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THE EARLY EMBRYOLOGY

THE CHICK

PATTEN

THE EARLY EMBRYOLOGY

THE CHICK

BRADLEY M. PATTEN

ASSISTANT PROFESSOR OF HISTOLOGY AND EMBRYOLOGY
SCHOOL OF MEDICINE, WESTERN RESERVE UNIVERSITY

WITH 55 ILLUSTRATIONS CONTAINING
182 FIGURES

PHILADELPHIA

P. BLAKISTON'S SON & CO

1012 WALNUT STREET

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151

PREFACE

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

VI PREFACE

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
legends.

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.

CONTENTS

Page
Preface v

CHAPTER I
Introduction i

CHAPTER II

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.

CHAPTER III

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.

CHAPTER IV

The Establishment of the Entoderm 20

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

CHAPTER V

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.

CHAPTER VI

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.

CHAPTER VII

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.

Vlll CONTENTS

CHAPTER VIIl

Page
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.

CHAPTER IX

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.

CHAPTER X

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.

CHAPTER XI

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.

CHAPTER XII

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.

CONTENTS

CHAPTER XIII

Page

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.

APPENDIX

References for Collateral Reading 155

Index 161

CHAPTER I

INTRODUCTION

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

2 EARLY EMBRYOLOGY OF THE CHICK

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
impressions.

A knowledge of the phenomena of development is ordinarily

INTRODUCTION 3

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-

4 EARLY EMBRYOLOGY OF THE CHICK

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

INTRODUCTION 5

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-

O EARLY EMBRYOLOGY OF THE CHICK

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.

CHAPTER II

THE GAMETES AND FERTILIZATION

The ovarian ovum; maturation, ovulation, and fertiliza-
tion; THE FORMATION OF THE ACCESSORY COVERINGS OF

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

EARLY EMBRYOLOGY OF THE CHICK

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-

GAMETES AND FERTILIZATION

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-
witz.)

lO EARLY EMBRYOLOGY OF THE CHICK

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
length.

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,

GAMETES AND. FERTILIZATION II

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
schematically.

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
chapter.

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

12 EARLY EMBRYOLOGY OF THE CHICK

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-

GAMETES AND FERTILIZATION 13

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
temperatures.

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.

CHAPTER III

THE PROCESS OF SEGMENTATION

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

PROCESS OF SEGMENTATION

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

1 6 EARLY EMBRYOLOGY OF THE CHICK

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
segmentation.

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

PROCESS OF SEGMENTATION 1 7

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

EARLY EMBRYOLOGY OF THE CHICK

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.

PROCESS OF SEGMENTATION IQ

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.

CHAPTER IV
THE ESTABLISHMENT OF THE ENTODERM

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

BIRDS.

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

ESTABLISHMENT OF THE ENTODERM 21

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

EARLY EMBRYOLOGY OF THE CHICK

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

GASTRULATION IN PORM WITH ISOLECITHAL EGG HAVING ALMOST NO YOLK— AMPHIOXU&

GASTRULATION IN FORM WITH TELOLECITHAL EGG CONTAINING MODERATE
AMOUNT OF YOLK— AMPHIBIA.

GASTRULATION IN FORM WITH TELOLECITHAL EGG CONTAINING LARGE
AMOUNT OF YOLK— BIRDS.

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.

ESTABLISHMENT OF THE ENTODERM 23

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.

24 EARLY EMBRYOLOGY OF THE CHICK

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.

ESTABLISHMENT OF THE ENTODERM

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).

26 EARLY EMBRYOLOGY OF THE CHICK

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).

CHAPTER V

THE FORMATION OF THE PRIMITIVE STREAK AND
THE ESTABLISHMENT OF THE MESODERM

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

OF THE blastopore; THE FORMATION OF THE MESODERM.

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-

28 EARLY EMBRYOLOGY OF THE CHICK

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.

FORMATION OF THE PRIMITIVE STREAK

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

30 EARLY EMBRYOLOGY OF THE CHICK

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

FORMATION OF THE PRIMITIVE STREAK

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

yolk

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

32 EARLY EMBRYOLOGY OF THE CHICK

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.

CHAPTER VI

FROM THE PRIMITIVE STREAK STAGE TO THE
APPEARANCE OF THE SOMITES

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

PRIMITIVE gut; the GROWTH AND DIFFERENTIATION OF THE
MESODERM; THE FORMATION OF THE NOTOCHORD; THE
FORMATION OF THE NEURAL PLATE; THE DIFFERENTIATION
OF THE EMBRYONAL AREA.

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

EARLY EMBRYOLOGY OF THE CHICK

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

-r:

notochord
-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

PRIMITIVE STREAK TO SOMITE FORMATION 35

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
layers.

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.

36 EARLY EMBRYOLOGY OF THE CHICK

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

PRIMITIVE STREAK TO SOMITE FORMATION 37

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-

EARLY EMBRYOLOGY OF THE CHICK

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
streak

peUucida.

CHICK OF ABOUT 14 HOURS.

anterior horn of
mesoderm

...^n'i^+^.

]2 CHICK OF ABOUT 18 HOURS,
proamnion

dorsal mesoderm

primitive streak

V^ CHICK OF ABOUT 22 HOURS.

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

PRIMITIVE STREAK TO SOMITE FORMATION

■^^m^^^

prumtive gut

nucleus
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
dots.

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.

40 EARLY EMBRYOLOGY OF THE CHICK

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

PRIMITIVE STREAK TO SOMITE FORMATION

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

notochord

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

42 EARLY EMBRYOLOGY OF THE CHICK

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).

PRIMITIVE STREAK TO SOMITE FORMATION 43

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.

CHAPTER VII

THE STRUCTURE OF TWENTY-FOUR HOUR CHICKS

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

STRUCTURE OF TWENTY-FOUR HOUR CHICKS

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

.unsegmented
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

EARLY EMBRYOLOGY OF THE CHICK

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

(entoderm)

notochord

11 r :

margin of area opaca

ectoderm of head

" — mesenchyme

■ „ border of mesoderm

— — pericardial region
of coelom

~ — thickened splanchnic
mesoderm

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-

STRUCTURE OF TWENTY-FOUR HOUR CHICKS 47

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.

EARLY EMBRYOLOGY OF THE CHICK

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

proamnion
region

primitive
ridge

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.

STRUCTURE OF TWENTY-FOUR HOUR CHICKS 49

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
splanchnopleure.

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
separated.

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

50 EARLY EMBRYOLOGY OF THE CHICK

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
arise.

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).

STRUCTURE OF TWENTY-FOUR HOUR CHICKS 5 1

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.

CHAPTER VIII

THE CHANGES BETWEEN TWENTY-FOUR AND THIRTY-
THREE HOURS OF INCUBATION

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-
IZATION IN THE AREA VASCULOSA.

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

CHANGES BETWEEN 24 AND ^^ HOURS

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 /

neuropore

border of fore-gut

subcephalic pocket

mesenchyme

omphalo-
mesenteric vein

blood island

border ot ..... .^. -y -.» .

inesodenn. ' v^^^v^'^5?iT-;> '*•.

rhomboidalis
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

EARLY EMBRYOLOGY OF THE CHICK

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

prosencephalon

optic vesicle

ventral aortic root

ventral aorta

epi-myocardium
endocardium

line of endocardi al
fusion

margin of anterior
intestinal porta!

anterior horn of mesoderm

anterior neuropore

infundibulum

cephalic
mesenchyme

extra-embryonic
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

CHANGES BETWEEN 24 AND 33 HOURS 55

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
demarcation.

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-

56 EARLY EMBRYOLOGY OF THE CHICK

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
homologue.

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

CHANGES BETWEEN 24 AND 33 HOURS $7

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
formed.

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
advanced.

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

58 EARLY EMBRYOLOGY OF THE CHICK

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,
21).

CHAPTER IX

THE STRUCTURE OF CHICKS BETWEEN THIRTY-THREE
AND THIRTY-NINE HOURS OF INCUBATION

The divisions of the brain and their neuromeric struc-
ture; THE auditory PITS; THE FORMATION OF EXTRA-EM-
BRYONIC BLOOD vessels; THE FORMATION OF THE HEART;
THE FORMATION OF INTRA-EMBRYONIC BLOOD VESSELS.

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-

EARLY EMBRYOLOGY OF THE CHICK

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

neuromeric
enlargement

line of fusion
neural folds

rhombencephalon

prosencephalon

mesencephalon

metencephalon

myelencephalon

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

STRUCTURE OF THIRTY-THREE HOUR CHICKS

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-

prosencephalon

proamnion

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

EARLY EMBRYOLOGY OF THE CHICK

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

>-'5-

^fir ***»»»„,„

-v.^>

prosencephalon

cctodeim

^"'m,,^

^ optic vesicle

infundibulum -—^

' :!'^'

-^^m

L^m

^^^^

mesencephalon

^^m^

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

ventral

-''1

r^'HrTfWR

f^f

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 ^

-^H^^P^

t ,

myelencephalon ^-

{

^^^\

" ' irteriosus

cephalic neural ere at —

region of ganglion

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

VII VIII

t^iUHB ;AnL#'«HSpid

■ '

■■r

'AjPjBK-glW ■ ^ -,

'WmU^

*^ V >•

L^^^ S-fll^^

I ^^S vl^^ I

vein

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

STRUCTURE OF THIRTY-THREE HOUR CHICKS

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.

prosencephalon

nfundibulum

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

EARLY EMBRYOLOGY OF THE CHICK

STRUCTURE OF THIRTY-THREE HOUR CHICKS 65

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.

66 EARLY EMBRYOLOGY OF THE CHICK

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
appearance.

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

STRUCTURE OF THIRTY-THREE HOUR CHICKS

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.

yolk

ectoderm

central cells of
blood island

peripheral cell
of blood island

ectoderm

blood cells
entoderm cell

somatic
mesoderm
coelom

endothelial cell
lumen

yolk

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

68 EARLY EMBRYOLOGY OF THE CHICK

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

STRUCTURE OF THIRTY-THREE HOUR CHICKS 69

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

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

EARLY EMBRYOLOGY OF THE CHICK

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
splanchnopleure

splanchnic mesoderm

gut itrnncdiaoely caudal to
anterior intestinal portal

neural groove

epi-myocard

I somatopleure

\- splanchnopleure

myocardium

endocardium

gut immediately caudal to
anterior intestinal portal

dorsal mesoderm

fore-gut

epi-myocardium

endocardium

line of fusion of lateral margins of
anterior intestinal portal

dorsal mesoderm

fore-gut

dorsal mesocardium

ventral mesocardium

|— somatopleure

}- splanchnopleure
epi-myocardium

dorsal mesoderm
notochord

dorsal mesocardium

endocardium

} — splanchnopleure

epi-myocardium

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).

STRUCTURE OF THIRTY-THREE HOUR CHICKS

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

pericardial
_ _ _ region of coelom ^

epi-myocardium

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

1*.:\

ventral aortic
root

pericardial
^-•region of coelom -^.^

epi-myocardium
endocardium

omphalomesenteric

vein

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

72 EARLY EMBRYOLOGY OF THE CHICK

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
relationships.

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

STRUCTURE OF THIRTY-THREE HOUR CHICKS

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

ectoderm
of blastoderm

extra-embryonic
coelom

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

74 EARLY EMBRYOLOGY OF THE CHICK

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.

CHAPTER X

THE CHANGES BETWEEN FORTY AND FIFTY HOURS
OF INCUBATION

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

EARLY EMBRYOLOGY OF THE CHICK

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

mesencephalon

metencephalon

myelencephalon
auditory pit

sinus resion

somite,
lateral mesoderm-
lateral body fold

unsegmented dorsal
mesoderm

prosencephalon

optic vesicle

margin of
head fold of amnion

bulbo-conus arteriosus

ventricular region
atrial region
omphalomesenteric vein

extra-embryonic
vascular plexus

oipphalo mesenteric
artery

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

CHANGES BETWEEN 40 AND 50 HOURS 77

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

78 EARLY EMBRYOLOGY OF THE CHICK

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
albumen.

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

CHANGES BETWEEN 40 AND 50 HOURS 79

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.

CHAPTER XI

EXTRA-EMBRYONIC MEMBRANES

The folding off of the body of the embryo; the establish-
ment OF THE YOLK-SAC AND THE DELIMITATION OF THE
EMBRYONIC GUT; THE AMNION AND THE SEROSA; THE
ALLANTOIS.

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
folds.

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).

EXTRA-EMBRYONIC MEMBRANES 8 1

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

EARLY EMBRYOLOGY OF THE CHICK

embryo

lateral amniotic fold
lateral body fold

ex -embryonic
coelom

ectoderm ^
mesoderm J

mes")

pleure

splanch-
hopleure

yolk

amniotic cavity

lateral
amniotic fold

amnion
/ somatopleure)
serosa
Tsomatopleure)

embryo

allantois ( splanchnopleure )
yolk stalk

yolk-sac
/splanch-
nopleure \

albumen

vitelline membrane

Fig. 30.

EXTRA-EMBRYONIC MEMBRANES

allantoic cavity

allantois

amnion
amniotic

extra-embryonic
coelom

somatopleure

yolk-sac
/ splanchno-
pleure )

albumen

allantoic cavity

allantois
serosa

shell

sero-ammotic
cavity

yolk-sac

albumen

vitelline
membrane

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.

•84 EARLY EMBRYOLOGY OF THE CHICK

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
stalk.

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
accomplish.

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

EXTEA-EMBRYONIC MEMBRANES

ectoderm of neural plate
ectoderm of blastoderm

primitive pit

primitive streak

yolk

lii-^v^r^

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

fore-gut

neural tube
ectoderm of head

subcephalic pocket

splanchnopleure;
of yolk-sac

open neural groove
primitive pit

B pericardial region ' anterior intestinal

of coelom

portal

fore-gut

subcephalic pocket

extra-embryonic
coelom

•» ■d*'do*<'o''.

antenor posterior

intestinal portal intestinal portal

hind-gur

subcaudal pocket

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

splanchnopleure
of yolk-sac

post-anal gut
proctodaeum

mid-gut

splanchnopleure
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.

86 EARLY EMBRYOLOGY OF THE CHICK

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.

EXTRA-EMBRYONIC MEMBRANES 87

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.

EARLY EMBRYOLOGY OF THE CHICK

EXTRA-EMBRYONIC MEMBRANES

Ci"

•^

Lill
Fig.
ibry

C^"

^-^

X»

-IJ

-S

•<->

•S

'ti

Ox!

>»

-s-S

^ ^

'c3

y « a,

o.lj

"g g

go EARLY EMBRYOLOGY OF THE CHICK

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

EXTRA-EMBRYONIC ME MBR ANE S

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
notochord

amniotic cavity

sero-amniotic cavity
hind- gut

proctodaeum

' f«

neural tube -
notochord -

mesenchyme :^'~*-^"'~ -"*^« ^V-

mid-gut
entoderm
splanchnic
mesoderm •

yolk stalk If"'- If

#if

If 11

j^M'^%<

wt-

\ic

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

Mf , a'^ «* jr\ 0 •'. -f ' d^'6'- '*■'''■ ," " ' 0

u j^^;jjj^:^£,^^m

^ .

,0 -0:

amniotic cavity
cloaca

. cloaca 1

membrane

post-anal
gut

sero-amniotK
cavity

proctodaeum

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-
cubation.

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

The fusion of the allantoic mesoderm and blood vessels

92 EARLY EMBRYOLOGY OF THE CHICK

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.

CHAPTER XII

THE STRUCTURE OF CHICKS FROM FIFTY TO FIFTY-
FIVE HOURS OF INCUBATION

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

EARLY EMBRYOLOGY OF THE CHICK

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.

mesencephalon

metencephaMc region
dorsal aortic root
myelencephahc region

hyomandibular cleft
auditory vesicle
aortic archill

anL int. nnyfal

optic cup
/lens

epiphysis

choroid fissure

prosencephalon.

bulbo-conus
arteriosus
atrium

lateral mesoderm
marginof amnion
lateral body fold

neural tube
,29th somite

omphalomesenterif
artery

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).

STRUCTURE OF FIFTY-HOUR CHICKS 95

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
region.

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
body.

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

EARLY EMBRYOLOGY OF THE CHICK

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

prosencephalon
choroid fissure
Rathke's pocket

ventral aortic root-

anterior intestinal
portal

mesencephalon

cut ectoderm

metencephalon

anterior cardinal vein
myelencephalon

neuromere of

myelencephalon
auditory vesicle

aortic arches I. II, III.
pharynx

duct of Cuvier
posterior cardinal vein
dorsal aorta

omphalomesenteric vein

cut splanchnopleure
cut somatopleure

roots of oinphal(
mesenteric artery

lateral mesoderm

om phjjomesenter ic
artery

posterior intestinal
portal

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,

STRUCTURE OF FIFTY-HOUR CHICKS

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
cavity

fore-gut

intra-embryonic coelom

dorsal mesocardium
sero-amniotic raphe

extra-embryonic
coelom

epi-myocardium of
ventricle

somatopleure

splanchnopleure

vitelline vessels
extra-embryonic coelom

atnum

neural crest

dorsal aorta

post, cardinal v.

•embryonic coelom
intra-embryonic coelom
omphalomesenteric vein

lateral amniotic fold
amnion
serosa

mesonephric duct
mesonephric tubule
mid-gut

lateral
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-

98 EARLY EMBRYOLOGY OF THE CHICK

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

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

STRUCTURE OF FIFTY-HOUR CHICKS 99

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
neuromeres.

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

lOO

EARLY EMBRYOLOGY OF THE CHICK

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

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
chick.

(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
crest.

The neural crest should not be confused with the margin of

STRUCTURE OF FIFTY-HOUR CHICKS lOI

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.

I02 EARLY EMBRYOLOGY OF THE CHICK

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

STRUCTURE OF FIFTY-HOUR CHICKS 103

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

I04 EARLY EMBRYOLOGY OF THE CHICK

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
grasped.

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

STRUCTURE OF FIFTY-HOUR CHICKS IO5

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

io6

EARLY EMBRYOLOGY OF THE CHICK

neural fold

ectoderm of head

somite

intermediate mesoderm

somatic mesoderm
coelom
splanchnic mesoderm
entoderm

epithelial layer of somite

core of somite

pronephric tubule
(intermediate mesoderm)

somatic mesoderm

coelom
iplanchnic mesoderm
entoderm

epithelial layer of somite

cavity of somite
core of somite
migrating cells

posterior cardinal vein
mesonephric duct
mesonephric tubule
coelom
dorsal aorta

dorsal ganglion

(neural crest)

myotome

dermatome
sclerotome

myocoele

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

somites.
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.

STRUCTURE OF FIFTY-HOUR CHICKS 107

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
wanting.

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
only.

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
body.

Io8 EARLY EMBRYOLOGY OF THE CHICK

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.

CHAPTER XIII

THE DEVELOPMENT OF THE CHICK DURING THE
THIRD AND FOURTH DAYS OF INCUBATION

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

109

EARLY EMBRYOLOGY OF THE CHICK

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).

0 myelencephalon

ganglion IX
visceral cleft II

aortic arch IV

bulbo-conus
arteriosus

hyoid arch
auditory vesicle / . hyomandibular cleft

mandibular arch
ganglion V

metencephalon

ant. cardinal v.

mesencephalon

horoid fissure
— lens

sensory layer
pigment layer

appendage bud

posterior
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

STRUCTURE OF FOUR-DAY CHICKS

III

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).

myelencephalon
visceral arch III
bulbo-conusarteriosus
atrium

auditory vesicle

endolymphatic duct
ganglion IX/ / ganglion VII-VIII

hyomandi bular cleft
mandibular arch

ganglion V

meten-
cephalon

mesen-
cephalon

anterior
appendage bud

omphalo-
mesenteric
vein

border
mesoneph;

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

112

EARLY EMBRYOLOGY OF THE CHICK

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-

epiphytif

lateral telencephalic
vesicle

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

STRUCTURE OF FOUR-DAY CHICKS II3

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).

114 EARLY EMBRYOLOGY OF THE CHICK

The original neuromeric enlargements persist longest in the
rhombencephalon.

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

STRUCTURE OF FOUR-DAY CHICKS

(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.

metacoele
( ventricle IV )
thin roof of myelencephalon
myelocoele

cle IV )

ventral cephalic fold

spinal cord

recessus opticus
lamina termina

median telocoele
(ventricle III)
recessus neuroporicus

meso-metenceohalic fold

mesocoele
(Sylvian aqueduct j

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

metencephalon

mesencephalon

gangli
ganglion VII VIII

lamina ..

terminalis /median telocoele

( ventricle III )

foramen of Monro

(sylvian aqueduct^

lateral telencephalic
vesicle

metacoele
^ventricle IV )

myelocoele
( 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

ii6

EARLY EMBRYOLOGY OF THE CHICK

(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,
vein

tneionephros
somite

dortal aorta

tuberculum
posteriuB
infundibulum

allantoic vesicle

somite
allantoic stallr

proctodaeum
post- anal gut
cloaca

— 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-

STRUCTURE OF FOUR-DAY CHICKS II7

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-
cephalon.

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

Il8 EARLY EMBRYOLOGY OF THE CHICK

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

STRUCTURE OF FOUR-DAY CHICKS

119

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

ganglion

dorsal root
ventral root
spinal nerve

neuron of
ventral root
(motor)

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

I20 EARLY EMBRYOLOGY OF THE CHICK

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
viscera.

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

STRUCTURE OF FOUR-DAY CHICKS

121

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).

ectoderm

diocoele
mesenchyme

concentration of

mesenchyme
pigment layer
sensory layer

lens

area enlarged in B

corneal region

optic stalk

'•^

P-gr

' 'ill

pigment
layer of retina

sensory
layer of retina

developing
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; p.gr., 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

122 EARLY EMBRYOLOGY OF THE CHICK

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
cornea.

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

STRUCTURE OF FOUR-DAY CHICKS 1 23

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).

124 EARLY EMBRYOLOGY OF THE CHICK

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

STRUCTURE OF FOUR-DAY CHICKS 1 25

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

126 EARLY EMBRYOLOGY OF THE CHICK

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.
(Fig.46,£).

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-

STRUCTURE OF FOUR-DAY CHICKS I27

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
adult.

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

128

ganglion VII-VIII
auditoty vesicle

EARLY EMBRYOLOGY OF THE CHICK

ganglion V

myelocoele

branch of

int. carotid a.

anterior cardinal vem

branch of
ant. cardinal v.
metacoele

neuromere

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 \

visceral

cleft III/ / \

visceral arch WV \

visceral cleft

pericardial

region of coelom.^^

trachea^ \ ^^^

oesophagus

j^^^^N^^j;^— ^kj

neural i^^
tube— ^S

^^^^r 1

pharynx

int. carotid a.

ant. cardinal v.
mesococle

■'?;^

dorul aorta'

atnum
bulbo-conus arteriosus

pharyngeal pouch I

mandibular arch
'hyomandibular cleft
hyoid arch

diocoele

ventral body wall '

optic stalk

sensory layer of retina

pigment layer of retina

olfactory pit

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

lung bud

pleural region

Dof coelom left duct
of Cuvier

diocoele

pericardial region of coelom

Fig. 46

STRUCTURE OF FOUR-DAY CHICKS

129

ductus choledochus
mesonephric duct
dorsal mesentery

dorsal ganglion

neural tube

omphaloniesenteric vein
ventricle

lateral telencephalic
vesicle

ectoderm of hea4

dorsal
ganglion
post, cardinal v.

dorsal aorta
mesonephric duct

allantoic vein

vitelline
vessels

omphalomesenteric veins

entoderm

sub^ intestinal

vein
allantoic vein
allantoic stalk

allantoic art.
coelom
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.

130 EARLY EMBRYOLOGY OF THE CHICK

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
embryos.

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
fore-gut.

STRUCTURE OF FOUR-DAY CHICKS I3I

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

132 EARLY EMBRYOLOGY OF THE CHICK

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
conditions.

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

STRUCTURE OF FOUR-DAY CHICKS 133

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
misconception.

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

134

EARLY EMBRYOLOGY OF THE CHICK

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.

dorsal
aorta .

mesoncphros

^..Au*^

post, cardinal v
hind-KUt

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
observer.

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).

STRUCTURE OF FOUR-DAY CHICKS

.135

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

136 EARLY EMBRYOLOGY OF THE CHICK

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
assimilated.

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-

STRUCTURE OF FOUR-DAY CHICKS 137

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

138 EARLY EMBRYOLOGY OF THE CHICK

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
adult.

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

STRUCTURE OF POUR-DAY CHICKS 1 39

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

140 EARLY EMBRYOLOGY OF THE CHICK

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

STRUCTURE OF FOUR-DAY CHICKS 141

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
canal.

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

142

EARLY EMBRYOLOGY OF THE CHICK

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

STRUCTURE OF FOUR-DAY CHICKS

143

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

D38t
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-

144 EARLY EMBRYOLOGY OF THE CHICK

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

STRUCTURE OF FOUR-DAY CHICKS

145

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

fr-

pronephric

tubules

pronephric tubules
(degenerating) ^^

mesonephric

1??

pronephric

tubules with

l/^j^

duct

nephrostomes

/'^^^

— mesonephric
tubules

mesonephric

tubules without

nephrostom

mesonephric duct

I li

mesonephric •=:> i j]

tubules ^"nv-- ;

and duct
degenerating

mesonephric duct
metanephric duct
cloaca

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-

146 EARLY EMBRYOLOGY OF THE CHICK

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

STRUCTURE OF FOUR-DAY CHICKS

147

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

ntermediate
mesoderm

dorsal aorta

^ coelom

, notochord

X somite

/^ dorsal aorta

v/^

post, cardinal

^^K ^

^ vein

k^\/^

^ mesonephric

W^^^^

duct

^^^

mesonephric

<S^'^

tubule

-1 ^-"^

~ nephrostome

coelom

nephrostome

glomus

somite

dorsal aorta

:$.

nephrostome
glomerulus

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

148 EARLY EMBRYOLOGY OF THE CHICK

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

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

STRUCTURE OF FOUR-DAY CHICKS

149

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
coelom

jnesonephnc
duct

mesonephric
tubule

developing capsule
and glomerulus

mesentery

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

150 EARLY EMBRYOLOGY OF THE CHICK

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, pericardial, pleural 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

STRUCTURE OF FOUR-DAY CHICKS

151

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

A
B
C

neural plate
notochord
entoderm

dorsal mesoderm

intermediate mesoderm
lateral mesoderm

splanchnopleure

dorsal aorta
somatopleure

ntermediate mesoderm

somatic mesoderm

splanchnic mesoderm

splanchnopleure

mtermediate mesoderm

embryonic coelom
lateral body fold

extra-embryonic
coelom

dorsal aorta
post, cardinal v

mesenchyme

somatopleure
splanchnopleure r^r^^

mesonephric duct and tubule

(from intermediate mesoderm)
lateral amniotic fold

intra-embryonic coelom
extra-embryonic coelom

liver in

ventral •
mesentery

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

152 EARLY EMBRYOLOGY OF THE CHICK

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-

STRUCTURE OF FOUR-DAY CHICKS

153

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
stomach

large intestine

(pericardial
region)

allantoic stalk

coelom
(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

154 EARLY EMBRYOLOGY OF THE CHICK

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.

APPENDIX

REFERENCES FOR COLLATERAL READING

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.

155

156 EARLY EMBRYOLOGY OF THE CHICK

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.
207-212.

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.

APPENDIX 157

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.
35-72.

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.

158 EARLY EMBRYOLOGY OF THE CHICK

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.
205-235.

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.
.A.nz., Bd. XV, pp. 528-534.

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

APPENDIX 159

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.

l6o EARLY EMBRYOLOGY OF THE CHICK

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.
197-293.

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

Anomalies

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.

INDEX

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,
112

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

161

l62

INDEX

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,
66,67

formation of, f , 25, 51

location of, f. 15, f. 17
Blood-vessels, formation of, f. 25,
66, 72 (see also arteries and
veins).
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,
121

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

INDEX

163

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,

152
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

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

omphalomesenteric vein, q.

v.).

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-
tion).
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,

66
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),

118
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

164

INDEX '

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,
116

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-
lation).

Isolecithal ova, 14

Jugular vein (see vein, anterior cardi-
nal).

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

telencephalon).
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,
152

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,
150

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

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

INDEX

i6s

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

117
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,

150
in nervous system, f . 20, 59
Metanephros, f. 51, 144
Metacoele ( = lumen of metencephalon

q.v.)
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,

117
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

tube).
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),

123
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,

62,9s

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

z66

INDEX

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,
112

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.

33
fate of, 56

formation of, f. 9, f. 10, 28
interpretation of, f. 9, f. 10, 28,

35
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,
146

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

venosus).
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

communicans).

INDEX

167

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
V,q.v.).
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,

139
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-

cardium).
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,

III
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

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San Francisco Medical Center

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14 DAY
NOV 22 1970

25w-10.'67(H552584)4128

413^1

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Full text of "The early embryology of the chick"

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