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Copyright, 1920, by P. Blakiston's Son & Co. 

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The fact that most courses in vertebrate embryology deal to 
a greater or lesser extent with the chick seems to warrant the 
treatment of its development in a book designed primarily 
for the beginning student. To a student beginning the study 
of embryology the very abundance of information available in 
the literature of the subject is confusing and discouraging. He 
is unable to cull the essentials and fit them together in their 
proper relationships and is Hkely to become hopelessly lost in a 
maze of details. This book was written in an effort to set forth 
for him in brief and simple form the early embryology of the 
chick. It does not purport to treat the subject from the com- 
parative view point, nor to be a reference work. If it helps the 
student to grasp the structure of the embryos, and the sequence 
and significance of the processes he encounters in his work on the 
chick, and thereby conserves the time of the instructor for inter- 
pretation of the broader principles of embryology it will have 
served the purpose for which it was written. 

In preparing the text, details have been largely omitted and 
controverted points avoided for the sake of clarity in outHning 
fundamental processes. While I would gladly have avoided 
the matters of cleavage and germ layer formation in birds, a 
brief description of them seemed necessary. Without some 
interpretation of the initial phases of development, the student 
has no logical basis for his study of the already considerably 
developed embryos with which his laboratory work begins. 
The treatment which it is desirable to accord to gametogenesis 
and maturation as processes leading toward fertilization would 
vary so greatly in extent and view point in different courses 
that it seemed inadvisable to attempt any general discussion 
of these phenomena. 

The account of development has not been carried beyond the 
first four days of incubation. In this period the body of the 
embryo is laid down and the organ systems are estabHshed. 
Courses in general embryology rarely carry work on the chick 
beyond this phase of development. More extensive courses in 



which a knowledge of mammalian embryology is the objective, 
ordinarily pass from the study of three or four day chicks to 
work on mammalian embryos. 

While the text has been kept brief, illustrations have been 
freely used in the belief that they convey ideas more readily 
and more accurately than can be done in writing. Direct 
labeling has been used in the figures to facilitate reference to 
them. Most of the drawings were made directly from prepara- 
tions in the laboratory of Histology and Embryology of Western 
Reserve University School of Medicine. However, figures from 
other authors, particularly Lillie and Duval, have been used 
extensively for comparisons and for schemes of presentation. 
Several figures have been reproduced directly or with only 
slight modifications. These are designated in the figure 

I wish to acknowledge the assistance I received in the prepa- 
ration of material by Mrs. Mary V. Bayes, and in the drawing 
of the figures by Mrs. Bayes and Dr. Louis J. Karnosh. I am 
also indebted to my father. Prof. Wm. Patten of Dartmouth 
College for criticism of the figures, and to Dr. F. C. Waite of the 
School of Medicine, Western Reserve University for his helpful 
interest and cooperation in all phases of the preparation of the 
book and especially for his reading of the manuscript. 

Beadley M. Patten. 
Western Reserve University, 
School of Medicine. 
Cleveland, Ohio. 


Preface v 

Introduction i 


The Gametes and Fertilization 7 

The ovarian ovum; maturation, ovulation, and fertilization; the 
formation of the accessory coverings of the ovum; the structure of 
the egg at the time of laying; incubation. 


The Process of Segmentation 14 

The effect of yolk on segmentation; the unsegmented blastodisc; the 
sequence and orientation of the cleavage di\dsions in birds. 


The Establishment of the Entoderm 20 

The morula stage; the formation of the bias tula; the effect of yolk on 
gastrulation; gastrulation in birds. 


The Formation of the Primitive Streak and the Establishment of 

THE Mesoderm 27 

The location and appearance of the primitive streak; the origin of the 
primitive streak by concrescence of the blastopore; the formation of 
the mesoderm. 


From the Primitive Streak Stage to the Appearance of the Somites ss 
The primitive streak as a center of growth; the growth of the entoderm 
and the establishment of the primitive gut; the growth and differ- 
entiation of the mesoderm; the formation of the notochord; the forma- 
tion of the neural plate; the differentiation of the embryonal area. 


The Structure OF Twenty-four Hour CmCKS 44 

The formation of the head; the formation of the neural groove; the 
regional divisions of the mesoderm; the coelom; the pericardial region; 
the area vasculosa. 



The Changes Between Twenty-four and Thirty-three Hours of 

Incubation 52 

The closure of the neural tube; the diflferentiation of the brain region; 
the anterior neuropore; the sinus rhomboidalis; the fate of the primitive 
streak; the formation of additional somites; the lengthening of the 
fore-gut; the appearance of the heart and the omphalomesenteric 
veins; organization in the area vasculosa. 


The Structure op Chicks Between Thirty-three and Thirty-nine 

Hours of Incubation 59 

The divisions of the brain and their neuromeric structure; the auditory 
pits; the formation of extra-embryonic blood vessels; the formation of 
the heart; the formation of intra-embryonic blood vessels. 


The Changes Between Forty and Fifty Hours of Incubation 75 

Flexion and torsion; the completion of the vitelline circulatory channels; 
the beginning of the circulation of blood. 


Extra-embryonic Membranes 80 

The folding of! of the body of the embryo; the establishment of the 
yolk-sac and the delimitation of the embryonic gut; the amnion and the 
serosa; the allantois. 


The Structure of Chicks from Fifty to Fifty-five Hours of In- 
cubation 93 

I. External Features. 
II. The Nervous System. 

Growth of the telencephalic region; the epiphysis; the in- 
fundibulum and Rathke's pocket; the optic vesicles; the lens; 
the posterior part of the brain and the cord region of the neural 
tube; the neural crests. 
HI. The Digestive Tract. 

The fore-gut; the stomodaeum; the pre-oral gut; the mid-gut; 
the hind-gut. 
IV. The Visceral Clefts and Visceral Arches. 
V. The Circulatory System. 

The heart; the aortic arches; the fusion of the dorsal aortse; the 
cardinal and omphalomesenteric vessels. 
VI. The Differentiation of the Somites. 
Vn. The Urinary System. 





The Development of the Chick During the Third and Fourth Days 

OF Incubation 109 

I. External Features. 

Torsion; flexion; the visceral arches and clefts; the oral region; 
the appendage buds; the allantois. 
II. The Nervous System. 

Summary of development prior to the third day; the formation 
of the telencephalic vesicles; the diencephalon; the mesen- 
cephalon; the metencephalon; the myelencephalon; the ganglia 
of the cranial nerves; the spinal cord; the spinal nerve roots. 

III. The Sense Organs. 

The eye; the ear; the olfactory organs. 

IV. The Digestive and Respiratory Systems. 

Summary of development prior to the third day; the establish- 
ment of the oral opening; the pharyngeal derivatives; the 
trachea; the lung-buds; the oesophagus and stomach; the 
liver; the pancreas; the mid-gut region; the cloaca; the procto- 
daeum and the cloacal membrane. 
V. The Circulatory System. 

The functional significance of the embryonic circulation; the 
vitelline circulation; the allantoic circulation; the intra-embry- 
onic circulation; the heart. 
VI. The Urinary System. 

The general relationships of pronephros, mesonephros, and 
metanephros; the pronephric tubules of the chick; the meso- 
nephric tubules. 
VII. The Coelom and Mesenteries. 


References for Collateral Reading 155 

Index 161 



The only method of attaining a comprehensive understanding 
of embryological processes is through the study and comparison 
of development in various animals. Many phases of the 
development of any specific organism can be interpreted only 
through a knowledge of corresponding processes in other 
organisms. The beginning student, however, must acquire his 
knowledge of embryology through intensive study of one form 
at a time, depending at first on older workers in the field for 
interpretation of the phenomena encountered. Building on 
the f amiharity with fundamental processes of development thus 
acquired, he may later broaden his horizon by the comparative 
study of a variety of forms. 

The chick is one of the most satisfactory animals on which 
student laboratory work in embryology may be based. Chick 
embryos in a proper state of preservation and of the stages 
desired can be readily secured and prepared for study. Used 
as the only laboratory material in a brief course they afford a 
basis for understanding the early differentiation of the organ 
systems and the fundamental processes of body formation 
common to all groups of vertebrates. In more extended courses 
where several forms are taken up, the chick serves at once as a 
type for the development characteristic of the large-yolked 
eggs of birds and reptiles, and as an intermediate form bridging 
the gap between the simpler processes of development in fishes 
and amphibia on the one hand and the more complex processes 
in mammals on the other. In medical school courses where a 
knowledge of human embryology is the end in view the chick 
not only makes a good stepping stone to the understanding of 
mammalian embryology, but also provides material for the 
study of early developmental processes not readily demon- 
strable in mammalian material. 

This book on the development of the chick has been written 


for those who are beginning the study of embryology and has 
accordingly been kept as brief and as uncomplicated as possible. 
Nevertheless it is assumed that the beginner in embryology 
will not be without a certain back-ground of zoological 
knowledge and training. He may reasonably be expected to 
be familiar with some of the aspects of evolution and heredity, 
with the recapitulation theory, the cell theory, the nature of 
the various types of tissues, and the more general phases of 
the morphology of vertebrates. Before laboratory work on 
the chick is begun in any course in embryology the nature of 
sexual reproduction, and the processes of gametogenesis, 
maturation, fertilization and cleavage, will have been taken 
up. It therefore seems unnecessary to include here any pre- 
liminary, general discussion of these phenomena. References 
for collateral reading on this and other phases of the subject 
are given in the appendix. 

Like other sciences embryology demands first of all accurate 
observation. It differs considerably, however, from such a 
science as adult anatomy where the objects studied are rela- 
tively constant and their component parts are not subject to 
rapid changes in their inter-relations. During development, 
structural conditions within the embryo are constantly chang- 
ing. Each phase of development presents a new complex of 
conditions and new problems. 

Solution of the problems presented in any given stage of 
development depends upon a knowledge of the stages which 
precede it. To comprehend the embryology of an organism 
one must, therefore, start at the beginning of its development 
and follow in their natural order the changes which occur. 
At the outset of his work the student must realize that proper 
sequence of study is essential and may not be disregard-ed. A 
knowledge of structural conditions in earlier stages than that 
at the moment under consideration, and an appreciation of the 
trend of the developmental processes by which conditions at 
one stage become transmuted into different conditions in the 
next, are direct and necessary factors in acquiring a real com- 
prehension of the subject. Without them the story of 
embryology becomes incoherent, a mere jumble of confused 

A knowledge of the phenomena of development is ordinarily 


acquired by studying a series of embryos at various stages of 
advancement. Each stage should be studied not so much for 
itself, as for the evidence it affords of the progress of develop- 
ment. In the study of embryology it does not suffice to acquire 
merely a series of *' still pictures" of various structures, however 
accurate these pictures may be. The study demands a constant 
application of correlative reasoning and an appreciation of the 
mechanical factors involved in the relations of various structures 
within the embryo to each other, and in the relation of the 
embryo as a whole to its environment. In order to really 
comprehend the embryological significance of a structure one 
must know not only its relations within the embryo being 
studied at the time, but also the manner in which it has been 
derived and the nature of the changes by which it is progressing 
toward adult conditions. To get absolutely the whole story it is 
obvious that one would have to study a series of embryos with 
infinitely small intervals between them. Nevertheless the 
fundamental steps in the process may be grasped from a much 
less extensive series. The fewer the stages studied, however, 
the more careful must one be to keep in mind the continuity 
of the processes and to think out the changes by which one stage 
leads to the next. 

The outstanding idea to be kept in mind by the student begin- 
ning the study of embryology is that the development of an 
individual is a process and that this process is continuous. The 
conditions he sees in embryos of various stages are of importance 
chiefly because they serve as evidence of events in the process 
of development at various intervals in its continuity, as his- 
torical events are evidences of the progress of a nation. Just 
as historical events are led up to by preparatory occurrences and 
followed by results which in turn affect later events, so in em- 
bryology events in development are presaged by preliminary 
changes and when consummated affect in turn later steps in 
the process. 

In certain respects the laboratory study of embryological. 
material involves methods of work for which courses in general 
zoology do not entirely prepare the student. Some general 
suggestions as to methods of procedure are, therefore, not out 
of place. 

In dissecting gross material it is not unduly difficult to- 


appreciate the complete relationships of a structure. The 
nature of embryological material, however, introduces new 
problems. Embryos of the age when the establishment of the 
various organ systems and processes of body formation are being 
initiated are too small to admit of successful dissection, but 
npt sufficiently small to permit of the satisfactory micro- 
scopical study of an entire embryo, except for its more general 
organization. To study embryos of this stage with any degree 
of thoroughness they must be cut into sections which are 
sufficiently thin to allow effective use of the microscope to 
ascertain cellular organization and detailed structural relation- 
ships. In preparing such material the entire embryo is cut into 
sections which are mounted on slides in the order in which 
they were cut. A sectional view of any region of the embryo 
is then available for study. 

While sections readily yield accurate information about local 
regions it is extremely difl&cult to construct a mental picture 
of any whole organism from a study of serial sections alone. 
For this reason it is necessary to work first on entire embryos 
which have been prepared by staining and clearing so they may 
be studied as transparent objects. From such preparations 
it is possible to map out the configuration of the body, and the 
location and extent of the more conspicuous internal organs. 
In this work the fact that embryos have three dimensions must 
be kept constantly in mind and the depth at which a structure 
lies must be determined as well as its apparent position in 
surface view. While conventionally entire chick embryos are 
represented in dorsal view, much additional information ma}^ be 
gained by following a study of the dorsal, with a study of the 
ventral aspect. Unless the preliminary study of entire embryos 
is carefully and thoroughly carried out the study of sections 
will yield only confusion. 

In studying a section of an embryo it is necessary first of all 
to determine its location. The plane of the section under 
consideration, and the region of the embryo through which it 
passes should be ascertained by comparing it with an entire 
embryo of the same age as that from which the section was cut. 
Only when the exact location of a section is known can the 
structures appearing in it be correlated with the organization of 
the embryo as a whole. Probably nothing in the study of 


embryology causes students more difficulties than neglect to 
locate sections accurately with the consequent failure to ap- 
preciate the relationships of the structures seen in them. Too 
great emphasis cannot be laid on the vital importance of fitting 
the structures shown by sections properly into the general 
scheme of organization as it appears in whole-mounts. It 
must by no means be inferred that the possibilities of the whole- 
mounts have been exhausted by the preliminary study accorded 
them before taking up the work on sections. | Further and more 
careful study of entire embryos should constantly accompany 
the study of serial sections. Many details which in the initial 
observation of the whole-mount were inconspicuous or abstruse 
will become significant in the light of the more exact information 
yielded by the sections. 

In the discussion of structures and processes in embryology, 
it is necessary to use terms designating location and direction 
which are referable to the body of the embryo regardless of the 
position it occupies. The ordinary terms of location, which are 
primarily referred to the direction of the action of gravity, 
such as above, over, under etc. are not sufficiently accurate. 
In gross human anatomy, there still persist many terms that 
are referred to gravity, and are therefore, because of the erect 
posture of man, not applicable to comparative anatomy or to 
embryology. The most confusing of these are anterior and 
posterior as used in gross human anatomy to mean, respec- 
tively, pertaining to the belly and to the back. In comparative 
anatomy and in embryology, anterior has reference to the head 
region and posterior to the tail region. The use of these terms 
in embryology in the sense usual in gross human anatomy 
is likely to lead to confusion and is entirely avoided in this 
book. The terms anterior and posterior have been replaced 
to a large extent by their less confusing synonyms, cephalic 
and caudal. 

In addition to the adjectives of position, such as dorsal, 
ventral, cephalic, caudal, mesial, lateral, proximal, distal, 
corresponding adverbs of motion or direction are commonly 
used in embryology. These adverbs are formed by adding the 
suffix -ad to the root of the adjective, as dorsad meaning toward 
the back, cephalad meaning toward the head, etc. These 
must not be used as adjectives of position but should be ap- 



plied only to the progress of processes, or to the extension of 
structures toward the part indicated by the root of the adverb. 
Cultivation of the use of correct and definite terms of posi- 
tion and direction in dealing with embryological processes will 
greatly aid accurate thinking and clear understanding. 



The ovarian ovum; maturation, ovulation, and fertiliza- 

THE ovum; the structure of the egg at the time of 
laying; incubation. 

The Ovarian Ovum. — The formation of the ovum, the phe- 
nomena of fertihzation, and the stages of development occurring 
prior to the laying of the egg have been more completely worked 
out in the pigeon than in the hen. The observations which 
have been carried out on the hen's egg indicate, as might be 
expected from the near relationship of the pigeon and the hen, 
that the processes in the two forms are closely comparable. 
The following account which is based chiefly on observations 
made on the pigeon's egg may, therefore, be taken to apply 
equally well in all essentials to the hen's egg. 

The part of the egg commonly known as the ''yolk" is a 
single cell, the female sex cell or ovum. Its great size as com- 
pared with other cells is due to the food material it contains. 
While the egg cell is still in the ovary, material which is later 
used by the embryo as food is deposited in its cytoplasm. This 
deposit which is known as deutoplasiii consists of a viscid fluid 
in which are suspended granules and globules of Various sizes. 
As the deutoplasm increases in amount the nucleus and the cyto- 
plasm are forced toward the surface so that eventually the 
deutoplasm comes to occupy nearly the entire cell. This 
abundance of deutoplasm accumulated in the ovum furnishes 
a readily assimilable food supply, which makes possible the 
extremely rapid development of the chick embryo. 

A section of the hen's ovary passing through a nearly mature 
ovum (Fig. i) shows the ovum and the tissues which surround 
it projecting from the ovary but connected to it by a constricted 
stalk of ovarian tissue. The protuberance containing the ovum 
is known as a follicle. The bulk of the ovum itself is made up of 




the yolk. Except in the neighborhood of the nucleus the active 
cytoplasm is but a thin film enveloping the yolk. About 
the nucleus a considerable mass of cytoplasm is aggregated. 
The region of the ovum containing the nucleus and the bulk of 
the active cytoplasm is known as the animal pole because this 
subsequently becomes the site of greatest protoplasmic activity. 
The region opposite the animal pole is called the vegetative 
pole because while material for growth is drawn from this 
region it remains itself relatively inactive. 

young follicle 

connective tissue 

stalk of follicle 

germinal epithelium 
of ovary 

white yolk 

yellow yolk 

cellular (granular) 
zone of follicle 

theca folliculi 

Fig. I. — Diagram showing the structure of a bird ovum still in the ovary. 
{Modified from Lillie, after Patterson.) The section shows a follicle containing 
a nearly mature ovum, together with a small area of the adjacent overian tissue. 

Enclosing the ovum is a thin non-cellular membrane, the 
vitelline membrane, which is a secretory product of the cyto- 
plasm of the ovum. Outside the vitelHne membrane and very 
difficult to differentiate from it, is another secreted membrane 
the zona radiata, so called because of its delicate radial stria- 
tions. Immediately peripheral to the zona radiata is an invest- 
ment of small polygonal cells, the cellular or ** granular" zone 
of the follicle, which is in turn enclosed in a highly vascular 
coat of connective tissue, the theca folliculi. The nutriment 
for the growing ovum is supplied by the mother from the prod- 


ucts of her digested food. It is brought in through the blood 
vessels of the theca, absorbed by the follicular cells and trans- 
ferred by them to the ovum. Within the ovum this material is 
elaborated into deutoplasm. 

Maturation, Ovulation and Fertilization. — When the full 
allotment of deutoplasm has accumulated in the ovum the 
nucleus undergoes its first maturation division. Maturation 
is a process occurring before fertilization, in which there is 
an equal mitotic division of the nucleus of the ovum but a 
markedly unequal division of the cytoplasm and its contents. 
y The result of this division is the formation of one very large cell 
containing the entire dower of deutoplasm and one very small 
cell containing practically no deutoplasm. This small cell is call- 
ed a polar body because it is budded off at the animal pole of the 
ovum. Since this unequal division of the ovum typically 
occurs twice we speak of the first and second 
maturation divisions and of the first and second 
polar bodies. 

In one of these maturation divisions the 
chromosomes do not split at the metaphase stage 
as happens in ordinary mitoses. Instead, half of 
the original number of chromosomes migrate 
bodily to each pole of the spindle, with the result 
that each daughter nucleus receives but half the 
number of chromosomes normal for the somatic 
cells of the species. Such a modified mitotic 
division is known as a reduction division. After 
the maturation divisions, one of which is a reduc- 
tion division, the nucleus of the ovum now ready 
for fertilization, is called the female pronucleus. 

Although maturation in the male sex cells 
differs in some respects from the maturation of 
the ovum, there also, a reduction division occurs. 
The result is that the nucleus of each matured 
cell contains but half the species number of chromo- 
somes. When in the process of fertilization the nucleus of the 
male cell unites with the female pronucleus the full species 
number of chromosomes is restored. 

At about the time of the first maturation division the follicle 
ruptures, and the liberated ovum passes into the oviduct. If 

Fig. 2.— 
S permatozoon 
of the pigeon. 
(After Ballo- 


insemination has taken place meanwhile, the spermatozoa 
(Fig. 2) make their way along the oviduct where for several 
days they may remain alive and capable of performing their 
function of fertilization. Penetration of the ovum by sperma- 
tozoa takes place in the region of the oviduct near the ovary, 
before the albumen and shell have been added to the ovum. 
Coincidently the second polar body is extruded. Although in 
birds normally several spermatozoa penetrate the ovum, only a 
single one unites with the female pronucleus. The fusion of the 
male and female pronuclei in fertilization initiates the develop- 
ment of the embryo and the cleavage divisions are begun while 
the ovum is passing through the oviduct toward the cloaca and 
receiving meanwhile its accessory coverings. 

The Formation of the Accessory Coverings of the Ovum. 
The albumen, the shell membrane, and the shell are non-cellular 
investments secreted about the ovum by the cells lining the 
oviduct. In the part of the oviduct adjacent to the ovary a 
mass of stringy albuminous material is produced. This ad- 
heres closely to the vitelline membrane and projects beyond 
it in two masses extending in either direction along the oviduct. 
Due to the spirally arranged folds in the walls of the oviduct, 
the egg as it moves toward the cloaca is rotated. This rotation 
twists the adherent albumen into the form of spiral strands pro- 
jecting at either end of the yolk, known as the chalazae (Fig. 
3). Additional albumen, which has been secreted abundantly 
in advance of the ovum by the glandular lining of the oviduct, 
is caught in the chalazae and during the further descent of the 
ovum is wrapped about it in concentric layers. These lamellae 
of albumen may be easily demonstrated in an egg which has had 
the albumen coagulated by boiling. The albumen secreting 
region of the oviduct constitutes about one-half of its entire 

The shell membranes which consist of sheets of matted 
organic fibers are added farther along in the oviduct. The 
shell is secreted as the egg is passing through the shell gland 
portion of the oviduct. The entire passage of the ovum from 
the time of its discharge from the ovary to the time when it is 
ready for laying has been estimated to occupy about 22 hours. 
If the completely formed egg reaches the cloacal end of the 
oviduct during the middle of the day it is usually laid at once, 


otherwise it is likely to be retained until the following day. 
This over night retention of the egg is one of the factors which 
accounts for the variability in the stage of development reached 
at the time of laying. 

The Structtire of the Egg at the Time of Laying. — The 
arrangement of structures in the egg at the time of laying 
is shown in Figure 3. Most of the gross relationships are 
already familiar because they appear so clearly in eggs which 
have been boiled. If a newly laid egg is allowed to float free 
in water until it comes to rest and is then opened by cutting 

nucleus of Pander _ blastoderm 

neck of latebra 

white yolk ^^55^..^ ^»^^^^v less dense albumen 

yeUow yolk^ 'vitelline membrane 

Pig. 3. — Diagram of the hen's egg in longitudinal section. (After Lillie.) 
The relations of the various parts of the egg at the time of laying are indicated 

away the part of the shell which lies uppermost, a circular 
whitish area will be seen to lie atop the yolk. In eggs which 
have been fertilized this area is somewhat different in appear- 
ance and noticeably larger than it is in unfertilized eggs. The 
differences are due to the development which has taken place in 
fertilized eggs during their passage through the oviduct. The 
aggregation of cells which in fertilized eggs lies in this area is 
known as the blastoderm. The structure of the blastoderm and 
the manner in which it grows will be taken up in the next 

Close examination of the yolk will show that it is not uniform 
throughout either in color or in texture. Two kinds of yolk 


can be differentiated, white yolk, and yellow yolk. Aside from 
the difference in color visible to the unaided eye, microscopical 
examination will show that there are differences in the granules 
and globules of the two types of yolk, those in the white yolk 
being in general smaller and less uniform in appearance. The 
principal accumulation of white yolk lies in a central flask- 
shaped area, the latebra, which extends toward the blastoderm 
and flares out under it into a mass known as the nucleus of 
Pander. In addition to the latebra and the nucleus of Pander 
there are thin concentric layers of white yolk between which lie 
much thicker layers of yellow yolk. The concentric layers of 
white and yellow yolk are said to indicate the daily accumula- 
tion of deutoplasm during the final stages in the formation of 
the egg. The outermost yolk immediately under the vitelline 
membrane is always of the white variety. 

The albumen, except for the chalazae, is nearly homogeneous 
in appearance, but near the yolk it is somewhat more dense 
than it is peripherally. The chalazae serve to suspend the yolk 
in the albumen. 

The two layers of shell membrane lie in contact everywhere 
except at the large end of the egg where the inner and outer 
membranes are separated to forni an air chamber. This 
space is stated (Kaupp) to appear only after the egg has 
been laid and cooled from the body temperature of the hen 
(about io6°F.) to the ordinary temperatures. In eggs which 
have been kept for any length of time the air space increases 
in size due to evaporation of part of the water content of 
the egg. This fact is taken advantage of in the familiar method 
of testing the freshness of eggs by "floating them." 

The egg shell is composed largely of calcareous salts. These 
salts are derived from the food of the mother and if lime con- 
taining substances are not furnished in her diet the shell is 
defectively formed or even altogether wanting. The shell is 
porous allowing the embryo to carry on exchange of gases with 
the outside air by means of specialized vascular membranes 
arising in connection with the embryo but lying outside it, 
directly beneath the shell. 

Incubation. — When an egg has been laid, development ceases 
unless the temperature of the egg is kept nearly up to the body 
temperature of the mother. Cooling of the egg does not, how- 


ever, lesult in the death of the embryo. It may resume its 
development if it is brooded by the hen or artificially incubated 
even after the egg has been kept for many days at ordinary 

The normal incubation temperature is that at which the egg 
is maintained by the body heat from the brood-hen. This is 
somewhat below the blood heat of the hen (io6°F.). When an 
egg is allowed to remain undisturbed the yolk rotates so that 
the developing embryo lies uppermost. Its position is then 
such that it gets the full benefit of the warmth of the mother. 

In incubating eggs artificially the incubators are usually 
regulated for a heat of ioo°-ioi°F. (37°-38°C.). At this 
temperature the chick is ready for hatching on the twenty-first 
day. Development will go on at considerably lower tempera- 
tures but its rate is retarded in proportion to the lowering of the 
temperature. Below about 21 degrees Centigrade develop- 
ment ceases altogether. 

In incubating eggs which have been cooled after laying for 
some particular stage of the embryo which it is desired to secure, 
three or four hours are ordinarily allowed for the egg to become 
warmed to the point at which development begins again. For 
example if an embryo of 24-hours incubation age is desired the 
egg should be allowed to remain in the incubator about 27 hours. 
Even with allowance made for the warming of the egg and with 
exact regulation of the temperature of the incubator, the stage of 
development attained in a given incubation time will vary 
widely in different eggs. The factor of individual variabiHty 
which must always be reckoned with in developmental proces- 
ses, undoubtedly accounts for some of the variation. The 
different time occupied by different eggs in traversing the ovi- 
duct, the over-night retention of eggs not ready for laying till 
toward sundown, and especially the varying time different eggs 
have been brooded before being removed from the nest, account 
for further variations. The designation of the age of chicks in 
hours of incubation is, therefore, not exact, but merely a con- 
venient approximation of the average condition reached in 
that incubation time. 



The effect of yolk on segmentation; the unsegmented 
blastodisc; the sequence and orientation of the 
cleavage division in birds. 

The Effect of Yolk on Segmentation. — Immediately after 
its fertilization the ovum enters upon a series of mitotic divisions 
which occur in close succession. This series of divisions 
constitutes the process of segmentation or cleavage. In birds 
segmentation takes place before the egg is laid, during the time 
it is traversing the oviduct. 

A mitotic division, whether it be a cleavage division of the 
ovum or the division of some other cell, is carried out by the 
active protoplasm of the cell. The food material stored in an 
egg cell as deutoplasm is non-living and inert. The deutoplasm 
has no part in mitosis except as its mass mechanically influences 
the activities of the protoplasm of the cell. It is obvious that 
any considerable amount of yolk will retard the division, or 
prevent the complete division, of the fertilized ovum. The 
amount and distribution of the yolk will therefore determine 
the type of segmentation. 

Figure 4 shows diagrammatically the manner in which the 
first cleavage division is carried out in three types of eggs 
having different relative amounts and different distributions of 
yolk and protoplasm. In the egg of Amphioxus the yolk is 
relatively meager in amount and fairly uniformly distributed 
throughout the cell. An ovum with such a yolk distribution is 
termed isolecithal (homolecithal). An isolecithal egg under- 
goes a type of cleavage which is essentially an unmodified 
mitosis. The yolk is not sufficient in amount, nor sufficiently 
localized to alter the usual mode of cell division. 

In Amphibia the ovum contains a considerable amount 
of yolk and the accumulation of the yolk at one pole has crowded 
the nucleus and active cytoplasm of the ovum toward the 
opposite pole. An egg in which the yolk is thus concentrated 




at one pole is termed telolecithal. Cleavage in such an egg is 
initiated at the animal pole where the nucleus and most of the 

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active cytoplasm are located. The division of the nucleus is a 
typical mitotic division. The division of the cytoplasm is 
effected rapidly at the animal pole of the egg where the active 


cytoplasm is aggregated. When, however, the yolk mass is 
encountered, the process is greatly retarded. So slowly, in 
fact, is the division of the yolk accomplished, that succeeding 
cell divisions begin at the animal pole of the egg before the first 
cleavage is completed at the vegetative pole. 

The eggs of birds are also telolecithal, but the amount of 
yolk which they contain is both relatively and actually much 
greater than that in Amphibian eggs. Cleavage in bird's eggs 
begins as it does in the eggs of Amphibia, but the mass of the 
inert yolk material in them is so great that the yolk is not 
divided. The process of segmentation is limited to the small 
disc of protoplasm lying on the surface of the yolk at the animal 
pole, and is for this reason referred to as discoidal cleavage 
(Fig. 5). The fact that the whole egg is not divided is indicated 
by designating the process as partial (meroblastic) cleavage 
in distinction to the complete cleavage (holoblastic) seen in 
eggs containing less yolk. The cells formed in the process of 
segmentation are known as blastomeres whether they are com- 
pletely separated as results in holobastic cleavage or only 
partially separated as results in meroblastic cleavage. 

The Unsegmented Blastodisc. — In the egg of a bird which is 
about to undergo cleavage, the disc of active protoplasm at the 
animal pole (blastodisc) is a whitish, circular area about three 
millimeters in diameter. The central portion of the blastodisc 
is surrounded by a somewhat darker appearing marginal area 
known as the periblast. The protoplasm of the blastodisc, 
especially in the periblast region, blends into the underlying 
white yolk so that it is difficult to make out any line of demarca- 
tion between the two. It is in the central area of the blasto- 
disc that cleavage furrows first appear. Neither the nuclei 
resulting from the early cleavages nor the cleavage furrows 
invade the marginal periblast until very late in the process of 

The Sequence and Orientation of the Cleavage Divisions in 
Birds. — The nature of the series of divisions in the meroblastic, 
discoidal cleavage characteristic of the eggs of birds is largely 
determined by the amount and distribution of the yolk. An- 
other determining factor is the tendency of mitotic spindles to 
develop so that the long axis of the spindle lies at right angles 
to the axis of least dimension of the mass of unmodified cyto- 
plasm. The cleavage furrow always arises at right angles to 


the long axis of the mitotic spindle. Figure 5 shows the succes- 
sion of the cleavage divisions in the egg of the pigeon. The 
diagrams represent surface views of the blastodisc and an area 
of the surrounding yolk, the shell and albumen having been 
removed. The observer is looking directly at the animal pole. 
Figure 5, ^, should be compared with Figure 4. The diagrams 
of Figure 4 are of sections cut in a plane which passes vertically 
through the blastodisc and which is at right angles to the plane 
of the first cleavage (Fig. 5, A, I-I). The first cleavage furrow 
cuts into the egg in a plane coinciding with the imaginary axis 
passing through the animal pole and the vegetative pole. The 
two daughter cells or blastomeres resulting from the first 
cleavage are not completely walled off but each remains 
unseparated from the underlying yolk (Fig. 4). 

In each of the two blastomeres resulting from the first cleav- 
age division, mitotic spindles initiating the second cleavage arise 
at right angles to the position which was occupied by the first 
cleavage spindle. This determines that the two second cleav- 
age furrows will be at right angles to the first. Since these 
two second cleavage furrows lie in the same plane and are 
apparently continuous they are usually considered together. 
They mark the position of the second cleavage plane which cuts 
the egg in the animal- vegetative axis but which lies at right 
angles to the first cleavage plane (Fig. 5, B, II-II). A very 
good way of getting a clear conception of the orientation of the 
ojeavage planesJs to cut them in an apple. Let the core of the 
apple represent the animal- vegetative axis of the egg. The first 
cleavage furrow can be represented by notching the apple 
lengthwise, that is as one ordinarily starts to split an apple into 
halves. The second cleavage furrow can be represented by 
cutting into the apple again in a plane passing through the 
axis of the core, but at right angles to the first cut, as one would 
start to quarter the apple. 

The third cleavage furrows are variable in number and in 
position. In the most typical cases each of the four blastomeres 
established by the first two cleavages divides again so that eight 
blastomeres are formed (Fig. 5, C). Frequently, however, the 
third cleavage appears at first in only two of the blastomeres, 
so that six cells result instead of eight. 

The fourth series of cleavages takes place in such a manner 



Fig. 5. — Surface aspect of blastoderm at various stages of cleavage. {Based 
on Blount's photomicrographs of the pigeon's egg.) The blastodenn and the 
immediately surrounding yolk are viewed directly from the animal pole, the 
shell and albumen having been removed. The order in which the cleavage 
furrows have appeared is indicated on the diagrams by Roman numerals. 

A, first cleavage; B, second cleavage; C, third cleavage; D, fourth cleavage; 
£, fifth cleavage; F, early morula. 


that the central (apical) ends of the eight cells established by 
the third cleavage are cut off from their peripheral portions. 
The combined contour of the fourth cleavage furrows forms a 
small irregularly circular furrow the center of which is the point 
at which the first two cleavage planes intersect (Fig. 5, D). 
The central cells now appear completely separated in a surface 
view of the blastoderm, but sections show them still unseparated 
from the underlying yolk. 

After the fourth, the succession of cleavages becomes irregular. 
In surface view it is possible to make out cleavage furrows that 
divide off additional apical cells, and other, radial furrows that 
further divide the peripheral cells. Figure 5, E and F, show the 
increase in number of cells and their extension out over the 
surface of the yolk, resulting from the succession of cleavages. 
When the process of segmentation has progressed to the stage 
in which the succession of cleavages is irregular and the number 
of cells considerable, the term blastoderm is applied to the entire 
group of blastomeres formed by the cleavage of the blastodisc.^ 

In addition to the cleavages which are indicated on the sur- 
face, at about the 3 2 -cell stage sections show cleavage planes of 
an entirely different character. These cleavages appear below 
the surface and parallel to it. They establish a superficial layer 
of cells which are completely delimited. These superficial 
cells rest upon a layer of cells which are continuous on their deep 
faces with the yolk. Continued divisions of the same type 
eventually establish several strata of superficial cells. This 
process appears first in the central portion of the blastoderm. 
It progresses centrifugally as the blastoderm increases in size 
but does not extend to its extreme margin. The peripheral 
margin of the blastoderm remains a single cell in thickness and 
the cells there lie unseparated from the yolk. 

1 While but a single spermatozoon takes part in fertilization other spermatoza 
become lodged in the cytoplasm of the blastodisc. The nuclei of these sperma- 
tozoa migrate to the peripheral part of the blastoderm where they are recog- 
nizable for some time as the so-called accessory sperm nuclei. Some of them 
appear to undergo divisions which are accompanied by slight indications of 
division in the adjacent cytoplasm. The short superficial grooves thus formed 
are termed accessory cleav^age furrows. No cells are formed by the accessory 
"cleavages." The sperm nuclei soon degenerate, the superficial furrows fade 
out, and usually as early as the 3 2 -cell stage all traces of the process have dis- 
appeared without, as far as is known, affecting in any way the development of 
the embryo. 


The morula stage; the formation of the blastula; the 
effect of yolk on gastrulation ; gastrulation in 


The Morula Stage. — It should by no means be inferred that 
cell division ceases with the cleavage divisions. The end of the 
segmentation stage is not marked by even a retardation in the 
succession of mitoses. Segmentation is regarded as ending when 
the progress of development ceases to be indicated merely by 
increases in the number of cells, and begins to involve locaHzed 
aggregation and differentiation of various groups of cells. 
Development progresses from phase to phase without abrupt 
change or interruption. The nomenclature and limitation of 
the various phases of development are largely arbitrary and the 
use of terms designating phases or stages of development should 
not be allowed to obscure the fact that the whole process is a 
continuous one. 

In eggs without a large amount of yolk, segmentation results 
in the formation of a rounded, closely packed mass of blasto- 
meres. This is known as a morula from its resemblance to the 
mulberry fruit which is in form much like the more familiar 
raspberry or blackberry. At the end of segmentation the 
chick embryo has arrived at a stage which corresponds with the 
morula stage of- forms with less yolk. It consists of a disc- 
shaped mass of cells several strata in thickness, the blastoderm, 
lying closely appUed to the yolk. In the center of the blasto- 
derm the cells are smaller and completely defined; at the per- 
iphery the cells are flattened, larger in surface extent, and are 
not walled off from the yolk beneath. 

The Formation of the Blastula. — The morula condition is of 
short duration. Almost as soon as it is established there begins 
a rearrangement of the cells presaging the formation of the 
blastula. A cavity is formed beneath the blastoderm by the 



detachment of its central cells from the underlying yolk while 
the peripheral cells remain attached. The space thus estab- 
lished between the blastoderm and the yolk is termed the seg- 
mentation cavity (blastocoele). The marginal area of the 
blastoderm in which the cells remain undetached from the yolk , 
and closely adherent to it, is called the zone of junction. With 
the establishment of the blastocoele the embryo is said to have 
progressed from the morula to the blastula stage. 

Figure 7, D, shows the conditions seen on sectioning the 
blastula of a bird. Only the blastoderm and the immediately 
underlying yolk are included in the diagram. At this mag- 
nification the complete yolk must be imagined as about three 
feet in diameter. The structure of the bird embryo in these 
stages may be brought in line with the morula and blastula 
stages of forms having little yolk if the full significance of the 
great yolk mass is appreciated. Instead of being free to aggre- 
gate first into a solid sphere of cells (morula) and then into a 
hollow sphere of cells (blastula), as takes place in forms with ^ 
little yolk, the blastomeres in the bird embryo are forced 
to grow on the surface of a large yolk sphere. Under 
such mechanical conditions the blastomeres are forced to be- 
come arranged in a disc-shaped mass on the surface of the yolk. 
If one imagines the yolk of the bird morula removed, and the 
disc of cells left free to assume the spherical shape dictated by 
surface tension its comparability with the morula in a form 
having little yolk becomes apparent. 

The process of blastulation also is modified by the presence 
of a large amount of yolk. There can be no simple hollow 
sphere formation by rearrangement of the cells if the great 
bulk of the morula is inert yolk. But the cells of the central 
region of the blastoderm are nevertheless separated from the 
yolk to form a small blastocoele. The yolk constitutes the 
floor of the blastocoele and at the same time by reason of its. 
great mass nearly obliterates it. If we imagine the yolk 
removed from the blastula and the edges of the blastoderm 
pulled together the chick blastula approaches the form of the 
blastula in embryos with little yolk. 

The Effect of Yolk on Gastnxlation. — The process of gastrula- -^ 
tion begins as soon as blastulation is accompHshed. Gastrula- 
tion as it occurs in birds is not difiicult to understand if one 



grasps its fundamental similarity to the corresponding process 
in forms with scanty yolk. In Amphioxus, gastrulation is an 
inpocketing of the blastula (Fig. 6). A double layered cup is 
formed from a single layered hollow sphere much as one might 




Auu^^' .^•~S<^^^"^atic diagrams to show the effect of yolk on gastrulation. 
Abbreviations: blc, blastocoele; bid., blastoderm; blp., blastopore; ect., ectoderm; 
ent., entoderm; mit., cell undergoing mitosis; yk., yolk; vk.g., yolk granules: 
yk.p.. yolk plug. 

push in a hollow rubber ball with the thumb. The new cavity 
in the double walled cup is termed the gastrocoele. The open- 
inir from the outside into the gastrocoele is called the blastopore. 


In gastrulation the single cell layer of the blastula is doubled 
upon itself to form two layers. The outer cell layer is known 
as the ectoderm and the inner layer as the entoderm. These 
layers differ from each other in their positional relationship to 
the embryo and to the surrounding environment. Each has 
different functional potentiaHties and each will in the course of 
development give rise to quite different types of structures and 
organs. It is the importance of their later history rather than 
any complexity or veiled significance about the way in which 
they arise that attaches such importance in embryology to the 
establishment of these two layers. 

In the gastrulation of Amphibian embryos (Fig. 6) the yolk 
forces the invagination of the blastoderm toward the animal 
pole, but the inpocketing takes place into the blastocoele and 
the interrelationships of ectoderm, entoderm, and gastrocoele 
are established in fundamentally the same way as in Amphioxus. 

Gastrulation in birds is greatly modified by the large amount 
of yolk present (Fig. 6). Infolding must be effected in a disc 
of cells resting like a cap on a large yolk sphere. The smallness 
of the blastocoele sharply restricts the space into which the 
invagination can grow. Instead of arising as a relatively 
large circular opening the blastopore appears as a crescentlc 
slit at the margin of the blastoderm. The crescentic blastopore 
may be regarded as a potejitially circular opening which has 
been flattened as it develops between the growing disc of cells 
and the unyielding yolk which underhes them. The invagi- 
nated pocket of entoderm which grows in from this compressed 
blastopore is also flattened, conforming to the restrictions 
of the shape and size of the blastocoele. Moreover the floor 
of the invagination is represented only by a few widely scattered 
cells lying upon the yolk. It is as if the lower layer in its in- 
growth was impeded and broken up by the yolk. The scattered 
cells representing the floor of the invagination soon disappear and 
the yolk itself comes to constitute the floor of the gastrocoele. 
Notwithstanding the great displacement of the blastopore and 
the gastrular invagination toward the animal pole ajid the 
restricted size and incomplete floor of the gastrocoele, the cell 
layers and the cavity established can be homologized with the 
corresponding features in forms where the course of develop- 
ment has not been so extensively modified by yolk. 


A comparative review of the diagrams of Figure 6 will afford 
a general understanding of the infolding process of gastrulation. 
These diagrams aim to convey merely the scheme of the process. 
They are therefore simplified and emphasize the similarities 
of gastrulation in forms with widely varying amounts of yolk, 
rather than the details of the process in any one form. With 
this general groundwork we may now profitably return to the 
blastula stage and consider in somewhat more detail the process 
of gastrulation as it occurs in birds. 

Gastrulation in Birds. — We have already estabhshed the 
blastula as a disc of cells lying on the yolk but separated from it 
centrally by a flattened blastoccele or segmentation cavity. 
The peripheral part of the blastoderm where the marginal cells 
lie unseparated from the yolk has been termed the zone of 
junction (Fig. 7, Z^). This part of the blastoderm is also called 
the area opaca because in preparations made by removing the 
blastoderm from the yolk surface, yolk adheres to it and renders 
it more opaque. This opacity is especially apparent when a 
preparation is viewed under the microscope by transmitted 
light. The central area of the blastoderm, because it is sepa- 
rated from the yolk by the segmentation cavity, does not bring 
a mass of adherent yolk with it when the blastoderm is removed. 
It is for this reason translucent and is called the area pellucida. 
The area opaca later becomes differentiated so that three more 
or less distinct zones may be distinguished: (i) a peripheral 
zone known as the margin of overgrowth where rapid prolifera- 
tion has pushed the cells out over the yolk without their becom- 
ing adherent to it; (2) an intermediate zone known as the zone 
of junction in which the deep-lying cells do not have complete 
cell boundaries but constitute a syncytium blending without 
definite boundary into the superficial layer of white yolk and 
adhering to it by means of penetrating strands of cytoplasm; 
(3) an inner zone known as the germ wall made up of cells 
derived from the inner border of the zone of junction which have 
acquired definite boundaries and become more or less free from 
the yolk. The cells of the germ wall usually contain numerous 
small yolk granules which were enmeshed in their cytoplasm 
when they were, as cells of the zone of junction, unseparated 
from the yolk (Fig. 7, By E). The inner margin of the germ 
wall marks the transition from area opaca to area pellucida. 


The changes in the blastula which indicate the approach of 
gastrulation are, first, a thinning of the blastoderm at its caudal 
margin and, second, freeing of the blastoderm from the yolk 

in the same region (Fig. 7, Z)). The separation of the blasto- 
derm from the yolk is evidenced in surface views by a crescentic 
gap in the posterior quadrant of the zone of junction (Fig. y, A). 


This region where the blastoderm is thin and free from the yolk 
marks the position of the blastopore. 

Gastrulation begins with the undertucking of the cells at the 
free margin of the blastoderm. Figure 7, B, is a diagrammatic 
surface view of the blastoderm represented as a transparent 
object. The position and the extent of the invaginated ento- 
derm seen through the overlying ectoderm are indicated by 
the cross hatched area. The appearance of the blastopore 
locates the caudal region of the future embryo and permits the 
definition of its longitudinal axis. This axis is indicated by the 
line b-b on Figure 7, B. A diagram of a section cut in the 
longitudinal axis and passing through the blastopore of an 
embryo of this stage is shown in Figure 7, E. The invaginated 
cells which constitute the entoderm form a layer extending 
cephalad from the thickened lip of the blastopore. The yolk 
forms the floor of the gastroccele. Figure 7, C, is a diagrammatic 
surface-view of a later stage in the same process. The extent 
of the entoderm is marked by cross-hatching as in the diagram 
of the previous stage. The undertucking of the cells at the 
blastopore has ceased by this time, and as indicated in Figure 
7, C. by the black area, and in Figure 7, F, by the solid mass of 
cells seen in section, the blastopore has become closed. 

During the entire time that the process of gastrulation has 
been in progress there has been constant cell proliferation going 
on in the blastoderm as a whole. The growth of the blastoderm 
has been evidenced especially by increase in its surface extent 
which has resulted in a general spreading of its peripheral mar- 
gins over the yolk. This extension has taken place uniformly 
at all parts of the margin except in the posterior quadrant where 
the blastopore is located. Here the cells proliferated, instead 
of spreading out over the yolk have turned in at the lip of the 
blastopore to form the invaginated entoderm. This particular 
part of the margin of the blastoderm, having contributed the 
cells formed in its growth to the entoderm which grows back 
toward the center of the blastoderm, takes no part in the 
general peripheral expansion. As a result the blastopore region 
is, as it were, left behind and the rapidly extending margin of 
the blastoderm on either side sweeps around and encloses it. 
The blastopore at the time of its closure thus comes to lie 
within the recompleted circle of the germ wall (Fig. 7, C). 



The location and appearance of the primitive streak; 
the origin of the primitive streak by- concrescence 


The Location and Appearance of the Primitive Streak. 

The stages of development described in the preceding chapters 
take place before the egg is laid. The first conspicuous struc- 
tural feature to make its appearance in the embryo after the 
laying of the egg is the primitive streak. In eggs that have been 
incubated about i6^hours the primitive streak is well developed 

cephalic end 

Hensen's node 
area pellucida 

area opaca 

primitive pit 

primitive groove 

primitive ridge 

Fig. 8. 

■Dorsal view ( X 14) of entire chick embryo in the primitive streak stage 
(about 16 hours of incubation). 

as a linear groove flanked on either side by ridge-like thickenings, 
extending from the inner margin of the area opaca to approxi- 
mately the center of the blastoderm (Fig. 8). The primitive 
streak Hes in the longitudinal axis of the future embryo. The 
end adjacent to the area opaca is its posterior (caudal) end, 
the opposite extremity is its anterior (cephalic) end. The ce- 



phalic end of the primitive groove is deepened and often some- 
what expanded to form a depression known as the primitive pit. 
Directly anterior to the primitive pit the right and left primitive 
folds merge with each other in the mid-line to form a small 
rounded elevation called Hensen's node. Hensen's node is of 
importance as a landmark rather than because it gives rise to 
any particular structure. 

As early as the beginning of gastrulation the shape of the 
blastoderm responds to local inequality in the rate of growth. 
One of the early manifestations of differential growth is the 
more rapid extension of the embryo cephalad than either 
laterad or caudad. This results in a definite elongation in 
the antero-posterior axis by the time the primitive streak is 
established (Fig. 8). 

The Origin of the Primitive Streak by Concrescence of the 
Blastopore. — The significance of the primitive streak has been 
the subject of much controversy. The divergences of opinion 
have been due chiefly to incomplete knowledge of the stages 
of development passed through prior to the laying of the egg. 
Our present knowledge of these early stages is, however, suffi- 
cient to furnish the basis of an interpretation of the primitive 
streak which is now widely accepted. This interpretation is 
outlined below without reference to other, opposed views. 

The primitive streak is to be regarded as a scar-like thicken- 
ing arising from the fusion of the edges of the anterior lip of the 
blastopore. To understand the origin of the longitudinally 
placed primitive streak from the marginally located, crescentic 
blastopore it is necessary to follow carefully the growth proc- 
esses taking place during the closure of the blastopore. 

We have already seen how the ingrowth of entoderm from 
the anterior lip of the blastopore, caused the blastopore to lag 
behind the other parts of the margin of the blastoderm in the 
process of radial extension over the yolk surface. During this 
process the blastopore is compressed from either side toward 
the mid-line by the rapidly extending margins of the blastoderm 
adjacent to it and is eventually encompassed by them (see 
Chap. IV and Fig. 7). Because of the insweeping, converging 
tendency of the growth which first causes the blastopore to be 
laterally compressed and finally causes its margins to grow 
together the process has been termed concrescence. 



A schematic interpretation of four steps in the concrescrnce 
of the margins of the blastopore is given in the diagrams of 
Figure 9. The blastoderm shown in surface- view plan in 
Figure 9, ^, is approximately at the same stage of gastrulation as 
that indicated in Figure 7, B. To avoid complicating the 
diagarm, the entoderm has not been shown in Figure 9. Num- 
bers have been placed along the lip of the blastopore to facilitate 

marginal notch 

Fig. 9. — Schematic diagrams to illustrate the concrescence theory of the origin 
of the primitive streak. {After Lillie.) For explanation see text. 

following the changes in position undergone by the points to 
which they are affixed. As the margins of the blastoderm 
adjacent to the blastopore grow, they tend to converge in the 
direction indicated by the arrows in Figure g, B. The anterior 
lip of the blastopore is folded on itself by this converging growth. 
The middle point of the lip, i, comes to lie within the margin of 
the blastoerdm, and points, 2, 2, which formerly lay laterally are 


brought into apposition in the mid Hne. Figures C, and D, 
show how, by the continuation of the same converging growth, 
the edges of the blastopore are folded together into a line of 
fusion at right angles to the Original marginal position of the 
blastopore. At the completion of concrescence, the germ wall of 
the blastoderm has coalesced posterior to the blastopore leaving 
the line along which the blastopore lips have fused within the 
area pellucida. The non-committal term primitive streak was 
given to this structure before its origin by fusion of the lips of 
the blastopore was suspected. 

The Formation of the Mesodenn. — In its early condition the 
primitive streak is a scarcely recognizable thickening of the 
blastoderm marking the line of fusion of the hps of the blasto- 
pore. The well defined groove with thickened ridges on either 
side, seen in chicks of 15 to 1 6 hours incubation, is a later devel- 
opment. A new process, the formation of the mesoderm, is 
taking place at this region and the change in the configuration 
of the primitive streak is its outward manifestation. It will 
be recalled that the lip of the blastopore is in all forms a region 
of rapid cell proHferation. It is a region from which we can 
trace the addition of cells to the differentiated germ layers, but 
it is itself indifferent. Ectoderm and entoderm both merge 
into this indifferent area at the lip of the blastopore. It is 
impossible to fix, except arbitrarily, where ectoderm begins and 
entoderm ends. Later when the mesoderm appears, we can 
trace the origin of its cells directly or indirectly to the same 
area of indifferent, rapidly prohferating cells. It is therefore 
wholly in Hne with the embryology of other forms to find the 
mesoderm of the chick arising at the fused lips of the blastopore. 

The manner in which the mesoderm arises can be understood 
only by the study of sections or diagrams of sections. Figure 
10, A, represents schematically the conditions which would be 
seen in a section cut in the hne h-h across the marginal notch 
of an embryo of the stage depicted in Figure 9, B. The mar- 
gins of the blastopore at the point where this section is located 
have been folded so they lie in close proximity to each other. 
A Httle later they would be fused as shown in Figure 10, B. 
At the region of fusion, that is to say at the primitive streak, 
the entoderm and ectoderm merge in a mass of rapidly dividing 
cells (Fig. 13, Z>). A section across the primitive streak at a 



somewhat later stage (Fig. 10, C) shows cells extending to 
either side of the undifferentiated cell mass, between the ecto- 
derm and the entoderm. These cells are the primordium of 
the third of the germ layers, the»mesoderm. The outgrowth of 
the mesoderm and the median depression in the primitive streak 
appear synchronously. This median depression in the primi- 
tive streak is the primitive groove. It is not unhkely that the 
formation of the primitive groove is due to cell rearrangement 

lips of blastopore 


y^jj ^^-'"■^ I ^*^~ entodenn 

primitive g;ut 


primitive gut 

primitive groove 

Fig. 10. — Diagrams showing schematically the relations of the germ layers 
during the formation of the primitive streak by concrescence of the margins of 
the blastopore. A, hypothetical section of blastoderm at the stage represented 
in Fig. 9, B. The plane of the section is indicated by the line h-h Fig. 9, B. 
B, hypothetical section of blastoderm at the stage represented in Fig. 9, D. 
The plane of the section is indicated by the line d-d. Fig. 9, D. C, schematic 
transverse section through the primitive streak at the stage represented in 
Fig. 8. 

in this region entailed by the rapid outgrowth of the cells con- 
stituting the mesoderm. (See arrows in Figure lo, C.) 

With the formation of the mesoderm the chick has estab- 
lished the three germ layers characteristic of all vertebrate 
embryos. The importance of these layers lies in the uniformity 
of their origin and history. From them the development of all 
the organ systems may be traced. The ectoderm gives rise to 


the outer epithelial covering of the body and its derivatives 
(feathers, claws, skin glands, etc.) , the nervous system, and the 
sense organs. The entoderm gives rise to the epithelial lining 
of the digestive tube and of the respiratory organs and the 
epitheHum of their associated glands. The mesoderm becomes 
differentiated to form the fibrous and rigid connective tissues 
(except neuroglia) the muscle, the epithelial lining of the body 
cavities, the organs of the circulatory system, the* blood, the 
lymphatic organs and the major part of the urino-genital 
system of the adult. 



The primitive streak as a center of growth; the growth 
of the entoderm and the establishment of the 


The Primitive Streak as a Center of Growth. — The impor- 
tance of the primitive streak embryologically, is due chiefly to the 
way it is involved in the estabHshment of the germ layers. 
Representing as it does the fused lips of the blastopore it marks 
the location of entoderm invagination. The mesoderm also 
arises at the primitive streak region. The general appearance 
and the location of the primitive streak are both well shown in 
embryos of i6 hours of incubation (Fig. 8). In embryos which 
have been incubated i8 hours (Fig. ii) the primitive streak is 
still the most conspicuous feature. Structurally it is little 
changed from the conditions seen in 1 6-hour chicks, but it appears 
to be somewhat more caudally located. In 21 to 2 2 -hour em- 
bryos (Fig. 14) the primitive streak lies still farther caudal in 
the blastoderm. Its change in position is relative rather than 
actual. The apparent change in the position of the primitive 
streak is due to the fact that growth is taking place more rapidly 
cephalic to it than caudal to it. This tendency is in evidence 
throughout the early growth of the embryo. The cephalic 
region is precocious in development. As development pro- 
gresses we shall find the primitive streak occupying a constantly 
more posterior position in the body and being more and more 
overshadowed by the greater growth of the structures lying 
cephalic to it. 

The structure of the primitive streak region is best shown 
by transverse sections. In the sections diagrammed in Figure 
3 . 33 



13, a different conventional scheme of representation has been 
employed to indicate each of the germ layers. The ectoderm is 
vertically hatched, the cells of the mesoderm are represented 
by heavy angular dots when they are isolated or by solid black 
lines when they lie arranged in the form of compact layers, 
and the entoderm is represented by fine stippHng backed by a 
single line. This same conventional representation of the 
different germ layers is observed in all diagrams of sections in 

anterior border 
of mesoderm 

neural plate. 

embryonal area ■ 

area pellucida- 
area opaca 


-Hensen's node 

'primitive streak 

caudal end 
Pig. II. — Dorsal view ( X 14) of entire chick embryo of 18 hours incubation. 

order to facilitate following the way in which the organ systems 
of the embryo are constructed from the germ layers. Details 
of cell structure are for the most part omitted with the expecta- 
tion that the student will acquire a knowledge of them in his 
own study of sections. The plane in which each of the sections 
diagrammed passes through the embryo is indicated by a line 
drawn on a small outline sketch of an embryo of corresponding 
stage. For interpretation these outline sketches should be 
compared with actual specimens or detailed drawings of entire 
embryos of the same stage of development. 

In embryos of the stage under consideration the relationship 
of the germ layers at the primitive streak still indicates their man- 
ner of derivation (Fig. 13, C and D). The ectoderm and the 


entoderm are continuous with each other without any demarca- 
tion. The mesoderm arises from the primitive streak where 
ectoderm and entoderm merge and grows laterad on both sides of 
the primitive streak extending into the space between ectoderm 
and entoderm. The mass of cells in the floor of the primitive 
groove is to be regarded as constituting an undifferentiated area 
from which new cells are being proUferated rapidly and are 
emigrating to become components of one or another of the germ 

To those who have studied the embryology of more primitive 
vertebrates, particularly the Amphibia, the fact that the lips 
of the blastopore constitute centers of growth from which cells 
are pushed forth to take part in the formation of the differenti- 
ated germ layers will already be famiHar. The fact that the 
blastopore of the chick has suffered a change in position due to 
concrescence, and has in the same process become closed by 
fusion of its Ups must not be allowed to obscure its homologies. 
In attempting to bring the relationships of the germ layers in 
the chick into Hne with the relationships of the germ layers in 
embryos having less yolk, it will be of great assistance to picture 
a chick lifted off the yolk and the lateral margins of the blasto- 
derm pulled together ventrally; or, the method of comparison 
may be reversed if one imagines the embryo of a form having 
less yolk, such as an amphibian, to be split open along the mid- 
ventral line and spread out on the surface of a sphere as a chick 
lies on the yolk. 

In Figure 13, D, a small region at the primitive streak has 
been drawn at higher magnification to show the characteristic 
cellular structure of the undifferentiated region in the floor of 
the primitive groove and of the various layers merging at this 
place. The cells of the ectoderm are much more closely packed 
together and more sharply delimited than those of the other 
germ layers. Where the ectoderm is thickened in the primitive 
ridge region, it is several cell layers thick (stratified). (Fig. 13, 
D.) In regions lateral to the primitive ridge it gradually be- 
comes thinner until it consists of but a single cell layer (Fig. 13, 
E). The rapid extension that the mesoderm is at this time 
undergoing is indicated by the loose arrangement and sprawling 
appearance of its cells. Their irregular cytoplasmic processes, 
make them look much Hke amoebae fixed during locomotion. 


The cells of the entoderm are neither as closely packed nor as 
clearly defined as are the ectoderm cells. Nevertheless, in 
contrast to the condition of the mesoderm at this stage, the 
entoderm cells form a definite, unbroken layer. 

The Growth of the Entoderm and the Establishment of 
the Primitive Gut. — Sections of embryos of this stage show 
how the entoderm has spread out and become organized into a 
coherent layer of cells merging peripherally with the inner mar- 
gin of the germ wall and overlapping it to a certain extent 
(Fig. 13, C, E, F). The cavity between the yolk and the ento- 
derm which has been called the gastrocoele is now termed the 
primitive gut. The yolk floor of the primitive gut does not 
show in sections prepared by the usual methods. The reasons 
for this are to be found in the relations of the embryo to the 
yolk before it is removed for sectioning. In the entire central 
region of the blastoderm the yolk is separated from the ento- 
derm by the cavity of the primitive gut. When the embryo is 
removed from the yolk sphere the yolk floor of the primitive 
gut, not being adherent to the blastoderm, is left behind. In 
contrast the peripheral part of the blastoderm lies closely ap- 
pHed to the yolk. Some yolk adheres to this part of the blasto- 
derm when it is removed. This adherent yolk is shown in the 
section diagrams of Figure 13. Its presence clearly indicates 
why this region (area opaca) appears less translucent in surface 
views of entire embryos. 

In embryos of 18 hours the primitive gut is a cavity with 
a flat roof of entoderm and a floor of yolk. Peripherally it is 
bounded on all sides by the germ wall (Fig. 13, C, F). The 
merging of the cells of the entoderm with the yolk mass is 
shown in the small area of the germ wall drawn to a high mag- 
nification in Figure 13, £. In the germ wall cell boundaries 
are incomplete and very difiicult to distinguish but nuclei can 
be made out surrounded by more or less definite areas of cyto- 
plasm. This cytoplasm contains numerous yolk granules in 
various stages of absorption. It will be recalled that the nuclei 
of the germ wall arise by division from the nuclei of cells lying 
at the margins of the expanding blastoderm. They appear to 
be concerned in breaking up the yolk in advance of the ento- 
derm as it is spreading about the yolk sphere. 

About the twenty-second hour of incubation indications can 


be seen of a local differentiation of that region of the primitive 
gut which underHes the anterior part of the embryo. By focus- 
ing through the ectoderm in the anterior region of a whole- 
mount of this age a pocket of entoderm can be seen (Fig. 14). 
This entodermal pocket is the first part of the gut to acquire a 
floor, other than the yolk floor, and is called from its anterior 
position the fore-gut. Consideration of the fore-gut except to 
note the location of its first appearance can advantageously be 
deferred because its origin and relationships are more readily 
appreciated from the study of somewhat older embryos. 

The Growth and Differentiation of the Mesoderm. — The 
mesoderm which arises from either side of the primitive streak 
spreads rapidly laterad and at the same time each lateral 
wing of the mesoderm swings cephalad. Figure 12 shows 
schematically the extension of the mesoderm during the latter 
part of the first day of incubation. The diagonal hatch- 
ing represents the mesoderm seen through the transparent 
ectoderm. The principal landmarks of the embryos are 
sketchily represented. 

It will be noticed that the manner in which the mesoderm 
spreads out leaves a mesoderm-free area in the anterior portion 
of the blastoderm. This region is known as the proamnion. 
The name might carry the inference that this area is the primor- 
dium of the amnion, a structure which first appears near this 
region somewhat later in development. Such is not the fact. 
The term proamnion was applied to this region before its true 
significance was understood. It is not the precourser of the 
amnion. In dorsal views of entire embryos the proamnion is 
readily located by reason of its lesser density. The proamnion 
is bounded anteriorly by the area opaca, posteriorly in the mid- 
line by the thickened anterior part of the embryo, and poste- 
riorly on either side by the anterior bordero f the mesoderm 
(Fig. 12). The importance of the proamnion lies chiefly in the 
indication it gives of the progress of mesoderm extension. The 
rapid growth that the mesoderm of the anterior region is under- 
going at this stage is clearly indicated by the diminution in 
area of the proamnion in embryos of 22 hours as compared with 
embryos of 18 hours (Fig. 12). 

Sections passing through the primitive streak of embryos of 
this stage show the pair of loosely aggregated masses of meso- 



derm extending to either side between the ectoderm and ento- 
derm. As would be expected from the method of origin, little 
mesoderm appears in the mid-line except posterior to the primi- 
tive streak. Immediately to either side of the mid-line the 
mesoderm is markedly thicker than it is farther laterad (Fig. 
IS, B). In whole-mounts the positions of the regional thicken- 

^.J^ primitive 



anterior horn of 



dorsal mesoderm 

primitive streak 


Pig. 12. — Schematic diagrams to show the extension of the mesoderm during 
the latter part of the first day of incubation. Some of the more prominent 
structural features of the embryos are drawn in lightly for orientation but the 
ectoderm is supposed to be nearly transparent allowing the mesoderm to show 
through. The areas into which the mesoderm has grown are indicated by 
diagonal hatching. ^^ 

ings of the mesoderm are evidenced by the greater opacity they 
impart to the embryo locally (Fig. 14). These thickened zones 
of the mesoderm are the primordia of the dorsal mesodermic 
plates. Because of the way in which they are later divided into 




prumtive gut 

cell in mitosis ^ ^^^ „f ^^j^ granules - 

entoderm indifferent cells 

I J High power thru primitive streak at region (a) 
on section C. 

"C^ High power thru edge of germ wall 
at region (b) on section C. 

Hensen'snode primitive 

neural plate | .primitive pit ridge 

'j)rimitive groove ' 

extent of primitive gut and of area pellucida 

Pig. 13. — Sections of iS-hoxir chick. The location of each section is indicated 
by a line drawn on a small outline sketch of an entire embryo of corresponding 
age. The letters affixed to the lines indicating the location of the sections 
correspond with the letters designating the section diagrams. Each germ 
layer is represented by a different conventional scheme: ectoderm by vertical 
hatching; entoderm by fine stippling backed by a single line; and the cells of 
the mesoderm which at this stage do not form a coherent layer, by heavy angular 

A, diagram of transverse section through notochord; B, diagram of transverse 
section through primitive pit; C, diagram of transverse section through primitive 
streak; D, drawing showing cellular structure in primitive streak region; E, 
drawing showing cellular structure at inner margin of germ wall; F, diagram 
of median longitudinal section passing through notochord and primitive streak. 


metamerically arranged cell masses or somites they are fre- 
quently designated as the segmental zones of the mesoderm. 
The segmental zones are in early stages most clearly marked 
somewhat cephalic to Hensen's node, where the first somites 
will appear. As they extend caudad on either side of the 
primitive streak they gradually become less and less definite. 

The sheet-like layers of mesoderm which are characteristic 
of the mid-body region do not extend to the anterior part of 
the embryo. The mesoderm of the future head region is 
derived from mesoderm cells which invade the head from the 
more definitely organized layers of mesoderm lying posterior to 
it. The cephaHc mesoderm for this reason never shows the 
regional differentiations and the organization into definite layers 
which later appear in the mesoderm of the mid-body region. 

The Formation of theNotochord. — The notochord arises in the 
chick as a median out-growth from the rapidly proliferating, 
undifferentiated cells at the cephalic end of the primitive streak 
(Fig. is,F). The way in which the notochord grows cephalad 
from the anterior end of the primitive streak, just as in other 
vertebrate embryos it arises from the region of the anterior lip of 
the blastopore, is one of the points which confirms the identifica- 
tion of the primitive streak of the chick as the closed blastopore. 

Largely because of the way in which the notochord arises in 
Amphioxus, a primitive vertebrate of doubtful relationships, it 
has usually been considered of entodermal origin. In Amphibia 
and in birds it arises not from any definite germ layer but from 
the undifferentiated growth center about the blastopore which 
is giving rise to both entoderm and mesoderm. Even in Am- 
phioxus the notochord arises at the same time and in the same 
manner as the mesoderm. In its later differentiation the noto- 
chord resembles mesodermal derivatives more closely than 
entodermal. The common origin of notochord and mesoderm, 
and the unmistakably mesodermal characteristics of the fully 
developed notochord should be emphasized rather than the 
early association of the notochordal primordium with the 
entoderm and its doubtful origin therefrom. For these reasons 
the notochord is in this book treated as a mesodermal structure. 

In entire embryos of i8 to 22 hours (Figs. 11 and 14) the 
notochord can be seen in the mid-line extending cephalad from 
Hensen's node. Hensen's node is at once the posterior limit 



of the notochord and the anterior end of the primitive streak. 
The notochord and the primitive streak together clearly mark 
the mid-line of the embryo and estabUsh definitely the longitu- 
dinal axis of the developing body. In sections (Fig. 13, ^, F) 
the notochord is not at this early stage sharply differentiated 
from the loosely arranged mesoderm cells adjacent to it. In 
later stages, however, the cells composing it become aggregated 
to form a characteristic rod-shaped structure, circular in cross 
section and with clearly defined boundaries (Fig. 52, C). 

The Formation of the Neural Plate. — In surface views of en- 
tire chicks of about 18 hours (Fig. 11) areas of greater density 

cephalic end 

ectoderm of head 

border of fore-gut 

margin of anterior 
intestinal portal 


primitive streak 

area pellucida 

area opaca 

caudal end 
Fig. 14. — Dorsal view ( X 14) of entire chick embryo of about 21 hours incubation. 

may be made out on either side of the notochord. These areas 
extend somewhat anterior to the cephaUc end of the notochord 
where they appear to blend with each other in the mid-hne. 
Sections of this region (Fig. 13, A) show that the greater 
density seen in whole-mounts is due to thickening of the ecto- 
derm. Rapid cell proHferation has resulted in the ectoderm 
in the middle region becoming several cells in thickness. This 


thickened area is known as the neural (medullary) plate. 
Laterally the thickened ectoderm of the neural plate blends 
without abrupt transition into the thinner ectoderm of the 
general blastodermic surface. Anteriorly the neural plate is 
more clearly marked than it is posteriorly. At the level of 
Hensen's node the neural plate diverges into two elongated areas 
of thickening one on either side of the primitive streak. 

In embryos of 21 or 22 hours (Fig. 14) the neural plate 
becomes longitudinally folded to estabHsh a trough known as 
the neural groove. The bottom of the neural groove lies in 
the mid-dorsal line. Flanking the neural groove on each side 
is a longitudinal ridge-like elevation involving the lateral por- 
tion of the neural plate. These two elevations which bound 
the neural groove laterally are known as the neural folds. The 
folding of the originally fiat neural plate to form a gutter, 
flanked on either side by parallel ridges, is an expression of the 
same extremely rapid cell proUferation which first manifested 
itself in the local thickening of the ectoderm to form the neural 
plate. The formation of the neural plate and its subsequent 
folding to form the neural groove are the first indications of the 
differentiation of the central nervous system. 

The Differentiation of the Embryonal Area.^Due to the 
thickening of the ectoderm to form the neural plate and also 
to the thickening of the dorsal zones of the mesoderm, the part 
of the blastoderm immediately surrounding the primitive streak 
and notochord has become noticeably more dense than that 
in the peripheral portion of the area pellucida. Because it is 
the region in which the embryo itself is developed this denser 
region is known as the embryonal area. Although the embry- 
onal area is at this early stage directly continuous with the 
peripheral part of the blastoderm without any definite Une of 
demarcation, they later become folded off from each other. 
The peripheral portion of the blastoderm is then spoken of as 
extra-embryonic because it gives rise to structures which are 
not built into the body of the embryo, although they play a 
vital part in its nutrition and protection during development. 

The anterior region of the embryonal area is thickened and 
protrudes above the general surface of the surrounding blasto- 
derm as a rounded elevation. This prominence marks the 
region in which the head of the embryo will develop (Fig. 14). 


The crescentic fold which bounds it is termed the head fold 
and is the first definite boundary of the body of the embryo. 
Throughout the course of development we shall find the head 
region farther advanced in differentiation than other parts of 
the body. This is a repetition of race history in the develop- 
ment of the individual, for phylogenetically the head is the 
oldest and most highly differentiated region of the body. It is 
one of many manifestations of the law of recapitulation, in 
conformity with which the individual in its development rap- 
idly repeats the main steps in the development of the race to 
which it belongs. 



The formation of the head; the formation of the neural 
groove; the regional divisions of the mesoderm; the 
ccelom, the pericardial region; the area vasculosa. 

The Formation of the Head. — In embryos of 21 to 22 hours 
the anterior part of the embryonal area is thickened and ele- 
vated above the level of the surrounding blastoderm, with a 
well defined crescentic fold marking its anterior boundary. 
Between 21 and 24 hours this region has undergone rapid 
growth (Fig. 15). Its elevation above the blastoderm is much 
more marked and it has grown anteriorly so it overhangs the 
proamnion region. The crescentic fold which formerly marked 
its anterior boundary appears to have undercut the anterior 
part of the embryo and separated it from the blastoderm. The 
changes in relationships are due, however, not so much to a 
posterior movement of the fold as to the anterior growth of the 
embryo itself. This anterior region which projects, free from 
the blastoderm, may now properly be termed the head of the 
embryo. The space formed between the head and the blasto- 
derm is called the subcephalic pocket (Fig. 17, E). 

In the mid-Une the notochord can be seen through the over- 
lying ectoderm. It is larger posteriorly near its point of origin 
than it is anteriorly. Nevertheless it can be readily traced into 
the cephaUc region where it will be seen to terminate somewhat 
short of the anterior end of the head (Fig. 15). 

The Formation of the Neural Groove. — The neural plate in 
chicks of 18 hours was seen as a flat, thickened area of the ecto- 
derm. In embryos of 21 to 22 hours a longitudinal folding had 
involved it establishing the neural groove in the mid-dorsal 
line flanked on either side by the neural folds. At 24 hours of 
incubation the folding of the neural plate is much more clearly 
marked. In a dorsal view of the entire embryo (Fig. 15) the 
neural folds appear as a pair of dark bands. The folding which 




establishes the neural groove takes place first in the cephalic 
region of the embryo. At its cephalic end the neural groove 
is therefore deeper and the neural folds are correspondingly 
more prominent than they are caudally. The folding has not, 
at this stage, been carried much beyond the cephalic half of 
the embryo. Consequently as the neural folds are followed 
caudad they diverge slightly from each other, and become less 
and less distinct. 

ectoderm of head 

border of fore-gut 

subcephalic pocket 

Hensen's node 

Jy'^^'.'-'i'i^f^yC'^'^ mesoderm 

l^&piW^W^ ' V primitive 
i-<':-.A-iV=:s,..':35C*«- ■ -,treak 

border of mesoderm 

blood island 

area vasculosa 

Pig. 15. — Dorsal view ( X 14) of entire chick embryo having 4 pairs of meso- 
dermic somites (about 24 hours incubation). 

Study of transverse sections of an embryo of this stage affords 
a clearer interpretation of the conditions in neural groove for- 
mation than the study of entire embryos. A section passing 
through the head region (Fig. ly, A) shows the neural plate 
folded so it forms a nearly complete tube. Dorsally the mar- 
gins of the neural folds of either side have approached each 
other and lie almost in contact. The formation of the neural 
folds takes place first in about the center of the head region, 
and progresses thence cephalad and caudad. By following 
caudad the sections of a transverse series, the margins of the 



neural folds will be seen less and less closely approximated to 
each other. 

The Establishment of the Fore-gut. — In the outgrowth of the 
head, the entoderm as well as the ectoderm has been involved. 
As a result the entoderm forms a pocket within the ectoderm, 
much like a small glove finger within a larger. This entodermic 
pocket, or fore-gut, is the first part of the digestive tract to ac- 
quire a definite cellular floor. That part of the gut caudal to the 
fore-gut where the yolk still constitutes the only floor, is termed 
the mid-gut. The opening from the mid-gut into the fore-gut 
is called the anterior intestinal portal (fovea cardiaca) . 

margin of anterior 
horn of mesoderm 

pourior margin of '^ 
subcephalic pocket 

margin of fore-gut -Js 

margin of Aiterior 

intestinal portal 



11 r : 

margin of area opaca 

ectoderm of head 

" — mesenchyme 

■ „ border of mesoderm 

— — pericardial region 
of coelom 

~ — thickened splanchnic 

neural fold 

Pig. i6. — Ventral view ( X 37) of cephalic region of chick embryo having 5 pairs 
of somites (about 25-26 hours of incubation). 

The topography of the fore-gut region at this stage can be 
made out very well by studying the ventral aspect of entire 
embryos. The margin of the anterior intestinal portal appears 
as a well defined crescentic Une (Fig. i6). The lateral boun- 
daries of the fore-gut can be seen to join the caudally directed 
tips of the crescentic margin of the portal. Considerably 
cephalic to the intestinal portal an irregularly recurved hne can 
be made out. On either side it appears to merge with the ecto- 
derm of the head. This Hne marks the extent to which the 
head is free from the blastoderm. It is due to the fold at the 
bottom of the subcephalic pocket where the ectoderm of the 
under surface of the head is continuous with the ectoderm of the 
blastoderm. Comparison of Figure 16 with the sagittal section 
diagrammed in Figure 17, -E, will aid in making clear the rela- 


tionships of fore-gut to the head. From the sagittal section it 
will also be apparent why the margins of the intestinal portal 
and of the subcephalic pocket appear as dark lines in the whole- 
mount. In viewing an entire embryo under the microscope by 
transmitted light one depends largely on differences in density 
for locating deep-lying structures. When a layer is folded so 
the light must pass through it edgewise, the fold stands out as a 
dark hne by reason of the greater thickness it presents. 

The Regional Divisions of the Mesoderm. — The first con- 
spicuous metamerically arranged structures to appear in the 
chick are the mesodermic somites. The somites arise by divi- 
sion of the mesoderm of the dorsal or segmental zone to form 
block-Hke cell masses. In the embryo shown in Figure 15 three 
pairs of somites are completely delimited and a fourth pair can 
be made out which is not as yet completely cut off from the 
dorsal mesoderm posterior to it. 

The regular addition of somites as embryos increase in age 
makes the number of somites the most reliable criterion of the 
stage of development. Chicks which have been incubated for 
a given number of hours show wide variation in the degree of 
development attained; chicks of a given number of somites 
vary but little among themselves. ' 

Cross sections passing through the rnid-body region show the 
formation of the somites and the beginning of other changes in 
the mesoderm (Fig. 17, C, cf. also Fig. 28, E). Following the 
mesoderm from the mid-line toward either side three regions or 
zones can be made out: (i) the dorsal mesoderm which at this 
level has been organized into somites, (2) the intermediate 
mesoderm, a thin plate of cells connecting the dorsal and lateral 
mesoderm and (3) the lateral mesoderm which is distinguished 
from the intermediate by being split into two layers with a space 
between them. 

The somites are compact cell masses lying immediately 
lateral to the neural folds The cells composing them have a 
fairly definite radial arrangement about a central cavity which 
is very minute or wanting altogether when the somites are first 
formed but which later becomes enlarged (Fig. 38). Cephalic 
and caudal to the region in which somites have been formed the 
dorsal mesoderm is differentiated from the rest of the mesoderm 
simply by its greater thickness and compactness. 



In 24-hour embryos the intermediate mesoderm shows very 
little differentiation. In the chick it never becomes segmentally 
divided as does the dorsal mesoderm. The fact that it is 
potentially segmental in character is indicated, however, by 
the way in which it later gives rise to segmentally arranged 



Fig. 17. — Diagrams of sections of 24-hour chick. The sections are located 
on an outline sketch of the entire embryo. The conventional representation of 
the germ layers is the same as that employed in Fig. 13 except that here where 
its cells have become aggregated to form definite layers the mesoderm is repre- 
sented by heavy solid black lines. 

nephric tubules. Because of the part it plays in the establish- 
ment of the excretory system the intermediate mesoderm is 
frequently called the nephrotomic plate. 


In the chick the lateral mesoderm like the intermediate 
mesoderm, shows no segmental division. In 24-hour embryos 
(Fig. 17, C) it is clearly differentiated from the intermediate 
mesoderm by being split horizontally into two layers with a 
space between them. The layer of lateral mesoderm lying 
next to the ectoderm is termed the somatic mesoderm, the layer 
next to the entoderm is termed the splanchnic mesoderm, and 
the cavity between somatic and splanchnic mesoderm is the 
coelom. Because in development the somatic mesoderm and 
ectoderm are closely associated and undergo many foldings in 
common, it -is convenient to designate the two layers together 
by the single term somatopleure. Similarly the splanchnic 
mesoderm and the entoderm together are designated as the 

The Coelom. — The coelom, like the cell layers of the blasto- 
derm, extends over the yolk peripherally beyond the embryonal 
area (Fig. 17, C). Later in development foldings mark off the 
embryonic from the extra-embryonic portion of the germ layers. 
This same folding process divides the coelom into intra-em- 
bryonic and extra-embryonic regions. In the 24-hour chick, 
however, embryonic and extra-embryonic coelom have not been 

It is evident from the manner in which the coelomic chambers 
arise in the lateral mesoderm that the coelom of the embryo con- 
sists of a pair of bilaterally symmetrical chambers. It is not 
until later in development that the right and left coelomic 
chambers become confluent ventrally to form an unpaired 
body cavity such as is found in adult vertebrates. 

The Pericardial Region. — In the region of the anterior intes- 
tinal portal the coelomic chambers on either side show very 
marked local enlargements. Later in development these 
dilated regions are extended mesiad and break through into 
each other ventral to the fore-gut to form the pericardial cavity. 
In their early condition these enlarged regions of the coelomic 
chambers are usually called amnio-cardiac vesicles. With their 
later fate in mind we may avoid multiplication of terms and 
speak of them from their first appearance as constituting the 
pericardial region of the coelom. 

The relationships of the pericardial region of the coelom in 
embryos of 24 hours can be most readily grasped from a study 


of transverse sections. Figure 17, B, shows the great dilation 
of the coelom on either side of the anterior intestinal portal as 
compared with its condition farther, caudad (Fig. 17, C). 
Where the splanchnic mesoderm lies closely applied to the 
entoderm at the lateral margins of the portal it is noticeably 
thickened. It is from these areas of thickened splanchnic 
mesoderm that the paired primordia of the heart will later 

In entire embryos of this age the thickened splanchnic 
mesoderm can be made out as a dark band lying close against 
the crescentic entodermal border of the anterior intestinal 
portal (Fig, 16). If the preparation is favorably stained the 
boundaries of the pericardial regions of the coelom can be traced 
(see Fig. 16). Following mesiad from the easily located thick- 
ened areas, the mesodermic borders can be seen to extend from 
either side parallel to the entodermic margins of the portal 
nearly to the mid-line. They then turn cephalad. When they 
encounter the ectodermal fold which constitutes the posterior 
boundary of the subcephalic pocket they swing laterad parallel 
with it and can be traced outside the embryonic region where 
they constitute the cephalic borders of the anterior horns of 
the mesoderm (see also Fig. 27, A). 

The portion of the coelom, the borders of which we have just 
located between the subcephalic pocket and the anterior in- 
testinal portal, is an important landmark from another stand- 
point than the part it is destined to play in the formation of the 
pericardial region. It is the most cephalic part of the coelom. 
There is no coelom in the head. In the head region the meso- 
derm is not aggregated into definite masses or coherent cell 
layers. The mesodermic structures of the head are derived 
from cells which migrate into the cephahc region from the meso- 
derm lying farther caudally. These migrating cells are termed 
mesenchymal cells in distinction to the more definitely aggre- 
gated cell layers of the mesoderm. By careful focusing on the 
whole-mount the mesenchyme of the head can be seen as an 
indefinite mass lying between the superficial ectoderm and the 
entoderm of the fore-gut. The distribution of the mesenchymal 
cells and the characteristic irregularity of shape correlated 
with their active amoeboid movement may be readily made out 
from sections (Fig. 17, ^4). 


The Area Vascvilosa. — In a 24-hour chick the boundary be- 
tween area opaca and area pellucida has the same appearance 
and significance as in chicks of 18 to 20 hours. There is, how- 
ever, a very marked difference between the proximal portion 
of the area opaca adjacent to the area pellucida and the more 
distal portions of the area opaca. The proximal region is much 
darker and has a somewhat mottled appearance (Fig. 1 5) . The 
greater density of this region is due to its invasion by mesoderm 
which makes it thicker and therefore more opaque in transmitted 
light (Fig. 17, D). The boundary between the inner and outer 
zones of the area opaca is established by the extent to which 
the mesoderm has grown peripherally. The distal zone is 
called the area opaca vitellina because the yolk alone underlies 
it. The proximal zone into which mesoderm has grown is 
known as the area opaca vasculosa, because it is from the meso- 
derm in this region that the yolk-sac blood vessels arise. The 
mottled appearance of this region is due to the aggregation of 
mesoderm into cell clusters, or blood islands, which mark the 
initial step in the formation of blood vessels and blood corpus- 
cles. Later in development the formation of blood islands and 
vessels extends in toward the body of the embryo from its 
place of earhest appearance in the area opaca and involves the 
mesoderm of the area pellucida. The histological nature of 
the blood islands will be taken up in connection with later 
stages where their development is more advanced. 



The closure of the neural tube; the differentiation 
of the brain region; the anterior neuropore; the 
sinus rhomboidalis; the fate of the primitive streak; 
the lengthening of the fore-gut; the appearance 
of the heart and omphalomesenteric veins; organ- 

In dealing with developmental processes the selection of 
stages for detailed consideration is more or less arbitrary and 
largely determined by the phenomena one seeks to emphasize. 
There is no stage of development which does not show some- 
thing of interest. It is impossible in brief compass to take up 
at length more than a few stages. Nevertheless it is important 
not to lose the continuity of the processes involved. By calling 
attention to some of the more important intervening changes, 
this brief chapter aims to bridge the gap between the 24-hour 
stage and the 33-hour stages of the chick both of which are 
taken up in some detail. 

The Closure of the Neural Tube. — In comparison with 24- 
hour chicks, entire embryos of 27 to 28 hours of incubation 
(Fig. 18) show marked advances in the development of the 
cephalic region. The head has elongated rapidly and now pro- 
jects free from the blastoderm for a considerable distance, with 
a corresponding increase in the depth of the subcephalic pocket 
and in the length of the fore-gut. 

In 24-hour chicks the anterior part of the neural plate is 
already folded to form the neural groove. Although the neural 
folds are at that stage beginning to converge mid-dorsally the ^ 
groove nevertheless remains open throughout its length (Fig. 
ly. A, B, C). By 27 hours the neural folds in the cephalic 
region meet in the mid-dorsal line and their edges become fused. 

The fusion which occurs is really a double one. Careful 
following of Figures 26, A to £, will aid greatly in understanding 




the process. Each neural fold consists of a mesial component 
which is thickened neural plate ectoderm, and a lateral com- 
ponent which is unmodified superficial ectoderm (Fig. 26, A), 
When the neural folds meet in the mid-dorsal line (Fig. 26, -B, C) 
the mesial, neural plate components of the two folds fuse with 
each other, and the outer layers of unmodified ectoderm also 
become fused (Fig. 26, D). Thus in the same process the 
neural groove becomes closed to form the neural tube and the 

proamnion prosencephalon 

anterior / 


border of fore-gut 

subcephalic pocket 


mesenteric vein 

blood island 

border ot ..... .^. -y -.» . 

inesodenn. ' v^^^v^'^5?iT-;> '*•. 

Hensen's node 

.■.-^' ^'&f.^"':: < :: ■ ■* extra-embryonic 
^- vascular plexus 

Fig. 18. — Dorsal view ( X 14) of entire chick embryo having 8 pairs of somites 
(about 27-28 hours incubation). 

superficial ectoderm closes over the place formerly occupied by 
the open neural groove. Shortly after this double fusion the 
neural tube and the superficial ectoderm become somewhat 
separated from each other leaving no hint of their former con- 
tinuity (Fig. 26, E). 

The Differentiation of the Brain Region. — By 27 hours of 
incubation the anterior part of the neural tube is markedly 
enlarged as compared with the posterior part. Its thickened 



walls and dilated lumen mark the region which will develop 
into the brain. The undilated posterior part of the neural tube 
gives rise to the spinal cord. Three divisions, the three primary 
brain vesicles, can be distinguished in the enlarged cephahc 
region of the neural tube (Fig. i8). Occupying most of the 
anterior-part of the head is a conspicuous dilation known from 
its position as the fore-brain or prosencephalon. Posterior to 

ectoderm of head 


optic vesicle 

ventral aortic root 

ventral aorta 


line of endocardi al 

margin of anterior 
intestinal porta! 

anterior horn of mesoderm 

anterior neuropore 



vascular plexus 

Fig. 19. — Ventral view ( X 45) of head and heart region of chick embryo of 9 
somites (about 29-30 hours incubation). 

the prosencephalon and marked off from it by a constriction is 
the mid-brain or mesencephalon. Posterior to the mesenceph- 
alon with only a very slight constriction marking the boundary 
is the hind-brain or rhombencephalon. The rhombencephalon 
is continuous posteriorly with the cord region of the neural tube 
without any definite point of transition. 

In somewhat older embryos (Fig. 19) the lateral walls of the 
prosencephalon become out-pocketed to form a pair of rounded 
dilations known as the primary optic vesicles. When the 


optic vesicles are first formed there is no cgnstriction between 
them and the lateral walls of the prosencephalon, and the 
lumen of each optic vesicle communicates mesially with the 
lumen of the prosencephalon without any definite hne of 

The relation of the notochord to the divisions of the brain is of 
importance in later developmental processes. The notochord 
extends anteriorly as far as a depression in the floor of the 
prosencephalon known as the infundibulum (Fig. 19). There- 
fore, the rhombencephalon, mesencephalon, and that part of the 
prosencephalon posterior to the infundibulum he immediately 
dorsal to the notochord (are epichordal) while the infundibular 
region and the parts of the prosencephalon cephalic to it project 
anterior to the notochord (are pre-chordal) . 

The Anterior Neuropore. — The closure of the neural folds 
takes place first near the anterior end of the neural groove and 
progresses thence both cephalad and caudad. At the extreme 
anterior end of the brain region closure is delayed. As a result 
the prosencephalon remains for sometime in communication 
with the outside through an opening called the anterior neuro- 
pore. The anterior neuropore is still open in chicks of 2 7 hours 
(Fig. 18). In embryos of 33 hours the neuropore appears much 
narrowed (Fig. 21). A little later it becomes closed but leaves 
for some time a scar-like fissure in* the anterior wall of the 
prosencephalon (Fig. 23). The anterior neuropore does not 
give rise to any definite brain structure. It is important simply 
as a landmark in brain topography. Long after it has disap- 
peared as a definite opening the scar left by its closure serves to 
mark the point originally most anterior in the developing brain. 

TheSinusRhomboidalis. — The rhombencephaUc region of the 
brain merges caudally without any definite line of demarcation 
into the region of the neural tube destined to become the 
spinal cord. The neural tube as far caudally as somite forma- 
tion has progressed is completely closed and of nearly uniform 
diameter. Caudal to the most posterior somites the neural 
groove is still open and the neural folds diverge to either side of 
Hensen's node (Fig. 18). In their later growth caudad the 
neural folds converge toward the mid-line and form the lateral 
boundaries of an unclosed region at the posterior extremity of 
the neural tube known because of its shape as the sinus rhom- 


boidalis (Fig. 21). Hensen's node and the primitive pit lie in 
the floor of this as yet unclosed region of the neural groove and 
subsequently are enclosed within it when the neural folds here 
finally fuse to complete the neural tube. 

This process in the chick is homologous with the enclosure of 
the blastopore by the neural folds in lower vertebrates. In 
forms where the blastopore does not become closed until after 
it is surrounded by the neural folds, it for a time constitutes an 
opening from the neural canal into the primitive gut known as 
the neurenteric canal or posterior neuropore. In the chick the 
early closure of the blastopore precludes the estabHshment of an 
open neurenteric canal but the primitive pit represents its 

The Fate of the Primitive Streak. — In embryos of about 27 
hours the primitive streak is relatively much shorter than in 
younger embryos (Cf. Figs. 8, 11, 14, 15, and 18). This is 
due partly to its being overshadowed by the rapid growth of 
structures lying cephalic to it, and partly to actual decrease 
in the length of the primitive streak itself. The cells in the 
primitive stieak region would appear to be contributed to 
surrounding structures. Whatever the exact fate of its cells 
may be, the primitive streak becomes less and less a conspicuous 
feature in the developing embryo. By the time the caudal end 
of the body is delimited, the primitive streak as a definitely 
organized structure has disappeared altogether (Cf. Figs. 18, 
21, 29, 34). 

The Formation of Addifional Somites. — The division of the 
dorsal mesoderm to form somites begins to be apparent in 
embryos of about 22 hours. By the end of the first day three 
or four pairs of somites have been cut off (Fig. 15). As develop- 
ment progresses new somites are added caudal to those fiist 
formed. In embryos which have been incubated about 27 
hours eight pairs of somites have been established (Fig. 18). 

It was formerly beHeved that some new somites were formed 
anterior to the first pair. The experiments of Patterson would 
seem to indicate quite definitely that the first pair of completely 
formed somites remains the most anterior and that all the new 
somites are added posterior to them. The experiments referred 
to were carried out on eggs which had been incubated up to the 
time of the formation of the first somite. With thorough 


aseptic precautions the eggs were opened and the first somite 
marked, in some cases by injury with an "electric needle" 
in other cases by the insertion of a minute glass pin. Following 
the operation the shell was closed by sealing over the opening a 
piece of egg shell of appropriate size. After being again in- 
cubated for varying lengths of time the eggs were reopened. In 
all cases the injured first somite was still the most anterior 
complete somite. All the new somites except the incomplete 
''head somite" had appeared caudal to the first pair of somites 

The Lengthening of the Fore-gut. — Comparison of the rela- 
tions of the crescentic margin of the anterior intestinal portal 
in embryos between 24 and 30 hours shows it occupying pro- 
gressively more caudal positions (Fig. 27). This change in the 
position of the anterior intestinal portal is the result of two 
distinct growth processes. The margins of either side of the 
portal are constantly converging toward the mid-Une where they 
become fused with each other. Their fusion lengthens the fore- 
gut by adding to its floor and thereby displaces the crescentic 
margin of the portal caudad. At the same time the struc- 
tures cephalic to the anterior intestinal portal are elongating 
rapidly so that the portal becomes more and more remote from 
the anterior end of the embryo with the further lengthening of 
the fore-gut. 

As a result of these two processes the space between the sub- 
cephalic pocket and the margin of the anterior intestinal portal 
is also elongated (Fig. 27). This is of importance in connection 
with the formation of the heart for it is into this enlarging 
space that the pericardial portions of the coelom extend and 
in it that the heart comes to Ue. 

The Appearance of the Heart and Omphalomesenteric Veins. 
Although the early steps in the formal ion of the heart take 
place in embryos of this range, detailed consideration of them 
has been deferred to be taken up in connection with later stages 
when conditions in the circulatory system as a whole are more 

In dorsal views of entire embryos the heait is largely con- 
cealed by the overlying rhombencephalon (Fig. 18) but it may 
readily be made out by viewing the embryo from the ventral 
surface (Fig. 19). At this stage the heart is a nearly straight 


tubular structure lying in the mid-line ventral to the fore-gut. 
Its mid-region has noticeably thickened walls and is somewhat 
dilated. Anteriorly the heart is continuous with the large 
median vessel, the ventral aorta, posteriorly it is continuous 
with the paired omphalomesenteric veins. The fork formed 
by the union of the omphalomesenteric veins in the posterior 
part of the heart lies immediately cephalic to the crescentic 
margin of the anterior intestinal portal, the veins lying within 
the fold of entoderm which constitutes its margin. 

Organization in the Area Vasculosa. — The extra-embryonic 
vascular area at this stage is undergoing rapid enlargement 
and presents a netted appearance instead of being mottled as 
in the earlier embryos. The peripheral boundary of the area 
vasculosa is definitely marked by a dark band, the precursor 
of the sinus terminalis (marginal sinus) . Its netted appearance 
is due to the extension and anastomosing of blood islands. 
The formation of the network is a step in the organization of a 
plexus of blood vessels on the yolk surface which will later be 
the means of absorbing and transferring food material to the 
embryo. The afferent yolk-sac or vitelline circulation is estab- 
lished in the next few hours of incubation when this plexus of 
vessels developing on the yolk surface comes into communica- 
tion with the omphalomesenteric veins already developing 
within the embryo and extending laterad. The efferent vitelUne 
circulation is established somewhat later when the omphalo* 
mesenteric arteries arise from the aorta of the embryo and 
become connected with the yolk-sac plexus. (Cf. Figs. 15, 18, 



The divisions of the brain and their neuromeric struc- 

Chicks which have been incubated from S3 to 39 hours are 
in a favorable stage to show some of the fundamental steps in 
the foimation of the central nervous system, and of the circu- 
latoi;y system. In this chapter, therefore, attention has been 
concentrated on these two systems. 

During this period of incubation there are also changes in 
the fore-gut region and in the somites, and differentiation in 
the intermediate mesoderm which presages the formation of 
the urinary organs. Consideration of these structures has, 
however, been defeired until their development has progressed 
somewhat farther. 

The Divisions of the Brain and Their Neuromeric Structure. 
The metameric arrangement of structures which is so striking 
a feature in the body organization of all vertebrates, is masked 
in the head region of the adult by superimposed specializations. 
In the brain of young vertebrate embryos, however, the meta- 
merism is still indicated. Dissections of the neural plate of 
chicks at the end of the first day of incubation show a series of 
eleven enlargements marked off from each other by contric- 
tions (Fig. 20, A). Concerning the precise homologies of indi- 
vidual enlargements with specific neuromeres in other forms 
there is not complete agreement. The controversies center 
about the question of neuromeric fusions in the anterior part 
of the brain. For the beginning student the fact that meta- 
merism is present is to be emphasized rather than the contro- 
versies concerning the homologies of neuromeres. With the 
reservation that some of the anterior enlargements may repre- 




sent fusions of more than one neuromere, the series of enlarge- 
ments seen in the brain region of the chick may be regarded as 
neuromeric. For convenience in designation the neuromeres 
are numbered beginning at the anterior end. 

anterior neuropore 

cut ectoderm 

neural groove 

Hft neural fold 


line of fusion 
neural folds 






Pig. 20. — Diagrams to show the neuromeric enlargements in the brain region 
of the neural tube. (Based on figures by Hill.) 
A , lateral view of neural plate from dissection of chick of 4 somites (24 hours) ; 
B, dorsal view of brain dissected out of 7-somite (26 to 27-hour) embryo; C, 
dorsal view of brain trom lo-somite (30-hour) embryo; D, dorsal view of brain 
from 14-somite (36-hour) embryo. 

\\ ith the closure of the neural tube and the establishment of 
the three primary brain vesicles we can begin to trace the fate of 



the vaiious neuromeric enlargements in the formation of the 
brain regions. The three anterior neuromeres form the prosen- 
cephalon; neuromeres four and five are incorporated in the 
mesencephalon; and neuromeres six to eleven in the rhom- 



anterior neuropore 

optic vesicle 

omphalomesenteric vein 

lateral m 

sinus rhomboidalis 

primitive streak 

Pig. 21. — Dorsal view ( x 14) of an entire chick embryo of 12 somites (about 
33 hours incubation). 

b^ncephalon (Fig. 20, B). Anteriorly the interneuromeric 
constrictions soon disappear except for two; namely, the one 
between the prosencephalon and mesencephalon, and the one 



between the mesencephalon and rhombencephalon. The 
rhombencephalic neuromeres, however, remain clearly marked 
for a considerable period. 

By about 33 hours of incubation the optic vesicles are estab- 
lished as paired lateral outgrowths of the prosencephalon. 
They soon extend to occupy the full width of the head (Fig. 
20, C and Fig. 21). The distal portion of each of the vesicles 


^fir ***»»»„,„ 






^ optic vesicle 

infundibulum -—^ 

' :!'^' 







^^_^....r^-^ aortic arch 







if He Vi m3 T 


,- — i*^ notochord 


■i^JR y i jMI i 

f / 

siSm { ^^Km 


HeHI << '''^^n'ln^ 


^ ** r f 

region of ganglion V 

VWF Imv^''^1 


metencephalon ^ 




t , 

myelencephalon ^- 




" ' irteriosus 

cephalic neural ere at — 

region of ganglion 

^^T^n-i^Jv*?^ i 


t^iUHB ;AnL#'«HSpid 

■ ' 


'AjPjBK-glW ■ ^ -, 



*^ V >• 

L^^^ S-fll^^ 


I ^^S vl^^ I 


Pig. 22. — Dorsal view ( x 45) of head and heart region of a chick embryo of 17 
somites (38-39 hours incubation). 

thus comes to lie closely approximated to the superficial ecto- 
derm, a relationship of importance in their later development. 
At first the cavities of the optic vesicles (opticoeles) are broadly 
confluent with the cavity of the prosencephalon (prosoccele) . 
Somewhat later constrictions appear which mark more defi- 
nitely the boundaries between the optic vesicles and the prosen- 
cephalon (Fig. 20, D and Fig. 22). 

There arises also at this stage a depression in the floor of the 



prosencephalon known because of its peculiar shape as the 
infundibulum (Figs. 23 and 24). The infundibular region is 
the site of important changes later in development. At this 
stage, conditions are not sufficiently a^dvanced to warrant more 
than calling attention to its origin from, and relations to, the 
prosencephalon, and to the anterior end of the notochord as 
shown in the figures referred to. 



bulbo-conus arteriosus 
cut epi-myocardium 

ventricular region . 
atrial region 

-anterior intestinal portal 

ventral aortic roots 

cut ectoderm 

dorsal aortae 

stnus venosus 

lateral mesoderm 

cut splanchnopleure 

Pig. 23. — Diagrammatic ventral view of dissection of a 35-hour chick embryo. 
{Modified from Prentiss.) The splanchnopleure of the yolk-sac cephalic to the 
anterior intestinal portal, the ectoderm of the ventral surface of the head, and 
the mesoderm of the pericardial region, have been removed to show the under- 
lying structures. Figure 24 should be referred to for the relations of the peri- 
cardial mesoderm. 

In chicks of about 38 hours indications of the impending 
division of the three primary vesicles to form the five regions 
characteristic of the adult brain are already beginning to ap- 
pear. In the establishment of the five-vesicle condition of 
the brain, the prosencephalon is subdivided to form the 




telencephalon and diencephalon, the mesencephalon remains 
undivided, and the rhombencephalon divides to form the 
metencephalon and myelencephalon. 

The division of the prosencephalon into telencephalon and 
diencephalon is not completed until a much later stage of 
development, but the median enlargement at this stage ex- 
tending anterior to the level of the optic vesicles indicates where 
the telencephalon will be established (Fig. 20, D). The optic 
vesicles and that part of the prosencephalon lying between them 
go into the diencephalon. 

The mesencephalon, as stated above, undergoes no subdivi- 
sion. The original mesencephalic region of the three-vesicle 
brain gives rise to the mesencephalon of the adult. This region 
of the brain does not undergo any marked differentiation until 
relatively late in development. 

At this stage the division of the rhombencephalon is clearly 
marked (Fig. 20, D and Fig. 22). The two most anterior 
neuromeres of the original rhombencephalon form the meten- 
cephalon and the posterior four neuromeres are incorporated 
in the myelencephalon. 

The Auditory Pits. — As is the case with the central nervous 
system, the organs of special sense arise early in development. 
The appearance of the optic vesicles which later become the 
sensory part of the eyes has already been noted. The first 
indication of the formation of the sensory part of the ear 
becomes evident at about 35 hours of incubation. At this age 
a pair of thickenings termed the auditory placodes arise in the 
superficial ectoderm of the head. They are situated on the 
dorso-lateral surface opposite the most posterior inter-neuro- 
meric constriction of the myelencephalon. By 38 hours of 
incubation (Fig. 22) the auditory- placodes have become 
depressed below the general level of the ectoderm and form 
the walls of a pair of cavities, the auditory pits. When first 
formed the walls of the auditory pits are directly continuous 
with the superficial ectoderm, and their cavities are widely open 
to the outside. In later stages the openings into the pits 
become narrowed and finally closed so that the pits become 
vesicles lying between the superficial ectoderm and the myelen- 
cephalon. As yet they have no connection with the central 
nervous system. 


The Formation of Extra-embryonic Blood Vessels. — In 

dealing with the circulation of the chick we must recognize 
at the outset two distinct circulatory arcs of which the heart is 
the common center. One complete circulatory arc is estab- 
lished entirely within the body of the embryo. A second arc is 
established which has a rich plexus of terminal vessels located 
in the extra-embryonic membranes enveloping the yolk. These 
are the vitelline vessels. The vitelline vessels communicate 
with the heart over main vessels which traverse the embryonic 
body. The chief distribution of the vitelline circulation is, 
however, extra-embryonic. Later in development there arises 
a third circulatory arc involving another set of extra-embryonic 
vessels in the allantois, but with that we have no concern until 
we take up later stages. Neither the intra-embryonic, nor the 
vitelline circulatory channels have as yet been completed but 
the heart and many of the main vessels have made their 

The formation of extra-embryonic blood vessels is presaged 
by the appearance of blood islands in the vascular area of 
chicks toward the end of the first day of incubation (see Chapter 
Vll). Figure 25 shows the differentiation of blood islands to 
form primitive blood corpuscles and blood vessels. At their 
first appearance the blood islands are irregular clusters of meso- 
derm cells lying in intimate contact with the yolk-sac entoderm 
(Fig. 25, A). When the lateral mesoderm becomes split 
forming the somatic and splanchnic layers with the coelom 
between, the blood islands lie in the splanchnic mesoderm ad- 
jacent to the entoderm. In embryos of 3 to 5 somites fluid 
filled spaces begin to appear in the blood islands with the result 
that in each blood island the peripheral cells are separated from 
the central ones (Fig. 25, -B). As the fluid accumulates and the 
spaces expand the peripheral cells become flattened and^ushed 
outward, but they remain adherent to each other and com- 
pletely enclose the central cells. At this stage the single layer 
of peripheral cells may be regarded as constituting the endo- 
thelial wall of a primitive blood channel (Fig. 25, C). Exten- 
sion and anastomosis of neighboring blood islands which have 
undergone similar differentiation results in the establishment of 
a network of communicating vessels. Meanwhile the cells 
enclosed in the primitive blood channels have become separated 



from each other and rounded. They soon come to contain 
haemoglobin and constitute the primitive blood corpuscles. 
The fluid accumulated in the blood islands serves as a vehicle 
in which the corpuscles are suspended and conveyed along 
the vessels. 



central cells of 
blood island 

peripheral cell 
of blood island 


blood cells 
entoderm cell 


endothelial cell 


Fig. 25. — Drawings to show the cellular organization of blood islands at 
three stages in their differentiation. The location of the areas drawn with 
reference to the body of the embryo and other structtires of the blastoderm 
can be ascertained by reference to Fig. 17, D. 

A, from blastoderm of 18-hour chick; B, from blastoderm of 24-hour chick;. 
C, from blastoderm of 33-hour chick. 

The differentiation of the blood islands in the manner de- 
scribed begins first in the peripheral part of the area vasculosa 
and from there extends toward the body of the embryo. By 
33 hours of incubation the extra-embryonic vascular plexus has 
extended inward and made connection with the omphalomesen- 
teric veins which, originating within the body of the embryo 


have grown outward. Thus are established the afferent vitel- 
line channels (Fig. 21). 

The efferent vitelline channels have not yet appeared and 
there is no circulation of the blood corpuscles which are being 
formed in the area vasculosa. Th^ intra-embryonic blood 
vessels remain empty until the extra-embryonic circuit is com- 
pleted. The embryo meanwhile draws its nutrition from the 
yolk by direct absorption. 

The Formation of the Heart. — The structural relations of 
the heart and the way in which it is derived from the mesoderm 
can be grasped only by the careful study of sections through 
the heart region in several stages of development (Fig. 26). 
The fact that the heart, itself an unpaired structure, arises 
from paired primordia which at first lie widely separated on 
either side of the mid-line, is likely to be troublesome unless its 
significance is understood at the outset. The paired condition 
of the heart at the time of its origin is due to the fa.ct that the 
early embryo lies open ventrally, spread out on the yolk sur- 
face. The rudiments of all ventral structures which appear at 
an early age are thus at first separated, and lie on either side 
of the mid-line. 

As the embryo develops, a series of foldings undercut it and 
separate it from the yolk. This folding off process at the same 
time establishes the ventral wall of the gut and the ventral body 
wall of the embryo by bringing together in the mid-line the 
structures formerly spread out to right and left. The primordia 
of the heart arise in connection with layers which are destined 
to form ventral parts of the embryo, but at a time when these 
layers are still spread out on the yolk. As the embryo is com- 
pleted ventrally the paired primordia of the heart are brought 
together in the mid-line and become fused (Fig. 27). 

The first indication of heart formation is to be seen in trans- 
verse sections passing through a 2S-hour chick immediately 
caudal to the anterior intestinal portal. Where the splanchno- 
pleure of either side bends toward the mid-line along the lateral 
margin of the intestinal portal there is a marked regional thick- 
ening in the splanchnic mesoderm of either side (Figs. 26, A 
and 27, yl). This pair of thickenings indicates where there has 
been rapid cell proliferation preliminary to the differentiation 
of the heart. Loosely associated cells can already be seen 


somewhat detached from the mesial face of the mesoderm layer. 
These cells soon become organized to form the endocardial 

In a chick of about 26 hours, sections through a corresponding 
region show distinct dfferentiation of the endocardial and epi- 
myocardial primordia (Fig. 26, B). The endocardial primordia 
are a pair of delicate tubular structures, a single cell in thick- 
ness, lying between the entoderm and mesoderm. They arise 
from the cells seen separating from the adjacent thickened meso- 
derm in the 25-hour chick. As their name indicates they are 
destined to give rise to the endothelial lining of the heart. By 
far the greater part of each of the original mesodermic thicken- 
ings becomes applied to the lateral aspects of the endocardial 
tubes as the epi-myocardial primordium which is destined to 
give rise to the external coat of the heart (epicardium) and to 
the heavy muscular layers of the heart (myocardium). 

In chicks of 27 hours the lateral margins of the anterior intes- 
tinal portal have been undergoing concrescence lengthening 
the fore-gut caudally and involving the heart region. In this 
process the former lateral margins of the portal swing in to 
meet each other and fuse in the mid-line, and the endocardial 
tubes of the right and left side are brought toward each other 
beneath the newly completed floor of the fore-gut (Figs. 26, C 
and 27, B). In the 28-hour chick the endocardial primordia 
are approximated to each other (Figs. 26, D and 27, C) and by 29 
hours they fuse in their mid-region to form a single tube (Figs. 
26, E and 27, D). 

At the same time the epi-myocardial areas of the mesoderm 
are brought together first ventrally (Fig. 26, D) and then dor- 
sally to the endocardium (Fig. 26, E). Where the splanchnic 
mesoderm of the opposite sides of the body comes together dor- 
sal and ventral to the heart it forms double layered supporting 
membranes called respectively the dorsal mesocardium and the 
ventral mesocardium. j The ventral mesocardium is a transitory 
structure, disappearing almost as soon as it is formed (Fig. 26, 
E). The dorsal mesocardium, although the greater part of it 
disappears in the next few hours of incubation, persists in em- 
bryos of the stage under consideration, suspending the heart 
in the pericardial region of the coelom. Conditions reached in 
the heart region at 33 hours of incubation are shown in section 



in Figure 28, C. The heart here is enlarged and displaced 
somewhat to the right of the mid-line but its fundamental 

neural plate ectoderm 
donal meaoderm 

■uperficial ectoderm 
neural groove 

j — somatopleure 

splanchnic mesoderm 

gut itrnncdiaoely caudal to 
anterior intestinal portal 

neural groove 


I somatopleure 

\- splanchnopleure 



gut immediately caudal to 
anterior intestinal portal 

dorsal mesoderm 




line of fusion of lateral margins of 
anterior intestinal portal 

dorsal mesoderm 


dorsal mesocardium 

ventral mesocardium 

|— somatopleure 

}- splanchnopleure 

dorsal mesoderm 

dorsal mesocardium 


} — splanchnopleure 


Fig. 26. — Diagrams of transverse sections through the pericardial region 
of chicks at various stages to show the formation of the heart. For location of 
the sections consult Fig. 27. 

A, at 25 hours; B, at 26 hours; C, at 27 hours; D, at 28 hours; E, at 29 hours. 

relations are otherwise the same as in a 29-hour embryo (Fig. 
26, E). 



The gross shape of the heart and its positional relations 
to other structures are best seen in entire embryos. The fusion 
of the paired cardiac primordia establishes the heart as a 
nearly straight tubular structure. It lies at the level of the 
rhombencephalon in the mid-line, ventral to the fore-gut 
(Fig. 19). By ^^ hours of incubation the mid-region of the 


_ _ _ region of coelom ^ 


margin of 
• anterior intestinal - — - - - y' 



ventral aortic 

^-•region of coelom -^.^ 




Fig. 27, — Ventral-view diagrams to show the origin and subsequent fusion 
of the paired primordia of the heart. The lines A, C, D, and E indicate the 
planes of the sections diagrammed in Fig. 26, A, C, D, E, respectively. 

A, chick of 25 hours; B, chick of 27 hours; C, chick of 28 hours; D, chick of 
29 hours. 

heart is considerably dilated and bent to the right (Fig. 21). 
At 38 hours the heart k bent so far to the right that it extends 
beyond the lateral body margin of the embryo (Fig. 22). This 
bending process is correlated with the rupture of the dorsal 
mesocardium at the mid-r-egion of the heart. The breaking 


through of the dorsal and ventral mesocardia is of interest 
aside from the fact that it leaves the heart free to undergo 
changes in shape. It makes the right and left ccelomic cham- 
bers confluent, the pericardial region thus being the first part 
of the coelom to acquire the unpaired condition characteristic 
of the adult. 

Although there are as yet no sharply bounded subdivisions of 
the heart, it is convenient to distinguish four regions which later 
become clearly marked off from each other (Fig. 23). The 
most caudal part of the heart where the omphalomesenteric 
veins join is the sinus venosus; the caudal part of the region 
of the heait which is dilated and bent to the right will become 
the atrium; the cephalic part of the heart bend is the ventricular 
region; and the region where the ventricle swings into the mid- 
line and becomes narrowed is known as the bulbo-conus ar- 
teriosus. Approximately at the stage of development indicated 
in Figure 23 irregular twitchings occur in the heart walls, but 
regular pulsations are not established until about the 44th hour 
of incubation. 

The Formation of the Intra-embryonic Blood Vessels. — Co- 
incident with the establishment of the heart, blood vessels have 
arisen within the body of the embryo. Concerning the exact 
nature of the process of blood vessel formation there is some 
disagreement. The weight of evidence seems to indicate 
that the early vessels are formed from mesodermal cells which 
lie in the path of their development. They grow by organi- 
zation of cells in situ as a drain might be built from bricks 
already deposited along its projected course. In later stages 
it seems probable that vessels extend by the formation of bud- 
like outgrowths from their walls, as well as by organization of 
cells in- their path of development. When first formed, the 
blood vessel walls are but a single cell in thickness. There 
is no structural differentiation between arteries and veins 
until a considerably later period. Recognition of the vessels 
depends wholly, therefore, on determining their course and 

The large vessels connecting with the heart are the first of 
the intra-embryonic channels established. From the bulbo- 
conus arteriosus the paired ventral aortic roots extend cephalad 
ventral to the fore-gut (Fig. 23). At the cephalic end of the 



fore-gut the ventral aortic roots turning dorsad curve around 
it, and then extend caudad, dorsal to the gut, as the paired 
dorsal aortae (Figs. 23, 24 and Fig. 28, B). Few conspicuous 

of blastoderm 


mesoderm 1 lateral plate 

splanchnic mesoderm J of mesoderm 

Fig. 28. — Diagrams of sections of 33-hour chick. The location of each section 
is indicated on a small outline sketch of the entire embryo.t 

branches arise from the aortae at this stage but as development 
"progresses branches extend to the various parts of the embryo 
and the aortae become the main efferent conducting vessels of 


the embryonic circulation. Both the ventral aortic roots and 
the omphalomesenteric veins are direct continuations of the 
paired endocardial primordia of the heart. The epi-myocardial 
coat is formed about the original endothelial tubes only where 
they are fused in the region destined to become the heart. The 
development of the heart at this stage is an epitome of its 
phylogenetic origin. The local investment of the endocardial 
tubes by the epi-myocardium, as seen in the formation of the 
chick heart, is a recapitulation of the evolutionary origin of 
the heart by the local addition of a heavy muscular coat about 
the walls of a blood vessel. 

During early embryonic life the cardinal veins are the main 
afferent vessels of the intra-embryonic circulation. The main 
cardinal trunks are paired vessels symmetrically placed on 
either side of the mid-line. There are two pairs, the anterior 
cardinals which return the blood to the heart from the cephalic 
region of the embryo, and the posterior cardinals which return 
the blood from the caudal region. The anterior and posterior 
cardinal veins of the same side of the body become confluent 
dorsal to the level of the heart. The vessels formed by the 
junction of the anterior and posterior cardinals are the ducts of 
Cuvier or common cardinal veins. The right and left ducts of 
Cuvier turn ventrad, one on either side of the fore-gut, and enter 
the sinus-venosus along with the right and left omphalomesen- 
teric veins, respectively (Fig. 24). 

In chicks of 33 hours the anterior cardinal veins can usually 
be made out in sections (Fig. 28, B, C). By 38 hours the an- 
terior cardinals and the ducts of Cuvier are readily recognized. 
The posterior cardinals appear somewhat later than the an- 
terior cardinals but are ordinarily discernible in the region of the 
duct of Cuvier by 33 to 35 hours and well established by 38 
hours. For the sake of simplicity and clearness the cardinal 
veins have been represented in Figure 24 larger and more 
regularly formed than they are in actual specimens. Like all 
the other blood vessels of the embryo they arise as irregular 
anastomosing endothelial tubes, only gradually taking on the 
regularity of shape characteristic of fully formed vessels. 



Flexion and torsion; the completion of the vitelline 
circulatory channels; the beginning of the circu- 
lation of blood. 

Flexion and Torsion.— Until 36 or 37 hours of incubation the 
longitudinal axis of the chick is straight except for slight for- 
tuitous variations. Beginning at about 38 hours, processes are 
initiated which eventually change the entire configuration of the 
embryo and its positional relations to the yolk. These proc- 
esses involve positional changes of two distinct types, flexion 
and torsion. As applied to an embryo, flexion means the bend- 
ing of the body about a transverse axis, as one might bend the 
head forward at the neck, or the trunk forward at the hips. 
Torsion means the twisting of the body, as one might turn the 
head and shoulders in looking backwards without changing the 
position of the feet. 

In chick embryos the first flexion of the originally straight 
body-axis takes place in the head region. Because of its loca- 
tion it is known as the cranial flexure. The axis of bending in 
the development of the cranial flexure is a transverse axis pas- 
sing through the mid-brain at the level of the anterior end of the 
notochord. The direction of the flexion is such that the 
fore-brain becomes bent ventrally toward the yolk. The proc- 
ess is carried out as if the brain were being bent about the 
anterior end of the notochord. Until the cranial flexure is well 
established it is inconspicuous in dorsal views of whole-mounts 
but even in its initial stages it appears plainly in lateral views 
(Fig. 24). 

To appreciate the correlation between the processes of flexion 
and torsion it is only necessary to bear in mind the relation of 
a chick of this stage to the yolk. As long as the chick lies with 
its ventral surface closely applied to the yolk, the yolk consti- 
tutes a bar to flexion. Before extensive flexion can be carried 



out the chick must twist around on its side, i.e., undergo tor- 
sion, as a man lying face down turns on his side in order to 
flex his body. 

Torsion begins in the cephalic region of the embryo and pro- 
gresses caudad. The first indications of torsion appear almost 
as soon as the cranial flexure begins and the two processes then 
progress synchronously. In the chick, torsion is normally car- 
ried out toward a definite side. The cephahc region of the 



auditory pit 

sinus resion 

lateral mesoderm- 
lateral body fold 

unsegmented dorsal 


optic vesicle 

margin of 
head fold of amnion 

bulbo-conus arteriosus 

ventricular region 
atrial region 
omphalomesenteric vein 

vascular plexus 

oipphalo mesenteric 

neural tube 

primitive plate 

Fig. 29. — Dorsal view ( X 14) of entire chick embryo having 19 pairs of 
somites (about 43 hours incubation). Due to torsion the cephalic region appears 
in dextro-dorsal view. 

embryo is twisted in such a manner that the left side comes to 
lie next to the yolk and the right side away from the yolk. 
The progress of torsion caudad is gradual and the posterior 
part of the embryo remains prone on the yolk for a considerable 
time after torsion has been completed in the head region. Fig- 
ure 22 shows the head of an embryo of about 38 hours in which 
the cranial flexure and torsion are just becoming evident. In 
chicks of about 43 hours (Fig. 29) the further progress of both 
flexion and torsion is well marked. 

The processes of flexion and torsion thus initiated continue 


until the original orientation of the chick on the yolk is com- 
pletely changed. As the body of the embryo becomes turned 
on its side the yolk no longer impedes the progress of flexion. 
Following the accomplishment of torsion in the cephaUc region, 
the cranial flexure becomes rapidly greater until the head is 
practically doubled on itself (Fig. 34). As development pro- 
ceeds, torsion progresses caudad involving more and more of 
the body of the embryo. Finally the entire embryo comes to 
lie with its left side on the yolk. Concomitant with the progress 
of torsion, flexion also appears farther caudally, affecting in 
turn the cervical, dorsal, and caudal regions. The series of 
flexions which accompany torsion bend the head and tail of 
the embryo ventrally so that its spinal axis becomes C-shaped 
(Fig. 40). The flexions which bend the embryo on itself so 
the head and tail lie close together are characteristic of all 
amniote embryos. The torsion which in the chick accompanies 
flexion is correlated with the fact that it develops on the surface 
of a large yolk. 

The Completion of the Vitelline Circulatory Channels. — In 
chicks of $$ to 36 hours the omphalomesenteric veins have been 
established as postero-lateral extensions of the same endocardial 
tubes which are involved in the formation of the heart. As 
the omphalomesenteric veins are extending laterad, the vessels 
developing in the vitelline plexus are extending and converging 
toward the embryo. Eventually the vitelline vessels attain 
communication with the heart by becoming confluent with the 
omphalomesenteric veins. This establishes the afferent chan- 
nels of the vitelline circulation. 

The vessels destined to carry blood from the embryo to the 
vitelline plexus develop in embryos of about 40 hours (Fig. 29). 
Like the afferent vitelline channels, the efferent channels have 
a dual origin. The proximal portions of the efferent channels 
arise within the embryo as branches of the dorsal aortae, and 
extend peripherally. The distal portions of the channels arise 
in the extra-embryonic vascular area and extend toward the 
embryo. The efferent vitelHne vessels are estabhshed when 
these two sets of channels become confluent. In its early stages 
the connection is through a network of small channels rather 
than definite vessels, the aortae breaking up posteriorly into 
, small channels some of which communicate laterally with the 


extra-embryonic plexus. Later some of these channels become 
confluent, others disappear, and gradually definite main vessels, 
the omphalomesenteric arteries, are estabHshed. For some 
time after their formation, the omphalomesenteric arteries are 
Hkely to retain traces of their origin from a plexus of small 
channels and arise from the aorta by several roots (Fig. 35). 

The Beginning of the Circulation of Blood. — At about 44 
hours of incubation, coincident with the completion of the 
vitelline vessels, the heart begins regular contraction, and the 
blood which has been formed in the extra-embryonic vascular 
area is for the first time pumped through the vessels of the 
embryo. In tracing the course of either the embryonic or the 
vitelline circulation the heart is the logical starting point. 
From the heart the blood of the extra-embryonic vitelline circu- 
lation passes through the ventral aortae, along the dorsal aortae, 
and out through the omphalomesenteric arteries to the plexus 
of vessels on the yolk. 

In the small vessels which ramify in the membranes envelop- 
ing the yolk the blood absorbs food material. In young 
embryos, before the allantoic circulation has appeared, the 
vitelHne circulation is involved also in the oxygenation of the 
blood. The great surface exposure presented by the multitude 
of small vessels on the yolk makes it possible for the blood to 
take up oxygen which penetrates the porous shell and the 

After acquiring food material and oxygen the blood is 
collected by the sinus terminalis and the vitelline veins. The 
vitelline veins converge toward the embryo from all parts of 
the vascular area and empty into the omphalomesenteric veins 
which return the blood to the heart (Fig. 48) . 

The blood of the intra-embryonic circulation, leaving the 
heart enters the ventral aortae, thence passes into the dorsal 
aortae, and is distributed through branches from the dorsal 
aortae to the body of the embryo. It is returned from the 
cephalic part of the body by the anterior cardinals, and from 
the caudal part of the body by the posterior cardinals. The 
anterior and posterior cardinals discharge together through the 
ducts of Cuvier into the sinus region of the heart (Fig. 24). 

In the heart, the blood of the extra-embryonic circulation 
and of the intra-embryonic circulation is mixed. The mixed 


blood in the heart is not as rich in oxygen and food material as 
that which comes to the heart from the vitelhne circulation 
nor as low in food and oxygen content as that returned to the 
heart from the intra-embryonic circulation where these ma- 
terials are drawn upon by the growing tissues of the embryo. 
Nevertheless it carries a sufficient proportion of food and oxygen 
so that as it is distributed to the body of the embryo it serves to 
supply the growing tissues. 



The folding off of the body of the embryo; the establish- 

The Folding off of the Body of the Embryo. — In bird embryos 
the somatopleure and splanchnopleure extend over the yolk 
peripherally, beyond the region where the body of the embryo 
is being formed. Distal to the body of the embryo the layers 
are termed extra-embryonic. At first the body of the chick has 
no definite boundaries and consequently embryonic and extra- 
embryonic layers are directly continuous without there being 
any definite boundary at which we may say one ends and the 
other begins. As the body of the embryo takes form, a series 
of folds develop about it, undercut it, and finally nearly separate 
it from the yolk. The folds which thus definitely estabHsh the 
boundaries between intra-embryonic and extra-embryonic 
regions are known as the limiting body folds or simply the body 

The first of the body folds to appear is the fold which marks 
the boundary of the head. By the end of the first day of incu- 
bation the head has grown anteriorly and the fold originally 
bounding it appears to have undercut and separated it anteriorly 
from the blastoderm (Figs. 15 and 17, E). The cephalic limit- 
ing fold at this stage is crescentic, concave caudally. As this 
fold continues to progress caudad, its posterior extremities 
become continuous with folds which develop along either side of 
the embryo. Because of the fact that these folds bound 
the body of the embryo laterally, they are known as the lateral 
bod}' folds (lateral hmiting sulci). The lateral body folds, at 
first shallow (Fig. 28, D) become deeper, undercutting the body 
of the embryo from either side and further separating it from 
the yolk (Fig. 36, £ and Fig. 30). 



During the third day a fold appears bounding the posterior 
region of the embryo (Fig. 31, C). This caudal fold undercuts 
the tail of the embryo forming a sub caudal pocket just as the 
sub-cephaHc fold undercuts the head. The combined effect of 
the development of the sub-cephahc, lateral body, and the sub- 
caudal folds is to constrict off the embryo more and more from 
the yolk (Figs. 30 and 32). These folds which establish the 
contour of the embryo indicate at the same time the boundary 
between the tissues which are built into the body of the embryo, 
and the so-called extra-embryonic tissues which serve temporary 
purposes during development but are not incorporated in the 
structure of the adult body. 

The Establishment of the Yolk-sac and the Delimitation of 
the Embryonic Gut. — The extra-embryonic membranes of the . 
chick are four in number, the yolk-sac, the amnion, the serosa 
and the allantois. The yolk-sac is the first of these to make its 
appearance. The splanchnopleure of the chick instead of 
forming a closed gut, as happens in forms with little yolk, 
grows over the yolk surface. The primitive gut has a cellular 
wall dorsally only, while the yolk acts as a temporary floor 
(Fig. 31, ^). The extra-embryonic extension of the splanchno- 
pleure eventually forms a sac-like investment for the yolk 
(Figs. 30 and 32). 

Concomitant with the spreading of the extra-embryonic 
splanchnopleure about the yolk, the intra-embryonic splanchno- 
pleure is undergoing a series of changes which result in the 
establishment of a completely walled gut in the body of the 
embryo. The interrelations of the various steps in the forma- 
tion of the gut and of the yolk-sac make it necessary to repeat 
some points and anticipate other points concerning the forma- 
tion of the gut, in order that their relation to yolk-sac formation 
may not be overlooked. 

It will be recalled that the first part of the primitive gut to 
acquire a cellular floor is its cephalic region. The same folding 
process by which the head is separated from the blastoderm 
involves the entoderm of the gut. The part of the primitive 
gut which acquires a floor as the sub-cephalic fold progresses 
caudad is termed the fore-gut (Fig. 31, B). During the third 
day of incubation the caudal fold undercuts the posterior end of 
the embryo. The splanchnopleure of the gut is involved 




lateral amniotic fold 
lateral body fold 

ex -embryonic 

ectoderm ^ 
mesoderm J 





amniotic cavity 

amniotic fold 

/ somatopleure) 


allantois ( splanchnopleure ) 
yolk stalk 

nopleure \ 


vitelline membrane 

Fig. 30. 



allantoic cavity 





/ splanchno- 
pleure ) 


allantoic cavity 







belly stalk 

Fig. 30. — Schematic diagrams to show the extra-embryonic membranes 
of the chick. {After Duval.) The diagrams represent longitudinal sections 
through the entire egg. The body of the embryo, being oriented approximately 
at right angles to the long-axis of the egg, is cut transversely. 

A, embryo of about two days incubation; B, embryo of about three days 
incubation; C, embryo of about five days incubation; D, embryo of about fourteen 
days incubation. 


in the progress of the sub-caudal fold so that a hind-gut is 
established in a manner analogous to the formation of the fore- 
gut (Fig. 31, C). The part of the gut which still remains open 
to the yolk is known as the mid-gut. As the embryo is con- 
stricted off from the yolk by the progress of the sub-cephalic 
and sub-caudal folds, the fore-gut and hind-gut are increased in 
extent at the expense of the mid-gut. The mid-gut is finally 
diminished until it opens ventrally by a small aperture which 
flares out, like an inverted funnel, into the yolk-sac (Fig. 31, Z)). 
This opening is the yolk duct and its wall constitutes the yolk 

The walls of the yolk-sac are still continuous with the walls 
of the gut along the constricted yolk-stalk thus formed, but the 
boundary between the intra-embryonic splanchnopleure of the 
gut and the extra-embryonic splanchnopleure of the yolk-sac 
can now be established definitely at the yolk-stalk. 

As the neck of the yolk-sac is constricted the omphalomesen- 
teric arteries and omphalomesenteric veins, caught in the same 
series of foldings, are brought together and traverse the yolk- 
stalk side by side. The vascular network in the splanchno- 
pleure of the yolk-sac which in young chicks was seen spreading 
over the yolk eventually nearly encompasses it. The embryo's 
store of food material thus comes to be suspended from the gut 
of the mid-body region in a sac provided with a circulatory arc 
of its own, the vitelline arc. Apparently no yolk passes directly 
through the yolk-duct into the intestine. Absorption of the 
yolk is effected by the epithelium of the yolk-sac and the food 
material is transferred to the embryo by the vitelline circula- 
tion. In older embryos (Fig. 30, C and D) the epithelium of 
the yolk-sac undergoes a series of foldings which greatly increase 
its surface area and thereby the amount of absorption it can 

During development the albumen loses water, becomes 
more viscid , and rapidly decreases in bulk. The growth of the 
allantois, an extra-embryonic structure which we have yet to 
consider, forces the albumen toward the distal end of the yolk- 
sac (Fig. 30, D). The manner in which the albumen is encom- 
passed between the yolk-sac and folds of the allantois and 
serosa belong to later stages of development than those with 
which we are concerned. Suffice it to say that the albumen 



ectoderm of neural plate 
ectoderm of blastoderm 

primitive pit 

primitive streak 



w&mmm^^^'^^mi^ii'^f^:^ ? '^ 


neural tube 
ectoderm of head 

subcephalic pocket 

of yolk-sac 

open neural groove 
primitive pit 

B pericardial region ' anterior intestinal 

of coelom 



subcephalic pocket 


•» ■d*'do*<'o''. 

antenor posterior 

intestinal portal intestinal portal 


subcaudal pocket 

)- amnion 
— extra-embryonic 
■3^:5;;^ coelom 

of yolk-sac 

post-anal gut 


of yolk-sac 

allantoic bud 
yolk- stalk 

Fig. 31. — Schematic longitudinal-section diagrams of the chick showing: 
four stages in the formation of the gut tract. The embryos are represented as 
unaffected by torsion. 

A, chick toward the end of the first day of incubation; no regional differentia- 
tion of primitive gut is as yet apparent. B, toward the end of the second day^ 
fore-gut established. C, chick of about three days; fore-gut, mid-gut and hind- 
gut established. D, chick of about four days; fore-gut and hind-gut increased 
in length at expense of mid-gut; yolk-stalk formed. 


like the yolk, is surrounded by extra-embryonic membranes by 
which it is absorbed and transferred over the extra-embryonic 
circulation to the embryo. 

Toward the end of the period of incubation, usually on the 
19th day, the remains of the yolk-sac are enclosed within the 
body walls of the embryo. After its inclusion in the embryo 
both the wall and the remaining contents of the yolk-sac 
rapidly disappear, their absorption being practically completed 
in the first six days after hatching. 

The Amnion and the Serosa. — The amnion and the serosa 
are so closely associated in their origin that they must be con- 
sidered together. Both are derived from the extra-embryonic 
somatopleure. The amnion encloses the embryo as a saccular 
investment and the cavity thus formed between the amnion 
and the embryo becomes filled with a watery fluid. Suspended 
in this amniotic fluid, the embryo is free to change its shape 
and position, and external pressure upon it is equalized. Mus- 
cle fibers develop in the amnion, which by their contraction 
gently agitate the amniotic fluid. The movement thus im- 
parted to the embryo apparently aids in keeping it free and 
preventing adhesions and resultant malformations. 

The first indication of amnion formation appears in chicks 
of about 30 hours incubation. The head of the embryo sinks 
into the yolk somewhat, and at the same time the extra-embry- 
onic somatopleure anterior to the head is thrown into a fold, 
the head fold of the amnion (Fig. 32,-4). In dorsal aspect the 
margin of this fold is crescentic in shape with its concavity 
directed toward the head of the embryo. The head fold of the 
amnion must not be confused with the sub-cephalic fold which 
arises earlier in development and undercuts the head. 

As the embryo increases in length its head grows anteriorly 
into the amniotic fold. Growth in the somatopleure itself 
tends to extend the amniotic fold caudad over the head of the 
embryo (Fig. 32, B). By continuation of these two growth 
processes the head soon comes to lie in a double walled pocket 
of extra-embryonic somatopleure which covers the head like a 
cap (Fig. 29). The free edge of the amniotic pocket retains 
its original crescentic shape as, in its progress caudad, it covers 
more and more of the embryo. 


The caudally-directed limbs of the head fold of the amnion 
are continued posteriorly along either side of the embryo as 
the lateral amniotic folds. The lateral folds of the amnion 
grow dorso-mesiad, eventually meeting in the mid-line dorsal 
to the embryo (Fig. 30, A-C). 

During the third day, the tail-fold of the amnion develops 
about the caudal region of the embryo. Its manner of de- 
velopment is similar to that of the head fold of the amnion 
but its direction of growth is reversed, its concavity being 
directed anteriorly and its progression being cephalad (Fig. 
32, B, C). 

Continued growth of the head, lateral, and tail folds of the 
amnion results in their meeting above the embryo. At the 
point where the folds meet, they become fused in a scar-like 
thickening termed the amniotic raphe (sero-amniotic raphe). 
(Fig. 32, C). The way in which the somatopleure has been 
folded about the embryo leaves the amniotic cavity completely 
lined by ectoderm which is continuous with the superficial 
ectoderm of the embryo at the region where the yolk-stalk 
enters the body (Fig. 30, D). 

All the amniotic folds involve doubling the somatopleure on 
itself. Only the inner layer of the somatopleuric fold is in- 
volved in the formation of the amniotic cavity. The outer 
layer of somatopleure becomes the serosa (Fig. 30, B). The 
cavity between serosa and amnion (sero-amniotic cavity) is part 
of the extra-embryonic coelom. The continuity of the extra- 
embryonic coelom with the intra-embryonic ccelom is most 
apparent in early stages (Fig. 30, A and B). They remain, 
however, in open communication in the yolk-stalk region until 
relatively late in development. 

The rapid peripheral growth of the somatopleure carries the 
serosa about the yolk-sac, which it eventually envelops. The 
albumen-sac also is surrounded by folds of serosa, and the 
allantois after its establishment develops within the serosa, 
between it and the amnion. Thus the serosa eventually 
encompasses the embryo itself and all the other extra-embryonic 
membranes. The relationships of the serosa and allantois 
and the functional significance of the serosa will be taken up 
after the allantois has been considered. 


















































































^ ^ 

















y « a, 



"g g 


The Allantois. — The allantois differs from the amnion and 
serosa in that it arises primarily within the body of the embryo. 
Its proximal portion is intra-embryonic throughout develop- 
ment. Its distal portion, however, is carried outside the con- 
fines of the intra-embryonic coelom and becomes associated with 
the other extra-embryonic membranes. Like the other extra- 
embryonic membranes the distal portion of the allantois 
functions only during the incubation period and is not incorpor- 
ated into the structure of the adult body. 

The allantois first appears late in the third day of incubation. 
It rises as a diverticulum from the ventral wall of the hind-gut 
and its walls are, therefore, splanchnopleure. Its relationships 
to structures within the embryo will be better understood when 
chicks of three and four days incubation have been studied, but 
its general location can be appreciated from the schematic 
diagrams of Figures 32 and 33. 

During the fourth day of development the allantois pushes 
out of the body of the embryo into the extra-embryonic coelom. 
Its proximal portion Hes parallel to the yolk-stalk and just 
caudal to it. When the distal portion of the allantois has 
grown clear of the embryo it becomes enlarged (Fig. 32, C). 
Its narrow proximal portion is known as the allantoic stalk, 
the enlarged distal portion as the allantoic vesicle. Fluid 
accumulating in the allantois distends it so the appearance of 
its terminal portion in entire embryos is somewhat balloon-like 
(Fig. 40). 

The allantoic vesicle enlarges very rapidly from the fourth 
to the tenth day of incubation. Extending into the sero- 
amniotic cavity it becomes flattened and finally encompasses 
the embryo and the yolk-sac (Fig. 30, C, D). In this process 
the mesodermic layer of the allantois becomes fused with the 
adjacent mesodermic layer of the serosa. There is thus formed 
a double layer of mesoderm, the serosal component of which is 
somatic mesoderm and the allantoic component of which is 
splanchnic mesoderm. In this double layer of mesoderm an 
extremely rich vascular network develops which is connected 
with the embryonic circulation by the allantoic arteries and 
veins. It is through this circulation that the allantois carries 
on its primary function of oxygenating the blood of the embryo 
and relieving it of carbon dioxide. This is made possible by the 



position occupied by the allantois, close beneath the porous 
shell (Fig. 30). In addition to its primary respiratory function 
the allantois serves as a reservoir for the secretions coming from 

neural tube 

amniotic cavity 

sero-amniotic cavity 
hind- gut 


' f« 

neural tube - 
notochord - 

mesenchyme :^'~*-^"'~ -"*^« ^V- 

mesoderm • 

yolk stalk If"'- If 


If 11 








yolk-sac-p^p^^ ^" J.^'^'^v;^^:^*,^ 



Mf , a'^ «* jr\ •'. -f ' d^'6'- '*■'''■ ," " ' 


u j^^;jjj^:^£,^^m 

^ . 

,0 -0: 

amniotic cavity 

. cloaca 1 





Pig. 33. — Schematic longitudinal-section diagrams of the caudal half of the 
embryo to show the formation of the allantois. 
A, chick of about three days incubation; B, chick of about four lays in- 

the developing excretory organs and also takes part in the ab- 
sorption of the albumen. 

The fusion of the allantoic mesoderm and blood vessels 


with the serosa is of particular interest because of its homology 
with the establishment of the chorion in the higher mammals.^ 
The chorion of mammalian embryos arises by the fusion of 
allantoic vessels and mesoderm with the inner wall of the 
serosa, and constitutes the embryos's organ of attachment to 
the uterine wall. In mammalian embryos the allantoic, or 
umbiUcal circulation as it is usually called in mammals, serves 
more than a respiratory function. In the absence of any 
appreciable amount of yolk, the mammalian embryo derives its 
nutrition through the allantoic circulation from the uterine 
blood of the mother. Thus the mammalian allantoic circula- 
tion carries out the functions which in the chick are divided 
between the vitelhne and the allantoic circulations. 

* By reason of this homology the serosa of the chick is sometimes called chorion. 
It seems less likely to lead to confusion if the use of the term chorion is re- 
stricted to mammalian forms, especially as the serosa alone is the homologue 
of only part of the mammalian chorion. In some books the term outer or false 
amnion will be found used to designate the structure called serosa in this book. 
The term false amnion is not, however, in general use in this country. 



I. External Features. 
II. The Nervous System. 

Growth of the telencephahc region; the epiphysis; the 
infundibulum and Rathke's pocket; the optic vesicles; 
the lens; the posterior part of the brain and the cord 
region of the neural tube; the neural crest. 

III. The Digestive Tract. 

The fore-gut; the stomodaeum; the pre-oral gut; the 
mid-gut; the hind-gut. 

IV. The Visceral Clefts and Visceral Arches. 
V. The Circulatory System. 

The heart; the aortic arches; the fusion of the dorsal 
aortae; the cardinal and omphalomesenteric vessels. 
VI. The Differentiation of the Somites. 
VII. The Urinary System. 

I. External Features 

In chicks which have been incubated from 50 to 55 hours 
(Fig. 34) the entire head region has been freed from the yolk 
by the progress caudad of the sub-cephalic fold. Torsion has 
involved the whole anterior half of the embryo and is completed 
in the cephalic region, so that the head now lies left side down 
on the yolk. The posterior half of the embryo is still in its 
original position, ventral surface prone on the yolk. At the 
extreme posterior end, the beginning of the caudal fold marks 
off. the tail region of the embryo from the extra-embryonic mem- 
branes. The head fold of the amnion has progressed caudad, 
together with the lateral amniotic folds impocketing the em- 
bryo nearly to the level of the omphalomesenteric arteries. 

The cranial flexure, which was seen beginning in chicks of 
about 38 hours, has increased rapidly until at this stage the 
brain is bent nearly double on; itself. The axis of the bending 




being in the mid-brain region, the mesencephalon comes 
to be the most anteriorly located part of the head and the 
prosencephalon and myelencephalon lie opposite each other, 
ventral surface to ventral surface (Fig. 34). The original an- 
terior end of the prosencephalon is thus brought in close 
proximity to the heart, and the optic vesicles and the auditory 
vesicles are brought opposite each other at nearly the same 
antero-posterior level. 


metencephaMc region 
dorsal aortic root 
myelencephahc region 

hyomandibular cleft 
auditory vesicle 
aortic archill 

anL int. nnyfal 

optic cup 


choroid fissure 



lateral mesoderm 
marginof amnion 
lateral body fold 

neural tube 
,29th somite 


caudal fold 

Pig. 34. — Dextro-dorsal view ( X 14) of entire embryo of 29 somites (about 
55 hours incubation). 

At this stage flexion has involved the body farther caudally 
as well as in the brain region. It is especially marked at 
about the level of the heart in the region of transition from 
myelencephalon to spinal cord. Since this is the future neck 
region of the embryo the flexure at this level is known as the 
cervical flexure (Fig. 34). 


II. The Nervous System 

Growth of the Telencephalic Region. — The completion of 
torsion in the head region causes rapid changes in the configura- 
tion of the brain as seen in entire embryos from 40 to 50 hours 
of incubation. The same fundamental regions can, however, 
be identified throughout this range of development. The an- 
terior part of the brain has undergone rapid enlargement. A 
slight constriction in the dorsal wall (Fig. 35) indicates the 
impending division of the prosencephalon into telencephalon 
and diencephalon. Except for its considerable increase in size 
no important changes have taken place in the telencephalic 

The Epiphysis. — In the mid-dorsal waU of the diencephalic 
region a small evagination has appeared. This evagination is 
the epiphysis (Fig. 34 and 35). It is destined to become dif- 
ferentiated into the pineal gland of the adult. 

The Infimdibulum and Rathke's Pocket. — In the floor of the 
diencephalon the infundibular depression has become deepened 
and Hes close to a newly formed ectodermal invagination known 
as Rathke's pocket (Fig. 35). The epithelium of Rathke's 
pocket is destined to be separated from the superficial ectoderm 
and to become permanently associated with the infundibular 
portion of the diencephalon to form the hypophysis or pituitary 

The Optic Vesicles. — The optic vesicles have undergone 
changes which completely alter their appearance. In 33-hour 
chicks they are spheroidal vesicles connected by broad stalks 
with the lateral walls of the diencephalon (Fig. 21). At this 
stage the lumen of each optic vesicle (opticoele) is widely con- 
tinuous with the lumen of the prosencephalon (prosoccele) 
(Fig. 28, A). The constriction of the optic stalk which begins 
to be apparent in 38-hour embryos (Fig. 22) is much more 
marked in 55-hour chicks. 

The most striking and important advance in their develop- 
ment is the invagination of the distal ends of the single-walled 
optic vesicles to form double walled optic cups (Fig. ^6, B). 
The concavities of the cups are directed laterally. Mesially 
the cups are continuous with the ventro-lateral walls of the 
diencephalic region of the original prosencephalon over the 



narrowed optic stalks. The invaginated layer of the optic cup 
is termed the sensory layer because it is destined to give rise 
to the sensory layer of the retina. The layer against which 

choroid fissure 
Rathke's pocket 

ventral aortic root- 

anterior intestinal 


cut ectoderm 


anterior cardinal vein 

neuromere of 

auditory vesicle 

aortic arches I. II, III. 

duct of Cuvier 
posterior cardinal vein 
dorsal aorta 

omphalomesenteric vein 

cut splanchnopleure 
cut somatopleure 

roots of oinphal( 
mesenteric artery 

lateral mesoderm 

om phjjomesenter ic 

posterior intestinal 

Fig. 35. — Diagram of dissection of chick of about 50 hours. (Modified from 
Prentiss.) The splanchnopleure of the yolk-sac cephalic to the anterior in- 
testinal portal, the ectoderm of the left side of the head, and the mesoderm in 
the pericardial region have been dissected away. A window has been cut in 
the splanchnopleure of the dorsal wall of the mid-gut to show the origin of the 
omphalomesenteric arteries. 

the sensory layer comes to lie after its invagination is termed 
the pigment layer because it gives rise to the pigmented layer 
of the retina. The double-walled cups formed by invagination, 



are also termed secondary optic vesicles in distinction to prim- 
ary optic vesicles, as they are called before the invagination. 
The formerly capacious lumen of the primary optic vesicle is 

visceral furrow 

sero- amniotic 


intra-embryonic coelom 

dorsal mesocardium 
sero-amniotic raphe 


epi-myocardium of 



vitelline vessels 
extra-embryonic coelom 


neural crest 

dorsal aorta 

post, cardinal v. 

•embryonic coelom 
intra-embryonic coelom 
omphalomesenteric vein 

lateral amniotic fold 

mesonephric duct 
mesonephric tubule 

body fold 

telline vessels 

mesonephric duct '' 

mesonephric tubule 

post, cardinal 
dorsal aorta 

Fig. 36. — Diagrams of transverse sections of 5S-hour (30-somite) chick. The 
location of the sections is indicated on an outline sketch of the entire embryo. 

practically obliterated in the formation of the optic cup. What 
remains of the primary opticoele is now but a narrow space be- 


tween the sensory and the pigment layers of the retina (Fig. 
36, B). ■ Later when these two layers fuse this space is entirely 

While the secondary optic vesicles are usually spoken of as 
the optic cups, they are not complete cups. The invagination 
which gives rise to the secondary optic vesicles, instead of be- 
ginning at the most lateral point in the primary optic vesicles, 
begins at a point somewhat toward their ventral surface and is 
directed mesiodorsad. As a result the optic cups are formed 
without any lip on their ventral aspect. They may be likened 
to cups with a segment broken out of one side. This gap in 
the optic cup is the choroid fissure (Fig. 35). In Figure 36, By 
a section is shown which passes through the head of the embryo 
on a slight slant so that the right optic cup, being cut to one 
side of the choroid fissure appears complete while the left optic 
cup being cut in the region of the fissure shows no ventral lip. 

The infolding process by which the optic cups are formed 
from the primary optic vesicles is continued to the region of 
the optic stalks. As a result the optic stalks are infolded so 
that their ventral surfaces become grooved. Later in develop- 
ment the optic nerves and blood vessels come to lie in the 
grooves thus formed in the optic stalks. 

The Lens. — The lens of the eye arises independently of the 
optic vesicles, from the superficial ectoderm of the head. The 
first indications of lens formation appear in chicks of about 
40 hours as local thickenings of the ectoderm immediately over- 
lying the optic vesicles. These placodes of thickened ectoderm 
sink below the general level of the surface of the head to form 
small vesicles which extend into the secondary optic vesicles. 
Their opening to the surface is rapidly constricted and even- 
tually they are disconnected altogether from the superficial 
ectoderm. At this stage the opening to the outside still persists 
although it is very small (Fig. 36, B, right eye). In sections 
which do not pass directly through the opening, the lens vesi- 
cle appears completely separated from the overlying ectoderm 
(Fig. 36, B, left eye). 

The derivation of the lens from a placode of thickened epi- 
thelium which sinks below the general surface, and eventually 
loses its connection with the superficial ectoderm, is strikingly 
similar to the early steps in the derivation of the auditory 


vesicle. But these primordia once separated from the ectoderm 
follow divergent lines of differentiation leading to adult condi- 
tions which are structurally and functionally totally unlike. 
The origin of these two structures from cell groups similarly 
folded off from the same germ layer, but which once established 
undergo each their own characteristic differentiation, exempli- 
fies a sequence of events so characteristic of developmental 
processes in general as to call for at least a comment in passing. 

The Posterior Part of the Brain and the Cord Region of the 
Neural Tube. — Caudal to the diencephalon the brain shows no 
great change as compared with the last stages considered. The 
mesencephalon is somewhat enlarged and the constrictions 
separating it from the diencephalon cephalically and the 
metencephalon caudally are more sharply marked. The meten- 
cephalon is more clearly marked off from the myelencephalon 
and its roof is beginning to show thickening. In the myelen- 
cephalon the neuromeric constrictions are still evident in 
the ventral and lateral walls (Figs. 34 and 35). The dorsal wall 
has become much thinner than the ventral and lateral walls 
(Fig. 36, A and B) and shows no trace of division between the 

In the cord region of the neural tube the lateral walls have 
become thickened at the expense of the lumen so that the 
neural canal appears slit-like in sections of embryos of this age 
(Fig. 36, £) rather than elliptical as it is immediately after 
the closure of the neural folds. At this stage the closure of 
the neural tube is completed throughout its entire length. The 
last regions to close were at the cephaHc and caudal ends of the 
neural groove. In younger stages where they remained open 
these regions were known as the anterior neuropore and the 
sinus rhomboidalis, respectively. 

The Neural Crest.— In the closure of the neural tube the 
superficial ectoderm which at first lay on either side of the 
neural groove, continuous with the neural plate ectoderm^ 
becomes fused in the mid-line and separated from the neural 
plate to constitute an unbroken ectodermal covering (Cf. Figs. 
17, Bf and 28, B). At the same time the lateral margins of the 
neural plate become fused to complete the neural tube. There 
are cells lying originally at the edges of the neural folds which 
are not involved in the fusion of either the superficial ectoderm 



or the neural plate. These cells form a pair of longitudinal 
aggregations extending one on either side of the mid-dorsal 
line in the angles between the superficial ectoderm and the 
neural tube (Fig. 37, A). With the fusion of the edges of the 
neural folds to complete the neural tube, and the fusion of the 
superficial ectoderm dorsal to the neural tube, these two longi- 
tudinal cell masses become for a time confluent in the mid-line 

neural tube 

neural tube 

Pig. 37. — Drawings from transverse sections to show origin of neural crest 
cells. The location of the area drawn is indicated on the small sketch to the 
left of each drawing. 

A, anterior rhombencephalic region of 30-hour chick; B, posterior rhomb- 
encephalic region of 36-hour chick; C, mid-dorsal region of cord in 5S-hour 

(Fig. 37, B). But because this aggregation of cells arises from 
paired components and soon again separates into right and left 
parts it is to be considered as potentially paired. On account 
of its position dorsal to the neural tube it is known as the neural 

The neural crest should not be confused with the margin of 


the neural fold with which it is associated before the closure 
of the neural tube. The margin of the neural fold involves 
cells which go into the superficial ectoderm and into the neural 
tube, as well as those which are concerned in the formation of 
the neural crest. 

When first established the neural crest is continuous antero- 
posteriorly. As development proceeds, the cells of the neural 
crest migrate ventro-laterally on either side of the spinal cord 
(Fig. 37, C), and at the same time become segmen tally clus- 
tered. The segmentally arranged cell groups thus derived from 
the neural crest give rise to the dorsal root ganglia of the spinal 
nerves, and in the head region to the ganglia of the sensory 
cranial nerves. (For a later stage of the dorsal root ganglia see 
Figure 44.) 

in. The Digestive Tract 

The Fore-gut. — The manner in which the three primary 
regions of the gut-tract are estabUshed has already been con- 
sidered in a general way (see Chapter XI and Fig. 31). In 
50 to 55-hour chicks the fore-gut has acquired considerable 
length. It extends from the anterior intestinal portal cephalad 
almost to the infundibulum (Fig. 35). 

As the first region of the tract to be established, the fore-gut 
is naturally the most advanced in differentiation. We can 
already recognize a pharyngeal and an oesophageal portion. 
The pharyngeal region lies ventral to the myelencephalon and 
is encircled by the aortic arches (Fig. 35). The pharynx is 
somewhat flattened dorso-ventrally and has a considerably 
larger lumen than the oesophageal part of the fore-gut (Cf . Fig. 
36, B and C). 

The Stomodaeum.^There is at this stage no mouth opening 
into the pharynx. However, the location where the opening 
will be formed is indicated by the approximation of a ventral 
outpocketing near the anterior end of the pharynx, to a depres- 
sion formed in the adjacent ectoderm of the ventral surface of 
the head (Fig. 35). The ectodermal depression, known as the 
stomodaeum, deepens until its floor lies in contact with the ento- 
derm of the pharyngeal out-pocketing (Fig. 35). The thin 
layer of tissue formed by the apposition of the stomodaeal ecto- 
derm to the pharyngeal entoderm is known as the oral plate. 


Later in development the oral plate breaks thiough bringing 
the stomodaeum and the pharynx into open communication. 
Growth of surrounding structures deepens the original stomodaeal 
depression, and it becomes the oral cavity. The region of the 
oral plate in the embryo becomes, in the adult, the region of 
transition from oral cavity to pharynx. 

The Pre-oral Gut. — It will be noted by reference to Figure 
35 that the oral opening is not established at the extreme 
cephalic end of the pharynx. The part of the pharynx which 
extends cephalic to the mouth opening is known as the pre-oral 
gut. After the rupture of the oral plate, the pre-oral gut 
eventually disappears, but an indication of it persists for a time 
as a small diverticulum termed SeesselFs pocket(Cf.Figs. 35 
and 43). 

The Mid-gut. — Although the mid-gut is still the most ex- 
tensive of the three primary divisions of the digestive tract, 
it presents little of interest. It is nothing more than a region 
where the gut still lies open to the yolk. It does not have 
even a fixed identity. As fast as any part of the mid-gut 
acquires a ventral wall by the closing-in process involved in 
the progress of the subcephalic and subcaudal folds it ceases to 
be mid-gut and becomes fore-gut or hind-gut. Differentiation 
and local specializations appear in the digestive tract only in 
regions which have ceased to be mid-gut. 

The Hind-gut. — The hind-gut first appears in embryos of 
about 55 hours (Fig. 35). The method of its formation is 
similar to that by which the fore-gut was estabhshed. The 
sub-caudal fold undercuts the tail region and walls off a gut 
pocket. The hind-gut is lengthened at the expense of the 
mid-gut as the sub-caudal fold progresses cephalad and is 
also lengthened by its own growth caudad. It shows no local 
specializations until later in development. 

IV. The Visceral Clefts and Visceral Arches 

At this stage the chick embryo has unmistakable visceral 
arches and visceral clefts. Although only transitory, they are 
morphologically of great importance not only from the com- 
parative view point, and because of their significance as struc- 
tures exemplifying recapitulation, but also because of their 


participation in the formation of the embryonic arterial system, 
of some of the ductless glands, of the eustachian tube, and of 
the face and jaws. 

The visceral clefts are formed by the meeting of ectodermal 
depressions, the visceral furrows, with diverticula from the 
lateral walls of the pharynx, the pharyngeal pouches. During 
most of the time the visceral furrows are conspicuous features 
in entire embryos, they may be seen in sections to be closed by 
a thin double layer of tissue composed of the ectoderm of the 
floor of the visceral furrow and the entoderm at the distal ex- 
tremity of the pharyngeal pouch (Fig. 36, A). The breaking 
through of this thin double layer of tissue brings the pharyngeal 
pouches into communication with the visceral furrows thereby 
establishing open visceral clefts. In birds an open condition of 
the clefts is transitory. In the chick the most posterior of the 
series of clefts never becomes open. Although some of the 
clefts never become open and others open for but a short time 
the term cleft is usually used to designate these structures which 
are potentially clefts, whether open or not. 

The position of the visceral clefts is best seen in entire em- 
bryos. They are commonly designated by number beginning 
with the first cleft posterior to the mouth and proceeding 
caudad. The first post-oral cleft appears earliest in develop- 
ment and is discernible at about 46 hours of incubation. Vis- 
ceral cleft II appears soon after, and by 50 to 55 hours three 
clefts have been formed (Fig. 34). 

Between adjacent visceral clefts, the lateral body walls about 
the pharynx are thickened. Each of these lateral thickenings 
in the mid-ventral line meets and merges with the corresponding 
thickening of the opposite side of the body. Thus the pharynx 
is encompassed laterally and ventrally by a series of arch-like 
thickenings, the visceral or gill arches. The visceral arches like 
the visceral clefts are designated by number, beginning at the 
anterior end of the styles. Visceral arch I lies cephalic to the 
first post-oral cleft, between it and the mouth region. Because 
of the part it plays in the formation of the mandible it is also 
designated as the mandibular arch. Visceral arch II is fre- 
quently termed the hyoid arch, and visceral cleft I, because of 
its position between the mandibular and hyoid arches, is known 
as the hyomandibular cleft. Posterior to the hyoid arch the 


visceral arches and clefts are ordinarily designated by their 
post-oral numbers only. 

There are other structures which are just beginning to be 
differentiated in the pharyngeal region and fore-gut of embryos 
of this stage, but it seems better to consider them in connection 
with later stages when their significance will be more readily 

V. The Circulatory System 

The Heart. — In embryos of 30 to 40 hours incubation we 
traced the expansion of the heart till it was bent to the right of 
the embryo In the form of a U-shaped tube (Figs. 19, 21, 23). 
The disappearance of the dorsal mesocardium except at its 
li posterior end, leaves the mid-region of the heart lying unat- 
' tached and extending to the right, into the pericardial region of 
the coelom. The heart is fixed with reference to the body of the 
embryo at its cephalic end where the ventral aortic roots lie 
embedded beneath the floor of the pharynx, and caudally in the 
sinus region where it is attached by the omphalomesenteric 
veins, by the ducts of Cuvier, and by the persistent portion of 
the dorsal mesocardium. 

During the period between 30 and 55 hours of incubation the 
heart itself is growing more rapidly than is the body of the 
embryo in the region where the heart lies. Since its cephalic 
and caudal ends are fixed, the unattached mid-region of the 
heart becomes at first U-shaped and then twisted on itself to 
form a loop. The atrial region of the heart is forced somewhat 
to the left, and the conus region is thrown across the atrial 
region by being twisted to the right and dorsally. The ven- 
tricular region constitutes the loop proper (Cf. Figs. 22, 29 and 
34). This twisting process reverses the original cephalo- 
caudal relations of the atrial and ventricular regions. Before 
the twisting, the atrial region of the heart was caudal to the 
ventricular region as it is in the adult fish heart. In the twist- 
ing of the heart the atrial region, by reason of its association 
with the fixed sinus region of the heart, undergoes relatively 
little change in position. The ventricular region is carried, over 
the dextral side of the atrium and comes to lie caudal to it, thus 
arriving in the relative position it occupies in the adult heart. 
The bending and subsequent twisting of the heart lead toward 


its division into separate chambers. As yet, however, no indi- 
cation of the actual partitioning off of the heart is apparent. It 
is still essentially a tubular organ through which the blood passes 
directly without any division into separate channels or currents. 

The Aortic Arches. — In 33 to 38 hour chicks the ventral 
aortae communicate with the dorsal aortae over a single pair of 
aortic arches which bend around the anterior end of the pharynx 
(Figs. 23 and 24) . With the formation of the visceral arches new 
aortic arches appear. The original pair of aortic arches comes 
to lie in the mandibular arch, and the new aortic arches are 
formed caudal to the first pair, one pair in each visceral arch. 
In chicks of 50 to 55 hours, three pairs of aortic arches have been 
established and a fourth is usually beginning to form (Figs. 
34, 35, and 36, A and 5). 

The Fusion of the Dorsal Aortae. — The dorsal aortae arise as 
vessels paired throughout their entire length (Fig. 23). As 
development progresses they fuse in the mid-line to form the 
unpaired dorsal aorta familiar in adult anatomy. This fusion 
takes place first at about the level of the sinus venosus and 
progresses thence cephalad and caudad. Cephalically it never 
extends to the pharyngeal region. Caudally the whole length 
of the aorta is eventually involved. At this stage the fusion 
has progressed caudad to about the level of the 14th somite 
(Figs. 34, 35, 36). 

The Cardinal and Omphalomesenteric Vessels. — The rela- 
tionships of the cardinal veins and the omphalomesenteric 
vessels are little changed from the conditions in 40 to 50 hour 
chicks. The posterior cardinals have elongated, keeping pace 
with the caudal progress of differentiation in the mesoderm. 
They lie just dorsal to the intermediate mesoderm in the angle 
formed between it and the somites (Fig. 36, D). The entrance 
of the omphalomesenteric veins into the sinus venosus, and the 
origin of the omphalomesenteric arteries from the dorsal aortae 
show little change from conditions familiar from the study of 
younger embryos. 

VI. The Differentiation of the Somites 

When the somites are first formed they consist of a 
nearly solid mass of cells derived from the dorsal mesoderm (Fig. 
sSj A). The cells composing them show a more or less radial 



neural fold 

ectoderm of head 


intermediate mesoderm 

somatic mesoderm 
splanchnic mesoderm 

epithelial layer of somite 

core of somite 

pronephric tubule 
(intermediate mesoderm) 

somatic mesoderm 

iplanchnic mesoderm 


epithelial layer of somite 

cavity of somite 
core of somite 
migrating cells 

posterior cardinal vein 
mesonephric duct 
mesonephric tubule 
dorsal aorta 

dorsal ganglion 

(neural crest) 




posterior cardinal vein 

mesonephric duct 
mesonephric tubule 

dorsal aorta 

intra-embryonic coelom 

extra-embryonic coelom 

Pig. 38. — Drawings from transverse sections to show the differentiation of the 

A, second somite of 4-somite chick; B, ninth somite of 12-somite chick; C, 
twentieth somite of 30-somite chick; D, seventeenth somite of 33-somite chick. 


arrangement. In the center of the somite a cavity is usually 
discernible. This cavity is at first extremely minute. In 
somites which have been recently formed it may be altogether 

As the somite becomes more sharply marked ofif the radial 
arrangement of the outer zone of cells appears more definitely 
(Fig. 38, B). The boundaries of the central cavity are con- 
siderably extended but its lumen is almost completely filled by 
a core of irregularly arranged cells. In sections which pass 
through the middle of the somite, this central core of cells is 
seen to arise from the lateral wall of the somite where it is 
continuous with the intermediate mesoderm. 

A little later in development the outer zone of cells on the 
ventro-mesial face of the somite loses its originally definite 
boundaries and becomes merged with the central core of cells. 
This ill-defined cell aggregation, known as the sclerotome, be- 
comes mesenchymal in characteristics, and extends ventro- 
mesiad from the somite of either side toward the notochord 
(Fig. 2)^, C and D). The cells of the sclerotomes of either side 
continue to converge about the notochord and later take part 
in the formation of the axial skeleton. 

Duting the formation of the sclerotome the dorsal part of 
the original outer cell-zone of the somite has maintained its 
definite boundaries and epithehal characteristics. The part of 
this outer zone which lies parallel to the ectoderm is known as 
the dermatome (Fig. 38, C and D). It later becomes asso- 
ciated with the ectoderm and forms the deeper layers of the 
integument, the ectoderm giving rise to the epithelial layer 

The dorso-mesial portion of the outer zone of the somite be- 
comes the myotome. It is folded somewhat laterad from its 
original position next to the neural tube (Fig. 2>^, C) and comes 
to lie ventro-mesial to the dermatome and parallel to it (Fig. 
38, D). (A later stage in the differentiation of the somite is 
shown in Figure 44) . The portion of the original cavity which 
persists for a time between the dermatome and myotome 
is termed the myocoele. The myotomes undergo the most 
extensive growth of any of the parts of the somite, giv- 
ing rise eventually to the entire skeletal musculature of the 


VII. The Urinary System 

In the section-diagrams of Figure 36, Z) and E, certain parts 
of the urinary system which have been established in chicks of 
50 to 55 hours will be found located and labeled. The urinary 
system is relatively late in becoming- differentiated. Only a 
few of the early steps in its formation can at this time be made 
out. Many structures which later become of great importance 
are not represented even by primordial cell aggregations. Ex- 
cept for those well grounded in comparative anatomy, any 
logical discussion of the structures which have appeared must 
anticipate much that occurs later in development. Consider- 
ation of the mode of origin and significance of the nephric 
organs appearing at this stage has, therefore, been deferred. 



1. External Features. 

Torsion; flexion; the visceral arches and clefts; the oral 
region; the appendage buds; the allantois. 
II. The Nervous System. 

Summary of development prior to the third day; the 
formation of the telencephaHc vesicles; the diencepha- 
lon; the mesencephalon; the metencephalon; the 
myelencephalon; the gangUa of the cranial nerves; 
the spinal cord; the spinal nerve roots. 

III. The Sense Organs. 

The eye; the ear; the olfactory organs. 

IV. The Digestive and Respiratory Systems. 

Summary of development prior to the third day; the 
establishment of the oral opening; the pharyngeal 
derivatives; the trachea; the lung-buds; the oesopha- 
gus and stomach; the liver; the pancreas; the mid- 
gut region; the cloaca; the proctodaeum and the cloa- 
cal membrane. 
V. The Circulatory System. 

The functional significance of the embryonic circulation; 
the vitelHne circulation; the allantoic circulation; the 
intra-embryonic circulation; the heart. 
VI. The Urinary System. 

The general relationships of pronephros, mesonephros, 
and metanephros; the pronephric tubules of the chick; 
the mesonephric tubules. 
VII. The Coelom and Mesenteries. 

I. External Features 

Torsion. — Chicks of three days incubation (Fig. 39) have 
been affected by torsion throughout their entire length. Tor- 
sion is complete well posterior to the level of the heart but 




the caudal portion of the embryo is not yet completely turned 
on its side. In four-day chicks the entire body has been 
turned through 90 degrees and the embryo lies with its left side 
on the yolk (Fig. 40). 


ganglion IX 
visceral cleft II 

aortic arch IV 


hyoid arch 
auditory vesicle / . hyomandibular cleft 

mandibular arch 
ganglion V 


ant. cardinal v. 


horoid fissure 
— lens 

sensory layer 
pigment layer 

appendage bud 

appendage bud 

vitelline artery 

Pig. 39. 

-Dextro-dorsal view ( X 14) of entire chick embryo of 36 somites 
(about three days incubation). 

Flexion. — The cranial and cervical flexures which appeared 
in embryos during the second day have increased so that in 
three-day and four-day chicks the long axis of the embryo shows 
nearly right-angled bends in the mid-brain and in the neck 
region. The mid-body region of three-day chicks is slightly 
concaved dorsally. This is due to the fact that the embryo 
is still broadly attached to the yolk in that region. By the 
end of the fourth day the body folds have undercut the embryo 
so it remains attached to the yolk only by a slender stalk. 
The yolk-stalk soon becomes elongated allowing the embryo to 
become first straight in the mid-dorsal region, and then convex 



dorsally. At the same time the caudal flexure is becoming more 
pronounced. The progressive increase in the cranial, cervical, 
dorsal, and caudal flexures results in the bending of the embryo 
on itself so that its originally straight long-axis becomes 
C-shaped and its head and tail lie close together (Fig. 40). 

visceral arch III 

auditory vesicle 

endolymphatic duct 
ganglion IX/ / ganglion VII-VIII 

hyomandi bular cleft 
mandibular arch 

ganglion V 



appendage bud 



posterior appendage bud 

Fig. 40. — Dextral view of entire chick embryo of 41 somites (about four days 

incubation) . 

The Visceral Arches and Clefts. — A fourth visceral cleft has 
appeared caudal to the three that were already formed in 55- 
hour chicks. The visceral arches are thicker and more conspicu- 
ous than in earlier embryos. In lightly stained whole-mounts 
of a three-day chick it is still possible to make out the aortic 
arches running through the visceral arches. In a chick of four 
days the visceral arches have become so much thickened that it 
is very difficult to see the vessels traversing them. 

The Oral Region. — The cervical flexure presses the pharyn- 
geal region and the ventral surface of the head so closely to- 
gether that it is difficult to make out the topography of the oral 



region by study of entire embryos. If the head and pharyngeal 
region are cut from the trunk and viewed from the ventral 
aspect the relations of the structures about the mouth are well 
shown (Fig. 41). The mandibular arch forms the caudal 
boundary of the oral depression. Arising on either side in 
connection with the mandibular arch are paired elevations, the 
maxillary processes, which grow mesiad and form the cephalo- 
lateral boundaries of the mouth opening. The nasal pits 
appear as shallow depressions in the ectoderm of the anterior 
part of the head which overhangs the mouth region. Surround- 


lateral telencephalic 

Pig. 41. — Drawing to show the external appearance of the structures in the oral 
region of a four-day chick. Ventral aspect. 

ing each nasal pit is a U-shaped elevation with its limbs directed 
toward the oral cavity. The lateral limb of the elevation is the 
naso-lateral process, and the median limb is the naso-medial 
process. As development proceeds the two naso-medial proces- 
ses grow toward the mouth and meet the maxillary pro- 
cesses which are growing in from either side. The fusion of 
the two naso-medial processes with each other in the mid-line, 
and the fusion of each of them laterally with the maxillary 
process of its own side gives rise to the upper jaw (maxilla). 
The fusion in the mid-line of the right and left components of 
the mandibular arch gives rise to the lower jaw (mandible). 

The Appendage Buds. — Both the anterior and posterior ap- 
pendage-buds have appeared in embryos of three days. They 


are formed by bud-like outgrowths from somites. The anterior 
appendages arise opposite somites 17 to 19 inclusive, and the 
posterior appendages arise opposite somites 26 to 32 inclusive. 
During the fourth day the appendage buds increase rapidly in 
size and become elongated but otherwise their appearance and 
their relationships show little change. 

The Allantois. — The development of the extra-embryonic 
membranes has already been considered (Chap. XI) and needs 
no further discussion here. In order to show the embryos more 
clearly, the extra-embryonic membranes, except for the allan- 
tois, have been removed from the specimens drawn in Figures 
39 and 40. The cut edge of the amnion shows at its anterior 
attachment to the body, opposite the anterior appendage bud 
and just caudal to the tip of the ventricle. The allantois in 
the three-day chick is as yet small and is concealed by the pos- 
terior appendage buds. In four-day embryos it has undergone 
rapid enlargement and projects from the umbilical region as a 
stalked vesicle of considerable size. 

II. The Nervous System 

Simmiary of Development Prior to the Third Day. — The 

earliest indication of the formation of the central nervous sys- 
tem appears in chicks of 16 to 18 hours as a local thickening of 
the ectoderm which forms the neural plate (Fig. 11). The 
neural plate then becomes longitudinally folded to form the 
neural groove (Figs. 14 and 15). By fusion of the margins of 
the neural folds, first in the cephalic region and later caudally, 
the neural groove is closed to form a tube and at the same time 
separated from the body ectoderm. The cephalic portion of 
the neural tube becomes dilated to form the brain and the re- 
mainder of the neural tube gives rise to the spinal cord (Figs. 
18 and 21). 

In its early stages the brain shows a series of enlargements 
in its ventral and lateral walls, indicative of its fundamental 
metameric structure. In the establishment of the three vesicle 
condition of the brain, the lines of demarcation between pros- 
encephalon, mesencephalon, and rhombencephalon are formed 
by the exaggeration of certain of the inter-neuromeric constric- 
tions and the obliteration of others (see Chap. IX and Fig. 20). 


The original neuromeric enlargements persist longest in the 

The three-vesicle condition of the brain is transitory. By 
forty hours the division of the rhombencephalon into meten- 
cephalon and myelencephalon is clearly indicated (Figs. 20, D 
and 22). The division of the prosencephalon and the estabhsh- 
ment of the five-vesicle condition characteristic of the adult 
brain, does not take place until somewhat later. 

In chicks of 55 hours (Figs. 34 and 35) the appearance of the 
cranial flexure has resulted in the bending of the brain so that 
the entire prosencephalon is displaced ventrad and then toward 
the heart. At the same time the head of the embryo has under- 
gone torsion and lies with its left side on the yolk. Although 
flexion and torsion have thus completely changed the general 
appearance of the brain as seen in entire embryos, the regions 
already established in 40-hour chicks are still evident. The 
prosencephalon has, however, become very noticeably enlarged 
cephalic to the optic vesicles, and a slight constriction in its 
dorsal wall indicates the beginning of the demarcation of the 
telencephalic region from the diencephalic region. 

The Formation of the Telencephalic Vesicles. — By the end 
of the third day the antero-lateral walls of the primary fore- 
brain have been evaginated to form a pair of vesicles lying one 
on either side of the mid-line (Figs. 39, 41, and 42, B). These 
lateral evaginations are known as the telencephalic vesicles. 
The openings through which their cavities are continuous with 
the lumen of the median portion of the brain are later known 
as the foramina of Monro. The telencephahc division of 
the brain includes not only the two lateral vesicles but also 
the median portion of the brain from which they arise. The 
teloccele has therefore three divisions, a median, broadly con- 
fluent posteriorly with the diocoele, and two lateral, connecting 
with the median through the foramina of Monro (Fig. 42, C). 

Before the formation of the telencephalic vesicles the most 
anterior part of the brain lay in the mid-line, but the rapid 
growth of the telencephalic vesicles soon carries them anteriorly 
beyond the median portion of the teloccele. The median ante- 
rior wall of the teloccele which formerly was the most anterior 
part of the brain, and which remains the most anterior part of 
the brain lying in the mid-line, is known as the lamina terminalis 



(Figs. 42, A, and C, and 43). The telencephalic vesicles become 
the cerebral hemispheres, and their cavities become the paired 
lateral ventricles of the adult brain. The hemispheres undergo 
enormous enlargement in their later development and extend 
dorsally and posteriorly as well as anteriorly, eventually cover- 
ing the entire diencephalon and mesencephalon under their 
posterior lobes. 

( ventricle IV ) 
thin roof of myelencephalon 

cle IV ) 

ventral cephalic fold 

spinal cord 

recessus opticus 
lamina termina 

median telocoele 
(ventricle III) 
recessus neuroporicus 

meso-metenceohalic fold 

(Sylvian aqueduct j 

location of 
posterior comm issure 
mescKliencephalic fold 
tuberculum posterius 
diocoele( ventricle III ) 
velum transversum 



ganglion VII VIII 

lamina .. 

terminalis /median telocoele 

( ventricle III ) 

foramen of Monro 

(sylvian aqueduct^ 

lateral telencephalic 

^ventricle IV ) 

( ventricle IV) 

position of 
auditory vesicle 

spinal cord 

Fig. 42. — Diagrams to show the topography of the brain of a four-day chick. 
A, plan of sagittal section. The arbitrary boundaries between the various 
brain vesicles (according to von Kupffer) are indicated by broken lines. B, 
dextral view of a brain which has been dissected free. C, schematic frontal 
section plan of brain. The flexures of the brain are supposed to have been 
straightened before the section was cut. 

As a matter of convenience in dealing with the morphology 
of the brain, more or less arbitrary lines of division between 
the adjacent brain regions are recognized. The division be- 
tween telencephalon and diencephalon is an imaginary line 
drawn from the velum transversum to the recessus opticus 



(Fig. 42, A). Velum transversum is the name given to the 
internal ridge formed by the deepening of the dorsal constriction 
which was first noted in chicks of 55 hours as indicating the 
impending division of the primary fore-brain (Fig. 35). The 
recessus opticus is a transverse furrow in the floor of the brain 
which in the embryo leads on either side into the lumina of thp 
optic stalks. 

The Diencephalon. — The lateral walls of the diencephalon at 
this stage show little differentiation except ventrally where the 

mandibular arch 

Seetiell's pocket 

Rathke's pocket 


omph. met, 


dortal aorta 


allantoic vesicle 

allantoic stallr 

post- anal gut 

— splanchnopleure 
of yolk sac 

Fig. 43. — Diagram of median longitudinal section of four-day chick. Due 
to a slight bend in the embryo the section is para-sagittal in the mid-dorsal 
region but for the most part it passes through the embryo in the sagittal plane. 

optic stalks merge into the walls of the brain. The develop- 
ment of the epiphysis as a median evagination in the roof of the 
diencephalon has already been mentioned (Chap. XII). Ex- 
cept for some elongation it does not differ from its condition 
when first formed in embryos of about 55 hours. The in- 
fundibular depression in the floor of the diencephalon has be- 


come appreciably deepened and lies in close proximity to 
Rathke's pocket with which it is destined to fuse in the forma- 
tion of the hypophysis (Fig. 43). Later in development the 
lateral walls of the diencephalon become greatly thickened to 
form the thalami, thus reducing the size and changing the 
shape of the diocoele, which is known in adult anatomy as the 
third brain ventricle. The anterior part of the roof of the 
diencephalon remains thin and by the ingrowth of blood vessels 
from above is. pushed into the third ventricle to form the an- 
terior choroid plexus. 

The boundary between the diencephalon and the mesen- 
cephalon is an imaginary line drawn from the internal ridge 
formed by the original dorsal constriction between the primary 
fore-brain and mid-brain, to the tuberculum posterius (Fig. 
42, A). The tuberculum posterius is a rounded elevation in 
the floor of the brain of importance chiefly because it is regarded 
as marking the boundary between diencephalon and mesen- 

The Mesencephalon.— The mesencephalon as yet shows no 
specializations, beyond a thickening of its walls. The dorsal 
and lateral walls of the mesencephalon later increase rapidly 
in thickness and become the optic lobes (corpora quadrigemina) 
of the adult brain. The optic lobes should not be confused with 
the optic vesicles arising from the diencephalon of the embryo. 
They are entirely different structures. The floor of the mesen- 
cephalon also becomes greatly thickened and is known in the 
adult as the crura cerebri. It serves as the main pathway of the 
fiber tracts which connect the cerebral hemispheres with the 
posterior part of the brain and the spinal cord. The originally 
capacious mesocoele is thus reduced by the thickening of the 
walls about it to a narrow canal (Aqueduct of Sylvius). 

The Metencephalon. — The boundary between the mesen- 
cephalon and metencephalon is indicated by the original inter- 
neuromeric constriction which separated them at the time^of 
their estabHshment (Cf. Figs. 20 and 42). The caudal boun- 
dary of the metencephalon is not definitely defined. It is 
regarded as being located approximately at the point where 
the brain roof changes from the thickened condition character- 
istic of the metencephalon to the thin condition characteristic 
of the myelencephalon. The metencephalon shows practically 


no differentiation in four-day chicks. Later in development 
there is ventrally and laterally an extensive ingrowth of fiber 
tracts giving rise to the pons and to the cerebellar peduncles 
of the adult metencephalon. The roof of the metencephalon 
undergoes extensive enlargement and becomes the cerebellum 
of the adult brain. 

The Myelencephalon. — In the myelencephalon the dorsal 
wall has become greatly reduced in thickness indicative of its 
final fate as the thin roof of the medulla. Like the roof of the 
diencephalon, the roof of the myelencephalon later receives a 
rich supply of small blood vessels by which it is pushed into 
the myelocoele to form the posterior choroid plexus (choroid 
plexus of the fourth ventricle). The ventral and lateral walls 
of the myelencephalon become the floor and side-walls of the 
medulla of the adult brain. 

The Ganglia of the Cranial Nerves. — In the brain region, cells 
derived from the cephalic portion of the neural crest have be- 
come aggregated to form ganglia. The largest and the most 
clearly defined of the gangha present in four-day chicks is the 
Gasserian ganglion of the fifth (trigeminal) cranial nerve (Fig. 
42, B). It lies ventro-laterally, opposite the most anterior 
neuromere of the myelencephalon. From its cells sensory 
nerve fibers grow mesiad into the brain and distad to the face 
and mouth region. In four-day chicks the beginning of the 
ophthalmic division of the fifth nerve extends from the ganglion 
toward the eye, and the beginning of the mandibulo-maxillary 
division is growing toward the angle of the mouth (Fig. 40). 
Immediately cephahc to the auditory vesicle is a mass of neural 
crest cells which is the primordium of the ganglia of the seventh 
and eighth nerves. The separation of this double primordium 
to form the geniculate ganglion of the seventh nerve and the 
acoustic ganghon of the eighth nerve begins during the fourth 
day. Posterior to the auditory vesicle the ganglion of the 
ninth nerve can be clearly seen even in whole-mounts (Fig. 40). 
The gangha of the tenth (vagus) nerves can be recognized in 
sections of chicks at the end of the fourth day but are difficult 
to make out in whole-mounts. 

The Spinal Cord. — The spinal cord region of the neural tube 
when first established, exhibits a lumen which is elliptical in 
cross section. As development progresses the lateral walls of 



the cord become greatly thickened in contrast with the dorsal 
and ventral walls which remain thin. In this process the lumen 
(central canal) becomes compressed laterally until it appears in 
cross section as little more than a vertical slit. The thin dorsal 
wall of the tube is known as the roof plate; the thin ventral 
wall as the floor plate; and the thickened side walls as the 
lateral plates. 

The Spinal Nerve Roots. — During the fourth day the estab- 
lishment of the spinal nerve roots has begun. The growth of 
nerve fibers from the neuroblasts can only be traced with the aid 
of special methods of staining. The more general steps in the 

spinal cord 



dorsal root 
ventral root 
spinal nerve 

neuron of 
ventral root 

Pig. 44. — Drawing to show the structure and relations of a spinal ganglion 
and the roots of a spinal nerve. The left half of the drawing represents struc- 
tures as they appear after treatment by the usual nuclear staining method. The 
right half of the section shows schematically the nerve cells and the fibers grow- 
ing out from them as they may be demonstrated by the Golgi method. {Nerve 
cells and fibers after Ramon y Cajdl.) 

development of the roots of the spinal nerves can, however, be 
followed in sections prepared by the ordinary methods. 

In the adult each spinal nerve is connected with the cord by 
two roots, a dorsal root which is sensory in function and a ven- 
tral root, which is motor in function. Lateral to the cord the 
dorsal and ventral roots unite. The spinal ganglion (dorsal 
root ganglion) is located on the dorsal root between the spinal 
cord and the point where dorsal and ventral roots unite. Distal 
to the union of dorsal and ventral roots is a branch, the ramus 


communicans, which extends ventrad to a ganglion of the sym- 
pathetic nerve cord. 

When first formed from the neural crest cells, the spinal 
ganglion has no connection with the cord (Fig. 37). The dorsal 
root is established by the growth of nerve fibers from cells of 
the spinal ganglion mesiad into the dorsal part of the lateral 
plate of the cord. At the same time fibers grow distad from 
these cells to form the peripheral part of the nerve (Fig. 44). 
The fibers which arise from the dorsal root ganglion conduct 
sensory impulses toward the cord. 

Coincident with the establishment of the dorsal root, the 
ventral root is formed by fibers which grow out from cells 
located in the ventral part of the lateral plate of the cord 
(Fig. 44)'. The fibers which thus arise from cells in the cord 
and pass out through the ventral root, conduct motor impulses 
from the brain and cord to the muscles with which they are 
associated peripherally. 

The sympathetic ganglia arise from cells of the neural crest 
which migrate ventrally and form cellular masses lying on 
either side of the mid-line at the level of the dorsal aorta. 
By the end of the fourth day these cells constitute a pair of 
cords in which enlargements can be made out opposite the spinal 
ganglia. These enlargements are the primary sympathetic 
gangha. Each sympathetic ganghon is connected with the 
corresponding spinal nerve by a cellular cord which is the 
primordium of the ramus communicans. The sympathetic 
ganglia later receive both sensory and motor fibers from the 
spinal nerve roots by way of the rami communicantes, and from 
nerve cells in the sympathetic ganglia, fibers extend to the 

III. The Sense Organs 

The Eye. — The primary optic vesicles arise in chicks of about 
30 hours as dilations in the lateral wall of the prosencephalon 
(Figs. 19 and 23). At first the optic vesicles open broadly 
into the brain, but later constrictions develop which narrow 
their attachment to the form of a stalk (Fig. 22). In chicks 
of 55 hours the primary optic vesicles are invaginated to form 
the double-walled secondary optic vesicles or optic cups. The 
invagination takes place in such a way that the ventral wall 



of the cup is incomplete, the gap in it being known as the choroid 
fissure (Figs. 35 and 36, B). 

The lens arises as a thickening of the superficial ectoderm 
which becomes depressed to form a vesicular invagination ex- 
tending into the optic cup (Fig. 36, B). 



concentration of 

pigment layer 
sensory layer 


area enlarged in B 

corneal region 

optic stalk 





' 'ill 

layer of retina 

layer of retina 

lens fibers 

Pig. 45. — Drawings to show structure of the eye of a four-day chick. 
A, diagram to show topography of eye region; B, drawing to show cellular 
organization of the pigment and sensory layers of the retina. Abbreviations: 
mes., mesenchymal cell;, pigment granule; C, drawing to show cellular 
organization of the lens. 

In chicks of four days the choroid fissure has become nar- 
rowed by the growth of the walls of the optic cup on either side 
of it (Figs. 40 and 42, B). The orifice of the optic cup becomes 


narrowed by convergence of its margins toward the lens (Fig. 
45, A). Meanwhile the lens has become freed from the super- 
ficial ectoderm and forms a completely closed vesicle. Sections 
of the lens at this stage show that the cells constituting that 
part of its wall which lies toward the center of the optic cup 
are becoming elongated to form the lens fibers (Fig. 45, C). 

At this stage we can identify the beginning of most of the 
structures of the adult eye. The thickened internal layer of 
the optic cup will give rise to the sensory layer of the retina 
(Fig. 45, B). Fibers arise from nerve cells in the retina and 
grow along the groove in the ventral surface of the optic stalk 
toward the brain to form the optic nerve. The external layer 
of the optic cup gives rise to the pigment layer of the retina. 
Mesenchyme cells can be seen aggregating about the outside of 
the optic cup. From these the sclera and choroid coat are 
derived. Some of the mesenchyme makes its way into the 
optic cup through the choroid fissure and gives rise to the cellu- 
lar elements of the vitreous body. The comple:?^ ciHary appar- 
atus of the adult eye is derived from the margins of the optic 
cup adjacent to the lens. The corneal and conjunctival epi- 
thelium arise from the superficial ectoderm overlying the eye. 
Mesenchyme cells which make their way between the lens and 
the corneal epithelium give rise to the substantia propria of the 

The Ear.- — Of the structures taking part in the formation of 
the ear, the first to appear is the auditory placode. The audi- 
tory placode is recognizable in 36-hour chicks as a thickened 
plate of ectoderm. Almost as soon as it appears the placode 
sinks below the level of the surrounding ectoderm to form the 
floor of the auditory pit (Fig. 22). By constriction of its open- 
ing to the surface the epithelium of the auditory pit becomes 
separated from the ectoderm of the head and comes to lie close 
to the lateral wall of the myelencephalon (Fig. 36, ^). A tubu- 
lar stalk, the endolymphatic duct, remains for a time adherent 
to the superficial ectoderm, marking the location of the original 
invagination (Fig. 40). 

The degree of development reached by the ear primordium 
in four-day chicks gives little indication of the nature of the 
later processes by which the ear is formed. The auditory 
vesicle by a very complex series of changes will give rise to the 


entire epithelial portion of the internal ear mechanism. Nerve 
fibers arising from the acoustic ganglion grow into the brain 
proximally and to the internal ear distally establishing nerve 
connections between them. There is at this stage no indication 
of the differentiation of the external auditory meatus. The 
dorsal and inner portion of the hyomandibular cleft which 
gives rise to the eustachian tube and to the middle ear chamber 
has not yet become associated with the auditory vesicle. 

The Olfactory Organs. — The olfactory organs are represented 
in three-day and four-day chicks by a pair of depressions in the 
ectoderm of the head. These so-called olfactory pits are located 
ventral to the telencephalic vesicles and just anterior to the 
mouth (Figs. 40 and 41). By growth of the processes which 
surround them, the olfactory pits become greatly deepened. 
The epitheHum lining the pits eventually comes to lie at the 
extreme upper part of the nasal chambers and constitutes the 
olfactory epithelium. Nerve fibers grow from these cells to 
the telencephalic lobes of the brain to form the olfactory nerves. 

IV. The Digestive and Respiratory Systems 

Summary of Development Prior to the Third Day. — The 

primary entoderm which gives rise to the epithelial Hning of the 
digestive and respiratory systems and their associated glands 
becomes estabhshed as a separate layer before the egg is laid. 
In its early relationships the entoderm is a sheet-like layer of 
cells lying between the ectoderm and the yolk and attached 
peripherally to the yolk (Fig. 7). The primitive gut is the 
cavity bounded dorsally by the entoderm and ventrally by the 
yolk (Fig, 31, A). 

Only the part of the entoderm which lies within the em- 
bryonal area is involv-ed in the formation of the enteric tract. 
The peripheral portion of the entoderm goes into the formation 
of the yolk-sac. There is at first ho definite line of demarcation 
between the entoderm destined to be incorporated into the 
body of the embryo and that which remains extra-embryonic 
in its associations. The foldings which appear later separating 
the body of the embryo from the yolk, establish for the first 
time the boundaries between intra-embryonic and extra-em- 
bryonic entoderm (Figs. 30 and 32). 


The first part of the gut to acquire a complete entodermic 
lining is the fore-gut. Its floor is formed by the caudally 
progressing concrescence of the entoderm which takes place as 
the subcephalic and lateral body folds undercut the cephalic 
part of the embryo (Figs. i6 and 31, 5). At a considerably 
later stage the hind-gut is formed by the progress of the sub- 
caudad fold (Figs. 35 and 31, C). Between the fore-gut and the 
hind-gut, the mid-gut remains open to the yolk ventrally. As 
the embryo is more completely separated from the yolk the 
fore-gut and hind-gut increase in extent at the expense of the 
mid-gut. By the fourth day of incubation the mid-gut is re- 
duced to the region where the yolk stalk opens into the enteric 
tract (Figs. 31, -D and 43). 

The Establishment of the Oral Opening. — When first estab- 
lished the gut ends as a blind pocket both cephalically and 
caudally. The mouth opening does not appear until the third 
day, the cloacal opening is not established until much later in 
incubation. In embryos of 55 hours the processes leading to- 
ward the establishment of the oral opening are clearly indicated. 
A mid-ventral evagination of the pharynx is estabhshed im- 
mediately cephalic to the mandibular arch (Fig. 35). Opposite 
this out-pocketing of the pharynx, and growing in to meet it, the 
stomodeal depression is formed. The thin membrane formed 
by the meeting of the pharyngeal entoderm with the stomodeal 
ectoderm is known as the oral plate. The communication of the 
fore-gut with the outside is finally established by the breaking 
through of the oral plate. 

The formation of the mouth opening in the manner described 
does not take place at the extreme anterior end of the fore-gut. 
A small gut pocket extends cephalic to the mouth. ^ This so- 
called pre-oral gut rapidly becomes less conspicuous after the 
breaking through of the oral plate. The small depression 
which in older embryos marks its location is known as Sees- 
selFs pocket (Fig. 43). Even this small depression eventually 
disappears altogether. Its importance lies wholly in the fact 
that it indicates for some time the place at which ectoderm 
and entoderm originally became continuous in the formation 
of the oral opening. 

The Pharyngeal Derivatives. — Several structures arise in the 
pharyngeal region which do not become parts of the digestive 


system. Nevertheless the origin of their epithelial portions 
from fore-gut entoderm and their early association with this 
part of the gut tract makes it convenient to take them up in 
connection with the digestive system. 

The thyroid gland arises as a median diverticulum from the 
floor of the pharynx which makes its appearance at the level of 
the second pair of pharyngeal pouches. Toward the end of 
the fourth day the thyroid evagination has become saccular and 
retains its connection with the pharynx only by a narrow open- 
ing at the root of the tongue known as the thyro-glossal duct 
(Fig. 43). In mammaha the thyroid is contributed to by pri- 
mordia which arise laterally from the fourth pharyngeal pouches 
as well as by a median evagination from the floor of the 
pharynx. It is possible that evaginations which in the chick 
arise from the fourth pharyngeal pouches are homologous with 
the lateral thyroid primordia of mammals. In the chick, how- 
ever, these evaginations do not form typical thyroid tissue. 

The thymus of the chick does not appear until after the fourth 
day of incubation. It takes its origin primarily from divertic- 
ula arising from the posterior faces of the third and fourth 
pharyngeal pouches. The original epithelial character of the 
thymus is soon largely lost in an extensive ingrowth of mesen- 
chyme and the organ becomes chiefly lymphoid in its histolog- 
ical characteristics. 

The Trachea. — The first indication of the formation of the 
respiratory system- is an outgrowth from the pharynx. In 
chicks of 3 days a mid- ventral groove is formed in the pharynx, 
beginning just posterior to the level of the fourth pharyngeal 
pouches and extending caudad. This groove deepens rapidly 
and by closure of its dorsal margins becomes separated from the 
pharynx except at its cephaUc end. The tube thus formed is 
the trachea, and the opening which persists between the cephal- 
ic end of the trachea and the pharynx is the glottis (Fig. 43). 
The original entodermal evagination gives rise only to the 
epithelial lining of the trachea, the supporting structures of the 
tracheal walls being derived from the surrounding mesenchyme. 

The Lung-buds. — The tracheal evagination grows caudad 
and bifurcates to form a pair of lung-buds. As the lung-buds 
develop they grow into the loose mesenchyme on either side of 
the mid-line. The adjacent splanchnic mesoderm is pushed 


ahead of them in their caudo-lateral growth and comes to 
constitute the outer investment of the lung-buds. The ento- 
dermal buds give rise only to the epithehal Hning of the bronchi, 
and the air passages and air chambers of the lungs. The 
connective tissue stroma of the lungs is derived from mesen- 
chyme surrounding the lung-buds, and their pleural covering 
from the investment of splanchnic mesoderm. 

The Oesophagus and Stomach. — Immediately caudal to the 
glottis is a narrowed region of the fore-gut which becomes the 
oesophagus, and farther caudally a slightly dilated region which 
becomes the stomach (Fig. 43). The concentration of mesen- 
chyme cells about the entoderm of the oesophageal and stomach 
regions foreshadows the formation of their muscular and con- 
nective tissue coats (Fig. 46, C). 

The Liver. — In all vertebrates the Hver arises as a diverticu- 
lum from the ventral wall of the gut immediately caudal to the 
stomach region. In chick embryos the liver diverticulum 
appears just as the part of the gut from which it arises is 
acquiring a floor by the concrescence of the margins of the 
anterior intestinal portal. As a result the liver evagination 
appears for a short time on the Up of the intestinal portal, and 
grows cephalad toward the fork where the omphalomesenteric 
veins enter the sinus venosus. As closure of the gut floor is 
completed, the Kver diverticulum comes to lie in its character- 
istic position in the ventral wall of the gut. In embryos of four 
days the original evagination has grown out in the form of 
branching cords of cells and become quite extensive in mas^ 
(Fig. 43). In its growth the liver pushes ahead of it the 
splanchnic mesoderm which surrounds the gut, with the result 
that the hver from its first appearance is invested by mesoderm. 

The proximal portion of the original evagination remains open 
to the intestine, and serves as the duct of the hver. This 
primitive duct later undergoes regional differentiation and gives 
rise in the adult to the common bile duct, to the hepatic and cys- 
tic ducts, and to the gall bladder. The cellular cords which bud 
off from the diverticulum become the secretory units of the 
liver (hepatic tubules). 

The same process of concrescence which closes the floor of 
the fore-gut involves the proximal portion of the omph3.Io- 


mesenteric veins which, when they first appear, lie in the lateral 
folds of the anterior intestinal portal (Fig. 35). As the intes- 
tinal portal moves caudad in the lengthening of the fore-gut, 
the proximal portions of the omphalomesenteric veins are 
brought together in the mid-line and become fused. The fusion 
extends caudad nearly to the level of the yolk stalk (Fig. 47). 
Beyond this point they retain their original paired condition. 
In its growth the liver surrounds the fused portion of the om- 
phalomesenteric veins (Figs. 43 and 46, D, and E). This early 
association of the omphalomesenteric veins with the liver 
fore-shadows the way in which the proximal part of the afferent 
vitelline circulation is to be involved in the establishment of the 
hepatic-portal circulation of the adult. 

The Pancreas. — The pancreas is derived from evaginations 
appearing in the walls of the intestine at the same level as the 
liver diverticulum. There are three pancreatic buds, a median 
dorsal, and a pair of ventro-lateral buds. The dorsal evagina- 
tion appears at about 72 hours, the ventro-lateral evaginations 
toward the end of the fourth day. The dorsal pancreatic bud 
arises directly opposite the liver diverticulum and grows into 
the dorsal mesentery (Fig. 43). The ventro-lateral buds arise 
where the duct of the liver connects with the intestine so that 
the ducts of the liver and the ventral pancreatic ducts open 
into the intestine by a common duct (ductus choledochus). 
Later in development the masses of cellular cords derived 
from the three pancreatic primordia grow together and 
become fused into a single glandular mass, but usually two 
and in rare cases all three of the original ducts persist in the 

The Mid-gut Region. — In chicks of four days the enteric 
tract shows no local differentiation from the level of the liver 
to the cloaca except where the yolk-sac is attached. All of the 
gut tract between the stomach and the yolk-stalk, and the 
anterior third of the gut lying caudal to the yolk-stalk is des- 
tined to become the small intestine. The posterior two-thirds 
of the hind-gut becomes large intestine and cloaca. 

The Cloaca. — The beginning of the formation of the cloaca 
is indicated in chicks of four days incubation, by a dilation of 
the posterior portion of the hind-gut (Fig. 43). Although ex- 
tensive differentiations in the cloacal region do not appear 


ganglion VII-VIII 
auditoty vesicle 


ganglion V 


branch of 

int. carotid a. 

anterior cardinal vem 

branch of 
ant. cardinal v. 


aortic arch 11 

aortic arch 

"^\ ^V 

aortic arch IV 

^^-^.^^ ^\^J— ^ 

dorsal ^^ 
ganglion ^.,.^^^—-5 

neural /S^Sm 

notochord ^ 


dorsal aorta/ / / ^"^m^ 
ant. cardinal vV y^ J \ 


cleft III/ / \ 


visceral arch WV \ 

visceral cleft 


region of coelom.^^ 

trachea^ \ ^^^ 


j^^^^N^^j;^— ^kj 

neural i^^ 
tube— ^S 

^^^^r 1 


int. carotid a. 

ant. cardinal v. 


dorul aorta' 

bulbo-conus arteriosus 

pharyngeal pouch I 

mandibular arch 
'hyomandibular cleft 
hyoid arch 


ventral body wall ' 

optic stalk 

sensory layer of retina 

pigment layer of retina 

olfactory pit 

bulbo-conus arteriosus 
sinus venosus 
right duct of Cuvier 
cardinal v, 

lung bud 

pleural region 

Dof coelom left duct 
of Cuvier 


pericardial region of coelom 

Fig. 46 



ductus choledochus 
mesonephric duct 
dorsal mesentery 

dorsal ganglion 

neural tube 

omphaloniesenteric vein 

lateral telencephalic 

ectoderm of hea4 


post, cardinal v. 

dorsal aorta 
mesonephric duct 

allantoic vein 


omphalomesenteric veins 


sub^ intestinal 

allantoic vein 
allantoic stalk 

allantoic art. 
post, appendage 

Fig. 46. — Diagrams of transverse sections of a four-day chick. The location of 
the sections is indicated on a small outline sketch of the entire embryo. 


until later in development, certain of its fundamental relation- 
ships are established at this stage. 

The cloaca of an adult bird is the common chamber into 
which the intestinal contents, the urine, and the products of 
the reproductive organs are received for discharge. The first 
appearance of the cloaca in the embryo as a dilated terminal 
portion of the gut establishes at the outset the relations of 
cloaca and intestine familiar in the adult. 

Although the urinary system is not at this stage developed 
to conditions which resemble those in the adult the. parts of it 
which have been estabhshed are already definitely associated 
with the cloaca. The proximal portion of the allantoic stalk 
which is the homologue of the urinary bladder of mammals 
opens directly into the cloaca (Fig. 43). When the urinary 
system of the embryo is considered, we shall see that the ducts 
which drain the developing excretory organs also open into 
the cloacal region on either side of the allantoic stalk. 

There is at this stage but little indication of the for- 
mation of the gonads. The relation of the sexual ducts 
to the cloaca can be made out only by the study of older 

The Proctodaeum and the Cloacal Membrane. — Indications 
of the formation of the cloacal opening to the outside appear 
during the fourth day of incubation. Its establishment is 
accomplished in much the same manner as the establishment 
of the oral opening. A ventral out-pocketing of the hind-gut 
arises just caudal to the point at which the allantoic stalk 
opens into the cloaca (Fig. 43) . At the same time a depression 
appears in the overlying ectoderm. The external depression 
which grows in toward the gut pocket is known as the procto- 
daeum. The double epithelial layer formed by the meeting of 
gut entoderm with proctodeal ectoderm is the cloacal mem- 
brane. The formation of the proctodaeum and the cloacal 
membrane cleaily indicate the location of the future cloacal 
opening although an open communication is not established 
by the rupture of the cloacal membrane until considerably 
later. The cloacal opening does not form at the extreme pos- 
terior end of the hind-gut and there is, therefore, a post-anal 
pocket of the hind-gut suggestive of the pre-oral pocket of the 


V. The Circul-\tory System 

The Functional Significance of the Embryonic Circulation. 
The arrangement of the embnonic circulation is dimciilt to 
understand only when its functional significance is overlooked. 
In the embtyo as in the adult the main circulatory channels 
lead to and from the centers of metabohc acti\^ty. The circu- 
lating blood carries material from the organs of digestion and 
absorption to remote parts of the body; ox\'gen to all parts 
of the body from the organs which are specially constructed 
to take up oxygen from the surroimding medium; and waste 
materials from the places of their h*beration, to the organs 
through which they are eliminated. The differences between 
the course of the circulation in the embr\'o and in the adult are 
due to the fact that their centers of metaboUc activity are 
differently located. 

The organs which in the adult cany out such functions as 
digestion and absorption, respiration, and excretion are ex- 
tremely complex and highly differentiated structures. They 
are for this reason slow to attain their definitive condition and 
do not become functional until toward the close of embryonic 
life. Moreover the conditions by which the developing adult 
organs are surrounded during embryonic life are in some in- 
stances an absolute bar to their becoming functional were they 
sufficiently developed so to do. Suppose the lungs, for example, 
were fuUy formed at an early stage of development. The fact 
that the chick embr\^o is living submerged in the anmiotic fluid 
would render them as incapable of fxmctioning as the lungs of a 
man under water. Were the embrj'o dependent on the es- 
tablishment of the organs which carry on metabolism in the 
adult, development would be at an impasse. To develop, the 
embr>'o must have not only the raw food material suppHed it 
by the mother in the form of yolk, it must have a means of 
digesting the yolk, absorbing it, and canying it to the places 
where it can be utilized. The utilization of food material to 
produce the energy- expressed in growth processes depends on 
presence of ox\-gen. For growth there must be a means of 
securing oxygen and canying it, as weU as food, to all parts of 
the body. Xor can continued growth go on unless the waste 
products Hberated by the growing tissues are elinunated. At 


the outset of its development the embryo must, therefore, 
establish organs for the digestion and absorption of food, the 
securing of oxygen, and the elimination of waste products. 
These organs serve the embryo but temporarily and are dif- 
ferent in structure and in location from the organs which carry 
out the corresponding functions in the adult, their nature and 
location depending on the exigencies of the embryo's living 

The main channels of the circulation in young embryos lead 
to and from their temporary organs of digestion and absorption, 
respiration, and excretion. The arrangement of the main 
vessels characteristic of the adult appears only as the organs 
characteristic of the adult develop. The changes by which the 
circulatory system acquires its adult arrangement are of neces- 
sity gradual. Any changes which were sufficiently abrupt to 
interfere with the circulation would result in disaster for the 
embryo. Even slight curtailment of the normal blood supply 
to any region would cause its growth to cease; any marked local 
decrease in the circulation would result in local atrophy or 
malformation; complete interruption of any important circula- 
tory channel, even for a short time, would inevitably mean the 
death of the embryo. Consequently the arrangement of 
vessels characteristic of the embryo persists during the forma- 
tion of the adult organs, and becomes altered only gradually as 
the adult organs and the vessels associated with them become 
ready to function. 

If the various circulatory channels of young chick embryos 
are considered in the light of their functions, the differences 
between the embryonic and the adult circulations should not 
be troublesome. The circulation of young chick embryos in- 
volves three main arcs of which the heart is the common center 
and pumping station. One of these circulatory arcs, the vitel- 
line, carries blood to the yolk-sac where food materials are 
absorbed and then returns the food-laden blood to the heart for 
distribution within the embryo. Another arc carries blood to 
and from the allantois. The distal portion of the allantois lies 
close beneath the egg shell and the blood circulating in the 
allantoic vessels is thereby brought into a location where inter- 
change of gases can be carried on with the air which penetrates 
the shell (Fig. 30, C and D). It is in the allantoic circulation 


that the blood gives off its carbon dioxide and acquires a fresh 
supply of oxygen. The allantoic circulation is also the em- 
bryo's means of eliminating nitrogenous waste material from 
the blood. The remaining circulatory arc is confined to the 
body of the embryo. The intra-embryonic circulation has 
many distributing and collecting vessels but all of them are 
alike in function in that they bring food material to, and 
carry waste material from, the various parts of the developing 
body. Nowhere in their course are the vessels of the intra- 
embryonic circulation involved in adding food material or 
oxygen to that already contained in the blood they convey, and 
nowhere do they free the blood from waste materials until well 
along in development, when the nephroi become functional. 

In the heart the blood from the three circulatory arcs is 
mingled. As it leaves the heart the mixed blood is not as rich in 
food material as the blood coming in through the omphalo- 
mesenteric veins, nor as free from waste materials and as rich 
in oxygen as the blood returned over the allantoic veins. Its 
condition of serviceability to the embryo is, however, constantly 
maintained at a good average by the incoming viteUine and 
allantoic blood. 

There is a tendency among students who have done but 
little work on the circulation to regard any vessel which carries 
oxygenated blood as an artery," ailti any vessel which carries 
blood poor in oxygen and high in carbon dioxide content as a 
vein. This is not entirely correct even for the circulation of 
adult mammals on which the conception is based. In com- 
parative anatomy and especially in embryology it is far from 
being the case. It is necessary, therefore, in dealing with the 
circulation of the embryo to eradicate this not uncommon 

The differentiation between arteries and veins which holds 
good for all forms, both embryonic and adult, is based on the 
structure of their walls, and on the direction of their blood flow 
with reference to the heart. An artery is a vessel carrying 
blood away from the heart under a relatively high fluctuating 
pressure due to the pumping of the heart. Correlated with the 
pressure conditions in it, its walls are heavily reinforced by 
elastic and muscle tissue. A vein is a vessel carrying blood 
toward the heart under relatively low and constan 



pressure from the blood welling into it from capillaries. Corre- 
lated with the pressure conditions characteristic for it, the walls 
of a vein have much less elastic and muscle tissue than artery 
walls, and more non-elastic fibers reinforcing them. 

The Vitelline Circulation. — The earHest indication of blood 
and blood vessel formation is at the chick's source of food supply. 
Blood islands appear in the extra-embryonic splanchnopleure 

pharyngeal pouches I -IV 

ant. cardinal v 
aortic arch IV 

aortic arch I 
^disappearing j 

int carotid a. 

ext. carotid a. 

aorta . 



post, cardinal v 

ext. iliac artery 
cloaca — 

allantoic artery ^ 
proctodaeum OUMV\iA 
post -anal gut 

Pig. 47. — Schematic diagram to show the location of the more prominent 
internal organs of the four-day chick. Except for the omphalomesenteric 
arteries and veins paired structures are represented only on the side toward the 

of the yolk-sac toward the end of the first day of incuba- 
tion, and rapidly become differentiated to form vascular endo- 
thehum enclosing central clusters of primitive blood corpuscles 
(Fig. 25). By extension and anastomosing of neighboring 
islands a plexus of blood channels is formed in the yolk-sac. 
Further extension of the vitelUne plexus brings it into communi- 
cation with the omphalomesenteric veins which have been de- 
veloped in the embryo as caudal extensions of the heart (Fig. 21). 



Toward the end of the second day of development the om- 
phalomesenteric arteries establish communication between 
the dorsal aortae and the vitelHne plexus. (See Chap. X and 
Figs. 29 and 35.) There is now a system of open channels lead- 
ing from the embryo to the yolk-sac, and back again to the embryo. 
With the completion of these channels the heart begins to 
pulsate, circulation of the blood is thereby estabhshed, and the 

Pig. 48. — Diagram to show course of vitelline circulation in chick of about 
four days. (After Lillie.) For the intra-embryonic vessels see Fig. 47. Abbre- 
viations; A, dorsal aorta; A.V.V., anterior vitelline vein; L.V.V., lateral vitelline 
vein; M.V., marginal vein (sinus terminalis); P.V.V., posterior vitelline vein; 
V.A., vitelline artery. The direction of blood flow is indicated by arrows. 

blood cells formed in the yolk-sac are for the first time carried 
into the body of the embryo. 

The course of the vitelline circulation in chicks of four days 
is shown diagrammatically in Figures 47 and 48. Circulating 



in the rich plexus of small vessels on the yolk, the blood finally 
makes its way either directly into one or another of the larger 
vitelline veins, or to the sinus terminalis which acts as a collecting 
channel, and then over the sinus terminalis to one of the vitel- 
line veins. The vitelline veins converge toward the yolk-stalk 
where they empty into the omphalomesenteric veins. The 
omphalomesenteric veins at first paired throughout their 
entire length have been brought together proximally by the 
closure of the ventral body wall and become fused to form a 
median vessel within the body of the embryo. It is through 
this vessel that the vitelline blood eventually reaches the 
heart. In the heart the blood of the vitelline, intra-embryonic, 
and allantoic circulations is mingled. The mixed blood passes 
out by the ventral aorta and the aortic arches into the dorsal 
aorta. Leaving the dorsal aorta through the vitelline arteries 
the blood is returned to the yolk-sac. 

It should not be inferred that the blood stream ''picks up" 
deutoplasmic granules and carries them to the embryo. The 
acquisition of food material by the blood depends on the activ- 
j ities of the entodermal cells lining the yolk-sac. These cells 
secrete digestive enzymes which break down the deutoplasmic 
granules. The liquified material is then absorbed by the yolk- 
sac cells and transferred to the blood. The blood carries the 
food material in soluble form to the embryo where it is finally 

The Allantoic Circulation. — The allantoic arteries arise by 
the prolongation and enlargement of the segmental vessels 
arising from the aorta at the level of the allantoic stalk. Their 
size increases rapidly as the allantois increases in extent. From 
them the blood is distributed in a rich plexus of vessels which 
ramify in the mesoderm of the allantois (Fig. 47). 

The situation of the allantois directly beneath the porous 
shell is such that the blood can carry on interchange of gases 
with the outside air (Fig. 30, D). It is in the rich plexus of 
small allantoic vessels where the surface exposure is very great 
that the blood gives off its carbon dioxide and takes up oxygen. 

At a later stage of development the ducts of the embryonic 
excretory organs open into the allantoic stalk near its cloacal 
end. As the excretory organs become functional the allantoic 
vesicle becomes the repository for the nitrogenous waste mate- 


rials eliminated through them. The watery portion of the 
waste materials is passed off by evaporation. The remaining 
soHds are deposited in the allantoic vesicle. They accumulate 
in the extra-embryonic portion of the allantois and there remain 
until that portion of the allantois is discarded at the close of 
embryonic Hfe. 

The blood from the allantois is collected and returned to the 
heart over the allantoic veins. From the distal portion of the 
allantois the smaller veins converge and unite into two main 
vessels, right and left, which enter the body of the embryo with 
the allantoic stalk (Fig. 46, H). After their entrance into the 
body the allantoic veins extend cephalad in the lateral body 
walls (Figs. 47 and 46, H to D). They enter the sinus venosus 
on either side of the entrance of the omphalomesenteric vein. 

The Intra-embryonic Circulation. — The earUest vessels of 
the intra-embryonic circulation to appear are the large vessels 
communicating with the heart. In chicks of 33 hours the 
ventral aorta leads off from the heart cephalically and bifur- 
cates ventral to the pharynx giving rise to a single pair of 
aortic arches. The aortic arches pass dorsad around the antero- 
lateral walls of the pharynx and are continued caudally along 
the dorsal wall of the gut as the paired dorsal aortae (Fig. 23). 

When, toward the end of the second day of incubation, vis- 
ceral clefts and visceral arches appear, the original pair of 
aortic arches comes to lie in the mandibular arch. In each of 
the visceral arches posterior to the mandibular, new aortic 
arches are formed connecting the ventral aortae with the dorsal 
aortae. By 55 hours three pairs of aortic arches are present 
and a fourth is beginning to form (Fig. 35). 

At about this stage extensions of the dorsal aortic roots grow 
out anteriorly. The vessels thus derived extend cephalad in 
close association with the brain as the internal carotid arteries. 
In a later stage vessels arise from the ventral aortic roots and 
grow cephalad as the external carotid arteries (Fig. 47). 

By the end of the fourth day of incubation two more pairs 
of aortic arches have appeared posterior to the four formed in 
55 to 60-hour chicks. From their first appearance the fifth 
aortic arches are very small and they soon disappear altogether. 
The first and second pairs of aortic arches have by this time 
suffered a great diminution in size which is indicative of their 


final disappearance. In many embryos of this age the first 
arches, and in a few the second also, have disappeared alto- 
gether. This leaves only the third, fourth, and sixth pairs of 
aortic arches. These arches persist intact for some time, and 
parts of them remain permanently, being incorporated in the 
formation of the aortic arch and the main vessels arising from 
it, and in the roots of the pulmonary arteries. 

In reptiles, birds, and mammals the main adult vessels which 
connect the heart with the dorsal aorta are derived from the 
fourth pair of aortic arches of the embryo. The paired condi- 
tion of these arches persists as the adult condition in reptiles, 
but in birds and mammals one of the arches degenerates before 
the end of embryonic fife. In birds the left arch degenerates 
leaving the right one as the adult aortic arch; in mammals the 
right arch degenerates leaving the left as the aortic arch of the 

The dorsal aortae, at first paired, later become fused to form a 
median vessel. The fusion begins at about the level of the 
sinus venosus and progresses cephalad and caudad (Fig. 35). 
Fusion extends cephalad but a short distance, never involving 
the region of the aortic arches. Caudally the aortae eventually 
become fused throughout their entire length. 

Early in development the aorta gives rise to a segmentally 
arranged series of small vessels which extend into the dorsal 
body wall. At the level of the anterior appendage buds a pair 
of the segmental arteries become enlarged and extend into the 
wing buds as the sub-clavian arteries. Coincident with the 
development of the allantois, segmental vessels opposite the 
allantoic stalk become enlarged and extend into it as the allan- 
toic arteries. The external iliac arteries to the posterior ap- 
pendage buds arise as branches of the allantoic arteries close to 
their origin from the aorta (Fig. 47) . 

The three main arteries which in the adult supply the ab- 
dominal viscera are represented in four-day chicks only by the 
omphalomesenteric arteries. The omphalomesenteric arteries 
arise as paired vessels (Fig. 35), but in the closure of the ventral 
body wall of the embryo they are brought together and fused to 
form a single vessel which runs in the mesentery from the aorta 
to the yolk-stalk (Fig. 47). With the atrophy of the yolk-sac 
the proximal part of the omphalo-mesenteric artery persists as 


the superior mesenteric of the adult. The coeliac and the 
inferior mesenteric arteries arise from the aorta independently 
at a later stage. 

The cardinal veins are the principal afferent systemic vessels 
of the early embryo. They appear toward the end of the second 
day as paired vessels extending anteriorly and posteriorly on 
either side of the mid-line. At the level of the heart the anterior 
and posterior cardinal veins of the same side of the body become 
confluent in the ducts of Cuvier and turn ventrad to enter the 
sinus venosus (Figs. 24 and 35) . Chicks of four days show little 
change in the relationships of the cardinal veins (Fig. 47). 
Later in development the proximal ends of the anterior cardinals 
become connected by the formation of a new transverse vessel 
and empty together into the venous atrium of the heart. Their 
distal portions remain in the adult as the principal afferent 
vessels (jugular veins) of the cephalic region. 

The posterior cardinals lie in the angle between the somites 
and the lateral mesoderm (Fig. 36, D, E). When the mesone- 
phroi develop from the intermediate mesoderm, the cardinal 
veins lie just dorsal to them throughout their length (Figs. 52, C 
and 46, E to H). In young embryos the posterior cardinals 
are the main afferent vessels of the posterior part of the body. 
Later in development they are replaced by a new vesssel, the 
inferior vena cava. The changes by which posterior cardinals 
become reduced and broken up to form small vessels with new 
associations, belong to stages of development beyond the scope 
of this book. 

The Heart. — The heart in adult vertebrates is a ventral 
unpaired structure. Its origin in the chick from paired primor- 
dia is correlated with the way the young embryo lies spread out 
on the yolk surface. When the ventral body wall is completed 
by the folding together of layers which formerly extended to 
right and left over the yolk, the paired primordia of the heart 
are brought together in the mid-Hne. Their fusion establishes 
the heart as an unpaired structure lying in the characteristic 
ventral position (see Chap. IX and Figs. 26 and 27). 

After the fusion of its paired primordia the heart is a nearly 
straight, double-walled tube (Figs. 49, A and 19). The primor- 
dial endocardium of the heart has the same structure and arises 
in the same manner as the endothelial walls of the primitive 


embryonic blood vessels with which it is directly continuous. 
The epi-myocardial layer of the heart is an outer investment 
which surrounds and reinforces the endocardial wall. As 
development progresses the epi-myocardium becomes greatly 
thickened and is finally differentiated into two layers, a heavy 
muscular layer, the myocardium, and a thin non-muscular 
covering layer, the epicardium. 

In the apposition of the paired primordia of the heart to each 
other the splanchnic mesodeim from either side of the body 
comes together dorsal and ventral to the heart. The double- 
layered supporting membranes thus formed are known as the 
dorsal mesocardium and the ventral mesocardium, respectively 
(Fig. 26). The ventral mesocardium disappears shortly after 
its formation, leaving the heart suspended in the body cavity 
by the dorsal mesocardium (Fig. 26 E, D). Somewhat later 
the dorsal mesocardium also disappears except at the caudal end 
of the heart. Thus the heart comes to lie in the pericardial 
cavity unattached except at its two ends. The cephalic end of 
the heart remains fixed with reference to the body of the 
embryo where the ventral aorta lies embedded ventral to the 
floor of the pharynx, and the caudal end of the heart is fixed by 
the persistent portion of the dorsal mesocardium and the 
omphalomesenteric veins. 

The straight tubular condition of the heart persists but a 
short time. The unattached ventricular region becomes 
dilated and is bent out of the mid-line toward the embryo's 
right while the fiLxed bulbo-conus arteriosus and the sinus 
venosus are held in their original median position (Fig. 49, 
A-E). This bending of the heart to form a U-shaped tube 
begins to be apparent in embryos of 30 hours and becomes 
rapidly more conspicuous, until by forty hours the ventricular 
region of the heart lies well to the right of the embryo's body 
(Cf. Figs. 21 and 22). 

The bending of the heart to the side involves a considerable 
factor of ''mechanical expediency." The initiation of the 
bending process depends on the fact that the heart is becoming 
elongated more rapidly than is the chamber in which it lies 
fixed by its two ends. The fact that the bending takes place to 
the side rather than dorsally or ventrally may be attributed to 


the impediment offered to its dorsal bending by the body of the 
embryo, and to its ventral bending by the yolk. 

The lateral bending of the heart attains its greatest extent 
at about 40 hours of incubation. At this stage torsion of the 
body of the embryo changes the mechanical limitations in the 
heart region. As the embryo comes to lie on its left side the 
heart is no longer pressed against the yolk (Cf. Figs. 21 and 29). 
As a result the bend begins to swing somewhat ventrad and Hes 
less closely against the body of the embryo (Figs. 49 and 50, 

At about this stage of development a new factor affects the 
changes in the shape of the heart. The closed part of the 
U-shaped bend is forced caudad and at the same time becomes 
twisted on itself to form a loop (Figs. 49, F-I and 50, F-I). 
In the formation of the loop the atrial region is forced sHghtly to 
the left {i.e., toward the yolk) and the conus is thrown across the 
atrial region by being bent to the right {i.e., away from the yolk) 
and then caudad. The ventricular region constitutes the closed 
end of the loop. This twisting process reverses the original 
cephalo-caudal relations of the atrial and ventricular regions. 
The atrial region which was at first caudal to the ventricle now 
lies cephalic to it as in the adult heart. 

The atrial region and the ventricular region which formerly 
were continuous without any line of demarcation, are by this time 
beginning to be marked off from each other by a constriction 
(Fig. 49, /, a.v.). As both the atrium and the ventricle be- 
come enlarged, this constriction is accentuated (Fig. 49, L, a. v.). 
The constricted region is now termed the atrio-ventricular 

During the fourth day the bulbo-conus arteriosus becomes 
closely applied to the ventral surface of the atrium. As the 
atrium grows it tends to expand on either side of the depression 
made in it by the pressure of the bulbo-conus (Figs. 49, J-L 
and 50 J-L). These lateral expansions of the atrium are the 
first indication of the division of the atrium into right and left 
chambers which are later completely separated from each 
other. At the same time a sHght longitudinal groove appears 
in the surface of the ventricle (Fig. 49, L, i.v.) which indicates 
the beginning of the separation of the ventricle into right and 
left chambers. The division of the bulbo-conus to form the 



root of the adrta and the pulmonary artery does not appear 
until a later stage of development. 

During the changes in the external shape of the heart which 
have been described, the whole heart has come to occupy a 
more caudal position with reference to other structures in the 

M lomitc* 

Pig. 49. — Ventral views of the heart at various stages to show its changes 
of shape and its regional differentiation. All the drawings were made from 
dissections with the aid of camera lucida outlines. The outer of the two layers 
shown is the epi-myocardium ; the inner, the endocardium. In the stages repre- 
sented in Figs. E-H torsion of the embryo's body is going on at the level of the 
heart. Since torsion involves the more cephalic regions first and progresses 
caudad the transverse axis of the body of the embryo is at different inclinations 
to the yolk at the cephalic end and at the caudal end of the heart. In drawing 
these figures their orientation was taken from the body at the level of the conus 
region of the heart, the sinus region therefore appears inclined. Abbreviations: 
a.v., constriction between atrium and ventricle; i.v., interventricular groove. 

embryo. When the heart is first formed it lies at the level of 
the rhombencephalon. As development progresses it moves 



farther and farther caudad until at the end of the fourth day 
it Hes at the level of the anterior appendage buds. Being un- 
attached to the body, the ventricular region of the heart is 
carried farthest caudad (Cf. Figs. 19, 29, 34, and 40). 

The changes which take place in the heart wall can be seen 
best in sections. The endocardium in the heart of a four-day 

16 I 


76 HOVtS 
3t tomitct 

Fig. 50. — Dextral views of the same series of hearts shown in ventral view 
in Pig. 49. The heart drawings in Figs. 49 and 50 should be compared with 
actual specimens or with drawings of entire embryos of corresponding age for 
the relation of the heart to the body of the embryo. 

chick is still a single cell layer lining the lumen. The original 
epi-myocardium at this stage can be differentiated into an 
inner myocardial portion and an outer epicardial portion. The 
myocardium has become greatly thickened and the cells in it 
are elongated and beginning to show the histological character- 


istics of developing muscle cells. Their arrangement in bun- 
dles which project toward the lumen fore-shadows the formation 
of the muscle bands (trabeculae carneae) which ridge the inner 
wall of the adult heart. The cells of the epicardial portion of 
tlie epi-myocardium are becoming flattened to form the epi- 
thelial and connective tissue covering of the heart (epicardium) . 
Lying between the endocardium and the myocardium in the 
region of the atrio- ventricular canal and of the opening of the 
ventricle into the bulbo-conus, there are loosely aggregated 
cells which are mesenchymal in characteristics. These cells 
constitute what is called endocardial cushion tissue. They 
later take part in the formation of the septa which divide the 
heart into chambers and in the formation of the connective 
tissue frame-work of the cardiac valves. 

VI. The Urinary System 

The General Relationships of Pronephros, Mesonephros 
and Metanephros. — In the development of the urinary system 
of birds and mammals there are formed in succession three dis- 
tinct excretory organs, pronephros, mesonephros, and meta- 
nephros. The pronephros is the most anterior of the three, 
and the first to be formed. It is wholly vestigial, appearing 
only as a slurred-over recapitulation of structural conditions 
which exist in the adults of the most primitive of the vertebrate 
stock. The mesonephros is homologous with the adult excre- 
tory organs of fishes and amphibia. It makes its appearance 
in the embryo somewhat later than the pronephros, and is 
formed caudal to it. The mesonephros is the principal organ 
of excretion during early embryonic life, but it also disappears 
in the adult except for parts of its duct system which become 
associated with the reproductive organs. The metanephros 
is the most caudally located of the excretory organs, and the 
last to appear. It becomes functional toward the end of em- 
bryonic life when the mesonephros is disappearing, and per- 
sists permanently as the functional kidney of the adult. 

Figure 51 shows schematically some of the main steps in the 
embryological history of the nephric organs, which it will be 
helpful to have in mind before taking up in detail any of the 
phases of their formation in the chick. The pronephros, meso- 
nephros and metanephros are all derived from the intermediate 



mesoderm, and are all composed of units which are tubular in 
nature. In the different nephroi these tubules vary in struc- 
tural detail but their functional significance is in all cases much 
the same. They are concerned in collecting waste materials 
from the capillary plexuses which are developed in connection 
with them. In the accompanying diagrams conventionahzed 




pronephric tubules 
(degenerating) ^^ 




tubules with 





— mesonephric 


tubules without 



mesonephric duct 

I li 

mesonephric •=:> i j] 

tubules ^"nv- - ; 

and duct 

mesonephric duct 
metanephric duct 

Fig. 51. — Schematic diagrams to show the relations of pronephros, meso- 
nephros, and metanephros at various stages of development. For explanation 
see text. 

tubules have been drawn to represent the three nephric organs. 
No pretense is made of representing either the exact shape or 
the actual number of the tubules. 

In the first stage represented (Fig. 51, ^) only the pronephros 
has been established. It consists of a group of tubules empty- 
ing into a common duct, called the pronephric duct. The pro- 



nephric ducts of either side are formed first at the level of the 
pronephric tubules and then extend caudad, eventually reach- 
ing and opening into the cloaca (See arrows in Fig. 51, A). 

As the pronephric ducts are extended caudal to the level at 
which pronephric tubules are formed they come in close prox- 
imity to the developing mesonephric tubules. In their growth 
the mesonephric tubules extend toward the pronephric ducts 
and soon open into them (Fig. 51, B). Meanwhile the pro- 
nephric tubules begin to degenerate. Thus the ducts which 
originally arose in connection with the pronephros are appro- 
priated by the developing mesonephros. After the degenera- 
tion of the pronephric tubules these same ducts are called the 
mesonephric ducts because of their new associations (Fig. 51, C). 

At a considerably later stage outgrowths develop from 
the mesonephric ducts near their cloacal ends (Fig. 51, C). 
These outgrowths form the ducts of the metanephroi. They 
grow cephalo-laterad and eveiitually connect with the third 
group of tubules developed from the intermediate mesoderm, 
the metanephric tubules (Fig. 5 1 , Z>) . With the establishment 
of the metanephroi or permanent kidneys the mesonephroi 
begin to degenerate. The only parts of the mesonephric 
system to persist, except in vestigial form, are some of the ducts 
and tubules which in the male are appropriated by the testis 
as a duct system. 

The Pronephric Tubules of the Chick. — The pronephros 
in the chick is represented by tubules which first appear at about 
36 hours of incubation. The pronephric tubules arise from the 
intermediate mesoderm, or nephrotome, lateral to the somites. 
They are paired, segmen tally arranged structures, a tubule 
appearing on either side opposite each somite from the fifth to 
the sixteenth. Transverse sections passing through the loth to 
14th somites of an embryo of about 38 hours show the proneph- 
ric tubules favorably. Each tubule arises as a solid bud of cells 
organized from the intermediate mesoderm near its junction 
with the lateral mesoderm (Fig. 52, ^). At first the free ends 
of the buds grow dorsad, passing close to the posterior cardinal 
veins. Later the end of each tubule is bent caudad coming in 
contact with the tubule lying posterior to it. In this manner 
the distal ends of the tubules give rise to a continuous cord of 
cells, the primordium of the pronephric duct. The pair of cell 



cords thus formed continue to extend caudad beyond the 
pronephric tubules and soon become hollowed out to form open 
ducts. When they eventually reach the level of the cloaca they 
turn ventrad and open into it. 

The significance of the rudimentary structures in the chick 
which represent pronephric tubules, can be most readily 
understood by comparing them with fully developed and func- 
tional pronephric tubules. Figure 52, B, shows the scheme of 


dorsal aorta 

^ coelom 

, notochord 

X somite 

/^ dorsal aorta 


post, cardinal 

^^K ^ 

^ vein 


^ mesonephric 







-1 ^-"^ 

~ nephrostome 






dorsal aorta 



Fig. 52. — Drawings to show nephric tubules. A, drawing from transverse 
section through twelfth somite of i6 somite chick to show pronephric tubule. 
(After Lillie.) B, schematic diagram of functional pronephric tubule. {After 
Wiedersheim.) C, drawing from transverse section through seventeenth somite 
of 30-somite chick, to show primitive mesonephric tubule; D, schematic diagram 
of functional mesonephric tubule of primitive type. {After Wiedersheim.) 
For a later stage of the mesonephric tubules of the chick see Fig. 53, 

organization of a functional pronephric tubule. The ciHated 
nephrostome draws iij fluid from the coelom. As the fluid passes 
the capillaries of the glomus, waste materials from the blood are 
transferred to it. The nephric duct serves to collect and 
discharge the fluid passing through the tubules. Vestiges of 
a nephrostome opening into the coelom appear in the pronephric 
tubules of the chick (Fig. 5 2, A) but the tubules never become 


completely patent, and never acquire the vascular connections 
characteristic of the functional pronephros in primitive 

The Mesonephric Tubules. — The mesonephric tubules de- 
velop from the intermediate mesoderm caudal to the pronephros. 
The early steps in their formation are well shown in transverse 
sections of chicks of 29 to 30 somites (about 55 hours). In 
the posterior somites conditions are less advanced than they 
are more anteriorly. Consequently by studying the posterior 
sections of a transverse series first and then progressing cephalad 
a graded series of developmental stages may be obtained. 

The mesonephric tubules appear first as cell clusters formed 
in the intermediate mesoderm. They lie ventro-mesial to the 
cord of cells which is the primordium of the pronephric duct. 
The cells of the developing tubules acquire a more or less radial 
arrangement, and at the same time become more distinctly 
isolated from the surrounding mesoderm cells. By 55 hours of 
incubation the primordial cell cord representing the pronephric 
duct has become hollowed out to establish a definite lumen. 
The most anterior of the mesonephric tubules also have 
acquired a lumen. The growth of the tubules brings them in 
close association with the duct. In some of the more differen- 
tiated tubules indications can be made out of their opening into 
the duct which is soon to be definitely established. The more 
posterior mesonephric tubules do not become associated 
with the duct until somewhat later, but remain as a series of 
isolated vesicles. 

Figure 52, Z), shows the scheme of organization of a functional 
mesonephric tubule of primitive type. As is the case with the 
pronephric tubule, its ciliated nephrostome draws in fluid 
from the coelom. The mesonephric tubule differs from the 
pronephric chiefly in its relation to the blood vessels associated 
with it. It develops a cup-like outgrowth into which a knot 
of capillaries is pushed. The cup-shaped outgrowth from the 
tubule is called the capsule (of Bowman) and the tuft of capil- 
laries, a glomerulus. Waste-laden fluid is extracted from 
the capillaries of the glomerulus, mingles with the fluid coming 
in by way of the nephrostome. and is eventually discharged into 
the nephric duct. In mesonephric tubules of a more highly 
differentiated type the nephrostome becomes closed and all the 



fluid passing through the tubule is drawn from the glomerulus 
and other capillaries adjacent to the tubule. 

In the chick a few of the more anterior mesonephric tubules 
are of the primitive type and show vestiges of a nephrostome 
opening into the ccelom (Fig. 52, C). These anterior meso- 
nephric tubules, however, persist for but a short time, do not 
attain the characteristic relation to a glomerulus and never 
become functional. Even in chicks of four days' incubation 
the mesonephric tubules have not attained their full develop- 
ment. It is possible, however, to make out most of their 

post cardinal v.-v 



developing capsule 
and glomerulus 


Fig. 53. — Drawing from transverse section of four-day chick to show meso- 
nephric tubule and duct. For the location of the area drawn consult Fig. 46, F, 

fundamental parts (Fig. 53). The tubules lying in the ven- 
tro-Iateral portion of the mesonephros have been longest estab- 
lished and are somewhat more advanced in development than 
those lying in the dorso-mesial portion. Nearly all of the 
tubules have become elongated and somewhat coiled. At one 
end they open into the mesonephric duct or a diverticulum of 
the duct which acts as a collecting tubule. At their other end 
a cluster of closely packed cells indicates the place at which 
the capsule and glomerulus will appear. The glomeruH develop 
very rapidly. Circulation is usually estabhshed in them by 
the fifth day. From this time until about the eleventh day 


of incubation the functional activity of the mesonephros is at 
its height. After the eleventh day the developing metanephros 
begins to become active and the mesonephros degenerates. 
The establishment of the metanephros and the development 
of the genital organs occur in stages which are too advanced 
to come within the scope of this book. 

VII. The Ccelom and Mesenteries 

In a^^lt birds and mammals the body cavity consists of three 
regions, peri cardial, pleur al and-pmtOJieaL The pleural divi- 
sion is paired, each of the pleural chambers being a laterally 
situated sac containing one of the lungs. The pericardial 
chamber containing the heart, and the peritoneal chamber con- 
taining the viscera, other than the lungs and heart, are un- 
paired. These regions of the adult body cavity are formed by 
the partitioning off of the primary body cavity or coelom of 
the embryo. 

In the chick the coelom arises by a splitting of the lateral 
mesoderm of either side of the body (Fig. 54, A, B). It is 
therefore, primarily a paired cavity. Unlike the coelom of 
some of the more primitive vertebrates, the coelom of the chick 
never shows any indications of segmental pouches correspond- 
ing in arrangement with the somites. The right and left 
coelomic chambers extend antero-posteriorly without interrup- 
tion through the entire lateral plates of mesoderm. This dif- 
ference in the formation of the coelom does not imply any lack 
of homology between the coelom of the chick and that of more 
primitive forms. The process of coelom formation in the chick 
may be considered as being accelerated with a resultant slur- 
ring over of the early phases. The coelom first appears in a 
condition which is comparable with the coelom of more primi- 
tive forms at that period of differentiation when the segmen- 
tally arranged coelomic pouches have broken through into each 
other and their cavities have become confluent. 

The coelomic chambers are not limited to the region in which 
the body of the embryo is developing. They extend on either 
side into the mesoderm, which in common with the other germ 
layers, spreads out over the yolk surface. A large part of the 
primitive coelomic chambers thus comes to be extra-embryonic 



in its associations. (See Chapter XI and Figures 30 and 32.) 
The portion of the coelom which gives rise to the embryonic 
body cavities is first marked off by the series of folds which 


neural plate 

dorsal mesoderm 

intermediate mesoderm 
lateral mesoderm 


dorsal aorta 

ntermediate mesoderm 

somatic mesoderm 

splanchnic mesoderm 


mtermediate mesoderm 

embryonic coelom 
lateral body fold 


dorsal aorta 
post, cardinal v 


splanchnopleure r^r^^ 

mesonephric duct and tubule 

(from intermediate mesoderm) 
lateral amniotic fold 

intra-embryonic coelom 
extra-embryonic coelom 

liver in 

ventral • 

right and left 
coelom confluent 

Fig. 54. — Schematic diagrams of cross sections at various stages to show the 
establishment of the coelom and mesenteries. For explanation see text. 

separate the body of the embryo from the yolk (Fig. 54, C, D) . 
As the closure of the ventral body wall progresses (Fig. 54, 
E, F) the embryonic coelom becomes completely separated from 


the extra-embryonic. The delayed closure of the ventral body 
wall in the yolk-stalk region, results in the embryonic and 
extra-embryonic ccelom retaining their open communication at 
this point for a long time after they have been completely 
separated elsewhere. 

The same folding process which establishes the ventral 
body wall completes the gut ventrally (Fig. 54, C to F) . Mean- 
while the right and left ccelomic chambers are expanded mesiad. 
As a result the newly closed gut comes to He suspended between 
the two layers of splanchnic mesoderm which constitute the 
mesial walls of the right and left ccelomic chambers, respec- 
tively. The double layers of splanchnic mesoderm which thus 
become apposed to the gut and support it in the body cavity 
are known as mesenteries. The mesentery dorsal to the gut, 
suspending it from the dorsal body wall is the primary dorsal 
mesentery, and that ventral to the gut, attaching it to the ven- 
tral body wall is the primary ventral mesentery. 

When the dorsal and ventral mesenteries are first established 
they constitute a complete membranous partition dividing the 
body cavity into right and left halves. The primary dorsal 
mesentery persists in large part but the ventral mesentery early 
disappears bringing the right and left ccelomic chambers into 
confluence ventral to the gut and establishing the unpaired 
condition of the body cavity characteristic of the adult. 

In considering the early development of the heart (Chapter 
IX) the formation of the dorsal and ventral mesocardia was 
taken up. In their relation to the other mesenteries of the 
body, the inesocardia are to be regarded as special regions of the 
primary ventral mesentery. In the most cephalic part of the 
body cavity, the gut lies embedded in the dorsal body wall 
instead of being suspended by the primary dorsal mesentery as 
it is farther caudally (Cf. Fig. 26, E and Fig. 54, F). The 
ventral mesentery is, however, developed in the same manner 
anteriorly as it is posteriorly and when the heart is formed it is 
suspended in the most anterior part of the primary ventral 
mesentery. The dorsal and ventral mesocardia are the parts 
of the primary ventral mesentery lying dorsal to the heart, and 
ventral to the heart, respectively (Fig. 26, D). 

When the ventral mesocardium, and a little later the dorsal 
mesocardium, breaks through, the primary right and left coe- 



lomic chambers become confluent to form the pericardial 
region of the body cavity (Figs. 24 and 55). Later in develop- 
ment the ventral mesentery farther caudally disappears so that 
caudally as well as cephalically an unpaired condition of the 
coelom is brought about (Fig. 54, H). 

In the liver region the ventral mesentery does not disappear. 
The liver arises as an outgrowth from the gut and in its develop- 
ment extends into the ventral mesentery (Fig. 54, G). The 
portion of the ventral mesentery dorsal to the liver persists as 

ventral pancreas 
dorsal pancreas 

astro- hepatic omentum 

large intestine 


allantoic stalk 

(peritoneal region) 

Pig. 55. — Schematic lateral view of dissection of four-day chick to show the body 
cavity and the more important mesenteries. 

the gastro-hepatic omentum, and the portion ventral to the 
liver persists as its ventral ligament (falciform ligament) 

(Fig. 55)-^ 

The primary dorsal mesentery persists and forms the sup- 
porting membranes of the digestive tube. In the adult its 
different regions are named according to the parts of the digest- 
ive tube with which they are associated, as for example, meso- 
gaster that part of the primary dorsal mesentery which suspends 
the stomach, mesocolon, that part of the primary dorsal mesen- 
tery supporting the colon, etc. 

The separation of the body cavity into pericardial, pleural, 
and peritoneal chambers is accomplished by the formation of 


septa growing in from the body wall. Consideration of the 
details of their formation would lead us into stages of develop- 
ment beyond the scope of this book. Those interested in 
following the later embryology of the chick will find in the 
appendix references to more exhaustive books, and to a few of 
the more recent original papers on its development. 



For a comprehensive Bibliography of the subject reference 
should be made to Minot (1893) and to LilHe (1908). The 
references given here have been selected as representative of the 
original work which has been done in various parts of the field. 
By placing before the student references to a few of the more 
readily accessible articles it is hoped to encourage him to do 
collateral reading of original papers on subjects which arouse 
his interest. 

General Development of the Chick 

Duval, M., 1889. Atlas d'embryologie. Masson, Paris. 116 pp., 40 plates. 

Foster, M., and Balfour, F, M., 1883. The Elements of Embryology, Part I. 
The History of the Chick. Macmillan, London and New York. Second Edi- 
tion, xiv + 486 pp. 

Her twig, O., 1 901- 190 7. Handbuch der Vergleichenden und Experimentellen 
Entwickelungslehre der Wirbeltiere. (Edited by Hertwig, written by numerous 
collaborators.) Fischer, Jena. 

Kaupp, B. F., 1918. The Anatomy of the Domestic Fowl. Saunders, 
Philadelphia and London, 37 s PP- 

Keibel, F., and Abraham, K., 1900. Normaltafeln zur Entwickelungs- 
geschichte des Huhnes (Gallus domesticus). Fischer, Jesna. 132 pp., 3 plates. 

Kellicott, W. E., 1913. Outlines of Chordate Development. Holt, New 
York. V -|- 471 pp. 

Kerr, J. G., 1919. Textbook of Embryology. Vol. II. Vertebrata with the 
Exception of Mammalia. Macmillan, London and New York, xii +591 pp. 

Lillie, F. R., 1908. The Development of the Chick. Holt, New York. 
Second Edition, 1919. xi + 472 pp. 

Marshall, A. M., 1893. Vertebrate Embryology. (Chap. IV, The Develop- 
ment of the Chick.) Putnam, New York and London, xxiii + 640 pp. 

Minot, C. S., 1893. A Bibliography of Vertebrate Embryology. Memoirs, 
Boston Soc. Nat. History, Vol. IV, Number XI, pp. 487-614. 

Minot, C. S., 1903. Laboratory Text Book of Embryology. Blakiston's 
Son, Philadelphia. Second Edition, 191 1. xii + 402 pp. 

Waite, F. C, and Patten, B. M., 1918. An Outline of Laboratory Work in 
Vertebrate Embryology. Part I. The Chick. Judson, Cleveland. 27 pp. 

Gametogenesis and Fertilization 

Bartelmez, G. W., 19 12. The Bilaterality of the Pigeon's Egg. A Study in 
Egg Organization from the First Growth Period of the Oocyte to the Beginning 
of Cleavage. Jour, of Morph., Vol. 23, pp. 269-328. 

Firket, Jean, 1920. On the Origin of Germ-cells in Higher Vertebrates. 
Anat. Rec, Vol. 18, No. 3. 



Guyer, M., 1909. The Spermatogenesis of the Domestic Chicken. Ant. 
Anz., Bd. 34, pp. 573-580. 

Harper, E. H., 1904. The Fertilization and Early Development of the 
Pigeon's Egg. Am. Jour. Anat., Vol. Ill, pp. 349-386. 

Kellicott, W. E., 1913. A Text-book of General Embryology. Holt, New 
York. V + 376 pp. 

Marshall, F. H. A., 1910. The Physiology of Reproduction. Longmans, 
Green, London, xvii + 706 pp. 

Pearl R., and Curtis, M. R., 191 2. Studies on the Physiology of Reproduction 
in the Domestic Fowl. V. Data Regarding the Physiology of the Oviduct. 
Jour. Exp. Zool., Vol. 12, pp. 99-132. 

Riddle, 0., 191 1. On the Formation, Significance and Chemistry of the 
White and Yellow Yolk of Ova. Jour. Morph., Vol. 22, pp. 455-492. 

Swift, C. H., 1914. Origin and Early History of the Primordial Germ-cells 
in the Chick. Am. Jour. Anat., Vol. 15, pp. 483-516. 

Swift, C. H., 1915. Origin of the Definitive Sex-cells in the Female Chick 
and Their Relation to the Primordial Germ-cells. Am. Jour. Anat., Vol. 18, 
pp. 441-470. 

Swift, C. H., 1916. Origin of the Sex-cords and Definitive Spermatogonia in 
the Male Chick. Am. Jour. Anat., Vol. 20, pp. 375-410. 

Cleavage, Gastrulation, Genn -layer Formation, and the Early Dififerentiation 

of the Embryo 

Bartelmez, G. W., 1918. The Relation of the Embryo to the Principal 
Axis of Symmetry in the Bird's Egg. Biol. Bull., Vol. 35, pp. 319-361. 

Blount, M., 1907. The Early Development of the Pigeon's Egg, with Especial 
Reference to the Supernumerary Sperm Nuclei, the Periblast, and the Germ-wall. 
Biol. Bull., Vol. XIII, pp. 231-250. 

Edwards, C. L., 1902. The Physiological Zero and the Index of Development 
for the Egg of the Domestic Fowl. Am. Jour. Physiol., Vol. VI, pp. 351-397. 

Eycleshymer, A. C, 1907. Some Observations and Experiments on the 
Natural and Artificial Incubation of the Egg of the Conmion Fowl. Biol. Bull., 
Vol. XIII, pp. 360-374. 

Hubbard, M. E., 1908. Some Experinients on the Order of Succession of 
the Somites of the Chick. Am. Nat., Vol. 42, pp. 466-471. 

Lewis, Warren H. and Lewis, Margaret R., 1912. The Cultivation of Chick 
Tissues in Media of Known Chemical Constitution. Anat. Rec, Vol. 6, pp. 

McWhorter, J. E., and Whipple, A. C, 191 2. The Development of the 
Blastoderm of the Chick in Vitrio. Anat. Rec, Vol. 6, pp. 1 21-140. 

Patterson, J. T., 1907. The Order of Appearance of the Anterior Somites in 
the Chick. Biol. Bull., Vol. XIII, pp. 1 21-133. 

Patterson, J. T., 1909. Gastrulation in the Pigeon's Egg; a Morphological and 
Experimental Study. Jour. Morph., Vol. 20, pp.65-123. 

Patterson, J. T., 1910. Studies on the Early Development of the Hen's Egg. 
I. History of the Early Cleavage and of the Accessory Cleavage. Jour, of 
Morph., Vol. 21, pp. 101-134. 

Peebles, F., 1904. The Location of the Chick Embryo upon the Blastoderm. 
Jour. Exp. Z06I., Vol. I, pp. 369-384. 

Piatt, J. B., 1889. Studies on the Primitive Axial Segmentation of the Chick. 
Bull. Mus. Comp. Zool. Harv., Vol. 17. 


The Nervous System and Sense Organs 

Abel, W., 191 2. Further Observations on the Development of the Sympa- 
thetic Nervous System in the Chick. Jour. Anat. and Physiol., Vol. 47, pp. 

Beard, J., 1888. Morphological Studies, II. The Development of the 
Nerv^ous System of Vertebrates, Pt. I. Elasmobranchs and Aves. Quar. 
Jour. Micr. Sc, Vol. XXIX, pp. 153-228. 

Cajal, S. R. y.,.1889. Sur la morphologie et les connexions des Elements de 
la retine des oiseaux. Anat. Anz., Bd. IV, pp. 111-121. 

Cajal, S. R. y., 1890. Sur I'origine et le ramifications des fibres nerveuses de 
la moelle embryonnaire. Anat. Anz., Bd. V, pp. 85-95 a-nd 111-119. 

Carpenter, F. W., 1906. The Development of the Oculomotor Nerve, the 
Ciliary Ganglion, and the Abducent Nerve in the Chick. Bull. Mus. Comp. 
Zool. Harv., Vol. XL VIII. 

Cohn, F., 1903. Zur entwickelungsgeschichte des Geruchsorgans des Hiinch-' 
ens. Arch. mikr. Anat. u. Entw., Bd. LXE, pp. 133-150. 

Cowdry, E. V., 1914. The Development of the Cytoplasmic Constituents 
of the Nerve Cells of the Chick. Am. Jour. Anat., Vol. 15, pp. 389-430. 

Hill, C, 1900. Developmental History of the Primary Segments of the 
Vertebrate Head. Zool. Jahrbiicher, Abth. Anat., Bd. XIII. 

Kupffer, K. v., 1905. Die Morphogenie des Central nervensystems. Hert- 
wig's Handbuch, etc., Bd. II, Teil 3, K. VIII. 

Lewis, W. H., 1903. Wandering Pigmented Cells Arising from the Epithelium 
of the Optic Cup, with Observations on the Origin of the M. Sphincter Pupillae 
in the Chick. Am. Jour. Anat., Vol. 2, pp. 405-416. 

Marshall, A. M., 1878. The Development of the Cranial Nerves in the 
Chick. Quar. Jour. Micr. Sc, Vol. XVIII. 

Retzius, G., 1881-1884. Das Gehororgan der Wirbelthiere. II. Theil, 
Reptilien, Vogel, Sanger. Stockholm. 

Weysse, A. W., and Burgess, W. S., 1906. Histogenesis of the Retina. Am. 
Naturalist, Vol. XL, pp. 611-638. 

The Circulatory System 

Boas, J. E. v., 1887. Ueber die Arterienbogen der Wirbeltiere. Morph. 
Jahrb., Bd. XIII, pp. 115-118. 

Chapman, W. B., 1918. The Effect of the Heart-beat upon the Development 
of the Vascular System in the Chick. Am. Jour. Anat., Vol. 23, pp. 175-203. 

Clark, Eleanor Linton, 191 5. Observations on the Lymph Flow and the 
Associated Morphological Changes in the Early Superficial Lymphatics of Chick 
Embryos. Am. Jour. Anat., Vol. 18, pp. 399-440. 

Evans, H. M., 1909. On the Development of the Aortae, Cardinal and 
Umbilical Veins and other Blood-vessels of Vertebrate Embryos from Capillaries. 
Anat. Record, Vol. 3, pp. 498-518. 

Greil, A., 1903. Beitrage zur vergleichenden Anatomie und Entwicklungs- 
geschichte des Herzens und des Truncus arteriosus der Wirbelthiere. Morph. 
Jahrb., Vol. 31, pp. 123-310. 

Hochstetter, F., 1906. Die Entwickelung des Blutgefasssystems. Hertwig's 
Handbuch, etc., Bd. Ill, Teil 2. 

Locy, W. A., 1906. The Fifth and Sixth Aortic Arches in Chick Embryos 
with Comments on the Condition of the Same Vessels in other Vertebrates. 
Anat. Anz., Bd. XXIX, pp. 287-300. 


Mackay, J. Y., 1888. The Development of the Branchial Arterial Arches 
in Birds, with Special Reference to the Origin of the Subclavians and Carotids. 
Phil. Trans. Roy. Soc. London, Vol. 179, Ser. B, pp. 111-139. 

Masius, J., 1889. Quelques notes sur le developpement du coeur chez le poulet. 
Arch. Biol., T. IX, pp. 403-41 8. 

Miller, A. M., 1903. The Development of the Postcaval Vein in Birds. Am. 
Jour. Anat., Vol. 2, pp. 283-298. 

Miller, A. M., and McWhorter, J. E., 1914. Experiments on the Develop- 
ment of Blood Vessels in the Area Pellucida and Embryonic Body of the Chick 
Anat. Rec, Vol. 8, pp. 203-227. 

Patterson, J. T., 1909. An Experimental Study on the Development of the 
Vascular Area of the Chick Blastoderm. Biol. Bull., Vol. 16, pp. 83-90. 

Sabine, Florence R., 191 7. Preliminary Note on the Differentiation of 
Angioblasts and the Method by which they Produce Blood-vessels, Blood- 
plasma and Red Blood-cells as seen in the Living Chick. Anat. Rec, Vol. 13, 
pp. 199-204. 

Stockard, C. R., 1915. An Experimental Analysis of the Origin of Blood and 
Vascular Endothelium. Memoirs Wistar Inst. No. 7, 174 pp. 

Twining, Granville H., 1906. The Embryonic History of the Carotid Arteries 
in the Chick. Anat. Anz., Bd. XXIX, pp. 650-663. 

The Digestive and Respiratory Systems and the Division of the Body Cavities 

Boyden, Edward A., 191 8. Vestigial Gill Filaments in Chick Embryos 
with a Note on Similar Structures in Reptiles. Am. Jour. Anat., Vol.23, pp. 

Brouha, M., 1898. Recherches sur le developpement du foie, du pancreas^ 
de la cloison mesent6rique et des cavities hepato-enteriques chez les oiseaux. 
Jour, de I'anat. et phys., T. XXXIV. 

Butler, G. W., 1889. On the Subdivisions of the Body-cavity in Lizards, 
Crocodiles, and Birds. Proc. Zool. Soc. London for 1889, pp. 452-474. 

Hammar, G. A., 1897. Ueber einige Hauptzuge der ersten embryonalen 
Leberentwickelung. Anat. Anz., Bd. XIII, pp. 233-247. 

Lockward, C. B., 1888. The Early Development of the Pericardium, Dia- 
phragm and Great Veins. Phil. Trans. Roy. Soc. London, Vol. CLXXIX, B, 

pp. 365-384- 

Locy, W. A., and Larsell, O., 1916. The Embryology of the Bird's Lung 
Based on Observations of the Domestic Fowl. Am. Jour. Anat., Vol. 19, pp. 
447-504 and Vol. 20, pp. 1-44. 

Mall, F. P., 1 89 1. Development of the Lesser Peritoneal Cavity in Birds and 
Mammals. Jour. Morph., Vol. V, pp. 165-179. 

Minot, C. S., 1900. On the Solid Stage of the Large Intestine in the Chick. 
Jour. Bos. Soc. Med. Sc, Vol. IV. 

Minot, C. S., 1900. On a Hitherto Unrecognized Form of Blood-circulation 
without Capillaries in the Organs of Vertebrata. Proc. Bos. Soc. of Nat. Hist, 
Vol. XXIX, pp. 185-215. 

Ravn, E., 1899. Ueber die Entwickelung des Septum Transversum, Anat., Bd. XV, pp. 528-534. 

Schreiner, K. E., 1900. Beitrage zur Hitologie und Embryologie des Vorder- 
darms der Vogel. Zeitschr. wiss. Zool., Bd. LXVIII. 


The Urinogenital System 

Felix, u. BiJhler., 1906. Die Entwickelung der Harn- und Geschlechts organe. 
Hertwig's Handbuch, etc., Bd. Ill, Teil I, K. II. 

Firket, Jean, 1914. Recherches sur I'organogen^se des glands sexuelles chez 
les oiseaux. Arch, de Biol., Tome 29, pp. 201-351. 

Retterer, E., 1885. Contribution a I'etude du cloaque et de la bourse de 
Fabricius chez les oiseaux. Jour, de 1' anat. et de la phys. XXI, pp. 369-454. 

Sedgwick, A., 1880. Development of the Kidney in its Relation to the 
Wolffian Body in the Chick. Quart. Jour. Micr. Sc, Vol. XX, pp. 146-166. 

Sedgwick, A., 1881. On the Early Development of the Anterior Part of the 
Wolffian Duct and Body in the Chick Together with Some Remarks on the 
Excretory System of Vertebra ta. Quart. Jour. Micr. Sc, Vol. XXI, pp. 432-468. 

Schreiner, K. E., 1902. Ueber die Entwickelung der Amniotenniere. Zeitschr. 
wiss. Zool., Bd. LXXI. 

The Skeletal and Muscular Systems 

Brachet, A., 1893. Etude sur la resorption de cartilage et le developpement 
des OS longs chez les oiseaux. Internat. Monatschr. Anat. und Phys., Bd. X. 

Engert, H., 1900. Die Entwickelung der ventralen Rumpfmuskulatur bei 
Vogeln. Morph. Jahrb., Bd. XXIX, pp. 169-185. 

Isaacs, Raphael, 191 9. The Structure and Mechanics of Developing Con- 
nective Tissue. Anat. Rec, Vol. 17, pp. 243-270. 

Johnson, Alice, 1883. On the Development of the Pelvic Girdle and Skeleton 
of the Hind Limb in the Chick. Quar, Jour. Micr. Sc, Vol. XXIIl. 

Kingsbury, B. F., 1920. The Developmental Origin of the Notochord. 
Science, N. S., Vol. 51, pp. 190-193. 

Parker, W. K., 1869. On the Structure and Development of the Skull of the 
Common Fowl (Gallus domesticus). Phil. Trans. Roy. Soc, London, Vol. 
CLIX, Part II, pp. 755-807. 

Parker, W. K., 1888. On the Structure and Development of the Wing of the 
Common Fowl. Phil. Trans. Roy. Soc, London, Vol. 179, Ser. B, pp. 385-398. 

Paterson, A. M., 1888. On the Fate of the Muscle Plate and the Develop- 
ment of the Spinal Nerves and Limb Plexuses in Birds and Mammals. Quart. 
Jour. Mic. Sci., Vol. 2S, pp. 109-130. 

Williams, L. W., 1910. The Somites of the Chick. Am. Jour. Anat., Vol. 
"> PP- S5-IOO. 

Extra-embryonic Membranes 

Danchakoff, Vera, 191 7. The Position of the Respiratory Vascular Net 
in the Allantois of the Chick. Am. Jour. Anat., Vol. 21, pp. 407-420. 

Duval, M., 1884. Etudes histologiques et morphologiques sur les annexes 
des embryoAS d'oiseaux. Jour, de I'anat. et de la phys., T. XX. 

Lillie, F. R., 1903. Experimental Studies on the Development of the Organs 
in the Embryo of the Fowl (Gallus domesticus). i. Experiments on the Amnion 
and the Production of Anamiote Embryos of the Chick. Biol. Bull., Vol. V, 
pp. 92-124. 

Popoff, D., 1894. Die Dottersackgefasse des Huhnes. Wiesbaden. 

Shore, T. W., and Pickering, J. W., 1889. The Proamnion and Amnion in the 
Chick. Jour, of Anat. and Phys., Vol. XXIV, pp. 1-2 1. 

Stuart, T. P. A., 1899. A Mode of Demonstrating the Developing Membranes 
in the Chick. Jour. Anat. and Phys., Vol. XXV, pp. 299-300. 


The Ductless Glands 

Atwell, W. J., and Si tier, Ida, 191 8. The Early Appearance of the Anlagen 
of the Pars Tuberalis in the Hypophysis of the Chick. Anat. Rec, Vol. 15, 
pp. 181-187. 

Poll, H., 1906. Die vergleichende Entwickelungsgeschichte der Nebennieren 
systeme der Wlrbeltiere. Hertwig, O., Handbuch der Vergleichenden und 
Experimentellen Entwickelungslehre der Wirbeltiere. (Edited by Hertwig, 
written by numerous collaborators.) Fischer, Jena. Bd. Ill, Teil i, K. II, 2. 

Soulie, A. H., 1903. Recherches sur le d^veloppement des capsules surrenales 
chez les vert6br6s superi^urs. Jour, de I'anat. et physiol., T. XXXIX, pp. 

Verdun, M. P., 1898. Sur les d^riv^s branchiaux du poulet. Comptes rendus 
See. Biol., Tom. V. 


Alsop, Florence M., 1919. The Effect of Abnormal Temperatures upon 
the Developing Nervous System in the Chick Embryos. Anat. Rec, Vol. 15, 

pp. 307-323- 

Glaser, O., 1913. On the Origin of Double-yolked Eggs. Biol. Bull., Vol, 
24, pp. 175-186. 

Mitchell, P. C, 1891. On a Double-chick Embryo. Jour, of Anat. and 
Physiol., Vol. 25, pp. 316-324. 

Pohlman, A. G., 1920. A Consideration of the Branchial Arcades in Chick 
Based on the Anomalous Persistence of the Fourth Left Arch in a Sixteen-day 
Stage. Anat. Rec, Vol. 18, pp. 159-166. 

O'Donoghue, C. H., 1910. Three Examples of Duplicity in Chick Embryos 
with a Case of Ovum in Ovo. Anat. Anz., Bd. 37, pp. 530-536. 

Stockard, Charles R., 1914. The Artificial Production of Eye Abnormalities 
in the Chicken Embryo. Anat. Rec, Vol. 8, pp. 33-42, 

Tannreuther, G. W., 1919. Partial and Complete Duplicity in Chick Em- 
bryos. Anat. Rec, Vol. 16, pp. 355-367. 


To facilitate the use of this book in connection with others in which the termi- 
nology may dififer somewhat, many synonyms which were not used in the text 
have been put into the index and cross-referenced to the alternative terms used 
in this book. For example, WolflSan body, a term not used in this text, is fre- 
quently applied to the mesonephros. It appears in the index thus: Wolflfian 
body (= mesonephros, q.v.). 

Both figure and page references are given in the index. The figure references 
are preceded by the letter f . 

Accessory cleavage, 19 
Accessory coverings of ovum, f. 3, 10 
Acoustico-facialis ganglion ( = gang- 
lion complex of VII and VIII 
cranial nerves) f. 40, 118 
Acoustic ganglion, f. 42, 118, 123 
Air space, f. 3, 12 
Albumen, f. 3, 10 
Albumen-sac, f. 30, f. 32, 84, 87 
Alecithal ovum (see isolecithal). 
Allantoic, circulation (see circulation). 

diverticulum, f. $$, 90 

stalk, f. 33, f. 43, 90 

vesicle, f. 30, f. 32, f. 33, f. 40, 
90, 113 
Allan tois, fate of, 137 

formation of, f. 33, 90 

function of, 90, 137 

relations of, f. 30, f. 32 
Amnion, formation, f. 30, f. 32, 86, 87 

fuaiction of, 86 

muscle fibers of, 86 

relations of, f. 30, f. 32 
Amnion, false, 92 
Amnio-cardiac vesicles, 49 
Amniotic, cavity, f. 30, f. 32, 87 

fluid, 86 

folds, f. 30, f. 32, 87 

raphe, 87 
Anal plate (see cloacal membrane). 
Animal pole, 8 

Anterior horns of mesoderm, f . 1 2 
Anterior intestinal portal, f. 16, f. 17, 

f. 31, 46, 57, 69 
Anterior neuropore, f. 19, 55, 99 

Aortas dorsal, formation of, 73 

fusion of, 105, 138 

position of, f. 23, f. 24, f. 35, f. 47 
Aorta, ventral, f. 23, f. 24, f. 35, f. 47, 

f. 73,- los, 137 
Aortic arches, fate of, 138 

formation of, 105 

position of, f. 24, f. 35, f. 47 
Aortic roots, dorsal, f. 34, f. 47, 137 

ventral, f. 23, f. 35, f. 47, 72, 137 
Appendage buds, anterior, f. 39, f. 40, 

posterior, f. 39, f. 40, 112 
Aqueduct of Sylvius, f. 42, 117 
Area opaca, f. 11, f, 13, 24, 36 

vasculosa, f. 15, f. 17, 51 

vitellina, f. 15, f. 17, 51 
Area pellucida, f. 11, f. 13, 24 
Area vasculosa, 51, 58 
Arteries, allantoic, f. 47, 138 

aortic (see aorta) 

carotid, ext. f. 47, 137 

carotid, int. f. 47, 137 

coeliac, 139 

definition of, 133 

iliac, f. 47, 138 

mesenteric, 139 

omphalomesenteric, f. 29, f. 47, 
78, los, 138 

pulmonary, 138 

segmental, 138 

sub-clavian, 138 

vitelline, f. 48, 135 
Atrium, f. 23, f. 49, f. 50, 72, 104, 141 
Atrio-ventricular constriction, f. 49, 141 





Auditory, ganglion (see acoustic), 
nerve, 123 
pit, f. 22, 65 
placode, 65, 122 
vesicle, f. 36, f. 40, 65, 122 

Bile duct, common, 126 
Blastocoele, f. 6, 21, 23 
Blastoderm, f. 6, 20, 24 

zones of, f. 7, 24 
Blastodisc, 16 
Blastomere, 16 
Blastopore, f. 6, 22 

closure of, 26 

concrescence of, f. 9, 28 

formation of, in birds, f . 7, 26 

homologies of, 23 
Blastula, 20, 21, 24 
Blood, as a carrier of food, 79, 132 

oxygenation of, 78, 133 
Blood cells, origin of, f. 25, 66 
Blood islands, differentiation of, f. 25, 

formation of, f , 25, 51 

location of, f. 15, f. 17 
Blood-vessels, formation of, f. 25, 
66, 72 (see also arteries and 
Body cavity (see coelom) , 
Body folds, f. 30, f. 32, 80 
Bowman's capsule, 148 
Brain, first differentiation of, 53 

neuromeric structure of, 59 

primary vesicles, f . 20, 54, 60 

secondary vesicles, f. 42, 63, 114 

ventricles of, f. 42, 115 
Branchial arches (see visceral arches). 
Bulbo-conus arteriosus, f . 23 , f . 49, 

f. 50, 72, 141 
Bulbus arteriosus (see bulbo-conus). 

Capsule of Bowman, 148 
Caudad, usage of term, 5 
Caudal, usage of term, 5 
Caudal fold, f. 31, 81 
Caudal flexure, 1 1 1 
Central canal of spinal cord, 119 
Cephalad, usage of term, 5 
Cephalic, usage of term, 5 
Cephalic limiting fold, 80 
Cephalic mesoderm, 40, 50 
Cephalic neural crest, f. 22, loi 

Cerebellar peduncles, 118 

Cerebellum, 118 

Cerebral ganglia (see ganglia, cranial). 

Cerebral hemispheres, 115 

Cervical flexure, 94, iii 

Chalaza, f. 3, 10 

Chorion, 92 

Choroid coat of eye, 122 

Choroid fissure of eye, f. 35, f. 42, 98, 

Choroid plexus, 117, 118 

Circulation, allantoic, f. 47, 136 
course of embryonic, 78, 132 
establishment of, 78 
intra-embryonic, f. 47, 137 
significance of embryonic, 131 
vitelline, f. 48, 68, 77, 134 

Cleavage, accessory, 19 
discoidal, f. 5, 16 
holoblastic, f. 4, 16 
meroblastic, f. 4, 16 
process of, in birds, f. 5, 16 

Cleavage cavity (see blastocoele). 

Cloaca, f. 31, f. 43» 130 

Cloacal membrane, f. 31, 130 

Cloacal opening, 130 

Coelom, divisions of embryonic, 150 
extra-and intra-embryonic, f. 28, 

f. 30, f. 32, 49, 151 
formation of, f, 54, 49> 150 
pericardial region of, f. 16, f. 24, 
f. 26, f. 27, 49» 72, ISO 

Concrescence, of blastopore, f. 9, 28 
of anterior intestinal portal, 69 

Conus arteriosus (see bulbo-conus). 

Conjunctival epithelium, 122 

Cornea, 122 

Corpora quadrigemina, 117 

Corpus vitreum (see vitreous body). 

Cranial flexure, 75, 11 1 

Crura cerebri, 117 

Cutis plate (see dermatome). 

Cystic duct, 126 

Deutoplasm, 7 

effect of on cleavage, f . 4, 14 
effect of on gastrulation, f. 6, 21 

Dermatome, f. 38, f. 44, 107 

Diencephalon, f. 42, 65, 116 

Diocoele (= lumen of diencephalon, 
q. v.). 

Dio-mesencephalic boundary, f. 42, 117 



Dio-telencephalic boundary, f. 42, 115 

Discoidal cleavage (see cleavage). 

Dorsad, usage of term, 5 

Dorsal aorta (see aorta). 

Dorsal flexure, in 

Dorsal mesentery, f. 54, f. 55, 152 

Dorsal mesocardium, f. 26, 69, 71, 140, 

Dorsal nerve roots, f. 44, 119 
Dorsal pancreatic bud, 127 
Dorsal root ganglia, f. 44, 119 
Dorsal, usage of term, 5 
Duct of Cuvier (= common cardinal 

vein, q. v.). 
Ductus arteriosus (part of aortic arch 

Ductus choledochus, f. 46 E., 127 
Ductus endo-lymphaticus, f. 40, 122 
Ductus venosus (= fused portion of 

omphalomesenteric vein, q. 


Ear, 122 

Ectoderm, derivatives of, 31 

establishment of, 23 
Egg, membranes, f. 3, 10 

ovarian, f. i, 7 

shell, 10, 12 

structure of at lajdng, f. 3, 11 
Embryo, external form of, 93, 109 

separation of from blastoderm, 
f. 30, f. 32, 80 
Embryonal area, 42 
Embryonic circulation (see circula- 
Endocardial cushion tissue, f. 46 D, 144 
Endocardial primordia, f. 26, f. 27, 69 
Endocardium, 143 
Endolymphatic duct, f. 40, 122 
Entoderm, derivatives of, 32 

establishment of, 20, 23 
Endothelium, origin of vascular, f. 25, 

Epicardium, 69, 143 
Epichordal portion of brain, 55 
Epimyocardium, fate of, 140, 144 

formation of, f. 26, f. 27, 69 
Epiphysis, f. 35, f. 42, 95, 116 
Eustachian tube, 103, 123 
Extra-embryonic ccelom (see coelom). 
Extra-embryonic membranes, f. 30, 
f. 32, Chap. XI 

Extra-embryonic vascular plexus (see 
vitelline circulation and 
blood-vessels, origin of). 

Eye, 120 

Facial region, f. 41. in 

Facial nerve (= cranial nerve VII), 

Falciform ligament, 153 
Fertilization, 9 
Flexion, 75, no 
Floor plate of spinal cord, 119 
Foramen of Monro, f. 42, 114 
Follicle, ovarian, f. i, 7 
Fore-brain (see prosencephalon). 
Fore-gut (see gut). 
Fovea cardiaca (= anterior intestinal 

portal q. v.). 
Frontal process, f. 41 

Gall bladder, 126 

Gametes, 7 

Ganglia, cranial, f. 42, 118 

dorsal root (see spinal). 

spinal, f. 44, 119 

sympathetic, f. 44, 120 
Ganglion jugulare (= ganglion of 

cranial nerve X.) f. 42, 118 
Gasserian ganglion (= ganglion of 
cranial nerve V) f. 40, 118 
Gastrocoele, f, 6, f. 7, 22, 26 
Gastro-hepatic omentum, 153 
Gastrulation, Chap. IV 

effect of yolk on, f. 6, 21 

in Amphioxus, 22 

in Amphibia, 23 

in birds, f. 7, 24 
Geniculate ganglion (= ganglion of 
cranial nerve VII); f.42, 118 
Germ cells (see gametes). 
Germ layers (see ectoderm, entoderm 

and mesoderm). 
Germinal disc (see blastodisc). 
Germinal epithelium of ovary, f, i 
Germinal vesicle ( = nucleus of ovum, 

q. v.). 
Germ wall, 24 

Gill arches (see visceral arches). 
Glomerulus, f. 52, f. 53, 148 
Glomus, f. 52 

Glossopharyngeal nerve (= cranial 
nerve IX), f. 42, 118 



Glottis, 125 

Granular zone of follicle, 8 
Gut, delimitation of embryonic, 81 
fore-, f. 17, f. 31, 46, 57, 84, loi 
hind-, f. 31, 84, 102, 130 
mid-, f. 31, 84, 102, 127 
pre-oral, f. 31, 102, 124 
primitive, f. 13, f. 31, 36 
post-anal, f. 31, 130 

Head fold, 43, 80 
Head fold of anmion, f. 29, 86 
Head process (see notochord). 
Heart, differentiation of, f. 49, f. 50, 
104, 139 

establishment of f. 26, f. 27, 57, 68 

primordia of, 50, 71 
Heart-beat, 72 

Hensen's Node, f. 8, f. 11, f. 13, 28 
Hepatic duct, 126 
Hepatic-portal circulation, 127 
Hepatic tubules, 126 
Hind-brain (see rhombencephalon). 
Hind-gut (see gut). 
Holoblastic cleavage (see cleavage). 
Homolecithal ova ( = isolecithal, q. v.) . 
Hyoid arch, f. 39, f. 41, 103 
Hyomandibular cleft, f. 34, 103, 123 
Hypophysis, 95, 117 

Incubation, 12 

Infundibulum, f. 35, f. 42, f. 43, 63, 95, 

Intermediate mesoderm (see meso- 
derm). • 

Internal ear, 123 

Interventricular sulcus, f. 49, 141 

Intestine, 127 

Intra-embryonic ccelom (see coelom). 

Invagination of entoderm (see gastru- 

Isolecithal ova, 14 

Jugular vein (see vein, anterior cardi- 

Kidney (see metanephros). 

Lamina terminalis, f. 42, 114 
Latebra, f. 3, 12 
Lateral body folds, f. 30, 80 
Lateral limiting sulci (= lateral body 
folds, q. V.) 

Lateral mesoderm (see mesoderm). 
Lateral plate of spinal cord, 119 
Lateral telencephalic vesicles (see 

Lateral wings or horns of mesoderm, f. 

12, 37 
Lens, differentiation of, f. 45, 121 

fibers, 122 

origin of, 98 

vesicle, f. 36, 98 
Liver, f. 43, f. 46, 126 
Lung buds, f. 46, 125 

Mandibular arch, f. 36, f. 4I; 103, 112 

Mandible, 112 

Marginal notch, f. 9 

Margin of overgrowth, f. 7, 24 

Maturation of gametes, 9 

Maxilla, 112 

Maxillary process, f. 41, 112 

Meatus venosus (= ductus venosus, 

q. v.). 
Medulla, ji8 
Medullary plate (= neural plate, 

q. v.). 
Meroblastic cleavage (see cleavage). 
Mesencephalon, f. 42, 54, 65, 117 
Mesenchyme, 50 
Mesenteries, dorsal, f. 54, f. 55, 152 

formation of, 150 

ventral, f. 54, f.s 5,15 2 
Mesoblast (= mesoderm, q. v.). 
Mesocardium, dorsal, f. 26, 69, 71, 140, 

ventral, f. 26, 69, 140, 152 
Mesocolon, 153 

Mesocoele ( = lumen of mesencepha- 
lon, q. v.). 
Mesoderm, derivatives of, 32 

differentiation of, 37 

dorsal, f. 17, f. 29, f. 54, 38, 47 

early growth of, f. 12, 37 

formation of, f. 10, 30 

intermediate, f. 28, f. 54, 47, 144 

of the head, 40, 50 

regional divisions of, 47 

segmental zone of, 40 

somatic layer of, f. 28, f. 54, 49, 

somites of, f. 38, 47, 56, 105 

splanchnic layer of, f. 28, f. 54, 
49, 66, 150, 152 



Mesodermic somites (see mesoderm). 
Meso-diencephalic boundary, f. 42, 117 
Mesogaster, 153 
Meso-metencephalic boundary, f. 42, 

Mesonephric duct, f. 51, f. 52, f. 53, 

146, 149 
Mesonephric tubules, f. 51, f. 52, f. 53, 

146, 148 
Mesonephros, f. 47, 144 
Mesothelium (= epithelial layer of 

mesoderm lining coelom) f . 54 
Metamerism, in mesoderm, 40, 47, 48, 

in nervous system, f . 20, 59 
Metanephros, f. 51, 144 
Metacoele ( = lumen of metencephalon 

Metencephalon, f. 42, 65, 117 
Metanephric duct, f. 51, 146 
Metanephric tubules, f. 51, 146 
Mid -brain (see mesencephalon). 
Middle ear, 123 
Mid-gut (see gut). 
Morula, 20, 21 
Mouth opening, 112 
Muscle plate (see myotome). 
Myelencephalic tela (= thin roof of 

myelencephalon) f. 42, 118 
Myelencephalon, f. 42, 65, 118 
Myeloccele (= lumen of myelen- 
cephalon q. v.). 
Myelo-metencephalic boundary, f, 42, 

Myocardium, 69, 143 
Myocoele, 107 
Myotome, f. 38, f. 44, 107 

Nasal pit (see olfactory pit). 
Naso-lateral process, f. 41, 112 
Naso-medial process, f. 41, 112 
Naso-optic groove, f. 41 
Neck of latebra, f . 3 
Nephric tubules, f. 51, 145 
Nephrostome, f. 52, 147 
Nephrotomic plate, 48 
Nerves, cranial, 118 

spinal, f. 44, 119 

sympathetic, t2o 
Neural cagial ( = lumen of neural 

Neural crest, f. 37, 99, 120 

Neural fold, f. 17, 42, 45, 99 
Neural groove, f. 17, 42, 44 
Neural plate, f. 11, f. 13, 41 
Neural tube, 52, 99 
Neurenteric canal, 56 
Neuromeres, f. 20, 59 
Neuropore, anterior, f. 19, 55, 99 

posterior, 56 
Notochord, f. 11, f. 13, 40, 55 
Nucleus of Pander, f. 3, 12 

(Esophagus, f. 43, loi, 126 
Olfactory nerve (= cranial nerve I), 

Olfactory pit, f. 40, f. 41, f. 46, 112, 123 
Optic chiasma, f . 42 
Optic cup, f. 42, 95, 121 
Optic lobes, 117 
Optic nerve (= cranial nerve II) 

98, 122 
Optic stalk, f. 45, 98, 122 
Optic vesicle, primary, f. 23, f. 28, 54, 


secondary, f. 36, 97, 120 
Opticoele (= lumen of primary optic 

vesicle, q. v.). 
Oral cavity, 102 
Oral opening, 1 24 
Oral plate, f. 31, 124 
Oral region, f, 41, in 
Orientation of embryo within egg, f . 30 
Otocyst (see auditory vesicle). 
Ovum, fertilization of. 9 

maturation of, 9 

ovarian, f. i, 7 
Ovulation, 9 

Pancreas, f. 43, 127 
Pander's nucleus, f. 3, 12 
Pellucid area (see area pellucida). 
Petrosal ganglion (= gangh'on of 
cranial, nerve IX) f. 42, 118 
Periblast, 10 
Pericardial region of coelom, f. 24^ 

f. 27, f. 55, 49, 1^^ 150 
Peritoneal region of coelom, 150 
Pharyngeal pouches, f. 36, 103 
Pharyngeal derivatives, 124 
Phar)mx, f. 35, loi 
Pigment layer of retina, f. 45, 96, 122 
Pineal gland, 95 
Pituitary body, 95 



Placodes, auditory^ 65, 122 
lens, 98 

Pleural region of coelom, f. 46D, 150 

Plica encephali ventralis (= ventral 
cephalic fold) f. 42 

Pocket, subcaudal, f. 31, 81 
subcephalic, f. 31, 47 
Rathke'sf. 35, f. 43, 95, 117 
Seessell's, f. 43, 102, 124 

Polar bodies, 9 

Polyspermy, 10 

Pons, 118 

Post-anal gut (see gut). 

Posterior appendage bud, f. 39, f. 40, 

Posterior commissure, f . 42 

Posterior intestinal portal, f . 3 1 

Posterior neuropore, 56 

Post-oral arches, 103 

Post-oral clefts, 103 

Prechordal portion of brain, 55 

Pre-oral gut (see gut). 

Primitive groove, f. 13, 31 

Primitive gut (see gut). 

Primitive node (= Hensen's node, 
q. v.). 

Primitive pit, f. 13, 28 

Primitive plate, f. 29 

Primitive ridge or fold, f. 13, 28 

Primitive streak, as growth center. 

fate of, 56 

formation of, f. 9, f. 10, 28 
interpretation of, f. 9, f. 10, 28, 

location of, f. 8, f. 11, 27 

Primordial follicle ( = very young 
ovarian follicle) f. i 

Proamnion, f. 12, 37 

Proctodaeum, f. 31, 130 

Pronephros, f. 51, 144 

Pronephric duct, 146 

Pronephric tubules of chick, f. 52, 

Prosencephalon, f. 20, 54, 61, 95, 114 

Prosocoele (= lumen of prosen- 
cephalon, q. v.). 

Ramus communicans, 119 
Rathke's pocket, f. 35, f- 43> 9S» ii7 
Recapitulation, 43, 102, 144 
Recessus neuroporicus, f. 42 

Recessus opticus, f. 42, 115 
Reduction division of gametes, 9 
Retina, pigment layer of, f. 45, 96, 122 
sensory layer of, f. 45, 96, 122 
Rhombencephalon, f. 20, 54, 61, 65 
Rhombocoele (= lumen of Rhomben- 
cephalon, q. v.). 
Roof plate of spinal cord, 119 

Sclera of eye, 122 

Sclerotomes, f. 38, f. 44, 107 

Sections, location of, 4, 34 

Seessell's pocket, f. 43, 102, 124 

Segmentation, 14 (see also cleavage). 

Segmentation cavity (see blastocoele). 

Sensory layer of retina (see retina). 

Septa of yolk sac, f. 30, 84 

Serial sections, 4 

Sero-amniotic cavity, f. 30, f. 32, 87 

Sero-amniotic raphe, f. 30, f. 32, 87 

Serosa, f. 30, f. 32, 86 

Sex cells (see gametes) . 

Shell, f. 3, 10 

Shell membranes, f. 3, 10 

Sinus region of the heart (see sinus 

Sinus rhomboidalis, f. 21, 55, 99 
Sinus terminalis (= terminal vein, 

q. v.). 
Sinus venosus, f. 23, f. 49, f. 50, 72 
Somatic mesoderm (see mesoderm). 
Somatopleure, f. 17, 49 
Somites, diflferentiation of, f. 38, 105 

formation of, 56 
Spermatozoa, f. 2, 10 
Spinal cord, 54, 118 
Spinal ganglia (see ganglia). 
Spinal nerve roots, development of, 

f. 44, IT9 

Splanchnic mesoderm (see mesoderm). 
Splanchnopleure, f. 17, 49 
Stomach, f. 43, 126 
Stomodaeum, f. 31, f. 35, loi, 124 
Subcaudal space or pocket, f. 31, 81 
Subcephalic space or pocket, f. 17, 

f. 31, 47 
Subgerminal cavity (= blastoccele 

q. v.). 
Sylvian aqueduct, f. 42, 117 
Sympathetic ganglia, f. 44, j2o 
Sympathetic nerve roots (see ramus 




Tail,!. 39, 81 

Tail fold of amnion, f. 32, 87 

Telencephalon, later development of, 


lateral vesicles of, f. 42, 114 

median, f. 42, 114 

origin of, 65, 95 
Teloccele (= lumen of telencephalon, 

q. v.). 
Telo-diencephalic boundary, 115 
Telolecithal ova, f. 4, 15 
Thalami (optici), 117 
Theca folliculi, f. i, 8 
Thymus, 125 

Thyro-glossal duct, f. 43, 125 
Thyroid gland, 125 
Torsion of embryo, f. 29, 75, 109 
Trabeculae carneae, f, 46D, 144 
Trachea, f. 43, 125 

Trigeminal ganglion (= Gasserian 
ganglion of cranial nerve 
Trigeminal nerve (= Cranial nerve 

V), 118 
Tuberculum posterious, f. 42, 117 

Ureter (derived from metanephric 
duct, q. v.). 

Vagus nerve (=« cranial nerve X), 118 

Vegetative pole, 8 

Vein, allantoic, f. 47 

cardinal, ant. f. 24, 74, 105, 139 

cardinal, common (= Duct of 

Cuvier) f. 24, f. 47, 74, 105 

cardinal, posterior, f. 24, 74, 105, 

definition of, 133 
omphalomesenteric, f. 21, f. 47, 

57, 74, 105, 127 
terminal (= sinus terminalis), 

f. 21, f. 48, 136 

vena cava, 139 
vitelline, f. 48 
Velum transversum, f. 42, 115 
Ventrad, usage of term, 5 
Ventral, usage of term, 5 
Ventral aorta (see aorta). 
Ventral aortic roots (see aortic roots) . 
Ventral cephalic fold, f . 42 
Ventral ligament of liver, 153 
Ventral mesentery (see mesenteries). 
Ventral mesocardium (see meso- 

Ventral nerve roots, f. 44, 119 
Ventricle, f. 23, f . 49, f. 50, 72, 141 
Ventro-lateral pancreatic buds, 127 
Visceral arches, f. 34, f. 40, f. 46, 102, 

Visceral clefts, f. 34, f. 40, 102, 11 1 
Visceral furrows, f. 36, f. 46, 103 
Visceral pouches (= pharyngeal 

pouches),f.36, 103, 125 
Vitelline blood-vessels (see arteries and 

veins) . 
Vitelline circulation (see circulation). 
Vitelline membrane, f. i, f. 3, 8. 
Vitreous body of eye, 122 

Wolffian body ( =mesonephros, q. v.). 
Wolffian duct (= mesonephric duct, 
q. v.). 

Yolk, absorption of, 84, 136 

effect of on gastrulation, f. 6, 21 

effect of on segmentation, f. 4, 14 

white, f. I, f. 3, 12 

yellow, f. I, f. 3, 12 
Yolk duct, 84 

Yolk-sac, f. 30, f. 32, 81, 84,86 
Yolk stalk, f. 30, f. 31, f. 32, 84 

Zona radiata, f. i, 8 

Zone of junction, f. 7, 21, 24 

Zones of the blastoderm, 24 



San Francisco Medical Center 


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