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{{Historic Disclaimer}}
{{Historic Disclaimer}}
=Outline of Comparative Embryology=
=Outline of Comparative Embryology=
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Aute Richards
Aute Richards


Professor  0 7,00/ugy
Professor  of Zoology
Univrr.r1' 0 0/c/ahomc:
 
University of Oklahoma


New York
New York
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==Table of Contents==
==Table of Contents==
 
{|
Part One General Embryology
! width=300px|Part One General Embryology
! width=300px|Part Two Embryological Problems
|-
|
* [[Book - Outline of Comparative Embryology 1-1|Chapter I Historical Development of Embryology]]
* [[Book - Outline of Comparative Embryology 1-1|Chapter I Historical Development of Embryology]]
* [[Book - Outline of Comparative Embryology 1-2|Chapter II The Germ-Cell Cycle]]
* [[Book - Outline of Comparative Embryology 1-2|Chapter II The Germ-Cell Cycle]]
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* [[Book - Outline of Comparative Embryology 1-10|Chapter X Formation of the Mammalian Embryo]]
* [[Book - Outline of Comparative Embryology 1-10|Chapter X Formation of the Mammalian Embryo]]
* [[Book - Outline of Comparative Embryology 1-11|Chapter XI Egg and Embryonic Membranes]]
* [[Book - Outline of Comparative Embryology 1-11|Chapter XI Egg and Embryonic Membranes]]
 
|
Part Two Embryological Problems
* [[Book - Outline of Comparative Embryology 2-1|Chapter I The Origin And Development Of Germ Cells]]
 
* [[Book - Outline of Comparative Embryology 2-2|Chapter II Germ-Layer Theory]]
* [[Book - Outline of Comparative Embryology 2-3|Chapter III The Recapitulation Theory]]
* [[Book - Outline of Comparative Embryology 2-4|Chapter IV Asexual Reproduction]]
* [[Book - Outline of Comparative Embryology 2-5|Chapter V Parthenogenesis]]
* [[Book - Outline of Comparative Embryology 2-6|Chapter VI Paedogenesis And Neoteny]]
* [[Book - Outline of Comparative Embryology 2-7|Chapter Vii Polyembryony]]
* [[Book - Outline of Comparative Embryology 2-8|Chapter VIII The Determination Problem]]
* [[Book - Outline of Comparative Embryology 2-9|Chapter IX Ecological Control Of Invertebrate Larval Types]]
|}


==Preface==
==Preface==
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A. R.
A. R.


==Part One General Embryology==
{{Historic Disclaimer}}
 
===Chapter VI Types of Blastulae===
 
It is customary to say that cleavage continues from the fertilization
of the cell to the formation of the blastula. We usually think of a blastula
as a hollow spherical embryo consisting of a single layer of cells, and
indeed the most typical blastulae are so constructed. Actually, however,
there are many different forms of blastulae, of which the hollow, onelayered type is but a single one, and these different types of blastulae are
now to be .considered.
 
The different forms of blastulae occur as the end stage of many varied
cleavage processes, as has been seen in the foregoing sections. The
cleavage types are largely traceable to the amount and distribution of
yolk present in the egg, a factor which differs widely in the several
groups of animals. For the same reasons it is to be expected that the
different cleavage types will lead to difierent kinds of blastulae, and this
expectation is borne out. There are seven types of blastulae as follows:
coeloblastula, stereoblastula, morula, placula, amphiblastula, superficial
blastula, and discoblastula.
 
A. COELOBLASTULA
 
The simplest type of blastula is that known as a eoeloblastula, the
kind having a cavity at the center. Coeloblastulae may be further subdivided, depending upon the size of the segmentation cavity and upon
the relative sizes of the cells. They include both equal and unequal
blastulae, distinguished as to whether the cells are of uniform size
throughout the embryo, and each of these is again of two distinct subtypes, depending upon the size of the blastocoele cavity. If the altitude
of the cells is low so that they resemble a sort of cuboidal epithelium,
then necessarily the cavity is very large, and we have the simplest type,
the equal eoel0blastula—the one with which we are most familiar, since
it occurs in amphioxus. If, on the other hand, the altitudes of the cells
are greater than their breadth, the cavity is correspondingly reduced;
there is still a blastocoele but it is very tiny and is surrounded by a very
thick cell wall (consisting nevertheless of only a single layer of cells).
This occurs in Sagitta, a member of a group closely related to nematodes.
 
Usually in the equal coeloblastulae the cells are about the same size
 
91
92 TYPES OF BLASTULAE
 
and in about the same condition. Very evidently the equal coeloblastula
is a type in which there is very little differentiation among the cells of
the embryo as the cells are in approximately the same condition and
of about the same size. Those at the vegetative pole usually show a
slight size difference because of their content of yolk, but these cells do
not have much yolk and the distinction is not very great.
 
Equal coeloblastulae occur in the following groups but do not include
all members of these divisions. They are found in coelenterates, in
nematodes, Sagztta, echinoderms, Phoroms, brachiopods, Balanoglossus,
and amphioxus. It will be seen that these forms have equal cleavage
which is mostly radial or bilateral cleavage. (The spiral type, however,
does not entirely lack the coeloblastula, and there are a few annelids
 
 
fiG 57 Blastula of amphioxus. Fm 58 (‘oc[0b1astu1,; of 30,.
(After C0I‘f0flWm0) mtta (Redrawn from Korsehelt
and Heider, after Hertwig )
 
which rather closely approach the coeloblastula type.) Gastrula formation in types having coeloblastulae is usually by invagination; however,
the method to be discussed presently, polar ingrowth, sometimes applies
to this type.
 
The unequal type of coeloblastula is derived from the equal, with
increased difference in size of the blastomeres at the animal and vegetal
poles. Those at the animal pole are shorter than those at the vegetal pole.
The blastocoele is not often very large and, owing to the larger size of
the vegetative cells, it is pushed into the animal hemisphere. Eggs of
this kind are characterized by a more sharp differentiation between yolk
cells which are to form endoderm and animal cells which are to form
ectoderm. The eggs are mostly spherical, sometimes a little elongated,
and because of the difference in yolk content variations appear, just as
in the equal type of coeloblastulae; among them are variations in the
thickness of the wall, and in the size of the cleavage cavity.
 
The unequal coeloblastula is widespread in eggs which cleave spirally.
STEREOBLASTULA 93
 
Therefore we should expect to find it in the polyclads, annelids, molluscs,
Bryozoa (fig. 59) and among the holoblastic eggs of vertebrates (fig. 26).
The blastulae of vertebrates can readily be distinguished from the other
types, for in them we always find a great many cells in the wall. In the
vertebrates, epithelium is differentiated into many layers of cells. It is as
if this differentiation that is characteristic of adult vertebrates makes
itself felt even in the cleavage stages, so that the wall of the blastula
consists of many cells, and each germ layer, ectoderm and endoderm, is
several cells thick. This characteristic is clearly seen in the amphibian
type, the frog and salamander, with such modifications as the difference
in yolk would involve. Unequal coeloblastulae are derived from unequal
 
.\l7i/"
silt»
 
 
fiG 59 Unequal eoeloblastula fiG 60 Equal stereoblastula
of flustrella hzsmda (Redrawn of Lucernaruz (Redrawn from
from Korschelt and Herder, after Kcrsehelt and Heider, after
Pace) Bergh)
 
total cleavage. Gastrulation is commonly through invagination, although
polar ingrowth and epiboly also are found in these eggs.
 
B. STEREOBLASTULA
 
The stereoblastula (the term means a solid blastula) is obviously
derived from the coeloblastula, and may be equal or unequal, depending
upon whether it is produced from the equal or unequal type of c0eloblastula. If the cleavage cavity in the type of equal coeloblastula with
small blastoeoele continues to be reduced until it vanishes, we have the
equal type of stereoblastula such as is found in Lucernarza. With increase
in volume of cells and decrease in size of blastocoele we get a stereoblastula.
 
More common than this, however, is the unequal type of stereoblastula
such as we find in Crepzdula. The unequal stereoblastula is derived
through unequal cleavage and may occur either in the spiral types or the
more extreme of the bilateral types. Gastrulation regularly occurs in this
94 TYPES OF BLASTULAE
 
type by epiboly. The spiral types lead easily to this type of blastula
in which by continued growth the ectoderm cells will surround the
endoderm cells and so form a gastrula by epiboly.
 
r C. MORULA
 
A second type of blastula in which there is no blastocoele is the morula.
It was formerly customary to include this stage in almost all the types;
that is, it was said that the morula followed the 16-cell stage, and in the
strictly radial type there is some reason for that description, but we do
not speak now of a morula stage. However, in some types there are
formed blastulae which can best be described as morulae or solid blastulae. In Clava we have an example of the solid blastula which illustrates
the difference from the stereoblastula type, for inside the morula there
are cells, whereas in the stereoblastula there were no cells which did not
 
 
fiG. 61. Unequal storeoblustulu of Crepidula. (After Conklin.)
 
have a boundary at the surface of the egg. Superficially the two are quite
alike, but actually there is an important distinguishing feature. The
morula is produced by a characteristic shifting of the spindle position
during cleavage. In all the other cases that we have dealt with the
spindle may be said to occupy a paratangential position; the result is
that the new cleavage plane divides the cell in such a way that part of it
touches the surface and part the center of the egg. However, the morula
comes about by a shifting of the spindle to a radial rather than a paratangential position, and the result is that some of the daughter cells
touch the surface and others are only in the interior of the egg. So the
morula, although superficially similar to the stereoblastula, is really a
distinct and different type. Morulae occur chiefly in coelenterates.
 
D. PLACULA
 
The placula presents another kind of modification which has been
produced from the equal coeloblastula. Let us suppose that, instead of
SUPERfiCIAL BLASTULA 95
 
the cavity vanishing, the egg is compressed from the animal to the vegetative pole. The result would be a flattened blastula consisting of two
plates of cells. This is the placula and is found especially well developed
in the ascidians and to a less extent in the nematodes. The edge of the
placula corresponds to the equator of the coeloblastula, the upper layer
 
of cells to the animal hemisphere, and the lower layer to the vegetative
hemisphere.
 
 
Tie. 62 Morula of (‘lava 9qua- fiG 63 Placula of Cynthia pamta (After
mam (Redmwn from Korschelt and Conklin)
Heider, after Harm )
 
Gastrulation takes place by two different methods, epiboly and the
sinking in of the flattened plates; that is, it is accomplished by a combination of epiboly and invagination.
 
E. AMPHIBLASTULA
 
The amphiblastula of the sponge is of somewhat different type. This
structure was first described by Haeckel for the free-swimming larval
stage of calcareous sponges, and hence does not strictly correspond to
other blastulae which we have described. This larval form, however, is
usually spoken of as an amphiblastula. The cells at the animal half are
very sharply distinguished by their small size and ciliated covering from
those in the vegetative part of the egg. This type is not particularly
important although it is necessary to include it.
 
F. SUPERfiCIAL BLASTULA
 
The superficial blastula, or periblastula, is characteristic of those
forms having superficial cleavage, an example of which is the crab,
Dromza (figs. 36f and 37d). The result of superficial cleavage is the
formation of a layer of cells around the inner yolk mass. There is no
blastocoele and it is usual to say that the blastocoele is occupied by the
96 TYPES OF BLASTULAE
 
yolk mass. But the case is not quite so simple. Actually it will be recalled
that the superficial cleavage resulted in the formation of blastomeres
which at first were continuous with the yolk at their inner end. These
blastomeres presently are completely out off, a protoplasmic blastomere
being separated from the yolk-laden inner mass. Their inner ends, or the
outer part of the yolk mass, therefore, is not homologous to the cavity.
It is only that very small part of the mass which was never segmented at
all which is homologous to the cavity.
 
Reference has already been made to the role of the yolk cells, the
vitellophages within the yolk mass Some of the nuclei during cleavage
remain behind and are presently to be described as yolk cells for they
 
 
fiG 64. Amphiblastula of Sycandra mphanuv (Redrawn from Korschelt and Helder.
after Schulze )
 
digest the yolk. In this process the yolk becomes divided into areas
around these nuclei, a process of division which is often spoken of as the
yolk cleavage. But by some these nuclei are regarded as endoderm.
If this latter VIOW is adopted, there would be no such thing as a superficial blastula because the embryo would consist mostly of two cell layers,
the outer being ectoderm, and these internal yolk cells endoderm. This
designation of these cells as endoderm has not, however, come into
general use. Rather we say that the superficial is a true blastula.
 
G. DISCOBLASTULA
 
finally we have the discoblastula, the end stage of the eggs having discoidal cleavage. It is derived from the unequal coeloblastula (fig. 52)
upon the assumption that the yolk becomes so abundant and so dense as
DISCO BLASTULA 97
 
to hinder quite completely the separation of the cells in the vegetative
half of the egg. Recalling that discoidal cleavage occurs both in the
vertebrates and invertebrates we should say at once that discoblastulae
are of two sorts, the vertebrate type (fig. 55) and the invertebrate
(fig. 44); the latter consists of the single layer of cells which is found in
all invertebrates having diseoidal cleavage in contrast to the former
which is of many cells. Usually in all types having discoidal cleavage
there are some cells, perhaps around the edge of the disc or perhaps
elsewhere, which are continuous with the yolk. These cells, however,
usually do not take an active part in the formation of the body of the
embryo. In the vertebrates these cells are designated as the periblast or
the yolk sac endoderm. In the cephalopods they are the blastocones.
Gastrulation is usually by the limited type of invagination, invagination
taking place in one segment of the disc only.
 
These are‘ the different types of blastulae. They are obviously related
by the differing types of cleavages and they lead us to the different types
of gastrulation which is the next step in the development of the animal’s
body.
 
BIBLIOGRAPHIC Nora
 
Among the more important accounts of the subjects contained in this chapter
are the following: Korschelt and Heider, Minehin, Maas, Hertwig, Wilson, Conklin,
Schultze, Brauer, Whitman and Eyclcshymer, O. Herting, Ziegler, Brooks and Bittenhaus. These works are cited in full in the bibliography on page 406.
 
 
===Chapter VII Endoderm Formation===
 
I. METHODS OF GASTRULATION
 
After the formation of the blastula, which in its simplest condition
is a spherical mass (usually hollow) of more or less undifferentiated
 
 
   
 
\\
 
I
 
 
 
is
 
 
 
fiG 65 Two stages in the gastrulation of Terebratulma septentnonalts (After
Conklm.)
 
cells, the next stage in the development of the embryo is the formation
of a gastrula. The gastrula develops
from the blastula by the differentiation of two layers of cells, an outer
or cctodermal layer, and an inner
or endodermal layer. From the
eetoderm develops the nervous
system and the outer parts of the
future animal, and from the endoderm comes the lining of the
alimentary canal.
 
There are several different types
of gastrula formation, depending
partly on the type of blastula preceding the gastrula. We shall consider
each of these types and describe its
method of formation.
 
A. EMBOLIC GASTRULATION
 
The best-known type of gastrula
is the embolie or invaginate gastrula.
Gastrulae of this kind occur in embryos with total cleavage, resulting
in cells of either equal or slightly
unequal size. The blastula resembles
 
a. hollow sphere whose wall, except in vertebrates, has a. thickness of one
cell. A blastoeoele cavity is often, though not always, present inside
the sphere, but sometimes it is quite restricted, as in Terebratulina,
a. brachiopod which has a thick-walled type of coeloblastula. The cells of
the blastula are often wedge shaped, with the wedge narrowing inwardly.
 
98
EMBOLIC GASTRULATION 99
 
In one part, the vegetative half, the cells are typically larger than elsewhere, and sometimes markedly so.
 
The first sign of gastrulation is a slight flattening of the vegetative
region. This flattening gradually deepens and the resulting gastrula has
the appearance of a rubber ball which has been pushed in at one point
by pressure with a finger. The inpushing of the cells at the vegetative
pole continues until this invaginated layer lies close to the cells of the
outer wall. In this way a two-layered gastrula is formed and two cell
layers are differentiated. The outer or ectodermal layer covers the
gastrula and is continuous with the inner or endodermal layer at the
 
 
fiG. 66. Gastrula of amphioxus. (After Cerfontaine.)
Oriented with respect to the future embryonic axis.
 
point of invagination. Between the two layers there remains for a while
a cavity which is the remnant of the segmentation cavity or blastocoele.
The blind cavity, which communicates with the outside through a single
blastoporal opening and which is formed by the inturned cells as the lip
of the depression gradually narrows, is the primitive gut cavity, or the
archenteron.
 
It will be seen at once that the conditions in an invaginate gastrula
closely resemble those of the adult coelenterate which has two cell layers
and whose gut has a single opening to the outside. However, it is to be
noted that in only a few coelenterates are the gastrulae formed by
invagination, and that the same result in these forms is attained in
another way.
 
The mechanism which causes invagination has been attributed by
different workers to different causes. Rhumbler regarded it as an active
100 ENDODERM FORMATION
 
attempt at migration by the cells of the vegetative half, a process which
in the last analysis is to be attributed to chemotactic influences. If this
explanation is correct, then the migration of the endodermal cells must
be connected with a change in surface tension at the boundary between
the endoderm and the blastocoele content, especially in the region of the
cells which undergo invagination.
 
Some of the causes which play a part in the invagination may be the
following: (a) Differences in the rate of growth between the ectodermal
and endodermal portions of the blastodcrm by which a lateral pressure is
exerted on the endodermal plate. (b) Resistance of the closely pressed egg
membrane, so that the surface increase of the blastodcrm is possible only
internally. This factor is probably not often effective, for in many cases
the egg membrane appears pushed away by the pcrivitelline fluid and the
blastocoele is not an empty cavity but is filled with fluid which would
have to be displaced. (c) The constantly decreasing fluid of the blastocoele which perhaps exerts a sucking effect on the endodermal plate.
We must at the present time regard this factor as of doubtful occurrence and significance.
 
The size of that part of the old segmentation cavity or blastocoele
which remains after gastrulation may be very small, as in amphioxus, or
it may be quite extensive, as in the echinoderms in whose embryos the
primitive gut is relatively small. The fate of the fluid or gelatinous
content of the blastocoele is uncertain; some authors think that it is
resorbed by the endoderm cells. If this process could be satisfactorily
demonstrated it would be regarded as a causal factor in gastrulation.
 
A monaxial structure, with the axis from the middle of the blastopore
opening to the opposite pole, is characteristic of the early gastrula.
In many forms the gastrula becomes later bilaterally symmetrical as the
blastopore becomes narrowed and the gut laterally compressed. In most
coelenterates the monaxial structure remains.
 
A special type of gastrulation occurs in Lumbricus and the ascidians.
Here the blastula is a placula having a two-layered, plate-like structure.
Gastrulation is brought about by the hemispherical inbending of the
placula which then rounds out so that a complete sphere is formed. In
some cases there is an active increase by epiboly in the ectodermal cells
preceding invagination. This may be one of the causes for the invagination in placulae, but on the other hand the process may be due to the
same causes that lie back of typical invagination.
 
Invagination occurs in the following forms: some actinians, some
syphopolyps; Sagitta, Pedicellina, brachiopods; Phoronis, nemerteans;
echinoderms; some arthropods, as crayfish, Palimonetes; some insects;
many annelids, as Polygordius, Podarke, Eupomotus; some molluscs, as
EPIBOLIC GASTRULATION 101
 
Chiton, Dentalium, Dondersia; lamellibranchs, as Cyclas, Pisidium, Unio,
Ostrea; gasteropods, as Paludina, Planorbis; Balanoglossus, amphioxus;
the vertebrates in general.
 
It will be observed that this type of gastrulation is typical of primitive
forms. Hence it is most striking that very few eoelenterates belong to
this group. Invagination with a preceding placula includes the following:
some nematodes, some ascidians, some Lumbricidae. Many forms are
transitional between the type of pure invagination and the Dlacula type.
 
B. EPIBOLIC GASTRULATION
 
In the invaginate or embolic gastrula just described, the blastomeres
were approximately equal in size. In many other embryos, however,
 
fiG. 67. Gastrulation by epiboly in Crepidula. (After Conklin.)
 
there is a great difference in size between the small cells at the upper or
animal pole and the large cells at the lower or vegetative pole. The
small cells are called micromeres, and the large ones which contain
much yolk and are few in number are called the macromeres. In the
blastulae of embryos which have undergone this kind of cleavage, the
cleavage cavity is small or absent.
 
It is obvious that there is no room for invagination of endoderm cells
102 EN DODERM FORMATION
 
in embryos with practically no cleavage cavity. Gastrulation, which
cannot be embolic, occurs in the following way. There is a multiplication
of the small cells at the animal pole and an overgrowth or migration of
these cells down over the larger cells at the vegetative pole. These large
yolk-filled cells seem to take no active part in the process. The free edge
of the growing cap is called the blastopore, and the protruding yolkfilled cells, the yolk plug. When the overgrowth by the small cells is
complete, the blastopore usually closes and the large cells are enclosed.
The small, overgrowing cells are ectodermal and the large yolk cells
endodermal. A gut cavity is not present at first but is formed later by a
splitting and solution of the yolk in the solid endoderm cells. The cause
of epiboly, or gastrulation of this kind, has usually been ascribed to the
activity of the micromeres, but there is no evidence of a lack of activity
on the part of the large, inwardly migrating macromeres.
 
The part of the gut so formed is known as the mesenteron, for it is
the middle portion of the entire tract. The anterior end, or stomodaeum,
and the posterior end, or proctodaeum, are formed by ingrowth of the
ectodermal cells which later unite with the mesenteron so that there is
a continuous lumen through the gut.
 
There are many transitions between epibolic and embolic gastrulation.
If in the embolic gastrula the endoderm cells are larger and the lumen
of the invagination correspondingly smaller, then the gastrulation
approaches the epibolic type.
 
Epiboly is very widespread and occurs in all cases where the eggs are
sharply telolecithal and where there are, as a result, size differences of
the cells at the animal and vegetative poles.
 
Epibolic gastrulation occurs in ctenophores (fig. 14B), rotifers,
turbellarians, some molluscs, some annelids, and many crustaceans
including many parasitic copepods.
 
C. POLAR INGRESSION
 
1. Restricted Unipolar Ingression
 
In some cases of gastrulation there is neither a sharp invagination
nor an epibolic overgrowth. In these cases there is a total, unequal
cleavage, resulting in an embryo with a micromere cap resting on a few
large yolk-laden cells. The micromeres continue to multiply, and a
blastula is formed of cells of very unequal size; in it a well—developed
blastocoele is present. The large cells, never many, the common anlage
of mesoderm and endoderm, reach the interior not by invagination or
epiboly, but through their own active inward migration.
 
The mechanism by which the large cells get into the interior is little
MANY-CELLED UNIPOLAR INGRESSION 103
 
understood, and the term polar ingression is not adequately applied.
This method of gastrulation is often not sharply separated from either of
the preceding types.
 
The following forms have gastrulation by restricted unipolar ingression: some holoblastic Crustacea (some schizopods and Cladocera),
Ascaris megalocephala and other nematodes, and some molluscs (Patella).
 
2. Many-Celled Unipolar Ingression
 
In the ciliated blastulae of the coelenterates occurs a second form of
gastrulation by polar ingrowth. In it there is an elongated, oval or sausageshaped, free-swimming stage (called
a planula) which is really a blastula
with a large blastocoele and with thickened cells at the posterior pole. Here
there takes place the migration of cells
to a position within the blastula
which is responsible for a second type
of unipolar ingression. This migration
extends from the pole over the nearby
portion of the embryo. The cells which
first migrated into the blastocoele lie
isolated in the jelly contents but, later,
 
when migration takes place en masse, Fm. ex. Endoderm formation in ‘the
a plugof cells turns inward from the fgiggigfi 1;;j’;m”“,§,§r;$g;‘“;n';*8',§:§g;';;
posterior pole and gradually fills the after Patten.)
 
blastocoele. The migration of cells in
ward is not limited to the vegetative pole, but reaches to neighboring
parts. There is no interruption in the continuity of cells at the hinder
pole, and no gap in the outer superficial cell layer. At the end stage of
the gastrulation, there is an embryo with an outer superficial epithelial
layer and with a solid cell mass filling the interior of the larva. This
stage is variously called a stereogastrula or a parenchymella.
 
The formation of the gut cavity follows later by dehiscenee. A gradually widening split occurs in the interior of the endoderm cell mass and
later breaks through to the outside, forming the mouth. During this
process, the endodermal cells become arranged in a layer.
 
It will be seen that there is a close relation between gastrulation
by invagination and gastrulation by polar ingression. Both methods
might be regarded as modifications of one process. In the invagination
process a closed epithelial layer is shifted by infolding to the interior,
and in the ingrowth process the cells of the vegetative half pass inward
as a solid cell mass, later taking on an epithelial character, and develop104 EN DODERM FORMATION
 
ing a lumen. Metchnikoff concluded that the polar ingression was
brought about by a simple migration of cells without differential division.
 
There are transitional types between gastrulation by invagination
and gastrulation by polar ingrowth. In many forms, as in Aurelia aurita
 
fiG. 69. Endodenn formation by unipolar ingression in the plrmuln of Aequoria according to Claus. (Redruwn from Korschelt and Heider.)
 
and Eupomotus, there are invaginate gastrulae in which the gut lumen
is reduced to a very narrow split. If we think of the originally solid
invaginated mass as broken up into cellular parts, we have a picture of
 
unipolar ingression.
DELAM INATION 105
 
Examples of unipolar ingression are found in the following forms:
hydroids which have free medusae and whose eggs produce ciliated
swimming blastulae (Tima and Obelia), some anthomedusae, some
scyphomedusae, and some leptomedusae. This type of gastrulation is
widespread in arthropods.
 
3. Multipolar Ingression (Apolar Ingtession)
 
A process similar in many respects to the two types of polar ingrowth
just described and perhaps related to those types is that of multipolar
ingression. It differs from the preceding only
in the inward movement of a small number
of cells from several places instead of a single
one on the surface of the blastula. It might
be spoken of as apolar ingrowth as distinguished from that which proceeds from a
single restricted portion of the blastula.
However, since the processes are so similar
to those already described in this section it
seems desirable to assign this type to the
same division even if it presents some departures from the other cases placed here.
 
Multipolar ingression occurs in coeleblastulae when cells, few in number at first,
pass inside the embryo from various places
on the surface. The blastocoele is in this
way filled up with endoderm. The resulting
stage is a solidly built mass of cells like a
morula. It may be called a pseudo-morula,
differing from the typical morula in that
there is no differentiation of cells in the latter _ Fm. 70. Multipolar ingreswhereas here the endodermal cells, now a ?‘§:d‘?a$:”°;::f:‘§’Zg;;:fl“Z:‘§
solid mass, have already arisen by an inward Heider. after Metchnikofi.)
movement of some of the outer cells. The
gut cavity appears later inside the endoderm. Cases of this sort of
endodermal formation seem to be rare. The best investigated case is
that of Aeginopsis (Metchnikoff).
 
 
D. DELAMINATION
 
In the cases already studied, there was a separation of the inner
or endodermal layer from the vegetative pole, or from the vegetative
half of the embryo. There is, however, another type of endodermal
formation, common in coelenterates, in which there is no polar localiza106 ENDODERM FORMATION
 
tion of endoderm-forming cells, for in these the endoderm comes from
diffused parts of the embryo. The endoderm may arise in one of the
following ways: by migration into the coeloblastula from visible spots
in the embryo, by cutting off from the cell wall of the coeloblastula by
division, or, when the end stage of cleavage is a solid embryo, by histological differentiation of an epithelial outer layer from the parenchymous inner mass. There are many types which belong here. It will
be observed that multipolar ingrowth might from some points of view be
included under this heading. The term delamination has been used to
bring together processes of different kinds and is no longer a definite
term of definite meaning. Many of the forms intergrade with each other
through transitional stages. It is best to consider, under the head of
delamination, all cases of endoderm formation which are not derived
from invagination, epiboly, or polar ingression (including multipolar
ingression).
 
Delamination occurs in those forms whose embryos are set free late
in development either from spore sacs or from eggs with membranous
and gelatinous coverings. Many forms classified here belong to the
intergrading or mixed type of endoderm formation.
 
1. Coeloblastic or Mixed Delamination
 
When, in a coeloblastula, paratangential division planes which are
differential in character cut off single cells into the interior of the blastoeoele and these subsequently become arranged into a layer, coeloblastic
delamination may be said to occur. These inner cells constitute the
endoderm and at length fill the blastocoele. By dehiscence within them
the gut subsequently arises. In many cases of this mixed delamination,
there is a combination of the origin of endoderm by cell division and by
multipolar migration. Many of the hydroids, of which Hydra is the best
example, show this mixed delamination. Geryonia, the actinians, and
some syphomedusae have coeloblastic delamination.
 
2. Morula Delamination
 
In morula delamination, also called secondary delamination, cleavage
results in the formation of an embryo without a blastocoele, that is, in
one solid from the first. Early in cleavage there occur both radial and
paratangential division planes with no histological differentiation
resulting between the inner and outer cells. An embryo arising in this
manner is a true morula in which a cleavage cavity never develops.
Haeckel thought that the morula, the stage of solid aggregates of blastomeres, always preceded the blastocoele. But it is now well known that a
MORULA DELAMINATION 107
 
blastocoele cavity appears in some forms as early as the 4-cell stage,
and that true morulae, as the above, are formed only in certain cases.
In multipolar ingrowth and in coeloblastic delamination, the pseudo
fiG 71. Hydra embryo (Redrawn from Korschelt and Heider. after Brauer)
 
A, showing early migration of some endoderm cells inward and the origin of others
by cell division. B, a later stage in which the endoderm fills up the cauty
 
morula follows the blastocoele stage instead of preceding it, differing
from Ha.eckel’s description of a typical embryo.
 
In morula delamination, differentiation of layers follows the solid
stage of undifferentiated cells. In Clava (fig. 62) the cells at the surface
108 EN DODERM FORMATION
 
take on a prismatic character and lose their polyhedral shape. An
undulating line of separation is first formed between the outer or
ectodermal cells and the inner or future endoderm cells. The basement
membrane is later differentiated, and the inner cells connected with it
become epithelial. The cells adjoining them lose their yolk content and
take positions among the outer endodermal cells. The innermost cells
of the yolk mass finally liquefy and are resorbed, thus giving rise to the
gastrula cavity. The formation of a definite endoderm is accomplished,
and the planulae, now ciliated, swarm out.
 
Morula delamination occurs also in
 
Trachymedusae, Siphonophora, in alcyonians, Stauromedusae, and Cubomedusae.
 
3. Syncytial Delamination
 
Syncytial delamination occurs in those
coelenterates whose embryos show a
similarity to the superficial cleavage of
arthropods. In these embryos, only a few
cell boundaries may be seen, and there is
a solid syncytial inner mass, instead of a
morula stage. The ectoderm becomes
 
fiG. 72. Endoderm formation separated from the inner mass, which in
 
3;affggaogmgfgjgggigglzfiggg; part forms the endoderm and in part
 
layers by difierentiation. (Redrawn gradually is used up.
‘mm K°“°h°” '”‘d Held” me’ In Turritopsis there is at first total
Hum) cleavage, but in later stages the blastomeres
flow together and form a syncytium. In this case the syncytial nuclei
at the surface multiply, cell boundaries cut in and a delicate basement
membrane is formed. Differentiation of the endoderm comes later,
when its cell boundaries begin to appear. The primitive endoderm
cells are irregularly disposed, but later, when a split forms inside, representing the gut cavity, they are definitely formed into an epithelial layer.
In the hydrocorals, according to Hickson, there is no separation into
blastomeres and the embryo is a syncytium from the first, recalling the
cleavage of insects. Nuclear fragmentation of the first cleavage nucleus
has been described in these forms as the source of the nuclei of the
plasma islands, which arise, according to this account, from regenerating
chromatin particles. About the plasma islands cell boundaries appear,
and later the ectoderm becomes differentiated as a layer and development proceeds.
 
There is considerable doubt as to whether all the cases classified as
SYNCYTIAL DELAMINATION 109
 
syncytial belong here, as different authors give different accounts for
the same material and describe many doubtful processes. Some of their
 
fiG 73. Development of Turruopsts. (Redrawn from Korschelt and Helder, after
Brooks and Rlttonhouse )
 
A. morula. B, fusion 01 blastomeres, C, young planula Wltl) definitely formed ectoderm.
 
material may be improperly fixed, and a reinvestigation may furnish
more complete knowledge of their development.
Many hydroids probably belong in this group which develops by
 
syncytial delamination.
l 10 ENDODERM FORMATION
 
II. THE DISCOGASTRULA
A. VERTEBRATES
 
All the forms of gastrulae studied so far have eggs in which there is
not a great quantity of yolk. In those forms, however, which have a
discoblastula, a mass of yolk occupies the greater part of the egg and
 
Fm 74. Gastrulation in Petromyzan fluvumlis (Redrawn from Ziegler, after Goette)
A, B. beginnings of gastrulation, C, formation of an anlage of the medullary tube.
 
the protoplasmic part is limited to a small disc at one end. The inert
yolk is incapable of division and the protoplasmic disc alone undergoes
segmentation. Gastrulation usually takes place by the inturning of
the edge of the disc and the spreading out of this inturned layer between
the protoplasmic disc and the yolk mass. This inturned layer is the
endoderm and the two—layered embryo thus formed is a. discogastrula.
VERTEBRATES 1 1 1
 
The discogastrula lies on top of the yolk and spreads around it. The
edge of the embryo is the blastopore.
 
In order to understand this process of gastrulation thus briefly
described it will be necessary to take up at greater length the gastru
|IIIIIIIlIn.,,’
__....§
4"""lIIn\:
 
fiG. 75. Series of diagrams showing gastrulation. (After Ziegler.)
 
A, B. sections through embryos of an amphibian or a dipnoan in the stage of the circular blastopore; C, gastrula of a hypothetical intermediate between Amphibia and
Amniota; D, gastrula of a reptile. y., yolk plug; ec., eetoderm; bl., blastocoele; g.,
gastrocoele; m., medullary plate; d.. dorsal lip of the blastopore; s., subgerminal cavity.
 
lation of the frog (figs. 22, 51, and 74-76); although its egg has total,
unequal cleavage and gastrulation is therefore chiefly embolie, the study
of its egg enables us to interpret much better the conditions in a true
discogastrula. In the lower or vegetative part of the frog’s egg, the white
portion, there is an accumulation of yolk material; the animal half or
dark colored part of the egg, however, is not entirely devoid of it.
I12 ENDODERM FORMATION
 
Because of the small amount of yolk the animal half divides more
rapidly than does the vegetative half. Cleavage thus results in an
embryo with large and small blastomeres, the larger ones serving to
force the cleavage cavity nearer the animal pole. Between the pigmented
and the lighter portions of the egg is the gray crescent. The bilateral
arrangement of the egg substances is shown in some amphibia, but the
appearance of the so-called gray crescent which is similar to that of the
ascidians cannot always be made out.
 
fiG. 76. Development of embryo of Rana showing closure of blastopore, formation of
neural folds, and development of body form.
 
Invagination begins as a slit-like groove at the border of the gray
crescent somewhat below the equatorial region. The large amount of
yolk in the vegetative region prevents an equal invagination. The slit—like
invagination is the dorsal lip of the blastopore. The invagination
gradually extends to each side of the gastrula and the groove becomes
crescent shaped.
 
Previous to the invagination a change in the distribution of the black
pigment has occurred, for the small black cells have started to move
down over the white cells and the black pigment extends below the
equator. It will be seen at once that overgrowth, or epiboly, as well as
invagination, plays a part in gastrulation of the frog’s egg.
VERTEBRATES 1 13
 
The crescent groove follows the border of the pigment zone as the
latter gradually extends over the yolk and represents the dorsal side of
the egg. The ventral hp of the blastopore appears later, when invagination takes place there, and the blastopore then becomes circular. The
dorsal lip advances over the yolk more rapidly than does the ventral,
probably on account of the greater amount of yolk in the latter region.
The gullet, formed by invagination, is of a circular, s1it—like character,
and the yolk mass extends as a plug in the primitive gut lumen. As the
 
   
 
. B
Bio 77. Embryos of Rana A at time of first indication of gill slit, B, Just before appearance of external gills at time of hatching
 
ring-shaped blastopore grows together, owing to the greater downgrowth
of the dorsal lip, it draws down on the yolk plug and finally becomes a
small median, slit-like furrow. This process of the growing together of
the edges of the blastopore is concrescence We may then regard concrescence as a third factor in the gastrulation of the frog.
 
At first the dorsal, and later the ventral, blastopore lips become
differentiated with distinct ectodermal and endodermal layers. The cells
of the yolk mass, which have extended as a plug in the blastopore,
become pushed within as the blastopore grows together. We might thus
1 14 ENDODERM FORMATION
 
consider this kind as a solid cell ingrowth, perhaps a fourth factor in
gastrulation.
 
Four factors may be said to enter into the gastrulation of the frog’s
egg: invagipation, epiboly, concrescence, and a solid cell ingrowth.
 
a. Selachians. We may now contrast the selachian egg with that of the
frog. In the former, a protoplasmic disc rests on the top of the yolk
mass, and there is thus a sharp division between protoplasm and yolk,
instead of a gradual transition as in the frog. The disc—shaped protoplasmic mass of the selachian becomes furrowcd by cleavage planes, but
the yolk mass remains unsegmented. That part of the endodermal mass
of the frog which we have called the yolk plug must be represented in the
selachian by the uncleaved yolk mass. Although the yolk does not cleave,
in it are to be found scattered nuclei of various origins, but these nuclei
appear to take no further part in development. Some of the scattered
nuclei may be metamorphosed sperm nuclei, for polyspermy exists in
the selachians. A part of the nuclei originate from the peripheral cleavage
 
 
fiG. 78. Median section through the gastrula of Torpedo (After Ziegler)
 
cells and are called the periblast cells. These periblast nuclei are comparable to the eephalopod blastocones; that is, they are blastomeres not
cut off from the yolk mass by cleavage.
 
In the selachians the cell mass of the germ disc forms a many-layered
embryo which lies in a depression in the surface of the yolk. The cells
of this mass are at first round, indifferent cells, not arranged in an
epithelial layer. Between the cell mass and the surface of the depression a
space known as the germ cavity appears which may be regarded as the
cleavage cavity. It does not extend equally under the embryo, but is
pushed toward one side which corresponds to the hinder end of the
future embryo.
 
The first change in the germ disc of the selachian is the formation of
an epithelial layer from the superficial cells which become flattened and
broadened. This layer begins to form at the hinder part of the embryo
where the cleavage cavity is larger and the germ disc thinner and
spreads from this region over the whole germ disc.
 
Gastrulation begins as a depression at the hinder edge of the germ
disc where the cells begin to turn under. Thus is formed the primitive
gut cavity, lying between the inturned cells and the surface of the yolk
VERTEBRATES 1 15
 
which has previously become covered with so-called periblast. The
invaginating cells are formed from the round cells of the blastoderm,
spreading as an iris-like ingrowth from the edge of the germ disc and of
the growing epithelial endoderm. The invaginated gastrula cavity is at
first crescent shaped, comparable to that of amphibians, but with an
axial cavity in addition to the peripheral cavities of the crescent. The
edge of the entire germ disc may be thought of as a blastopore.
 
fiG 7‘) G1-«itriilitiam of the salmon. Salmo salar; ll. growth of the bl i-itoderm of
the salmon, (‘, emlirvonal shield stage, the germ ring covering one-li ilf of the yolk (After
Ziegler )
 
The anterior edge of the blastopore becomes extremely active and
begins to grow down over the yolk. finally it grows entiiely over the
yolk, passing over the vegetative pole, and reappearing behind the
embryo as the ventral lip of the blastopore. The yolk thus becomes
entirely covered and the blastopore eventually closes.
 
b. Teleosts. In the teleosts the process of gastiulation is essentially
similar to that in the selachians. The formation of the blastopore begins
at the posterior edge of the germ disc where invagination bi iiigs about
the origin of the primitive gut. There is a slight invagination at the
lateral and anterior edges also, and the yolk is finally enclosed by the
blastoderm, the anterior margin becoming the ventral lip of the blaste1 16 ENDODERM FORMATION
 
pore. In the elasmobranchs, teleosts, and also in the myxinoids, there
are two periods in the closure of the blastopore. During the first period
the overgrowth is practically limited to the dorsal lip, and the material
for the formation of the body of the embryo is produced. During the
second, the lateral and anterior margins of the blastoderm gradually
cover the yolk. Thus only the dorsal lip takes part in the formation of
the future embryo, while the lateral and ventral lips are entirely extraembryonic.
 
c. Reptiles and Birds. In all the vertebrates thus far described, the
Anamnia, the blastoporic lip appears at the edge of the blastoderm. In
the reptiles and birds, which have embryonic membranes and hence
belong to the Amniota, the blastoporic lip lies wholly within the blastoderm. The archenteric cavity is well developed only in primitive forms
and is usually represented only by the neurenteric canal. In most cases
 
 
fiG. 80. Gastrula of pigeon. (After Patterson.)
 
Thirty-six hours after fertilization. Section through the posterior portion of the blastodisc
showing the blastopore and its dorsal lip, d.b.
 
the upper layer or future ectoderm alone gives rise to the blastopore and
archenteron.
 
In the chick the blastoderm or germ disc lies on top of the yolk mass,
as in the fish. The endoderm is formed by an inturning of the germ disc
at the posterior margin and by ingrowth from the inturned portion. At
the posterior part of the germ disc the primitive streak is formed by a
linear thickening of the upper layer of the blastoderm. The endodermal
layer in the chick gradually grows around the yolk and the yolk sac is
thus formed. The ectoderm does not directly cover the yolk sac, however, as here conditions are complicated by the presence of embryonic
membranes, the amnion, which encloses the embryo, the allantois, and
the chorion.
 
In the chick the primitive streak represents the fused lips of the
margin of invagination and therefore is to be considered as the closing
blastopore. In the primitive streak the germ layers are fused, the differentiated part of the embryo being formed in front of it, the anus at the
posterior end, and the neurenteric canal at the anterior end. We must
o
 
 
d-b- v.b.
 
i J
fiG 81 Dlagram to Illustrate dxfierence between the blastopores of Annmnm and Ammcte.
(After Jenklnson )
 
a—c Closure of blastopore 1n frog or sxmxlar form Stlppled reglon 1s the blastoderm.
The edge of the blnstoderm represents the edges of the blastopore d-—f Ventral hp of blustopore xs absent m such a. form as Lemdoszren The heavy solld lxne represents the portlon
whmh forms the lips of the blastopore g, h Only a. small part at the postenor end becomes
the blastopore as In the Gymnophlona. The yolk remams uncovered 1. J The condxtlon
of the blastopore 1n Ammota The embryomc shleld IS darkly stlppled and Is equwalent
to the entxre blastoderm of the Anamma The ammote blustoderm extends further as
mdxcated by the hght stxpplmg
11 8 EN DODERM FORMATION
 
therefore consider the primitive streak of the bird as an elongated
blastopore since the relations are similar to those found, for example,
in the frog.
 
In the reptiles there IS a so-called embryonic shield at the posterior
end of the blastoderm. This IS a circular or oval area of columnar cells
resting upon a lower layer and surrounded by a region of flattened cells.
 
 
\
 
   
 
B C
 
fiG 82 Bali'our’s diagrams showing homology between bliistopore and the primitive
streak (After Ziegler )
 
At the posterior margin of the embryonic shield the two layers come
together A depression in the primitive plate appears here which is the
beginning of the archenteron, and its anterior margin is the dorsal lip of
the blastopore Lateral lips which are formed later turn back and fuse,
in some cases forming a vertical or even actual ventral lip, although cases
occur in which there is no ventral lip at all.
 
A mass of primitive cells surrounded by the dorsal and lateral lips
SCORPIONS 1 19
 
corresponds to the yolk plug. It will be seen that cells which are the
morphological equivalents of the yolk cells of the Amphibia are thus to
be found in the reptilian blastoderm. Here, as in the birds, the blastopore
arises inside the blastoderm and not from its edge as in the Anamnia.
The comparison of the Anamnia and Amniota can best be understood
by observing the development of the gymnophionan egg. Here the
blastoderm is an oval layer of columnar cells resting upon a partly segmented yolk. Only a part of the edge of the blastoderm at its posterior
end is converted into a blastoporic lip which is at first dorsal. Later the
lateral lips turn back around a small part of the yolk, and then join to
form the ventral lip. The anterior part of the blastoderm thus plays no
part in the formation of the blastopore. In this form the yolk remains
uncovered. We have seen that, in other Anamnia, the ventral lip develops
from the anterior edge of the blastoderm and the yolk is necessarily covered where_the blastopore closes.
 
The embryonic shield of the Amniota must be represented, in the
Gymnophiona, by the blastoderm, and the marginal zone of the amniotes,
together with the lower layer with which it is connected at the primitive
plate, must be represented by the yolk cells or nucleated yolk. It seems
natural to suppose that in the transition from forms like the Gymnophiona to the higher vertebrates, as the yolk material in the egg increased
in amount, segmentation has become restricted, not to the blastoderm
alone as in the fishes, but to the blastoderm and those adjacent and
subjacent cells which in the Gymnophiona are partly segmented from
the yolk.
 
These points may make it clear why the blastopore of the amniote
is formed inside the blastoderm but at the edge of the embryonic shield
which is really equivalent to the anamnian blastopore.
 
B. SCORPIONS
 
The discoidal type of gastrulation is not limited to the vertebrates
alone, for the scorpion and the eephalopod eggs are also of this type.
Gastrulation is of course dependent on the structure of the egg, and
an egg with a protoplasmic disc resting on a large yolk mass will belong
to this type, regardless of whether it is an invertebrate or a vertebrate egg.
 
The scorpion egg (fig. 39) is rich in yolk and the cleavage of the egg is
discoidal. In young stages there is found a small, one-layered cap on the
yolk. The blastoderm spreads gradually from this point and advances
over the yolk. Scorpion eggs, since they have cleavage of this type, are
comparable to eggs in which there is superficial cleavage with early
formation of the blastodisc on one portion of the egg only. The scorpion
condition is probably an extreme case and is to be traced back to the
120 ENDODERM FORMATION
 
type which is widespread among the arachnids. The scorpion egg,
therefore, represents a modification of the type common to its group
(as is also indicated by its viviparous mode of development).
 
The endoderm arises by the differentiation of the cells of the germ
disc which lie next to the yolk and form a regular epithelium. The
irregular cells which remain between the outer layer or ectoderm and the
inner or endodermal layer become arranged into two symmetrical mesodermal bands.
 
It will be seen at once that in the scorpions, as in the myxinoids, the
endoderm does not develop from the edge of the germ disc and thus
the edge of the germ disc cannot be regarded as the blastopore.
 
C. CEPHALOPODS
 
The cephalopod eggs are unusually rich in yolk and consequently
they are considerably larger than are the eggs of other molluscs. There
is a considerable difference in egg size throughout the group, but the
yolk takes up by far the most of the egg. The entire egg is covered
with a thin layer of protoplasm, which becomes thicker to form a disc
at the upper or future animal pole. The germ disc thus formed is
sharply marked off from the yolk mass.
 
The cephalopod egg is bilateral even before cleavage sets in. At the
part of the germ disc which is to become the anterior end of the embryo,
the disc extends farther down toward the equator. Since the cleavage
furrows pass into the thin layer of protoplasm surrounding the yolk,
the first cleavage cells and later the outer cells of the disc, the blastocones,
are not cut off from the peripheral protoplasm. The germ disc spreads
out and increases in size, at first chiefly at the expense of the formative
yolk with which the blastocones are connected. The germ disc, one cell
in thickness and covering only a small part of the egg, becomes thickened at the periphery as it spreads. When the cleavage cells have
increased to a considerable number the peripheral blastocones become
detached from the germ disc. These cells, according to Vialleton, wander
beneath the germ disc and become arranged into a layer which spreads
over the food yolk, forming a yolk epithelium. The exact origin of the
yolk epithelium seems still to be in doubt. Some say it originates from
the nuclei within the yolk, others from cells of the germ disc itself. The
origin of the layer need not be of very special concern to us at this
time, for the yolk epithelium, though it surrounds the yolk mass, does
not become the endoderm.
 
While the yolk epithelium is forming and the edge of the germ disc
is becoming thickened, the outer cells of the disc increase rapidly (fig.
44). This outer layer extends gradually over the whole egg (and thus
CEPHALOPODS 121
 
covers the growing yolk epithelium) and forms the ectoderm. These
two layers, the ectoderm and the yolk epithelium, are soon followed by
a third or middle layer, which also covers the yolk. There are thus two
definite regions in the egg at this time, the germ disc which forms the
embryonic rudiment, and the yolk sac composed of three layers.
 
The function of the yolk epithelium is to form an envelope for the yolk
and to make it available to the embryo. In later stages this envelope
surrounds the yolk as in the earlier development. There gradually
forms an outer yolk sac of part of the yolk not covered by the developing
embryo, and an inner yolk sac of that part which is embraced by the
embryo’s body; the latter remains always connected to the outer yolk
sac, but the connection becomes restricted to a narrow duct. The
external yolk sac evidently passes on its contents to the internal sac and
then the nutritive material is conducted to the embryo from the inner
yolk sac by aid of the yolk epithelium. This seems the most logical
method of absorption, for there are no known vessels in the external sac.
 
The extension of the germ disc over the yolk varies greatly in different
cephalopods. In Sepia the germ disc is very small and the yolk sac very
large. In forms like Loligo and Octopus the external yolk sac is more
reduced and the embryo contains the greater part of the yolk. Grenacher
studied a form in which there was scarcely any external yolk sac and
at an early stage the small yolk mass was enclosed by the embryonic
rudiment.
 
We have seen how the yolk sac and germ disc are formed and how
their outer layers become ectodermal. We have still to describe the
method of formation of the endoderm. About the time when the first
rudiments of organs appear externally in the embryo, there may be
seen, next to the yolk, an epithelial plate of only a few cells. It is the
first indication of the enteron. It soon increases in size and becomes
sac like, finally separating from the yolk. The yolk epithelium, previously lacking at this point, now grows under the enteron. The origin
of the endodermal plate thus described is probably from the thickened
peripheral mass at the edge of the germ disc which evidently represents
meso-endoderm. The whole process is thus to be regarded as a much
modified invagination, and the edge of the germ disc is the blastopore
filled by the large yolk plug, which also fills the whole enteric cavity.
 
BIBLIOGRAPHIC NOTE
 
Among the more important accounts of the subjects contained in this chapter
are the following: Korschelt and Heider, Conklin, Selys-Longchamps, Patten, Claus,
Lankester. These works are cited in full in the bibliography on page 406.
 
===Chapter VIII Mesoderm Formation===
 
Mesoderm is the layer between the outer epidermis and the midgut
epithelium. It produces the muscles, coelome, and the structures belonging to the coelome, all the body and intestinal musculature, the gonads,
the kidneys (except the Malpighian vessels) and the anlagen of connective tissue and blood vessels.
 
The concept mesoderm lacks a genetic unity throughout the animal
kingdom and is really a collective name, since the mesoderm has a
number of different origins within the same group. In spite of the lack
of genetic unity of mesoderm, the anlagen of mesodermal structures
have a common origin in single great groups of the rnetazoa. There is a
definite homology in the mesoderm of all forms with a spiral type of
cleavage, as turbellarians, nemertines, molluscs, annelids, and also the
arthropods. The mesoderm of all these forms is endodermal, arising
from the endoderm, and therefore the anlagen of the mesoderm bands
are in genetic unity. It is also true that the ectomesoderm or mesoderm
arising from the ectoderm of many forms is homologous. It is furthermore probable that the enterocoeles of echinoderms, Enteropneusta,
and chordates are of common origin.
 
I. ECTOMESODERM
 
We will now consider the different kinds of mesoderm formation.
Since the mesoderm is preceded by the ectoderm and endo(ler1n there
are only these two possible origins for the third layer. We will consider
first the eetomesoderm.
 
Ectomesoderm arises from the primary ectoderm and usually produces mesenchymatous muscle cells and connective tissue. This kind of
mesoderm occurs in the flatworms, rotifers, nematodes, annelids, and
molluses. Although the coelenterates are usually considered as two
layered, there is often present a third layer, mesogloea, which, though
not cellular, may be considered as eetomesodermal. In sponges, the
dermal layer contains both ectoderm and mesoderm (using the term in
a doubtful sense) and consists of (a) outer epithelium, (b) canal system
except the flagellated chambers which are not included here, (c) connec—
tive tissue, and (d) sex cells.
 
122
ECTOMESODERM 1 23
 
In coelenterates a distinction can hardly be made between ectoderm
and mesoderm. Although hydroids have only two layers, still the interstitial cells which are at the bases of the epithelial cells and which later
form the gonads may be considered as forerunners of the mesoderm.
 
In the Actinozoa, the distinction between ectoderm and endoderm is
more sharply defined than in hydroids. In the Alcyonaria, there is often
connective tissue with skeletal structure, and this layer is ectodermal.
The ectoderm becomes many layered, and a jelly substance is secreted
between the cells of the deeper layers which become separated from
each other. Thus two layers are formed, an outer epithelium and an
inner gelatinous layer which may be thought of as representing ectomesoderm.
 
In the ctenophores the mesoderm becomes more highly differentiated
histologically. A definite mesodermal layer is here present and this layer
is now known to be ectomesodermal in origin. Kowalevsky and Chun
found that the mesoderm originates from ectoderm in the region of the
gut. (See fig. 14B.) This is of particular interest because in forms with
the spiral type of cleavage the larval mesoblast originates in relation
to the blastomeres which produce the stomodacal invagination. In the
polyclads, according to Surface, the ectomesoderm produces chiefly
musculature of the pharynx.
 
Since the work on cell lineage, the development of annelids and
molluscs is more definitely understoo(l, and we now know that the part
of the mesoderm which is to become the mesenchyme of the trochophore
arises from the ectoderm. In all forms with spiral type of cleavage, the
first three quartettes form the ectoderm. Wilson has shown for polyelads that the mesoderm cells are formed by division of the cells of the
second quartette, and that the third quartette probably also shares in
the formation of mesoblast. The mesoderm formed in this way is the
larval mesoblast, the adult mesoderm arising from cell 4d as in molluscs
and annelids and therefore being endodermal in origin.
 
The relations in other flatworms, nernerteans and nematodes, is not
clear. In rotifers the entire mesoderm appears to be larval mesoblast
and some of this has been shown to be ectodermal. There are no mesoderm bands and the gonads come from primary endoderm and may
represent the mesoderm bands of related forms.
 
In a number of the annelids the ectomesoderm arises definitely from
three cells of the third quartette, 3a, 3c, 3d. The anlage is thus asymmetrical, being paired on the dorsal side, while on the ventral only the
left forms it. In some molluscs the ectomesoderm arises exclusively from
the third quartette. In Trochus (fig. 33, 34, Table p. 56) it arises from
3c and 3d from the dorsal cells of the quartette. In other forms the second
124 MESODERM FORMATION
 
quartette also contributes. Part of the body musculature of the annelids
is also known to be of eetodermal origin. The presence of ectomesoderm
in arthropods is not clearly shown.
 
Ectomesoderm produces connective tissue and larval musculature of
the trochophore larva. For annelids and molluscs it seems to be a provisional tissue degenerating upon metamorphosis. It is doubtful whether
the ectomesoderm produces excretory organs, but the kidneys of some
molluscs are known to be of ectodermal origin.
 
We have seen that ectomesoderm occurs in many coelenterates and
also in many groups which are near the trochophore type; these may be
collectively called Prostomia. Endomesoderm appears to be lacking in
the Molluscoidea. It seems striking that the entire group called Deuterostomia (composed of Enteropneusta, Echinodermata, and Chordata)
shows scarcely any ectomesoderm. Thus we recognize two great stems
of the animal kingdom, in so far as mesoderm formation is concerned.
 
II. ENDOMESODERM
 
We will now consider the formation of the endomesoderm, which
includes all the mesodermal structures in the embryo that come from
endoderm. Endomesoderm may arise as bands of cells, as hollow coelomic
pouches or through the coming together of mesenchyme cells. We shall
consider each of these cases separately under the following heads:
(a) Teloblastic mesoderm band formation. In these cases paired mesoderm bands take their origin from two primitive mesoderm cells as in
annelids and molluscs. (b) Secondary or derived mesoderm band formation. Those cases belong here in which paired mesoderm bands are laid
down without primitive mesoderm cells. They are often modifications
of the first type, since they occur among forms derived from annelids and
molluscs. Examples are arthropods and cephalopods. (c) Enterocoele
formation. The formation of coelomic sacs by outfolding from the
primitive gut characterizes this type. (d) Coelome formation by solid
ingrowth. Obviously this case is closely related to the foregoing type.
(e) Mesenchymatous coelome formation. The coelome is formed through
the coming together of mesenchyme cells.
 
It might seem natural to consider mesenchyme structures as different
from mesoderm. Mesenchyme is, however, not a genetically uniform
structure, but only a histological conception. It may arise by migration
from various places of origin: (a) from the coelome walls, (b) from the
primitive gut, (c) from the blastoderm of the coeloblastula, or (d) from
the reduction of the mesoderm band, as in molluscs. Mesenchyme cells
may come together and form a coelome as in the collar and body coelome
TELOBLASTIC MESODERM BAND FORMATION 125
 
of some tornaria. The multiplicity of the origin of mesenchyme shows
that there is no unity in the term.
 
1. Teloblastic Mesoderm Band Formation
 
In cases of teloblastic band formation, a pair of originally solid
mesoderm bands is formed by the budding of two terminally lying
primitive mesoderm cells. This type of mesoderm formation occurs in
forms with the spiral type of cleavage.
 
The two primitive mesoderm cells arise always from the 4d and thus
must be considered as primary endoderm, since the ectoderm is complete
with the third quartette and whatever comes from blastomeres arising
 
 
fiG. 83. Mesoderm of the snail, Physa. (Redrawn from Korschelt and Heider, after
Wierzejski.)
The four larger cells M“, M", M“, and M“ and three pairs of micromeres m‘, m1,
m3, give rise to the endomeeoderm.
 
later is to be regarded as endodermal. The two primitive mesodermal
cells are more nearly like endoderm than ectoderm in appearance, size,
and yolk content. This intimate relation of 4d to primary endoderm is
shown by the fact that, besides the primitive mesoderm, 4d often produces other cells which contribute to the formation of the midgut.
 
In most forms the third quartette is given off dexiotropically and 4d
by laeotropic division. The next division of cell 4d, now called M, is
again dexiotropic or simply bilateral and the two daughter cells are
symmetrical. Cell M, originally in the region of the endoderm plate,
early sinks inside the remnant of the cleavage cavity and cells M1 and
M 2 become symmetrically arranged. By these first divisions, small cells,
enteroblasts which take part in midgut formation, are formed. An equal
division of M1 and M 2 takes place and thus four large dorsal cells are
126 MESODERM FORMATION
 
formed, the two median ones of which, M 1’ and M?’-’, become the primitive cells of the mesoderm bands. The two other large cells in some forms
(pulmonates) have been said to give rise to the primitive kidney of the
trochophore, A series of divisions of primitive mesoderm cells now
follows and two rows of small cells are formed. These become surrounded
by the ectodermal products of the first quartettes.
 
In many yolk-poor eggs, as in oligochaetes, mesoderm bands are
formed very early before the beginning of gastrulation, and lie in the
blastocoele at the blastula stage. The mesoderm bands are at first
dorsal and produce cells ventrally. With changes of body form they go
through changes of position. The bands are given off horizontally and
become lengthened parallel to the prototroch. (See p. 127.) Since the
 
 
fiG. 84. Embryo of Crepidula. at the time of the closure of the hlastopore and the
formation of the stomodaeum. In addition mesodormal cells (In) and the gut cavity are
to be seen. (After Conklin.)
 
middle of the embryo is taken up by the gut they must bend, so both
become curved and form a right and a left curve lying in a horizontal
plane. When later the blastopore closes and pushes ventrally, the bands
shift and lengthen ventrally. The original large mesodermal cells soon
divide into smaller ones.
 
In annelids, the mesoderm bands break up later into segments which
hollow out and become coelomic sacs. From their walls develop the trunk
and gut musculature, gonads, and nephridia. Ectodermal cells, however,
often take part in the formation of the nephridia.
 
In molluscs, mesoderm bands do not elongate as in annelids. Early
in development they are lost in the mesenchyme and, according to one
author, produce only connective tissue and musculature while the
anlagen of the definitive kidney, pericardium, and gonads are from the
ectoderm. Subsequent authors indicate that, in some molluscs, kidney,
SECONDARY OR DERIVED MESODERM BAND FORMATION 127
 
gonads, and pericardium come from the mesoderm, bringing the later
development of mesoderm bands of molluscs more nearly in line with
that of the annelids.
 
2. Secondary or Derived Mesoderm Band Formation
 
In the arthropods, as in the annelids, we find a pair of mesoderm
bands. At first solid and sometimes single layered, these bands later
 
fiG 85 Diagrams of the development of Trochophorn showing the shift in position
of the mesoderm bands (After Korsehelt and Heider)
 
g, gut, t , teloblast cells, t b , teloblastic mesoderm bands
 
become segmented and coelomic cavities develop in them. We cannot
doubt the homology of the mesoderm bands of arthropods and annelids,
but the method of formation of these bands is very different. In the
few-celled embryo of the annelids, as we have seen, the combined anlage
of the entomesoderm sinks into the cleavage cavity as two cells, the
128 MESODERM FORMATION
 
paired mesoderm cells, and from them mesodermal bands develop.
These bands arise through teloblastic growth, by successive cell proliferation from the sides of the original mesoderm cells. In the arthropods, on
the other hand, the anlage of the mesoderm bands is many layered from
the beginning. From the moment that they may be recognized as separate cell groups no original mesodermal cells are observed and no teleblastic cells increase. Gastrulation in most of the arthropods is in the
form of a many-celled solid ingrowth. The ingrowing cells form the
primitive entoderm which spreads itself under the ectoderm as a so-called
under layer since it pushes up to the opposite side of the central yolk
mass. Now there is a division into an endodermal cell mass and into
paired mesoderm bands. These latter spread out and divide into segmented sections.
 
In some few arthropods there has been observed a special place of
ingrowth for the mesoderm. In the crustaceans, Astacus and Asellus, this
special place is the region of the forward blastopore lip; in Peripatus,
at the hinder blastopore region. Certain crustacea deviate from the
general scheme given for mesoderm formation in the annelids, because
their cleavage is more nearly total. In these forms (e.g., Branchipus)
there are paired mesoderm cells or cells which because of their position
and fate may be compared to paired mesoderm cells. They are similar
to the annelid type.
 
A teloblastic method of mesoderm growth is found in the isopods.
Here there is at the hinder end a cross row of eight teloblasts which
through division.produce the mesoderm of the metanauplius germ band.
There is here only a distant relation to the annelid type as the conditions are entirely different.
 
In the cephalopods there is no trace of the spiral type of cleavage and
cleavage is typically discoidal. The growth at the edge of the germ disc
leads to the formation of the endoderm. Later a cell ingrowth in the
hinder part of the germ disc takes place and this produces mesoderm
and gonad cells. Thus we see that the arthropods and cephalopods are
sharply contrasted to the annelids, for in many arthropods and in the
cephalopods the mesoderm originates from groups of cells rather than
from a single mesodermal cell anlage.
 
A consideration of the mesoderm formation of the Enteropneusta will
lead us naturally to the other chordates. The Enteropneusta form an
ancestral group through which the echinoderms are brought into connection with the chordates. In this small group different types of coelome
formation may be observed, the type of simple enterocoele formation
and the type of coelome formation by the coming together of single
SECONDARY OR DERIVED MESODERM BAND FORMATION 129
 
mesenchyme cells. Since all these types of mesoderm formation belong
in such a small genetic group of animals, they evidently must belong
together. Let us consider first the coelome of Balanoglossus. Here there
are, corresponding to the three body regions, three coelomic cavities;
the head, unpaired but showing by its two pores and incomplete mesentery a double nature, the collar, and the body coelornes. The latter coelome consists of paired spaces separated by a median mesentery. The
head coelome is known to be formed by the cutting off of a vesicle at
the forward end of the primitive gut, the end opposite the blastopore.
The water vesicle of the tornaria larva is the anlage of the head coelome.
 
There are several descriptions of the method of formation of collar
and body coelome. In those forms of
Balanoglossus which have no tornaria, but
develop directly, two pairs of gut diverticula become_ the collar and body coelomes.
In another form these two pairs of sacs
are cut off behind from the first-formed
coelomic vesicle, the water vesicle. Here
in a form without tornaria there is a
similarity to the formation of the enterecoele in most echinoderms which also
form an originally forward vesicle through
the fusion of three pairs of coelomic sacs,
the forward enterocoele, the hydrocoele,
and the hinder enterocoele.
 
In the New England tornaria the collar
coelome is formed by paired cell proliferations at the side of the stomach, the trunk F“, 86. Diagram of the coelome
coelome by solid evaginations of the intes- forrxxzmtion of Balanoalossus Kowalevtine. In the tornaria from the Bahamas, §aft'e‘;':n§°’s°h°lt and
on the other hand, these coelomic spaces
are formed at a considerable distance from the gut by aggregations of
single mesenchyme cells. In one form they arise from the wall of the
acorn coelome.
 
There are thus, in this one group of Enteropneusta, three types of
coelome formation: (a) through diverticula of the gut, (b) through cell
proliferation, (c) through aggregations of mesenchyme cells.
 
The second type is easily derived from the first, as solid cell proliferation is one step beyond a diverticulum. The third type differs, but may
be considered to fall into line if we think of the cells of a solid proliferation as having lost their connection and become scattered mesenchyme
 
cells.
130 MESODERM FORMATION
 
3. Enterocoele Formation
 
In the eehinoderms and also in amphioxus the coelome is formed by
outpocketings from the alimentary canal, that is, by the formation of
* an enterocoele. We must first consider the
 
inesoderm formation of echinodeiins.
 
In eehinoderms, niesoderm formation is in
general like that of Enteropneusta, by an
evagination of the ceeloinic sac fiom the
primitive gut. At the same time iiiesenchyine
cells migrate into the blastocoele. Mesonchyme formation may begin very early, even
before the beginning of gastrulation, or may
not begin until later. Following this process
there occurs in echiiioids and in Comatula,
at the place which will become the top of the
 
Fm 87 Diagram of the me_ primitive gut, a cell migration into the gelati
lgiimg forniation Km Cgnlnatulad nous blastocoele. By the time gastrulation is
ra n rom orse e 1; an - Hefdenvvufter Scehger ) completed, cell migration from the top of the
 
gut has already been going on for some time.
There are two types of coelome formation in the echinodeims. Com
atula is an example of one type. In this form the hydiocoele develops
 
 
"1
 
 
 
0 at
 
V
e h
CT2
mg 0 C2
3. mg
i
A B C
fiG 88 Metamorphosis of the coelome sacs in the eehinoids (A, B. redrawn from
Korschelt and Heider after Theel, C, redrawn from Korsehelt and I-Ieider after Bury)
 
a, anus, C1, left anterior enterocoele, 02, left posterior enterocoele, en, right anterior
enterocoele, crz, right posterior enterocoele, h, left hydrocoele anlage, 1. intestine, mg,
stomach, in, ectodermal mouth invagmatien, oe, oesophagus.
 
 
as an outgrowth of the forward part of the gut and the enterocoele as
 
outgrowths from the posterior part of the gut. The hydrocoele is the
anlage of the ambulacral system.
COELOME FORMATION BY SOLID INGROWTH 131
 
The other type of coelome formation in the echinoderms is illustrated
by the echinoids. In these forms coelomic spaces arise from the division
of an unpaired coelomic pouch given off at the top of the primitive gut.
This vesicle soon divides into right and left halves, each of which divides
again producing anterior and posterior right and left enterocoeles. The
anlage of the hydroeoele or ambulacral system develops from the left
forward enterocoele sac.
 
In chaetognaths and the brachiopods also we find enterocoele formation. Amphioxus must also be considered since its mesoderm is formed
as an enterocoele, paired diverticula originating on the dorsal side of the embryo and
later surrounding the gut. Hatschek thought
that there were primitive mesoderm cells in
amphioxus, and such cells are figured in
many text-books, but they do not exist. The
enterocoelous diverticula of the alimentary
canal occur shortly after gastrulation when
the embryo is lengthening. The notochord
forms on the dorsal side of the alimentary
canal by folding and is cut off lengthwise.
At the sides of the notochord are the two Fm. 89. Cross section of an
grooves at the anterior end of which paired inS:‘0‘:l“:)i;‘cff
evagmations occur. These evaginations are tion with the enterou. (Rethe anlagen of the segments and increase in    “"d
number as new ones are formed behind.
 
They become completely separated from the gut and form paired coelomic
sacs which are the primitive segments of the embryo.
 
 
4. Coelome Formation by Solid Ingrowth
 
In many cases the coelomic sacs are formed by solid outgrowth from
the gut. As already mentioned, the collar and body cavities of the New
England tornaria originate by outgrowths from the gut. There are similar cases among the eehinoderms, for in Ophiothrix fragz'l2's the two coelome anlagen have at first no lumen, and also among the brachiopods a
similar condition prevails. In the tunicates likewise mesoderm originates
as a solid outgrowth from the primitive gut.
 
The mesoderm formation of vertebrates may also be considered to
belong to this type. In the embryo of Triton there is at each side of the
notochord a small region of the gut from which coelomic sacs take their
origin. These sacs appear as two many-layered cell masses which push
in at the sides between the ectoderm and the entoderm. A split occurs
in each mass and thus is begun the separation between the outer somatic
132 MESODERM FORMATION
 
and inner splanchnic layers of the mesodermal sacs. The vertebrates do
not show the division of the mesodcrm into primitive segments from
the first, as does amphioxus, but the segmentation appears later in the
form of ring-shaped invaginations. Under the dorsal lip of the blastepore the invagination is deep and elsewhere it is hollow. The mesodcrm
formed near the dorsal lip is called the gastral mesodcrm, and the mesoderm formed all around the blastopore itself is called the peristemial
mesodcrm.
 
 
fiG. 90. Gastrula of Rana fusca. (Redrawn from Ziegler, after Schwink.)
ch, chorda anluge; ec, ectederm; en, endoderm. n1, mesodcrm, g, gastral cavity.
 
In the frog there is a trace of the outpoeketing of the endodcrm
to form the mesoderm sacs, for a groove occurs on each side of the
notochord so that the notochord endedcrm is separated from the lateral
endoderm.
 
In selachians mesodcrm formation occurs around the entire disc
edge. At the anterior region and on the forward parts of the lateral
edges the mesodcrm un(ler the blastocoele becomes split and later the
blood islands form here. In the more posterior region of the embryo
the mesodcrm is formed by ingrowth of cells from mesodcrm forming
grooves of the endoderm. One of these grooves is adjacent to the notechordal region and the other is peripheral. From these grooves groups of
cells grow into the peripheral blastocoele.
THEORIES OF THE ORIGIN OF THE COELOME 133
 
5. Mesenchymatous Coelome Formation
 
The origin of coelomic sacs by combination of originally free or
independent cells seems to occur. It has already been stated that Morgan
found this method of mesoderm formation to occur in the tornaria from
the Bahamas.
 
In general the mesoderm formation of Phoromls-, one of the Molluseoidea, is from scattered mesenehyme. Phoronis has an invaginate gastrula. At this stage single endodermal cells migrate into the blastoeoele
and become mesenehyme. This migration appears to be especially great
in the region of the edge of the blastopore. The mesenchyme cells which
are at first scattered in the blastecoele early show an inclination to lie
on the inner surface of the ectoderm,
and later on the gut endoderm. Thus
are formed the somatopleure and
the splanchnopleure.
 
It is doubtful whether or not such
a method of mesoderm formation is
 
fiG. 91. Oblique section through gas
prhnltiva We "light infer that Such trula of Phm-om's sahatieri. (Redrawn from
 
is the case since Morgan’s tornaria Iforst-halt and H_eidor. after Selys-Lomzfrom the Bahamas shows this kind cmnms) Sh°w‘(';§es_;'_"°s°n°hyme cells
of mesoderm formation and other
 
Enteropneusta do not. It may be, however, that a secondary change
 
has occurred in the matter of mesoderm formation.
 
III. THEORIES OF THE ORIGIN OF THE COELOME
 
A discussion of the origin of the mesoderm involves also a consideration of the origin of the coelome. We might define the coelome as a body
cavity lined by peritoneum from which arise the gonads. The tissue of
the coelome, as of all other mesoderm, must necessarily arise from the
ectodcrm or endoderm. We have already discussed the double origin of
the mesoderm, but have not yet considered the origin of the coelomic
cavity itself.
 
The theories of the origin of the coelome are of course hypothetical.
There are three main theories, the enteroeoele theory, the gonoeoele
theory, and the nephrocoele theory. The enteroeoele theory was first
suggested by Leuekart in 1848 in one of his first papers on the coelenterates. According to this theory, the coelome of higher forms is represented by the radial canals and gastric pouches of medusae. The gastric
cavity of coelenterates thus corresponds to both the gastric cavity and
coelome of worms and higher forms. This original idea was suggested
134 MESODERM FORMATION
 
long before Kowalevsky and Metchnikofi found that the coelome of
forms such as Sagitta, brachiopods, echinoderms, and amphioxus really
develops from gut pouches. The enterocoele or gut-po11ch theory was
taken up with enthusiasm by many, including Balfour and Lang.
Lang developed the theory, illustrating it by Gunda. He regarded the
metamerism of higher animals as resulting from the separation of paired
gastric pouches. Each diverticulum of the gut had perhaps originally the
task of producing genital products as well as the excretory function. As
the diverticula separated from the gut, new structures must be formed
to bear the functions of gonoducts or nephridia. Since the ancestry of
the vertebrates is so problematical, this theory as applied to them must
be largely conjectural. Lang finally gave up this theory for another.
 
This theory may be true as applied to the entcrocoelous or vertebrate
series of animals, but is evidently not true in the old sense as applied
to the teloblastic series of animals where the coelome is derived from a
pair of pole cells.
 
Hatschek is responsible for the gonocoele theory of coelome formation,
suggesting it in 1876. According to this theory, the pole cells of the teleblasts are primordial germ cells, and the germ band, in which the
coelome develops, is homologous to a gonad. Lang and others took 11p
this theory and assumed that the original ancestral type has essentially
the same morphology as a rotifer or flatworm. They suggested that the
original gonad cavity was still connected to the outside by the gonoduct.
Along with the extensions of the gonad cavity, a corresponding reduction
in the parenchyma took place and the walls of the gonad became partly
sterile, muscles developing in them. It is thus clear why the gonoduct
does not connect directly with the gonad, for since the walls of the
gonad are partly sterile, the eggs or sperm fall into the coelome and
are taken up by the gonoducts. This theory explains also the reduction
of the spaces in the flat worm occupied by the circulatory fluid. These
spaces are entirely outside the body cavity and from them are formed the
blood vessels. In some annelids there is a sinus-like blood system in at
least part of the body and this is regarded by Lang as a primitive
condition.
 
The nephrocoele theory is due chiefly to Ziegler, who regards the
coelome as primarily and originally an organ of excretion. This organ
consisted of a vesicle, the nephrocoele, and its duct. By its expansion a
modification of the coelome is produced.
 
These three views are not as sharply distinguished from each other
as might perhaps seem, since cases may be cited in which the coelome
functions in such a manner as to suggest all of them.
THEORIES OF THE ORIGIN OF THE COELOME . 135
 
BIBLIOGRAPHIC Non:
 
Among the more important accounts of the subjects contained in this chapter
are the following: Korschclt and Heider. See also note at end of Chapter VII, and
Hatschek, Wicrzejski. Buteson. These works are cited in full in the bibliography
on page 406.
136
 
Phylum
 
Porifera.
 
Coelenterata.
 
Ctenophora
Platyhelminthes
 
Annelida.
 
Molluscoidea.
 
TYPES OF INVERTEBRATE LARVAE
 
Larger Group
 
Hydrozoa.
 
Scyphozoa
 
Actinozoa
 
Turbellaria
Polyclads
Trematodes
 
Cestodes
 
Nemertinea.
 
Chaetopoda.
Gephyrea
Phoronidn
 
Polyzoa.
 
Brachiopoda
 
Larva
 
AMPHIBLASTULA
(Pseudogastrula)
 
Parenchymula.
Actinula.
PLANULA
 
SCYPHISTOMA (Hydratuba)
Scyphula
Ephyra
Strobila.
 
Arachnactes
 
Zoanthella _ _ _ . _ I . _ . _
Zoanthins.
Cydippid larvae
 
MI’JrLLEn’s Larva
Sporocyst, Miricidium, Redia, Cercaria.
Cysticercus
PILIDIUM
Larva of Desor
Tnocnopuonn
Mitraria
Trochophore
 
Actinotrocha.
Cyphonautes (Closely
related to trocho
phore)
(Related to trochophore)
 
TYPES OF INVERTEBRATE LARVAE
 
Type Genus
 
Sycandra raphnnus
 
Leucosolenia vari
abilis
Clathrina blancu
Tubularia
Most Hydrozon
Many Actinozon
Aurelia
 
Actinia urticinia
In family Cere:Lnthidue
 
Zoanthidac
Order Cydippidae
 
Planocera
 
Cerebratulus
Lineus
 
Phascolosoma.
Sipunculus
Phoronis
Mcmbranopnra
 
Terebratulina
TYPES OF INVERTEBRATE LARVAE 137
 
 
 
Phylum R Larger Group Larva Type Genus
 
'l‘ro<:l1clmintl1e.s Rotifora (Supposed to be per
sistent trochophore,
 
but early develop
ment is not in ac
cord with this view)
Cllrzetognzltlla (Fairly direct) Sagitta
AI'f_‘1I‘()])0dd. Crustncea NAUPLIUS A few schizopods
 
A few decapods
 
Metanauplius, Protozoaea, Zoaea, Calyptopsis, Copepodid,
Metazoaea, Mysis,
Phyllosoma, Mega—
lops, Cypris
 
Erichthoidina
Erichthus (Pseud0- Stomotopod
zoaea)
Alima
Insecta Larva, pupa, caterpillar (eruoiform)
Campodeiform
Mollusca Gastropoda Ctenophore stage Patella
TROCHOPHORE Drcissensia.
Lamellibranchia VELIGER Unio, Dreissensia
Glochidium
Echinodermata Asteroidea BIPINNARIA Asterias
Ophiuroidea Ophiopluteus Ophiothrix
Echinoidea. Echino- Pluteus Echinus
pluteus
Holothuroidea Auricularia Synapta
' Crinoidea Pentacrinoid Antedon
I’rotochordata Enteropneusta Tornaria Balanoglossus
Tunicata. Tadpole
oozoid
Cyathozoid
Ascidiozooid Salpa.
Trochozooid
 
Phorozooid
 
===Chapter IX Types of Invertebrate Larvae===
 
The development of the eggs of the many invertebrate animals shows
an amazing diversity in the methods by which the adult is reached after
the period of germ-layer formation has been passed through. In some
groups most complicated life histories involving adaptations to environments that are totally different from that in which the cleaving egg
found itself are present, while in other groups development is simple
and direct. Of these many types of invertebrate larvae it is possible to
describe only a few in this chapter. No attempt is made here to describe the cases of direct development as they occ11r in the various
phyla, but it is desired to explain how certain important invertebrate
larval types undergo their metamorphoses and reach the adult condition. In the table showing the occurrence of the Various types of invertebrate larvae these forms which are selected for description are indicated by small capitals, while the others mentioned are of less general
 
significance and are for reference.
 
I. THE PORIFERA
The Amphiblastula
 
The free—swimming larva which occurs in all families of the Porifera
is known as an amphiblastula. Its development has been investigated
in a number of forms, among the best known of which is Sycandra
raphanus (see fig. 64) studied by Schultze in 1875. Other important
studies are the series of papers of Maas on various sponges, and the
studies of Minehin on Leucosolenia.
 
The eggs are fertilized in the supporting jelly of the sponge wall, a
position which they occupy when ripe and where the early stages of
development are passed. (In Cliona, the boring sponge, the early stages
of development take place externally.) In a cavity near a flagellated
chamber which has a definite cellular lining the cleavage stages are
undergone, forming an embryo of characteristic appearance known as an
amphiblastula. At length the embryo emerges into the flagellated
chamber and thence passes to the outside to become free swimming.
After twenty—four to forty-eight hours of swimming about, it gradually
finds lodgment and attachment to a substratum, a process which is
 
138
THE AMPHIBLASTULA 139
spoken of as fixation, and which involves a complete and quite sudden
metamorphosis. In different genera of sponges the events do not all take
place in exactly the same order nor do the larvae reach the same degree
of advancement at the time of emergence or of fixation. The essential
principles of development are probably not dissimilar, however.
 
The free-swimming larva is at first an ovoid blastula in which there
are cells of two obviously different sorts. The large anterior portion
of the embryo is composed of flagellated cells and the posterior portion
of larger, non-flagellated, granular cells. Originally open at both ends,
the blastula soon grows so that the pointed end is closed and rounded
out and the cells become columnar in form and flagellated. The opening
at the other end is surrounded by the granular cells which upon its
closure take the form of a flat layer, some of whose cells proliferate and
presently push into the cavity. It is supposed
that the flattening is due to pressure against
the unyielding Inass of spicules, while the
columnar cells produce a swelling into the space
of the flagellated chamber adjacent. This is the
condition in which the embryos are extruded
to form free-swimming larvae.
 
In Leucosolenia, Minchin has described the
columnar cells each as differentiated into two
regions, a refractile portion at the internal end
and a sharply marked-off granular part at the
outer end‘. In living embryos the two.portions fiG 92‘ Amphiblasmln of
are so distinct as to give superficially the Sycandra. (After Schultze.)
appearance of an inner layer of refractile cells
covered by an outer granular layer of cells; they are, however,
merely parts of the same layer. Between the columnar and the
posterior granular cells of this form is a zone of intermediate cells
which are flagellated and entirely granular. The flagellated cells
are much more numerous but much smaller than the granular cells.
As development proceeds, the number of granular cells increases at the
expense of the flagellated ones.
 
The larvae of Leucosolenia are transparent so that a mass of yellowishbrown pigment at the center may be easily seen. This is shown by
sections to have the form of a tube open in front and behind, enclosing
a lens-like body of gelatinous character which fills the central, blasteaoelic space. The central cells are so arranged that Minchin regarded
this structure as a premature, light-perceiving organ of larval significance only. i
 
The free-swimming stage of the amphiblastulae is not of long duration.
140 TYPES OF INVERTEBRATE LARVAE
 
They remain at the surface for perhaps a day, then sink to the bottom
and after another twelve hours of swimming there they are ready for
fixation. fixation takes place at the anterior pole, the granular cells
growing about and enclosing the flagellated cells in the process of
metamorphosis. This process involves in some genera also the active
invagination of the flagellated
cells. At this stage only the two
kinds of cells may be distinguished,
the central cells appearing to be
thrown out with the pigment in
metamorphosis (Minchin). The
outer cells become the dermal or
covering layer, the inner the
gastral tissues.
 
Postlarval changes in both
layers now set in by which the
adult condition is reached. The
dermal layer differentiates and
two kinds of cells result, one
superficial, the other migrating
beneath the former. They differ
also in the type of spicules which
they are to secrete, the superficial
producing the monaxones and the
other the triradiate spicules. The
gastral cells take on a radial ar~
rangement, a cavity appears in
the center of the organism which
 
 
F10. 93.
 
fixation of the larx a of Sycandra
 
Iaphanus. (After Sehultze)
 
A, flagellated cells retreating into the interior; B, cup—shaped larva attached by
amocboid processes of the outer granular
layer, f.c., flagellated cells; g.c., granular
cells.
 
presently (in five or six days) dcvelops an opening to the outside,
the osculum, and becomes more
complicated. The cells themselves
elongate and assume the typical
 
collared appearance of choanocytes. The development of the pores and canals is a matter of slow
growth, involving the formation of pouches and the rearrangement of
cells, the secretion of spicules and gelatinous intercellular substance.
Other types of larvae have been described for sponges but they may
all be regarded as modifications of the amphiblastula type just described,
as was shown by Maas (1898). Some sponges also reproduce by formation of gemmules, but this is a process of budding and no free-swimming
larvae are developed.
THE PLAN ULA 141
 
II. THE COELENTERATA
 
The larvae of the coelenterates exhibit a considerable variation in
appearance in conformity to the wide range of adult conditions to be
met with in the phylum. Like the adults, the embryos have, in spite of
dissimilarities of form, a fundamentally common type of structure.
Numerous experiments into developmental possibilities seem to have
been tried out by the coelenterates with many diverse results, considering
the paucity of material and restricted structural limitations. The
structural simplicity is visible throughout the general similarities that
may be discovered in the different kinds of embryos.
 
1. The Planula
 
The typical eoelenterate swimming larva is a planula. It occurs in
nearly all_Hydroz0a (Tubularia is an exception) and in very many
 
 
and the character of the ciliated planula. (After Metschnikofi.)
 
Actinozoa and Seyphozoa. Because of its simple character and its widespread occurrence, an evolutionary significance as the ancestral coelenterate is suggested. It is the most important larval stage of this phylum.
 
The term planula was formerly applied to a blastula stage, but the
usage is now obsolete. The blastula develops by the migration of cells
inward, and by cell division into a two—layered, ciliated, swimming larva.
The outer layer is in the form of a ciliated, columnar ectoderm; the
inner is usually, in the Hydrozoa, a solid endoderm mass formed by
many-celled, unipolar ingressions. There are numerous cases in both
Actinozoa and Scyphozoa in which the endoderm is hollow. The gastral
cavity does not appear in the hydroids until about the time of attachment of the swimming larvae. In Pennaria the hydranths are not
covered by a hydrotheea; each has two circles of tentacles, one about the
142 TYPES OF INVERTEBRATE LARVAE
 
oral end and another at the aboral end. At the time of maturity a
row of medusa buds appears around the middle of each zooid which
gradually enlarges and differentiates into the somewhat reduced medusae
characteristic of the genus. These p1'0duce the germ cells and do not
become free until the sex products are shed. Sexes are separate. After
fertilization inside the bell of the medusa, the eggs are immediately shed.
The medusae are then free, and after a few hours of feeble swimming,
they die. In this genus the Inedusa is the less important of the two
generations. The fertilized egg as described by Hargitt goes through a
very irregular cleavage, forming an irregular cell mass which differentiates into a solid planula of two layers, the
outer ciliate(l. After perhaps twelve hours of
swimming about, the planula begins to settle
down and at length attaches to grow into a
new hydroid colony.
 
2. The Actinula
 
In some forms, notably Tubularia, an
intermediate larval form, the aetinula, intervenes between the planula and the attached
stage. It is neither fixed nor swimming, but
creeping, and is formed by the appearance
upon the planula of blunt protuberances, the
 
Fm 95_ Enema, features of tentacle buds, which gradually grow longer.
the various stages of develop- first appear the rudiments of the aboral
 
ment of the embryo of Tubularm _ - ,
mdmm (Rcdmwn fmmmlmen ) tentacles dnected toward the future aboral
 
A, plnnnln beginning to bud on end. The gastral cavity now is evident with
‘*b°ml t°"“1°1°5-B-CvA°“““l‘*e- thinned walls at one point where the mouth
ab.t., aboral tentacles; o.t., oral . .
n,nn,n1es_ opening Wlll presently break through about
 
the time when the buds of the oral tentacles
appear. The aetinula now escapes and creeps about on the bottom, oral
end downwards. It later tips over, attaches by the aboral end, elongates
rapidly and gives rise to the buds which are to form the different zooids
of the colony. Thus the aetinula larva is important as the ancestor
hypothecated by Brooks for the origin of the diverse kinds of coelen
terates.
 
 
3. Origin of Coelenterate Larvae
 
The grouping of the various members of this phylum depends upon
the presence and degree of development of two primary structural forms,
the polyp and the medusa. In the Hydrozoa both are present; in the
Actinozoa the polyp form is especially developed, and in the Scyphozoa
ORIGIN OF COELENTERATE LARVAE 143
 
the medusa. is the structural type. Within the Hydrozoa it is possible, as
is commonly done, to form a series with Cumna and Lmope at one end,
 
fiG 96 A, gonophores of Tubularuz mdwzsa containing embryos B, creeping Actinula
larvae, C, attached form of Tubularza, mdwzsa (Redmwn from Allman )
 
in which the hydranth generation is quite lacking, and Hydra at the
other end, in which there is no medusa. These forms are as follows:
 
Cumna, Lmope (meduszi only)
Gommwmus (very rndnnentary hydmnth ulternatmg with medusa generation)
‘ 144 TYPES OF INVERTEBRATE LARVAE
 
Obelia, Bougainvillea (medusa and hydranth alternating and of equal importance)
Pennaria (medusa fixed during sex cell stage, and of reduced importance)
Gonothryca
 
Tubularia (In these four cases the fixed medusa undergoes more and
Claw, Hydfactinia more reduction in structure and importance.)
Campanularia, female
 
Judendrium, Oampanularia, male (remnant of mcdusa bud)
Hydra (no medusa, hydranth only)
 
It is evident for reasons that need not be gone into here that the
evolution of this series cannot have been gone through from Hydra
toward Cunina. On the other hand to assume the medusa. to be the more
primitive form of the two types is hardly in keeping with obvious structural features, and for this reason it is not possible to regard this series
as having begun with a form similar to Cunina and to have been evolved
in the reverse order. Rather some such suggestion as that made long ago
by Brooks (1885) seems better adapted to the facts. According to this
suggestion the most primitive type is neither a medusa nor a hydranth,
but some small generalized form like the actinula. From this it may be
supposed that four, perhaps five, series of forms have been derived.
first there is the hydroid colony like Obelia in which both medusae and
hydranths are present in alternating fashion. The remainder of the
series from Obelia through Pennaria to Eudendrium and possibly to
Hydra may be derived from this hydroid by the gradual degeneration of
the medusa. A second series radiating from the actinula-like ancestor
produced Cunina and Aeginopsis in which no hydranth is present.
Perhaps a third produced hydra-like forms at the other end with no
medusae. The Scyphozoa and the Actinozoa are the fourth and fifth
series respectively which owe their origin to this primitive form of
coelenterate, the actinula—like form.
 
Of this form the planula is the larval type (fig. 94). It is the freeswimming larva common to all coelenterate groups. In some, the
Hydrozoa and many Aetinozoa, it is a solid mass of endoderm with an
ectodermal covering. In others, the Scyphozoa and some Actinozoa, the
endoderm is a definite layer with a gastral cavity. The latter is held by
some workers to be the more primitive of the two, for it is argued that as
the organisms were evolved an animal with a solid internal mass of cells
would be quite unable to support itself. An embryonic type developing
from stored yolk material would find no such difliculty, and so the solid
form of the planula was thought to be secondary.
 
The general plan of coelenterate embryology is now clear. The fertilized egg develops gradually into a planula which swims about for a
time and, it may be after intervening larval stages have been passed
SCYPHOZOAN LARVAE ' 145
 
through, settles down, attaches, and elongates into a hydra-like form
representing the hydranth generation. This may grow into a hydroid
colony or into the coral polyp or actinian, or go through further development processes to produce asexually a. rnedusa which in turn produces
new germ cells.
 
4. Actinozoan Development
 
In the Aetinozoa the development of the sea anemones is very similar
to that of the Seyphozoa up to a certain point. The planula is reached in
the usual manner. The early stages of
their development may be undergone in
the gastral cavity of the mother in some
cases, shedding of the embryos in the
gastrula stage or thereabouts occurring
through the mouth, or the eggs may be
discharged from the mouth and fertilized
among the tentacles or free in the sea
water. After the free-swimming period
the attachment at the broader end takes
place. At the other end a narrow pit
forms asthe beginning of thestomodaeum ;
it deepens and its lower end breaks
through, connecting the gastral cavity
with the outside. The subsequent history
is largely one of differentiation especially
of the mesenteries. Some special forms
of larvae occur in various subdivisions
of this group but the general features
are similar.
 
5. Scyphozoan Larvae
 
In the Scyphozoa the development of
Aurelia may serve as a convenient type. F1 G. 97.
 
_ _ . A, free-swimming plaThe eggs are shed 1nto the digestive nula of Aurclia aurita; B. section
 
through s(-yplustoma having four
 
cavity’ pass out through the mouth after tentacles. (Redmwn from Hein.)
 
fertilization to pockets on the inside of
 
the oral arms where they undergo those processes which lead to the planula
stages. Then they emerge and swim about freely. Histological differentiation continues, and the larvae are ready for attachment in four or
five days. After attachment the larva elongates and broadens out, the
mouth opening becomes widened and four tentacle buds appear between
which the taenolae, endodermal ridges projecting into the gastral
146 TYPES OF INVERTEBRATE LARVAE
 
cavity, develop. This larva with its flattened, broadly open, oral disc is
spoken of variously as a scyphistoma, scyphula, or hydra-tuba. Secondary tentacles develop between the original four and then continue to
form until the appropriate number is reached. After further differentiation, the process sets in which distinguishes scyphozoan development
from other types. It is the cutting off of its oral disc by means of a constriction around the scyphistonia to form an ephyra larva. This process
is known as strobilization and iii a well—fed scyphistoma may take place
repeatedly until a dozen or fifteen cphyrae are formed from the one larva.
 
 
1‘i(. ‘)5 iSti‘obiliz.it1on of Auiclia amila (Rednivm from Claus)
t, tentacles of strobila t..ie taeniolac, g fiist tiiuisx crsc giome, I, lobes of cphvi 1
 
The more usual condition is for each scyphistoma to produce two 01
three ephyrae. The constrictions appear piogressively later as they
pass down the lawn, and in the well—fed individuals the appearance of a
pile of saucers is ieadily suggested
 
The ephyra now continues rapidly its development and differentiation
leading to the form of the adult jellyfish. The scyphistoma tentacles aie
resorbed and in their place the characteristic lobes of the ephyra appear.
The oral cone lengthens into the manubrium and other changes occur
which result in the metamorphosis of the ephyra into the jellyfish.
 
III. THE PLATYHELMINTHES
 
Development in the flatworms presents many diverse aspects. Some
eggs undergo no metamorphosis but pass directly into the adult condiMULLER’S LARVA 147
 
tion. Others reach their final development only after passing through
 
‘the most complicated life histories, involving (lifferent hosts, totally
 
different environmental conditions, and totally different types of organization. Since it is not the purpose of this chapter to follow through life
histories, but merely to show the relations of types of larvae to embryos
and adults to which they are related, only meager reference can be made
to the group as a whole. One well-known form is Mul1er’s larva, the
 
S J ’ mo.
1 . p’
. (ix
;‘ W ‘ M
s.
., _,4 . _,,
< A
r- *7 _ Irv-W ‘_
gr. ,  { *
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Q.” T‘. ls;-,’..\ (‘if :r Jicm
« V’ 5, t'::7'\$\.«" ,‘ K3,,’
-* z ) ;,_ ‘ R» an,
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4
(' V
5.0.
A
B
 
ll(. ‘)0 \ smobilmd sn phisloxn L of Auului tlunla H uphv. 1 lll\ I. of Aurclirz mmta
tftu lll)(‘I‘Iil()n (l{e(lrmn from ( lms)
 
gf Lttslrlt hl um ms mu nmnth rl, \ uious ruli ll lobes of H1111-lll\(‘ an! ‘I n m 11gm ll sense org ins
 
free-swimming larva of the polyelad Tuibellaiia named after its discoverer, Johannes Muller.
 
1. Mii1ler’s Larva
 
The development of the polyclads is known chiefly from an older
study by Lang or Yungza and a later and more detailed investigation
by Surface on the embryology of Planocera mquzlma. The cleavage is
of the spiral type as found in such groups as gastropods and annelids‘.
The cell lineage is similar in the early stages and the localization of
formative substances surprisingly like that in the higher forms; the
similarity is especially surprising when it is remembered that the
Turbellaria agree closely with the etenophores in many points of structure Gastrulation is by the method characteristic of eggs with spiral
148 TYPES OF INVERTEBRATE LARVAE
 
cleavage, namely epiboly. An oval embryo with ciliated ectoderm and
endoderm results. The stomodaeum opens into a rather broad gastral
sac, in the wall of which are only small endoderm cells in place of the
large endomeres of an earlier stage. Mcsodcrm, ectomesoderm, and
ganglion cells are also present in the embryo of Planocera when it is ready
for escape from the capsule. Eight ciliated lobes appear at this time just
below the equator; these are the characteristic features of Mi'1ller’s larva.
 
Lang followed through the metamorphosis of Yungza in detail. The
position of the mouth shifts from the pole to the ventral side of the
 
 
Fro 100 A, B, C, dorsal, ventral, and lateral view; of free-swimming larva of Yunma.
(After Lang)
 
elongating larva. Symmetry is lost because of the inequality in the rate
of growth of the two sides of the larva. Of the eight lobes one is dorsal,
one ventral, and the others make up three pairs laterally placed, and all
are connected by a continuous ciliated band. Growth in length with the
gradual reduction of the lobes until the usual form of a flatworm is
reached brings about the external changes. Among the internal changes
involved are the development of eye-spots, the development of the
parenchyma (which fills in the interior of the adult, and of which some
cells differentiate into muscle cells), and the differentiation of the
brain and genital organs. The most marked changes, however, are those
MU LLER’ S LARVA 149
 
concerned with the development of the protusiblc pharynx. There is an
invagination of the larval stomorlaeum, H] which the pharynx arises as a
ridge-like thickening. The pharynx itself grows in length and the
stomodaeum becomes everted to form the sheath of the pharynx.
Surface records that the early cleavages as well as the maturation
divisions require about one hour each. By forty—eight hours small ectodermal cells cover the entire embryo, which become ciliated, and during
the third day rotation is set up in the capsule. Eye-spots appear about
the fourth day. By the end of the fifth day the ciliated lobes appear, and
 
 
Tm 101 A, B, dorsal and xentrnl news of l‘lI‘\ are of Yungm aurrmtzaca. in process of
metamorphosis (After Lang )
 
on the sixth the larva breaks from the egg membranes to become freeswimming. It swims for some time, eventually settling to the bottom
and assuming the shape and habits of a typical polyclad.
 
Some of the turbellarian larvae, owing to disproportional development
of some lobes, resemble fairly closely the pilidia of the nemerteans.
There is resemblance between this larva in turn and the trochophore
which Balfour thought was derived from it. Obviously, therefore, larval
forms of this group are of importance in working out the ancestral history
of invertebrate types, and by some the history is thought to run from
the etenophores through the turbellarian forms to the pilidium and
trochophore.
150 TYPES OF INVERTEBRATE LARVAE
 
2. Trematode Larvae
 
Trematodes are commonly divided into Monogenea and Digenea,
depending upon whether one or more than one host is necessary for their
development. Since only one host is necessary in the Monogenea, development is direct or nearly so, whereas in the Digenea there are often
several intervening stages. In the sheep liver—fluke, which may be chosen
as an example, the egg undergoes the early part of its development in a
chitinous shell while it is passing through the alimentary canal of the
 
 
flo 102 A B, same as above but older
 
sheep. After it has been passed from the body of the host it at length
escapes from the shell as a ciliated larva, the miracidium. This larva
swims about in water or moves over damp vegetation until it comes in
contact with a pond snail or perishes. It is said to be sensitive to the
presence of the snails and to move toward them actively. At this time
the larva is in many respects similar to a rhabdocoele turbellarian without gonads. It has nearly the shape of a slender cone with two eye-spots
near the head end (the broader end). There is a brain, a pair of flame
cells representing the excretory system, and an imperfect intestine.
The rest of the body is filled with germ cells. After the miracidium has
penetrated the body of the snail it loses its ciliated ectoderm, the
enteron degenerates, and it elongates into a sporocyst, which is thus
CESTODE LARVAE 151
 
merely a transformed miracidium.Within the sporocyst, germ balls*
are budded ofl" and each begins a development similar to total cleavage
to form a blastosphere which in its turn is converted into a gastrula. This
passes then into the larval type known as the redia. The redia is usually
looked upon as parthenogcnetically produced, and the alternation of
generations thus involved differs from that seen in eoelenterates in that
here a sexually developed sporocyst gives rise parthenogenetically to the
redia. In the winter the rediae produce other rediae in a similar manner,
but in summer they develop into another type of larvae, the cercaria.
The rediae differ externally from miracidia in the absence of cilia, of
eye-spots, and in the presence of a pharynx and a simple sac-like intestine, and their general shape is more cylindrical with a collar or circular
ridge near the anterior end and short locomotor processes near the posterior. The cercariae have in an undeveloped condition all the organs
which are found in the fluke and some other structures including a tail
which are of brief duration and last only during larval life. The cercaria
leaves the snail, encysts upon a blade of grass, and must be eaten by a
sheep to continue its development. Its final metamorphosis consists in the
loss of its tall, the rapid growth of the organs already present, and the
development of its reproductive organs.
 
Variations from this case occur; in some forms stages are omitted and
the cerearia may develop without a tail. The complication of two or more
hosts and an intermediate larva which reproduces paedogenetically
recalls the cases of polyembryony recorded in numbers of groups
throughout the animal kingdom.
 
3. Cestode Larvae
 
Cestode larvae and life histories are only a little less complicated and
involved than are those of the trematodes. The eggs of cestodes, like
those of the trematodes, are surrounded in the uterus by a thin eggshell. In some forms there are also included “yolk cells” which contribute
food to the developing embryo. Cleavage is irregular in type, although
characteristic features are to be recognized. An outer layer of cells is
formed from micromeres which separate from the larger cells early in
cleavage. In most cases this layer of superficial cells gives rise to a
chitinous coat which is thrown off ultimately. Only the central mass of
cells which is enclosed by the superficial layer takes part in the formation of the embryo. This mass of cells develops a series of six hooks and
becomes the hexacanth embryo. The development of the hexacanth
 
* There is reason to doubt whether these germ balls are true germ cells involving
a reduction of chromosomes in their development. If these are not germ cells then
the rediae are asexually produced and a true alternation of generations exists.
152 TYPES OF INVERTEBRATE LARVAE
 
embryo (onchosphere or proscolex) and the formation of the chitinoid
coat with its inclusions of yolk material take place within the uterus
of the posterior proglottids, and in this condition the embryo is passed
to the outside; it must await its appropriate intermediate host for further development. .
 
If it is ingested by the proper animal (often along with the entire
proglottid in which it was produced) the digestive juices soften the coat
of the embryo, which is set free and at once begins boring its way through
the intestinal wall and passes into liver, mesentery, peritoneum, brain,
or other organ. Here it encysts but continues its development. If the
intermediate host is an invertebrate the next stage is a cysticercoid; if
a vertebrate, a cysticercus. The difference is chiefly in the large bladder
or caudal vesicle of the latter. The cysticercoid has typically three parts:
scolex (the tapeworm head), a body, and a caudal vesicle, the latter
forming an enclosure for the other developing parts inside it. In the final
host the scolex is pushed out, attaches with its hooks to the wall of the
alimentary tract and begins to grow.
 
The cysticercus is attained from the hexacanth embryo in the following manner. The hexacanth embryo, having reached its place of encystment, enlarges markedly and its interior becomes filled with fluid or
with loose spongy tissue. For this reason it is called the bladder worm
stage. A small invagination into one side appears which deepens and
develops into the scolex, but in an inverted condition. An elevation at
its bottom becomes the rostellum, and the suckers appear on the inside
of the lateral walls near their base. Metamorphosis of such a larval
form takes place after transference to the final host by the eversion of
the scolex and very active growth in the region just behind it to form
proglottids.
 
In a few instances instead of a single scolex many are produced by the
cysticercus by budding from its interior. This is the case in Taenia
coenurus, which produces as invaginations from its wall many scolices
that are later to be everted. In Taenia echinococcus this polyembryonic
development may go even farther, the ingrowths from the wall becoming separated off to drop into the cavity as secondary bladders. Each of
these goes on actively producing new crops of scolices.
 
IV. THE NEMERTINEA
 
Of the four groups of the nemertean worms only one so far is known
which develops by metamorphosis. In this (Heteronemertini, Schizonemertini) there are two families and the characteristic and important
larval form is the pilidium. In one of the families, however, there occurs
a creeping form which is really a pilidium modified for creeping in keepTHE PILIDIUM 153
 
ing with the similar habit of the adults. This is known as the larva of
Desor and is that of the genus Lineus. The nemerteans, while showing a
distinct advance over forms already considered in acquiring a second
opening to the alimentary tract, the anus, exhibit many primitive features which relate them to the flatworms and also to the ctenophorcs.
The pilidium itself also is prophetic in certain of its features of the
 
trochophore larvae of higher groups. Cerebmtulus has been most studied
in America as a type of nemertean development.
 
The Pilidium
 
The eggs of Cerebratulus cleave spirally and form blastulae and gastrulae in the manner typical for such eggs. The free-swimming pilidium
is a helmet-shaped larva with a spike of long cilia arising from the apical
plate of cells. The cilia elsewhere are uniform in size and distribution
except at the margins where a ciliary wreath may be seen. This is the
locomotor organ of the embryo, the prototroch. The sides of the umbrella-like portion are prolonged downward into hanging lobes or lappets.
The pilidium is produced from the symmetrical gastrula by the unequal
development of certain parts so that the blastopore opening becomes
oval in shape and the invaginated enteron grows in length and bends
 
over to one side, the bent sac-like portion becoming the stomach and
the open funnel the oesophagus.
 
From two large cells which pass into the blastocoele the mesenehyme
is produced. It consists of a mass of stellate cells whose amoeboid movements may be seen through the transparent outer covering. The pseudopodia which are put out enable the cells to attach and some are converted into muscle fibres. The pilidium is completed in this condition
and swims about for a considerable period, perhaps two weeks, feeding
at the surface of the sea upon microscopic organisms.
 
The metamorphosis of the pilidium has proven elusive since it is not
yet possible to rear the animals under laboratory conditions and only
fragmentary information has been gleaned from the material collected
from the sea. We have to do here with the first of these transformations,
numerously observed in the invertebrate groups, in which only part of
the larval structures are included in the adult animal. In this case the
larval ectoderm, prototroch, lappets, and apical sense organ, as well as
the fused outer parts of the amniotic invaginations about to be described,
form a double bell-shaped structure which is left behind like a cap after
the little worm is differentiated and has constricted itself away. This
 
larval rudiment swims about for a time, and then, unable to feed and
exhausted, it dies.
154 TYPES OF INVERTEBRATE LARVAE
 
The formation of the worin's body from the larval pilidium begins
with four eetodermal invaginations which appear on the flattened lower
surface. These amniotic invaginations form, in their deeper portions, the
imaginal discs which contribute largely to the definitive body of the
worm. They are distinguished as right and left anterior, in front of the
 
fir: 103 A. pilidium larva of Cerebralulus lactus (Redrawn from M:icBri(le, after
C‘ B Wilson) lap , lappet, oes , oesophagus, st , stom ieh, II|("a0ll , iiie-seneliyme cells
a p . apical plate B, a. pilidium Just before metamorphosis (Redr l.Wll from Mac Bride, ziftei
Metchnikofi ) 9, p , apical plate, a im , anterior imagimil disc oes , oesophagiis, pr , anlage
of proboscis; pt. im., posterior imaginal disc
 
mouth, and right and left posterior behind it. They continue to deepen
and broaden, growing up over the already formed alimentary canal until
they finally meet and coalesce. Their outer walls form a temporary
larval covering known as the amnion, a delicate envelope separating the
body of the worm from the covering of the larva, and the inner fused
portion is the skin of the future worm. The intestine of the pilidium is
THE PILIDIUM 155
 
thus included in the body of the new worm and becomes the endodermal portion of the latter.
 
Rudiments of the other organs of the worm are developing meanwhile.
The proboscis develops as an ectodermal invagination projecting into
a mesodermal mass which is to become the proboscis sheath. The brain
 
fiG 104 l‘ullv dt-xcloped pllulinm uitli young Il(_‘l11(‘ll\ Ill sutlun its amniotic mu‘
(ltcdumn flolu lunschnlt and Hculu, after liutsrhli )
 
rm, iunnion (l , inushnc of pilidium lama surrounded bv worm, cc, cctodmm of
\\o1m, in . mouth of piluliuin, n , l)Q;£1l\lllng()f ncnous svstem, r , probosus so excrcton
organ
 
is of compound origin, arising as an cctodermal proliferation from the
anterior imaginal discs. The formation of the anus and certain other
organs has not been followed through because of the lack of material.
However, from the cndodermal portion of the pilidium and the inner
part of the amniotic invaginations comes the material from which all
the later structures are derived. The outer part of the fused invagina—
tions, such as the lining of a cap of which the larval walls are the chief
156 TYPES OF INVERTEBRATE LARVAE
 
parts, is cast off, and the young animal which it covered is the young
worm ready for life upon the sea bottom.
 
V. THE ANN ELII)A AND MOLLUSCA
1. The Trochophore Larva
 
The trochophore larva is typical of annelids and molluscs. Other
smaller groups, among which are the Polyzoa, Sipunculoidea, and
Echiuroidea, also have trochophore larvae, and still other larval forms
show relationships to the trochophore which are more or less close. In
some larvae simple modifications are present and in others the relationships are harder to trace. It is unquestionably the most important invertebrate type of larva, viewe(l from a phylogenetic standpoint.
 
The trochophore larva in its simple condition is ovoid and possesses
certain characteristic features, most conspicuous of which is the prototroch, a ciliated band about the equator. The prototroch is the chief
organ of locomotion and participates in getting food. A group of cells
known from its position as the apical organ functions as a sense organ,
and from these sensory cells apical cilia grow out as a tuft. In some cases
a metatroch, a secondary belt of cilia, is present posterior to the prototroch and a second tuft of cilia known as a tclotroch is present at the
pole opposite to the apical tuft. Departures from the typical arrangement of cilia occur in various species. Larvae with the primary ciliated
band only are spoken of as monotrochal. In some, called atrochal, the
prototroch is not developed, but cilia are present all over; in others,
without a prototroch, a mctatroch only is developed. Polytrochal larvae
also occur, but these are later stages in which secondary bands of cilia
are formed about the developing post-trochal region.
 
Internally a trochophore has a complete digestive tract with mouth,
large, bulb-like stomach, short intestine, and an anus. The mouth of
annelids is the old blastopore or an opening developed at the same place
as the blastopore after a very temporary closure. The intestine meets
an ectodermal invagination, the proctodaeum, with which it fuses. and
an opening breaks through completing the alimentary tract. An archinephridium is present, running from the ocsophageal region diagonally
to the end of the intestine. Each contains a flame cell, or solenocyte,
with a cavity and a tuft of cilia, and an excretory tube leads from it. In
some trochophores there is an eye-spot containing red pigment cells; it
is sensitive to light. The mcsoblast cells, or teloblasts, derived from 4d,
are present. (or their descendants) and later elongate into two strings of
cells, the mesoderm bands.
THE ANNELID TROCHOPHORE 157
 
A typical trochophore as described is derived from the gastrula by
seine simple changes, the chief of which is the shift of the blastopore
from the vegetative pole to the lateral position. In this process several
factors take part. One is the increase in rate of development and in the
actual number of cells of the dorsal posterior cells, particularly the
descendants of the 3d cell. This inequality of growth tends to push the
opening sideways. In some forms the blastopore also becomes oval in
shape, then constricts in the middle, and the portion in the a-b quadrants is pushed anteriorly by the growing cells of the d quadrant. Of
these two openings the anterior one becomes the mouth and the posterior one after temporary closure reopens to become the anus. This
procedure is made much of by some authorities who reason that in this
manner must have come the separation of the original ingestive opening
into two, one of which is ingestivc and the other egcstivc.
 
In the fully grown trochophore larvae of all the groups in which it occurs are found the points of structure as described. Indeed, the homologies
between the various groups are complete even to the details of trochophore development. When one considers the remarkable array of organisms which in spite of total absence of agreement in adult features have
this type of larval structure, he must find the fact of their common
method of origin very surprising and significant. Nemerteans, rotifers,
annclids, molluscs (except cephalopods), and bryozoa, form a series
which certainly presents a complete gamut of adult variation, yet all
come from larval forms with features that are in general the same. It
would, however, be even more surprising if there were not minor differences to be found in the trochophores. There are variations in the relation
of the mesoderm mother cells to the gut wall, of the persistence of the
protonephridia, the presence of the anal vesicle, of a prototroch, of the
gastropod shell gland, and in other special organs which are the peculiarities of particular groups. It is notthese differences, however, which
deserve emphasis, but the common features of development which
find expression in the widespread trochophore type.
 
2. The Annelid Trochophore
 
The metamorphosis of the trochophore into an adult annelid may
next be considered. It consists chiefly in the growth in length of the
post—troehal region and in the differentiation of certain elements found
there. The essential features of the metamorphosis are (a) the elongation
of the post—troehal region to form the body of the worm (post-cephalic
portion) and its consequent segmentation; (b) the apparent reduction
(which is not real, but simply relative) of the troehal and preoral regions
158 TYPES OF INVERTEBRATE LARVAE
 
and their resulting changes to form the head of the worm; and (c) the
disappearance of the ciliated bands. The processes are of course accomplished gradually, there being no moment at which the trochophore ends
and the adult begins. The post-trochal region is one of active growth,
differentiation, and cell multiplication. As an example of the metamorphosis of the annelid trochophore, Polygordzus has been often studied,
 
fiG. 105 Troehophorc of P(ll_Ij(]0rdLu8. (After Woltereck) An , .irch1ncphr1d1um
 
11 p . apical plate, mt. intestine, mtt, mctatroeh, 0 , mouth. pr t. prototroch st
stomach, ti 1: . telotroch.
 
and no other is probably better known. It has been figured by Hatschek,
Agassiz, and others, but is best known from the work of Woltereck.
The elongation of the post-troehal region in Polygordzus involves
especially the growth and division of the cells of the intestinal walls, the
multiplication of ectoderm cells and the growth and differentiation of
the cells of the mesoderm bands. The descendants of the 4d cell form the
mesoderm bands, symmetrically placed on the two sides of the intestine
The pole cells from which they came are known as teloblasts. The bands
multiply not only in length but in thickness and in each a series of cavities
THE ANN ELID TROCHOPHORE 159
 
gradually appears. These are the mesoblastie somites, and they are
marked off from each other by constrictions which are traced on the
surface by transverse grooves in the ectodermal covering. Their cavities
grow progressively, and as they expand they fill up the surrounding
space which was the remnant of the blastocoele. Ultimately they meet
above and below the intestine, their walls fuse and break through,
making a continuous pouch in each segmfint instead of a pair. Evidently
in the growing worm, segments are not a
in the same degree of advancement.
 
The origin of the excretory organs shows
two stages in development in the annelids.
The archinephridium by the addition of
other cells from the third quartette and
by increase in number of its own cells
becomes a protonephridium, a rather complicated structure whose basis is flame
cells. The origin of the permanent nephridia
has been the cause of controversy among
embryologists, particularly as to their derivation from ectoderm or mesoderm.
These posterior or permanent ncphridia
or metanephridia grow from strings of
cells lying in the wall of the embryo and
running posteriorly. These break up into
loops and a lumen appears which later
becomes the tubular nephridrum. In
N crezs, Wilson described these as of
eetodermal origin except for the funnelshaped opening which he hsaid lils meso- P115;-orfilfiy agljlgrdliisziiigwlirégvftgi
dermal. Others consider t at t e entire ‘fiolmeck
end is mesodermal and secondarily at- a_ anus? 1,. posterlor b(,,d(., 0;
tached to the eetoderm. Still others think  h:*:‘:o““1i:E:SDI1 v I>F0t0neDh“d1«*
theentirestructureisectodermal.Although ' D '
the details in Polygordzus are not fully known, Woltereek holds to the
ectoderrnal origin.
 
The nervous system begins with the mass of nerve cells that lies under
the apical tuft. This is the cerebral ganglion and from it radiate eight
nerves to the cells of the prototroeh. Two, the lateral nerves, continue
across the prototroch around the oesophagus to form the ventral nerve
cords.
 
These are the beginnings of the more important organ systems of the
transformed trochophore. For the details of the metamorphosis and for
160 TYPES OF INVERTEBRATE LARVAE
 
the conditions as found in special forms reference should be made to the
monographs and special articles dealing with these matters.
 
3. The Molluscan Trochophore
 
The metamorphosis of the molluscan trochophore is more complicated
and involves the interposition of another larval stage, the veliger. While
in the trochophore the characteristic larval organs are present, in the
veliger there are also the rudimentary stages of the adult organs. There
are three characteristic organs of this stage: the velum, the shell gland,
 
 
fiG. 107. Young trochophore of Patclla cocrula. (After Wilson.)
 
a.p., apical plate; 111., mesodermnl cell; m.b., beginning of mesodermal band; 1no.,
mouth; s.g., shell gland; st., stomach.
 
and the foot. The velum is derived from the prototroch of the trochophore and is in the form of a bilobed, much enlarged projection abundantly provided with cilia. It serves as the locomotor organ of the voliger and disappears with metamorphosis. The shell gland is at first a
simple invagination opposite the month which may open out to form a
flattened disc or actually evert. Its cells secrete a thin, horny cuticle
which is the shell of the trochophore. In the case of the bivalve molluscs
the rapid extension of this area forms the mantle and calcareous as well
as horny material is secreted, thus forming the two valves of the shell
THE MOLLUSCAN TILOCHOPIIORIQ 161
 
connected by a region known as the hinge. The variations in the shape
of the mantle lobes and the shell secreted by it and in the length and
proportions of the hinge correspond to the various systematic groups.
The foot in the earliest stages is a thickening of the ectoderm cells just
ventral to the mouth. In the cavity of the slight hollow forming behind
this bulging foot are mesenehyme cells which contribute to the differentiation of the organ. Other organs make their appearance in the developing veliger, including a larval kidney which disappears as the foot
grows out, the muscles, the ganglia, gills, coelome, liver, and secondary
structures as crystalline sac and otocyst. The details of their development are beyond the scope of the present account.
 
The metamorphosis of the veliger into an adult-like form is not a
process of long duration. The appearance of the organism is surprisingly
 
 
Fm. 108. A, embryo of a heteropod. (llcilmwu from Balfour after Fol.)
 
u.. arelienteron; 0., body r-avity; f., foot; mo., mouth; s.g., shell gland; v., velum. B,
young veliger of I’l(mr0l2runL'hidium. (Redrxuvn from Balfour after Lancaster.) in., loop of
intestine; y., residual yolk spheres; n.g.. nerve ganglion; ot., otoeyst.
 
changed largely because of the sloughing off of the cells which formed
the velum; this process and some others coincident with it allow the
organism to assume the external shape of a small adult. The larval
muscles disintegrate, the anterior region with the mouth shrinks, drawing closer together the mouth and anterior adductor and advancing the
front end of the foot. As a result the position of the developing gills is
changed and the intestine is shifted and straightened. Although now the
organism has the recognizable form of an adult, it is of course very immature and numerous internal changes have yet to be undergone. Labial
palps and gill filaments in the bivalves, adult kidneys, pericardium, the
final relations of the mantle cavity, development of the gonads and
their ducts, all these and other minor processes of differentiation are
still to be undergone before the final condition is reached.
162 TYPES or INVERTEBRATE LARVAE
 
VI. THE CRUSTACEA
Nauplius Larva
 
O. F. Mjiller long ago studied some forms of copepods which we now
know are larval,‘ but he thought them adults and gave them the name
Nauplms. In this way originated the term that now represents a stage
common to all Crustacea. In the lower forms it is usually a free~swimming
larva and in many. of the higher ones it is simply a stage passed through
in the egg, but it IS represented in the development of all Crustacea
 
 
Fm. 100. A, ventral View of gastrula stage of .l.staru.s flzwialflis. (Redrzmn {min MacBride, after Reichenbach.) e. l., cephalic lobe; th. ab., thoracic abdominal thickening.
 
B. nauplius stage of the same. an., anus; at‘, rudiment of first antenna; at‘~’, rudiment
of second antenna; car.. ridge making the first trace of the carapace; e.l., cephalic lobe;
lah.. lahrium; m.. mouth; mn., rudiment of mandible; pr. c., protocerebrum; th. ah.,
rudiment of thorax and abdomen.
 
Crustacean eggs show a great range of developmental types, and the
various stages show no uniformity throughout the different groups.
Cleavage may be superficial or it may be total and nearly equal. A cleavage cavity is usually lacking because of the large amount of yolk, but
some species have it in more or less restricted condition. Gastrulation is
usually by epiboly and ingression, but here again conditions vary. Cross
fertilization is usual, but there are cases of self—fertilization, and parthenogenetic development may alternate with normal fertilization. There
are some cases in which only parthenogenesis has so far been discovered.
But in all cases a nauplius stage is at length reached.
 
The form named nauplius by Muller actually had four pairs of appendages, whereas the stage now known as the nauplius has only three
NAUPLIUS LARVA
 
163
 
pairs. It was Claus in 1858 who named the three-appendage stage which
is of such widespread occurrence throughout the Crustaeea. A nauplius
 
 
Pro 110 Continuation of I15: 10‘)
 
at‘
 
at’
 
nm
 
In A the rudiments of muxill K‘ have appearul
 
and the caudal fork is VlSll)l0 In B thoracic appendages are seen and the abdomen Ill
 
segmen tmg
 
larva, therefore, has three pairs of appendages, first and second antennal,
 
and mandlbular. But the degree of
development toward independent existence in the nauplius stage is by no
means uniform in the difieient Crustacea. There is in fact a series of larval
stages in the C1 ustacea, the most important of which are nauplius, metanauplius, protozoaca, zoaea, mysis, all
leading to the adult. There are, also,
others less generally important, but
more specialized for pai tieular groups.
Of those mentioned a completed
series occurs in the higher crustaceans
only, in some forms of which all are
represented. For every stage listed
there is some group of higher crustaceans in which the larva hatches from
the egg at the corresponding time.
That is, hatching, or the breaking
out of the free-living’ form from the
 
 
fiG 111
 
Nnuphus of Cyclops (After
Claus)
 
an‘, first antenna; an’, second antenna. man , mandibular appendage.
lab , labrmm, ex , exopodlte. en , endopodxte
 
egg membrane, is a variable process and some certain species may be
164 TYPES OF INVERTEBRATE LARVAE
 
found to illustrate each stage as a newly hatched larva. Evidently those
which hatch in the more advanced stages (for example, the decapods)
do not show the nauplius in a full functioning condition as do those in
which the nauplius is a free-swimming larva, as in the barnacles. In the
 
fiG. 112. Zones. of Penaeus, ventral view. (After Claus.)
 
uni, first antenna; an“, second antenna; e., eye stalk; mn., mandible; mx‘, mx’. first and
second maxilla; mxp*, mxp’, mxp3. first, second. and third muxillipeds; pl., beginning
of pleopods; ur, uropod; e.f.. caudal fin.
 
crayfish, for example, the nauplius condition is shown by three pairs of
mere thickenings or buds instead of developed appendages and there are
in the embryo in addition only two cephalic lobes, two thoracico-abdominal
rudiments, and the endodermal rudiment; this is far from a free-swimming
embryo.
 
The nauplius of Cyclops is an elliptical form with no external sign of
NAUPLIUS LARVA 165
 
segmentation, but with an enlarged labrum, openings of the alimentary
tract, a single median eye, and the three pairs of appendages. The first
antennal appendage shows no sign of a biramous character, but both the
second antennal and the mandibular have at least partially developed
both exopod and endopod. Examples of forms hatching in this condition
are the copepods as well as Penaeus, and Balanus. In Balanus this stage
is preceded by one in which three primary segments are recognizable.
These become subdivided into eight lobes, which are the labrum, right
and left first antennal from the first primary segment, the right and left
second antennal from the second segment, and the right and left mandibular and the telson from the third. Future growth takes place between the mandibular lobes and the telson. From this stage the next
changes lead to the metanauplius.
 
 
Fm 113 Mysis larva of the lobster. Ilomarua amcncanus. lateral view. (After Herrick )
Exopoditcs of the walking legs are to be noted (ex.).
 
The metanauplius condition is reached at the end of the first molt
in those forms which hatch as nauplii, but occurs before hatching in
such forms as Branchipus and Lucifer. Two additional pairs of appendages are present, the first and second maxillae, and segmentation is
beginning.
 
In the protozoaea, illustrated by a newly hatched Squzlla, the first
and second maxillipeds are present as well as the appendages of the
earlier types, the abdomen is partially segmented, but not the thorax,
and the compound eyes are making their appearance.
 
The zoaea, the stage in which the crab hatches, possesses third maxillipeds, some of the thoracic appendages, the number varying with different forms, compound eyes, an abdomen completely segmented, but
the thorax showing as yet incomplete indications.
 
The mysis stage, characteristic of the genus of that name, has all
166 TYPES' OF INVERTEBRATE LARVAE
 
five pairs of walking legs with exopods, six pairs of pleopods (although
in some they are hardly developed at hatching), and segmentation is
complete. The lobster also hatches in an advanced mysis stage.
 
finally in the fresh-water shrimp, Crangon, the condition of the adult
is reached so far as external features are concerned at the time of
hatching.
 
Of the less important larval types of Crustacea, no mention will be
made here.
 
VII. THE INSECTA
 
Among the insects development may involve the formation of very
complex larvae and more or less complete metamorphosis, or may be
direct. The structure and cleavage of typical insect eggs have already
been described in the section on superficial cleavage. The cleavage of
the centrolecithal egg results in the formation of a blastoderm which
may be of uniform thickness in development or may have early shown
a differentiation on the ventral side of an aggregation of cells which
will become the primitive streak.
 
Even if the blastoderm is at first of uniform thickness, it gradually
becomes thicker in the ventral region by the multiplication of the cells,
and thus in this case too the primitive streak or germ band is formed.
Mesoderm is formed by one of three methods. (1) Along the medial
line of the germ band an invaginating groove is presently to be seen in
many embryos of which those of the Coleoptera may be taken as an
example. From the material of this invaginating groove comes the inner
layer from which is derived the mesoderm and endoderm. (2) In certain
other insects the formation of the mesoderm may be accomplished without the formation of a tube but rather from a middle plate which remains nearly flat and is overgrown at the edges by the lateral folds. It
occurs in certain Lepidoptera and other forms.
 
(3) Still another type of mesoderm formation takes on the character
of a proliferation and invagination of cells from a median ventral blastoderm region. This is characteristic of the Orthoptera. At the edges of
the germ band the blastoderm begins a folding process and at length the
two folds meet over the band in the middle region. Their union produces
two membranes, the outer one, known simply as a serosa, and the inner
one, the amnion. The germ band continues its own growth and the marks
of segmentation become apparent shortly as transparent grooves. An
anterior pocket growing dorsally from the ventral germ band is the
beginning of the stomodaeum and the foregut, and a similar one at the
posterior end forms the proctodaeum. A pair of large prc—eephalic lobes
at the anterior end of the germ band develop in time into the lateral
THE INSECTA 167
 
eyes, and antennae and mouth parts appear as rudiments in proper
serial fashion. The appendages likewise are outpocketings of the ectodermal germ bands. It is evident of course that the variety of structures
found among the insects means great variability in details by which
these steps are accomplished. The general body form of the insect is
 
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Fm 114 Developing eggs of Bmchus quadnmaculatus (After Brauer )
 
A, tmrisverse section, showing completed blastoderm Dorsal side of egg toward top
of page B, section of egg 9. little older than in A through anterior region Cells of veiitml
blastoderm are crowded, but dorsal blastoderm is thin and flattened eh . chorion, v pl
ventral plate.
 
completed by the growth of the margins of the germ band dorsally
until they finally close over and form a dorsal wall. While this has been
going on the progress and development of the internal structures has
likewise been considerable and the embryo continues its development
until finally ready to hatch into a larva.
 
During the larval stage the insect feeds, sometimes voraciously, storing up nutritive material for its subsequent development. In the more
168 TYPES OF INVERTEBRATE LARVAE
 
specialized insects this development is very complicated involving a complete metamorphosis with entire changes of form and often of function
as well. The groups of insects which undergo this indirect type of
development” or complete metamorphosis are spoken of as the Holometabola and include the Coleoptera, Strepsiptera, Neuroptera, Mecoptera, Trichoptera, Lepidoptera, Diptera, Siphonaptera, and Hymenoptera. The less specialized groups comprise the Heterometabola in which
 
fiG. 115. (‘ontinuation of 114.
 
A, Transverse section of egg after closure of gastral invagination. mes., mesoderm; am.
ser.. amnio-serosal fold. B, Longitudinal section of an embryo of 32 hours. Am , amnion,
ant. mes., anterior mesenteron anlage; caud. pl., caudal plate, mes., mesoderm; post.
mes., posterior mesoderm anlage; ser., sorosa; st., stomodaeum.
 
development is direct and metamorphosis incomplete. These forms lack
a true pupal period. They include Orthoptera, Dermaptera, Platyptera,
Placoptera, Ephemeridae, Odonata, Thysanoptera, and Hemiptera.
Since a distinction between larvae and pupae is lacking it is common
to use the term nymph to apply to the young insects after hatching
and several molts or ecdyses may be gone through among these forms.
The terms, stages or stadia, are used to designate the intervals between
the melts; and the term, instar, is frequently used to designate the insect
at any particular stage. The Thysanura and the Colembola develop
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3 ‘°.?g9;ooao%§g§$u°°°%
 
 
 
1,.,........'a.'.¢,=r u
 
 
F10. 116. Successive stages through the embryonic area. of Hydrophzlus. (From Korschelt and Hc-ider, after Helder)
 
A, Formation of invaginnted groove wluch 15 to produce the under layer B, Origin ol
ammon. C. Amnion completed over embryonic area. Yolk has undergone cleavage D.
Ongin of somxtes. E, Formatmn of tmchne F. Formatlon of coolome
 
Am.. amnion; c , coolomc, eat, octodcrm. end , ondodorm, mm, mesoderm. m ‘I. fit?!
 
m\I.4 hf mnundnum mu. m....\..n....u~. unvv\)Cn 4.. o...,.l.,... ..I .....l....I........ .. .... .,mo...,l
170 TYPES OF INVERTEBRATE LARVAE
 
without any metamorphosis and hence are often spoken of as the
Ametabola.
 
Upon hatching, the larvae emerge with certain characteristics depending upon the group to which they belong; one is usually able to classify
the insect into its order by mere reference to the type of larva. Common
 
65%
‘
E
 
F I0. 117. Types of larvae. (From Folsom.)
 
A, B, Thysanum; C, thysanuriform nymph; E—I, eruciform larvae; A. Fampadea; B,
Lep7.'.9ma,' C, perlid nymph (Placoptera); D, Libellula (0donata); E, Tenthredopsis
(Hymenoptera); F, Lachnostema, (Coleoptera); G. Melanotus (Coleopteru); H. Bombus
(Hymenoptera); I, Hypoderma (Diptera).
 
names are given to the larvae, such as the caterpillar of the Lepidoptera,
the grub of the Coleoptera, and the maggot of the Diptera. The types
of larvae are known to entomologists under several terms but they are
fundamentally of two groups, the campodeiform and the eruciform. The
campodeiform are also spoken of as the thysanuriform in reference to
their generalized structure. They are flattened, have a long body, often
THE INSECTA 171
 
with long legs and antennae, hard body plates, caudal cerci with welldeveloped mandibles and active habits. These are characteristics of the
adult thysanurans, especially of the genus Campodea, but in the insects
which undergo metamorphosis they are of transitory importance only.
The eruciform larva is illustrated by the caterpillar or maggot with the
cylindrical body which may grow to become more or less spindle shaped,
weak integument, and with mouth parts, antennae, legs, and caudal
cerei reduced, even to complete disappearance; correspondingly it leads
 
 
110 118 Successive stages in the de\ clopment of a pluteus of the Ophiuroidea and
Echmoidea (After Leuckart )
 
ad e , adoral ciliated band, :11 , alimentary canal, an. anus, ar, arms, mo . mouth,
per 0 c . porioral cllrated band
 
a very inactive life. Between these two types transitional forms are
easily recognized, for instance, in the genus M antzspa of the Neuroptcra
the larva which hatches from the egg is distinctly campodeiform and
active but it enters the egg sac of a spider and becomes sedentary, loses
use of its legs and completely changes its form, that is, becomes an cruciform larva. For the changes which occur during the growth of the larvae,
the frequency of the melts, and the great variety of adaptive structures
that are assumed in the various larvae of the insects, the reader must
refer to treatises on entomology. Likewise the formation of the pupa is
a subject which varies too much in detail to be discussed in this work.
172 TYPES OF INVERTEBRATE LARVAE
 
The internal changes which accompany the metamorphosis of insects
are only incompletely understood. In those forms in which metamorphosis is incomplete certain organs are of larval significance only and
their tissues must give way and provide the materials for other struc—
tures characteristic of the imago. This destruction of larval tissue, or
 
int.
 
fiG. 119. Successive stages in the development of u. hrpmnaria of the asteroids. (After
Leuckart.)
 
ad. c., adoral ciliated band, int., intestine. mo., mouth. oes . oesophagus; pr. 0. c., pre
oral ciliated band; pt. o.c., post-oral ciliated band.
histolysis, takes place commonly during the pupal period through the
activity of phagocytes and is followed by a period of the construction
of imaginal tissues or histogenesis. At the end of this constructive period
the animal is ready for the final metamorphosis which converts it into
an active adult or image.
 
VIII. THE ECHINODERMATA
 
In the phylum Echinodermata are to be found some of the most
remarkable forms of larvae of any group in the animal kingdom, and
THE ECHINOIJERMATA 173
 
in this group metamorphosis has a peculiar and unusual significance.
The larval stages are preparatory for the changes which are to adapt
the adult forms to a great variety of living conditions, and they bridge
the gap from a rather simple ancestral form to the diverse conditions
found among the five classes of living echinoderms. One has only to
consider the different types of adults found among the asteroids, echinoids, ophiuroids, the holothurians and the crinoids to appreciate the
problem which confronts the simple type of ancestral larval form. Such
extensive metamorphoses as are found here have for their special function the adapting of the organism to the very changed conditions in
which it finds itself. Since the larval condition is retained to the last
possible moment in development, although internal changes of the most
 
 
Fm. 120. Successive stages in the development of an auricularia of the holothuroldi
(After Leuckart )
Letters as in 118 and 119.
 
profound character are taking place, metamorphosis is of a typo sometimes spoken of as cataelysmal.
 
The gastrula of all the echinoderms develops into a form similar to
what was probably the hypotheticalancestor of all the classes of the
group; it is known as a. dipleurula. From this dipleurula it is conceived
that the echinopluteus of the sea-urchin, the ophiopluteus of the brittlestar, the bipinnaria of the starfish, and the auricularia of the holothurian
are derived. Of these four larval forms the first two are more closely
related to each other than to the other group, in which also affinities
are discoverable to the larvae of the crinoids. It is not feasible to undertake here a description of the development of the larvae and their
metamorphoses in all these cases. For particular reasons and also because
it is the form most commonly studied, we choose to follow through the
development of the starfish larva, the bipinnaria, from its origin from
the gastrula to its metamorphosis.
174 TYPES OF INVERTEBRATE LARVAE
 
1. The Bipinnaria
 
It is characteristic of echinoderm larvae that there should be a bilateral symmetry. Two important trends are noticeable as the transition
from larva to’ adult takes place, namely the great development of the
left side of the larva with the corresponding decrease of the right side,
and the complete change of symmetry to a radial type whose axis is at
right angles to the former larval axis. The egg of the starfish goes through
a rapid and regular process of radial cleavage resulting in a blastula of
about equal—sized cells. The cells become ciliated uniformly, the embryo
bursts the egg membrane and, rising to the surface, begins its larval
life. Gastrulation has in the meantime been going on, but the formation
of mesenchyme is not completed until after the
f ree—swimming stage is reached. The larva elongates,
becomes somewhat flattened on the ventral side,
the blastopore is metamorphosed into the anus, and
the larval mouth breaks through anteriorly. The
cilia disappear except for certain specialized ciliated
_ bands which take on a shape characteristic of particular species. Gradually there appear as outgrowths certain special processes which as they
grow carry out the ciliated bands to their borders
 
 
uc‘;:‘:)f‘;3O1‘;ngI‘l‘l‘l‘r°\fi:‘el and give the larva its bipinnatc form to which is
of Asterms (Arm due the name “bipinnaria” given it by Sars.
“3“““-) The earlier investigators were inclined to the
al , alimentary - - _ ‘
mm mm” mouth; opinion that the starfish arose as a bud on the 1: ft
 
pr o 0., pre—oral
Cllldtcd band; pt. o.c._
p 03 t- oral ciliated
band.
 
side of the larva. It is now realized that this appearance is superficial only and that the larger part of
the larval body is involved in the production of
 
the adult. The earliest trace of the adult body
appears as a five-lobed structure in the left posterior portion of the
larva. By the growth and dilferentiation of this structure and the loss
of the larval mouth and oesophagus and the formation of the new
opening, the metamorphosis into the little starfish is accomplished.
In the case of the starfish a temporary fixed stage which is not found
in all types of echinoderm is passed through. During this stage
certain other larval arms and processes are developed and the larva is
spoken of as a brachiolaria.
It is now desirable to follow in more detail the changes which have
been thus briefly sketched.
THE DIPLEURULA 175
 
2. The Dipleurula
 
All echinoderm larvae agree, while showing much variation from each
other on other points, in the possession of the following features: they
are bilaterally symmetrical, have a locomotor organ in the form of a
curved and bent longitudinal ciliated band with preoral and anal loops.
They possess a V—shaped adoral ciliated band; the alimentary canal
 
fiG 122 A, Bipinnai-1.1 of Astcmas (Frontal view) B, Side view of an older bipinnaria.
Median brarhioliirian process beginning to grow out at b (After Agassiz )
 
a , anus, a d a . anterior dorsal arm, ad e , adoral eiliated band, int , intestine. L eoel .
left coelome,m d a, median dorsal arm,mo , mouth, oes. oesophagus. pt d a . posterodorsiil arm, pt 1 a . postero-lateral arm, pt 0 a , post~oral arm, pt 0 e . post-oral band of
fllld, pr .1, pre—oral arm, pr 0 c. pre-oral band of cilia, r eoel , right coelomic sac, st,
stomach
 
consists of the typical four parts, namely, the mouth parts, oesophagus,
enlarged stomach and intestine. The coelome is budded off from the
apex of the archenteron as a pouch which divides into two lateral
pockets and has communication with the exterior by a ciliated canal
opening on the dorsal surface to the left of the median line. This canal
is the stone canal. Since these features are common to all the different
groups of echinoderms it is believed that they must have been the
characteristics of an ancestral type from which the different classes of
176 TYPES OF INVERTEBRATE LARVAE
 
the echinoderm existing today have been derived. This hypothetical
ancestor is known as a dipleurula. To this larva the characteristic features of the ophiuroids most faithfully conform, and of all echinoderm
types it is the most nearly bilaterally symmetrical, for which reason,
along with ‘others, it is probably to be regarded as the most primitive.
In addition to the features ascribed to the hypothetical dipleurula, it
is assumed to possess right and left coelomes more or less divided into
three parts, anterior, middle, and posterior. However, a departure from
the characteristic dipleurulan condition is seen in Asterias in that the
coelome is divided into only two parts (unless the stone canal and its
connections are to be regarded as the homologues of the anterior coelome
of the dipleurula and the anterior coelome of the starfish is homologous
to the middle portion of the dipleurulan structure). The middle part of
 
m'p' s.c. rt.md.coel.
 
 
l.pt.coel.
 
fiG. 123. Diagrammatie reconstruction of ancestral dipleurula.
 
u.. anus; an. coel., anterior coelome; l. hyd.. left hydrocoelc; l.pt. coel., left posterior
coelome; m.p.. madroporic pore; rt. md. coel., right middle coelome; r.pt. coel., right
posterior coelome; s.c., stone canal.
 
the body of dipleurula has lobe-like processes extending outwards and
covered with ciliated epithelium into which the middle coelome extends.
These processes permit a comparison with the lip of the braehiopods
and so-called lophophore which bears ciliated tentacles. In both cases
the organs function to direct food-bearing currents of water to the
mouth. Resemblances have also been pointed out between dipleurula
and a simple ctenophore plan of structure, and upon the basis of these
suppositions it has been concluded by some that there once existed a
class of simple marine animals one member of which was of the general
character of a dipleurula and another the ctenophore-like ancestor of
the annelids and molluscs. These speculations seem also to give a basis
for consideration of the similarities that exist between the trochophore
type of larva and those of the echinoderm and at the same time of the
very great differences that are to be seen in the early development of
 
these types.
METAMORPHOSIS OF ASTERI AS 177
 
As an example of the development of an echinoderin, although it is
hardly to be regarded as a type of the other classes, the embryology of
Asterzas is now to be traced in detail.
 
3. Metamorphosis of Asterias
 
By the end of the first day after hatching the free-swimining blastula
has been converted into a gastrula which is distinguished from the usual
type of invaginate gastrula in that the archenteron occupies only a small
portion of the inner space, leaving a large blastocoele still present. Into
this space are early budded mesenchymc cells which send out processes
and make a network in a gelatinous fluid
filling the blastocoele. The gradual leiigthening of the gastrula to take on the form of a
cylinder with round ends, the differentiation
of the ciliated apical plate and especially of
the longitudinal eiliated band, involving a
thickening of the epithelial cells where it is
to form,with a general increase in the number
of cilia on them and a corresponding decrease
of the cilia elsewhere on the larval body, are
the next characteristic changes through which
the young larva passes (fig. 122). In the
meantime the coelomic sacs are budded off pm 124 Larva of Asmm
from the apex of the arclienteron as in the *1‘ days Old. from dorsal surface
case of dipleurula. The gut grows forward, (Alflgjeflgiwftu) I m.
becomes constricted into the intestine, (left), persicscoiiixiniidigpiiiiéiiiirg,
stomach,and oesophagus, and the oesophagus ;f"‘v’~:‘1‘,l‘:l"t‘;1(;”’§:::,“‘ ' ii: 2 2 v
turns forward and ventrally to meet an in- post,-()r.),l aimed band, smm:
vagination from the ectoderm, the stomo- "‘°“‘°d“““"‘- 5“ 5‘°“"‘°hv °°‘Sv
 
_ _ _ _ oesophagus.
daeuin, with which it fuses. The anus is the
 
blastopore of the gastrula stage. With the formation of the arms the
bipinnaria attains the completion of its outer features. The structure
of these arms varies in the different species. In Asterzas vulgarzs, there
are borne by the preoral band two larval arms called the preoral and
a median dorsal one, while in A. glaczalzs, A. rubens, and A. berylmus
(fig. 122), European species, there are also on this preoral band a
median ventral arm and a. median dorsal one which are directed forward;
there are also in both cases a pair of antero—dorsals, and a pair of
postero-dorsals, a pair of postero-laterals, and a pair of post-oral arms.
When the time for metamorphosis has been reached and the larva begins
to take on its temporarily attached condition there grows out from its
anterior part a series of processes known as brachiolas, a median and two
178 TYPES OF INVERTEBRATE LARVAE
 
dorsals, and the larva is termed a brachiolaria. Into these arms extensions of the coelome push out and in this particular they differ from
the arms of the bipinnaria. These arms as listed include all the lobe-like
outgrowths which are found in other starfish larvae.
 
The Coelomé. The development of the structures connected with the
coelome form the most important contribution to the starfish body.
After a period of slow enlargement near the oesophagus where they
originated, the coelomic sacs begin a remarkable series of transformations. The right sac in some of the
larvae grows to form a canal leading
to the outside through the right
madroporic pore, which soon closes
up and is lost; and in other larvae it
is never found. The left coelomie
pouch, however, always makes a
short vertical growth to the dorsal
surface, forming the pore canal and
uniting with an eetodermal depression to form the primary madroporic
pore. Through the beating of its cilia
water is passed into the coelome.
These structures of the left side are
significant for the future of the
FM 135_ 1.~m,,m1V;Cw(,;u1;mchio1,.,;,. larvae, for it is the left side which
 
(3°m°“’h“t 3"“ AB*‘5Si”)- will develop to the greater part of
a., anus; a.d.a., anterior dorsal arm; the adult Starfish, While the right
 
br.a., anterior median brachiolar arm; _ _ _
int., intestine;l.p.c.,left posterior coelome; contributes only a minimum. Never
pt.l.a., posterior lateral arm; pt.o.a., post- ‘
oral arm; pr.o.a.. pre-oral arm; pt.d.a., thelebs’ anccstrally the larva‘ was
 
posterior dorsal arm; st., stomach. symmetrical and the two sides
originally produced similar organs.
 
The sacs now grow in length and the right and left fuse together in
the pre-oral lobe, although not elsewhere. A partial constriction of the
left sac just behind the madroporic pore divides it into the left anterior
and posterior coelomes. The hinder part of the left anterior coelome
swells out to form a rather circular five-lobed outgrowth. This is the
beginning of the water vascular system and is known as the hydrocoele.
In some forms (Asterina) a right hydrocoele and the right anterior and
posterior coelomes are also formed, but this is not the ease in Asterias.
A madroporic vesicle is formed near the median line from the right
anterior coelome. Its origin and position have been variously described,
but the best opinion now seems to derive it from the right coelome.
These developments complete the structure of the free-swimming biMETAMORPHOSIS OF ASTERI AS 179
 
pinnaria. It is now ready to settle down, become attached, grow into
the brachiolaria and begin the metamorphosis which will produce the
adult starfish. Between the bases of the brachiolar arms a region of
fixation appears by means of which the larva becomes attached (fig.
126B). It is a thickening of the ectoderm, which becomes glandular,
enabling it to fix the little animal to the substratum. The attachment
takes place near the anterior end of the larva and gives to that portion
 
I.br.l.
 
pt.l.a.
 
l.pr.o.a.
m.d.a.
 
r.pr.o.a.
 
r.br.l.
 
br.a.
 
 
 
Fm. 126. Lateral \ iews of bruoliiolnria ol'As(cr2as1uIgan~r in process of fixation. (Modified
from Goto.)
 
A, Left side of earliest stage. temporary fixation bv the bruchioluriun arms; B, part
of older brachiolaria corresponding to the base of A and showing the permanent fixation
by means of the fixing disc, the pre—oral lob'e liming shrunk. 1-5, lobes of hydrocoelc
growing out to corresponding enlargements of the body wall, I——V, the unlugen of the arms.
 
br.l., lateral braehiolar arm; fix, disc by which the larva attaches itself; 1.pr.o.a., left
pro-oral arm; m.d.a., median dorsal arm; oes., oesophagus; p.d.u., posterior dorsal arm;
p.l.a., posterior lateral arm; r.pr.o.a., right pre-oral arm; stom., stomodaeum.
 
of the body the function of a stalk for the enlarging posterior portion
or disc. As development continues the stalk shortens and the disc grows.
In the latter are the right and left coelomes, the hydroeocle, stomach,
and intestine. In the former are the anterior coelomes, oesophagus,
mouth, and madroporie vesicle.
 
While the larva is becoming attached and constrictions which divide
both right and left coelomes into anterior and posterior parts are becom180 TYPES OF INVERTEBRATE LARVAE
 
ing more evident, the left posterior sends a process over to the right side
around the gut. This at length fuses with the right anterior coelome,
and as the left and right anteriors were already joined in the prc-oral lobe
the entire co_1nplex presently becomes metamorphosed into the single
anterior coelome. The right posterior coelome, however, is entirely c11t
off from the right anterior and forms the epigastric coelome of the adult.
During the time that the left anterior and posterior coelomes were divided from each other by a septum formed by their opposed portions,
there appears a groove on the anterior side which is to form the stone
canal, while one on the posterior side is the first sign of the perioral
coelome. The stone canal becomes connected with the madroporic pore
canal and runs down to the hydrocoele. The perioral coelome becomes a
crescentic tube about a bud of the stomach which represents the adult
stomach. The further development of the alimentary tract is as follows:
The stomodaeum gradually disappears, having first become disconnected from the midgut. The oesophagus itself gradually shortens and
atrophies as does the intestine, the larval anus having closed. It is stated,
however, that a remnant of the intestine persists and from it the rectum
of the adult arises. From the left side of the larval stomach the bud
referred to above grows to form the cardiac stomach of the adult which
may be cverted for the purposes of food getting. As it grows it is surrounded by the perioral coelome. At a point on the left side of the larva,
which consequently is to be known as the oral side of the adult, the growing bud makes connections with the ectoderm and an opening appears
forming the mouth. The rectum and adult anus do not appear until the
body form of the young starfish is practically complete.
 
final Metamorphos1's. Since the left side of the larva becomes the oral
side the right side is the future aboral and the first signs of the body
form are seen as five thickened lobe-like elevations of the ectoderm which
are the rudiments of the arms and indicate the position of the aboral
disc. With the growth of the disc portion, the coelomes become displaced
backward in the larva to occupy what will be their position in the new
body region. The hydrocoele becomes entirely separated from the anterior coelome. It sends out lobes which are the ru(Iiments of the radial
canals of the water vascular system and from which tube feet and outer
parts of the system are later formed. The stalk portion, becoming less
and less both in size and in importance owing to changes in the shape
of its cells and to phagocytic action on some of the others, is reduced
until it is included in the disc area and is covered by the oral disc. Only
a small projection from the oral disc holds the larva fast to the substratum and at length it is broken as the little starfish completes its
body form and wrenches itself free. The further changes which the
ENTEROPNEUSTA l 81
 
organ system undergoes are gradually accomplished during the growth
of the young animal.
IX ENTEROPNEUSTA
Tornarza of Balanoglossus. The modes of development in Balanoglossus
and its ielated genera present a great deal of variation. In the genus
 
fiG 127 New England tornarm. from left side (After l\Iorgan )
 
a . anus, a d l , axitenor dorsal loop of the longitudinal r-iliated bind up . apical plate;
up m , apical muscle band, 011 long longitudinal minted band (-001 H first, second,
third. pairs of (oelomie ca\ mes g p, gill pouches mt , intestine o mouth oes , oesophagus per , penoardml sac, pl 1 , posterior lateral ll‘!!! of the lomzitudm 11 mliatod band.
prol, pre—oral loop of the longitudinal cihated bind, st, atom l(‘h ttr telotroch,
wp , water—pore.
 
Dolzchoglossus there is a large yolky egg which by a mueh—abridged
series of stages reaches the adult without the intervention of any independent larval form. In several of the species of Balanoglossus a type of
development which is probably more primitive is found, involving the
presence of a special larva known as the tornaria. Originally when this
larva was first found i_n towings it was assumed to belong to some genus
of the Asteroidea, but the works of Bateson, Morgan, Ritter, and Heider
have left no doubt as to its relations to Balanoglossus. Strangely enough
C
 
fiG. 128. Metamorphosis of tornaria from Bahamas. (After Morgan.)
 
A, just before metamorphosis; B, during metamorphosis; C, young balanoglossid worm
with three pairs of gill slits. ap . apical plate, cil. long., degenerating longitudinal ciliated
band; col., collar region, col.p, collar-pore; ex., excretory tissue in posterior wall of
proboscis coelom, gp., endodermic gill pouch, g.s., gill-slit; pr.p., proboscis-pore; tb ,
 
tongue-bar dividing the gill-slit; ttr.. telotroch; a.ttr., accessory telotroch characteristic
of the Bahamas larva.
ENTEROPNEUSTA 183
 
not all of the types of tornaria which have been described agree in all
points, and several different methods for example of inesoderm formation and development of the coelomic cavities have been recorded for
this larva. The work of Heider, although the most recent, is the only
one which deals with the early stages. He was able to follow through
the cleavage and development of the larva up to the tornaria. stage, but
could keep his specimens alive only eight days. Morgan’s account from
species taken at Woods Hole begins about where Heider’s specimens
died so a fairly complete history is available. The structure of the tornaria larva superficially resembles that of the young bipinnaria and it
is possible to apply the designations used on
the bipinnaria to the longitudinal ciliated
band and the posterior transverse ciliated
band. This latter is also known as atelotroch,
corresponding roughly to the same structure
of the annelid trochophore. From the anterior
end of the growing archenteron a vesicle is
budded off which becomes the anterior
coelome or the coelomc of the proboscis of
the adult worm. From the posterior wall of
the anterior coelome are developed rudiments
of the pericardium and the peculiar dorsal
heart of the Balanoglossus, as well as the
rudiments of the head kidney. The more
posterior part of the archenteron proliferates
two groups of cells which are the begin- ‘ i
 
nings of the middle or collar coeloine and the 
posterior or trunk coeloine. At a level in c, anterior coelome; p.('.,
front of the collar coelome a constriction 9°” ““"“_1E “."p" ‘3"‘"°' *’°“"
 
, _ 0., mouth, 1., intestine.
 
appears which marks the separation of the
 
proboscis from the collar region of the adult. These two posterior coelomes
are formed by different methods in the tornaria taken by Morgan at
Woods Hole and those later studied by him in the Bahamas. In the
former a solid outgrowth of cells from the gut wall is the rudiment of
the coelome. In the latter the wall of the body cavity is formed by the
aggregation of scattered mesenchyme cells, a procedure which is rarely
witnessed in the animal kingdom. At the time of the constriction dividing the proboscis region from that posterior to it a dorsal strip of ectoderm
remains unconstricted and becomes depressed beneath the surface in the
form of a groove. This is the neural groove which is folded off and forms
a neural tube in the fashion characteristic for vertebrate embryos. Below
 
it from the anterior part of the oesophagus a median dorsal pouch grows
184 TYPES OF INVERTEBRATE LARVAE
 
out to form the notochord. Gill pouches develop as several pairs of pockets
from the sides of the oesophagus. The further development of the larva
consists largely in the formation of the modifications of the coelome, the
formation of the collar pores and of the genital organs. The metamorphosis is brought about by the development of a fold in the region
between the collar and trunk coelomes and the general growth "in length
of the trunk portion of the animal. No such complications of development and metamorphosis are found here as characterize the echino—
derms, for the adult itself is of comparatively simple structure. Since
the aim of this discussion is merely to show how the embryo is transformed into a young worm similar to the adult, it seems unnecessary
to follow through further the details of the development of this very
interesting animal.
 
BIBLXOGRAPHIC Nora
 
Among the more important accounts of the subjects contained in this chapter
are the following: Schultze, Minchin, Maas, Metchnikoff, Géttc, MacBride, Brooks,
Appelliif, Korschelt and Heider, Salensky, Lang, Surface, Woltereck, Balfour, Claus,
Grave, Bury, field, Batcson, Morgan, Ritter, I-leider on Balanoglossus. These works
are cited in full in the bibliography on page 406.
 
 
===Chapter X Formation of the Mammalian Embryo===
 
(NOTE: In developing a knowledge of comparative embryology especially as it
applies to the vertebrate groups the most logical procedure at this stage (in which
we have considered various invertebrate larval forms) would be the detailed study
of various vertebrate embryos. It would be proper to consider in detail the embryology of amphioxus, the shark, a teleost fish, the frog, and the chick, as is so commonly
done in courses dealing with this subject, and of course there are other forms also
\vhich might be r-hosen.]
 
So much material is available upon these various forms that it has seemed Wiser
not to devote space to a discussion of the embryology of any of them. Most textbooks of vertebrate embryology discuss at least some of these, and both brief and
detailed expositions of the subject are easily available in English. Indeed the choice
of forms difiers a great deal with instructors so that it would perhaps be necessary
to include all of them to satisfy the selections that would be made in different institutions. In our own case it is our practice to ask the student to obtain a copy of
Patton's “Embryology of the (‘hick” and to study the chick intensively in the
laboratory. Because of the good accounts which are so generally available and because it is felt that nothing could be added in the present volume that is not easily
available in other accounts, it has been decided not to ofier any special discussion
of the groups mentioned.
 
On the other hand, the mammals present many embryological variations from
the other vertebrate groups, the understanding of which is by no means so easy to
obtain as the preceding cases. In the discussions in the chapters on cleavage, gastrul.-ition, etc., it has often been said that the conditions throughout the animal kingdom are as stated except for the mammals. For these reasons it has seemed best to
include here an aiccount of the formation of the mammalian embryo and to leave
other groups and the later history of the mammalian embryo for more detailed works.
 
Considered from the point of view of the embryological differences
which are manifested in the class Mammalia, three distinct groups are
found: the monotremes, the marsupials, and the higher mammals. In
the monotremes, eggs containing a large amount of yolk are laid after
the fashion of the reptilian groups, and the special features of the
embryology of these forms hark back to the type of development as
found in the reptiles more than they forecast conditions of the higher
 
mammals. A detailed discussion of the monotreme seems to be unnecessary.
 
I. MONOTREMES
 
The monotreme egg is the largest of all mammalian eggs since it contains yolk varying in diameter from 2.5 to 4.0 mm. The accounts as
 
given for Echidna and Ornithorhynchus do not all agree in the exact size
185
186 FORMATION OF THE MAMMALIAN EMBRYO
 
but variations are within the limits indicated. The egg is developed
within a follicle consisting of only one or two layers of cells and when
it is passed to the outside receives a covering of albumen and a shell.
In Ornithorhynchus the shell is said to be calcified. _
 
Owing to the presence of a large amount of yolk, segmentation is
discoidal, forming a blastoderm upon an unsegmented yolk mass. Semen
failed to find yolk nuclei here as is the usual case in eggs with discoidal
cleavage. The first two furrows are meridional while the third is parallel
to the first and at right angles to the second. A many-layered blastederm is formed having the shape of a biconvex lens, the deeper-arched
side of which is imbedded in the yolk.
 
The chief departure of the monotreme egg from other discoidal eggs
comes in the rapid closure of the blastopore which takes place relatively early. The edges meet in a spot where yolk and upper and lower
cell layers are continuous with each other, a condition which has given
rise to some misconceptions as to the homologues of these structures
with those of lower forms. The blastopore itself is the elongated primitive groove.
 
II. THE MARSUPIALS
 
The embryology of marsupials has been the subject of study during
the last fifty years on the part of several investigators. The work of
 
Caldwell and Selenka in 1887 represents the first attempt at a study of
the early stages of development, the subject of the former study being
the Australian marsupial, Phascolarctus, and of the latter the North
American opossum, Didelphys v2'rg1'm'anus. In 1910 Hill’s study of the
Australian native cat, Dasyurus viverrinus, appeared, and this study in
connection with the work of Hartman in 1916 and 1919 on the opossum
gives us our best understanding of the embryology of this group. Other
workers have been Minot, and Spurgeon and Brooks on the opossum,
but the two mentioned are the chief source of our information.
 
The ovarian egg of Dasyurus, the largest mammalian egg known outside of the monotremes, measures 0.28 mm. according to Hill, while
that of the opossum varies from 0.14 to 0.16 mm. The egg of the former
is scantily supplied with albumen, whereas around the latter albumen islaid
down in delicate concentric lamellae. The eggs of marsupials are richly
supplied with yolk compared to other mammalian eggs but a strange
phenomenon occurs by which yolk is extruded from the cells themselves
into the space surrounding the blastomeres. In Dasyurus (fig. 130),
according to Hill, extrusion takes place before cleavage begins in the
form of a yolk body at the vegetative pole, but in Didelphys the yolk
THE MARSUPIALS 187
 
is passed out during the first few cleavages and at no time forms a concentrated mass. It is thrown out from both ends or from all sides in
greater or less amount during the early divisions. The greatest amount
seems to be given off between 2- and 4-cell stages and since the yolk is
distributed around the periphery of the egg no one point is the center
of the extrusion. The orientation of the eggs likewise differs in these two
genera. According to Hill the accumulation of the yolk marks the vegetative pole. The first three cleavages of Dasyurus are meridional but
the fourth is horizontal and divides the eight blastomeres into an upper
ring of eight small lighter-staining cells and a lower ring of larger more
darkly staining blastomeres. The upper cells are regarded by Hill as
formative or embryonic and the
lower ones as non-formative giving
rise to the outer layers of the
embryos which are spoken of as
trophoblastic. The embryonic portion is derived from the small cells
of the 16—cell stage and therefore
from the vegetative half of the egg
as marked by the earlier extrusion
of the yolk body. The larger cells
from the animal region of the egg
produce the trophoblastic portion.
In Dzdelphys no such orientation
can be found. Here the first cleavage wF)‘?mg2 ( flfgvage Smges Bugle :0‘
divides the egg into two blastomeres mrgtlnianus EAR;  D 1,8
without any indication of polarity A. sectlon through 2-0811 stage. B.
 
... .. tth h4—llt PB,l
or of qualitative differentiation. The f,e(:i;,°’nY 32$‘ ma°s:e:' ;“°P' zonapggf
 
Second cleavage plane is in general lueida, C, section through stage with
about at right angles to the first,  D’ mm" th'°"gh “age mm
but a shift takes place by which two
 
opposite blastomeres come into contact with each other as is typical of
many eutherian eggs. Thus no section can be cut through the centers
of all four blastomeres.
 
From the 4-cell stage on, the cleavage of the opossum egg is irregular,
it being possible to find stages of 6, 8, 10, 12, 15, cells and others. The
space between the blastomeres represents a blastocyst cavity and even
in the early stages the blastomeres tend to migrate to the wall of the
“ovum” and arrange themselves in contact with it. Here they flatten
and their outer surfaces take on the curvatures of the surrounding
albumen layer. Thus the yolk is left within the cavity formed by the
 
dividing cells which are uniform in size and structure throughout. The
188
 
FORMATION OF THE MAMMALIAN EMBRYO
 
embryo is now spoken of as a blastocyst which is regarded as completed
 
by the 32—cel1 stage.
 
 
fiG. 131.
 
 
Drawings from models of the opossum egg. (After Hartman.)
 
A. 2-cell condition; B. 6-cell stage showing polarity and the fate of the two l’)lu.StUI1ll:I‘(“$
of the preceding stage; C, 16-cell stage; D, a blastocyst of 40 to 50 cells in which no e\ idence of polarity is seen. although it will shortly be reestablished with reappearance of
 
the endoderm.
 
The blastocyst of Dasyurus is formed in a different manner. Here the
cells of each ring multiply rapidly but continue to occupy their hori
 
   
 
C
 
Sections through the
(After
 
fiG. 132.
blastocyst of the opossum.
Hartman.)
 
A. section through the blastocyst of
70 cells but without endoderm, B,
section through blastocyst of 82 cells
showing six of the ten endoderm
mother cells; C. little later blastocyst
showing differentiation of the embryonic area and trophoblastic ectoderm.
 
zontal positions. Upon reaching the
periphery they too become applied to
the inner surface of the shell, the formative cells at one pole and the non-formative at the other. This constitutes a
blastocyst of one layer of cells, a unilaminar blastocyst. Here too the yolk
remains within the cavity. Presently
the cells of the formative ectoderiii
become differentiated and a little later
endoderm formation begins. Individual
cells (called endodermal mother cells)
migrate in an amoeboid manner below
the surface and there unite to form a
second layer, the endoderm. This layer
continues to proliferate and finally
closes up to form a complete lining for
the entire blastocyst, the primitive
endoderm. This description of the
formation of the endoderm by Hill
seems to concern an entirely different
method from that found elsewhere
among the mammals.
 
Hartman also describes endoderm mother cells which detach themselves from their place in the blastocyst wall and behave in the manner
THE MARSUPIALS 189
 
closely resembling that described for Dasyurus. The important difference
here lies in the impossibility of distinguishing formative and nonformative cells among the early blastomeres a11d of relating such cells
to the trophoblast and to the ectodcrm of the unilaminar blastocyst.
 
B
 
fiG. 133. Continuation of fig. 125. A. B, showing progressive differentiation of the
endoderm and trophoblast.
 
Clearly there is no way by which the endoderm mother cells can be
traced back in the opossum to the early cleavage stages and, as Hartman remarked, cleavage is entirely indeterminativc.
 
While the cleaving ovum of Dasyurus shows a greater degree of determination and much more marked polarity than is the case in Didelphys,
190 FORMATION OF THE MAMMALIAN EMBRYO
 
Hartman is in agreement with Hill on the general facts as to marsupial
development. Even in the opossum egg a polarity of a sort is shown in
the fact that the cells in one hemisphere divide more rapidly than those
in the other and it may be assumed that the embryonic area is formed
by the cells of the more rapidly dividing group and the trophoblast
from those of the other. In discussing the formation of the embryo of
Eutheria it will appear that the “inner cell mass” of the latter is homologous with the embryonic area of the marsupials and the trophoblast of
both groups show a complete homology, a view in which both Hartman
and Hill join. In the Eutheria, however, it is held that the trophoblast
comes from one of the two blastomeres of the 2-cell stage and the inner
cell mass from the other. Clearly the fate of the two blastomeres is different in these two groups for in the marsupials one half of each blastomere goes into the production of the embryonic area and the other half
into the trophoblast.
 
Endoderm Formation
 
The embryonic area having become localized, a number of small cells
undergo modification and become the endodermal mother cells previously referred to. This process begins to take place in blastocysts
containing 50 to 60 cells. The cells increase in size, project into the
blastocyst cavity, and undergo other recognizable changes. Presently
they free themselves from the wall of the blastocyst and by putting out
extended tips come in contact with each other so that a layer of endoderm is formed. Sometimes several divisions take place on the part of
these cells before they have detached from the wall. The process of true
endoderm formation in the opossum and in Dasyurus as well is thus one
of the multiplication and migration of cells differentiated as endodermal
mother cells from one pole of the blastocyst wall and in no case does it
include more than one half of the entire blastocyst, the other half being
made up of trophoblastic cells. It will prove interesting to compare this
process with that of the placental mammals.
 
Hartman holds that the opossum egg is intermediate between that
of Dasyurus and the placental mammals in its type of development. In
size, in absence of polar differentiation in the unsegmented egg, in the
crossed arrangement of blastomeres in the 4-cell stage, in indeterminate
cleavage, and in early proliferation of endoderm it approaches the conditions of the Eutheria. But in the lack of a morula stage, of an inner
cell mass as such (although the embryonic area is homologous with it),
and in the method of endoderm formation it resembles Dasyurus. The
large size of the latter as compared to other mammals, and the localization of the yolk mass in one portion of the egg (not far removed from
ENDODERM FORMATION 191
 
the telolecithal condition), remind one of the derivation of these forms
from a reptilian ancestry.
 
The blastocyst of the opossum during its later stages undergoes some
important changes, most of which are concerned with its growth and
enlargement. Its growth takes place by means of spreading and attenuation as well as by the more rapid multiplication of the trophoblastic
 
 
D
 
Fm. 134. Later blastoeysts of the opossum. (After Hartman.)
 
A. just completed bilaminar blastoeyst. B, a later blastocyst nearly ready for the uppeurance of the mesoderm; C, D, sections showing details of the trophohlast and of the
embryonic eetoderm respectively.
 
emb. ec-t., embryonic ectoderm; tr. ect., trophoblastic ectoderm; s.m., shell membrane; alb.,
albumen.
cells. finally a maximum size of 1.0 to 1.5 min. is reached and the
trophoblastic region has come to occupy from four—fifths to five-sixths
of the entire surface of the blastocyst. That is, the increase in size concerns the trophoblastic region mainly, the embryonic area growing very
 
slowly if at all.
The cells of the embryonic area become much crowded and the endo
derm attains a depth of three or four cells without taking on an epithelial character. The’ cells of necessity are irregular in size and shape.
Then largely because of the migration of the endoderm cells they begin
192 FORMATION OF THE MAMMALIAN EMBRYO
 
to spread. While this migration is active on the part of the cells, no
amoeboid movement has been detected by Hartman. With this process
the blastocyst becomes biconvex in form, the flattening occurring in the
direction of the egg axis with the formative area pressed against the
shell membrane. The continuous growth of the trophoblastie area finally
brings it also in contact with the shell membrane, thus effecting for the
blastocyst a. return to the spherical shape and completing the formation
of the blastoderm.
 
Meantime the endoderm continues its lateral migration until it has
reached the trophoblastic pole of the egg, that is, until it has reached
the point opposite its own place of origin, and thus a closed endodermal
sac is formed within the ectoderm. During all this time the ectoderm
has remained as a single layer of quite flat cells. N ow, however, these
gradually thicken and become cuboidal. With this condition reached,
the formation of the blastocyst of the opossum is completed. From the
formative area, the embryo proper is developed in a manner quite comparable to that of the placental mammals; this phase of its embryology
is not taken up here as a separate subject for discussion, since the formation of the embryo in the placental mammals is the subject matter of
the next division of this chapter.
 
III. HIGHER MAMMALS
 
1. General Discussion
 
The third distinct embryological group of mammals is made up of
the Eutheria or Placentalia. The eggs differ from all others in a number
of characteristics, the first of which is the size, for all are microscopic.
They range from 0.07 mm. in the mouse to 0.145 mm. in the dog and
0.13 to 0.14 mm. in man. (These figures are from Hartman’s calculations.) Even at this small size, however, the eggs are large in comparison
to other cells of the body, for here as in other animals there is an accumulation of yolk within the egg. In the older works it was commonly said
that the eggs of mammals are alecithal or yolkless. As already pointed
out in an earlier chapter this is untrue, for although it is small in amount
in the eggs of Eutheria some yolk is present in every sort of egg.
 
The term isolecithal or homoleeithal previously used in this work for
such eggs as these is better applied here than alecithal and some writers
use also the terms mieroleeithal, or small-yolked, to distinguish these
eggs from the more usual and larger-yolked types which are spoken of
as megaleeithal. Although more sparsely distributed than in other eggs,
spherical yolk granules and often fat globules as well are to be found
in the eggs of mammals.
DEVELOPMENT UP TO THE BLASTOCYST 193
 
The lack of yolk in the eggs of placental mammals is one of the two
major factors which are responsible for a very extensive modification
found in the early embryology of these forms. Derived as they are from
forms that are highly laden with yolk with an extremely discoidal type
of development, it is not to be expected that the reduction in yolk
would mean for the Placentalia a return to the simple methods of development which are found in the holoblastic regularly cleaving forms, as
for example the echinoderms and amphioxus. The presence in all forms
of Plaeentalia of a yolk sac, which is derived through the discoidal
ancestry, is an evidence, although it contains no yolk, of the lack of
simplicity in the development of these forms. The marsupials we saw
constituted a step toward the reduction in yolk, for there the yolk was
eliminated during the first cleavages. Not even the elimination takes
place among the higher mammals for so little is present that it is easily
used up during the early divisions. The lack of a yolk—filled hemisphere
in the uneleaved mammalian egg very obviously means a most striking
modification of the type of development, for in the discoidal monotreme
only the animal half of the egg participates in the formation of the
embryo. The fate of the yolkless vegetative half in the formation of the
trophoblastic portion of the egg has already been foretold in the formation of the blastodise of the marsupials.
 
The second major factor in bringing about the modifications which
are characteristic of higher mammals is also correlated with the yolkless
condition. It is the (levelopment of an entirely different mechanism for
supplying nourishment to the embryo and foetus before birth and takes
the form of a placenta. The segmenting ovum becomes related to the
uterine wall in a most intimate manner. This process is called placentation.
 
As a result of the factors mentioned the mammalian egg develops
through a blastoeyst stage. Clearly it is difficult to work out the hon1ol—
ogy between this type of embryo ‘formation and that of the forms
described in previous chapters. Indeed some writers on mammalian
embryology have positively denied the homologies that would be implied
if we use the terms descriptive of the embryology of earlier forms for
the conditions in the mammals. Such terms as formation of germ layers
and primitive streak, ete., may lead to confusion and even contradiction
 
2. Development up to the Blastocyst
 
The ovarian egg of mammals exhibits certain characteristic features.
It is formed within a follicle which consists morphologically of the same
sort of germ cells as itself, but after one of them differentiates in an
early embryological stage to become the ovum the remainder develop
I 94 FOR M ATION 01*‘ THE M AM M ALIAN EM BR YO
 
only into follicle cells. The ovary of the mammal at the time of its biith
is said to contain in an undifferentiated condition all of the oogonia.
which are to be developed during its later life.* That is, the multipli—
 
‘I\\ ‘
lll ll \\\\§\\ ‘,2
 
l \§_u
 
J’
 
fiG 135. Section thioiigli ow an of ('4 dog (l min Kellicott, iiftcr \\ aldeyer)
 
0., ‘ Germinzil epithelium ', l) egg tubes c, suiiill ox anon follicles, d. older Uvflrldll follicles, c, ovum surrounded by discus proluzerus, f, semnd ovum in follicle with (- (Onlv
rarely are two ov.i thus found in in single follicle) 3:, outer capsule of the follicle, h, inner
capsule of the follicle. i, nieinbmmi granulosa, k, collapsed, degenerating follicle, 1, blood
vessels. in. sections through tubes of the parovarium, y, iiivolutcd portion of superficial
epithelium, z, tmiisitioii to p(‘l‘lt0l'|C"tl epithelium.
 
cation period is past at the tiuie of birth. Many of these cells are utilized
only in the production of the follicle cells which surround each developing ovum. They multiply, become columnar, and form a follicular epitheliuin. On one side only of the follicle a definite accumulation of cells
 
* In 8. recent paper, Hargitt (Jour Morphology and Physiology, Vol 50, 1930)
l’m1l((‘\ the claim that in the ovanes of some mammals the production of germ cells
ifi continuous
DEVELOPMENT UP TO THE BLASTOCYST 195
 
known as the discus proligerus surrounds the ovum while on the other
side a cavity is left by the separation of the cells of the follicle from
each other as the structure enlarges. This cavity becomes gradually
larger, and is filled with a liquid, the liquor folliculi.
 
The fully grown follicle is known as a Graaflan follicle. The egg itself
passes through its growth period in this follicle and becomes surrounded
by definitely recognizable layers. The presence of the vitelline membrane, derived from the ovum, is a matter of dispute in various main
Fru. 136. Fully grown human ooeyte just removed from the ovary. (From Kellieott.
after Wuldeyer.)
 
Zena pellueida and follicular epithelium (corona radiata) outside the oot-yte. Nucleus
in germinal vesicle stage.
 
mals. The secondary membrane derived from the follicle is present as
a zona pellucida. Often this membrane is so perforated by tiny canals
as to give the appearance of radiation in the membranes and hence is
spoken of as the zona radiate. In some forms this is surrounded by a
layer of regularly arranged follicle cells spoken of as the corona radiate.
 
The beginning of maturation occurs at the end of the growth period
when the egg is ready to escape from the ovary. The first polar body is
given off before the ovum has eserred. In the mouse this process is
said to take place one-half hour before ovulation. Then the Graafian
196 FORMATION OF THE MAMMALIAN EMBRYO
 
follicle is ruptured, the ovum escapes into the periovarian space, and is
carried into the fimbriated ostium of the oviduct which is in close proximity. The second polar spindle has already been formed and the second
polar body is given off after fertilization in the upper part of the oviduct.
Related to ‘the process of ovulation are changes in the follicle, which is
converted into a corpus luteum, as well as physiological changes of great
importance to the organism. However, the history of the embryo, which
is the subject of this discussion, does not require the further consideration of these changes connected with the ovary itself, although they are
of greatest physiological importance. The cleavage stages occur slowly
as the egg passes down the oviduct. Twenty—four to forty-eight hours
elapse before the completion of the first and second cleavages in the
mouse. In the rabbit fourteen or fifteen hours are occupied by the first
cleavage and a correspondingly longer time elapses before the ovum
reaches the uterus. Eighty hours are required in the mouse for this
passage through the oviduct, four days in the rabbit, eight to ten days
in the dog and in certain ungulates it is said that the ovum remains
over the winter in the oviduct. Cleavage is total and at first nearly
equal, but rapidly becomes very irregular. figures are available for
various animals showing cleavage stages consisting of almost any number of cells up to sixteen or twenty. Evidently it is impossible to determine for these eggs the orientation, polarity, and such facts of promoi-—
phology as have been shown to apply to eggs of lower forms. Cleavage
results in a mass of cells spoken of commonly as a morula. The cells
at the outside become differentiated to form a subzonal layer lying next
to the zona pellucida while those within the mass constitute the inner
cell mass. The inner cell mass is in contact with the subzonal layer on
one side but elsewhere a cavity is formed between it and the outer cells.
The subzonal cells are also spoken of as a trophoblast or simply as the
wall of the blastodisc vesicle, and their relation to the trophoblast of
the marsupials is clear from the description already given for those
 
forms.
 
3. The Blastocyst
 
The homology of the inner cell mass with the embryonic or formative
area of the marsupial as shown by both Hartman and Hill has also
been mentioned. The view held by some that the trophoblast of the
Eutheria comes from one of the two blastomeres of the 2-cell stage while
the inner cell mass is derived from the other is based on evidence from
some forms only and probably cannot be maintained with certainty for
all mammalian types owing to the difficulties in determining the orientation. The cavity of the blastodermic vesicle or blastocyst becomes filled
fiG. 137. Developing eggs of the rabbit. (After Van Beneden.)
A, so-called metagastrula gtage preparatory to the formation of the blastocyst; B, beginning of znstrula cavity. the formation of the inner cell mass.
198 FORMATION OF THE MAMMALIAN EMBRYO
 
with a fluid which is supposed by some to represent the yolk of lower
forms. The subsequent history of the blastocyst varies in different groups.
 
There are three important stages in connection with the early history
of the formation of the embryo. The first is the growth of the blastodermic vesicle during which it takes on the form typical of the particular
animal discussed. The second is the formation of the embryo body proper;
this stage involves the subsequent history of the surrounding layers of
cells. The third is the implantation of the blastocyst in the uterine wall
and the formation of the placenta; this stage scarcely comes within the
scope of this discussion and can be considered only in passing.
 
The growth of the blastocyst takes place in a manner similar to that
described for the marsupial, the trophoblastic cells becoming extended
and flattened and the cells increasing rapidly in number. Cell division
at this stage takes place much more rapidly than in the earlier cleavage
stages, for in three days after the embryo has reached the uterus in the
rabbit it is ready for implantation. In other cases a somewhat longer
period is necessary. The size of the vesicle at the end of its growth like
the size of the mammals themselves is variable, as is also its shape. It
is spherical in the mouse, ovoid in the rabbit, and in the ungulates is
long and tapering, reaching a length of 20 cm. in the sheep of twelve
days although the diameter remains nearly constant, a couple of millimeters. This growth, as in the opossum, is limited to the trophoblast,
the inner cell mass remaining very small and restricted.
 
Up to the conclusion of the growth of the blastocyst no distinction
as to ectoderm and endoderm has been possible among its cells. Formation of the endoderm now begins as described for the opossum from the
differentiation of those cells of the inner cell mass which border the
cavity of the blastocyst. Here these cells multiply rapidly and at the
same time migrate so that they come to form a layer over the entire
inner surface of the trophoblast which in this manner becomes twolayered and may be spoken of as a gastrula. Obviously this method of
endoderm formation is more closely related to that of eggs cleaving discoidally than to that of the holoblastic types. In some mammals, notably
the primates, the endodermal layer remains much smaller than the
blastocyst itself, thus forming a double-layered vesicle whose outer layer
is separated from the inner by reason of its more rapid growth. Thus
of the inner cell mass the layer bordering the cavity becomes embryonic
endoderm and the remainder is spoken of as the embryonic ectoderm.
From this mass is to be differentiated the body proper of the embryo.
It is formative in the strict sense, for all of the embryo is derived from
it. The cavity of the blastocyst with its endodermal lining is now spoken
of as the yolk sac and, although it contains no yolk, is reminiscent of the
Fm. 138. Continuation of 130. A, B. growth stages in the formation of the blastula
cavity and the transformation of the inner cell mass into a plate.
200 FORMATION OF THE MAMMALIAN EMBRYO
 
large-yolked reptilian forms. The inner cell mass minus the yolk sac
endoderm which, though once part of it, has migrated away is now
restricted to embryonic endoderm and embryonic ectoderm above it; by
this time it should be spoken of as the embryonic knob. It is the history
of the embryonic knob which especially concerns us.
 
fiG. 139. A. B, diagram showing the early formation of the blastocyst and the relation of the ectoderm, endoderm, and trophoblast; C, diagram of the development of the
insectivore Tupaija from Hubrecht's observations showing the development of the cavity
of the ectoderm which opens out to form the embryonic shield: I), development of hedgehog type, also after Hubrecht‘s observations. (Modified from Keibel.)
 
At about the time when the embryonic knob is distinctly recognizable,
implantation takes place. That is, the blastocyst becomes attached by
means of the trophoblast to the wall of the uterus and the placenta
begins to form. Of implantation there are three types.
 
(a) Central, found in Carnivora and Ungulata, in some rodents including the rabbit in which it was first described and in the lower primates. In this type the blastodermic vesicle attaches directly to the
uterine wall, projecting as it grows into the cavity of the uterus.
THE BLASTOCYST 201
 
(b) Eccentric, as in the mouse and Inseetivora where a uterine fold
forms in which the vesicle lies and is later enclosed as the edges of the
fold come together.
 
 
 
 
 
     
 
I’-/7‘
1.
 
Fro. 140. Series of diagrams to show development with entypy of the germ. A, the
relations of the embryonic knob, the endoderm, and the trophoblast; B, later stage showing the cells of the embryonic knob arranging themselves to form an embryonic shield
with the amniotic cavity and Rauber’s layer above it; C‘, later stage in its development.
I), Still later stage showing inversion of germ layers. (Modified from Hubrecht’s observa
tions on the hedgehog.)
 
(c) Interstitial, as in the guinea pig, most rodents, and in man. Here
the vesicle makes its way into the mucous lining of the uterus and after
becoming embedded therein is entirely covered over by the mucosa.
 
The time relations of the development of early stages in the mammals seems worthy of note, for a very much greater amount of time in
202 FORMATION OF THE MAMMALIAN EMBRYO
 
relation to the entire embryonic period is consumed by these earlier
stages in the mammals than is the case in tlie Sauropsida or in other
lower forms. Even the cleavage stages take place much more slowly.
It has been suggested that the delay in the development of the embryonic shield (sce below) until after implantation has been accomplished
 
fiG. 141. A, B, diagram showing the rapid enlargement of the extraembryonic coelome
and the cliorionic vesicle. (B, modified from Bailey and Miller.)
 
is due to the very meager nutrition of the embryo during the period in
which it is free in the uterus. This view is perhaps borne out by the
sudden rapid development which takes place immediately after implantation has been accomplished. Yet it is hard to understand why the
cleavages should be slowed down to such an extent as we find to be the
case if the factor of nutrition is the only one involved, for during the
cleavage stages at least a small amount of yolk is always available.
THE AMN ION 203
 
In the meantime the embryonic knob has continued its development
and mesoderm has been formed. As the extraembryonic mesoderm grows,
it pushes in between the trophoblast and the yolk sac endodcrm and
the entire extraembryonic wall takes part in the formation of the socalled chorion, the serosa. Sometimes the trophoblast is spoken of as
the chorionic ectoderm. The formation of the mesoderm in the mammal
is a less conspicuous process than in some of the lower forms. It takes
place entirely by delamination and migration of cells which are usually
from the ectoderm. In some forms it is stated that the mesoderm is
related to the endoderm but certainly the usual derivation is from the
embryonic ectoderm. It will be noted that this separation of the mesodermal layer takes place before the formation of a primitive streak or
any other elements of the body proper.
 
4. The Amnion
 
We may now return to the behavior of the embryonic knob as such.
From this structure are derived not only the embryonic shield, which
corresponds in a general way to the blastodermic disc of Sauropsida,
but also the amnion and the structures connected with it. It is necessary
to consider the formation of the amnion before taking up the origin of
the embryonic shield. Mammals show two separate methods of the formation of the amnion depending apparently upon the relations of the
trophoblast to the embryonic knob. In some forms the trophoblast comes
to be interrupted over the embryonic knob which thereupon develops
in a manner that is entirely different from the cases in which the trophoblast is continuous. In the latter case the trophoblast cells are said to
constitute Rauber’s layer.
 
The details of the formation of the amnion under these two conditions
vary in the different orders of the mammals and cannot be gone into
here. The important features only can be pointed out. Taking up first
the case in which the trophoblast is interrupted above the embryonic
knob, we find two different methods by which the amnion is established
although its subsequent history is quite alike in both cases. In the one
which is illustrated by the inseetivore Tupaija studied by Hubrecht,
the knob develops a cavity which opens to the outside as a groove. The
edges of this groove make contact with the trophoblast adjoining them
and later fold over to form the amnion itself. The bottom portion of the
groove gradually flattens out and it is this area which becomes the embryonic shield and from which the body of the animal develops. In the
other case as illustrated by the rabbit, the cells of the knob take on the
form of a flat plate without the formation of a groove, but their edges
are connected with the trophoblast and fold upward to form the amnion
204 FORMATION OF THE MAMMALIAN EMBRYO
 
as in the preceding case. There is here suggested a certain relation to
the method of formation of the body of the embryo and the amnion
in those forms having typical discoidal cleavage such as the birds and
reptiles. The subsequent development of the embryonic shield in these
forms also recalls that of the sauropsidan blastoderm. (figs. 139 and
140.)
 
flu. l42.—Sections through four stages in the early development of the insectivorc
Tupaua javanica. (From Kellicott, after Hubrecht.)
 
A, blastodermic vesicle completely closed. endoderm still continuous with the embryonic ectodcrm. B, C, embryonic ectoderm split and folding out upon the surface of the
vesicle. pushing away the trophohlnst cells: D, embryonic cctoderm forming a flat disc
on the surface of the blastodcrmic vesicle.
 
E, inner cell mass ("ectodermal shield"); ec., embryonic ectoderm; en.. endoderm; tr.,
trophoblast.
 
The second method of formation of the amnion differs in many particulars from the first. The trophoblastic layer entirely covers the embryonic knob, a condition which is known to mammalian embryologists
as entypy of the germ, and because of it the so-called inversion of the
germ layers is brought about. It will be recalled that the embryonic
C
 
   
 
 
 
 
 
 
2,.  u..@...
 
5.1.  nu.
 
 
 
.«>..\hK
 
 
 
fiG. 143. Sections through the blastodermic vesicle and blastocyst of the albino rat.
 
(After Huber)
A, stage of 6 days 14 hours; B, 7 days; C, egg cylinder stage of 8 days.
206 FORMATION OF THE MAMMALIAN EMBRYO
 
knob may be likened to a hanging drop projecting within the cavity of
the vesicle and that the lining of the cavity is endoderm, although this
actually covers the outer or convex surface of the knob. Within the
ectodermal portion of the knob where the cells are loosely arranged
spaces now appear which gradually coalesce and they form the amniotic
cavity. The ectodermal cells forming the roof of the cavity become the
ectodermal layer of the amnion. The floor of the cavity on the other
hand becomes the embryonic shield. The inner layer of the shield is
thus ectodermal while the layer which for a time is actually the outer
is endodermal. (fig. 143.)
 
In some cases, of which the guinea pig and the mouse are examples,
the embryonic knob moves gradually to a position well down inside
the blastocyst. This process carries with it the lengthening of the endodermal layer on the outside. Earlier students of these forms removed
the outer layers of the blastocyst and came upon the embryonic knob
which they properly regarded as the formative area. Because of the
removal of the outer layers, however, they completely misinterpreted
the method of development and were surprised to discover this covering
layer to be of endoderm. Hence they spoke of the inversion of the germ
layers in these forms and the phrase is still retained in the literature of
mammalian embryology, although of course it has no real significance
as will be seen from the future development of the body form.
 
In some forms it happens that the trophoblast layer covering the
embryonic knob becomes thickened forming a trophoblastic knob above
the embryonic knob proper. This is the Trdger of various writers on
mammalian embryology. This may enlarge and in the forms just referred
to accompanies the embryonic knob in its growth into the cavity of the
vesicle. Within this trophoblastic knob a second cavity may occur called
the false amniotic cavity. It has no relation to the true amnion, a completely closed vesicle, and presently disappears without further significance. In certain cases other spaces also develop as in the case of the
interamniotic cavity between the cavities of the true and false amnions
in the guinea pig. The false cavity may reach a relatively large size in
the early stages while the true amniotic cavity remains quite small.
Later on the relations are reversed.
 
5. Embryonic Shield
 
Regardless of the methods of formation of the amnion there arises
in the development of all higher mammals a plate of cells from the
lower cells of the embryonic knob in connection with the endoderm
which lies just beneath it. This plate of cells is the embryonic shield
and from its subsequent development the embryo proper is derived. Of
EMBRYONIC SHIELD 207
 
the entire blastocyst and all the structures connected with it, it is the
only true embryonic portion.
 
In many respects the embryonic shield of the mammal is comparable
in its developmental processes to the blastoderm of the chick or other
discoidal type. Its development has been studied in a great variety of
mammals including the bat, dog, mouse, rabbit, guinea pig, mole, hedgehog, pig, and of course man.
 
As one looks down upon the shield after the trophoblast has been
removed from above, the similarity to the chick is so striking that a
very brief description will be sufficient to make clear the main point in
development. It consists of a layer of embryonic ectoderm three or four
 
 
fiG. 144. Surface view of the embryonic shield of a dog. 13 to 15 days. (After Kellicott.)
sh., embryonal shield; k.n., Henson's node; p.s., primitive streak.
 
cells thick under which is a single-celled layer of endoderm. This stage
is reached during the seventh day in the rabbit and about the fourteenth
in the dog. Then there occurs in the middle region of the disc a thickening and condensation of the cell layers to form Hens0n’s node or the
primitive knot, and extending backward from this is a rather broad
line which disappears in the thicker cells of the posterior margin of the
shield. Henson’s node and this broad line are of course recognizable as
the primitive streak, and shortly extending along its middle the primitive groove is to be discerned. In front of the node the mesoderm can
be easily made out in sections appearing as a sheet between the ectoderm and the endoderm. This sheet early separates and, as has already
been stated, its extension into the extraembryonic area participates
in the formation of the serosa. It is supposed that the mesoderm takes
208 FORMATION OF THE MAMMALIAN EMBRYO
 
its origin from the region of Henson’s node. From the primitive streak
stage on, the arrangement of the layers and parts of the blastoderm are
not different in any fundamental particulars from that already noted
for the Sauropsida. This is to be expected from the relations of the yolk
sac, as already remarked, and shows that the conditions found in the
mammals represent a modification of the type of development where a
large mass of yolk is present. The development of the body cavity,
embryonic and cxtraembryonic, of the splanchnic and somatic layers of
the mesoderm, appearance of the head fold, and the other characteristic
features of the sauropsidan type of development have their counterparts here, and as it is not the purpose of this chapter to discuss mammalian embryology after the body form has been established, it seems
unnecessary to go into these matters. For a discussion of them the
 
reader is referred to the many available accounts particularly of human
embryology.
 
BIBLIOGRAPHIC NOTE
 
Among the more important accounts of the subjects contained in this chapter
are the following: Caldwell, Gatenby; Hill, Hartman; Assheton, Jenkinson, W.
Heape, Heuser and Streeter, Huber, Hubrecht, Patterson, Minot, B. M. Patten,
 
Van Beneden, Wilson and Hill. These works are cited in full in the bibliography on
page 406.
 
===Chapter XI Egg and Embryonic Membranes===
 
I. EGG MEMBRANES
 
The eggs of all animals are covered with one or more membranes
and in these coverings there is a wide range of variation due largely to
the environment and to the rate of development of the eggs. Those
which are surrounded by water develop rapidly and are produced in
great numbers, as are eggs of marine invertebrates, and are scantily
provided with coverings. Those which take a long time for development,
 
as birds’ eggs, or those which are exposed to unfavorable conditions,
as insect eggs, have more and thicker egg membranes.
 
Egg membranes are classified with reference to their origin. Primary
egg membranes are formed by the egg itself, secondary by the follicle
cells around the egg, and tertiary by the uterus or oviduct. All three
types of membrane are sometimes found covering one egg, as in one
of the cockroaches, Periplaneta.
 
If only one egg covering occurs, this can be secondary or tertiary,
for example the egg of Distoma which is covered by a secretion from the
oviduct. Only in exceptional cases are the egg membranes cellular as
the zona radiata of Taenia, the spindle—like egg-shell of Echinorhynchus,
the chitinous indented shell of Hydra, and the layers covering the
ascidian egg. These membranes are really embryonic membranes. In
the case of Hydra there are two membranes which are formed after
cleavage from the ectodermal cells.of the developing embryo.
 
The eggs of some animals have been described as naked. Although
they may possess none of the three membranes described above as
primary, secondary, or tertiary, still they are not actually naked. We
now know that all eggs possess a cortical layer, the outer part of which
has been called a plasma membrane. This structure is really a delicate
surface layer of cytoplasm which cannot be distinguished from that
which underlies it but which is physically different from it. The presence
of the layer has been demonstrated by micro-dissection experiments
(Chambers and others) which show that the surface of the egg is firm
and somewhat elastic, offering resistance to mechanical injury. Plas
molysis experiments have shown that this layer is a semi-permeable membrane and that it plays an important role in regulating the exchange
which takes place between the cell and its surroundings.
 
In the animal kingdom as a whole there is an astonishing variability
in the manner in which egg coverings appear. In sponges, the development of the egg within the adult body makes membranes unnecessary.
They are lacking also in Hydrozoa, Siphonophora, and Anthozoa, although some coelenterates do have them. In some of the lamellibranchs,
as Drezssensza, no membranes are present, and the eggs of some others,
as M ytilus, have them in the beginning of their development and later
 
 
fiG 145 Cross section of egg of Hydra arzsea (Redmwn from Korsehelt and Heidor,
after Ehrenberg and Brauer )
 
cc, ectoderm, en. endoderm with volk granules, im , inner membrane, om. outer
membrane
 
throw them off. In some animals, as echinoderms, the eggs are without
membranes when shed into the water but the fertilization membrane
is formed as soon as the sperm enters the egg.
 
A. PRIMARY MEMBRANES
 
Vitellme Membrane. In many and perhaps in all eggs, there is a
vitelline or fertilization membrane. This membrane is the most constant
of the primary membranes, though it is often difficult to see before
fertilization. Early workers had thought that the fertilization membrane
was formed at the moment of fertilization, for, in many eggs, as for
example in those of echinoderms, it separates from the egg immediately
after fertilization. The presence of this membrane, often some distance
from the egg, is an index of fertilization. Its origin is not clearly known.
PRIMARY MEMBRANES 211
 
It has been thought by some to represent a precipitation reaction, by
others to be merely the outer layer of
 
the egg which has been lifted away,
or to be a substance produced at the
time of fertilization. The separation
of the vitelline membrane may be due
to several causes, as follows: the egg
itself may lose water and shrink, the
membrane may swell, or the substance
between the egg and membrane may
absorb water. The space so formed
between the egg and its fertilization
membrane is the perivitelline space.
(See fig. 7 ) Its size varies considerably
in different species.
 
In some eggs the vitelline membrane
is apparently lacking and the egg is
covered directly by a chorion or secondary membrane as in the cephalopods.
In many eggs it is present before the
sperm touches the egg, though the
evidence that all eggs possess it is not
conclusive. There are many vertebrates
in which it has not been recognized,
although for some representatives of
nearly all classes of vertebrates it has
been described. In these animals it is
frequently termed the zona pellucida
or, if it is traversed by pores, the zona
radiata. It is possible that the vitelline
membrane of the ripe vertebrate egg
may be the result of the fusion of the
primary and secondary membranes of
an earlier stage.
 
Amphioxus is described as having a
thin vitelline membrane formed near
the end of the growth period. When
the egg is shed into the water, another
membrane, the perivitelline, is formed
inside the first, a space intervening fie 146 Successive stages in the
 
between the two. ‘But immediately c,l,,e.:/ne,l?f:,l,'::":,,°fC31:‘:la:““(:'}:r"'§‘$$.‘f
 
upon the entrance of the sperm, the facher.)
212 EGG AND EMBRYONIC MEMBRANES
 
inner membrane hardens and the two fuse. Thus is formed the fertilization membrane which is separated from the egg by the perivitelline space.
 
The vitelline membrane is usually structureless, transparent, and
devoid of canals. It is found throughout all the animal phyla, although,
it may be, ndt universally. Often it forms very quickly at the moment
of fertilization as just mentioned, but there are cases in which it appears
more gradually. In the latter instance, as in Cycles, the attachment
of the egg to the ovarian wall remains as the micropyle. A micropyle
is not always present in the vitelline membrane, for sometimes it is
unnecessary, since in some eggs fertilization may take place before its
formation and in others it is porous and easily penetrable by the sperm.
There are, however, some invertebrates, as cephalopods, in which the
vitelline membrane is lacking.
 
The true vitelline membrane is a part of the egg itself, but it proves
difficult in some eggs to determine whether the membrane which has
been designated the vitelline is really primary or secondary. Confusion
also seems to exist regarding the origin of the zona radiata, the membrane which lies next to the vitelline membrane. In some eggs, as in
selachians and in Petromyzon, the zona radiata lies inside it, and in
others, as in the teleosts, the zona radiata lies outside it. This membrane
derives its name from the radiations which are seen in cross section and
which in the vertebrates at least are due to fine canals.
 
To classify properly the vitelline membrane and zona radiata of a
particular form as belonging to the primary membranes we must know
their origin, and this may be very difficult to ascertain. A review of the
text—books will show that these names have been given to diverse
coverings in many cases without any knowledge of their origin. Hence
it will be clear that the membranes as so named are not homologous in
all forms. The question is not of great importance, but is considered
only because of confusion in the terminology.
 
It is obvious that the egg itself, if not surrounded by follicle cells,
must secrete its own membrane. However, if follicle cells are present
they take a greater or less part in forming the coverings of the egg.
 
Zona Radiata. The zona radiata occurs in some echinoderms, worms,
and molluscs, but there is much doubt as to its origin in these forms.
In some cases it is evident that the membrane is a product of the egg
itself.
 
Lillie has shown that the zona radiata in the Nereis egg is not a
membrane at all but merely the outer layer of the egg protoplasm, and
that it consists of closely crowded alveoli. “The zona radiata,” he says,
“is in fact a coarse emulsion or foam structure. The jelly is formed by
the extrusion or the diffusion of the alveolar contents of the cortical
PRIMARY MEMBRANES 213
layer through the vitelline membrane.” The zona radiata of Nereis
thus secretes the jelly which surrounds the egg. The structures which
seem to be radiations are the collapsed walls of the alveoli. The socalled zona radiata of Nereis is thus not homologous to the membrane
of that name in other forms.
 
The zona radiata has a wide distribution among vertebrate eggs
and is found in all classes. It is in many cases doubtful whether this
layer is formed from the outer part of the egg or from the follicle epithelium. In cases where there are two or more egg coverings it probably
arises from the egg itself. When the zona radiata
arises later than the egg membrane outside it, it
must be formed from the egg, as Eigenmann has
shown for Fundulus.
 
The purpose of the zona radiata in many vertebrates is clear. Through the delicate canals of this
layer, protoplasmic processes of the follicle cells _
penetrate. Nutrient substances from these cells are 5-f
     
 
   
 
passed through the processes to the egg. The pur— fe
pose of the zona radiata is thus that of a nourishing ' I 
membrane. In the vertebrates it is of considerable v.m. —
thickness during the development of the egg. After y
the growth of the egg the layer often diminishes B
 
greatly in size. Fro 147. A portion
 
In the shark’s egg (Balfour, Giacomina) the zona
radiata develops inside the vitelline membrane which
is here a true primary membrane, being formed
before the follicle cells themselves. The zona in this
form is a provisional egg covering for the development of the egg in the ovary. When the egg development is complete, it becomes a thin membrane.
 
Contrasted with the provisional zona radiata of
the selachians is the permanent layer of that name
 
of the egg follicle and
surface layer of the egg
of Scyllmm cam'cula.
(Redrawn from Korschelt and Hcider, after
Balfour.)
 
f.e., follicular epithelium; s.f., secondary
follicular epithelium;
v.m., vitelline membrane; y., yolk; z.r., zona
radiata.
 
of cyclostomes, teleosts, and ganoids. In these fishes the zona radiata
is often divided into two layers or at least there are two radially
striped layers which have the same origin. In some of the fishes as
Perca there is a. gelatinous layer outside of it through which run cell
processes that connect it with the follicle cells. This and other similar
structures frequently present on the surface of the teleost egg would
seem to be ehorionic membranes. However, Eigenmann has shown that
in Fundulus they are derived from the egg itself.
 
Although the origin of the zona radiata from the egg has been determined for the selachians and for Fundulus, more work must be done
214 EGG AND EMBRYONIC MEMBRANES
 
to ascertain what part the follicle cells may have in the formation of
this layer in other fishes.
 
In the bony fishes, since the egg membrane, which is often sticky, is
present before fertilization, the micropyle must be formed in a different
manner from‘ that mentioned above for many of the invertebrates.
 
Eigenmann has described its formation
 
in Pygosteus in which each micropyle
' is due to a long process of one of the
follicle cells that reaches to the egg and
passes through the zona radiata.
 
The eggs of amphibians and reptiles
have a vitelline membrane which later
forms a zona radiata. The formation of
this layer has been clearly described
by Rctzius for one of the lizards, Lacerta
 
 
fiG 148 Section through the fol- _ _ _
hole and outer layers of the egg of vzmdzs. In this form the early follicle 1S
 
fi:'l§:rfi)“”“”l” (‘Um K°“’°h°” and one—layered. In it cells of two sizes may
 
fc’ follicular eI,,the1,um, L gala. be distinguished, large cells, the centers
tmous layer. ov. ovarml epithelium: of which are filled with round nuclei,
§f,‘,,‘,;,,‘§{°°“‘°“‘°“"" ' ’°"" ' ' ' ‘°““ and smaller cells with oval nuclei. The
egg itself has a delicate surface layer,
the first anlage of the zona radiata. This membrane, as in the selachians
and Fundulus, is formed from the egg itself. During the growth of the
egg the zona radiata grows thicker, the large follicle cells become pear
shaped and send processes to the egg. Some of the cells remain round
and lodge between the stalks of the pear-shaped cells. The small cells
take up a more distal position, and meanwhile the processes of the larger ones become branched to penetrate the plasma
of the egg. The follicle now thickens and
the zona takes on its characteristic radiate
structure. finally the follicle cells diminish in size and the follicle itself is thinner. , fiG 149 Mwropyle formation
The nuclei of the large cells lose much of  mus “mamas
their chromatin as the cells are stretched fc , follicular epithelium, t r ,
more closely over the egg. The zona ‘h°°”' ‘°““’““’ Y’ y°‘‘‘' “' 2°“
_ _ radiata.
radiata, in which two layers can now be
distinguished, is likewise thinner. The nourishing function of the follicle
is thus clear, for it is evident that substances are passed to the egg
through the long processes of the follicle cells which penetrate the zona
radiata. It is seldom that the ormation of the membrane is as clear as
 
in this form. (fig. 150.)
!'-?«"?3"-:'o'
fiG. 150. The origin of the egg membranes of Lacerta viridis. (Redmwn from Buchner.
pfter Retzius.) For description, see text.
216 EGG AND EMBRYONIC MEMBRANES
 
In the bird’s egg the primordial follicle contains the ovum surrounded
by a one—ce1led layer of cubical follicle cells,
the granulosa. The zona radiata is later
formed between the ovum and the follicle
cells and there has been considerable discussion as to its origin. Bartelmez thinks
that it is formed from the follicle cells; at
any rate it has a function similar to that
described for the reptiles. The follicular
cells are connected to the ovum by delicate
strands of protoplasm which pass through
Fm_151_ Primordialoggfollicle the zonaradiata.Nutrimentdiffusesthrough
from ovary of hen. (Redrawn from these protoplasmic bridges, there being no
Lime’ after H°u') evidence of the passage of solid food particles.
In the bird the primary vitelline membrane formed immediately
 
 
Fro. 152. Section through an ovarian egg and follicle of the egg of a pigeon. (Redrawn
from Lillie.)
 
ex.. theca externa; g.. granulosa; g.v., germinal vesicle; in., theca interns; p., peripheral
protoplasm; s~s, stalk of the follicle; z.r.. zona radiate.
SECONDARY MEMBRANES 217
 
over the egg as in other animals is a structureless membrane usually
considered as from the egg itself, though some workers have thought
it to be a product of the follicle cells. It is very diflicult to differentiate
the vitelline membrane from the zona radiata and the former may be
in part the anlage of the latter, as in the case of Lacerta which we have
just described.
 
In mammals, the origin of the vitelline membrane is uncertain. Some
authors say that there is no true vitelline membrane; the transparent
zona pellucida next the egg is thus referred to by others. However, if
 
 
 
 
’ ,lusaUu\‘\n.vn
, Ilralnm gunulocum
 
zona Plxl.\L€.\a.I.
 
   
 
co uldul ' \
i..'.3.i.i1u..i.' vilclluicb \\,g,qg. ‘mime: uunm a nun
In unlrun mam rune
 
fiG 153 An ovarian follicle approaching maturity (From Patten )
 
this layer is secreted by the follicle cells, as some workers believe, it is
of course a secondary membrane. The zona pellucida may be fairly
thick, and in the mole, pig, rabbit, and sheep it takes on a radiate
appearance and hence becomes a zona radiata.
 
The term zona radiata is unfortunate in the mammals, for outside
this structure is a cellular layer of radially elongated follicle cells called
the corona radiata and confusion is apt to exist between these two.
 
B. SECONDARY MEMBRANES
 
Secondary membranes are formed by the follicle cells which surround
the ovum and are therefore the product of maternal tissue. These membranes, which are truly chorionic in nature, may take on a variety of
218 EGG AND EMBRYONIC MEMBRANES
 
forms, depending upon the activity of the follicle cells. The distribution
of the chorion is more restricted than that of the vitelline membrane,
but some eggs which lack the latter possess a chorion. It may arise as a
cuticular secretion of the follicle cells forming a delicate membrane
which later thickens to assume the character of a chitinous-like shell,
as in the insect egg. On the other
hand, it may be formed by direct
transformation of the follicle cells themselves. Its substance is, according to
Tichomirow, chemically like keratin
 
 
F 154 A t 1' th fll l - - - .
epitlieelium WltlIlJ0tll1;Ol:lh?)r)0: oof lDc‘:ct8': and much “Cher In nitrogen than 15
 
ms bwolor (Redrawn from Korschelt chitin,
 
and Heme’) Both primary and secondary mem
branes are often present before fertilization takes place, and since they
are usually impenetrable to the sperm they are perforated by one or
more micropyles situated at or near one of the poles of the egg. In
nemerteans and in most molluscs the micropyle is near the lower pole,
but in cephalopods and also in echinoderms, insects,
and fishes, it is near the upper pole. In the Orthoptera
it may be either at the lower pole or at the side of the
egg, and in Oedzpoda there is a circle of 30 to 40 micropyles at the lower pole.
 
The chorion of insect eggs is very different in different
species. In the simplest cases it is smooth, one-layered,
and structureless. Its surface may have elevations or
may be divided into polygonal areas so that it looks like
an epithelium. In certain forms, as in the locust, the
follicle cells send out processes to these polygonal areas
of the chorion around which a shell is secreted. After
formation of the shell, the cell processes are withdrawn.
 
Porous canals through which the egg obtains air often .. _
penetrate the chorion. In Ranatra and N epa, water fiG 155 An
scorpions, in which the eggs are sunken into plant iii
stalks, the chorion is drawn out at the end of the seven processes
 
. . . h h
egg into delicate processes which serve to aereate the §{,b‘§, s‘(’R':d:::,l,:
 
egg_ from Korschelt
 
The micropyle is formed in a characteristic manner and Held”)
in insects as has been described in the locust M econema vamans. One of
the follicle cells sends a long conical process down to the egg. This
process remains during the secretion of the chorion and then is drawn
back into the follicle. The chorionic pores referred to are formed in
the same way. Also the micropyle of the bony fishes is formed in a
SECONDARY MEMBRANES 219
 
similar manner, but as has been earlier mentioned, the membrane perforated in this case is a zona radiata and not a chorion. (See fig. 191.)
 
In Octopus the chorion is drawn out into a stalk which becomes
twisted and serves to anchor the eggs. Among the chitons there are
different types of chorions. Some of the eggs have a knobbed surface
 
and some are covered with needle-like processes. Many actinian eggs
also have sharp processes.
 
 
Fro. 156. The egg membranes of Meconema varians. (From Korschelt and Heider.)
ch., chorion; f., follicular epithelium; m., micropyle.
 
The myxinoids have a characteristic shell. At each pole of the egg are
attached stiff anchoring filaments which end in lobed umbrella-like
expansions. At the germinal pole of the egg the shell is marked by a
furrow-like ring so that a lid is formed which the animal pushes off at
the time of hatching. There is considerable disagreement about the
 
 
fiG. 157. The upper part of the egg of Bdellostama stouti. (Rcdrawn from Ziegler, after
Doflein.)
 
A, section showing nucleus and above it the micropyle between the bases of the processes. B. Opereulum and processes.
 
origin of this shell. Cunningham says that it is the product of the egg
itself, and Doflein derives it from the follicle cells. The membrane is
usually considered as a true chorion.
 
In Petromyzon the inner egg membrane is covered with a mucous
layer which causes the egg to hang onto stones. This membrane is
formed through transformation of the follicle cells themselves. In some
220 EGG AND EMBRYONIC MEMBRANES
 
of the ganoids also there is a similar adhesive membrane formed from
the follicle cells. Under this layer are two membranes, the chorion and
the vitelline membrane.
 
The follicle cells of the ascidians show a special type of modification.
five envelopes are formed by these cells and thus we have a unique
example of an egg covered by five secondary membranes. When the
ascidian egg is still young it is surrounded by a primary follicular epithelium derived from undifferentiated ovarian cells. Beneath this epithelium is a band of structureless membrane. These flat epithelial cells
multiply and become cubical. Some of them find their way inside the
epithelium and form an inner layer called the test—cell layer while certain of them wander into the egg. The cells of this layer do not give
rise to the test of the adult ascidian as was formerly supposed to be the
case. As the egg matures, these test cells degenerate and later are found
in a gelatinous mass over the egg.
 
In the solitary ascidians the follicle layer of the egg takes on a special
character. These cells, instead of remaining cubical, increase in size and
become highly vacuolated, resembling a foam structure. They also
develop processes which support the egg and enable it to float.
 
In addition to the follicular membrane and the test-cell layer, two
other membranes are formed around the ascidian egg. Beneath the
two layers already described, the follicle cells secrete a structureless
membrane called the chorion. Still another membrane is formed between
the basement membrane and the follicle cells. This is the external pavement epithelium and it may be regarded as another layer of follicle cells.
There are thus five membranes over the ripe ascidian egg. Next the egg
is the gelatinous layer of test cells, and over this are the following
layers, the chorion, the foam-like follicle epithelium, the external pavement epithelium, and the basal, follicle membrane. Since all these membranes are derived from the follicle cells they are secondary membranes.
 
In the Dipnoi the primary membranes are covered by the gelatinous
tertiary membranes, and secondary membranes are absent. In the frog’s
egg there is a thin but tough membrane around the vitelline membrane
and this is secreted by the follicle cells. Over this is the jelly formed by
the oviduct, so the frog egg has all three types of membranes. In the
urodeles this secondary membrane appears to be lacking. In reptiles
and birds the chorion seems to be entirely lacking, for the egg white
and shell are tertiary membranes.
 
From the descriptions just given it will be seen that the chorion has
a variety of forms and that its special characteristics are adaptations
to the needs of the different species.
 
Comparable to the chorion in a certain sense is the mammalian
SECONDARY MEMBRANES 221
 
follicle which is here described in some detail. Although of course
it cannot be considered as a membrane, still it is formed by the follicle
cells. As described in an earlier chapter, the mammalian ovum is highly
specialized because of the intra-uterine development of the embryo.
There is only a very small amount of yolk present in the egg as contrasted with the large amount in the eggs of birds and reptiles. Secondary
and tertiary membranes are entirely lacking, but the Graafian follicle
 
Fm 158 The developing ovum and follicle cells of the cat (Redrawn from Buchner)
See text for description.
 
which surrounds the egg is a product of the follicle cells. (fig. 153.) In
earlier times mammals had eggs similar to those of reptiles and birds, for
the monotremes, the simplest mammals, possess an egg with shell and
egg albumen. In the entire animal kingdom the Graafian follicle is probably the most specialized structure produced as a modification of the follicle cells. In the middle of the follicle is a cavity filled with liquid, known
as the liquor folliculi. The ovum itself, surrounded by the zona pellucida
and the zona radiata, is attached to the Wall of the Graafian follicle by
a group of cells known as the discus proligerus. The cells of the discus
222 EGG AND EMBRYONIC MEMBRANES
 
are continued into the cells of the follicle wall known as the membrana
granulosa, which consists of many layers. Outside the membrana
granulosa the ovarian connective tissue is differentiated into two investing layers, the theca folliculi. The outer of these is densely fibrous,
and the inner cellular, penetrated by small blood vessels. Buehner
describes the growth of the Graafian follicle in the cat (fig. 158), where
it begins as a simple follicle in which the ovum is surrounded by a
cellular layer, the granulosa. The cells about the ovum multiply rapidly,
and part of them lose their connection with the upper surface of the
egg to wander out to form a second loose ring around it. The rings
separate sharply from each other
and each becomes many-layered,
while a cavity known as the antrum
appears between them. This cavity
becomes filled with a liquid which
is secreted into it and quickly enlarges. The outer ring of follicle
cells is crowded to the periphery
and forms the stratum granulosum.
The ovum itself at first bulges
slightly into the cavity of the
follicle, and later as its surrounding cells are undercut protrudes
farther into it, its attachment to
the follicle being new a delicate
stalk of cells, the discus proligerus.
When the egg is ready to escape,
me. 159. Follicle and portion of cyto- this narrow sta‘k is broken, and
plasm and nucleus of ovum of a rabbit. (Re the follicle ruptures, the egg passes
drawn from Buchner.) _
through the tube into the uterus.
The follicle now undergoes a transformation and becomes the corpus
luteum. Sometimes the follicle cells immediately around the egg are
found clinging to it after its discharge.
 
The mammalian ovum and its surrounding follicle are thus seen to
be highly specialized. The presence of only a very small amount of
yolk and the preparation for the attachment of the ovum to the uterus
are all adjustments to the intra-uterine development of the embryo.
The role of the follicle cells as a nourishing membrane has been definitely
determined in the dog by experiment. The follicle cells are filled with
mitochondria. When lecithin is injected into a dog these mitochondria
increase in number. However, if the dog is allowed to become hungry,
the mitochondria decrease. They seem to act as store houses for the
TERTIARY MEMBRANES 223
 
developing egg. The identification of lecithin or of a similar substance
has been observed by Russo in the protoplasmic bridges which penetrate
the zona radiata.
 
C. TERTIARY MEMBRANES
 
Tertiary membranes, unlike primary and secondary, are formed after
the egg has left the ovary. They are secreted by the oviduct or uterus
or by special glands connected with them. Tertiary membranes are of
various kinds, gelatinous, horny and chitinous, or cocoon-like. The
type of membrane shows adaptive correlation to the needs of the developing embryo. The gelatinous type of covering is frequently seen in
fishes and in amphibians and also in many invertebrates, as Geryonia,
and Sagitta. Chitinous shells cover the eggs of the phylopods, Apus
and Branchipus, and a horny capsule covers the shark’s egg. Under the
tertiary membranes there may be a primary or secondary membrane
or both for in some eggs all three types are present.
 
In the cephalopods the tertiary membranes show different modifications. The egg of Sepia and its surrounding albumen is covered by a
black leathery capsule, but in Loligo the eggs, each in a firm envelope,
are arranged in a gelatinous mass known as “dead men’s fingers.” The
flatworms have cocoons which are formed in the ovary. There are
various kinds. Branchiobdella has a stalked capsule containing one egg.
The rhabdocoele turbellarian cocoon contains several eggs. In this
capsule and in that of the trielad Dendrocoelum there are a great number
of yolk cells included beside the egg and these serve to nourish it. The
trematode capsule contains one egg and is either stalked or provided
with a lid or both may be present. The polyelad capsule is similar to
that of the trematode but there are several eggs in one cell.
 
Coeoons are sometimes formed by special skin glands. Thus in the
lumbricids and in the Hirudinea the cocoon which has a ring-like form
is secreted by a special skin gland and drawn off over the anterior end
of the worm. In it is deposited albumen for the nourishment of the
embryo.
 
In the gastropods the cocoon is large though the eggs themselves
are small, for they are surrounded by albumen. In Limax, Helix, and
Paludina there is only one egg in a cocoon. In some gastropods only
one egg is deposited but in other cases there are a number, all but one
of which are utilized to contribute to the growth of the embryo formed
from that one. (This is the phenomenon called by some “cannibalism.”)
Some insects also have cocoons which are tertiary membranes as contrasted with the larval cocoon formed for the pupa of the butterfly.
Periplaneta has a cocoon which is carried by the female attached to the
224 EGG AND EMBRYONIC MEMBRANES
 
posterior end of the abdomen. In this cocoon the eggs are laid each enclosed in the vitelline membrane and the chorion. H ydrophilus, the water
beetle, has a round cocoon in the form of a web. The female places
the cocoon on the under side of a leaf to which it is attached by a stalk.
There are fofty-five to fifty eggs in palisade-like arrangement within the
cocoon nourished from the substance of the web.
 
The selachians, when not viviparous, have tough egg membranes.
The albumen and the horny capsule are deposited about the egg while
it is in the oviduct. The capsule differs in different species. In the sharks
its four corners are drawn out into fibers which permit the egg to cling
to water plants. Occasionally several eggs are found in one capsule.
 
Water-living animals frequently have eggs with gelatinous coverings.
They are laid singly in the urodeles and in Ceratodus. In many other
animals, however, the eggs are laid in gelatinous masses of varying
sizes which may be irregular (cephalopods and frogs), plate-like (some
polyclads, gastropods and insects), or rope-like (some nemerteans and
annelids).
 
A gelatinous covering over the egg is typical of the amphibia. In
many of the amphibia there are special modifications of these tertiary
envelopes. An interesting example of this kind is that of a tropical
anuran. At the time of egg laying the oviducal secretion which surrounds
the eggs is beaten up by the hind legs of the parents into a fine foam
containing many air bubbles. This foam is sometimes placed on the
surface of the pond and floats about or it may also be placed in a wet
hollow on the ground. Some of the frogs deposit the eggs in a mass of
jelly on one or more leaves. Sometimes the single leaf is bent by the
copulating frogs into a funnel which retains its shape by means of the
adhesive jelly around the eggs. Some of the Dipnoi (Ceradotus and
Lepidosiren) have a gelatinous tertiary envelope similar to that of the
amphibians. In Lepz'dosz'ren this layer may be very thin or very well
developed.
 
In birds there are a series of tertiary membranes. The hen’s egg may
be described as typical. Immediately around the yolk is deposited a
spirally wound layer of egg albumen, the edges of which are twisted
into the chalazae, stretching from the yolk to the poles of the egg. About
this layer is deposited another layer of egg albumen and over the entire
mass the shell is formed. The shell membrane is double and the two
layers are separated at the blunt end of the egg to form an air chamber.
The shell membrane lies immediately below the shell, which is porous and
brittle and impregnated by calcium salts, even to the extent of 98 per
cent of the substance. The tertiary membranes of birds are in general
like those of the hen’s egg, the differences which occur being due to
INVERTEBRATES 225
 
size, shape, and color of the shell. The egg that is relatively largest is
that of Apteryz, for in this species it weighs one-fourth of the body
weight of the parent.
 
The eggs of reptiles are much like those of birds, but the chalazae are
lacking. In some forms, as in the lizards and snakes, the shells are more
like parchment, little calcareous matter being deposited. The egg-shells
of crocodiles and of some turtles are hard like those of birds.
 
Tertiary membranes are entirely lacking in the mammals with the
exception of the primitive monotremes. The egg of Echidna is much like
a bird’s egg but the egg—shell is formed of keratin and not of calcareous
salts. The mammals have adapted themselves to a terrestrial life by the
development of a series of embryonic membranes, as the birds and
reptiles have done with egg membranes, but in the higher group it has
been found necessary to forsake entirely the devices which were adequate
for the lower forms. The membranes of the embryos are considered in
the second part of this chapter.
 
II. EMBRYONIC MEMBRANES
 
A. INVERTEBRATES
 
In addition to the membranes which properly are classed with the
egg itself the animal kingdom possesses numerous cases of accessory
membranes which are developed by the embryo. These are in the
nature of cellular sheets which by various invaginations, foldings, outpushings, etc., cover the embryo or parts of it. They are especially well
developed in the vertebrates and to that group most of the attention
is paid by embryologists. Nevertheless, among the invertebrates there
are a good many illustrations of the development of different embryonic
membranes. Most common are the amnion and the membrane which is
formed in connection with it, the serosa. But there is also an invertebrate
yolk sac, surrounded by a yolk membrane, and even a placenta occurs
in a prevertebrate group, the ascidians of the family Salpidae. Of course
this latter structure is very rudimentary. It is really nothing but a
tubercle or knob of rather specialized maternal tissue which becomes
richly vascular and to which the zooid already budded off attaches
itself for nourishment.
 
Of the invertebrates proper certain molluscs show the development
of the yolk sac. The amnion occurs more or less developed in the pilidium
larva of the nemerteans, in the developing Polygordius, in the echinopluteus when it is undergoing a metamorphosis, in the larva of insects
and of the scorpions. Some of these groups also show the possession of 8.
serosa in connection with the amnion.
226 EGG AND EMBRYONIC MEMBRANES
 
The Yolk Sac
 
The true yolk sac can occur only in forms having an extreme telolecithal type of egg structure. Among the invertebrates the cephalopods
 
fiG. 160. Various stages in the development of 0. squid, showing the relations of the
yolk sac. (Modified from Harmon and Gardiner.)
 
B and C. dorsal views; D, sagittal section. a., arm rudiment; {., funnel; m., mouth; o.c.,
optic cup; y.ex., external yolk; y.in., internal yolk.
 
are the only forms which show a well-developed yolk sac. As is described
in Chapter V, the cleavage of the protoplasmic cap of the cephalopod
THE AMNION 227
 
egg results in the formation of a series of blastoccnes arranged about
a germinal area consisting of blastomeres. These blastocones separate
entirely from the blastoderm and rapidly extend themselves over
the surface of the yolk underneath the growing blastoderm. They
constitute a yolk membrane enclosing the large mass of yolk. Over
them the blastoderm gradually extends and when the embryo proper
is formed it becomes marked off by a groove from the yolk sac, as
it may now be properly called. The yolk sac takes on the appearance
of an appendage which it maintains until the development of the
embryo is far advanced. Actually the yolk mass becomes divided into
two portions, one of which is contained within the body of the embryo
and constitutes the internal yolk sac in contrast with the external one
which has just been mentioned. The yolk masses of the two are joined
at all times, however. The further growth of the embryo results in proportionate decrease in the size of the external yolk sac which is gradually
included within the body of the young animal. Morphologically this
structure represents a precocious median development of the mass of
tissue which produces the arms of the squid and is comparable to the
developing foot of other molluscs. Strictly speaking it is not merely an
embryonic appendage, for all of it is finally withdrawn into the body
of the growing animal. A somewhat similar ventral protrusion from the
foot of the snail, Helzlr, was described by Lankester and while not a
true yolk sac it is indicative of the tendency so markedly illustrated
by the squid.
 
The Amnion
 
The first structure in the animal kingdom which may be designated
as an amnion is seen in the metamorphosis of the pilidium larva of the
nemerteans which is described on page 153 (figs. 103 and 104). On the
flattened under surface of the helmet-like pilidium, four amniotic invaginations form. They consist of 'ciliated ectoderm and other deeper
parts and are known as the imaginal discs. Their continued inward
growth upward and over the alimentary tract finally results in their
fusion. The inner parts, or the imaginal discs, form the outer covering
of the little worms while the remaining portions of the coalesced invagination make up the amnion which is a temporary covering entirely
lost with metamorphosis.
 
The second appearance of the amnion is seen in the metamorphosis
of the annelid, Polygordius. This structure superficially resembles that
of the pilidium, for here also four invaginations appear arising from a
circular groove which is known as the amniotic fold. It serves as a
covering for the folded portion of the worm which remains in this con228 EGG AND EMBRYONIC MEMBRANES
 
dition until the time of metamorphosis when, by severe contraction,
the worm becomes straightened out and the amnion has no further
function.
 
An amniotic invagination is described in the metamorphosis of the
echinopluteus of the sea-urchin. It occurs on the left side of the larva as
a pit which deepens and broadens until it comes in contact with the
wall of the hydrocoele. The tissue which lies between the amniotic in
 
fiG. 161. Transverse sections of embryos of Clytia. (Redrawn from Folsom after
Lecaillon.)
 
A, through germ band at gastrulation; B, through germ layers and amniotic folds;
C, stage later than B; D, through germ layers. a., amnion; a.c., amniotic cavity; c.,
coelome sac; e.. ectodcrm; i., inner layer; g., germ bond; n., neuroblasts (primitive nervous
cells); 59., serosa.
 
vagination and the hydrocoele undergoes important changes and is
involved in the formation of the so-called echinus rudiment. Into the
amniotic cavity this rudiment and especially the tube feet develop.
 
In the scorpion, according to Brauer, an amnion is formed shortly
after the two-layered stage shown in fig. 39. At the edge of the blastederm a sheet of cells arises and grows backward and presently a second
layer is formed over the first. The outer is the serosa and the inner the
amnion. Underneath these the embryo develops.
 
The amnion of invertebrates reaches its highest development among
the insects, and of these the Coleoptera show it most clearly. There are
THE AMNION 229
 
really two types of development with respect to the relations of formative area. and of yolk shown in the insects. In the one type, called by
 
some “overgrown,” the germ band retains its original position in the
blastoderm and the folds of the amnion and serosa arise at its sides and
 
fiG. 162. Diagrammntie sagittal sections of Calopteryx. (From Folsom, after Brandt.)
 
A-D, illustrate invaginution of germ band; E-F, illustrate rex olution of embryo. a.,
anterior pole; a.c., amniotic cavity; am., amnion; z1iit., antenna; b. blastodcrm, d.,
dorsal; g.. germ band; h., head end of germ band; 1., laliriuin, l‘-l“, thoracic legs; m., mandible; mx., maxilla; p., posterior pole; 5., sorosa; v., ventral; y , yolk.
 
grow over it. This occurs in the Coleoptera, and it is for this reason that
the formation of the amnion is most clearly shown there. In the other
type, called “invaginated,” the germ band invaginates at one end of the
egg, and is finally carried into a cavity formed within the yolk mass;
after the closure of the opening of the invagination the formative portion
develops entirely within the egg. Due to this invagination the ventral
230 EGG AND EMBRYONIC MEMBRANES
 
surface of the developing embryo comes to face the dorsal side of the
egg and a subsequent process of revolution is necessary before the
embryo at length resumes its original orientation. This type occurs in
the Odonata. The relations of the folds of the amnion are shown in
fig. 116, which illustrates the development of Hydrophilus, and also
in fig. 161, which shows the formation of the amnion in the beetle
Clytra. Folds of the blastoderm arise at the side of the germ band and
continue their growth until they meet above it and fuse. The membrane
thus formed directly above the germ band is the amnion, and the outer
one, the serosa. The formation of the amnion and serosa in Calopterya:
is shown in fig. 162.
 
Students of the embryology of the insects are not entirely in agreement in regard to the morphological relations of the embryonic membranes found throughout the group and several types of classification
have been proposed. It hardly seems necessary to consider the various
classifications or the points upon which they have been based. Serosa
and amnion occur together in the Coleoptera, Lepidoptera, Diptera,
Dcrmoptera, Isoptera, and Odonata. An amnion only is found in Xenos,
a strepsipteran parasite, and even it is vestigial in such forms as M usca
and Drosophila. A serosa only is formed in a few of the Hymenoptera
including the honey bee, wasps, and ants.
 
B. VERTEBRATES EXCEPT MAMMALS
 
Embryonic membranes are especially well developed in the vertebrates where they serve for protection, nutrition, and respiration. These
are the yolk sac, amnion,serosa or chcrion,allantois, and its derivative,
the placenta. Since the name “chorion” is also correctly used for the
secondary membrane secreted by the follicle cells, it is confusing to use
this term for an embryonic membrane of different origin. We shall
therefore always designate this embryonic membrane as serosa although
it is quite customary among mammalian embryologists to use “chorion”
in both senses. A
 
For an introduction to the nature of the embryonic membranes of
the vertebrates and of the parts they play, the conditions as found
in the chick may be taken as a type. Of course these conditions apply
particularly to the Sauropsida; however, they may be looked upon as
providing a point of departure for the entire study. They have often
been described, so a brief reference here is all that is necessary. The
first membrane to appear in the chick is the yolk sac. As the blastoderm
grows over the yolk its lower edge consists after gastrulation of primary
ectoderm. At an early stage the endoderm and later the mesoderm may
be seen back of the edge gradually making their way over the yolk. The
VERTEBRATES EXCEPT MAMMALS 231
 
mesoderm divides into two layers, and the investments of the yolk are
first the splanchnopleure (endoderm and mesoderm), then the extra
Fra 163 Diagrams of the extraemhryomc membranes of the chick (From Duv9.l’s
Atlas)
 
A, 2-day embryo, B, 3-day embryo a , air space, of , ammotlc fold, a c , amniotic cavity,
all , allantois, alb , albumen, e , embryo e e c , extruembryomc eoelome, ect , ectoderm,
end , endoderm, In , mesoderm, ser. serosn; s , shell, sm . shell membrane, so. soma.topleure. sp , splanchnopleure, v , vltellmo membrane, y , yolk, y s . yolk sac
 
embryonic coelome, and last the somatopleure (mesoderm and ectoderm). The anterior and posterior parts of the gut are the first to develop
232 EGG AND EMBRYONIC MEMBRANES
 
a cellular floor. The midgut remains open to the yolk for some time. As
the embryo becomes constricted off from the yolk the two ends of the
gut enlarge further, and the extent of the opening of the midgut is decreased. finally, the latter is connected to the yolk only by a narrow
 
a1l.c.
 
flu 164 (‘ontmuation of fig 163
A, 5—day embryo, B, 14-day embryo
 
am , amnion, all e . allantoie cavity, all s , allantolc stalk, u , umbilical stalk
neck called the yolk stalk. At the yolk stalk the inner and the extraembryonic splanchnopleure are continuous. The absorption of yolk
material through the yolk stalk probably does not occur directly but
is brought about by the vitelline circulation. Deep yolk sac septa which
are folds of the splanchnopleure grow down into the yolk, and glandular
VERTEBRATES EXCEPT MAMMAIS 233
 
absorbing cells aid in its digestion and in passing it to the vitelline
circulation. The yolk mass decreases toward the end of the incubation
period, and finally the entire structure is drawn into the body.
 
During the early growth of the blastoderm over the yolk the amnion
and the serosa are being formed. The amnion arises by folds of the
extraembryonic somatopleure near the anterior region of the embryo.
first to form is the head fold of ectoderm and endoderm, for the mesoderm has not yet reached this region, and this is joined by lateral folds
of somatopleure so that the entire region is covered. Later a similar tail
fold covers that region and is continued forward until it meets the
anterior lateral folds. The fusion of these folds encloses the embryo in
an ectodermal cavity, the amniotic cavity. The union of its two folds
has caused the somatopleure to double back on itself and thus to enclose
the embryo in two membranes of similar nature although of inverted
order. The inner membrane or amnion consists of ectoderm continuous
with that ‘over the embryo and of somatic mesoderm. The outer membrane or serosa consists of somatic mesoderm and of ectoderm continuous with the outer covering of the yolk. Between the amnion and the
serosa is the extraembryonic coelome which is connected with the body
cavity of the embryo. The serosa is merely a continuation of the somatopleure which has made its way nearly around the yolk. It also covers
the allantois which later develops within the extraembryonic coelome.
Thus it comes to line the shell and covers the embryo and the other
three membranes.
 
The allantois arises as a diverticulum from the hind gut within the
body of the embryo. As development proceeds it extends out into the
extraembryonic coelome, its connection with the gut being designated
as the allantoic stalk. Since it arises from the gut, it has necessarily a
lining of endoderm and an outer layer of mesoderm, that is, it is an
extension of the splanchnopleure. It grows very rapidly and unites
with the serosa so that there is now a double layer of mesoderm in its
outer wall, splanchnic on the inside and somatic from the serosa on the
outside, and over all is the ectoderm of the serosa. The rapid growth of
the allantois carries it first over the amnion, with which it fuses, and
then over the yolk sac. finally, pushing the serosa before it, it extends
even over the albumen, which has become dense from loss of water,
forming an albumen sac which is lined by the ectoderm of the serosa.
The allantois has a rich blood supply in a network lying close to the
porous shell, through which the exchange of gases is made easy. The
chief function of the allantois is respiratory but it also serves as a receptacle for the excretory wastes from the kidney of the embryo. Shortly
before the chick hatches, its beak breaks through into the air space of
234 EGG AND EMBRYONIC MEMBRANES
 
the egg, pulmonary respiration begins, and the circulation of the allantois becomes slower and slower, until at hatching time the dried allantois
remains inside the shell.
 
With conditions as found in the chick as a starting point, the development of the various vertebrate membranes may be appropriately
taken up.
 
The Yolk Sac
 
The yolk sac is the only accessory structure which may be looked
upon as of general occurrence among the vertebrates. It will be recalled
that all vertebrate eggs show a distinction between yolk pole and animal
 
 
fiG. 165. Embryo of toad fish showing large yolk sac attached.
 
pole. (See Chapters IV and V.) The eggs are markedly telolecithal
whether the cleavage is holoblastic or meroblastic. The relation between discoidal and holoblastic eggs is discussed and illustrated earlier
(fig. 51) where it is shown that the condition of the large yolk-laden
endoderm cells of the bilateral type is gradually converted into the
yolk mass of the discoidal type. The latter is incapable of segmentation,
yet the homology between them is complete. The yo1k—laden endoderm
cells which make up the ventral portion of the enteron and serve as a
source of food supply for the growing embryo may be regarded as the
antecedent of the yolk sac of the meroblastic vertebrates. They do not
constitute a true yolk sac, but the mass of cells is the equivalent of an
internal one and corresponds in a general way to the outer sac of fishes,
reptiles, birds, and mammals. For all of these it is an important nutritive
structure.
 
In myxinoids, elasmobranchs, and teleosts, in all of which the eggs
are extremely telolccithal, a well-developed yolk sac is characteristic.
THE AMNION 235
 
Before the blastoderm spreads over the yolk the embryo has formed
and has become folded 0E. The yolk sac, therefore, is formed by the
extraembryonic blastoderm which grows over the yolk and it is attached
to the embryonic body by a stalk, narrow in elasmobranchs but wide in
teleosts. The yolk sac has an area vasculosa that is rich in blood vessels
by which the food material of the yolk is brought to the embryo.
 
Although it is an outgrowth of the gut the connection of the yolk
sac with that structure may be interrupted early in development as is
found among the teleosts (for example the salmonids), in which case
the absorption of the yolk is brought about exclusively by the vitelline
vessels. In addition to its nutritive function, the yolk sac often acts
as a respiratory organ. It functions in this manner in the lower vertebrates whcre an exchange of gases takes
place between the blood vessels of the yolk
sac and the surrounding water and also in
the early stages of higher vertebrates where
the exchange takes place between its blood
vessels and the medium surrounding the
egg. Even in mammals the yolk sac may have a respiratory function. In the mono- ‘
tremes it still retains its yolk and hence its
nutritive function. In the placental mammals, however, it is devoid of yolk but
may still be functional in early stages when
it is quite vascular and helps to absorb fiG 166 Embryo of Torpedo
nourishment from the maternal tissues. §l;?,Y,‘“§sb?:“:f0r,;°:
 
Structurally the yolk sac is developed in from the posterior part of the
about the same manner throughout the embm’ (After zlegler’)
lower classes of vertebrates. A distinction is to be observed in the
appearance of the mesoderm of the elasmobranchs, as Torpedo, and
in teleosts, as the salmon. In the former the mesoderm is an undivided
layer which grows out peripherally from the posterior portion of the
embryo and then anteriorly about the edge of the blastodisc. In the
latter case the mesoderm splits into somatic and splanchnic layers which
grow laterally from the embryonic area and carry the body cavity as
the extraembryonic coelome out over the yolk.
 
The Amnion
 
In the Sauropsida (reptiles and birds), we have the first appearance
of the amnion, serosa, and allantois. This group and the mammals make
up the Amniota, which possess the amnion and are contrasted with the
Anamnia which lack it. Since most of these latter lay their eggs in a
236 EGG AND EMBRYONIC MEMBRANES
 
fluid medium, usually water, the developing embryos are not subjected
to injury through violent motion or through changes in temperature or
in humidity, and thus no special covering of the embryo is necessary.
All the higher vertebrates either lay their eggs in a shell or hold them
in the mother’s body during the embryonic period and some kind of
protection is heeded to prevent the embryo from drying or from pressure
or stress that might reach it. Therefore these embryos are protected by
two membranes, the amnion and the serosa. When fully formed the
amnion has always an inner layer of ectoderm and an outer layer of
mesoderm.
 
Of the Amniota the reptiles are the most primitive. It is interesting
to note that in them the amnion develops earlier than in the birds at
a time before the head has become prominent and before the mesoderm
 
 
fiG 167 Diagrammatxe transverse section through a (‘helonian embryo (Cl€m"l1I8)(Redrawn from Kerr. based on a figure of Mitsukuri.)
 
has split into its two layers. In the Chelonia the amnion is at flrst formed
of ectoderm and endoderm, the mid-dorsal part being of solid ectoderm.
Later after the mesoderm has split it is drawn up into the amniotic
folds and the endoderm takes no further part in the formation of the
amnion. This is different from the condition in the chick in which the
amnion is formed from the somatopleure except in the proamnion region
where there is no mesoderm. (A proamnion region is characteristic of
reptiles in general.) The broad ectodermal band in the roof of the
amnion in the Chelonia has its counterpart in a small area known as
the scro-amniotic isthmus in the amniotic roof of the chick. This latter
may be considered as the remains of the broader layer of the reptiles.
The amniotic fold in the Chelonia begins at the head end and proceeds backward until the whole embryo is covered. By the backward
growth of this flap there is formed a long tunnel-like cavity covering
the embryo and extending posterior to it. Later this posterior extension
becomes partly obliterated and the cavity is closed. This again is quite
THE AMN ION 237
 
different from the formation of the amnion in birds in which a head fold,
lateral fold, and a tail fold take part. In some reptiles, however, as the
chameleons, amnion formation is similar to that of birds, from lateral
folds around the embryo, and is not due to the elongation of one an
5
fiG 168 A and B Chelonnn blastodorms showing stages in the formation of the
amnion A, Cheli/dra, B, Clemmys (Redrawn from Kerr after Mitsukuri)
 
a . amnion showing neural groove beneath it, a f , edge of amniotic fold, a t . amniotic
tunnel.
 
terior fold. Since the amnion appears earlier in the reptiles than in birds,
and its cavity is formed before the embryo is marked off from the yolk,
there is no need for the amniotic folds to grow upward as in the chick.
The development of the amnion in the birds as a group offers nothing
different in principle from the type already described, that is, from this conditions in the chick. The amnion of the mammals presents new
features, however. Their character has already been discussed in the
chapter on the formation of the mammalian embryo, Chapter X, to
which the student is referred, and the chief facts regarding it are again
mentioned a little later in this chapter under the head of the membranes of the mammalian embryo.
 
The Allantois
 
The allantois appears first in reptiles and is developed in all amniota.
It always originates as an outgrowth of the hind gut and has therefore
an endodermal lining and an outer layer of mesoderm. In amphibians
it is represented by the urinary bladder. In reptiles the outgrowth has
been described as solid, but it has also been maintained that the contracted space in which it develops causes it to be collapsed and so to
take on the appearance of a solid structure. In birds it has a three-fold
function. It increases in size, probably on account of the large amount
of excretory Wastes collected during the embryonic life in the shell. Its
large size and its position next to the air space in the end of the egg and
just inside the shell are correlated with its new use as a respiratory
organ. Also, pushing the serosa before it, it forms a double-layered sac
over the albumen. This sac is thus lined with ectoderm. Since it absorbs
the albumen, the allantois thus has a nutritive function, although of
course this is of less importance than the similar function of the yolk sac.
 
The allantois of mammals acquires no further function. It aids the
trophoblast in the formation of the placenta which is for the mammal
an embryonic organ of nutrition, respiration, and the removal of excretion. It thus becomes the most important embryonic membrane of
mammals, for through the participation of its blood vessels it has the
chief part in the formation of the placenta.
 
Viviparity among the vertebrates is especially related to the functions
of the allantois and the adaptations which it makes, but other embryonic
membranes are also employed in bringing about this mode of caring
for the embryo. Viviparity occurs in all the vertebrate groups, beginning
with the fishes, except the ganoids, lung fishes, and birds. It is possible
that it may have been characteristic of some fossil ganoids, but probably
the birds because of their habit of flight have never been able to develop
this method of caring for their young. There are many parallel methods
of relating the embryo to the maternal tissues, and functional placentae
are not confined to the mammals. In all forms below the mammals the
embryo is chiefly nourished by the yolk sac even though other structural
modifications supply additional sources of food. Development within
the body of the mother always serves the same function, protection in
THE ALLANTOIS 239
 
the struggle for existence. Among the elasmobranchs there are several
genera in which there is intra—uterine development. In Acanthias the
typical egg membranes are formed but the horny egg-shell is thin and
disappears in later stages. The uterine wall contributes to the nourishment of the embryo by supplying the albuminous fluid which is enclosed
in the egg-shell. In this form the lining of the uterus during later stages
of development is thrown into folds which are brought into contact
with the yolk sac. In Torpedo the folds are prolonged in trophonemata,
nutritive threads which reach the pharynx of the embryo through its
spiracles. In M ustelus laevis the folds of the uterus fit into grooves in
 
 
Fm. 169. Yolk sac placenta of Muslclus lacvis. (Rcdmwn from Corning after Joh.
Muller.)
 
u., wall of uterus; y.o., yolk sue.
 
the yolk sac and, as both are highly vascular, they form a functional
yolk sac placenta. A placenta used in this broad sense means any structure which brings about, by means of an abundant vascular supply, an
intimate relation between maternal and embryonic tissue, for the purpose
of conveying nourishment from the one to the other. Here the yolk sac
functions in this manner, but in the Amniota it is usually the allantois.
 
The teleosts include a number of viviparous forms. In some the eggs
are developed in the ovary itself where vascular processes on the surface
contain the eggs and act as placentae. In others the embryos develop in
the enlarged oviduct _or uterus. Sometimes (Scorpaenidae) the maternal
body merely holds the embryo which obtains its food supply entirely
240 EGG AND EMBRYONIC MEMBRANES
 
from the yolk. In other cases (Anableps) the yolk sac sends out villi to
the uterine wall.
 
Viviparity is uncommon among the amphibia. In one of the salamanders (Salamandra atra), however, development takes place in the
oviduct but usually only one of the eggs reaches maturity for the others
break up and are absorbed by the outer gills of the developing embryo.
The embryo has additional nourishment from the blood which escapes
from the uterine wall.
 
 
fiG 170 Embryo of (‘hulcides tndactylus (Redrawn from Kerr after Giaconiine)
 
A, 7-mm embryo, B, 15-16-mm embryo seen from apical pole all, allantois, pl,
allantoic placenta (foetal portion) . y s , yolk sac
 
The reptiles include a number of viviparous forms. In some, the
blind worm and the viper, there is a thin shell and the embryo is simply
held in the uterus, the lining of which remains unchanged. In the lizard,
Chalczdes ocellatus, the shell breaks and finally disappears, the uterine
wall becomes vascularized, and 1S thrown into folds which fit other
folds on the yolk sac. Both the allantois and the uterus adjoining it are
highly vascularized but the placenta-like folds develop only on the
yolk sac. A type of placenta more nearly approaching that of the
mammals is found in still another lizard, Chalczdes trzdactylus. The condition of its allantois and yolk sac may be regarded as transitional from
that typical of the Sauropsida to that of the mammals, for both function
as placenta and projections from both vascularized sacs interlock with
MAMMAIS 241
 
similar projections from the uterus. But of the two the allantoic
placenta is the more highly developed. Thus the true allantoic placentae
are not limited to the mammals but appear also among the reptiles.
 
Evidently the problem of relating the embryo to the maternal tissues
has been solved in similar ways, although employing different structures
in the different groups of the vertebrates. In the mammals the wall of
the uterus is highly developed as a special adaptation of the maternal
tissue to accomplish this function. In other forms the oviduct sometimes takes care of the need so far as the mother is concerned, and even
the ovary may serve in this capacity. On the part of the embryo, the
yolk sac of lower forms often carries on the function, while in the higher
forms it is taken over by the allantois.
 
C. MAMMALS
 
Of the embryonic membranes of mammals the greatest interest is in
connection with the allantois and the placenta which it helps to form.
The yolk sac and amnion are also present, however, and show features
which are new. In the entire early development of mammals there is a
rather general lack of structural homology with that of other classes of
vertebrates, and although similar results are reached convergently so far
as the structure of the embryonic membranes is concerned, their methods of origin in some forms is very different.
 
There are two great types of development found in the mammals. The
monotremes are unlike all the others in that their eggs are large and
yolk-laden and their cleavage discoidal. The animals are oviparous, the
development of the embryo taking place within the egg-shell, as in the
case of the Sauropsida. Cleavage, germ-layer formation, and the development of the embryonic membranes is comparable to these processes
in that group. The membranes are of the same kind and are probably
formed in the same manner.
 
The marsupials are the lowest mammals which have intra—uterine
development. The young are born in an immature condition, and are
placed in the abdominal pouch where they become attached to the
teats of the mammary glands, Here the immature period is completed.
Since at birth the young are so miniature, the allantois, which in the
higher vertebrates functions as a medium for obtaining nourishment
from the uterus, is usually small. The yolk sac contains no yolk, though
it is large and well developed. Its wall opposite the embryo contains
only endoderm, and the extraembryonic coelome is absent in this part
of the blastoderm. During uterine life there is usually a yolk sac placenta.
 
The marsupials include a number of forms which taken together make
up a series similar to that described for the lower vertebrates and illus242 EGG AND EMBRYONIC MEMBRANES
 
trate the change from a yolk sac placenta to an allantoic placenta. The
first of the series is the opossum, Didelphys, in which the yolk sac has 9,
nutritive function. This membrane makes connection by means of folds
 
 
 
 
   
 
.
on: 077777;!‘ 6
 
 
Fm. 171. A, diagram of a section through monotremo embryo; B. diagram of a. section
through marsupial embryo. Ectodcrm, solid line; mesoderm, dotted line; endoderm, dashed
line.
 
a., amnion; a.c., amniotic cavity; 3.11., allantois; e., embryo; e.e.c.. extraembryonic coelome;
sen, serosa; y.s., yolk sac.
 
with the uterine wall. The latter secretes a nourishing fluid which is
absorbed by the trophoblast and the endoderm of the yolk sac, and
thus is transported to the embryo. In Dasyurus we have a further step
THE YOLK SAC 243
 
in the series. The allantois is still small and the yolk sac large. The
trophoblast forms a syncytium with pseudopodial processes which
attack the uterine wall and engulf uterine blood vessels. The nourishment is passed on to the yolk sac which may be correctly called a yolk
sac placenta, for the connection between the uterine wall and the yolk
sac is very close. Parameles illustrates the last step in the series. In this
form the yolk sac is large and probably has some function in absorbing
nourishment. The allantois, however, grows larger, develops a richer
blood supply, and reaches the trophoblast. The uterine wall, at the
place where the trophoblast touches it, develops a syneytium and becomes vascular. The trophoblast disappears and the blood vessels of
the allantois and the uterus come into close contact. There are no true
villi as in the higher mammals. This is the first case we have met of a
true allantoic placenta and the only one known for the marsupials. It
differs from all others in that the syncytium is entirely of uterine origin
and does not develop from the trophoblast as it does in those mammals
having a discoidal, deciduate placenta.
 
The development of the eggs of the true placental mammals involves
the formation of a blastocyst with differentiated trophoblast and inner
cell mass as is described in Chapter X. The embryo resembles a hollow
vesicle with a drop hanging from one spot on its inner surface. The
inner cell mass is the formative or embryonic portion. The trophoblast is non-formative and produces only ectoderm of the serosa. After
this stage the inner cell mass or embryonic knob differentiates into two
portions, an upper eetodermal layer from which will be derived the
ectoderm and amnion of the embryo and a lower endodermal layer from
which will be derived the enteric canal, the yolk sac, and the allantois.
The embryo proper at this stage is called the embryonic shield and consists of a layer of ectoderm covering a layer of endoderm. (See fig. 144.)
 
Jenkinson has offered an interesting suggestion about the significance
of the early development of the mammal. He compares the blastocyst
stage with the later stage of the reptile or bird in which the yolk sac has
become completely covered and the serosa contains the embryo in the
amnion with its yolk sac and allantois attached. In the mammals also
there is a stage of a closed sac, the blastocyst, which contains in the
inner cell mass all the material for the embryo and its membranes.
J enkinson regards this as a precocious separation of the materials of the
mammalian embryo due to the loss of the yolk on the part of the ovum.
 
The Yolk Sac
 
The yolk sac has the same layers as that of the lower forms, but in
the placental mammals it arises in a different way and is functional
244 EGG AND EMBRYONIC MEMBRANES
 
only in early stages, if at all. The endodermal layer is formed from the
innermost layer of the inner cell mass. These cells proliferate and spread
around the inside of the trophoblast until they form a closed sac just
as would have happened had a central yolk mass been present and they
had grown around it. Sometimes the cavity is very small and the yolk
sac correspondingly restricted, as in man, when it forms a very small
vesicle owing to its slow growth. In other cases the endoderm is quite
closely applied to the inner side of the trophoblast and a large yolk sac
is thus formed. In no case, however, does it contain yolk. It is therefore
an insignificant structure and the function which it serves in the lower
 
 
Fro. 172. Diagram of a. section of rodent embryo. p., placenta; other letters as in fig. 171.
 
forms is presently taken over by the allantois. The completion of the
yolk sac comes only when in later stages the mesoderm is formed between the endoderm and the trophoblast.
 
The formation of the mesoderm begins in the embryonic area and
some time elapses after its separation into its two layers before it grows
out into the space between the endoderm and the trophoblast of the
vesicle; but at length it pushes out from the embryonic area and grows
between these two layers. An early split in this mesodermal layer completes the yolk sac which thus consists of endoderm and splanchnic
mesoderm. The vitelline circulation develops to provide the usual
vascular supply.
 
In many of the higher forms it is merely a vestige of the membrane
through which the embryos of simpler forms obtain their food. In some
cases, however, it retains something of its earlier function in that in
THE YOLK SAC 245
 
early stages it absorbs nutrirnent from the uterus. In these cases it becomes a yolk sac placenta. When this occurs, as in the ungulates, camivores, and rodents, the yolk sac is large and its blood supply is rich and
comparable to that of the chick. In marsupials, in which the uterine
development is of short duration, the yolk sac placenta often functions
until birth.
 
In rodents the yolk sac is always large and invagination of its upper
wall by the embryo gives apparent inversion of the germ layers. This
may take place early in development as in the mouse and guinea pig, or
 
,r,. .\‘.'«-c
 
W PM‘ i W‘! Ls...
_ ..~:x.“~’“} ,3 *9 /» :;,.,;..
‘ I
 
z
‘1 \ '
5"» \
.3_I,» 7%» I
 
(
 
   
 
la‘
,0“...
. . -_.,
1)‘ ;. V’
 
31?, ' ' ‘wig?
 
~ 1'
 
. - v‘ if
'£i..vY" 5
: —""g.
. x
5:’ 25
 
3. ‘ _,,,»',~‘!
 
..,r k .5?
 
-..,,i .5
a, *3"
 
fiG. 173. Area vasculosa of the yolk sac of the rabbit (After Jenkinson.)
 
later as in the rabbit and squirrel. In some cases the lower wall of the
yolk sac is never formed. In others it disappears along with the trophoblast, and the cavity of the yolk sac is in communication with the cavity
of the uterus. The upper wall of the yolk sac absorbs the material secreted
by the uterus and its supply of blood vessels carries this to the embryo.
Thus the yolk sac acts as an accessory placenta.
 
In the rabbit the yolk sac, which contains a nourishing fluid, is very
large and in early stages practically fills the blastodermic vesicle. A
rich supply of blood vessels develops in the side of the yolk sac which
is toward the embryo. The opposite side contains no mesoderm and
fuses with the trophoblast. Later the yolk sac shrivels and since its
outer wall is fused with the trophoblast it remains as a mushroom-shaped
246 EGG AND EMBRYONIC MEMBRANES
 
membrane. The two walls of the shrunken vesicle thus come close together and later they fuse. Since the inner wall of the yolk sac was highly
vascularized its blood vessels continue to supply a large part of the
blastoderm. The rest of the blastoderm is fed by blood vessels of the
allantois which help form the placenta. The yolk sac of the rabbit is
probably a more important nutritive organ than the allantois. The
vitelline artery ends in the sinus terminalis and the blood is returned to
the heart by the vitelline veins.
 
In the Insectivora the yolk sac is often large in early stages and its
blood vessels may begin to form a yolk sac placenta as in Tupaija. In
 
 
 
 
 
'1
0 ',
I 2
0"
 
 
 
,-0"0-o.....ooo°
,_-_-_;J
 
Fm. 174. Diagram of 11 section of embryo of insectivore. u., wall of uterus; other letters
as in fig. 171.
 
some insectivores the mesoderm never covers the lower wall of the yolk
sac (Sores: and Talpa). This organ is unimportant in later stages.
 
The yolk sac circulation in most mammals is of importance in early
stages only, while the allantois is being formed. Later, when the allantois
has established its relation to the uterine wall, there is a retrogression
of the yolk sac. This is true of man, in which the yolk sac becomes a
solid strand of cells extending; out into the body stalk or umbilical cord.
In some forms, as the insectivores, the yolk sac remains until birth.
 
The Amnion
 
The formation of the amnion is due to the development of the upper
portion of the inner cell mass. It is accomplished by one of the two
THE PLACENTA 247
 
methods described in Chapter X. In the one case, there may be a fold
or a series of folds of the extraembryonic somatopleure similar to those
of the chick, as in most ungulates and some insectivores. In the other
case, the cavity may arise in situ in the embryonic knob or between it
and the trophoblast, and thus may never open into any other cavity,
as in the mouse, guinea pig, bat, other insectivores, and many primates,
including man.
 
The Allantois
 
The allantois arises as a diverticulum from the gut in the same manner
as in the chick. In the rabbit this diverticulum extends out into the
extraembryonic eoelome and soon comes into relation with the trophoblast. In many rodents, as the mouse and guinea pig, it is often small
and its endoderm may not grow beyond the body of the embryo. In Tarsius and in man the vesicle never extends freely into the extraembryonic
eoelome but is enclosed as a vestigial structure in the body stalk. This
latter is an enlargement of the primitive connection between the embryo
and the trophoblast, a connection which is never lost. It is regarded as
the equivalent of the allantoic stalk of other forms.
 
The allantois of lower mammals assumes the function of nutrition
but retains its cavity which may serve as a receptacle for urinary wastes.
The size of the cavity is progressively reduced until in some forms it
disappears completely with the inner endodermal layer and only its
mesodermal portion remains. This part becomes highly vascularized
and, together with the trophoblast, forms the embryonic part of the
placenta, a structure which comes into relation with the circulatory
system of the mother and so takes care of the functions of respiration,
nutrition, and excretion. Thus the mesodermal portion of the allantois
accomplishes the function which in lower forms the entire structure
serves.
 
The Placenta
 
A placenta is any organ which brings about an intimate relation and
vascular connection between maternal and foetal tissues. The formation
of a yolk sac placenta has been described for some of the fishes and
reptiles and is again found among the marsupial mammals. Among the
higher mammals, however, it is always the allantois which brings about
this relation between the embryo and the mother. In these forms, the
actual contact is made by the trophoblast, as part or all of it comes into
relation with the uterine walls. It is the allantoic vessels, however, which,
through contact with the trophoblast, furnish the foetal part of the
 
placental circulation. _
The placenta is necessarily a compound structure. Its embryonic
248 EGG AND EMBRYONIC MEMBRANES
 
parts are trophoblast (sometimes lined with mesoderm) and the allantois
with its blood vessels. Its maternal part is the vascular uterine wall.
The foetal and maternal parts may be merely in apposition or they may
be in such close relation that they are actually fused. In both cases an
intimate physiological relation results. The blood vessels of the allantois
(umbilical arteries and veins) are brought close to those of the uterus,
making possible an exchange of substance by diffusion. The embryo is
thus able to obtain oxygen and food materials and also to dispose of
its waste products. There is never any direct connection between foetal
and maternal blood vessels.
 
The placentae of mammals are of two general types, deciduate and
non—deciduate. The non—deciduate placenta is sometimes called a semiplacenta. The name deciduate was given to indicate the loss, at birth,
of the lining of the uterus. Although this loss is not significant in all socalled deciduate forms, the name has still been retained. The following
brief classification of types of placentae of the Placentalia is partly based
on the conception of Jenkinson. The types are closely related to the
method of implantation of the ovum in the uterine wall. Of implantation
there are three types, central, eccentric, and interstitial, as mentioned in
Chapter X. Implantation is central if the embryo becomes attached
superficially to the uterine wall; eccentric if it is enclosed by folds of
the uterus; or it is interstitial if the embryo burrows down into the
uterine wall. The classes of placentae are as follows:
 
The non—deciduate type is that in which the surface of the trophoblast develops villi which fit into crypts or depressions in the uterine
wall. In the simplest cases, the uterine epithelium persists in these
crypts and at birth the villi are drawn out without damage to the uterus.
In other cases, the uterine epithelium is destroyed and there is a closer
union between foetal and maternal tissues. This type of placenta is
characteristic of the ungulates, but is also found in the Cetacea, Edentata, Sirenia, and Lemuroidea except Tarsius.
 
The second type is the deciduate in which the uterine epithelium
is always destroyed by the trophoblast. Foetal and maternal blood are
in close relation. There are two subdivisions of this type as follows:
 
(a) Zonary deciduate placenta. The maternal blood circulates in
capillaries of the uterus. The placenta, which is zonary or band shaped,
is composed of foetal and maternal tissue in very close relation. At
birth part of the wall of the uterus is destroyed and there is a true
decidua. This type of placenta is characteristic of the Carnivora. (b)
Discoidal deciduate placenta. The trophoblast destroys not only the
uterine epithelium but also the subepithelial tissue. The maternal blood
circulates in lacunae or spaces in the trophoblastic wall. These spaces
NON-DECIDUATE PLACENTA 249
 
represent maternal blood vessels which have been engulfed by the
trophoblast and they are the chief part of the placenta contributed by
uterus. Blood is the principal maternal tissue lost at birth, and the
deciduae are thin and more or less degenerate. The portion of the trophoblast which is involved in the placenta is disc-shaped. Placentae of this
type are found among rodents, insectivores, bats, in Tarsius, monkeys,
and man. These three types of placentae require a more detailed
description.
 
Non—decz'duate Placenta. The non—deciduate placenta may be illustrated by that of the ungulates. In these forms the allantois enlarges
rapidly and occupies the length of the trophoblast. The surface of the
trophoblast forms villi into which extend the mesoderm and blood
vessels of the allantois. These may be single or branched. They may be
scattered over the surface of the trophoblast (diffuse placenta, as pig);
 
 
Fm. 175. Diagram of embryo of ungulate contained in uterus. Wall of semen has been
cut, showing embryo in section. c.. cotyledon; ed., edge of cut in serosa.
 
they may be situated in groups or cotyledons (cotyledonary placenta)
when they are also branched (ruminants), or there may be a combination
of the two types, both cotyledons and simple villi being interspersed
(intermediate placenta). Also the cotyledons may be grouped in a band
around the trophoblast.
 
The trophoblastic villi fit into crypts or corresponding depressions in
the uterine wall. When the villi are in groups or cotyledons, the corresponding groups of crypts on the maternal side are called maternal
cotyledons. These latter are in some cases stalked and the foetal cotyledons are then concave.
 
In the difiuse placenta, the uterine epithelium persists as the lining
of the crypts and at birth the villi are withdrawn with no injury to the
uterus. In the cotyledonous placenta the uterine epithelium, except that
of the glands, degenerates and there is a much closer union of maternal
and foetal tissues. Consequently the two portions of a placenta of this
type separate with some difficulty.
 
In the diffuse placenta the uterine and trophoblastic epithelia are in
contact, but in the cotylcdonary placenta the contact of the tropho250 EGG AND EMBRYONIC MEMBRANES
 
blastic epithelium is with a highly modified and vascular subepithelial
connective tissue. In the latter case, however, there is no true fusion of
foetal and maternal tissue as is true of the deciduate placentae. The
maternal connective tissue and trophoblastic villi are both rich in capillaries. Nourishment is obtained by the trophoblast in two Ways. Both
the villi and the trophoblastic cells at their base absorb nourishment
(“uterine milk”) from the maternal tissues, and extravasted blood and
 
u
9
a
 
QC
5:".
 
F10. 176. Cross sections of placentae. A, pig; B, cow; C, out. (Modified from Grosser.)
 
d.. degenerating uterine epithelium; 0., embryonic capillary; m., maternal capillary;
mes., mesoderm of serosa; s., epithelium of serosa; u., uterine epithelium; v., villus.
 
cell débris from the crypt walls are ingested by pseudopodia from the
cells of the trophoblast. Absorption and respiration also are brought
about by diffusion between the maternal and foetal capillaries. The
blood in these vessels is separated by very thin layers of tissue only.
The placental layer consists, on the foetal side, of the capillary walls,
connective tissue, and trophoblast, and on the maternal side of connective tissue, eapillary walls and, in the diffuse placentae, of uterine
epithelium also. Thus diffusion between foetal and maternal blood
vessels is easily carried on.
DECIDUATE PLACENTA 251
 
In the allantoic fluid of ungulates are found bodies of queer shapes
called hippomanes. These are formed as accumulations of coagulable
material from the uterine milk and become saturated with calcium oxalate crystals. They push, pocket-like, into the trophoblastic wall between the cotyledons and later are pinched off into the cavity of the
allantois, surrounded by trophoblast and allantoic wall.
 
Fm. 177. Embryo of sheep enclosed in embryonic membranes and showing cotyledonous
placenta characteristic of many ungulates. (Redrawn from Corning after 0. Schultze.)
 
a., amnion; c., cotyledon; e., atrophied end of blastodermie vesicle; u., umbilical cord.
 
Deciduate Placenta. In deciduate placentae the union of maternal
and foetal tissues is closer than in placentae of the non-deciduate type.
In deciduate placentae, part or all of the trophoblast, called the trophoderm, becomes specialized and, by the aid of enzymes, erodes the
uterine wall. At birth the lining of the uterus is removed as part of the
placenta. In the zonary deciduate type, this lining or decidua is in close
union with the foetal blood vessels, so that maternal and foetal tissues
are removed together. In the discoidal deciduate type, however, the
252 EGG AND EMBRYONIC MEMBRANES
 
maternal blood, which circulates in spaces in the trophoblast, is the
chief tissue lost from the uterus, for the deciduae are thin and degenerate.
 
The placenta of the zonary deciduate type occurs only in the Carnivora.
This placenta may in some respects be considered as intermediate
between the naon-deciduate and the discoidal deciduate types. In the
Carnivora, the trophoblast destroys the uterine epithelium (but not the
subepithelium) and eats its way into the wall of the uterus. Here trophoblastic villi invade the connective tissue of the
uterus and come in contact with the maternal
capillaries which are much richer than in the
nondeciduate placenta. Foetal capillaries
grow into the villi and foetal and maternal
blood are thus brought close together. This
placenta is therefore formed by fusion of
foetal and maternal tissues. The trophoblast,
connective tissue, and the capillaries of the
allantois contribute the embryonic part, and
the capillaries and connective tissue of the
uterus contribute the maternal part. The
maternal blood is separated from the foetal
blood only by these structures. The placenta
is at first thin, but becomes thicker owing to
the elongation and branching of the villi and
the growth of the connective tissue. When
birth takes place the blood vessels and connective tissue of the uterus are removed along
with the foetal vessels and the connective
tissue. It is possible that this placenta may
have originated from the non-deciduate type
by a closer association of the maternal and
 
pm 173_ Embm, 0f dog foetal tissues after the erosion of the uterine
 
showing band-shaped placenta wall_
11 te ' t' fth ' . . . .
((:R:iui*(:a.wrtisfil'(dxl)1 Co:§ill.:.1)vorcs The placenta of the dzscozdal deczduate type
 
differs from the carnivorous placenta in that
the cavities in which the maternal blood circulates are not maternal
 
capillaries but broad laeunar spaces which have formed in the walls
of the trophoblast itself. The tissue of the placenta is almost entirely of foetal origin. The placenta of the mouse may be taken as
typical of this type. In this form the trophoblast erodes the uterine
epithelium and attaches itself to the subepithelial tissues of the
uterus. It then develops lacunar spaces in its wall. Later after the
allantois has developed and has reached the somatopleure its capillaries
DECIDUATE PLACENTA 253
 
grow in between the lacunae of the trophoblast. Further growth of the
placenta is brought about by the thickening of this wall. Maternal blood
from ruptured vessels of the eroded uterine wall circulates in the lacunae.
The maternal and foetal blood, however, are separated from each other
only by the walls of the trophoblastic lacunae, a small amount of connective tissue, and the walls of the capillaries themselves. As these
lacunae are in such close relation to the allantoic capillaries, diffusion
is easily possible between them. The placenta of the mouse is typical
of the deciduate placentae of the discoidal type. Since maternal blood
 
 
fiG. 179. Diz1.gr:un of embryo of carnivore enclosed in uterus. Band—shuped placenta
IS represented as if transparent, showing embryo in section below. Letters as in fig. 171.
 
circulates in lacunar spaces in the trophoblast one can readily understand why the uterus loses only blood and a slight amount of connective
tissue at birth.
 
The discoidal deciduate placenta of the Anthropoidea is similar to
that of the rodents.
 
When a human trophoblast reaches the uterus it bores its way into
the wall and implantation is thus interstitial. The trophoblast becomes
differentiated into two layers, plasmotrophoblast, which is a plasmodial
covering without cell walls but containing many nuclei, and an inner
cytotrophoblast or layer of Langhans, which consists of distinct cubical
cells. The plasrnotrophoblast at its place of attachment to the uterus
erodes the uterine epithelium and dissolves the wall. The outer trophoblast has a spongy character and the spaces become filled with maternal
254 EGG AND EMBRYONIC MEMBRANES
 
blood from the eroded uterine wall. Later the spongy network is transformed into villi which are surrounded by the trophoblastic spaces that
now have the character of lacunae. These villi are at first solid, with
the syncytial layer on the outside and cells within except in late stages
when the cellular layer disappears. Some of the villi branch freely into
the lacunar spaces, but others anchor the trophoblast to the uterine
wall. The lacunae are lined everywhere, even on the maternal side, by
a syncytial layer. Later the mesoderm of the serosa wanders into the
villi which are now branched and which become vascularized by the
allantoie blood vessels. These so—called villi are very different from the
 
 
Fro. 180. Diagram of human embryo 1n utero.
d.r., decidua reflcxa; c.u., cavity of uterus, um., umbilical cord.
 
villi of ungulates, which are projections from the wall of the trophoblast.
They are not villi at all in this sense but are more like the foetal capillaries of rodents which are covered by the trophoblast into which they
have pushed. They are merely the irregular walls of the lacunae of the
trophoblast.
 
The villi are at first over the whole surface of the trophoblast (diffuse
placenta), but later, those nearest to the cavity of the uterus degenerate
so that here the surface is smooth. The villi of the other side remain
giving rise to a diseoidal-shaped placenta.
 
The uterine covering over the trophoblast is known as the decidua
reflexa or decidua capsularis. The part of the uterus where the embryo
is attached is known as the decidua basalis or serotina, and the opposite
wall the decidua Vera. In man the decidua capsularis comes in contact
with the decidua vera in the fifth month and the uterine cavity is
obliterated. Later the capsularis becomes non-vascular and gradually
DECIDUATE PLACENTA 255
 
disappears so that the trophoblast is in contact with the decidua Vera.
This in turn, becomes degenerate, as only the inner portion of the
uterine lining remains. The decidua basalis, on the other hand, takes
an important part in the formation of the placenta. The uterine capillaries increase and maternal blood from this region supplies the placenta.
In late stages, the basalis is reduced to a very thin membrane.
 
When birth takes place the amnion is ruptured, the amniotic fluid
escapes and contractions of the uterus expel the embryo, the break
taking place across the degenerate deciduae. Later, there is discharged
an afterbirth, which consists of the placenta with the thin layer of
decidua basalis and the attached membrane composed of fused amnion,
serosa, and deciduae capsularis and vera. It is thus evident that the
 
 
 
fiG. 181.
e.h., capillary of the decidua basalis; e.v., capillary of a villus; i, inter-villous cavity
 
filled with maternal blood; L., Langhan's cells (cytotrophoblast); m., mesoderm of the
serosa; s., syncitial layer (plasmotrophoblast); v.f.. fixation or anchoring villus.
 
only maternal tissue which is lost is uterine blood and a small amount
of connective tissue representing the thin layer of the degenerate lining
of the uterus. The largest part of the placenta is of foetal origin, but
maternal blood accompanies it.
 
In some of the monkeys, the placenta is double. There is, of course,
only one umbilical cord, but the two placentae are connected by blood
vessels. In the orang and gibbon there is a single placenta. The lower
monkeys have no decidua reflexa.
 
The following outline lists the characteristics of the embryonic
membranes and placentae in the different orders of mammals. In many
cases the embryology of only a few forms has been investigated. It is
probable that further investigation may show that some animals do
not follow in all respects the usual types found in their orders. Indeed,
it may be found that some show quite aberrant types, as is true of the
lemur, Tarsius.
EMBRYONIC MEMBRANES OF MAMMALS
 
 
Monotremata
 
Marsupialia
 
Artiodactyla
 
Yon: SAC
 
Like bird, contains yolk on
left side of embryo
 
Large well-developed, but
 
contains no yolk No extraembryonic coelome in
blastoderm opposite embryo During uterine life
there is yolk sac placenta
with exception of Pera—
melee
 
Small functional only in
 
early stages, when it is
vascular
 
Aiimion
 
Has sero—amniotic connection and is probably
formed :13 in Sauropeida
 
Probably formed by folds
 
Inner cell mass moves upward pushing trophoblast
away The folds from edge
of embryonic shield form
amnion
 
Penssiodactyla
 
Cetacea
 
Sirenia
 
Proboscidea
 
As in artiodactyls
 
As in artiodact) ls
 
Large amnion of Orca obIiteratc-s exttaembry onic
cavity
 
Amnion obliterates extra
embryonic coelome in Elephas
 
ALLANTOIB
 
Well-developed. on right
side of embryo
 
Small, since young are
born immature
 
Large, occupying most of
uterus Goat embryo 2
inches long has allantoia 2
feet long Hippomanea in
allantoic fluid
 
As in artiodactyls
 
In Halicore is large. as in
8|’tl0d8.Cl.\lS Hippomanea
in allantoic fluid
 
PLACENTA
 
None
 
Found only in Peramelas
Trophoblaat not involved
in its production, uterine
wall develops vascular
ayncytium
 
Rnimnxs
 
Oviparoifa egga with hard
shell Young fed milky secretion from primitive abdominal mammary glands
 
Series of forms through
Dtdelphys. Dan/uriia, and
Perameles showing transfer
of placental function from
yolk sac and allantoia
 
.\on—deciduate Most ruminants cotyledonary
Pig diffuse unbranched
villi Deer hippopotamus
earrel, girafle intermediate
 
l\on-deciduate placenta
Hfirse branched difiused
V] l
 
l\on-deciduate placenta
With diffuse, branched villi
 
‘Ion-deciduate W itli
branched difiuae villi arranged in band around
tropboblast (Really zonary non-deciduate )
 
fuse villi \ot classified
yet as to deciduate or nondeciduate but villi seem to
be like those of articdactyls
 
Central implantation
 
Membranes incompletely
described
 
Zonary placenta Vlltll dif
Embryology not Sufi
ciently investigated
 
256
 
EGG AND EMBRYONIC MEMBRANES‘
Carnivora
 
Edentata
 
Rodentia
 
Chiroptera
 
Insectivora
 
Primates
Lemuroidea
 
Anthropoidea
 
Large yolk sac probably
functional in early stages
 
Disappears
 
Large Invagination of upper wall gives apparent inversion of germ layers
 
Lpper wall acts as accessory placenta That of rabbits is more important nutn tive organ than allant ois
 
Functional onl
stage Repla
tois
 
in early
by allian
Large Yolk sac placenta
formed in Tupaija Mesoderm restricted to upper
wall in Talpa and Sore:
Persists until birth
 
Rabbit amniotic posterior
 
Formed from series of
folds
 
Large amniotic cavity oblitcrating extraembryonic
coelomc
 
folds formed after embryonic shield has taken superficial place on blastoderm
\/louse, rat giunea pig
closed sac inside inner cell
mass
 
Vespertillw confluence of
irregular spaces in embryonic knob forms amnion
 
Extremely large Grown
between 5 olk sac and trophoblast completely lining serosa
 
Small
 
Often small and endoderm does not grow out
beyond body as in mouse
and giinea pig
 
Replaces yolk sac
 
Hedgehog forms a closed Groves out prominently
cavity in embryonic knob dwarfing yolk sac
 
Talpa Sore: Tupaua
formed by folds
 
Small yolk sac early disappears (Tarnus small
vascular)
 
Small yolk sac with cavity
and vascular in early
stages
 
Tarsms formed by folds
 
Amniotic cavity formed in
inner cell mass
 
Very large fills extraembryonic space Tarsms
small outgrowth of gut remains in base of umbilical
cord
 
Small contained in stalk
of umbilical cord
 
 
Zonary deciduate
 
May be zonary oval bellshaped or difluse Marius
non-decidiiate with simple
diffuse villi Tatusm modfied discoidal deciduate
 
Discoidal deciduate
 
Discoidaldeciduate saucer
 
shaped or bell shaped
 
Discoidal deciduate usuallv concave In hedgehog
is decidua reflexa like that
of man but formed differently In mole acontradeciduate condition (allantoic capillaries separated at birth from placental trophoblast which
is absorbed by uterine
walls)
 
Non-deciduate diffuse
(Tarsius discoidal deciduate)
 
Deciduate. discoidal
 
Central implantation
 
Little known about mem
branes of edentates Central implantation in Ta!usm
 
Implantation is central in
rabbit eccentric in mouse.
interstitial in guinea pig
and gopher
 
Implantation eccentric (in
some forms)
 
 
Implantation central
 
Implantation interstitial
 
 
MEMBRANES OF MAMMALS 257
258
 
APPENDIX TO PART ONE
 
THE FMBRYOLOGICAL CONDITIONS OF ANIMALS FOUND IN THE VARIOUS PHYLA ‘
 
 
Germ
1' or- Types of
ma— Cleavage
 
Typra of
Blaatulae
 
Mesoderm
 
Ty pea of
Formation
 
Gaatrulation
 
i
 
«Xe =Occutrence in the
Phylum
 
X =0ccurrence in
Smaller Divisions of Phyla
 
Larval Forms
 
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Porifera . . . . . . . . . . . . ‘%
 
Coelenterata . . . . . . . :2 age
Ctenophora‘ . . . . X
Hydrozoa . . . . . . . X X
SC)’ hozoa . . . . . .. X
Ant ozoa . . . . . . . . . . X 3X
 
Platyhelminthes . . . . . .
 
, Amphiblastula and Parent.-hymula
— — — - -
 
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Treznatoda . . . . . . .
N emertmea. , . . . . .
 
Nemathelminthes. . .
Nematoda . . . . . .
 
T1-ochelminthes . . .
Rotifera. . . . . . .
 
Molluscoidea . . . . . . . .
Phoronida , . . . .
Brachiopoda . . . .
Bryozoa.
 
X
X
X
X
 
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3:e><
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Supposed to be nrochophore
 
X
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X
 
><><>< #>< at->< %é><><
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X ‘ X I Dlrc-ct development
 
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X Trochophorc, Blntrarxa
X I Trochophore
 
Uphxupluteus, Bipinnaria, Echmopluwua.
Aunculana
 
2
 
Annelida. . . . . . . . . . . . %%
Polychaeta . . . . . . . . X
Oligochaeta . . . . . . . .
 
Echinodermata..... 9%! i
 
Asteroidea . . . . . . .
Echinoidea . . . . . .
Ophiuroidea. . . _
Holothuroidea . . . . . .
 
Mollusca . . . . . . . . . . .
Amphineura. . . .
Pelecypoda . . . . . .
Gaateropoda . . .
Cephalopoda . . . . . . .
 
Arthxopoda . . . . . . . . . .
 
Ki3%>(><
 
m%‘é><><
 
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¥ xxxx
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Glochidxum
 
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and others
 
9%
ae
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Cruatacea_ . . . . . . . . .
Bx-anchnopoda. . . .
Ostracoda . . .
Copepoda . . . . . .
Eucopepoda. . . . .
Cimpedia . . . .
Amphipodn. . . .
Schizopoda ..
Decapoda . . . . . .
 
Myriapoda. .
 
Insecta . . . . . . . . . .
Coleoptcra . . .
 
Arachmda . . . ..
Ax-aneida .
Scorpionida. . . .
 
Chordata . . . . . . . . . . fié
Enteropncusta
Tumcata . . .
Cephalochordata X
Vercebrata .. .....
 
Cyclostomata
Petromyzontm
Myxinoidea .
 
Elaamobranchii. . .
 
Ganoidea. . . .. .
 
Teleoatei . . . . . .
 
Amphibia . . . . . .
 
Reptilia . . . . . .
 
Aves . . .
 
Mammalia . . X X
 
XX
X
 
x# X xxxxxx
xxxxx
x
 
Larva. pupa, and others
 
xxxxxxx
x x x x
 
xxxx xxx
% xxxxxxxxxxxxxxx
x x
 
 
tr”
 
X Tomnria.
Tadpole and others
 
#xx fixxxxxxxxxx
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#
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Tadpole
 
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X.
260
 
APPENDIX TO PART ONE
 
TABLE OF ANIMAL CLASSIfiCATION INCLUDING EXAMPLES OF
 
EMBRYOLOGICAL SIGNIfiCANCE
 
(None: This table does not include the forms listed in certain chapters in
Part Two, in which the systematic position is given in the text.)
 
Phylum Porif’era
 
Class 1. Calcarea
Order 1. Homocoela.
Leucosolenia
Order 2. Heterocoela,
Grantia, Sycandra
Class 2. Hexactinellida
Euplectella
 
Class 3. Demospongia
 
Order 1. Tetraxonida
Geodia, Cliona
 
Order 2. Monaxonida
Spongella
 
Order 3. Keratosa
Euspongia
 
Phylum Coelenterata
 
Type 1. Cnidaris.
Class 1. Hydrozoa
 
Order 1. Anthomedusae (Tubularia)
Hydra, Hydractimea, Pennaria, Bougainvillia, Clava, Clavellina,
Turritopsis, Eudendrium, Tubularia, Margelis, Nemopsis, Sarsia,
Podocoryne, Protohydra, M icrohydra, Pol:/podium
 
Order 2. Leptomedusae
Obelia, Campanularia, Plumularia, Sertularia, Clytia, Cory/morpha
M onocaudis, Gcmothyrca, Tima, Aequoria
 
Order 3. Trachymedusae
Campanella, Geryonia, Trachynema, Persa, Liriope, Aeginopsis,
Gombmmus, Haleremita
 
Order 4. Narcomedusae
Cunina, Cunocantha, Aegina
 
Order 5. Hydrocorallinae
M illepora, Stylaster
 
Order 6. Siphonophors.
Physophom, Nanomia, Diphyes, Physalia, Porpita, Velella, Halistemma
 
Class 2. Scyphozoa.
 
Order 1. Stauromedusae
Tessara, Lucemaria
 
Order 2. Peromedusae
Pericolpa, Periphylla
ANIMAL CLASSIfiCATION 261
 
Order 3. Cubomedusae
Charybdea
 
Order 4. Discomcdusae
Aurelia, Pelagia, Cassiopea, Cg/anea, Ulmaria, Stomolophus, Polyclonia
 
Class 3. Anthozoa (Actinozoa)
Subclass 1. Alcyoniaria
 
Order 1. Stolonifera (Tubiporidae)
Tubipom
 
Order 2. Alcyonacea
Alcyonium
 
Order 3. Gorgonacea
Corallium
 
Order 4. Pennatulacea
Pennalula, Ifenilla
 
Subclass 2. Zoantharia (Hexacoralla)
 
Order 1. Edwardsiidae
 
' Edwardsia
 
Order 2. Actinaria
Metridium, Halcampa, Paranemonia, Bunodes, Sagartia, Tealia,
Bicidium, Epizoanthus
 
Order 3. Madreporaria
Sclerophylla, Oculi/La, Aslrangirc, Aslrca, Faira, Fungia, Madrepora, Porites, Astroides, Mcandrina
 
Order 4. Antipatharia
Antipathes, Gerardia
 
Order 5. Zoanthidea
 
Order 6. Cerianthidea
Cerirmlhus
 
Type 2. Ctenophora
Class 1. Tenmculata
Cullianira, Plcurobrachia, IIrmm'phora, Mnemiopsis, Bolina, Cestus
Class 2. Nuda
Bertie, I dyia
Phylum Platyhelminthes
Subphylum 1. Platoda
Class 1. Turbellaria
Order 1. Rhabdocoelida
M icrostoma, Vortex, M onosceles, M onops, Stenostoma
 
Order 2. Tricladida
Poly/scelis, Planaria, Dendrocoelzmz, Bipalizzm, I2’(.’elloum, Gunda, Poly
chaerus, Syncoelidium, Phagocata
Order 3. Polycladida
Leptoplana, Stylochus, Thysanozoon, Discocoelis, Planocera, Yungia
Class 2. Trematoda.
Order 1. Monogenea (Polystomea, Heterocotylea)
262 APPENDIX TO PART ONE
 
Polystomum, Sphyranura, Epibdella, Gyrodactylus, Diplozoon, Tristoma,
Microcotyle
Order 2. Digenea (Distomeae)
 
Distomum (Fasciolaria), Monostomum, Bilharzia, Clonorchis, Paragonimus
 
Class 3. Cestoda.
Caryophyllaeus, Archigetes, Ligula, Tetrarhynchus, Echinobothrium,
Acanthobothrium, Bothriocephalus, Taenia, Anoplocephala, M oniezia,
Dipylidium
 
Subphylum 2. Nemertinea
Class 1. Nemertea
Order 1. Protonemertini
Carmella
Order 2. Mesonemertini
Cephalathrix
Order 3. Metanemertini
Geomzmertes, Tetmstemma, Amphiporus, Malacobdella, Nectonemertes
Order 4. Heteronemertini (Schizonemcrtini)
Lineus, M icrura, Cerebratulus, Zygeupolia
Phylum Nemathelminthes
 
Class 1. Nematoda
Ascaris, Ancylostoma, Trichinella, filaria
 
Class 2. Gordiacea
Gordius
 
Class 3. Acanthoccphala
Echinorhync/zus
 
Phylum Trochelminthes
 
Class 1. Rotifera
 
Philodina, H ydatina
Phylum Molluseoidea
Subphylum 1. Podaxonia
 
Class 1. Phoronida
Phoronis, Echiurus, Bonellia
 
Class 2. Gephyrea
Sipunculus
 
Subphylum 2. Polyzoa
 
Class 1. Entoprocta.
Urnatella, Pedicellina, Loxosoma
 
Class 2. Ectoprocta
 
Order 1. Gymnolaemata
Gemmellaria, Bugula, flustra, flustrella, Eschara, Crisia, Tubulipora,
Alcyanidium, Valkeria, Paludicella
Order 2. Phylactolaemata.
Plumatella, Pectinatella, Cristatella
Subphylum 3. Brachiopoda
 
Terebratula, Terebratulina, Lingula, Waldheimia, Rhynchonella
ANIMAL CLASSIfiCATION 263
 
Supplementary group of uncertain position, showing some relations to Entero pneusta:
 
Pterobranchia
Cephalodiscus, Rhabdopleura
Phylum Chaetognatha
Sagitta, Spadella
Phylum Annelida
Class 1. Archiannelida
Polygordius
Class 2. Chaetopoda
Subclass 1. Polychaeta
Order 1. Phanerocephala
Nereis, Podarke, Aphrodite, Lepidonotus, Autolytus, Polymie, Diopatra, N othria, Eunice, Syllis, Trypanosyllis
Order 2. Cryptocephala
Eupomatus, Hydroides, Spiroides, Arenicola, Amphitrite, Terebella,
Sqbella
Subclass 2. Oligochaeta
Order 1. Microdrili (Limicola)
Tulnfex, Dcro, Nais, Sparganophilus, Lumbriculus, Ctenodrilus,
Branchiobdclla
Order 2. Macrodrili (Terricola)
Lumbricus, Allolobophora, Diplocardia
Class 3. Hirudinea
Order 1. Gnathobdellidae
Ilirudo, Jllacrobdella
Order 2. Rhynchobdollidae
Clepsine, Pontobdella, Piscicola
Phylum Echinodcrmata
Class 1. Asteroidea
Asterias, Asterina, Astropecten, Heliaster, Pythonaster, Asteriscus, Culcita,
H ippasteria, Ctenodiscus
Class 2. Ophiuroidea.
Ophiura, Ophiothrzlt, Ophiopholis, Amphiura, Astrophyton
Class 3. Echinoidea
Cidaris, Arbacia, Toxapneustes, Strcmgylocentrotus, Coelopleurus, Spawngus, Echinocardium, Brissus, Echinarachnius, Clypeasler, M ellita
Class 4. Holothuroidea
Holothuria, Cucumaria, Psolus, Thyone, Caudina, M olpadia, Synapta
Class 5. Crinoidea
Rhizocrinws, Pentacrinus, Comatula, Antedon
Phylum Mollusca
Class 1. Amphineura
Order 1. Placophora (Chitonida) A
Amicula, Trachydermon, Chiton, I schnochiton, Cryptochiton
264 APPENDIX TO PART ONE
 
Order 2. Aplacophora (Solonogastres)
Proneomenia, Conchoderma, C/Laetoderma, Dondersia
Class 2. Scaphopoda
Dentalium
Class 3. Pelecypoda (Lamellibranchiata, Acephala)
 
Order 1. Protobranchia
N ucula, Leda, Yoldia, Solenomya
 
Order 2. filibranchia
Arca, M ytilus, M odiola, Anemia, Trigonia
 
Order 3. Pseudolamellibranchia
Pecten, Ostrea, M eleagrina, Lima, Pinna
 
Order 4. Eulamellibranchia
Anodonta, Unio, Pisidium, Cg/clas, Cardium, Astarte, Mg/a, Pholas,
Teredo, Aspergillum, Venus, M actra, Tellina, Salem, Dreissensia
 
Order 5. Septibranchia.
Silenia, Cuspidaria, Poromya
 
Class 4. Gasteropoda.
Order 1. Prosobranchia.
Suborder 1. Aspidobranchia
Acmaea, Palella, Haliotis, Margarita, Trochus
Suborder 2. Pectinibranchia
 
Littorina, Strombus, Sycotypus, Busycon (Fulgur), Crepidula, Urosalpinx, Murex, Paludina, Carinaria, Pleurobranchidimn
 
Order 2. Opisthobranchia
 
Suborder 1. Tectibranchia
Bulla, Philine, Aplysia, Haminea, Umbrella
Suborder 2. Pteropoda
Cymbiliopsis, H yalaea, Clione
Suborder 3. N udibranchia
 
Doris, Asolidia, fiona, Staurodoris
 
Order 3. Pulmonata
Helix, Bulimus, Limax, Lymnaea, Physa, Planorbis
 
Class 5. Cephalopoda
 
Order 1. Tetrabranchia
Nautilus
 
Order 2. Dibranchia
 
Suborder 1. Decapodn.
Spimla, Ommastrephes, Architeuthis, Loligo, Sepia
Suborder 2. Octopoda.
Octopus, Allopasus
Phylum Arthropoda
Class 1. Crustacea.
 
Subclass 1. Entomostraca
 
Order 1. Phyllopoda
Suborder 1. Branchiopoda
Branchipus, Artemia, Apus
ANIMAL CLASSIfiCATION 265
 
Suborder 2. Cladocera
 
Daphnia, Simocephalus, Leptodora, Polyplwmus
 
Order 2. Ostracoda
Cypris
 
Order 3. Copepoda.
 
Suborder 1. Eucopepoda.
Cyclops, Lemaea
Suborder 2. Branchiura.
 
Argulus
 
Order 4. Cirrepedia
 
Suborder 1. Eucirripedia
Balanus, Lepas
Suborder 2. Rhizocephala.
Sacculina
Subclass 2. Malacostraca
Superorder 1. Leptostraca
 
Order 1. Phyllocarida
 
Nebalia
Superorder 2. Arthrostraca
 
Order 1. Amphipoda
Gammarus, Caprella
 
Order 2. Isopoda
Asellus, Porcellio
 
Superorder 3. Thoracostraca
 
Order 1. Cumacea.
Diastylis
 
Order 2. Stomatopoda.
Squilla
 
Order 3. Schizopoda.
M ysis
 
Order 4. Decapoda
 
Suborder 1. Macrura
Palaemonetes, Crangon, Penaeus, Lucifer, Astacus, Homarus
Suborder 2. Brachyura
Dromia, Cancer
Class 2. Onychophora.
Peripatus
Class 3. Myriapodu
 
Order 1. Pauropoda.
Pauropus
 
Order 2. Diplopoda.
J ulus
 
Order 3. Chilopoda.
Lithobius, Scutigera, Scolopendra
 
Order 4. Symphyla
Scutigerella
266 APPENDIX TO PART ONE
 
Class 4. Insecta.
Macrotoma, 9. thysanuran; Hydrophilus, the water beetle; M iastor, the
fly; Leptinotarsa, the potato beetle; Copidosoma, parasitic hvmenoptera
Class 5. Arachnida
Order 1. Araneida
, Epeira
 
Order 2. Scorpionidea
Buthus, Euscorpius
 
Order 3. Phalangidea
Phalangium
 
Order 4. Acarina
Lepas, Izodes
 
Order 5. Pedipalpi
Tarantula
 
Order 6. Palpigradi
Kaenenia
 
Order 7. Solpugida
Eremobates
 
Order 8. Pseudoscorpionida
Chelifer
 
Order 9. Xiphosura
Limulus
 
Order 10. Eurypterida
Eurypterus
 
Supplementary Arachnid groups of doubtful relationship
Pantapocla, Tardigradn, Pentastomidea (Linguatulina)
Phylum Chordata
Subphylum 1. Enteropneusta
Balanoglossus, Dol2'choglossu.s, Ilarrimania
Subphylum 2. Tunicata
Cynthia, (Hana, Molgula, Appcndicularia, Distaplia, Botryllus, Salpa, Pyrosoma, Doliolum
Subphylum 3. Cephalochordata
Amphioxus, Branchiostoma
Subphylum 4. Vertebrate.
Series 1. Anamnia
Class 1. Cyclostomata
Order 1. Myxinoidea
M yzine, Bdellostoma
Order 2. Petromyzontia
Petromyzon, Lampetra
Class 2. Pisces
Subclass 1. Elasmobranchii
Superorder 1. Selachii
Squalus, M ustelus, Galeus, Raia, Acanthias, Scyllium, Carcharias, Cestracion, H exanchus, N otodanus, Pristiurus, Torpedo
ANIMAL CLASSIfiCATION 267
 
Superordcr 2. Holocephali
 
Chimaera
Subclass 2. Ganoidea
Amia, Acipemer, Lepisosteus (Lepidosteus)
Subclass 3. Teleostei
Serranus, Ctenolabrus, Bclonc, Salmo, Fundulus, Perca
Subclass 4. Dipnoi
Cemtodus, I’rotopterus, Lcpidosiren,
Class 3. Amphibia.
Subclass 1. Stegooephalia
Subclass 2. Lissamphibia
 
Order 1. Apoda ((iym11ophiona.)
Dermo]2Izis, Coocilia
 
Order 2. Urodela
 
Fam. 1. Proteidae
N ecturus, Proteus, Typhlomolge
Farm. 2. Sironidac
Siren, Pseudobmnchus
Farm. 3. Amphiumidac
Amphiuma, Cryptobranchus
Farm. 4. Salmnandridac
 
Ambystoma (Amblystoma, Siredon), Diemyctylus, Salamandra, Triton, Plcthmlon, Eurycea (Hpelerpes), Desmognathus
 
Order 3. Anura
Bufo, Rana, Pseudacris (Chorophilus), Ilyla, Pipa, Alytes
 
Series 2. Amniota
Division 1. Sauropsida.
Class 4. Reptilia
 
Order 1. Rhynchocephalia.
Sphcnodon
 
Order 2. Squamata.
 
Suborder 1. Sauria (Lacertilia)
Gecko, Draco, Anolis, Lacerta, Varamts, Iguana
Suborder 2. Serpontis (Ophidia)
 
Python, Boa, T/zamnophis, H ydroplzis, Elaps, Vipera
 
Order 3. Loricata (Crocodilia)
Alligator, Crocodilus, Gavialis
 
Order 4. Testudinata (Chelnnizi)
Testudo, Cizrysemys, Clemmys, Chelone
 
Class 5. Birds
Division 2. Mammalia
Subclass 1. Prototheria.
 
Order 1. Monotremata.
 
Echidna, Ornithorhynchus
Subclass 2. Eutheria
Division 1. Didelphia.
268 APPENDIX TO PART ONE
 
Order 1. Marsupialia
Didelphys, Perameles, Dasyurus, M acropus, Phascolomys,
Phascolarctus
Division 2. Monodelphia (Placentalia)
Section A. Unguiculata (Clawed Mammals)
' Order 1. Insectivora
Sorex, Talpa, Erinaceus, Tupaija
Order 2. Dermoptera
Galeopithecus
Order 3. Chiroptera
Vespertilio, Pteropus, Desmodus, M yotis
Order 4. Carnivore.
Suborder 1. fissipedia.
Canis, Hyaemz, Procyon, Felis
Suborder 2. Pinnipedia.
Odobalnus
Order 5. Rodentis.
Lepus, Sciurus, Mus, Camla
Order 6. Edentata,
Bradypus, Dasypus, Tatusia
Order 7. Pholidota. (Lepidota)
Manis
Order 8. Tubulidentata
Org/cteropus
Section B. Primates
Order 9. Primates
Suborder 1. Lemuroidea
Lemur, Tarsius
Suborder 2. Anthropoidea.
Cebus, Ateles, Simia, Gorilla, Cynocephalus, Homo
Section C. Ungulata (Hoofed Mammals)
Order 10. Artiodactyla
Bos, Camelus, Sus, Dicotyles, Hippopotamus, Corvus
Order 11. Perissodactyla
Equus, Tapirus, Rhinoceros
Order 12. Proboscidea.
Elephas, Loxodonta
Order 13. Sirenia
M anatus, Halicore
Order 14. Hyracoidra.
Procavia (Hyrax)
Section D. Cetacea
Order 15. Odontoceti
Dolphin, Delphinus, Phocaena, Grampus
Order 16. Mystacoceti
Balaena
 
==Part Two Embryological Problems==
 
CHAPTER I THE ORIGIN AND DEVELOPMENT OF GERM CELLS
 
A problem of very considerable embryologieal interest is that of the
origin and subsequent history of the germ cells. This is a matter of
great theoretical interest because of its bearing on the Weismannian
doctrine of the continuity of the germ plasm, and one which has been the
cause of much controversy, at least as regards certain of its aspects.
There are really three important phases of the problem; the place of
origin of the germ cells, the path of their migration to the definitive
gonads, and the subsequent history after reaching the germ glands.
 
A. VERTEBRATES
 
In Vertebrates the gonads arise from the genital ridges which develop
on the dorsal side of the body cavity between the mesentery and the
beginning kidney. This ridge is covered by the epithelium of the coelome
or peritoneum, which is known as “germinal epithelium.” From the
differentiation of this germinal epithelium in the four-day chick embryo
Waldeyer (1870) first described the beginning of the sex cells or germ
cells. Waldeyer’s view was accepted by the workers of his time as an
adequate explanation of the origin of the germ cells and has been given
as the only explanation in all of the text-books until quite recently. It
is, moreover, supported by the observations of a school of investigators
 
of the present day. It is, of course, true that with the formation of the '
 
gonad the germ cells are to be found in that organ and they appear
to have arisen from its epithelial covering.
 
In 1880 Nussbaum, as a result of his observations on the development
of the trout and the frog, reached the conclusion that the germ cells
were of blastomeric origin, being segregated in the early stages of deVelopment in a region outside that which will see the formation of the
embryonic body. They actively migrate or else are carried into the
body proper and into the germ gland by the growth forces which operate
to give the organism its body form. Since Nussbaum’s time the evidence
has steadily accumulated that in many vertebrates, as in well-known
cases among the invertebrates, the germ cells are early set apart from
the somatic cells and develop independently from them. Their history
may be traced backward from their appearance in the germ gland to
 
211
272 THE ORIGIN AND DEVELOPMENT OF GERM CELLS
 
very early stages and the path of their migration clearly made out in
many cases. Many careful investigations (Hoffmann, 1892; Eigenmann,
1892; Beard, 1900; Woods, 1902; Allen, 1906, 1907, 1911; Dodds, 1910;
Swift, 1914, 1915, 1916; Jordan, 1917; Okkelberg, 1921; Richards and
Thompson, 1921; Swingle, 1926; Hahn, 1927) have failed to reveal any
conditions not in accord with Nussbaum’s theory. It has been demonstrated that the primordial germ cells arise widely scattered in the
 
 
In. 125.2 Tr.ms\ erse section through .1 4 mm land of the bowhn Anna uzlza (After
Allen )
 
Gut end . gut cudodorm roof end , roof endoderm, penph end, peripheral ondodcrm,
Wolff cl . Wolfhan duct, s c . sex cells, lat mes , lateral mesoderm
 
endodeun or in the-splanchnic mesoblast in the extraembryonic area.
From this point of origin they pass with progressive development to
the region of the body axis. This movement has been accounted for in
three ways; it is usually thought that the cells actively migrate in an
amoeboid manner, passing up the mesentery and into the region of the
gonad. Swift found that the primordial germ cells of the chick are
carried in the blood stream, and in Fundulus it has been shown that
the forces which are responsible for the formation of the embryo body
carry the germ cells to their place. The movement of the cells of the
germ ring by confluence and the other normal processes which lead to
VERTEBRATES 273
 
the formation of the axial region of the body brings about the translocation of the germ cells as well as the somatic cells. Along the path
of migration there is no difficulty in recognizing the germ cells for they
have clearly marked characteristics. On these points there is rather
general agreement.
 
The subsequent history of these cells appears to be an uncertain
prob1em———one much involved at the present time in controversy. Some
investigators claim that some of these. cells never find their way into
the gonad, but undergo degeneration in various parts of the body.
Some (firket, von Berenberg—Gossler, Ilargitt, and others) claim also
that the primordial cells which may have arrived in the gonad by
 
 
flu. 183. 'l‘rans\'(-rse section through the hind gut of l).l—mm. larva of Amid crzlva.
(After Allen.)
 
coel., coelomie cavity; gut end., gut endodorm; mes., mesentery; s.e., sex cells; Wolfi’.d..
Wolffian duct.
 
migration in the manner indicated _do not actually give rise to the
definitive germ cells, for they find degeneration of these cells along
with proliferation of a second group of germ cells derived directly from
the genital epithelium. These latter, or even in certain cases a third
proliferation, are the source of the definitive germ cells. The primordial
germ cells in these cases may pass far through their cycle before degenerating, as shown by Kingery for the mouse and Swinglc for the
tadpole, in both of which the maturation cycle is practically completed
before the degeneration occurs.
 
In a recent account Swingle has reviewed the progress of the investigations on the Anura, He has shown from embryological studies that
there are in various parts of the United States “local races which differ
274 THE ORIGIN AND DEVELOPMENT OF GERM CELLS
 
markedly in regard to the time of occurrence and character of the
developmental processes involved in the formation of the definitive
testes.” He is convinced that the sex cells appear first in the endoderm,
and give origin to those cells which produce ripe sex products. Every
stage from the origin of the primordial sex cells to the fully developed
spermatozoa has now been traced in the bull frog, and no doubt now
remains as to the continuity of the germ line in this form. On the other
hand Hargitt and others have claimed that the germ cells arise in
urocleles from differentiated mesoderm, the peritoneum. Swingle sug—
gests that the discrepancy is due to an origin and segregation earlier
than their appearance in the peritoneum, and that after their segregation they wait in the layer where they are later seen for an appropriate
time for development. This is in agreement with his finding that local
races differ in the time of development of the sex cells. In the urodeles
they are incorporated in the mesoderm in an early stage whereas in
the Anura they are in the endoderm, but it is not necessary to assume
their origin in either layer because of the fact that later they appear in
the one or the other.
 
It is to be noted that none of the writers who find degeneration have
satisfactorily proven that all the primordial germ cells degenerate or
that none of them are left to produce definitive germ cells. It is also
noteworthy that recently certain evidence has been found which indicates that in an ordinary course of events the definitive germ cells are
derived from the primordial cells. However, owing to the power of
regulation which animals possess under the stress of unusual and harmful circumstances which bring about the degeneration of the primordial
cells, secondary sex cells may be proliferated from the germinal epithelium and produce the definite sperms or ova. At the present time the
safest interpretation seems to be that as a rule the primordial germ
cells thus early segregated in the vertebrates give rise to the definitive
germ cells, but that in exceptional cases, where the regular events are
interrupted and the primordial cells so disturbed as to cause their
degeneration, the organism responds by proliferating from the germinal
epithelium new cells which take their place. It must never be forgotten
that the chief characteristic of protoplasm, especially embryonic protoplasm, is its plasticity, its power of regulation and of adaptation to new
conditions. “Life is a constant adjustment of internal and external
conditions.”
 
Although the matter is still involved in controversy, some important
theoretical conclusions have already resulted from the investigations.
first of all, it is an obvious fact of major importance that heredity is
a matter of germ cells, and that the germ cells contain organized material
THE INVERTEBRATES 275
 
through which the continuity from generation to generation is carried
on. The germ cell mechanism is the mechanism of inheritance. Not only
is there continuity of germ cells but of the organized system (germ
plasm) which they convey. Secondly, the distinction between germ cells
and somatic cells is often more or less artificial and has in many cases
been emphasized unduly. Weismann himself spoke with less certainty
about the continuity of germ plasm than many of his followers have
done, although he without doubt was expressing a fundamental truth.
Yet there still remained a theoretical question which his formulation
of his doctrine did not fully state, namely, the possibility of the soma
contributing to or becoming part of the germ plasm. Various views on
this point have already been given.
 
It is the author’s opinion that with the possible exception of the
mammals no group has as yet presented evidence of positive character
that contradicts the view that germ cells as well as germinal material
are distinct from the somatic from a very early period. In the mammals
the situation is 11ot yet clear. It is worthy of note that the cases in
which uncertainty or confusion exists are exactly those which have
proven least satisfactory for cytological and accurate embryological
studies. When favorable material is available there is general conformity
to the expectations of those who would emphasize the importance of
the germ plasm. These include cases of determinative cleavage where
the germ—cell cycle has been followed in case after case, and also those
which have yielded clear figures for chromosome studies.
 
If in addition the recent view be accepted that the chromatin of all
cells represents the germ plasm and the cytoplasm the soma, as is now
held by numbers of students, the history of the germ cells becomes a
study of the specialization of chromatin and nuclei and that of the
soma one of cytoplasmic specialization. The general problem of the
germ-cell cycle is thus given its proper place as one of embryology,
where it is of great interest, and it is no longer one of theoretical significance to geneticists.
 
B. THE INVERTEBRATES
 
In the invertebrates there are many forms in which no suchMuncertainty prevails as in the case of the vertebrates. There are two chief
methods by which germ path is recognizable: 1.e., chromatin diminution
and germ-cell determinants. There are of course many cases in which
nothing is known of the development of the germ cells, but there are
in several groups of the invertebrates cases in which the germ path
(Keimbahn) has been-worked out in practical completeness. In the
coelenterates primordial germ cells were found by Weismann, Kleinen276 THE ORIGIN AND DEVELOPMENT OF GERM CELLS
 
berg, and others in a wandering condition early in the development
of hydroids. The details of Weismann’s observations have been disputed
by Hargitt, but his main contention is borne out that the germ cells
are recognizable long before the sexual individuals appear. The case
 
fiG. 184. The dexelopment of the germ cells of Sagilta. (After Elpatiewsky.)
 
A, fertilized egg showimz the “germ cell determinant,” B, 2-cell stage, germ cell determinant in one blastomere only; (‘, H—cell stage; D, szastrula with two primordial germ
cells. '
 
t 2., germ cell determinant; p.b.. polar bodies; p.g.c.. primm'diul germ cells.
 
which has been of greatest interest from the standpoint of the history
of the germ cells is that of Ascaris megalocephala as brilliantly worked
out in great detail by Boveri. In Ascaris (see Chapter IV, Section 3)
the first cleavage division results in two blastomeres, one of which is
purely a somatic cell while the other is a stem cell. The history of each
'rm«: INVERTEBRATES 277
 
fiG 185 Early stages In the development of Cyclops fuscus (After Amma)
 
A, first cleavage nucleus, 13, (laughter nuelex reconstructed with the ectosomes or germ
cell determrnants 1n one blastomere only, 0, second elenvage dnmon wrth the germ cell
determmants agmn l1m1ted to one blmtomere, D, l()-cell stage All the blustomeres m the
 
restmg condltmn except the stem cell, E, gastrula In whlch two pnmordral germ cells are
to be dlstmgulshed from the endoderm cells.
278 THE ORIGIN AND DEVELOPMENT OF GERM CELLS
 
of these cells has been fully described by Boveri. They are distinguishable
by means of a process known as chromatin diminution, part of the chromatin (the thick ends of the chromosomes) of the somatic cell being
cast from the nucleus into the cytoplasm, because of which process the
 
1
 
fiG. 186 A, longitudinal section through an oocyte of M iastor americami. (After Hegncr )
 
n c , nurse chamber, g v . germinal vesicle, p Pl , pole plusm, f ep , follicular epithelium
B, later stage of same in which somatic cells are beginning to form and blastoderm and
the two pl'll‘flB.!’y germ cells containing the pole plasm are already cut of?
 
somatic nuclei in subsequent cell generations are both lighter in color
and smaller than the germ cells. All the chromatin of the stem cell is
retained in this second division, but of the daughter blastomeres produced from it, one undergoes the diminution process while the other
divides directly in the regular manner and becomes again a stem cell.
Of the products of its division the same relation holds, for the process
THE INVERTEBRATES 279
 
is repeated four times. Thus, at the end of the fourth cleavage there
are fifteen somatic cells (which will give rise only to somatic cells
ordinarily) and one cell which is the primoridal germ cell and the
ancestor of all the germ cells. At the next division this divides again
 
Fm. 187. Continuation of fig. 186. A, similar stage of eight germ cells, blastoderm
complete; B, sagittal section through embryo with eight germ cells near the end of the
tail fold.
 
and the two cells thus produced give rise later on in the interior of the
embryo to all its sex cells.
 
In Sagitta, Elpatiewsky recognized in the fertilized egg a structure,
called a “germ-cell determinant,” which does not divide with the egg.
(fig. 184.) The blastomere containing it becomes a stem cell. In the fifth
division the stem cell produces a somatic cell and a primordial germ cell.
280 THE ORIGIN AND DEVELOPMENT OF GERM CELLS
 
In an early gastrula four cells have resulted
from two divisions of the primordial cell. The
subsequent divisions of the four are responsible for the formation of both male and female
germ cells (for the animal is hermaphroditic).
It is said that the two anterior give rise to
the ovary and the two posterior to the testes.
 
Among the arthropods there are many cases
of the early segregation of germ cells, and their
recognition is possible either through cytoplasinic inclusions (germ-cell determinants) or
by distinctive characteristics, particularly
chromatin diminution. In the Entomostraea
are two outstanding cases, M oina (Grobben)
and Cyclops (Haecker, Amma). Here the
stem cells are distinguished from the first
cleavage onwards. In the unsegmented egg
of (71/claps (fig. 185) certain granules (ectosomes) are to be found accumulating at one
pole of the spindle as the cleavage mitosis
advances. These granules are thus segregated into one of the
blastomeres which becomes the stem cell.
This process continues
through the fourth division and results in the
segregation of the primordial germ cells.
 
In the insects a germ path is recognizable in
several orders. In the Diptera (Mzestor, Kahle,
1908, Hegner, 1914, Chironomus, Hasper, 1911,
and in other cases) the germ cells appear at the
 
Fm. 188.
 
Longitudinal
section through ovarian egg
of ( hpixlosoma. almost ready
to be laid. (After Hegner.)
 
The germ cell determinant
(k) lies near the posterior end
of the egg.
 
 
posterior end of the egg as pole cells and can be
traced into the larval gonads. Here polar granules,
germ-cell determinants, or pole plasm, as the mass
is variously called, are present in the uncleaved
egg and enter the pole cells. In addition to this
in M iastor (figs. 186, 187) the pole cells are provided with two nuelei from the third cleavage
which have not undergone chromatin diminution
as distinguished from the other six. In the Hymenoptera. (fig. 188) an “oosome” is present in
 
fiG. 189. Longitudinal section through the
egg of Leptinotarsa drmlvnlirieata. (After Hegner.) The'posterior end
was killed with :1. hot
needle just after the
egg was laid. The egg
was then allowed to
develop for 24 hours.
bl., blastoderm; g.c.d.,
germ cell determinants; k.. portion of
the egg killed.
THE INVERTEBRATES 281
 
the unscgmented egg which in the 4—eell stage becomes associated at
the posterior end with the forming primordial germ cells. finally, in the
chrysomelid beetles (fig. 189), Hegner found a “polar disc” composed
of germ-cell determinants which participate in the formation of the
primordial germ cells. This relationship was made more certain by an
experiment which he performed. With a hot needle he killed the posterior end of the egg, l)ut allowed the remainder of the egg to develop. A
blastoderm was formed which was normal in every particular (up to
a certain stage) except that it was entirely lacking in germ cells.
 
These cases prove conclusively that among many invertebrates we
may regard the early segregation of the germ cells as satisfactorily
established. In addition to these there are many cases of cell lineage in
which there is no question but that the germ cells arise from blastomeres
segregated at a quite early stage. It is to be noted also that these cases
are among the best known of all animals, the material being abundant
and most favorable for the study of entire life cycles.
CHAPTER II
 
GERM-LAYER THEORY
 
It will be recalled that the old issue between preformation and epigenesis finally resulted in the overthrow of the cruder type of preforn1ation which held that development was simply an unfolding of parts
already existing in egg or sperm. As better understanding of the facts of
development was obtained it became clear that, although preformation
did not occur, there were definite signs of organization within the egg.
The developing organs could be traced farther and farther back until
it was evident that in general they came from what might be called
three plates or layers of tissue lying one over the other. These layers
give rise by various processes of folding, outpocketing, unequal growth,
etc., to the fundaments of the future organs. It was further obvious
that there is a great similarity in regard to this method of origins from
these layers in different kinds of embryos. These facts were known in
whole or in part to many of the early embryologists, including von
Baer (1828), and others, even back to the time of Wolff (1768). ()f
course the proper interpretation of cells and cell structure in the animal
kingdom had not as yet been made and it had proven impossible to
explain the origin of the layers in terms of any other lower units of
organization. It is not surprising, therefore, that these early embryologists should have looked upon the formation and subsequent development of the germ layers as the most critical processes of embryonic
life.
 
The germ-layer theory, which is distinctly an attack on the problem
of the organization of the embryo, has been one of the most fruitful of
all biological speculations. After the true nature of cells and their
methods of reproduction and growth came to be understood, the theory
acquired new significance and, in the hands of Oscar and Richard
Hertwig, had attained the status of a full-fledged theory of development
by the early eighties. Through a great variety of forms, blastulae and
gastrulae were identified, their methods of origin understood, and the
remarkably uniform character of all the processes involved in germlayer formation and in the laying down of the fundaments of the organs
was made out. Exceptions occur; indeed, some of them are of great
importance, but considered as a whole there is striking uniformity in
 
282
GERM-LAYER THEORY 283
 
the relationships of the layers to each other and to the subsequently
developing organs.
 
The essential point of the theory is that the three layers are homologous throughout the animal kingdom above the Porifera. In the
coelenterates, as in the gastrulae, there are present only ectoderm and
endoderm. Since the layers are homologous, the organs which arise
from them are also homologous wherever they are found.
 
In all metazoa there normally develops following the blastula, a
stage called the gastrula, of which the two component layers are known
as primary germ layers, the outer being the primary ectoderm (epiblast,
ectoblast), and the inner the primary endoderm (hypoblast or endoblast). The primary ectoderm in etenophores, turbellarians, rotifers,
annelids, and molluses contributes with the primary endoderm to the
formation of the middle germ layer, the mesoderm (mesoblast) giving
rise to the distinction of ectomesodcrm and cndomesoderm respectively.
From the outer layer also come: (a) the covering tissues with all their
modifications and appendages including hair, horns, nails, scales, skin,
glands, (b) the nervous system and sensory epithelium, and (c) in many
cases the stomodaeum and proctodacum (extreme anterior and posterior
regions of the alimentary canal).
 
The primary endoderm, in addition to cndomesoderm, produces the
lining of the midgut and of all the organs which are derived from it, as
pancreas, liver, etc. There is also exceptionally endoderm participation,
for example, in the formation of a part of the nervous system in some
coclentrates, but in some other cases, as in formation of blood cells
and endothelium of blood vessels, the evidence is not yet clear as to
whether it takes part.
 
The mesoderm may come, as already indicated, from the two primary
germ layers, but except as mentioned above, only the endoderm seems
to be involved in its production. There are several methods of mesoderm
formation. Isolated endoderm cells may push into a space between the
two layers at the same time with the secretion of a jelly-like substance,
thus giving rise to a filling-in layer known as mesenchyme from which
certain organs or parts of organs take their origin. In a second method
the typical epithelial character of the primary germ layers is preserved
and by outfoldings from the walls of the archenteron (primitive gut),
which becomes entirely disconnected from it, lateral coelomic pouches
are formed. This type of mesoderm is known as mesothelium. There
are also other processes by which coelomic walls may in special cases
be produced. The inner or splanchnic wall of the coelomic pouch unites
with the endoderm to form the splanchnopleure, and the outer or
somatic layer forms with the ectoderm the somatopleure. In some
284 GERM-LAYER THEORY
 
animals the middle germ layer is entirely mesenchymous; in others,
entirely mesothelial; and in many, both types are present. Either one
may develop first; in the echinoderms the mesenchyme arises before
the mesothelium and in the vertebrates after it. The mesoderm gives
rise to muscles, blood, skeletal and connective tissues, the excretory
organs (at least in part) and usually to the sexual organs, but not the
sex cells.
 
The surprising uniformity with which these relationships are held
throughout the higher groups of animals has been responsible for the
great importance of the germ-layer theory as outlined by the Hertwigs.
Probably no other theory or working hypothesis, with the exception of
Darwin’s own contributions, has been so fruitful as a stimulus for constructive zoological work. The germ-layer theory has to its credit much
of the most important embryological accomplishment. As a working
hypothesis it is of the greatest importance.
 
As an analysis of the problem of organization of the embryo, less
can be said for the germ-layer theory. Researches of later years with
careful technique have shown that the exceptions which formerly were
overlooked are in many cases difficult to harmonize with the theory
and, indeed, often operate decidedly to limit its usefulness.
 
Among the objections that have been cited are the following: inverse
relationships of the layers found in the sponges; the fact that the outer
layers of the (-estodes are in part or in toto thrown off leaving the covering
tissues doubtfully related to the eetoderm; the varying derivation
(depending upon the viewpoint of the observer) of the notochor(l
and mesenchymous connective cells in different chordate groups; the
composite nature of some organs, for example the nephridia, from
more than one germ layer; the identification of the mesoderm as the
4d cell, not a layer at all, in the individuals with spiral cleavage; and
especially the facts of budding, differentiation, and regeneration. Some
of these objections have proven difficult to answer although this fact
should not make us underestimate the value of this conception as a
whole. However, it is now known that there are many evidences of
organization appearing long before germ layers are formed. The promorphology of the ovum in the eggs with determinative cleavage and
the possibility of tracing out the cell lineage during cleavage and organ
formation in embryos of this class distinctly minimize the importance
of the germ layers. Back of this the organization of the chromosomes
and their part in shaping development as is now known from studies
of cytology and genetics again detract from the value of the theory.
 
We have now come to view the germ layers as representing a stage
in development just as we regard the blastula or gastrula as progressive
GERM-LAYER THEORY 285
 
steps. It is an essential stage in most cases through which the course
of development must pass, but in special cases adaptive modifications
have arisen. Homologies exist between blastomeres—sometimes, as
in the 4d cell and the “cross” of the annelids and molluscs, of very
striking character; they also exist between germ layers, between organs
and between organ systems. All are important, perhaps equally so.
But the germ layers are probably best regarded as temporary embryonic
organs which play their part and give rise to subsequent stages of development rather than as units of organization which determine the
future course of development.
CHAPTER III
THE RECAPITULATION THEORY
 
The corner-stone of the science of embryology as it developed during
the last half of the nineteenth century was the recapitulation doctrine.
This doctrine is also called the biogenetic law, or in Haeckel’s term,
the fundamental law of biogenesis. To it was due much laborious and
painstaking research, and the interpretations based upon it have had
far-reaching significance. Yet during the last decade critical studies
have dethroned this doctrine so that as a “law” it is now of value only
historically. As a tendency, however, recapitulation is still a useful
conception for it unquestionably expresses a partial truth, a fact to
which is due the long-continued interest in the doctrine and the stimulating effect it has had upon embryological studies.
 
Recapltulation refers to the parallel which exists between the history
of the race, in its largest sense, and the development which an individual
organism belonging to that race goes through. “Ontogeny rccapitulates
phylogeny.” The life cycle of an individual is a brief summary of racial
history. The animal kingdom presents innumerable instances which
illustrate this principle. The development of the frog tadpole, through
stages showing successively external gills, hind legs, front legs appearing
later, and the disappearing tail and gills, closely parallels the taxonomic
series of legless apoda and the salamanders. This series begins with the
lower urodeles which have external gills and weak legs, then comes
Amphzuma with small posterior legs, the Salamandridae in which external gills are lost, the legs are about equally developed, and the tail
is about equal to the body in length, and finally the Anura which have
no gills or tail and the hind legs are the better developed. (fig. 190.)
 
The development of the decapod Crustacea, in which the larvae
pass through stages comparable to those characteristic of some other
orders of the Malacostraca (fig. 191), is an often-cited case to illustrate
the biogenetic law. Another illustration involves the ascidians (fig.
192) which superficially resemble shapeless jelly-like masses, and whose
relationships are therefore difficult to decipher. A study of their embryology revealed the fact that they pass through a tadpole stage with
dorsal nerve chord, notochord, etc., all recognizable as vertebrate char
acters, but when they settle down and become sessile these structures
286
THE RECAPITULATION THEORY 287
 
gradually undergo degeneration and the creature loses all recognizable
signs of its former organization. An analogous situation obtains in the
 
d 8
fiG. 190. Early stages in the development of a frog tadpole compared with adults of
Siren (e), Amphiuma. (f), Desmoonathus (0), and an adult frog (h).
 
Cirripedia or barnacles. Barnacles have heavy shells, are sessile, and in
general are quite unlike the ordinary Crustacea to which their developZ66 'l‘l'1l!2 RECAPITULAT ION THEORY
 
inent clearly shows them to be allied. A second suborder of the Cirripedia doubtless presents the most extreme case of modification to be
found in the animal kingdom. This is Rhizocephala to which the parasitic Sacculina belongs. (fig. 193.) During its larval stages Sacculina is
a free-swimming form having about the usual external features of a
young braiichiopod crustacean. It attaches itself to the abdomen of a
crab, sends root-like branches into the body by means of which it obtains
nourishment, and completes its development to the adult stage. The
 
F1G- 191 -\. \ young lobster at the time of the third molt (after Herrick), and Ii. An
adult A1’,[”37-'3 (after Verrill).
 
(~x., exopodite, en., endopodite.
 
adult is so degenerate that it has no crustacean characteristics but is
merely a tumor-like sac on the abdomen of the crab in which even the
usual internal organs are scarcely present, the body being chiefly filled
with the gonads and their products. Only its life cycle reveals its relation to the other Cirripedia. The anatomical relationships by means
of which its phylogenetic position is determined are made clear by a
study of its cmbryological development.
 
Vaguely foreshadowed by the writings of Meckel and others of the
period, the recapitulation principle is first directly hinted at in the
writings of von Baer. Indeed, by some von Baer’s laws have been conTHE RECAPITULATION THEORY 289
 
fused with the recapitulation theory. These laws are, however, Inore
properly regarded as alternative to certain phases of recapitulation.
They were formulated by Von Baer in 1828 as follows:
 
“1. The more general features of a large division of animals arise in
the embryo earlier than the special features.
 
“2. From the most general features of structure arise those that are
less general, and so on until the most specific features arise.
 
“3. The embryo of a definite species tends away from the specific
forms of other species, instead of passing through them.
 
 
In. 19.2 An adult mcidmn (\) ((}Illl)LlrUd \\lli| 1 lirxal {min of the same type (B)
( Uter Deluge and Huounrd )
 
“4. Fundamentally, therefore, the embryo of any higher species is
never like the lower species, but only its e1nbryo”—(Lillie).
 
It will be noted that these laws antedate the cell doctrine and the
publication of the “()rigin of Species,” and that the simultaneously
enunciated germ-layer theory represented the last word in emhryological
knowledge of the time in the matter of early structural organization.
The advances made possible by the cell doctrine resulted in the enunciation by Fritz Muller in 1863 of the recapitulation doctrine as such.
Haeckel developed the theory and applied it in his famous blasteagastrea hypothesis.
 
Haeckel’s hypothesis lays stress on the importance of the universal
occurrence in the embryology of animals of the single-celled egg, the
290 THE RECAPITULATION THEORY
 
blastula, and the gastrula, and supposes that the phylogenetic development has taken a similar course. The protozoa represent the first step
and are comparable to the egg stage in individual development. No
animal is known which exactly corresponds to the blastula or the
gastrula, although there are protozoan colonies quite like the former in
some respects and simple eoelenterates have features in common with
the latter. Haeckel, therefore, supposed that there must have been stages
corresponding to each of these forms which had now ceased to exist,
 
and to these hypothetical forms he gave the names “Blasted” and
“Gastrea.”
 
 
Fm. 193. A nauphus (A) and u (‘ypris larva (B) compared with an adult ((‘) Saeculma
carcmt. (After Deluge.)
 
Haeckel also pointed out the significance of certain characters as
indicating phylogenetic history whereas others are to be regarded as
embryological adaptations of importance to the individual organism,
but not to the race. Characters of the first class are spoken of as palingenetic; of the second, as cenogenetic. A chick embryo, for instance,
has a good many characters which recall fish or amphibian conditions,
but it could not exist in the environment where these forms dwell, and
is different in numbers of other characteristics including the important
one that it will develop not into a fish or amphibian, but a bird. It cannot, therefore, in its development represent with entire correctness the
ancestral forms. Some of its characters are those which adapt it to
development in a shell at a temperature of 37° C. and enable it to live
in the peculiarities of its own environment. These are new or ceno—
genetic characters. Other features, as the aortic arches, gill slits, brain
THE RECAPITULATION THEORY 291
 
vesicles, and others, are supposed to be of ancestral significance and
are, therefore, palingenetic.
 
A critical consideration of many cases which may be cited, however,
shows that the facts do not all easily fit into the biogenetic interpretation.
When one attempts to classify clear cases such as the shell tooth on the
one hand or the aortic arches on the other as adaptive or ancestral
little difliculty is experienced, but the problem of applying the same
classification to a doubtful ease becomes much more complex, and as a
rule the results cannot be certainly relied upon. Indeed, recognition of
a particular character as palingenetic or cenogenetic may be quite an
impossible task.
 
Other difficulties may be cited which require modification of the strict
biogenetic way of looking at the animal kingdom. For example, there
is a general tendency which becomes more marked the higher one goes
in the animal kingdom to shorten and condense the ancestral phases of
an organism’s development in favor of the specializations which relate
it to its own environment. This tendency, in addition to complete
changes of developmental conditions (for example, the long placental
life of mammals, or the abundance of yolk in bird eggs), may result in
the entire omission of certain stages (as in the case of embryos where
gills do not develop in connection with gill arches).
 
This abbreviation or contraction of development is called by some
writers tachygenesis. In the brief period of embryonic development,
if reeapitulation occurs even in the most sketchy fashion, an immense
contraction of stages must be thought to take place so that the necessary
abbreviation may be accomplished. To this shortening of the developmental time, or tachygenesis, there are two aspects, the actual quickening of the rate of development and the fusion and omission of certain
stages. The one aspect may occur without the other in special cases as
in the response of the developmental rate to rise in temperature, where
the rate is hastened without fusion or omission of stages.
 
Hcterochrony also presents an argument against the reeapitulation
doctrine, as was pointed out by Keibel, Mehnert, and others. By heterochrony is meant the disturbances, which now are known to be of quite
common occurrence, in the time of appearance of structures in a known
sequence of stages.
 
These modifications in the rates of development bring about results
which cannot be interpreted either as of phyletic or adaptive significance.
Stockard has lately pointed out the importance of the arrest of development, even over a small part of the germ ring, whereby various types
of monsters are produced. Evidently, here are structural modifications
not to be related to recapitulation. Furthermore, the normal develop292 THE RECAPITULATION THEORY
 
ment of the organ systems of the embryos of different classes does not
preserve the same synchrony as may be noted by comparing tables of
the development, let us say, of the chick and pig (Keibel, N ormentafeln).
In addition, there are extreme cases in which the actual order of development is the reverse of what would be demanded by recapitulation,
as, for example, in those cases in which the joints become rounded off
before movement is acquired. Another illustration is the formation of
the tongue and the teeth. There is no question that in the phylogenetic
series teeth made their appearance before tongues, but in the embryological development of mammals the teeth are much later developed
than the tongue. Ontogeny not only fails to recapitulate phylogeny
in this case, but completely misrepresents the facts.
 
In a recent discussion De Beer has summarized the possibilities of
variation which heterochrony offers in comparing the appearance of
structures in the individual with that in the ancestral forms. This
summary with no further elaboration is sufficient to make clear that
some of the possible variations not only do not fit in with the conception
of recapitulation but are actually opposed to it. The summary is as
follows 2*
 
“A character which is present or makes its appearance in the young
stage of an ancestral animal may in the ontogeny of a descendant
 
appear:
 
“A. In the young stage only, producing youthful adaptations or
caenogenesis,T not affecting phylogeny.
 
“B. In the young and adult stage, producing a substitution of the
new adult condition for the old, resulting in a progressive denation in the ontogeny of the descendant from that of the ancestor.
 
“C. In the adult, by a relative retardation of the development of
the bodily structures as compared with the reproductive organs,
resulting in paedogenesis and neoteny.
 
“A character which is present in the young and adult stage of an
ancestral animal may in the ontogeny of a descendant appear:
 
“D. In the young stage only, resulting in the reduction of the
character to a vestige.
 
“A character which is present or makes its appearance in the adult
stage of an ancestor may in the ontogeny of a descendant appear:
 
“E. In the adult stage, resulting in those differences which distinguish individuals, varieties, and races: adult bariation.
 
* Reprinted from De Beer's “Embryology and Evolution,” by permission of Oxford
University Press.
’{ The same as cenogenesis.
THE RECAPITULATION THEORY 293
 
“F. In the late adult stage, 1'.e., too late, resulting in the reduction
of the character to a vestige by retardation.
 
“G. In the same stage, which is no longer adult, the new adult
stage being relatively delayed, resulting in overstepping the
previous ontogenies or hypermorphosis.
 
“H. In the young stage, producing precocious appearance of the
ancestral character and acceleration.
 
“Cases B and C which produce phylogenetic efiects by introducing
youthful characters into the line of adults may be combined under the
term paedonzorphosis. Cases E, G, and H which produce phylogenetic
eliects by modifying characters which were already present in the line
of adults may conveniently be included under the term geront0morphos2's.”
 
In Inany forms the problem is further complicated by the prolongation of certain stages while internal processes are going on. If the
gradual internal development of a caterpillar were accompanied by
gradual conversion of the biting type of mouth parts to the sucking
type, the insect would starve, for during the transition the mouth parts
would be adapted to neither the larval nor the adult method of nutrition. By the prolongation of the biting stage until the internal parts
are ready for the metamorphosis, the animal’s relation to its surroundings are unchanged until the internal conditions are right when a sudden
metamorphosis brings about the necessary adjustment to a new environment without loss to the insect. These facts are not in keeping
with the biogenetic law as usually interpreted.
 
Experimental embryology and genetics have not been without their
bearing upon the doctrine of recapitulation. It is now possible to show
that external factors reacting with the internal, inherited constitution
of the organism can produce such effects upon the oflspring that its
entire ontogeny including the adult is modified. As stated elsewhere,
Stockard has shown, for example, that developmental arrests will
produce many types of modifications in Fundulus, including two heads,
trunks, or even two individuals where only one would have otherwise
been formed, and conversely that the age-old tendency of the egg to
produce two eyes on the fishes’ head can be changed by the simple
addition of a little magnesium chloride. The internal, inherited control
of development is thus capable of modification. And Muller has shown
that by exposure to X-rays the developing Drosophzla can be induced
to react in such a manner that entirely new mutations, that is, selfperpetuating strains, can be produced, even at will. Thus is phylogeny
deceived by ontogeny’. For these reacting ontogenies have produced
an entirely new series of adults which can undoubtedly become an294 THE RECAPITULATION THEORY
 
cestral to others later to appear. Now phylogeny means to most thinkers
just a series of adult forms having racial significance. Hence it would
appear that such experiments as that of Muller have brought us face
to face with an exact reversal of the usual causal role attributed to
phylogeny, for here phylogeny is the direct result of ontogenetic modification and certainly not the controlling cause of it, as it is usually
considered to be by the adherents of recapitulation.
 
From the criticisms which have been given the student can understand why the so-called “fundamental law of biogenesis” has passed
from the high position of a natural law, and is little more than a general
tendency. It is a tendency, furthermore, which is more valuable in
retrospect than as a means of prediction. And since prediction upon the
basis of known facts and postulates is the goal of science and the fundamental test of a “natural law,” this doctrine does not measure up to
scientific expectation and cannot be regarded as a law.
 
Yet the partial truths which are involved are of sufficient value in
view of the widespread occurrence of the tendency represented to
warrant a revaluation of the essential idea of the doctrine. We find an
attempt of this kind expressed some years ago by Lillie in his work on
the embryology of the chick. His views appear to go far in the direction
of harmonizing the useful parts of recapitulation and at the same time
to avoid some of the contradictions which have been mentioned. He
conceived that the entire life history of an organism is as necessary for
the definition of species as any other character. Ontogenies are inherited
also and are subjected to variation with resulting modification. Ontogenies of closely related species are more nearly alike than those less
related. In the evolution of a species those stages of ontogeny latest to
have arisen (those found in the adult) are the ones most easily to be
modified and hence the embryo as a rule retains the ancestral resemblances the longest. This is not because these have phylogenetic, that
is palingenetic, significance, but because the embryo is less susceptible
to outside influences and therefore its characters are less the material
upon which selection may operate. Embryonic resemblances being more
conservative and actually older are nearer the ancestral condition.
They are statements of historical facts rather than causes of recapitulation. But because of the chronological sequence of stages in a great
many observed cases, the older recapitulationists came to regard each
stage as strictly causal to the succeeding ones and thus to look upon
the tendency exhibited as a law of nature.
CHAPTER IV
ASEXUAL REPRODUCTION
 
Asexual reproduction occurs in a great many plants and in many
animal groups. Among the invertebrate phyla it is lacking only in the
arthropods, molluscs, and nematodes of the more important groups;
while among the chordates, the tunicates present many illustrations of
this mode of reproduction. It should also be noted in passing that even
in certain mammals a process of budding in the embryonic state occurs.
This matter is discussed at length in the chapter on polyembryony
where it is shown that the blastocyst of the armadillo regularly buds
to produce four embryos. This gives asexual reproduction a place even
among the highest groups.
 
In spite of the fact that this method of reproduction manifests itself
in many different forms, it is essentially a very simple process. It occurs
in organisms (or in portions of organisms) which have retained to a
considerable extent their embryonic, undifferentiated character, and is
really a mass division, due especially to the cells of some particular area
undergoing a proliferation which presently results in the constriction
and cutting ofi” of a greater or lesser portion of the animal. If the portions
are approximately equal the process is spoken of as fission; if unequal,
as budding. These, with sporulation, are the common forms of asexual
reproduction, but each shows many variants in the animals in which
it occurs.
 
Sexual reproduction, involving the participation of two individuals,
is known as amphigony; asexual, since only a single individual is necessary, is monogony. In the former, germ cells or their equivalents are
produced; in the latter, there are no special cells employed for the purpose. The alternation of a sexual with an asexual generation is called
metagenesis. The alternation of a biparental sexual generation, that is,
a case of amphigony, with a uniparental, a parthenogenetic, generation
is heterogony. Sexual reproduction was further called gamocytogony
or cytogony by Hartman, and asexual, agamocytogony (also agamogony).
 
fission is the division of an organism into two parts which are approximately equal and into whose formation very little new material has
gone. The parent organism is lost in the production of the daughters,
 
which therefore can have no living ancestors, and can undergo only
295
296 ASEXUAL REPRODUCTION
 
what may be termed accidental death. It occurs when growth has taken
place in excess of the needs of the individual. Contrasted to the condition in sexual reproduction, the new organism is at once provided
with at least part of the organs which characterize the adult, and differentiation is always well advanced, considering that the organism is
seldom high in the scale of animal life. Two categories were distinguished
by F. von Wagner for organisms undergoing fission: in the one, paratomy,
a special zone, in which the constriction will occur, is prepared before
fission begins; in the other, architomy, no preparation is made, constriction taking place more primitively with little bodily reorganization. It
should be noted that both of these categories may apply to either longitudinal or cross fission. Under the general head of fission may also be
placed those cases of fragmentation, such as occur in oligochaetes and
starfish, due to external influences, which may, if conditions are suitable,
develop into mature individuals. These cases are also spoken of as
autotomy, and sometimes as augmentation.
 
Budding, although not much more complex as a process than fission,
is productive of much more complicated organisms and life cycles. It
often is the means by which colonies are formed, and results in marked
polymorphism with some of the individuals of the colony being specialized for nutritive and vegetative purposes and others for reproduction.
Commonly where a considerable degree of specialization follows the
budding processes the life cycle includes a sexual as well as an asexual
phase and we have alternation of generations. A bud is a small portion
of the parent organism which has begun to grow actively and to proliferate and from which will be derived a new individual having the full
degree of differentiation characteristic of the species. There are buds
in some triploblastic animals which involve only one of the germ layers,
whereas in other animals the buds may include more than one layer.
Furthermore budding may occur in embryonic, larval, or mature
animals. Abundant illustrations of all these cases may be cited.
 
There are several types of budding. The most familiar are the external
buds such as occur in Hydra for example in which a small portion of
the parental tissue grows and constricts off to become a new, small
hydra. In some of the hydroids, however, the separation is incomplete
and the new individual remains as a permanent bud. The so-called “free
buds” of certain forms are also of the external type. As buds they break
off and become for a time at least free swimming. A second type includes
the internal buds among which are the gemmulae of sponges, the statoblasts of the bryozoa, the germ balls of trematodes and others. A group
of proliferating cells becomes isolated within the mother organism and
in time results in a new organism. A third type involves the formation
OCCURRENCE OF ASEXUAL REPRODUCTION 297
 
of a stolen or a “runner” from which numerous buds arise. This might
seem to be really a kind of external budding but it is sufficiently distinct
from the usual cases of this kind to warrant special mention. finally a
fourth series of processes should be included under budding, although
they are often overlooked; they are the processes known as frustulation
and laceration in which small fragments separate off from the parent
organism, when unfavorable conditions arise, and form new individuals.
 
Closely related to asexual reproduction and of much significance to
the comparative embryologist are the phenomena of regeneration.
Morphogenic processes are involved in the reorganization of portions
of the old individuals to produce new ones which do not greatly differ
from the preceding. These processes involve the regeneration of the
organism or of portions of it. The student of comparative embryology
should give careful thought to these processes, for in them are manifested
fundamental capacities and characteristics of living protoplasm. Indeed
some of these processes take us far into the innate organization and
give an insight into the nature of living stuff which the Inorc usual
studies fail to offer.
 
The formation of colonies is closely correlated with the occurrence
of asexual reproduction. Colony formation occurs in certain phyla in a
striking manner, and it is in these very phyla that asexual reproduction
is a dominant method. It may be taken as a general rule (not, however,
without exception), that whenever individuals are found organized into
colonies, either asexual reproduction, or polyembryony, or parthenogenesis will be found to occur in the same groups. The simple sexual
mode of reproduction seems not usually adequate to produce enough
individuals to be associated together in a permanent colony, and one of
those three accessory modes must be depended upon for the increased
task.
 
OCCURRENCE or AsEx}JAL REPRODUCTION
 
The first examples of asexual reproduction to be found in the animal
kingdom are in the protozoa, but the process here is one of single cells
and perhaps is thus somewhat outside the general problems of embryology. We may begin our study therefore with the Porifera.
 
Porzfera. In the phylum Porifera, asexual reproduction predominates;
here are to be found fission, budding, formation of free buds, and of
gemmulae. Since most sponges exist as colonies it is easy to see how the
dividing processes have lacked completion resulting in a degree of union
that is more or less extensive. Asexual reproduction commonly leads to
formation of colonies rather than to independence of organisms. But
budding and fission are shown to advantage in Leucosolenia. Some of
298 ASEXUAL REPRODUCTION
 
the individuals indicate fission as their mode of reproduction for the
products are equal in size although they remain attached at the basal
end. However, the presence of small immature individuals on certain
 
 
Fm 194 Budding and fission in Leucosolema blanca. (From Korsehelt and Heider)
 
specimens as well as the mode of colonial formation shows that budding
is often the actual method of their origin. When fission does occur it
begins as a split at the osculum and progresses toward the base. When
 
 
fiG. 195. A, Budding in Leucosolema botryozdes B, A bud which has become free and
attached to an algal filament. (From Korschelt and Heider, after Vasseur.)
 
it is not complete the beginning of a colony is seen and these colonies
 
often become quite complex.
In another species of Leucosolenia (botrymdes), Vasseur long ago
THE PORI FERA 299
 
found free bud formation. The buds form from an indifferent group of
cells, grow irregularly from the parent individual, undergo differentiation to a considerable extent, and at length break off, the ruptured end
forming the osculum of the new little sponge; they then settle down to
produce young sponges.
 
The sponges show what is perhaps their highest degree of asexual
reproductive activity in the formation of gemmulae, seen to best advantage in the Hexactinellidae. They are derived from parenchymal
cells which have wandered into the mesoglea and become separated
from their original layers. Aggregates of these “archeocytes” (also
called “sorites” by some) take on an oval or rounded shape, become
 
 
I‘it. 106 (:(‘lllI‘n1ll( forination in Eph;/dalm blrmbmata (From Korschelt and Heider.
Liter Evans )
 
A, an early stage showing the aggregation of the ‘ germ" cells (g) from those which
make up the covering membrane (m) B, the cutieular membrane (c) is beginning to form
from the outer membrane
 
surrounded by a special membrane and thus make up a gemmulc.
During conditions which are not favorable, this structure, which is
really an internal bud with a protective covering, tides over the organism
until a more suitable time. Thus this form of reproduction is a device
which enables these sponges to adapt themselves to changing environments. The parental tissue degenerates and dies after the gemmules are
formed. When the gemmules begin to grow, the cells multiply rapidly,
those at the surface arrange themselves in a layer, and from the gemmules a larva issues which is strikingly similar to the sexually produced
young in form, structure, and ciliation.
 
Division among sponges is often accidental so far as the organism is
concerned, and the animals offer opportunity for experimental fragmentation as well as normal. H. V. Wilson’s work and that of J. S.
300 ASEXUAL REPRODUCTION
 
Huxley give illustrations of the extent to which sponges may be dismembered (in these cases by being squeezed through bolting cloth) and
subsequent regeneration serve to produce new sponges. Often cell
masses come together, fuse, and grow into a new individual from which
a colony is formed. This is called concrescence and may also occur
between larvae as they creep about on the bottom.
 
Coelenterata. By the eoelenterates many developmental experiments
along the lines of asexual reproduction seem to have been tried as well
as those which have already been shown for the various types of embryos,
cleavage patterns, and methods of gastrulation. Nearly all types of
asexual reproduction are exhibited somewhere in the phylum. In addi
 
Fm. 197. Trunsversc fission in Protohydra. (From Korschclt and Heider. ufter Aders.)
 
tion there is often manifested an extreme polymorphism in the forms
which are thus produced, and the details of the manner of their production especially where a compound type of budding is involved are
often extremely complicated. Mention here can be made of only a few
cases which constitute a very meager outline indeed. fission, both
transverse and longitudinal, budding both larval and adult, and colony
formation by the production of permanent buds, metagenesis, stolen
formation, fragmentation, frustulation, laceration, and the related,
although in its results opposing, process of concrescence, occur in this
group.
 
The Hydrozoa exhibit only a few types of asexual reproduction. Transverse fission occurs in Protohydra, according to Aders, and consists in
THE HYDROZOA 301
 
the simple constriction of the animal around the region of its greatest
diameter. The constriction cuts the animal into a proximal and a distal
portion. The one develops a new base, the other a new oral region. A
similar type of division may occur in Hydra; although undoubtedly very
rare, this was one of the earliest cases to be described (Trembly, 1744;
see also Koelitz, 1908). It is of essentially the same character as in
Protohydra, the chief points of difference between the two being in the
simpler structure and the lack of tentacles on the part of the latter.
Longitudinal fission has been described for Polypodium only among
hydrozoa.
 
Budding by larval as well as by adult hydroids is not uncommon. An
example of budding in the larval condition occurs in Gonioncmus and in
Ilaleremita as described by Schaudinn, Perkins, and others; the details
of the life cycle in these forms have been lately worked out by Joseph.
The egg hatches into a tiny planula larva. It develops a mouth and
creeps about actively while feeding in Haleremita, although the planula
of Gonionemus is sessile. On the sides of these larvae protuberances
appear which grow into buds that gradually elongate to become like
the planula, then constriet at their bases, and at length separate. The
descriptions of the processes differ greatly in detail as described by the
different investigators. For example, from one to six buds have been
reported by the various students, according to Joseph, near the base of
the larva, although Perkins found them about the middle rather than
the base. In some cases the endoderm of the bud is said to be solid, in
others to contain a cavity derived from the gastrovaseular cavity of the
mother larva. There are also other differences in the details as given,
some of which are doubtless to be attributed to the fact that both
European and American forms have been used by the investigators.
Lateral buds also have been described as occurring on Microhydra,
where they may form tiny colonies of three or four polyps.
 
Among adult hydrozoans budding occurs in both polyps and medusae.
In Hydra and the colonial hydroids it is of such common occurrence
that mere reference to it is suflicient. The bud of Hydra consists of a
protuberance which grows, develops tentacles, a hypostone, and at
length a mouth, after which it is ready for separation from the parent.
Both layers of the body wall participate in the formation of the bud,
and the gastrevascular cavity is continuous between parent and bud
until the time of complete constriction of the latter. Budding is much
more common than sexual reproduction. In hydroids the process is
essentially the same except that it is usually incomplete, the bud remaining in connection _with the parent stalk; in this manner a colony is
formed. ’
302 ASEXUAL REPRODUCTION
 
A special case of hydroid budding is that which gives rise to the
medusa which is morphologically the equivalent of a bud from a polyp.
There are cases, to be sure, where the ontogeny is so abridged that the
polyp stage is extremely rudimentary or even entirely lacking, unless
the planula be regarded as representing it, and the egg develops continuously into the medusa. But in general the medusoid generation is
produced by budding from the hydroid generation or the polyp. The
main stalk, or hydrocaulus, has attached to it in Obelia, modified
hydranths, called gonangia, which bud to produce medusae. In Obelia
these become detached to swim freely. In the Narcomedusae a proliferating stolon buds off medusae which may remain in clusters or may
separate off completely. In the siphonophore, Halistemma, the planula
develops an ectodermal thickening at the aboral pole which develops
into the pneumatophore or float. Part of the planula becomes the
eoenosarcal axis from which spring buds which become several different
kinds of individuals. Those near the float are bell-shaped medusae,
through whose efforts the colony is enabled to swim. Next come a series
of covering scales which seem to be retrogressed medusae; they are protective in function. At various places along the coenosarc are feeding
tubes in general similar to a hydranth. The tentacles and feelers also
are probably to be looked upon as hydranths. finally there are the
reproductive individuals which resemble certain types of medusae.
 
It will be seen from a consideration of all these cases that budding in
the hydrozoa directly results in the formation of colonies. All hydroids
which bud form colonies. Usually the planula develops directly into
the first hydranth and the colony is formed by the subsequent branching
and budding. This brings about in all except the simplest cases a very
considerable degree of polymorphism. There are defensive and sensory
individuals and in these the cnidoblasts are well developed. The gonanth
or gonangium has for its purpose the function of reproduction, and
various modifications of gonangia are to be found throughout the group.
Medusae which are free swimming show a greater degree of differentiation than any of the other types of individuals produced in a hydroid
colony. There are, however, numbers of medusa forms in which the
development is incomplete, and some of them are quite simple in
structure. As an accompaniment to the more complex polymorphism
which we find in these colonies metagenesis, the alternation of generations, is perhaps shown here to a degree of completeness that scarcely
exists elsewhere in the animal kingdom. The sexual functions are transferred to certain individuals while others specialize along the lines of
feeding and protecting the colony. Hydroid colonies not uncommonly
reproduce by another asexual method, namely stolonization. From the
THE HYDROZOA 303
 
hydrorhiza of the original polyp cylindrical projections grow out which
elongate, creep about on the bottom and may branch or even anastomose. These are stolons or runners upon which new hydranth buds
appear to produce new individuals. Bougainvillia and Clavularia both
serve as illustrations of colonies which grow by stolon formation.
 
In the second class of coelenterates, the Anthozoa, transverse fission
occasionally occurs in young animals which have not yet developed sex
organs. In Fungia as described by Bourne, the development of the larva
at a certain stage results in the separation of its distal part and after a
complicated series of processes two individuals are produced. Longitudinal fission is common among the Anthozoa. It is a slow process
beginning at the oral pole in some cases, although in Actinia it may take
place simultaneously from the aboral as well. In the adult Sagartia and
in Paranemonia a constriction begins at the pedal disc and passes in the
course of twenty-four hours to the oral region. In some others it is much
more rapid. Furthermore the constriction of one individual to produce
several at the same time may take place. In this case the resulting individuals will be of varying size, and it has been observed that one
division may not even be completed before a new one begins. Strange
complications thus arise in which the individuals may have several
mouths or several systerrs of septa at the same time owing to this
multiple fission. In the Anthozoa irregular longitudinal fission sometimes
gives the appearance of budding. True budding, however, is rarely met
with in the sea anemones. In the alcyonarians, however, much-branched
colonies are formed by budding and the individuals undergo modification and even produce a very considerable polymorphism. The Zoantharia likewise owe their extremely complicated type of development
to both fission and budding. In both these latter groups stolon formation
and subsequent budding are commonly observed.
 
One of the most striking forms of asexual reproduction is that manifested by the scyphozoa in the process of strobilization. This has already
been described in the chapter on “Types of Invertebrate Larvae.” The
planula develops into a hydranth-like form called the scyphistoma. By
a series of divisions which may be repeated perhaps a dozen times there
are constricted off from the scyphistoma, ephyra larvae of which there
may be one or several. If there is only a single ephyra strobilization is
said to be monodiscal, if several are produced it is polydiscal. The
question arises as to the nature of these divisions. The first ephyra is
commonly said to be formed by terminal budding and it would seem
that if the successive ones are produced only slowly they likewise are
terminal buds. However, in certain well-fed scyphistomae the process
of strobilization takes place so rapidly that the lower individuals are
304 ASEXUAL REPRODUCTION
 
already indicated by constrictions before the upper ones have progressed
to any considerable degree of independence. It would seem that the
distinction between terminal budding and transverse fission in this
case is a difligult one to draw. The scyphistoma also for a considerable
part of the year produces other scyphistomae by lateral budding in a
manner similar to that in Hydra. All at length, however, undergo strobili—
zation and produce ephyrae which gradually develop into adult jellyfish.
In certain scyphozoans another type of asexual reproduction occurs in
the formation of stolons from the original hydranth. They grow out
from its base but remain in connection with it and their buds form a
colony.
 
Before leaving the coelenterates the attention should be called to the
other methods of asexual reproduction already discussed, namely,
fragmentation or laceration and frustulation. In the actinians laceration
is rather frequently seen, especially when the conditions of the water
become unfavorable. A part of the basal rim begins to spread out, the
ectoderm develops quite profusely and endodermal portions grow out
into this new area. This then separates from the main body owing to
the contractions of the latter and from the pieces so produced new
anemones may at length regenerate, although the ability to do so is
dependent upon the number of septa present. Frustulation occurs in
the hydroids. Occasionally a small bud-like branch is observed to constrict off from the parent colony, to settle down on the bottom in which
condition it is called the frustulum, to grow and to produce a hydranth.
In hydranths also a process somewhat similar to laceration has been
observed, although in this case it is spoken of as fragmentation, for a
basal portion of the polyp is cut off and may develop into a young polyp.
 
A final question in connection with the coelenterates naturally arises
as to which condition is the more primitive. There are three possibilities:
one, that budding is the primitive type of asexual reproduction; two,
that fission is primitive; and three, that both arose independently of
each other. There have been interesting discussions of this question
and transitions between them have been pointed out. It need only be
said here that the evidence is not conclusive for either view.
 
Platyhelminthes. In the phylum Platyhelminthes the dominant type
of asexual reproduction is fission, although there are also causes of
budding. It is most common among the Turbellaria, although the polyclads have not been shown to reproduce asexually. Undoubtedly the
phenomenon of asexual reproduction in this division of the animal
kingdom is closely concerned with the ability which all members of the
phylum have for extensive regeneration. In its simplest form, as for
example, in the triclads, Planaria abissima and P. alpina, the reproducPLATYHELMINTHES 305
 
tion really consists in the separating of the animal by transverse fission
into two portions each of which proceeds to regenerate the missing head
or tail. In Planaria all the species described show that regeneration may
take place at various levels proceeding from the anterior to the posterior.
An area of regenerating tissue
appears which enlarges and then
differentiates. Sometimes a second
fission makes its appearance before
the complete regeneration following
the first, and indeed there are recorded cases of several divisions with
the appropriate organs already developing before the first is completed.
 
Among the rhabdocoels fission is
an even more general phenomenon.
The small fresh-water M zcrostoma
reproduces mainly by fission. Commonly this process occurs before the
young have developed sex organs in
this form and in Stentostoma, and the
divisions may take place in such rapid
succession that chains of individuals
incompletely divided are the result.
Division takes place by paratomy
very slowly, that is, a zone of division
is prepared and the organs of the new
portion of the animal are already developed to a considerable extent
when constriction occurs. If the constrictions follow each other more
rapidly they come under the category
of architomy, no special region being A
prepared in advance. The distinction pm 195
 
S\l(‘('(“§‘\l\(‘ lI‘f'lH§V€l'EaC fis
betwcon pal-altolny and 3'1-chit/Oxny sions 111 (A) Stuwstmnum SM-boldi, and
 
. (B) '11 trrnslomum lmcarr (From Kormay perhaps be made clear by Saylng schelt and Holder after v Grofi )
 
that the regeneration Of the new Pharvnx is shown for each single inorgans precedes the actual fission in dividual, and the dn 131 111 planes of the
 
_ different ranks are numbered
paratomy, no great change in the
 
organization of the animal taking place at the exact moment of division. On the other hand, in architomy, regeneration and subsequent
reorganization follow the constriction.
306 ASEXU AL REPRODUCTION
 
In general, asexual reproduction in the trematodes is rare and certainly
never occurs in any individuals which have a complete set of sex organs.
The situation with regard to the germ balls which produce the rediae
has already been referred to in connection with the chapter on in
vertebrate larvae and also that on polyembryony. It is still looked upon
as an open question as to whether parthenogenesis or asexual reproduction is the method by which the germ ball that forms the new rediae
is produced. It has been pointed out that originally they
were regarded as asexually produced, more recently as
developed in parthenogcnie ova, and finally that the
cytological study of these supposed ova has not yet
shown evidence of a reduction division such as would
be necessary to establish surely the fact of their parthenogenic nature. If we are to regard them as asexually
produced then this type becomes of much more widespread occurrence among the trematodes than is usually
considered.
 
Among the cestodes there are two aspects to the
question of asexual reproduction. One has to do with the
formation of the proglottids from the scolex, the other
with multiplication of the eysticercus. The first of these
involves a decision as to the fundamental nature of the
proglottids. Is the tapeworm to be looked upon as a
colony of individuals or as a single one? If the latter
 
fiG 199 * view is taken there eanof course be noquestion of asexual
 
fzvsli::;:::;;::)‘lf,? reproduction involved. If on the other hand the pro~
T‘”"“‘ "‘”““7’3 I ttid is re arded as an individual since each h‘
“ltll an accessory g 0  . ’  a
v(..,,,.1e attached complete genital apparatus and since each has the ability
S°°l°°°5 “"3 to live at least for some time after the separation from
present in both _ _
(From Korschelt the remainder of the worm, then its method of forma;‘3';‘:tI){°'d°" “Mr tion must be looked upon as budding, it being thus
 
. produced from the scolex. It is the writer’s opinion that
 
the colonial view is not as generally held now as formerly.
 
There can be no question that in the development of the tapeworm
from the eysticercus budding does occur. The egg develops into the
onchosphere, the six-hooked embryo, in which condition it escapes from
its adult host, and is taken in by the intermediate one. From it develops
directly the eysticercus. The scolex of the eysticercus arises from a
thickening in the wall of the bladder which becomes depressed into the
cavity and later this bud-like structure is cverted to form the little worm.
 
It occasionally happens that two or more scoleces are formed by budPOLYZOA 307
 
like thickenings on the wall of the same bladder. This multiple production of scolices is rather rare but occurs regularly as is well known in
Taenia echinococcus with disastrous results to the host. This is of course
reproduction by budding. In some forms the bladders themselves may
constrict and produce two vesicles each of which buds into a scolex.
Polyzoa. Since the Bryozoa, or Polyzoa as it is now becoming custom~
ary to call them, commonly form colonies, it is to be expected that
asexual reproduction will be found in this group, and the expectation is
borne out. Three asexual methods, as well as polyembryony, are found
here. They are budding, stolonization, and the formation of statoblasts.
As a manifestation of the complicated condition which asexual reproduction may reach in a single group, the Bryozoa probably exceed any
other branch of the animal kingdom. A student of the subject will find
much to interest him in the group and may expect to see an everchanging variety of detail as he studies the different divisions of it. For
 
 
Fm. 200. Buds of ('ris!aleHa muredo in median section. (From Korschelt and Ileider.
after Braem.)
ee , ectoderm, m., mesoderm.
 
the general student of comparative embryology, however, it seems unnecessary to give more than a very brief consideration to the general
types of asexual reproduction as they are developed here. From a consultation of the table of classification on page 260 the student will
observe that the phylum Molluscoidea, of which the Polyzoa are a
portion, consists of animals very diverse in structure and in their
method of development. They range from rather simple colonies to
aggregations of organizations which are complex in the extreme. Among
the simplest genera is Cristatella, coming under the ectoproct order,
Phylactolaemata. All the individuals of a colony of this form can be
traced to the first one which develops from the larva. This individual
produces buds commonly as thickenings of the pharynx on the oral
side, both ectoderm and mesoderm participating in the process, although
the ectoderm contributes a larger portion to the formation of the new
individual. As the bud enlarges it grows out from the parent individual
and its inner cell mass undergoes a very considerable differentiation.
The intestinal tracts commonly remain in communication at least for
308 ASEXUAL REPRODUCTION
 
some time. An entire series of buds which in their turn repeat the process
is involved in the production of the colony. The development of buds in
the Endoprocta closely resembles that just described. The bud is first
an enlargement of eetoderinal cells which receives migrations of meso
W
 
 
 
0
 
F16. 201. A piece of Plumalella fungnsa showing the formation of the primary buds and
of those which arise secondarily.
 
dermal cells as it develops. In this group a stalk makes the bud rather
more independent than in the preceding. In some forms, notably the
ectoproet groups Crissia and Tubulipora, budding takes place in the
embryonic stages even before any differentiation of the blastomeres
begins. The primary embryo produces a
 
32 B13 C D E F great number of buds in such a case and
B, may become a stem and retain the others
as secondary embryos or it may be en—
tirely destroyed in their production. Of
course the secondary embryos may also
reproduce asexually. It is rather rare that
the buds should separate naturally from
each other, for it is by their uninterrupted
relation to each other that the colony is
Fm 202. Dmgmmmntic “_pm_ formed. They may branch laterally from
 
aem,m.,n of the method 0; i,m,ci.- the main stalk or may continue in a direct
 
in“ i" P“”"“"'”“ f"‘“‘”"*"“' (l“'°’“ line of the main branch. It is obvious that
Korsehelt and Heider, after _ , . _ ’
Bmem) in such a highly organized type of animal
as this, polymorphism of the individuals is
to be expected. Special morphological changes take place so that some
of the individuals of the colony become very much changed from the
typical form and have very different functions. The Bryozoa. always reproduce by sending out stolons which then bud many times. The formation
of the stolon itself is like that of the bud but it grows out as a stalk which
 
by repeated incomplete divisions produces a new portion of the colony.
 
A
 
I V
AB3B‘~’BBC‘C D E 1‘ G
POLYZOA 309
 
Some fresh-water forms produce hibernacula. which.‘ are essentially
winter buds, club-like swellings on the stolons which enclose themselves
in a cutaneous capsule during the period of severe winter. In the spring
their development continues to form new colonies. Accidental subdivision of a colony is of course common, but the multiplication of the
colony by fragmentation appears also to occur naturally.
 
fiG. 203. Production of zooecia ns buds from stolons (st.) of Pedicellina erhinala.
(From Korschelt and Heider, after Ehlors.)
 
A final method of asexual reproduction is the formation of statoblasts.
According to an old view a statoblast is supposed to arise from a single
cell and upon the basis of this it was thought to be a sort of winter egg.
It is now realized that the statoblasts are modified buds which have
become changed into reproductive buds. They vary in shape, but are
enclosed in a cutaneous capsule and contain several cells. They are
310 ASEXUAL REPRODUCTION
 
able to withstand extremes of temperature and thus serve to carry on
 
the colony during the cold of the winter.
Amwlida. Asexual reproduction is of common occurrence in the two
most important groups of the annelids, namely the polyehaetes and the
 
 
Fm. 204. Statoblasts of Cristatella mucedo. (From Korschelt and Heider, after Kraepelin.)
 
oligochaetes. This is due to the remarkable uniformity in the structure
which the annelid body possesses, each segment being very similar to
its neighbor. The growth of the annelid worm is accomplished by the
 
   
 
J __ ._5B.'5:'l!
 
w
 
 
 
 
 
C
‘SIN! _
.. " ifl‘-Jijurvl
‘ .u1l1“‘L4“ .
 
 
 
F10. 205. Developmental stages of the statoblasts of Crietazella. (From Korschelt and
Heider, after Verworn.)
 
addition of the somites to the posterior end primarily, although anterior
zones of budding are also found. In some instances the formation of new
somites takes place more rapidly than their separation from the animal
ANNELIDA 31 1
 
and thus a chain of individuals is formed. In a simple annelid chain in
which the individuals of a series are spoken of as zooids in anticipation
 
 
fiG. 206. Germinating statoblasts of Cristatella. (From Korschelt and Heidcr, after
Braem.)
 
A. the “germ disc" stage. B, its invagination preparatory to further growth.
 
of their future development to individual worms the anterior individual
represents the original worm and is obviously the oldest. At its posterior
 
 
fiG. 207. Posterior end of Trypanosyllis misakiensis showing buds of difierent ranks.
(From Korschelt and Heidor. after Johnson.)
 
end is a reproductive zone where the budding oil’ of new individuals
takes place. The first individual budded off is of course the most posterior
3 12 ASEXUAL REPROD1 'C'l‘ION
 
of the chain, the others grading in age and size
toward the middle of the worm where the budding
zone is located. In the more complicated cases, of
which the syllids are the extreme example, we
may have not only terminal budding but also
lateral and even ventral. In one of these forms,
Trypanosyllis misakiensis, single budding soon
produces numerous buds in all
directions differing in age but
,.,:‘:.:-as *;:::r;..:" Merwisc giving the W231‘(Fmm Komheltamui ance of a rosette of small zooids.
after v. Kenr}x]<:)l.) Between these two extremes lie
gen‘: 0,  S ‘V various degreesof complication
in the forms produced. In many
marine polychaetes a differentiation with respect to
reproductive capacity is observed between the (lif
ferent parts of the animal. The anterior portion of
 
 
the individual is sexless and is spoken of as the atoke. = H
At the time of sexual maturity this slow-moving
worm becomes very active, the hinder somites de- = 1
 
velop gonads, and special 1
 
‘W bristlesandparapodiagrow
 
El ‘ W _ out on them, developing
 
lllllllll  them for rapid and exten
sive movement. This sexual
 
portion is spoken of as the __
 
cpitoke, and individuals of "
 
this kind were earlier given
 
special systematic descrip
tions. It is now clear, how
ever, that N ereis, for ex— Fm- 209. Diu. grains to show the
 
ample; passes Over "Ito divisions zones in
 
H eteronereis or the epito— £0": hmlzaa. d(fir{or}1
- . . t kous stage. In many po1.v- dfflfnir c‘L'how..,°.3
 
chaetes, the epitokous por
tion separates from the remainder and swims
: ' , ' ' d t th —
 
Fm. 210 The mlom about a(t1vely for a certain perio a e sur
 
worm. Eunice vimkiis, show- face of the sea. This is the swarming which
 
5”‘! ‘he ‘“”°’°“°° be‘“"~‘°" takes place in N ereis and is especially notable
the anterior ntokous part , ' . . . .
and the posterior epitokous in the palolo-worm, Eumce 1)27'Zd’l8, whose
 
portion. (From Korschelt . ‘ ' ' ' d
and Heme“ aim W00d_ swarmxngm the south Paeificisoften observe
 
ward.) as a very unusual phenomenon.
ANNELIDA 313
 
A further (-lassificatioii of tho asexual methods of reproduction in this
group may he based upon the degree of preparation which precedes
 
fiG. 211. J! yriamda fumata with 29 zooids. (From Korscholt and Heider. after
Maluquin.)
 
the division. In the simpler cases the division of the worm takes place
between two segments with no special zone of separation having been
developed. Following the division regeneration occurs producing a head
314 ASEXUAL REPRODYCTION
 
or tail, or in some cases where a portion of the middle of the worm is
cut off from both ends both head and tail are regenerated. As has been
pointed out this regeneration after division is known as architomy in
contradistinction to paratomy where a. separation zone is developed
before division. Such a zone is really the beginning of an early regeneration and may be present in variable degrees all the way from a simple
region of constriction to the formation of a well—developed head and
sensory apparatus.
 
Architomy is illustrated in Ctenodrzlus monostylus where without
much preparation the worm divides into an anterior and posterior part
by constriction and the lacking parts
are regenerated. Regeneration begins
at once, although the new worms continue to creep about actively in spite of
the fact that they cannot for a short
while take in food. Architomy may be
accomplished by autotomous division
of the worm. A number of polychaetes
and oligochaetes have such great powers
of regeneration that they are enabled
to separate without external stimulation. Lumbnculus is an annelid of this
type.
 
Paratomy is illustrated by certain
species of Ctenodrzlas also, especially
C. serratus, in which the regenerative
powers are so great that even single
segments may in certain cases produce
new worms. Beginning a few segments
 
Fm 012 Tami”: mulomm with a back of the head, cellular prolrferations
pnmaw" ,e;;(.,,e,a,,,,g Dome" and mo takeplacewhichgraduallyformthicken  ings on the anterior side of each segment.
 
' They become the head folds and give
rise to the organs of the head region in the new zooids. Thus a chain of
zooids is formed asexually. Additions of this sort produce what is functionally an alternation of generations. It is scarcely developed with the
regularity that characterizes this process in such forms as hydroids. The
original individual was developed from the egg. It produces asexually
a chain of zooids which separate from each other and when weather
conditions become suitable develop further into individuals which reproduce sexually. Of course second and third asexual generations may
be produced in the same manner as the first one.
PTEROBRANCHIA 315
 
Echinodermata. Among the echinoderms asexual reproduction is
described, but it is certainly of rare occurrence and one has difliculty in
distinguishing it from an extreme type of regeneration. Spontaneous
division of the arms and in some cases the splitting of the disc have been
described in the asteroids, ophiuroids, and in the holothurians. Asteroids
have been seen to split and separate, beginning at the gullet, and then
 
flu. 213. S1/Ilis ramosa showing anterior end of worm and the complex branching. The
gut is stippled in the figure. (From Korsehelt and Heidor. after Maclntosh.)
 
the missing arms and organs of the disc to become gradually regenerated.
It is of course well known that where accidental separation of the parts
of an echinoderm is brought about extensive regenerations follow and
theoretically there is no great difference between this and a natural
type of division followed by regeneration. However, the latter is certainly of earlier occurrence.
 
Pterobranchia. The two genera Cephalodiscus and Rhabdopleura which
compose the anomalous Pterobranchia both illustrate asexual reproduc316 ASEXUAL REPRODUCTION
 
tion by budding. Their doubtful position showing similarities both to
Balanoglossus and to the Bryozoa is nevertheless in line with their type
of reproduction. Cephalodiscus occurs as a single individual from the
side of which a stalk grows out. This stalk bears a bud as is shown in
the well-known figure often copied from Maclntosh. The bud arises from
the apex of the ventral stalk and after a certain age breaks off. The
animal lives in a gelatinous coenoecium where a large number of free
individuals may be found. The animal possesses practically all the
important organs found in Balanoglossus and structurally seems related to that form. Its method of asexual reproduction, however, much
more strongly resembles that of the Polyzoa. Resemblance to the latter
group is rather more striking in Rhabdopleura which lives in a tube and
reproduces in a manner similar to that
of the stoloniferous Bryozoa. The general
anatomy, however, closely resembles that
of Cephalodiscus. In Rhabdopleura the individuals derived from the buds remain
close together and form small colonies
living in branched tubes. They are con—
nected by a muscular cord which passes
back to join a common stem or stolen.
The cord is the narrowed proximal portion
of the body. By its contraction the animal
is retracted into a stalk. The stolen is developed as a bud from the original zooid,
 
1«'.c.. 214. ('c1)Iw,lod£scus with but the details of the process are not well
§:f:‘lt'i$;:f’)“‘M“°I“t°*h'“'i”"“°‘ll‘ understood. Part of the stolen loses its
 
formative power and becomes merely a
connection between the creeping parts of the colony. The remainder,
however, buds, and the buds give rise to branches. In the free-growing
part there always appear two buds, an anterior, well—developed one
and a posterior much younger.
 
Tunicata. Among the tunicates asexual reproduction is widespread
and occurs as an important means of multiplication in two of the main
divisions of this subphylum, the composite ascidians and the salps.
The dominant type is budding but the details show various departures
from the simple form and even instances of fission are observed within
this group. It will perhaps serve our purpose to limit our discussion to
the budding in the two cases mentioned, understanding that there are
some other minor examples to be met with in this group. The embryology of the ascidians has been described in Part One of this book. The
young embryo grows and in many cases begins its process of budding
TUNICATA
 
317
 
before it has become attached and begun its metamorphosis. It is customary to speak of the individual which is produced from the egg as an
oozooid whereas the individuals which are produced from buds are
blastozooids. However, the individuals so called may become modified
 
in various ways and be given other names to indicate functional and morphological differences
which later occur, for budding in the tunicates as in
some other groups leads to polymorphism and to
alternation of generations.
 
In the compound ascidians there are two main
types of budding, palleal and stolonial, differentiated
according to the position on the oozooid in which
they occur. By palleal budding, which also goes
under the name of peribranchial or atrial, or also
cntero-epicardial, is meant the growth of a bud as
an oesophageal or even intestinal outgrowth; it is
thus derived near the atrial wall and under the
mantle or pallium. It is common for the buds to be
formed as lateral evaginations of the body Wall in
symmetrical parts, but usually only one of them
develops. Mesoderm and germ cells migrate from
the tissues of the mother into the bud which gradually becomes a complete individual. The processes
are the same in the asexually produced blastozooid
and in the oozooid which are developed from the
egg, but the oozooid undergoes a retardation in development and never reaches sexual maturity
whereas the blastozooid develops fully although it
is to be noted that both may reproduce asexually
as well as sexually. The oozooid is short lived. After
it has reached the typical form of the ascidian it
undergoes retrogression and its tissues are used to
build up new individuals. In the composite aseidians
although the buds are independent of each other
they yet remain enclosed in a common cellulose
mantle, and after a number of generations have
 
         
 
   
 
‘ ‘~ .-..-.-I!l!‘."'€.;',.7,_,,’
 
Fm. 215. Budding in
Rhabdopleura normanni.
 
(From a diagram by
Korschelt and Heider.)
 
b. buds of different
ranks from a common
stolon (st.).
 
been produced the mass takes on the form of buds united into a very
definite system built upon the plan of concentric circles of buds. As
the system becomes more and more complicated some of the individuals
become crowded out of their proper place and so become the center of
a new irregular subdivision of buds. In this way a colony is formed.
The place of origin of the buds varies in difierent genera, a fact which
318 ASEXUAL REPRODUCTION
 
gives rise to the marked differences in appearance of different colonies
of compound ascidians. Thus we have pyloric budding which is also
called oesophageal, epicardo-oesophageal, and epicardo-rectal budding.
In this type when the blastozooid buds it is really of compound origin,
the new process arising from abdominal and thoracic outgrowths, the
abdominal bud being an invagination of the oesophagus and the thoracic
formed largely from the epicardium. From a diverticulum of the left
portion of the epicardium the nervous system is derived. It is thus
endodermal in origin in the blastozooid, although in the oozooid it is
derived in the regular manner from the ectoderm. Pyloric budding is
described chiefly in the didemnids and the diplosomids. Among the
modifications of the general type of budding described for the compound
ascidians are the cases spoken of as pseudo-stolonial, occurring especially in the distomid Distaplia and in the polyclinids. Authorities differ
in the manner in which they regard the budding of these forms, some
tracing it to the formation of a stolon and others regarding it as more
nearly related to the type already described. In Distaplia the formation
of the “primordial buds” has been described as coming from the epicardium, but Salensky, Julin, Della Valle, and others have described
this as a proliferating stolon from the intestine. The first generation
of these buds never develops sex products but later generations of buds
may reproduce sexually. It may be noted that the epicardium is wrongly
named in that it does not participate in the formation of the pericardium
and the heart, although it was so described by van Beneden and J ulin.
Actually it is the endodermal element of each bud. In the polyclinids
the budding of the posterior part of the animal resembles horizontal
division, for the caudal part of the larva clongates and constricts, forming thorax, abdomen, and post-abdomen; gonads and heart develop in
the latter which subsequently segments to form buds. By some this
entire caudal portion is regarded as a stolon.
 
As an example of stolonial budding reference may be made to Perophora and to Clavellina. In Clavellina, after its attachment, root—like
processes are sent out from the base giving it a more firm hold. At least
one of these processes becomes the proliferating stolon (stolo prolzfer).
The stolon consists of the three germ layers in addition to the cellulose
tunic which covers it. From it arise buds as well as side branches. If a
particular outgrowth contains an endodermal layer it would develop
into a bud. Otherwise it is merely a sterile branch. Buds arise near the
growing tip of the stolon, but simultaneously with their development
the top continues to grow, so those near the base of the stolon are the
more mature. Younger ones sometimes arise as a new generation of
buds between the older ones. Stolonial budding takes place only from
TUNICATA 319
 
the oézooid for the blastozooid can reproduce sexually. It should be
noted in regard to the formation of colonies that although the usual
condition is the production of an entire colony from a single oozooid,
yet small colonies sometimes grow so close together that concrescence
results and they fuse into a larger colony.
 
 
 
     
   
 
ooooo
 
g’
 
   
 
   
 
F16. 216 An adult of Clavellma with a stolen and .i young individual budded ofi from
it (From Korschelt and Hcider, after Secliger )
 
In many respects the most interesting case of asexual reproduction
in the tunicates is the formation of the Salpa chains from a proliferating
stoloii. When investigators first began to study Salpa, solitary individuals were found, and also others which appeared to have a significantly different structure and were connected together like a chain or
even a rosette were also occasionally discovered. At length the relation
between the two was made out by the poet, Chamisso, who discovered
that the solitary individuals can produce the chain salps and that
certain individuals of the chains developed sex organs from which the
320 ASEXUAL REPRODUCTION
 
solitary individuals were again formed. The solitary individual always
reproduces asexually but is itself produced from a fertilized egg. From
the ventral side of the posterior half of such a solitary individual a bud,
which first arose from the pharyngeal endostyle and is therefore in its
beginning eiidodermal, grows out. As it enlarges, the mesoderm and
ectoderm surround it, and finally it becomes a projection from the tunic
as well. It is a direct continuation of the ectoderm and endoderm of the
 
     
 
""-‘Kw;
 
- 41;!!!
 
St Iliasc
 
 
fiG 217. Nearly adult stages of Dolwlum dentwulatum (From Korschclt and H0|d(‘r,
after Neumann.)
 
cl , cloacu, d c , dorsal horn or cadophore to which buds Will be uttuchcd, st , \CIlU‘dl
stolon from whuh buds are produced, t , mil with chorda
 
parent individual and its parts are likewise related to the organs which
develop in its buds derived from it. This is the ventral proliferating
stolen and the individual producing it is the oozooid developed from
the single egg of the gonozooid.
 
The history of the ventral stolon differs somewhat in Salpa and
Doliolum. Perhaps the latter, as described by Uljanin, is the one more
familiar to students. As in the compound ascidians the oozooid produces
no sexual organs but a great many buds arise from it in a complicated
manner and the chain thus produced exhibits a high degree of polyVERTEBRATA 321
 
morphism. Indeed, the oozooid itself degenerates until it becomes
nothing but a locomotor organ of the rest of the chain. The buds are
produced continuously for a considerable time from the ventral stolon.
They do not remain in that part of the body, however, but migrate
dorsally to a posterior dorsal horn, or cadophore, which is an outgrowth
resembling somewhat a stolen but does not of itself bud. Its epithelial
cells become specially suited for the attachment and nourishment of
the migrating buds which will presently reach it. As a matter of fact,
however, there are more buds in the dorsal cadophore than were produced from the ventral stolon, multiplication in the form of a simple
division having taken place during the migration. The cadophore continues its growth and more and more buds are attached to it. They
arrange themselves in two lateral rows and one dorsal median row.
The lateral blastozooids which are attached by a short stalk are nutritive and respiratory. They are apparently unable to reproduce
and are morphologically independent of the rest of the colony. The
median blastozooids are spoken of as nurse individuals, or phorozooids.
They are rounded and have a stalk on the ventral side. It is this stalk
which bears the buds that in their turn are to give rise to the sexual
forms. Like the lateral blastozooids, the nurses are non-reproductive.
The buds which arise from the stalk of the phorozooids are usually
spoken of as protogonozooids. From these the sexual blastozooids, that
is, the gonozooids, are produced. They are free swimming, undergo a
considerable change in their general structure, develop sex organs, and
the cycle is completed, for from the fertilized egg comes the new zooid
ready to begin the asexual cycle again. Thus there are two distinct
asexual generations, the oozooid and the protogonozooid, and some of
the blastozooids have also multiplied by simple division in passing to
the dorsal cadophore. These two asexual generations alternate with the
one sexual generation. The development of all forms of Salpa is not
understood yet and in some cases it is difficult to interpret the forms
that have been found. The life cycle of Doliolum, however, illustrates
satisfactorily the degree to which asexual reproduction is developed in
these forms.
 
Vertebrate. In forms higher than the tunicates asexual reproduction
does not commonly occur. However, the case of the armadillo which is
described in detail in the chapter on polyembryony must be mentioned.
Here a blastocyst is formed as a result of the cleavage of the egg which
produces by budding four individuals. This is, of course, an asexual
method of multiplication, and may be of general significance, as is
suggested by the production of identical twins in various other forms
of mammals.
CHAPTER V
PARTHENOGENESIS
 
I. NORMAL PARTHENOGENESIS
 
A. GENERAL DISCUSSION
 
As an embryological problem the phenomenon of parthenogcnesis has
been of interest since its discovery in 1762 when Bonnet found that the
summer generations of aphids reproduce by means of unfertilized eggs.
The literature dealing with the subject is a vast one, for parthenogencsis
is of wide occurrence in the animal kingdom and is also known among
the plants. In spite of the vast amount of research on the problem,
however, it has only recently become possible to bring the known cases
into any kind of systematic order. The problem also has a great deal 01
cytological and genetical interest for we are here dealing with uniparcntal
inheritance and it is obvious that the chromosomal mechanism which
explains the inheritance of bisexual forms must undergo some modification to account for the appearances in unisexual organisms. While the
cytological and genetieal aspects of parthenogenesis are closely related
to the embryological, we can treat them only briefly and must devote
ourselves chiefly to the embryological problems.
 
Confusion sometimes develops in the mind of the student in relation
to parthenogencsis for at first thought one is apt to class all types of
uniparental inheritance together and think of parthenogcnesis as a
modified asexual type. The fallacy of this conclusion is easily seen,
however, for parthenogenesis deals with the development of an egg
although without the cooperation of a spermatozoon. It is clearly a
gametic form of reproduction; its relationships are perhaps more easily
understood if we speak consistently of unisexual and bisexual reproduction. It would perhaps be still clearer to use the terms monogametic
and digametie, although these are not commonly found in the literature.
The critical point in the evidence that we are here dealing with a second
type of sexual reproduction is seen in the formation of polar bodies and
the behavior of the chromosome during the maturation division. In
some cases of parthenogenesis polar bodies are often seen to be formed
and in other cases the behavior of the chromosomes in reduction is
 
well known. In addition to this evidence, the sporadic occurrence of
322
TERM INOLOGY 323
 
parthenogenesis in diverse classes of the animal kingdom, the occasional
occurrence of parthenogenesis along with the bisexual method in the
same species of animal, as for example the bee, and the not uncommon
alternation of the parthenogenetic mode with typical sexual reproduction in the course of several generations within the same animal all bear
out the same conclusion. Furthermore, the fact of artificial parthenogenesis, that is, the activation of an egg which would otherwise develop
only by fertilization, shows that we are dealing with what must be a
modification of the usual type of bisexual reproduction. Artificial parthenogenesis means the initiation of development on the part of the
egg by chemical or physical stimulation artificially induced to take the
place of the type of initiation usually to be seen only when the sperm
enters the egg. It is really a study in experimental embryology which
has been of the greatest value in giving an insight into the true nature
of the process of fertilization.
 
a. Terminology. Throughout the animal kingdom parthenogenesis
occurs in a wide variety of types and under many different conditions.
Owing to this fact the literature concerning it contains many descriptive
terms that are of special application and about which some confusion of
meaning has grown up, as has been the case in certain other processes
that are familiar but not clearly understood by the majority of students.
In some species parthenogenesis is of rare occurrence and the eggs
simply possess the power of developing without the intervention of the
sperm, although they usually develop after fertilization. Such cases are
known as facultative or optional and are of such irregular occurrence
in the series as to be of no great embryological significance. Obligatory
parthenogenesis occurs regularly in the life cycle of organisms which
show it as a constant feature or only at certain intervals. Its importance
is manifested by the fact that parthenogenetic eggs are often structurally different from those that are to be fertilized and there are morphological differences between the animals which are produced parthenogenetically and those which are produced bisexually. For instance, the
eggs of daphnids which are fertilized usually develop only during the
colder seasons of the year; they are known as winter eggs and have
a protective shell that is very different from the summer eggs. Oftentimes cases of obligatory parthenogenesis show an alternation of
generations although not of an asexual generation with a sexual, but of
a unisexual generation or a series of them, with a bisexual generation.
Where this type of development is firmly established a series of par
thenogenetic generations may be developed to such an extent that it
becomes the predominant method of reproduction and sexual genera3 24 PARTHENOGENESIS
 
tions appear only at infrequent intervals. Many of the more familiar
cases of parthenogenesis are of this type.
 
Even in the extreme obligatory type it is often possible by experimental means to induce the sexual process, for instance, by a change
of the environmental conditions. The rotifer, Hydatina senta, as shown
by Shull and by Whitney, in old culture infusions will continue parthenogenetically for long periods of time, but if a fresh culture fluid is used
bisexual animals soon make their appearance. Conversely, it is possible
by maintaining appropriate conditions to postpone or even entirely to
suppress the sexual process, as in the case of the rose aphid when cultivated through a series of years in a greenhouse.
 
In cases where structural differences are to be observed between the
parthenogenetic and the bisexually developed eggs, a functional difference also is frequently seen in that the eggs of certain individuals are
exclusively male producing, that is arrhenotokous, and of others female
producing, or thelytokous. Where both males and females are produced
in one brood, parthenogenesis is said to be amphoterotokous. Where the
number of parthenogenetic generations which occurs before the sexual
animals are produced is indefinite we say that the species has an “open
life cycle.” Such cases occur in the aphids and in some species of phylloxerans. In others the female which produces the parthenogenetic eggs and
hence is known as the stem mother must develop directly from the
previous fertilized egg. This is the “ closed ” type, and it occurs in certain
other phylloxerans and in the gall flies.
 
Considering the embryological aspects we should classify known
cases according to the grade or degree of parthenogenesis shown. It is
possible to distinguish seven or eight different grades of parthenogenesis
as follows: (a) Pathological. In the ova of birds it is frequently observed
that a few cleavages take place resembling the normal but not leading
to the formation of the blastula. Similar phenomena have been observed
in some other eggs as well. (b) Casual parthenogenesis. In the case of the
silk moths under exceptional conditions aspermic development takes
place. (0) Occasional parthenogenesis. In the ants, bees, and wasps, the
development of the egg without fertilization always produces a male.
(d) Partial parthenogenesis. The queen bee by the copulation on the
nuptial flight receives all of the sperm which she will ever use, and
afterwards she can fertilize the egg to produce a female, that is, a
worker or a queen, or leave it to develop parthenogenetically into a
male, since she has control over the process. (e) Seasonal parthenogenesis.
In the case of Daphnia already mentioned and other Entomostraca and
also the aphids the summer eggs are parthenogenetic and the winter
fertilized. (f) Larval parthenogenesis. The case of Miastor is described
CYTOLOGICAL RELATIONSHIPS 325
 
in the chapter on paedogenesis. Some larvae are produced parthenogenetically and inside of them others through a number of generations.
each eating its way out and producing yet others. finally the last larvae
pupate, undergo metamorphosis, and develop bisexual forms. (g) Total
 
parthenogenesis. Only parthenogenetic eggs occur through many generations as is especially illustrated by the rotifers.
 
b. Cytological Relationships. A consideration of the cases of parthenogenesis upon the basis of their cytological conditions leads to the common
classification of haploid and diploid parthenogenesis. By haploid parthenogenesis is meant the development without fertilization of an egg
which has gone through the process of chromosome reduction. Haploid
eggs in general are sexual, and in most cases in which aspermic development is possible the eggs are found to be capable of development either
with or without fertilization. Hymenoptera, some of the Hemiptera,
and the arachnids often exhibit haploid parthenogenesis. One case, the
nematode Rhabdites (R. aberrans according to Kruger and R. pellio
according to P. Hertwig), is worthy of note, however. Here the eggs
develop parthcnogcnetically and are of the haploid type but the penetration of the sperm is necessary to initiate the development although
it takes no further part and no true fertilization is accomplished. After
it has penetrated the cortex of the egg, and thus set going the developmental processes, the sperm degenerates and the further development
of the egg is as much parthenogenetic as if no sperm had been involved.
 
Diploid parthenogenesis is much more frequent, occurring in most
of the other groups where parthenogenesis is found at all. Copepods,
ostraeods, and the Hemiptera-Homoptera have this type characteristically whereas trematodes, nematodes, echinoderms, the phyllopods,
the Orthoptera, and the Lepidoptera exhibit it in certain forms. An
intermediate condition is found in the rotifers, both diploid and haploid
parthenogenesis having been described for these forms. Triploid parthenogenesis is also known but is not common. The best understood case is
that of the plant genus Hieracium which has been described by Rosenberg. There are two sections of this genus which differ in their cytological
behavior. The sexual form of H. umbulatum has a diploid chromosome
number of 18 whereas the variety linearifolium has a diploid number
of 27. There are also some in which the diploid number is 36. The parthenogenetic Archieracium, which is closely related to this species,
shows a chromosome number of 27. Rosenberg explains these facts
upon the basis of hybridization. The triploid races, Rosenberg maintains, cannot easily beproduced by the usual bisexual processes. Triploid
parthenogenesis, however, is of rare occurrence, and the triploidy in
326 PARTHENOGENESIS
 
animals which result from fertilization of a diploid egg, if that can
occur, certainly produces only an abnormal zygote.
 
Usually the number of polar bodies which is given off by the animal
egg permits, the observer to distinguish whether he is dealing with the
haploid or diploid mode of development; in the haploid case two polar
bodies are produced in the haploid manner, whereas in the diploid a
 
single maturation division produces only one polar body and no reduc-'
 
tion of chromosomes can take place. There is one special case of parthenogenesis to which was early ascribed theoretical significance in working
out a theory of fertilization. O. Hertwig in 1890 described a process in
the maturation of the starfish Astropecten which has been many times
referred to since, namely, the reunion of the nucleus of the second polar
body with that of the egg. A similar condition was reported by Lefevre
for the egg of Thalessema in which the second polar body is not extruded,
the spindle remaining “submerged” in the cytoplasm of the egg. Upon
the basis of these observations parthenogenesis was for a long time supposed to be explained as a kind of fertilization by the polar body. It is
now known, however, that such cases seldom occur. A somewhat analogous case is that of the wasp H abrobracon in which a cytological study
shows parthenogcnetieally produced males to be haploid on account of
the fact that the first spermatocyte division is abortive while the second is
equational (A. Whiting, 1927). Of course cases in which only one maturation division occurs are not rare.
 
c. Parthenogenesis and Sex. Much of the work upon parthenogenesis
has been due to the bearing of the problem upon sex determination.
Many experiments have been made for the purpose of discovering what
factors can influence the production of males or females within the
parthenogenetic strains. Especially have the rotifers been used for
experiments of this kind. Punnett observed various kinds of females as
follows: arrhenotokous females or those which produce males; thelytokous females (female producers) of three kinds, namely, those which
produce, respectively, a large percentage, a small percentage, and those
which produce no arrhenotokous females. In the attempt to influence
the sex of the progeny of these forms conflicting results have been obtained. The studies of rotifers have been most extensively carried on by
Whitney and by Shull. In general Shull’s experiments on the modification of sex have yielded positive results, for he has found a relationship
between metabolism and sex determination. When the quantity of food
given H ydatina senta is small the number of male producers is increased;
old food reduces the number. Creatin, ammonium salts, beef extract,
and low temperature prevent the formation of male producers. Longcontinued parthenogenesis results in a decrease in male production.
INTERSEXES 327
 
Oxygen in the water increases it, although osmotic pressure, alkalinity,
and acidity were not found to be effective. Whether the egg is to develop
into a male or a female producer is decided during the growth period
but not in the early oogonial stages. Sex is determined a generation in
advance.
 
Whitney, on the other hand, has found less evidence that male production is a response to external conditions, although he did find that
crowding in H. senta permitted the development of fewer male producers in direct proportion to the degree of the crowding. He found,
however, that neither oxygen, temperature, nor starvation is a factor.
One of his strains when fed continuously upon a diet of Polytonia produced nearly all females for twenty-five generations, only three per
cent of the daughters being male producing. But a change of diet to
Dunaliella increased the percentage to 57. When they were fed again
upon Polytonia, the percentage fell off. The influence of the food was
found to be upon the grandmother.
 
In addition to the work of Shull and of Whitney, Noyes has reported
a series of experiments on Proales decipiens lasting through 250 generations in which no males appeared although the animals were subjected
to various environmental changes including changes of chemical composition, of temperature, and of feed. More found Brachionus to give
increased arrhenotekous females upon treatment with chemicals such
as ferric chloride (FeCl), whereas constant diet and temperature gave
only thelytokous individuals.
 
Banta has studied the sex production in the parthenogenetic Cladocera,
especially in M oina macrocopa. His studies with Brown upon sex control
showed that experimental crowding brought about male production
along with lowered metabolism in the females. The amount of food was
not found to affect the results but a change in its character did have a
profound effect. Male production was associated with an accumulation
of excretory substances. Aeration with oxygen decreased the production
of males even in crowded cultures. Similarly carbon dioxide, urea, and
ammonium salts as well as other products related to excretion reduced
the number of males.
 
d. Intersexes. Another problem in relation to sex has appeared in
some of the parthenogenetie strains of Cladocera. It is the condition of
intersexes or, as originally described by Banta, sex intergrades. The
intersex condition manifests itself through the secondary sex characteristics in that a typical female has a series of eight secondary sex characters which are identified with her sex, and similarly for a typical male.
The eight characters are as follows: (1) body size, the females are the
larger at maturity; (2) size and position of the eye, the eyes of the
328 PARTHENOG EN ESIS
 
females being smaller and crowding the margin of the head less than
those of the males; (3) outline of the head, the angle of the anteroventral margins of the head being more acute in the male; (4) absence
in the female of the nuchal protuberance; (5) and (6) character of first
antennae, the males having swollen basal portions and two lateral
stylets; and (7) and (8) the outline and armature of the lateral postabdominal margins, these being more concave and not serrated in the
female. The intersex individuals may have the sex organs of either sex
accompanied by from one to several of the secondary sex characters of
the other sex. There are also hermaphroditic forms with various combinations of the male and female secondary characters. It is Banta’s
opinion that these intersex conditions in Cladocera and other parthenogenetically reproducing forms are probably determined by environmental factors.
 
A relation of hermaphroditism to parthenogenesis appears in certain
cases and it has been suggested by Winkler that it is one of transition,
hermaphroditism leading over into parthenogenesis. At least the case
of Rhabdites aberrans as described by Kruger points in that direction.
These animals are free-living nematodes found in moist earth and are
almost exclusively females, two counts showing four males out of 10,000
females and thirty-two males out of 2026 individuals, respectively. But
the females are hermaphroditic and the entrance of sperm into the egg
is necessary for the initiation of development, although it takes no
further part in the process and the cleavage of the egg is as truly parthenogenetie as if no sperm had penetrated into it. In addition to this
relationship, hermaphroditism may be superimposed upon parthenogenesis at least in one family of the Phyllopoda where it appears that
Lepidurus which under favorable conditions reproduces parthenogcnetically “may become hermaphroditic when food is scarce ” (Bcrnard,1896).
 
e. Geographical Races. Another matter of interest is the occurrence
of geographical races which are parthenogcnetic. The phyllopod, Artemia
salina, according to Artom, reproduces differently in different localities.
Races which are exclusively parthenogcnetic occur in Marseilles, at
Capodistria and in certain other Italian localities. Bisexual races occur
in Cagliari in Italy and in Utah; and a third class in which both bisexual
and parthenogcnetic modes occur is found at Odessa in Russia. Vandel
described the conditions in the isopod, Tr2‘chom'scus provisorius, in which
there are two distinct races, one bisexual in the usual sense, and the
other a female-producing parthenogcnetic race. These occupy distinct
regions, the latter occurring in northern Europe, but at some points the
two may co-exist. These two races are looked upon by Vandel as incipient species. Geographical parthenogenesis has also been observed
CAUSES OF PARTHENOGENESIS 329
 
in the moth Solenobia by Seiler. Solenobza triquetrella and S. znfleti occur
in both bisexual and parthenogenetic forms, the latter being permanent
and thelytokous. Of S. triquetrella the parthenogenetic form is widely
distributed in Germany, Austria, and Switzerland, but the bisexual
form has been found in a single locality only. In S. pineti the bisexual
form is common but the parthenogenetic is restricted to a very few
localities. finally Trialeurodes vaporariorum, a white-fly has two races,
according to Schrader, that are unlike in their parthenogenesis, in that
the English race produces females with only three per cent males and
the American parthenogenetic females produce males only.
 
f. Causes of Parthenogenesis. Of the causes of natural parthenogenesis
little is known. It would seem that the developmental mechanism of
the egg is capable of activation in more than one manner. Usually the
entrance of a sperm into the egg sets off the processes which are involved.
This initiatory action is capable of imitation by both chemical and
physical means as in the cases of artificial parthenogenesis. There are
also conditions in which, it would appear, development may go forward
automatically, the participation of the sperm being entirely dispensed
with. In the case of the normal fertilization of any egg there is no reason
for regarding the developmental processes of the egg as brought to a.
standstill before the sperm enters. Rather they are slowed down to a
speed from which they will not recover unless external influences are
operative, usually in the form of the sperm. Perhaps monogametie
development is possible only where the inhibition is less intense, thus
giving automatically normal parthenogenesis. On this hypothesis the
failure to induce the development of sperm, by placing them in suitable
media as has been reported by Locb and others, may mean nothing more
than that the developmental processes in the sperm are reduced to a
still lower speed from which no means thus far tried have been effective
to return them to a functional level.
 
Other suggestions have also been ‘made as to the factors which are
responsible for parthenogenesis. Issakowitsch held that in Cladoeera
the alternation of bisexual and parthenogenetic stages was governed by
changes in the nucleo-cytoplasmic ratio. Papanicolau reached similar
conclusions. Shull, however, investigated the nucleo-cytoplasmic ratios
in the rotifer, H ydatina senta, without finding any correlation between
it and the mode of reproduction. Although it has been claimed that
food, oxygen content, and other similar external factors influence the
sex ratios of parthenogenetically produced animals, there is no good
evidence that these factors are responsible. Banta thought the formation
of an ephippium (winter egg, which develops upon fertilization) to be
330 PARTHENOGENESIS
 
due either to unintentional change in the media, in which parthenogenetic
daphnids had been developing, or to overcrowding.
 
Another suggestion (which is so far merely record of an observation
rather than a cause) relates to the lagging chromosome of the phylloxerans which is observed to accompany parthenogenesis. Peacock and
Harrison working upon lepidopteran crosses reached the conclusion
that parthenogenesis is a result of hybridity and later supported this
conclusion by a study of the data of other crosses including Nabours’
experiments on parthenogencsis in Apotettix. finally Nabours, working
upon Parateltirc, studied genetically two strains one of which was highly
parthenogenetic and the other had never so reproduced. He obtained
genetic evidence that parthcnogenesis is a character which segregates
in a Mendelian manner and believes it due to certain genes. Robertson’s
cytological studies on Nabours’ material fall into line with this hypothesis. The entrance of the sperm is necessary for the second polocyte
division, and when it is lacking the diploid chromosome number is
retained. In this latter case if the specific genes for parthenogenesis are
present development is initiated. It is to be noted that Agar working
upon Daphnia and Whiting upon Habrobracon failed to find genetic
evidence of the cause of parthenogenesis. But Punnett as long ago as
1906 had suggested the probability that the question is concerned with
the zygotic constitution of the egg and thought that it might be a
matter of Mendelian segregation. These different hypotheses show
the need of much further study of this most elusive subject.
 
B. THE OCCURRENCE or NORMAL PARTHENOGENESIS
 
Natural parthenogenesis is of much wider occurrence in the animal
kingdom than is generally recognized, and it is not rare among the
plants. Examples are found in the following groups of animals: rotifers,
nematodes, trematodes, Dinophilus, three orders of Crustacea, myriapods, arachnids, and ten orders of insects. It seems desirable to point
out some of the important studies in each of these groups, although no
attempt can be made toward inclusiveness. For references and a more
nearly complete listing of cases the reader should consult Winkler.
 
a. Rotzfera. Among the rotifers, as already described, typical arrheno—
tokous parthenogenesis occurs in the same groups of animals with
thelytokous parthenogenesis. The studies on Hydatina senta are among
the best known of all studies on the type of reproduction. Three types
of females, as previously indicated, are found here, and by experimental
means it is possible to change the strains from parthenogenetic to
bisexual.
CRUSTACEA 331
 
b. Nematode. For the nematodes the case of Rhabdites aberrans as
described by Kriiger has already been mentioned. The trematodes are
commonly described as giving rise to rediae from cells which are segregated at one end of the body of the sporocyst and become an ovary.
The new rediae arise from these so-called “ova,” which must be thought
to develop parthcnogenetically if the view of their origin is maintained
that these are true eggs. This controversial subject is discussed in other
chapters in this work.
 
c. Annelida. Among the annelids parthenogenesis is suspected in
Dinophilus conklini from the preponderance of females. In the leech
Ilemiclepsis marginata the early finding of parthenogenesis has failed
of confirmation in more recent experiments (Brumpt, 1900).
 
d. Crustacea. Two orders of the Entomostraca exhibit parthenogenesis and include in their number some cases that have been given a
great amount of study, while a third offers a case which is suspected to
be parthenogenetic. Among the Phyllopoda examples may be cited
from both the Branchiopoda and the Cladocera. Of the former, Apus,
Lepidurus, and Artemia are well known. Reference has already been
made to Lepidurus because of its hermaphroditic relationships. Thelytokous parthenogenesis occurs in these forms. Artemia salina likewise
has been mentioned in connection with geographic parthenogenesis.
On this form the most recent studies are those of Artom (1912). Two
polocytes are formed in the development of the egg. Regularly a reduction of chromosomes from 42 to 21 takes place. The parthenogenetic
forms are tetraploid and of a type called somatic. There are therefore
two strains of Artemia, one diploid and bisexual, the other tetraploid
and thelytokous parthcnogenetic. The following explanation has been
upon the basis of the very slight evidence that in the parthenogenetic
strain only one polocyte is formed (Brauer) and that without reduction.
If the egg and polocyte nuclei, both of which retained their somatic
number of 42 chromosomes, should fuse, then an individual with the
tetraploid number would be produced. As yet this explanation must be
looked upon as purely speculative. Numerous others of the true phyllo«
pods, such as Branchipus streptocephalus, have been observed to repro
duce parthenogenetically and still others are suspected because of the
scarcity or absence of males.
 
Of the work on the Cladoeera, which dates from Weismann’s studies
in 1879, the general facts are well known. Bisexual generations are
followed by parthenogenetic which may continue indefinitely. The
various races differ greatly in the number of generations produced within
a year and in the frequency of the bisexual forms. Apparently most if
not all forms are parthenogenetic at some stage of their life cycles, but
332 PARTHENOGENESIS
 
those genera most studied have been Daphnia, Simocephalus, M oina,
Bosmina, Chydorus, Polyphemus, and Leptodora, the first four being
best known. The more recent students of the group include Olofsson
(1918), Woltereck (1909-1911), Langhans (1911), Kuehn (1908),
Chambers‘ (1913), Taylor (1914), Thiebaud (1913), and especially
Banta and his co-workers, whose work is published in a series of papers
beginning in 1914 and is not yet completed. In all forms the males are
rarely seen and in some species are unknown. As already stated much of
the work concerns the control of sex and the intersex conditions in these
 
forms. There is good evidence that sex ratios and intersex conditions are
both subject to environmental influences.
 
In the order Ostracoda, parthenogenesis was discovered in 1880 by
W. Mueller and by Weismann for a number of genera, it having been
shown that virgin females produced eggs that developed into females;
that is, produced a thelytokous race. No reduction division was found
to occur by Woltereck (1898) or by Schleip (1909) for a considerable
number of forms which they studied and parthenogenesis for these
animals is therefore of the diploid or somatic type. In 1914 Wohlgemuth
studied carefully the reproduction of numerous fresh-water ostracods
and thought they fall into two groups, one of a purely bisexual and the
other of a purely parthenogenetic type, although there are transitional
forms between the two. Other investigators of the Ostracoda have been
Menzel (1911), Alm (1916), and Olofsson (1918). Their chief concerns
have been to describe the facts of parthenogenesis, the relation of the
bisexual generation to the parthenogenetic, the duration of each and
the conditions under which they occur. Not much of importance to an
embryological account is gained from these forms, although SchIeip’s
work on the various species of C3/pris offers perhaps the best cytological
description of parthenogenesis in any crustacean form. His observation
of synapsis not followed by reduction is worthy of note. It may be
remarked that some of the studies of ostracods have taken up the
question, raised for many Crustacea, as to the possible impairment of
vigor of a strain due to long-continued parthenogenesis. Here as elsewhere among the members of the class the general consensus of opinion
seems to be that no loss of vigor can be noted.
 
Mention should be made of the possibility of parthenogenesis in the
third order of the Entomostraca, the Rhizocephala. In the genus Sylon
belonging to that suborder Smith reported his complete failure to find
males and so suspected that parthenogenesis is the method of reproduction.
 
In one order of Malacostraca parthenogenesis has been reported,
INSECTA 333
 
namely in the Isopoda. Vandel (1928) has given an account of geographical parthenogenesis, already mentioned in Trichoniscus. Two
races occupying different localities were described, one bisexual, the
other exclusively parthenogenetic. In some places they may exist side
by side, but mating does not occur between the two races. Physiological
factors tend to keep the two races distinct and to increase the divergence
between them. The parthenogenetic race is found to be triploid in its
chromosome relations. The eggs of the parthenogenetic female do not
undergo synapsis.
 
For both of the two Inyriapod groups, the Chilopoda and the Diplopoda,
cases of suspected parthenogenesis are recorded. Of the former Geophilus
and Lomyctes, and of the latter N opoiulus and Polyxenus, have been
studied. All of these include races which either lack males entirely or
in which they are to be found in certain localities only. In addition
observations were long ago made by Sograff (1882) upon Geophilus
proximus of which unmated females laid eggs that began to develop.
 
Among the spiders accounts of parthenogenesis have been reported
for nearly a century and it may still be suspected, but Montgomery in
1903 concluded that it is “very rare among spiders, and it is probable
that most species do not show it at all.” Since Montgomery’s finding, it
does not appear that any work has been done which successfully establishes parthenogenesis in these animals.
 
Among the mites there is no doubt that parthenogenesis occurs, for
Ewing (1914) described the process in the bisexual Tetranychus telarius
and showed that the unfertilized eggs give rise to males exclusively. It
is arrhenotokous parthenogenesis. Among the ticks, the Brazilian form,
Amblyomma agamum, has been shown by Aragas (1912) to multiply by
thelytokous parthenogenesis.
 
It has been conjectured by Hennecke (1911) that the tardigrade.
M acrobiotus macronyx, has an alternation between parthenogenesis and
bisexual generations.
 
0. I nsecta. Parthenogenesis is of very general distribution in the
insects, having been described in the ten orders. The following table,
compiled in part from Winkler, summarizes the occurrence of the
phenomenon. For references to most of these cases the reader is referred
to Winkler, but a few of especial significance are mentioned following
the table.
 
Aptera
 
M achilzls. Heymons, 1-905 ; doubtful but could find no males.
Forbicina. Verhoeff, 1912; all females, so no doubt parthenogenesis occurs.
334 PARTHENOGENESIS
 
Orthoptera
Mantidae
 
Mantis religiosa Przibram, 1909; induced experimental parthenogenesis,
Sphodromantis not natural.
 
Phasmidad
 
Eurycnema. v. Wuelfing, 1899; three generations of parthenogenetic females in Java.
Hanitsch, 1902; two generations of parthenogenetic females.
 
Bacillus. Dominique, 1896-99; two thelytokous generations of parthenogenesis. Males are rare.
Also Stadelmann, v. Bachr, Cameron, Daiber.
 
Dixippus. Pantel and de Sinety, 1908. Parthenogenesis established.
Schmitz, 1906. Four generations of thelytokous partheno
genesis.
 
Hammerschmidt, 1910. five generations of thelytokous parthenogenesis.
 
Jeziorski, 1918. Four generations of thelytokous parthenogenesis.
 
Phasma. Thurau, 1899. Only females.
 
M onandroptera P .
Raphidems }Bordoz, 1913. arthenogenetic.
Leptinia. de Sinety, 1900. Thelytokous parthenogenesis. Pantel and
 
Ucles also found parthenogenesis.
Phyllium. Bordas, 1898. Suspected parthenogenesis.
 
Locustidae
Saga pedo. Claus-Grobben, 1917. Report parthenogenesis.
Gryllidae
M yrmecophila acervorum. Schimmer, 1909, suspected parthenogenesis.
Tettigidae
fig Nabour and colleagues, 1919-1929. Thelytokous parthenogen' . B .
Telmatemx esis est understood cases
 
Coleoptera. Parthenogenesis is of rare occurrence and most of the older accounts are not trustworthy.
 
Tropiphorus carinatus. Calwer, 1916, reported parthenogenesis.
Otiorrhynchus turca. Ssilantjew, 1906
0. ligustici. Wassiliew, 1909 Thelytokous parthenogenesis.
0. cribricollis. Grandi, 1913
Calandra oryzae. Hinds and Turner, 1911, report parthenogenesis common.
Eggs produce both sexes.
 
Strepsiptera
Stylops}Brues, 1903
Xenos Nassonov, 1910
Elenchus. Muir, 1906
 
Parthenogenesis probable due to morphology of
female genitalia.
IN SECTA 335
 
Thysanoptera
 
Most species are bisexual. Many may multiply parthenogenetically. The1ytokous parthenogenesis is established for Parthenothrips, Anaphothrips, Heliothrips, Taeniothrips, and Liothrips; for a number of others it is probable.
Arrhenotokous parthenogenesis is experimentally shown for Antlwthrips verbasci.
 
Corrodentia
Ectopsocus. Ribaga, 1904. Probably parthenogenetic.
 
Hemiptera
 
Aleurodes. Morrill and Back, 1911. Arrhenotokous parthenogenesis.
 
Trialeurodes. Schrader, 1920. English race thelytokous. American race ar
rhenotokous.
 
Aphididae. Many species of Aphis are known to be parthenogenetic and
types vary. In north they reproduce bisexually during colder
seasons but in south may be exclusively parthenogenetic.
 
Other genera include Callipterus, Ceratophis, M acrosiphum, M yzus, Pemphigus, Rhopalosiphum, Schizoneura, Toxoptera; Chermcs, Pincus,Phyllozera.
 
Coccidae. Many genera of scale insects are described as parthenogenetic
although some cases are not known. Included are Aspidiotus,
Ceroplastes, Cryptococcus, Diaspis, Eriopeltis, Lecanium, Lep1.'dosaphes, Orthezia, Parthenolecanium, Pseudococcus, Pulvinaria,
Saissetia.
 
Lepidoptera
All proven cases belong to family Psychidae or are closely related to it.
Acanthopsyche, Pachythelia, Psyche, Sterrhopteryx, Phalacropteryx, Apterona,
Cochlophora, and Lufia are included. The best known is Solerwbia liclwnella.
Hoffmann, 1859.
 
Solenobia triquetrella. Hofimann, 1859-1869. Usually bisexual. Both bisexual
 
and parthenogenetic modes described. Geographical parthenogenesis.
v. Seibold, 1871; Rolph, 1884; Rebel, _1906; Dampf, 1907; Seiler, 1918.
Solenobia pineti
 
Diptera. Parthenogenesis seldom found in this group.
 
Chirmwmus. Godlewski, 1914. Paedogenesis and parthenogenesis intermingled.
Corynoneura. Goetghebeur, 1913. Rarely parthenogenetic.
M etriocnemus. Picado, 1913. Males few in number.
 
Hymenoptera. Six families show parthenogenesis.
 
Tenthredinoidea
The following show thelytokous parthenogenesis:
Albia fasciala ' Allantus pallipes
 
Allantus canadensis Amauronematus puniceus
336 PARTHENOGENESIS
 
Amauronematus semilacteus Phyllotoma aceris
Caliroa limaama Phyllotoma nemorata
Cimbex connata Pontania capreae
Croesus varus Pontania viminalis
Emprfu abdominalis Pristiphora pallipes
Empria pulverata Pristiphora fulvipes
H emichroa alml Pteronidea spiraeae
Hemichroa crocea Pteronidea tibialis
Nematus erichsoni Thrimax mixta
 
Pachynematus obductus
The following are probably thelytokous:
 
Caliroa aethiops Selandria stramineipes
Phyllotoma vagans Strzmglylogaster lineata
Producing both males and females are:
Ametastegia equiseti Pseudoclavellaria amerinae
The following are arrhenotokous:
 
Albia nitens N ematus luteus
 
Allantus cinetus Periclista albida
Allantus viennensis Phymatocera aterrima
Ametastigia glabrata Priophorus padi
 
Arge, all species Pristiphora conjugate
Caliora annulipes Pristophora crassicornis
Cladius Pristiphora geniculata
Croesus brischkei Pristiphora testacea
Croesus litipes Pristiphora alnivom
Croesus septentrionalis Pteronidea, 15 species
Lophyrus, all species Trichiocampus viminalis
Nematus coeruleocarpus Trichiocampus lucorum
 
Cynipoidea.
 
The following genera contain species which are parthenogenetic and in most
cases the males are unknown, so they are probably thelytokousz
 
Andricus ' Cynips Rhodites
 
Aulacidea Drastrophus Dryophania
Ceroptres Phanacis N euroterus
 
Ichneumonoidea
Chalcids
 
The following are arrhenotokous:
 
Ageniaspis Entedon Paracopidoswnopsis
Anaphmldea Litomastix Pentarthron
Copidosoma M elittobia Pteromalws
Encarsia M icrtmzelus Schedius
 
Encyrtus M icroterys Tropidopria
IN SECTA 337
 
The following are thelytokous:
 
Asphclinus Coccophagus Tetrastichus
Aspidiotiphagus Odtetrastichus Tripoctenus
 
The following contain species that produce both sexes or are uncertain as
to sex although parthenogenetic:
 
Eupelmus I sosoma Scutellista
H abrocytus Paniscus Trichogramma
 
Braconids: All parthenogenetic species are described as arrhenotokous.
 
Ichneumonids: All parthenogenetic species produce mixed broods.
 
Proctrotrupids: Anagrus, Gonatopus are thelytokous. Balus, Paranagrus,
Phanurus produce mixed broods, or first females then later
males.
 
Doubtless many more parasitic hymenoptera are parthcnogenetic.
 
Formicoidea
 
Arrhenotokous parthenogenesis is very widespread among the ants. Many
workers are fertile and lay unfertilized eggs from which males develop.
Some hold the view that both males and females may develop from parthenogenetic eggs. A few cases are recorded in which thelytoky is claimed
to be established. Certainly it is much less common than arrhenotoky.
 
Vespoidea
 
Parthenogenetic eggs of queens and workers develop into males only. Examples are Polistes gallicus, v. Seibold, 1871
Vespa germanica, Marchal, 1896
 
Apoidea
For many bees arrhenotokous parthenogenesis is conclusively established.
Haploid males are so produced, and diploid males probably do not occur,
that is, males produced from fertilized eggs, although that possibility has
not yet been excluded. In a few genera both males and females are produced
 
parthenogenetically but this is not usual. Queens and workers are females
produced bisexually.
 
As is to be seen from the preceding table, a great deal of work has
 
been done upon insect parthenogenesis. It has, however, been to a
large extent concerned either with the general life cycle or with the
cytological and genetical aspects of the problem. Many studies of very
fine character have been made upon gametogenesis and sex determination, and upon the factors involved in the control of sex. Of recent
years the problems which are bound up with uniparental inheritance
have attracted much attention. It must be admitted that much of this
work has not advanced our general embryological knowledge of the
insects to any great extent.
 
Among the many investigations may be mentioned a few to which
338 PARTHENOGENESIS
 
the reader is referred if he would pursue further these aspects of the
problem. The work of Nabours and his collaborators upon the various
forms of grouse locut promises much in the cytological analysis since
grasshopper chromosomes are among the most favorable for study. The
saw flies have been studied especially by Doncaster and by Peacock
and Harrison. Of the aphids and phylloxerans a very careful cytological
study was made by Morgan. An earlier study by Tannreuther is a good
account of the general embryology of the aphids. Parthenogenesis in
the moths is most recently made known to us by the studies of Goldschmidt and of Seiler. Of the Hymenoptera the extensive work done by
Patterson on Paracopidosomopsis will serve to introduce the student
to the relation of parthenogenesis and polyembryony, and the best
detailed account of the cytology of the bee is undoubtedly that of
Nachtsheim. Other investigations have already been mentioned in
connection with other aspects of the general parthenogenesis problems.
 
f. Plants. Among plants a considerable number of cases of parthenogenesis are already known and it is thought of interest to mention the
conditions found there in this discussion although the problems involved
are outside the scope of this work. It is difficult without careful study
among the plants to distinguish between cases of parthenogenesis and
those of the simple vegetative apogamy. Among higher plants haploid
parthenogenesis is exceedingly rare, although several cases have been
described for the lower forms. Haploid parthenogenesis is also described
as generative parthenogenesis by Winkler and as true parthenogenesis
by Strasburger. Diploid parthenogenesis is less common among the
lower forms but more so among the vascular plants. It is due to the
failure of the maturation process to occur to completion. The forms
which are known to be parthenogenetic are as follows:
 
Haploid parthenogenesis: Spirogyra, Ernst, 1918; Vaucheria, von
Wettstein, 1920; Ectocarpus, Kylin, 1918; Fucus, Overton, 1912 (probably haploid); Gastrodia, Kusans, 1915; Oenothera, Haberlandt, 1921,
1922; Datura, Blakeslee and Belling, 1922, evidence from breeding
experiments; Nicotiana, Clausen and Mann, 1924.
 
Diploid parthenogenesis: Chara crinita, Ernst, 1918; Athyrium fel2':cfoemina, var. clarissima, Farmer and Digby, 1907; Scolopendrium
vulgare, Farmer and Digby, 1907; Marsilia Drummondii, Strasburger,
1907 ; Allium odomm, Haberlandt, 1923 ; Atamosco texamz, Pace, 1913;
Calycanthus, Schiirhofi, 1923; Alchemilla, Murbeck, 1901, Strasburger,
1905, Boos, 1917; Wikstroemia, Winkler, 1906; Eupatorium glandulosum,
Holmgren, 1919 ; Erigeron annuus, Tahara, 1921; Antennaria alpina,
Juel, 1900; Chondrilla, Rosenberg, 1912; Taraxacum, Juel, 1904, Osswa,
1913, Sears, 1922; Archieracium, Rosenberg, 1917.
ARTIfiCIAL PARTHENOGENESIS 339
 
II. ARTIfiCIAL PARTHENOGENESIS
 
Of great embryological significance is the phenomenon of artificial
or experimental parthenogenesis. It has been the subject of much of the
work on experimental embryology of the present century and its chief
consideration should be a matter for a treatise on experimental embryology. However, its importance for an understanding of matters which
have to do with the normal embryological process is so great that a brief
account should be included here. For details and bibliography the
reader is referred to the extensive accounts which have been published
by Loeb (see his “Artificial Parthenogenesis and Fertilization”) and by
Morgan in his “Experimental Embryology.” Wilson has also critically
considered the cytological aspects of the problems concerned with artificial parthenogenesis in “The Cell.”
 
The student should be reminded of the double function which fertilization serves in normal development; the one is hereditary in character
in that fertilization provides the mechanism for conveying the contribution of the male to the offspring. The other is strictly developmental
in that it sets in motion those processes which have been inhibited or
are latent in the egg at the time of maturation. It is with this second
aspect of fertilization that experimental or artificial parthenogenesis
deals. These experiments have sought to imitate and to interpret the
normal processes of development as initiated by fertilization, and
because of that a much clearer understanding of the normal process has
been reached. The experiments have shown that it is possible to cause
the unfertilized egg of a great many animals to develop into larvae
largely under the influence of chemical treatment, although physical
means have also been used to accomplish the same end less perfectly.
 
The work on parthenogenesis is chiefly a monument to the insight
of Jacques Loeb and his analytical experiments have been of the most
importance in solving the many problems involved. However, numerous
other students have contributed to the progress of the work both before
and since his announcement of the discovery that it was possible to
induce eggs to develop artificially. Among the preliminary studies
which antedated Loeb’s discovery in 1899 may be mentioned the paper
of Loeb himself in 1892 in which he studied the effect of addition of
sodium chloride to the sea water in which the eggs of Arbacia developed;
Richard Hertwig’s observation (1896) on the effect of treating unfertilized sea-urchin eggs with strychnine; a series of experiments by
Morgan (1896, 1899, 1900) on the effect of salt solutions on the segmentation of eggs and the formation of artificial asters; the work of
Mead (1896-98) showing that unfertilized eggs of Chaetopterus will
340 PARTHENOGENESIS
 
form polar bodies in certain solutions in which the amount of sodium
chloride is increased. Loeb’s papers upon this subject are many, and to
him is due the chief credit for the developing of our knowledge of the
subject. Ampng those who early worked upon the problem was Delage,
who in a series of papers from 1900 to 1913 added a great deal to the
understanding of this difficult subject; he succeeded in rearing through
metamorphosis the larvae of both sea-urchins and starfish which had
been induced to develop by artificial parthenogenesis. Loeb and Bancroft (1913) brought a parthenogenetic frog through metamorphosis
and found that its sex glands contained eggs. Shearer and Lloyd (1913)
succeeded even better than Delage in bringing parthenogenetic larvae
of Echinus through metamorphosis, and more recently (1918) Loeb has
brought a considerable number of parthenogenetic tadpoles to the adult
stage. It is to be noted, however, that only in the case of frogs has it
been possible to imitate in the laboratory the conditions of nature sufficiently to bring animals developed by parthenogenesis to sexual
maturity. Since Loeb’s work, Bataillon, R. S. and F. R. Lillie, Goldschmidt, Gray, Harvey, Heilbrunn, Herbst, Herlant, and Just are
among the many who have made extensive studies into the embryological phases of artificial parthenogenesis.
 
VVhen one begins to consider the significance of artificial parthenogenesis he is at once led to inquire as to how general the phenomenon
is or how generally it may be expected to be possible in the animal
kingdom. It may well be that eggs are so constituted as to permit their
development without fertilization, at least into the cleavage stages, and
that we are merely unable to understand the requirements in each case
and to devise the correct procedure. A broad generalization of this character is hardly safe, however, for up to the present time the only forms
in which it has been possible to induce experimental parthenogenesis
are those in which the experiment is relatively easy to perform. In
every case the eggs are of the type which is shed freely into the water.
The difficulties of the experimental work which is involved may be the
reason for this limitation or it may be that a deeper limitation is operative so that eggs which are adapted for other kinds of development
may not be stimulated to cleave artificially. Thus far the following
groups have responded to the treatments that have been devised to
induce parthenogenesis artificially. By far the most work has been
done on the sea-urchins. Arbacia, Strongylocentrotus, T0:copneus'es, and
Paracentrotus have all shown themselves excellently adapted to experiments of this type and they have been used for much important work,
especially the first two mentioned. The sand dollar, Echinarachnius,
has proved adaptable for similar experiments. Among the starfishes
ARTIfiCIAL PARTHENOGENESIS 341
 
the eggs of the commoner species of Asterias as well as some of the
more unusual starfishes, as Asterina gibbosa, have been used successfully. It is to be noted, however, that the methods which have proven
most successful with the sea—urchin give but very poor results with
the starfish, and conversely little success has been obtained by applying
the two best methods of inducement for the development of the starfish
egg, namely, carbon dioxide and mechanical shaking, to eggs of the
sea-urchins. The eggs of the frog, Rana fusca, have often been induced
to develop by parthenogenesis, and the most successful treatment has
been again a mechanical one, namely the simple pricking of the surface
of the egg. Various annelids have been studied, especially Chaetopterus,
Amphitrite, Thalessema, but the best results in this group have unquestionably been gotten for the eggs of Nereis. Here again the means of
inducing parthenogenesis is physical rather than chemical, namely, the
subjecting of the egg to heat.
 
A second question arises in attempting an embryological interpretation of the experiments in artificial parthenogenesis, namely, do these
experiments produce animals that are fairly normal. As already pointed
out Loeb’s own studies led him to the belief that “parthenogenetic
larvae may be normal and apparently healthy,” and indeed, he said,
“if the raising of the larvae was not such a tedious process parthenogenetic animals would exist today in large numbers.” His methods have
certainly produced, both in his own hands and in those of other investigators as well, larvae which resemble the normal in every particular,
and Delage, Shearer, and also Fuchs were able to bring parthenogenetic
larvae to adulthood. The chromosome relations of the individuals as
produced, however, have not been made out with certainty as yet and
it is still doubtful whether haploid larvae produce normal adults.
Parmenter (1925) has shown that in the larval and adult stages Loeb’s
parthenogenetic frogs have the diploid chromosome number. The direct
evidence is entirely lacking as to whether the adults produced from
diploid larvae can themselves produce offspring. It should be said that
most investigators are of the opinion that the parthenogenetic larvae
which are experimentally produced are not merely normal in appearance
but that they really are in every respect what they seem, that is, normal
animals.
 
‘Loeb developed a theory of parthenogenesis as a result of his experiments, and what he spoke of as his improved method is based upon
that theory. According to his View the formation of the egg membrane
is the deciding criterion by which the initiation of development may be
recognized. Indeed he traced a causal relation between the formation
of the egg membrane and the subsequent development of the egg and
342 PARTHENOGENESIS
 
attached much more importance to this process than had previously
been done. Membrane formation is the deciding condition of development. Not all later workers have agreed with Loeb in this view, but
unquestionably his explanations have not been out of harmony with
the facts which he observed.
 
The so-called improved method of Loeb for inducing artificial parthenogenesis consists of two steps. Its details as to concentration and
length of exposure must be worked out for the particular species of
sea—urchin eggs used and indeed different individuals will respond
differently so far as the duration of the exposures are concerned. With
regard to these points the method is entirely an empirical one. The
 
procedure as worked out for Arbacia eggs is as follows: Unfertilized
 
. . . . N .
eggs are placed in a sea water mixture containing 2 cc. of T6 butyric
 
acid to 50 cc. of sea water. Apparently any monobasic fatty acid would
 
serve equally well for this purpose but Loeb found butyric to be satis
N
factory for the experiments (2.8 cc. of I5 butyric were necessary in the
 
case of Strongylocentrotus purpuratus eggs). The duration of the exposure must be brief, from 1% to 3 mintues. The eggs are then transferred to normal sea water and after 10 or 15 minutes to hypertonic
sea water consisting of 8 cc. of 2% M NaC1 to 50 cc. of sea water. At a
temperature of 23° the eggs must remain in this solution from 17% to
25 minutes after which they are transferred to normal sea water. The
effect of this double treatment has been shown many times and in many
different localities. A very large percentage, usually about as great as is
obtained from the development of fertilized eggs, go ahead with the
cleavage process and develop to larvae; doubtless the inability to rear
the larvae is not in any way due to the fact that they were parthenogenetically produced.
 
The explanation of this double procedure has been a matter of some
discussion. Loeb believed that membrane formation sets going certain
chemical reactions upon which the future development of the egg depends. These chemical reactions, however, leave the egg in a condition
from which it will not itself recover, and unless a second factor is employed in the process it will disintegrate rapidly. These reactions are
on the nature of oxidations and are at least to a certain extent cytolytic
in nature. The second factor is therefore necessary as a corrective to
regulate the extensive oxidization which is produced by the exposure
to the first solution. Loeb’s conclusion that cytolysis must take place
unless corrected by the hypotonic solution has been questioned by some
ARTIfiCIAL PARTHENOGENESIS 343
 
later experimenters, notably by Just, who has been able to induce the
development of normal plutei of Arbacia by the use of hypertonic solutions alone. The exact preparations of the salts which are used to render
the sea water hypertonic and the durations of the exposure to this
mixture must be regulated with a great exactness if successful results
are obtained. His optimum solution is made up of 22 parts of 2% M
NaCl or KCI plus 78 parts of sea water, although variations from this
mixture were also used. Of course great care was used to control the
experiment in every way necessary. Eggs subjected to a treatment with
this solution form membranes while still in the solution. Subsequently
the eggs are returned to sea water and their development proceeds.
Upon the basis of these experiments Just holds that the treatment with
the fatty acid is not necessary and therefore that the hypertonic sea
water is not serving as a corrective to stop the cytolysis induced by the
unusual step in Loeb’s procedure. He is disposed to relate the activation
of the sea-urchin eggs by this treatment to the egg secretion, fertilizin,
which is given off by the unfertilized eggs into the sea water and which
has been shown to be a necessary intermediary to normal fertilization
with sperm. Just suggests that the activating agent which will accomplish experimental parthenogenesis serves to bind the fertilizin produced
by the egg and thus to complete the necessary cortical changes whic}
 
must take place if development is to proceed. The full explanation or
the artificially induced changes has perhaps not yet been offered with
regard to the experimental facts. However, there is no question that the
 
entire subject has been one of the most successfully studied of all problems of experimental embryology.
CHAPTER VI
PAEDOGENESIS AND NEOTENY
 
A series of conditions is known that have to do with the early sexual
maturity and reproduction of certain animal forms which otherwise
retain their youthful characteristics. These are to be taken up under
the general heads of paedogenesis and neoteny although not all the
cases included come under a strict definition of either of these terms.
They occur in a great many widely scattered groups of the animal
kingdom and present a great many variations some of them so wide
that they are scarcely to be recognized as of related processes. When
such diverse conditions appear, it goes without saying that confusion
is to be found in the literature dealing with them. Regarding the processes
under consideration in this chapter exactly such confusion is found,
some writers using the terms loosely and failing to classify with sharpness the cases cited.
 
The biogenetic law comes into the discussion for the reason that one
may regard a particular phenomenon as recapitulating past phylogenetic
conditions, or he may look upon the animal showing it as exhibiting
neoteny, at least of the characters in question, and perhaps generally. Thus the familiar axolotl which is the sexually mature, unmetamorphosed Amblystoma is the usual example of neotenous development,
but it is also cited by the proponents of recapitulation as explained by
the general progress in development of the Proteus, Necturus, Amblystoma, Salamandra series of urodele recapitulation. Most of the cases
of this kind, however, are concerned with adult conditions quite as
much as with those of immature forms and therefore would seem to be
rather outside the scope of the present discussion.
 
The general subject of neoteny also calls up the problems of heterochrony, by which is meant a disturbance of the synchrony of development. That is, if one might take the normal series of developmental
time stages with each organ in its proper relation to the others as a
standard, representing perhaps the phylogenetic series, then any departure from this standard would be spoken of as heterochrony. (See
also Chapter III, Part Two, for discussion of heterochrony.) Similarly,
the sequence of embryonic events when disturbed, as in neotenous
development, involves heterochrony. The principle is one with an
 
344
PAEDOGENESIS AND NEOTENY 345
 
interesting history, recalling especially the work of two investigators,
Oppel and Keibel, although many others have contributed to it, some
independently and others in collaboration with Keibel in the publication
of his famous “Normentafeln zur Entwickelungsgeschichte der Wirbeltiere.” Oppel began this study comparing the different developmental
stages of different animals and arranging them in tabular form to show
the comparative progress of the most important organs of vertebrates.
He thought himself to have found similar ontogenetic stages and to be
able to compare the young stages among themselves as well as the
adults among themselves. The recapitulation doctrine found support
in his Work in that the young stages of higher forms are similar to the
older stages of the lower animals. Departures from the series thus
established were to be attributed to heterochrony. Keibel as a result
of his studies and tables concluded that the time of the appearance of
an organ is dependent upon the time at which it will be required to
function. Thus the order of appearance of organs in a developmental
series is of itself of phylogenetic significance. But Keibel did not recognize the biogenetic law as valid in these cases.
 
Another early student of heterochrony in vertebrates was Mehnert,
who devoted his attention particularly to the relation of the subject to
recapitulation. His view on this matter is of interest, for he thought
that only the early development of an organ had recapitulatory value in
any precise fashion, whereas in later stages the processes are quite
schematic. He studied also organs which undergo regression as well as
those whose development is only progressive. Heterochrony he found
to be due (1) to precocious development of an anlage, (2) to rapidity
of growth, (3) to rapidity of histological differentiation, and (4) to
abbreviation or omission of intermediate stages. Retardation of these
processes as well as their acceleration call forth heterochrony.
 
Heterochrony is thus seen to deal with parts of organisms rather
than the animal as a whole and to-show the effects of disturbances of
developmental rate and rhythm upon the entire animal only through
its effect on its component organs. At first thought paedogenesis might
be considered as but very indirectly concerned with a matter such as
this, but a reconsideration of the facts easily brings out a very clear
relation, for we find paedogenesis to mean merely that, in an animal
exhibiting this phenomenon, the organs of the body which have to do
with reproduction have been much accelerated in development, while
at least some other parts of the body have failed to keep up the pace
set by these organs; or in some cases we must think that the reproductive
organs and related parts have retained their customary pace while the
others have been very considerably inhibited.
346 PAEDOGENESIS AND NEOTENY
 
During the present century many investigators have contributed to
the knowledge.of the general subject. It will perhaps serve as an illustration to point out the importance of Stockard’s very extensive study
on the development of Fundulus, particularly with regard to the effect
of changes in the rate and to the various means by which abnormalities
may be produced, notably by temporary arrests of development.
 
It is thus clear that the matters which are the subject of this chapter
really constitute but special cases of heterochrony. In assigning to these
phenomena as a causal factor the disturbance of the speed of development, we bring them all into one category. It is sometimes difficult to
decide whether one organ has undergone a retardation of development
or whether another is accelerated with respect to the normal and so it
has not always proven easy to separate sharply the processes which are
involved. By some, especially Giard, Chun, Kollmann, and others, fine
distinctions have been drawn, the need for which is not entirely clear if
we but relate the different processes to heterochrony.
 
By paedogenesis is meant sexual reproductive maturity in a pre-adult
stage; it is of two types, parthenogenetic and bisexual. As a special form
of paedogenesis, Packard has given the term “chrysallogenesis” to a
case in which the pupa of Chironomus has been found to lay eggs.
 
By progenesis is meant the permanent retention on the part of the
somatic structures of the conditions reached at the time when sexual
maturity is attained.
 
Neotenous organs have youthful characters although the animal
possessing them has developed its adult condition. Or, to put it in
another way, animals with neotenous organs retain the ancestral larval
conditions in the particular structures which show neoteny.
 
Disogeny is the “sexual maturity of one and the same individual in
two different conditions, between which a metamorphosis with retrogression of the sex products occurs” (Chun).
 
It is true that these definitions savor of dogmatism and of course
require much elaboration. It would seem, however, that neoteny and
progenesis are not far apart and that paedogenetic animals may easily
exhibit disogeny. It will perhaps be best for the purposes of our present
discussion if we limit ourselves fairly sharply to the cases which illustrate
neoteny and paedogenesis. Of these there are certain classical ones which
should receive especial attention. There are only a few of these cases in
which the animals as a whole are spoken of as paedogenic or neotenous,
but when we come to consider the organs to which the latter conception
in particular may be applied, the illustrations abound and important
explanations of obscure phenomena have been worked out on this basis.
 
Of all the cases undoubtedly the axolotl is the best known. As already
PAEDOGENESIS AND NEOTENY 347
 
stated, Amblystoma tigrinum occurs in two forms, the one of which is
technically immature, although it is sexually active. This paedogenic
form was first described from the lakes about Mexico City and was
thought to belong to the genus Siredon (S. lichenoides). The relation of
this form to the well-known salamander was only discovered accidentally
in Paris in 1865. Sexual maturity is reached at six months of age and
sex products are shed. This is paedogenesis, for the animals have not
yet lived long enough for metamorphosis.
 
However, metamorphosis may never occur. In many high mountain
lakes axolotls live their entire life without undergoing the necessary
 
 
Fro. 218. External views of an axolotl (A) and an Amblystoma showing difierences of
gills. body form. and leg development.
 
changes to transform them into Amblystoma. The reason for this is not
clear. If the animal be fed on thyroid, if it be forced gradually to leave
the water and adopt a land life, if it be transferred from deep to shallow
water, from cold to warm, or if it be brought into the presence of certain
chemicals it will undergo metamorphosis promptly, but the causal
mechanism is not yet understood. If it remains in the same environment
as that in which it became paedogenetically mature, however, it will
live its entire life without metamorphosis. This is neoteny, for the
larval characters are retained long after the normal time.
 
The neotenous animal differs in a number of important characters
from the type form. It has large external, red gills with gill slits, its tail
is long and broad but flattened laterally so that it is adapted for swimming, and the body features are those of a water-living animal. Internal
conditions likewise show immaturity, the skull bones, for example,
never becoming properly developed. With metamorphosis the animal
348 PAEDOGENESIS AND NEOTENY
 
undergoes a very extensive transformation. It loses its gills, its legs
develop for crawling upon land, and the tail becomes rounded and
tapering. It is now a land salamander resorting to the water only for
egg laying.
 
The neotexiy of axolotl is thus facultative, for with the proper conditions the animal does not remain neotenous but becomes an adult
Amblystoma. Other urodeles, the perennibranchiates, correspond in
their adult structure very nearly to axolotl and may be looked upon as
permanently neotenous. Typhlomolge, of the underground streams of
Europe and Texas, Proteus, Necturus, and Siren, belong to this group.
 
Another illustration from the chordates is the tunicate group called
Appendicularia or Larvacea. These animals are small tadpole-like
creatures averaging about half a centimeter in length and living perhaps
one year. They swim in the surface waters of the sea of all parts of the
world and the young have been taken in plankton between February
and summer, but their development is almost unknown. There is no
evidence of reproduction by budding, gemmation, or other modes of
asexual type such as are found in the Salpidae, for example, nor is any
metamorphosis known. Development is direct and the small appendicularia correspond in a general way to the tailed larvae of the ascidians;
that is, they retain the tail portion of the body with its typical chordate
characteristics which is lost in the metamorphosis of the more familiar
forms such as Molgula, Ciona, Cynthia, etc. Hence the group has been
named Larvacea and the animals have been looked upon as larval
forms which have become sexually mature. They have also been looked
upon by some as primitive forms from which other Tunicata have been
derived, and, it must be noted, by some they have been thought of as
larvae of some adult form which is pelagic. In any case the sex glands
are developed and the products shed by the animals as known to us,
and we have a clear case of neoteny.
 
Among the insects a number of cases are known, and some of these
are among the most important of all for they illustrate parthenogenetic
paedogenesis. The example usually given is M iastor, a cecidomyiid fly,
but certain species of the genus Cecidomyia also show it. The case of
M iastor has long been known as an illustration of paedogenesis, and is
given by Hertwig along with certain other Diptera as an example
proving his statement that paedogencsis is parthenogenesis in an
immature organism. As is already seen, this statement is much too restricted, for the term paedogenesis is of equal application to cases in
which inheritance is biparental.
 
In Miastor paedogenesis occurs normally during the spring, early
summer, and autumn, according to Hegner who has been the principal
PAEDOGENESIS AND NEOTEN Y 349
 
student of this genus in America. No reproduction takes place during
the winter, and the process is interrupted in midsummer by the appearance of male and female adults. The larva of Miastor possesses two
ovaries in the tenth and eleventh segments. In each are thirty-two
 
oocytes each with nurse cells and follicular epithelium. After a time
one of these oocytes with its nurse cells and its follicular epithelium is
separated off from the rest of the ovary and in a distant part of the
body grows and develops at the expense of the tissues of the mother
larva. This process is repeated until five to seventeen separated growing
oocytes are thus produced from one mother larva. Then one division
takes place, the polar body which is given off divides again and both
products degenerate. Parthenogenetic cleavage follows with chromatin
diminution as previously described in connection with the history of
the germ cells, the pole plasm is segregated and the embryo gradually
takes on its characteristic form. No oviducts are present in the mother
larva nor is there provision for the escape of the young thus paedogenetically produced. They escape by rupturing the body wall of the mother
larva, which is left to die. After the production of a number of generations in this manner, the last larvae pupate and emerge as normal adult
males and females.
 
In the spring of 1869 Grimm found a pupa of Chironomus laying
eggs. To this form of paedogenesis in the chrysalis Packard gave the
name chrysallogenesis, although the differences from other types of
paedogenesis are so slight as to make the retention of the term of doubtful necessity. In the autumn other pupa change to flies without laying
eggs and these adults are more prolific than the spring pupae were.
The process was described as a seasonal phenomenon depending upon
temperature.
 
Pacdogenetic reproduction has also been reported for the Tenthredinidae, the saw flies, thus extending this phenomenon to a second order
of the insects, the Hymenoptera. '
 
The molluscs show one case of neoteny in the shell-less snail, Stamedorsia verrucosa, which according to Cuénot reproduces long before true
adulthood is reached.
 
Among the trematodes paedogenesis is found in the most striking
form. Two excellent illustrations occur in the suborder Monogena, and
conditions in the Digenea offer material for interesting speculation. In
the former group the genus Gyrodactylus exhibits what is perhaps the
nearest approach to the old preformationist theory of “emboitement”
to be found in the animal kingdom. The young individual comes to
sexual maturity before it is born and produces young in its own uterus.
350 PAEDOGENESIS AND NEOTENY
 
This process is repeated and as many as four generations have been seen,
one within the other.
 
The second case of this group is that of Polystoma integerrimum originally described by Zeller in 1872. The embryo hatches in the water
and swims Freely. It seeks for a young frog tadpole which it must find
within twenty-four hours or die. If one is found it creeps over the surface
until it finds the branchial opening, which it quickly enters; it undergoes
metamorphosis, and passes down the alimentary canal to the rectum
and thence to the urinary bladder. Here it remains for three years to
become sexually mature. However, it may happen that the young worm
has attacked a very young tadpole which still has external gills. In this
case it remains in the gill chamber where nutriment is abundant, grows
rapidly, and becomes sexually mature in the short space of five weeks.
It does not then pass further along the alimentary tract but dies before
the metamorphosis of its host. It differs in its structure as well as its
life cycle from the usual form, in that it develops but one male gland
instead of several, and it lacks entirely the intromittent organ, vagina,
and uterus, or they are developed only to rudimentary vestiges. It is
of interest to note that Polystoma ocellatum is structurally quite similar
to the paedogenetic P. integerrimum.
 
Among the digenetic trematodes the life cycle of the liver-flukes involves questions which are of interest in this connection. The main facts
are well known and are referred to in several chapters of this work. In
both rediae and cercariae reproduction may take place and daughter
rediae, and daughter cercariae may be produced. If it can be shown
that these daughter forms are produced from eggs, either parthenogenetically or bisexually, then this is a case of paedogenesis. However,
it has lately been shown for some flukes that the germ balls from which
the daughter larvae develop are budded off asexually and never undergo
any chromosome reduction (F. G. Brooks), so that for these forms at
least it cannot be said that paedogenesis occurs in the flukes. It has been
the usual view, however, that there is here the production of parthenogenetic ova, and hence paedogenesis.
 
Of the examples usually recognized, the final one is that of the lobate
ctenophore, Bolina hydatina. Here the cydippid larvae become sexually
mature, producing eggs and sperm. Fertilization follows and the eggs
develop in the regular manner. The larval gonads subsequently degenerate, metamorphosis takes place, a new set of gonads appear, the
animals again attain sexual maturity, producing eggs and sperm, this
time as adults.
 
These are the classical cases, and they illustrate both neoteny and
paedogenesis, both parthenogenetic and bisexual.
PAEDOGENESIS AND NEOT ENY 351
 
In addition to these, experimentally produced delay or acceleration
of development are well known. Frogs transferred as larvae to alpine
heights where the winters come early have remained in the larval condition over the winter. High temperatures hasten sexual maturity.
Brackish water or fresh water will often hasten the maturity of oceanic
forms. Hunger in some forms and overfeeding in others result in heterochronic growth. Termites which are fed in a certain manner mature
very early while the wings are still undeveloped and eyes have not yet
appeared (Grassi). Parasitism may be looked upon as a strong factor
accelerating maturity because of the abundant food supply.
 
It may be observed that there have been omitted many cases of
larval budding and other forms of asexual reproduction such as may be
so commonly found, for example, among jellyfishcs, liver—flukes, bryozoa,
and tunicates. These cases, though not a far step from the types discussed in this chapter, are not properly considered here, for paedogenesis
and neoteny are matters of sexual reproduction. It is admitted that in
some cases, as already shown for the 1iver—flukes, the distinctions are
hard to draw, but for the sake of clarity it is usually thought wiser to
adhere to the definitions given.
 
Thus far we have discussed this subject from the point of view of
the entire organism. There still remains the matter of neotenous organs
rather than organisms which deserves mention before the subject is
closed. This phase of the subject was developed by Garstang and by
Bolk and recently discussed by De Beer. There are many instances in
the animal kingdom of forms having organs that retain embryonic
characters although the organism as awhole has passed on to a new adult
condition. Organs of this kind are neotenous. In the succession of
somatic stages the organs in question have fallen behind the others, in
short they have become distinctly heterochronic. Bolk has discussed
the features of man which resemble the structure of embryos of anthropoid apes, assuming that the latter‘are nearer the ancestral forms of
structure. Among the features of man which show resemblance to the
embryonic structures of the ancestral types, for which he uses the term
foetalization, are the relatively high weight of the brain, the retention
of the embryonic cranial flexure with the resulting erect posture as Bolk
thinks to have demonstrated, the position of the foramen magnum, the
late closure of the skull sutures, the flatness of the face, lack of hair on
the body, and others. Bolk’s study of cranial flexure and human posture
comparing both adult and ancestral conditions is particularly interesting. He finds as a result that the flat face as compared with the elongated
muzzle of other mammals is largely responsible for the trend of human
evolution with regard to vision and other special senses, the character
352 PAEDOGENFSIS AND NEOTENY
 
of the teeth and of the anterior end of the alimentary canal. And all
the characteristics which are distinctly human are clearly neotenous
and related to the embryological derivatives from the ancestors.
 
One other illustration, from those given by De Beer, may be cited to
show the part that neoteny may have played in evolution. It is a comparison between the important structural characteristics of adult insects
and larval myriapods. The larva of Iulus has a head composed of six or
seven segments, an elongated segmented body, the first three metameres
of which bear pairs of legs whereas posterior segments bear only rudimentary legs at the time of hatching or shortly thereafter (Metchnikoff).
These features are quite insect like, in that the insect head has six or
seven segments, the thorax three, each bearing a pair of legs, and the
abdomen of about ten segments, legless or bearing appendages only as
a larva. Insects are known among the lower orders whose structure
corresponds more closely with this immature myriapod than does the
structure of insects of the very specialized higher orders, and it is sug—
gested by students of these matters that the ‘insect derivation passes
through these intermediate forms from neotenous larvae at least not
unlike those of the myriapods.
 
From these cases it would appear that the study of neoteny from the
standpoint of embryology offers a productive field of quite a new order
for investigations and that the conclusions reached from researches of
this kind may profoundly affect our ideas of phylogeny.
CHAPTER VII
POLYEMBRYONY
 
By polyembryony is meant among zoologists the production of
multiple embryos from a single egg. (This definition does not apply to
botanical nomenclature.) The number of individuals produced from a
single egg ranges from hundreds as in the parasitic Hymenoptera down
to two, although in the latter case the condition is usually known as
twinning, and not all types of twins are properly thought of as polyembryonic.- Polyembryony occurs very widely distributed through the
animal kingdom in groups which are totally unrelated to each other.
Because of this wide distribution the literature to which reference can
be made in this connection is really very extensive and the significance
of some of the cases extends beyond the realm of embryology. Of the
numerous investigators who have studied the question only a few need
be mentioned here, but it may be noted that a reference to their work
will serve as an introduction to the much broader literature which is
not included in this discussion. Patterson has summarized the knowledge
of polyembryony in a paper in Volume II of the Quarterly Review of
Biology and it is suggested that the student consult this paper in beginning a more extensive study of these problems.
 
Patterson recognized three types of polyembryony: “ (1) experimental
polyembryony, or the production of multiple embryos by artificial
means; (2) accidental or sporadic polyembryony, or the occasional production of multiple embryos in the species which is typically monembryonic; (3) specific polyembryony, or the habitual production of
multiple embryos in a given species.” The general student of comparative embryology is interested in the last type much more than in
the first two, although cases of the first two throw much light upon
many fundamental problems of organization of the egg and embryo
and offer a very stimulating field for the experimental embryologist.
Many types of eggs whose normal development includes no hint of
polyembryony can be induced to produce double monsters and even
complete embryos by experimental means.
 
Cases of occasional or sporadic polyembryony are recorded for coelenterates, cestodes, annelids, echinoderms, arthropods, and vertebrates. Perhaps because the latter group is so much more studied, there
 
353
354 POLYEM BRYONY
 
have been more cases reported for the vertebrates than for the others
and, as Patterson points out, it is here that the occasional identical
twins of the human species should be classified.
 
Specific polyembryony, to which our attention is drawn as the
special problem of the comparative embryologist, is found in the following groups of animals: flatworms, bryozoa belonging to the Cyclostomata, earthworms, parasitic Hymenoptera, and the mammals, especially
as illustrated by the armadillo. It is of more widespread distribution,
however, than is indicated by these groups, but here are included the
more important cases.
 
An inspection of this list is sufficient to show that polyembryony has
no phylogenetic or taxonomic significance, for the groups are too widely
separated and too diverse in structure to admit of an interpretation of
this kind. Moreover, the structural differences both of adults and
embryos in these various groups are so great that it is not possible to
look for the causes of the phenomena in any simple embryological
process common to all. Doubtless in the final analysis all these processes
have a common underlying causal factor which is bound up with the
innate protoplasmic organization of the egg substance.
 
As Patterson has pointed out, it is really not much more strange for
an egg to give rise to two embryos than to one. The remarkable fact is
that a new organism can be produced from an egg at all, and those
qualities of the living substance which make possible its reproduction
are basic to the one case no more than to the other. We must recognize
that specific polyembryony is as much a characteristic of certain animals
as is the formation of a coelome. At a certain stage in development there
occurs a series of events which lead perhaps to two buds, or more, from
each of which individuals grow. Very little thought is necessary to
convince oneself that the directive forces behind this type of budding
are not much more astonishing than those which cause, in the other
case, the archenteron to bud out to form an enterocoele.
 
A. THE Causns or POLYEMBRYONY
 
Of the explanations of polyembryony, probably the most prevalent
is the theory of blastotomy, according to which the blastomeres of the
cleaving egg become separated in the 2-, 4-, 8-cell stage or later, and
lead entirely independent existences, each arriving at length at the
stage of a completely formed embryo. This theory is the basis of the
familiar explanation of the origin of identical twins in human beings,
that the blastomeres in the 2-cell stage become separated and each
gives rise to an embryo. This is a view with few observational data to
support it, but it may be presumed to find considerable support in the
THE CAUSES OF POLYEMBRYONY 355
 
experimentally induced development of isolated blastomeres. Numerous
experimental devices are well known by which blastomeres can be
separated. To mention only two of these devices as examples, it is
possible more or less successfully to cut apart the blastomeres with a
knife or delicate thread drawn about the egg, or to keep them apart by
subjecting the eggs to calcium—free sea water in which the blastomeres
do not cohere to one another. In some of these experiments the isolated
blastomeres have lived and developed for a time; in others they have
produced partial larvae (ascidians etc.); and in others they have developed into whole larvae (amphioxus, Cerebratulus). But in forms
where direct evidence for blastotomy is possible none has been found
which forces one to this view for cases of polyembryony. As will be
seen presently, the facts in the armadillo make the explanation based
on blastotomy untenable there, and render it highly doubtful elsewhere.
 
A second explanation takes the form of an assumption that polyovular
follicles, that is, follicles containing several ova fused together, may
provide the mechanism by which polyembryony is accomplished. It is
only necessary to say that the evidence for this supposition is entirely
insufficient and the theory may now be regarded as abandoned.
 
In the budding theory we have what is perhaps a closer correspondence
with the observed facts, although it is more of a descriptive explanation
than an attempt at developmental analysis. After cleavage there arise
in the blastulae or gastrulae of lower animals or in the blastocyst of
mammals certain areas or “growing points” which are essentially buds.
If a single one is produced it becomes the apical or head end of a normal
embryo and assumes dominance over the remaining parts. If two are
formed they are the beginnings of twin embryos. Similarly secondary
buds may be formed and four or more embryos result, depending upon
the number of buds. The facts observed in the armadillo will be seen to
harmonize well with this explanation.
 
This ‘theory of budding has been criticized rather severely, particularly by Assheton, on the grounds that budding cannot take place unless
there is a stock from which the buds may arise and the presence of a
stock Assheton claims was not demonstrated in the cases to which the
theory was applied. Rather he interprets the described facts as cases of
fission. The blastocyst of several mammals, for he was particularly considering the theory as applied to the armadillo, he described as undergoing direct fission into two embryonic rudiments. As a matter of fact
the fission hypothesis does not differ from the idea of budding in relation
to the facts as described, but is primarily a redefinition of them, for in
both cases the embryonic vesicle is regarded as divided into several
primordia, each of which is the beginning of a distinct formative area
356 POLYEM BRYONY
 
and consequently will give rise to a separate embryo. Whether the
emphasis is placed upon the embryonic mass which is thought to bud
or upon the separate areas which arise from it as would be the case
in fission does not seem to involve any particular difference in the result
nor to carry the explanation of the environmental processes much
further toward a final analysis.
 
As an explanation of the process a physiological interpretation must
be called on. Stockard has pointed out that if a developmental pause
occurs at the critical moment in the formative stages of an embryo, a
series of consequences ranging from simple malformation up to the production of double monsters or even two individuals may result. He
applies this conception to the explanation of polyembryony, supposing
that the reason for the loss of dominance of the first formative region
of the embryo and the subsequent ascendency of the primary and
secondary buds is connected in some way with the developmental pause.
He points out that in the armadillo a period of physiological isolation
intervenes at one of the critical moments, making possible the four
resultant buds. Certain observed facts bear out this conclusion. In any
case within the growing germ the isolation of formative areas occurs
and from these formative areas the multiple embryos are produced.
 
An obvious connection exists between the phenomenon of polyembryony and that of metagenesis which involves at least the alternation
of one sexually produced generation with an asexually produced one. It
is usually the practice to limit alternation of generations to the lower
forms of animal life and to say that it does not occur in higher forms,
including the vertebrates. Stockard, however, speaking in terms of the
budding hypothesis, has pointed out the fact that the embryonic mass
of cells may be looked upon as one generation, namely the one produced
from the fertilized egg, and that it is completed when it becomes a
stock from which other buds, that is growing points, begin their development. This point of view has its application even to mammals
whether only a single organism results or several as in the case of the
armadillo. Here the blastocyst would be regarded as the sexually produced individual and the buds which give rise to the four young as
those asexually produced from it.
 
Stockard says, “From a general biological standpoint the adult body
of higher animals may be very correctly considered to be derived from
a sexually produced embryonic axis, the stock which gives rise by an
asexual method of budding to the various special organs. The vertebrate
body is thus composed of a group of different zooids, the organs. There
are seeing, hearing, excretory zooids, and so on, comparable to the
zooids of a siphonophore colony.
OBSERVED CASES OF POLYEMBRYONY 357
 
“Alternation of generations is here considered a phenomenon, not
limited as is generally taught to lower forms, but occurring throughout
the animal kingdom.”
 
If the blastocyst is to be looked upon as a sexually produced individual from which arises asexually another or several others of a
second generation, it is suggested that in this fact lies the explanation
 
fiG. 219. The development of the ovicell in Crista remosa. (From Patteron, after
Harmer.)
 
A, external view. B, median longitudinal section of young ovicell. fol., follicle formed
from polypide-bud; ov., ovary; ovi., oviccll.
 
of the difliculties that have met every attempt to homologize the early
development of the mammals with that of the lower vertebrate classes.
These differences have been discussed in Chapter X on the formation
of the mammalian embryo; they constitute a problem of major importance to the comparative embryologist.
 
B. Onsnnvnn CASES or POLYEMBRYONY
 
We may now devote ourselves to the consideration of the groups of
organisms in which specific polyembryony has already been noted to
358 POLYEM BRYON Y
 
occur, bearing in mind the different types of explanations that have
been offered and attempting to discover how the facts conform to the
suggested explanations.
 
flatworms. Among the flatworms are many cases which depart from
the usual methods of reproduction. Of these some which do not fully
fit into the classification have been described
from time to time as polyembryony. There
is one flatworm in which polyembryony undoubtedly occurs, however; it is the cestode
Taema echmococcus, or Echmococcus coenurus
as it is sometimes known. This small tapeworm produces eggs which develop into
the usual hooked embryo, the onchosphere,
and these in their turn produce a cyst which
becomes the bladder worm or cysticercus.
As is usual in the further development
of a cysticcrcus, an invagination from the
outside wall of the bladder into its cavity
develops a new scolex and neck region
which will later become inverted and form
the new tapeworm. However, the matter
is complicated in this case in that many
scolices may be produced within a single
bladder by the budding process, and even
secondary bladders which produce multiple
scolices in their turn are described. Thus
the encysted worm may grow to an enormous size to endanger the life of the host and
oftentimes bring about its death.
 
Bryozoa. Polyembryony occurs in the
cyclostomatous bryozoa belonging to the
Gymnolaemata of the Endoprocta. These
animals live in colonies made up of zooecia
 
fiG 220- Section through which are in general tubular with densely
 
a follicle of Cnaza remosa show- - mg primary embryo (1) which calcareous walls. The circular orifices of the
 
§>ré>dt:)c1I(IiL(zisecorZ<I‘i‘ary erlgnbgnis zooecia give the group their name. At the time
son, Xftei’ H$fi;e,_,r°m 3 e ' of the breeding season a curious specialized
zooecium develops which is called the oecium
 
or ovicell. In this is developed the young embryo. Fertilization of a
rather unusual sort having been successful, the oecium serves as a brood
chamber about the developing embryos and larvae. The primary embryo
undergoes a process of budding, and secondary and tertiary buds are
EARTHWORM 359
 
produced all of which may develop into larvae, as many as 150 being
on record from a single egg. They develop into ciliated larvae and each
is capable of forming a new colony upon escape from the oecium.
Earthworm. In the earthworm of the species Lumbricus trapczoides
(Helodrilus caliginosus trapezoides) polyembryony results in the production of twins, a process which by Kleinenberg was regarded as
universal for the species, but by Vejdovsky was held to be abnormal.
It is due to a process of fission of the embryo. The cleavage of the egg
 
 
C D
 
fiG. 221. Twinning in the earthworm, Lumbncus trapezoides. (From Patterson, A, B, C.
after Kleinenberg.)
 
A, Section of young twin embryos. the right one being the more developed. B, Double
embryo, in section. C, Double embryo about to break apart. D, Type of double monster
formed when embryos fail to separate.
 
is much modified from the typical spiral form of the annelids and indeed
is variable. A blastula is formed, the endoderm and mesoblast cells pass
into the cavity and the entire mass begins to elongate. Across the
equator of the elongating mass a transverse furrow now appears from
one side. As it deepens, the embryo is divided into two hemispheres
held together by a few ectodermal cells only. Each half is destined to
form one of the twins. Differentiation, gastrulation, and the completion
of the internal organization go ahead while the worms remain connected.
But at length they separate after a series of rotations which breaks them
apart, except in a certain proportion of cases which become double
360 POLYEMBRYONY
 
monsters of various degrees of union. Thus from the single egg twin
earthworms are produced.
 
In two other genera of oligochaetes double monsters have been described, and one infers that the twinning phenomena, though rare, may
occur in a number of families. These cases were Tubifea: tubifex, found
by Welch, Tubzfex rivulorum by Penner, and Sparganophilus eiseni by
Hague.
 
Parasitic Hymenoptera. In the parasitic wasps we find some of the
most important and complex cases of polyembryony in the entire
animal kingdom, and certainly here the results of the process are exemplified in the most striking manner. In a single brood hatching from
one parasitized caterpillar hundreds of individuals may be seen to
issue all developed from one egg. Our knowledge of polyembryony in
insects dates from the work of Marchal in 1898 and of Silvestri in 1906.
Although a number of important points still remain to be satisfactorily
cleared up, a number of investigators have contributed to this subject
since then. Among them are Martin (1914), Patterson (1915, 1917,
1921, 1927), Hill (1922, 1923), and Leiby and Hill (1923, 1924), as well
as others. The important genera studied include Litomastix truncatellus,
Ageniaspis fuscicollis, several species of Copidosoma, Paracopz'dosomopsis floridanus, and three species of Platygaster. The most recent study
is that of Parker (1931) upon the braconid, M acrocentrus. Undoubtedly
many other forms of insects show polyembryony, but the ones mentioned
include the more important cases studied.
 
The manner by which a single egg produces multiple embryos in
these forms is perhaps best understood by beginning as Patterson has
done in the paper earlier referred to with a description of Platygaster
hiemalis, a parasite of the Hessian fly, which usually produces two individuals from one egg. From this comparatively simple case we have
a gradual increase in complexity which at the end of the series is only
incompletely understood, but the simpler cases at least are suggestive
of the methods by which the more complicated probably develop.
 
In this species the parasite lays from four to eight eggs either in the
egg or young larva of the host. If fertilized, the egg nucleus divides
twice, producing two polar body nuclei; these are not passed to the
outside of the egg but remain in the cytoplasm where after a time they
come together to form a large polar nucleus called the paranucleus.
With the fusion of the male and female pronuclei the egg becomes
differentiated into two separate regions. The cleavage nucleus and
cytoplasm surrounding it become cut off from the remainder and
constitute the embryonic region, for only from it comes the material
which will go into the formation of the developing embryos. The rePARASITIC HYMENOPTERA 36 I
 
mainder of the egg containing the paranucleus and its own cytoplasm
entirely surrounding the embryonic region functions to absorb and
 
fiG 222. Polyembryonie development of Platyoaster hwmalw (From Patterson, after
Leiby and Hill )
 
A. Egg of four hours, showing sperm head and first maturation division B, Egg showing two polocytes. and both pronuclei C, Egg with pronuclei in comunction and polar
nucleus D. Embryo, two polar nuclei and a. parasitic body showing four nuclei E, Enclosed within a cyst formed from tissue of the host are two embryonic bodies each surrounded by trophamnion F. A later stage in the development of two embryos G, A
thirteen-day-old polygerm in section, showing several embryos.
 
elaborate the tissues of the host for the nourishment of the young
embryos and it is therefore spoken of as the trophamnion. In this
species, although it is not characteristic of all, the host tissues form a
362 ‘ POLYEMBRYON Y
 
cyst wall around this developing body which then is spoken of as the
parasitic body.
 
The paranucleus as development proceeds divides amitotically twice
and the daughters distribute themselves in the trophamnion surrounding the embryonic region. The zygotic nucleus of the embryonic region
divides first into two, then four, embryonic nuclei. Thereupon, the
embryonic region becomes constricted and presently separated into
two regions, each provided with two nuclei, and the trophamnion with
its paranuclei also divides into two corresponding regions. The two
halves of the parasitic body thus differentiated remain held together
within a single cyst of host tissue, but develop independently. Four,
eight, and sixteen nuclei arise from the division of each of these germs,
as they are called, and these arrange themselves into the form of a
typical spherical blastula, the cell walls being cut off around each
nucleus. The remainder of the development is unimportant, for the
process characteristic of these blastulae go forward through regular
stages. There is produced from each a new individual which hatches in
the next year.
 
In another species of this genus, P. vernalis, eight embryos are regularly developed. Here the process has a fundamental similarity to that
just described, but the details of development differ. The parasitic body
develops a number of embryonic nuclei surrounded by an appropriate
amount of cytoplasm and a cell membrane. Each of these becomes a
germ for the production of the later embryo and the entire mass is
spoken of as a polygerm. It happens that the more complex cases were
studied before the development of Platygaster was understood and
some of the problems that were not clearly worked out would now
probably be more easily followed through. It is known now that in
Copidosoma gelechiae in the formation of the polygerm many primary
germs are produced in a manner similar to the eight of Platygaster
vernalis. These separate germs of the last polygerm stage all divide and
give rise to two which develop into separate embryos.
 
Leiby and Hill believe that in Paracopidosomopsis, which is even
more complicated, a secondary germ divides to form tertiary ones before
the larval differentiation begins.
 
Armadillo. The final case of polyembryony to be discussed is perhaps
the one in which the greatest interest lies. The Texas nine-banded
armadillo Dasypus (Tatusia) novemcinctus normally produces four
young from a single egg, the quadruplets being identical in respect to
sex and to most of their morphological features. The work on the
armadillo from the standpoint of polyembryony is of rather recent
date, Fernandez concluding in 1909 that it occurs in a South American
ARMADILLO 363
 
species Dasypus hybridus, and Newman and Patterson in the same year
publishing the beginning of their important studies on the Texas species.
Subsequent publications by these authors working independently have
made available an account of the development of this form which is
practically complete. The processes have been shown to be identical in
respect to all important features in the two species which have been
studied. The reader is referred to Chapter X for a discussion of the
formation of the blastocyst in mammals.
 
In the armadillo as in other mammals, a monodermic blastocyst is
formed which becomes differentiated into a trophoblastic portion and
a formative portion, the inner cell mass. Then from the inner cell mass
the endoderm is differentiated off, the remainder becoming ectoderm.
Up to this point the blastocyst has remained free in the uterine cavity,
but now attaches to the uterine mucosa. Attachment takes place directly
over the embryonic ectoderm and the Trdiger forms at this point; then
the inward growth of the spherical endodermal mass begins which
brings about the so-called inversion of the germ layers. Within the
ectodermal mass the formation of the ectodermic vesicle marks the
beginning of the amniotic cavity. Above it an extraembryonic cavity
is formed in the mesoderm. With progressive development the shift of
the ectodermal cells takes place, resulting in the formation of the em~
bryonic shield with its thick ectoderm and the true amnion above it.
In this stage the first sign of polyembryony makes its appearance, for
from opposite sides of the ectodermal vesicle thus formed blunt projections extend laterally. Patterson called these primary buds. By this
time that portion of the trophoblast which has not become involved
in the attachment to the uterine wall disappears and the yolk sac
endoderm is directly exposed in the uterine cavity. The two primary
buds now divide each to form two secondary buds, making in all four
buds which are rudiments of the four embryos subsequently to arise.
Although they arise in this bilateral fashion and develop in the right
and left halves of the uterus respectively, they later come to occupy
positions that are about equally spaced from each other.
 
Meanwhile the vesicle grows, and the endoderm of the yolk sac, including those portions with which the embryonic ectoderm of each bud
is in contact and which will form the gut endoderm of the embryo,
faces the uterine cavity. The anterior ends of all the embryos point
toward the apex of the common ectodermal vesicle, that is, toward the
original amniotic cavity, and the entire vesicle may now be spoken of
as the common amniotic vesicle. The entire structure now grows very
rapidly, especially that portion of it which originated from the trophoblastic knob or the Trdger. This growth finally comes to occupy most
364 POLYEMBRYONY
 
of the space in the fundus of the uterus. The further history is especially
concerned with the embryonic buds. Their posterior ends lengthen out
with the growth of the vesicle and finally unite at a point opposite the
original attachment and from their point of union the umbilicus later
arises. The common amniotic vesicle by this growth procedure is left
 
fiG. 223. The development of the blastocyst of the armadillo. (After Patterson.)
ec., ectoderm; en., endoderm; icm., inner cell mass; mes.. mesoderm; tr., trager; tro.,
trophoblast; u.. uterus.
 
as a small structure at the lower apex, in contact with each bud, while
most of the remaining portion of the cyst mass with its developing
embryos is derived from the growth of the Trdger. The buds meanwhile
continue their growth, each forming a primitive streak, which is a substitution for the embryonic shield as described for other mammals.
The further development of the embryos and the subsequent changes
which lead to the production of the four foetuses need not be traced
ARMADILLO 365
 
since it is simply a problem of organogenesis and of the steps normally
following. The relations which are necessary for the understanding of
 
fiG. 224. A, The uterus and entire blastocyst of the armadillo showing paired origin
01' embryos. B, Half-grown foetuses spread out from uterus wall. (After Patterson.)
 
the polyembryonic condition all grow out of the budding processes of
the embryonic vesicle and are completed with the establishment of the
four embryos. There are many interesting problems connected with
366 POLYEMBRYONY
 
the later stages from the standpoint of later embryology and hereditary
correlations of the characters of the four offspring as well as from other
points of view, but the special problem of polyembryony is explained
by these earlier stages.
 
C. EXAMPLES or DOUBTFUL POLYEMBRYONY
 
Two other cases which resemble polyembryony in some respects
should be mentioned. As a matter of fact there are some departures in
each of them which do not justify their inclusion with this type of
development.
 
Among the trematodes the egg of Fasciola hepatica, the sheep fluke,
is fertilized in the body of the adult fluke, makes its way down the bile
duct and out of the intestine of the sheep and hatches when it rains
as a tiny ciliated larva, a miricidium. Entering the intermediate host,
the snail, the miricidium becomes a sporocyst and within it parthenogenetic ova appear which develop into rediae, the next larval form.
Within the body of the rediae the process may be repeated but at length
cercariae are developed which escape from the snail and bring about
the reinfestation of the adult host. This case has been called polyembryony by some, but by others it is regarded as paedogenesis, for
here the new larvae are said to be produced not asexually but from
parthenogenetic ova, a difierence in method which, if true, would
seem to be fundamental. However, the reservation must be made that
if the germ masses from which the new larvae arise are not ova, but are
produced asexually (as F. G. Brooks believes, having found no maturation phenomena or other egg—like behavior), then we have to do here
merely with asexual reproduction, and not even paedogenesis,
 
A second case which at first thought suggests polyembryony occurs
in the tunicates. Among the Thalaceae as represented by the genus
Salpa it has long been known that two forms of individuals are to be
expected, one a solitary form and the other a colony which is usually
found as a chain of individuals. The first of these develops asexually,
although produced from a fertilized egg. The second is known to be
budded ofi’ from a stolon which grows out from the asexual individual,
and among the colonial forms some at least are sexual, producing the
eggs and sperm which in their turn start the cycle over again. The genus
Dolielum is rather more complicated than Salpa but it seems to illustrate
the situation quite well and it is here that the type of development of
particular interest to us may be said to occur.
 
In Doliolum an oozoid is developed from the fertilized egg and it
reproduces asexually. By some it is regarded as a larval zooid, and
certainly it has not yet reached its final character. If it is correct to
EXAMPLES OF DOUBTFUL POLYE-MBRYON Y 367
 
regard the oozoid as a larval form, this case is very closely akin to
polyembryony. From the ventral posterior part of the oozoid a proliferating stolon is formed as a protrusion of the ectoderm into which
the mesoderm penetrates. From the stolon buds arise which break loose
in a very immature condition and Worm their way upward and dorsally
over the surface of the parent. Since the number given off from the
ventral stolon is less than the number later found on the dorsal process,
it is assumed that the buds must divide en route, and some evidence of
this process has been found. Arrived at the dorsal side of the oozoid,
the buds attach themselves to a posterior process of the test which
arises as a middorsal projection (occasionally spoken of incorrectly as a
dorsal stolon). These bodies attach themselves in three longitudinal
rows to the outgrowth. The two lateral rows of buds are known as
trophozooids or gasterozooids and their only function is to nourish the
colony. The dorsal row of buds undergoes metamorphosis into several
kinds of zooids. Some become phorozooids or nurse zooids, and according to some investigators they produce from a ventral stalk buds which
are protogonozooids or primary sex buds. These latter either by budding
or fission produce the sexual animals, the gonozooids or blastozooids, in
which with further development sex organs are formed and the cycle is
completed. Here an alternation of generations occurs in which there are
three asexual generations and one sexual generation in one cycle. Whether
it is to be regarded as polyembryony depends upon the interpretation
of certain stages. It is very complicated in the extreme, and is at least
close to true polyembryony.
CHAPTER VIII
THE DETERMINATION PROBLEM
 
A. INTRODUCTION AND STATEMENT or PROBLEM
 
A problem which has run through the entire history of embryology
and is yet a live question at the present time concerns the extent to
which the egg represents a fixed and definite system whose course is
set when its development has begun. This is the determination problem.
It first became a live issue during the controversy between the preformationists and the epigenesists of the seventeenth and eighteenth centuries
and was even in that crude form an attempt to solve the question of the
organization of the egg. The one school held that development was
 
simply an unfolding of an organism already present in an infolded con—'
 
dition; that is, organization was complete and development brought
forth nothing new. The other held that the egg was unorganized and
that everything in development was new. The history of embryology
since these crude beginnings, at least of that part of the science which
has concerned itself with the earliest stages in ontogeny, has been
an attempt to make clear the manner in which the organization of the
egg becomes manifest. Except for historical reasons it is not necessary
to trace the course of these studies nor would it be possible except in
a much more extensive treatment of the subject than is given here, for
the literature is voluminous. It is not even possible to summarize in a
short discussion the work which has been done. All that can be attempted
is to bring together briefly the lines of work which have been responsible
for the present conceptions in regard to determination.
 
Two sets of facts confront the student who would consider the determination problem. Neither bears directly upon the question at issue,
but both serve to limit it. In the first place an egg goes through certain
steps with surprising uniformity and produces an individual which is
structurally very complex and very much differentiated. It is organized
in the highest conceivable degree. In the second place modern genetics
has shown that the egg to begin with possesses in the mechanism by
which the genes are controlled and distributed a type of organization
likewise complex in the extreme; and there is no doubt that this mechanism operates to produce the conditions found in later ontogeny. Yet
differentiation is a matter of the cytoplasm of the cells. The repeated
 
368
INTRODUCTION AND STATEMENT OF PROBLEM 369
 
mitoses do not affect in a differential fashion the elements of the nucleus
and it is clear that the nucleus contains in the chromatin the non
differentiating material, the germ plasm, while the cytoplasmic portion
of the cell is the basis of specialization and is indeed the somatoplasm
which gives rise to all the differentiations later seen in the course of
ontogeny. Between these two sets of facts must lie the third set, little
understood and often little appreciated at the present time. Almost
nothing can be offered in the way of explanation as to the method by
which the gene mechanism produces its fundamental effect upon
differentiation. The gene mechanism concerns heredity, that is, by it is
explained the similarity existing between generations, but as yet its
study has offered little which enables us to understand its relation to
the differentiating soma. It was earlier said that heredity was the
central problem of biology. Differentiation is certainly a central problem
of development, and, let it be said, at the present time one of the most
elusive. The questions of differentiation and of determination have
dominated a surprisingly large part of the embryological work of the
last century.
 
These two questions are really two aspects of the problem of organization, for differentiation is the manifestation of the operative mechanism
of the egg as modified by extrinsic factors. To discover the extreme to
which this operative mechanism is already present in the early stages
and to which it gives a definite “set” to the differentiating embryo is
the aim of the work on determination. If differentiations become visible
early and are little modified by extrinsic factors with the result that
the course of development is orderly in a high degree, we say that the
egg is strongly determinative. But if the egg retains its embryonic
plasticity and easily adapts itself to environmental disturbances, that
is, is easily modified by extrinsic factors, it is said to be indeterminative
or of the regulatory type. If differentiations manifest themselves early,
little regulatory capacity is retained by the egg. In other words, the
capacity of the egg for regulation is inversely proportional to the
progress of differentiation.
 
It must be borne in mind also in considering the problem of differentiation (and hence of determination) that the chemico-physical organization of the cell limits the conclusions which may be reached. Differentiation manifests itself through colloidal materials. The chemistry of the
protoplasmic system is so imperfectly known that whatever conclusions
are reached regarding these problems must be subject to revision when
a better understanding shall have been attained, for example of the
phenomena of gelation which plays a very important part in the physical
expression of mitotic phenomena. It has been shown by the studies of
370 THE DETERMINATION PROBLEM
 
Conklin and of others that the position and size of the spindle are
matters of great importance in differentiation. Yet the physico-chemical
factors which are involved in spindle behavior have not yet been adequately analyzed. Other problems of physico-chemical nature similarly
affect our"conclusions. It is not too much to say that in spite of the vast
amount of embryological research differentiation and its mechanism is
one of the least understood fields of biology.
 
It has been pointed out that the function of cleavage is to sort out
the materials of the egg into cells so that differentiation may progress.
The uncleaved egg represents all of the materials present, although not
necessarily all that are later to appear. Yet the progressive development
of the organism in its usual course at least as indicated by our present
knowledge depends upon getting these materials separated from each
other. It does not follow, however, that this sorting-out process of
cleavage is the cause of the subsequent development. Rather there must
be a fundamental underlying mechanism of organization, the manifestations of which are the cleavage phenomena. Primarily determination
concerns itself with the manifestations of these underlying methods of
organization. It seeks for evidence of pre—1ocalization of areas or substances within the egg or even of an early promorphology which gives
visible expression to the underlying mechanism. Some of the questions
involved may perhaps be formulated in the following manner: Are there
special structures or substances or fundaments which exist in the egg
at the very beginning of development and which are independent of
each other and of other parts of the egg? If so, how are they formed?
Must all appear at the same time, or may some appear later on? Conversely, are the definite structures of the embryo never independent of
each other? Are the parts always influenced by the whole of which they
are constituents? Or finally, are there some eggs which are determinative
in their character and others which are not, or are some parts of the
individual embryo determinative and other parts not? Perhaps all these
questions may be said to depend most largely for their answers upon
this one. At what time and from what sources do differentiations begin
in the embryo? It may be noted that the answers to these questions
are not the same for all organisms.
 
B. CLASSICAL THEoR1Es or THE NATURE or DEVELOPMENT
 
Historically there have been a number of theories developed in
response to these questions. They represent the various forms which
the answers of different investigators have taken and must be considered
from the standpoint of the information available when they were
formulated. One of them was the theory of organ-forming regions of
CLASSICAL THEORIES OF THE NATURE OF DEVELOPMENT 371
 
Wilhelm His (1874). This is the doctrine that definitely localized areas
perhaps even in the unsegmented egg are the forerunners of the'organs
and parts of the embryo, that “the germinal disc [of the chick] contains
the preformed germs of the organs spread out over a flat surface, and
conversely . . . every point of the germinal disc is found again in a
later organ.” Ray Lankester supported His in his views, saying that
it was quite possible for the cell to “contain already formed and individualized, various kinds of physiological molecules. The visible process
of segregation is only the sequel of a differentiation already established
and not visible.” Whitman as a result of his work on Clepsine concluded
that the embryo is predetermined, even if not predelineated. Rabl and
van Beneden likewise were among the early supporters of the view that
even in the unsegmented egg an organization of protoplasmic particles
which predetermines the development of the embryo is present. In the
bald form in which this doctrine was proposed by His it can scarcely be
accepted, however, and as a matter of fact His had no great amount of
observational and experimental evidence on which to base it. The study
of cell lineage offers what of evidence there is in support of this doctrine
but even at best it does not force as rigid an interpretation as His placed
upon it. Many authors have denied it in its entirety and there are few
who do not criticize it.
 
Another form of answer to the question of determination is the
theory of organ-forming substances, according to which the materials
within the egg rather than the areas which they occupy receive the
chief attention. Here again it is obvious that not all materials within
the egg, even though they be definitely localized, are formative. Yolk,
pigment, oil globules, and other inclusions in the cytoplasm are definitely
located in many eggs, yet clearly are not formative. In some instances
visibly differentiated substances within the unsegmented egg have been
shown to have no formative function. At least they have been displaced
by pressure or by centrifugal force, and normal embryos have nevertheless resulted. Yet in other forms the materials of the egg have been
traced in a precise manner to the organs of the embryo. Surely a principle
of determination is here involved which is too important to deny because of a particular formulation of a doctrine. Perhaps the importance
of the visible organ-forming substances has been overemphasized and
these are but manifestations of a more fundamental mechanism. Yet
in very many eggs the mechanism undoubtedly exists, and later researches have certainly demonstrated the essential correctness of the
principle involved in the conception that the egg is not without an
organization before cleavage begins which conditions the future course
of its development.
372 THE DETERMINATION PROBLEM
 
As a result of the early work on cell lineage by Whitman, Rabl, van
Beneden and others the former view that blastomeres were indifferent
both in position and significance was gradually replaced by another
to the effect that the cleavage pattern was in the nature of a mosaic,
and that a blastomere occupied its particular place because of the
material contained in it, that is because of its mosaic character. The
views were supported not only by the extensive studies on cell lineage,
but also by the experiments of Roux, Chabry, Conklin, Wilson, and
others. These experiments are discussed later in this chapter.
 
The mosaic theory of development, if understood in a sense not too rigid
to take account of the fundamental plasticity of living protoplasm,
certainly expresses one of the underlying truths of embryology. One
may, however, raise the question of the manner and the time of origin
of the mosaic work and also whether it is so fixed that it is not subject
to the regulatory processes of which the organism is capable.
 
The question of regulation brings up yet another theory of historical
significance which We owe to Driesch. His terms prospective significance,
prospective potency, his equipotential system, are all well known to
those who are familiar with the history of the determination problem.
By prospective significance of a cell he meant the actual destiny in the
developmental process. By prospective potency he meant the possible
fate which the cell might attain. Prospective potency includes the sum
of the different developmental possibilities. As the result of numerous
experiments, Driesch reached the conclusion which he thought of
general application, that the egg is essentially an equipotential system,
for the cells of a blastula of a sea-urchin, for example, are of uniform
material and might be interchanged like balls in a pile without affecting
the result in the development of the embryo; in other words that the
fate, the prospective significance, of a particular blastomere is a “function of its position.” Driesch’s theory was in opposition to the mosaic
theory of development according to which the fate of the blastomeres
did not depend upon their position alone but upon their organization.
It was based upon the conception current at the time when work on
cell lineage first rose to an important place. Pfliiger had held that the
egg and its blastomeres were homogeneous throughout and that cleavage
simply multiplied the units out of which diiferentiations were later to
arise. This view was also favored by Oscar Hertwig. Driesch, who
although chiefly interested in philosophy, set himself to carry out
experiments in development upon which certain philosophical decisions might be based, made this conception the starting point of his
theory of development.
 
Some experimental evidence is at hand upon which to a certain
MORPHOLOGICAL EVIDENCE 373
 
extent the theory of Driesch may be based, while there is also evidence
upon which the mosaic conception may rest. On the one hand certain
eggs possess a high degree of regulatory capacity and are hence indeterminative in their cleavage. On the other hand certain other eggs
show the marks of differentiation appearing at a very early stage in the
 
development of the egg; these eggs possess but slight regulatory ability
and are hence determinative in character. Between the mosaic type
 
and the regulatory type no sharp boundary line can be drawn. Rather
there is a gradation from one extreme of the series to the other. If we
sum up the results of these researches we may arrange the animal series
from the regulatory to the mosaic forms in about this order: amphioxus,
teleosts, mammals, nemerteans, urodeles, anura, ctenophores, annelids,
molluscs, arthropods, nematodes, and ascidians. But it is to be noted
that purely regulatory and purely mosaic types do not occur. In this
we are merely emphasizing what has been said before, that the time at
which differentiation appears is the real criterion upon which we may
recognize the differences between determinative and indeterminative
types of eggs. In other words if differentiation sets in early the regulatory
capacity of the egg is correspondingly reduced. Conversely, eggs with
high regulatory capacity show little evidences of early differentiation.
 
C. EVIDENCE BEARING ON DETERMINATION
 
The present status of opinion in regard to the determination problem
has been reached as the result of two different lines of evidence. One of
these is the morphological study of normal embryological stages. The
other line of evidence embodies the results of many experiments which
 
have sought an insight into the fundamental nature of developmental
problems.
 
1. Morphological Evidence
 
Of the morphological evidencesthat some type of determination
exists to some extent in all eggs reference should perhaps be made first
to the contributions of genetics. The breeding experiments of this
century have very clearly shown the existence of hereditary units
within the germ cells. Although we do not by any means identify these
units with visible structures in the egg cell nor do we know how they
express their influence upon the developing organism, yet any theory
of particulate inheritance (that is inheritance based upon the presence
of organized particles within the germ cell) is, in so far as it is justified,
evidence in favor of a morphological basis of determinate development.
This evidence bears out the conclusion stated above that, although
374 THE DETERMINATION PROBLEM
 
the regulatory processes may dominate in certain types of eggs, there
are none which are purely regulatory.
 
The first signs of differentiation in the developing egg have to do with
the general features of polarity, symmetry, and pattern of the egg.
From these’ general features more detailed diiferentiations with respect
to polarity, symmetry, location, and pattern of the constituent cells
and parts of the embryo arise and later the differentiations of tissues
and the beginning of organs. Development is thus progressive, and
differentiation, at first relating only to the most general features, gradually passes to specialized details. Since polarity, symmetry, and cleavage
pattern are general in character their importance is sometimes overlocked by the student, yet very little thought is required to convince
one that they are really basic. Our morphological knowledge with regard
to the development of polarity and symmetry has been discussed in the
chapters which have to do with the different types of cleavages and
reference should be made to those chapters. These observations have
been checked by many experiments of the greatest importance and it
will perhaps suflice to refer to these experiments under the second line
of evidence as listed here.
 
Morphological studies of the cleavage pattern, as has already been
indicated, became the foundation for the mosaic theory of development
in the studies at the hands of the students of cell lineage. It early became
clear that certain types of cleavage were predominately determinative.
Some eggs with bilateral cleavage, certain types of eggs with superficial
cleavage, those with spiral cleavage, with disymmetrical, and even an
occasional form having radial cleavage, such as Strongylocentrotus, were
shown at that time to be determinative in their development. Most
forms with radial cleavage, some with bilateral, and even occasional
examples of eggs with spiral cleavage show the regulatory type, however.
For a discussion of these the student is referred to the chapters on
cleavage types.
 
2. Experimental Evidence
 
The second line of evidence which bears upon the problem of determination is perhaps no more important than the morphological evidence
but is certainly not less so and is much more recent. It is obtained from
those special experiments* which have to do with this problem.
 
‘ As pointed out in the chapter which deals with history of embryology, the present
is the period of acperimental embryology. Much of morphological character remains
to be learned, but nevertheless the dominant note in embryological research of the
present day is the experimental one. It is now sought to discover those underlying
principles which account for the form changes by which the structure of the organism
is produced rather than simply to give a descriptive account of those characters.
EXPERIMENTAL EVIDENCE 375
 
The first series of experiments of significance for study of determination is concerned with the localization of the median plama. Here as with
the other experiments to be summarized the student is referred to
Morgan’s critical discussion as well as to the original papers which
describe them. It would be impossible in a work of this size to give
even a brief account of the experiments themselves. Reference can only
be made to those which seem most significant.
 
The matter of the localization of the median plane is of importance
because it indicates the early determination of symmetry and polarity
on the part of the egg. According to some the polarity of the egg may
be traced back even into an ovarian condition, and some believe that
the type of symmetry is determined in the egg cytoplasm before fertilization. Although the evidence of these relationships seems good in
some cases it has not been made clear how much the appearance of
symmetry_in these early stages is related to the cleavage plane or the
symmetry of the embryo. No mechanism for bringing this about has
 
Experimental embryology has seemed to cover a wide range of topics and the results
of the investigations in this field are scattered throughout many journals. There
have been but few attempts to bring this material into the scope of a single volume.
The first section of Korschelt and Heider’s “Lehrbuch der vergleichenden Entwicklungsgeschichte der wirbcllosen Thiere” deals with the experimental results obtained
up to that time (1902). In 1909 Jenkinson published his book entitled “Experimental Embryology” and summarized much of the work available at that time.
The contribution to experimental embryology most important now, however, is the
volume by Morgan entitled “Experimental Embryology” and published in 1927.
Morgan has promised a further volume which will deal with such topics as growth,
reflex reactions, tropisms of the larvae, the influence of environment upon the embryos,
the source of energy of development, etc. It is to be hoped that this volume will
appear at no distant date.
 
In spite of the diversity of topics which have engaged the attention of experimental embryologists it is possible to classify them into a few divisions. (1) The early
students of this field were specially interested in the discovery of the effect that
external factors have upon the developing embryo. Among these factors are gravitation, mechanical agitation, electricity, light, heat, atmospheric pressure, osmotic
pressure, and the chemical composition of. the medium in which development takes
place. (2) In addition to this the growth problem, the problems centering around
fertilization, have occupied much attention during the present century. Something
of the nature of these problems is suggested in the section of this book which has
to do with artificial parthenogenesis, although this is but one of the many topics
that have been studied. (3) finally a great deal of attention has been given by
experimental embryologists to those problems which are concerned with the forrna—
tive changes of the egg. These factors are internal in their nature and seem to take
the experimenter further in his attempts at the analysis of the innate, vital character
of the organism than do the other problems enumerated. The experiments which
bear on the problem of determination come under this head. Those experiments
which have sought light on this problem fall chiefly within a few animal groups,
namely: the ctenophores, some hydromedusae, the nematodes, annelids and molluscs,
echinodcrms, ascidians. It may be remarked that not only are these the forms which
seem to have yielded results most capable of analysis but they are also the forms
upon which it is easiest to experiment.
376 THE DETERMINATION PROBLEM
 
been demonstrated. In many cases where a relationship between the
first cleavage plane and the planes of symmetry of the later embryo
have been made out it is thought that the point of entrance of the
spermatozoon and the path traveled by the sperm pronucleus in approaching the egg pronucleus determine the position of the plane.
Suggestions have also been made that the pressure of the enveloping
membrane of the egg or pressure from the oviduct or other external
factors may be related to the position of the plane. Certainly the causal
character of such factors has not been demonstrated. It may be said,
however, that so long as the possibility remains of a relationship for
example at the point of entrance of the spermatozoon it is necessary
to assume that the symmetry of the embryo goes back to a predetermined symmetry of the egg.
 
The question of a relationship of the median plane and the first
cleavage plane arises in the history of embryology in relation to the
frog egg. As long ago as 1851 Newport had reported that the two coincide, and from that time the question has been often discussed. In
the frog egg at the time of cleavage there is already present a bilaterality
as shown by the presence of the gray crescent. The real question involved
in determining the symmetry relationships is: what in the uncleaved
egg causes the material to take the position of the gray crescent, and
why does the first cleavage plane cut through the middle of it? Experiments have shown that its position is determined after fertilization and
that any meridian of the unfertilized egg may become the median plane.
After fertilization the meridians are not equivalent in this respect,
however, for usually the crescent forms opposite the point of entrance
of the sperm. A long series of experiments can be cited to show that in
nearly two-thirds of the cases the first cleavage plane does coincide
with the middle of the gray crescent. It is clear, however, that if 30 per
cent or more of the eggs fail to show this relationship the mechanism of
determination is by no means a fixed one. In other amphibia the experiments of Jordan indicate that the first cleavage plane is at right angles
to the axis of the egg of Diemyctylus, and Spemann has found for Triton
that the second cleavage plane coincides with the median plane of the
embryo. Of course it is immaterial from the standpoint of determination
as to whether it is the first or second plane which shows the relationship.
In the teleost fishes according to the work of Morgan and of Clapp no
definite relation between the second plane and the median plane of the
body can be made out. For the sea-urchin a considerable amount of
evidence is available. In Toxopneustes, Wilson and Mathews related the
appearance of the first cleavage plane to the entrance of the spermatozoon, and Boveri held that it coincided with the median plane of the
EXPERIMENTAL EVIDENCE 377
 
embryo. In the eggs of Echinus, Driesch found the second plane to
correspond to the median plane and Runnstrém assumed that the first
cleavage coincides with the median plane. Recently Von Ubisch has
performed a very ingenious experiment by which certain portions of
the egg were stained with intra vitam stains; in three species of seaurchins he obtained results which are in agreement. He was able to
demonstrate no fixed relation between the planes of symmetry and
planes of cleavage, but found some evidence that the first cleavage
plane more nearly coincides with the median plane. On the whole for
the sea-urchins perhaps this is the most acceptable conclusion. In his
study of ascidian embryology Conklin determined that the first cleavage
plane is the median plane of the embryo, and that in Cynthia its position
is indicated before the pronuclei meet. In the nematodes, according to
Boveri’s work on Ascaris, the third cleavage plane of the dorsal cells is
the median plane of the embryo. In Nereis, Just has found that the
second cleavage plane usually corresponds to the median plane of the
embryo but the first cleavage plane is determined by the position of
the entering spermatozoon. Insect eggs are distinctly bilateral so far as
their orientation is concerned, the position of the egg as laid corresponding to the symmetry of the mother’s body and definitely indicating the
position of the embryo in the egg. For the chick and pigeon Bartelmez
has held that bilaterality is present even in the small ovarian eggs.
 
A second series of experiments related to the problem of determination
has sought to discover to what extent localization of germinal areas is
present before cleavage, using as a method the development of egg fragments. Eggs of Cerebratulus were out along definite planes by Wilson,
Zeleny, and Yatsu. Cuts were made both before and after fertilization
and development followed without difficulty. The cleavage of the fragments in general corresponded to the type of cleavage of the whole egg
but upon a much reduced scale. It was not found to make a difference
from which part of the egg the fragment was taken. The experiments
show that either factors which determined cleavage were not yet
definitely localized at the time of maturation or the egg is capable of
very extensive regulation. According to Yatsu if the operation occurred
between the formation of the first and second polar bodies the cleavage
was entirely regular but if it was after the second division irregularities
developed in some of the cases. Wilson experimented with fragments
of the egg of Dentalium. Here the presence of the yolk lobe complicates
the result. If the yolk lobe is entirely present and only the apical portion
of the egg cut off, the resulting larva is nearly normal; likewise an entirely
symmetrical division of the yolk lobe seems not seriously to interfere
with the course of development. If the cuts are made in any other
manner, however, irregularities appear. The ctenophore Beroé when out
into fragments in the unsegmented condition produces in some cases
partial embryos and in others whole ones depending on whether the cut
is symmetrical or oblique. Driesch, Morgan, Yatsu, and fischel have
experimented with this form. With sea-urchin eggs conflicting results
have been obtained from experiments with the development of fragments. Taylor and Tennant using accurate methods of cutting with a
micro-dissecting machine obtained small pluteae from the developing
fragments which were like the normal ones. But Harnley obtained
evidence that the materials of the egg were qualitatively different.
finally experiments on the development of parts of Triton eggs have
been performed by Spemann and Baltzer. Non-nucleated fragments,
obtained by separating the egg by means of a hair tied around it, developed but rarely and the nucleated fragments produced dwarf larvae
which did not live long enough to undergo metamorphosis although
normal in most particulars.
 
An interesting result of these experiments is the conclusion that the
entrance of the sperm into the egg is not of itself sufficient to start
development, for, if an egg is cut just after the penetration of the sperm
so that the female pronucleus is in one half and the male pronucleus in
the other, it is the half containing the sperm pronucleus that develops
but not the other. Something else besides the mere initiation of division
is accomplished by the entrance of the spermatozoon. The cleavage of
egg fragments demonstrates that for many types of eggs the pattern
develops along with the mitotic figure.
 
Another series of experiments has sought to discover to what extent
it is possible for a whole embryo to develop from an isolated blastomere.
In some few eggs it is possible to cut the blastomeres apart at the time
when they are most widely separated from each other as the first cleavage is closing. In others it has been found possible to separate them by
shaking them in a tube of water, or by squirting them from a pipette.
Again eggs of echinoderms permit the easy separation of the blastomeres
if they are kept in calcium-free sea water while the first cleavage is
taking place. Isolation experiments have been performed on sea-urchins,
the hydroid Clytia flavidula, Cerebratulus, amphioxus, teleost fishes,
Triton, and the frog, and in all these cases whole embryos were obtained
from the isolated blastomere. On the other hand blastomeres of ctenophores, molluscs, and ascidians when isolated give rise to half embryos
only. It would seem that this emphasizes again the distinction between
determinative and regulatory eggs.
 
The question arises as to whether the development of the isolated
blastomere is strictly comparable with the results that would be obtained if the material of the missing portion of the egg were present.
Experiments have been performed in which the single blastomere has
been allowed to develop in contact with the material of its sister cell,
which owing to various kinds of injury was prevented from any active
participation in the normal result. Experimenting upon the frog, Roux
injured one blastomere with a hot needle but did not kill it. He thought
that the subsequent development of the uninjured blastomere in contact
with the inactive one was in the nature of regulation and that gradually
the missing portion of the embryo was restored. This conclusion seems
doubtful as there is now good evidence that the resulting embryo is more
nearly one-half than a whole. Later studies have shown that, in experiments of this kind, if the plane of the first cleavage goes through the
middle of the gray crescent a half embryo results. If the plane is parallel
to the gray crescent and the injured blastomere is the one which contains it, nothing recognizable is produced from the opposite one. But
if the opposite blastomere is injured the one containing the gray crescent
will produce the anterior end of the embryo. Even if the cleavage plane
is at other angles the blastomere containing most of the gray crescent
will produce an anterior end.
 
McClendon working on the tree frog, Chorophylus (Pseudacris),
sucked out the injured blastomere to determine whether its presence
has any effect. In his experiments the remaining blastomere produced
a normal whole embryo of one—half size. Injuries to one blastomere of
the egg of Ascaris led to the conclusion in the experiments of Stevens,
of Boveri, and of Schleip that each individual cell contains the factors
which are responsible for its own development; in short, that there is
little self-regulation on the part of the blastomeres. The egg of Cyclops
after the injury to one blastomere has been studied by Fuchs and by
Miss Jacobs. The evidence goes to show that for this egg the contact of
the injured blastomere with the uninjured one does not materially
affect the result of the development of the latter. This results in a
partial embryo. In this same connection the experiments of a number
of investigators, of whom Hegner and Reith are typical, on the effect
of injury to the eggs of insects should be mentioned. Insect eggs apparently may be among the most determinative with which we have to deal,
for these experiments indicate that different cytoplasmic areas on the
surface of the egg are fixed in their prospective significance even before
the cleaving nuclei with their surrounding cytoplasmic islands migrate
to the surface and they have no great powers of readjustment. There is
indeed a considerable degree of independence in the development of the
respective parts. If the injury is not too severe to a certain localized
portion of the egg the remainder will go ahead and develop without much
dependence upon the injured portion, but will produce only that part of
the embryo which was to be expected. Reith found that, if the posterior
end of the egg of the house fly is injured, the parts normally resulting
from the anterior end will develop. If the anterior end is the location of
the injury, a larva without a head end develops, and in some cases injury to the middle portion of the egg was not so severe but that both
anterior and posterior organs developed.
 
Hegner’s experiments on the eggs of the chrysomelid beetles Calligrapha multipunctata and Leptinotarsa decemlineata are Well known.
Here the posterior end of the egg is the location of the pole plasm which
Hegner found to pass into the germ cells in development. By injuring
this region with a hot needle he was able to secure embryos without
germ cells. Evidently the cytoplasmic regions in the eggs of these insects
are very early set aside to produce definite parts of the embryo. Yet it
must not be inferred that the regions in question retain no powers of
adjustment. As cleavage progresses the possibilities of readjustment
are lessened but are not entirely lacking.
 
A very important series of experiments carried out in the laboratory
of Spemann on the embryos of Triton have shown that the future of
certain ectodermal areas in the gastrula are much modified by their
position. The method by which these experiments were carried out was
that of transplanting a portion of the ectoderm by means of a micro-pipette
from one portion of the body to another and studying its relationship
to the development of the neural plate. From this study it appeared
that the presence of the endomesoderm beneath the surface of the
ectoderm is immediately necessary for the neural plate to be formed.
Spemann and his collaborators have shown that the prospective ectoderm
is capable of producing entirely different organs upon transplantation.
For instance ectoderm from the top of the young blastula or gastrula
implanted on the lip of the blastopore and carried to the interior may
become notochord, mesoblastic somites, pronephros, or perhaps other
organs. Ectoderm taken from a slightly later stage, that is, after the
closure of the blastopore, if carried into the mesoderm becomes mesodermal somites; if carried into the endoderm goes to the formation of
the archenteron. It should be pointed out that particular organs which
differentiate from given substances may through the process of rearrangement be induced in an entirely different direction from that
which their normal determination indicated. Throughout the animal
kingdom there are many cases which serve to emphasize the difference
between the determination of an organ and the actual differentiation
which sometimes results from the modification of normal processes.
What is shown by such cases, however, is not that the unusual condition
is one of indetermination but that the organism has responded to modi—
fying factors to produce a result different from that which would have
occurred had not the unusual factors been present. Determination of
an embryo does not always correspond to its differentiation.
 
A problem which has given rise to a great deal of experimentation in
relation to the question of determination is the influence of pressure
upon cleaving eggs. The work began with the experiments of Pflfiger
in 1884 in compressing the eggs of frogs between two glass plates. The
direction of the first three cleavage planes was found to be at right
angles to the plane of compression. When the compression was released,
normal embryos developed. Similar experiments have been performed
in numerous other eggs with the result that normal development is
found to follow the release of pressure on eggs of hydroids, sea-urchins,
frogs, and Cerebralulus. In eggs of N ereis, Ciona, and molluscs, abnormal
development follows compression. In the first group of eggs it is to be
noted that differentiation does not begin until there is relatively a
large number of cells present. In the second group signs of differentiation are to be noted very early. This series of experiments was used by
0. Hertwig and by Driesch in support of their opposition to the mosaic
theory of development. Perhaps the experiments are less crucial than
was formerly believed and merely emphasize the distinction previously
insisted upon that there are two types of eggs with respect to their
capacities for regulation as distinguished from determination.
 
finally the literature of experimental embryology contains many
records of attempts to bring about the redistribution by centrifuging
of egg substances, particularly those which are visibly different. These
materials as well as the formed materials of the egg yolk, pigment, fat,
and other inclusions are often of different specific gravity and hence
respond to centrifuging by redistributing themselves in different zones
or strata. This transfer of materials throughout the egg takes place as
a rule without injury to its living substance. The use of the centrifuge
in experimental embryology began with the work of Lyon in 1906,
although it had been utilized for the study of the constitution of the
cytoplasm by Gurwitsch in 1904. Lyon’s paper is a classical one in
embryology both because of the introduction of a new method and
because of his discovery that the redistribution of the egg constituents
does not afiect the development of the eggs from the standpoint of
determination. Many other investigators have used this method for
the study of eggs through a wide range of animal forms. The results of
the experiments with the centrifuge have rather uniformly indicated
that the visibly stratified substances in the egg are not determinative in
the sense that they are organ forming. It would seem that the method,
though productive of results which have great value from other standpoints, has failed to give critical evidence as to the determinative character of development in the eggs to which it has been applied.
 
As a conclusion to this long catalogue of evidences, the position
earlier talfen in this chapter may be reiterated. The animal series can
be arranged in such a manner as to show a transition from eggs which
are highly regulatory to those that are highly determinative in character.
N 0 eggs are known which are purely regulatory or purely determinative,
but at one end of the series differentiation sets in very late and the
regulatory capacity is high. At the other end the marks of difierentiation
begin even before cleavage and the powers of regulation are correspondingly lessened.
 
 
==CHAPTER IX ECOLOGICAL CONTROL OF INVERTEBRATE LARVAL TYPES==
 
Throughout the animal kingdom many diverse environmental relations surround the eggs and young so that many responses might be
catalogued. Environmental influences find expression in the places
where the eggs are laid, in the amount and kind of food provided for the
young during the early development, in the different devices for their
protection, in specialized modifications for accomplishing locomotion
and other vital activities, and in many cases in the production of forms
of larvae ‘which are totally different from the adult organisms. These
special types of larvae present a great range of variations from the
modes of direct development with which the student of the embryology
of vertebrates is familiar. These larval types involve a metamorphosis
to the adult form which may be more or less complete and which in
such cases brings the growing organism into an environment quite
unlike that of its earlier development; metamorphosis is necessary in
those forms in which the food and habits of the adult are unsuitable
for developing young. If we assume the sea to have been the original
home of most primitive stocks, an assumption which is more or less
common and seems in line with the fact that very many types of animals
develop in a moist atmosphere or liquid medium, we should expect the
majority of unusual larvae to be found in the species living in salt water.
The transition from salt water to fresh or to the terrestrial forms of life
has presented many difficulties to the developing young and as a result
those animals which live in fresh water or are terrestrial are more often
characterized by direct development than are the salt-water forms.
It may be regarded as an axiom of development that sessile adults
have active young. This activity has two obvious results; first, the
species secures its dispersal through the migration of the young, and
econd, it extends the range. The migration is commonly passive but
over a period of time serves to extend the range of the species as successfully as if the adults themselves were able to move. To insure dispersal,
vast numbers of gametes must be produced, for the chance method of
fertilization that usually accompanies such cases results in a failure of
very many eggs and sperm to become further activated, and of those
eggs which are fertilized only a few can come to maturity. The larval mortality is very high indeed, for these young are the food of many
species as well as the victims of physical forces and of their own inability
to find continuously satisfactory conditions for growth. The vast number
of eggs produced may be realized by reference to the turbot which produces 9,000,000 in a single season, the cod with 5,000,000, and to the
flounder with 1,000,000. In higher animals the reproductive energy
is conserved by various means for caring for the young during early life,
but in marine forms this is usually not the case. The second consequence
of larval activity is to bring the growing forms into an entirely difierent
range. This is illustrated in the case of the lobster, which is a bottom
feeder, lurking in the crevices between stones and elsewhere to capture
whatever prey may come within its reach, or feeding upon such dead
forms as may be found nearby. The larvae, up to the time of the fourth
molt, however, swim at the surface of the sea water. In addition to this,
they are positively phototropic to light of the intensity of ordinary
daylight, but the adults are negative. Thus the pelagic larvae are brought
into a range of environment where their food, which consists of plankton,
especially copepods, is abundant. Special structural modifications adapt
these larvae to their surface pelagic life. They are the better enabled to
swim on the surface of the water because of the possession of exopods,
the outer branches of the walking legs characteristic of lower crustaceans
but not present in the adults of the higher forms. These are retained to
the fourth molt, when they are cast off, being no longer useful; the larva
then goes to the bottom. Herrick makes note of several changes in
structure and instincts which take place at the beginning of the fourth
stage, which marks the most surprising leap in the whole history of development. Among these are the following: the primitive swimming
branches of the thoracic appendages are lost; the cuticle becomes shell—
like, containing more lime; the pigments are denser, the colors brilliant,
and the color pattern variable; otocysts are present and orientation is
perfect; rotation of the great forceps is complete; the animal, during
at least a part of this stage, moves toward the light and swims steadily
at the surface with the great claws directed forward and held close
together; the preying instinct is more marked; the fighting instinct,
the instinct of fear, “feigning,” and hiding are all developed by the
close of the fourth stage or in the fifth, when the animal goes to the
bottom to stay. In many other animals similar gain is accomplished
by a specialized form of larval structure. The larva finds itself adapted
to-securing food which is suitable for it, and structures which have
only temporary employment are present and useful. It follows, however,
that the gain to the larva would become a loss if the subsequent stages
in the life cycle were not radically changed in such a way as to enable
the organism to undertake a new mode of life. In other words, metamorphosis in such cases is a necessity for bringing about those adaptations which fit the organism to live in its permanent environment and
 
there to undergo those further changes which look toward the production of new germ cells.
 
It is not usual to find metamorphosis in animals which live in fresh
water, although there are some outstanding cases in which larvae
totally unlike the adult are developed in species inhabiting fresh water.
It may, however, be taken as a general rule that development in freshwater forms with the exception of certain few highly specialized cases
is direct. Fresh water presents a great lack of constancy in living conditions as compared with those of the sea. With but few exceptions the
bodies of fresh water lack sufficient depth and area to maintain even a
low degree of constancy. Fresh water becomes heated much more easily
than the sea, it freezes comparatively quickly, its streams are subjected
to periods of flood during which the water runs rapidly and scours out
the beds or overflows, and when it recedes leaves innumerable forms of
life stranded to perish. Every stream has narrows and depths where it
runs rapidly and flats where its current is slow, an environment in
which the fragile larvae would scarcely be able to maintain themselves,
and there are but few animals which go through an independent larval
history in fresh water. The lack of suitability of fresh water to larval
development without doubt explains why so many groups of marine
animals have not been able to gain a foothold in fresh water. A very few
sponges, almost no coelenterates, occur in this environment, and many
groups of marine fish and ascidians, cephalopods, king crabs, and some
of the worm groups have not a single representative in fresh water.
Animals that cannot produce eggs which develop into young like the
adult are prevented from gaining ‘a. foothold by such a changeable
medium as fresh water. In addition to the difficulties of fresh-water life
already noted, a zone of brackish water between the fresh water and
the sea is itself an almost impassable barrier to the entrance of marine
forms.
 
Terrestrial life presents to developing larvae even more dangers
than fresh water. To this situation is due the fact that in land forms
development is either direct and fairly simple or else specialized with
complicated devices for caring for the young during their immature
period. The latter condition is illustrated by many forms of insects in
which metamorphosis is complete, often involving very complicated
life histories. Some of the disadvantageous features of the terrestrial
386 ECOLOGICAL CONTROL OF INVERTEBRATE LARVAL TYPES
 
environment are the following: temperature undergoes a wide range
of variation, often passing quickly between the extremes. This condition is quite unknown in the ocean and is much less in fresh water.
The very changeableness as well as the extremes of heat and cold are
hardships for the developing larvae. The weight of the body is no
longer buoyed up by water and must be supported at every moment.
This involves consumption of much energy as compared with the almost
passive drifting of larvae in aquatic habitats, and renders movement
much more difficult and restricted. Food no longer streams by as in
the contrasting case, but must be actively sought, is often very much
more restricted as to kind, and presents an increased toughness since
in the composition of land forms the percentage of water is much less,
and the food is necessarily more difficult to find. The glare of daylight
and the consequent difficulty of avoiding enemies puts the terrestrial
larvae to a disadvantage which forms living in the subdued shadows of
the water do not share. finally the rapid evaporation to which terrestrial forms are subjected requires special devices for protecting the soft
exterior of the organism. A heavy shell, mucous glands, and other
similar devices show what a serious drain upon the organism requirements of this kind cause.
 
These considerations account in a large measure for the lack of
uniformity in the occurrence of larval types throughout the different
groups of the animal kingdom. The particular forms of larvae within a
group are of adaptive rather than taxonomic significance.
 
The general subject of the care of young animals was briefly but
instructively discussed by Gamble in “The Animal World” (Holt and
Company). Some of the ideas mentioned on the three preceding pages
are suggested by his discussion. Gamble sums up the responses of
animals to different environmental conditions in which the young must
be produced as follows:* “We find isolated examples of the retention of
the young by diminution in the size of the family. Speaking generally,
marine animals pour their eggs broadcast, and leave their minute larvae
to complete their metamorphosis unaided and unsheltered, but in
every group there are malthusian species which not only restrict their
families in number, but enclose them by protective envelopes. The
varied experience of larval life in this curtailed and direct development
supplants metamorphosis. The eggs become larger and the young
stronger at birth.
 
“In fresh water the limitation and protection of the family is more
generally the rule. Insects and Amphibia are the only large classes
 
‘ Quoted by permission of Henry Holt & Co.
 
which go through their larval life in fresh water. But the protection
 
is usually of the simplest kind and is confined to the earlier stages of
development.
 
“On land the insects form the only class in which the majority still
pursues a free larval history. Others develop directly, either growing
up into full stature without guidance or protection, or carried and fed
by their parents for some time both before and after hatching.”


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Richards A Outline of Comparative Embryology. (1931)

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This historic 1931 embryology textbook by Richards was designed as an introduction to the topic. Currently only the text has been made available online, figures will be added at a later date. My thanks to the Internet Archive for making the original scanned book available.
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1931 Richards: Part One General Embryology 1 Historical Development of Embryology | 2 The Germ-Cell Cycle | 3 Egg and Cleavage Types | 4 Holoblastic Types of Cleavage | 5 Meroblastic Types of Cleavage | 6 Types of Blastulae | 7 Endoderm Formation | 8 Mesoderm Formation | 9 Types of Invertebrate Larvae | 10 Formation of the Mammalian Embryo | 11 Egg and Embryonic Membranes | Part Two Embryological Problems 1 The Origin And Development Of Germ Cells | 2 Germ-Layer Theory | 3 The Recapitulation Theory | 4 Asexual Reproduction | 5 Parthenogenesis | 6 Paedogenesis And Neoteny | 7 Polyembryony | 8 The Determination Problem | 9 Ecological Control Of Invertebrate Larval Types

Historic Disclaimer - information about historic embryology pages 
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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)

Outline of Comparative Embryology

By

Aute Richards

Professor of Zoology

University of Oklahoma

New York John Wiley 8: Sons, Inc. London: Chapman & Hall, Limited 1931

1951

Table of Contents

Part One General Embryology Part Two Embryological Problems

Preface

As the result of a number of years of experience in introducing students to the subject of embryology, the writer has found it desirable to ‘depart from the common practice of studying chiefly the special embryology of the chick, pig, and perhaps of amphioxus and the frog, and to devote much attention to the principles of general embryology. This procedure is based upon the assumption that a broad background of general knowledge forms a desirable starting point for the study of special embryology to be taken up later. As comparative anatomy has proven to be the best basis for the later study of anatomy, so comparative embryology forms a proper basis for a study of special embryology. Unfortunately there has been no book in our language which brings together in a small compass the principles of general comparative embryology.

In this book it is the aim to set up the general principles of development so that the student may see how his special case—chick, starfish, or other form—is merely one of several types and what its relation to the other types may be. The writer holds that the most effective presentation of the subject matter of embryology is the laboratory study of desirable types, supported by text-book and “quiz” work on these forms and accompanied by the consideration from a comparative standpoint of the broad principles of the subject, such as types of egg structure, of cleavage, of gastrulation, and the critical consideration of classical embryological doctrines, etc. To present the material in brief form for this general part of a course in Comparative Embryology this volume is designed. '

In Part One are taken up those phases of development which are passed through in the embryology of most higher forms of animals. A comparative study of these phases no doubt forms the basis of ninetenths of the courses in this subject. Of the vast amount of material from which choice must be made, the decision as to whether any certain topic should be discussed has been based always upon a single criterion. It is sought to show only how the single-celled fertilized egg arrives at the multicellular condition characteristic of the fully formed, but undifferentiated, young organism in which the organ systems are established. In an outline of comparative embryology it is not possible to follow through all the details nor to repeat descriptions whose general features apply to more than one kind of animal. Nor is it possible to follow through for these forms the later stages in their development and differentiation. If completeness were the goal, it would be necessary to include the special embryology of the many forms about which investigators would desire information, an obviously impossible task. It is hoped, however, that a basis is here laid for understanding the detailed embryology of any of the types and for working out later stages in whatever group the student’s interest may lie.


Part Two considers numerous miscellaneous problems that have arisen in connection with the history of embryology. Here the choice of topics has been governed largely by questions asked by students both beginning and more advanced. No attempt is made to cover all the classical topics of embryology, nor to arrange the ones chosen in an order to develop any particular thesis. It is simply thought to satisfy in some measure student interest in them and to make them easily available. Discussions of many of them are not available in brief form in any English text, although they concern matters about which students of zoology should be informed, for they are chiefly problems of normal development.


The embryology of the present day is experimental embryology. Its aim is to secure an insight into the real nature of those steps by which a single-celled egg becomes a completed adult. An understanding of development in its true sense is its goal. Many aids to experiment used only by chemists or physicists in years gone by are now every-day tools of the embryologists, for descriptive embryology alone is inadequate to give a complete understanding of development. Yet experimental embryology runs the danger of considering only processes and those out of relation to structures. It is in structures that functions are inherent, for one cannot understand the workings of a machine with which he is unfamiliar. Morphology in its descriptive phases is therefore basic to a proper attempt to work out functional relations. Our admiration for the attempts to secure an intelligent conception of the mystery which underlies the pageant of development must not allow us to disregard the importance of a foundation of knowledge of descriptive embryology. Perhaps the errors which may be avoided by the study of descriptive embryology in its comparative phases may serve to recompense the student for the time lost from experimental embryology.


Undoubtedly numerous errors are to be found in this volume. Much that is discussed has been the subject of life-long study by many investigators and has concerned material collected from all over the world. To understand all adequately so that each may be mentioned correctly and weighted properly in a brief outline, is a task hardly to be accomplished, and many inconsistencies of treatment must be apparent to the reader. It must be borne in mind, however, that not an extended treatise but an outline of principles is the intent of the book, and the intent places many limitations upon what can be undertaken.


Acknowledgments are due for assistance in almost every section. The material treated in a work of this kind is by no means new, and it would be impossible to present any one phase of it without finding parallel treatment in some source of information available to students of embryology of this day. There is no claim to originality in the book, not even in the treatment of many chapters. The book will have served its purpose, however, if it appears to have sufficient pedagogical background and if it presents in sufficiently compact form these principles, many of which I think are not briefly summarized elsewhere in the English language, and which are needed to give students a basis for work in special embryology,-either medicalor experimental.


Korschelt and Heider’s “Lehrbuch der vergleiehenden Entwicklungs— geschichte” is a great treasure house of embryological learning to which constant reference has been made. In many places (particularly in Chapters VII and VIII, Part One) even their arrangement has been so much the best that only minor departures from it are to be found here. In others an entirely different organization of the same material is here adopted. But the debt to Korschelt and Heider is a very great one. I appreciate very mucl_1-the gracious verbal permission to use their material freely which was given me by both Doctors Korschelt and Heider. .”_


Drawings to illustrate ,the text are from many sources and not many are new. The writer is not impressed with the desirability of replacing pictures made by investigators on specialforms with new ones when the former are well known and of proven value. The drawings in every case are accompanied by a legend giving the name of the investigators to whom indebtedness is due.


Permission has been granted by the following publishers to make use of the figures indicated either as modified, or in the case of numbers 1, 2, 3, 135, 136, 142, 153, 1-81 of the figures themselves. By Henry Holt & Co. permission has been given to use from Loey’s “Biology and Its Makers,” our figures 1, 2, and 3; to use from Kellicott’s “General Embryology” our figure 5; from Kellicott’s “Chordate Development” our figures 135, 136, 142, 144, and 181; and from Lillie’s “Embryology of the Chick” our figures 151, 152. By P. Blakiston’s Son & Co., Inc., permission has been given to use from Folsom’s “Entomology with Special Reference to Its Ecological Aspects,” 3rd edition, our figures 117, 161, and 162; and from Patten’s “Embryology of the Pig,” figure 7. The Oxford University Press has permitted the use from Jenkinson’s “Vertebrate Embryology” of our figures 81 and 173. The Princeton University Press has granted permission to use from Conklin’s “ Heredity and Environment” our figures 7 and 8. The U. S. Bureau of fisheries has given permission to use from Herrick’s “American Lobster” figures 113, and 1973.. And William Wood & Co. have permitted the modification of figures from Bailey and Miller’s “Textbook of Embryology” represented in figures 140 and 141. Macmillan & Co., Ltd., has sold us permission to make use of our figures 103, 109, 110 from McBride’s “Textbook of Embryology, Vol. I, Invertebrate Embryology,” and of our figures 167, 168, and 170 from Graham Kerr’s “Textbook of Embryology, Vol. II, Vertebrate Embryology.” The graciousness of the various publishing companies in thus facilitating our work is deeply appreciated.


Especial acknowledgment for help in many ways including aid with the materials used and the reading of parts of the text is due to 1ny wife, Mrs. Mildred Hoge Richards. My colleagues of the Department of Zoology of the University of Oklahoma, Doctor A. O. Weese and Doctor A. I. Ortenburger have assisted with advice and have read portions of the text. Professor J. F. Paxton of the Department of Greek has aided me with questions of terminology. And finally my assistants Mrs. Celeste Whaley Taft and Miss Kara J. Fullerton have given the most painstaking attention to a multitude of details. To all of these I am deeply grateful.

A. R.

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)

1931 Richards: Part One General Embryology 1 Historical Development of Embryology | 2 The Germ-Cell Cycle | 3 Egg and Cleavage Types | 4 Holoblastic Types of Cleavage | 5 Meroblastic Types of Cleavage | 6 Types of Blastulae | 7 Endoderm Formation | 8 Mesoderm Formation | 9 Types of Invertebrate Larvae | 10 Formation of the Mammalian Embryo | 11 Egg and Embryonic Membranes | Part Two Embryological Problems 1 The Origin And Development Of Germ Cells | 2 Germ-Layer Theory | 3 The Recapitulation Theory | 4 Asexual Reproduction | 5 Parthenogenesis | 6 Paedogenesis And Neoteny | 7 Polyembryony | 8 The Determination Problem | 9 Ecological Control Of Invertebrate Larval Types

Cite this page: Hill, M.A. (2026, November 3) Embryology Book - Outline of Comparative Embryology. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Book_-_Outline_of_Comparative_Embryology

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