
cornified like those in the
main part of the shaft. The
hair is then detached from the
' papilla, and easily comes out
F18; 343-—‘1,’h°‘°‘_‘1i°1'€’g"‘Pl‘ °f the ?‘‘me of the follicle. Later the new
section of hair as in Fig. 342, taken with a . . . .
lower magnification to show relations to ha” 15 f91'med In the Same fol‘
neighboring hairs and also to a sebaceous 1ic]e_ The papilla which has
gland and erectile muscle. .
shrunken 1S restored, and the
remaining live epidermal cells which cover it start to multiply. The
latter presently give rise to both a new inner sheath and hair shaft in
a manner similar to the original process.
 
:1
NAILS, HOOFS, AND HORNS
It is not feasible to give a discussion of the development of these
structures in a volume of this size and character. However it may be
noted that once more both nails (claws) and hoofs arise as modifications of epidermal cells, involving mainly their cornification. Horns of
one type such as those of the Cow are cornified epidermal sheaths supported by bony cores. The antlers of deer on the other hand are mostly
bone covered by a layer of skin (dermis and epidermis) which soon dies
REFERENCES T0 LITERATURE 665
and is rubbed off. The bony horn itself is shed annually, and renewed
by a remarkably rapid growth of nomcartilaginous bone. The two lastnoted structures are not strictly speaking embryological since they never
appear until after birth. Because of their developmental similarity in
some respects to the other dermal and epidermal appendages, however,
it was thought worth while to mention their origins.
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666 THE MAMMAL
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668 THE MAMMAL
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Schott, R. G.. “Rate of Sperm Travel and Time of Ovulation in Sheep," Anat.
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INDEX
Page numbers in italics indicate a definition or special reference; those in
heavy-face type indicate illustrations.
Abel, S., 459
Abraxas type,
sex chromosomes in, 35
acrosome, M
Adelmann, H. B., 161
adrenals, in Frog, 232, 232, 233; in
Chick, 428. 1:75; in Fig. 644
cortex of, 645
medulla of, 645
air capillaries, 443
air chamber, in Chick egg. 286
air sacs. in Chick, 440, 14/43, 4-44abdominal, 444, 44-4, 445
cervical, 444, 4-4-4interclavicular, 4116, 4-44
intermediate, 4-4-4
alae, in Pig, 609
Albaum, H. G., 194
albuginea, 5, in Chick, 471, /I72
albumen, in Chick, 282, 286, 366
dense, source of, 288, 289
thin, source of, 288, 289
albumen-sac, in Chick, 364, 365, 366
Alden, ll. H., 541
Alexander, L. l5., 354
alimentary tract, in Frog, I62. 163,
200-208; in Chick, 335-338, 371377, 398-401, 2342-609
sources of, 67
allantoic cavity, in Pig, 535
allantoic placenta, in Marsupials, 532,
533, 533
allantoic stalk, in Chick, 364. 364-, 365.
4-4-9; in Pig, 568. 569, 582, 583,
583, 64-5, 64-6, 64-7
allautois. in Chick, 360, 361, 362, 363,
363, 364-, 365, 366, 375, 376. 376,
377. 445, 4-1-8, 4-55, 4-57, 176: in
Mammal, 529; Monotremes. 530.
531, 532, 533; Cat, 538, 539, 5/:0;
Rabbit, 5/I3; Primates, 546. 547,
5/18, 550; Pig, 531-, 535, 536', 536,
537, 54-8, 563, 564-, 574-, 575, 576'
source of blood corpuscles in, in Pig,
586'
Allen, B. M., 6, 174
Allen, E., 4-91
alveoli, 632
Amblystoma, 160, 168, 188, 239
arnelz%asts, in Pig, 658, 659, 660, 661,
ameloblast layer, in Pig, 623
amnio-cardiac vesicles, ‘in Chick, 306.
321, 326, 339, 341; in‘Pig, 558
amnion, in Chick, 359, 359, 360, 361,
364, 365, 380, 476
formation of, 358-361
amnion, in Mammal, Primates, 546,
547, 550; (Man and Apes). 557;
Pig, 535, 562, 563, 564, 569, 571
formation of, in Chick, 358~361; in
Pig, 515, 515, 517
methods I and II compared, 522-525
methods of formation, in Reptiles
(Sauropsids), 523; in Mammals
(I), 51/1, 515, 515, 516, 517, (II),
517, 518, 519, 520, 521
amniota, 357
amniotic cavity, in Chick, 359, 360, 364,
365; in Mammal, Monotremes,
530; Marsupials, 530; Primates,
54-6, 54-7, 548
amniotic fluid, in Chick, 360
amniotic folds, in Chick, 334, 358, 358;
in Pig, 574
anmiotic umbilicus, in Chick, 359
Amphibians, 38, 60, 132, 133, 189, I90,
219, 238, 239
Amphioxus, 75
Amphioxus and Frog,
summary of early development, 144146'
Amprino, B., 4-16
ampulla, in Frog ear, 193,. 194; in
Chick, 389, 422, 422, 423
of gonads, in Frog, 237, 238
anal plate, in Chick, 338, 338, 376,
377, 377, 4-4-8; in Pig, 574, 58!,"
6'64 mmmniota. 357
Anasa lristis, spcrmatogenesis in, 31
Andrews, F. N., 506
674 INDEX
androgamones, 39
animal pole, of egg, 8, 10, 55; in Amphioxus, 79, 80, 82, 84, 85; in
Frog, 109, 110, 117, 123, 125, 129;
in Fish, 262
annulus tympanicus, in Frog, 196, 249
anoestrum, in Mammal, 495, 496, 501
anterior chamber of eye, in Chick,
418, 421
anus, in Frog, 207, 208; in Gymnophimm, 275; in Chick, 31,5, 449; in
Pig, 583, 645, 648, 653
aorta or artery, dorsal or main systemic, in Frog, 21.9, 219; in Teleost,
274; in Chick, 341, 343, 344, 373,
378, 404, 451, 452, 452, 453, 453,
454; in Pig, 536, 569, 576, 578,
587, 590, 591, 593, 594, 595, 635
ventral, in Chick, 342,. 343, 344,
344; in Pig, 569
aortic arch or arches, in Frog, 139,
M2, 216, 217; in Chick, 334, 344,
345, 346, 373, 378, 378, 379, 330,
403, 404, 404, 452, 452, 453, 453,
454, 454, 461; in Pig, 576, 590,
591, 592, 593, 593, 635, 636
alterations in at hatching or birth,
454, 455
reasons for disappearance of left
fourth in Bird, 453, 454, 454
aqueduct of Sylvius, in Frog, 181; in
Chick, 413; in Pig, 612
aqueous humor, in Chick, 421
archenteron, 53, 55; in Frog, 130, 131,
133, 157; in Teleost, 265, 265,
271; in Gymndphiona, 275, 277,
277; in Chick, 302, 302; in Mammal, 510, 512, 513; Pig, 508
area opaca, in Chick, 301, 301, 302,
302
area pellncida, in Chick, 294, 301, 301,
302, 302, 3I8,'322
area vasculosa, in Chick, 317, 322, 345,
346, 347; in Mammals, Marsupials,
531, 532; Pig, 534, 585
area vitelliua externa, in Chick, 317,
318, 322
area vitellina interna, in Chick, 306,
' 318, 318, 322
areolae, in Pig, 536 .
artery or arteries,
allantoic, in Chick, 364, 406, 407
hasilar, in Pig, 569, 592, 593, 594,
5.95
brachiooephalic (innominate), in Pig,
594, 635
carotid, common, in Chick, 404, 452,
453, 454, 457; in Pig, 592, 594,
635, 637; external, in Frog, 219,
219; in Chick, 346, 380, 403, 404,
452, 452, 453, 454, 457, 4-60,
461; in Pig, 592, 593, 594, 595,
635; internal, in Frog, 203, 219,
219; in Chick, 346, 380, 403,
404, 452, 452, 453, 454, 457,
460, 461; in Pig, 593, 594, 595,
635
caudal, in Chick, 378; in Pig, 569,
593
central, of retina, in Pig, 617
coeliac, in Chick, 457 460, 461; in
Pig, 593, 596', 637
hyaloid, in Pig, 617
iliac, in Frog, 220
common, in Pig, 637
external, in Pig, 637
internal, in Pig, 637
intestinal, in Pig, 536
lingual, in Frog, 218, 219
lumbar, in Frog, 220
mammary, in Pig, 636, 637
meseqteric, in Frog, 220; in Chick,
457, 460, 461; in Pig, 593, 596,
637
palatine, in Frog, 218
pharyngeal, in Frog, 218, 220
pulmonary (or pulmo-cutaneous in
Frog), in Frog, 218, 219; in Chick,
404, 404, 451, 451, 452, 453, 456,
457, 460, 461; in Pig, 591, 592,
593, 594, 594, 636', 641
renal, in Chick, 406; in Pig, 596‘,
637, 644
sciatic, in Chick, 404, 406, 407, 457,
461, 463
segmental (or intersegmental), in
Chick, 343, 396; in Pig, 590, 591,
593, 595, 636
spinal, in Pig, 587
subclavian, in Frog, 220; in Chick,
404, 404-, 451, 452, 453, 457, 460,
461; in Pig, 591, 592, 593, 594,
595, 635, 636, 637
umbilical, in Chick, 406, 457, 461,
463; in Pig, 536, 569, 582, 583,
593, 596, 605
vertebral, in Pig, 592, 593, 594, 5.95
vitelline, in Chick, 333, 343, 347, 379.
INDEX
382, 407, 408, 457, 4-63; in Pig,
536, 569, 582, 595
Ascaris, 23 ,
Aschheim-Zondek test for pregnancy,
50.?
Asdell, J. A., 504, 507
Asmundsen, V. S., 239
astrocytes, in Pig, 567
atrio-ventricular aperture, in Frog, 221
atrio-ventricular canal, in Chick, 401,
450; in Pig, 58.9, 641
atrio—ventricular valves, in Chick, 459
(See mitral and tricuspid valves in
Pig)
' atrium or atria, in Frog, 178, 212, 213;
in Chick, 31:1, 31:2, 378, 379, 380,
384, 401, 4-02, 403, 451; in Pig,
536, 569, 578, 587, 588, 588, 640,
641
Atwell, W.‘ J., 174
auditory capsule or vesicle, in Frog,
189, 193, 195, 248, 249, 250; in
Chick, 353, 355, 379, 421, 422, 423,
440; in Pig, 571, 573
auditory organ, in Pig, 6'17
auditory pit, in Chick, 355; in Pig, 564
auditory placode, in Frog, 15.9, 165
aux-icles of heart, in Chick, 1:51; in Pig,
643
auricular-rump axis, in Pig, 563
autonomic ganglia or nerves (See under
nerves)
axes, of Frog egg, 115
axial filament, of sperm, 12
Axolotl, 189; gastrulation in, 137, 139;
maturation of germ cells in, 18, 19
Bacon, R. L., 168
Baker, B. L., 503 *
Bakst, H., 460
balancers, in Amblystoma, 161
Ballard, W. W., 133 ’
Bandicoot (See Perameles)
‘Bang, A., 343
barbs, in Chick feathers, 436
Barclay, A. E., 458
Barcroft, J., 458
Barron, D. H., 458
Bartelmez, G. W., 323
Barth, L. G., 141, 143
basicranial fontanelle, in Frog, 250
basil or basilar plate, in Frog, 248; in
Chick, 4/40; in Pig, 618, 655
Bat, 508
675
Bautzmann, H., 139
Becker, R. F., 458
Beckwith, C. J ., 190
Bidder’s organ, in Frog, 238
bile duct, in Frog, 206'; in Chick, 374,
374, 445; in Pig, 569, 580 (See also
ductus choledochus)
Birds, sex determination in, 38
bladder, urinary, in Pig, 604
Blandau, R. J ., 507, 508
blastema cells, mesonephric, in Frog,
233
blastocoel or segmentation cavity, 53,
55, 55; in Amphioxus, 88; in Frog,
124, 124-, 125, I30, 131, 132, 133;
in T eleost, 263, 264; in Chick, 294,
295, 296, 297; in Mammal, Primates, 5-’I8, 548, 549, 549; Pig,
508, 575
blastocyst, in Mammal, 509, 510, 510,
521; Ungulates, 534; Carnivores,
539; Primates, 5/18, 548, 549, 549,
553. 556; early Human, 552, 553;
Pig, 535, 535 (See also blastodermic vesicle)
distribution in horns of uterus, Pig,
537
blastoderm, 53; in Teleost, 263; in
Chick, 286, 294, 298, 306; in Mam—
mal, 510; Primates, 548, 549; Pig,
522, 524, 525
homologies of margin, in Chick, 303,
318, 31.9
potentialities, in Chick, 312, 313
blastodermic vesicle, in Pig, 509, 510,
511, 535, 535
blastodisc, 10, -53; in Teleosts, 262, 263
blastoporal lip, 55, 55; in Amphioxus,
88, 8.9, 90; in Frog, 127, 128, 129,
130, 131, 132, 133, 134; in Teleost,
265, 265, 266, 266, 267, 268, 268:
in Gymnophiona, 274», 275
homologies of, in Chick, 298,299,
303, 314, 318, 319
blastopore, 55, 55; in Amphioxus, 88,
89, 90; in Frog, 129, 130, 131, 152;
in Teleosts, 266, 267; in Gymnaphiona, 273; in Chick, 314, 318; in
Mammal, 513, 526, 527 "
blastula, 53; in flzkmphioxus, 87; in Frog,
117, 124, 124, 132; in Teleost, 263;
in Chick, 298
blood corpuscles, source of, in Frog,
216; in Chick, 316, 340; in Pig, 586
6%
blood islands, in Frog, 216; in Chick,
305, 306, 307, 316, 322; in Pig,
585
blood system, source of, 67
blood vessels, of bone in Frog, 246, 252;
placental in Man, 554, 555; of villi
in Pig, 586
“blue babies,” cause of, 458
body cavities, in Chick, 465, 466; in
Pig, 633, 634
body shape, in Chick, fifth day, 433
bone,
cancellous, in Frog, 241, 244, 245; in
Chick, 439, 440; in Pig, 657
compact, in Frog, 242, 245
dermal, in Frog, 250, 251
endochondral or cartilage, in Frog,
244, 245; in Chick, 439, 439, 440,
441; in Pig, 655, 656, 657
histogenesis, in Frog, 240-246. 252,
253, 254; in Chick, 439, 440; in
Pig, 656, 657
lamella, 245, 246, 252
membrane or membranous, in Frog,
245, 246; in Chick, 439, 441; in
Pig, 655
periosteal, 245, 245, 246, 252; in
Chick, 439, 439; in Pig, 656
skull (See skull)
trabeculae of mandible, in Pig, 623
bones, of limbs, in Frog, 252, 253. 254;
in Chick, 438, -439, 440; in Pig,
657, 658
bony-labyrinth, in Chick, 423; in Pig,
619
Bowman’s capsule, in Frog, 232; in
Chick, 390; in Pig, 604, 644
Brachet, A., 59, 109, 133
brain,
development and divisions of, in,
Frog, 156, 157, 158,176, 177, 177,
178, 17.9, 180; in Chick, 348-351,
348, 349, 383, 384, 384, 409-413,
410, 411, 412; in Pig, 566, 567,
610-613, 610
lobes of, in Pig, 610
branchial or gill,
arch, in Frog, 150, 153, 163, 164,201,
201, 217, 218, 219
chamber, in Frog, 1752, 202, 203
circulation, in Frog, 202, 216, 217
cleft or clefts, in Frog, 150, 151, 160,
169, 170, 201 ,.
plate, in Frog, 148, 150, 151
:
INDEX‘
pouches, 160, 162, 201, 201, 202, 204,
205, 205
takers, in Frog, 203, 204
breeding season, in Mammals, 496
Bremer, J. L., 453
Brewer, J. l., 552
Brizee, K. 11, 387
broad ligament (mesovarium), in Pig,
647, 648, 653
bronchial tubes, in Pig, 632
bronchus or bronchi, in Chick, 373,
443; in Pig, 577, 57.9, 632
primary, secondary, and tertiary, in
Chick, 4-I-3. 44-3, 4-4-4recurrent. in Chick, 444, 445
Bruner, J. A., 239
Bueker, E. D., 386
bulbo—conus (arteriosusl, in Pig, 536,
587
bulbo-urethral gland, in Pig, 645, 64-6,
648
bulbus arteriosus, in Frog, 212. 214; in
Chick, 341, 342. 342, 346, 378, 379,
380, 384, 401, 402, L30, 4-51
Burmester, B. N., 289
Burns, R. K., 239
bursa Fabricii, in Chick, 448, 44.9, 449
Bryce-Teacher, blastocyst, 552
caecum, intestinal, in Pig, 581, 627, 629
Cairns, J. M., 436
Calkins, G. N., 48
Cameron, J. A., 216
canals, of Gfirtner, in Pig, 649, 653
Carnivores,
allantois in, 538, 540
implantation in, 540
Placenta in, 540
pro-oestrurn in, 537
yolk-sac in, 537, 538, 538
carotid gland, in Frog, 204, 205, 205
carotid loop, in Chick, 334, 343
cartilage,
arytenoid, in Pig, 624
basal, or basilarplate, in Frog, 248;
in Chick, 440; in Pig, 655
basibranchial, in Frog, 250
basihyal, in Frog. 250
basioccipital, in Chick, 441
ceratohyal, in Frog, 251, 253
cricoid, in Pig, 624
diaphysial, in Chick, 439
epiphysial, in Frog, 243; in Chick, 43
exoccipitals, in Chick, 441
INDEX 577
hypobranchials, in Frog, 250, 251
in bone-making, 243, 243, 244
mandibular, in Pig, 621
matrix, in Frog, 244
Meckel’s, in Frog, 248, 251; in Chick,
441; in Pig, 655
mesotic, in Frog, 248, 250
nasal,~in Pig, 621
occipital, in Frog, 250
olfactory, 249
palato—quadrate, in Frog, 203, 248,
24-9, 251; in Chick, 441
parachordals (or parachordal plate),
in Frog, 248, 248; in Chick, 440;
in Pig, 655
thyroid, in Pig, 6'24
trabecular, in Frog, 203, 248, 250; in
Chick, 440; in Pig, 6'55
vertebral, in Frog, 247, 247
caruncles, in Mammals, Ungulates, 536
Cat,
allantois in, 538, 540
amnion in, 538
egg of, 505
ovulation in, 493
parturition stimulus in, 504
placenta in, 538, 540, 593
sexual cycle in, 496
yolk—sac in, 538
caudal flexure, in Chick, 370, 395; in
Pig, 562, 566
caudal knob, in T eleost, 269
caval fold, in Chick, 406'
cell layer, of Langhaus, in Mammals,
Man and Apes, 554, 555, 556
cells,
central, in Chick blastoderm, 294,
295, 296'
chromaffin, in Chick, 475; in Pig, 645
marginal, in Chick blastoderm, 294-,
295, 296
of Rauber, in Mammals, Rabbit,
_ 514; Pig, 516
cement, of tooth, 651
cementum, of tooth, 6'60
central body, 10
oentriole, 11, 12
cent;-ooome, 11, 12, 17; in Frog egg,
108; in Chick egg; 285
centrum, in Frog, 247, 247; in Chick,
437; in Pig, 655
cerebellum, in Frog, 181; in Chick, 412,
413; in Pig. 610, 613
cerebral suture, anterior, in Chick, 328
Cerebratulus, loss of chromatin in, 27
cerebrum or cerebral hemispheres, in
Frog, 177; in Chick, 350, 409, 410,
411, 4-12, 413; in Pig, 6:10, 610, 611
Cerfontaine, P., 75
cervical flexure, in Chick, 333, 333, 334,
370, 379, 395, 409, 433; in Pig, '‘
562, 566
cervical sinus, in Pig, 563, 565
cervix, in Pig, 649
chalazae, in Chick, 236
source of, in Chick, 238, 289, 290
chalaziferous membrane, in Chick, 286
source of, in Chick, 286, 288, 290
Chang, C. Y., 239
Chen, B. K.., 300 chiasma (chiasmatypy), 20, 23, 24
chondrin, 243, 244
chrondrioblasts, 244
chordae tendineae, in Pig, 641, 642
chorio-allantoic membrane‘, in Chick,
364
chorion (false amnion), in Chick, 360,
361, 364, 364, 365, 366, 380; in
Mammal, 513, 517; Monotremes,
530; Cat, 539; Man and Apes, 546,
547, 554, 555, 556, 556; Pig, 537,
563, 564 '
frondosum, in Mammal, Man and
Apes, 557, 559
laeve, in Mammal, Man and Apes,
557, 559
chorionic trophoblast, in Mammal, Pig,
535, 574, 575 (See also trophoblast)
choriouic villi, in Mammal; Cat, 539,
540; Man and Apes, 546, 547, 554,
555, 556, 557
choroid coat, in Frog, 192; in Chick,
418, 419
choroid fissure, in Frog, 190, 190, 191,
192; in Chick, 353, 354, 380, 419,
419, 435
choroid knot, 192
choroid plexus,
anterior, in Frog, 178, 179, 180; in
Chick, 411, 412; in Pig, 612
posterior, in Frog, 178, 181; in Chick,
4-12, 413; in Pig, 613
chromafiin cells (See cells) "
chromatid, 18:24, 37
chromatin, 16, 24, 27
loss in egg, 26, 27
nucleolus in, in Chick egg, 285; in
Frog, 159
r.~.;.-x.,.,A.«.-.v~,w-nae:-an-,«.u:.n>xaivs;:.taau9vgu‘. - ‘ 2 _  _-'.-*-';1 ~ “' ' -'3“  " "  i‘  _
678
chromonema, 16-21, 24, 25, 27, 28, 37;
in Frog, 109
chromosomes, 16-38; in Frog, 108, 109;
in Chick, 285
cicatrices, in Amphioxus, 79; in Chick,
282, 287
ciliary processes, in Chick, 418, 418
circle of Willis, in Pig. 594, 595
circulation,
embryonic, in Chick, 457; in Mammal, 457 _ extra-embryonic, 346, 347
circulatory changes at birth or hatching, 454-460; in Cat, 458
circulatory system, in Frog, 167-168,
210-225; in Chick, 339~347, 377382, 401-408, 450-465 ; in Pig,
585-603, 634-642
Clark, S. L., 459
clavicle, in Frog, 254; in Chick, 438
claw, in Chick, 436
cleavage (or segmentation) (See also
segmentation)
Clements, L. P., 632
clitoris, in Pig, 645, 647, 652, 654
cloaca, in Frog, 105, 208; in Chick,
282, 283, 368, 376, 391, 400, 427,
448, 448, 449, 449, 467; in Pig,
568, 569, 583, 583, 645, 647
cloacal membrane, in Chick, 368, 448,
44.9, 449; in Pig, 583 (See also anal
plate) a
club-shaped gland, in Amphioxus, 9
clutch of eggs, in Chick, 291 , 292,
coelom, 6'3, 64; in Amphioxus, .96, 98;
in Frog, 164, 165, 210; in Teleost,
274; in Chick, 322, 326’, 329; in
Mammal, 528; Pig, 569, 575, 578,
579, 633, 634
extra-embryonic, in Mammal, 516,
517; Man, 552
pericardial, in Pig, 569
coelomic space, in Pig, 528
Cole, H. K., 289
collecting ducts or tubules, in Chick,
390, 427, 474; in Pig, 644
colliculi,
inferior, in Pig, 612
'superior. in Pig, 612
colon, in Pig, 627, 629 «,
ascending, in Pig, 629
descending, in Pig, 629
columella, in Frog, 196; in,Chick, 424;
in Pig, 619
INDEX
commissure, in Frog, 180
anterior, in Chick, 383, 411, 412
habenular, in Chick, 412
infundibular, in Chick, 412
pallial, in Chick, 412
posterior, in Chick, 411, 412
spinal, in Chick, 412
trochlearis, in Chick, 411
common trunk, of pronephros, in Frog,
226
competence, in induction, in Frog, 141
conchae, in Pig, 616
concrescence,
in gastrulation, 61, 61
or convergence, in Teleost, 267
confused or diffuse stage, in meiosis, 23
Congdon, E. D., 453
conjugation, in Protozoa, 48
Conklin, E. G., 75
Conrad, R. M., 289
contraction stage, in meiosis, 17, 18
convergence, 61, 62; in Amphioxus, 90;
in Telecst, 269; in Frog, 127, 128,
134; in Chick, 305, 306
Copenhaver, W. M., 168, 215, 216
coprodaeum, in Chick, 448, 448, 449,
449
copula, in Frog, 251
copulation path of sperm, 44, 46; in
Frog, 114, 115, 116
copulation plane, in Frog, 115
coracoid, in Chick, 438
cords of Pfliiger, in Mammal, 490
cornea, in Frog, 192; in Chick, 418, 421
Corner, G. W., 498, 499, 504
Cornman, 1., 113
cornu, greater and lesser (See hyoid)
corona radiata, in Mammalian follicle,
490, 492, 492
coronary sinus, in Pig, 640
corpora quad:-igemina, in Pig, 567,
610. 612
corpora striata, in Chick, 409, 411
corpus lutcum, in Mammal, 494, 495,
495, 496, 497, 499,‘ 500, 502
cortex,
of gonad, in Chick, 468
of hair, in Pig, 663
cortical substance of adrenal, in Frog,
232, 233; in Chick, 428, 475
costal process, in Chick (see transverse); in Pig, 655, 656
cotyledons, ‘in Mammal; Ungulates
(Cow), 536
INDEX 579
Cow,
implantation in, 536, 537
placental villi in, 502, 534, 536
pro—oestral bleeding in, 496
Cowper's glands, in Mammal, 488
cranial flexure, in Chick, 322, 333, 349,
370, 379, 395, 409; in Pig, 562,
566'
cranial ganglia and nerves, in Frog,
182-187 ; in Chick, 352, 353, 415,
416 (See also ganglia and nerves)
cranium, in Chick, 440-441; in Pig, 655
crop, in Chick, 446'
crossovers, genetic, 21
mechanisms of, 37, 38
crown, of tooth, 6'60, 661, 662
crown rump axis, in Pig, 563
crura cerebri; in Frog, 181; in Chick,
413; in Pig, 6'12
cumulus oiiphorus, in Mammal, 492
cushion septa, in Chick, 4.02, 403, 450,
451; in Pig, 589, 641
cuticle, in hair, 663
cutis layer, in Amphioxus, 100
cutis plate (See dermatomel
cystic duct, in Chick (ductus cysticus),
447; in Pig, 580, 580, 630
cytoplasm, of egg, 10
dahlite, in tooth, 660
Danchakofl‘, V., 340Dasyurus,
allantois in, 530, 532'
implantation in, 532
yolk-sac in, 530, 532
yolk-sac placenta in, 530, 532
decidua, in Mammal; Man, Apes, 559
basalis (serotina), in Mammal; Man
and Apes, 552, 554-, 555, 557, 559
capsularis (reilexa), in Mammal; 552,
557, 55.9
compacta, in Mammal; Cat, 539:
Man and Apes, 558
spongiosa, in Mammal; Cat, 539;
Man and Apes,'558
vera, in Mammals; Man and Apes,
557, 559
delamination,
gastrulation by, 58, 59; in Frog, 133;
in Chick, 303; in Mammal, 510
mesoderm separation by, 65, 66; in
Frog, 134
dental lamina or ledge, in Pig, 624, 658,
661
dentgggapilla (pulp). in Pix. 623, 658,
dental sac, in Pig, 623, 651
dentine, in Pig, 623, 658, 659, 6'60, 661,
662
dermatome (cutis plate), 64, 69; in
Amphioxus, 99, 100; in Frog, 166',
166; in Chick, 329, 335, 371, 396,
397; in Pig, 585
dermis, in Frog, 209; in Chick, 371, 436;
in Pig, 585
Detwiler, S. 11., 209, 386
developmental concepts, 143, 144
diakinesis, in meiosis, 20, 23, 24, 37
diaphragm, in Pig, 573, 633, 633, 634
diaphragmatic ligament, in Pig, 646,
650, 651
diaphysis, in Frog, 243, 252, 253, 254;
in Chick, 439, 440; in Pig, 656, 657
Didelphys (See Opossum)
d.iencep_halon, in Frog, 179, 180; in
" Chick, 333, 334, 349, 350, 380, 383,
384, 410; in Pig, 566', 568, 610, 611,
612
digestive system, in Pig, 573-584. 622632 (See also alimentary tract)
digits, in Chick, 439', in Pig, 6'06, 607,
657
dioestrum, 494, 495, 497, 498, 502
diploid, in meiosis, 17
diplotene, 18-21, 18, 21, 23, 27, 30
Discoglossus, gastrulation in, 137, 139
discus proligerus, in Mammalian follicle, 490, 491
Dog,
allantois in, 538
amniotic cavity in, 538
egg of, 492, 510
mesometrium in, 538
placenta in, pro-oestral bleeding in,
496
sex cycle in, 495, 496, 501
dorsal flexure, in Pig, 562
dorsal thickening of brain, in Frog, 157
Drosophila, 24, 35, 36
ductus Botalli, or arteriosus, in Frog,
219; in Chick, 404, 404, 452, 453,
453, 456, 457, 459, 460; in Pig, 6'36,
643 "
ductus choledochus, in Chick, 375, 447;
in Pig, 630, 631
ductus cochlearis, or cochlear duct, in
Chick, 422, 422; in Pig, 618, 618,
619
680 ‘ INDEX
ductus Cuvieri, in Frog, 218, 220, 221,
221; in Chick, 333, 334, 345, 34-6,
378, 379, 38.1, 381, 405, 408, 463;
in Pig, 589, 596, 597, 598, 599,
6'38, 639
ductus reuniens, in Pig, 618, 618
ductus venosus, in Chick, 3115, 346, 347,
381, 405, /106', 4-08, 457, 465; in Pig,
569, 579, 596, 600, 602, 638
Dudley, J., 336
duodenal-jejunal flexure, in Chick, 445,
4/47
duodenum, in Frog, 206; in Chick, 399,
445, 445, /:46, 447; in Pig, 580, 627,
629
Du Shane, G P., 209
dyads, in Ascaris, 23
car,
external, in Pig, 607, 608, 621
homologies of bones in, in Pig, 620,
622
inner, in Frog, 1.92, 193, 194; in
Chick, 1:21, 422, 422, 423; in Pig,
573, 617, 618, 619 (See also auditory vesicle)
middle, in Frog, 1.95, 196'; in Chick,
4-23, 4211; in Pig, 618, 619, 620
origins of, 67
Eastlick, H. L., 386
Echidna, 531
ectobronchus, in Chick, 444
ectoderm, 53; in Amphioxus, 88, 92;
in Frog, 134; in Teleost, 270, 270;
in Gymnophiona, 277; in Chick,
302, 306, 307, 308, 30.9, 309; in
Mammal, 516, 517; Pig, 527, 528
movements during gastrulation, in
Amphibia, 136', 137, 137, 138, 138,
139
products of, 67
Edwards-Jones-Brewer blastocyst, in
Mammal, 549, 552
egg (or ovum), 8, 9, 10; in Frog, 106'120; in Fish, 262, 263; in Chick,
281-290; in Mammal, /I89-/493
cylinder, 51:0
cytoplasm, reaction to fertilization,
r 40-43, 41, 42
fertilized, in Amphioxus, 79, 79
influence compared with that of
sperm on early development, 49
meiosis of, 21, 27, 27, 23, 30, 44, 4-5;
in Amphioxus, 77, 78 '
numbers spawned, in Frog, I12
symmetry and orientation, in Amphioxus, 79, 80, 81, 82, 83 (See also
embryonic)
tooth, in Chick, /J76
ejaculatory duct, in Pig, 646, 6/48
Elephant, retention of testes in, 488,
651
embryology,
nature of, 2
relation to genetics, 49
embryonic axis, determination of, in
Chick, 320. 321, 322
embryonic knob, in Mammal, 513, 52.3:
Rabbit, 514; Pig, 515, 515; Hedgehog, 517, 518; Guinea Pig, 518,
519; Mouse, 520, 521; Primates,
548
embryonic shield, in Teleost, 268; in
Chick, 301
embryonic symmetry, in Ampl1i0.\'us
(See under egg), in Frog, 115, 119,
120, 121, 122
enamel, in Mammal, 623, 658, 659, 661,
662
formation, in Mammal, 660
organ, in Mammal, 623, 658, 658,
65.9, 660, 661
pulp, in Mammal, 623, 658, 659
end knob, in sperm, 13
end piece, in sperm, 12
endocardial cushion, or cushion septum, in Chick, 339, 402, 403; in
Pig, 578, 589, 589, 641
endocardium, or endothelial lining, in
Frog, 168, 189, 210, 211; in Chick.
339, 340, 341, 402, 403; in Pig, 586',
588
endochondral bone, 243-244
endocrine glands, effect of on laying, in
Chick, 2.91
endoderm, 5.3’; in Amphioxus, 88, 92:
in Frog, 131, 134; in Teleost, 270
270, 271; in Gymnophiona, 277:
in Chick, 302, 306, 307, 308, 30.9.
309, 315, 316, 322; in Mammal.
517; Pig, 521, 527, 528; Primates,
548, 549, 549
movements during gastrulation m
Amphibia, 136', 137, 137, 138, 138
products of, 67
endolymphatic duct, in l*‘.rog, 193, 194;
in Chick, 389, 389, 421, 422, 423;
in Pig, 573, 617, 618
INDEX
endolymphatic outgrowth, in Anura,
19-’:
endolymphatic sac (saccus endolym~
phaticus), in Chick, 421, 422
endometrium, in Mammal, /18.9, 4-94,
500; in Ungulates, 535, 537
endomixis, 48
endoplasm, of egg, in Amphioxus, 77
endostcum, in Frog, 2142
enterocool, in Amphioxus, 92
enteroa.-oelic method of mesoderm
formation, 63, 64enterocoelic pouches, in Amphioxus, 98
enteron, in Frog, 162, 163
entohronchus, in Chick, 4-44
entrance cone, 41, 41
entrance path of sperm, 44, 46; in Frog
egg, 111, 114, 115
entrance-path plane, in Frog egg, 115
entypy, in Mammal, 517
epenrlymal cells, in Frog, 181, 182; in
Chick, 351, 38/4; in Pig, 567, 570,
613, 614epiblast. 5-1-; in Amphioxus, 88, 89; in
Frog, 132, 13-1-; in Teleost, 265,
265; in Gymnophiona, 273; in
Chick, 302, 305, 308, 309; in Mam~
mal, 510; Pig, 515, 515
epiboly, in gastrulation, 60. 60: in Amphioxus, 90; in Frog, 127, 131. 13-1',
in Teleost, 277: in Gynmophiona,
277: in Chick, 318, 319, 361
epicardium, in Pig, 508, 510, 512, 588
epidermis, in Amphioxus, 99', in Frog,
125; in Chick, 396
source of, 67
epididymis. in Chick, 1:72, 4-73; in Pig,
646. 647, 647, 631
appendix to, 647, 649
epiglottis, in Pig, 6'97
epiphysial cartilage, in Mammal, 243
epiphysial plate, in'Mammal, 657
epiphysis, in Frog, 177, 177, 178, 180;
in Chick, 350, 379. 383, «L10, 411,
412, -1-35; in Pig, 612
of bone, in Frog, 253, 254; in Chick,
/43.9, -1-39, 4-4-0: in Mammal, 656, 657
epiploic foramen, in Pig, 626, 6'29
epithelioid bodies, in Frog, 202, 204-,
2()."), 205, 217
epithelial vestig , in Chick, 442, 443;
in Pig, 62/4, 625, 625 (See parathyroids. posthranchial bodies, thymus, and tonsils)
681
epithelium,
of oviduct, -'1-89
of uterus, -L97
epoiigggron, in Chick, /:73; in Pig, 64!),
equational meiotic division, 1.9, 21, 22,
24, 25
erectile muscles of hair, in Pig, 6'6//, 66L
Erythrocytes (See blood corpusch-5)
esophagus, in Frog, 207; in Chick, 372,
373, 39.9, 1:45; in Pig, 568, 569, 578,
579, 6'27, 627
Etkin, W., 171Eustachian tube, in Frog, 195: in
Chick, 423; in Pig, 573, 618, 690
Everett, N. B., 6, 7
evocation, in Frog, 141
excretory system, in Frog, 225-233: in
Chick, 3:35—.?:37, 390, 391, 627-1428.
466-468, 468; in Pig, 605. 6113, 6'44
exocoolom, in Mammal, Pig, 5:23:
Primates, 5-L6. 5- 7, 5-19
exoplasm, of egg, in Amphioxus, 77
external appearance, in Chick, at live
days. 533-436; in Pig, at 10 mm.,
562-666’, later, 606-609
external auditory meatus, in Chick,
/4:2/I. /433
external limiting membrane of nerve
cord. in Pig, 570
eye, in Frog, 189; in Chick, 353, 35/3,
379, 388, /417-421. 435; in Pig, 564,
617
lid, in Chick, 4-35; in Pig, 609
sources of, 67
transplantation to tail, in Frog, 174,
175 - 1
face, in Chick, 633, 436, 4-35; in Pig,
566, 608, 608, 609 .
falciform ligament, in Pig, 626, 631, 633
Fallopian tubes, in Mammal, 489 (See
also oviduct)
false amniotic cavity, in Mammal,
Guinea Pig, 519; Mouse, 520, 521
Farris, E. J., 507
fasciae, in Amphioxus, 100
fat bodies, in Frog, 105, 105, 238
feather, source of, 67
feather barbs, in~Chick, 436'
feather down, in Chick, 436
feather germs, 433, 435
feather pulp, /435, 436
feather quill, 436
1
fifl
feather rachis, 436
femur, in Pig, 650
fenestra ovalis, in Frog, 196; in Chick,
423, 424; in Pig, 618, 619, 620
fenestra rotunda, in Chick, 423; in Pig,
618, 619
fertilization, 39-48; in Amphioxus, 79;
in Frog, 113-116; in Chick, 287; in
Mammal, 506
consequences of, 47-48
effect on of numbers and motility ‘of
sperm, 507, 508
nature of, 2
fertilization membrane, 40; in Amphioxus, 77, 79, 80
fertilizin theory, 43
fetal circulation, changes in at birth,
643 (See also circulation)
fibers of Sharpey, 247
fibroblasts, 240, 241, 241, 242, 24-3, 244
fibula, in Pig, 658
Figge, F. H. J ., 174
Finnegan, C. V., 216
Firket, J ., 470 ,
flagellum, of sperm, 12, 12
flexures and torsions, in Chick, 332,
333, 370, 395, 409; in Pig, 562, 606
follicle, of egg, 4, 5; in Frog, 107, 108,
237; in Chick, 281, 282, 283, 472
follicle, Graafian, in Mammal, 490, 491,
4-93, 495, 495, 498, 500, 501
follicular cavity, in Mammal, 491
foramen caecum, in Man, 627
foramen ovale, in Mammal, closure at
birth, 450, 459; in Pig, 641, 642, 64-3 '
foramina of Monro, in Frog, 179; in
Chick, 350, 411; in Pig, 611
fore-brain (See prosencepbalon)
fore-gut, in Frog, 162; in Chick, 306,
320, 323, 324, 328, 335-337, 371375, 398, 399, 442-446; in Pig,
574, 576-580, 625-628
formative materials of egg, in Amphi,oxus, 79, 82, 83
distribution of in Frog and other
Amphibia (See map)
fovea, in Frog egg, 109, 110
Franklin, K. J., 458
Fraps, R. M., 292
Fraser, R. C., 303, 3'10
Friedman, test for pregnancy, 503
Frog,
early -flevelopment: external, 147155; internal, 155-169
INDEX “
later development, 169-254
reasons for study of, 104
stages, external, 170
frontal process (See naso—frontal)
Fundulus, egg of, 263
fundus, of eye, in Chick, 388, 417
‘ fusion, of egg and sperm nuclei, in Am
phioxus, 80; in Frog, 114
gall bladder, in Frog, 178, 206; in
Chick, 374, 375, 447; in Pig, 580,
580, 582, 630
gametes, 3
gamones, 39
ganglia or ganglion, cranial,
acustico-facialis, VII, VIII, in Frog,
185, 186, 187; in Chick, 352, 353,
379, 387, 388, 415; in Pig, 568, 570
' (See also geniculate)
ciliary, in Chick, 416
glossopharyngeal, IX, in Frog, 186';
in Chick, 352, 353, 353, 379, 415;
in Pig, 570, 571, 571
jugulare, X, in Chick, 4-15, 416; in
Pig, 568, 571, 615
neumogastric, X, in Chick, 415
nodosum, X, in Chick, 416; in Pig,
568, 571, 615
petrosal, IX, in Pig, 568, 571, 571
trigeminal or Gasserian, V, in Frog,
185; in Chick, 334, 352, 353, 387,
415; in Pig, 568, 570
vagus, in Frog, 186; in Chink, 352,
353 ganglia or ganglion, spinal, in Frog,
187, 187, 188; in Chick, 329, 351,
385, 396; in Pig, 568, 569, 569,
570, 571, 572
accessory or Foriep’s, in Pig, 568,
571,571,615 .
sympathetic, in Frog, 189; in Chick,
387, 414, 414; in Pig, 572, 616
gastro-hepatic ligament, in Chick, 375;
in Pig, 630
gastrula, of Amphioxus, 88; of Triton,
137; of Teleost, 269; of Gymnophiona, 277
gastrular cleavage, in Frog, 134
gastrular movements, in Frog, 136,
137, 137, 138, 138
gastrulation, in Amphioxus, 87-91; in
Frog, 126-134, 126, 130, 131; in
Teleosts, 264-269; in Gymnopliiona, 273-276; in Chick, 300-316',
INDEX 533
320; in Mammal, 508, 511-513,
527
general discussion of, 50, 53-63, 5.3,
57, 58, 60, 61, 62
Geinitz, B., 140
genes, 27, 37
geniculate, VII cranial ganglion, in
Mammal, Pig, 570 .
genital cavity, in Frog, 236, 236, 237,
237
genital eminence, in Pig, 653
genital fold, in Pig, 652, 653
genital ridge, in Pig, 582
genital ridges, 3; in Frog, 235
genital swelling, in Pig, 652, 653, 654
genital tubercle, 645, 652, 653
genitalia, in Pig, 652, 653—654
germ cells, 3; in Frog, 236, 236, 237,
237; in Chick, 469, 469, 470, 472
germ layers, inversion of, in Mammal,
521, 522
germ ring, 55, 62, 63; in Amphioxus,
91, 97; in Frog, 128; in T eleost,
270; in Gymnophiona, 274, 276
germ wall, in Chick, 294, 297, 301, 308,
310, 317, 320, 322
germinal cells, in Chick, 351; in Pig,
567
germinal disc, 282, 284
germinal epithelium, 3, 4-; in Chick,
390, 469, 4-69, 470, 470, 471, 471;
in Mammal, 4.90, 490, 4-91
germinal vesicle, 9; in Chick, 281, 287
Gilbert, M. S., 502
gill chamber (opercular), in Frog, 202,
203
gill circulation, in Frog, 202, 216, 217
gill plate, in Frog, 148, 150, 151
gill rakers, in Frog, 203, 204
gills, in Frog, 170, 171, 202, 203, 203
gizzard, in Chick, 445, 446, 447
glandular part of oviduct, in Chick
(magnum), 475
glia cells, in Frog, 181; in Chick, 351,
385'
glomerulus, in Frog, 232; in Chick, 390,
391,474»; in Pig, 579, 604, 644
glomus, in Frog. 226, 227, 228, 229; in
Chick, 356
glottis, in Frog, 178, 206'; in Chick, 398,
, 44-3, 445; in Pig, 627
glycogen tissue, in Mammal, 543, 544,
545
Godwin, M. C., 625
Goerttler, K., 137
Golgi apparatus, in Frog egg, 109
Goldsmith, J. B., 469
gonad or gonads, 3; in Amphioxus, 76,
76; in Frog, 234-240; in Chick,
427, 445, 468, 472, 474; in Pig,
605, 645
gonoducts, in Frog, 233; in Chick, 428
Cross, C. M., 216
granulosa, in Chick, 281, 283
gray crescent, in Frog, 117, 118
inducing material, in Frog, 138, 140
plane, in Frog, 1,16, 118
gray matter, of nerve cord, in Frog.
181, 182; in Chick, 385; in Pig, 614
Grier, N., 113
Gruenwald, P., 376, 490
gubernaculum, in Pig, 64-6, 650, 651
Guinea Pig,
amnion formation in, 518, 519, 519
blastocyst in, 518, 519
circulation changes in at birth, 45.‘)
embryonic knob in, 518, 519
endoderm in, 513
inversion of germ layers in, 521
sex cycle in, 496, 500, 501, 507
survival of egg in, 508
survival of sperm in, 508
yolk—sac in, 519, 545
gum, in Pig, 658
gut, in Amphioxus, 92, 93; in Frog, 162,
163, 200-208; in Teleost, 274-; in
Chick, 335-338, 371-377, 3.98~401,
442-449; in Pig, 568, 582, 583
diverticulum, in Amphioxus, 93, 100,
I01
folding—ofl' of, in Pig, 574, 574, 575,
575
formation of, in Mammal, 513; Pig,
573
loop, in Pig, 569, 581. 582
post anal or cloacal, in Chick, 375,
376, 377; in Pig, 568, 583
gynogamones, 39
hair, in Mammal, 662-664
follicle, 663
germ, 663
matrix, 662
papilla, 662, 663, 664, 664root, 663
shaft, 664
sources of, 6*.’
half embryo, in Frog, 121
flfl
lImnbm'ger. \'.. 386
llmmnoncl, W. S., 387. 416, 44-3
lmpluid, chromosome number, 17, 18,
22. 21
hard palate, in Pig, 6'22
liarelip, 6'09
ll:u'gitt., G. T., 491
llurtman, G. T., 493, 498
llurvo_v, -155
l|2li('lliXl‘,‘,‘, of Chick, 475. 476'
llulst-lick, B., 75
Iluvi-x'.~'ian canal, 2&4, 245
Hmm-.~:ian system, 245, 24-5, 656'
In-ad and neck region, in Pig, 6'07-609
ll('2i(l of spornl. 11, 12
houd fold, in Chick, 320, 321, 323. 32/4,
324lwml process, in Chick, 305, 306, 30",
309, 309, 310, 311
lwart,
clianges in at hatching or birth, 4154/I60
development. of", in Frog, 767-168,
i’I()—f.’13; in Chick. 339, 3/11. 3112,
3/43, 344, /401-/403, /:50, /451; in
Pig, 565, 574, 586', 587, 588, 583,
58.9, 589, 633, 641, 6/13
initiation of heat in, in Frog, 21/4,
215; in Chick, 3112, 3/13
muscle, in Frog, 167
potentiality of parts, in Frog, 168
heat (See oestrus)
Hedgehog,
amnion in, 518
blastopore in, 526, 526
yo1k—sac in, 518 ‘
Helff, O. M., 174, 176, 196
Hemichromis, 266, 268
Hensen's node or knot, in Chick, 305,
305, 306, 307, 308, 309, 310; in
Mammal, Pig, 523, 524-, 525, 526
(See also primitive pit)
hepatic ducts, in Pig, 580, 580 (See
also bile)
hepatic portal system, in Frog, 22!; in
Chick, 457, 1461, 462; in Pig, 597,
600, 638 '
, Hertig, A. T., 553
Hertig-Rock blastocyst, 552 ,
Hertwig, 0., 48 «heterotypic chromosomes, 18, M, 24, 37
Hibbard, H., 109
Hilleman, H. H., 3731 .
hind—brain (&e r
INDEX
hind-gut, in Frog, I63, 207; in Chick,
337, 338, 375-377, 1400, 401: in Pi,r.,§
574, 576, 581
hmd-liml), buds, in Chick, 404
Hinsey, J. C., 501
Hisaw, F. L., 500, 501
Holtfreter, J., 126, 143, 144
Holley, E., 174
Holtzer, H., 247
homolecithal eggs, 10
homotypical chromosomes, 24
hoofs, 664
Hook, S. J., 503
horns, 67, 6'64
human embryo, 558, 559
humerus, in Chick, 4-00
llumphrey, R. H., 239
Hunt, E. A., 386
Hunt, 'l‘. E., 300, 309
Huth, 'l‘., 174
hyoid arch, in Frog, 153, 160; in
Chick, 336; in Pig, 565, 566, 576
hyoid cornu or horn, in Frog, 251, 253;
in Chick, /41:1; in Pig, 62!:
hyomandibular cleft, in Frog, 150, 151;
in Pig, 564, 565, 576
hyomandibular pouch, in Frog, 160,
I62, 195, 201, 201; in Chick, 336'.
398: in Pig, 573, 577, 619
hypoblast, 54; in Amphioxus, 88, 89;
in Frog, I32, 133, 134; in Chick.
302, 302, 303, 304, 309; in 'l‘elenst.,
265, 265; in Gymnophiona, 273;
in Mammal, 512; Pig, 508, 511),
511, 513, 515, 515
hypobranchial apparatus, in Frog, 250,
251, 251, 253
hypobronchial plate, in Frog, 203
hypochordal rod, in Frog, I63, 164
Hypogeophis, gastrulation in, 275, 276,
277
hypophysis (See pituitary)
Ichthyophis, gastrulation in, 27 6
idiozome, 11
ilium, in Chick, /438; in Pig, 627, 629,
657
illumination, effect on laying, in Chick,
292
imhntation, 513; in Ungulates, Pig,
535; in Carnivores, 539-560; in
Rodents, 540-543; in Primates,
556-551; Man and Apes, 553-558
inducing substance, 142-1143
"—-—-—j*—*—
l
i
1
INDEX 1 535
induction or evocation,
general principle, 14!, 143-144
special cases, 140, 14-1, 142, 143, 161,
190
infiltration,
gastrulation by, 58, 59: in Chick,
303
rne.<-odc-run origin by, in Chick, 309
mfundilmlum,
of brain, in Frog, 157, 158. 177, 178,
178; in Chick, 348, 34.9. 34-9, 371,
372, 381-, 4-10, 411, 4-12; in Pig, 567,
6' I I
of oviduct, in Frog, 107; in Chick
(also ostium), 282. 283. 475; in
l\-lanunal, 489: in Pig, 6'49
ingression, in Frog, 133
inguinal canal, in Pig, 646, 6'5!
inguinal ligament (in adult Poupart/s),
646. 647, 650, 653
inner cell mass, in mammals, 508, 509,
510, 510, 512, 513
inner ear (See membranous labyrinth)
inner tubule of mesonephros, in Frog,
230, 231
inner zone, of nephrogenous tissue, in
Chick, 467, 468, 468, 4-74
lnsectivores, amnion formation in, 514interatrial foramen or foramina, in
Chick, 455, 457, 459; in Pig (primum), 588, 589, 589, 593, 642,
(secundum), 588, 589, 589, 641,
641, 642
interatrial septum, in Frog, 213; in
Chick, 377, 402, 403, 450, 4-57; in
Pig (primum), 588, 588, 641, 641,
6-12, (secundum), 589, 589, 641,
64-1, 6'42
intermediate cell mass, 69
intermenstrual bleeding, in Man, 498
internal limiting membrane,
of eye, in Frog, 192; in Chick, 417
of neural tube, in Pig, 567, 570
internasal septum, in Chick, 441; in
Pig, 616, 621
interorbital septum, in Chick, 441
intersomitic fissure, in Chick, 396
interventricular foramen, in Pig, 589,
593
interventricular groove, in Chick, 402
interventricular septum, in Chick, 4-02
403, 450, 451; in Pig, 578, 589,
589. 64-2
intervertebral fissure, in Chick, 396
intestinal caecae, or caecal processes,
in Chick, 400, 445, 447, 448
intestinal portal,
anterior, in Chick, 323, 324, 339, 4-05;
in Pig, 574
posterior, in Chick, 337, 338, 376,
377; in Pig, 574 intestine, in Frog, 178, during metamorphosis, l71, 173; in Chick,
'445, 446, 447, 448; in Pig, 581,
627, 628, 629
invaginataion,
gastrulation by, 54, 55, 57; in Amphioxus, 87, 88; in Frog, 131, 132,
134; in Chick, 303, 305, 309
mesoderm separation by, 66, 67
involution,
gastrulation by, 56', 56, 57; in Amphioxus, 87, 88; in Frog, 131, 133,
134; in Teleost, 264, 265; in Gymnophiona, 277; in Chick, 302, 302
mesoderm separation by, in Chick.
302, 308, 309; in Pig, 527
iris, in Frog, 192; in Chick, 418, 418
ischium, in Chick, 438; in Pig, 657 _
islets of Langerhans, in Pig. 6'31
isthmus,
of brain, in Chick, 379, 384, 384-, 4-10;
in Pig, 567, 570
of oviduct, in Chick, 282, 283, 289
iter (See aqueduct of Sylvius)
Jacobson, W., 303
.lacobson’s organ, in Frog, 197, 199
James, R. G., 207
jaw, in Chick, 434: in Pig, 608
jejunum, in Pig, 627 (See also small
intestine)
jelly, of egg, in Frog, 111, M2
effect on temperature, 1 13
Jennings, H. B., 48
Jones, D. S., 352, 387, 415
Jordan, E. S., 508
Kaan, H. W , 195
karyosome, 28
Kellogg, H. B., 458
Kemp, N. E., 109
Kennedy, J. A., 458
kidney, in,Frog,~l05, 229-232, 230
head, in Frog, 155
Klapper, C. E., 624Knoulf, R. A.,_.185
Kollros, J. J., 181
1
{B6
Kuo, Z. Y., 476
Kupfi‘er’s vesicle, in Teleost, 265, 269,
270, 314
labio-dental, ledge or lamina, in Pig,
624, 658
lahio—gingival groove, in Pig, 623, 624,
. 658
labium majora, in Pig, 647, 652, 654
labium minora, in Pig, 647, 652, 654
lachrymal duct, in Pig, 609
lachrymal groove, in Chick, 434, 435;
in Pig, 564, 607, 608, 609
lacunae in placental trophoderm, of
Hedgehog, 518; of Guinea Pig,
519; of Rabbit, 543, 545; of Mouse,
544; of Man and Apes, 554, 555,
556
lagena, in Frog, 193, 195', in Mammal,
6'18, 618
lamina,
post optica, in Pig, 611
termin-alis, in Chick, 350; in Pig, 569
laryngotracheal groove, in'Chick, 372,
373, 373; in Pig, 579
larynx, in Frog, 206; in Chick, 337,
398, 443; in Pig, 627
latebra and neck of, in Chick, 281, 284,
286
lateral closing folds, in Chick, 465
lateral limiting sulcus, in Chick, 329
lateral line organs (ramus lateralis), in
‘r , 198, 199 ,
lateral nasal process, in Chick, 433,
435, 435
lateral neural ridges or folds, in Frog,
136, 148
lateral plate, 64, 68; in Amphioxus, 99;
in Frog, 165; in Chick, 324, 333,
395
lateral rotation, in Chick, 333, 395
lateral torsion, in Pig, 563
lateral ventricles, of brain, in Frog,
177; in Pig, 511
latero—b1-onchi, in Chick, 444
laying periodicity in Hens, 290-292
Iegs, in Frog, 172
_ Lemurs, sex cycle in, 497
"lens of eye, in Frog, 190, 190, 191, 192;
in Chick, 354, 354, 388, 417, 418,
420, 435; in Pig, 573. 576
lenticular zone, in Chick, 417
Ieptotene, stage in meiosis, 16, 18, 20
Levi—Montalcini, R., 416
INDEX
Lewis, W. H., 190
lids, of eye, in Chick, 418, 421
Liedke, K. B., 190
Lillie, F. H., 376, 378, 416
limb or limbs, in Chick, 438, 439; in
Pig, 6'06
buds, in Chick, 370, 395, 433; in Pig,
564, 565, 578, 579, 583
determination of axes in, in Frog,
172; in Chick, 333, 334
limiting sulci, in Chick, 362
Lindeman, V. F., 174
lips, in Frog, 200
liquor folliculi, in Mammal, 491
liver, in Frog, 206; in Chick, 337, 374,
374, 399, 405, 445, 446, 4-65; in
Pig, 565, 568, 569, 578, 579, 580,
581, 581, 582, 626, 630, 633
evagination, in Frog, 157, 162, 165,
177
source of, 67
lumbo-sacral flexure, in Pig, 562
lungs, in Frog, 206; in Chick, 372, 373.
380, 381, 384, 443, 444; in Pig, 568,
569, 577, 578, 632, 632
homologues, 337
Lygeaus bicrucis,
meiosis in, 30
sex—chromosomes in, 30, 34, 34, 35, 36
lymphatics, in Frog, 225
magma reticulare, in Man, 548, 549
549
magnum, in Chick oviduct, 282, 283,
289
main piece, of sperm, 12
malleus, in Mammalian ear, 618, 619,
620, 655
Malpighi, 280
Malpigliian body, in Frog, 232; in
Chick, 357, 427, 436, 471, 475
Malpighian layer, in Chick, 436
Mammal, ,
early stages of, 506-560
embryological significance, 486, 487
gastrulation in, 58,59
sexual cycle in, 493-504
Man,
allantois in, 546, 547
amnion in, 547
amniotic cavity in, 546, 547, 548, 552
hlastocyst in, 548, 548, 549, 549
blastoderm in, 548, 548, 549, 549
Heuser’s membrane in, 548, 549
INDEX 537
implantation in, 553-558
ovary in, 488
sexual cycle in, 497, 498, 503
sperm travel in, 507
uterus in, 548
yolk-sac in, 546, 547, 549, 54-9
mandibular arch, in Frog, 151, 160,
163, 201, 201; in Chick, 334, 336',
434-, 435; in Pig, 564, 565, 566, 57 6,
. 608, 608
mandibular cartilage, in Pig, 621
mandibular nerve, in Frog, 185
mandibular ridges, in Frog, 200
Marigold, 0., 139
mantle layer, in neural tube, Pig, 567,
568, 570, 613, 614
map of formative materials in pregastrular stages, in Amphibia, 138,
139; in Teleost, 271, 272, 273; in
Chick, primitive streak blastederm, 311, 312
margin of overgrowth, in Chick, 322
marginal layer of nerve cord, in Pig,
568
Markee, J. F., 504
marrow, 242, 246; in Frog, 252; in
Chick, 439. 440
Marsupials,
allantois in, 530, 532
amnion in, 530
implantation in, 530, 532, 533
placenta in, 530, 532, 533
pouch of, 531
yolk-sac in, 530, 531, 532
Martin-Falkiner blastocyst, 550, 552
Marx, A., 140, 141
massa intermedia, in Pig, 612
maturation or meiosis, in Amphioxus,
78, 80; in Frog, 1 10, 1 14; in Chick,
287; in Mammal, 505, 509
maxillae, in Pig, 6'22
maxillary nerve, in Frog, 185; in Chick,
415, in Pig, 614maxillary process, in Frog, 249; in
Chick, 434, 435; in Pig, 564, 565,
566, 576, 607, 608, 608, 609, 622
McClendon, J. F., 121
Mcliwen-, R. S., 266
I\lcl{eehan, M. S., 354 '
mediastinum, in Pig, 632, 63-1
medulla.
of brain, in Frog, 181; in Chick,
413; in Pig, 610, 613
of hair, 663
medullary or neural folds, in Amphioxus, 91, 92, 94; in Frog, 136',
14-8, 152, 154; in Chick, 306, 323,
325, 327; in Pig, 562, 565
medullary or neural groove, 64, 70; in
Frog, 136', 148, 152; in Chick, 327 ;
in Pig, 562, 565
medullary or neural plate, 64, 70; in
Amphioxus, 88, 91, 92; in Frog
(or Amphibia), 134, 135, 136‘, 138.
139, 139, 14-8, 154; in Chick. 306,
308, 310, 326; in Pig, 565, 575
medullary substance,
of adrenal, in Frog, 232, 233; in
Chick, 428, 475; in Pig, 64-4, 61-5
of gonad, AL
meiosis, 16-26‘, 27, 28, 34
comparison of, in egg and sperm,
28, 29
significance of, 37
meiotic divisions, 19, 21, 22, 23, 24, 25,
25, 28, 29,30, 31-36, 37; in Amphioxus, 78, 80 (See also maturation)
membrana granulosa, in Mammal, 490,
49!
membrane propria, in Chick, 423; in
Pig. 618, 619
membrane or membranes, of egg, M
undulatory in sperm, 13
vitelline, 1 1, in Frog, 109; in Amphioxus, 77, 78, 79, 80; in Chick, 284,
286; in Mammal, 493
membranous labyrinth, in Frog, 192,
193; in Chick, 421-423, 4-22; in
Mammal, 617, 618, 619
menstrual cycle, 495, 497-501
menstruation (See menstrual cycle)
merocytes, in Teleosts, 264; in Cluck,
287, 294
mesectoderm, 54
mesencephalon (mid—brain), in Frog,
156, 157, 177, 178, 180, 181; in
Chick, 333, 334, 348, 348, 34-9,
350. 373, 383, 384, 410, 412, 413;
in Pig, 567, 568, 569, 570, 571, 6'12
mesenchyme, in Frog, 135: in Chick
eye, 419, 419, 420
mesentery, 64, 65; in Frog, 210, 235;
in Chick, 337, 338, 339; in Pig ‘
(dorsal and ventral), 626, 628, 629,
630
mesentoderm, 54
mesoblast, in Chick, 306, 307; in Pig,
548, 549 (See also mesoderm)
&%
mesocardiurn or mesocardia, in Frog,
211, 211
dorsal, in Chick, 341; in Pig, 588,
634
lateral, in Chick, 345, 381, 465,
466
ventral, in Chick, 340, 341; in Pig,
588
mesoderm, 53. 63~67; in Amphinxus,
92, 96, 97; in Frog, 131, 134,
135, 136, 137, 137, 133, 138; in
Teleost, 269—272, 271; in Gymnapliiona, 277, 277; in Chick. 302,
306, 307, 308, 309, 316, 317; in
Mammal, 515, 516, 517, 527, 527,
575, 575
allantoic, in Mammal, 540, 548
chorionic, in Mammal, 533, 537, 539,
540, 554-, 555, 556
intermediate, in Pig, 585
peristomial, in Amphioxus, 98; in
Frog, 130
products of, 67
somatic or parietal (somatopleure),
63, 64, 65; in Amphioxus, 99; in
Frog, 164, 165, 165; in Teleost,
274; in Chick, 322, 326, 397; in
Mammal, 527, 528; Pig, 585
splanchnic or visceral (splanchnopleure), 64, 65; in Amphioxus, 99;
in Frog, 164, 165, 165; in Teleost,
274; in Chick, 322, 326'; in Mammal, 527, 528, 585, 586
mesogastrium, in Pig, 626, 628, 632,
633
mesometric side of uterus, 541
mesonephric duct, in Frog (see Wolffian); in Chick (see Wolfijian); in
Pig, 568, 604, 605, 645, 648, 649
(See also Woliiian)
mesonephric tubules, in Frog, 231; in
Chick, 357, 390, 391, 427, 466,
472; in Pig, 604
mesonephric vesicles (units), in Frog,
229, 229, 230, 231
mesonephms or Wollfian body, in Frog,
229-232, 229; in Chick, 355, 357,
406, 426‘, 427, 44-5. 466, 4-67, 467,
468, 472, 4-73; in Pig, 565, 568, 569,
579, 585, 604, 605, 643, 644, 645
mesorcium, in Frog, 104, 236; in Chick,
281
mesovarium, in Frog, _236; in Chick,
282
INDEX
inetamurphosis, normal and experimental, in Amphibia, 173-176
metanephric-duct. (See ureter)
metanephric tubules, in Chick, 468
metaneplirns, in Chick, 355, 427, 466',
467, 474; in Pig, 568, 604, 644,
645, 646
metatar.~:als, in Chick, 439
metencephalon, in Frog, 180, 181; in
Chick. 333, 334. 349, 351, 384, 384-,
410, 413; in Pig, 566, 568, 569, 571,
612, 613
micropyle, 39; in fish egg, 268
mid—brain (See mesencephalon)
middle ear (tubo—tympanic cavity), in
Frog, 195; in Chick, 423; in Pig, 6' 19
middle piece of sperm, 11, 12, 13
mid-gut, in Frog, 162, 163, 207; in
Chick, 337, 375, 400, 446-448; in
Pig, 581
milk ridge and nipples, in Pig, 607
Miller blastocyst, in Man, 543, 552
Miller and Wiltberg, pregnancy test,
503
Mole,
blastopore in, 526
maturation in egg of, 505, 506
neurenteric canal in, 526
primitive streak in, 526
Money, W. L.,, 507
Monkeys and Tarsius,
implantation in, 550, 551, 551
sexual cycle in, 4.97, 499
monoestrus sex cycle, 496
monospermy, 39
Monotremes,
allantois in, 530, 531
amnion in, 530
yolk—sac in, 509, 530, 531
Morgan, '1‘. H., 121, 321
morula in Mammal, 509, 510
Mouse,
allantois in, 542
amnion in, 520, 521
egg size, 492
fertilization in, 508
implantation in, 540-542, 541
inversimi of germ layers in 521
mesometrium. 541 ,
placenta in, 541, 542, 543, 541, 545
sex cycle in, 496
umbilical cord in. 541
yolk-sac in, 540, 541, 543, 545
mouth, in Amphioxus, 93; in Frog,
INDEX
171, 200; in Chick, 433; in Pig,
609, 622
mucosa, of uterus, 494-, 495, 4-95, 496,
497. 502
mucous gland (“oral sucker”), in Frog,
150, 151, 161, 165. 170
mucous) layer of oviduct, in Mammal,
48
Miillerian duct (See oviduct)
Munro, S. F., 281
Murray, P. D. F., 371
muscle, in Chick, 397
fibrillae, 209
of oviduct, in Mammal, 489
source of, 67
myelencephalon, in Frog, 180; in Chick,
333, 334, 34-9, 351, 384, 384-, 410,
4-11, 413; in Pig, 567, 568, 569,
612, 613
myelin substance or sheath, 614, 615
myocardium, in Frog, 211, 211; in
Chick, 339, 340, 341, 377, 378
myocoel, 64; in Amphioxus, 99, 100;
in Frog, 166; in Chick, 335; in
Pig, 585
myotome, 64, 69; in Amphioxus, 99,
99; in Frog, 150, 155, 166, 166,
209; in Chick, 329, 335, 371, 397;
in Pig, 585
nails, 67, 664
nares,
external, in Frog, 199; in Chick, 434,
435; in Pig, 608, 609
internal, in Chick, 434; in Pig, 609,
621, 622, 623
nasal bridge, in Pig, 608
nasal cartilage, in Pig, 621
nasal cavities, in Frog, 199
nasal chamber, in Pig, 621
nasal pit. (See olfactory)
nasal septum, in Chick (see internasal);
in Pig, 608. 621
nasal sinus, in Pig, 616
naso-frontal process, in Chick, 433,
435; in Pig, 564, 566, 607, 608,
608, 609
naso—lachrymal groove, in Chick and
Pig (See lachrymal) .
naso—lat.eral process, in Chick (see
lateral nasal); in Pig, 564, 566,
607, 608, 609
naso-medial process, in Pig, 564, 566,
607, 608, 608, 609, 622
689
naso-turbinals, in Pig, 616
neck of sperm, 12, 12
Needham, J ., 143
neopallium, in Pig, 611
nephrocoel, 64, 69
nephrogenous tissue, in Chick, 329,
390, 467, 467, 474
nephrostome, in Frog, 201. 226, 226,
228, 229, 230, 231; in Chick, 356
nephrotome, 69; in F mg, 167, 229; in
Chick, 326, 391; in Pig,'585
nerve or nerves,
afferent, in Frog, 189?; in Chick, 386
axones, 188, 192; in Chick, 385
cord, 64, 70.; in Frog, 181, 182, 182;
in Teleost, 274 (See also neural
tube) efferent, in‘ Frog, 182, 187; in Chick,
386
mixed, in Frog, 185
plexuses, in Pig, 572
nerve or nerves, cranial,
abducent or VI, in Frog, 187; in
Chick, 416; in Pig, 568, 570, 614,
615
auditory or VIII, in Frog, 185, 186,
187; in Chick, 415; in Pig, 570,
614, 615
facial or VII, in Frog, 186; in Chick,
387, 415; in Pig, 568, 570, 614
glossopharyngeal or IX, in Frog, 186 ;
in Chick, 415; in Pig, 571, 615
hyoid. branch of VII, in Frog, 186
hypoglossal or XII, in Chick, 416;
in Pig, 568, 571, 615
mandibular and maxillary (also
maxillo-mandibular), branch of
V, in Frog, 185; in Chick, 379,
415; in Pig, 568, 570, 614
neural placode (See placode)
oculo-motor or III, in Frog, 187;
in Chick, 373, 387, 388, 416; in
Pig, 568, 570. 614
Olfactory or 1. in Frog, 185; in
Chick, 411, 4:46, 426; in Pig, 569,
616
ophthalmic, branch of V, in Frog.
185; in Chick, 379, 4-15; in Pig,
568, 570, 614
optic or II, in Frag, 192; in Chick,
417, 4-18; inPig, 569, 617
palatine, branch of V, in Frog, 186
spinal accessory, XI, in Chick, 416;
in Pig, 568,’ 571, 615
GM
trigeminal, or Vth, in Frog, 185; in
Chick, 387, 415; in Fig, 570, 674
trochlearis, or IV, in Frog, 187; in
Chick, 412, 416; in Pig, 568, 570,
614
vagus, or X, in Frog, 186; in Chick,
416‘; in Pig, 568, 578, 615
nerves, spinal,
autonomic (sympathetic and/or
parasympathetic), in Frog, 187,
18.9; in Chick, 385, 387, 413, 414,
414, 415; in Pig, 572, 573, 616
somatic, in Frog, 187, 187, 188; in
Chick, 385, 413, 4-14», 415, 416; in
Pig, 570, 572, 615
nervous layer, in Frog, 125
nervous system and sense organs, 67;
in Frog, 155-161, 177-199; in
Chick, 326-330, 348-355, 383-390,
409-426; in Pig, 565-573, 610-620
neural arches, in Frog, 247; in Chick,
397; in Pig, 654
neural canal, lumen or neurocoel, 64,
70; in Amphioxus, 92, 93, 94; in
Frog, 155, 157; in Chick, 327; in
Hgflfl
neural crests, in Frog, 154», 155, 159,
165, 183, 184, 185; in Chick, 329,
330, 351; in Pig, 567, 569
neural folds, in Amphioxus, 91 , 92; in
‘ Frog, 147, 148, 152, 154; in Chick,
325; in Pig, 562, 565
neural groove, in Frog, 136', 147, 148,
154; in Chick, ~321; in Pig, 524,
562, 565
neural plate, in Amphioxus, 91, 92
(See also medullary)
neural tube, in Amphioxus, 92, 94;
in Frog,147,143,149,155,157;
in Chick, 327, 323; in Pig, 566,
569, 570, 571, 613
neurenteric canal, 70; in Amphioxus,
93, 94; in Frog, 152, 154-, 157, 161;
in Gymnophiona, 275; in Chick,
315; in Mammal, 526, 529, 546; 547
neurilemma, in Pig, 615
neuroblasts, in Frog, 181 , 192; in Chick,
385, 385, 388, 414, 415, 425.‘ in
Pig, 568, 569, 613, 614
a
. neurones, in Chick, 385; in Pig, 572
neuropore, 70; in Frag, 156, 157; in
Chick, 327
nictitating membrane, in Chick, 418.
435 '
INDEX
nodes of Ranvier, in Pig, 616
nose, in Chick, 4-33
notochord, 64, 68; in Amphioxus, 92,
95; in Frog. 131, 134, 135, 135,
157, 177, 178, 180, 248; in Teleost,
269, 270, 270, 271, 272, 274; in
Gymnophiona, 277, 277; in Chick,
305, 307, 310, 312, 313, 314, 325,
328, 329, 396, 397; in Mammal,
527, 528, 529; Pig, 569, 575, 655
notochordal canal, in Mammal, 527
nucleoli, chromatin, in Frog, 108, 109
nucleus,
of egg, 9, 43, 44-, 45, 46; in Chick, 284,
285, 287; in Frog, 198, 109. 114-,
115; in Mammal, 492, 493, 505
of Pander, in Chick, 284, 286
of sperm, 13, 505
of Terni, in Chick, 414
odontoblast, in Mammalian tooth,
658, 659, 660, 661
odontoblast layer, in Mammalian
tooth, 623
oestrogens, in Mammal, 503
oestrone (theelin), in Mammal, 499,
500, 501, 503
oestrus cycle, in Mammal, 494, 495,
-195, 498, 499
oil vacuole, in Teleost egg, 263, 266,
2167
olfactory bulb or lobe, in Frog, 179;
in Chick, 410, 412-, in Pig, 610,
611
olfactory capsules, in Frog, 250; in
Chick, 440
olfactory epithelium, in Chick, 390,
425, 425, 426
olfactory nerve (See cranial nerve)
olfactory organ, in Frog, 196, 197, 199;
in Chick, 389, 425, 426; in Fig,
616
olfactory pit, in Frog, 160, 160. 169,
170, 197; in Chick, 379, 3.90, 425,
426, 4-33, 435; in Pig, 564, 565,
566, 568, 573, 607, 609
omental bursa, in Pig, 626, 629, 632
omentum, great, in Pig, 626, 639
lesser or gastro-hepatic, in Pig, 626,
630
oocyte, 9; in Frog, 106, 107, 108, 109;
in Chick, 284, 285, 473; in Mammal, 491, 492, 505 (See also egg)
INDEX 591
oiigenesis, 8-11; in Amphioxus, 77; in
Frog, 107, 108; in Chick, 283-286;
in Mammal, 489—4.93
oiigonia. 9; in Frog, 106', 107; in Chick,
283, 284, 472; in Mammal, 489,
4-91
opercuium, in Frog, 172, 196, 202; in
Chick ear, 425
Old World Monkeys (Rhesus), sexual
cycle in, 4.97, 503
Opossum,
allantois of, 530, 532
implantation in, 532
placenta of, 530, 531
sperm of, 13
yolk—sac of, 530, 531, 532
Oppenheimer, J. M., 267, 271
optic chiasma, in Frog, 177, 177, 192;
in Chick, 349, 411, 412; in Pig.
569. 611
optic cup, in Frog, 190; in Chick, 353,
354, 354, 388, 417, 4-18; in Pig,
568, 573, 576
optic lobes, in Frog, 181; in Chick, 411,
413; in Pig, 567
optic nerve (See cranial nerves)
optic recess, in Frog, 177, 177; in Chick,
348, 34.9, 349; in Pig, 569, 611
optic stalk, in Frog, 159, 190. 191, 192;
in Chick, 350, 353, 354, 419, 420;
in Pig, 6'11
optic thalami, in Pig, 6'12
optic vesicle, in Frog, 159, 159, 165; in
Chick, 230, 328, 333, 342, 3/19,
353, 354; in Pig, 564, 565. 567, 573
ora serrata, in Chick eye, 417, 418
oral cavity, in Chick, 371, 373, 435; in
Pig, 564, 622
oral evagination, in Frog, 159. 162, 165,
177, 189
oral membrane or plate, in Frog, 178,
200; in Chick, 324, 348, 349, 384-;
in Pig, 574, 575
oral mucous gland (“sucker”), in Frog,
150, 151, 161, 165, 170
organ of Corti, in Mammalian ear, 618,
61.9
organizer, 141 .
organizer theory, evidence for, 138—144
Omithorhyncus, extra—embryonic memhranes and appendages in, 530
531
Orthoptera, synapsis in, 18
ossein fibers, 240, 241, 660
osteoblasts, 240, 241, 241, 242, 243,
244, 245, 246, 656
osteoclasts, 242, 244, 245, 246
ostium urogenitale, in Pig, 6'48, 652,
653, 654
otocyst (See auditory vesicle or capsule)
outer limiting membrane, of nerve cord,
568
outer tubules of mesonephros, in Frog,
230, 231
outer zone of metanephros, 468, 468,
474
ovarial sacs, in Frog, 237
ovary, 3, 4; in Frog, 106‘, 106; in Chick,
281, 282, 283, 472; in Mammal,
488, 489; Pig, 645, 64-9, 653
ovigerous cords, 4; in Chick, 422, 473
ovulation, in Frog, 110; in Chick, 287;
in Mammal, 493, 495, 495, 501
ovum (See egg)
pachytene stage in meiosis, 17, 18, 20,
21, 37
palatine process,
lateral, in Pig, 621, 622, 623
median, in Pig, 621, 622
palatio-quadrate cartilage (See cartiage)
pallial layer, 10 ‘
pancreas, 67; in Frog, 206'; in Chick,
374, 375, 399, 44-5, 446', 447; in Pig,
568, 580, 580, 582, 631
pancreatic acini, in Pig, 631
pancreatic ducts, in Frog, 206; in
Chick, 446; in Mammals, 632; in
Pig, 6'31, 631
papilla of feather germ, 435
papillary muscles, in Pig, 6'42
parabronchi, in Chick, 443, 4-44
parachordal cartilages or plates (See
cartilage)
paradidymis, in Chick, 472; in Pig,
6'47, 649
paraphysis, in Chick, 412
parathyroids, in Chick, 443; in Pig, 625,
625
parencephalon, in Chick brain, 383,
384, 410, 411
Parker, G. H., 506, 510
paroiiphoron, in Chick, 473
pars basilaris, in’ Frog ear, 193, 1.95
pars cavo-pulmonalis, in Chick, 450
pars distalis of pituitary, in Mammal,
158, 6' 12 ’
flfl
pars intermedia of pituitary, in Mammal, 1758, 6'12
pars tuberalis of pituitary, in Mammal,
158, 612
parturition, stimulation for, 503, 50!:
Pasteels, J., 137, 300, 303, 311
Patten, B. M., 343, 4.59
pecten, in Chick eye, 1:19, 419, /420, 420
pectoral girdle, in Frog, 254; in Chick,
/I38; (shoulder in Pig), 656
peduncle, in Pig, 612
Pelagia noctiluca, loss of chromatin in,
egg of, 26
pelvic girdle, in Frog, 254; in Chick,
438; in Pig, 657
pelvis, or pelvic portion, of kidney, in
Pig, 605, 644
penetration of sperm, 39, 1:0
penetration path of sperm (See entrance path)
penile raphe, in Pig, 65!:
penis, in Mammal, 488; Pig, 645, 646,
652, 653
Perameles,
allantois in, 530, 532
implantation in, 532, 533
placenta in, 533, 533
yolk-sac in. 530, 532
perferatorium, 13
periblast (central or subgerminal, and
marginal), in Teleost, 264, 264,
265, 265, 270, 271, 271, 274-; in
Chick, 293, 294, 295, 296, 297
perihlast nuclei, in Chick, 297
pericardial cavity, in Frog, 165, 167,
177, 189, 203, 211, 211, 215; in
Chick, 326', 339. 3111 , 381; in Mammal, Rabbit, 516; Pig, 578, 579,
633, 631:
pericardium, in Frog, 157, 167; in
Chick, 341, 466; in Pig, 633, 634
perichondrium, 244, 656
perichordal sheath, 396, 397
perilymphatic fluid, in Frog, 195; in
Chick, 423
perilymphatic space, in Frog, 195; in
Chick, /423; in Pig, 619
perineum, in Pig, 653
'' periosteum, 242, 246, 246, 2/47, 252,
254, 439, 623, 656'
peritoneal cavity, in 'Chick, 1:65, 466
(See also coelom)
peritoneal epithelium, in Mammal, 490.
491 '
INDEX
peritoneum, in Frog, 215; in Chick, 1:66‘
perivitelline membrane, in Amphioxus
egg, 78
perivitelline space, 4:0; in Frog, 114;
in Teleost, 263; in Chick. 286; in
Mammal, 493
Peter, K., 300, 303
Peter’s hlastbcyst, in Mammal. 552, 552
-pharyngeal region, in l“rog, 157; in
Chick, 335, 336, 372, 398, ~l.>l.‘2
pharynx, in Frog, 162; in Chick, 373,
384; in Pig, 566, 569, 576, 577, 624,
625
Phillips, B. E., 289
Phillips, R. W., 506
Piatt, J ., 386
Pig,’
allantois in, 534, 537
amnion formation in, 515
blastoderm, 515, 522, 524-, 525. 527
blastodermic vesicle (blastocyst),
254, 535, 535, 537
cleavage in, 508
gastrulation in, 510-513
implantation in, 535, 536
later development of, 561-654
oestrus cycle in, 494, 495, 496
placenta in, 5314-537
reasons for study of, 4-86, 487
yolk-sac in, 513, 535
pigment, in Frog egg, 109, 117, 118,
120
pigmented layer of retina or optic cup,
in Frog, 189, 190, 191, 192; in
Chick, 354, M7, 418
pineal gland, in Chick, 1412 (See also
epiphysis)
pituitary, in Frog. origin and nomenclature of parts, 157, 158, 15.9
anterior, in Chick, 335, 371, 384,
410. 4-12; in Pig, 577, 610, 611
effect on metamorphosis, in Amphibia, 17/4
effect on sex cycle, in Mammal, 501,
502 ‘
posterior, in Chick-, 37!, 372
placenta, in Mammals; Marsupials,
531-533, 533; Ungulates, 534-537,
534, 535; Carnivores, 538, 538,
539, 540; Rodents, 5/43, 544, 5145;
in Primates, 550-560, 554, 555
deciduate, 540, 545, 560
discoidal, 5115
indeciduate, 537
_..._——-v~——_._ ,.,,,,
INDEX 593
source of oestrogens, 502, 503
zonary, 539
placudes, in Chick, 352, 353, 415, 416;
in Frog, 160, 160, 184, 185, 186,
187, 201
plectrum collumella, in Frog, 196' '
pleura,
parietal, in Pig, 6'33
visceral, in Pig, 6'32
pleural cavity, in Chick, 466: in Pig,
632, 633, 63-1
pleuro-pericardial folds, in Pig, 634
pleuro-pericardial septum in Pig, 633,
634
pleuro-peritoneal folds, in Pig, 634
pleuro-perit.oneal septum, in Chick,
/.466; in Pig, 633
plica enceplml ventralis, in Chick
brain, 7111
Pohlman, A., 458, 460
polar bodies, 27, 28, 29, 41, «M-, -1.5; in
Am;ihioxx.:s, 77, 78, 80; in Frog,
108, ill, 111, 114-; in Clilck, 287;
in l\liilD.!'fl2?..l, 505, 505
p<:»lyoestru.<:, E’\/laxumals, -696
poiyspc-rIrr_y. 3.9; in l~"rog., 114; in Chick,
3‘u).7;s “\ aroilxi, in Chick, 3? 73; in Pig, 6'13
ponifiie ,lls:x'..are. in ('.lr§a~l:. (409, 41.1; in
Pig, 61.3‘
yrtrstaiial gut. in l7z‘0g, 17.07; in Chick,
375. ""6 3'77; in Pig, 583
g.-:z~,.tl>rai:c. “ Lu ' in Chick, 4-42,
/J-’.:5': in .lE’i_:r, .4
'pv:asi'.H'io1' eimml, ; je. in 1”“ mg, 190,
191; in Claiek., .?la'itl«, 3-30, 4-15}
iv.-.:.lgangli:.>rsi:r. liliurs oi’ sympatlietic
systeixi. in Chick. 387, 414,-1-16
post-redx1<‘.!.T2mz, .“:‘0., 20, 21, 22, 23, 24
preganglinuic lilwrs of synipathetic system, in Chick, 387, 4-14,», 416
pregnancy, 498, 502
tests for, 503
premaxillary region, in Pig, 608, 622
preoral gut, in Chick. 372; in Pig, 576
prcoral pit, in Ainplzioxus. 93, 101
prepuace, in Pig, 652, 65:?
prl?—r<-.(.lu('Lim\. 20, 20, 21, 21, 22, 24
Prichard, M. M. L., 4-58
primary (elastic) sheath of notochord.
in F mg, 208
Primates,
allantois in, 5/46, 546, 547, 548
implantation in, 550-560
 
placenta in, 550-560
sexual cycle in, 1:96-503
yolk-sac in, 546, 54-6, 547, 549, 549,
550, 551, 552, 557
primitive folds, in Chick, 305, 305, 306,
307
primitive groove, in Chick, 304, 305,
306, 307, 321, 325
in Mammal; in Pig, 524, 526, 528
primitive knot, or Hensen’s knot, in
Chick, 305, 305, 306, 307, 309,
310: in Mammal; Pig, 523, 524,
525, 526, 528
primitive pit, in Chick, 305, 305, 307,
309, 315: in Mammal, Pig, 529
primitive plate, in Chick, 305, 306
primitive streak, 65, 66; in Frog, 152,
153; in Teleost, 269, 270; in Gymnophiona, 275; in Chick, 301, 302.
304, 305, 306, 308, 308, 309, 311,
313, 314, 315, 320, 328, 333; in
Mammal, 513, 522, 523, 525, 525,
526, 526, 527, 528, 529, 562
primordial germ cells, 4, 6, 7; in Chick,
469, 4-70, 471, 472; in Mammal.
470, 489, 491
proamnion, in Chick, 305, 317, 320,
321; in Mammal; Rabbit, 516;
Pig, 529, 574.
processus vaginalis, in Pig, 646, 650, 651
proctodael pit, or proctodaeum, in
Frog, 152, 153, 154, 157; in Chick,
448, 4119, 4-4-9; in Pig, 653, 583
progesterone, in Mammal, 499, 500, 501, 502, 503
prolactin, in Mammal, 500
Prolan A and B, in Man, 503
proliferation, origin of mesoderm by,
65, 66; in Chick, 309, 317; in Pig,
527
pronephric capsule, in Frog, 227
prouephric chamber, in Frog, 228, 229
pronephric duct (also segmentation or
Wolffian), in Frog, 201, 227, 228,
229; in Chick, 356'; in Pig. 6'03
ptonephric swelling, in Frog, 150
prouephric tubules, in Frog, 226, 226,
227; in Chick, 355, 356; in Pig, 603
pronephros, in Frog, 155, 164, 167, 227 . *
227; in Chick, 355, 39l;—in Pig, 6'03
pronuclei (See nucleus, of egg, of sperm)
pro-oestrum, in Mammal, 494, 495,
495, 498
ptophases in rn"eiosis, 18-24
694
prosencephalon, in Frog, 156, 157, 177,
177; in Chick, 343, 34s—35o, 383,
409-412; in Pig, 565, 567
prostate glands, in Mammal, 488; in
Fig, 645, 646, 648
proventriculus, in Chick, 1:/:6’
pseudopregnancy, 149$, 493, 562
pubis, in Chick, 438; in Plug, 657
pulmo-enteric recess, in Chick, 381
pulp cavity in tooth, 65.9, 660
pupil of eye, in Frog, 1.90; in Chick, 350
pygostyle, in Chick, /438
Quirring, D. P., 450
Rabbit,
allantois in, 516, 542, S43
amnion in, 514, 515, 516, 517
blastoderm, 514-, 515
blastodermic vesicle in, 510
cleavage in, 506
embryonic knob in, 514, 515
implantation in, 542, 543
maturation or meiosis in egg, S06
mesoderm formation in,.5l5, 516
movement of egg in oviduct in, 510
ovulation in, 493
placenta in, 542, 543
sperm in oviduct of, 506
yolk—sac in, 513, 516, 54-2, 5113, 545
radius, in Pig, 652
ramus communicans or rami communicantes, in Frog, 189; in Chick, 387,
M4, 414-, 415; in Pig, 572
Handles, C. A., 366
raphe, penile, in Pig, 652, 65!:
Rat,
corpora lutea in, 502
descent of testes in, 651
fertilization of egg, 508
movement of sperm in, 507, 508
sex cycle in, 496
spermatogenesis in, 15
Rathke-’s pocket, in Chick, 335, 349,
371, 372, 372, 373, 3844; in Pig, 563,
569, 577, 611, 612, 625
Rawles, M. E., 300, 311, 312
_recessus opticus, in Chick, 4-10, 411,
412 (See also optic recess)
rectal evagination, in Erog, 157
rectum, in Frog, 105, 207; in Chick,
' 282, 368, 400, 445, 44-8, 448, 4-49,
449; in Pig, 581, 584, 630, 64-5, 646,
647, 64-8, 653
INDEX
reductional division, 19, 20, 21, 22, 24
rejuvenescence, 47
relaxin, 501
renal capsule, in Frog, 232
reproduction, 47
reproductive organs or system. in Frog,
105, 106; in Chick, i’é}‘(}~?8-5, 282;
in Mammal, 488-4189
respiratory system, in Frog, 206'; in
Chick, 337, 398, 399, !':!:3~4451. in
Pig, 577, 579, 632
sources of, 67
rete cords, in Frog, 236, 236, 237; in
Chick, 470, 471, 471, 172
retina or retinal layer, in Frog. 1.89, 190,
191, 192; in Chick, 354, /:17, -1-18;
in Pig, 617
retinal zone, in Chick eye, {H 7
revitalization through conjugation, -1.3
rhinencephalon, in Pig, 6'11
rhombencephalon, in Frog, 156. I57,
177, 178, 180, 181; in Chick, 3 1.8,
351, 381:, 384-, 413; in Pig, 567, 6'12
Rhumbler, 58
ribonucleoprotein, in Frog, 109
ribs, in Chick, 437; in Pig, 656'
Rock, .I., 553
rods and cones in eye of Frog, 192
Bomanoif, A. L., 306
root, .
of hair, 663
of tooth, 660, 661, 662
root sheath, inner and outer, of hair,
662, 663, 664
-rotation of Frog egg during gastrula
tion, 129, 129
round ligament,
of liver, 638
of uterus and ovary, 647, 653
Roux, VV., 121
Rudnick, DL, 300, 311
Hugh, R., 110
rutting periods, in Mammal, 50-4
Sahatier, 455, /158
saccule, in Frog, 193, 191:; in Chick, 389
sacculus, in Pig, 617, 618, 618, 619
scala,
tympani, in Mammal, 618, 61.9
vestibuli, in Mammal, 618, 61.‘;
scale, in Chick, 436
scapula, in Chick, 438; in Pig, 656'
Schectman, A. M., 126, 132, 133
Schott, R. G., 506
INDEX
Schotté, O. E., 161
Schultze, 0., 121
Schwind, J. L., 174
sclerotic coat, in Frog, 192; in Chick,
4-18
sclerotomal cells, in Frog, 20.9
sclerotome, 64, 69; in Amphioxus, 99,
100; in Frog, 166; in Chick, 329,
335, 371, 396, 397; in Fig, 584, 585
Scott, H. M., 289, 291
scrotal ligament, in Pig. 646. €550
scrotal raphc, in Pig, 652, 6'54
scrotal sac, or scrotum, in Mammal,
488; Pig, 646, 650, 65], 652. 654
Sea Bass (Serranusl, 26%, 266', 266
sebaceous glands, in Mammal, 6'63, (:64
secondary or fibrous sheath of notochord, in Frog, 908
Seesell’s pocket, in Pig, 568, 569, 577,
625
Segal, S. J., 233
segmental (vertebral) plate, in Frog,
165; in Chick, 324
segmentation or cleavage, 50, 51, 52,
53; in Amphioxus, 83-87, 85; in
Frog, 117, 123, 124, 124', 125; in
Teleost, 262-264, 264; in Gymnaphiona, 273; in Chick, 292-299,
293; in Mammal, 508, 50.9, 510
accessory, in Chick, 293, 294
cavity (blastocoell, in Teleost, 263.
264 (See also blastocoell
holcblastic or total, 52
niereolilastic or discoidal, 53; in Teleost, 26,2, 264
unequal, 53
semen, in Mammal, 483
sperm per c.c. in, 507
semicircular canals, in Frog, 193, 194;
in Chick, 389, 422, 422: in Pig, 617,
618
semilunar valves, in Chick, 451; in Pig,
642
seminal vesicles, in Frog, 105, ‘I06; in
Mammal, 488; Pig, 615, 64-6, 6'48
seminifemus tubules, in Frog, 105, 238;
in Chick, 281, 471, 4-71, 472; in
Mammal, 488
sense organs, early development, in
Frog, 159
some plate, in Frog, 14-8, 149, 150. 151
::c§l:,a, in Frog heart, 213, 21-1; in Chick,
4-92, 403, 450; in Pig, 588, 583, 589,
589, 641, 641, 642
695
septum,
primum in Pig heart. 533, 539, 589,
641, 642, 643
secundum, in Pig heart, 588, 589,
589, 641, 642, 643 '
spuiium, in Pig heart, 589
transversum, in Frog, 215; in Chick,
465; in Pig, 579, 633, 633, 634
scro-amniot-ic connection, in Chick,
359, 360, 361, 364, 365, 366; in
Mammal, Rabbit, Pig, 517,.
serosa, in Chick, 360
serous membrane of uterus, in Mammal, 489
Sertoli cells, 6, 15, 15;‘ in Frog, 105; in
Chick, 471
Severinghaus, A. E., 503
sex-cell cord, in Frog, 235, 235
sex-cell ridge, in Frog, 235, 235
sex chromosomes, 30-37, 30, 31, 32. 33,
34, 35, 36
sex determination, 38
sex reversal, in Amphibia, 238-240
sexual cords, 5, 5; in Chick, 469, 471,
71, 472, 473
sexual cycle, in Mammals, female, nonPrimates, 493-496, 495; Primates
(menstrual), 4-95, 496-498; male,
non-Primates, 504
anovulatory, in Primates, 495, 499500
causes of, 499-501
functions of, 501, 503
Sheep,
inner cell mass in, 510
movements of sperm in, 506, 507
sexual cycle in, 496
shell membrane, in Chick, 282, 286,
288, 290
sinus,
rhcmhoidalis, in Pig, 562
terminalis, in Chick, 317, 322, 346,
347, 408, 409; in Mammal, Marsupials, 530
venosus, in Frog, 178, 212, 213; in
Chick, 3-13, 345, 34-8, 34-9, 381. 384.-;
in Pig. 536, 587, 589, 597, 598. 600,
639, 640, 642, 643 ‘
skeletogenous sheath, in Amphioxus:
100; in Frog, 247
skeleton, 67; in Frog, 240-254; in
Chick, 436-441; in Pig, 655-658
appendicular, in Frog, 252-254; in
Chick, ./I38-440; in Pig, 656’-658
fl%
skin, dermis and epidermis, 67
skull bones, in Frog. 248-251; in Chick,
440-441; in Pig, 655
alisphenoids, in Chick, 441
angulars, in Chick, 441
basisphenoid, in Chick, 441
dentals, in Chick, 441
epiotic, in Chick, 441
ethmoid, in Pig, 655
exoccipital, in Frog, 249
frontals, in Chick, 441
fronfo-parietals, in Frog, 249, 251
hyoid apparatus, in Chick, 441
internasal septum, in Chick, 441
interorbital, 441
jugals, in Chick, 441
'lachrym'als, in Chick, 441
maxillae or maxillary, in Frog, 249;
in Chick, 441
nasals, in Frog, 249; in Chick, 441
naso—turbinals, in Pig, 6'55
occipital, in Pig, 6'55
opercular, in Chick, 441
opisthotic, in Chick, 441
orbitosphenoid, in Chick, 441
palatine, in Chick, 441
parasphenoid, in Chick, 441
parietals, in Chick, 441
periotics, in Pig, 655
premaxillary and premaxillae, in
Frog, 249; in Chick, 441
proiitic, in Chick, 441
pterygoicl, in Frog, 249; in Chick, 441
quadrate, in Chick,’ 441; in Pig, 655
quadratmjugal, in Frog, 249; in
Chick. 441
sphenoids, in Pig, 6'55
squamosals, in Chick, 441
supra-angulars, in Chick, 441
supra-occipitals, in Chick, 441
vomer, in Chick, 441
snout of Pig, 609
Soderwall, A. L., 507
somatic cells, 3
somatopleure, in Frog, 165; in Chick,
326, 397 (See also somatic mesoderm)
somite, 69; in Amphioxus, 92, 93, 95,
r 96, 98; in Frog, 165, 166, 166, 208;
in Teleost, 274-; in Chick. 306, 322,
324, 325, 325, 328,’ 329, 333, 334-,
334, 335, 370, 371, 379, 395, 396,
396; in Pig, 525, 564, 565, 575, 584
Sonneborn, T. M., 48 "
INDEX
spawning, in Amphioxus, 78; in Frog,
11 ‘I
Spcmann, H., 139, 140, 143
sperm, ‘
development of, 14
ducts for, in Frog, 106
entrance point. plane of, in Frog egg,
115, 116
motility of, in genital tra<:.£, of Mammals, 506'. 507, 508
penetration of egg by, 39
survival time of, in genital tracts of
Mammals, 507, 508
varieties of, 13
spermatids, 14, 16
spermatocytes, 14, 15, 16, 18, 19, 28, 2 ;
Chick, 472
spermatogonia, 5, 14; in Chick, 471,
472
spermatozoa, 11, 12, 13; in Frog, 105
(See also sperm)
spinal cord, in Frog, 181, 182; in Chick,
351, 384, 385; in Pig. T0, 61.’).
614- (See also neural tube and nerve
cord)
spiracle, in Frog, 170, 172
spireme, 16
splanchnocoel, in Amphioxus, 99, 99;
in Frog, 210 (See also coelom)
splanchnocranium, in Chick, 441
splanchnopleure, in Frog, 165; in
Chick, 326'; in Pig, 573 (See also
mesoderm splanchnic)
spleen, in Frog, 216, 225; in Chick, 399;
in Pig, 626, 629
spongioblasts, in Pig, 567, 570, (514Spratt, N. T., 301, 303, 305, 308, 309,
310, 311, 313
Stanley, L. J ., 469
stapes, 424; in Pig, 618, 619, 620
Stellate cells, in Pig, 658
sternum, in Chick, 437; in Pig, 656
stigmata, in Chick, 282
stomach, in Frog, 207; in Chick, 372,
373, 399, 445; in Pig, 568, 579, 579,
580, 626, 627, 628, 631
stomodaeal invagination, in Frog, 150,
151
stomodaeum, in Frog, 157, 169, 170,
200; in Chick, 335; in Pig, 574, 576,
622
Straus, W. L., 397, 437
Streeter, G. L., 552‘
strepsinema, 19
INDEX 597
stroma, 4; in Frog, 107; in Chick, 283,
471, 472
stylohyal, in Chick, 425
styloid process, in Pig, 624
subgerminal cavity, in Chick, 294, 297,
303; in Mammal, 510
subzonal layer, in Mammal, 509, 510,
513
sulcus limitans, in Pig, 613
sulcus rhinalis, in Pig, 610, 611
summary, first day of Chick, 330-331;
second day of Chick, 367—369;
third day of Chick, 391-394;
fourth day of Chick, 428-432;
fifth day of Chick, 476-479
superfctation, 504
supernumerary nuclei (See merocytes)
Swift, C. H., 469
Swingle, VV. W., 238
sympathoblasts, in Frog, 233
synapsis, 17
synaptene stage, 16, 17, 18, 20
symcytiunx, in Teleost, 264
synencephalon, in Chick, 383, 384, 410
synizesis, 17, 18, 20
tail, in Mouse, 508
tail, of ~*»p«.<:rz::-1, L2, 12
tail bud, in Chick, 338, 375, 376, 377;
in Fig, 554tail folzi, in Chick, 338, 338
tarsals, in Chick, 439
Tarsius,
allantcis in, 551
amnion in, 550, 551
implwztation in, 550
piacenta in, 550, 551, 551
yolk-sac in, 551
tarso—metatarsals, in Chick, 43.9
Teacher, J. H., 552
tectoral membrane, in Pig, 613, 619
teeth. in Frog, 200; in Mammals, 623,
6'24, 658-662, 658
dentine in, 67, 658, 659
enamel and enamel organ in, 67, 658,
658 ~
telencephalon, in Frog, 179, 180; in
Chick, 333, 34-9, 350, 383, 384-, 409,
4-10, 411; in Pig, 567, 568, 610
telolecithal eggs, 10; in Frog, 109
temperature cfl'ect on Frog egg, 113
tendons, connections with bone, 247
tertiary egg coverings, in Frog, 111,
111, 112; in Chick, 286, 288, 289
testis, 3, 5, 5; in Amphioxus, 76'; ‘in
Frog. 104, 105, 105; in Chick, 280,
281, 468-472, 471; in Mammal,
; Pig, 645, 645, 646, 646, 650,
appendix of, in Pig, 649
descent of, in Pig, 646, 650, 651; in
Rat, 6'51
eifect of retention, 651
testosterone, use in sex reversal, 239
tetrads, in meiosis, 13—25, 19, 24
thalamus, in Chick, 441
theca of ovarian follicle, in Chick, 283
externa, in Frog, 107 ; in Chick, 280;
in Mammal, 491
interim, in Frog, 107; in Chick, 280;
in Mammal, 4.91
thymus, 67; in Frog, 203, 204, 205, 205;
in Chick, 442, 44-2, 443; in Pig, 624,
625, 625
thyroid, 67; in Frog, 78, 205, 205; in
Chick, 336, 319,372, 373, 384, 398,
442; in Pig, 568, 6'25, 625
effect on :'nct.amc-rphosis, in Frog,
174
tibia, in Chick, 439; in Pig, 658
Ting, H. P., 125
Tomes fibers, in Mammalian tooth.
658, 660
Tomes" processes, in Mammalian tooth,
658, 661
tongue, in Frog, 200; in Chick, 398; in
Pig, 62}, 6'23, 623 '
tonsils, in Pig. 6122, 6'24, 625
torus transversus, _in Frrsg, 1'77, 177;
in Chick, 383, 334», 411. 3:12
Towns, P. L.. 144 _
trabeculae carneae of heart, in Pig, 588.
593, 641, 642
trabeculae of bone, 243, 244, 24-6
trabeculae of cartilage (Sec cartilage)
trachea, in Chick, 3-37, 398, 443; in Pig,
568, 578, 579
transverse neural ridge or fold, in Frog,
136', 148
transverse (or costal) processes, in Frog,
247; in Chick, 437; in Pig, 6'56
triblastic, definition of, 63 ‘
trigerninal ganglion (See ganglia)
trigeminal ner"ve (See nerve," mandibular
and maxillary, also ophthalmic)
Triton, pregastrular map of formative
‘ materials in, 138
&%
trophoblast, in Mammal, 503, 598, 509,
510, 512, 513, 514-, 514-, 515, 515,
516, 518, 518, 519, 519, 520, 521,
530, 532, 533, 54-3, 54-9, 549, 550,
553
allantoidean, 5/:2
omphaloidean, 520, 54-1, 5/13, 544»
trophoderm, in Mammal, 516, 526, 5112,
54-4‘, M5, 552, 554, 555, 556, 557,
558, 559
allantoidean, 516, 519, 520, 541, 5132
truncus zu'tei-iosus, in Frog, 177, 178,
212, 21/4; in Chick, 341, 3112, 342,
3'58, 404-, 451, 452, 453, 4-54; in
Pig, 536, 569, 587, 588, 593, 594,
636. 642
tubal ridges, in Chick, 1:28
tnberculum,
impar, in Pig, 623
mammillare, in Chick, 4-12
posterius, in Frog, 156', 157, 177, 178,
180; in Chick, 31:9, 349, 410, 412;
in Pig, 569
tuho—tympanic cavity (See middle ear)
tubules of kidney, in Pig, 6111: (See also
mesmiepliric tubules and metanephric tubules)
tunica albuginea, in Frog,
Chick (See albugineal
tunica vaginalis, in Pig, 646, 6'5!
Tupaija javanica,
amnion in, 512. 51/1
blastodermic vesicle in, 512
inner cell mass in. 512
twins, in Frog, 121
tympanic cavity, in Frog, 195; in
Chick, see middle ear; in Pig, 6'20
tympanic membrane, in Frog, 195; in
Chick, sec tympanum; in Pig, 618,
6'20
tympanum, in Chick, 420
105; in
Uhlenliuth, E., 174
ulna, in Pig, 656'
ultinno-branchial (suprapericardial),
bodies, in Frog, 204.. 205. 205; in
Chick (postbranchiall, 442, 1:43;
in Pig (postbranchial), 625, 625
u'ml)ilical cord or stalk, in Mammal,
Rodent, 541; Primates, 546, 547,
5/18, 550, 556; Pig, 535, 565, 573,
606, 607, 64-5 ' ’
umbilical stalk, in Chick, 000, 4-45,
44-7
INDEX
umbilicus,
somatic, in Chick. 361, 36'2;‘in Pig,
573
yolk-sac, in Chick, 362, 365; in Pig,
573
Ungulates,
allantois in, 534, 536 .
blastodermic vesicle in, 510, 511,
535
implantation in, 535, 536, 537
placenta in, 534, 535, 536, 537
yolk—sac in, 53!:
unipolar ingression, in Triturus, 132
ureter, in Frog, 105, 106, 106; in Chick,
1:27, 467, 468, 468; in Pig, 604,
605, 605, 644‘, 64-5, 64-6, 647, 648,
64-9, 651
urethra in Mammal, 488; in Pig, 645,
646, 647, 6'48
penile, in Pig, 65/J
prostatic, in Pig, 65-’:
urinary bladder, in Frog, 105, 208; in
Pig, 645, 646, 64-7, 648, 649
homologue of, in Chick, 365
urinogenital or urogenital ducts, in
Frog, 233, 23/4, 234-, 235; in Chick.
390, 391. 4-27, 428, 473, 470. 4-74;
in Pig, 6/16-6-/49
urinogenital or urogenital sinus, in Pig,
584, 604, 645, 647, 648, 649, 653,
654
urinogenital or urogenital system, 67;
in Frog, 225-240; in Chick, 355357, 391, 4264428, 466-(:75; in Pig,
602-60.’, 6/13-—6'5l:
urodaeum, in Chick, 449, 4-49
Urodele, gastrulation in, 137, 137, 139
uro-rectal fold, in Pig, 58/4, M5, 647,
653
umstyle in Frog, 248
uterine endometrium, 1189, 49-1, 500,in Ungulates, 535, 537
uterine epithelium, U ngulates 536, 537;
Carnivores, 538; Rodents, 540,
541, 542, 543; Primates, 550, 551,
552, 553, 555, 556, 557
uterine glands, in Man and Apes, 552,
554, 555
uterine mucosa, Carnivores, 538; R0dents, 543; Man and Apes, 555,
556, 557, 558, 559 ,
uterine secretions (“milk”), in Marsupials, 532; Ungulates, 534; Carnivores, 538 INDEX 699
uterus or uteri, in Frog, 105, 107; in
Chick, 282, 283; in Mammal, 534,
54-1, 54-2, 54-3, 553, 556, 556, 557; in
Pig, 645, 647, 6-49
bicornis, in Mammal, 48.9
duplt-2x, in Mammal, 148.9
masculinus, in Pig, 649
products of and time spent. in, in
Chick, 28.9, 2.90
simplex, in Mammal, 25:89: Pig, 64-9
utricle, in Frog, 193. 19/1: in Chick, 389,
/:22, 422; in Pig, 6'17, 618, 618, 619
vagina, in Chick, 282, 283; in Mammal,
148.’); ‘Pig, 645, 61-7, 649, 054vagus (See ganglion and nerve)
valves of heart, in Pig,
mitral or bicuspid, 6-11, 0412
tricuspid, 6-11, 6-42
valvulae venosae, in Pig, 578, 589, 589,
596, 6/42, 6/13
variatiml, causes of, 4-8
\'as defercns, or vast: del'er'entia, in
Frog, 105, 106’, 233; in Chick, 281,
428, 471, 473; in Mammal, /488;
Pig, 645, 6:56, 616, 648, 651
vasa elfcrerxtia, in Frog, 105, 106', 233',
in Chick, 981, /I71
Vegetal pole of egg, 8, 10, 55; in Amphioxus, 79, 80, 82, 84-; in Frog,
109, 117, 129; in Fish, 262
vein or veins,
abdominal, in Frog, 224
anterior cardinals, in Frog, 220, 221,
221: in Chick, 3145. 346, 380, 382,
/106', 463; in Pig, 536, 576, 587, 539,
596, 597, 598, 599, 601, 638, 639
azygos, in Pig, 599, 640
caudal, in i71'og, 222, 223; in Chick,
461, 465
ce,rvic(>—Lhoracic, in Pig, 599, 640
femoral, in Frog, 223. 22!:
gspzxadal, in Pig, 599
lwpatic, in Frog, 218, 220, 221; in
Chick, 405, /462; in Pig, 596, 597,
(I00
hepatic portal, 220, 221, 223; in
Chick, 405, /462; in Pig, 581, 596,
597, 600, 637, 638
iliac (common, external, internal). in
Frog, 223, 22-4; in Chick, 464, 465;
in Pig, 598. 599. 637, 639, 6/10, 797
innominate, in Frog, 221, 222; in
Pig, 599, 639
intermediate, in C-hick, 383, 408, 109
intersegmcntal, in Pig, 601
intestinal, in Pig, 596
jugular (external, internal), in Frog,
203, 221, 221, 222; in Chick, 373,
379, 380, 461; in Pig, 596, 599, 601,
638, 63.9
median cardinal, in Frog, 222, 223
mesenteric, in Chick, 461, 461, -1-63;
in Pig, 599 ~
omphalnmesentcric (See vitelline) ~
pelvic, in Frog, 221, 223
posterior cardinal, in Frog. 220, 221,
221, 228, 235; in Chick, 329, 345,
34-6, 356, 380, 380, 381, 382, 390,
4()’:’, 462, 463, 46-1-, 4611», -165; in Pig,
536, 581, 582, 583, 587, 589, 596,
597, 598. 599, 601, 602, 605, 638,
639, 64.0
pulmonary, in Frog, 218, 22/4; in
Chick, -(I08, 457; in Pig, 577, 603,
640, 64-1
renal, in Frog, 2211; in Chick, 4641,
4-64; in Pig (unlal)el(2d). 599
renal portal, in l*‘rog, 221, 223, 22/1;
in Chick. 1462: in Pig, 639
sciatic, in Frog, 221, 223. 22/4
sulwai-(lirial, in Chick, 380, 1106', 407,
461, .069. 463, 464. 474: in Pig, 569,
582. 583, 596, 598, 599, 60!, 602,
63.9
subclavian, in l“r<>g, 2:31, 221: in
Chick, (I62, -163; in Pig, 578, 598,
599. 601. 638, 63*)
subscapulur, in Frog, 221. 222; in
Chick, 381
suprac,-ardinals., in. Pig. 599, 6/10
\1!lll)ll1(?i1l, in Chick, 379, 381, 382,
4-05, ((1)8, 457, 461: in Pig, 536, 569,
579 581, 582, 583, 587, 596, 597,
598, 600. 638
Ventral, of nms(meplims, in Pig, 581,
582, 583, 598, 599, 603, 605
vitelline, in l*'ro,I,>;, 213, 2228; in Chick,
328, 339, 3/10, 342, 3-14, EH3, 34-6,
3117, 379, 381, 382, 383, 405, 406',
4-08,"rL09, 4-57. /:60, 461: in Pig, 569,
579, 582, 587, 596. 597, 5 7, 598,
599, 600, 637 °
velar plates, ’in Frog, 202. 203, 20!:
velum transvcrsum, in Chick, 34-9, 350,
410
vena cava,
anterior in‘ superior, in Frog, 221,
700
vena cava,
222; in Chick, 457, 461, 463: in
Pig, 639, 611-1, 641
posterior or inferior, in Frog, 218,
221, 222, 232; in Chick, 406', 407,
457, 461, 463, 463, 464-, 4-61; in
Pig, 569, 578, 579, 581, 589, 596,
597, 598, 599 602, 603, 638, 639,
64-0
vena intervertebral, in Chick, 464
veno':s ring about gut, in Chick, 405,
/406'
yenous system, diagraln of development. of, in Pig. 598, 599
ventral horns in nerve cord, in Chick,
385: in Pig, 568, 570
ventral mesentery, in Pig, 57/:
\'ent;ricle or ventricles‘ of,
brain, in Frog, 177, 17.9, 183': in
Chick, 350; in Pig, (lll) GM, (JV)
613
heart, in Frog, 212, 2111; in Chick,
333, '34}. 342. 342. 377, 378, 3'7 ,
384-, 402, <‘?U..‘n’, 4-15, 456, 45?; in
Pig, 569, 578, 579. 587, 588, 588,
641, 64-1
vermiform appendix, in ‘fan, 6'29
vcrmis of brain. in Pig, 6. 3.?
\'eri.cbra or vertebrae, 69: in Frog, £237,
‘ 7; in Chick, 397, 736', 437, 4:37,
438; in Pig, 6'55
vertebral arch, in Chick, -I-37
vertebral plates (segmental), 64, 6'9
\'c.~"t.ihule, in Pig, 64-5, 647, 65!:
\ilii, in Pig, 536'; in Carnivores, 539,
540; in Man and Apes. 546, 547,
549, 553, 554:, 555, 556, 13:37,
559
visceral arches, in Frog, 250, 251, 251;
in Chick. 335, 336, 372, 373, 3.98,
403, 4-35, 12/41, 1:42, 4-42. 443; in
Mammals, Man. 559; in Pig, 563,
565, 566, 568, 576, 577, 593, 624
(See also branchial arches)
‘visceral clefts or furrows, in Chick, 336, ,
372, 372, 373, 398, 442, 442; in
Pig, 563, 564, 565, 576, 579 (See
also branchial clcfts)
visxzceral pouches, in Chick, 335. 336,
372, 372, 373. 398, 442, 4-4-2, 443;
in Pig, 624, 625, 625 ‘
visceral skeleton, in Frog, 251, 251; in
Chick, /441
vitelline membrane, of eg ,'H; in Am:
INDEX
phioxus, 77; in F mg, 109, 111; in
Chick, 361
vitreous chamber, in Frog, 190
vitreous humor, in Frog, 192; in Chick,
418; chamber, 354, 380, 418
Vogt, W., 136
Von Beer, 280
vulva, in Pig, 654
Wang, W. H., 453
Watterson, R. L., 437
Vveisman. A., 7, 4-8 *
Werner (Stieve) blastocyst, 548, 552
VVctzel, H., 311
Whale, size of egg in, .493
white matter of nerve cord, in Frog,
I81, 182', in Chick. 385; in Pig, 6'14
Whitehead, W. H., -158
Wilder, H. H., 194
Wilcns, S., 168
Wilson, E. B., 75
Wilson, H. V., 266
Wimsau, ‘V A., 508
Windle, VV. F., -1-58, -"159
wing-bud, in Chick, 379
Winiwarter, H., 352
Wislocki, G. B., 503
Witschi, E., 196, 216, 238, 239, 468
Wittek, M., 109
Woodruff, 48
\Voodside, G. L., 300, 315
Wolff, C. F., 280
Wolilian duct. (pronephric or «nownephric), in Frog, 93!, 233, 235, in
Teleost, 274-; in Chick, 32?), 3:31;.
399, 391, 4-48, 4--'1~9, 461?, 4-66, 463',
4-68, 4-70, 474, 4-74; in Pig, 568, <'.r'()11,
605, 645, 61-6, 64-7, 6-18, 649
X—chromosome, 32, 32, 33, 36
zzenopus capensis, section of notochord
in, 231-7
Y-chromosome, 30, 34, 36
Yntema, C. L., 186, 352, 387
yolk, 39,
blastopore, in Chick, 318, 320, 362
in egg of, Frog, 109, 122; Teleost,
271:; Chick, 2814, 285, 286, 286, 287
nuclei, in Teleost, 263; in Chick, 285
nucleus complex, 10
plug, in Frog, 130, 131, 132; in Gymnophiona, 2714, 275
INDEX 701
white, in Chick, 284, 286 endoderm (See endoderm)
yellow, in Chick, 281:, 286 septa, in Chick, 362, 364, 365 _
yolk nuclei, in Frog egg, 109 umbilicus, in Chick, 362, 364, 365,
yolk-sac, 61; in Chick, 319, 361, 362, 366 .
364», 365, 366, 448. 457, 475, 476; yolk—stalk, in Chick, 362, 44-5, 447; in
in Mammal, 512, 52.9; Mono- Pig, 568, 573, 582, 627, 629
1 tremes, 536, 531' ; Marsupials, 530, Young, VV. C., 507, 508
l 531, 532; Ungulates (Pig), 513,
516, 534, 535, 536, 563, 564, 569, zona pellucida or radiata, in Chick,
; 575, 575, 586'; lnsectivores, 512, 264; in Mammal, 492, 1:93, 506,
l 513; Carnivores, 513, 537, 538, 509, 510
' 538; Rodents, 512, 513, 516, 518, zone of Junction, in Chick, 294-, 2.97,
519, 520, 540, 541, 542, 543, 545; 298, 302, 322
Primates (Man), 546, 54-7, 549, Zwilling, E., 161, 194, 376 K
550, 552, 557 zygopophysis, in Chick, 437


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McEwen RS. Vertebrate Embryology. (1949) IBH Publishing Co., New Delhi.

   Vertebrate Embryology 1949: 1 Germ Cells and Amphioxus | 2 Frog | 3 Teleosts and Gymnophiona | 4 Chick | 5 Mammal | 1949 Vertebrate Embryology
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This 1949 third edition textbook by McEwen describes embryonic development.



1923 Edition

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Vertebrate Embryology

Robert S. McEwen

Professor Emeritus of Zoology, Oberlin College

Contents

Part I The Germ Cells and Early Development of Amphioxus

  • 1. Introduction
  • 2. Fertilization and Early Stages in Development
  • The Early Development of Amphioxus

Part II The Development of the Frog

  • The Frog: from the Production of the Germ Cells through Gastrulation
  • The Frog: Early or Embryonic Development Subsequent to Gastrulation
  • The Frog: Later or Larval Development

Part III The Teleosts and Gymnophiona

  • The Teleosts and Gymnophiona: their Segmentation and Gastrulation

Part IV The Development of the Chick

  • The Chick: the Adult Reproductive Organs, and the Development of the Egg Previous to Gastrulation
  • Gastrulation and Development through the First Day of Incubation
  • The Chick: Development during the Second Day of Incubation
  • The Chick: Development during the Third Day of Incubation
  • The Chick: Development during the Fourth Day of Incubation
  • The Chick: Development during the Fifth and Subsequent Days

Part V The Development of the Mammal

  • The Early Development of the Mammal and its Embryonic Appenclages
  • Development of the Pig to the Ten Millimeter Stage
  • The Later Development of the Pig
  • The Skeleton, Teeth, Hair, Hoofs and Horns

Index

Preface to the Fourth Edition

As in previous revisions, the fourth edition of this text does not purport to be a new book. It again frankly retains the fundamental plan and character of the older editions, in that it is primarily descriptive. but with enough experimental results interwoven with the descriptive material to stimulate interest, and to elucidate such principles of development as have been firmly established.

Though not radically altered, the older book has nevertheless been carefully gone over page by page, and, as before, changes have been made. wherever it was thought desirable in order to bring the subject matter up to date, to clarify statements, or to correct errors. In some cases. whole pages have been entirely rewritten, and in certain instances, as in the section on maturation of the germ cells, this has involved several successive pages. Mistakes in figures have also been corrected, and in a few cases. as in the diagram of frog gastrulation, the figure has been completely modified and, the writer believes, greatly improved.

Thanks are due to various colleagues who have made suggestions and pointed out errors. Especial gratitude is felt by the author to Dr. Roland Walker for his meticulous notations of errors both large and small, and for his constructive eiiorts to aid in their correction.

R. S. MCE. Oberlin College,

September, 1956.

Preface to the First Edition

This book is designed as an introductory text in Vertebrate Embryology, a work which seems to be justified on the following grounds: The older texts upon this subject, though in many cases excellent, do not cover exactly the field which is now covered in many colleges; these texts, moreover, are becoming somewhat out of date in various details. Among the newer books the best ones tend to do one of two things. Either, in the interest of thoroughness, they confine their attention entirely tn one form, e.g., the Chick, or else, for the sake of a broader viewpoint, they deal with a considerable number of animals, but in doing so touch only upon the earlier developmental stages of each. Now it is obvious that there is great value for the student, both in the accuracy gained by the careful intensive study of a single type, and also in the possession of less detailed knowledge of the history of other forms which are nearly related to it. Hence, what has seemed to be needed was a book which would, so far as is possible, make available both these advantages. To meet this need, the major part of the present text comprises a mo-,leratcl}‘ complete account of the development of two typical forms. i.e., the Frog and the Chick, each of which, in the writer’s opinion, has special features which justify such treatment. These relatively detailed discussions are then supplemented by chapters which present brief comparisons, not only with the Mammal, but also with certain other significant members of the Vertebrate group. Furthermore, the essentially embryological portion of the book is preceded by an optional introductory chapter dealing with the elements of cytology. Upon this basis the effort throughout the work has been to produce something adapted to the requirements of the general student of Zoology. us well as to the individual particularly interested in premedical preparation.


As i'crgzvx'tls certain details concerning the method of handling the topics involved, the following remains to be said. Because of the character of the book, the chapter upon cytology places special emphasis upon the structure, development, and function of the germ cells, with particular reference to nuclear phenomena and their genetic significance. The strictly cnibryological subject tn:-ttter is then introduced by a short general discussion of the more lundaixiierxtal and universal proc of Vertebrate development from the comparative standpoint. This includes a description of the various types of segmentation, gastrulation, and the formation of the rudiments of the nervous system and the main mesodermal structures. Following these introductory chapters,

‘Amphioxus is the first particular type to be considered lI(’('£lUSt‘. of the

relatively primitive character of most of its early history. The later development of this animal, i.e,, that following the fnrnizuion of the mt'.s'ndermal somites. is, however, quite highly distinguish it from the vast majority of Clionlates are without great significance for the general student. tliey are mniuml.

The Frog, as suggested above, is one of the two forms which have been treated at some length. The reasons for suvli extencled mnsirl<~ration in this instance and in that of the Chick are presunmbly olwious to every Zoiilogist. For the sake of the student. however. the uzlim uf these animals as subjects of enibryologitral study is lt\[llt‘txil,’il in tinparagraphs of the text which introduce them. ln the case ui lhv "I":-u;_». its early history has been presented under the head of c-ertuin fairly. well recognized stages which lend themselves well to corre-l;1tion with work in the laboratory. In further pursuance of this method the-. internal changes have been noted in alternation with those or-currin;__r cxtc-rnall_\ . This was done in order that the reader might obtain. so far as pm-s_<il»le. a correct idea of the really simultaneous character of tliese processes. It did not seem feasible, however, in a work of this St'(}pt.' to continue this plan throughout the entire course of development in this animal. The later external changes. therefore, are included under one lieading. while the more advanced details of organogeny are described in terms of particular systems.

Following the treatment of the Frog, there has been introduced a very brief account of segmentation and gastrulation in the Teleosts and the Gymnophiona. This has been done despite the realization that in the case of the latter group laboratory consideration will in most cziscs be impossible. The reason for this is the authors opinion that segnu-xi1;+ tion and gastrulation in these two classes of animals are extrem:-ly valuable in assisting the student to relate these processes in the Frog In those which he is about to study in the Bird. Experience, xnoremm‘, has seemed to indicate that the relation of avian and mammalian gztstrulzb tion to that in more primitive forms is always particularly clillicult for

i the beginner to grasp, and it is believed, therefore. that any legitinmte aid to this end is worth while.

In treating the early stages of the Chick a good deal of stress has been placed upon the method of segmentation and gastrulation. The latter especially has been emphasized because of its peculiar character, and the desirability of making clear its relationship to that in the forms already studied. The later history of this animal is then presented in daily periods, according to the well-known plan of Foster and Balfour. This has been done because it seems to the writer that at least in a beginning course, this method has certain marked advantages over that of stuclying the complete embryology of one system at a time. In the first place the Bird lends itself particularly well to treatment by periods, and secondly, the simultaneous development of all the systems is what is actually seen to occur in any animal. This latter fact it would seem well to impress upon the student when possible by the method of presentation. Finally it has appeared not only possible but easier to conduct the class work in correlation with the laboratory when development is studied by periods rather than by systems. It should be noted, nevertheless, that in this book the material has been so arranged that the student can readily follow through the complete growth of any one system if the instructor so desires.

As regards the Mamxnals, it is felt that the detailed differences between the organogeny of this group and that of the Birds are not, on the. whole, of great general biological significance. Of very considerable significance, however, are those unique characteristics of both mother and embryo connected with mammalian gestation. For this reason the discussion in this portion of the text is confined chiefly to the earlier developinental stages, which are treated largely from the comparative standpoint. The subject is introduced by a description of the structure and functions of the adult reproduetige organs in the,same manner as in the case of preceding forms. This involves the process of ovulation, and in that connection it has seemed worth while to describe briefly the peculiar cyclic phenomena which accompany this process in the mammalian female. Following this, the comparative idea is pursued with particular reference to the development of the extra-embryonic z1ppt’ll(l£lgC.‘.‘~. This is believed to be especially important from an evolutionary viewpoint because it shows how these appendages, already observed in the Chick. have been modified in the various Mammals. This discussion is naturally accompanied by a description of the structure and probable evolution of the placenta. For the general plan of treatmom of these latter topics the author frankly acknowledges his indebtedness to Professor Jenl<inson’s excellent book, Vertebrate Embryology.

Concerning bibliographical material, references to the more important literature of each subject are appended to the chapter which concludes consideration of the topic in question. As intimated, it will be quite obvious that these references make no pretense of being exhaustive. Their object is rather merely to point the way to further study for the reader who desires it. This is done, first, because the present volume is intended primarily as a text rather than as a book of reference, and, secondly, because it is felt that the beginner’s interest may be more effectively aroused in this manner than by presenting to him at once every reference available. The latter, if desired, can be readily obtained in the more advanced books which are cited.

It is recognized that illustrations constitute an extremely important feature in a text of this character, and the writer has spared no pains in the attempt to make the figures adequate both in number and quality. It will be evident, however, that the majority of them are not original. This is due to the fact that through the kindness of the authors and publishers indicated below, there were made available a large number of excellent illustrations, which it seemed hardly worth while to attempt to improve upon. Nevertheless, in every instance where it was felt that such improvement was possible, or where it appeared that a new figure would be profitable, original drawings have been inserted. Lastly. it remains to be. stated in this connection that in the case of all borrowed illustrations, great care has been taken to have the illustration and the terms used in its legend agree with the respective description and terminology in the text. The desirability of this, especially in an clexnemarj.' book, is obvious; yet, according to the writer’s observation, it is a feature which is too frequently overlooked.

In conclusion I desire to express my appreciation of the following favors. To Professor Frank R. Eillie and to Henry Holt and Co., I am indebted for their generous permission to use a large number of figures from Lillie’s Development of the Chick; to Professor T. H. Morgan. his co-authors, arid Henry Holt and Co., for certain illustrations from The Mechanism of Memlelian Heredity; to Henry Holt and Co., for numerous figures from Kellicott’s General Embryology and Chordate Development; and to the Delegates and Secretary of the Clarendon Press for a like favor as regards .lenkinson’s Vertebrate Embryology. It is also a pleasure to acknowledge a similar debt to Professor Morgan and The Columbia University Press fr;-2' figures from Heredity and Sex: to Professor J. Playfair McMurrich and P. Blakiston’s Son and Co. for cliches from McMurrich’s Development of the Human Body‘; to P. Blalcistozfs Son and Co. for further clichés from Minot’s Laboratory Text Book of Embryology; to Messrs. Longmans, Green and Co. for cliches from Quain’s Anatomy; to Messrs. G. P. Putnam and Co., for permission to use again certain figures from Marshall’s Vertebrate Embryology, copied and slightly modified by Kellicott; and to Professor 0. Van der Stricht and Dr. T. W. Todd for allowing the use of photomicrographs made in the Anatomical Department of Western Reserve University Medical School from preparations presented to that department by Professor Van der Stricht. In all cases the illustrations thus borrowed are acknowledged in the legends of the figures concerned.

I wish further to express particular gratitude to Professor T. H. Morgan for reading and criticizing the first half of the manuscript; to Professor J. H. McCregor for performing a similar service for the entire hook; to Professor M. M. Metcalf for suggestions regarding the earlier chapters: to my wife for assistance with the proof; and to Pro.fessor R. C. llarrison for the identification of the frog larvae used in niaking certain of my original drawings. Especial gratitude is also felt for the constant interest and helpfulness shown by my colleagues, Professors R. A. Budington and C. G. Rogers.

R. S. MCE.

Oberlin College, August 15, 1923.



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Pages where the terms "Historic" (textbooks, papers, people, recommendations) appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms, interpretations and recommendations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)
   Vertebrate Embryology 1949: 1 Germ Cells and Amphioxus | 2 Frog | 3 Teleosts and Gymnophiona | 4 Chick | 5 Mammal | 1949 Vertebrate Embryology

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