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=Vertebrate Embryology=
 
Vertebrate Embryology  


Comprising  
Comprising  
Line 12: Line 10:
J. W. Jenkinson, M.A., D.Sc.  
J. W. Jenkinson, M.A., D.Sc.  


Lectulter In Embryology, Oxford  
Lecturer In Embryology, Oxford  


Fellow Of Exeter College  
Fellow Of Exeter College  




Oxford London:


OXFORD
LONDON:


Oxford University Press
London
Humphrey Milford Publisher to the University


UNIVERSITY PRESS
Impression of 1925
HUMPHREY MILFORD


First Edition, 1913


Jenkinson, John Wilfrid, (1871-1915)


Oxford University Press
London
Humphrey Milford Publisher to the UNIVERSITY




Impression of 1925
TO  A. A. W. HUBRECHT


First Edition, 1913
[[Media:Jenkinson1913 - Vertebrate Embryology.pdf|PDF version]]
==Preface==


The publiccation in 1885 of Francis Balfour's great treatise on Comparative Embryology marked the first attempt to establish on a scientific basis our knowledge of the development of the animal organism.




TO
Since Balfour's day embryology has travelled far, and a multitude of new discoveries has thrown fresh light on the structure, origin, maturation, and fertilization of the germ-cells, on the mechanism of segmentation, on the significance of the germinal layers, as well as on the later organogeny in the several groups.


A. A. W. HUBRECHT


But while abroad all this material has found embodiment in such comprehensive manuals as those of Oskar Hertwig on Vertebrate, and of Korschelt and Heider on Invertebrate Embryology, hardly any serious endeavour has so far been made in this country to review the fresh data or to revise or enlarge the general conclusions drawn by Balfour.




==PREFACE==
It is true, of course, that several admirable text-books of Vertebrate embryology have been issued, among which those of Milnes Marshall, of Minot in America, and of Bryce are particularly worthy of mention, but these are all directed primarily to the needs of the medical student and are consequently somewhat limited in their scope.


The publiccation in 1885 of Francis Balfour's great treatise
on Comparative Embryology marked the first attempt to establish
on a scientific basis our knowledge of the development of the
animal organism.


Since Balfour's day embryology has travelled far, and a multitude of new discoveries has thrown fresh light on the structure,
It would seem, therefore, that the hour is ripe for a re-statement of the facts and a renewed examination of the problems that they raise, and the object of the present work is to supply this want, if only for one group of animals, the Vertebrata.  
origin, maturation, and fertilization of the germ-cells, on the  
mechanism of segmentation, on the significance of the germinal
layers, as well as on the later organogeny in the several groups.  


But while abroad all this material has found embodiment in
such comprehensive manuals as those of Oskar Hertwig on
Vertebrate, and of Korschelt and Heider on Invertebrate Embryology, hardly any serious endeavour has so far been made in
this country to review the fresh data or to revise or enlarge the
general conclusions drawn by Balfour.


It is true, of course, that several admirable text-books of Vertebrate embryology have been issued, among which those of
The Vertebrates have, however, provided the material for so many investigations that much may be learnt of the general questions alluded to from them alone.  
Milnes Marshall, of Minot in America, and of Bryce are particularly worthy of mention, but these are all directed primarily
to the needs of the medical student and are consequently somewhat limited in their scope.  


It would seem, therefore, that the hour is ripe for a re-statement
But modern research has by no means been restricted to the inquiry into the first stages of development.  
of the facts and a renewed examination of the problems that
they raise, and the object of the present work is to supply this
want, if only for one group of animals, the Vertebrata.  


The Vertebrates have, however, provided the material for so
Thanks very largely to the splendid labours of Hubrecht on the structure and development of the foetal membranes and placenta of the Mammals, a flood of light has been shed on much that was previously obscure in the early history of the human embryo.  
many investigations that much may be learnt of the general
questions alluded to from them alone.  


But modern research has by no means been restricted to the
inquiry into the first stages of development.


Thanks very largely to the splendid labours of Hubrecht on
The account of the general development of the embryo is therefore followed by a discussion of these embryonic organs, a discussion which I trust may be of genuine service to the medical man. No knowledge of human ontogeny can, however, be really sound which is not based upon and seen in the light of the broad facts of comparative embryology, and I hope that the earlier chapters will prove of value to the student of medicine as well as to the professed zoologist.  
the structure and development of the foetal membranes and placenta of the Mammals, a flood of light has been shed on much
that was previously obscure in the early history of the human
embryo.  


The account of the general development of the embryo is
therefore followed by a discussion of these embryonic organs,
a discussion which I trust may be of genuine service to the
medical man. No knowledge of human ontogeny can, however,
be really sound which is not based upon and seen in the light of
the broad facts of comparative embryology, and I hope that the
earlier chapters will prove of value to the student of medicine
as well as to the professed zoologist.


The detailed organogeny of the Vertebrates is outside my  
The detailed organogeny of the Vertebrates is outside my present aim, and must be reserved for a future volume.  
present aim, and must be reserved for a future volume.  


The illustrations have been drawn especially for the book,
with the exception of a few taken from my Experimental
Embryology. Where the figure is a copy due acknowledgement
is made.


At the end of each chapter a list will be found of the principal
The illustrations have been drawn especially for the book, with the exception of a few taken from my Experimental Embryology. Where the figure is a copy due acknowledgement is made.  
authorities cited ; the student who desires further information
may consult the complete bibliography to be found in Oskar
Hertwig's Handbuch der Entwicklungslehre der Wirbeltiere.  


It is a pleasant duty to express my obligations to the Delegates
At the end of each chapter a list will be found of the principal authorities cited ; the student who desires further information may consult the complete bibliography to be found in Oskar Hertwig's Handbuch der Entwicklungslehre der Wirbeltiere.  
of the Clarendon Press, in particular to Sir WilUam Osier, and
to their Secretaries for the pains that have been expended m
the production of this volume.  




It is a pleasant duty to express my obligations to the Delegates of the Clarendon Press, in particular to Sir WilUam Osier, and to their Secretaries for the pains that have been expended m the production of this volume.


==CONTENTS==
==Contents==
 
PAGE


[[Book - Vertebrate Embryology (1913)_1|CHAPTER I Introduction]]
[[Book - Vertebrate Embryology (1913)_1|CHAPTER I Introduction]]
Line 133: Line 89:


[[Book - Vertebrate Embryology (1913)_9|CHAPTER IX The Placenta]]
[[Book - Vertebrate Embryology (1913)_9|CHAPTER IX The Placenta]]
INDEX OP SUBJECTS
==CHAPTER I INTRODUCTION==
Embryology is the study of the development of the individual
organism -  ^that is to say, of that long and frequently complex
series of changes whereby from a relatively simple germ there
is produced a new individual which, within the limits of ordinary
variation, is like the parents that give it birth. Development,
in other words, is the production of the form characteristic of
the species ; it is the mechanism of inheritance. The startingpoint of the process may be a single cell, \^hich is either a fertilized ovum or at any rate the product of the union of two cells,
as in all cases of sexual reproduction, or else an unfertilized
egg-cell, as in parthenogenesis. Again, the ' germ ' from which
the new organism is to arise may be a multicellular body derived
from one or more of the tissues of the parent, as in budding.
Lastly, in regeneration, or the replacement of lost parts, Avhere
a new whole form is produced over again from a part of the
original -  whether that part is large or small -  the process starts
from a multicellular and a differentiated structure.
As a matter of common practice, however, the term ' development ' is often restricted to the first of these processes, and in
the Vertebrates with the greater justification in that reproduction
by budding does not occur in the group, although regeneration
does. Neither has natural parthenogenesis ever been observed.
Reproduction, then, in Vertebrates means sexual reproduction,
and the developing individual springs from the union of two
germ-cells.
These germ -cells are the vehicles whereby the inheritable
characters of the species are handed on from one generation to
the next ; they arc the material basis of inheritance.
In the study of this process two methods are at our disposal.
Either we may content ourselves with a description of the series
of changes which the ovum passes through, or else we may add experiment to observation in the attempt to discover the causes
of each stage in the chain of events, and so of the whole. In the
present treatise we shall limit ourselves to the former of these
two inquiries.
In every development there are involved three kinds of
activity -  growth, cell-division, and differentiation.
Growth is increase of size, more properly of mass.
Cell-division, preceded always by karyokinetic division of the
nucleus, is the first, or nearly the first, sign the fertilized ovum
gives of its activity, and continues throughout the period of
development, indeed throughout life itself, though at a diminishing rate.
But these are, relatively speaking, side issues. The problem
about which interest really centres is the problem of differentiation, or increase of structure. The egg has indeed a structure,
but that structure is not the structure of the parent that produced it, nor of the offspring to which it will give rise. It is
more simple, and in development structure is increased, the
simple gives way to the complex.
The process takes place in a series of stages which follow upon
one another in regular order and with increasing complexity.
When segmentation has been accomplished certain sets of cells,
the germ-layers, become separated from one another. Each
germ-layer contains within itself the material for the formation
of a definite set of organs-  the endoderm, for instance, contams
the material for the alimentary tract and its derivatives-giUsHts, lungs, liver, bladder, and the like. The germ-layers are,
therefore, not ultimate but elementary organs, and, elementary
organs of the first order.
In the next stage these elementary organs become subdivided
into secondary organs-the ectoderm is portioned into epidermis,
sense-organs, and nervous system-and in subsequent stages
these again become successively broken up into organs of the
third and fourth orders, and so on, until finally the ul imate
organs and tissues are formed each with special histological
characters of its own, as seen in the arrangement, shape, aiid
size of the cells, structure of the nucleus, structure of the cytoplasm, and nature of the substances secreted by the latter, whether internally, as, for example, the contractile substance of
muscle fibres, or externally, as in the matrix of bone. This end
is, however, not necessarily reached by all the tissues at the same
time. Indeed, it is no uncommon thing for certain of them to
attain their final structure while the others are yet in a rudimentary condition. Vacuolated notochordal tissue, for instance,
is differentiated in the newly-hatched tadpole of the frog, and,
speaking generally, larval characters are developed at a very
early stage.
Regular sequence of events, then, is one of the features of
ontogeny, or the development of the individual, and another is
composition, since the organs of the body are by no means
formed of single tissues -  bone, epithelium, blood, and the rest - 
but are compounded, often of very many.
While, therefore, in the last resort all differentiation is histological, that final result, the assumption by the cells of their
definitive form, is only achieved after many changes have taken
place in the position of the parts relatively to one another while
the organs are being compounded, and so its specific shape being
conferred upon the whole body.
But manifold though the changes are that occur in the relative
position of the parts, they may all be embraced in a comparatively few general expressions, relating to the movements of
single cells, or of cell-aggregates.
I. Movements of Single Cells
Amongst movements of single cells are comprised :
1. The migration of free amoeboid cells, for example, the
lower layer cells in the blastoderm of Elasmobranchs, and the
wanderings of the germ -cells in early stages.
2. The aggregation of isolated cells :
a. Linear aggregates, as in the formation of capillaries.
b. Superficial aggregates, as in the formation of the yolk-sac
of certain Mammals.
c. Massive aggregates, as in the spleen.
3. The attachment of isolated cells to another body, as in the
union of tendon to bone, or the application of skeletal cells to
the notochord.
4. Investment and penetration by isolated cells, as in the
septa of the corpus luteum, the cells which secrete the vitreous
humour in the eye.
6. Absorption by wandering cells, as in the phagocytosis of
the tadpole's tail during metamorphosis.
6. To these we may add here the frequent movements involving merely change of shape, as when fiat cells become columnar,
or when a nerve fibre grows out from a nerve-cell.
II. Movements of Cell Aggeegates
A. Linear Aggregates
1. Growth in length, as in the back growth of the segmental
duct.
2. Splitting.
a. At the end, that is, branching, for example, of nerves,
blood-vessels, kidney-tubules, glands.
b. Throughout the length ; for instance, the segmental duct
of Elasmobranchs, the truncus arteriosus of Mammals.
3. Anastomoses, as of nerves in the formation of nerveplexuses, of capillaries, of the bile-capillaries of the liver.
4. Fusion with other organs : of a nerve, for instance, with
its end organ, of the vasa efferentia with the tubules of the
mesonephros.
B. Superficial Aggregates
, 1. Increase in area, of a curved or of a plane superficies, as
in the growth of the Mammalian blastocyst, or in that of the
auditory vesicle, or of the medullary tube, or of the blastoderm
over the yolk.
When this growth is not equal in all parts of the surface the
result is a local outgrowth or ingrowth-that is, an evagmation
as in the outgrowth of the optic vesicles, or of the cerebral
hemispheres, or an invagination, as in the formation of the
medullary groove, or of the lens of the eye.
2. Alterations of thickness, by increase, as in the formation
of the placenta from the trophoblast in MammaUa, or by decrease,
as in the roof of the thalamencephalon and medulla, or m the
outer wall of the lens.
3. Interruptions of continuity by the atrophy of part of a layer,
as in the disappearance of Rauber's cells in certain Mammalian
embryos, or in the perforation of the floor of the archenteron in
Amniota, or by the detachment of a part of the layer, as when
the notochord is lifted out of the archenteric roof in Urodela
and Petromyzon.
4. Concrescence of layers, as in the union of the embryonic
plate vnth. the trophoblast in some Mammals, where the layers
unite by their, margins, or as in the union of the medullary
folds, or of the stomodaeum with the gut, where the concrescence
is by the surfaces. In the latter case the cavities on opposite
sides of the adherent layers commonly open into one another,
as when the stomodaeum opens into the gut, or the amnion
folds unite ; but not necessarily, as when the somatopleure fuses
with the trophoblast, or the allantois with the somatopleure.
5. SpUtting of a layer into two, for example, in the inner wall
of the pineal vesicle in Lacertilia.
C. Massive Aggregates
1. Changes in volume and shape, as in the outgrowth of limbbuds.
2. Rearrangement of material, as in the formation of the
concentric corpuscles of the thymus, or in the development of
kidney tubules in the metanephric blastema of Amniota ; or
again, when internal cavities are formed, such as the segmentation cavity, lumina of ducts and blood-vessels, of the coelom ;
or, lastly, by the dispersion of the cell-elements of an aggregate,
as in the liberation of the germ-cells.
3. Division of masses, as in the metameric segmentation of
the mesoderm and neural crest, or the separation of the (solid)
nervous system from the ectoderm in Petromyzon, and Teleostei.
4. Fusion of masses, as in the union of originally separate
ganglia.
5. Attachment of one mass to another, as of sclerotome to
notochord.
Differentiation then takes place by these various movements
of cells and of cell aggregates, and by the final assumption by
the cells of the histological characters appropriate to each tissue.
The cells all arise from the continued subdivision of one original
cell, the fertilized ovum.
But while this process of division is apparently necessary for
development, it must not be supposed that it is the division
which brings about the differentiation, for the simple reason
that some differentiation already exists in the ovum before
segmentation begins. Indeed, as we shall see in the sequel, the
ovum is no homogeneous mass, but a heterogeneous body, provided with a definite structure, and this initial structure is the
real cause of the differentiations that subsequently arise. A
scientific account of development must therefore begin with the
structure of the germ-cells.
For convenience' sake, however, we may first discuss very
briefly the chief features of the phenomenon of growth.
LITERATURE
C. B. Davenpoet. Studies in morphogenesis : iv. A preliminary catalogue of the processes concerned in ontogeny. Bull. Harvard Mus. xxvii,
1896.
J. W. Jenkinson. Experimental Embryology. Oxford, 1909.
==CHAPTER II Growth==
Growth may be defined as increase in size or volume. Since
then growth is increase in all three dimensions of space, it is
most accurately measured not by increase in some one dimension -  such as stature -  but by increase of mass or weight.
Growth depends upon the intake of food and the absorption
of water, and exhibits itself in the form of increase of living
matter or 'of secretions of watery or other substances, organic
or inorganic, intra-cellular or extra-cellular, such as chondrin,
fat, mucin, calcium phosphate, and the like.
That growth depends -  in later stages at least -  upon the intake
of food is obvious. That it is due to the absorption of water
has been demonstrated effectively for the tadpoles of Amphibia
{Amblystoma, Rana, Bufo). The method employed was to weigh
known numbers of the tadpoles at different ages, desiccate and
weigh agam. The results of the investigation are shown in the
accompanying figure (Fig. 1), from which it will be seen that
the percentage of water rises with remarkable rapidity -  from
56% to 96%-  during the first fortnight after hatching. After that
point the amount of water present slightly but steadily decUnes.
In later development the proportion of water slowly falls, as
may be seen more fully from the tables following, for the chick and
for the human embryo.
Showing the percentage of water in chick embryos at various stages up
to hatching. (From Davenport, after Potts.) The table also shows the
hourly percentage increments of weight.
Table I
Hours of
brooding.
48
54
58
91
96
124
264
Absolute
weight in
grammes.
Increase.
Hourly
percentage
increment.
Percentage
of water.
0-06
0-20
0- 33
1- 20
1- 30
2- 03
6-72
0-14
013
0-87
0-10
0-73
4-69
38-3
16-0
7-9
1- 7
2- 0
1-6
83
90
88
83
68
69
59
Table II
Sliowing the percentage of water in the human embryo
up to birth. (From Davenport, after FehHng.) The
the weekly percentage increments of weight.
Absolute
weight in Increase,
grammes.
0-98
Ago in
weeks.
6
17
22
24
26
30
35
39
36-5
lOO-O
242-0
569-0
924-0
928-0
1640-0
35-52
63-5
142-0
327-0
355-0
4-0
512-0
Weekly
percentage
increment.
331-2
34-8
71-0
67-6
15-6
0-1
13-8
at various stages
table also shows
Percentage
of water.
97-5
91- 8
92- 0
89-9
86-4
83-7
82-9
74-2
fO'/,
60%
6o%
6o 70 to ;a
Days 10 iO SO *0 â– fO
Era 1 - Curve showing change in percentage of water in frog tadpoles
from the first to the eighty-fourth day after hatching. Abscis^, days ;
ordinates, percentages. (After Davenport, from Korschelt and Heider.)
There are other external factors by which growth may be
affected-  such as heat, light, and atmospheric pressure. We
cannot consider these now. We may, however, profitably turn
our attention for a moment to one feature which is characteristic of growth in general, of the growth of the animal orgamsm
under normal conditions, and that is the change that takes place
during growth in the rate of growth itself.
The rate of growth may be measured by the percentage
increments of weight (or of other measurements where weight is not available) during a given interval of time ; that is to say,
by expressing the increase in weight during a given period as
a percentage of the weight at the beginning of that period. The
change of rate, if any, is found by taking such percentage increments for successive equal increments of time.
As a first example let us consider the data furnished by Minot
for the rate of growth, after birth, of guinea-pigs.
Table III
Showing tlie change of rate of growth in male and female guinea-j)igs, as
measured by daily percentage increments of weight. (From Minot.)
Age in
days.
Mean daily per
Age in
months.
Mean daily per
centage increments.
centage increments.
i>luiiCS.
1^ em ales.
IVTa Ida
iviaieo.
emciiu!s>
0-0
2-1
Q
O
0-05
0-2
4- 0
5-6
5-5
Q
V
0-3
0-2
7-9
5-5
54
10
d.\J
0-1
0-1
10-12
4-7
4-7
11
0-04
0-1
13-15
5-0
5-0
12
0-1
0-05
16-18
4-1
4-3
13
-0-2
0-3
19-21
3-9
3>5
14
0-5
-0-03
22-24
3-1
1-7
15
0-2
0-00
25-27
2-8
1-9
16
0.07
0-2
28-30
2-8
2-6
17
-0-1
-0-02
31-33
1-9
1^8
18
-0-05
-0-2
34-36
1-7
1-6
19-21
0-006
-0-1
37-39
1-9
1-8
22-24
0-02
-0-05
40-50
1-2
1-1
55-65
1-3
1-3
70-80
1-2
0-8
85-95
0-9
0-9
100-110
0-7
0-8
115-125
0-6
0-5
130-140
0-1
0-2
145-155
0-4
-0-03
160-170
0-3
0-5
175-185
0-2
0-2
190-200
0-2
0^
An inspection of the accompanying table and figure (Fig. 2)
will show at once that there is in both sexes almost from the
moment of birth a decline in the growth-rate. The decline is
not, however, uniform.
The rate falls rapidly between about the fifth day (when
it is from 5% to 6%) and the fiftieth, from the fiftieth day
onwards more slowly, becoming eventually very small, zero or
even negative.
1355 „
18
GROWTH
II
The younger the animal, therefore, the faster it grows ;
the more developed it is the more slowly it grows. The rate of
growth, in fact, diminishes as development proceeds.
This post-natal decline in the rate of growth is a continuation
of a process which has been going on for some time, perhaps
from the first movement at which growth began.
This may be gathered from the data given for the human
embryo in Table II, and is graphically represented in the curve
For the study of the post-natal growth of man numerous data
have been collected by various observers. Quetelet's measure
aim II a 29 ssn u
Fig. 2.-Curve showing the daily percentage increments in weight of
female guinea-pigs. (From Mmot, 1907.)
ments for boys are shown in the accompanying figure (Fig. 4).
This shows that at the end of the first year after birth the percentage increment is as high as 200%, or nearly, but that then
this increment drops to just over 20% at the end of the second
year. From this point onwards the decline is slow but sure,
until at the thirtieth year the annual percentage increase is on y
0-1%. The change of rate of growth in females is practically
the same as in males. u„f„^„ w,rih
The monthly percentage increment immediately before birth
is about 20% ; according to the curve (Fig. 4) this represents
ra::ual ptentage increment of, -y, 250y a ^ ~
increase at the end of the first year is about 200 ^ The post
natal is, therefore, a continuation of the pre-natal change.
II
GROWTH
19
There are, further, two points at which the rate diminishes
with great rapidity : between the fourth and sixth months of
300%
300%
200%
Fig. 3.-  Curve showing monthly pre-natal percentage increments in man;
(From Minot, 1907.)
pregnancy and between the first and second years after birth
Elsewhere the diminution is gradual.
A point of importance is that in both sexes there is a slight
temporary rise in the growth-rate about the time of puberty Tsee
the curve). This rise is always earlier in females than in males
A comparison of the growth of these two mammals is interestmg.
A guinea-pig reaches 775 grammes in 432 days.
^ j^an » 63,000 grammes in 9,428 days.
The average percentage increments are
Guinea-pig 0-47 grammes.
Man 0-02
YEAPS , J 5 « 5 6 7 8 . - "
4.-Curve showing the yearly P-f -f.^^^^^
boys. (From Minot, 1907.)
In the human being, therefore, growth is mnch slower than
in tie guinlpig, »d 'nran is only eventually the b.gger oi the
two beeause he goe. on growing for - â„¢ch "ng^^
It is of course a commonplace of embryology s
of all the organs of ^l^e -^^^^^^^^^^^^^^
as 'senescence . ine sai there is an increase
evidence to show that during differentiation there in the camount of cytoplasm in the cell, a decrease in the size
of the nucleus, and a decrease in the rate of nuclear and cell division. It is suggested that differentiation and senescence alike
depend on an increase in the cytoplasm. During segmentation,
Fig. 5. -  Curves showing the alteration during the first twenty years
of life of the rate of growth of stature, length of head, length of vertebi'al
column, and length of leg in the human being (males). (Constructed from
Quetelet's data.) Ordinatos, percentage increments ; abscissae, years.
that is, the initial process of cleavage of the fertilized ovum,
before differentiation begins, the reverse of this occurs, for, as
we shall see later on, the essence of segmentation probably lies
in a reduction of the cytoplasmic matter relatively to the nucleus
until a definite ratio between the two is attained. Then differentiation sets in.
22 GROWTH II
LITERATURE
F. Boas. The growth of Toronto children. U.S.A. Report of the
Commissioner of Education, ii, 1897.
C. B. Davenfobt. The role of water in growth. Proc. Boston Soc. Nat.
Hist, xxviii, 1899 (1).
J. W. Jenkinson. Experimental Embryology. Oxford, 1909.
C. S. MiNOT. Senescence and rejuvenation. Journ. Phys. xii, 1891.
_ The problem of age, growth, and death. Pop. Sci. Monthly, 1907.
A. QuETELET. Anthropometric. Bruxelles, 1870.
Note - Although in the foregoing account I have adhered to Minot's method of
meSna the rate of growto by the percentage increment, I should pomt out that
T TMlonTArTEnt. Melh. xxv%xvi 1908) ^as proposed to measur^^
simnlv bv the average increment per unit of time over a short mterval of I'^e ilius
i we ca^ the magnitude measured, say the weight, at any ^°^'^^\^>J'''i f^L^
cerUin interval^of time A* suppose the weight to have increased to x+A^, then
the increment during this interval per unit of time, measures the rate. Mmot's
Ax 100
percentage increment is of course -^-j- x -  •
The eranh of the gr"wth-rate constructed by Minot's method, as t^^e .^8"^^^
given abov?descends^apidly at first, more gradually later, and so presents alikeness
Jn'jffoSmLKu'm to a maxunum -d descending t^^^
has pointed out, a rate which, as the equation
^ = Mx) (A-x)
states, depends at any moment on the ^^-^,'^^^^^^17^^^^^ If xeactd.''^'
which has still to occur (A-x) before the end-point (^) ot^^^^^ ^^^^
Robertson suggests that gi'^^h is based on che^^^^^^^^^^ accomplished, and
^ifth1t^ETasl«^^ ,
It follows from the equation just cited that the velocity jis at a maxunum when
x = when the reaction is half over, and the theory that growth takes place in this
lerved (^^) with the theoretical (f ) growth-rates, and the observed with the theo
°1tJi:fth\1q«^
^=Mx) (.A-x)
At
^^l = k{A-x),
U will be seen whv Minot's gro wtf-Lt^curve should be similar to that of a unimolecular
reaction the equation for which is
^ = UA-x).
==CHAPTER III THE GERM-CELLS==
The male and female germ-cells -  ^the spermatozoon and
ovum -  are higUy specialized structures and as different from
one anoth'er -  except in their nuclei -  as any two cells could well
be, the former being a small, active body, the latter large and
inert. But though so unlike in their completed form, they are
derived from cells which are apparently identical in the two
sexes, the primordial germ-cells.
During the development and growth of the body of the parent
which encloses them, these primordial germ-cells pass through
a series of changes, the final result of which is the formation of
the ova and spermatozoa. The history of these changes is very
similar in the male and in the female. In each case it may be
divided into three periods, a period of multiplication, a period
of rest and growth, and a period of maturation (Fig. 6).
In the male sex the primordial germ-cells divide to form small
cells, the spermogonia, which in their turn divide a large number
of times. In all these divisions the nucleus divides by karyokinesis, and the number of chromosomes formed at each division
is the same as that observed in all the tissue-cells of the body.
This somatic number is constant for any given species of animal
(or plant), and is (except in certain insects and some other forms)
an even number. We shall speak of it as 2 w.
After a time, however, these spermogonia cease dividing and
enter upon the second period of rest, during which they grow.
The growth is not very great, but quite well marked. During
this time the nucleus undergoes intricate changes which are the
prophases of the first maturation division. The male germ-cells
are now known as primary spermocytes.
At the end of the resting period the primary spermocytes prepare once more to divide. Each is halved to form two secondary
spermocytes, the nuclear division being of an altogether peculiar
24
THE GERM-CELLS
III
character, and the number of chromosomes reduced to one-half
(n) of the normal number. Each secondary spermocyte then
divides again to give rise to two equal cells, the spermatids, the
number of chromosomes being again one-half that observed in
Fig. 6. -  Diagram to illustrate the history of the germ-cells in the male
(on the left) and the female (on the right).
I. Period of multiplication (many more divisions occur than are here
represented).
II. Period of rest and growth,
III. Period of maturation. Sp.g., spermogonia ; sp.c.l, primary,
sp.c.2, secondary spermocytes ; sp., spermatids ; sp.', spermatozoa ;
o.g., oogonia ; o.c.l, primary, o.c.2, secondary oocyte; o., ovum ; ]).b.l,
first polar body; p.b.2, second polar body; p.b.1.2, halves of
first polar body. (After Wilson, after Boveri.)
the spermogonia. Each spermatid becomes directly metamorphosed into a spermatozoon, there being no further division.
In the female the primordial germ-cells divide to produce
oogonia, and these in their turn divide, the nucleus breaking
up into the full number of chromosomes (2»). When the period
Ill
THE^ GERM-CELLS
25
of multiplication has come to an entl each oogonium rests while
the nucleus passes through the prophases of the first maturation
division. The whole cell then grows into a primary oocyte.
This growth is much greater than in the male sex, since it is
during this time that the yolk is deposited in the cytoplasm to
the accompaniment of other and very complex nuclear changes.
In the third or maturation period the ovum, like the spermatozoon, undergoes two divisions, and two only ; but whereas in
the male these two divisions are equal, giving four spermatids,
eventually four spermatozoa of the same size, in the female they
are markedly unequal. The primary oocyte divides unequally
into a large cell -  the secondary oocyte -  and a small cell, the
first polar body, the number of chromosomes being reduced to n.
A second unequal division results in the production of one large
cell -  the matme ovum -  and a small cell, the second polar body ;
meanwhile the first polar body has divided (usually) into two
small cells of the same size. The number of chromosomes is
again one-half the normal number.
The parallel between these processes in the two sexes is evident,
since each primary spermocyte or oocj^e by two divisions produces four cells, each one of which possesses only one-half the
number of chromosomes seen in the spermogonial and oogonial
mitoses. While, however, in the male the four cells are all of
the same size, in the female one, the ovum, is large, while the
remainder are small.
The germ-cells are supported, invested, and nourished in the
testis and ovary by certam elements known as follicle-cells.
These, like the primordial germ-cells, appear at an early stage
in the development of the parental body, and our first duty will
be to inquire into the origin of both. We shall then be at liberty
to discuss the structure and chemical composition of the mature
sexual elements, the disposition of the protecting follicles, the
nature of the membranes by which the ovum is enclosed, the intracellular and nuclear processes accompanying the deposition of
the yolk, the nuclear phenomena involved in the reduction of the
number of the chromosomes during the two maturation divisions,
the metamorphosis of the spermatid into the spermatozoon, and
finally the union of the two germ-cells in the act of fertilization.
26
THE GERM-CELLS
III
I. The Origin of thk Germ-Cells and of the
Follicle-Cells
The gonads -  testes and ovaries -  first appear, at an early date
in the development of the embryo, in the form of what are
known as the genital ridges. The genital ridges are a pair of
longitudinal bands of tissue in the abdominal region, each placed
between the root of the mesentery of the gut on the inside and
the Wolffian body or mesonephros on the outside, and each
projecting downwards into the peritoneal cavity.
Each genital ridge is covered by the peritoneum or coelomic
epithelium, which is here usually columnar. Under this epithelium are a number of small cells which are probably derived
by proliferation from the epitheUum itseK, together with others
which come from the retro -peritoneal tissue behind. In addition
there are conspicuous certain large cells -  ^usually with large
nuclei unlike those of the surrounding cells and in many cases
with yolk-granules in the cytoplasm, derived from the yolk of
the egg from which the embryo itself has arisen. These large
cells are placed some in, some below the epithelium. They are
the primordial germ-cells, and their position in the columnar
epithelium covering the genital ridge has very nationally given
rise to the belief that they are formed by modification in situ
of the cells of that epithelium, which has hence been termed the
germinal epithelium, The researches of recent years have, however, brought forward very strong evidence to show that the
first germ-cells are not formed in or from the germinal epitheUum,
but elsewhere in the body, and that they only reach what is
to be their final, resting-place by migrating there, the source
from which they spring being in general the endoderm or splanchnopleure (mesoderm) of the gut or yolk-sac. Later on, however,
it is generally admitted that germ-cells may arise from the
germinal epithelium. This is also probably the source of the
future follicle-cells, since these are derived from the small cells
which are proliferated from that epithelium. The other small
cells, retro-peritoneal, give rise to the thecae of the follicles and
to the vascular connective tissue (stroma) olf the ovary or testis.
Let us consider a few cases.
Fig. 7. -  Primordial germ-cells in the dogfish {Sci/llium).
A, Germ-cells in the mesoderm surrounding the gut.
B, Germ-cells (g.c.) creeping up the mesentery (m.).
c. Germ-cells in the germinal epithelium (g.ep.) of the genital ridge.
The yolk-granules are beginning to disappear.
Fio. 8.-  Primordial germ-cells (r/.c.) in the tadpole of the common frog
{Rana kmpomria). A, In the mesentery (hi.) ; b, In the genital ridge.
g.ep., germinal epithelium ; f.c, follicle-cell.
Ill THE GERM-CELLS 27
In the Elasmobraiich fishes the gerni-celLs are first found in
the extra-embryonic blastoderm, either between the yolk and
the mesoderm, or under the ectoderm. Thence they migrate
into the body of the embryo by way of the yolk-stalk (Fig. 7) ;
passing up by the splanchnopleure surrounding the gut, sometimes in the gut epitheKum itself, they reach the mesentery, and
thence to right and left into the two genital ridges, where they
make their way into the epithehum. The cells are large, the
cjrtoplasm crowded with yolk -granules, which, however, are
presently digested and disappear, the nucleus large, provided
with a large nucleolus, its chromatin in the form of small granules.
The accompanying table (from Woods) gives the number found
in the unsegmented mesoderm or ventral to the mesentery, in
the mesentery, and in the genital ridges, in successively older
Number
in genital
rid"cs.
34
69
193
710
the germinal
In the lamprey {Petromyzon) the primordial germ-cells, similar
m character to those of the Elasmobranchs, first appear in the
lateral plate mesoderm, whence they migrate to their definitive
position.
So also in the trout and salmon : in these there is also a later
formation of germ-cells from the epitheUum of the ridges.
In another bony fish {Cynmtogaster) the sex-cells can be distmguished even in segmentation stages; later they are found
at the posterior end of the body (where all the germ-layers are
fused together), whence they move forwards into the mesoderm
of the genital ridges.
Amongst the Amphibia the germ-cells of the frog appear at
these cells.
Length
of embryo
Number in
Total number
of germ-cells.
unsegmented
mesoderm or
Number in
in mm.
ventral to
mesentery.
2-75
98
mesentery.
98
3-5
230
230
6-0
256
222
8-0
296
154
73
11-5
408
78
137
34-0
710
More germ-cells are
later on formed from
epithelium.
28
THE GERM-CELLS
III
an early stage, in the ncwly-hatchcd tadjiolc ; they are derived
from the large yolk-cells of the gut. Being separated off on the
dorsal side they move up the mesentery (Fig. 8), and so, passing
to the right and left, reach the genital ridges. The cells are at
first crowded with yolk, but this soon disappears ; the nuclei
are not peculiar.
Fig. 9. -  Section of a 12-clay rabbit embryo, showing the migration of
the primordial germ-cells (indicated by black dots). Most are in the yolkstalk mesoderm, some in the mesentery (m), some in the genital ridge {g.r.)
internal to the mesonephros (M). y.sl., opening of the yolk-stalk into
the yolk-sac.
It is remarkable that, in the female at any rate, many of
these young germ-cells are expelled from their follicles and disintegrate in- the peritoneal cavity. There is an extensive formation of fresh ones by modification of cells of the germinal epithelium, which is also the source from which the folUcle-cells are
derived. The theca comes from retro-peritoneal tissue. (An
account of the follicle and the theca will be found in a subsequent
section.)
When we pass to the Reptiles we find the same migration
taking place. In the tortoises {Glmjsemys) the sex-cells arise in
the endoderm of the yolk-sac posteriorly. Becoming amoeboid
B.
Fig. 10.-  Primordial gorm-cells {g.c.) in the rabbit.
A Early stac'e in the formation of the genital ndge, covered by the
germinal epithelium {g.cp.). Below this are some germ-cells and connective
tissue and blood-vessels {b.v.). Germ-cells arc also seen in the mesentery {m.).
B, A germ-cell in the epithelium of the gut.
c, One from the yolk-stalk.
D, An epithelial cell from the yolk-sac.
P. 29
Ill THE GERM-CELLS 29
they migrate towards the middle line into the embryonic region.
Passing out of the endoderm into the splanchnopleure (the
mesoderm covering the gut), they travel up the mesentery into
the ridges. Many, however, fail to reach their destination, and
remain for some time in the epithelium of the gut. It is stated
that in this animal no germ-cells are ever formed from any
other source.
In the Birds, again, the germ-cells appear early, in a chick
on the third day of incubation. They seem- to originate from the
splanchnopleure of the yolk-sac, and pass, in the way already
described, to the genital ridges, and there into the germinal
epithelium. By the fifth day the migration is complete and the
cells begin once more to multiply.
In all these cases the identification of the primordial germcells is considerably facilitated by their retention of yolk-granules
at a time when these bodies have disappeared from the surrounding cells.
In the (placental) Mammals, however, where there is practically
no yolk, the distinction of these cells from the surrounding elements is a matter of some difficulty, and it has been, and is still
contended, that the germinal epithelium is their only place of
origin. Nevertheless, there is good reason for believing that the
Mammalia are no exception to the general rule.
In a rabbit embryo of eleven or twelve days (Figs. 9, 10) there
are to be found in the splanchjiopleure of the yolk-stalk large
numbers of rounded cells, distinguishable from the surrounding
cells by their cytoplasm-  which includes large oxyphile granules
- and their nuclei, which are round and large, with a fine achromatic reticulum bearing small granules of chromatin. The nuclei
consequently look pale. There is one, sometimes more, large
nucleolus. In all these respects the cells bear a close resemblance
to the large cells in the endodermal yolk-sac epithelium (Fig. 10 d).
Precisely similar cells may be found in the body of the embryoround the sides of the gut, and sometimes in the gut epithelium
in the mesentery, and finally below and in the columnar epithelmm (germinal epithelium) internal to the mesoncphros which
IS the beginning of the genital ridge. In earlier stages the same
ceils are found in increasingly smaller numbers in the genital
30
THE GERM-CELLS
III
ridges and mesentery, in increasingly larger numbers in the yolkstalk and endoderm. It can hardly be doubted, therefore, that
the same migration of these cells from the yolk-sac to the genital
ridges is occurring here as we have already observed in other
forms. There is equally little doubt that these cells, arrived at
the genital ridges, become germ-cells.
In the rabbit embryo of twelve days the genital ridge (Fig.
10 a) is very slight, consisting of a band of columnar epithelium,
below which are a few cells derived probably by immigration
Fig. 11. -  Ovary of rabbit fiom embryos of a, 18 days, and B, 21 days,
showing formation of cortex (G) and medulla, b.v., blood-vessels in
stroma {str.) of medulla ; md.c, medullary cords.
from that epithelium. These cells differ from the germ-cells
amongst which they lie in their nuclei -  which are oval in shape,
have more than one nucleolus, and a more open reticulum with
coarser granules of chromatin, and are of smaller size -  and in
their cytoplasm -  which includes no granules. Those which lie
below the surface are destined to give rise to the follicle-cells,
which will eventually be disposed in layers round the germ-cells.
Deeper still are connective tissue-cells and blood-capillaries
derived from the retro-peritoneal tissue ; from these will come
the thecae and the vascular stroma. Let us follow the development of this genital ridge into the sexual organ, and first into
the ovary.
The whole genital ridge is enlarged and made to project into
P.31
Ill
THE GERM-CELLS
31
the body-cavity by the increase of the connective tissue elements
and blood-vessels, or stroma, which thus forms a central core
or medulla to the whole organ. At the same time, by continued
proliferation of the germinal epithelium at the surface, an external
layer or cortex is formed. The germ-cells lie mainly in this
cortex, but a few -  those presumably which in migrating to the
genital ridge have never reached the surface -  lie in the stroma,
where they are grouped in rows known as medullary cords
(Figs. 11 A, 12 a). They seem to degenerate.
The cortex increases in thickness and becomes divided up into
columns or blocks by the ingrowth of vascular connective tissue
from the stroma. These columns -  ^which were at one time
believed to be produced by hollow invaginations of the germinal
epithelium and known as the epithelial tubes of Pfliiger -  are the
sex-cords (Figs. 11 b, 12 b). They consist of folHcle-cells derived
in all probability from the germinal epithelium, and of germ-cells
which have migrated into then- present position from their
source, the yolk-sac." The germ-cells have been increasing in
numbers : in the resting condition their nuclei present the same
characters as before. The cytoplasm, however, loses the oxyphile
granules. At about the twenty-second day the germ-cells cease
to divide and enter on the period of rest : they are in fact
primary oocytes, and their nuclei begin to undergo the changes
characteristic of the prophases of the first maturation division.
This mode of origin of the germ-cells does not of course preclude the formation of others from the cells of the sex-cords,
that is, from the germinal epithelium, and it is Indeed quite
possible that this occurs.
In the mouse and other Mammals (guinea-pig, mole, cat) the
germ-cells appear to come from a similar source. In the mouse
they are large cells with rounded bodies, dense, rather deeplystaining cytoplasm, and large nuclei, with a close reticulum,
small, scattered chromatin granules and one or two large nucleoli
(Fig. 13 A). They divide by mitosis for a time, but pass into
the resting condition at a comparatively early date, about the
fifteenth day (Fig. 1 3 B, c). They He intermingled with a number
of cells, the future follicle-cells, which may be regarded as of
epithehal origin. The meduUa of the ovary is formed late
32
THE GERM-CELLS
in
(Fig. 13 e), when the nuclei of the germ-cells have already
reached the pachytene ^ condition (see below), by ingrowth of
connective tissue from the base ; prior to this the whole thickness of the organ is composed of follicle-cells and germ-cells,
with but a few capillary blood-vessels. The sex-cords (' tubes ')
of the cortex arise, therefore, not so much by downgrowths of
epithehum as by rearrangement of the cortical, that is, foUicle
and germinal, and medullary, that is, stroma cells (Fig. 13*).
B
C
â– p-rp 13* _A B, Formation of medulla in ovary of mouse. sir
stroma of medulla; md.c, medullary eords; c, cortex of gerra-cells and
^''Sestisof embryo mouse, ep., eoelomie epithelium ; L, seminiferous
tubules.
A few germ-cells are found in the medulla, but as in the
rabbit, these probably never become mature. When the gerincell nuclei have reached the diplotenic or dictyate stage (J^ig.
13 F) (in the new-born animal) the formation of folUcles begnis,
by the grouping of the follicle-cells round the oocj^es, to form
a single flat layer. At the same time the oocytes enlarge. These
two processes always occur first at the deep end of the sex-cords.
Later (Fig. 14) the cells of the follicle become cubical, and then
increase in number till several layers are formed. Hence the
X A full explanation of this tern, will be found in the section of the next
chapter deahng with maturation.
Ill
THE GERM-CELLS
33
cortex of the young ovary comes to comprise several layers of
small oocjrtes, each surrounded by a single layer of flat cells
under the surface, and larger oocytes, surrounded by cubical
foUicle-cells, disposed in the more advanced deeper down in
Fig. 14.-  Part of cortex of ovary of young mouse (8 davs) In the
deeper parts the foUieles (/. 3) consist of two- or three-cell layeS" and Se
oocytes are arge. In the middle layers the follicles (/. 2) areTntlayered
but the cells are cubical, the oocytes smaUer. Under the s^SfaTe the
oocytes are smaUer still and the follicle-cell flat (/. 1). ep surf^e enithe
lium (germinal epithelium) ; h.v., blood-vessel ; strl\tfo^T,Z tW
many layers. It is not, therefore, that the folHcles and oocytes
enlarge as they pass in from their (supposed) origin at the surface
but that those which are inmost are the first to enlarge The
oocytes of the outermost layer often lie practically in the epithehum at this stage. Their nuclei, however, are not in the
condition seen in newly-formed germ-cells (oogonia), but in
the dictyate stage characteristic of oocytes
1355 _
34 THE GERM-CELLS m
In the male (Figs. 13 Bo^, 13* c) the sex-cords become early
shut ofi from the suiiace epithehum (peritoneum) by the formation of a sheet of comxective tissue [iunim albuginm), and from
one another in the same way. The sex-cords are the rudiments
of the seminiferous tubules of the testis. Each consists of an
outer layer of foUicle-cells, and an inner mass of germ-cells,
presenting the characters already described. These are spermogonia and divide mitoticaUy many times. Intermmgled wi h
Lm are a few of the folUcle-cells. In this sex there seems to
be no doubt that many of the first-formed g-m-cells d^^^^^^^^
and that in the adult fresh spermogoma are difierentiated from
"Lfy"on of the germ from the body or somatic "
ee^thet first appearance in a part of the body remote from,
^iCr gradualmigrationto their ^f^^f^^^
eesses which find a parallel in many, if not m aU, groups ot tne
aSmal ldngdom. Thus in the Hydroid Coelenterates, the germ
on xo become medusae or gono
tLrir^s Sgr^LX often pass foxward. and backphores. In tins migi<^t j round-worm
waxds from one 87;7„V ;t:eUs is distinguishable
Ascaris the parent cell ol tne g ^ t^e
"y --'-^ ^S^t^-  n C,!o,s. In
segmentmg oTum. Similaily â„¢ ^^Me
Oephalopod Moltaca and in S<=°:^P ^/^^^ i^cts
during the formation of the ^eâ„¢-' ^appearance
they may be -P--"f ^j'^^Cre^Ue difierLiation
of the blastoderm-or rather later, ^^e
the germ-layers or ater ^J^.^y ^o^Hged to migrate
mesoderm, and m aU these oases J j ^^i^^.
forwards into their ^f^Z::::Z ^ n Z from the germinal
saos ; lastly, they may be drfferent ^^^^
epitheUum of the ^j'-^^ ^ere we y,,,,^,,^, either
the double origm which we have .^^ subsequent
at an early date, independently °' ^ aate, from
migration into the f f no hard-and-fast
the germinal epithehum itself. It is clear
Ill
THE GERM-CELLS
35
rule can be laid down. All the germ-cells may be precociously
separated from the somatic cells and elsewhere than in the
generative organ, or some may have such an origin, while others
arise in the generative organ itself, or lastly, all may be developed
by the second method, as appears to be the case in most Annelid
worms and in Ascidians.
Nor need the conversion of what look like tissue-cells into cells
endued with the capacity of reproducing all the characters of the
species cause any particular astonishment when the widespread
capacity for regenerating lost parts possessed by the adult
tissues, and the remarkable facts of bud-reproduction, are borne
in mind. In these cases germ-plasm or reproductive substance
must be present in the regenerating or budding tissues, and yet
there is no obvious continuity between this germ-plasm and that
of the germ-cell from which the regenerating or budding individual
sprang ; as little should we expect to find a demonstrable continuity in the case of sexual reproduction.
II. The Structure of the Mature Germ-cells
A. The Ovum
The egg-cell is large and inert : it is quite incapable of locomotion ; only occasionally does it exhibit peristaltic contractile
movements, as in the formation of the polar rings at the time of
fertilization in Annelids, or slow changes of shape as in the
protrusion of the animal ends of the blastomeres in Petromyzon,
or the flattening at the animal pole of the frog's egg prior to
segmentation.
In shape it is nearly always spherical : exceptionally, as in
Myxinoids and Amia, ellipsoid or ovoid.
Size of the ovum. The ovum is always a large cell compared
to other cells of the body, even where, as in Placental Mammals,
it is actually very small, and it may be very large indeed, as in
the large-yolked ova of most fishes, and of birds and reptiles.
The size of the ovum is due to the contained reserve food material
or yolk, the amount of which varies very greatly in the different
groups.
O 2
36
THE GERM-CELLS
III
A small-yolked (microlecithal) egg is found in the lamprey
(Peiromyzon) and in the Anurous and Urodelous Amphibia. In
the frog the diameter of the ovum is about 1-6 mm. In the
Gymnophiona, and most 'Ganoid' fishes {Acipenser, Amia,
Lepidosteus), there is more yolk in the egg, while in the Myxinoid
Cyclostomes, Elasmobranch and Teleostean Fishes, Reptiles,
Birds, and Monotrematous Mammals, the egg is large-yolked
(megalecithal). Finally, in the Placental Mammals-  which are
descended fiom large-yolked forms-  the yolk has been reduced
to a very small amount.
The following table brings out the contrast between the size
of the eggs in the large-yolked Monotremes and the smallyolked other forms. It will be seen that amongst the latter
the Marsupials have the largest ovum. In this respect, as m
others, they are intermediate between the Monotremata and
the PlacentaUa.
Monotremata
MarsupiaUa :
PlacentaUa :
Echidna
Ornithorhynchus
Dasyurus
Didelphys
Canis
Homo
Lepus
Ovis
Talpa
Cavia
Erinacells
Mus
3-4 mm.
2-5 mm.
0-28 mm.
0-13 mm.
0-18 mm.
017 mm.
015 mm.
0-15 mm.
0 09 mm.
0-08 mm.
0 06 mm.
0 06 mm.
The yolk. The yolk is frequently termed deutoplasm m distinction from the living substance or protoplasm m which it hes.
ir s Losited in the cytopl-m of the ovum during the period
o ^oXh t the form of smaU bodies spoken of a. granules,
g ofls or platelets (Fig. 15). The size, shape, and structure
Ill
THE GERM-CELLS
37
of these vary. In the lamprey, frogs and toads, newts and
salamanders, the granules are oval or ellipsoid bodies, sometimes
vacuolated. In the Elasmobranch fishes they are oval plates,
sometimes spherical and vacuolated. In the Teleostean fishes
the separate yolk-globules run together at an early stage to form
one continuous yolk-mass. In the Birds there is white yolk and
yellow yolk, the former consisting of small globules enclosing
still smaller ones of varying size, while the latter is made up of
Fig. 15.-  Yolk-gvanules. a, Dogfish, b, Axolotl, the smaller from
the anmial, the larger from the vegetative hemisphere, c, White volk.
D, yellow yolk, from the Hen's egg.
larger spheres, each including a multitude of minute droplets.
In both kinds of yolk the smaller bodies are often set free by the
rupture of the larger enclosing envelopes. In the Placental
Mammals the yolk-granules are usually globular (Fig. 18, b).
All the granules which have been mentioned are protein in
nature, but in addition to these fat globules are not uncommon.
Fat is present in the hen's egg, in some Mammalia (guinea-pig)
(Fig. 18, c), while in the Teleostei a single large oil-drop is
characteristically present (Fig. 72).
The chemical composition of the yolk of a hen's egg is as
follows. The yolk-  that is, the ovum-  weighs from 12 to 18
38
grammes
include
THE GERM-CELLS IH
47-2 % of this is water ; the remaining solids
Protein .
Salts .
Fats
Lecithin
Cholesterin
15-63 %
0- 964 %
22-84 %
10-7 %
1- 75 %
51-884 %
The proteins include ovo-vitellin (for the greater part) and
some albumin.
The former is not a globulin but a nucleo-proteid ; on digestion
with pepsin it yields an iron-containing body, a pseudo-nuclein
known as haematogen, since it is supposed that it is the source
of the haemoglobin of the embryonic blood corpuscles. With
the ovo-viteUin the lecithin of the egg is closely associated. The
fats are oleates, palmitates. and stearates. With them must be
included certain phosphatides.
The salts are chlorides of sodium, potassium, magnesium, and
calcium. , . • i a
The reaction of the yolk is alkaline. The colouring is due to
lutein, a lipochrome. , . ,
Other ova have not been so fully investigated, but it is known
that the ichthulin of certain fish eggs (carp, cod) is a nucleoproteid, and lecithin (6 %) and nucleo-proteid (94 %) can be
demonstrated in the yolk of the frog's egg. The significance of
the presence of nucleo-proteids will be more evident when we
consider later on the part played by the nucleus during the
deposition of the yolk.
The yolk of the Monotreme egg is of a yellow colour, in
the lamprey it is a faint yellow, in the dogfish greenish, in the
Ganoid fish Amia brown. In Placental Mammals the yolk is
colourless. ,
The yolk is not scattered Irregularly through the cytoplasm,
but arranged in a very definite fashion, known as the telolecithal ;
that is to say, while the cytoplasm (or protoplasm) is concentrated
on one side of the egg, the yolk (or deutoplasm) is conceiitrated
on the opposite side. This does not imply, of course, that all
in
THE GERM-CELLS
39
the yolk is on one side, all the protoplasm on the other side,
but that most of the cytoplasm is on the one, with fewer and
smaller yolk-granules, while on the other the yolk-granules are
more abimdant and larger, with less cytoplasm in between them.
The transition from one extreme to the other in a small-yolked
egg such as that of an Amphibian is quite gradual (Fig. 16) :
there is a graded diminution in the concentration of cytoplasm,
A
I
Fig. 16. -  Diagram of a meridional section through a full-grown oocyte
of the frog. The yolk-granules are represented by stippUng, the pigment
by the thin black line. The arrow marks the egg-axis, its head the animal
pole.
an increase in the concentration of the yolk in passing from one
side to the other.
As the yolk increases the distinction between protoplasmic
and deutoplasmic portions becomes more and more marked, until
the limit is reached in the megalecithal type. Here the amount
of yolk is so enormous that the cytoplasm is reduced to a small
cap or disc-  the blastodisc-  at one side, the bulk of the ovum
being occupied by the yolk (Fig. 17). Yet eVen here small yolkgranules are found in the blastodisc, and the transition from
blastodisc to yolk is not absolutely abrupt.
In the Placental Mammals the telolecithal arrangement of the
yolk can stiU be seen, in spite of the small amount, at least when
40
THE GERM-CELLS
III
the nucleus, with some cytoplasm, goes to the surface just before
maturation (Fig. 18).
In the ovum of the Marsupial Dasyurus (Fig. 18, a) the yolkglobules run together at this time to form a single rounded
mass -  the yolk-body -  placed on the opposite side to the nucleus.
In the ova of Birds (Fig. 17) the white yolk is disposed in the
form of a central plug -  the latebra -  under the blastodisc. This
is surrounded by successive layers of yellow and white yolk,
alternately. The same feature is observable in the ova of
Reptiles, Gymnophiona, Amphibia, and Elasmobranch fishes,
where sheets of coarse and fine granules alternate.
The telolecithal disposition of the yolk confers upon the Vertebrate ovum a very definite structure and symmetry. In most
cases the ovum is a sphere, and it is evident that a line may be
drawn passing through the centre of the protoplasmic portion,
at the surface, the centre of the egg, and the centre of the deutoplasmic portion at the opposite surface. This line is the egg-axis,
and it is clear that its two ends, or poles, are unlike. The former,
the protoplasmic, is known as the animal pole, the latter as the
vegetative pole. These terms took their origin in the observation
that in such an egg as that of the hen the chick or animal is
developed from the blastodisc, at the side opposite to the inert
or vegetative yolk.
From what has akeady been said it further foHows that the
yolk and protoplasm are distributed about this axis in such
a way that the egg would be divided into precisely similar halves
by any section which included the axis, but by none other.
Hence the egg is said to possess a polarity and a radial symmetry
about the axis. In any one plane at right angles to the egg-axis
all radii are alike. The plane at right angles to the axis and
including the centre of the egg is equatorial.
In cases where the egg is ovoid or elUpsoid (Myxinoids, Aima)
the egg-axis is the major axis.
Yolk is heavier than protoplasm. Hence the Amphibian egg
which, after fertilization, is free to rotate inside its jeUy membranes, always turns over till its axis is vertical with the white,
vegetative pole below. The fuU-gromi ovarian egg-whether
alive or dead-behaves in the same way when floated m a fluid
I
kl.
I.
VJ/l
I^ct 17 - Hen's longitudinally biRected. (After Balfour, modified.)
The section includes" the axis of the ovum, the animal pole bemg to the
upper side of the figure, sli., shell, underneath it the external shellmembrane ; i.m., internal shell-membrane ; a.di., au' chamber ; c7i., chaiaza ;
hi blastodisc ; I., latebra of white yolk ; v.m., vitelline membrane.
Between iO and i 1
B. 3 C.
Fig. 18. -  Mammalian ova.
A, Dasijurus (a Marsupial). 1, The ovarian egg (oocyte) ; the nucleus
is near the surface at the animal pole ; the cytoplasm contains spherules
of jo\k. 2, The second maturation division. The first polar body has
been extruded, and the second polar spindle is seen. The yolk-spherules
have run together to form the yolk- body [y.h.) placed at the vegetative
pole. (After Hill.)
B, A ha,t [Vesferiilio). Both polar bodies have been extruded and
fertilization is taking place. The two pronuclei are seen. In the cytoplasm
are numerous globules of yolk (protein). (After Van Beneden.)
c, The guinea-pig (Cavia). Full-grown oocyte. In the cytoplasm are
mitochondria (cln'oraatic bodies) and fat globules (the former are black,
the latter clear in the figure). (After Lams and Doorne. ) z. , zona pellucida.
Ill
THE GERM-CELLS
41
of the same specific gravity as itself. Similarly the ovum
(yolk) of the hen's egg always turns over inside the shell till the
blastodise is uppermost. So in Elasmobranchs.
Pigment. The polarity and radial symmetry thus conferred
upon the egg by distribution of the yolk may be further emphasized by the disposition of the pigment where that is present
apart from the colouring matter of the yolk itself. In many
Amphibia (Anura and Urodela), in Ceratodus and Acipenser, pigment is present in the egg. The dark brown, almost black
pigment of the frog's egg will be familiar. Chemically it is
a melanin. In other cases {Siredon, for example, and the edible
frog) it is of a much lighter colour.
The pigment lies (Fig. 16), in the form of minute droplets, in
a dense superficial layer in the animal hemisphere of the egg,
extending a greater or less distance into the vegetative hemisphere. There is left round the vegetative pole as a centre
a circular unpigmented area. The symmetry of the egg, as
determined by the position of the yolk, coincides with that due
to the distribution of the pigment. There is also a less dense
mass internally in the animal hemisphere.
The Nucleus. The nucleus -  germinal vesicle -  of the fullgrown oocj^e is characterized by the presence of one (Placental
Mammals) or more nucleoli, usually chromatic. The history of
these nucleoli and of other parts of the nucleus wiU be dealt
with later. What interests us at the moment is the position of
the nucleus. This is always in the axis of the egg, but excentric
(Fig. 16), and always nearer the animal than the vegetative
pole. In a microlecithal egg the nucleus lies in the protoplasmic
portion, in. a megalecithal egg in the blastodise (Fig. 17). It is
placed, therefore, in what is termed, in Oskar Hertwig's first
rule, the centre of its field of activity. The importance of this
will be appreciated when we come to the study of the phenomena
of segmentation.
Structure and symmetry of the ovum. It will be obvious from
the foregoing that the egg is no homogeneous body, but heterogeneous with a definite polar structure -  radially symmetrical
about an axis determined conjointly by the disposition of the
yolk, the distribution of the pigment, when that is present, and
42
THE GERM-CELLS
HI
the position of the nucleus. The first two characters are purely
cytoplasmic. The significance of this initial structure of the
/
2
Fig. 19.-0vary of the tadpole, showing development of the ovarian
cavity (o.c.) and numerous germ-cells in diSerent stag^ 1 ^Wntene
with the nuclei in different conditions. 1, Earliest stage ; 2, bynaptene
Tpachvtene 4 Diplotene ; 5, Formation of nucleoli. The largest oocytes
L sSnded by f ofiicles. ep.', coelomic epithelium (germmal epithehum).
egg cytoplasm in development cannot be over-estimated, for it
is related in a perfectly definite way to the structure of the
embryo which will come from it. Thus, to take one example.
um.
Fig. 20. -  Small ovarian egg of the frog surrounded by Its follicle (/.) and
theca {ill.), which is continued into the pedicle (^.). h.v., a blood-vessel
between follicle and theca ; v.m., vitelline membrane ; dr., chromatin
filaments, now aclu-omatic ; n., chromatic nucleoli, ejected from the
nucleus in' .\ and becoming achromatic (54".).
n
^ -Liu ''
A
r
'J
-O.
-th.
B.
Fig. 21. -  a, young, and b. older oocytes from the pigeon's ovary.
r'^T cytoplasm of the oocyte; v.m., vitelline membrane;
/., follicle ; Ih., theca.
P. 12
CO
ill
8
Ill • THE GERM-CELLS 43
the anterior end of the embryo is developed always near the
animal pole of the frog's egg, the egg-axis making a certain
constant angle with the longitudinal axis of the embryo ; or,
in other words, the anterior and posterior regions of the embryo
are predetermined in the structure of the egg.
That the relation is a necessary and causal one is shown by
those experiments-  performed on the eggs of various animals - 
in which, some one part of the cyioplasm being removed, some
definite organ of the embryo or larva is lacking. The different
portions of the egg cytoplasm are therefore so many organforming substances, and since the organs are part of the sum
total of the inheritable characters of the species, the cytoplasmic
substances, on which their development depends, are factors
determinant of inheritance.
The egg-follicle. In the ovary the egg-cell is invested by one
or more layers of follicle-cells, the function of which is not only
to protect, but also to nourish, the growing oocyte. These are
derived, as we have seen, from the germinal epithehum of the
genital ridge. The follicle in its turn is surrounded by a theca
of flattened connective tissue-cells.
In the Amphibia there is but one layer of cells in the follicle ;
they are flat. The ovary is hollow (Pig. 19), and the theca cells
are continued into the stalk by which each ovum is suspended
to the wall of the ovarian cavity (Fig. 20). Between theca and
foUicle there are blood-vessels.
In the Elasmobranchs and Birds (Fig. 21) there is but one
cell-layer in the young follicle, but the number is subsequently
increased to two or more. The cells are cubical or polyhedral
in shape.
Li the Monotreraata the number of cell-layers is only one or
two, but in all other Mammals (Fig. 22) it is greatly increased, and
a cavity filled with an albuminous fluid -  the liquor foUicuh -  is
developed in between the cells, thus leading to the development
of the characteristic hollow Graafian follicle. The cavity appears
first on one side of the ovum as a narrow crescentic sUt ; soon
this enlarges and extends round the ovum, which is then attached
to the wall of the cavity only by a short stalk-  the so-called
discus prohgerus. On its free side a few layers of follicle-cells remain adherent to it, the cumulus proligorus. Finally, by the
further extension of the cavity, the stalk is ruptured and the
ovum, with its corona of cells, floats freely in the folUcular
cavity. The ripe foUicle, which has now returned from the deep
parts to the surface of the ovary, bursts, and the ovum, with
its corona, is expelled and passes into the mouth of the oviduct
(Fig. 43) to be fertilized.
The expulsion of the ovum is known as ovulation. In multiparous Mammals several are, of course, expelled at the same time
and from both ovaries.
Fto 22 - Part of the cortex of an adult mouse ovary. </./., cavity of
JSaSan follicle ;/.,fomck^
proligerus ; ej)., surface (coelomic) epithelium ; th., theca , b.v., Dlooa
vessel.
After ovulation the foUicle collapses, but it does not immediately degenerate. It becomes altered mto a corpus luteum.
The foUicle-cells divide for some little time, and then, ceasmg
to do so, hypertrophy (Fig. 23). They secrete fat and lutem
(to which the corpus luteum owes its yeUow colour). Amongst
these enlarged folUcle-cells grow vascular strands from the mnermost layer of the theca. The theca cells, which mcrea.e m
numbers by division, are fusiform, and. lymg obliquely, or
tangentially, or radially, iii the follicle, divide up the luteal
tissue into ii-regular blocks. The larger strands contain blood vessels. There is a central cavity filled with stellate cells and
extravasated blood corpuscles.
It has been shown that the corpus luteum secretes a substance
which passes into the blood, and by that channel reaches the
wall of the uterus, Avhere it appears to be necessary for the
proper attachment of the embryo by means of the placenta.
Fig. 23.-  Marginal portion of a section through the corpus luteum of
a mouse 14 days after parturition (i.e. after ovulation). /., hypertrophied
follicle-cells ; s., septa of connective-tissue cells ; th., theca ; b.v., blood vessels.
The membranes of the ovum. These may be of three kinds,
primary, secondary, and tertiary. A primary membrane is one
secreted by the cytoplasm of the egg itself; a secondary,
one secreted by the follicle-cells and often termed ' chorion ' ;
while tertiary membranes (albumen, shell) are secreted by the
epithehum of the oviduct as the egg passes to the exterior.
The ovum of Vertebrates is always immediately surrounded
by a vitelline membrane, frequently termed a zona pellucida
(Figs. 16, 17, 18, 20, 21). This membrane may be traversed by fine radial pores, by nieans of which nutrient material passes
from the folhcle -cells to the ovum : it is then spoken of as a
zona radiata.
It is a matter of great difficulty in most cases to determine
whether the vitelline membrane is primary or secondary, but
it is stated that there is a membrane secreted by the ovum
itself, inside another secreted by the folhcle -cells, in most forms
(Elasmobranch fishes. Amphibia, Reptiles, Birds). The radial
striations of the uuier primary membrane disappear before the
ovum is full grown. The viteUine membrane of the ripe egg
is possibly the result of the fusion of both the primary and
secondary membranes of an early stage.
The so-called ' chorion ' of Teleostei and the Ganoid Lepidosteus, a very thick membrane, is apparently primary. In it
the radial striations are persistent. The Myxinoids, however,
possess a true chorion which is provided, at the animal pole,
with a number of hooks, by which the egg is attached. In
Petromyzon, Teleostei, and Lepidosteus, the vitelhne membrane
is perforated by a passage at the animal pole through which the
spermatozoon enters. This is the micropyle.
In Mammals (Marsupiaha and PlacentaUa) there is much
uncertainty as to the origm of the vitelline membrane. It varies
a good deal in thickness, and is not generaUy radiate unless thick.
It is a zona radiata in the rabbit (Fig. 60), mole, pig, and sheep.
ChemicaUy the vitelline membrane (of Birds) is an albummoid
alhed to keratin.
The tertiary membranes are secreted by the oviduct. The
innermost of these is the albumen, white of egg, or jelly. This
is found in Elasmobranch fishes, Amphibia, Tortoises, and Crocodiles but not Snakes and Lizards, Ends (Fig. 17), Monotremata,
Marsupials (Fig. 68), and sometimes in Placental Mammals
(rabbit). .
The white of the hen's egg is wound round the ovum m layers,
spiraUy arranged. The layers are separated from one another
by a thin but tough membrane, the albumen in between successive membranes being fluid. Owing to the rotation of he
egg as it passes down the oviduct these layers are spiraUy tw^ted
up into cords (the chalazae) on two opposite sides. The chalazae
5/1 77!.
23*.- Section tliroTigh the shell of the egg of the ostrich Cafter
VAaldeyer, after Konigsborn). c, cuticle ; sp., spongy layer of stratified
snbstance pierced by canals, which open internally between the bases of
the conical processes of the mammillarv layer {m.) sJi.m., shell-membrane. are always placed iii the equator of the ovum so that the blastodisc is midway between them, and they lie in the long axis of
the egg-shell.
The white of the egg, which has an alkaUne reaction, contauis
85-88 % water
10-13 % protein
0-7 % salts
0-5 % . . . • • dextrose
and traces of fats, soaps, lecithin, cholesterin, and lutein (to
which the faint yellow colour is due).
The proteins are ovo-globulin (6-7 %), ovo-albumin (a mixture
of at least two proteins), and ovo-mucoid.
The salts are sodium and potassium chloride, phosphates, and
salts of calcium, magnesium, and iron.
In some birds (Insessores) the egg-white does not become
opaque on boiling, but gives a transparent jelly, similar to
alkali albuminate.
In Fishes and Amphibia the egg-white is a jelly, composed
of mucin.
A shell is present, outside the egg-white, in Elasmobranch
jfishes. Birds (Fig. 17) and Reptiles, Monotremata, and some
Marsupials (Fig. 68).
In the fishes referred to the shell is horny and attached by
tendril-like strings to some foreign body. It is composed of
keratin.
In Birds and most Reptiles the outer layer of the shell is calcified, the iimer layer being then known as the sheU-membrane.
Calcification, however, does not occiu: in some cases (Lacerta
vivipara). The shell-membrane is made up of a network of
fibriUae of keratin.
The calcareous layer consists -  in a Bird's egg -  of three sheets
(Fig. 23*) : an outer dehcate porous cuticle, a middle spongy
sheet, and an inner mamnullary sheet of columns whose conical
ends impinge upon the sheU-membrane.
The shell contains 3-7 % of organic matter (keratin), 90 % of
calcium carbonate, and small quantities of magnesium carbonate
and earthy phosphates.
The colour of the shell is due to bile-pigments. In the
hen's egg the shell-membrane is separable into two sheets :
between these two air collects at the blunt end of the shell
after the beginning of incubation, so forming the air-chamber.
This air is for the chick to breathe just before hatching
(Pigs. 17, 121).
The Monotremes possess a shell which in Ornithorhynchus is
calcified.
Amongst Marsupials a horny shell is present in Dasyurus and
Phascolarctos. In Placentaha the shell is invariably absent.
B. The Spermatozoon
In striking contrast to the large inert egg-cell, the spermatozoon is a smaU, actively-moymg body, capable of swimming
towards and enteruig the ovum in fertiUzation.
While there is great variety in the form of the animal spermatozoon, two principal types may be recognized, the flageUate or
tailed, and the tailless.
The Vertebrate spermatozoon is flagellate. It consists typically
of two parts, a head and a tail (Fig. 24).
In the head there is at the anterior end the acrosome or
perforatorium, used in perforating the surface of the ovum,
and behmd this the nucleus. The nucleus is always dense and
homogeneous, and highly chromatic.
The tail consists of an axial filament and a cytoplasmic
envelope. Centrosomes are always present in it. Three
portions may be recognized : an anterior part including the
centrosomes ; this is the pars conjunctionis ; a middle part,
pars principalis, as far as the end of the cytoplasmic envelope
of the taU ; and a pars' terminalis, in which the axial filament
is naked. -v *
The axial filament (probably the seat of the contractihty of
the tail) runs throughout the length of the tail. Anteriorly it
termmates m the most anterior centrosome-  referred to sometimes as the end-knob-placed immediately behmd, or even
embedded m, the nucleus. Behind this are one or more other
centrosomes.
The cytoplasmic envelope of the tail extends from the
front end of the first to the hmd end of the second region.
In the third region only the axial filament is present.
The small part interposed between
the head and the tail, that is, between
the hind end of the nucleus and the
front end of the axial filament, and
. containing only the anterior centre some, is sometimes spoken of as the
neck, or middle piece. This usage
cannot be justified in all cases, as the
axial filament may pass right through
the anterior centrosome to the nucleus
(as in the Amphibian Discoglossus) .
The term should therefore be dropped,
or apphed to the anterior region of the
tail, including aU the centrosomes
Though always of the flagellate type,
the form of the Vertebrate spermatozoon is variable. Thus, to take a
few illustrations (Figs. 25, 26), the
acrosome may be large and flattened
(spoon-shaped) as in the guinea-pig,
or, as is more usual, narrow and
pointed (some Amphibia, Reptiles,
and Elasmobranch fishes), or much
reduced {Phalangista), or apparently
absent (Teleostean fishes, possibly
Bu-ds). Whether it is really absent
or not can, however, only be stated
when the origin of the spermatozoon
from the spermatid has been studied
in these forms. In Birds there is often
a remarkable spirally-coiled membrane
round the head.
The nucleus may be short and rounded (Teleostei), or short
and flat (guinea-pig), or cuneiform (Phalangista), or oval
T5
Fig. 24.-  Diagram of a
typical vertebrate spermatozoon. H., head; a., acrosome ; n., nucleus ; T, tail;
T.l, pars conjunctionis ;
T.2, pars principalis ;
T.3, pars terminalis; a.c,
anterior centrosome ; p.c,
posterior centrosome ; /,
axial filament ; c, cytoplasm ; e., envelope.
{Tropidonotus), or pointed and elongated, sometimes
exces
1355
50
THE GERM-CELLS
III
sively (Urodela). The anterior
end-knob, single (Fig. 25, 2, 3,
25, 1), or much enlarged, as in
centrosome may be a small
4, Fig. 26) or multiple (Fig.
Urodeles especially. In Bom
17ra 2^5 -Various spermatozoa. 1. Guinea-pig (Cama) (after Meves).
4. FringUla (the chaffinch). (3 and 4 after Ballowitz.)
binator (a toad) its position near the anterior end of the
nucleus is remarkable. The tail filament xs mser ted, there
fore, near the front end of the head m this form Thexe
ma; be (Pnalangista) one or more intermedxate es.
The posterior one, at the end of the first portion of the^d,
and therefore some way back, is frequently rmg- ox dxsc
Ill THE GERM-CELLS 51
shaped. Iii Urodeles it lies very far back indeed. The cytoplasm of the anterior region often presents transverse or spiral
Fig. 26. -  ^Various spermatozoa. 1. Bufo (the toad) (after King). 2.
Bomhinator (a toad) (after Broman). 3. Siredon (the Axolotl). 4. Perca
(perch). 5. Eaia (skate). (4 and 6 after Ballowitz.)
markings. In the anterior and middle regions (or in the middle
region only) the cytoplasm is frequently in the form of a fin,
which may have a thickened undulating border, or be spirally
coiled round the axial filament.
Spermatozoa also vary very greatly in length, as the following
D 2
62 THE GERM-CELLS III
table will show. The lengths are given in thousandths of a
millimetre.
Crocodilus 20-27
Esox 43
Homo 52-62
Boa 66
Bufo 62-91
Erinacells ..... 85
Cavia . . . . . 93
IIus 107
Eaia 215
Siredon 360-^30
Discoglossus .... 2250
The gigantic spermatozoa of the Amphibian which comes last
in the Hst are not, it is hardly necessary to say, proportionately
broad. It may be added that even this length is exceeded
by the spermatozoa of an Ostracod Crustacean, Pontocypris
monstrosa, which are 5-7 millimetres long.
The Chemistry of the Spermatozoon. The most accurate determinations of the chemical composition of the spermatozoon are
those carried out on fish sperms.
In the salmon the head (nucleus) of the sperm consists of fat
and nuclein and other substances. The nuclem is itself a compound of nucleic acid (C.^ H^g N^^ 0,J with a protamine known
as salmm (C30 Hg^ N,^ 0^), the proportions bemg roughly 60%
and 35 % respectively of the head, after removal of the fat.
The remaining 5 % consists of inorganic matter (Ca3(P04)2,
CaSO^) 2-5%, and an iron-containing organic material (the
remainder).
In the herring the protamine known as clupein is apparently
the same ; scombrin (mackerel) and sturin (sturgeon) are other
protamines obtained from the sperm-heads of fishes.
The tail, in the salmon, contains heat coagulable proteids to
the extent of 42 %, and fatty substances, 58 %. The latter
include lecithin (50 %), fat (30 %), and cholesterin (20 %).
The metamorphosis of the spermatid into the spermatozoon. As
has already been stated, four small cells, the spermatids, are produced from each primary spermocyto by the two maturation
divisions. Each spermatid is then directly metamorphosed into
a spermatozoon.
Fig. 27.-  Metamorphosis of the spermatid into the spermatozoon in the
salamander (after Meves) 1-6, the whole cell ; 7-9, the anterior end;
10-ld, the posterior end of the head. (For explanation see text. )
The investigation of thjs process in many forms, including
several Vertebrates, has shown that there is a remarkable constancy in the changes that take place. One or two examples
will suffice.
As a first, let us take the salamander (Fig. 27). The spermatid,
emergmg from the second maturation division, is a rounded cell, in which the chromosomes are clumped together while the centrosome, lying in the middle of the centrosphere or sphere of attraction (Idiozom), has divided into two, placed tangentially with
regard to the surface of the cell (Fig. 27, 1). While the nuclear
membrane is being formed round the chromosomes, the centroeomes detach themselves from the sphere (Fig. 27, 2) and adopt
a radial position. When the chromosomes break up into granules,
a fine filament-  the axial filament of the tail-  grows out from
the centrosome nearest the surface (Fig. 27, 3). This is the
posterior centrosome, and it soon becomes first discoidal, then
ring-shaped, the axial filament passing through the ring to attach
itself to the other or anterior centrosome (Fig. 27, 4). Meanwhfie
the sphere-  in which a spherical vacuole has been developed - 
moves away from the centrosomes to the opposite side of the
nucleus, which is of course the anterior end (Fig. 27, 4-6). Here
it becomes gradually changed into the acrosome or perforatorium. It becomes oval and an axial rod is formed in it. It is
protruded from the cell, becomes pointed, and finaUy much
elongated and barbed at its extremity, while the vacuole disappears (Fig. 27, 7-9). At the other, the posterior end of the
cell, further changes are taking place. The anterior centrosome
first attaches itself to the hinder end of the nucleus (Fig. 27, 5)- 
now elongated and finely granular-  then enlarges and embeds
itself in the nucleus (Fig. 27, 6), finally lengthening to form
a long eUipsoid body. The axial filament has remained inserted
into Tt (Fig. 27, 10). In the meantime, an outgrowth of cytoplasm has occurred on one side (dorsal) of the tail filament to
form the fin (Fig. 27, 10). When the fin is weU developed, the
posterior ring-shaped centrosome breaks into two halves. One
half travels down the other (ventral) side of the tail, carrying
some cytoplasm with it, and eventuaUy reaches a point near
the end of the middle region (pars principaHs). The other
haK remains behind and is fused with the anterior centrosome
(Fig. 27, 11-13). The nucleus continues to elongate to form the
sperm-head, finally becomes homogeneous, and is divested of
its cytoplasmic covering.
The history of the sperm in other types, the gumea-pig for
instance, is almost the same (Fig. 28).
Ill THE GERM-CELLS
In the spermatid can be seen the sphere-  including some dark
granules-  the chromatoid accessory body, and the two centrosomes (Fig. 28, 1). These are dumb-boll-shaped, the outer or
Fig. 28. -  ^Metamorphosis of the spermatid into the spermatozoon in
the guinea-pig (after Meves). 1-4 show the whole cell; 5-9 the head and
the front part of the tail ; 9 is seen in profile. In 1 the accessory chromatoid body is rendered in black. In this and the following figures the sphere
is shaded or (acrosome) stippled. In 6 and 7 the granules of von Ebner
are shown in black. (A full explanation will be found in the text.)
posterior is placed radially and bears the axial filament, the
inner tangentially.
The chromatoid body disappears. The sphere moves round
to what will be the anterior end ; in it two portions are
56 THE GERM-CELLS III
distinguishable. A spherical body with a dense central spherule,
this is derived from the dark granules of the previous stage, and
an irregular body applied to the first, derived from the outer
portion of the original sphere. This irregular body presently
moves back to the hind end and disappears, but the spherical
part becomes transformed into the acrosome (Fig. 28, 2-4). It
is applied to the front end of the nucleus, and becomes lenticular
(concavo-convex) (Fig. 28, 5). The central dense body then
vanishes, the whole projects from the front end of the cell, being
attached to the front and sides of the nucleus. Finally it becomes
thin and curved (spoon-shaped) (Fig. 28, 9). The nucleus meanwhile having become homogeneous is also flattened and curved,
its curvature being opposite to that of the acrosome.
The centrosomes have aU this time been passing through
comphcated changes. The anterior one becomes flattened against
the nucleus, the posterior hook-shaped, one hmb of the hookdirected outwards-  bears the tail filament, while the other, or
anterior Kmb, is at right angles to it (Fig. 28, 2).
The hinder limb of the posterior centrosome now becomes
divided into a ring behind and a knob in front (Fig. 28, 4). The
tail filament passes through the ring, on to the Imob, and then
on to the middle of the anterior Hmb. The anterior centrosome
and the anterior Hmb of the posterior centrosome then become
divided, each into three knobs (Fig. 28, 5). The arrangement
is therefore as foUows. A row of three knobs united by filaments
next the nucleus ; each of these knobs being similarly united
to one of the three knobs of the next row, also united together.
The middle knob of the second row is miited to another knob,
and into this is inserted the axial filament of the taU which
passes through the ring. Later the ring passes backwards some
Httle way; it marks the end of the first region of the tail
(Fig. 28, The tail filament thickens, the posterior knob
being fused with it. . . -i i '
A curious, quite transitory, structure is the tail-sleeve
^Fie 28 4 5) This is a felt-work of fibriUae developed round
the froni end of the filament to form a sort of tube. Its existence
is short. Most of the cytoplasm-which has by this time passed
away from the nucleus to the middle -piece-is peeled off (Fig. 28,
ih
Fig. 29. -  Sperm-cells of Amphibia in tlieir cysts or follicles.
A, Section of a single seminiferous tubule from the immature part of the
testis of a newt (in winter). The spermogonia [^sp.g.) are enclosed ni follicles (/".c.) ; the theca surrounding the tubule, -ex
B, "Bundle of ripe spermatozoa inside a cyst (c), from the testis of tbe
Azo'lotl. B.C., Sertoli-cell in which the acrosomes of the spermatozoa are
embedded.
P. 57
Ill
THE GERM-CELLS
67
6, 7), with the remains of the sphere and a number of stainable
bodies -  the granules of von Ebner -  which always appear at this
time. The remains of the cytoplasm form a sheath round the
middle-piece (pars conjunctionis), and apparently a thin investment for the principal part of the tail. In the middle-piece the
characteristic transverse (? annular) striations appear (Fig. 28,
8, 9).
These examples are tj^ical of spermogenesis in general. The
acrosome is formed from the sphere, the tail filament grows out
from the centrosome ; and even where (as in many Crustacea)
the tail is absent, the two centrosomes are still present, and the
posterior one becomes transformed into a ring.
The close relation between the locomotory organ of the cell
and the centrosome is not peculiar to spermatozoa. In certain
Protozoa there is a central corpuscle which not only -acts as
an organ of cell-division, but also serves as a base of insertion
for the flagella or for the axial filaments of the pseudopodia
{Dimorpha, Acanihocystis).
The centrosome of the spermatozoon and the sphere -  which
becomes the acrosome -  are both parts of the original division
apparatus. They have, however, distinct functions to perform
in fertihzation, for while the latter is the perforatorium, employed
for ensuring the penetration of the sperm below the surface of
the egg, the latter is the centre round which the primary spermsphere is formed. We shall see, nevertheless, that these distinct
processes probably depend upon a property which is common
to both bodies, and may be due to their community of origin.
The follick-cells of the testis. Like the ova, the male cells are
associated with certain nutrient cells in the testis, known also
as foUicle-cells, though they do not always form a covering for
the germ-cells. Their origin from the germinal epitheUum has
already been referred to.
In the lower Vertebrates the germ-cells commonly occur in
bundles, each of which is enclosed in a wrapping of folKcle -cells,
a cyst, or foUicIe. The cysts are arranged round the walls of
the seminiferous tubules. In the immature tubules of the testis
the cysts will be found to be small, each containing only one or
two spermogonia (Fig. 29 a). But the number of the latter is
58
THE GERM-CELLS
III
soon moreased by division, and quantities of germ-cells are
subsequently found in each single cyst. In each cyst all the
germ-cells are usually in the same stage-  whether spermogonia,
spermocytes, spermatids, or spermatozoa, complete or incomplete- but in the different cysts in the same tubule different
stages are found, though they are not usually very widely
different in adjacent cysts (Fig. 30).
Fig 30 -Four cysts or follicles from the same seminiferous tubule of
the testis of the Axolotl. 1, contains spermatids ; 2, 3 and 4, three successive stages of the metamorphosis of the spermatid into the spermatozoon.
/., foUicle ; b.v., blood-vessel outside the tubule.
The mature spermatozoa become arranged in bmidles, and
inserted, in each bundle, by their acrosomes into a smgle basal
cell of the cyst (Fig. 29 b), facing the wall of the tubule. The
cyst which has been much distended, then gives way, and the
tails of the sperms project freely into the lumen of the tubule.
The basal cells in which the heads of the spermatozoa are
embedded are apparently nutrient as well as supportmg. They
are known as the cells of Sertoh, a term first apphed to the
corresponding cells of the Mammahan testis.
In the Mammaha the germ-cells are also grouped m bundles.
Pia 31 - Testis of mouse. A small part of a section tlu-ongh a seminiferouV tubule in six different conditions {a-f) 1-20 stages in spermogeneiis (for further explanation see text). 8., Sertoli-cell ; th., theca.
P. 59
Ill THE GERM-CELLS 69
but are not enclosed in cysts ; further, they are disposed in
several layers, and different stages in development are found in
the several layers at one and the same point in a seminiferous
tubule (Fig. 31).
The basal layer contains the supporting cells or cells of Sertoh,
which (in the mouse) are recognizable by the presence in the
nuclei of one large nucleolus and two large spherules of chromatin.
In addition to these there are the spermogonia (indifferent cells),
which are derived , either from the central cells of the young testis
(see Fig. 13) or from the surrounding follicle-cells, or from both.
Internal to this basal layer are about three others, in each of
which the germ-cells are in a different stage. For the sake of
illustration the whole spermogenesis may be divided into twenty
stages, as follows :
1. Indifferent cell or spermogonium.
2. Transition to spermocyte.
3. Primary spermocyte : leptotene stage.
4. Transition to synaptene stage.
5. Advanced synaptene.
6. Pachytene,
7. Pachytene to diplotene.
8. Later diplotene.
9. Commencement of ring-formation.
10. Ring-shaped (heterotypic) chromosomes formed.
11. First matviration division.
12. Secondary spermocytes.
13. Second maturation division.
14. Spermatids.
15. Later spermatids.
16.
17. Commenciag metamorphosis, with short tail filament.
18. Later stage.
19. Appearance of von Ebner's granules.
20. Peeling off of cytoplasm ; spermatozoon complete.
Beginning with, for example, a stage in which the spermogonia
of the basal layer are in stage 1, the cells of the second layer m
the fourth,, those of the third layer iii the tenth, and those of the
fourth layer in the sixteenth stage, the progress of development
60
THE GERM-CELLS
III
in each layer may bo readily watched. As layer ii passes into
stage 5, layer in shows first maturation spindles, while the
spermatids of the fourth layer begin to be metamorphosed into
spermatozoa, and so on. By the time that the spermatozoa of
the fourth (inmost) layer are ripe and ready to drop into the
tubule, the cells of the third layer have reached the spermatid
stage ; those of the second are in a late prophase of the first
maturation division, whUe the somewhat flattened spermogonia
of the basal layer are becoming cubical and preparing to grow
into spermocyiies. By the time the ripe sperms have been thrown
off, the young spermocytes have detached themselves from the
basal layer and he in a distinct second layer below the third
and fourth layers, which are respectively in the ninth and
fifteenth stages, and so the starting-point is reached once more.
The germ-cells, therefore, originating in the basal layer, are
brought nearer and nearer the lumen of the tubule as the ripe
sperms of the inner layer are cast ofE and fresh layers formed
from below. As the spermatids undergo their metamorphosis,
they become grouped into bundles ; and, in each bundle, the
spermatozoa are inserted by their acrosomes into the extremity
of an elongated Sertoh cell, which is retracted once more when
the spermatozoa have been set free. The tails, therefore, float
out into the seminiferous tubulev
The ovum and the spermatozoon are obviously different from
one another in almost every respect. The former is large, inert,
and, when fully ripe, as we are shortly to see, without a centrosome. It is rich in cytoplasm, contams reserve food material,
arid has a structure, related in a very definite way to the structure of the embryo which is to be developed from it.
The spermatozoon, on the other hand, is motile and small,
has httle cytoplasm (except hi the tail, which is of no importance
in fertiUzation, smce it may be left outside the egg) but is provided with one or more centrosomes, as well as with an apparatus
for entering the ovum.
We have still to examme the structure of the nuclei of the
germ-cells, a structure which is the result of the pecuhar nuclear
changes mvolved m maturation. This exammation will show us
that in their nuclei the germ-cells are alike.
LITERATURE
B. M. Allen. The origin of the sex-cells of Chrysemys. Anal. Am. xxix,
1906.
E. Ballowitz. Untersuchungen uber die Struktur der Spermatozoen.
L Arch. mikr. Ami. xxxii, 1888. III. Arch. mikr. Anal, xxxvi, 1890.
E. Ballowitz. Die merkwiirdigen, 2\ Millimeter langen Spermien des
Batrachiers Discoglossus pictus. Arch. mikr. Anal. Ixiii, 1904.
J. Beard. The germ-cells. Journ. Anal, and Phys. xxxviii, 1904.
E. VAN Beneden et C. Julin. Observations sur la maturation de
I'cellf chez les Chiropteres. Arch, de Biol, i, 1880.
U. Bbm. Beitrage zur Entwickelungsgeschiehte der Leibeshohle und der
Genitalanlage bei den Salmoniden. Morph. Jahrb. xxxii, 1904.
I. Beoman. Ueber Bau und Entwickelung der Spermien von Bomhinator
igneus. Anal. Anz. xvii, 1900.
R. BuRLiN. Chemie der Spermatozoen. Ergebn. Physiol, v, 1906.
C. A. EiGENMANN. On the precocious segregation of the sex-cells in
Micrometry aggregatus. Journ. Morph. v, 1891.
0. Hammaesten. Text-book of Physiological Chemistry, trans, by J. A.
Mandel. New York, 1911.
H. D. King. The egg of Bufo lentiginosus. Journ. Morph. xvii.
K. VON KoRFF. Zur Histogenese der Spermien von Phalangisla vulpina.
Arch. mikr. Anal. Ix, 1902.
E. KoKSCHBLT u. K. Heider. Vergleichende Entwickelungsgeschiehte
der wkbellosen Thiere. Allg. Th., Lief. L ii, Jena, 1902.
H. Lams et J. Doorme. Nouvelles recherches sur la maturation et la
f6condation de I'cellf des Mammiferes. Arch, de Biol, xxiii, 1908.
F. McClendon. On the nucleo-albumin in the yolk-platelets of the
frog's egg. Amer. Journ. Phys. xxv, 1909.
F. Meves. Ueber Struktur und Histogenese der Samenfaden von
Salamandra. Arch. mikr. Anal. 1, 1897.
F. Meves. Ueber Struktur und Histogenese der Samenfaden des Meerschweinchens. Arch. mikr. Anal, liv, 1899.
W. Rubaschkin. Ueber das erste Auftreten und Migration der KeimzeUen bei Vogelembryonen. Anal. Hefte, l^e Abt., xxxv, 1908.
W. RuBASCHKiN. Ueber die UrgeschlechtzeUen ' bei Saugetieren
Anal. Hefte, I'e Abt., xxxix, 1909.
J. SOBOTTA Ueber die Entstehung des Corpus luteum der Saugethiere.
Aiiat. Hefte, 2'^ Abt., viii, 1899.
O VAN DER Stricht. La structure de I'cellf des Mammiferes. Arch,
de Btol. XXI, 1905.
W. Waldeyer. Die Geschlechtzellen, in 0. Hertwig, Handhuch der
JLnlwicklungslehre der Wirheltiere. Jena, 1906.
1902 ^^^"""^"^"^^l^P^^nt and inheritance. New York.
vZ'JrZ '''T^^''- ^^'^^'^^^^ I'ovogen^se et I'organogendse de
1 ovaire des Mammiferes. Arch, de Biol, yiyn, \mi
CHAPTER IV THE GERM-CELLS {continued)
III. The Maturation of the Germ-cells
A. In the male.
The Urodelous Amphibia have always been a favourite object
for the study of these changes, and may conveniently be taken
by us as a type.
It AviU be recalled that duriag the spermogonial divisions the
full somatic number of chromosomes is seen. The mitosis is of
the ordmary character (Fig. 32). The granules of chromatm
increase, run together m the form of beaded rows, which become
the V-shaped chromosomes. The nuclear membrane has m the
meantime broken down, the centrosome has divided, and around
each daughter centrosome an aster is appearmg. The chromosomes then undergo longitudmal fission and, so spht, are placed
on the equator of the spmdle now developed between the two
centrosomes. The daughter chromosones are then puUed apart
by the spmdle-fibres attached to them to the opposite spmdle
poles, and there passmg through the same series of changes in
the reverse order become the daughter nuclei. Meanwhile a celldivision has occurred m the equatorial plane of the spmdle, m
which process the mtermediate bodies-thickenings of the spmdle
fibres-  play an important part.
AU the features of an ordmary mitosis are here : the chromatm
is the only part of the nucleus to be divided ; for that purpose it is thrown mto the form of chromosomes, which ^ht
lengthways mdependently of any external agency , a divis on
a^tatuLasters and sphidle-is ^onst^f^^/^^^ f^e
centrosomes and probably by them, the function of -^^^f^ '^
puU apart the halves of the aheady divided chromosomes and to
LL?the division of the cell. When the W--/^^ceased dividing they enter upon a
time the nucleus passes through complex changes, ^vhlch are m
IV THE GERM-CELLS 63
reaUty the prophases of the fost of the two maturation divisions.
This first division is of a very different character to an ordinary
mitosis. There ensues the second division. This, with one
important exception, resembles the mitoses of the spermogonia.
« 2 3
Fig. 32. -  Stages in the karyokinetic division of the spermogonia
of the newt.
The first maturation division (Figs. 33, 34). In the nucleus of
a spermogonium the chromatin is in the form of fairly coarse
lumps uniformly distributed over a wide achromatic reticulum.
As the growth of the cell and its nucleus begin the chromatin
becomes subdivided mto finer granules, which soon arrange
themselves m rows or filaments ; in each row the granules are
64
THE GERM-CELLS
IV
connected by threads of the achromatic reticulum, while similar
threads pass from one filament to another. This is the narrow
thread or leptotene'^ stage. As the nucleus enlarges still more
Fig. 33.-  Prophases of the heterotype division in the male Axolotl.
1, Nucleus of spermogonium or young spermocyte ; 2, Early leptotene ;
3, Transition to synaptene; 4, Synaptene with the double filaments converging towards the centrosome ; 5, Contraction figure ; 6, 7, Pachytene ;
8, Early, 9, Later diplotene ; 10, The heterotypic double chromosomes ; the
nuclear membrane is disappearing.
it is seen that on one side some of the filaments are arranged
in pairs, and converge towards one point, the point where the
centrosome m its centrosphere is placed. On the other side of
1 These and the followmg terms were first proposed by von Winiwarter
in his classical work on the oogenesis of the rabbit.
IV
THE GERM-CELLS
65
the nucleus the filaments pass into the general network. This
is the paired thread or synaptene stage.
By coalescence of the component granules the filaments become
shorter and thicker : at the same time in each pair the filaments
approach one another so closely that only a narrow slit is left
between them. On one side the pairs of filaments still converge
towards the centrosome, but on the other are inextricably coiled
Fig. 34. -  ^First maturation division in the male. 2, Salamander, the
remainder Axolotl. 1, 2, The heterotypic chromosomes on the spindle
(metaphase) ; 3, Anaphase ; 4, 5, Telophase ; 6, Resting nuclei ; 4-6, Celldivision into two secondary spermocytes.
and tangled together into a bunch which is withdrawn some
little way from the nuclear membrane. The pairing of the filaments can, however, be seen in the tangle. The several pairs
are still imited by achromatic threads, the filaments being
toothed at each point of insertion of such a thread. A few
threads stretch across the empty space between the tangle and
the membrane. This is the contraction figure.
The members of each pair of filaments now unite throughout
their length, so that the longitudinal sHt disappears. The thick
filaments still converge towards the centrosome side, where
66
THE GERM-CELLS
IV
apparently they end against the nuclear membrane. There is,
therefore, not one continuous filament or spireme, but several.
The other ends of the filaments pass into the tangle, which is
still retracted from the nuclear membrane, but becoming looser
as the nucleus enlarges. The coil is soon still more unravelled
and occupies the whole of its side of the nucleus. This is the
pachytene stage.
The several filaments now separate from one another, so that
the polar convergence is lost, and coil in various directions
through the nucleus. At the same time the longitudinal sUt
reappears in each, and the filaments are once more paired, so
reaching the diplotene condition. Their surfaces are still toothed
where the connecting achromatic threads are inserted. Soon,
however, these cross threads disappear and the filaments become
smooth. At the same time the members of the several pairs
begin to separate a little from one another, in places if not
throughout their length.
The nuclear membrane now breaks down and disappears, the
pairs of filaments shorten and thicken, and assume the most
various shapes and sizes. A pair may be in the form of
two straight parallel rods, or two curved parallel rods, either
V-shaped, or C -shaped, or two rods parallel at one, divergent at
the other extremity, and so -||--shaped ; or the sht between
them may be expanded in two or more places, and then the two
may be tAvisted over one another mto a figure of g or or by
expansion of the whole sht, while the rods are united at the
ends, may be ring-shaped, while finally the ring may be pushed
in in four places and assume the form of a cross, =[}:. These
bizarre double bodies are the chromosomes of the first maturation division. It seems clear that they are derived from the
separate paired filaments of the diplotene stage, these from the
thick filaments of the pachytene stage, and these again from
the paired filaments of the synaptene nucleus. The origm of
these we shall have to discuss later on.
The number of the double chromosomes, and therefore of
the several double filaments in the earUer diplotene, pachytene,
and synaptene stages, is one-haK that seen in the spermogoma.
The reduction from the somatic number {2n) to the germ
IV
THE GERM-CELLS
67
number (n) has already taken place. It seems that this half
number must be estabhshed in the synaptene nucleus.
The actual division now occurs (Fig. 34). A spindle is formed
in the ordinary way, and the double chromosomes are thrown
upon its equator in such a way that the two ends of each member
of a pair he in the equatorial plane. This is easily seen where
the pair retains the original form of two closely-parallel rods
separated by a longitudinal slit, and can often be made out in
the ring- and cross-shaped and other chromosomes.
The members of the pairs now come apart and travel to
opposite spindle poles, where they coalesce and pass into the
condition of resting nuclei. The cell, meanwhile, has divided
and the two secondary spermocytes have been formed. The
nucleus of each of these, it is clear, contains only one -half of the
ordinary number of chromosomes.
The division which we have just witnessed is unlike an ordinary
mitosis in at least two respects. First, the number of chromosomes is reduced from the somatic to the germ number, and
second, the chromosomes are double and frequently of extraordinary shape. For these reasons the division is spoken of as
heterotypic, or xmlike the usual type. The term meiotic or
reducing, also appHed to it, refers to the numerical lessening of
the chromosomes.
We have now to inquire whether this division is or is not like
an ordinary mitosis in another respect, the manner ia which the
chromosomes are divided. Ordinarily, as we know, the chromosomes are longitudinally divided ; but on this occasion it is held
by many observers that the division, albeit in appearance longitudinal, is in reahty transverse.
The uiterpretation of the nuclear changes is a matter of considerable difficulty, and very diverse opinions are entertained
(1) as to the origin of the double filaments seen in the synaptene
and later stages of the prophase, and (2) as to the mode of formation of the ring-shaped chromosomes seen in the actual mitosis ;
different combination of these diverse opinions has led to the
formulation of three principal views.
I. It is held that (I) the double filaments of the synaptene
stage arise by longitudinal fission of the filament, that the
£ 2
68
THE GERM -CELLS
IV
longitudinal split disappears, but reappears (2) to form the cavity
of the rings. Hence the actual division is longitudinal (Meves).
This is illustrated in the accompanying diagram (Fig. 35, I).
For the sake of simpUcity we will suppose that the full number
of chi'omosomes is four, the reduced number two. We will further
I
II
UI
Fio. 35.-Diagram to iUustrate three interpretations of the first matoasee text.)
suppose ttot these four chromosomes are really diff^^'
Tne another though apparently identical. Let us caU them
7 A' B, and B: In the prophase of the mitosis two mstead
of' four filaments appear. We may suppose that each of th«a
consists of two ordinary chromosomes muted end to end say
aTo 4' and B to B'. Each filament becomes then spht lengthwa^ll 1). the sHt widens out untU each filament assumes
IV THE GERM-CELLS 69
a ling shape (I, 2), and the rings are then so placed on the equator
of the spindle that the ends of the chromosomes lie in the equator
(I, 3). Hence, smce each half ring consists of an A and an A',
or of a 5 and a jB', when the halves are separated and travel
towards the spindle poles, each daughter nucleus of a secondary
spermocyte will receive a chromosome of each kind, A, A',
B, and B'.
II. On the second view (von Winiwarter, Schreiner, Agar),
(1) while the paired filaments of the sjmaptene stage are believed
to arise, not by longitudinal fission of the leptotene, but by
apposition of distinct chromatin filaments (that is, chromosomes),
the formation (2) of the rings from these double ' filaments is in
accordance with the first view.
The diagram (Fig. 35, II, 1) shows the four chromosomes
united in pairs by their entire length, though presenting every
appearance of longitudinally spht rods : A is paired with A', and
B with B'. The chromosomes of each pair then separate to form
rings, remaining united only by their ends, and then are placed
on the spindle ua such a way that these ends lie in the equator.
It follows that A and B face towards one. A' and B' towards
the opposite pole, and hence that each nucleus of a secondary
spermocyte receives not all tour chromosomes, but only two,
say A and B, ov A' and B'.
The division, therefore, is not really but only apparently
longitudinal : the result is the same as though A and A' (and
B and B') had been united end to end, and then separated by
a transverse division of the double chromosome so formed.
III. On the third view (Farmer, Montgomery), (1) the double
thread of the synaptene and pachytene is formed by the longitudinal sphtting of the chromatm filament ; but (2) the rings
do not arise by the opening out of the spUt. The longitudmal
division disappears, and the filament is first gathered up into
half as many loops as there are chromosomes in the spermogonia, and these loops then separate as the n ring-shaped chi omosomes. The rings are therefore open at one end only, and the
cavity of the ring arises, not by the opening out of the longitudinal split (for that has disappeared), but by the bending of
the two halves, united end to end, of each double chromosome
70
THE GERM-CELLS
IV
upon one another (Fig. 36, III). That is, the filament, consisting
of Aj A', B, and B', is first gathered up into two loops, A being
bent on A', and B on B', and then the loops separate. In the
mitosis (III, 3) the rings are so placed on the spindle that A
becomes separated from A' and B from B', so that one secondary
spermocyte receives A and B, the other A' and B' (or, of course,
A and B', A' and B).
FiQ. 36.-  Second maturation division in the male (Axolotl). 1, Prophase
(split spireme); 2, The homoeotypic spht chromosomes on the spindle;
3, Polar view of the same ; 4, Anaphase ; 5, Telophase ; 6, Resting nuclei
and completion of cell-division ; in each spermatid the centrosome has
divided, and the sphere has become detached.
The result is therefore the same as on the second hypothesis.
Considering the diversity of opinion, it would be rash to
dogmatize, but it may be pointed out that the evidence on the
whole is agamst the mode of formation of the rings adopted by
the third view. It does seem as though the rings were made
by the opening out of the double filaments. We are left, therefore, with the choice between the first and second hypotheses.
We can only say that the way in which the members of the
pairs of filaments diverge into the general network in the fourth
stage (Fig. 33, 4) suggests apposition rather than fission, and
this involves ultimately a transverse division of double chromosomes, and that the phenomena of maturation observed in
a number of Invertebrate forms corroborate this view.
Before discussing the theoretical significance of this mode of
division, we shall describe the second maturation division (Fig. 36).
The nucleus of the secondary spermocyte soon emerges from
the resting condition, and a chromatic filament appears. This
filament becomes longitudinally split and then divided into
a number of V-shaped chromosomes, themselves therefore split
lengthways. The number of chromosomes is the half somatic, n.
A spindle is developed, the spht chromosomes are placed on its
equator, and division takes its ordinary course, resulting in two
spermatids, the nucleus of each of which therefore possesses
n chromosomes. La the V-shape of the chromosomes, as well
as in their longitudinal division, this second mitosis is of the
ordinary type. Hence it is called homoeotypic. Each spermatid
becomes metamorphosed into a spermatozoon in the fashion
already described.
The phenomena of maturation in the male are, as far as is
known, similar in other forms {Myxine, Elasmobranchs, Mammaha). Each ripe male cell, therefore, is provided with only haK
the number of chromosomes seen in the spermogonia and in the
tissue cells of the body. Whether the n chromosomes in all
the spermatozoa are or are not alike depends upon the interpretation placed on the first maturation division, as well as upon
our views of the nature of the chromosomes.
B. In the female
While m the male the first or heterotypic division follows
immediately upon the prophases, in the female the two episodes
- prophase and division-  are separated by an interval, sometimes of great length, a year or more-  during which the yolk
is deposited in the cytoplasm to the accompaniment of complex
nuclear changes.
Prophases of the heterotypic division. The oogonial divisions
come to an end at a fairly early period, and growth of the oocyte
begins almost at once. The prophases of the heterotype are
therefore usually found only in very young animals-  in the tadpole of the frog, or the new-born or embryonic Mammal.
72
THE GERM-CELLS
IV
These two afford good examples. The nuclear changes which
are readily seen in the tadpole's ovary (Fig. 37) are obviously
closely j)arallel to what we have observed in the other sex.
A stage in which the chromatin is in the form of scattered
granules is followed by one in which the granules run together
to form the leptotene filament. Then comes the synaptene, with
parallel filaments, followed by the contraction figure. The paired
filaments emerge from the tangle to converge to one pole, the
tangle itself beiiag withdra-WTi from the other side of the nucleus.
The pachjiiene and diplotene follow in due course. A remarkable
change now occurs in the straining capacity of the chromatm
filaments. Up to the diplotene stage they behave in the usual
way, showing great affinity for chromatin stains (carmine, haematoxylin, and basic aniline dyes) ; but from now onwards they lose
this faculty and stain only with the acid plasma dyes. Meanwhile, the number of nucleoh (these also stain in acid dyes) is
increasing, and presently it is seen that granules of chromatin
(that is, granules which are coloured by the ordinary chromatin
dyes) begin to settle upon (? be precipitated round) the nucleoh.
By what appears to be a continuation of this process the nucleoh
become converted into highly chromatic bodies.
The filaments (chromosomes) persist for a while, but will
eventually disappear.
Precisely similar phenomena are seen in the young Mammahan
ovary (Fig. 38), and only one or two points require to be mentioned. There is a very obvious centrosphere with included
centrosome on one side of the nucleus (this usually goes by the
name of the yolk-body of Balbiani), towards which the filaments
of the synaptene and pachytene converge. In the early stage
of contraction the paired filaments are seen to emerge from the
rather open tangle on this side, while on the other a few filaments, also paked, stretch out to the nuclear membrane. In
the later contraction figure the latter are retracted and the
tangle, much closer, hes wholly on the side of the centrosphere.
After the diplotene stage the ruig-shaped figures of eight and
other forms of double chromosomes are seen, but then the
chromosomes break up into their constituent granules and range
themselves along the achromatic threads which make a network
Fig. 37. -  Prophases of the heterotypic division in the female (ovary of
tadpole). 1, Nucleus of oogonium ; 2, Leptotene ; 3, Synaptene ; 4, 5,
Contraction figures ; 6, Pachytene ; 7, Later pachytene, multiplication of
nucleoli ; 8, 9, Diplotene : the chromatin filaments are becoming achromatic ; granules of chi'omatin are being deposited on the nucleoli.
:â– . r-Xj
Fig. 38. -  Prophases of the heterotypic division in the female (Mammals).
1-6, Kitten three days old ; 7, Mouse embryo shortly before birth ; 8, Mouse
eight days old.
1, Nucleus of oogonium or young oocyte ; 2, Leptotene ; 3, Synaptene ;
4, Contraction figure ; 5, Pachytene ; 6, Diplotene ; 7, Heterotypic clnomosomes ; 8, Dictyate.
In 2-5 the centrosphere and centrosome (volk-body of Balbiani) are
shown with the chromatic filaments of the nucleus converging towards them.
P. 72
j'j-G. 38*.-  Small ovarian egg of the frog surrounded by its foUicle (/.)
and theca (th.), which is continued into the pedicle {p.). b.v., a bloodvessel between follicle and theca ; v.rn., vitelline membrane ; ch., clu'omatin
filaments, now achi'omatic ; n., chromatic nucleoli, ejected from the
nucleus (n'.) and becoming achromatic (w".).
V. 73
IV THE GERM-CELLS 73
through the nucleus. This is the diciyale condition, and in this
the nucleus remains through the growth period until the moment
of maturation arrives.
The period of growth and deposition of yolk. The nuclear
changes accompanying the deposition of the yolk in the oocyte
have only been studied in the Amphibia, to which we must now
accordingly return (Fig. 38*).
We have seen that after the prophases the chromatin filaments
become achi-omatic, while the nucleoH increase in number and
become chi-omatic. The filaments gradually break up into a
number of small granules, which disappear, or at least become
indistinguishable from the general ground substance -  or magma
-  of the nucleus.
The nucleoli become more numerous, larger, and more chromatic. They pass into the cytoplasm in one of two ways : either
they are bodily ejected from the nucleus, lose their staining
capacity and break up into small fragments, or else they disintegrate inside the nucleus, the products of their disintegration
then passing out -  either in the form of small particles or in
solution -  through the nuclear membrane into the cytoplasm.
The nucleoli consist of nucleo -protein, and the result of their
transference to the cytoplasm is that the latter first acquires
an affinity for the chromatin stains, and then begins to secrete
yolk-granules. There is thus a direct connexion between the
nucleo-protein of the nucleoli and that which, as we have seen,
is demonstrable in the yolk.
It appears that this cycle of changes is repeated many times
during the growth of the oocyte, fresh nucleoli being formed,
moving to the centre of the nucleus, and there disintegrating.
This passage of material from the nucleus to the cytoplasm
of the egg-cell during the time of growth and yolk-formation
is of constant occurrence in animals. The material may be solid
and bodily ejected or liquid and diffusible, it may be chromatic
or achromatic, but it is always given off and is always concerned
m yolk-secretion. The chemical changes are, unfortunately, not
fully understood.
The material is known generally as ' yolk-nucleus '. It has
sometimes been confounded with another quite distinct structure, the sphere and centrosome. In Mammalian ova the sphere
has indeed long been known as the yolk-body of Balbiani
(Pig. 39). In the Mammals the sphere usually divides into two
or more bodies, which persist for some time, but disappear (in
the bat) when there are two or three cell-layers in the follicle.
In some Mammals {Cavia, Vespertilio) chromatoid bodies are
found in the cytoplasm. These may be of nuclear origin and
correspond to the yolk-nucleus of Amphibia.
The yolk-nucleus is a very important contribution made by
the nucleus to the structure of the cytoplasm : a second contribution has still to be made.
With the growth of the oocyte the nucleus has been enlarging
pari passu, and by the time growth is completed is of considerable
size. It lies in the axis, but excentrically, near the surface in
the animal half of the egg. The oocyte is now ready for the
first maturation division.
Maturation. The nuclear membrane breaks down and disappears. From a very small part of the achromatic substance
of the nucleus a spindle -  the first polar spindle -  is formed
(Fig. 41), and on this are placed the heterotypic chromosomes,
of which we shall speak in a moment. The whole of the rest
of the contents of the nucleus -  chromatic nucleoli and achromatic granular ' magma ' -  are cast into the cytoplasm. This is
the second contribution made by the nucleus to the cytoplasmic
structure, and it is of considerable importance, since on it
in part depends the diflEerence between animal and vegetative
hemispheres.
As we have already had occasion to observe, there is a definite
relation between the polar structure and symmetry of the egg
and the structure of the embryo which is to come out of it,
inasmuch as the anterior end is always developed near the animal,
the posterior end near the vegetative pole. The structm-e of the
embryo is at this moment bemg predetermmed in the egg, by
the dispersal of the contents of the nucleus.
This is a fact of universal occurrence. When the germinal
vesicle breaks down, only a smaU part of it is utihzed m the
formation of the chromosomes which take part in the maturation
mitosis. The remainder is given to the cytoplasm, of which it forms henceforward a definite and integral part. Experiment
has sho^vn that that part is causally related to the development
of certain organs, is therefore a vehicle of inheritance. It will
be noticed that this process is without parallel in the male sex.
We return to the first polar spindle and its chromosomes.
The chromosomes appear first, as beaded filaments of heterotypic form -  wrings, crosses, figures of eight, curved rods, and so
on (Fig. 40). Their number is the half -somatic or germ-number n.
It has been disputed whether these chromosomes are identical
with those which were formed
at the end of the prophases,
in the young oocyte.
It must be remembered, in
discussing this question, that
the hypothesis of the individuahty of the chromatin A
does not necessarily involve 'p^-'\X^
that of the individuality of
the chromosomes. We have so™1-from^?SS''i? th?o»y?;
seen elsewhere that there is of the Axolotl (Siredon) just before
reason for beheving that the membrane breaks down.
chromatia of the nucleus comprises a number of quahtatively
unlike bodies-  not merely that the chromosomes are different,
but that they are composed of individually different granules.
It is also probable, to say the least, that chromosome formation
is a nratter of precipitation from solution, for there is certainly
much more chromatin in a dividing than in a resting nucleus,
and the chromatin often disappears from view in the latter
condition. But a body endowed with certain properties wiH
retain those properties in solution and emerge from solution with
the same, and in a mixture of unlike bodies each wiU retain its
own properties in solution and exhibit them afresh when reprecipitated. The chromatin granules are such bodies, and wo may
weU suppose that they do retain their properties in spite of their
disappearance. It does not foUow, however, that the granules
are associated always in the same order to form chromosomes,
though that may be so. Hence the chromatin granules may
well retam their individuaUty while the chromosomes do not.
76 THE GERM-CELLS TV
The chromatin, therefore, of those heterotypic cliroinosomes
that now apj)ear may, on this view, bo regarded as identical
with the chromatin of the prophases.
Fig. 42.-  The maturation divisions in the female (Axolotl). 1, First
polar spindle with heterotypic chromosomes ; 2, Extrusion of first polar
body ; 3, Appearance of second polar spindle ; longitudinal division of
chromosomes in egg and in first polar body ; 4, Second polar spindle radial ;
homoeotypic chromosomes on equator (metaphase) ; 5, Polar view of the
same ; 6, Anapliase ; 7, Extrusion of second polar body ; 8, Second polar
body with resting nucleus ; 9, Female pronucleus in resting condition,
closely surrounded by yolk-granules.
When the spindle is formed the chromosomes are placed on
it and shorten and thicken (Fig. 41). The spindle then moves
to the surface at the animal pole, Avhere it takes up a radial
position, closely surrounded by yolk-granules. The actual
maturation divisions now occur.
Fig. 41. -  Germinal vesicle of the oocyte of the frog just before maturation (after Carney). The nuclear membrane has disappeared. The first
polar spindle, bearing the heterotypic cliromosomes, is seen in the middle
of the nucleus {p.s.). n., nucleoli ; v.m., vitelline membrane ; /., follicle ;
th., theca.
+ i^*^' Oocyte of mouse with heterotypic spindle from the Fallopian
tuDe. ihe oocyte is still surrounded by the cumulus of follicle-cells.
The first maturaiion division (Fig. 42, 1, 2). The heterotypio
chromosomes are placed upon the spmdio in the same way as
in the male -  that is, Avitli the extremities of the half -rings in the
equators. The half-rmgs break away from one another and pass
to the spindle poles. Cell-division now occurs. This is extremely
unequal. The outer group of chromosomes, with a small quantity
of cytoplasm, is cut off as the first polar body from the egg ; it
lies in a depression at the surface. The inner group of chromosomes remain in a clear area in the egg, now the secondary oocyte.
The first polar spindle is found (in Siredon, and generally in
Amphibia, also in Bnds) in the egg as it passes mto the oviduct.
Li Mammalia -  ^where it is also known to be heterotypic (Fig. 43)
-  ^it may be formed while the egg is in the ovary, or after it has
passed into the Fallopian tube.
The first maturation division in the female evidently involves
similar changes to those seen in the male : the prophases, the
number and form of the chromosomes are all exactly the same.
The interpretation of the manner of division of the chromosomes
-  ^whether longitudinal or transverse -  which is adopted for the
one, may therefore be applied to the other.
The second maturation division (Fig. 42, 3-9). Without passing
into a resting condition the V-shaped chromosomes in the egg
undergo longitudinal fission, as also do those in the first polar
body. A number of parallel fibres, tangentially placed, now
appear -  the second polar spindle. The spindle is soon rotated
into a radial position and the V-shaped chromosomes, already
split, are thrown upon its equator with their apices towards the
spindle axis, as in the male. Their number is, of course, n.
The halves of the chromosomes then separate and pass to the
spindle poles. Another miequal cell-division now occurs. The
outer group of chromosomes, together with a httle cytoplasm
and one or two yolk-granules, is extruded as the second polar
body, while the inner group remain in the now mature ovum as
the female nucleus, or rather pronucleus, to employ the more
usual term.
In both the second polar body and the ovum the chromosomes break up, a membrane is formed round them, and the
nucleus passes into the resting condition.
Since the chromosomes are V-shaped, are longitudinally
divided, and are present in half the normal number, this division
is evidently homoeotypic, as in the male.
The second polar spindle is formed as the egg passes down
the glandular region of the oviduct (in Siredon and most other
Amphibia). In the uterus the polar spindles are in metaphase
(with the chromosomes in the equator). The division is not
completed until after the egg has been fertilized (which is just
after the egg is laid).
Where fertihzation is internal (Elasmobranchs, Birds, Reptiles,
Mammals) the second polar body is extended while the egg is in
the oviduct.
Although the chromosomes of the first polar body have divided,
cell-division (in Siredon) does not usually follow. In other cases
the first polar body does divide.
A centrosphere -  if not an actual centrosome -  is present at
the poles of both the first and second spindles. In the mature
ovum there is, however, no trace of it. The female pronucleus
is immediately surrounded by yolk-granules (Fig. 42, 9).
Nature of the reducing division. We have already assumed for
the purposes of illustration that the several chromosomes of
a nucleus are genuinely different from one another. We may
now add that there is experimental evidence (which we cannot
discuss here) in support of this ; it is further probable that the
granules of which each chromosome is composed are again of
different values. Secondly, there are cases where the chromosomes are of different sizes (certain Insects), and in these cases
they are found in pairs (in tissue- and in yomig germ-cells), the
two members of a pair being of the same size. In the heterotypic division of maturation the members of the paks get
separated from one another, so that each secondary spermocyte
(and consequently each spermatid after the second homoeotypic
division) receives a similar set of different-sized chromosomes.
Attention has akeady been called to the difference in size of
the ring-shaped chromosomes in Siredon.
Now when a row of granules (or chromosome) is divided
lengthways each half contains its due portion of each granule,
and hence each daughter nucleus receiving half of each chromosome receives ipso facto a specimen of each different gi'anule.
The two daughter nuclei are therefore alike and a longitudinal
division of the chromosomes is merely quantitative.
If, on the other hand, the row of granules (or chromosome) is
transversely divided, or, what is the same thing, if two different
chromosomes are separated from one another, each daughter
nucleus will not receive a specimen of each different granule or
chromosome, but only one-half, the remainder passing to the
other nucleus, and the division is quaKtative.
The first condition may be represented by some such formula
as this (where a-h are the quahtatively different granules in
a chromosome, A,A',B, B', &c., whole chromosomes) :
abcdefgh A A' B B' G C D D'
abcdefgji' A A' B B' G C D D''
the line being the division, while the second condition will be
represented by
abed A B G D
or
efgh A' B' G' D'
Ordinary somatic mitoses are therefore quantitative, and so
is the second homoeotypic maturation division. If, however, we
adopt the view that in the heterotypic mitosis a transverse
division of the chromosomes is involved, then we must further
beheve that the division is quahtative, and consequently that
the secondary spermocytes, and eventuaUy the spermatozoa,
receive chromosomes of different kinds. Of every four spermatozoa produced from a single primary spermocyte, therefore, two
wiU be aUke of one kind (containing, say, A, B, Sec), while two
will be alike of another kind (containing A', B', &c.).
But it is evident from the foregoing that identical nuclear
changes occur during maturation in the two sexes. The prophases
of the first division-  with the leptotene, synaptene, pachytene,
and diplotene stages-  are the same, and whatever view is taken of
these phenomena must hold good for both sexes. In the female
the growth period intervenes between the prophases and the
actual division, but when this division occurs it is of the same
form as in the male, heterotypic. The second division is homoeotypic in both sexes.
While, however, the cell-divisions are equal in the male-  resulting in four spermatozoa -  in the female they are unequal - 
giving one large ovum which receives practically the whole of
the cytoplasm and the yolk, and three small polar bodies. The
similarity of the nuclei shows that in spite of their small size
these polar bodies are in reality potential ova, and there are
cases where they are large -  as large as the ovum -  and can be
fertilized and develope.
Like the spermatozoa, the ovum (and polar bodies) receives only
one-half the somatic number of chromosomes. As we shall see
more fully in the next section, these chromosomes form a complete
set, as do those of the male. If-  as is probably the case-  there
are varietal differences between hidividual spermatozoa in respect
of these chromosomes, the same will be true of the ova.^
But what the further significance of these difEerences is, if they
exist, we do not know. The chromosomes of the spermatozoon
and ovum are certainly vehicles of inheritance -  ^that is, concerned
in the transmission of at least some of the inheritable characters
of the species from one generation to the next. But since every
spermatozoon or ovum can perform this function as well as
every other, we are driven to conclude that each one possesses
a complete set of the necessary specific chromosomes ; but that
in different spermatozoa or ova the chromosomes may be of
different varieties-  that is, be concerned in the transmission of
different varieties of the same inheritable character.
This may be expressed by the followmg scheme.
A B, G, D, Sec, are the n different specific chromosomes.
In the tissue-cells and young germ-cells there are 2n, each
kind bemg represented by two slightly different varieties, namely,
A and A', B and B', G and G', &c.
In the prophases of the heterotype division A and A' unite,^
and so B and B', G and G'.
In the actual heterotype division A and A', B and B', G and
G' are separated from one another, so that each secondary
spermocyte or oocyte has A or A', B or B', and so on.
1 Provided of course that priraary oocytes differ inter se in the arrangement and distribution of the heterotypic chromosomes.
2 If the union is by parallel apposition it is further possible to suppose
that the individual granules of"^ which 4 and^' are composed pair ofi
each with each, namely a with a', b with b', and so on.
The homoeotypic division is quantitative, hence each spermatozoon or ovum obtains A or A', B or B' , and so on ; that is,
a complete set of the various kinds of chromosomes.
In only one respect are there chromosomal differences between
the two sexes. In certain forms (Insecta), and possibly in others
also, there is an accessory chromosome or heterochromosome
(often paired), which not only differs in size and behaviour from
the ordinary chromosomes, but is not the same in spermatozoon
and ovum. The variations in the behaviour of this body or
bodies are too complex to be discussed here, but those who have
investigated it beheve it to be concerned in the determination
of sex. Apart from the heterochromosomes and the varietal
differences of the ordinary chromosomes, the germ-nuclei are
exactly alike.
We have now to see how the two nuclei -  each containing
one-half the somatic number of chromosomes -  are brought
together when the germ-cella unite in the act of fertilization.
IV. Fertilization
The Axo\otl- 8iredon- wi\\ serve as a type (Fig, 44). The
spermatozoon-  which is of the same form as that of the newt
and salamander -  after passing through the mucin jelly surrounding the egg, reaches the surface of the latter. It approaches
the egg with its anterior end-  acrosome -  and always in the
pigmented animal hemisphere, sometimes near the equator, but
more usually near the animal pole.
The acrosome pierces the surface-layer of the egg-cytoplasm,
and immediately the egg reacts in a remarkable manner. From
all sides there begins to flow towards the acrosome what appears
to be a watery albuminous fluid : it is hyaline, but coagulable.
This becomes concentrated round the acrosome in the form of
a conical plug, the base of which projects at the surface, the
apex towards the interior of the ovum (Fig. 44, a). This plug
is the entrance-funnel, its base bemg known as the entrancecone (' cone of attraction ' is an erroneous expression, as it is
not formed prior to the contact of the sperm with the egg).
The entrance-funnel enlarges and extends more and more . into the interior of the ovum, being directed usually towards the
axis : it carries in with it a number of the superficial pigment
granules and the spermatozoon. The latter, therefore, after
moving actively up to the surface of the ovum and penetrating
it with its acrosome, is passively carried in by the inflow of the
entrance-funnel ; this movement is apparently due to a difference
in surface tension between the entrance-funnel and the surrounding cytoplasm. The acrosome presently gets caught in the
side of the entrance-funnel, but the substance of the latter, still
moving on, carries the head and tail of the sperm with it. The
result is that the anterior end of the head now faces outwards,
while the posterior end Kes at the bottom of the funnel, where
the head is bent on the tail, and the whole sperm-head has been
rotated through 180°. Between the head and the tail -  and
therefore now at the inner end of the funnel -  is the large anterior
centrosome (Fig. 44, c).
Fig. 44. -  Fertilization in the Axolotl.
A and B. Meridional sections of the whole egg. a, Formation of entrancefunnel (first part of sperm-path), b, Formation of sperm-sphere and aster ;
o3 male pronucleus ; ? female pronucleus ; p.b the t^^^ polar bodies.
c Formation of the sperm-sphere round the middle piece (anterioi
centrosome) ; narts only of the head (black) and tail are sho^vn.
X. Formation of the sperm-aster. The centrosome has disappeared ; the
head besinning to be vacuolated, is separated from the tail.
T'FuSr shortening and vacuolation of the sperm-nucleus. There
is still no centrosome.
F, Appearance of the definitive centrosome. g, h. Division of thn
centrosome.
(In c-H the arrow marks the direction of entrance of tlie spermatozoon.)
I, Approach of the two pronuclei. Formation of spindle-fibres
J, i?ormation of asters, elongation of spindle, further enlargement of
pronuclei, and appearance of clu'omosomes.
K, Further elongation of spindle, and formation of a ccntrosnhere
irfhe'Toindr^r""" ^he pronudear men.branes are breakSg 5ow,x
ana trie spindle-hbres passing in.
L, The fully.formed fertilization spindle. In the equator are the chromoomes, now longitudinally split, and attached to large spiiidle fi'bre Tu
each centrosome the centriole has divided.
The entrance-funnel soon disappears, but the pigment carried
in by it remains for some time as a streak, usually known as the
first part of the sperm-path (Fig. 44, b).
A clear, yolk-free area now appears round the centrosome ;
this is the sperm-sphere (Fig. 44, c). Very soon radial fibres
or processes of some kind begin to pass out from the sphere
amongst the yolk-granules ; this is the sperm-aster (Fig. 44, d).
Meanwhile the head or sperm-nucleus has become detached from
the tail, and the centrosome which was between them has totally
disappeared. It seems that the formation of the sperm-sphere
and aster-  like that of the entrance-funnel-  is due to the extraction of water from the cytoplasm, in the case of the entrancefimnel by the acrosome, in the present case by the centrosome ;
and that the centrosome is completely used up, in fact dissolved,
in the process.
The tail of the spermatozoon will not concern us : it degenerates and vanishes. The head of course remains to become the
sperm-nucleus or male pronucleus. It shortens and thickens :
as it does so it becomes vacuolated. By further shortening and
vacuolation it becomes transformed into an ordinary nucleus
(Fig. 44, E). It Hes on the outside of the sperm-aster.
It is at this moment that the definitive centrosome makes its appearance (Fig. 44, v). On the side towards the sperm-aster
the nuclear membrane breaks down, and through the aperture
something comes out of the nucleus which appears, when outside,
as a rounded granular body. This is the definitive centrosome.
It is not preformed in the sperm-nucleus and then ejected, but,
probably, is due to a precipitation of the albumins of the cytoplasm by the nucleic acid of the sperm-nucleus. But, whatever
interpretation be put upon the process, the centrosome is of male
origm.
The male pronucleus, preceded by its centrosome and aster,
now advances to meet the female pronucleus which has aheady
left its position at the animal pole and is retm-ning towards the
centre of the egg. The line in which the male pronucleus is now
moving is knomi as the second part of the sperm-path. This
does not necessarily lie in the same straight line, nor even in the
same meridional plane as the first or entrance part of the path.
This depends in part on the position of the female pronucleus
(Fig. 46).
The first or entrance part of the path is usually directed
towards some point in the egg axis, that is, it Hes in a meridional
plane of the egg. If, as also is usual, the female pronucleus hes
in the axis, it is evident that the second part of the sperm-path
or line of union of the two pronuclei will he in the same plane.
In that case it may be in the same straight line with the first
part, or, more usually, make an angle with it, smce the pomt
in the axis at which the pronuclei meet is at a fairly constant
distance from the animal pole, while the point of entrance o the
spermatozoon in the animal hemisphere is variable. If, however while the first part of the path is in a meridional plane the
female pronucleus is not in the axis, then the sperm -nucleus
must turn out of its meridional plane to meet the female pronucleus at some point which is not in the axis. The converse
of this is seen when the entrance-path is not m a meridional
plane while the female pronucleus is in the axis ; m this case
also the sperm must turn aside. Thirdly, both sperm-entrance
path and female pronucleus may be out of their normal direction
"^Li'::hrwords, the meridional plane which includes or is
IV
THE GERM-CELLS
85
parallel to the entrance-path does not necessarily coincide with
the meridional plane which includes or is parallel to the line of
union of the pronuclei.
During the advance of the sperm-nucleus the centrosome
divides (Fig. 44, g, h) at right angles to the direction in which
the sperm-nucleus is travelKng, that is, to the second part of
the sperm-path, and also to the meridional plane in which the
path lies. The daughter centrosomes therefore lie in a plane
parallel to the equator of the egg. Hence, when the pronuclei
have met, they lie together between the daughter centrosomes,
which lie in a plane parallel to the equator of the egg.
The two pronuclei are now closely apposed, but not fused,
inside the sperm-sphere and aster. Next, the centrosomes send
out fine fibres in all directions (Fig. 44, i, j). On the one hand
these impinge upon the pronuclear membranes -  ^these are the
begimiing of the fertilization spindle ; on the other hand they
radiate out until they pass into the radiations of the original
aster inside which they He.
The pronuclei enlarge, and presently in each granules of chromatin appear and run together in rows to form chromosomes
(Fig. 44, j). The number of these in each pronocleus is the same
as that which entered into it at the close of maturation, namely
n, the germ-number. Meanwhile the asters round each centrosome have been growing larger, the spindle-fibres longer, and the
latter now break through the pronuclear membranes to meet
their fellows from the opposite pole (Fig. 44, k). The membranes,
achromatic network, and nuclei are now all dispersed, and the
two sets of chromosomes, paternal and maternal, are placed side
by side on the equator of the fertilization spindle, where they
undergo longitudinal fission as in ordinary mitosis (Fig. 44, l).
Hence, when the daughter chromosomes pass to the spindle
poles, each daughter nucleus will receive a complete set of
paternal, and a complete set of maternal chromosomes. The
full somatic number, 2 n, is now restored, and with each repetition of nuclear and cell-division each cell in the body comes to
possess 2 w chromosomes, one-half of which are derived from the
father, one-half from the mother.
With the apposition of the two sets of chromosomes in the equator of the division apparatus -  asters and spindle -  the act
of fertilization may be said to be complete.
The whole falls into two periods. In the first the spermatozoon is carried into the egg by means of the entrance-funnel,
which in turn is due to a stimulus of some kind imparted to the
egg cytoplasm by the acrosome ; the acrosome is the modified
centrosphere. In the second the definitive centrosome is formed
from the male pronucleus and the division apparatus made
between its two halves while the pronuclei meet. The mechanisms involved in both periods are therefore centrosomal.
The details of fertilization have been studied in many animals,
including several Vertebrates. In Vertebrates it is a rule for
the sperm to enter during the second maturation division of the
ovum, as in the Axolotl {Petromyzon, Salmo, Triton, Mus), but
in other cases it may enter at an earlier or later period. The
tail may be left outside {Mus), but is more often taken in : it
always degenerates.
The pronuclei may fuse to form a segmentation nucleus, from
which 2 n chromosomes arise {Pristiurus, Salmo, Petromyzon) ;
but the newt and the mouse resemble the Axolotl in the separate
formation of the chromosomes in each pronucleus.
It is certain that in all cases the female centrosome disappears.
Whether the definitive cleavage centrosome is identical with the
centrosome seen in the spermatozoon, that. is, in the spermatid,
or is, as in the Axolotl, a new formation from the sperm-nucleus,
is not certainly known, but there is little doubt that it is invariably a male centrosome.
As a rule only one spermatozoon enters the egg, and the
presence of more than one leads to serious derangements of
development (pathological polyspermy).! in what is known as
physiological polyspermy, however, two or more, sometimes
a great number, normally get in, as in some Amphibia (including
the Axolotl), Reptiles, Birds, and Elasmobranch fishes, in which
last they are very numerous and known as 'merocytes'
(Riickert). In these cases only one of the sperm-nuclei fuses
1 As in the sea-urchin, where the several nuclei fuse and their chromosomes become irregularly distributed. Where, however as m the frog
Srseveral nuclei remain apart the polyspermy need not cause abnormal
^eveToprenHM. Herlant, Arch, de Biol. xxvi. 1911) although the superfluous sperm-nuclei do take part in the edification of the embryo.
IV
THE GERM-CELLS
87
with the egg-nucleus. The remainder lie about in the yolk, each
develops its own centrosome and aster, and may divide (with n
chromosomes) many times. Ultimately the accessory sperm-nuclei
degenerate without contributing to any embryonic structure.
It remains for us to discuss the significance of fertilization.
It has commonly been supposed that its essence is to be found
in the union of the pronuclei of the germ-cells, both nuclei being
held to be necessary for the development of a normal individual.
This view is based partly on the phenomena of conjugation in
certain Infusoria, but also very largely on the assumption that the
nuclei of the germ-cells are the sole vehicles for the transmission
of inheritable characters ; this again rests upon the fact that it is
only in their nuclei that the germ-cells are alike, while in every
other respect they differ, and upon the supposition that the paternal
and maternal contributions to the total inheritance are equal.
Now, whatever view we may take of the parts played by
nucleus and cytoplasm respectively in the handing on of the
characters of the species, it is most assuredly certain that for the
production of a normal individual both pronuclei are not a necessity. In the first place, there is the phenomenon of parthenogenesis, natural and artificial. In the former the ovum develops
without fertilization by the sperm and without artificial assistance
(as in Aphidae and some other Insects, and in certam Crustacea).
In the latter the stimulus usually given by the sperm is replaced
experimentally by some physical or chemical agent. Thus the
ovum of a sea-urchin or Mollusc may be stimulated by treatment
with hypertonic sea-water, or butyric acid or other substance,
or by mechanical shock, or a lowering of the temperature ; in
the case of the frog it is sufficient to pierce the egg with a fine
needle. In all these instances some physical or chemical alteration
(or both) IS produced in the egg, as a result of which it begins
to segment and develop. The process, if care is taken, may be
perfectly normal, and the individual reach the adult condition A
sexually mature (male) sea-urchin has been reared in this way
In all cases of parthenogenesis only the female pronucleus is
The converse is seen in what is called merogony, where the egg
(of a sea-urchin, Worm, or Mollusc) is divided into two halves, only
88
THE GERM-CELLS
IV
one of wlucli contains the nucleus. Both halves can be fertilized,
the nucleate and the enucleate, and will develop into normal
larvae. In the latter case only the male pronucleus is present.
On the other hand, a nucleus must of course be present, and
actual experiment has shown that what is really necessary for
normal development is the presence in the ovum, and ultimately
in every cell of the body developed from it, of a complete set
of the n unlike chromosomes characteristic of the species.
Hence, both male and female pronuclei are not necessary, and
we must look elsewhere for the significance of fertilization.
As we know already, the germ-cells of both sexes pass through
two maturation divisions, and two only, after which their
capacity for reproducing themselves is lost. The first effect, or
almost the first effect, of their union is that their product, the
fertilized ovum, begins to segment and continues to do so. In
other words, the power of reproduction by cell-division which was
previously lost is in fertilization restored. It is mutually restored.
That the ovum regains the power of nuclear and cell-division
is obvious : we see the maternal chromosomes undergo longitudinal fission, as they lie on the spindle, and subsequently we
see the egg cytoplasm divide. In the case of the male Ave see
the male chromosomes divide in ordinary fertilization as they
lie alongside the female ; in the fertilization of enucleate eggfragments the stimulus imparted by the female cytoplasm to the
male chromosomes is still more evident.
A study of fertilization reveals the mechanism by which this
stimulation is effected. For ordinary nuclear and cell-division
an apparatus is necessary, the spindle with its asters ; this
apparatus is made by the centrosomes in the cytoplasm, the
two centrosomes proceeding from the division of one, and its
function is first to pull apart the halves of the divided chromosomes, and second, to ensure cell-division by the cell-plate or
intermediate bodies developed in the equator.
The mature ovum possesses no centrosome : the mature
spermatozoon possesses little cjrtoplasm, and that only in the
tail. In fertilization the centrosome is either introduced by the
male cell or made by it after entering the egg : the necessary
cytoplasm in which this centrosome can divide and make the
IV
THE GERM-CELLS
89
asters and spindle is provided by the female. The wholly
different structures of the two germ-cells are therefore mutually
complementary in the stimulation by which the lost power of
cell-division is restored, and this is the significance of fertilization.
The experiments on artificial parthenogenesis suggest that
a physico-chemical expression may be found for this stimulus.
This is not, however, its only effect. A very common, if not
universal, result of the approach of the sperm is the exudation
by the ovum of a peri vitelline fluid. In some cases (for instance,
the sea-urchin) a membrane which prevents the entry of more
spermatozoa is secreted at the same time and pushed out by the
peri vitelline fluid. In the frog it remains as a thin fluid layer
between the ovum and the jelly ; it is the exudation of this
fluid which enables the egg previously adherent to the mucin
jelly to turn over till its axis is vertical and the white pole
below : this occurs shortly after insemination.
Of greater importance than this is the change in the cytoplasmic structure of the egg brought about at this time.
A few hours after insemination there appears in the frog's
egg a crescentic grey patch on one side along the border of the
pigmented area (Fig. 45). The grey crescent is due to the
immigration of pigment from the surface into the interior, and
this in turn is caused by the entrance of the spermatozoon. The
grey crescent always appears on the side of the egg opposite to
that on which the sperm has entered. We know that a watery
fluid flows towards the sperm from the cytoplasm (the entrancefunnel flrst, and later the sperm-sphere, are due to this), and
we may suppose that this streaming movement drags the pigment granules away from the surface on the opposite side,
whence the grey crescent.
The grey crescent is actually opposite to-  that is, in the same
meridional plane as-  the first or entrance part of the sperm-path
(Fig. 46). Hence it does not necessarily lie in the same meridional
plane as that which includes the line of union of the pronuclei.
We shall see in the next chapter that the meridional plane
of the first division always includes the line of union of the
pronuclei, and hence does not always coincide with the meridional
plane of the grey crescent.
90
THE GERM-CELLS
IV
It is clear that, whereas the unfertilized egg was radially
symmetrical about its axis, it can now be divided into similar
halves by only one plane, that which includes the axis and
the middle point of the grey crescent. About this plane it is
bi-laterally symmetrical. The greatest interest attaches to this
alteration of symmetry, since the side of the grey crescent will
become the dorsal side of the embryo, the side on which the sperm
A B
C
D
Fig. 45. -  Formation of the grey crescent in the frog's egg (R. ternporaria). a, b from the side ; c, d from the vegetative pole. In A, c
there is no crescent, in b, d a part of the border of the pigmented area
has become grey.
entered its ventral side. Since the animal and vegetative poles
mark respectively the future anterior and posterior ends (approximately), it follows that the plane of symmetry of the fertiUzed
but unsegmented egg coincides with the median longitudmal or
sagittal plane of the future embryo. The whole bilateral symmetry of the embryo is now predetermined in the cytoplasmic
structure of the egg.
That the blastodisc has a bilateral structure in Birds and
Elasmobranch fishes also seems to foUow from the fact that the
IV
THE GERM-CELLS
91
cells in both these cases are larger at one end of the blastoderm
than at the other. Further, this structure is definitely related
to that of the embryo since the large-celled end becomes anterior.
Whether the change from the original radial to the definitive
bilateral symmetry is in these cases also brought about by the
spermatozoon, future researches must show.
In the Teleostei the concentration of the superficial cytoplasm
(periblast) to form the blastodisc is an effect of fertihzation.
l^' ^^r" Diagrams to show the relation between the first and second
parts of the sperm-paths. The paths are projected on a plane perpendicular to the axis. In a the two parts are in the same meridional plane, in
B m different meridiona.1 planes. 1, First part of the sperm-path ; 2. Second
part; o^, male pronucleus ; ?, female pronucleus ; ^.c, grey crescent : on
the opposite side (side of entrance of the sperm) the superficial pigment
Z rS; ' «,<^^ has divided in a plane perpendicular to thf a^
at right angles to the second part of the path. '
In conclusion we may attempt to estimate the parts played
by the cytoplasm and the nucleus of the germ-cells in inheritance.
That some at least of all the inheritable characters of the
species-  and not only specific but varietal and individual characters as well-  can be inherited from the father as readily as from
the mother is obvious. Since the nucleus, beside the centrosome which is merely an organ of cell-division, and the acrosome
which merely provides for the entrance, is the only part of the
male cell which is always incorporated in the fertilized ovum
for the tail may be left outside, we are obliged to regard the
B
92
THE GERM-CELLS
IV
nucleus, that is, the chromosomes, as the vehicles by which
tliese characters are transmitted.
The chromosomes of the nuclei of the germ-cells -  which, as
we have already pointed out, are different from one another - 
are in some sense the determinants of inheritance in the offspring :
on their presence depends the ultimate appearance in the offspring of certain characters, and, in respect of their capacity for
transmitting these characters, the two germ-cells are similar :
each possesses a full set of the necessary chromosomes. In
ordmary sexual reproduction the offspring receives two such
sets, but one will suffice, as in parthenogenesis and merogony.
It does not, however, follow that the determinants for the
whole of the inheritance are located in the nucleus.
As we have just seen, the material for the different parts of
the body of the embryo is present in the cytoplasm of the
fertilized but unsegmented egg ; to that structure the spermatozoon has . contributed nothing, beyond the rearrangement of
material, the substitution of a bilateral for a radial symmetry.
Experiment teaches us that the various parts of this structure
are so many organ-forming substances, causally related to the
development of certain organs, and therefore determinants of
a part of the whole inheritance ; and recent researches on heterogeneous hybridization show clearly what this part is. The ovum
of a sea-urchin, if the proper precautions are taken, may be
fertilized by the sperm of a starfish, a feather-star (both of
which of course are, like the urchin, Echinoderms), or even of
a Mollusc or Worm. The result is always the same. A typical
sea-urchin larva is developed. Even an enucleate egg-fragment
will develop a little way when so fertilized, and exhibits the
maternal characters alone. The spermatozoon employed does
nothing but convey to the egg a stimulus, which sets the process in action ; its chromosomes sometimes persist, sometimes
do not.
Hence the characters, the determinants of which reside in the
cytoplasm, are the large characters which put the animal in its
proper phylum, class and order, which make it an Echinoderm
and not a Mollusc, a Sea-urchin and not a Starfish ; and these
large characters are transmitted through the cytoplasm and
IV
THE GERM-CELLS
93
therefore through the female alone. The smaller characters - 
generic, specific, varietal, individual -  are equally transmissible
by both germ-cells, and the determinants of these are in the
chromosomes of their nuclei.
And yet the cytoplasm of the egg-cell is indebted very largely
for its structure to the activity of the nucleus. As we have
seen, the nucleus makes two contributions to the cytoplasm,
first, the so-called ' yolk-nucleus ', the substances concerned in
the deposition of the yolk, and second, the contents of the
germinal vesicles dispersed when the latter breaks down at
matm'ation. These processes are perhaps independent of the
chromosomes. Further, they find no parallel in the male sex.
Even if, therefore, the cytoplasmic determinants are ultimately
to be assigned to the nucleus, the share taken by the female in
the transmission of the whole heritage is greater than the part
played by the male.
LITERATURE
W. E. Agab. The spermatogenesis of Lepidosiren paradoxa. Quart.
Journ. Micr. Set. Ivii, 1911.
G. Belikens. Die Reifung und Befruchtung des Forelleneies. Aiiat.
Hefte, x; 1898.
J. B. Caenoy et H. Lebeun. La v6sicule germinative et les globules
polaires chez les Batraciens, La Cellule, xii, xiv, 1897, 1898.
J. B. Farmer and J. E. S. Moore. On the meiotic phase in animals and
plants. Quart. Journ. Micr. Sci. xlviii, 1905.
K. Herfort. Die Reifung und Befruchtung des Eies von Pelromyzon
fluviatilis. Arch. miJcr. Anat. Ivii, 1901.
'J. W. Jenkinson. Observations on the maturation and fertilization of
the egg of the Axolotl. Quart. Journ. Micr. Sci. xlviii, 1904.
E. KoRSCHELT u. K. Heider. Vergleichende Entwicklungsgeschichte
der wirbellosen Tiere. Allg. Th., Lief. 2, Jena, 1903.
F. Meves. Ueber die Entwicklung der mannlichen Geschlechtszellen
von Salamandra mactdosa. Arch. mikr. Anat. xlviii, 1896.
F. Meves. Es gibt keine parallele Conjugation der Chromosomen !
Arch. Zellforsch. i, 1908.
T. A. Montgomery. The heterotypic maturation mitosis in Amphibia
and its general significance. Biol. Bull, iv, 1903.
A. Oppel. Die Befruchtung des Reptihencies. Arch. mikr. Altai, xxxix,
94
THE GERM-CELLS
IV
J. RijOKEET. Zur Bofruchtung des Selacliioroies. Ami. Am. vi, 189L
A. u. K. E, SoHEEiNER. Uio Rcif ung der maiinlichen Geschlechtszelleu
von Salamandra maculosa, Spinax niger und Myxine gluHnosa. Arch, de
Biol, xxii, 1906.
J. SoBOTTA. Dio Befruchtung und Furohung des Eies der Maus. Arch,
mikr. Anat. xlv, 1895.
E. B. Wilson. The cell in development and inheritance. New York,
1902.
H. VON WiNrwABTER. Rechcrches sur I'ovogentee et I'organogcneso de
I'ovaire des Mammif^rea. Arch, de Biol, xvii, 1901.
==CHAPTER V SEGMENTATION==
Apart from the exudation of the circum- vitelline fluid, and,
in some cases at least, the assumption .of a definite bilateral
symmetry, the first sign that the fertilized ovum gives of its
activity is cleavage or segmentation. In this process the material
of the egg-cell, which, as we have seen, has a certain structure,
is cut up by successive nuclear and cell-divisions into an increasingly greater number of increasingly smaller elements. The
division of the nuclei is always by karyokinesis.
These cleavages pass through the egg substances in a perfectly
definite way, which may be readily described by reference to
the structure and symmetry of the egg, its axis, poles, and
equator.
As a type we may consider the cleavage of such an egg as that
of the common frog {Ham, temporaria). The egg is of the smallyolked or microlecithal type, and its cleavage is total or holoblastic, that is to say, the whole substance of the germ is divided
(Fig. 47).
The first cleavage is a meridional one, that is, is in a plane
which includes the axis of the egg. The cleavage begins at the
ammal pole, and is seen externally as a fairly wide f m-row. The
division is extended inwards, and at the surface of the eg<r
gradually round to the vegetative pole. At the very beginning"
therefore, it may be seen that the protoplasm is divided more
readily than the yolk. Prior to the division the surface of the
egg at the animal pole is markedly flattened. At the sides of
the furrow are a number of smaU wrinklings in the superficial
skm or membrane of the cytoplasm (not the vitelline membrane
but the surface layer of the egg itself). These wrinklings which
are at right angles to the furrow at the animal pole and directed
away from the animal pole at either end, are quite transitory
96
SEGMENTATION
V
effects of the internal forces to which cleavage is due. As soon
as it is completed the furrow becomes narrowed.
By a meridional furrow the egg is necessarily divided into
equal parts or blastomeres. The cleavage may, however, be
parallel to a meridian and therefore unequal. This is not, however, in any way prejudicial to a perfectly normal development.
The two blastomeres soon prepare for the simultaneous divisions
of the second phase. As before, the division is preceded by a
flattening of the egg at the animal pole, and the same transverse
wrinklings are seen. In each blastomere the furrow begins at the
animal pole, proceeds internally and round to the vegetative pole.
Usually the two divisions of this phase are again meridional
and intersect the first fuiTow at right angles. In that case there
are four surfaces of contact between blastomeres intersecting in
one line, the egg-axis. This is cleavage of the pure radial type.
But it may happen, owing to slight inequality of division in
either one or both of the two blastomeres, that the second
furrows fail to meet, either at the animal or at the vegetative
pole, or at both. There is then intercepted between them a small
portion of the first furrow, known as the cross- or polar-furrow.
By shifting of the blastomeres the polar-furrow soon comes to
make an angle with the remaining portions, that is the ends,
of the first furrow, these two ends being parallel to one another.
There are now five surfaces of contact between blastomeres,
surfaces which intersect approximately at angles of 120°, and
cleavage is no longer radial.
There are now four blastomeres, each of which has a similar
portion of the animal, pigmented, and vegetative, unpigmented,
regions of the egg. The simultaneous divisions of the third phase
separate these regions, for the cleavage is latitudinal, or parallel
to the equator and nearer the animal than the vegetative pole.
The divisions intersect the first two cleavages at right angles.
The result is four small animal, four large vegetative blastomeres,
the former wholly, the latter partly pigmented. During the
progress of the division the transitory superficial wrinklings may
again be seen.
In the fourth phase of cleavage division begins rather earlier
in the animal than in the vegetative cells. In direction it is on
â– piQ, 47. -  Segmentation of the egg of the frog [Rana iemporaria) except a
{Raiia esculenta). (e, h, from Morgan, after Schulze ; g, after Roux.)
A. First furrow, from the side of the grey crescent. The furrow is in the
plane of symmetry, that is, in the middle of the grey crescent. The
furrow has not quite reached the vegetative pole.
B. First furrow from the animal pole. The division is not quite meridional in this case ; the two cells are therefore unequal.
c. From the vegetative pole. First furrow completed, and now closing
up. Second division with a wide furrow coming round from the animal
side. The first furrow has cut the grey crescent obliquely (the grey
crescent is at the top of the figure).
D. Beginning of the second division, from the animal pole.
E. Second division in which the furrows do not intersect the first furrow
at the same point ; the part of the first furrow intercepted between them
is a polar furrow, and the first furrow is bent twice.
-E. Typical division of the fourth phase, seen from the side opposite the
grey crescent. The thu'd latitudinal division is completed ; the fourth is
completed in the animal, but not yet in the vegetative cells.
G. The bilateral foiirth division in the egg of Rana esculenta, from the
animal pole. The fii-st division runs up and down the page, the second
from side to side. The third is in the plane of the page. The upper side of
the figure is the side of the grey crescent (dorsal). The second division
has been unequal, the two dorsal cells being smaller. On this side the
furrows of the fourth phase run into the second furrows, while on the
opposite ventral side these divisions run into the fii'st.
H. Fourth division. Abnormal case in which the furrows are paraUel to
the first. (From the animal pole.)
I Fourth division. Usual appearance from the animal pole. The
furrows do not meet exactly, but pass into the first or second near
the animal pole.
J. Side view of the fifth (latitudinal) division.
K. Later stage, seen from the left side, the grey crescent being on the
right of the figure.
L End of segmentation from the same point of view as the last. The
grey crescent has become white and the original white area so enlarged.
Between 90 and 97
V
SEGMENTATION
97
the whole meridional, and at angles of 45° to the first two
cleavages, and therefore of the radial type ; but there are manydepartures from this rule. Thus, instead of intersecting at the
animal pole, the furrows may run into the first or second, and
in a variety of ways ; in one variety the resulting arrangement
is isobilateral (with two planes of symmetry), in another it is
bilateral (with only one plane of symmetry), and the latter is
stated to be the normal method of the fourth cleavage in the
edible frog (Sana esculenta). But though liable to much variation the divisions are always parallel to a meridional plane, or
only slightly oblique ; they are never parallel to the equator.
As has been already pointed out, these irregularities of cleavage
do not involve any abnormality in development.
In the fifth phase the furrows are once more latitudinal, and
result in the production of four tiers of eight cells each. In
the animal cells the division is approximately equal, in the
vegetative imequal, four smaller pigmented blastomeres being
separated from four larger, partly unpigmented. In this phase,
again, division begins first in the animal cells. Departures from
accurately latitudinal division are of irequent occurrence.
Up to this moment segmentation has been fairly regular, and
synchronous in each phase, at least in cells belonging to the
same region of the egg ; but from now onwards there is little
regularity in direction, or simultaneity in time of division.
The only rule that is rigidly adhered to is seen in the more
rapid division of the small, pigmented, protoplasmic animal
cells, the less rapid cleavage of the larger, yolky, unpigmented
vegetative cells.
Further, while up to now all the furrows have been perpendicular to the surface, tangential divisions, separating the outer
from the inner portion of a cell, now occur, and the segmentation
cavity or blastocoel is formed (Pig. 48). The first sign of this
may indeed be detected in the eight-cell stage, as a small space
between the cells, in the axis of the egg, but nearer the animal
than the vegetative pole. The cavity is soon enlarged, partly
by the secretion of albuminous material, partly by the absorption
of water from outside, and becomes eventually an extensive
hemispherical cavity in the animal portion of the egg
1356
98
SEGMENTATION
V
As a result of all these processes -  continued division, more
rapid in the animal cells, and tangential as well as perpendicular
to the surface, and enlargemerit of the segmentation cavity - 
the frog's egg, now known as a blastula, presents at the end of
cleavage the following appearance (Fig. 48*) : the roof of the
segmentation cavity is formed of about four layers of small
animal cells. The cells of the outermost layer are deeply pigmented, and an-anged in a cubical, or shortly columnar epithelium ; in the next two layers the cells are rounded, or by
mutual pressure polyhedral; in the innermost layer they are
Fig 48 - Meridional section through the egg of the frog in an early
â–  stage of segmentation, showing the segmentation cavity.
again in the form of a cubical epithelium. These animal cells
contain only small yolk-granules. The floor of the segmentation
cavity is occupied by about twenty layers (in the greatest thickness, that is, in the axis) of large cells heavily laden with large
granules of yolk, while the intermediate region, round about the
equator of the egg, is occupied by cells which in size, amount
of yolk, and size of the yolk-granules, are intermediate between
the above two kinds. The superficial pigment extends beyond
the equator into the vegetative region, but on one side, that on
which the grey crescent was formed and the unpigmented area
Ton equen'y enlarged, it is less extensive than on th. other.
The segmentation cavity is symmetrically placed about the eggaxis, but Hes wholly in the animal hemisphere.
SEGMENTATION
99
It is evident that by the process of cjeavage the unlike
material of the egg has been cut. up into a number of cells, the
characters of which are derived directly from the characters of
that region of the egg-substance from which they come. There
is thus, during segmentation, no differentiation-  beyond the
formation of the blastocoel-  no new structure formed, and the
significance of the act is probably to be sought in the reduction
of the c3^oplasm relatively to the nucleus. " Initially, the cytoplasm is too large, by cleavage it is reduced, and when a definite
numerical nucleo-plasma ratio
has been reached segmentation
as such comes to an end and
new events -  of differentiation
-  begin.
But while cleavage is thus
not a process of differentiation, it is yet true that the
particular pattern adopted in
cleavage -  ^in our own case the
radial pattern -  is very definitely related to the initial
structure of the ovum. That
structure, as we have seen, is
a polar one, with a radial symmetry about the axis, and the
first three furrows are very
definitely related to this axis,
being successively meridional, meridional, and latitudinal. The
direction taken by these and subsequent divisions may very
probably be particular cases of the rules known by the names of
Balfour and Hertwig.
According to Balfour's rule yolk impedes nuclear and celldivision, and that, as we have seen abeady, and shall see again
when we deal with large-yolked eggs, is certainly the case in the
Vertebrates. According to Hertwig's first rule the nucleus places
Itself m the centre of its sphere of activity, and this in a telolecithalegg is in the axis but excentrically, and nearer the animal
than the vegetative pole. According to the second rule of
G 2
Fig. 48*. Sagittal section through
the frog's egg at the beginning of
the formation of the blastopore.
d.l., dorsal lip; i.z., intermediate
zone.
100
SEGMENTATION
V
Hertwig, the dividing nucleus -  or mitotic spindle -  elongates in
the direction of greatest protoplasmic mass (Fig. 49), or as
Pfliiger phrased it, the direction of least resistance, the resistance
being offered by the yolk, and by the surface of the egg. Hence
the first spindle has its equator in the axis in the animal portion
of the egg, and elongates in a plane perpendicular to the axis,
as the disposition of the yolk about the axis makes this a direction of least resistance ; the resulting division is therefore meridional. Similarly in each of the first two blastomeres the greatest
protoplasmic mass or least resistance is again in a plane perpendicular to the axis, and, in this plane, in a direction parallel to
the first furrow. In this direction the spindle elongates, and
once more the division is meridional, and at right angles to
the first.
In the third phase, however, the greatest protoplasmic mass
in each cell is in a direction parallel to the axis ; at the same
time, in each cell the nucleus lies in the protoplasmic portion,
near'the animal end : hence the latitudinal division. The direction of division in subsequent stages, as far as it can be followed,
may be similarly explained.
Attention has already been called to the effect of the yolk
on the rate of division and on the size of the cells.
We have still, however, to inquire into the cause which determines the particular meridian occupied by the first furrow out
of the infinite number possible.
As we have seen, prior to segmentation the egg assumes
a bilateral symmetry, owing to the formation of the grey crescent
on the side opposite the entrance of the spermatozoon. The
plane of the grey crescent or plane of symmetry of the egg is
of course a meridional plane, and it might be inmgmed that it
is this which determines the meridian to be occupied by the first
fui-row But this is not so. There is no definite or necessary
relation between the two. The first furrow may pass through
the centre of the grey crescent (Fig. 47, a), or be oblique (Fig^
47 c) or at right angles to the plane m which it lies. The
reVon for this divergence of the plane of the first furrow from
he plane of symmetry lies in the fact that tha latter is
determined by the first, the fo.mer by the second part of
A B
p. 100
V
SEGMENTATION
101
the path taken by the spermatozoon in the egg, and that
the two parts do not necessarily lie in the same meridional
plane (Fig. 46).
The sperm enters the egg and immediately passes inwards ;
this is the first part of its path, and opposite this the grey crescent
is formed. The sperm then turns to meet the female pronucleus,
I^G 50.-  Diagrams illustrating the various relations between thp fir«f
and this is the second part of its path. The centrosome divides
at right angles to the meridional plane which includes the line
ot union of the pronuclei, the spindle is formed between the two
centrosomes, and the division falls in the equator of the spindle
that IS, in the second part of the path (Fig. 50). The two parts
ot the path may, but need not, lie in the same meridional plane •
102
SEGMENTATION
V
hence the first furrow may, but need not, lie in the plane of the
grey crescent.
While, therefore, as far as it is meridional, the direction of
the first furrow is definitely related to the original polar eggstructure, the particular meridian it occupies is not so related
to the bilateral structure imposed on the egg at the time of
fertilization. That structure, on the other hand, as we are
soon to see, is the actual forerunner of the bilateral symmetry
of the embryo.
It is clear, then, that the factors which determine differentiation are distmct from those to which the pattern of segmentation
is to be attributed. The former, for reasons which cannot
be more fully set forth now, are to be looked for in certain
cytoplasmic organ-forming substances, the latter in the
relation between the nuclei, with their centrosomes, and the
cytoplasm.
We may now turn to the cleavage of other Vertebrate eggs.
Petromyzon, Ceratodus, and the Urodelous Amphibia have
small-yolked holoblastic ova. The course of segmentation is
very similar to that in the frog, and, as a result, a similar
blastula stage is reached with segmentation cavity in the animal
hemisphere. In Petromyzon, however, the roof of the segmentation cavity consists of but one layer of cells. In Ceratodus the
third furrows are stated to be meridional, the fourth and fifth
latitudinal.
In the so-called Ganoid fishes Lepidosteus, Amia, Acipensei ,
as well as in Lepidosiren and in the Gymnophiona, the egg is
intermediate between the small-yolked and large-yolked types.
The additional amount of yolk exerts an influence upon the
cleavage, and the vegetative portion of the egg is divided but
slowly. Indeed, nuclear division here outruns cell-division, and
at the end of segmentation there is produced a larger or smaller
cap of small animal cells resting on an incompletely cUvided but
multinucleate yolk-mass. The segmentation cavity is small
(Fig. 51, B). ^ , •
The direction of the furrows of the first few phases differs m
the different cases, although the first two are always meridional
and at right angles to one another. In Acipenser the third furrows
p. 102
I
B.
B
r> i^*''';i'3/P^v--ir/^ • 53. -  Sections tlu-ough the segmenting blastodisc c£
• X/';^-y^>-f '• f.^- / Elasmobranchs. (After Riickert.) A, B, c, Successive stages ;
' A and B, Torpedo ; c, Pristiurus. In c the left side is the
anterior end. /. fine, c. coarse, yolk ; m., merocj^^es.
Fio. 52. -  Surface views of
segmentation of the blastodisc in
Elasmobranchs. ( After Riickert. )
A, 7-8-ceIled stage {Torpedo).
B, 8-16-celled stage [Torpedo).
c. Blastoderm (Sci/llium).
In all the figures the upper is
I the anterior end. Note the larger
cells at this end in c.
V
SEGMENTATION
103
are again meridional or parallel to the first, in Lepidosteus the
fuiTOws of the third phase are parallel to the first, those of the
fourth phase parallel to the second (as in Teleostei). In Amia
the third are meridional, the fourth latitudinal and quite close
to the animal pole, the fifth tangentia I in the animal, meridional
in the vegetative blastomeres (Pig. 51, a).
In the Myxinoids, Elasmobranchs, Teleostei, Reptiles, Birds,
and Monotrematous Mammals the egg is very large-yolked and
segmentation is meroblastic or partial -  that is to say, is confined
to the blastodisc or cap of cytoplasm which lies at the animal
pole upon the voluminous yolk. As a result of segmentation
the blastodisc is cut up into cells and becomes the blastoderm,
resting upon an unsegmented yolk. The yolk may, however,
contain nuclei, and these may continue to divide for a considerable time.
In all these cases the first two divisions are meridional and
at right angles to one another. In Myxinoids the furrows of
the third phase are again meridional. Cleavage then becomes
irregular. When it is ended the blastoderm consists of a columnar
upper layer, some lower layer rounded cells, and a third layer
closely appUed to the yolk. In the yolk are nuclei without
cell-divisions. In Elasmobranchs (Figs. 52, 53) the third division
is in some cases meridional, in others latitudinal, but so near the
animal pole as to have the appearance of a circular furrow.
Divisions perpendicular to the surface contmue, and tangential
divisions soon begin to occur.
At one end-  the future anterior-  of the blastoderm the marginal cells are distinctly larger than at the opposite end. The
first furrow, however (Fig. 52, a), bears no definite relation to
the antero -posterior axis.
The tangential divisions separate cells lying at the surface
from cells which are still continuous with the yolk below. More
tangential divisions increase the number of layers of cells, but
the lowermost layer is always continuous with the yolk. Iii the
same way at the margin of the blastoderm divisions perpendicular to the surface separate cells at the edge which are continuous with the yolk from cells inside. The marginal cells and
the cells of the lowest layer feed upon the yolk, grow, divide
104
SEGMENTATION
V
again, and so the whole blastoderm increases in diameter and
in thickness.
Segmentation therefore leads to the formation of a manylayered blastoderm. The cells of the uppermost layer are
arranged in a columnar epithelium. Those below are rounded
elements, aggregated especially at the (future) anterior end ;
they are known as the lower layer cells, and between them
and the yolk is a segmentation cavity, more spacious at the
posterior end. In the yolk are numerous nuclei, some of which
are derived from the fertilization nucleus, while others, as we
have seen, are due to accessory spermatozoa (merocytes).
The nuclei in the yolk divide for some time by mitosis, but
eventually abandon this method of multiphcation. They enlarge,
become highly and coarsely chromatic, irregular in shape, probably amoeboid, and divide amitotically. Their function is now
to break up the yolk, possibly by some fermentative action, and
render it suitable for absorption by the embryo. Eventually,
when this duty has been performed, they disintegrate and
disappear without participating in the development of any
embryonic tissue.
In the Teleostei (Fig. 54) the second division is parallel to the
first, the fourth parallel to the second. In the nest phase the
division is radial (with regard to the centre of the blastoderm)
in the corner cells, parallel to the edge in the remaining marginal
cells, and tangential in the four central cells. Further divisions
result in the completed blastoderm, a compact discoidal mass of
cells resting upon, but not contmuous with, the yolk. The
upper layer of the blastoderm is epithelial : in the lower layers
the cells are polyhedral. The Teleostean segmentation is often
described as ' discoidal '.
The detachment of the blastoderm from the yolk is effected
at a fairly early stage, but not before a very important process
has taken place, the separation of the yolk-nuclei. At a certain
stage the marginal cells with their nuclei sink back into the
periblast-  or hyaline layer surrounding the yolk. cell-divisions
disappear and there is left a ring of nuclei round the margm
of the rest of the blastoderm. The latter becomes now completely separated from the periblast around it and below it.
r tI f *;T^egf°.eitation of the egg of the plaice, a, 2 cells ; b, 4 cells •
the fir,?^ P^'^^'",^ *° fi^-^^t fig"i-e« are so placed t at
Se f^urt?rr. P^g^)' ^oniPleted, the furrows o
the lourth phase are appearing ; d. Fifth division.
A
B
eggs).' segmentation of the hen's egg (from oviducal
in pro'J-Sr""""""^ l^^^-^ = the fourth (latitudinal) is
posterior end ^' small-cellod area is towards the
P. 104
V
SEGMENTATION
105
The yolk-nuclei then migrate into the layer of periblast underneath the blastoderm. There they cease to divide mitotically,
swell up, become vacuolated, irregular, and very chromatic. As
in the Elasmobranchs they are concerned with the liquefaction
and elaboration of the yolk, and eventually disintegrate and
disappear (Fig. 54*).
In some cases (Salmonidae and others) the periblast or yolknuclei are formed not only at the margin but also at the under
surface of the blastoderm.
In the Reptiles and Birds (Fig. 55) segmentation quickly
becomes irregular after the first two or three meridional divisions. Tangential divisions soon occur, and a blastoderm is
Fig. 54*.-  Sagittal section through the blastoderm of Serramis during
the formation of the germinal layers (after Wilson) ; showing beginning
of overgrowth at dorsal Hp {d.l). par. parablast (periblast).
formed composed of two layers only, an upper and a lower.
In the hen's egg the cells at what will be the anterior end of the
blastoderm are larger than at the posterior end. At the margin
the two layers are united with one another and continuous
with the yolk, as in other cases (Fig. 56). In Reptiles,
though not so easUy in Birds, there may be distinguished in the
upper layer two regions, an oval are-i in the centre composed of
columnar cells (this is the embryonic shield), and a surrounding
extra-embryonic area of flattened cells. The lower layer consists
of scattered rounded cells, many of which are, in the Reptiles,
still continuous with the subjacent yolk. The lower layer cells
umte together finally to form a flat epithelium, the lower layer
or paraderm (Fig. 57) (endoderm of most authors, but the term
should be avoided at this stage).
In the Reptiles the upper and lower layers remain continuous
at one pomt up to the time when the germ layers begin to be
tormed. This point is at what will be the hinder margin of the
106
SEGMENTATION
V
embryonic shield, and is known as the primitive plate. It is
here that the blastopore will be formed (see Fig. 83).
In the Monotremata amongst the Mammals segmentation
is also meroblastic, and it is known that the first two
A
â–  â–  ' -~fmâ– .:^--â– 
Fig. 56. -  a, Longitudinal section through the segmented blastoderm
of the hen's egg ; s.g.c, subgerminal cavity. The anterior end with the
larger cells is on the right.
B, Section through the blastoderm of the unincubated hen's egg. In
the centre of the blastoderm the lower layer cells lie scattered in the subgerminal cavity ; at the edges the lower layer cells are closely packed and
rest on the yolk.
YiG 57 - Part of a section of the blastoderm of the chick after six
" hours' incubation, u.l., upper layer ; l.l, lower layer.
furrows are meridional, the third parallel to the first and at
right angles to the second. At the end of segmentation there
are two layers.
In all these Amniota the blastoderm originates by cleavage
in precisely the same way as in the large-yolked eggs amongst
Fig. 58. -  Segmentation of the ovtim of the Marsupial Dasyurus. (After
Hill.) 1, 2 cells ; 2, 4 cells ; 3, 6 cells ; 4, 16 cells, sh., shell ; a., albumen ;
z., zona pellucida ; y.b., yolk-body.
r
Fig. 59.-  Formation of the blastocyst in Dasunruti. (After Hill.)
1, Blastocyst in which all the cells are alike. _
2, Older blastocyst, one half (e.) of which is the embryonic, the other {ir.)
the trophoblastic area.
JSstwesn 100 anrf 107
ifiH;
3
|||iiip^=:|ii
liiilli
1. ^°^^it^rts:rr:^z:!^'^''
V
SEGMENTATION
107
the Anamnia. In the next stage of development, however, their
behaviour is different, for in the latter group the blastopore is
formed at the edge of the blastoderm, while in the others it
always arises inside the blastoderm at the edge of the embryonic
shield, so that it is the latter structure which in its future
conduct is comparable to the Anamnian blastoderm.
In the Amniota the groAvth of the blastoderm over the yolk
goes on independently of the development of the blastopore and
of the embryo ; only at a comparatively late period is the yolk
finally enclosed at the vegetative pole. In the Monotremata,
however, this enclosure is effected with great rapidity, and as
the edges meet there is produced a spot where yolk, upper layer,
and lower layer are all continuous with one another. This
(accepting Assheton's interpretation) is the proper explanation
of what Wilson and Hill have identified erroneously with the
primitive plate of Reptiles (see Fig. 92).
In the remaining Mammalia the egg, as we have seen, is small
by loss of yolk, and its cleavage is holoblastic.
In the Marsupial Dasyurus (Fig. 68) a curious phenomenon
occurs before cleavage, the extrusion of the yolk-body at
the vegetative pole. The first two divisions are meridional and
at right angles to one another, the third again meridional. The
eight cells lying in a ring round the centre of the zona pellucida
now divide unequally, the smaller cells lying on that side on
which the yolk-body is situate. Further divisions, perpendicular
to the surface of the zona pellucida, lead to the formation of
a hollow sphere, the blastocyst, in which two regions become
later distinguishable (Fig. 59, 1, 2). In one hemisphere the cells
are small, in the other large. The former is the embryonic and
derived (according to Hill) from the small cells of the sixteencelled stage, and therefore from the vegetative hemisphere, since
it is on this side that the yolk-body was extruded. The latter
hemisphere is the trophoblastic, and derived from the larger
cells (of the animal region of the egg) in the sixteen-celled stage.
In the embryonic hemisphere individual cells become amoeboid,
migrate below the surface, and there unite to form a lower layer
or ^ endoderm ' (Fig. 69, 3-6), which presently grows round the
mside of the blastocyst and forms a completely closed sac,
108
SEGMENTATION
V
the yolk-sac or umbilical vesicle. The remaining cells of
the embryonic hemisphere become cubical or columnar, and
are thus sharply marked off from the flat elements of the
trophoblast.
In the Placental Mammals the first division is meridional
(Fig. 60). After this segmentation is irregular, and results in
a spherical mass of cells, in which an outer layer of cubical
soon becomes differentiated from an inner mass of rounded
elements. By the absorption of fluid a cavity is then formed
between these two groups of cells except
at one point, the future embryonic pole,
where the inner mass remains adherent
to the outer layer. Thus the blastocyst stage is reached. The cells of the
outer layer or trophoblast (which will
give rise to the ectoderm of the false
amnion) now become flattened, while
the inner mass is differentiated into
a round embryonic knob of closely
packed cells (this contains the material
for the embryo and the ectoderm of
the true amnion) and a lower layer of
flattened cells (Fig. 60*). The latter
quickly grow round the inside of the
trophoblast and form the closed yolk-sac. Rarely (in the guineapig) the distal, lower or anti-embryonic wall of the yolk-sac is
never developed. The lower layer gives rise to the gut, the
yolk-sac epitheUum, and the allantois.
At the stage we have reached, therefore, the material for the
embryo, true amnion, yolk-sac, and allantois is shut up in
a completely closed sac, the trophoblast or false amnion. All
Placental Mammals pass through such a stage, however the
amnion may ultimately be formed, and in this respect differ
strikingly from the Marsupials, where the embryonic area is at
the surface of the blastocyst, and the trophoblast confined to
one hemisphere of the latter.
It will be noticed that in the Placental Mammals it is not
possible to state what relation exists, if any, between the axis
Fig. 60* . -  Blastocyst of
the mouse. The inner mass
has been differentiatedinto
embryonic knob (e.k.) and
lower layer {l.l.). tr., trophoblast.
V
SEGMENTATION
109
of the blastocyst -  ^the line drawn from embryonic to antiembryonic pole -  and the original axis of the ovum. In the
Marsupials, if Hill's interpretation is correct, these axes coincide,
but the vegetative becomes the embryonic pole.
LITERATURE
R. AsSHETON. A re-investigation into the early stages of the development of the rabbit. Quart. Journ. Micr. Set. xxxvii, 1894.
R. AssHETON. The segmentation of the ovum of the sheep. Quart.
Journ. Micr. Sci. x\i, 1898.
R. AssHETON. The development of the pig during the first ten days.
Quart. Journ. Micr. Sci. xli, 1898.
E. VAN Beneden. Recherches sur I'embryologie du lapin. Arch, de
Biol, i, 1880.
W. Heape. The development of the mole. Quart. Journ. Micr. Sci. xxvi,
1886.
0. HERTVsaa. Die ZeUe und die Gewebe. Jena, 1893.
J. P. Hn-L. The eariy development of the Marsupiaha, with special
reference to the native cat [Dasyurus viverrimus). Quart. Journ. Micr. Sci.
Ivi, 1910.
F. R. LuxiE. The development of the chick. New York, 1908.
W. Roux. Ueber die Zeit der Bestimmung der Hauptrichtungen des
Froschembryo. Ges. Ahh. xvi, Leipzig, 1883.
J. RucKERT. Die erste Entwickelung des Eies der Elasmobranchier.
Festschr.f. C. von Kupjfer, Jena, 1899.
R. Semon. Die Furchung und Entwickelung der Keunblatter bei
Ceratodusforsteri. Zool. Forschmigsreise in Australien, 1901.
R. Semon. Zur Entwickelungsgescliichte der Monotremen. Zool.
Forschungsreise in Australien, ii. 1, 1894.
L. Will. Beitrage zur Entwickelungsgeschichte der ReptiUen, Zool.
Jahrh. vi, 1893.
==CHAPTER VI THE GERMINAL LAYERS==
By the germ-layers we understand certain groups of cells which
contain in themselves the materials for certain definite groups
of organs and tissues. These groups of cells are definitely
separated from one another at an early period of development,
and the process of their separation is spoken of as the formation
of the germinal layers.
The germinal layers in a Vertebrate are three in number, the
ectoderm, the endoderm, and the mesoderm. The ectoderm is
that group of cells which contains within itself the material for
the formation of the epidermis and epidermal derivatives like
hair, feather, skin-glands, the enamel of the teeth, the nervous
system both central and peripheral, and the sense organs, and
further the stomodaeum and proctodaeum, or entrances to the
mouth and anus ; the endoderm contains the material for the
lining epithelium of the alimentary canal and its outgrowths,
such as gill-slits, thyroid, thymus, lungs, liver, pancreas, bladder ;
while from the mesoderm-  with which we include the notochord
- skeleton and connective tissues, muscles, blood and vascular
system, coelom and urogenital organs will be derived.
The germ-layers are thus definable by thek fate in development. They may also be defined with reference to their position
in the embryonic body when they have been definitely segregated
from one another, for then the ectoderm is the outside layer,
the endoderm the inside layer, while the mesoderm with the
notochord is in between. Prior to that moment, however, it is
difficult if not impossible, to give generaUy valid definitions of
these sets of cells by their position, since the method of theur
origin from the different cells into which the substance of the
ovum is divided by cleavage varies in the several groups.
In a Vertebrate the germinal layers are segregated durmg
a process which is known as the formation and closure of the
VI
THE GERMINAL LAYERS
111
blastopore, or in an older terminology ' gastrulation the ' gastrula ' being the name bestowed on this stage in which a new
cavity, the ' archenteron ' or primitive gut, is formed and is in
communication with the exterior by an aperture, the blastopore.
This opening, and -ndth it the germinal layers, is from the first
bilaterally symmetrical. This is true of all Vertebrates, but in
the method of its origin the phylum must be divided into two
great groups, those in which the blastopore arises at the edge
of the blastoderm -  ^the Anamnia -  and those in which it appears
inside the blastoderm -  the Amniota. By the help of the Gymnophiona, however, the gap between the two may be bridged.
Anamnia
We shall begin with the Anamnia, in which the conditions are
much simpler.
As a type we shall take the common English frog {Eana
iemporaria) .
The first sign of the formation of the germ-layers is given as
soon as segmentation is at an end by the appearance of the
structure known as the dorsal lip of the blastopore (Fig. 61).
This is a short, deeply-pigmented rim bounding a groove, placed
parallel to the equator, and a little below it (about 25°) at that
point in the boundary between the pigmented and unpigmented
regions of the egg where the latter area is most extensive. This
is the side on which the grey crescent was formed and the original
unpigmented area so increased. The plane which includes the
egg-axis and the dorsal lip will shortly become the median
longitudinal or sagittal plane of the embryo ; it coincides evidently with the plane of symmetry of the unsegmented ovum.
The egg is still in the position into which it turned at the time
of insemination with its axis vertical, and the heavy white pole
below. The changes that now take place as seen from this
vegetative pole are as follows. The rim of the groove begins
to travel downwards over the surface of the egg towards the
vegetative pole, the area over which it passes becoming covered
by cells which are as deeply pigmented as those of the animal
portion of the egg. At the same time the rim elongates, becoming
crescentic ; in other words, the processes of rim formation and
112
THE GERMINAL LAYERS
VI
overgrowth are extended to the right and left along the margin
of the pigmented area, and the lateral lips of the blastopore come
Fig. 61. -  Diagrams of the closure of the blastopore in the egg of the
common frog {R. temporaria). In a-d the egg is viewed from the vegetative pole, in E, F from below. 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.
into being. As the dorsal lip (the middle region of the rim)
continues on its course towards the vegetative pole, and as
continually fresh parts are drawn into the process at the sides,
the blastoporic lip becomes first semicircular, and then three
VI
THE GERMINAL LAYERS
113
parts of a circle, until finally, when that part which is diametrically opposite to the dorsal lip, namely the ventral lip, also
begins to grow down, it attains the form of a circle enclosing
the still uncovered portion of the vegetative hemisphere, the
yolk-plug. The dorsal lip has now moved down to or a little
beyond the vegetative pole.
At this moment the whole egg begins to rotate about a horizontal axis in the opposite direction to that in which the dorsal
lip moved ; and this rotation continues -  the circle of the blastopore becoming smaller all the time -  until the dorsal lip has
returned, rather beyond the point from which it started, to the
new equator, or horizontal plane through the centre of the egg.
The end now occupied by the blastopore is posterior. The angle
subtended by the arc traversed by the dorsal lip -  both before
and during the rotation -  is 75°, and the angle through which
the whole egg rotates is 100°. It follows that the vertical line
now drawn through the centre of the egg, which will be the
dorso-ventral line of the embryo, makes the same angle of 100°
with the original egg-axis ; that the animal pole is situated below
what will be the anterior end of the embryo (Fig. 62, f), since
the blastopore is posterior ; and that the antero -ventral haK of
the embryo is developed over the animal, the postero -dorsal half
over the vegetative hemisphere of the egg. The dorsal and ventral
lips are now actually dorsal and ventral.
It is clear that the lip of the blastopore which is thus formed
and closed arises along the whole of the boundary between small
pigmented and large yolk-cells, and that the process is bilateral,
taking place, as it does, first and most rapidly at the dorsal lip,
last and least rapidly at the ventral lip, and at an intermediate
rate at the lateral lips in between.
The examination of sections (Fig. 62) will now show us that
the closure involves (1) a movement of the yolk-cells into the
segmentation cavity together with (2) an overgrowth and ingrowi^h of cells at the blastoporic lip, resulting in the formation
of a new cavity, the ' archenteron ' ; and that during the process
the material for the germinal layers is brought into position and
laid down.
A sagittal section of the egg passing through the dorsal lip
1355 XT
114
THE GERMINAL LAYERS
VI
at its first appearance shows the groove placed about 25° below
the equator in the zone of intermediate cells. The radial disposition of the cells immediately about the groove marks the
beginning of a process of overgrowth and ingrowth which becomes
more obvious a little later, when it is seen that a fold of small
cells has grown over a certain area of yolk-cells. This fold consists naturally of two sheets, an outer and an inner. The cells
of the outer sheet resemble closely the small pigmented cells of
the animal hemisphere into which they are uninterruptedly continued ; like the latter, they are arranged in about four layers,
the outermost of which is epithelial. At the lip of the blastopore
the outer passes into the inner sheet, the cells in the outermost
layer of the former being gradually turned over into the innermost layer of the latter. This inner sheet also consists of several
layers of cells, the innermost of which is pigmented and epitheUal, the remainder being more irregularly disposed. The inner
sheet forms the outer, or, as it will be when the egg has rotated,
the upper wall of the slit-like cavity between itself and the yolksurface now covered up. This cavity is the archenteron and the
inner sheet of the fold is its roof ; the original vegetative surface
of the egg forms its floor.
This overgrowth and ingrowth of cells, with consequent formation of an archenteric cavity, takes place in an exactly similar
fashion at the lateral (Fig. 63, a) and ventral lips. By the time
the latter has appeared the archenteric cavity is much enlarged,
first by its being extended in an anterior direction into the yolkcells that have meanwhile been pushed up into the segmentation
cavity on the dorsal side, and secondly in a lateral and finaUy
a ventral direction by a movement of the mass of yolk-cells
towards these regions of the egg also. The segmentation cavity
is thus first reduced to a small space upon the ventral side and
then obliterated altogether. In a small percentage of cases
however, the segmentation cavity communicates with the front
end of the archenteron, is surrounded by yolk-cells, and mcorTiorated in the front end of the gut.
' t the shifting of the heavy yolk-cells to the ventral s.d
tZ alters the eentre of gravity and so ca,.es the rotafou of
the egg until equilibrium is regained.
arch
mes
mes. Y.
F, After rotation ^'*''^°P°'^'^- before rotation ; e, During rotation ;
archenteron; y p! yolk fri^f/-'^ segmentation cavity; arcL,
formed below th;;^! ^ ^'^"'^ = mesoderm
pushed into the segment; Sty."""^"'" ''""^'^ '^'^"^ "^'^ ^-^k-cella
116
THE GERMINAL LAYERS
VI
With the exception of the yolk-plug the outer surface of the
egg is now covered by a sheet of small cells, disposed in about
four layers, the outermost of which is epithelial and pigmented.
This sheet is the ectoderm. In part it comes from the original
animal cells which formed the roof of the segmentation cavi. r â–  but
part of it is derived from the outer sheet of the blastoporic fold.
The notochord and the dorsal mesoderm are differentiated out
of the roof of the archenteron (Figs. 63 B, 64). The latter sheet
of cells becomes split into (1) a thin layer next the cavity (this
TljC.h
es2
252
Pi
Fig 63 - Transverse sections of the frog's egg. A, During the closure
of The blastopJie • B, After, mes. 2, mesoderm differentiated from the
yoM Tus^^^^^^^ segmentation cavity (in B these are seen to be
Central); U., lateral lip of the blastopore; n.c/^., notoehord.
will be the roof of the ahmentary canal) and (2) a layer next
the outside. This outer layer is divided into (a) a median strip
or rod, which is the notochord, and (6) two lateral shee s, the
dorsal mesoderm. The notochord is not separated miti after
the sheets of mesoderm have been detached. The separation o
both notochord and mesoderm begins at the anterior end and
proceeds backwards. At the lip of the blastopore there is thus
for a time an undiiferentiated mass of tissue in which ectoderm
notochord, mesoderm, and roof of the alimentary ^canal are all
continuous (Fig. 62, e). It will be remembered that the front
end of the archenteron arises by an extension of that cavity
into the yolk-cells ; here, therefore, yolk-cells form the roof, and
it is from them that the anterior portions of notochord and
VI
THE GERMINAL LAYERS
117
dorsal mesoderm are formed. The posterior portions, however,
arise in that part of the archenteric roof which comes into position
as the inner sheet of the blastoporic fold.
The ventral mesoderm (Fig. 63, b) has a similar double origin.
In front the floor of the archenteron is formed of the yolk-cells
pushed into the segmentation cavity ; the cells next the ecto
TLcTl
I^G. 64.-  Three stages in the differentiation of the roof of the archenteron
in the irog. arch, archenteron; n.ch., notochord ; mes., dorsal mesoderm.
derm subdivide and become mesoderm. Behind mesoderm arises
from the inner sheet of the fold at the ventral lip. At the sides
of the embryo dorsal and ventral mesoderm pass continually
into one another. The middle layer, therefore, taken as a whole,
arises anteriorly and ventrally from the yolk-cells, posteriorly
and dorsally from the blastoporic overgrowth ; the former is in the
onginal animal, the latter in the original vegetative hemisphere.
Smce mesoderm is formed also at the lateral lips, the two
sheets of this tissue which flank the notochord aje necessarily
118
THE GERMINAL LAYERS
VI
continuous, around the blastopore (Fig. 64*), with the mesoderm
at the ventral lip (Fig. 62, e) ; only at the dorsal lip, where the
notochord is formed, is there an interruption in the middle layer.
The endoderm or lining of the gut cavity is what is left of the
roof and floor of the archenteron, the roof of the gut being
the thin layer left when the notochord and mesoderm have been
detached, the floor the bulky mass of yolk-cells after the separation of the ventral mesoderm.
It must be remembered that though the differentiation of
these germ-layers is only completed when the blastopore has
closed, it has in reality been in progress during the earlier stages.
fie.
Fro 64* - Horizontal section of an older stage showing the sheets of
mesoderm passing back into the lateral Ups of the blastopore (b.j).).
It stiU remains for us to discuss very briefly the origm of
the cells from which the blastoporic fold is derived, that is, the
origin of parts of each of the three germ-layers. The inner layer
of the fold is certainly derived neither wholly from the smaU
cells of the animal hemisphere, nor whoUy from the large cells
of the vegetative hemisphere, but from the region about the
egg-equator, in which the cells are of a character intermediate
between these two (Fig. 62, i, z.). The outer layer of the fold
comes from the same source, and from an extension of the roof
of the segmentation cavity. These intermediate cells divide
rapidly and give rise to the fold, which, as we have seen, contains ectodermal, endodermal, and mesodermal elements.
VI
THE GERMINAL LAYERS
119
To sum up, the ectoderm of the frog comes partly from the
cells of the animal hemisphere, partly from the intermediate
cells ; the endoderm in part from the latter, in part from the
yolk-cells, while the mesoderm and notochord have a similar
double origin ; and the materials for these layers are brought
into their definitive positions during the bilateral closure of the
blastopore, which arises all along the line separating animal from
vegetative cells.
We shall see that a similar statement may be made for the
remaining Anamnia.
Fig. 65. -  ^Formation of the germ-layers in Petrornyzon. (After Scott.)
A, Sagittal section ; b, c. Transverse sections of two stages ; arch., archenteron ; d.l., dorsal lip of the blastopore ; n.ch., notochord ; d.m., dorsal
mesoderm ; v.m., ventral mesoderm ; m.t., medxillary tube (here a solid
wedge of cells).
Cyclostomata
In Petrornyzon (Fig. 65) the formation and closure of the
blastopore, the origin and extension of the archenteron, resemble
the same processes in the frog, with the exception that a ventral
lip is never developed. The ventral mesoderm is diflferentiated
from the yolk-cells pushed into the segmentation cavity, as in
the frog, and these latter cells form the floor of the gut. They
give rise, however, to much more than that, since the roof of
the archenteron is converted wholly into the notochord and the
gut is then completed by the upgrowt.h of yolk-cells from the
sides and underneath the notochord. The dorsal mesoderm arisea
m connexion with the overgrowth at the lip of the blastopore
120
THE GERMINAL LAYERS
VI
In the Myxinoids (Fig. 66) segmentation produces a blastoderm at one end of the elHpsoid egg. At one point in the edge
of this blastoderm a dorsal blastoporic lip appears, and the
material for the germ-layers of the embryo is laid down during
the bilateral overgrowth and ingrowth of cells in this region.
The yolk is not wholly covered by this process, but as soon as
-piQ, 66-  Bdellostoma. Overgrowth of the posterior edge or dorsal lip
of the blastoderm over the yolk, d.l, dorsal lip (posterior edge) ; v.l,
ventral lip (anterior edge) ; op.r., operculum of the shell. (After Bashford
Dean.)
the body of the embryo is formed all parts of the edge of the
blastoderm grow down and the blastopore eventually closes at
the vegetative pole.
Elasm obe anohh
Germ-layer formation begins with the appearance at one point
in the edge of the blastoderm of a fold or overturning of cells
of the superficial layer. This point is, as will appear, in the
middle line and at the posterior end. The fold, the rim of which
is the dorsal lip of the blastopore, is slightly raised and covers
over a space-  the beginning of the archenteron-  between itself
and the yolk (Figs. 67, 68). By the continued backward growth
of the fold and by the ingrowth of its under layer the archenteron
attains a considerable length. The floor of the archenteron is
Fig. 67. -  Overgrowth of the lip of the blastopore and formation of the
embryo in Elasmobranchs. (a-c after Riickert, d-f after Ziegler.) c.s.,
caudal swelling ; l.L, lateral lip. In r the formation of a lip has extended
almost to the anterior edge. In d, e, the medullary folds are still open, in
r they are closed.
P. 120
122
THE GERMINAL LAYERS
VI
formed of yolk, into which yolk-nuclei subsequently make their
way ; its roof consists of a columnar epithelium derived in
part from the overturning of cells at the lip of the blastopore,
in part possibly from the posterior marginal cells of the lower
layer.
But while this process is taking place at the dorsal lip, that is,
at the median posterior margin of the blastoderm's edge, it is
also being extended, though in a far less degree, to the neighbouring regions, the lateral lips, on the right and on the left.
The archenteron thus comes to assume a crescentic shape, with
a median anterior prolongation ; the latter underlies the embryonic portion of the blastoderm, while the crescentic part is
wholly extra-embryonic, and remains very shallow, though it is
subsequently prolonged to the right and left round the edges of
the blastoderm until a slight overgrowth is formed even at the
anterior margin.
With the overgrowth at the lips of the blastopore the material
for the germinal layers is laid down (Fig. 69). The superficial
layer is now the ectoderm. The mesoderm consists of two
parts : (1) two sheets of cells lying one on each side of the
middle line over the embryonic portion of the archenteron ;
posteriorly these sheets pass into the caudal swellings-  two
thickenings at the edge of the blastoderm, one on each side of
the middle line -  where they are continuous with the roof of the
archenteron, out of which they have been differentiated ; (2) the
formation of mesoderm is, however, not limited to the parts
immediately adjacent to the dorsal lip, but is carried on at the
lateral lips, and, as these extend forwards round the whole edge
of the blastoderm, at the anterior edge as well. This extraembryonic mesoderm is naturally continuous in the caudal
swellings with the embryonic mesoderm first described ; it takes
part only in the formation of the area vasculosa.
The notochord is formed from a median strip of cells which
is cut out of the roof of the archenteron ; the process, like the
differentiation of the mesoderm, takes place from before backwards. With the separation of the notochord and mesoderm
the remainder of the archenteric roof is endoderm, and gives rise
to the alimentary canal, the front end and sides bending dovm
VJ
THE GERMINAL LAYERS
123
Fig. 69.-  Five successive transverse sections through the hinder
(embryonic) portion of the blastoderm of the dog-fish during tlie formation
ot the germinal layers a is posterior, cutting the two caudal sweUings ;
E, Anterior through the head of the embryo, arch., archenteron; mes
mesoderm; e.m., embryonic mesoderm; ex.m., extra-embryonic mesoderm ; w.c^., notochord ; lateral lip of the blastopore
124
THE GERMINAL LAYERS
VI
and meeting to form the ventral wall. The yolk in the floor of
the archenteron plays no part in this process (Fig. 70).
Up to the present it is the posterior edge or dorsal lip which
has been principally active, but now the anterior and lateral
margins of the blastoderm become exceedingly vigorous and
begin to grow over the yolk, the overgrowth being accompanied,
as stated above, by a slight marginal invagination ; and eventu
y.n.
Fig. 70.-  Two stages in the formation of the gut of the dog-fish by the
bending down and fusion of the edges of the roof of the archenteron.
y.n., yolk-nuclei.
ally the anterior edge makes the whole ckcuit of the yolk, passmg
round the vegetative pole and reappearmg behind the embryo
as the ventral lip of the small ' yolk-blastopore ' (Fig. 71). At
the dorsal hp backgrowth of the caudal sweUings is responsible
for the posterior elongation of the body of the embryo alone,
the body being raised above the surface of the yolk. Where the
body passes into the hinder edge of the blastoderm growth of
the latter ceases, but the lateral edges immediately adjacent
to this point swing backwards untU they bound a narrow
median strip of yolk by which alone the aperture at the dorsal
lip now communicates with the rest of the blastopore.
as
B
a.e = i/.l.
C. D.
f M^*^" Extension of the blastoderm over the yolk after formation and
loldmg ofiE of the embryo in an Elasmobranch. a, The lateral lips liave
swung back parallel to one another behind the dorsal lip, so enclosino- a
narrow strip of yolk. B, Side view of the same, c, The anterior ed-o
(«.e.) has passed beyond the vegetative pole, and in d it appears behind the
embryo as the ventral lip (yi.) ; y.b., yolk- blastopore.
P. 124
VI
THE GERMINAL LAYERS
125
Teleostei
The processes are essentially the same as in the Elasmobranchs.
Blastopore formation begins at the posterior edge, where the
Fig. 72.-  Growth of the blastoderm over the yolk after the formation of
the material for the embryo in the Teleostean fish Serramis. (After Wilson )
d.L, dorsal hp of the blastopore (posterior edge of the blastoderm) â–  a e
anterior edge of the blastoderm or ventral lip {v.l.) of the blastopore •
s.c, segmentation cavity ; o.g., oil-globulc. '
backward growth of the dorsal lip with concomitant development of an archenteric cavity gives rise to the body of the
embryo, but the process is extended to the lateral and anterior
edges, where there is a slight invagination. By the growth of
Fig. 73.-  Sagittal sections through the blastoderm of Serranm during
the formation of the germinal layers. (After Wilson.)
A, Beginning of overgrowth at dorsal lip {d.l.).
B, Overgrowth at anterior edge.
c, Later stage of posterior edge. t u i
D, The anterior edge has become theventraUip {v.l.); n.cA., notochord ;
end., endodorm ; m.p., medullary plate ; par., parablast (periblast) ; y.f.,
yolk-plug ; K.v., Kuppfer's vesicle.
Fig. li.- Serra^ms. Transverse sections showing differentiation of the
roof of the archenteron into notochord
(n.ch.), mesoderm (mes.), and cndodprm
{end.); j^ar., parablast (periblast). (After
Wilson.)
aic. 3
Fig. 75. -  Serranus. Formation of the gut (a/.c.) by the
bending down of tlie sides of the
roof of the archenteron. s.n.ch.,
sub-notocliordal rod; aid., cndoderm. (After Wilson.)
VI
THE GERMINAL LAYERS
127
these extra-embryonic edges the yolk is finally enclosed and the
anterior margin is then the ventral lip (Fig. 72). Notochord
and mesoderm are differentiated in the roof of the embryonic
part of the archenteron, the rest of this layer giving rise to
the alimentary canal, as in Elasmobranchs. Extra-embryonic
mesoderm arises at the remaining edges of the blastoderm
(Figs. 73-75).
v.l.
Fig. 76.-  Formation of the germ-layers in Ganoid fishes, a, b, in the
Sturgeon {Acipenser) (after Bashford Dean) ; c, d, in Amia (after Sobotta) ;
arch.^ archenteron ; d.l, dorsal lip ; v.l., ventral lip ; n.ch., notochord ;
mes., mesoderm.
Ganoidei
Our knowledge of the differentiation of the germinal layers is
very slight, but it is known that the closure of the blastopore
is bilateral, and that mesoderm is formed at its lips, the notochord in the middle dorsal line (Fig. 76).
128 THE GERMINAL LAYERS VI
DrPNOi
The holoblastic egg of Ceralodus resembles that of the frog
very closely in the development of its archenteron. The roof
Fig. 77. -  Formation of the germ-layers in Dipnoi. A, B, in Ceralodus
(after Semon) ; c, D, in Lepidosiren (after Graham Kerr), arch., archenteron-; d.l, dorsal lip ; n.ch., notochord ; ines., dorsal mesoderm.
of this cavity, however, takes no part in the formation of the gut,
but is differentiated simply into median notochord and lateral
plates of mesoderm. The yolk-cells then grow up to complete
the dorsal wall of the aUmeutarx, canal (Fig. 77, A, u).
VI
THE GERMINAL LAYERS
129
Lepidosiren resembles the frog in all respects, except that the
yolk is more vokimmous and that a ventral lip is never developed
(Fig. 77, c, D).
Urobelotjs Amphibia
The method of germ-layer separation is here practically identical with that which is observed in the frog, except in one
important respect. In the bilateral closure of the blastopore,
the presence of a ventral as well as of a dorsal lip (Fig. 78, A)
and the formation of the mesoderm from a double source, the
two groups closely resemble one another ; but while in the frog
the under layer of the roof of the archenteron persists as the
dorsal lining of the alimentary tract, in the Urodeles the roof
of the archenteron becomes wholly converted into the notochord,
as in Petromyzon, and the gut must be completed dorsally by
an ingrowth of yolk-cells from the sides (Fig. 78, b, c).
The Anurous Amphibia, such as the toad, generally resemble
the frog in this matter, but in one case the notochord is described
as being formed from the middle streak of the whole thickness
of the roof, and even in the frog such a procedure may be
experimentally instigated by subjecting the embryos to the
influence of cane sugar and other substances.
A comparison of these processes in the small-yolked and the
large-yolked types shows that :
1. The blastoderm of the large-yolked corresponds to the
animal region of the small-yolked egg, the yolk to the vegetative
part, and that the edge of the blastoderm in the former is equivalent to the boundary between animal and yolk cells in the latter.
2. In both this bounding line becomes in its entirety the lip
of the blastopore (except where the ventral lip is absent), the
posterior point of the edge in the large-yolked being equivalent
to the dorsal lip of the small-yolked, the anterior point to the
ventral lip.
3. In both the germinal layers are laid down during the
bilateral closure of this blastopore, the notochord stretching in
front of the dorsal lip, the mesoderm springing from the lateral
lips in two sheets which are continuous with one another behind
the ventral lip.
1355 T
130
THE GERMINAL LAYERS
VI
4. The principal points of difference are two. First, the closure
of the blastopore in Elasmobranchs, Myxinoids, and Teleostei,
is effected in two periods ; during the first the overgrowth is
almost confined to the dorsal lip and produces the material for
-piQ. 78 - Formation of the germ-layers in the Axolotl.
A, Sagittal section after completion of the blastopore and rotation of
the egg.
B, Transverse section of the same stage. i. u a
c Dorsal part of a transverse section of a later stage, n.ch., notochord;
d.l.', dorsal hp ; v.l, ventral lip ; mes.v., mesoderm formed ^Wentral hp ;
mei.l, dorsal mesoderm ; mes.2, ventral mesoderm (from the yolk-cellh
pushed into the segmentation cavity) ; end., endoderm.
the formation of the embryo ; in the second the yolk is gradually
covered by an extension of the blastoderm in which the lateral
and anterior margins are alone concerned. Secondly, in these
cases a part only of the blastoporic hp is involved in the formation of the embryo, the lateral and ventral lips remaining wholly
extra-embryonic.
VI
THE GERMINAL LAYERS
131
Gymnophiona
In this group the egg is so laden with yolk that in it segmentation nearly approaches the meroblastic type and results in a
blastoderm lying on a partially divided yolk. This blastoderm
consists of a superficial epithelium of columnar cells, covering
Fig. 79.-  Formation and closure of the blastopore in the Gymnophiona.
A-D, Surface views of the blastoderm of Hypogeophis. The lateral lips are
seen to meet behind, and so form the ventral lip ; y.p., yolk-plug (after
Brauer). e. Embryo of Ichthyophis lying on the partially segmented yolk
which is still uncovered by the blastoderm. (After the brothers Sarasin.)
several irregular layers of scattered cells which are more abundantly supplied with yolk. The cavities between these cells are
equivalent to the ordinary segmentation cavity. Below these
again is the yolk, divided at its surface into cells, and containing
nuclei scattered through its substance. Immediately round the
blastoderm the surface of the yolk is also partially segmented.
At one point-  the posterior middle point-  of the edge of this
I 2
132
THE GERMINAL LAYERS
VI
blastoderm the dorsal lip appears (Fig. 80) ; it exhibits the
usual radiate arrangement of cells. The lip quickly grows back
and so produces a long archenteron which comes to open into
80.-  Formation of the germ-layers in Hyi)0!7eoi)te. (After Br auer.)
A-c Sagittal sections of three successive stages, d, Transverse section
Lough^he blastopore and yolk-plug {y-v.) ; s.c, ^^tlX /f
into which in B and o the archenteron {aroh.) opens ; U., dorsal hp , l.L,
lateral lip ; and vX., ventral Up.
the segmentation cavity in front. The roof of the archenteron
which seems to be derived entirely from the superficial layer of
the blastoderm, consists of a plate of columnar cells, its floor of
the partially segmented yolk.
VI
THE GERMINAL LAYERS
133
The process of overgrowth is not limited to the dorsal lip,
but extends to the immediate right and left. Surface views
(Fig. 79, a-d) show that the transversely placed li]p soon becomes
crescentic, and that the horns of the crescent then grow not
only backwards, but towards the middle line as well, approaching
one another until they meet and so form what is the ventral
lip of the now circular blastopore. In section it is seen that
there is a slight ingrowth at the lateral and at the ventral lips
of a plate of cells continuous with the similarly formed jolate
Â¥iG. 81.-  Transverse sections of HypogeopMs showing the differentiation
ot the root of the archenteron into notochorcl (nxh.) and mesoderm, and
Z fXf (Iftttrarxg"' ^"'^-^
which forms the roof of the archenteron in front ; beneath the
plate is a slit-like space, also, of course, archenteric ; in the midst
of the blastopore is the projecting typically Amphibian yolk-plug.
But m spite of this resemblance there is a very serious difference between the ventral lip of the Gymnopliiona and that of
ail other Anamnia. For while in the latter the whole of the edge of
the blastoderm or small-celled area is converted into a blastoporic
hp, the posterior point being the dorsal, the diametrically
opposite anterior point becoming sooner (in small-yolked eggs)
or la er (m large-yolked eggs) the ventral lip, and while consequently the whole of the vegetative surface of the egg is covered
up when the blastopore closes, in the former the anterior and
134
THE GERMINAL LAYERS
VI
a large part of the two lateral edges take no iiart in this process,
which is confined to the posterior and immediately adjacent
portions of the edge ; this small portion gives rise to the dorsal
and two lateral lips, which latter by their fusion produce the â– 
remarkable similitude of the ventral lip of other forms. As
a result the vegetative hemisphere is still uncovered when the
blastopore has become circular (Fig. 79, d, e). The importance
of this fact for the correct understanding of the relations of the
blastopore to the blastoderm in the Amniota cannot possibly be
over-emphasized.
To return to the germinal layers. The superficial layer is now
the ectoderm. The roof of the archenteron becomes divided
into a median strip-  the notochord, and two lateral sheets-  the
mesoderm which are continuous with one another behind the
yolk-plug by means of the cell-plate invaginated at the lateral
and ventral hps (Fig. 81). The mesoderm has in fact precisely
the same relations as in other Anamnia at this stage. The
notochord passes back into the dorsal lip. No additions are
made to either notochord or mesoderm from any other source.
The roof of the gut (endoderm) is completed by upgrowth and
ingrowth of vegetative cells underneath the midcUe layer.
Amniota
Whereas in the Anamnia the blastoporic lip appears at the
edge of the blastoderm, in the Amniota it hes wholly within the
latter. The blastopore leads into an archenteron, and with the
formation of these structures the materials for the germinal
layers are laid down. Only in the more primitive forms is the
archenteric cavity well developed ; usually it is much reduced
and represented only by the ' neurenteric ' passage or ' chordacanal In primitive forms the upper and lower layers are still
united at the point where the blastopore and archenteron arise,
and both layers may perhaps be said to share in their formation ;
but in most cases all these parts are derived from the upper
layer of the blastoderm alone, the subsequent fusion with the
lower layer being purely secondary. The edge of the blastoderm,
which is entirely independent of the blastopore, grows steadily over
the surface of the yolk, finally enclosing it at the vegetative pole.
i
IPiG 82 - Three stages in the formation of the blastopore at the hinder
end of the embryonic shield of a Reptile {PlaUjdacUjlus). Sm'face views.
(After Will.)
P. 1S5
II
VI
THE GERMINAL LAYERS
136
The Reptiles will be considered first as the whole process is
far clearer in them than in the other two groups.
Rbptilia
There is distinguishable in the blastoderm at the close of
segmentation a circular or oval area placed excentrically towards
the posterior end ; this area is the embryonic shield. The upper
layer of the blastoderm consists of cyHndrical cells in the embryonic shield, of flat cells in the surrounding region ; below it
is the segmentation cavity. The lower layer is an irregular sheet
of scattered rounded cells, not arranged at present in an epithelium, and is constantly being reinforced by the addition of
cells from the nucleated yolk beneath. Between the lower layer
and the yolk is a shallow cavity, the subgerminal cavity. In
some forms, such as Platydactylus and Lacerta, there is one point
in the margin of the embryonic shield where upper and lower
layers are continuous ; this is the primitive plate, and it is
situate at what will be the hinder end (Fig. 83, a). The lower
layer cells before long arrange themselves in a flat epithelium.
Meanwhile a depression has appeared in the primitive plate ;
this is the beginning of the archenteron, and its anterior margin
is the dorsal lip of the blastopore. Seen from the surface (Fig. 82)
the dorsal lip presents the appearance of a transverse rim bounding a groove at the hinder edge of the embryonic shield. The
rim rapidly becomes crescentic, the horns of the crescent turn
back, meet, and fuse behind the primitive plate which now
corresponds exactly to the Gymnophionan yolk-plug.
During the backgrowth of the horns of the crescent, which
are the lateral blastoporic lips, the cavity of the archenteron
has rapidly extended until it reaches the anterior end of the
embryonic shield (Fig. 83) ; the cavity is broad. The roof consists of a layer of columnar cells which at the dorsal lip turn
over in the ordinary way into the cells of the upper layer. The
floor is in front distinct from the lower layer, and here it consists of a single layer of cubical cells ; behind the dorsal lip -  in
the primitive plate-  it is much thickened, and from this thickenmg there proceeds backwards a narrow tongue of cells between
the upper and the lower layers.
136
THE GERMINAL LAYERS
VI
A transverse sectign (Figs. 84, a ; 86) through the blastopore
shows the mass of cells of the primitive plate flanked on each
side by a projecting blastoporic lip and sending out between
the upper and lower layers two lateral sheets of cells.
Fig. 83. -  Sagittal sections of the blastopore and archenteron in the
Gecko Platydadylus. (After Will.) a-e, Successive stages ; jj.^p., primitive
plate ; pd., lower layer or paraderm ; s.g.c, subgerminal cavity ; arch.,
archenteron ; d.l, dorsal lip ; y.p., yolk-plug ; mes.v., mesoderm formed
at the ventral lip.
The resemblance between these structures and those in the
Amphibian, and particularly the Gymnophionan egg when the
blastopore has become circular, is sufficiently obvious. The
dorsal and lateral lips (there is no ventral lip in the Reptiles)
clearly correspond in the two cases ; the mass of cells in the
primitive plate embraced by these lips is the yolk-plug ; the
Fio. 84. -  Four successive transverse sections through the blastopore
and archenteron of Plalydactylus. (After Will. )
A, Posterior section through the yolk-plug {y.f.) ; l.l, lateral lip ; 2^(1. ,
lower layer ; mes., mesoderm springing from the lateral lips.
B is more anterior, just behind the dorsal lip.
c is just in front of the dorsal lip, where the floor of the archenteron
{arch.) is still intact, and
D more anterior, where the archenteron communicates with the subgerminal cavity.
c
arc?-..
c
138
THE GERMINAL LAYERS
VI
cavity of invagination is the archenteron in which floor corresponds to floor and roof to roof ; lastly, the sheets of cells
projecting beneath the upper layer at the sides of and behind
the blastopore are the equivalents of the mesoderm formed at
the lateral and ventral lips in the Amphibia.
From this comparison it follows of course that cells which are
the morphological equivalents of the yolk-cells of the Amphibia
are to be found in the upper layer of the Reptihan blastoderm.
That layer, therefore, cannot be termed the ectoderm until the
process of invagination is complete.
The floor of the archenteron now fuses throughout with the
lower layer, and as soon as the fusion is completed perforations
-PTP 86 - Transverse section of the blastopore and yolk-plug (y.p.) of
thTS^itoise (Trionyx). (After Mitsukuri.) U., lateral lip ; > m/so^erm
produeed at the lateral lips ; pel., lower layer not yet detaehed from the
yolk (stippled).
begin to appear in tte fused layers (Figs. 83, E ; 84, e). They
seem to be unable to keep pace with the general gro^vth of the
blastoderm and to become first stretched and then fenestrated.
But to whatever causes the perforation may be due, the floor
of the archenteron with the underlying lower layer completely
disappears, and the archenteron then communicates freely with
the subgerminal cavity. The roof of the archenteron is now
inserted by its edges into the surrounding lower layer.
The median strip of the roof next thickens to form the notochord (Fig 85), and separates from the two lateral portions which
then become the mesoderm. The notochord passes posteriorly
into the dorsal lip. the plates of mesoderm into the latei^hps
of the blastopore, and here the latter are perfectly contmuous
with the mesoderm produced at the sides of and behind the
I
Fig 87*.-  Area pellucida of the lien's egg. a, After 12 hours , b, After
18 hours' incubation, as seen by transmitted light. J5r.£/., prnnitive groove ;
n.ch., notochord ; pr.am., pro-amnion.
P. 139
VI THE GERMINAL LAYERS 139
blastopore (Figs. 84, a, b ; 86). The mesoderm thus exhibits
all the relations which it has in the Anamnia.
The Uning epithelium of the alimentary canal (endoderm) is
derived from the lower layer, which grows in from the sides
below the mesoderm and notochord (Fig. 85, c, d). From this
layer the gut is subsequently folded off, the remainder being
yolk-sac epithelium. In several cases the lip of the blastopore
is not the only source of origin of notochord and mesoderm,
both receiving additions in front, and the mesoderm at the sides
also, from the lower layer.
Fig. 87. -  ^Formation of the primitive streak and groove of the chick by
proliferation of cells of the upper layer. Transverse sections.
A, At 10 hours. There is at present no sign of the primitive groove ;
the lower layer {'pd.) takes no part in the proliferation.
B, At 15 hoiu's. The primitive groove has appeared. It is occupied
by a projecting mass of cells, tlie yolk-plug {y.'p.), and bounded by the
lateral hps {U.). The proliferated cells spread out on cacli side as the
lateral sheets of mesoderm {mes.).
AVES
The conditions observed in the Birds are very readily derived
from and very easily understood in the light of those which
obtain in the Reptiles.
There appears in the posterior region of the blastoderm a proliferation of cells in the upper layer (Fig. 87, a) ; this rapidly
extends in the median line, and along it there appears a narrow
groove. The cell proliferation is the ' primitive streak ', the
groove the ' primitive groove ' (Fig. 87*).
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142
THE GERMINAL LAYERS
VI
This primitive groove is simply an elongated and laterally
compressed blastopore. In front of the anterior end -  the dorsal
lip -  the notochord is produced (Figs. 88, 89) ; to right and left
of the notochord are the sheets of mesoderm which, springing
from the sides -  the lateral lips -  of the groove (Fig. 87, b), are
continued into one another behind its posterior end, where there
may be an actual ventral lip (Fig. 90). The archenteric cavity
■n «^
j^G. 90. -  ^Anterior (a) and posterior (b) halves of a sagittal section
through the primitive streak and associated structures of the sparrow.
(After Schauinsland.) There is a sUght cavity, archenteron, below the
dorsal Hp (d.i.), and a well-marked ventral lip {vL). n.ch., notochord ;
p.s., primitive streak ; 7nes.v., mesoderm behind the ventral lip ; p.a.,
lower layer.
end.
mes.
ii.c/i.
Yict 91. ^Transverse section of the anterior end of the blastoderm of the
chick "at 15 hours showing the formation of anterior notochord (n.ch.) and
mesoderm (mes.) directly from the lower layer {end.) ; ec., ectoderm.
has, however, in most cases disappeared, though a vestige of it is
sometimes to be seen (Fig. 90) . Between the sides of the groove- 
which still exhibit the structure characteristic of blastoporic hps, is
merely a mass of cells-  representative of the yolk-plug (Fig. 87, b)
- fused with the lower layer. The so-called ' neurenteric canal ' ,
which appears later, is the sole remnant of the archenteron
together with the communication which we have seen to become
established between it and the subgerminal cavity in Reptiles.
The primitive streak and groove invariably originate in the
VI THE GERMINAL LAYERS 143
upper Icayer, fusion with the lower layer being merely secondary ;
only after the germ-layers have been formed can the upper layer
be described as ectoderm.
The notochord and mesoderm receive increments in front from
the lower layer (Fig. 91).
The gut (endoderm) is formed as in Reptiles.
Mammaija
In the Monotremata there is a long archenteron with a much
reduced lumen produced from the upper layer. The blastopore
is an elongated ' primitive groove '. The notochord and mesoderm have the usual relations to these structures. The interpretation put by Wilson and Hill on their observations -  namely,
that the dorsal lip and archenteron are derived from the ' primitive plate ' while the primitive streak and groove are of distinct
origin -  is probably erroneous. We may accept Assheton's
explanation that the ' primitive plate ' of the authors is simply
the point of final enclosure of the yolk by the blastoderm,
a precociously rapid process in this form, and that archenteron
and primitive groove are, as everywhere else, parts of one and
the same structure (Fig. 92).
We are still in ignorance of the formation of the germinal layers
in Marsupials, though we may hazard the conjecture that the embryonic area of the blastocyst wall will be found to behave like the
embryonic shield in Reptilia, that a blastopore and archenteron will
be developed near its posterior edge in connexion with which the
notochord and mesoderm will arise in the usual way, that the
archenteron will break through into the subgerminal cavity below
the lower layer, and that this layer will give rise to the gut.
This indeed is what occiurs in the Placental Mammals, the
only diflference being that here the embryonic area is from the
first enclosed in the sac of the trophoblast as part of the embryonic knob. This knob, as we have already seen, is, together
with the lower layer, differentiated from the original inner mass.
The embryonic area (Fig. 92*), derived from the embryonic
knob, behaves precisely as the embryonic shield of the upper layer
in Reptiles, giving rise to an archenteron and blastopore ; this event
is, however, postponed until after the amnion has been formed.
trek a
Fid. 132. Diagiain of the egg of Ornithorhynchus after formation of the
gorniinal layers. (After Assheton's modification of Wilson and HiU.) x, the
point at which the blastoderm has finally enclosed the yolk ; here the
upper layer (double line) and lower layer (broken line) are continuous with
one another and with the yolk. This is the ' primitive plate ' of Wilson and
Hill, a to p, primitive streak ; a, anterior end (dorsal lip) ; p., posterior
end. In front of a. is the archenteron (arch.), behind p. the mesoderm of
the ventral lip {mes.v.).
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Fig. 92*.-  Embryonic shield of the dog. (After Bomiet.) In the embryonic shield, where the cells are columnar, the nuclei are more closely packed
than in the surrounding trophoblast, where the cells are flat. At tne
posterior end is a notch, the blastopore (lower end in the fagure).
VT
THE GERMINAL LAYERS
145
When the archenteron has been developed it behaves in the
manner we are already acquainted with. Its floor fuses Avith
the lower layer, and then the two break away so that the archenteron comes to communicate with the subgerminal or yolk-sac
cavity (Fig. 93). The notochord is differentiated out of its
roof, the mesodermal sheets pass into the lateral lips and are
3
Fig. 93. -  ^a. Longitudinal section of the embryonic shield and blastopore
of the bat, VesperlUio. (After Van Beneden.) The archenteron (arch.) has
broken through into the subgerminal cavity [s.g.c.) or cavity of the blastocyst. Below tlie dorsal lip (d.l.) is the blastopore (so-called neurcnteric
canal), and behind this the yolk- plug {ij.j}.). (With this should be compared
Fig. 138, which shows a human embryo in the same stage.)
B, Transverse section showing the origin of the notochord [n.cli.) from
the roof of the rudimentary archenteron in the mouse. The floor of the
archenteron has already disappeared, mes., mesoderm ; 'pd., lower layer.
Above is the ectoderm of the medullar}^ plate.
continuous with one another behind the blastopore. Accessory
notochordal and mesoblastic material is proliferated in front from
the lower layer. After this the lower layer is endoderm, and
gives rise to the gut and yolk-sac, after growing in from the
sides underneath the notochord.
The archenteron may be well developed (as in VesperUlio), but
more usually is reduced to a narrow canal, the ' chorda-canal '
or, so called, ' ncurenteric ' passage.^
^ Neurenteric passage means properly the communication between the
medullary tube and the hmd end of the archenteron. See below, chap. vii.
1355 V
VI
THE GERMINAL LAYERS
147
The Relation between the Amniote and the
Anamnian Blastopore
The facts we have now reviewed will have made it evident
that there are certain features common to the separation of the
germinal layers in all Vertebrates.
Thus in all cases the material for the germ-layers is laid down
during an overgrowth and ingrowth of cells which takes place
at the lip of the blastopore during the formation and closure
of the latter. This closure is always bilaterally symmetrical,
beginning at the dorsal lip and taking place most actively there,
less actively at the lateral lips, and least of all at the ventral
lip. It leads to the formation of a bilateral archenteron, the
extent of which is greatest anteriorly, least posteriorly. The
layer that now remains outside is the ectoderm. The notochord
is differentiated out of the roof of the archenteron in the middle
line in front of the dorsal lip, while the mesoderm sheets which
flank the notochord pass back to the lateral lips and are confluent with one another behind the ventral lip.
A, 1-3, The closure of the blastopore in such a form as the frog ; 1, 2,
before, 3, after rotation of the egg. The blastoderm, or small-celled area,
is heavily stippled. Its whole edge, which becomes the lip of the blastopore, is represented by a thick continuous line, d.l., dorsal, v.l., ventral lip.
B, 1-3, Three similar stages in such a form as Lepidosiren, where the
ventral lip is absent. Only that part of the edge of the blastoderm which
becomes converted into a blastoporic lip -  namely, the posterior and immediately adjacent parts -  is indicated by the thick continuous line, d.l,
dorsal lip. '
c, 1, 2, The condition seen in the Gymnophiona, where still less of the
edge of the blastoderm-  only a small part at the posterior end, represented
by the thick line-  becomes the lip of the blastopore, but the lateral lips
swing back, meet, and fuse to form the ventral lip, v.l. Thus the yolk
(white) remains uncovered.
D, 1, 2, The Amniote blastopore. The heavily stippled area is the
embryomc shield, the central portion only of the Amniote blastoderm
but the equivalent of the whole blastoderm of the Anamnia. From the
posterior part of its margin a blastoporic lip is formed (d.l, dorsal lip)
and by the bending back and union of the lateral lips a ventral lip (v I )
as m the Gymnophiona. i' v
The lightly stippled area outside this represents the extra- embryonic
Fâ„¢,"? blastoderm; which is equivalent to the yolk-cells immediately
surrounding the blastoderm of the Gymnophiona ^
xlr^l^^-^l the unsegmented yolk (white). Thus the blastopore of the
f^t lTfC formed inside its blastoderm, but at the edge of what is equiva
Th« blastoderm, namely, the embryonic shield. ^
lUe yolk is finally covered later on by the growth of the blastoderm
k2
148
THE GERMINAL LAYERS
VI
So far there is general agreement. There is, however, a very
serious difference between the two great groups of Vertebrates
in respect of the reh^.tion of the blastoporic lip to the blastoderm
-  the cap of cells produced at the end of segmentation in a largeyolked egg or the area of small cells in a small-yolked egg -  for
in the Anamnia the blastopore arises from the edge of this
blastoderm (Fig. 94, a), while in the Amniota it arises inside it
(Fig 94, d). By the help of the Gymnophiona, however, the
second condition may without difficulty be derived from the first.
In the Gymnophiona (Fig. 94, c) (1) the blastoderm is an
oval area of columnar cells resting upon and surrounded by
a partially segmented yolk. (2) Only a part of the edge of the
blastoderm is converted into a blastoporic lip, namely, a small
region at the posterior end. Here a dorsal lip is formed and
lateral lips quickly follow ; the lateral lips then turn back,
encircling a small area of the yolk, behind which they meet and
fuse to form a ventral lip to the now circular blastopore. In
this process the anterior margin of the blastoderm is wholly
unconcerned. (3) The archenteron opens into the segmentation
cavity, notochord and mesoderm are derived from its roof, the
endoderm from the yolk-cells which lie in its floor. The notochord stretches in front of the dorsal lip ; the mesoderm sheets
springing from the lateral lips are continuous with one another
behind the ventral lip.
As a result of this peculiarity in the formation of the ventral
lip the yolk remains uncovered. In all other Anamnia, however,
where the ventral lip is developed from the anterior edge of the
blastoderm, the yolk is necessarily covered up by the closure of
the blastopore.
We turn now to the Amniota, to the Reptiles for instance,
and find (1) that the embryonic shield is a circular or oval
area of columnar cells resting upon a lower layer, and surrounded
by a zone of flattened cells. (2) At the posterior margin of this
embryonic shield upper and lower layers are continuous. Here
a dorsal lip is formed and lateral lips quickly follow ; the lateral
lips turn back encircling a small area of the outer zone of cells- 
where these are continuous ^\'ith the lower layer-  behind which
they meet and fuse to form (a virtual, in some cases an actual)
VI
THE GERMINAL LAYERS
149
ventral lip to the now circular blastopore. In this process the
anterior margiji of the embryonic shield is wholly unconcerned.
(3) The archenteron opens into the subgerminal cavity, notochord
and mesoderm are derived from its roof, the endoderm from the
lower layer. The notochord stretches in front of the dorsal lip,
the sheets of mesoderm springing from the lateral lips are continuous with one another behind the ventral lip.
It seems clear, then, that the embryonic shield of the Amniota
is the representative of the blastoderm of the Gymnophiona
(and of all Anamnia), while the marginal zone of the upper
layer, together with the lower layer with which it is at one
point -  ^the primitive plate -  still united, represents the yolk-cells
or nucleated yolk.
In passing from the Gjrmnophiona to the higher Vertebrates
we have therefore to suppose that with the further increase of
yolk segmentation has become restricted not to the blastoderm
alone (as in Fishes), but to the blastoderm and those circumjacent and subjacent cells which in the Gymnophiona are partially
segmented from the yolk. In the most primitive Reptiles the
lower layer cells are still crowded with yolk and still retain
a connexion, in the primitive plate, with the marginal cells of
the upper layer. In other Reptiles, in Birds, and in Mammals this
primitive connexion is lost, and it is only secondarily, after the
formation of the primitive groove and streak, that the upper
fuses with the lower layer.
The Gymnophionan condition must in turn be derived from
some Anamnian blastopore in the formation of which the anterior
edge takes no part, in which consequently no ventral lip is formed.
Such a form may be found in Lepidosiren (Fig. 94, b), in which
the yolk is less abundant than in the Gymnophiona, but more
abundant than in the typical smaU-yolked egg. Here the formation of a blastopore is restricted to the dorsal and lateral Jips.
The absence of a ventral lip may be a very primitive feature,
smce none is found in Petromyzon.
It may also be noticed that the union of segmentation cavity
with archenteron occurs here and there in various Anamnia,
sometimes in Eana, and in Petromyzon, thus foreshadowing the
condition seen in Gymnophiona and the Amniota.
150
THE GERMINAL LAYERS
VI
In the Anamnia, indeed, the archenteron has a direct relation
to the endoderm in that, after notochord and mesoderm have
been differentiated, the aUmentary canal is formed from its roof,
or floor, or both. But as we pass up the series the archenteric
cavity loses this significance, its lumen dwindles and finally
disappears, and its function is reduced to the differentiation of
notochord and mesoderm alone. The endoderm is then derived
from the lower layer cells -  ^representative of yolk-cells -  ^which
line the segmentation cavity.
The same lower layer cells may contribute to the notochord
and mesoderm anteriorly, and this, as we have seen, is of constant occurrence in such small-yolked Anamnian types as the
Amphibia, and Petromyzon ; not, however, in the large-yolked
eggs of Fishes.
The Significance of the Gebminal Layers
It will have been repeatedly noticed that the same elementary
organ or germ-layer may come into being by different processes.
This is true of the front end of the notochord and mesoderm,
and still more obviously of the endoderm, for the lining epithehum
of the alimentary canal may be derived from the roof only of
the archenteron (Elasmobranchs and Teleostei), from the floor
only {Petromyzon, Urodela, Ceratodus), from both roof and floor
{Rana, Lepidosiren), from the yolk-cells in the floor and from
those in the segmentation cavity (Gymnophiona, occasionally
Rana), or from the lower layer (yolk-) cells of the segmentation
cavity alone (Amniota).
In considering such discrepancies in the mode of origin of
homologous structures-  and discrepancies of this kind are of
common occurrence, not only in development from the egg but
also in budding and regeneration-  it must be borne in mind
that experiment has shown the formation of the embryonic
organs-  such as the germ-layers-  to be dependent on the
presence of certain stuffs in the cytoplasm of the ovum, but
that these stuffs are not necessarily deposited in the situations
which will eventually be occupied by the organs to which they
give rise, nor even in the same position in the ova of animals
belonging to the same group. Thus they may occupy dissimilar
VI THE GERMINAL LAYERS 151
positions also in the segmented ovum, and again in the later
stage which we speak of as gastrulation or the closure of the
blastopore. The necessary materials -  now cut up into cells - 
have then to move into their definite positions, and thus we
witness the roof of the gut being formed by an upgrowth of
yolk-cells, or its floor by a bending down of the roof of the
archenteron.
The way in which an organ is developed is not, therefore,
necessarily a criterion of its homologies. Homologous structures,
that is, those derived, like the alimentary tract of the Vertebrate, from some common ancestral structure, may differ in their
origin during individual development. The stuffs on which their
differentiation depends are doubtless comparable, but the paths
by which that differentiation is achieved may be diverse.
LITERATURE
R. AsSHETON. Professor Hubrecht's paper on the early ontogenetic
phenomena in Mammals. Quart. Jotirn. Micr. Sci., 1909.
E. VAN Beneden. Untersuchungen iiber die Blatterbildung, den
Chordakanal und die Gastrulation bei Siiugetieren. Anat. Am. iii, 1888.
R. Bonnet. Beitrage zur Embryologie des Hundes. Anat. Hefte,
Abt. ix, 1897.
A. Beaueh. Beitrage zur Entwickelungsgeschichte der Gymnophionen.
Zool. Jahrb. x, 1897.
Bashfoed Dean. The early development of gar-pike and sturgeon.
Journ. Morph. xi, 1895.
Bashfoed Dean. On the embryology of Bdellostoma stouti. Festschr.
f. C. von Kupffer, Jena, 1899.
L. F. Hennequy. Embryog6nie de la truite. Journ. de VAnat. et de la
Phys. xxiv, 1888.
J. W. Jenkinson. Remarks on the germinal layers of Vertebrates and
on the significance of germinal layers in general. Mem,. Manchester Lit.
and Phil. Soc. I, 1906.
J. Geaham Keeb. The development of Lepidosiren paradoxa. Quart.
Journ. Micr. Sci. xlv, 1901.
K. MiTSUKUEi and C. IsmKAWA. On the formation of the germinal layers
in Chelonia. Quart. Journ. Micr. Sci. xxvii, 1886.
J. Ruckeet. Die erste Entwickelung des Eies der Elasmobranchier.
Festschr. f. C. von Kupffer, Jena, 1899.
H. ScHAUiNSLAND. Studien zur Entwickelungsgeschichte der Sauropsiden. Zoologica, xvi, 1903.
162
THE GERMINAL LAYERS
VI
11. Semon. Die Furchung und Entwickelung dcr Keimbliitter bei
Ceralodiis forstcri. Zool. Forschiivgsreise in Anslralien, 1901.
A. E. Shipley. The development of Pctromyzon jluvialilis. Quart.
Joum. Micr. Sci. xxvii, 1887.
J. SoBOTTA. Die Gastrulation von .4»n{aaZw. VerJtaiidl. Anat. Geaellsch.
Berlin, 1896.
C. O. Whitman and A. C. Eycleshymer. The egg of Aviia and its
cleavage. Journ. Mor]}h. xii, 1897.
L. Will. Die Entwickelungsgescliichte der Ileptilien. Zool. Jahrh. vi, ix.
H. V. Wilson. The embryology of the sea- bass {Scrramts alrarius).
Bull. U. S. Fish Commission, ix, 1889.
J. T. Wilson and J. P. Hill. Observations on the development of
Ornilhorhynchus. Phil. Trails. Roy. Soc, Series B, cxcix, 1907.
H. E. ZiEGLEE. Beitrage zur Entwickelungsgeschichte von Torpedo.
Arch. mikr. -Anal, xxxix, 1892.
i
Fig. 95. -  External features of the development of the tadpole of the
Frog.
a. Medullary plate, anterior end : the three divisions of the brain are
apparent.
h. The same embryo from the posterior end : the sides of the medullary
plate pass back on either side of the blastopore. The blastopore is now
reduced to a narrow slit by the approximation of the lateral lips ; at the
dorsal and ventral lips the aperture is rather wider.
c. Medullary folds and groove, anterior end : the three divisions of the
brain are readily seen, and the anterior part of what will be the spinal
cord. External to the inner medullary folds are the outer, and these pass
in front into the broad gill-plates, in front of which again are the senseplates.
d. Closure of medullary folds, but the suture is still visible : the gill-plate
is divided on each side into two, and in front of it is the sense-plate ; behind
the gill-plate is a slight constriction.
e. Anterior view of the same embryo : the medullary folds have not
quite closed in front. Beneath their anterior end is a depression, the
stomodaeum, and on either side of this the sense-plates ; the gill-plates can
just be seen behind these.
f. Posterior view of the same embryo : the medullary folds have closed
over the dorsal division of the blastopore (neurenteric canal) while the
ventral remains as the proctodaeum. The middle region of the blastopore
is marked by a very narrow suture.
g. Later embryo from below showing the stomodaeum, in front of the
V-shaped sucker, and posteriorly the proctodaeum at the base of the tailstump.
h. Older embryo from the right side. The tail is rather longer, the
proctodaeum at its base : the stomodaeum can be seen in front between
the two halves of the sucker. At the side of the head in front is the
nostril, behind the gill-slits.
i. Older embryo (ready to hatch) with well-developed tail and external
gills.
Betweenl52 andlG")
1
t
I
==CHAPTER VII THE EARLY STAGES IN THE DEVELOPMENT OF THE EMBRYO==
A. In the Anamnia
The common frog ajEEords a very good type of the development
of the embryo from a small-yolked egg.
We left the frog's egg at the moment when the rotation was
complete, the blastopore had been reduced to a small circle, and
the material for the thi-ee germinal layers laid down and brought
into position.
The circular blastopore soon becomes laterally compressed and
so reduced to a narrow vertical slit, the yolk-plug being at the
same time withdrawn into the interior. The opposite sides Avill
in a little while meet together and fuse, so dividing the blastopore into a dorsal and a ventral portion. The dorsal portion
will become the neurenteric canal. The ventral portion will
close but reopen later as the proctodaeum or anus (Fig. 95).
Meanwhile, the rudiment of the nervous system has appeared
in the form of a raised area of thickened ectoderm upon the
dorsal side of the egg. This area is triangular or rather pearshaped, being broad in front, narrow behind (Fig. 95, a). It is
known as the medullary plate. From the broad anterior end
the brain will be developed, from the narrow posterior end the
spinal cord. The edges of the medullary plate fade away on each
side of the slit-shaped blastopore (Fig. 95, b).
There presently appears in the middle Hne a groove running
the whole length of the medullary plate, the medullary groove.
In the brain region this is wide and divided by transverse ridges
into three depressions, the rudiments of the fore-, mid-, and
hind-brains, in the region of the spinal cord narrow. At the
same time the edges of the medullary plate begin to rise up on
each side as the medullary ridges or folds. These folds are each
154 EARLY DEVELOPMENT OF THE EMBRYO VII
divided longitudinally into two, an outer and an inner fold. The
latter will for in the wall of the medullary tube. The outer fold
is especially wide and prominent in front, where it is divided by
a slight transverse furrow into two areas, the sense-plate and the
gill-plate (Fig. 95, c). The posterior part of the outer medullary
fold is narrow.
The outer medullary fold is due to the presence below the
surface of the neural crest, a ridge of ectodermal cells from
which the ganglia of the spinal nerves and of some of the cranial
nerves are derived. The sense-plate contains the material
for the fifth and seventh cranial nerve ganglia, the giU-plate
that for the ninth and tenth, while the posterior narrow portion
gives rise to the spinal ganglia.
The inner medullary folds now approach one another in the
middle line, meet and fuse (Fig. 95, d). The groove is thus
converted into a closed canal, the medullary tube ; from the
wide anterior portion of this the ventricles of the brain will be
formed, from the narrow posterior portion the canal of the
spinal cord. At the extreme hind end, as we have already
seen, the medullary folds pass into the sides of the blastopore.
When they meet in this region they naturally cover over the
dorsal half of the latter. The enteron therefore no longer opens
to the exterior by means of the blastopore, but into the hinder
end of the medullary tube. In this way the dorsal part of the
blastopore is converted into a passage of communication between
the nervous system and the gut : it has become the neurenteric
canal (Fig. 95, f).
The ventral division of the blastopore is not covered by the
medullary folds. It closes, but will reopen as the proctodaeum
or anus.
The embryo now begins to elongate (Fig. 95) and a constriction
appears behind the gill-plate separating the head from the trunk.
At the anterior end and rather on the ventral side a depression
is now seen -  the stomodaeum or mouth invagination -  and a little
way behind this a V-shaped groove with prominent lips, the apex of
the V pointing backwards. This is the cement gland or sucker.
At the hinder end the proctodaeum is now visible in the place
where the ventral division of the blastopore closed (Fig. 95, Q).
VII EARLY DEVELOPMENT OF THE EMBRYO 155
The body is at this time ciHated ; by this means the embryo
turns over and over inside the jelly.
The tail appears as an outgrowth of the posterior end above
the proctodaeum (Fig. 95). Apparently single, the tail is in
reaUty double, as it is due to the fusion in the middle line of
two separate tail buds or caudal swellings. These two tail buds
arise one on each side of the blastopore, and the lateral compression of the latter is in reality the approximation of the two
buds. The double (bilateral) origin of the tail is clearly to be
seen in those cases where, as by the application of some external
agent (heat, salt solution, and so on), the blastopore is prevented
from closing, the tail buds are unable to meet, and consequently
the tadpole has two tails.
At the anterior end the olfactory pit is seen on each side.
The front end of the head is obliquely truncated. The V-shaped
sucker is now divided into two. The gill-plate has become subdivided by transverse furrows into three bars, the first, second,
and third branchial arches. The hyoid and mandibular arches
lie in the region of the sense-plate (Fig. 95, h).
The trunk is laterally compressed dorsally, but ventrally
swollen out by the yolk in the floor of the gut. Later the tail
grows longer and is provided with a ventral and a dorsal fin,
the latter being continued into the trunk region. On the dorsal
side of the body and in the tail the myotomes or muscle segments
become clearly visible.
The embryo elongates still more (Fig. 95, i), the external gills
are developed as branched filaments on the three branchial
arches in regular order from before backwards, the eye and the
divisions of the brain cause prominent swellings at the side of
the head, while another lateral swelling -  behind the gills -  marks
the position of the pronephros or larval kidney. The caudal
fin becomes wider.
Soon after this the embryo hatches out of the jelly as the
larva or tadpole. The mouth now opens and the tadpole, fastening
on to the jelly by its suckers, begins to feed on it. The suckers,
however, are transitory organs and soon disappear. The mouth
becomes transversely elongated and provided with rows of horny
teeth. The external gills are soon covered by the operculum,
166 EARLY DEVELOPMENT OF THE EMBRYO VII
a membranous fold growing back from the hyoid arch, which
becomes fused with the body behind, leaving only one aperture,
the spiracle, by which the water taken in at the mouth and
passed out by the gill-slits can escape. This is on the left side.
The external gills atrophy and are replaced by internal gills.
Further details of the tadpole's structure and its metamorphosis
into the frog do not, however, concern us here, and may be
passed over.
We turn to the changes that have been taking place internally,
and begin with the organs derived from the ectoderm. These
are the epidermis and the nervous system and the sense-organs :
the stomodaeum and proctodaeum may be considered with the
alimentary canal.
The ectoderm is composed of two layers, an outer pigmented
epidermal layer of columnar cells, and an inner nervous layer of
polyhedral cells. Both layers are present in the medullary plate,
but while the epidermal layer remains thin, the nervous layer
is very considerably thickened, being composed here of six or
more layers of cubical or columnar cells. The whole medullary
plate is seen in section (Fig. 96, a) to be divisible into five tracts,
a median, two internal lateral, and two external lateral. In the
median tract the ectoderm is thin, in the lateral tracts it is
thickened.
As the medullary folds rise up (Fig. 96, b), meet and fuse
(Fig. 97), it is seen that the thin median tract becomes the floor
of the medullary tube, the thick inner lateral tracts (which are
the inner medullary folds) the thick side walls of the medullary
tube, while the outer lateral tracts (the outer medullary folds)
are carried up in the angle of the folds on either side as wedgeshaped masses of cells, the neural crests. When the folds have
finally closed the outer layer of ectoderm is detached from the
thin roof of the medullary tube, while the neural crests remam
adherent to the latter. The neural crests are longitudinal
ridges. Later they become transversely divided into segments in
accordance with the segmentation of the mesoderm (see below).
In the region of the spinal cord these segments become the
gangUa and give rise to the dorsal roots of the spinal nerves.
In the region of the brain they give rise to the roots and gangha
VII EARLY DEVELOPMENT OF THE EMBRYO 157
of some of the cranial nerves, namely, the fifth, seventh, eighth,
ninth, and tenth.
Fig. 96. -  ^Transverse sections of the embryo of the frog at two succeeding
stages, A and b. a 1, b 1, Sections transverse to the trunk. A 2, b 2, Sections
transverse to the head and therefore cutting the blastopore (b.p.) behind,
m.p., medullary plate; in./., medullary fold; m.g., medullary groove;
n.c, neural crest ; n., notochord ; m., mesoderm ; d.ni., dorsal mesoderm ;
v.m.., ventral mesoderm ; ec, ectoderm ; g., gut. The mesoderm in this
and the following figures is shaded.
The ventral roots of the spinal nerves are not formed from the
neural crest, but by outgrowth of cells of the spinal cord. The
third, foiu-th, and sixth cranial nerves (all purely motor) are
158 EARLY DEVELOPMENT OF THE EMBRYO VII
formed in the same way as ventral spinal-nerve roots. The first
cranial nerve arises by outgrowth of the front end of the brain,
while the fibres of the second grow back from cells in the retina.
The retina is, however, itself a derivative of the brain, as we are
now to see.
The brain, as pointed out already, is divided into fore-, mid-,
and hind-brains (Fig. 98).
By what is known as the primary cranial flexure the forebrain is in the embryo bent ventrally upon the mid-brain, so
n ^ mt.
â– piG, 97. -  Transverse sections of frog embryos showing the further
development of the nervous system and mesoderm, m.t, medullary tube ;
nc neural crest; n., notochord ; s.n., sub-notochordal rod; m.v.p.,
vertebral plate, m.l.p., lateral plate of the mesoderm ; my., myotom ; scl,
sclerotom ; c, coelom (splanchnocoel) ; so., somatopleure ; sjjL, splanchnopleure ; prn., pronephric ridge ; v.v., vitelline vein ; g., gut ; I., liver.
that the latter is brought to the front end of the body (Fig. 98).
The brain, however, soon straightens out again.
The hind-brain gives rise to the medulla oblongata and cerebellum, its cavity becomes the fourth ventricle ; the mid-brain,
whose cavity becomes the iter, gives rise to the optic lobes and
crura cerebri, while the fore-brain becomes divided into the
prosencephalon and thalamencephalon. The first comprises
the two cerebral hemispheres, which are lateral outgrowths of the
fore-brain, the rest of which then becomes the thalamencephalon ;
its cavity, the third ventricle, is produced into a hollow dorsal
I.
B.
VII EARLY DEVELOPMENT OF THE EMBRYO 159
outgrowth, the pineal body, a hollow ventral outgrowth, the
infunclibulum, and two ventro-lateral outgrowths in front of
the infundibulum, the optic vesicles.
The optic vesicles (Fig. 99, a) are the rudiments of the retinae
of the eyes. Each hollow outgrowth communicates at first by
a wide aperture with the lumen of the fore-brain, but the aperture soon becomes narrowed to a tube, the optic stalk. The
optic vesicle then becomes converted into the optic cup, by the
pushing in of the outer and thicker wall (Fig. 99, b). The cavity
Fig. 98. -  Median longitudinal section of a trog embryo, when the medullary tube has closed and the proctodaeum {pr.) has opened, f.b., fore-brain ;
i., infundibulum; m.b., mid-brain; h.b., hiud-brain; sp.c, spinal cord;
n.e.c, neurenteric canal ; n., notochord ; p.b., pituitary body ; sL, stomodaeum ; pc, pericardium ; ht., heart ; v.m., ventral mesoderm ; I., liver.
of the vesicle is thus obliterated. It is essential for the due
comprehension of the embryology and anatomy of the eye to
observe that this inpushing is not confined to the outer surface
of the optic vesicle, but is extended along its ventral surface as
well. There is therefore an opening to the optic cup on its
lower as well as on its outer side, and when the latter is closed
by the lens the former remains as a narrow slit through which
mesodermal structures-  blood-vessels and the cells which secrete
the vitreous humour-  pass into the cup. This slit is the choroid
fissure. The wall of the cup, from the mode of its formation,
IS composed of two layers : the outer, which is thin, consisting
of one sheet of cells, becomes the pigment layer of the retina,
160 EARLY DEVELOPMENT OP THE EMBRYO VII
whil(; the inner, which soon comes to consist of several sheets
of cells, becomes the retina itself, except at the edge of the
cup (Fig. 100). Here it remains thin, and together with the
outer layer, with which it is continuous, gives rise to the ciliaryprocesses and iris.
Fig. 99.-  Sections illustrating the formation of the eye (a, b), ear, and
heai-t (c, D) in the frog, f.h., fore-brain ; h.h., hind-brain ; o.v. optic
vesicle ; o.c, optic cup ; o.sL, optic stalk ; le., lens ; p.h., pituitary body ;
St., stomodaeu'm ; s., suckers ; n., notochord ; a., aorta ; a.v., auditory
vesicle; lit., heart endothelium; U.m., muscular wall of the heart;
'pc, pericardium.
The lens is derived from the superficial ectoderm by invagination of the deep or nervous layer opposite the mouth of the cup.
The invaginatcd cells become detached as a hollow vesicle, which
is then fitted into the mouth of the optic cup. The cells of the
outer wall of the lens vesicle remain cubical, and are the lens
epithelium, but those of the inner waU become elongated into
VII EARLY DEVELOPMENT OF THE EMBRYO 161
the lens fibres. The cavity of the vesicle is thus obliterated.
The sclerotic, choroid, vitreous body and cornea are all mesodermal structures ; the first and second are formed from cells
applied to the outer wall of the optic cup, the third from
cells which migrate in by the choroid fissure, the fourth from
cells which pass between the superficial ectoderm and the lens.
The pigment soon disappears from this superficial ectoderm.
The muscles of the eyeball -  ^recti and obliques -  are derived
from the mesodermal head somites, to which we shall refer later.
O.C.h
OCX
o,st. -  ;
Fig. 100. -  Section, transverse to the body, of the eye at a later stage.
The section therefore passes down the length of the choroid fissure, o.st.,
optic stalk; o.c.l, outer layer of optic cup (pigment layer of retina);
o.c. 2, inner layer of optic cup (retina) ; U., lens ; co., cornea ; i;.6., vitreous
body mesoderm ; h.v., blood-vessel ; sd.ch., mesoderm which will form the
sclerotic and the choroid.
The optic nerve-fibres are outgrowths of nerve-cells situated
in the retina : the fibres pass out by the choroid fissure and back
to the brain along the optic stalk. The stalk, therefore, merely
serves as a guiding path to the fibres. The passage of the fibres
through the choroid fissure explains the apparent perforation of
the back of the eyeball by the optic nerve.
The olfactory pit (Fig. 104) arises by simple invagination of
both layers of the ectoderm : it later becomes deepened to form
the olfactory sac, the aperture being the nostril. The auditory
vesicle-  which wiU develop into the labyrinth or internal ear- 
1366
162 EARLY DEVELOPMENT OF THE EMBRYO VII
is formed, like the lens of the eye, by invagination of the nervous
layer of the ectoderm (Fig. 99, c, d). Its connexion with the
ectoderm is soon severed, the ductus endolymphaticus being
the remains of the communicating passage.
The organs derived from the mesoderm are the muscular and
skeletal systems, the connective tissue, the blood and vascular
system, the coelom and urogenital organs.
We have seen how the mesoderm is laid down in the form of
two sheets of tissde lying between the ectoderm and the endo
derm, separated dorsally in the middle line by the notochord
(and when it is formed, by the medullary tube as well), but
continuous with one another below the gut (Fig. 96, a1, b1).
The first diflEerentiation that occurs in the mesoderm is the
separation on each side of a smaU dorsal portion-  the vertebral
plate -  ^from a large ventral portion-  the lateral plate (Fig. 97, a).
The vertebral plates of the two sides are separated, but the
lateral plates are continuous below. The vertebral plate soon
becomes segmented transversely into a number of protovertebral
or mesodermal somites, which give rise to the skeletal tissue and
the muscles of the trunk and Umbs. This segmentation begins
at the front end and extends backwards, there being therefore
for some time at the hind end and eventually in the tail a strip
of unsegmented mesoderm (Fig. 101). The first mesodermal
somite is found behind the auditory vesicle. In front of this
the mesoderm is not compact, but composed of scattered cells,
and no traces of segments are found. This is also true of aU
higher Vertebrates, but there is good reason for behevmg that
virtual if not actual somites are present in this region, smce m
Elasmobranch fishes and in Cyclostomes head somites are clearly
visible The number of these somites is three, one in front of
the mandibular visceral arch, one at the level of the mandibular
arch, and one at the level of the hyoid arch. From these somites
the recti and oblique muscles of the eyeball are formed.
The part of the head in which the mesoderm is thus cut up
into somites comparable with the somites of the trunk is the
posterior part, including the mid- and hind-brains and the
anterior extremity of the notochord. It is of the greatest
interest to observe that the cranial nerves which anse from these
VII EARLY DEVELOPMENT OF THE EMBRYO 163
two regions of the brain are also derived from segmental nerves,
comparable, though not in every detail, with the segmental
nerves of the trunk. We have already seen that in the trunk
the neural crest becomes segmented, in confot-mity with the
segmentation of the mesoderm, into a number of pieces, out of
which the gangUa and dorsal roots of the spinal nerves are
developed, while the ventral roots arise separately from the
spinal cord. The neural crest is continued into the posterior
region of the head and is divided into segments, the first of which
lies between the first and second head
somites and gives rise to the ramus
ophthalmicus of the fifth nerve, the
second between the second and third
head somites and gives rise to the main
branch of the fifth nerve, the third between the third head somite and first
trunk somite and gives rise to the
seventh and eighth nerves, the fourth
between the first and second trunk
somites and gives rise to the ninth nerve,
while the fifth between the second and
third trunk somites gives rise to the
tenth nerve ; the next segment of the
neural crest becomes the ganglion and
dorsal roots of the first spinal nerve.
It is clear, therefore, that the fifth,
the seventh with the eighth, the ninth,
and the tenth cranial nerves are developed in the same way
as the dorsal roots of spinal nerves, and represent the dorsal
roots of the nerves corresponding to the head somites and
anterior trunk somites. The corresponding ventral roots -  of
the first, second, and third head somites -  become the motor
nerves innervating the eye-muscles, namely, the third, fourth,
and sixth. These three are therefore the ventral roots of the
same somites to which the fifth (two divisions) and the seventh
with the eighth belong. The ventral roots corresponding to the
ninth and tenth disappear (in the lamprey).
Hence the part of the head containing the anterior extremity
L 2
Fig. 101. -  Horizontal
section of the hind end
of a frog embryo ; m.s.,
mesodermal somites ; m.,
posterior imsegmented
mesoderm ; m.t., medullary tube; w., notochord;
ew., endoderm ; ft.y., hind
gut ; ec., ectoderm.
164 EARLY DEVELOPMENT OF THE EMBRYO VII
of the notochord and the mid- and hind-brains consists in reality
of a number of trunk segments with their corresponding dorsal
and ventral nerve roots, fused together and telescoped on to the
back of a more anterior region which comprises the fore-brain with
its sensory nerves, the olfactory and optic. The relations of these
dorsal nerve roots, ventral nerve roots, and somites are shown
in the accompanying table.
Segments of
neural crest
Nerves derived
from them
I
II
III
IV
V
VI
V
ramus
ophthalmicus
V
main
branch
VII
and
VIII
IX
X
dorsal
root of
Ist
spinal
Mesodermal
Somites
Ventral
roots
Nerves
derived
from them
Head Somites
Premandibular
III
Mandibular
II
IV
Hyoid
III
VI
Trunk Somites
1st
IV
disappears
2nd
3rd
V
VI
dis
ventral
appears
root of
1st spinal
4th
To return to the mesoderm. The somites remain for some
little time connected to the lateral plate, each by a Httle neck
of tissue, the intermediate cell-mass. These necks of tissue are,
Uke the somites, metamerically segmented. They are a morphologicaUy distinct part of the mesoderm of great importance,
since from them is derived the whole of the system of kidneytubules and ducts. For this reason they are termed the nephrotoms. The lateral plate mesoderm remains unsegmented and
unpaired ; it is continuous below the gut from the right side
to the left, and also from the anterior end to the posterior.
The coelomic cavity soon appears, as a narrow space in the
mesoderm (Fig. 97, b). It is not only found in the lateral plate,
bu* extends into the intermediate cell-mass and somite. Three
VII EARLY DEVELOPMENT OF THE EMBRYO 165
distinct divisions of the coelom may therefore be recognized - 
the muscle coelom or myocoel of the somite, the nephrocoel,
the canal of the nephrotom or intermediate cell-mass, and the
splanchnocoel or gut-coelom in the lateral plate. The third of
these extends ventrally below the gut and from the front to the
hind end of the body. The three divisions of the coelom communicate freely with one another as long as the intermediate
en.
section of a dog-fish embryo, through the front
end of the body, m t., medullary tube ; n.c, neural crest ; n., notochord ;
my.c, myocoel; scZ., sclerotom ; nt.c, intermediate canal or nephrocoel;
prn., pronephric tubule growing out from the somatopleure of the nephrocoel; s^,i.c., splanchnocoel; so., somatopleure; spl., splanchnopleuref en.,
endoderm of gut (here open to yolk-sac). ' ^ ' i' >â–  > '^'<';
cell-masses remain in connexion with the somites on the one
hand and the lateral plate on the other. In the frog the relations
of these parts are not so clear, as the intermediate cell-masses
soon become detached from the somites and merged in the
lateral plates, and the myocoel is smaller. They are, however
easily made out in, for example, an Elasmobranch embryo'
(Fig. 102).
From the ventral inner end of the somite the skeletal cells
are produced, by simple emigration, or by outgrowth of a partially
hollow mass, suggesting an evagination. These several segmental
166 EARLY DEVELOPMENT OF THE EMBRYO VII
groups of cells produced from the segmental somites are known
as sclerotoms. The cells pass in and up, round the notochord
and the medullary tube to form later the centra and neural and
haemal arches of the vertebrae (Figs. 97 B, 102).
The remainder of the somite, now termed a myotom, gives
rise to the muscles of the back, limbs, and body -wall. The
m.t.
Fig. 103.-  Transverse section of an advanced frog embryo, m.t.,
meduUary tube ; n., notochord ; s.n., sub-notochordal rod ; ?ny., myotom ;
a., aorta ; p.c.v., posterior cardinal vein ; prn., pronephric tubule ; pm.J.,
pronephric funnel ; gl., glomus ; c, coelom ; so., somatopleure ; spl.,
splanchnopleure ; g., gut ; I., liver ; v.v., vitelline vem ; ec, ectoderm.
myocoel disappears, the cells of the inner wall become differentiated as muscle fibres, while those of the outer waU form
a connective tissue cutis.
From the nephrocoel the kidney is derived. Kidney tubules
arise by outgrowth-  hollow or solid-  of the outer wall or
somatopleure of the nephrocoel. In all cases the pronephros
is the first part of the kidney system to appear (Fig. 97, b). In
the frog the pronephros consists of three well-developed tubules,
produced by outgrowth of the somatopleure of the nephrotom
VII EARLY DEVELOPMENT OF THE EMBRYO 167
(but after that has become merged in the lateral plate) : each
tubule opens by a ciliated funnel into the coelom, and at its other
extremity into a longitudinal duct which in turn discharges its
contents into the cloaca. The duct is split off from the somatopleure, from before backwards, its anterior end being ab origine
in continuity with the outgrowths which give rise to the tubules.
The pronephric tubules coil amongst the capillaries of the
posterior cardinal vein. The glomus is a bunch of blood-vessels
Fig. 104. -  Horizontal section through the head of an embryo of the
same age as the last, ol., olfactory pit ; /.&., fore-brain ; i., infundibulum ;
o.st., optic stalk ; a., aorta ; 1, 2, 3, 4, 5, the five gill-slits (hyomandibular
and four branchial) ; e.g., external gills on the first and second branchial
arches. Those on the third are not yet formed. The mandibular arch
Hes in front of gill-slit 1, the hyoid in front of gill- slit 2. ph., pharynx ;
p.c.v., posterior cardinal vein ; pm.f., pronephric funnel ; prn.t., pronephric
tubule.
hanging into the coelom at the root of the mesentery of the gut
opposite the mouths of the pronephric tubules : its blood-supply
is from the aorta. The pronephros is the larval kidney.
The origin of the germ-cells has been described in a previous
chapter.
The coelom of the lateral plate or splanchnocoel becomes the
body-cavity of the adult. Its anterior end contains the heart, and
is subsequently shut off as the pericardium from the posterior
end or peritoneal cavity in which lie the gut, liver, kidneys, and
gonads. When the lungs are developed and pushed into this
168 EAKLY DEVELOPMENT OF THE EMBRYO VII
cavity it is pleuro-peritoneal. The epithelium lining it is of course
the peritoneum, and reflected over the gut and other viscera.
The mesentery of the gut is therefore a double layer of peritoneum.
The coelom naturally divides the mesoderm into an outer and
an inner layer. The former, next the body wall, is the somatopleure ; the latter, near the gut, the splanchnopleure (Fig. 97, b).
From the splanchnopleure come the muscles of the alimentary
canal and of the heart.
The endothelial lining of the heart is derived from some
scattered cells detached from the floor of the fore-gut (Fig. 99, c).
As we have already seen, the ventral mesoderm is separated off
from the yolk-cells which lie in the floor of the archenteron.
The separation of these heart-cells is to be regarded as a later
phase of the same process. The scattered cells soon unite to
form a tube, the heart, which quickly pushes the splanchnopleure
of the gut in front of it and so projects into the coelom, now the
pericardium (Fig. 99, d). The splanchnopleure svirrounding the
endothelial tube becomes the muscular wall of the heart. For
a short time the heart is attached to the ventral body-wall
by a ventral mesocardium, but as soon as the two sides of the
pericardium coalesce this disappears. At its anterior end the
heart gives off the arterial arches : of these there are at first
three, passing to the external gills on the first, second, and third
branchial arches : later a fourth is added. These are the four
afferent branchial arteries : from the gill capillaries the blood
passes by the four efferent arteries into the two dorsal aortae,
which are united only some way back into a single median
aorta. In the frog there are no arterial arches in the mandibular
and hyoid arches.
Posteriorly the heart receives the two ductus Cuvieri, bringing
back the blood from the cardinal veins in the body- wall, and the
two vitelline veins bringing blood from the liver and gut. These
last are formed from the ventral surface of the gut in the same
way as the endothelial cells of the heart, and are to be looked
upon as retarded ventral mesoderm. Blood corpuscles are
derived from the same source and immediately fall into the veins.
Other blood-vessels, aortae, cardinal veins, and so on, are produced
by the union of scattered mesoderm cells, that is, wandering cells
VII EARLY DEVELOPMENT OF THE EMBRYO 169
detached from the general mesoderm. Other cells detached in
the same way form the connective tissue.
The notochord, which, we have seen, takes its origin at the
same time and in the same way as the dorsal mesoderm, quickly
assumes its characteristic histological features. It becomes
cylindrical, the cells flat and discoidal, placed at right angles
to the length of the notochord, and highly vacuolated. The
notochord is surrounded by a delicate cuticular sheath, the
chordal sheath or membrana elastica interna. Round it the
vertebral column is laid down by the skeletal cells of the sclerotoms. Anteriorly the notochord terminates at the pituitary body
behind the fore-brain.
The alimentary canal is derived from the endoderm, with the
exception of the short stomodaeum and proctodaeum.
From the dorsal side of the stomodaeum the pituitary body
grows, as a cord of ectodermal cells, up towards the infundibulum
to which it becomes attached. By the formation of the floor of
the skull it is shut off from the mouth (Figs. 98, 99 a).
From the endodermal lining of the alimentary canal come the
thyroid, gill-sUts, thymus, lungs, liver, pancreas, and bladder.
The gill-slits are endodermal outgrowths met by slight ectodermal ingrowths. There are five in the tadpole, the hyomandibular and four branchial (Fig. 104). The hyomandibular is never
open. The remaining become perforated and functional.
The first or hyomandibular persists as the Eustachian passage.
The gill-arches alternate with the gill-slits. The mandibular
lies in front of the first, then come in order the hyoid and four
branchial arches. The arterial arches (of which in the frog there
are only four pairs) run in the branchial arches.
The thyroid is a median ventral diverticulum of the pharynx
opposite the second gill-sHt. The thymus is formed from dorsal
epithelial remains of the gill-slits. The carotid gland and the
epithelial corpuscles are ventral epithelial remains. The parathyroid is a rudimentary sixth giU-sUt. Lungs, liver, pancreas
and bladder arise as ventral diverticula of the gut.
The mass of yolk-cells in the floor of the gut of the embryo
becomes slowly absorbed. While present it forms what might
almost be termed a yolk-sac.
170 EARLY DEVELOPMENT OF THE EMBRYO VII
In the forms with large -yolked eggs, Myxinoids, Elasmobranchs,
and Teleosts, there is a well-developed yolk-sac. The embryo is
developed from the median and posterior area of the blastoderm
before that has spread over the yolk, and is folded oflE from it.
The extra-embryonic blastoderm then encloses the yolk, the sac
so formed being attached by a narrow (Elasmobranchs) or wide
(Teleostei) yolk-stalk to the body (see above, Figs. 71, 72). The
ectoderm of the embryo is thus continuous with that of the
yolk-sac, the endoderm passes out on to the yolk, and a layer
of mesoderm extends in between these two.
The general development of the embryo itself is quite similar
to that in small-yolked forms, and only one or two points need
to be mentioned. The tail is paired in origin, being formed by
the coalescence of the two caudal swelUngs. The tail grows
back freely above the surface of the yolk. On its upper surface
is the hinder end of the medullary tube, on its lower side the tail
gut or post-anal gut. This is formed by the bending down of the
sides of the archenteric roof -  after separation of the notochord
and mesoderm -  ^until they meet and fuse ventrally. At the hind
end -  the dorsal lip of the blastopore -  all three germ-layers unite
in a common cell-mass, and behind this point the medullary tube
and post-anal gut are in communication by a neurenteric canal.
The heart is formed, after the fore-gut has been folded ofE from
the yolk-sac, in the same way as in the frog, as a single median
tube. The nervous system usually arises by medullary folds,
but in Teleostei, Petromyzon, Lepidosteus, and Lepidosiren there
is a solid wedge-shaped ingrowth of ectoderm along the middle
dorsal line (see above, Figs. 65 c, 75 a). In this the cavity
of the medullary tube appears later on. The rudiments of optic
vesicles, auditory vesicles, and olfactory pits are similarly sohd
at first.
The yolk-sac is provided with an area vasculosa of blood vessels by which the food material is conveyed to the body of
the embryo. In Elasmobranchs there are in this area at first
two venous rings, one peripheral -  the sinus terminalis-  and
connected with the subintestinal vein of the embryo at the root
of the tail ; the other central, pouring its blood directly into the
heart. The latter becomes converted into an arterial ring by
(
t
Fig. 104*. -  Development of the area vasculosa in the Elasmobranch
Torpedo. (After Riickert.)
A, Early stage. There are two venous rings ; the external one (sinus
terminalis) at the edge of the blastoderm opens into the sub-intestmal veins
of the embryo behind ; the internal ring opens into the heart in front.
B, Later stage when the internal ring has become arterial, bemg now
connected to the aorta.
c, Last stage, when the arterial ring has become modified to form the
anterior median artery (stippled) while the sinus terminalis is reduced to
a small ring as the blastoderm encloses the yolk.
1'. 171
VII EARLY DEVELOPMENT OF THE EMBRYO 171
being connected directly to the aorta, disconnected from the
heart. The arterial ring then becomes broken into two arteries,
which finally fuse by their bases into a single median stem.
As the blastoderm encloses the yolk the marginal sinus terminalis
is correspondingly reduced (Pig. 104*).
B. In the Amniota.
In all Amniota the embryo is developed from the central area
of the blastoderm only, the remainder being extra-embryonic.
This central embryonic area is at first 'spread out flat like
the rest of the blastoderm -  but as the embryo is developed it
becomes gradually folded and constricted off from the surrounding
blastoderm, as in the large-yolked Fishes. Here, however, the
process is complicated by the development of the amnion, a sac
enclosing the body of the embryo. The development of the
chick may be taken as tjrpical.
As we have already seen, the blastoderm of the chick at the
beginning of incubation consists of an upper and a lower layer.
The upper layer is a columnar epithehum ; the lower layer is
a sheet of scattered cells. At its edge the blastoderm rests upon
the yolk, with which its marginal cells are continuous : in the
yolk immediately surrounding the blastoderm are numerous
nuclei, without cell-divisions. This nucleated ring is the syncytium or germinal wall.
Between the upper and lower layers is the segmentation
cavity, and between the lower layer and the yolk the subgerminal cavity (continuous with and a part of the segmentation
cavity).
After incubation has been in progress for a short time the lower
layer cells unite to form a definite membrane or lower layer. The
segmentation cavity is now separated from the subgerminal cavity.
Marginally the lower layer is continuous with the germinal wall
and with the upper layer. The blastoderm grows over the
yolk by nuclear and cell division in this marginal zone, and
several layers of cells are formed. At the surface is a layer continuous on the one hand with the upper layer of the blastoderm,
on the other by its extreme marginal cells with the yolk. Underneath this are several layers of cells continuous with the lower
172 EARLY DEVELOPMENT OF THE EMBRYO VII
layer of the blastoderm : the lowermost cells and the marginal
cells are still continuous with the nucleated yolk or syncytium.
The subgerminal cavity below the central area of the blastoderm gives to it a transparent appearance ; this area is hence
known as the area pellucida ; but the marginal zone, resting
directly on the yolk, is opaque, and termed the area opaca.
The extension of the subgerminal cavity is less rapid than the
cell-division going on in the marginal zone, hence the area
opaca increases more quickly than the area pellucida and soon
forms a broad zone round about it (Fig. 106, a). The area pellucida
meanwhile becomes pear-shaped, the broad end being anterior,
and soon the first sign of the embryo appears (about the twelfth
hour of incubation) in the form of the primitive streak, a dark
median line in the posterior part of the area, down the axis of
which runs the primitive groove (Pig. 105).
The area pellucida -  and therefore later the embryo -  ^is always
oriented in a definite way with regard to the egg-shell, in which
the ovum is so placed that the long axis of the pear-shaped area
pellucida lies transversely to the long axis of the shell, while the
broad anterior end is away from the observer when the blunt end
of the shell is on his left.
As we already know, the primitive groove is an elongated
laterally compressed blastopore, and the primitive streak the
mesoderm produced at its sides and hinder end, the notochord
being given off in front. (To the notochord the term ' head
process of the primitive streak ' has been applied.)
The sheets of mesoderm grow forwards on the right and left,
flanking the median notochord ; at the anterior end -  ^in front
of where the head of the embryo will be -  ^they diverge somewhat,
leaving between them a space in which the ectoderm rests
directly upon the endoderm. This space is known as the proamnion. In front of the proamnion the mesoderm -sheets (at
a later stage) meet and fuse, and eventually the proamnion is
invaded by mesoderm and so disappears. Meanwhile a third
area -  the area vasculosa -  has begun to appear between the
pellucida and the opaca (Fig. 106).
The vascular area is first seen in the form of blotches of tissue
along the inner edge of the area opaca, behind and at the sides
- Jit. am.
/
I :
if
A B
"Fig. 105.-  Area pellucida of the hen's egg. a, After 12 hours', b, After
18 iiours mcubation, as seen by transmitted light, fr.g., primitive eroove ;
n.cli., notochord; pr.am., pro-ainnion.
1^ 172
I
i
f
a.o.
A
B
Fig. 106-  a, Blastoderm of the hen s egg after 20 hours' incubation.
7h.f., head-fold of the embryo ; a.p., area pellucida; a.v., area vasculosa;
a.o., area opaca. 1 1 . j
B, Embryo, area pellucida, and area vasculosa of the same blastoderm,
m./, medullary folds. Other abbreviations as before. Both as seen by
transmitted light.
P. 173
VII EARLY DEVELOPMENT OF THE EMBRYO 173
of, but not in front of, the area pelliicida. These blotches are
the blood-islands. They are formed from the masses of cells in
Fig. 107.-  a. Edge of the blastoderm of the unincubated hen's egg.
U.I., upper layer ; l.l., the lower layer cells in several sheets, the lowermost
of which is continuous with the yolk.
B, Edge of the blastoderm after 15 hours' incubation, u.l., upper layer ;
lower layer continued into the mass of cells lying on the yolk (area
opaca). The lowermost of these cells are continuous with the yoUc. In the
yolk are also nuclei with no cell-boundaries, the yolk-syncytium (y.syX
This extends a httle way below the subgermmal cavity {s.g.c).
the area opaca which lie between the upper layer above and the
nucleated yolk below, between the lower layer on the central side
and the nucleated yolk again on the peripheral side (Fig. 107).
174 EARLY DEVELOPMENT OF THE EMBRYO VII
The cells become closely packed in groups, which are the bloodislands : from them the blood-vessels and blood-corpuscles of
the area vasculosa are derived (Fig. 108). In each group the
outermost cells become arranged in a thin flat epitheUum - 
which becomes the endotheUum of a capillary vessel -  while the
Fig. 108. -  Formation of a blood-vessel (b) from a blood-island (a).
blood-island ; h.v., blood-vessel ; ec, ectoderm ; so., somatopleure ;
c."' coelom ; s-p., splanchnopleure ; y.sy., yolk-syncytium ; y.s.ep., yolk-sac
epithelium.
rounded cells inside are the corpuscles. By the secretion of fluid
cavities appear in between these cells, and the cavities run
together to form the lumen of the capillary, inside which the
corpuscles float freely. By the anastomosis of the blood-islands
with one another the network of vessels of the area vasculosa
is formed. The vessels soon come into connexion with others
formed in the area pellucida.
Fib 109 - Chick with area pelKicida and area vasculosa after 24 hours'
iacubatlon: fore-gat ; ..I viteim.e vein ; Ts Sen by
m.l.V; mesoderm of lateral plate. Other letters as before. As se.n oy
transmitted light.
P. 175
VII EARLY DEVELOPMENT OF THE EMBRYO 175
There is an evident similarity between the mode of formation
of these vessels and corpuscles and the origin of the bloodcorpuscles and endothehum of the vitelhne veins in the frog.
As these vessels and their corpuscles are derived in the frog from
the large yolk-laden cells of the gut, so here the blood-islands
arise from the thickened margin of the lower layer or endoderm :
and just as in the former case, so in the latter we may consider
this to be a retarded development of mesodermal structures
from the yolk-cells.
In the meantime the outline of the body of the embryo has
begun to appear in the form of the medullary plate (Fig. 109).
This lies in front of the primitive groove. The notochord and
mesoderm extend beneath it.
Down the middle of the plate the medullary groove is soon
formed, bordered on each side by the mediillary folds, which
diverge behind and then pass inwards into the sides of the
primitive groove. In front the groove is wide, and divides later
on into the three regions of fore-, mid-, and hind-brains ; behind
it is narrow, the spinal cord. By the fusion of the folds the
groove is converted into the closed medullary canal.
The head of the embryo now begins to be hfted up and folded
off from the blastoderm. This is known as the head-fold of the
embryo (Figs. 109, 111). By an exactly similar process lateral
folds and a tail-fold are formed, and so the whole body of the
embryo is graduaUy constricted off from the blastoderm. We
shaU see later that the gut of the embryo, which is at the same
time and in the same way folded off from the yolk-sac, remains
connected to the latter by the yolk-stalk, but that the body-wall
of the embryo is united with the amnion.
Before the embryo has been folded off from the blastoderm
there is no ventral side to its body : the ventral side can only
be made by the folding off, during which process parts which
lie in front, at the sides of, and behind the embryonic area are
bent underneath it.
The head of the embryo is immediately over the mesodermfree area, or proamnion. In front of this there soon rises up
a fold of the extra-embryonic blastoderm. This is the head-fold
of the amnion. It grows back, as a sort of hood, over the head
176 EARLY DEVELOPMENT OF THE EMBRYO VII
and body of the embryo : presently it is met by side-folds and
a tail-fold, and eventually all the folds meet over the back of the
embryo in the posterior region, and the amnion becomes closed.
The mesoderm undergoes the same differentiation that we
have made ourselves familiar with in the frog (Fig. 110). It
becomes divided on each side into a vertebral plate next the
notochord and medullary tube, and a lateral plate which extends
outwards into the extra-embryonic region of the area pellucida
and finally into the area vasculosa. The vertebral plate is
Fig. 110. -  Chick. Differentiation of the mesoderm, a, Posterior; b,
Anterior section of the blastoderm at 24 hours, m.g., medullary groove ;
n., notochord ; m., mesoderm ; m.l.p., lateral plate ; m.v.p., vertebral
plate ; en., endoderm.
segmented into somites. The separation and segmentation of
the vertebral plate take place in regular order from before
backwards, so that at the hinder end there is a strip of mesoderm still unsegmented and still imited with the lateral plate,
and passing back to the primitive groove (Fig. 109).
The first somite is at the side of the hind-bram-  immediately
behind the auditory vesicle, but, as abeady stated, there is every
reason to beheve that virtual if not actual somites exist in the
mesoderm in front of this.
Each somite remains connected to the lateral plate for some
time by an intermediate cell-mass or nephrotom. From the
VII EARLY DEVELOPMENT OF THE EMBRYO 177
nephrotoms are produced the kidney tubules (Figs. 112, 118).
The anterior tubules or pronephros are rudimentary in the chick
(and in all Amniota), but the segmental duct is formed from
their union. The mesonephric or Wolffian tubules are, however,
well developed, and function as the embryonic kidney. The
adult kidney or metanephros is formed from more posterior
tubules.
The coelom comprises the mj'^ocoel of the mesodermal somite,
the nephrocoel of the nephrotom, and the splanchnocoel of the
lateral plate (Fig. 110). The first soon disappears. The somite
Fig. 111. -  Diagram of a longitudinal section of a chick of about 30 hours,
to show the folding off of the head of the embryo from the blastoderm,
the folding off of the fore-gut from the yolk-sac, and the position of the
heart, h.f., head-fold of embryo; f.b., fore-brain; m.b., mid- brain ;
h.b., hind-brain ; sp.c, spinal cord ; p.s., primitive streak ; n., notochord ;
gjj., endoderm ; f.g., fore-gut ; a.i.p., anterior intestinal portal ; st., stomodaeum ; ht., heart ; p.c, pericardium ; pr., proamnion. 1-5, The planes of
the sections shown in Fig. 112.
is differentiated into sclerotom and myotom. The second
persists as the cavity of the capsule of the kidney tubule. The
third also persists. In the embryonic region it becomes subdivided into the pericardium in front and the pleuro-peritoneal
cavity behind (in Mammalia the pleural cavities become of course
separated by the diaphragm from the peritoneal cavity). In
the extra-embryonic region it extends out to the edge of the
mesoderm. Here, therefore, the somatopleure lies against
the extra-embryonic ectoderm, the splanchnopleure against the
(endodermal) epitheUum of the yolk-sac. In the area vasculosa,
therefore, the splanchnopleure lies over the top of the blood
1355
M
Fio. 113.-  Chick of 30 homs as seen by reflected light on a dark background, a from above, b from below, f.b., fore-brain with optic vesicles ;
m.b., mid-brain ; h.b., hind-brain ; a.i.p., anterior intestinal portal ; j}.s.,
primitive streak ; b.i., blood-islands ; ht., heart. Other letters as before.
VII EARLY DEVELOPMENT OF THE EMBRYO 179
islands, and the capillaries, when they are formed, are between
the splanchnopleure and the yolk-sac (Fig. 108).
There is thus an extra-embryonic as well as an intra-embryomc
coelom. The former is coextensive with the mesoderm, is found,
therefore, behind and at the sides of the embryo, but not in the
proamnion in front.
A network of blood-vessels soon appears in the area pellucida,
continuous with those of the area vasculosa. It seems that
these arise, not by encroachment of the capillaries of the latter
region upon the former, but in situ. They are formed from the
splanchnopleure and come into connexion with the others.
The blood-vessels of the embryo, the two dorsal aortae and the
cardinal veins, are also formed in situ from loose connective
tissue, mesodermal cells which come together to form tubes,
the vessels. The heart of the chick (and of all Amniota) is not,
however, formed in the body of the embryo after that has
been folded off from the blastoderm (as is the case in Fishes),
but from the union of two veins which lie on the right and
left, in the area pellucida, apparently outside the body of the
embryo.
These are the vitelUne veins, into which flows the blood from
the capillaries of the area vasculosa. By the actual process of
folding off the head and with it the fore-gut from the blastoderm,
the two veins are made to lie side by side underneath the foregut (Fig. Ill), where they coalesce to form a single median tube,
the heart (Figs. 112, 113). The heart lies in a cavity, the pericardium, which is simply the anterior portion of the coelom of the
lateral plate. As the head is folded off, somatopleure and
splanchnopleure are naturally folded off with it, and with them
the coelom. In the pericardium the heart is suspended by a
mesocardium to the ventral side of the gut. The vitelline veins
merely form the endothelium of the heart. Its muscular coat
comes from the splanchnopleure covering it.
Though thus derived from two separate veins the cavity of
the heart soon becomes single. The double origin has nothing
whatever to do with the subsequent division into systemic and
pulmonary portions. It is due simply to the fact that the veins
are there before the gut is folded off from the yolk-sac. In
M 2
180 EARLY DEVELOPMENT OP THE EMBRYO VII
Fishes the reverse is the case, and the heart is a single tube
from the beginning.
The heart continues to receive the two vitelUne veins at its
hinder end. These come from the anterior region of the area
vasculosa, which extends just as far as the mesoderm, that is,
up to the edge of the proamnion on each side.
The two viteUine veins reach the heart by travelHng along
the anterior edge of the opening of the fore-gut into the yolksac, or, to put it in another way, along the line which marks
the posterior limit of the head-fold of the endoderm. This
opening is the anterior intestinal portal.
At its anterior end the heart gives rise to the aortic arches
which pass round the sides of the throat between the gill-slits.
These take the blood into the two dorsal aortae, whence it
escapes, by the vitelline arteries, on to the area vasculosa again.
We shall study the distribution of the blood-vessels in the yolksac later on.
Just as the fore-gut so is the hind-gut folded off from the
yolk-sac, the opening being the posterior intestinal portal. The
middle region remains for some time widely open to the cavity
of the yolk-sac below, the communication being the yolk-stalk,
but as development j)roceeds this becomes reduced to a narrow
tube.
The changes we have so far described -  closure of the medullary
tube, differentiation of the mesoderm, formation of the coelom,
folding off of the head and fore-gut, and development of the
heart -  have all taken place before the thirtieth hour of incubation. Other events now occur (Eigs. 114, 115). The optic
vesicles become apparent as lateral outgrowths of the fore-brain,
the auditory vesicles are visible as two shallow pits Ijang one
on each side of the hind-brain, and between the thirtieth and
thirty-sixth hours the heart begins to be bent to the right-hand
side. The part of the heart that is so bent is the' ventricle, and
Avill become divided into the two ventricles of the adult heart.
In front of the ventricular region is the truncus arteriosus ; this
remains in the middle line and gives off the aortic arches. Behind
the ventricle is the auricle, also in the middle line, and behind
that the sinus venosus receiving the two vitelline veins.
.{J
ua.
A B
Fig. 114. -  Chick of 36 hours as seen, by transmitted light. A, from
above, b, from below. The heart is bent out to the right. The head-fold
of the amnion {am.) lias begun to grow over the head, o.v., optic vesicle ;
a.v., auditory vesicle ; v.a., vitelline artery. Other abbreviations as
before.
P. LBO
"0,0
p ram. dO ^ ^ r ' ' ^
-CS-c^TTT^T -  '.-Cc'-'^'
o r . .. , â–  â–  -g- -  Cv . -  -  = o.u
\
Fig. 115. -  Cliick of 44 hours' incubation with area pellucida and area
vasculosa, seen by reflected light. At x the mesoderm sheets have met in
front of the pro-amnion. au., auditory vesicle ; a.t;., area vasculosa. Other
letters as before. The head is beginning to turn to the right.
P. 180
am
/
, ^^^^ --^ L Wi'
A B
]TiG 116.-  Chick of 60 hours, A, from above by transmitted light, b, from
below'bv reflected light. The head is turned to the right and lies with its
left Tide on the yolk-sac. The fore-brain is bent down on the mid-brain
crania flexure) Ld the hind-brain slightly bent on the body (cervical
Kre) Three gill-slits are present (1, 2, 3) and three aortic arches
fman^bular hyoid. and first branchial). The optic cup and lens are
formed the'auditory vesicle has sunk into the head. The head-fold of
the amnion has groin over the head and partly over the trunk. The
hind-2ut is bei^inning to be folded ofi from the yolk-sac.
Z%oid arch ; h.g., hind-gut ; /./., tail-fold of embryo.
1'. 181
VII EARLY DEVELOPMENT OF THE EMBRYO 181
The head of the chick now begins to be turned to the right,
so that it lies with its left side upon the blastoderm (48 hours).
At the same time the fore-brain is beginning to be bent down
below the mid-brain so that the latter comes to lie at the anterior
end of the body. This is Imown as the primary cranial flexure.
Later, by the cervical flexure, the hind-brain becomes bent
down upon the body.
At the sides of the fore-brain may be seen the two optic cups - 
formed by pushing in the outer wall of the optic vesicles -  and
opposite the mouth of each optic cup the lens is being invaginated
from the superficial ectoderm. The head-fold of the amnion has
grown a little way back over the head.
By the middle of the third day (Fig. 116) all the four gill-slits
are formed, and there are three pairs of aortic arches conveying
the blood into the dorsal aortae. The blood which is distributed
to the body of the embryo makes its way back to the heart
by the anterior and posterior cardinal veins, and the ductus
Cuvieri.
The cerebral hemispheres are beginning to .be protruded from
the front of the fore-Dxain. The lens invagination has closed.
The auditory vesicle has sunk into the head and lost its connexion with the exterior. The amnion has grown back over the
head and front part of the trunk. By the end of the third day
the aminion is closed and the allantois is visible outside the body
of the erdbryo at the posterior end.
The foundations of the various systems of organs are now well
estabhshed. It will be clear that they arise in essentially the
same manner as in the frog. The nervous system -  medullary
tube and neural crest -  and the sense-organs do not differ in
any important particular. It may be pointed out, however, that
the lens (Fig. 117) and the auditory vesicle (Fig. 112, 5) are, in the
chick, invaginations of the whole thickness of the ectoderm, and
not merely of an inner layer. The pituitary body is a hollow,
not a solid upgrowth from the stomodaeum. The differentiations
of the primary mesoderm are the same in the two cases. Attention has already been directed to the mode of formation of the
heart. From the endoderm the same set of structures arises,
the gut and its outgrowths or derivatives, thyroid, gill-slits,
182 EARLY DEVELOPMENT OF THE EMBRYO VII
thymus, lungs, liver, pancreas, and bladder or allantois. We
shall have to refer to the last-mentioned again, as it is one of
the foetal membranes or appendages. Though the chick -  like
other Amniote embryo -  possesses gill-slits, formed in the same
way as in the frog by outgrowths of the pharynx wall, gills
are never present. The number of these gill-slits is four, namely,
the hyomandibular and three branchial. The first three are
perforated and remain open up to the fourth (first and second)
or fifth (third) day. The fourth slit is never open. The
Fig. 117. -  Development of the eye in the chick. A, Section including
the choroid fissure (transverse to the head) ; B, Section horizontal to the
head ; c. Section parallel to the sagittal plane of the head and so transverse
to the choroid fissure, o.st., optic stalk ; o.c.l, outer layer of optic cup ;
0.C.2, inner layer of optic cup ; le., lens ; ch.f., choroid fissure ; f.b., forebrain.
hyomandibular cleft remains to form the tympanic cavity and
Eustachian passage. The arterial aortic arches bear the same
relation to these gill-clefts as in the lower water-breathing forms,
but are not divided by the gill-capillaries into afferent and
efferent portions, and so pass uninterruptedly from the ventral
aorta (truncus arteriosus) to the dorsal aortae.
By the middle of the third day three aortic arches are formed.
A fourth is added at the end of the third day, and later two
more, thus making six in all. The first of these is the mandibular, the second the hyoid, the remaining the four branchial
aortic arches, being named from the gill-arches in which
they run.
0.C /
A
VII EARLY DEVELOPMENT OF THE EMBRYO 183
The two dorsal aortae unite posteriorly into one (Fig. 118).
The foetal membranes. The real difference between the early
development of the Amniota and the Anamnia is due to the
presence in the former of certain wrappings and appendages,
known as the foetal membranes.
The foetal membranes are the amnion, the false amnion or
chorion, the yolk-sac, and the allantois.
so
aTTl.C:
Fig. 118. -  Section through the hind end of the chick on the third day
when the amnion is closing, ec, ectoderm of false anmion with so., its
somatopleure ; ec'. and so'., ectoderm and somatopleure of true amnion ;
am.c, amniotic cavity ; c, extra-embryonic, c'., intra- embryonic coelom ;
u., umbilicus; m.L, medullary tube; d.r., dorsal root of spinal nerve;
7ny., myotom ; s.d., segmental duct (Wolffian duct after degeneration of
pronephros) ; cv., cardinal vein ; a., aorta ; v.a. vitelline artery ; spl.,
splanchnopleure ; en., endoderm ; g., gut.
The yolk-sac is the layer of endoderm with its covering of
vascular splanchnopleure which encloses the yolk. It is connected to the gut, which has been folded off from it by a hollow
stalk, the yolk-stalk (Fig. 120). In the splanchnopleure are the
vessels of the area vasculosa.
The origin of these has already been seen. The arrangement
of the main vessels undergoes considerable modification during
the first few days of incubation (Fig. 119).
At about the thirtieth hour the two vitelline veins (anterior
viteUine veins) come from the anterior end of the area vasculosa.
186 EARLY DEVELOPMENT OF THE EMBRYO VII
passing along the inner edge of the mesoderm which borders the
proamnion ; there they are seen to arise from an annular vessel - 
the sinus terminalis -  ^which runs round the edge of the area
vasculosa. Into this venous ring the blood leaks from the
capillaries of the area, to which it is brought by a pair of vitelline arteries which are given off from the aortae. These vitelline
arteries are only just being differentiated out of the network in
the area (Fig. 119, a).
A little later (44 hours) the vitelline arteries and their branches
are well developed. The two (anterior) viteUine veins are beginning to unite in front, just where they spring from the sinus
terminalis. At the same time traces of two new lateral viteUine
veins can be seen (Fig. 119, b).
On the third day the anterior vitelline veins are united in
front, and the right-hand one is being reduced in diameter. The
lateral viteUine veins are further advanced and receive their
blood from a central part of the network, which is now no longer
arterial but venous. This venous network is placed at the sides
of and behind the embryo. Veins-  called intermediate-  open
from it into the sinus terminaUs. The viteUine arteries-  which
are still better developed-  pass right through the venous network before breaking up into capiUaries in the marginal part
of the area vasculosa (Fig. 119, c).
On the fourth day the right anterior viteUine vein has nearly
disappeared, while the new lateral vitelUne veins are conspicuous,
receiving their blood from the central part of the area vasculosa.
From this central part the blood passes also in the other direction
by the intermediate veins into the sinus terminaUs. There is
also a single posterior vitelline vein which, arises from the sinus
terminaUs : it lies on the left-hand side.
The arteries go through the central venous area as before
to reach the marginal part. They course alongside the mam
venous trunks, lying always on the ventral side of the latter
(Fig. 119, D). . ....
FinaUy (on the tenth day) the anterior and posterior vitelline
veins, the intermediate veins, and the sinus terminaUs aU disappear, and only the lateral veins are left.
The Uning epitheUum of the yolk-sac-which is made of large
VII EARLY DEVELOPMENT OF THE EMBRYO 187
vacuolated columnar cells -  is produced internally into septa
(Fig. 121), which are perforated by stomata.
The septa are suppUed with blood-vessels from the area
vasculosa.
As the blastoderm grows over the yolk the latter becomes
more and more completely enclosed by the yolk-sac, the edges
of which finally almost meet.
With the growth of the blastoderm the mesoderm and the
extra embryonic coelom have also been advancing, so that
the yolk-sac with its covering of vascular splanchnopleure
becomes more and more detached from the somatopleure,
until only a very small connexion is left between the two
(Fig. 120, 4).
On the nineteenth day the yolk-sac, togethet with the adherent
albumen sac (see below) is drawn into the body-cavity through
the umbilicus, where it remains visible for some time as an
appendage of the ahmentary canal.
The amnion arises (Figs. 118 and 120, 1-3) by the formation
of a fold of the extra embryonic ectoderm, together with the
somatopleure which is appUed to it. The yolk-sac and its
splanchnopleure have no share in the process.
There are four parts to the amnion fold, the head fold, which
arises first and is much larger than the others, the tail fold, and
the two lateral folds.
The extra-embryonic coelom is continued into the folds, each
of which consists of two layers. The folds grow up over the
back of the embryo and meet and fuse towards the posterior
end of the body. When the fusion is complete the outer layer
of the folds is separated from the inner by the coelom. Each
is composed of a sheet of ectoderm and a sheet of somatopleure.
The outer layer, now detached from the body of the embryo,
is continuous with the two upper layers, ectoderm and somatopleure, of the extra-embryonic blastoderm. It is known as the
false amnion or chorion or serosa. The inner layer, on the other
hand, also composed of ectoderm and somatopleure, is continuous
with the two corresponding layers of the body-wall of the embryo.
It is known as the true amnion. The embryo has meanwhile
been folded off, but a large aperture is necessarUy left on its
188 EARLY DEVELOPMENT OF THE EMBRYO VII
ventral side. This aperture is the umbilicus or navel. The
amnion, therefore, now forms a completely closed sac inside
which the body of the embryo is placed : the sac being inserted
into the edges of an aperture, the umbilicus, which is left on the
ventral side of the body. Through this aperture the intra embryonic is in free communication with the extra-embryonic
coelom ; through it pass out the stalks of the yolk-sac and the
allantois. The amriiotic cavity is filled with a fluid, the liquor
amnii. The function of the amnion is to act as a water-bath
and protect the embryo against shocks.
It has just been said that the false amnion becomes completely
separated from the true. This is not quite accurate, since a small
double strand of somatopleure is left at the point of closure, the
sero-amniotic connexion (Figs. 120, 4, and 121). On the eleventh
day this connexion becomes perforated and some albumen makes
its way from outside into the amniotic cavity.
The false amnion continues to grow round the yolk with the
rest of the extra-embryonic blastoderm, of which it is, of course,
the outer layer. At its edge it is continuous, as heretofore, with
the wall of the yolk-sac, the somatopleure of the false amnion
mth the splanchnopleure of the yolk-sac, the ectoderm of the
former with the epithelium of the latter (Fig. 120). With the
final enclosure of the yolk (Fig. 121) the false amnion practically
becomes a closed sac, inside which lies the embryo in its amnion
with its yolk-sac and its allantois.
The allantois is a median ventral diverticulum of the hind
gut (Fig. 120, 3). It is covered by a layer of splanchnopleure.
It grows out and through the umbilicus into the extra-embryonic
coelom, where it expands into a large sac occupying aU the available space between the amnion and yolk-sac on the inside, and
the false amnion on the outside (Fig. 120, 4). The splanchnopleure covering it is vascular, and by means of its blood-vessels,
the umbilical arteries and veins, the allantois is enabled to
function as a respiratory organ. It is appHed closely to the
inside of the porous shell ; and here oxygen is taken up and
carbon dioxide given oflE by the blood in its capillaries.
At the narrow end of the shell the allantois pushes out the
false amnion in the form of a circular fold which encloses the
VII EARLY DEVELOPMENT OF THE EMBRYO 189
Fig. 120. -  Diagrams shoMdag the formation of the amnion, false amnion,
yolk-sac, and allantois in the chick.
1, Transverse section. The lateral folds of the amnion are rising up ; the
gut is not yet folded oS from the yolk-sac.
2, Transverse section. The aimiion is closed and the gut is folded off
from the yolk-sac. The section passes down the yolk-stalk.
3, Longitudinal section, when the amnion is about to close and, the allantois is beginning to grow out.
4, Longitudinal section of a later stage, when the allantois has extended
into the extra-embryonic coelom, and the yolk has nearly been enclosed
at the vegetative pole.
In all the diagrams the ectoderm is represented by a thin continuous
Ime, the mesoderm by a thick line swollen at intervals, the endoderm by
a thick broken line, while the yolk is shaded. Lam., lateral amnion fold ;
A.am., head amnion fold; t.am., tail amnion fold; am., true amnion ;
J.am., talse amnion ; am.c, amniotic cavity ; s.a.c, sero-amniotic connexion ; M., umbilicus; c, extra- embryonic coelom; all., aUantois :
y., yolk in yolk-sac. '
190 EARLY DEVELOPMENT OF THE EMBRYO VII
albumen. This is the albumen sac (Fig. 121). The albumen
loses a great deal of water by evaporation during incubation.
What remains of the albumen sac passes along with the yolk-sac
through the umbilicus into the body cavity of the embryo.
At the time of hatching the amnion is broken and, with the
allantois and false amnion, shrivels up. Morphologically, the
Fig 121 - Diagram of the final arrangement of the foetal membranes
in the chick. (After Duval and LiUie.) sh., shell; a.ch., air-chamber;
all, allantois ; a.st, stalk of aUantois ; a.s., albumen sac ; x., pomt ot
closure of yolk-sac ; am.c, amniotic cavity ; s.a c., sero-ammotic connexion ; c, extra-embryonic coelom ; y., yolk m yolk-sac.
aUantois is an extra-embryonic bladder. It is, like the bladder
of Amphibia, a median ventral diverticulum of the hind gut.
Its veins, the umbilical veins, take the' same peculiar course as
is taken by the anterior abdominal vein of the Amphibia, which
receives the blood from the bladder, namely, in the ventral bodywaU, and thence into the capillary system of the liver. In the
Reptiles the umbiHcal veins of the embryo remain as the anterior
abdominal vein or veins of the adult. Lastly, the stalk of the
aUantois persists as the bladder in the Reptiles and Mammals.
In Birds the bladder is absent.
The same foetal membranes are present in all Ammota. in
VII EARLY DEVELOPMENT OF THE EMBRYO 191
the Ditrematous Mammalia they merit particular attention. The
variety of their behaviour is manifold ; the amnion has many
modes of formation, the yolk-sac, though innocent of yolk, is
always present to point to the descent of the small-yolked
MammaHan ovum from some large-yolked type, while the allantois vascularizes a placenta developed from the trophoblast, or
ectoderm of the false amnion. To the study of these questions
we may now proceed.
LITERATURE
F. M. Balfour. Comparative Embryology, vol. ii, London, 1885.
T. H. Bryce. Embryology, vol. i of Quain's Anatomy, London, 1908.
M. Duval. Atlas d'Embryologie. Paris, 1887.
0. Hektwig. Handbuch der Entwicklungslehre der Wirbeltiere. Jena,
1906.
0. Hertwig. Die Elemente der Entwicklungslehre des Menschen und
der Wirbeltiere. Jena, 1910.
N. K. KoLTZOFF. Entwickelungsgeschichte des Kopfes von Pelromyzon
planeri. Bull. Soc. Imp. Nat. Moscou, 1901.
F. R. LiLLiE. The development of the chick. New York, 1908.
A. IVIiLNES Marshall. Vertebrate Embryology. London, 1893.
C. S. MiNOT. A Laboratory Text-book of Embryology. Philadelphia,
1910.
T. H. Morgan. The development of the frog's egg. New York, 1897.
J. RiiCKERT. Die Entwickelung von Blut und Gefassen der Selachier,
in 0. Hertwig's Handbuch der Entwicklungslehre der Wirbeltiere. Jena, 1906.
==CHAPTER VIII THE FOETAL MEMBRANES OF THE MAMMALIA==
The same foetal membranes are found in the Mammalia as
in the Reptiles and Birds, namelj', the chorion or false amnion,
the true amnion, the yolk-sac, and the allantois. Here, however,
the yolk-sac, except in the Monotremata, is devoid of yolk ; but
it has the same anatomical relations, as an appendage of the gut,
as in the other groups, and in its splanchnopleure are developed
the blood-vessels of an area vasculosa supplied by a pair of
vitelline arteries from the aorta, and by a pair of vitelline veins
which enter the hind end of the heart. The size of the yolk-sac
varies greatly in the different orders of Placental Mammals.
The allantois is always found, though its cavity may be very
greatly reduced. Its function is, in the Placental Mammals, to
carry the foetal blood-vessels to and from the placenta. It may
also act as a receptacle for the waste products of the foetus.
Its stalk inside the body of the embryo always persists as the
bladder. The amnion is chiefly of interest owing to the peculiarities of its mode of formation in PlacentaUa. The false amnion
or chorion, enveloping as it does the embryo and these other
foetal membranes, naturally comes into contact with the uterine
wall, except in the Monotremata, and so brings about that
relation between foetal and material tissues which constitutes
a placenta. Its outer ectodermal layer is known as the trophoblast.
Monotremata (Fig. 122, a)
The formation of the foetal membranes has not so far been
described, but from the persistence, over the back of the embryo,
of the connexion between the false and the true amnion, it may
be gathered that the amnion was formed, as in the Sauropsida,
VIII FOETAL MEMBRANES OF THE MAMMALIA 193
by folds of ectoderm and somatopleure. Yolk-sac and aUantois
are both large, the former lies on the left, the latter on the right
of the embryo.
all
YiG. 122. -  Foetal membranes of A, Monotremata ; b, c, d, Marsupials.
B, Phalangista, Aepyprymnus, Didelphys, Bettongia ; c, Dasyurxis ; D,
Perameles and Halmaturus. (In Didelphys the proamnion persists as in
Dasyurus.) (a, b, d, after Semon; 0, after Hill.)
In this and the following diagrams of Mammalian foetal membranes the
trophoblast (ectoderm of false amnion) is stippled, the ectoderm of the
true amnion represented by a continuous line, the endoderm by a broken
line, and the mesoderm (somatopleure and splanchnopleure) by a thick line
swollen at intervals. aZZ., aUantois ; am.c, amniotic cavity; pr. proamnion ; y.s., yolk-sac ; s.t., sinus terminalis of area vasculosa.
Mabsupialia (Fig. 122 b, o, d)
We do not know the mode of origin of the amnion, but it is
to be presumed, from the description of the structure of the
blastocyst in Dasyurus, that the amnion is formed from folds,
and that these arise at the edge of the embryonic area. The
1355 -w
194 FOETAL MEMBRANES OF THE MAMMALIA VIII
inner laj'er of the folds -  true amnion -  would then be derived
from the embryonic area, while the outer layer -  false amnion - 
would come from the trophoblastic area, of which the other
part of the blastocyst is composed.
There is generally a large proamnion -  that region of the
amnion below the head of the embryo from which mesoderm
is absent -  and this may persist {Dasyurus, Didelphys, Perameles).
In all Marsupials the yolk-sac is very large, its upper wall
invaginated by the embryo. Between the lower (distal) wall
and the trophoblast the mesoderm never completely extends,
is absent in fact in the anti-embryonic half of the blastocyst,
and in the mesoderm the extra-embryonic coelom never extends
further than the line where the proximal turns over into the
distal wall of the yolk-sac. In the mesoderm of the yolk-sac
there is an area vasculosa, and at the extreme edge an annular
vessel -  ^the sinus terminalis. The allantois is always small. In
some cases -  Didelphys, Aepyprymnus, and others -  it altogether
fails to reach the false amnion, and its blood-supply is very
poor. In others, however {Phascolarctos, Halmaturus, Perameles),
the allantois is larger, reaches the trophoblast, and possesses
well-developed blood-vessels, which in Perameles vascularize a
placenta. This placenta, as we shall see below, has a very
peculiar stru'cture.
Placentalia
The first of the foetal membranes to claim our attention must
be the amnion, for though in a Placental Mammal the amnion
may ultimately be formed by folds resembling those of the Bu-ds
and Reptiles, yet this is not always so ; and even when that
method does obtain, there is very good reason for supposing it
to be not primary, but secondary.
In the Reptiles, Birds, and Monotremes we have seen that
sooner or later, with the final enclosure of the yolk by the blastoderm, the false amnion comes to be a completely closed sac, in
which lie the embryo in its amnion, with its yolk-sac and allantois.
The cavity of the sac is extra-embryonic coelom ; its wall consists
of an outer ectodermal and an inner somatopleuric layer.
In Placental Mammals this condition is realized almost in the
VIII FOETAL MEMBRANES OF THE MAMMALIA 195
first moment of development, for the first act of differentiation
is the separation of the inner mass from the outer layer, and, as
we are now to see, the inner mass contains within itself the
material for the embryo, its amnion, yolk-sac and aUantois, and,
we may add, the somatopleure and splanchnopleure of the extraembryonic coelom, while the outer layer or trophoblast is the
representative solely of the ectodermal covering of the false
amnion. It cannot be too often insisted that all Placental
Mammals pass through this stage in which the material for the
embryo with its membranes is shut up inside the sac of the
trophoblast.
The next step is the separation in the inner mass of the
embryonic knob-  which comprises the material for embryo and
amnion-  from the lower layer-  from which alimentary canal,
yolk-sac, and aUantois are derived. The lower layer quickly
grows round the inside of the blastocyst.
There follows the formation of the amnion ; two main types
of which may be distinguished. In the first of these the future
amniotic cavity is never open to the exterior, and the trophoblast over the embryonic knob persists. In the second the cells
of the trophoblast overlying the embryonic knob-  the so-called
cells of Rauber-  disappear, the embryonic knob comes up to
the surface and the amnion is eventually formed by folds in
a manner resembling that seen in Reptiles and Birds.
Of each of these types there are again two divisions.
I. (a) In the first division of the first type the future amniotic
cavity never opens into any other cavity at all ; it arises either
inside the embryonic knob (Cavia), or between that and the
trophoblast {Erinacells).
(b) In the second division are those cases in which the amniotic
cavity, developed in the embryonic knob, is in transitory
communication with another cavity formed in the thickened
overlying trophoblast. The connexion is soon lost and the
trophoblastic cavity disappears {Mus, Arvicola).
II. (a) In the first division of the second type the embryonic
knob is gradually folded out and becomes the embryonic plate.
This is seen in Talpa, Tupaia, Vespertilio, Sus, Tarsius.
(6) In the other division the embryonic knob simply flattens
, N 2
196 FOETAL MEMBRANES OF THE MAMMALIA VIII
oiit without the formation of any depression, and so becomes
the embryonic plate {Learns, Ovis, Sorex).
As a good example of type I (a), we may take the guinea-pig
iCavia) (Fig. 123). After the separation of the lower layer the
embryonic knob begins to move away from its original pole of
attachment to the opposite end of the oval blastocyst, as it does
so pushing the lower layer in front of it. This lower layer
represents here the upper wall of the yolk-sac only (and the
alimentary canal of the embryo), the lower wall being never
formed in the guinea-pig. The margins of the lower layer
remain attached to the trophoblast at the original embryonic
end. When the embryonic knob has reached the opposite end
a cavity appears in it ; this will be the amniotic cavity. The
cells lining this cavity are at first columnar, but a difference
soon appears between those next the yolk-sac and those on the
side facing the original embryonic pole. The former remain
columnar and represent the embryonic area of the upper layer
of a ReptiUan blastoderm ; from these cells the blastopore,
archenteron, notochord, and mesoderm presently originate, the
remainder being the ectoderm. The latter soon become flattened
and represent the inner part of the extra-embryonic blastoderm
of the Reptiles ; this wall of the cavity becomes the (true)
amnion. Meanwhile the germinal layers have been formed and
the mesoderm soon extends outside the embryonic region into
the space between the amnion below, the trophoblast above,
and the yolk-sac at the sides ; a cavity appears in this mesoderm
which is the extra-embryonic coelom, and is continuous with the
coelomic cavity in the embryo. Where this mesoderm covers
the trophoblast it is somatopleufe, where it hes over the upper
wall of the yolk-sac it is splanchnopleure, and where it passes
over the amnion it is somatopleure again.
The development of the embryo continues, and its body is
folded oflE from the amnion, the fine of attachment of amnion
to body-wall being brought continually nearer the mid-ventral
line of the embryo and the umbiUcus so narrowed. The gut of
the embryo has meanwhile been folded ofi from the yolk-sac,
the stalk of which passes through the umbihcal aperture.
The trophoblast has now essentially the same relations to the
VIII FOETAL MEMBRANES OF THE MAMMALIA 197
yolk-sac, embryo, and amnion, as has the false amnion of tho
chick when the blastoderm has completely invested the yolk.
In the chick at this moment the false amnion is a completely
closed sac enveloping the embryo in its amnion with its yolksac ; in the guinea-pig the trophoblast does the same, rhe
differences are due to : (1) the absence of a lower wall to
the yolk-sac ; (2) the restriction of mesoderm and coelom to the
re-ion between the trophoblast, the upper wall of the yolk-sac,
a.tr
tr.c.
Fig 123.-  Formation of the amnion in the guinea-pig (Caw'a). (After
Selenka.) a, early, B, later, c, latest stage, a.tr allantoidean (placental)
trophoblast; o.Jrf.omphaloidean trophoblast ; lacuna ; e.fc., embryonic
knob ; am.c, amniotic cavity ; y.s., yolk-sac.
and the embryo in its amnion ; and (3) to the invagination of
the embryo into the upper wall of the yolk-sac.
Thus the amniotic cavity has developed as a cavity closed
from its very inception.
The method of amnion formation in Monkeys and Man is not
yet known, but it seems very possible that it is according to
this first type.
The absence of the lower wall of the yolk-sac led, many years
since, to a curious misinterpretation of the development of the
guinea-pig, which w^as known as the ' Inversion of the Germinal
Layers '. Early investigators missed altogether the trophoblast
in the region of the yolk-sac-  which is indeed thin and closely
198 FOETAL MEMBRANES OF THE MAMMALIA VIII
adherent to the uterine tissues -  and then found the emhryo in
its amnion enveloped in a membrane which was -  as we now
know -  the upper wall of the yolk-sac. This membrane they
traced into the alimentary canal and so called it endoderm. At
the other end of the blastocyst the same membrane was found
adherent to the trophoblast -  here thickened in connexion with
the development of the placenta -  and believed to be continuous
with it. The wall of the blastocyst was therefore endodermal
Fig. 124. -  Formation of the amnion in thehedgehog (Erinacevs.) (After
Hubrecht.) ir., trophoblast ; y.s., yolk-sac ; e.k., embryonic knob ; cwi.,
amnion ; I., lacuna ; ec, ectoderm of embryonic plate ; n., notochord ;
m., mesoderm ; c, extra-embryonic coelom. a, early, b, later stage,
and the germinal layers had in some mysterious fashion become
turned inside out. The mistake was cleared up by the researches
of Selenka.
Although in the hedgehog the amniotic cavity is not formed
in quite the same way as in the guinea-pig, yet it never opens
to the exterior or into any other cavity. The embryonic knob
becomes detached in its centre from the trophoblast, while
remaining adherent to it by its edge. The space between the
two will be the cavity of the amnion. As the space enlarges
the embryonic knob becomes transformed into a ciirved plate
of columnar cells -  the embryonic plate -  ^the edges of which are
rather thinned out. The cavity continues to enlarge and the
thin edges, of flattened cells, grow up and in between the trophoblast and the cavity, so forming a roof to the latter. This roof
is the amnion. In the meantime the coelom has been formed
200 FOETAL MEMBRANES OP THE MAMMALIA VIII
and extends up with the amnion between the trophoblast and
the embryo (Fig. 124).
I. (b) In the mouse, rat and field-mouse the same invagination
of the embryo into the upper wall of the yolk-sac that we have
seen in the guinea-pig also occurs, and is indeed found, though
not necessarily at this early stage, in all Rodents. Here, however, the distal wall of the yolk-sac is complete. Further, the
embryonic knob never leaves the trophoblast at the original
embryonic pole, but is driven to the other end of the blastocyst
by a great thickening of the trophoblast, which is associated with
the formation of the placenta (Fig. 125).
Soon a cavity appears in the embryonic knob -  ^the amniotic
cavity -  and this immediately comes into communication with
a cavity in the trophoblast. As soon, however, as the extraembryonic coelom is formed it extends into this region, forces
the trophoblast away, and severs the connexion. The trophoblastic cavity disappears. That developed in the embryonic
knob then becomes the amniotic cavity in precisely the same
way as in the guinea-pig.
It is evident that here also the amnion is derived from the
material of the embryonic knob, that the trophoblast is the
homologue of the ectoderm of the false amnion alone.
II. {a) (Fig. 126). A depression appears in the embryonic
knob. By the disintegration of the overlying trophoblast cells this
depression comes to open to the exterior. The embryonic knob
increases in size, the depression becomes wider and shallower,
and the knob -  or, as we may now call it, the embryonic plate - 
finally comes up on a level with the surface of the blastocyst.
It is inserted by its edges into the surrounding trophoblast.
The amnion is formed by folds, which arise at the boundary
of the embryonic plate. It is difficult to be certain, but it seems
that the outer layer of the fold, that is, the false amnion, arises
from the trophoblast, while the inner or true amnion comes
from the embryonic plate itself.
II, (6) The amnion is formed in precisely the same way in
this division ; there is, however, no folding out of the embryonic
knob : it becomes directly flattened to form the plate. The
overlying cells of Rauber disappear (Fig. 127).
VIII FOETAL MEMBRANES OF THE MAMMALIA 201
Fig. 126. -  Formation of the amnion in Tupaia (an Insectivore). a-e,
Five stages ; e.p., embryonic plate ; R., cells of Rauber. Other letters as
before. (After Hubrecht.)
Fig. 127. -  Formation of the amnion in the rabbit (Lepus) ; i.m., inner
mass ; l.L, lower layer ; e.p., embryonic plate ; B., cells of Rauber. (After
Assheton.)
In this second type -  where the amnion is eventually formed
by folds, the tail-fold often arises, as in Tarsius and the rabbit,
before the head-fold (Fig. 128). Otherwise the resemblance
between the way in which this membrane of the foetus is
202 FOETAL MEMBRANES OF THE MAMMALIA VIII
developed iu Placental Majunials and that seen in other forms
is certainly very close, and this similarity has suggested that
this is the primitive method of amnion formation in Placental
Mammals -  as distinct from the rest of the class -  and that those
cases (type I) where the amniotic cavity appears inside the
embryonic knob are secondary modifications due to the restricted
space in which the blastocyst developes. It is perfectly true
that the blastocyst is compressed by the narrow limits of the
space in which it is fixed in Erinacells, Cavia, and Mtis. To the
Fig. 128. -  Further stages in the formation of the amnion in the- rabbit.
(After Van Bcneden.) h.am., head amnion fold ; t.am., tail anmion fold ;
e., embryo; aZZ., allantois ; a.<r., allantoidean trophoblast ; y.s., yolk-sac ;
olir., omphaloidean trophoblast ; c, extra-embryonic coelom ; s.t., sinus
terminalis of area vasculosa.
proposed hypothesis there is, however, one fatal objection, and
that is the presence of Rauber's cells in members of the second
type, the existence of a stage in which the material for the
embryo and amnion is wholly enveloped in a closed sac, which
is the homologue of the false amnion of Reptiles, Birds, and
Monotremes. This is a stage through which all Placental Mammals pass, and in an Insectivore, some Rodents, and possibly
in Monkeys and Man, the sac of the trophoblast remains closed.
In others, after the disappearance of Rauber's cells, the embryomc
knob comes to the surface and amniotic folds are developed.
We are justified, therefore, in regarding the first condition as
VIII FOETAL MEMBRANES OF THE MAMMALIA 203
the primitive, the second as derived from it, and in supposing
that one of the first effects of that loss of yolk which we know
the ovum of the Placental Mammals has undergone, as compared
first with the Marsupials and next with the Monotremes, was
a precocious separation of the material for the embryo and its
amnion from a closed sac, inside which the differentiation of the
germ-layers and of the other foetal membranes could take place,
secure from the pressure exerted by the contraction of the
uterine walls. The loss of the shell, still retained by the Marsupials, may have been a contributory cause. Such a development has been preserved in those cases where the uterine cavity,
or that part of it wherein the embryo is lodged, is narrow ; where
it is wider reversion to the original method of forming amniotic
folds has taken place, vmless we prefer to regard this as an
independent piece of evolution. (The possibiHty of such an
independent evolution is shown of course by the existence of
amniotic folds in other animals, for example, in Insects.) Since
the depression which marks the beginning of the folding out
of the embryonic knob is probably the remains of the closed
amniotic cavity seen in type I, the complete series illustrates
the process of reversion to the original MammaUan method,
while the distribution of type II over several orders (Insectivora,
Cheiroptera, Ungulates, Rodents, Primates) is sufficient evidence
of its repeated and independent occurrence.
The Yolk-sac ahd Allantois
In the extent to which they are developed these vary greatly
in the different orders.
In Rodents (Figs. 123, 125, 128) the yolk-sac is always large,
and its upper wall sooner {Cavia, Mus) or later {Lepus, Sciunis)
invagmated by the embryo. The mesoderm never extends
fiu-ther than the edge of the upper wall. In the sj)lanchnopleure
there is a well-developed area vasculosa, the blood-vessels of
which convey to the embryo the nutrient materials absorbed
by the yolk-sac from the uterus in the following way. The distal
(lower) wall of the yolk-sac always disappears (in Cavia it is
never formed) and then the lumen of the yolk-sac communicates
freely with the uterine cavity. In the fluid contained in this
204 FOETAL MEMBRANES OF THE MAMMALIA VIII
cavity is tho protoicl and fatty material secreted by tlie uterine
glands ; tliis is absorbed by the highly columnar, folded epithelium of the upper wall of the yolk-sac. The allantois is never
large but may be quite well developed. In the mouse and
guinea-pig, however, the ejiidodermal outgrowth of the hind-gut
is confined within the limits of the embryo's body, and only
the vascular splanchnople\ire passes out through the umbilicus
Fig. 128*.-  Area vasculosa of the yolk-sac of the rabbit. (After Van
Beneden and Julin.) ViteUine veins black, vitelKne artery and smus
terminalis stippled.
and across the extra-embryonic coelom to convey the foetal
blood-vessels to and from the placenta.
In the Camivora (Fig. 129) the yolk-sac is smaU compared to
the aUantois, and of no importance in the later stages of development, though large and no doubt functional at first. So also
in the Ungulates (Fig. 130). Of a fair size at first and provided
with an area vasculosa, it is rapidly outgrown by the allantois,
which attains enormous dimensions (Fig. 131), extending from
one end of the elongated chorionic (trophoblastic) sac to the
Fig. 129. -  ^Foetal membranes and placenta of the dog. m., mesometrium ; pi., zonaiy placenta. Other letters as before. (After Duval.)
Foetal blood-vessels in black in this and the following diagrams.
Fig. 130.
.- Foetal membranes of the horse, early stage. (After Bonnet.)
Letters as before.
206 FOETAL MEMBRANES OF THE MAMMALIA VIII
other, and occupying a very considerable space in the uterus.
In its cavity are found floating large oval bodies, often very
hard, known as hippomanes. These, as well as the fluid contents
Fig. 131.-  Foetal membranes of the horse, later stage. (After Bonnet.)
villus; eiJ.i^., epithelial thickenings of amnion ; A., hippomanes. Other
letters as before.
of the allantois, we shall describe when we deal with the
physiology of the placenta.
In the pig and sheep the tapering ends of the allantois and of
the chorion which covers them, the so-called ' diverticula allantoidis ', undergo a partial degeneration. They are sharply marked
off from the main body by an annular thickening pro^^ded with
a sphincter muscle.
VIII FOETAL MEMBRANES OF THE MAMMALIA 207
In the Insectivora (Fig. 132), again, the yolk-sac is usually
large in early stages of gestation, and its blood-vessels may
actually (Tupaia) begin to penetrate the placental thickening of
the trophoblast. But as the allantois dcvelopes it drives away
the yolk-sac, and the importance of the latter is diminished,
though it remains till the time of birth. In Talpa, Erinacells,
and So7-ex, the lower (anti-embryonic) wall of the yolk-sac is
Fig. 132. -  ^Foetal membranes and placenta of the hedgehog. (After
Hubrecht.) l.u., lumen uteri ; d.r., decidua reflexa. Other letters as before.
never covered by mesoderm. In Sorex the yolk-sac contains
a bright green pigment, which is either biliverdin or nearly
related to it, and is derived from the digestion of extravasated
maternal corpuscles which have been eaten by the phagocytic
trophoblast.
In the Cheiroptera (Fig. 133) similar conditions are found.
The yolk-sac, large and important in early stages, is later replaced
by the allantois.
Of the Edentate foetal membranes we know little, except that
in the sloth Choloepus the allantois is small, the amniotic cavity
208 FOETAL MEMBRANES OF THE MAMMALIA VIII
large enough to obliterate the extra-embryonic coelom, while
the yolk-sac in the stage described has vanished. The same
obliteration of the extra-embryonic coelom seems to occur in
the Cetacea {Orca) and Proboscidea (ElepMs).
nm.c.
aWr
{ ^
A''
B'tiT^ >1 Ik
1' \ r
\ rJi'
i t
mi
Fig. 133. -  ^Foetal membranes and placenta of the bat ( Vespertilio).
(After Nolf.) Letters as before.
In the Sirenia (Halicore) the aUantois is as large as in Ungulata,
extending to both ends of the chorionic sac.
In respect of their foetal membranes the Primates faU sharply
into two groups.
In the Lemuroidea (Fig. 134) the yolk-sac seems to disappear
early, while the aUantois is very large, as in an Ungulate ; the
placenta also, as we shall see, is of the Ungulate type. In the
VIII FOETAL MEMBRANES OF THE MAMMALIA 209
Authropoids-Moiikeys and Man-with which we must associate
Tarsius- nsnany classified as an aberrant Lemur-  the arrangement of the foetal membranes is utterly unlike anythmg found,
anywhere else amongst the Mammalia. The yolk-sac is dimmutive but vascular (Fig. 138), the endodermal cavity of the allantois is smaU and almost confined within the body of the embryo,
Fig. 134.-  Foetal membranes of the lemur. (After Turner.)
v., villi. Other letters as before.
its splanchnopleure alone passing out to the placenta, while the
extra-embryonic coelom is precociously developed.
In Tarsius the complete history of these membranes has been
given to us by the researches of Hubrecht (Fig. 135). As a result '
of a proliferation of cells at the hinder end of the embryonic
plate a sac is formed lying posteriorly between the trophoblast
and the small yolk-sac. This sac is the extra-embryonic coelom.
Very quickly it extends until it occupies a very large proportion
1355 o
210 FOETAL MEMBRANES OF THE MAMMALIA VIII
of the blastocyst. Where it covers the lower wall of the yolk-sac
it is, of course, splanchnopleure ; elsewhere, applied to the trophoblast, somatopleure. There is at present no mesoderm between
the embryonic plate and the yolk-sac. Thus this extra-embryonic
Fig 135-  Development of the foetal membranes in Tarsius. (After
Hubrecht ) a., blastocyst before Rauber's cells have disappeared ; b, the
embryonic knob (e.k.) is being folded out to the surface ; the yolk-sac is
complete ; c, the embryonic plate (e.p.) is at the surface, the extra-embryonic coelom (c) is formed ; d, the tail-fold of the ammon is growing forward It.am.), the allantois (all.) has penetrated 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 (pi.).
.mesodermal sac is well formed before the middle layer exists
in the embryo. The yolk-sac remains small. Meanwhile, the
amniotic folds have appeared, the tail-fold first, and a.s this
grows forwards over the back of the embryo a solid cord of
mesoderm is left connecting the hind end of the embryo with
the trophoblast. The amnion closes, the embryo is developed
Fig. 136. -  Two stages in the development of the foetal membranes in
a monkey [Cercocebus). (After Selenka). Letters as before.
Fig. 137. -  Early human cmbrj'o with its membranes. (After Peters.)
d.h., dccidua basalis (serotina) ; d.r.ep., uterine cjiitholium covering the
dccidua refloxa or capsulaiis ; I., lacuna in trophoblast (tr.) ; (il., \itorine
gland ; m.b.v., maternal blood-vessels opening here and tliore into lacunae ;
cl., clot niai-king (probably) the point of entrance of the blastocyst ; licro
the cpitlicliuiu is interrupted. Other letters as before.
O 2
212 FOETAL MEMBRANES OP THE MAMMALIA VIII
and folded o£E inside it, and the cord -  which carries the allantoic
or umbilical blood-vessels and is indeed the umbilical cord - 
moves round until it is inserted into the original anti-embryonic
pole of the trophoblast. It is here that the placenta is formed.
The base of the cord is penetrated by the rudimentary allantoic
outgrowth of the hind-gut.
If As??'
amc.
Fig. 138.-  a, Longitudinal section of older human embryo. The allantois has grown out and penetrated the base of the body-stalk (6.s<.) (future
umbilical cord). At the hind end of the embryo is a large blastopore (socalled neurenteric canal) leading into the yolk-sac. The gut has hardly
yet been folded off. Underneath the medullary plate and in front of the
blastopore is seen the notochord. (This figure should be compared with
that of the bat, Fig. 93, a.) h.v., blood-vessels in the splanchnopleure of
the yolk-sac. Other letters as before.
B. Transverse section of the body-stalk in the plane indicated at b in a.
Above is seen the amniotic cavity, below the aUantois, and at the sides
the umbilical arteries and veins. (After Graf Spee.)
The mutual relations of the membranes in Monkej's and Man
are similar, but their origin has not yet l^een seen. We do
know, however, that in the earliest human embryo yet described
(Fig. 137), and in the corresponding stage observed in Monkeys
(Fig. 136), there is a large extra-embryonic coelom, a smaU
yolk-sac attached firmly to the lower side of the embryonic
plate which itself forms the floor of a small cavity, the future
VIII FOETAL MEMBRANES OF THE MAMMALIA 213
amniotic cavity, the roof of which is the amnion. The embryo
in its amnion with its attached yolk-sac is suspended to the
somatopleure of the trophoblast by a short cord or stalk
of mesodermal tissue. In this the umbilical artery and vem
^^n\l be developed, while the rudimentary allantois will penetrate
its base (Fig. 138). This cord is the so-called ' ventral stalk ' ;
Fig. 139. -  ^Human foetal membranes and placenta. (After Balfour, after
Longet.) The amniotic cavity {am.c.) has enlarged and occupies nearly
the whole of the extra-embryonic coelom (c), being reflected over the
umbilical cord (u.c.) and yolk-sac {y.s.). d.b., decidua basalis (serotina) ;
d.r., decidua capsularis (reflexa) ; d.v., decidua vera ; l.u., lumen uteri ;
am., amnion ; pi., placenta ; o.d., oviduct.
but it is not in this early stage ventral in position, but rather
posterior and dorsal. Body-stalk (Minot) would be a preferable
term. Though we do not know the precise mode of developmsnt
of these structures, it would probably not be too hazardous to
surmise that the amniotic cavity has been formed, as in the
guinea-pig, inside the embryonic knob and not by folds, that the
extra-embryonic coelom was developed with the first formation
of mesoderm, and that the body-stalk is the attachment left
214 FOETAL MEMBRANES OF THE MAMMALIA VIII
between embryo and trophoblast when this cavity spreads under
the yolk-sac and over the amnion. The allantois -  or rather the
umbilical cord -  would not then grow out to reach the trophoblast, for it would have been united with it ab initio.
Later on the umbilical cord shifts its insertion on to the
ventral side of the body of the embryo, as the hinder end of the
latter is folded off inside the amniotic cavity. It retains its
original point of union with the trophoblast, for the placenta is
formed on this side.
In later stages of gestation the amniotic cavity is greatly
enlarged, and the extra-embryonic coelom suppressed. The
remains of the yolk-sac is thus squeezed up against the umbilical
cord, and the whole invested by the amniotic epithelium (Fig.
139).
{The literature will be found at the end of the following chajAer.)
==CHAPTER IX THE PLACENTA==
The placenta is that organ in which the blood-vessels of the
embryo are brought into intimate anatomical and physiological
relation with the spaces-  which may be blood-vessels or lacunae
of quite a difierent character-  in which maternal blood is circulating. Though the apposition of foetal to maternal bloodchannels is very close, there is yet never any communication
between the two ; an injection passed into the maternal mil
not make its way into the foetal vessels, and conversely. At
the same time the tissues that separate the two sets of channels
are so thin that substances can readily travel by diffusion from
the one to the other. In this way the embryo obtains its oxygen
and probably food-stuffs, while by the same means it gets rid
of its carbon dioxide and possibly of other waste products of
its metaboHsm. The foetal blood is brought to the capillaries
of the placenta by the allantois, which carries umbiUcal arteries
and veins, while the maternal blood-supply is from the uterine
vessels. The embryonic tissue which comes immediately in contact with the uterine wall is the trophoblast-  the outer or
ectodermal layer of the false amnion or chorion, -  and it is the
trophoblast which ensures the adherence of the embryo to the
uterine waU and plays a part of conspicuous importance in
the edification of the placenta, particularly in placentas of the
so-called ' deciduate ' type.
In addition to the placenta -  this organ formed by the trophoblast and vascularized by the capillaries of the allantois -  the
embryo has frequently other means of obtaining nutrition. Thus
the trophoblast is often phagocytic-  in early stages, before the
allantois is developed, and in later stages in regions where it is not
adherent to the uterine wall, the debris of dead maternal tissues
and extravasated maternal corpuscles are devoured by it and
passed on to the embryo inside. Again, in several forms, the yolk-sac with its absorptive epithelium and area vasculosa is instrumental in securing additional nutriment for the foetus. These
processes we shall consider individually in the several groups.
Although it has been usual to separate the Eutheria as Placental
Mammals from the Marsupials or Metatheria, it must yet be
remembered that in the latter group there are arrangements by
which the trophoblast is able to secure nourishment for the
embryo from the walls of the uterus, which is handed on by
means of the area vasculosa of the yolk-sac, and that in one
case there is a true allantoic placenta, though it is of a peculiar
type, not met with anywhere else.
The Marsupials thus stand apart in this as well as in
other reproductive characters (the birth of the young in a very
undeveloped condition, the large size of the egg, the presence
of an egg-shell, the mode of segmentation, and the structure
of the blastocyst), and we shall accordingly consider them
separately.
The Marsupials
The yolk-sac, as we have seen, is large and its upper wall
invaginated by the embryo. On this upper wall is an area
vasculosa, which extends only a short way over the outer or
lower wall, the greater part of the latter being directly in contact
with the trophoblast.
In Didelphys the trophoblast opposite the area vasculosa of
the yolk-sac is a columnar epithelium, thrown into folds. These
folds fit into corresponding depressions m the uterine wall from
which they appear to absorb nutrient material, which is then
handed on to the vessels of the yolk-sac.
In Dasyurus the same region of the trophoblast is apphed
closely to the uterine wall, and there is also beyond the limits
of the area vasculosa a conspicuous annular zone of thickened
trophoblast (Fig. 122, c). Cell-boundaries disappear and the
syncytium so formed sends out pseudopodial processes which
attack the uterine epithelium, grow in and enclose portions of
it and the subjacent capillaries. The enclosed capillaries enlarge
and maternal blood passes in between the trophoblast and the
yolk-sac ; presumably it serves as food, for, as we shall see when we come to the Placentalia, maternal corpuscles are the source
from which the embryo obtains its necessary iron.
In Perameles there is an allantoic placenta (Fig. 140). Where
the trophoblast over the allantois touches the uterine wall the
epithelium of the latter thickens to form a syncytium, from
which processes grow down into the connective tissue ; the
syncytium is soon invaded by maternal capillaries. Meanwhile
the thin trophoblast has disappeared and the foetal capillaries
of the aUantois, passing into the irregular depressions on the outside of the syncytium, are brought into fairly intimate relation
with the maternal vessels.
Fig. 140.-  Section through the placenta of PeromeZes. (After Hill.) all.,
allantoic epitheUum ; m., mesoderm of allantois together with somatopleure
of false amnion ; f.h.v., foetal blood-vessel ; ep.s., syncytium of uterine
epithelium; m.6.u, maternal blood-vessels; c.«., subepithelial connective
tissue.
At birth the allantois and its blood-vessels are left behind
and absorbed by maternal leucocytes. This condition has
been termed ' contra-deciduate '. The same fate befalls the
syncytium.
The foetal tissues are similarly absorbed in Dasyurus.
==The Placentalia==
It has long been the custom to sharply distinguish two
principal types of placenta from one another as the Indeciduate
and Deciduate. In the former the connexion between foetal
and maternal tissues is so slight that at parturition the first easily separate from the second, no maternal tissue is lost or
'deciduous', and the placenta is ' indeciduate '. In the other
type, however, the union of foetal to maternal tissues was held
to be so fast that at birth a considerable quantity of the latter
was carried away by the former, and there was, in the language
of a terminology which was invented when the histology of
the placenta was not understood, a 'decidua'. This entirely
erroneous conception of the structure of certain types of placenta
(found, for example, in Rodents, Insectivora, and the human
being), was based on the structure of the placenta in Ungulates.
In the Ungulata, as was then well known, the * indeciduate '
placenta arises by the penetration of foetal (chorionic or trophoblastic) processes into crypts or depressions in the uterine wall,
from v/hich crypts the processes or villi are readily puUed out
at birth. Not unnaturally, in ignorance of the facts, it was
surmised that the ' deciduate ' placenta originated in similar
fashion, with the difference that the chorionic villi adhered so
closely to the crypt walls that at birth they dragged away not
only crypts but connective tissue and blood-vessels as well.
Thus the term ' decidua ' came to be applied to the tissue of the
uterine wall, whether an embryo and placenta were present or not.
Now while it is true that the placenta of the Carnivora is
developed in this kind of way, modern research has conclusively
shown that in the majority of the so-called ' Deciduates ' the
genesis of the placenta proceeds on an entirely different plan.
If, therefore, we retain the name ' deciduate ' for the placenta
of the Rodents, Insectivora, Cheiroptera, and some Primates
{Tarsim, Monkeys, and Man), it must be on the distinct understanding that the word bears its original meaning no longer.
The term ' indeciduate ' is not inapplicable to the Ungulate
placenta, and there is no objection to its use.
We shall begin with the Ungulate as exhibiting structurally
the simplest type.
==Ungulata==
In Ungulata the placenta is of the indeciduate form. At the
surface of the chorionic sac there are produced finger-shaped
processes or villi, formed of a single layer of trophoblast, and provided with a core of mesodermal tissue in whieh are the
foetal eapillaries. The endodermal epithelium of the allantois
is not continued into the villi. These villi fit into depressions
in the wall of the uterus known as crypts. The crypts are hned
by an epithelium which is perfectly continuous with the ordinary
epitheUum of the uterus and persists throughout gestation. The
persistence of the uterine epithelium is the real mark by which
the indeciduate is distinguished from other placentas. Below
the epithelium of the crypts are the maternal capillaries and
connective tissue. The villi do not adhere closely to the crypt
all.
Fig. 141. -  Diagram of a foetal and maternal cotyledon of the cow. all.,
allantoic epithelium ; ir., trophoblast ; v., villus ; e'p., uterine epithelium
continued into crypt ; c.w., wall of crypt. The maternal connective tissue
is shaded.
Avails, and at birth are easily removed without damage to the
maternal tissues.
The Ungulate Placenta may be Diffuse, or Cotyledonary, or
of an intermediate type. In the first the whole surface of the
chorionic sac is covered uniformly with villi which may be simple
(as in the pig) or branched (as in the horse) (Fig. 131). In the
cotyledonary placenta the villi are gathered together into bunches
or cotyledons, the intervening regions of the chorion being smooth
(Fig. 141). The villi -  which are much branched -  fit into crypts
of a corresponding shape, the whole aggregation of crypts for
the reception of the villi of a single cotyledon being termed
a maternal cotyledon. The points in the wall of the uterus where these maternal cotyledons will be formed are predetermined and recognizable as raised areas -  the cotyledonary
caruncles -  ^before gestation, can be seen indeed in the uterus
of the unborn calf. The foetal cotyledons are scattered all over
the surface of the chorion, except at its extreme ends, the
' diverticula allantoidis ' so called.
A cotyledonary placenta is characteristic of the Ruminants.
In some cases (Cervus, Giraffa, Oreas, Tetraceros) tho placenta
is of an intermediate type, simple villi being found between the
cotyledons.
As examples of indeciduate placentation we may take the
cow and sheep.
Before describing the anatomy and physiology of the actual
placenta it will be convenient first to consider the changes that
take place in the wall of the uterus preparatory to the reception
of the embryo, as well as the nutrition of the embryo while it
is still free in the uterine cavity.
In the period known as the ' pro-oestrus ', which precedes •
heat or 'oestrus', the subepithehal connective tissue of the uterus
becomes h5rpertrophied, while the capillaries increase in number
and become enlarged. Numbers of corpuscles -  ^both haematids
and leucocytes -  are now extra vasated from these swollen blood vessels into the surrounding stroma of connective tissue, where
many of the haematids are devoured and digested by leucocytes
with the resultant deposition of pigment in the cytoplasm of
the latter. This brown jjigment, derived from the haemoglobin
of the extravasated corpuscles, may remain in the wall of the
uterus for a considerable time. Meanwhile, as a result possibly
of the pressure exerted by the congested capillaries, the uterine
epithelium has given way ; patches of it degenerate and are
cast into the uterine lumen along with some debris of subepithelial cells, haematids, and leucocytes. The fluid in the uterus
already contains proteid, glycogen, and fat secreted by the
uterine epithelium and glands. In this fat-secretion the outer
ends of the cells, containing fat-globules, are nipped off and
ejected. There are also present (in the sheep) rod-like or needleshaped bodies, composed of an albuminous substance and secreted
by the epitheUum. Iron, too, is found, derived from the digested
haemoglobin of the extravasated haematids. To all this must
be added the products of the cellular secretion of the glands
(Fig 142) Small tracts of the epithelial wall become invagmated
into the gland-lumen, are cut off, degenerate, and are thrown
out by the mouths. The secretion of fat and proteid, of the
albuminous rod-shaped bodies and of cell-masses by the glands,
is not confined to the period of ' pro-oestrus ' but occurs
throughout gestation.
Fig. 142.-  Cellular secretion in the glands of the viterus. a, horse (after
Kolster) ; B, clog (after Bonnet). In A a piece of the epithelium is being
invaginated into the lumen of the gland. In B this has been nipped off. In
A the secretion of fat (black globules) and pieces of cells is also shown.
The material thus provided is of a thick, viscid consistency and
of a yellow colour, like pus, and is known as ' uterine milk ' . It is
of the greatest importance for the nutrition of the embryo.
Ovulation or the escape of the ovum from the Graafian foUicle
occurs in ' oestrus ' : the ovum passes into the Fallopian tube,
where fertihzation takes place. Development begins and the
blastocyst enters the uterus. Here the trophoblast at once
begins to absorb the nutriment prepared for it. The cells are
phagocytic and ingest solid particles of the uterine milk : they
also absorb fat and possibly iron.
The blastocyst next becomes attached by its trophoblast to
the uterine wall, and the placenta is formed.
The uterine epithelium, where destroyed, has now been
restored. In the cotyledonary caruncles it is continued into the
crypts, which are now developed. If we may judge of what
happens now by what is known of the manner in which accessory
maternal cotyledons are formed in the later stages (in the cow), the
crypts 'arise (Fig. 143) by a pitting of the columnar cihated
epitheUum, the cells which are at the bottom of the pits becoming
shorter than the ordinary columnar cells around {a), followed
by the outfolding of the epithelium between the pits (6) ; into
these folds connective tissue soon penetrates (c), and later blood vessels.
Villi or finger-shaped processes of the trophoblast are now
formed and enter the crypts. The epithelium lining the latter
soon becomes modified, the cilia are lost, and the cells become
cubical (d, e) (in the cow) or very flat (in the sheep). Even in
the latter case, however, small patches of cubical cells remain,
from which fresh crypts are formed by downgrowth into the
subepithelial tissue (Fig. 144).
Fig 143. -  a-e. Five stages in the formation of a crypt in tlie cow.
a-c, pitting and folding of the epithelium; cl, the epithelium becomes
cubical ; e, the cilia are lost.
Fig. 144. -  Formation of accospory crypts in tlto sheep. In a and & the
(lowngrowth of epithchuni i.s still solid ; in c it i« becoming hollow ; in e it
is open to the old crypt.
With continued development the villi and crypts elongate and
branch repeatedly, and the maternal cotyledon is raised above
the level of the uterine wall (Fig. 141). The free surface is
convex in the cow, but deeply concave in the sheep, where also
the base of attachment is constricted to a narrow stalk.
In the cow the trophoblast covering the villi is composed of
rounded or cubical elements, amongst which are gland-cells and
curious oval binucleate cells (found also in the sheep). The core
of each villus is occupied by connective tissue (somatopleure of
the false amnion plus splanchnopleure of the allantois) and foetal
capillaries, the latter very close to the epithehal cells (Fig. 145, 1).
The crypt is lined by cubical cells which secrete fat and proteid,
the ends of the cells with the contained fat-globules being protruded, pinched off, and thrown into the space between crypt
and villus. Fat can be demonstrated in the trophoblast, which
doubtless absorbs the proteid also. The gland-cells may be of
importance in this respect.
Below the epithelium in the crypt-walls are maternal connective tissue and maternal capillaries. The foetal and parental
blood-streams are thus separated by the endothelium of the
foetal capillaries, some connective tissue (not always), the trophoblast, the epithelium of the crypts, the cormective tissue, and
the endothelium of the maternal vessels. Through these layers
oxygen diffuses from maternal to foetal blood, and carbon
dioxide in the reverse direction ; other substances may also
pass. In the cotyledons, therefore, the respiratory exchange
takes place and the absorption of fat and proteid.
It is, however, not merely by means of its cotyledonary villi
that the embryo obtains nutrition. At the bases of the villi
and therefore opposite the summits of the walls between the
crypts the trophoblast is very tall and columnar (Fig. 145, 2).
The outer ends of the cells are pseudopodial and ingest quantities
of cell-debris and maternal red blood-corpuscles. The capillaries
at the summits of the crypt-walls are gorged, blood is extravasated, and together with the remains of epithehal and subepitheUal cells eagerly devoured by the trophoblast, and digested.
The ingested haematids get clumped together in the cells, and
often surrounded by a food-vacuole (Fig. 145, 3). As intra
Fig. 145. -  Histology of the placenta in the cow and sheep.
1, Foetal and maternal tissues in a cotyledon, tr., trophoblast of a
villus ; the cells are absorbing fat (black). In the trophoblast are two
binucleate cells. Behind the trophoblast are the connective tissue and
Tilood-vessels of the allantois. ep., uterine epithelium lining a crypt.
Fat secretion is going on, the ends of the cells with fat-globules being
pinched off and thrown into the lumen of the crypt. Below the epithelium
are the maternal capillaries and connective tissue.
2, Columnar trophoblast cells from between the bases of the cotyledonary
villi. The cells are full of ingested matter (corpuscles, nuclear, and cell
debris).
3, Ingestion of extravasated maternal corpuscles by the trophoblast in
the sheep. The corpuscles are seen inside the cells. The cells also contain
pigment.
4, Deposition of pigment after digestion of the haemoglobin of ingested
corpuscles in trophoblast cells of the cow. The pigment-granules (black)
are seen to be deposited on irregular masses in the cells. cellular digestion proceeds little granules of yellow-brown pigment appear on the surface of the mass, and gradually the whole
assumes the same coloiar (Fig. 145, 4). The pigment probably
contains no iron, at least when digestion is completed, the iron
of the haemoglobin having been separated and carried o£E to
the embryo by the blood of the allantois. Thus the foetus
obtains its necessary iron in this as in earlier stages from the
haemoglobin of extravasated maternal corpuscles, devoured by
the trophoblast. The pigment remains in the trophoblast, where
large quantities of it are accumulated by the end of gestation.
In neutral solution it shows two bands very, nearly in the
position of those of oxyhaemoglobin, in acid solution two bands
almost exactly in the position of those of acid haematoporphyrin,
but in alkaline solution not the four bands of alkaline haematoporphyrin, but only the two seen in the neutral solution. It is
probably related to haematoporphyrin : it is certainly a haemoglobin derivative, and from it bile-pigments may be formed.
We have already had occasion to notice the curious roimded
or elongated, often flattened bodies, sometimes soft, sometimes
hard and brittle, found floating in the allantoic fluid and familiar
for many centuries under the title of ' hippomanes '.
In the cow they are white or pale yellow, in the sheep a dirty
brown. In the sheep they are formed by local accumulations
of the viscid uterine milk, which get into pockets of the trophoblast, between the cotyledons. Gradually, pushing the trophoblast and allantois in front of them, they make their way into
the cavity of the latter, in which they lie attached by a stalk
to the wall ; the stalk narrows and breaks, and they are free
in the cavity. At first they are surrounded by a membrane - 
the remains of their covering of allantois and trophoblast -  and
are soft : they are composed of a granular coagulable material,
full of cell-detritus, degenerating nuclei, globules of fat and
glycogen, and leucocytes. Later the membrane disappears, and
the bodies become hard by being saturated with calcium oxalate
in the form of ' envelope ' crystals. In the cow, when outside
the chorion and still soft, they are a bright orange colour, due
to the presence of bilirubin, doubtless derived from the extravasated corpuscles eaten by the trophoblast ; they are, indeed, found at the bases of the villi, just where these extravasations
occur.
Large allantoic bodies impregnated with calcium oxalate are
found in the horse.
Small quantities of glycogen are found in the uterine epithehura and subepithelial tissues, and in the uterine milk. Much
larger quantities are found stored up in the amniotic thickenings
-  ^masses of stratified epithelium on the inner surface of the
amnion. Towards the end of gestation the glycogen diminishes,
and the cells undergo fatty degeneration and are impregnated
with calcium oxalate. As the glycogen diminishes the dextrose
in the amniotic fluid increases (from 1 % to 0-37 %).
Glycogen also occurs in the trophoblast, in the connective
tissue of the chorion and in the umbilical cord round the
blood-vessels and allantoic epithelium. In the body of the
embryo it is abundant in all tissues, except in the liver, where
it only appears late, when it is disappearing from the others.
The glycogen in the amniotic bodies appears to be a reserve
store. We shall find a similar storage of glycogen in other cases.
Besides dextrose the amniotic fluid contains albumin, mucus,
and chlorides of sodium and potassium.
In the allantoic fluid are dextrose (0-3 %), albumin, mucin,
magnesium, sodium, and calcium phosphates, sodium chloride
and sulphate, and ' envelope ' crystals of calcium oxalate ;
further, a yellow pigment, and allantoin, the embryonic representation of urea.
It appears, therefore, that the allantois is a receptacle for the
waste products of foetal metabohsm.
Cetacea. In Orca the placenta appears to be indeciduate and
diffuse, uniformly studded with villi. The chorionic sac extends
into both cornua of the uterus. The villi, which are branched,
are only absent at the ends, opposite the Fallopian tubes, and
again opposite the os uteri,
Sirenia. Halicore possesses an indeciduate, diffuse placenta.
It is known that the uterine epithelium persists in the crypts.
The villi, which are slightly branched, are Umited to an annular
area surrounding the chorionic sac, not qmte in the middle of
the latter. When the region of the trophoblast, which enters into such intimate relations with the uterus as to form a placenta,
is of this annular shape, the placenta is spoken of as zonary.
(A zonary placenta may be of the deciduate type.)
Hippomanes are found in Hcdicore, but there are no amniotic
bodies.
Proboscidea. In the elephant the shape of the placenta is
zonary, though diffuse villi occur at the ends of the chorionic sac.
These villi appear to be of the nature of those found in Ungulates.
In the zonary region the villi appear to have become embedded
in the wall of the uterus by their ends, while maternal blood is
extravasated between their bases. In the absence of more exact
information this placenta cannot be properly classified. Brown
pigment abounds in the trophoblast of the villi, presumably
a haemoglobin derivative.
Hyracoidea. In Hyrax the placenta is zonary in shape, with
villous patches at the poles.
Edentata
The placenta is stated to be bell-shaped in Myrmecophaga and
Tatnandua, zonary in Orycteropus, oval in Dasypus, diffuse in
Manis and Choloepus, but we have no knowledge of its minute
structure.
Lemuroidea
In this, the lower division of the Primates, the placenta is of
the diffuse indeciduate tjrpe (except in Tarsius, which must
certainly be placed with Monkeys and Man).
In Galago (Fig. 146) the chorionic sac is large and occupies
both horns of the uterus. It is covered with short simple villi
at the extremity of each of which is a sUght pit, the cells of which
contain granular greenish masses (? haemoglobin derivatives).
The villi lie in grooves lined by a persistent epithelium, from
which they are easily pulled out. The chorionic vesicles are
invaginations of the trophoblast opposite depressions in the
uterine wall at the bottom of which glands open. Both chorionic
vesicles and depressions are filled with a granular material - 
uterine milk -  which appears to be absorbed by the villi which
spring from the floor of the vesicle.
Fig. 146. -  Placenta of the lemur Galago. (After Strahl.)
A, Section of a villus with the crypt in which it is lodged. The uteruie
epithelium (ep.) lining the crypt persists ; m.h.v., maternal blood-vessel ;
all, allantois epithelium ; f.b.v., foetal blood-vessel ; tr., trophoblast.
B, Section through a chorionic vesicle and the opposed depression of the
uterine wall ; tr., trophoblast ; v., small branching vilh protruding into the
chorionic vesicle ; gl., glands opening into the uterine depression ; m.h.v.,
maternal blood-vessels.
In the Carnivora we meet with a group which is from the
comparative anatomical point of view of the greatest importance,
since the placenta here holds an intermediate position between
the Indeciduate and Deciduate (so-called) types. While in the
disappearance of the uterine epithelium it must be ranked with
the latter, it differs widely from them in the fact that the
channels in which the blood of the mother circulates are the
capillaries of the uterine wall, between which the trophoblast
has penetrated after the destruction of the superficial epithelium.
In this mutual apposition of foetal vessels and maternal vessels
the Carnivorous does indeed resemble the Ungulate type, from
which it may conceivably have been derived, and comes very
near to fulfilling the original definition of a ' deciduate ' placenta,
since at birth the maternal vessels and connective tissue are
removed along with the foetal constituents. The shape of the
placenta is always zonary. The genera most carefully investigated
are the dog and cat.
We begin with a description of the processes preparatory to
the reception of the embryo.
In the period of pro-oestrus prior to ' heat ' the uterus becomes
swollen and hjrperaemic owing to the multiplication and enlargement of the blood-vessels and capillaries. Blood is extravasated
first into the subepithelial tissue, and masses of brown pigment
appear, as the result, presumably, of the digestion of the haemoglobin by the abundant leucocytes. Soon the superficial columnar
epithelium gives way, and quantities of haematids with a certain
amount of destroyed epithelial and connective tissue are
discharged into the lumen of the uterus.
The uterine glands are long and twisted, and branch ; they
apparently secrete some proteid material and masses of cells
in the way already described in the Ungulata (Fig. 142). In
addition there are the crypts, short tubular downgrowths of the
epitheUum.
During the following period of oestrus a regeneration of the
destroyed epithelium takes place. Should fertilization have
occurred the blastocyst is developed and makes its way into the uterus, in the placental regions of which the following changes
now occur.
While the blastocyst is still unattached fat appears in the superficial epithelium of the uterus, and in that of the necks of the glands
and crypts. The necks of the glands widen, so giving rise to the
' spongy ' layer. A thick layer of dense subepithelial tissue is
formed, in which run the capillaries. The surface epithelium next
becomes lower, while its nuclei begin to degenerate, and eventually
the whole epithelium disappears. The openings of the crypts and
glands are closed by masses of enlarged epithelial cells which, uniting to form syncytia, soon show signs of degeneration (Fig. 147, a).
Attachment now occurs. In the zonary placental region the
trophoblast is produced into finger-shaped villi -  which may be
solid or provided with a core of mesoderm -  and these villi make
their way into the connective tissue from which the epithelium
has now been removed, as well as into the plugs of degenerating
syncytia closing the mouths of the crypts and glands. To
these syncytia are added the cellular secretions of the glands.
The cells of the trophoblast are phagocytic and devour all this
detritus. Where the trophoblast invades the connective tissue
between the crypts and gland it comes into intimate relation
with the capillaries there, and as soon as the villi have been
penetrated by the foetal blood-vessels the placenta may be
said to have been established (Fig. 147, b).
•Below the placenta are the wide parts of the glands, separated
only by thin lamellae of connective tissue in which run the larger
blood-vessels. By these lamellae the placenta is attached to the
muscularis.
The placenta so formed is at first thin, but soon grows in
thickness by the simultaneous elongation of the trophoblastic
villi and of the connective tissue which covers them and includes
the maternal capillaries (Fig. 147, c). The villi meanwhile branch,
the branches being thin sheets (perpendicular to the surface)
and radiating out from the original villi : the foetal blood vessels of course branch correspondingly, as do, on the other
side, the maternal connective tissue and capillaries. In the cat
certain large cells are present in between the maternal capillaries
which are possibly hypertrophied connective tissue-cells, but they may be trophoblastic (Fig. 148). The trophoblast at the
base of the placenta continues to ingest and absorb the celldebris and fat supplied by the glands up to the end of gestation.
A feature of great physiological interest is the ' green border
a system of pockets in the trophoblast along both edges of the
placenta filled with masses of extravasated maternal blood, to
which extravasation indeed the formation of the pockets is due
(Pig. 147, d). Leucocytes are present, fibrin, and a green pigment (haematochlorine), a derivative of haemoglobin ; what its
relation is to biliverdin is not known. There is also a yellow brown pigment, and, at the end of gestation, a black one. All
this material is ingested by the trophoblast. The green border
is poorly developed in the cat.
It will be evident that the placenta we have just considered
is made of a compound tissue, foetal in the trophoblast and
connective tissue and capillaries of the allantois, maternal in the
connective tissue and capillaries surrounded and engulfed by the
invading vilH.
The placentas we have still to study are not constructed on
this plan, for though they have this much in common with that
of the Carnivora, that the uterine epithelium disappears, yet they
differ wholly from it in that the maternal blood circidates not
in blood-vessels enclosed by the trophoblast but in lacunae, excavated in that tissue, into which extravasated maternal blood
is poured. No maternal tissue, therefore, is lost at birth except
the blood, apart from fragments of connective tissue adherent
to the maternal side of the placenta.
A placenta of this kind is found in the Rodents, Insectivora,
Cheiroptera, and, amongst the Primates, in Tarsius, Monkeys,
and Man. We shall begin with the Rodents.
==RODENTIA==
The placenta is always discoidal in shape, and attached to
the mesometric side of the uterus.
As an example we may take the mouse. The uterine cavity
is bounded by a columnar eiVitheUum in which fat is secreted.
Into it open glands with long necks. These secrete a coagulable,
presumably proteid, material. These secretions are absorbed by the free blastocyst (Figs. 149, A ; 150, a). There is prepared
for the reception of the blastocyst a pit on the antiinesonietric
side of the uterus. This pit lies in the middle of a pronounced
swelling, due to the hyi)ertroj)hy of the subepithelial connective
tissue and enlargement and multiplication of the blood-vessels.
To this tissue may be applied Hubrecht's term ' trophospongia '.
By it the glands are driven away towards the muscularis, their
necks stretched and eventually broken. The mouse produces
a large litter of young, and there is a correspondingly large series
of these swellings along the uterus. The pit in the middle of
each swelling is open freely to the main cavity of the uterus
(towards the mesometrium), and in each pit a blastocyst is lodged
with its embryonic pole towards the opening of the pit. It is at
this pole that the trophoblast will thicken to form the placenta,
which is therefore on the mesometric side (Figs. 149, b ; 150, b).
Fig. 148. -  Histology of the placenta of the cat. a, Earlier ; b, later
stage (full time), f.c.t., foetal connection tissue ; tr., trophoblast (pale) ;
m.c.t., maternal connective tissue (dark) ; f.h.v., foetal capillary ; m.b.v.,
maternal capillary.
Where the trophoblast touches the sides of the pit the epithelium, clothing the latter, now disappears, the cells becoming
cubical, then flat, and finally vanishing. The nuclei are resolved
into spherules of chromatin, the cytoplasm undergoes fatty
degeneration. The fat is absorbed by the trophoblast. The
trophoblast is thus brought into immediate contact with the
subepithelial tissues.
The same degradation later attacks the epithelium at the
bottom of the pit, and later still extends to that hning the
main uterine lumen above it. This lumen then disappears and
each embryonic pit is isolated, as also are the inter-embryonic
regions of the viterus. At a subsequent stage a fresh lumen will
be formed on the anti-mesometric side of the embryo, and this
re-unites the inter-embryonic regions with one another and once
more there is a continuous uterine lumen.
At the embryonic pole the trophoblast now thickens and
drives the embryonic knob towards the opposite end, so mvagmating the upper wall of the yolk-sac ; the amnion is then developed
and separated from the temporary cavity in the trophoblast as
the extra-embryonic coelom extends between the two in the
fashion already described.
This thickening is the precursor of the placenta. It extends
towards the mesometrium and is at first conical (Figs. 149, c ; 150, c), but soon becomes discoidal as the embryo in its amnion
and extra-embryonic coelom enlarge. It is in contact with the
distended uterine capillaries, and very quickly these burst and
the extra vasated maternal blood is poured into irregular spaces
or lacunae excavated in the trophoblast. Many of the haematids
are phagocytically devoured by the trophoblast (Fig. 151, 8).
The blood enters these spaces in the centre, leaves them by
a number of wide vessels at the periphery. At its base this trophoblast remains cellular, but elsewhere it becomes syncytial by the
disappearance of cell-boundaries ; the two regions have been
termed respectively cyto- and plasmodi-trophoblast. Between
the blood-vessels that supply these trophoblastic lacunae is
the subepithehal connective tissue (Fig. 151, 7), and this soon
undergoes an important modification. While some of the cells
remain unaltered -  ^fusiform or stellate in shape -  as a supporting
tissue, others become rounded and filled with globules of
glycogen. The cells, though fairly closely packed, are distinct
from one another. The nucleus is spherical, not very chromatic,
and has one nucleolus. We shall speak of this tissue as the
maternal glycogenic tissue (Fig. 151, 4). It is at about the zenith
of its development by the time the foetal blood-vessels reach
the placenta.
The future placental region of the trophoblast may be distinguished as ' allantoidean ' from the ' omphaloidean ' region,
which lies immediately against the distal wall of the yolk-sac
and therefore on the anti-mesometric side. The cells here become
enormously hypertrophied and theix nuclei correspondingly
enlarged (hence the term ' megalokaryocytes ') : in the nuclei
there are large nucleoli, and the chromatin is in irregular strings.
They are incapable of mitosis. In contact with the subepithehal
tissues they eagerly devour debris of degenerate cells, leucocytes
and the haematids, which are abundantly extravasated in this
region also (Fig. 151, 6, 9). They apparently play an important
role in the nutrition of the embryo during this stage, prior to the
development of the allantois, but later they are less important
and disappear long before the end of gestation. Presumably
the stuffs they have digested are passed on by means of the area
vasculosa of the yolk-sac to the embryo.
V)
Fig. 151. -  Histology of the placenta of the mouse.
1, Foetal capillaries (with nucleated corpuscles) lying alongside the
lacunae of the trophoblast (stage e).
2, 3, Early and late stages of glycogenesis of the trophoblast (stages E and
later).
4, Maternal glycogenic cells with intervening connective tissue-cells
(stage d).
5, Fold of epithelium on the proximal wall of the yolk-sac with bloodvessel (stage E).
6, Megalokaryocyte from the omphaloidean trophoblast. On the right
extravasated maternal corpuscles, on the left the flat epithelium of the
distal wall of the yolk-sac (stage d).
7, Closely packed maternal sub-epithelial tissue with blood-vessels
(stage c).
8, Allantoidean trophoblast, the cells ingesting maternal corpuscles
(stage c).
9, Melagokaryocyte cf the omphaloidean trophoblast ingesting corpuscles
and detritus of maternal cells (stage c).
P. 230
1
jX THE PLACENTA 237
In the next stage (Figs. 149, d ; 150, d) the allantois is developed, grows with its blood-vessels across the coelom, reaches
the so'matopleure at the base of the allantoidean trophoblast, and
sends its capillaries into the latter in between the lacunae. The
necessary relation between the foetal and maternal circulations
which constitutes a placenta is now established. Further change
is mainly one of growth.
Firmly fixed in the trophoblast the capillaries soon elongate
and branch, mostly parallel to one another and perpendicular
to the surface of the placenta. The trophoblast with its lacunae
keeps pace, and so the whole organ, attaining a thickness many
times greater than that which it originally possessed, comes
ultimately to project button-like towards the centre of the
uterus (Figs. 149, e ; 150, b). The trophoblast lining the lacunae
becomes finally much attenuated except for the protrusions due
to the rather large nuclei (Fig. 151, 1).
On the foetal side of the placenta are somewhat large lacunae
to which blood is brought by chaimels passing directly through
the centre of the placenta ; hence it passes into the smaller
lacunae round the foetal capillaries and so into the efferent
maternal vessels which leate the organ peripherally. The
capillaries of the allantois, however, never penetrate the whole
thickness of the trophoblast. On the maternal side there is
a layer, increasingly broad, between the ends of the foetal vessels
and the maternal tissues, a layer only traversed by the large
channels which lead to and from the smaller lacunae (Fig. 150, e).
In this layer the secretion of glycogen begins at the stage when
the allantois has just reached the trophoblast, and soon attains
enormous dimensions (Fig. 151, 2, 3). The whole tissue consequently appears highly vacuolated. The cells -  ^if we may
indeed speak of cell-boundaries -  are oblong, the nuclei oval,
rich in chromatin and provided with several nucleoli, thus
differing from the maternal glycogen cells. We shall speak of
this as the trophoblastic glycogenic tissue.
The previously differentiated maternal glycogenic tissue ceases
to grow further, mth the enlargement of the whole uterus the
constituent cells get separated, the glycogen cells having given
up their glycogen collapse, disintegrate, and disappear, and only
238
THE PLACENTA
IX
the supporting cells are left between the maternal blood-vessels.
Upon the space so left vacant the trophoblastic glycogen tissue
encroaches, engulfing the blood-vessels as it does so, and finally
extends as far as the muscularis.
There can be no doubt that this tissue holds in reserve a store
of food material for the use of the embryo . As sugar the glycogen
passes into the maternal vessels and into the lacunae, and so is
absorbed by the foetal capillaries. When the glycogen is used
up the cells collapse, and their collapse may be a factor in
determining the moment of parturition, since it is across this
layer that the placenta breaks away. The trophoblastic is much
more voluminous than the maternal glycogenic tissue ever was.
In the omphaloidean regions important changes have meanwhile occurred. A new lumen has been formed on the antimesometric side, placing the inter -placental portions of the
uterus once more in communication with one another. This
new lumen (Fig. 149, d, e, I'.u') is separated from the cavity of
the yolk-sac by (1) the distal wall of the yolk-sac, (2) the omphaloidean trophoblast, (3) the subepithelial tissues, and (4) the
epithelium. All these layers cease to grow, become passively
stretched, and finally rupture, disintegrate, and disappear.
The 5^olk-sac now opens freely into the uterine lumen, and the
richly folded columnar epithelium (Fig. 151, 5) of the upper wall
is able to absorb the fat and proteid material secreted by the
uterine epithelium and glands. Thus the yolk-sac acts and
continues to act till the end of gestation as an accessory organ of
nutrition. It also forms a protective envelope, since its edge
is inserted into the margin of the placenta. This edge is
l^ter carried up some little way on the outer surface of the
placenta, the base of attachment of the latter to the uterine
wall being narrowed, while at the same time the yolk-sac
is inflected on the foetal side towards the insertion of the
umbilical cord.
In a placenta of this type the foetal is only separated from
the maternal blood by the endothelium of the capillaries and the
trophoblastic lining of the lacunae, the foetal connective tissue
being in the last stages negligible. There is no penetration of
foetal tissues into maternal (except for the encroachment of
jX THE PLACENTA 239
the glycogenic tissue of the trophoblast on the space between the
maternal blood-vessels), and there is no maternal tissue in the
organ but the blood in the lacunae (except again the blood vessels in the glycogenic region). The relation between maternal
and foetal blood-streams is brought about by the fastening of
the trophoblast upon the subepithelial tissues after the destruction of the uterine epithelium ; once fixed there lacunae are
excavated in it in which extravasated maternal blood circulates,
and it is finally vascularized from the foetal side by the capillaries
of the allantois.
In the guinea-pig {Cavia) the blastocyst is placed in a pit on
the anti-mesometric side ; it comes into contact with the subepitheUal tissues by burrowing beneath the epithelium, which
is then destroyed. The original lumen of the uterus is obliterated
in the embryonic swellings ; a new lumen is formed anti-mesometrically, and the tissues between it and the upper wall of
the yolk-sac are distended and disintegrate, thereby placing the
yolk-sac in contmuity with the uterine cavity, precisely in the
way akeady described for the mouse, except that the lower wall
of the yolk-sac has never been present. The placenta is discoidal
and mesometricaUy placed ; it is developed from a thickening
of trophoblast at the embryonic pole of the blastocyst. On its
maternal side is an abundant glycogenic tissue, but whether
this is of maternal or foetal origin, or both, has not been
determined.
In the rabbit and squirrel no anti-mesometric pit is formed
for the reception of the blastocyst. In the rabbit there are
on the mesometric side two prominent folds, the placental folds,
and in the future embryonic regions these become greatly
thickened by the proliferation of the subepitheUal tissue and
blood-vessels (trophospongia). They have been termed 'cotyledons ', but the expression is here inapplicable. To these two
swellings the blastocyst attaches itself by the trophoblast behind
and at the sides of the embryonic plate ; the latter is at the
surface when Rauber's cells have disappeared, but sinks inside
when the amnion closes (Fig. 152).
The uterine epithelium, where touched by the trophoblast
now disappears, and the latter is brought into immediate contact
240
THE PLACENTA
IX
with the subepithelial tissue and blood-vessels. The blood vessels are to a very slight extent engulfed by the growing
trophoblast, but their endothelial walls soon break down and
their extravasated blood is discharged into lacunae excavated
in the trophoblast, now much thickened and syncytial (plasmodi
FiG. 162. -  Foetal membranes and placenta of the rabbit, pr.am., proamnion. Other letters as before. (Aiter Duval and Van Beneden.)
trophoblast), except at its base, where cell-bomidaries remain
(cyto-trophoblast). The allantoic capillaries then make their
way into the trophoblast and the placenta is established.
The trophoblast with its lacunae and the foetal tissues grow
pari passu ; the placenta thus increases in thickness and projects
IX
THE PLACENTA
241
into the uterine cavity. In shape it is discoidal, but made up
of two distinct halves or lobes, due to the attachment of the
trophoblast to the two enlarged placental folds.
There is a voluminous glycogenic tissue on the maternal side,
stated to be entirely of maternal origin. A good deal of it is,
however, probably trophoblastic. It has been shown that the
glycogen of the placenta increases up to the twenty-first day of
gestation, but then diminishes till the end (twenty-ninth day).
The glycogen in the foetal liver, which is at first almost negligible,
increases rapidly during the last week of pregnancy. A glycogen
splitting ferment has also been isolated from the placenta ; it
is found, too, though less active, in the overlying maternal
tissues. In the placenta, therefore, the embryo has a means of
controlUng the glycogen metabolism ; but this function is taken
on by the foetal liver towards the close of gestation. The yolksac in these forms also is an accessory organ of nutrition. The
lower wall disappears, the cells of the upper wall then absorb
material from the uterine cavity, and pass it on to the embryo
by means of the area vasculosa.
Cheiroptera
In Vespertilio there is a discoidal placenta, or rather, since it
is concave, saucer-shaped or bell-shaped (Fig. 153).
The blastocyst attaches itself by its embryonic pole to the
anti-mesometric side of the right cornu of the uterus : only one
is present at a time.
Below the epithelium the connective tissue has thickened, and
the blood-vessels have increased in number and size. The uterine
epithehum disappears, and the trophoblast then fixes itself by
invading the subepithelial tissue and engulfing some of the
superficial capUlaries. The endothelium of these capillaries then
degenerates, and they are indistinguishable from the lacunae
formed in the way with which we have become familiar in the
Rodent placenta.
The blood-vessels of the yolk-sac are at first applied to this
mass of trophoblast, but as soon as the allantois is developed
it pushes the yolk-sac away and sends its capillaries into the
trophoblast. The placenta increases in thickness by the simul
Q
242 THE PLACENTA IX
taneous growth of capillaries and lacunar troplioblast, and in
area by an extension at the edges of the same process by which
it was formed. After the first fixation there is no further penetration of the maternal by the foetal tissues.
Fig. 153.-  Foetal membranes and placenta of the bat (V espertilio).
(After Nolf.) Letters as before.
On the anti-embryonic side (mesometric) the uterme epithehum
also disappears, the fatty debris, together with that of the
underlying connective tissue, being eaten up by the trophoblast.
In Pteropus the placenta is discoidal but mesometric : the
uterine epithehum seems to disappear.
IX
THE PLACENTA
243
Insectivora
In this order the placenta is again discoidal, and usually
concave ; but in Tupaia there are two placentas, one right,
the other left, at the sides of the uterus, and in Cenietes a large
niimber. Where there is only one {Erinacells, Sorex, Taljia) it
is anti-mesometric in position.
In all cases the uterine epithelium disappears in that region
where the placenta is formed : the thickened trophoblast fastens
on the subepithelial tissues, and lacunae are formed in it ; in
Fig. 154. -  Two stages in the formation of the decidua reflexa of the
hedgehog. (After Hubrecht.) d.r., decidua reflexa. Letters as before.
these the maternal blood circulates. The whole is then vascularized from the foetal side by the allantoic capillaries.
In Erinacells, the hedgehog, the most interesting feature is
the formation of a ' decidua reflexa ' or ' capsularis ' resembling
the structure known by that name in human embryology. ^
On the anti-mesometric side of the uterus there are formed two
thick folds by the proliferation of the subepithelial vascular
tissue (trophospongia). Between these two folds the blastocyst
is lodged with its embryonic pole turned away from the mesometrium (Eig. 154, a). By the closure of the lips of the folds
1 It is highly probable, however, that the human ' reflexa ' is formed
in a different manner. (See below.)
Q 2
244
THE PLACENTA
IX
and obliteration of the cavity in front and behind this point
the blastocyst is securely shut up in a coat of maternal tissue,
the ' decidua reflexa ' (Fig. 154, b). The whole of the trophoblast
now thickens enormously, becomes syncytial, destroys and
devours the epithelium lining the cavity which lodges it, while
into the lacunae hollowed out in it quantities of maternal blood
are soon discharged from the adjacent swollen capillaries. The
-am.c.
Fig. 155. -  Foetal membranes and placenta of the hedgehog. (After
Hubrecht.) l.u., lumen uteri ; d.r., decidua reflexa. Other letters as before.
yolk-sac and omphaloidean trophoblast, against which its lower
wall lies, are at the anti-embryonic end, that is, towards the
covering ' decidua reflexa ', while towards the opposite end the
allantois grows out and reaches the ' allantoidean ' trophoblast.
It is from this part that the placenta is formed (Fig. 155), the
foetal capiUaries being driven into the trophoblast between the
lacunae. The whole grows in thickness.
The ' deciduofracts ' are phagocytic trophoblastic cells which
eat up the maternal tissues adjoining the placenta.
In the omphaloidean region relations are at first established
IX
THE PLACENTA
245
between the yolk-sac and the trophoblast with its lacunae. But
as the allantoic placenta becomes increasingly functional the
yolk-sac dwindles in importance and is folded up under the
' decidua reflexa '. By the extension of the uterine cavity round
Fig. 156. -  Foetal membranes and placenta of the shrew {Sorex). (After
Hubrecht.) x, point where the omphaloidean trophoblast is in contact
with the maternal tissues ; tr.an., trophoblastic annvdus, or thickening of
trophoblast below x.
the base of the placenta the ' reflexa ' is enlarged, and surrounds
the embryo on all sides except at the placenta. It becomes
stretched, and the trophoblast beneath it much attenuated.
In the toole {Talpa) the uterine epitheUum is also destroyed
on the mesometric (non-placental) side ; the trophoblast comes
into immediate contact with the subepithelial tissues. At birth
246
THE PLACENTA
IX
the allantoic capillaries are pulled out of the placental trophoblast, which remains behind to be absorbed by the leucocytes of
the mother. This arrangement is known as ' contra-deciduate '.
In Sorex (Fig. 156) there is, prior to the attachment of the
trophoblast in the placental region, a conspicuous proliferation
of the uterine epithelium with concomitant development of crypts
between the glands on the anti-mesometric side. Into these the
syncytial trophoblast makes its way, and then the epithelium is
destroyed. The further stages in the development of the placenta
are similar to those occurring in other forms.
Laterally there are also independent proliferations of the
uterine epithelium to which the trophoblast becomes attached.
The fused maternal and foetal tissues afterwards degenerate
together and are dehisced from the wall ; the continuity of the
uterine lumen is then restored. The area vasculosa of the yolksac which had been applied to this region is at the same time
detached. Further towards the anti-embryonic polp there is an
annular thickening of the trophoblast. The cells are here phagocytic and ingest quantities of extra vasated maternal haematids.
Digestion of these presumably takes place in the trophoblast,
since a bright-green pigment (? haemoglobin derivative) fills the
yolk-sac. The iron would then be carried o£E by the blood vessels of the area vasculosa. At the anti-embryonic pole the
trophoblast is thin and not attached to the uterus ; here the
epithelium persists.
In Tupaia the yolk-sac, which has at first relations with the
placental regions of the trophoblast, is later displaced by the
allantois.
Tarsiits, Monkeys, and Man
As we have already had occasion to see, the aberrant Lemur
Tarsius agrees with Monkeys and the human being in the possession of a diminutive yolk-sac (provided, nevertheless, with an area
vasculosa), a large and precociously developed extra-embryonic
coelom, and a rudimentary allantois which only extends far
enough outside the body of the embryo to penetrate the base
of the ventral or body-stalk, which connects the embryo in its
amnion and with its yolk-sac to the wall of the blastocyst and
IX
THE PLACENTA
247
is to be developed into the umbilical cord. Such an arrangement
of the foetal membranes is found nowhere else amongst the
Mammalia. We have now to inquire whether in the origin and
minute structure of the placenta there is an equally complete
agreement.
Fig. 157. -  Foetal membranes and placenta of Tarsius. (After Hubrecht.)
Letters as above.
In Tarsius alone is the complete history of the placenta kno^vn,
and there is no doubt whatever here at any rate that the placenta
is of that type which prevails in Rodents, Insectivores, and
Cheiroptera. In form it is discoidal, or rather button-shaped,
protruding into the uterine cavity ; it is developed at the antiembryonic pole of the blastocyst, and is placed on the mesometric side of the uterus (Fig. 157). Here there is, prior to
fixation, a ' trophospongia ' or area of proliferating connective
248
THE PLACENTA
IX
tissue and enlarged blood-vessels, and with this the placental
trophoblast comes in contact as soon as, under its influence, the
epithelium has been destroyed. Firmly fixed here, the tropho
blast becomes hollowed out by lacunae, in which maternal blood
circulates and is invaded from the other side by the foetal
capillaries. The whole then grows into the lumen of the uterus
until the complete thickness of the placenta is attained. An
interesting feature is the conversion of much of the trophoblast
into * megalokaryocytes ', large cells with enormous nuclei containing big nucleoli, similar to those seen in the omphaloidean
trophoblast of the mouse.
Unfortunately, we have no such thorough knowledge of the
genesis of the placenta of Man and Apes, but the structure of
the fully formed organ is known, and such early stages as have
been described are comparable, without difficulty, with stages
in the development of such placentas as those of Tarsius,
Insectivores, and so on.
When completed, the placenta is discoidal in shape. Amongst
the Platyrhine (New World) Monkeys it is double in Cebus,
single (occasionally double) in Mycetes. The two placentas are
placed respectively on the dorsal and ventral walls of the utenis,
and are connected, of course, by blood-vessels. Where only one
is present it is ventral, but there is on the dorsal wall a placentoid -  a thickened region of widened blood-vessels -  as though
for the reception of a second placenta.
In the Catarrhines (Old World tailed Monkeys) there are
usually two placentas, dorsal and ventral, as in Semnopithecus
and Gercocebus (Macacus) (Fig. 136), but one (the ventral) may
be absent. Either of the two may be the primary one. The
umbilical cord in Gercocebus passes to the ventral placenta,
whence blood-vessels travel to the other.
In the Simiidae {Hylobates, the gibbon) and Simia (the orang)
and in Man there is but a single discoidal placenta, placed in
the two Apes on the anterior (ventral) waU of the uterus, in Man
usually on the posterior wall, though the position is variable.
Further, in these forms the blastocyst or chorionic sac is always
embedded in maternal tissue which forms, between it and the
lumen uteri, a layer known as the ' decidua reflexa ', or, in more
IX THE PLACENTA 249
modern parlance, the ' capsularis ' (Fig. 158). What has been
regarded as a precursor of this structure-  a ridge running round
the placenta -  has been observed in Mycetes and Cercocebus.
Human anatomists distinguish from the ' decidua reflexa ' or
' capsularis ' that maternal tissue to which the placenta is
attached as ' decidua serotina ' or ' basalis while the opposite
Fig. 158. -  ^Human foetal membranes and placenta. (After Balfour, after
Longet.) The amniotic cavity (am.c.) has enlarged and occupies nearly
the whole of the extra-embryonic coelom (c), the amnion being reflected over
the umbilical cord (u.c.) and yolk-sac (y.s.). d.b., decidua basalis (serotina) ;
d.r., decidua capsvdaris (reflexa) ; d.v., decidua vera ; l.u., lumen uteri ;
am., amnion ; pi., placenta ; o.d., oviduct.
wall of the uterus is known as the ' decidua vera '. The application of the term ' decidua ' to maternal tissues has already been
alluded to ; it dates from the time when the type of placenta
we are considering was supposed to include, and carry away at
parturition, a considerable portion of the uterine wall.
Structurally all these placentas resemble one another very
closely. The maternal blood circulates in large spaces known
as sinuses, which are supplied by the blood-vessels of the uterine
250
THE PLACENTA
IX
wall (the decidua serotina or basalis in the Simiidae and
in Man) (Fig. 158*). These sinuses are lined everywhere-  not
only over the foetal blood-vessels, but also on the maternal and
on the foetal sides -  by a syncytial layer, usually referred to as
the syncytium, below which is a layer of cells-  the cell-layer of
Langhans of human embryology. These two layers separate the
maternal blood in the sinuses from the foetal connective tissue
and blood-capillaries (Figs. 159, 160). The more usual way,
Fig. 158*. -  Diagram of the structure of the human placenta, m.b.v.,
maternal blood-vessels in the decidua basalis {d.b.) opening into the sinuses
of the placenta (s) in which the villi branch. The villi are covered and
the sinuses lined on all sides by trophoblast (ir.) (syncytial layer and cell
layer of Langhans). am., epithelium (ectoderm) of the amnion.
perhaps, of describing this arrangement is to say that the foetal
villi -  meaning by that the. capillaries, and coimective tissue and
the cell-layer and syncytium covering them -  branch about in
sinuses filled with maternal blood. The expression ' villi ' dates,
however, from the older conception of the origin of these structures from villi similar to those seen in an Ungulate, a conception
which is almost certainly erroneous. The foetal capillaries do
branch very considerably it is true, but the sjmcjTtium and celllayer are continued over the outer walls of the sinuses, next the
tissues of the serotina. The sinuses, in fact, are lined everywhere
by these two layers.
5.
<^'L -  /
4»
â– (v'
sy
A
r. 1^,
â– 7>
Fig. 160. -  Structure of the insertion of
a ' villus ' into the ' decidua basalis ' of
the human placenta. d.b., large cells
(' decidual cells ') of the basalis ; m.b.v.,
maternal blood-vessels ; s., sinus of the
placenta ; si/., syncytial layer, and c, celllayer covering villus ; f.h.v., foetal bloodvessel in villus ; c'., mass of vacuolated
cells continuous with the cell-layer and
covering the extremity of the villus. The
fat globules in the syncytium are rendered
in black.
A, Large glycogen cells from tlia
maternal side of the human placenta
(5 months).
Fig. 159.-  Middle strip of a section
through the middle of the human placenta
at 5 months, d.b., decidua basalis ; v'.,
-  ua. "^i'li inserted into basalis; s., sinus; v.,
villi in sinus ; f.b.v., foetal vessel in villus ;
- urn umbilical vein ; w.a., umbilical artery ;
am., epithelium of amnion.
The syncjiiium and cell-layer covering the villi and lining the
inuses are stippled. Notice that this cell-layer is found between
he end of the villus and the maternal tissue of the basalis.
200
jX THE PLACENTA 251
Further, the cell-layer at the outer extremities of the villi is
continued into a mass of cells which separate the villus from
the tissue of the decidua basalis. These cells are vacuolated,
containing glj^cogen.
In Mycetes there is a syncytial network between the ' villi
cutting up the sinuses into smaller cavities (? lacunae) : there
is no cell-layer.
In the human placenta the sjmcytium contains fat ; in late
stages the cell-boundaries vanish in the layer of Langhans also.
On the maternal side of the placenta in the ' basalis ' there
are in man, Simia, Hylobates, and the Catarrhines, enlarged
coimective tissue-cells, known as ' decidual ' cells (Fig. 160).
These decidual cells get intermingled with the masses of cells
which, continuous with the layer of Langhans, cover the outer
extremities of the villi and contain glycogen, the two together
being disposed in a sheet known as the chorio-basahs. In
Simia and in man there are also septa, that is, peninsulae of
basalis tissue projecting into the placenta proper.
In man the layer of the basalis next the placenta is known
as the compacta. In this are the necks of glands. As gestation proceeds the epithelial lining of these glands degenerates,
the inter -glandular tissue undergoes a fibrinous degeneration,
and there are extravasations of blood in between these cells and
into the glands. Similar extravasations occur in Hylobates and
Simia. The whole layer becomes stretched and thinned. Beyond
the compacta is the spongiosa, a layer of maternal tissue
in which the gland -necks are much enlarged. There is slight
degeneration here also. A spongiosa is found in Simia, but
not in Hylobates.
In the lower Monkeys which possess no decidua capsularis
the chorion is smooth except in the placental region or regions,
but in Hylobates, Simia, and Man the chorion which is covered
by the capsularis is in an early stage produced into ' villi '
(which become poorly vascularized), as well as that opposite
the basalis. Later the ' villi ' disappear, and this part of the
chorion is then, to use an old term, the ' chorion laeve ', as
distinct from the ' chorion frondosum ' of the placenta.
The capsularis is covered by a cubical epithelium (Fig. 158).
262
THE PLACENTA
IX
In it, at the sides only, are a few glands with openings
into the lumen uteri. There are blood-vessels and extravasations. The whole layer gets distended by the growth
of the embryo and eventually its tissues wholly degenerate.;
the chorion is then immediately apposed to and united with
the vera on the opposite side, and the uterine cavity Is
m.h.v. dJ>. tr.
Fig. 161. -  Early human embryo with its membranes. (After Pet«rs.)
d.h., decidua basalis (serotina); d.r.ep., uterine epithelium covering the
decidua reflexa or capsularis ; I., lacuna in trophoblast (tr.) ; gl., uterine
gland ; m.b.v., maternal blood-vessels opening here and there into lacunae ;
cl., clot marking (probably) the point of entrance of the blastocyst ; here
the epithelium is interrupted. Other letters as before.
obliterated. Only in the condition known as placenta reflexalis
does the maternal circulation continue on this side.
In the decidua vera the epithelium ultimately disappears,
the compacta is stretched and attenuated, and there are
slight degenerative changes.
Such is the structure of the placenta in Man and Apes. We
have still to discuss the mode of formation of the capsularis
and the nature of the ' villi ' and ' sinuses '.
<3&
<1SS
®
5y.
- c
Fig. 162.-  a small portion of the wall of the embryonic sac-  on the side
of the decidua basalis-  of the human embryo shown in the last figure. (After
Peters.) d.b., maternal connective tissue of decidua basalis ; end., endothelium of maternal capillary (m.c), opening into lacuna (/.) ; sy-^ sjaicytium (plasmodi-trophoblast) ; tr., cellular trophoblast (cyto-trophoblast) :
the syncytium is pale, the cyto-trophoblast more deeply staimng ; m.,
somatopleure lining the extra-embryonic coelom (c).
V. 253
IX
THE PLACENTA
253
In the hedgehog and mouse Ave have seen the blastocyst
embedded in a pit in the uterine wall, in which it becomes
securely enclosed. The pit is lined by a continuation of the
uterine epithelium, which, however, soon disappears. The
relation of the blastocyst to the enveloping maternal tissues is
then very similar to the relation between the human chorionic
sac and its capsularis, and it has not unnaturally been suggested that the latter is really developed in the same way.
There is, however, knoisTi to us another way by which the
mammalian blastocyst may come into contact with subepithelial
tissue, for, as we have seen, the blastocyst of the guinea-pig
bores its way through the epithelium. In the earliest human
embryos knoAvn to us -  those described by Peters and Bryce ^ - 
there are very strong indications that the human capsularis
is. formed in this way, for in both cases there is in the centre of
this layer an interruption in the continuity of the epithelium,
marked, in Peters's case, by a blood-clot (Fig. 161). This
would then be the spot where the ovum effected its entrance.
If so then there can never have been any uterine epithelium on
the other side of the blastocyst, the side of the basalis where
the placenta is developed. This should be borne in mind in
considering the next question, the origin of the ' villi ' and
' sinuses '. In the embryos described by Peters and Bryce the
somatopleuric wall of the extra-embryonic coelom is covered
on the outside by a layer of cubical cells. Next to and perfectly
continuous with this layer is a thick mass, composed of similar
but polyhedral cells or in some places of a sjnacytium, with nuclei
similar to those of the cellular tissue. In this mass are lacunae,
and in these are maternal blood-corpuscles (Fig. 162). Outside
all this is the subepithelial connective tissue of the uterus, with
glands and blood-vessels : the latter open into the lacunae.
There can be no reasonable doubt that the whole of this
lacunated mass, with a basal cellular layer next the somatopleure, is the trophoblast, which has become thickened and
^ The embryo described by Bryce is perhaps shghtly the younger of the
two, as the extra-embryonic coelom appears to be not yet ])roperly formed.
That described by Peters was, however, obtained mi silii in the uterus, and
so gives us more information as to the relation between the foetal and
maternal tissues.
254 THE PLACENTA ix
hollowed out for the reception of extravasated maternal blood.
We have seen this occurring in a part only of the trophoblasl^
as in the mouse-  or in the whole of it-  as in the hedgehog,
and there is no reason why any other interpretation should be
put upon this stage in human ontogeny. The steps in its formation have, however, not yet been observed. The comparative
anatomy of the placenta has taught us that in cases of this kind
the necessary relation between foetal and maternal blood-streams
is brought about by the penetration of the allantoic capillaries
into the trophoblast. Exactly the same process occurs presumably
in the human being : the embryonic blood-vessels, with their
surrounding connective tissue, make their way into the trophoblast between the lacunae. There they branch repeatedly and
become the ' villi ' of the completed placenta, while the sinuses
are the transformed lacunae. The syncytial and cellular layers
lining the sinuses and covering the villi are then both trophoblastic in origin, and similar to the plasmodi-trophoblast and
cy to -trophoblast seen in other placentas of this type, in the
mouse for example ; they may be derived respectively from
the outer and inner layers of trophoblast in the early stage. It is
now possible to understand why the sinuses are Uned throughout,
on the maternal side against the basahs, as well as over the
' villi ' and on the foetal side, by the syncytium and cell-layer,
and why the outer extremities of the villi are separated from the
decidual cells of the basahs by the cell-masses continuous
with the layer of Langhans.
If this interpretation is correct then such hypotheses as that
the sinuses are enlarged veins and the syncytium the endothehum of those veins, or that the sync3rtium is derived from
uterine epitheHum, must evidently be discarded ; the second of
these views is indeed already ruled out of cotu-t if the implantation of the blastocyst is really effected in the way we have
suggested, for there could be in that case no uterine epithehum
on the side of the decidua basahs.
Such views as these date from the period when it was beheved
that the human, like other ' deciduate ' placentas, was derived
from the condition found in Ungulates by a simple adherence
of the villi to the crypt-walls ; and this beUef was supported by the existence of ' chorionic villi that is, branching processes
of the trophoblast, all over the outer surface of the early blastocyst, before the foetal vessels had appeared. But these ' chorionic vilh ' Avere observed only in blastocysts removed violently,
perhaps after post-mortem changes, from the sac of the capsularis,
and a proper histological examination of foetal and maternal
tissues together has revealed their true nature ; they are not
' vilh' or processes plungmg into maternal tissues, but the irregular
walls between the lacunae excavated in a thickened trophoblast.
The placenta of Man and Monkeys is, then, of the same kind as
that seen in Tarsius, and in Rodents, Insectivora, and Cheiroptera,
It contains no maternal tissue except the blood circulating
in the sinuses or enlarged trophoblastic lacunae, and, in addition
to the blood, no maternal tissue is lost at birth beyond the thin
layer of the degenerate compacta -  in both the deciduae basalis
and vera -  across which the break occurs, and such septa as
may have forced their way into the placenta.
We may now briefly review the genesis of the Mammahan
placenta in its varied types.
In Marsupials the placenta is wholly dissimilar from anything
met with elsewhere, since the trophoblast degenerates while the
syncytium is of uterine epithelial origin.
The Ungulates possess a typical Indeciduate placenta, with
villi dipping loosely into crjrpts hned by a persistent epitheUum,
from which they may be readUy withdrawn without injury to
the maternal tissues. Haemorrhage from the uterine blood vessels does, however, occur during gestation, and is of physiological importance in foetal nutrition.
The placenta is similar in Cetacea, Sirenia, and in the Lemuroidea (except Tarsius).
In the Proboscidea these haemorrhages are perhaps more
extensive.
In the Camivora the conditions are different, for here the
trophoblast does not send vilh into specially prepared crypts,
but, after the destruction of the uterine epitheUum, eats its way
into the tissues, engulfing the maternal capillaries. These and
the surrounding connective tissue grow pari passu with the trophoblast to produce the full thickness of the placenta. The
foetal capillaries grow into the trophoblast. The placenta is
therefore compounded of foetal and maternal tissues.
In the remaining orders this is no longer the case, for, after
the destruction of the epithelium, the trophoblast merely fastens
on to the underlying tissues ; only occasionally are the immediately adjacent capillaries engulfed (in the rabbit and in the
bat), and even here their endothelium soon vanishes. Once fixed
to the uterine wall the trophoblast grows not into the wall but
from it towards the centre of the uterus, receiving into its
lacunae the stream of maternal blood ; from the other side it
is vascularized by the allantois.
But distinct though these three types of placentation are, it
is yet possible that the third might have been derived from the
second -  if we inxagine the centripetal growth of the trophoblast
to occur before the ingrowth into the maternal tissues has taken
place -  and the shght-' enclosure of maternal capillaries in the bat
and rabbit almost demonstrates the change, while the insertion
of the trophoblast into the newly formed cr3rpts in Sorex recalls
another Carnivorous character. The second, in turn, may have
sprung from the first by the suppression of the uterine epitheUum.
These, however, are mere speculations, for which alternative
hypotheses may without difficulty be substituted.
One other point requires brief consideration. It has been held
that the characters of the placenta are a valuable criterion of
genetic relationship, and may accordingly be used for classificatory purposes. Now while it must be pointed out that single
characters in regard either to the gross or the minute anatomy
cannot be employed legitimately in this way -  there is no justification, for example, in grouping together the elephant, Hyrax,
the Sirenia, Orycteropus, and the Carnivora, because they all
possess a zonary placenta, nor on the other hand do we beUeve
it is yet proposed to separate the Lemuroid Primates, with their
typically Indeciduate, from the Anthropoids, with their Deciduate
placenta -  yet a combination of characters is often found to be
a constant mark of a natural order -  for instance, the large
yolk-sac with its lower Avail lost and the mesometric discoidal
placenta of Rodents, the zonary shape of the (histologically) peculiar placenta of Carnivora-  £vnd it is for this reason that
we hold that the remarkable structure of its foetal membranes
and its placenta entitle Tarsius to be separated from the Lemurs
and ranked with Monkeys and Man.
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1 rw ^^'etensch. An.sterda:,^ tm2'
Lefpzfg,T89f D.KeimblasevonJ'a..-^.. Festsch.f. Gegenbaur.
J. W. Jenkinson. Notes on the histology and physiology of the placenta
in Ungulata. Proc. Zool. Soc, 1906.
F. Keibel. Zur vergleichenden Keimesgeschichte der Primatcn. Selenlca'a
Studien iiber Enlwicklungsgeschichte der Tiere, 10. Wiesbaden, 1903.
J. KoLLMAKN. Ueber die Entwickelung der Placenta bei dem Makaken.
Anat. Anz. xvii, 1900.
R. KoLSTEE. Die Embryotrophe placentarer Sauger. Anat. Hefle,
1'8 Abt. xviii, xix, 1902, 1903.
R. KoLSTEE. Weitere Beitrage zur Kenntniss der Embryotrophe bei
Indeciduaten. Anat. Hefle, l'" Abt. xx, 1903.
J. LocHHEAD and W. Ceamee. The glycogenic changes in the placenta
and the foetus of the pregnant rabbit. Proc. Roy. Soc. B. Ixxx, 1908.
F. H. A. Maeshall and W. A. Jolly. Contributions to the physiology
of Mammalian reproduction. Phil. Trans., Series B, cxeviii, 1905.
F. H. A. Maeshall. The physiology of reproduction. London, 1910.
F. H. A. Marshall. The oestrous cycle and the formation of the corpus
luteum in the sheep. Phil. Trans., Series B, cxcvi, 1903.
P. NoLF. Etude des modifications de la muqueuse uterine pendant
la gestation chez le Murin. Arch, de Biol, xiv, 1896.
H. Petees. Die Einbettung des menschUchen Eies. Leipzig, 1899.
E. Selenka. Keimblatter und Primitivorgane der Maus. Wiesbaden,
1883.
E. Selenka. Die Blatterumkehrung im Ei der Nagethiere. Wiesbaden,
1884.
E. Selenka. Die Entwickelung des Gibbon. Wiesbaden, 1899, 1900.
R. Semon. Die Embryonalhiillen der Monotremen und Marsupialier.
Zool. Forschungsreise in Australien, ii.
F. Geae von Spee. Neue Beobachtungen iiber sehr friihe Entwicklungsstufen des menschUchen Eies. Arch. Anat. u. Phys. {Anxit.), 1896.
F. Geaf von Spee. Die Implantation des Meerschweincheneies in die
Uteruswand. Zeitschr. Morph. u. Anthrop. iii, 1901.
H. Steahl. Ueber Primaten-Placenten. Selenka' s Stvdien vher Entwicklungsgeschichte der Tiere, 12. Wiesbaden, 1903.
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Studien uher die Entwicklungsgeschichte der Tiere, 13. Wiesbaden, 1905.
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Edinburgh, 1876.
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Journ. Anat. and Phys. xiv, 1879.
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==Index Op Subjects And Authors ==
Absorption by colls, 12, 217, 246.
-  of water, 15.
Acanthias, 27.
Acanthocystis, 57.
Acipenser, 36, 41, 52, 102, 127.
Acrosome, 48, 54, 56, 81.
AcpyprymmLS, 194.
Afferent branchial arteries, 168.
Agar, 69.
Aggregation of cells, 11.
Au'-chamber, 48, 190.
Albumen, 46, 47.
-  sac, 187, 190.
Albumin, 226.
Alimentary canal, 107, 110 sqq., 128,
139, 143, 150, 169, 179.
Allantoidean, 236, 244.
ADantoin, 226.
AUantois, 108, 181, 183, 188 sqq., 192,
203 sqq., 246.
Amblystoma, 15.
Amia, 35, 38, 40, 102, 103, 127.
Amitosis, 104.
Amnion, 171, 175, 181, 183, 187 sqq.,
194 sqq.
Amnion, false, 108, 183, 187 sqq.
Amniota, 106, 107, 111, 134 sqq., 147,
171 sqq.
Amniotic thickenings, 226 ; bodies,
227.
Amphibia, 15, 16, 27, 36, 39, 40, 43,
46, 47, 49, 77, 78, 86, 95, 102, 129,
190.
Anamnia, 107, 111, 133, 147.
Anastomoses, 12, 174.
Animal pole, 40, 95.
Annelids, germ-cells, 35 ; polar rings,
35.
Annular zone of trophoblast, 216, 246.
Anterior abdominal vein, 190.
Anterior intestinal portal, 180.
Anthropoidea, 209, 255.
Anti-mesometric pit, 234, 239.
-  placenta, 241, 243, 246.
Anura, 129.
Anus, 153, 154.
Aorta, 168, 179, 180, 183.
Aortic arches, 180, 181, 182.
Archenteron, 111 sqq.
Area, increase of, 12.
Area opaca, 172; peUucida, 172, 174;
vasculosa, 170, 172, 177, 183 sqq.,
203, 241, 246.
Arterial arches, 168, 169, 180, 182.
Arteries, branchial, 155, 169, 182 ;
umbilical, 188 ; vitelline, 171, 180.
Artificial parthenogenesis, 87,
Arvicola, 195.
Ascaris, 34.
Ascidians, 35.
Assheton, 107, 143, 201.
Auditory vesicle, 161, 170, 176, 180.
Auricle, 180.
Axial filament, 48, 54, 56, 57.
Axis of ovum, 40, 95, 111.
Axolotl, 41, 51, 52, 64, 77, 78, 81 sqq.,
130.
Balbiani, 72.
Balfour, 213.
Balfour's rule, 99.
BaUowitz, 50, 51.
Basal cells, in testis, 58, 59.
Bat, 74, 145, 195, 208, 241, 242.
Bddlostoma, 120.
Van Beneden, 145, 202, 204, 240.
Bilateral egg structure, 89, 90, 100.
-  segmentation, 97.
-  closure of blastopore. 111, 113, 147.
Bile-pigments, 48, 225, 246.
Bilirubin, 225.
Biliverdin, 232.
Binucleate cells, 224.
Birds, 29, 36, 37, 40, 43, 46, 47, 49, 77,
78, 86, 90, 103, 105, 139, 190.
Bladder, 169, 182, 190, 192.
Blastocoel, 97, 98, 132, 171.
Blastocyst, 107-9, 195, 263.
Blastoderm, 104, 107, 120, 129, 131,
133 sqq., 143, 147 sqq., 171, 187.
Blastomere, 96.
Blastopore, 111 sqq., 147 sqq., 172.
Blastula, 98.
Blood, 168, 174.
Blood-clot, 253.
Blood-islands, 173, 174, 177.
Blood-vessels, 168, 179.
Bomhinator, 50, 51.
Bone, 11.
Bonnet, 144, 205, 206.
Bos, 52, 220 sqq.
Brain, 153, 158, 175.
Branchial arches, 155, 169, 182.
Branchial arteries, 168, 169, 182.
Branchial clefts, 169, 182.
Brauer, 131 sqq.
Broman, 51.
Bryoe, 253.
Budding, 9, 35.
Bufo, 15, 51, 52, 129.
Butyric acid, 87.
Calcium oxalate, 226.
Oanis, 36, 144, 205, 229 sqq.
Capillary, 174, 179 ; of placenta, 216,
217, 220, 224, 229, 230, 236, 237,
238, 240, 244, 250.
Capsule of kidney tubule, 177.
Cardinal veins, 167, 168, 179.
Carnivora, 204, 229 sqq., 255, 256.
Carotid gland, 169.
Caruncle, cotyledonary, 220, 221.
Cat, 31, 229 sqq.
Catarrhines, 248.
Caudal swelling, 122.
Gavia, 17, 18, 20, 31, 36, 49, 50, 52,
55, 74, 108, 195-7, 203, 204, 239,
253.
Cavity, of segmentation, 97, 98, 132,
171.
-  subgerminal, 135, 149, 171 ; peritoneal, 167 ; pleural, 177 ; pleuroperitoneal, 168, 177 ; of amnion,
188 ; of trophoblast, 200.
Cebus, 248.
Cell-division, 10, 14, 88, 100.
Cell-layer of Langhans, 260, 251, 254.
Centeies, 243.
Centrosome, 48, 54-7, 65, 78, 83-5.
Centrosphere, 54-7, 74, 78.
Cephalopoda, 34.
Ceratodua, 41, 102, 128, 150.
Cercocehus, 210, 248, 249.
CerebeJlum, 158.
Cervical flexure, 168, 181.
Cervus, 220.
Cetacea, 208, 226, 255.
Chalaza, 46.
Change of growth-rate, 17, 22.
Cheiroptera, 203, 207, 218, 241 sqq.
Chemistry of yolk, 37 ; of egg-membranes, 46, 47 ; of spermatozoon, 52.
Chick, 15, 139-143, 171 sqq.
Cholesterin, 38, 47, 52.
Choloepus, 207, 227.
Chorda-canal, 134, 145.
Chordal sheath, 169
Chorio-basaHs, 252.
Chorion, of ovum, 45 ; (false amnion)
187, 192 ; laeve, 251 ; frondosum,
251,
Chorionic villi, 218, 255 ; vesicles, 227.
Choroid, 161.
Choroid fissure, 159, 161.
Chromatin, 23, 66 sqq., 78 sqq., 85,
87, 92, 93.
Chromatoid accessory body, 55.
-  body, 74.
Chromosomes, number of, 23, 66 sqq.,
78 sqq. ; division of, 79 ; accessory,
81 ; in fertilization, 85 ; in inheritance, 80, 87, 92, 93.
Chryaemys, 28.
Cilia, 165, 221.
Cijiiary processes, 160.
Cleavage, 95 sqq.
Closure of blastopore. 111 sqq.
Clot, 263.
Clupein, 52.
Coelom, 164, 165, 177.
Colour of yolk, 37, 38 ; of egg-shell,
48.
Concrescence of layers, 13.
Connective tissue, 166, 169.
Contraction figure, 65, 72.
Contra-deciduate, 217, 246.
Convergence of chromatic filaments,
66, 72.
Compacta, 251, 252, 255.
Composition, 11.
Cord, spinal, 156, 175.
Cords, medullary, 31 ; sex, 31, 34.
Cornea, 161.
Corpus luteum, 44.
Corpuscles, blood, 168.
extravasation of, 220, 224, 225,
227, 232, 236, 240, 246, 251.
Cortex of ovary, 31.
Cotyledon, 219.
Cotyledonary, 219.
Cow, 220 sqq.
Cranial flexure, 158, 181.
Crest, neural, 164, 156.
Grocodilus, 52.
Cross-furrow, 96.
Crura cerebri, 158.
Crustacea, 57.
Crypts, 219, 221 sqq., 226, 227, 229,
246.
Cumulus proUgerus, 43.
Cuticle of egg-shell, 47.
Cutis, 166.
Cyclops, 34.
Cyclostomata, 118, 162,
Cymatogaster, 27.
Cysts, of testis, 57, 59.
Cytoplasm, increase of, 21 ; significance of in development, 43, 73,
74, 92, 93, 102, 150.
Cyto-trophoblast, 236, 240, 264.
Dasypus, 227.
DasyuTus, 36, 40, 48, 107, 194, 216,
217.
Davenport, 14, 15, 16.
Dean, 120, 127.
INDEX OF SUBJECTS AND AUTHORS
261
Decidua, 218.
-  basalis, 249 sqq.
-  oapsularis, 243, 249 sqq.
-  reflexa. 243, 244, 245, 248. sqq.
-  serotina, 249 sqq.
-  vera, 249 sqq.
Decidual cells, 251.
Deciduato, 215, 217, 229, 256.
Deciduofracts, 244.
Deciduous, 218, 254.
Degeneration of uterine epithelium,
220, 229, 230, 234, 239, 241, 244,
245, 248, 252.
Determination of sex, 81.
Development, defined, 9.
Dextrose, 47, 226.
Diaphragm, 177.
Dictyate, 32, 33, 73.
Diddphys, 36, 194, 216.
Differentiation, 10, 14, 151.
-  histological, 11.
-  and senescence, 21 ; and segmentation, 102.
Diffuse, 219.
Dimorpha, 57.
Diplotene, 32, 59, 66, 72.
Dipnoi, 128.
Discoglossus, 49, 52.
Discoidal segmentation, 104.
-  placenta, 232, 239, 241, 242, 243.
Discus proligerus, 43.
Dispersion of elements, 13.
Ditrematous Mammalia, 191 sqq.
Diverticula allantoidis, 206, 220.
Division of cell-masses, 13 ; of cells,
14, 95 sqq. ; of chromosomes, 78,
79.
Dog, 36, 144, 205, 229 sqq.
Dorsal division of blastopore, 153.
-  lip of blastopore. 111 sqq.
-  placenta, 248.
-  roots, 156, 163, 164.
Duct, pronephric, 167.
Ductus Cuvieri, 168, 181.
Ductus endolymphaticus, 162.
Duval, 190, 205, 231, 240.
Ear, 161, 162.
von Ebner, granules of, 57, 59.
Echidna, 36.
Ectoderm, 108, 110 sqq., 156.
Edentata, 207, 227.
Edge of blastoderm, 122-7, 131.
Efferent branchial arteries, 108.
Elagmobranchs, 27, 36, 37, 40, 43, 46,
47, 49, 71, 78, 80, 90, 103, 105, 120
sqq., 130, 150, 162, 165, 170.
Elementary organs, 10.
Elephas, 208, 227, 256.
Embryonic area, 143.
Embryonic knob, 108, 143, 195 sqq.
-  plate, 198 sqq.
-  shield, 105, 107, 135, 143, 144, 148.
End-knob, 48.
Endoderm, 105, 107, 110 sqq., 150.
Endothelium, 168, 174, 179, 240, 241,
256.
Entrance-cone, 81.
Entrance-funnel, 81.
Epidermis, 150.
Epithelium, germinal, 26 ; of lens,
160 ; of uterus, 219 sqq., 220, 226,
229, 230, 234, 239, 241, 244, 245,
248, 252.
Equator, of ovum, 40, 95.
Erinacells, 36, 52, 195, 198, 207, 2435, 253.
Esox, 52.
Eustachian passage, 169, 182.
Eutheria, 216.
Evagination, 12.
Extra-embryonic coelom, 179, 187,
196, 209, 246.
Extravasation, 220, 224, 225, 227,
232, 236, 240, 246, 251.
Eye, 159 sqq.
Eyeball, 161.
Factors, external, 16.
Fallopian tube, 221, 226.
False amnion, 108, 183, 187 sqq., 192.
Farmer, 69.
Fat, 37, 38, 44, 47, 52, 204, 220, 224,
232, 234, 238, 251.
Feather-star, 92.
FehHng, 16.
Ferment, glycogen splitting, 241.
Fertilization, 81, sqq., 221.
Fibres, of lens, 161 ; of nerve roots,
156, 157 ; of optic nerve, 161.
Fibrin, 232, 251.
Filament, axial, 48, 54-7.
Fin, 155.
Flagellate spermatozoon, 48.
Flattening of egg, 35, 95.
Flexure, cranial, 158, 181 ; cervical,
181.
Foetal membranes, 183 sqq. ; of
mammals, 192 sqq.
Folds, medullary, 154, 156.
Follicle, 28, 32, 43-5, 221 ; cells of
ovary, 25, 32 ; of testis, 57
Food, 15.
Fore-bram, 153, 158, 175, 180.
Fore-gut, 180.
Fringilla, 50.
Frog, 15, 27, 35, 36, 37, 86, 89, 95 sqq..
Ill sqq., 147, 149, 150, 153 sqq.
Funnel, pronephric, 167.
Fusion of cell aggregates, 12.
INDEX OF SUBJECTS AND AUTHORS
Oalago, 227.
Ganglia, 154, 156.
Ganoids, 36, 46, 127.
Gastrulation, 111
Genital ridge, 26.
Germ-cells, vehicles of inheritance,
9, 23 sqq.
Germ-layers, 10, 110 sqq., 196 ; inversion of, 197.
Germ-number of chromosomes, 66, 67.
Germinal epithelium, 26, 29.
-  vesicle, 41.
-  wall, 171.
Gibbon, 248, 251.
GiU-plate, 154.
Gill-slits, 169, 180, 181, 182.
Gills, 155, 168.
Giraffa, 220.
Glands of uterus, 204, 221, 229, 230
232, 246, 252, 253.
Globules of yolk, 36.
Glomus, 167.
Glycogen, 220, 225, 226, 236, 237, 239,
241, 251.
Graafian follicle, 43, 221.
Granules of von Ebncr, 57, 59.
-  of yolk, 36, 73.
Gray crescent, 89, 98, 100.
Green border, 232.
Growth, 10, 15 sqq., 23, 73.
Guinea-pig, 17, 18, 20, 31, 36, 49, 50,
52, 55, 74, 108, 195-7, 203, 204,
239, 253.
Gymnophiona, 36, 40, 102, 111, 131
sqq., 136, 147, 148.
Haematochlorine, 232.
Haematogen, 38.
Haematoporphyrin, 225.
Haemoglobin, 220, 225, 227, 232,
246.
Haemorrhage, 220, 224, 227, 232, 236,
240, 246, 251.
Halicore, 208, 226.
Halmaturus, 194.
Head, length, 20.
Head-fold of amnion, 175, 181.
Head-process of primitive streak, 172.
Head somites, 161, 162-4.
Heart, 167, 168, 170, 179.
Heat, 229.
Hedge-hog, 36, 52, 195, 198, 207, 243-5,
253.
Hemispheres, 158, 181.
Herlant, 86.
Herring, 52.
Hertwig's rules, 99, 100.
Heterochromosomes, 81.
Heterogeneous hybridization, 92.
Heterotypic, 59, 67, 74, 75, 77.
Hill, 107, 143, 193, 217.
Hind-brain, 153, 158, 175, 180.
Hind-gut, 180.
Hippomanes, 206, 225, 227.
Holoblastic, 94.
Homo, 19-21, 36, 52, 197, 209, 212.
218, 248 sqq.
Homoeotypic, 71, 78.
Homology, 151.
Horse, 205, 219.
Hubrecht, 198, 201, 207, 209. 210.
234, 243, 245, 247.
Human embryo, 15, 18, 19, 211-14.
218, 248 sqq.
Hybridization, 92.
Hydroids, germ-cells, 34.
Hylobates, 248, 251.
Hyoid arch, 155, 168, 109, 182.
Hyomandibular cleft, 169, 182.
Hyperaemia, 229.
Hypertonic sea-water, 87.
Hypertrophy, 220, 229.
Hypogeophis, 131.
Hyracoidea, 227.
Hyrax, 227, 256.
Ichthulin, 38.
Ichthyophis, 131.
Idiozom, 54.
Increments, percentage, 16.
Indeciduate, 217, 218-28, 255.
Individuality of chromatin and chromosomes, 75.
Infundibulum, 159, 175.
Inheritance, chromosomes in, 80, 87 ;
cytoplasm in, 92, 93.
-  mechanism of, 9.
Inner mass, 108, 143, 195.
Insectivora, 203, 207, 218, 243 sqq.
Intermediate cell-mass, 164, 165, 176;
segmentation, 102 ; vitelline veins,
186.
Interruptions of continuity, 13.
Invagination, 12.
Investment by cells, 12.
Iris, 160.
Iron, 220, 224, 225, 246.
Iso-bilateral segmentation, 97.
Iter, 158.
Jelly, 46.
Julin, 204.
Keratin, 46, 47.
Kerr, 128.
Kidney, 164, 165, 177.
King, 51.
Knob, embryonic, 108, 143, 195.
-  end, 48.
von Korff, 50.
Labyrinth, IGl.
Lacerta, 47, 135.
Lacunae, 232, 236, 240, 241, 244, 248,
253-5.
Lamellae, 230.
Lamprey, 27, 35, 36, 37, 46, 86, 102,
119, 129, 149, 150, 163, 170.
Langhans, 250, 251, 254.
Large-yolked, 39, 103.
Latebra, 40.
Lateral amnion folds, 176, 187.
-  lips of blastopore, 112 sqq.
-  plate, 162, 176.
-  vitelline veins, 186.
Latitudinal, 96.
Layers of yolk, 40.
Lccitliin, 38, 47, 52.
Leg, length, 20.
Lemuroidea, 208, 227, 255, 256.
Length of head, 20 ; of leg, 20 ,• of
spermatozoon, 52 ; of vertebral
column, 20.
Lens, 159, 160, 161, 181.
Lepidosiren, 102, 128, 129, 147, 149,
150, 170.
Lepidosteus, 36, 40, 102, 103, 170.
Leptotene, 59, 64, 72.
Lepus, 29, 36, 196, 201, 203, 239-41.
Leucocytes, 217, 220, 225, 229, 246.
Lillie, 190.
Liquor amnii, 188.
Liquor foJIiculi, 43.
Liver, 169, 182.
Longet, 213, 249.
Longitudinal division, 79.
Loss of yolk, 203 ; of shell, 203.
Lower layer, 104, 107, 122, 135, 143,
149, 150, 171, 195.
Lumen uteri, reformed, 234, 238, 239.
Lungs, 167, 169, 182.
Lutein, 38, 44, 47.
Macacus, 248.
Mackerel, 52.
Magma, 73, 74.
Mammalia, 29, 36, 46, 71, 77, 78, 143,
177, 190, 192 sqq.
Mammillary sheet, 47.
Man, 19-21, 36, 52, 197, 209, 212, 218,
248 sqq.
Mandibular arch, 155, 168, 169, 182
Manis, 227.
Marsupialia, 46,47, 48, 107-9, 143, 193
216, 255. â– 
Maturation divisions, 23, 59, 62 sqq.
Mechanical shock, 87.
Mechanism of inheritance, 9.
Medulla oblongata, 158.
Medulla, of ovary, 31.
Medullary folds, 153, 156, 174
Medullary groove, 156, 174.
-  plate, 153, 174.
-  tube, 154, 156, 174.
Megalecithal, 39.
Megalokaryocytes, 236, 248.
Meiotic, 67.
Membrana elastica interna, 169.
Membrane, in fertilization, 89.
Membranes of ovum, 45-8; of foetus,
183 sqq., 192 sqq.
Meridional, 95.
Meroblastic, 103.
Merocyte, 86.
Merogony, 87.
Mesentery, 168.
-  germ-cells in, 27.
Mesocardium, 168, 179.
Mesoderm, 110 sqq., 162 sqq.
Mesometric placenta, 232, 239, 242,
247.
Mesonephros, 177.
Metameric segmentation,156, 162, 164.
Metamorphosis of spermatid into
spermatozoon, 52 sqq.
Metanephros, 177.
Metatheria, 216.
Methods, in embryology, 9, 10.
Meves, 50, 53, 55, 68.
Microlecithal, 36, 95.
Micropyle, 46.
Mid-brain, 153, 158, 175.
Middle-piece, of spermatozoon, 49.
Migratioii, of cells, 11 ; of germ-jcells,
27 sqq.
Minot, 17-21, 213.
Mitosis, 62.
Mitsukuri, 138.
Mole, 31, 36, 195, 207, 243, 245.
Mollusc, 92.
Monkeys, 197, 209, 212, 218, 248 sqq.
Monotremata, 36, 43, 47, 48, 103, 106,
107, 143, 192.
Montgomery, 69.
Mouse, 31, 36, 52, 59, 86, 145, 195,
200, 203, 232 sqq., 253.
Movements of cells and cell aggregates
11-13. ^
Mucin, 47, 226.
Mus, 31, 36, 52, 59, 86, 145, 195, 200,
203, 232 sqq., 253.
Muscles of eye-baU, 161 ; of trunk
and limbs, 166.
Muscular wall of heart, 168, 179
Mycetes, 248, 249, 251.
Myocoel, 165, 166, 177.
Myotom, 166, 177.
Myrmccophaga, 227.
Myxine, 71.
Myxmoids, 35, 36, 40, 46, 103, 120,
Neck, of spermatozoon, 49.
Nephrocoel, 165, 177.
Nephrotom, 165, 166, 176, 177.
Nerves, cranial, 154, 156, 162, 163 ;
spinal, 154, 156.
Nervous layer, 160, 162.
-  system, 153, 156, 170, 175, 181.
Neural crest, 154, 156, 162, 163, 181.
Neurenteric passage, 134, 142, 145,
153, 154, 170.
Newt, 63, 86.
Nolf, 208, 242.
Nostril, 161.
Notochord, 110 sqq., 169, 172, 174.
Nuclear contributions to cytoplasmic
structure, 73, 74.
Nucleic acid, 52.
Nuclein, 52.
NucleoU, 72, 73, 236, 248.
Nucleo-plasma ratio, 22, 99.
Nucleo-protein, 38, 73.
Nucleus, decrease of, 21 ; in inheritance, 80, 87, 92, 93 ; of ovum, 41 ;
of spermatozoon, 48.
Nuclei in yolk, 103, 104.
ObUques, 161, 162.
Oestrus, 220, 221, 229.
Oil, 37.
Olfactory pit, 155, 161.
-  sac, 161, 170.
Omphaloidean, 236, 238, 244.
Oocyte, 25, 31.
Oogonia, 24.
Operculum, 155.
Ophthalmicus, 163.
Optic cup, 159, 181.
-  lobes, 158.
-  nerve, 161.
-  stalk, 159, 16'1.
-  vesicle, 159, 170, 180, 181.
Orang, 248, 251.
Orca, 208, 227.
Oreas, 220.
Organ-forming substances, 43, 102,
150.
Origin of germ-cells, 26 sqq.
Ornithorhynchus, 36, 48, 144.
Oryckropus, 227, 256.
Ostracoda, 52.
Outer layer, 108, 195.
Ovary, formation of, 30, 31 ; of tadpole, 72.
Ovis, 36, 196, 220 sqq.
Ovo-albumin, 47.
Ovo-mucoid, 47.
Ovo-vitellin, 38.
Ovulation, 43, 221.
Ovum, 23, 35 sqq.
Pachytene, 32, 59, 66, 72.
Pairing of chromatin filaments, 65, 80.
Pancreas, 169, 182.
Parablast, 105.
Paraderm, 105.
ParathjToid, 169.
Parthenogenesis, 87.
Partial segmentation, 103.
Parturition, 238.
Peramdes, 194, 217.
Perca, 51.
Perforation of floor of archonteron,
148.
Perforatorium, 48, 54.
Periblast, 91, 104.
Pericardium, 168, 177, 179.
Periods, in history of germ-cells, 23.
Peritoneal cavity, 167, 177.
Peritoneum, 168.
Perivitelline fluid, 89.
Peters, 211, 253.
Petromyzon, 27, 35, 36, 37, 46, 86, 102,
119, 129, 149, 150, 163, 170.
Pfluger, 31, 100.
Phagocytosis, 12, 213, 221, 224, 229,
230, 231, 236, 242, 244, 246.
Phalangista, 49, 50.
Phascolarctos, 48, 194.
Phosphatides, 38.
Pig, 195, 219.
Pigment layer of retina, 159.
-  of cornea, 161; of ovum, 40; of
uterus and placenta, 220, 225, 227,
232, 246.
Pituitary body, 169, 181.
Pineal body, 159.
Placenta, 192, 215 sqq.
-  reflexalis, 252.
Placental mammals, 35, 36, 39, 41,
46, 48, 108, 194 sqq., 217 sqq.
Placentoid, 248.
Plane, of symmetry, lOO.
-  sagittal, 112.
Plasmodi-trophoblast, 236, 240, 254.
Platelets of yolk, 36.
Platydaclylus, 135.
Platyrhine, 248.
Pleural cavity, 177.
Pleuro-peritoneal cavity, 168, 177.
Polar bodies, 25, 77.
-  furrow, 96.
-  rings of Annelids, 35.
Poles of egg-axis, 40.
Polyspermy, 86.
Pontocypris, 52.
Post-anal gut, 170.
Posterior cardinal vein, 1G7.
-  intestinal portal, ISO.
-  vitelline vein, 186.
Potts, 15.
Primates, 203, 218, 227, 24G sqq.
Primitive groove, 139 sqq., 172, 174.
-  plate, 107, 135.
-  streak, 139 sqq., 172.
Primordial germ-cells, 23 sqq., 2C sqq.
PrisHurus, 86.
Pro-amnion, 172, 194.
Proboscidea, 208, 227, 255.
Proctodaeum, 153, 154, 156, 169.
Pronephros, 166, 167, 177.
Pronucleus, 83, 87.
Pro-oestrus, 220, 221, 229.
Prophases of first maturation division,
23, 25, 64, 65, 71, 72.
Prosencephalon, 158.
Protamine, 52.
Protein, 37, 38, 47, 204, 220, 224, 232,
238.
Proto vertebrae, 162.
Protozoa, 57.
Pteropus, 242.
Qualitative division, 79.
Quantitative division, 79.
Rabbit, 29, 36, 196, 201, 203, 239-241.
Radial type of cleavage, 96.
Haia, 52.
Sana, 15, 27, 35-7, 86, 89, 95, 97,
111 sqq., 147, 149, 150, 153 sqq.
Rate of division, 100.
-  of growth, 16 sqq.
Ratio of nucleus to cytoplasm, 22, 99.
Rauber's cells, 195 sqq., 234.
Re-arrangement of material, 13.
Recti, 161, 162.
Reduction of number of chromosomes,
24, 66 sqq., 78 sqq.
-  of plasma-nucleus ratio, 22, 99.
Regeneration, 9, 35.
Reptiles 28, 36, 40, 46, 47, 49, 78,
86, 103, 105, 135 sqq., 190.
Respiration, 188, 224.
Retina, 158-160.
Retro-peritoneal tissue, 28.
Ridge, genital, 26.
Ring-shaped centrosome, 54, 66.
-  chromosomes, 59, 66, 75.
Rodents, 200, 203, 218, 232 sqq.
Roots of nerves, 156, 157.
Rotation of frog's egg, 113, 114; of
sperm-head, 83.
Riickert, 86.
Rule of Balfour, 99.
-  of Hertwig, 99, 100.
Ruminants, 220.
Sagittal plane, 111.
Salamander, 53.
Salmin, 62.
Salmon, 27, 52, 86.
Salmonidao, 10.0.
Salts, 38, 47, 220.
Sarasin, 131.
Schauinsland, 142.
Schreiner, 69.
Sciurus, 203, 239.
Sclerotic, 161.
Sclerotom, 165, 177.
Scombrin, 52.
Scorpions, germ-cells, 34.
Scott, 119.
Secretion of cells, 221, 229, 230.
Segmental duct, 177.
Segmentation, 95 sqq. ; significance
of 22 99.
-  cavity, 97, 98, 132, 171.
-  of mesoderm, 162 ; of neural crest,
156.
Selenka, 197, 198, 211.
Seminiferous tubules, 34, 57.
Semnopithecits, 248.
Semon, 128, 193.
Senescence, 21.
Sense organs, 156, 181.
Sense-plate, 154.
Septa of yolk-sac, 187 ; of placenta,
251.
Sero-amniotic connexion, 188.
Serosa, 187.
Serranus, 125 sqq.
Sertoli, cells of, 58-60.
Sex, cords, 31, 34.
-  determination of, 81.
Sheep, 36, 196, 220 sqq.
Shell, 45, 47, 48, 172.
-  loss of, 203.
Shell-membrane, 47, 48.
Shield, embryonic, 105, 107, 135, 143,
144.
Side folds of amnion, 176, 187.
Simia, 248, 251.
Simiidae, 248, 250.
Sinus, 249 sqq.
Sinus terminalis, 170, 186.
Sinus venosus, 180.
Siredon, 41, 51, 52, 64, 77, 78, 81 sqq..
130.
Sirenia, 208, 226, 255.
Size of cells, 100 ; of ovum, 35, 30 ;
of spermatozoon, 52.
Skeleton, 165.
Small-yolked, 36, 95.
Soaps, 47.
Sobotta, 127.
Somatic number of chromosomes, 23,
60, 66.
Somatoplcure, 166, 168, 177.
Somites, 161, 162, sqq., 176.
Sorex, 196, 207, 243, 246.
Sparrow, 142.
Spec, Graf, 212.
Spcnn-astor, 83.
Sporm-path, 83-5, 89, 100-2.
Sperm-sphere, 83.
Spermatid, 24, 52 sqq., 59.
Spermatozoon, 23, 24, 48 sqq.
Spermocytcs, primary, 23, 59 ; secondary, 23, 24, 59, 67.
Spermogonia, 23, 57, 69.
Sphere of attraction, 54-7, 74, 78.
Spinal cord, 156, 175.
Spiracle, 157.
Splanchnocoel, 165, 167, 177.
Splanchnopleure, 168, 177.
Splitting of cell aggregates, 12, 13.
Spongiosa, 230, 251.
Squirrel, 203, 239.
Stature, growth of, 20.
Stomata, 187.
Stomodaeum, 154, 156, 169.
Strahl, 228.
Stroma, 26, 30.
Structure of germ-cells, 35 sqq.
-  increase of, 10.
-  of ovum, 14, 40, 41-43, 60, 95.
Sturgeon, 36, 41, 52, 102, 127.
Sturin, 52.
Sub-germinal cavity, 135, 149, 171.
Sub-intestiual vein, 170.
Sucker, 154.
Sus, 195, 219.
Symmetry of embryo, 90.
-  of ovum, 40, 41-3, 90, 95.
-  of segmentation, 99 sqq.
Synaptene, 59, 65, 72.
Syncytium, 171, 217, 230, 236, 250,
251, 254.
Tail, of spermatozoon, 48, 54-7, 83;
of tadpole, 155.
Tail-fold of amnion, 176, 187, 210;
gut, 170.
Tail-sleeve, 56.
Tcdpa, 31, 36, 195, 207, 243, 245.
Tamandua, 227.
Tangential division, 97, 103.
Tarsius, 195, 201,209-11,218, 246-8,
255, 257.
Teeth, 155.
Teleostei, 36, 37, 46, 49, 91, 103, 104,
125 sqq., 130, 150, 170.
Telolecithal, 38.
Tendon, 11.
Testis, origin of, 34 ; tubules of, 34,
57.
Tetraceros, 220.
Thalamencephalon, 158.
Theca, 26, 28, 30, 44.
Thickness, alterations of, 12.
Thymus, 109, 182.
Thyroid, 169, 181.
Toad, 15, 51, 62, 129.
Transverse division, 79.
Triomjx, 138.
Triton, 63, 86.
Trophoblast, 107, 143, 144, 192 sqq.,
215 sqq.
Trophospongia, 234, 239, 243, 247.
Tropidonotus, 49, 50.
Trout, 27.
Truncus arteriosus, 180, 182.
Tubes of Pfluger, 31.
Tubules, of testis, 34, 57.
-  of kidney, 166, 177.
Tunica albuginea, 34.
Twpaia, 195, 201, 207, 243, 246.
Turner, 209.
Tympanic cavity, 182.
UmbilicEvl arteries, 188, 212.
-  cord, 212, 214, 238, 247.
-  veins, 188, 190, 212.
-  vesicle, 108.
Umbilicus, 187, 188, 196.
Ungulates, 203, 204, 218 sqq., 255.
Union of pronuclei, 85, 87.
Upper layer, 104, 135, 143, 149, 171.
Urodela, 50, 51, 60 sqq., 102, 129, 130,
150.
Uterine epithelium, 219, 220, 226, 229,
230, 234, 239, 241, 244, 245, 248,
252.
-  glands, 204, 220, 227, 229, 230, 232,
252
-  milk, 221 227.
Vegetative pole, 40, 95.
Vein, anterior abdominal, 190.
-  cardinal, 167, 168, 179, 181.
-  subintestinal, 170.
-  umbilical, 188.
-  vitelline, 168, 175, 179, 180, 183-6.
Ventral aorta, 182.
-  division of blastopore, 153, 154.
-  lip of blastopore, 113 sqq.
-  placenta, 248.
-  roots, 157, 163, 164.
-  stalk, 213, 246.
Ventricles of brain, 158 ; of heart,
180.
Vertebral column, length, 20.
-  plate, 162, 176.
Vespertilio, 74, 145, 195, 208, 241, 242.
VUli, 218, 219, 221 sqq., 226, 227, 229,
250, 251, 252.
Vitelline arteries, 171, 180, 186.
-  membrane, 45, 46.
-  veins, 168, 175, 179, 180, 186.
Vitreous body, 159, 161.
Water, absorption of, 15 ; in cgg
whitc, 47 ; in yolk, 38.
Weight, growth of, 20 ; of yolk, 40.
Whito of egg, 46, 47.
Will, 136, 137.
Wilson, H. v., 105, 125 sqq.
-  J. T.. 107, 143.
von Winiwarter, 64, 69.
Wolffian tubules, 177.
Woods, 27.
Worm, 92.
Wrinkling of egg-surface, 95.
Yolk, 35, 36 sqq., 73, 74, 99, 100.
-  loss of, 203.
Yolk-blastoporc, 124.
Yolk-body, 40, 107 ; of Balbiani, 72, 74.
Yolk-eclls, 113 sqq., 128, 129, 150, 169.
Yolk-nuclei, 103-105, 122.
Yolk-nuclcuB, 73, 93.
Yolk-plug, 113, 114, 133, 135, 130,
142.
Yolkrsac, 108, 169, 170, 177, 180,
183 sqq., 192, 203 sqq., 238, 241,
244, 246.
Yolk-stalk, 27, 29, 170, 175, 180.
Zona pellueida, 45, 107.
Zona radiata, 46.
Zonary placenta, 227, 229, 256.




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Jenkinson JW. Vertebrate Embryology. (1913) Oxford University Press, London.

Vertebrate Embryology 1913: 1 Introduction | 2 Growth | 3 The Germ-Cells, their Origin and Structure | 4 The Germ- Cells, their Maturation and Fertilization | 5 Segmentation | 6 The Germinal Layers | 7 The Early Stages in the Development of the Embryo | 8 The Foetal Membranes of the Mammalia | 9 The Placenta | Figures
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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

Comprising

The Early History Of The Embryo And Its Foetal Membranes

By

J. W. Jenkinson, M.A., D.Sc.

Lecturer In Embryology, Oxford

Fellow Of Exeter College


Oxford London:


Oxford University Press London Humphrey Milford Publisher to the University

Impression of 1925

First Edition, 1913

Jenkinson, John Wilfrid, (1871-1915)


TO A. A. W. HUBRECHT

PDF version

Preface

The publiccation in 1885 of Francis Balfour's great treatise on Comparative Embryology marked the first attempt to establish on a scientific basis our knowledge of the development of the animal organism.


Since Balfour's day embryology has travelled far, and a multitude of new discoveries has thrown fresh light on the structure, origin, maturation, and fertilization of the germ-cells, on the mechanism of segmentation, on the significance of the germinal layers, as well as on the later organogeny in the several groups.


But while abroad all this material has found embodiment in such comprehensive manuals as those of Oskar Hertwig on Vertebrate, and of Korschelt and Heider on Invertebrate Embryology, hardly any serious endeavour has so far been made in this country to review the fresh data or to revise or enlarge the general conclusions drawn by Balfour.


It is true, of course, that several admirable text-books of Vertebrate embryology have been issued, among which those of Milnes Marshall, of Minot in America, and of Bryce are particularly worthy of mention, but these are all directed primarily to the needs of the medical student and are consequently somewhat limited in their scope.


It would seem, therefore, that the hour is ripe for a re-statement of the facts and a renewed examination of the problems that they raise, and the object of the present work is to supply this want, if only for one group of animals, the Vertebrata.


The Vertebrates have, however, provided the material for so many investigations that much may be learnt of the general questions alluded to from them alone.

But modern research has by no means been restricted to the inquiry into the first stages of development.

Thanks very largely to the splendid labours of Hubrecht on the structure and development of the foetal membranes and placenta of the Mammals, a flood of light has been shed on much that was previously obscure in the early history of the human embryo.


The account of the general development of the embryo is therefore followed by a discussion of these embryonic organs, a discussion which I trust may be of genuine service to the medical man. No knowledge of human ontogeny can, however, be really sound which is not based upon and seen in the light of the broad facts of comparative embryology, and I hope that the earlier chapters will prove of value to the student of medicine as well as to the professed zoologist.


The detailed organogeny of the Vertebrates is outside my present aim, and must be reserved for a future volume.


The illustrations have been drawn especially for the book, with the exception of a few taken from my Experimental Embryology. Where the figure is a copy due acknowledgement is made.

At the end of each chapter a list will be found of the principal authorities cited ; the student who desires further information may consult the complete bibliography to be found in Oskar Hertwig's Handbuch der Entwicklungslehre der Wirbeltiere.


It is a pleasant duty to express my obligations to the Delegates of the Clarendon Press, in particular to Sir WilUam Osier, and to their Secretaries for the pains that have been expended m the production of this volume.

Contents

CHAPTER I Introduction

CHAPTER II Growth

CHAPTER III The Germ-Cells, their Origin and Structure

CHAPTER IV The Germ- Cells, their Maturation and Fertilization

CHAPTER V Segmentation

CHAPTER VI The Germinal Layers

CHAPTER VII The Early Stages in the Development of the Embryo

CHAPTER VIII The Foetal Membranes of the Mammalia

CHAPTER IX The Placenta


Historic Disclaimer - information about historic embryology pages 
Mark Hill.jpg
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)

Jenkinson JW. Vertebrate Embryology. (1913) Oxford University Press, London.

Vertebrate Embryology 1913: 1 Introduction | 2 Growth | 3 The Germ-Cells, their Origin and Structure | 4 The Germ- Cells, their Maturation and Fertilization | 5 Segmentation | 6 The Germinal Layers | 7 The Early Stages in the Development of the Embryo | 8 The Foetal Membranes of the Mammalia | 9 The Placenta | Figures

Cite this page: Hill, M.A. (2024, June 21) Embryology Book - Vertebrate Embryology (1913). Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Book_-_Vertebrate_Embryology_(1913)

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