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OUTLINES OF

CHORDATE DEVELOPMENT

BY
WILLIAM E. KELLICOTT

PROFESSOR OF BIOLOGr IN QOUCHEH COLLEGE

NEW YORK
HENRY HOLT AND COMPANY

EARTH

SCIENCE*

MATTHEW LIBRARY

COPYRIGHT, 1913,

BY
HENRY HOLT AND COMPANY

August, 1927

.*. I I •! •*;.•••••* • •

PREFACE

In these " Outlines" the student is introduced to the study
of Chordate development through the embryological history
of Amphioxus. Whether or not Amphioxus represents a truly
primitive type of development, it affords, in simple diagram-
matic style, the essentials of early Chordate ontogeny. In
many respects the later phases of its history are highly modi-
fied, but this need be no objection to its use as an introductory
type, since it may serve immediately to put the student upon
his guard against a too exact phylogenetic interpretation of
embryological facts.

Following this is a rather full account of the development
of the frog, a form that represents, better than any other single
type, what we may regard as the general type of Chordate
development. The chapters on the chick are relatively briefer
and emphasis is laid upon the embryonic membranes, and upon
the early phases of development, which represent the most
frequent modifications of the type of Chordate development,
modifications correlated with the presence of the large yolk
accumulation of the Sauropsid ovum.

It is believed that the chapters on the frog and chick have
been written in such a way that either form may be omitted,
in a brief course of study. Or in case the study of the early
development of the frog is desired as a comparative introduc-
tion to the study of the embryology of the chick, Chapter III,
on the organogeny of the frog, may be omitted without serious
interruption of the continuity of such a course.

The final chapter on the Mammal includes only those phases
of development that are of chief interest to the general student,
namely, the earlier stages in the formation of the embryo,
the establishment of its relation with the maternal organism,,
the development of the embryonic membranes and appendages,
and the development of the external form of the human embryo.

iii

M79841

iv PREFACE

Several authors and publishers have very kindly permitted
the use of illustrations or cliches from their works. Especial
acknowledgement is made to Professor F. R. Lillie for permis-
sion to use a considerable number of the illustrations in his
" Development of the Chick" (Henry Holt and Co.). I am
also indebted to Professor C. S. Minot and P. Blakiston's Son
and Co., for several cliches from their " Laboratory Text-book
of Embryology"; to Professor J. Playfair McMurrich and P.
Blakiston's Son and Co., for cliches from their " Development
of the Human Body"; to Messrs. Longmans Green and Co.,
for cliches from "Quain's Anatomy"; to Messrs. G. P. Putnam
and Co., for permission to redraw, with some modifications in
most instances, certain illustrations in Marshall's " Vertebrate
Embryology"; to Professor T. H. Morgan and The Macmillan
Company, for cliches from their Development" of the Frog's
Egg"; and to Herr Gustav Fischer and the respective authors,
for cliches from 0. Hertwig's "Handbuch der vergleichenden
und experimentellen Entwickelungslehre der Wirbeltiere" ; 0.
Hertwig's "Lehrbuch der Entwickelungsgeschichte des Men-
schen und der Wirbeltiere"; and H. E. Ziegler's "Lehrbuch
der vergleichenden Entwickelungsgeschichte der niederen
Wirbeltiere." In all cases the cuts thus borrowed are separately
acknowledged in the figure legends. I desire also to express
my debt to the authorities of the Johns Hopkins University,
for library facilities generously afforded.

W. E. K

July, 1913.

CONTENTS

CHAPTER I

PAGE
THE DEVELOPMENT OF AMPHIOXUS 1

CHAPTER II

THE EARLY DEVELOPMENT OF THE FROG 62

CHAPTER III '

THE LATER DEVELOPMENT OF THE FROG! ORGANOGENY 126

CHAPTER IV

THE EARLY DEVELOPMENT OF THE CHICK I THE EMBRYONIC MEMBRANES

AND APPENDAGES 229

CHAPTER V

THE LATER DEVELOPMENT OF THE CHICK! ORGANOGENY 301

CHAPTER VI

THE EARLY DEVELOPMENT OF THE MAMMAL. THE MAMMALIAN EMBRY-
ONIC MEMBRANES AND APPENDAGES 368

INDEX . . 455

OUTLINES OF
CHORD ATE DEVELOPMENT

CHAPTER I
THE DEVELOPMENT OF AMPHIOXUS

PAGE

INTRODUCTION . ..... 2

I. THE GERM CELLS AND THEIR PRODUCTION . . . . ... 4

II. THE EMBRYONIC PERIOD . »

A. FHOM FERTILIZATION TO THE TIME OF HATCHING ... 9

1. Fertilization 9

2. Cleavage 11

3. Gastrulation 15

4. The Formation of the Central Nervous System .... 20

5. The Formation of the Notochord 23

6. The Formation of the Mesoderm and Enter ocoels ... 24

B. FROM HATCHING TO THE FORMATION OF THE MOUTH . 27

1. The Central Nervous System 27

2. The Notochord 28

3. The Mesodermal Somites and Ccelom 29

4. The Enter on and Its Appendages 33

III. THE LARVAL PERIOD ....... . . ....."... 37

1. The Central Nervous System 37

2. The Gill Slits , . . . 39

3. The Club-shaped Gland 43

4. The Endostyle . . "j, '.'.... 43

5. The Mouth and Associated Structures 44

6. The Preoral Pit and Its Derivatives . 44

7. The Blood-vessels 46

8. The Atrium 46

9. Larval Asymmetry 49

10. The Mesodermal Somites 51

11. TheNephridia 53

12. The Larva at the Critical Stage . .......... 54

IV. THE ADOLESCENT PERIOD . . 55

1

2 OUTLINES OF CHORDATE DEVELOPMENT

"As an introduction to the study of embryology, and as an
indispensable aid to a reasonable appreciation of the value
of embryological facts, the life-history of Amphioxus
provides an object which ... is perhaps unrivalled.
It is alike useful in a text-book of human embryology, and
in one of invertebrate zoology." (Willey, "Amphioxus,"
etc., p. 104.)

MOKPHOLOGICALLY Amphioxus (Branchiostoma lanceolatum)
is recognized as one of the important types of Chordata, for it
illustrates in simple form the essential characteristics of this
large group, most of the members of which are extremely com-
plex. And in its mode of development, no less than in its struc-
ture, Amphioxus serves as a key to the more complicated con-
ditions of the Craniate groups. The anatomical and embryolog-
ical simplicity of this creature is commonly regarded as an
indication of true primitiveness, although the morphologist
recognizes, as the embryologist must also, that the simplicity
of primitiveness is here obscured, in many respects, by conditions
which are obviously special adaptations or secondary alterations
of primary arrangements.

Many of the simple embryological characteristics of this form
are correlated with the freedom of the egg from a large yolk-
mass. This is equivalent to saying that the accumulation of
yolk in the eggs of most Chordates is a secondary character, and
is, to a considerable extent, the cause of many of those modifica-
tions of the course of development which lead to unusual con-
ditions, proving difficult of comparison with other develop-
mental types.

The egg of Amphioxus is small, and the deutoplasm, small in
amount, is scattered through its substance. In correlation
with this, cleavage is total and quite regular in its course, leading
to the formation of fairly typical blastula and gastrula. The
organ-rudiments are all formed first as simple epithelial struc-
tures, whose origins and fates are easily followed, for each part
is sharply outlined and remains clearly demarcated through
the course of its development. The embryo is free swimming
and externally ciliated. In all these respects Amphioxus illus-
trates primitive Chordate characteristics. Most of the second-

THE DEVELOPMENT OF AMPHIOXUS '2

ary modifications of development appear comparatively late in
its course, and many of them are obviously correlated with
rather unusual habits and activities.

The embryological history of Amphioxus is described here,
then, not only because of the morphological importance of this
form, but because of its embryological primitiveness and the
diagrammatic simplicity of its early stages, which will aid in
understanding the complicated development of the other Chor-
dates described. Here we have Chordate development re-
duced to its simplest terms. A fair knowledge of the anatomy
of Amphioxus is presupposed.

The whole developmental history of Amphioxus falls quite
naturally into four general periods.

I. PRODUCTION OF THE GERM CELLS. — This includes the
formation of the germ cells, oo- and spermatogenesis, and
spawning.

II. EMBRYONIC PERIOD. — This extends from fertilization to
the opening of the mouth. This phase of development is very
rapid: at normal seasonal temperatures of the water it may
occupy only thirty-six hours. The entire period is con-
veniently subdivided into two.

A. Before Hatching. — This includes fertilization, cleavage,
gastrulation, and the first mapping out of the embryo. The
conclusion of this period is marked by escape from the egg
membranes — eight hours or more.

B. After Hatching. — Here the chief systems and organs of
the embryo become definitely laid down. The embryo is free
swimming (pelagic) — twenty-eight hours or more. The actual
duration of these and the other periods depends chiefly upon
temperature; it may be nearly doubled in the cooler waters of
an early season.

III. LARVAL PERIOD. — From the opening of the mouth to
the cessation of pelagic life and the assumption of a burrow-
ing habit. Here development is slower and consists largely in
the elaboration of the parts marked out during the preceding
period — about three months. At the conclusion of this period

A :4c;: fjQUT^Ip^S.OF-.CHORDATE DEVELOPMENT
: -\ : :•*: /: v .*: • • /• ". . :

the larva is about 3.5 mm. long and has reached a condition

known as the "critical stage."

IV. ADOLESCENT PERIOD. — From the critical stage to sexual
maturity. This is marked by histological differentiation and
the gradual appearance of adult characteristics. Germ cells
are first brought to maturity in specimens about 2 cm. in length,
the age of which is doubtful. Growth to full size probably in-
volves several years and covers several spawning periods.

I. THE GERM CELLS AND THEIR PRODUCTION

We may first describe the germ cells as they are extruded
from the body.

The eggs of Amphioxus are spherical and only 0.10 to 0.13
mm. in diameter. Among the Chordates smaller eggs than
these are found only in some Mammals. The egg (Fig. 1) is
surrounded by two membranes, a thin outer, or vitelline mem-
brane, which at this time is usually separated by a space
from the surface of the egg, and a thick inner, or perivitelline
membrane, which at the time of laying is more or less fluid
and closely adherent to the surface of the egg. The egg is
richly supplied with deutoplasm in the form of very numerous
small granules. These are not uniformly distributed through
the cytoplasm for there are two definite regions comparatively
free from deutoplasm, namely, a narrow superficial layer, and an
irregular conical region toward one side of the egg. Strictly
speaking the egg of Amphioxus is thus telolecithal, but the deu-
toplasmic center is riot toward the vegetal pole of the egg but
toward one side, below the equator. The precise location of this
yolk-free area is important for it establishes in the egg a definite
bilateral symmetry which is also that of the future embryo.
The animal pole is marked by the apex of this clear area and by
the point at which the first polar body is given off. The first
polar body has already been formed at the time the egg is laid,
but since it lies outside the vitelline membrane it is ordinarily
lost. At this time the animal pole is marked, however, by
the position of the egg nucleus which is just in the equatorial

THE DEVELOPMENT OF AMPHIOXUS 5

plate of the second polar division. The arched base of the clear
protoplasmic region lies about at the level of the equator, and
the whole space lies eccentrically toward that side of the egg
which, from later development, is known to be anterior or

II

FIG. 1. — The egg of Amphioxus. C, after Cerfontaine, others after Sobotta.
A. Ovarian egg showing cortical plasm. B. Cortical layer forming a membrane
on the suface of the egg, within the vitelline membrane. C. Egg membrane
fully formed but still attached to surface of egg, D. Extruded, fertilized egg.
Membrane fully formed and beginning to leave the egg. c, Cortical layer; e,
endoplasm; m, egg membrane, externally vitelline, internally a product of the
exoplasm; p, perivitelline space; s, spermatozoon; v, vitelline membrane; /,
first polar body; //, second polar spindle.

antero-dorsal. A diagram of a sagittal section of the egg is
shown in Fig. 2, in the position usually assumed by the egg in
the water.

The spermatozoa are very small (15-20 micra in length); the

6

OUTLINES OF CHORDATE DEVELOPMENT

rather spherical head is about 1 micron in diameter — about the
size of a deutoplasm granule.

The gonads are metameric organs distributed through the
middle and posterior pharyngeal region. There are about
twenty-six pairs (twenty-three to twenty-eight), approximately
in segments ten to thirty-six. They first begin to develop in the
embryo before the mouth is opened, and apparently first come to
maturity when the organisms are 2 to 2.5 cm. in length. The
discharge of the germinal products involves the nearly complete
loss of the gonads as such, so that after each annual spawning
period they redevelop from small rudiments. Details of the

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FIG. 2. — Diagram of a median sagittal section through the fertilized egg of
Amphioxus at the stage of the fusion of the egg and sperm pronuclei. After
Cerfontaine. The arrow marks the direction of the chief or polar axis. AD,
Antero-dorsal region; n, egg and sperm pronuclei; p, region relatively free from
deutoplasm; PV, postero-ventral region; s, remains of tail of spermatozoon;
y, yolk or deutoplasmic bodies; II, second polar body.

development of the gonads will be described later. The par-
tially grown ovary, which the testis resembles in essentials, is a
large spheroid mass, projecting from the postero-ventral margin
of the segment into the atrium, covered of course by atrial
epithelium. Fig. 3 represents in diagrammatic form a section
through the half grown ovary in the so-called medusoid or
mushroom stage. An abundant vascular supply is derived

THE DEVELOPMENT OF AMPHIOXUS

from branches of the posterior cardinal veins, which divide the
germinal epithelium into dorsal and ventral portions. Inside
the gonad is a space known as the primary ovarian or peri-
gonadial cavity, in the outer wall of which the definitive germ
cells are developed. Out-
side the gonad, and sepa-
rating it from the atrial
epithelium and body wall
proper, is a secondary
ovarian cavity or gono-
coel. In the wall of the
gonocoel, just above and
below the stalk of attach-
ment through which the
blood-vessels pass, are
thickened patches in the
atrial wall of the gono-
ccel — the dorsal and ven-
tral cicatrices. During
the later stages of their
formation the germ cells
— oogonia or spermatogo-
nia, enlarge so consider- fe
ably as nearly to oblit- /
erate, by compression,
these cavities and even to
cause the gonads to en-
croach very considerably

vg

P9

upon the atrial cavity.
Toward the end of the

FIG. 3. — Diagram of a section through
the gonad of Amphioxus. After Cerfon
taine. 6, Peribranchial (atrial) epithelium;
c, cicatrix; /, true follicular epithelium; fe,
growth period the nucleus, external layer of follicular epithelium; 0,
, . , . , gonocoel; ge, germinal epithelium; o\, pri-

WniCIl Contains a large mary ovarian cavity; o2, secondary ovarian

nucleoluS, passes through C,avi*y; W 'Parietal layer of gonocoel; v car-

dinal vein; vg, visceral layer of gonoccel.

the synizesis stage and

the deutoplasm granules, whose formation began toward the
inner side of the oogonia when these were only about 0.05 mm.
in diameter, crowd the entire cell body except in the perinuclear

8 OUTLINES OF CHORDATE DEVELOPMENT

region and a narrow peripheral region which is occupied by
several rows of small clearer vacuoles. It is doubtful whether
there is a true cellular egg follicle: a thin layer of cells forming
the wall of the primary ovarian cavity forms an ovarian follicle
which folds in and covers almost completely the superficial
oogonia.

After the growth period is completed the process of maturation
commences while the oogonia are still within the ovary. The
chromatic nuclear membrane disappears and the whole nuclear
apparatus moves toward the atrial (i.e., attached) surface of
the cell, marking the animal pole and establishing visibly the
symmetry of the egg. As it reaches the surface a typical polar
spindle with asters forms, and the chromatin forms into twelve
tetrads, indicating 'a somatic chromosome number of twenty-
four. About this time the very thin vitelline membrane is
formed on the surface from the substance of the egg proper
(Fig. 1), and as the first polar body is cut off it pushes this before
it, so that a portion of the membrane is cut off with the polar
body which may no longer remain attached to the egg. Imme-
diately after the first polar body is given off the second polar
spindle forms, but the division halts in the mesophase (Fig. 1).
Just before or during the formation of the first polar body the
inner wall of the secondary ovarian cavity is ruptured by con-
traction of the body wall and of muscle fibers in the thin walls of
the gonoco3l, and the eggs are partly forced into the gonocoel.
All of these processes occur as the animals emerge from the sand
and swim about preparatory to spawning.

Spawning extends through the greater part of spring and sum-
mer in the warmer waters, and always occurs at a definite time
of day — about sundown, or from five to seven in the evening.
Strong contractions of the general body musculature rupture
the cicatrices and force the eggs from the gonocoel into the atrial
cavity, and thence they are carried by bodily contractions and
the respiratory current out through the atriopore into the free
sea water.

Contact with the sea water brings about the formation of a
thick mucilaginous second or inner membrane over the surface

THE DEVELOPMENT OF AMPHIOXUS 9

of the egg. The substance of this, the perivitelline membrane,
seems to be derived from the material of the peripheral layers
of vacuoles in the cytoplasm; these flow together forming a
homogeneous superficial layer quite distinct from the underlying
protoplasm (Fig. 1). The membrane is at first rather fluid
but in contact with the water it soon begins to toughen.
In this condition the eggs are ready for fertilization. The
formation of the spermatozoa is not so fully known but it seems
to occur in a manner parallel to the formation of the ova.

II. THE EMBRYONIC PERIOD

A. FROM FERTILIZATION TO THE TIME OF HATCHING
1. Fertilization

Eggs and sperm are discharged into the water at about the
same time and immediately each egg becomes surrounded by a
crowd of the spermatozoa. The perivitelline membrane has
been formed first in the region of the animal pole and at this
time is gradually extending thence toward the vegetal pole.
In this region then it remains longest in a more fluid condition
and it is at this vegetal pole that the sperm usually gain
entrance to the egg, after having penetrated first the thin
vitelline membrane and traversed the perivitelline space. No
micropyle has been discovered and polyspermy seems to be
very frequent. It is not surely known whether the entire
sperm or only the head usually enters the egg substance.
Immediately after the entrance of a spermatozoon the entire
perivitelline membrane is formed, toughens, leaves the surface
of the egg, and comes into contact with or even partially fuses
with the vitelline membrane (Fig. 1, D) obliterating the original
perivitelline space but leaving a wide secondary perivitelline
space between itself and the egg.

Entrance of the sperm affords also the stimulus to the
completion of maturation of the egg nucleus, which at this
time is still in the mesophase of the second polar division.
While the sperm, lying just inside the egg, is reconstituting a

10 OUTLINES OF CHORDATE DEVELOPMENT

normal nucleus together with sperm centrosome and aster, the
second polar body is formed and the mature egg nucleus
established. The second polar body forms about fifteen
minutes after entrance of the sperm. The division of the
sperm centrosome and aster, the approach and fusion of the
egg and sperm nuclei, and the constitution of the first cleavage
nucleus, are in no way unusual (Fig. 4).

The first cleavage spindle takes up a position definitely
related to the symmetry of the egg, lying horizontally, slightly

FIG. 4. — Prophase of first cleavage figure in Amphioxus. After Sobotta.
Inner and outer membranes fused and separated from the egg by a wide space
called the perivitelline space.

nearer the animal pole, and at right angles to the median plane.
The relation of this symmetry of the egg to that of the future
embryo is shown in Figs. 2 and 7, A. The median plane of
symmetry is determined by the points of polar body formation
and sperm entrance, and the eccentric position of the clear
protoplasmic region. This last is displaced toward the antero-
dorsal region of the future embryo: one result of this is the

THE DEVELOPMENT OF AMPHIOXUS 11

greater freedom from yolk of this region of the embryo, and
this has an important bearing upon subsequent development.
The egg axis is at an angle of roughly 30° to the antero-posterior
axis of the embryo : that is, the animal pole of the egg becomes
ant ero- ventral, the vegetal pole postero-dorsal. It is quite
probable that this bilateral symmetry, and certain that the
polarity of the egg, is determined while it is still within the
ovary; it gains visible expression through the assumption of a
peripheral position by the primary oocyte nucleus and the
eccentricity of the accompanying clear protoplasmic region.
The egg of Amphioxus seems to resemble that of the Echinoderm
rather than those of most other forms, in that the direction of
this eccentricity of the nucleus, i.e., animal pole, is toward the
region of attachment in the ovarian epithelium.

2. Cleavage

The cleavage of Amphioxus is total and unequal and,
though subject to much variation, it is in many eggs quite
regular. It is generally believed that the Amphioxus type of
cleavage is primitive among Chordates; and that the cleavage
modes of Craniates are to be derived from it, the chief cause of
modification being the accumulation of yolk. The first division
of the egg occurs about an hour after entrance of the sperm,
the second about an hour after the first, and subsequent
divisions about every fifteen or twenty minutes. The plane
of the first cleavage as indicated by the position of the first
cleavage spindle, is median (cleavage furrow meridional),
dividing the egg into exactly similar right and left halves,
which become the right and left halves of the embryo. The
second cleavage furrow is also meridional and the plane at
right angles to the first. Cleavage becomes unequal with this
division for the two cells are divided into two smaller antero-
dorsal, and two larger post ero- ventral cells, symmetrically
arranged on each side of the median plane (Fig. 5, A).

The third cleavage is at right angles to the first two and the
furrow equatorial, or rather latitudinal for again the division

12 OUTLINES OF CHORDATE DEVELOPMENT

is slightly unequal and each of the four cells forms a smallei
cell toward the animal pole, and a larger toward the vegetal.

FIG. 5. — Cleavage in Amphioxus. After Cerfontaine. A. Four-cell stage
viewed from animal pole. The two antero-dorsal cells are the smaller. B.
Eight-cell stage viewed from animal pole showing the four sizes of the cells. C.
Sixteen cells viewed from the left side. D. Thirty-two* cells viewed from vegetal
pole. E. Thirty- two passing into sixty-four cells, viewed from the antero-
dorsal region. F. Optical section of right half of young blastula. About 128
cells, a, Animal pole; ad, antero-dorsal; /, left; pv, postero-ventral ; r, right; v,
vegetal pole.

Thus in the eight-cell stage (Fig. 5, B) we have four pairs of
cells of four sizes; the four micromeres of the animal pole

THE DEVELOPMENT OF AMPHIOXUS 13

consist of two smaller anterior, and two larger ventral cells,
and the four macromeres of the vegetal pole, of two smaller
dorsal, and two larger posterior cells, the smaller macromeres
being larger than the larger micromeres. These relative in-
equalities in the quadrants, as well as their bilateral symme-
try, continue throughout cleavage.

Strict synchronism of cleavage is lost in passing from four to
eight cells, the smaller cells commencing their division before
the larger. In the early stages the intervals between successive
cleavages are such that, in spite of lack of synchronism, it is
still possible to speak of sixteen- and thirty-two-cell stages,
but after this the numerical progression is no longer regular.

Were the cleavage strictly regular the eight cells would
form sixteen by meridional cleavages passing symmetrically
through the entire egg, but as a matter of fact, during their
formation the spindles of the eight blastomeres change their
position so that the cleavage planes of the micromeres are
nearly perpendicular to the median plane, while those of the
macromeres are rather parallel with this plane. As a result
the sixteen-cell stage (Fig. 5, C) consists of eight micromeres
arranged in two rows of four cells each, parallel with the median
plane and becoming arched in the same direction, and of
eight macromeres in two rows of four cells each extending
across the median plane, i.e., from right to left, and arched in
this direction. The relation between the groups of micro- and
macromeres is much like that of the two hands when partly
closed and one in the palm of the other. The thirty-two-
cell stage (Fig. 5, D) is formed by the horizontal (latitudinal)
divisions of each of the sixteen, forming eight meridional rows
of four cells each. After thirty-two cells (Fig. 5, E) the
divisions become irregular in their appearance. To sum-
marize:

Cleavage 1st 2nd 3rd 4th 5th

!4 mi r ' 2 Sma11 = 4 Sma11 = 8 Cells

\2 large = 4 large = 8 cells

f2 small = 4 small = 8 cells

[4macr- 12 large = 4 large = 8 cells

Total number of cells 24 8 16 32

14 OUTLINES OF CHORDATE DEVELOPMENT

This typical arrangement of cleavage planes is by no
means invariable. Variations are indeed very frequent but
the cells are usually arranged according to definite plans. In
many cases the cleavage pattern is nearly radial, and in others
the blastomeres may shift more or less giving the appearance
of a spiral cleavage. In some eggs the micromeres of the
sixteen-cell stage may not all divide similarly but four may
divide vertically and four horizontally. These variations in
cleavage do not affect subsequent processes.

As a consequence of the early blastomeres remaining well
rounded a central space is formed among them. Virtually
present in the four-cell stage, this space becomes real at eight
cells, and as the cells multiply and gradually lose their rounded
form they push away from the center of the mass leaving a
definite space within, at first open at the poles (cleavage pores).
This is the beginning of the segmentation cavity or blastocoel.
By the time thirty-two cells are formed the poles close over
and soon the blastoccel is entirely closed. From about sixty-
four cells on (Fig. 5, E, F) the blastomeres lose their rounded
outline and become flattened and closely packed in a simple
epithelial layer. This arrangement of the blastomeres may be
taken as the beginning of the blastula stage, which may be
considered fully established when the number of cells reaches
one hundred and twenty-eight. The hollow spherical blastula
of this type (Fig. 5, F) is called a cceloblastula, and it is com-
monly regarded as the most primitive type of blastula. In
Amphioxus this is bilaterally symmetrical and the epithelial
wall is of varying thickness on account of the varying sizes of
the cells. The cells are relatively free from deutoplasm, and
therefore smaller, in the anterior region, richer in deutoplasm,
and therefore larger, in the posterior region, and uniformly
graded in size and deutoplasmic content between these regions.
The animal pole remains antero-ventral (Fig. 7, B). The
blastocoel is very large and, on account of the varying thickness
of its wall, may be said to be slightly eccentric toward the
anterior side.

THE DEVELOPMENT OF AMPHIOXUS 15

3. Gastrulation

By the time about two hundred and fifty-six cells have been
formed in the blastula, or about four hours after fertilization,
the process of gastrulation is commenced, by which the single
walled blastula is to be converted into a double walled gastrula.
We should notice in advance that the gastrula of Amphioxus
is formed by the three processes of inwufination, involution, and
epiboly, and so is not typical of Chordates generally, in which
the double walled or two layered condition results more
extensively from delamination, that is, by tangential divisions
in the wall of the blastula, together with some involution and
epiboly.

The first indication of gastrulation is the flattening of the
vegetal pole of the blastula (Fig. 6, A), which is soon followed
by the appearance of a slight infold on the antero-dorsal
aspect, at about the level of the equator (Fig. 6, B). This
infolding or invagination soon extends around the sides of the
blastula, and finally the whole flattened vegetal or postero-
dorsal region becomes folded down into the segmentation
cavity (Fig. 6, C). The process of infolding continues in a
more advanced stage in the antero-dorsal region where it com-
menced, and here the folded layer first comes into contact with
the inner surface of the cells of the animal pole so as to obliterate
the blastocoel there, at a time when this remains quite widely
open elsewhere. We may now speak of the invaginating and
non-invaginating layers as endoderm (hypoblast) and ectoderm
(epiblast) respectively, and of the whole structure as the
gastrula (Fig. 6, E). While the infolding of the endoderm
leads to the obliteration of the blastocoel, it leads to the forma-
tion of another cavity which is lined completely with cells of
one kind — endoderm. This cavity, which can be recognized
as beginning with the earliest infolding of the blastula wall, is
the archenteron or primitive gut cavity, which is to give rise to
the chief cavities of the later embryo. In many Chordates
this cavity is virtual rather than real on account of being
filled with yolk-cells. The gastrula of Amphioxus is often

16 OUTLINES OF CHORDATE DEVELOPMENT

FIG. 6. — Gastrulation in Amphioxus. After Cerfontaine. A. Blastul a show-
ing flattening of the vegetal pole and the rapid proliferation of cells in the postero-
dorsal region (germ ring). B. Flattening more pronounced; mitoses in cells of
germ ring. C. Commencement of the infolding (invagi nation) of the cells of
the vegetal pole. D. Continued infolding, and inflection, or involution, of
ectoderm cells in the dorsal lip of the blastopore. The blastoccel becoming
obliterated and the archenteron being established. E. Invagination complete.
Continued involution in the dorsal lip of blastopore. Mitoses in germ ring.
F. Constriction of blastopore and commencement of elongation of the gastrula.
Remnants of blastoccel in ventral lip of blastopore. G. Gastrulation completed.
Continued elongation, and narrowing of blastopore. H. Neurenteric canal
established by overgrowth of neural folds. Continued mitosis in germ ring.

THE DEVELOPMENT OF AMPHIOXUS

17

termed a ccelogastrula to indicate the fact that the archenteron
is an actual widely open cavity.

While cell multiplication continues in all parts of the embryo
during gastrulation, immediately after gastrulation begins, a
center of very rapid cell division appears just anterior to the
invaginating region on the dorsal side, and extending laterally
around the margin of the blastopore; on the ventral side of

FIG. 7. — Diagrams illustrating the relations between the adult axes and the
axes of the egg and early stages. After Cerfontaine. A. Fertilized egg. B.
Fully formed blastula. C. Gastrulation begun. D. Fully formed gastrula.
Note posterior elongation, a-p, Antero-posterior axis of adult; d, v, dorsal and
ventral surfaces of adult; x-y, chief egg axis (x, animal pole, y, vegetal pole).

the blastopore this region is less clearly marked, although
distinguishable. This band of rapidly proliferating cells is
to be identified as the germ ring, an embryonic region of greater
importance in the other Chordates. The increase of cells at
this point is so rapid that it disturbs, for a time, the simple

a, Animal pole; ar, archenteron; 6, blastoporal opening; ch, rudiment of noto-
chord; dl, dorsal lip of blastopore; ec, ectoderm; en, endoderm; gr, germ ring;
nc, neuenteric canal; nf, neural fold; np, neural plate; s, blastoccel or segmentation
cavity; v, vegetal pole; rl, ventral lip of blastopore; II, second polar body.

18 OUTLINES OF CHORDATE DEVELOPMENT

epithelial arrangement of the cell layers (Fig. 6, A) and com-
plicates somewhat the otherwise simple process of gastrulation.
The transitional region between ectoderm and endoderm is the
blastopore. The region of rapid cell multiplication, i.e., the
germ ring, is, therefore, described as located in the lip of the
blastopore, chiefly toward the dorsal side (Fig. 6, B-G).

After the cells within the dorsal lip of the blastopore have
partly folded in, the flattened plate of large endoderm cells of
the vegetal pole swings gradually inward without undergoing
much bending or arching, as if hinged at the lower lip of the
blastopore (Fig. 6, D). This process involves a much greater
extent of motion in the dorsal margin of this plate, and this is
made possible by the rapid multiplication of cells in the dorsal
margin of the blastopore, a sheet of which is left behind as the
endoderm cells swing inward. The obliteration of the blastocoel
continues gradually toward the ventral margin of the blasto-
pore, and though finally completed, for a long time a trace of
the cavity may be seen in the ventral lip. Occasionally the
entire blastocoel may be obliterated completely in a very early
stage but this is not a typical condition.

From this description of invagination it is evident that the
endodermal or inner layer cells are really of two kinds, first, the
large deutoplasmic cells of the vegetal pole of the blastula
forming the ventral region of the endoderm, and second, the
smaller cells from the dorsal region of the transitional zone
between the animal and vegetal poles of the blastula, which
come first to lie in the dorsal lip of the blastopore, and then by
rapid multiplication bud off a sheet of cells forming in general
the dorsal region of the endoderm. This group of more active
cells really lies just outside the margin of the blastopore so
that the cells contributed by it to the endoderm are really
turned in or inflected after their formation and a very brief
existence as ectodermal cells (Fig. 6, D, E). This inflection
(involution) of the marginal cells is of importance in comparing
the gastrula of Amphioxus with that of other forms.

But the cells formed by divisions in the dorsal blastoporal
lip (germ ring) are by no means all added to the endoderm layer.

THE DEVELOPMENT OF AMPHIOXUS 19

They contribute also to the ectoderm, and thus cause a steady
extension of the dorsal lip posteriorly; that is, gastrulation is
accomplished in part by epiboly, or the growth and extension
backward of part of the blastoporal region. So that while at
first the invaginated blastula is only little more than hemi-
spherical in form, it soon begins to elongate, and this elonga-
tion extends chiefly posteriorly and is accomplished mainly
by the rapid posterior elongation of the dorsal margin of the
blastopore (Fig. 6, F-H).

When the invaginating phase of gastrulation is completed
(Fig. 6, E) the archenteron has a nearly hemispherical form and
is widely open in the dorsal or postero-dorsal direction. In
Amphioxus the margin of the archenteric opening coincides with
the blastopore, though we have seen that in general the blasto-
pore should be regarded as that region where the ectoderm and
endoderm are continuous, whether this borders an opening or
not. As the dorsal margin of the blastopore extends backward
the diameter of its opening decreases, that is, the archenteron
becomes a more nearly enclosed cavity, considerably elongated
posteriorly. As the blastopore closes gradually the direction of
its opening becomes less dorsal and more posterior (Fig. 6, F, G).
Toward the end of gastrulation the sides as well as the dorsal
region of the blastoporal margin grow backward, and finally the
ventral region shares in the process so that the last stages in the
narrowing of the blastopore are accomplished by epiboly on
every side. The result of this is the formation in the endoderm,
just within the blastopore, of a band of cells, narrow below and
widening laterally, which have been formed differently from the
remainder of the ventral and lateral endoderm, and like the
endoderm forming dorsally. This has an important bearing
upon the development of later structures.

At the close of gastrulation the embryo has the form shown in
Fig. 6, G. The gastrula is bilaterally symmetrical, quite elon-
gated antero- posteriorly, flattened dorsally, rounded ventrally as
well as anteriorly, while at the postero-dorsal aspect the archen-
teron opens directly to the outside by a narrow blastoporal
aperture. The ectoderm forms a fairly uniform layer of super-

20 OUTLINES OF CHORDATE DEVELOPMENT

ficial cells, and during gastrulation these have developed motile-
cilia, almost flagelliform, so that the gastrula is slowly rotated
within the egg membranes which still envelop it. The endo-
derm cells lining the archenteron are somewhat unlike and of
three distinct kinds, according to their origin. First there are
the deutoplasmic cells, which are the descendants of the original
vegetal pole cells of the blastula, forming the greater part of the
floor of the archenteron; second, cells derived from the dorsal
margin of the blastopore which have been added to the endo-
derm through epiboly and inflection, forming a band along the
roof of the archenteron; and third, around the blastopore, a
rim of cells narrow ventrally but wider dorsally, formed also
through epiboly and inflection, from the ventral and lateral
margins of the blastopore. Thus the gastrula of Amphioxus,
although superficially resembling the simple type of invaginate
gastrula, such as that of many Coelenterates, in reality is not like
that, for here epiboly plays an important part in its formation.
This is a leading characteristic of the gastrulas of the Chordates
in general, and it is important to recognize in Amphioxus this
method of gastrulation in its simplest and probably most
primitive form. If one but imagines that in Fig. 6, F, the
endoderm cells derived from the vegetal pole are multiplied and
filled with a great mass of yolk, the result will be not widely
unlike Fig. 32, E, of a section through the gastrula of the frog.
Development up to this stage has been so rapid that the com-
pletion of gastrulation occurs only six to seven hours after ferti-
lization. During the brief period between this stage and the
escape of the embryo from the egg membranes, elongation
continues slowly, chiefly through the rapid multiplication of
cells in a sort of " growth zone" around the blastopore. And
before the close of this period certain important structures are
marked out: these are, the central nervous system, the noto-
chord, and the mesoderm and ccelom.

4. The Formation of the Central Nervous System

Along the dorsal flattened surface of the gastrula a median
strip of ectoderm cells becomes delimited from the adjacent cells

THE DEVELOPMENT OF AMPHIOXUS 21

np nf

D

FIG. 8. — Transverse sections through young embryos of Amphioxus, show-
ing formation of nerve cord, notochord, and mesoderm. After Cerfontaine.
A. Commencement of the growth of the superficial ectoderm (neural folds)
above the neural plate (medullary plate). B. Continued growth of the ecto-
derm over the neural plate. Differentiation of the notochord, and first indica-
tibns of mesoderm and enteroccelic cavities. C. Section through middle of
larva with two somites. Neural plate folding into a tube. D. Section through
first pair of mesodermal somites, now completely constricted off. E. Section
through middle of larva with nine pairs of somites. Neural plate folded into a
tube. Notochord completely separated. In the inner cells of the somites,
muscle fibrillse are forming (compare Fig. 10). ar, archenteron; c, enteroccel;
ch, notochord; ec, ectoderm; en, endoderm;/, muscle fibrillae; g, gut cavity; m,
unsegmented mesoderm fold; ms, mesodermal somite: nc, neuroccel; nf, neural
i'old; np; neural plate; nt, neural tube.

22 OUTLINES OF CHORD ATE DEVELOPMENT

and sinks slightly below the level of the general ectoderm (Fig.
8, A). This strip of cells is* the neural plate or medullary plate.
It extends from near the anterior (dorsal) margin of the blasto-
pore forward, almost to the extremity of the embryo, and back-
ward a short distance each side of and partially surrounding
the blastoporal opening. The ectoderm bordering the lateral
margins of the depressed area becomes slightly elevated, forming
the neural ridges or neural folds, and these gradually flow over
the margins of the neural plate as this becomes still farther
de pressed (Fig. 8, B). Posteriorly the neural folds extend along
the sides of the blastopore, and even posteriorly and ventrally
to it, completely surrounding it. The neural folds then rapidly
approach medially and soon they cover over the neural plate,
though separated from it by a shallow space (Fig. 8, C). These
processes of depression and roofing over do not occur at once
throughout the whole dorsal surface. The depression of the
neural plate commences just in front of the blastopore and pro-
ceeds thence anteriorly, while the neural folds appear first
somewhat further in front of the blastopore and usually,
although not invariably, fuse over the neural plate first in the
same region.

Posteriorly the neural folds arising from the lateral and
ventral margins of the blastopore, in fusing roof over this
structure without closing it, so that the blastopore no longer
opens directly to the outside but into the narrow space between
the neural plate and the superficial ectoderm layer formed by
the fused neural folds (Fig. 6, H) . In front of the point where
the folds first meet, this space remains widely open upon the
surface of the embryo. This opening to the cut-side is called
the neuropore, and as the fusion of the neural folds extends
rapidly forward the neuropore is carried along toward the
anterior end (Fig. 9, A). By the time of hatching it may be
found at almost any point between the middle of the embryo
and the anterior margin of the first somite (see below). In
this latter region the neuropore remains as a definite opening
until the middle of the larval period. There is some variation
in different embryos as regards the region of the first fusion of

THE DEVELOPMENT OF AMPHIOXUS 23

the neural folds. In some individuals, and these have usually,
and erroneously, been described as the more typical, the folds
meet first over the blastopore and gradually fuse thence ante-
riorly. The more frequent relation seems to be that just
described, and it is important to recognize that this agrees
with the method of closure of the neural folds in practically
all of the Craniates, where they meet and fuse first in the
middle or anterior to the middle of the embryo, and then fuse
in each direction from that region. Amphioxus differs, how-
ever, from all other Chordates in that the margins of the neural
plate do not remain connected with the neural folds for a time,
and are not elevated and closed into a tube at the same time
the neural folds close together: the folding of the neural
plate into a tube will be described presently.

5. The Formation of the Notochord

The chorda develops more slowly than the nervous system
and by the time of hatching has hardly more than commenced
its formation. The rudiment of the notochord is a median
strip of endoderm, six to nine cells wide, forming the roof of the
archenteron and lying consequently just beneath the neural
plate and in contact with its lower surface (Fig. 8, B). The
depression of the neural plate depresses also the flattened
dorsal wall of the archenteron, so that the chorda rudiment
pushes down into the archenteric cavity and appears in section
concavely arched. The chorda cells are those inflected at
the dorsal margin of the' blastopore together with their descend-
ants. While the gastrula or embryo is elongating the rudiment
of the notochord divides posteriorly, passing a short distance
around each side of the blastopore, and terminates in a growth
zone similar to that concerned in the extension of the neural
plate but lying just inside instead of outside the blastoporal
rim (Fig. 9, B). At the time of hatching the rudiment of the
chorda still remains as a flat plate of cells directly continuous,
laterally and anteriorly, with the endoderm lining the remainder
of the archenteron.

24 OUTLINES OF CHORDATE DEVELOPMENT

6. The Formation of Mesoderm and Enter occels

In the gastrula the rudiments of the middle germ layer are
found in a pair of longitudinal mesoderm bands of cells lying
either side of the chorda in the dorso-lateral regions of the
endodermal archenteric wall. Posteriorly these bands diverge
and pass either side of the blastoporal opening nearly or quite
to its ventral side. The extent of the mesoderm, as of the
neural plate and notochord, is increased chiefly by the addition
of cells from this blastoporal region (germ ring). At the close
of gastrulation therefore we can distinguish two general regions
of mesoderm; first, that lying either side of the anterior part
of the chorda, formed from the inflected dorso-lateral margins
of the blastopore and known as gastral mesoderm, and second,
that formed from the lateral and ventro-lateral margins of the
blastopore, known as peristomial mesoderm. The gastral
mesoderm is the earlier formed and remains limited to the
anterior region, while the peristomial mesoderm forms later
and during a long period after gastrulation is completed, and
really constitutes all the mesoderm posterior to the very
limited, and anterior gastral mesoderm. At the close of
gastrulation the only difference between the two kinds of
mesoderm is that of time and place of origin for they are directly
continuous and not visibly differentiated from one another.

The depression of the notochordal plate, consequent upon
the formation of the nerve cord, results in a rather sharp
folding longitudinally of the dorso-lateral mesoderm bands,
and the formation from the archenteric cavity there of a pair
of longitudinal grooves (Fig. 8, B). These grooves are the
first indications of the enteroccelic cavities and their walls are
to be spoken of as the mesoderm folds. The enteroccelic
grooves extend nearly the entire length of the archenteron
and, though at first shallow, rapidly deepen, particularly in the
anterior region. The mesoderm folds soon become sharply
differentiated from the adjoining chorda and endoderm (Fig.
8, (7), and very early their continuity becomes interrupted by
the appearance of paired transverse folds dropping down from

THE DEVELOPMENT OF AMPHIOXUS

25

their dorsal walls. The first pair of the transverse folds
appears a short distance back from the anterior ends of the

n ch

eg co

np cv

rd

Id

C9 gs

spc

FIG. 9. — Optical sections of young embryos of Amphioxus. After Hatschek.
The cilia are omitted. A. Two-somite stage, approximately at the time of
hatching, showing relation of neuropore and neurenteric canal. B. Nine-
somite stage, showing origin of anterior gut diverticula. C. Fifteen-somite
stage. End of the embryonic period, ap, Anterior process of first somite ; c,
neurenteric canal; ch, notochord (or its rudiment, in A); eg, club-shaped gland
(or its rudiment, in J5); ego, external opening of club-shaped gland; co, ccelomic
cavity of somite; cv, cerebral vesicle; g, gut cavity (enteron, mesenteron); firs,
rudiment of first gill slit; i, intestine; Id, left anterior gut diverticulum (preoral
pit in C) ; m, mouth; mes, unsegmented mesoderm; n, nerve cord (or its rudiment,
in A); np, neuropore; p, pigment spot in nerve cord; rd, right anterior gut diver-
ticulum (preoral head cavity in C); si, sz, first and second mesodermal somites;
spc, splanchnoccel (body cavity).

mesoderm folds and soon cuts off this region, forming thus
the first pair of mesodermal somites, as they are called. The

26 OUTLINES OF CHORDATE DEVELOPMENT

somites are at first nearly spherical or cubical, box-like divi-
sions, each containing a portion of the -original archenteric
space now to be known as the enterocoelic cavity of the somite
or enterocod, which in these early stages remains in direct
though narrowed continuity with the archenteron; later this
connection becomes entirely lost (Fig. 8, D). This transverse
cutting up of the continuous mesoderm folds and their cavities
into somites and enteroccels proceeds, in somewhat modified
form, from the anterior region posteriorly, as the embryo
elongates, and by the time of hatching two pairs of somites
have been constricted off (Fig. 9, A). The gastral mesoderm
is approximately limited to the region of these first two pairs
of somites, all of the posterior remainder forming from peri-
stomial mesoderm.

As compared with the higher Chordates the formation of
the somites in Amphioxus begins very early, for in those forms
the mesoderm first separates from the endoderm as a pair of
longitudinal bands which later and only in part become divided
into segments or somites. The formation of the somites here,
as actual enterocoelic diverticula from the archenteron, has
been considered of great theoretic importance on account
of its supposed primitiveness, for in all of the Craniates the
mesoderm bands are at first solid and later develop a cavity
never directly continuous with the archenteron. It is quite
possible, however, that the formation of solid peristomial
mesoderm bands is the primary arrangement and that the
connection between the mesoderm cavity and the archenteron,
which we shall see is limited to the somites of gastral meso-
derm, is in reality a secondary condition.

The first phase of embryonic development is terminated
about eight to fifteen hours after fertilization by the escape
of the embryo from the egg membranes, within which it has
been enclosed. During the remainder of the embryonic period
it swims freely near the surface by means of the covering of
long ectodermal cilia. We may conveniently summarize the
characters of the embryo at the time of hatching as follows
(Fig. 9, A). The embryo is in general cylindrical with a flat-

THE DEVELOPMENT OF AMPHIOXUS 27

tened dorsal surface; length nearly twice the diameter, and the
diameter about equal to that of the egg. External surface
completely ciliated. Blastopore completely roofed, so that
the only external opening is the neuropore, opposite the
anterior margin of the first somite. Mesoderm folds are
formed throughout and two pah's of somites are constricted off
anteriorly. Notochord delimited but not developed. Archen-
teron open to the outside only by way of the roofed over
blastopore, through the space between neural plate and super-
ficial ectoderm, to neuropore. All organs and parts are still
formed of a single layer of epithelially arranged cells.

During the remaining twenty-eight to sixty hours of the
embryonic period the chief developmental processes consist
in the elaboration of the rudiments already established rather
than the mapping out of new organs.

B. THE EMBRYONIC PERIOD, FROM HATCHING TO THE FORMA-
TION OF THE MOUTH

1. The Central Nervous System

If not already accomplished, the neural plate is now rapidly
roofed over and the neuropore is carried to the anterior margin
of the first somite, where it remains throughout the larval
period. Next the neural plate is converted into a tubular
structure, the neural tube, through the depression of its me-
dian region and the accompanying rolling up and together
of its margins (Fig. 8). As in other Chordates this process
begins in the region of the first somite and extends thence
posteriorly and anteriorly. The original space between the
neural plate and the covering ectoderm becomes the cavity
of the neural tube or neurocoel (Fig. 9, B). The cilia of these
originally superficial cells now line the neurocoel and continue
to beat toward the posterior end of the tube. In the region of
the blastopore the neural plate remains in connection with the
continuous ectoderm and endoderm of that region, so that the
neurocoel does not close posteriorly, but leads directly into
the opening of the blastopore and so to the archenteron. This

28 OUTLINES OF CHORDATE DEVELOPMENT

passage from the neurocoel to the archenteric cavity by way of
the blastoporal opening, is the neurenteric canal. This canal
remains open throughout the embryonic period, until after
the mouth opening is formed, so that this, in connection with
the neurocoel and neuropore, forms the Only path by which the
archenteron is in connection with the exterior (Fig. 9, A, B, C).
The beating of the cilia lining the neurocoel probably keeps
up an interchange of fluids between enteron and the outside.

Opposite the anterior margin of the first somite the medullary
tube is somewhat enlarged (Fig. 9, (7), while opposite its
posterior margin, and, indeed, throughout the remainder of
the tube, it becomes somewhat narrowed by the elongation
of that part of the embryo, and a so-called brain region is
thus marked out. About the close of this period, pigment
spots begin to appear in the neural tube opposite the fifth
pair of somites (Fig. 9, C) : these are the first indications of the
development of sense organs and are doubtless photo-receptors.
The large cranial pigment spot in the anterior wall of the brain
appears about the close of the embryonic period.

2. The Notochord

The establishment of the chorda from the plate of endoderm
cells lying between the mesoderm folds, commences in. the
region between the first and second somites (Fig. 8). Here
the plate becomes arched, its lateral halves folding together
ventrally. The folding extends posteriorly and anteriorly
from this region, and soon the folded plate is formed into a
solid strand lying below the neural tube, between the meso-
dermal somites (Fig. 8, E). Posteriorly the chorda extends
to the anterior wall of the neurenteric canal, and anteriorly
it slowly forms to the very extremity of the embryo, and
therefore in advance of the somites and neural tube (Fig. 9,
B, C). The extension of the chorda in front of the brain is a
peculiarity of Amphioxus, for in all other Chordates it forms
only to the region of the mid-brain. The chorda cells from
the two sides grow across the mid-line, interlocking and later

THE DEVELOPMENT OF AMPHIOXUS 29

extending from each side completely across the entire chorda.
By the time nine or ten somites are formed the notochord
becomes completely cut off from the endoderm layer, and the
two margins of the endoderm which were originally along the
outer margins of the mesoderm folds, come together in the
mid-line beneath the notochord, enclosing what remains of
the archenteron, as the definitive gut cavity or enteron (mesen-
teron) (Fig. 8, E). Finally vacuoles appear in the notochord
and, increasing in size, lead to the obliteration of the cellular
structure. The nuclei are displaced dorsally and ventrally
and a typical "notochordal tissue" is formed before the close
of the embryonic period (Fig. 9, C).

3. The Mesodermal Somites and Ccelom

After hatching, mesodermal somites posterior to the two then
present continue to form successively in the elongating meso-
derm folds. The cavities of the first two pairs do not become
completely separated from the archenteron until six to eight
pairs have been formed and constricted off, and their enteroccels
remain as definite spaces throughout their development. In
the somites just posterior to the first two pairs the enteroccels
close for a time just after the somites are formed, and in the
more posterior ones, even before the mesoderm is quite cut off
from the endoderm. In these somites cavities reappear later,
and the enterocoels may be said to be virtually if not actually
present throughout, for the cells composing their walls remain
definitely arranged about a central point in the regions of the
enteroccels (Fig. 10). Still farther posteriorly the mesoderm
folds develop as solid masses without any cavities whatever at
any time during their formation, but the condition in the ante-
rior region demonstrates that Amphioxus is a true enteroccelo-
mate organism. By the time fourteen pairs of somites have
been formed the mesoderm folds cut off completely from the
archenteric wall, and the remainder of the mesoderm is formed
directly from the proliferating cell region around the neurenteric
canal (blastopore), without ever having been included as a part

30 OUTLINES OF CHORDATE DEVELOPMENT

of the endodermal wall of the archenteron. At the close of the
embryonic period (Fig. 9, C) fourteen or fifteen pairs of somites
have been formed, and posterior to these remain short undivided
regions of mesoderm from which additional somites will be
formed during the larval period. These somites are of course
not all in the same stage of development, but passing along the
series in the anterior direction they rep-
resent successively more advanced con-
ditions. Advance is indicated by in-
crease in the size of the cavity of the
somite, thinning of the wall, and the
ventral and somewhat posterior exten-
sion of the somite between the wall of
the gut and the superficial ectoderm
(Fig. 8, E). By the end of the embry-
onic period the more anterior pairs are
already bent into the < -form character-
istic of the adult. The first pair of
somites send forward unusual extensions
from the antero-dorsal region along each
side of the notochord (Fig. 9, B) : it is

°ssible' thoush hard'y like]y> that these

larva with six pairs of indicate the former presence of an addi-

mesodermal somites, at ,. -, f ., . .-,• . .,

the level of the notochord tional pair of somites in this region: it
and somites. After Cer- seems more likely that the condition is

fontaine. a, Archenteron;

e, enteroccei;w, notochord; the result of the anterior prolongation of

d '/If rslaiteS.SiXth meS°- the notochord beyond the proper region

of the first somite. The walls of these

extensions later go through the same developmental history
as those of a typical somite.

By the time five or six pairs of somites are formed they begin
to show that bilateral alternation which is so characteristic of
the adult (Fig. 10). Only the first and the upper part of the
second pairs of somites lie exactly opposite. In the other pairs
the left member comes to lie in advance of the right, and farther
posteriorly the segments of the two sides exactly alternate.
It is also noticeable that the left side develops slightly in advance

THE DEVELOPMENT OF AMPHIOXUS 31

of the right, e.g., when there are eight somites on the left there
are but seven on the right.

The enlargement and ventral elongation of the somites men-
tioned above is accompanied by a differentiation of their walls.
That part of the somite lying just beneath and in contact with
the ectoderm becomes thinner and forms what is known as the
parietal wall of the somite, or the somatic mesoderm (Fig. 8, E) ;
the region in contact with the wall of the gut or enteron also
becomes thinner and forms the visceral wall or splanchnic meso-
derm: while the more restricted portion bordering the chorda
thickens by the horizontal flattening and antero-posterior
elongation of the cells through the extent of the somite. This
last region of the somite is called the myotome, while the somatic
and splanchnic regions together are termed the lateral plate.
In the myotome the cells begin, as early as the nine-somite stage,
to differentiate as muscle cells (Fig. 8, E) forming a muscular
epithelium. At the close of the embryonic period the more
anterior my o tomes are capable of muscular contractions.

The thinning of the parietal and visceral walls of the somite
and their downward extension, considerably enlarge the en-
closed cavity and carry it down around the sides of the enteron.
The cavities of the somites now become recognizable as the
beginnings of the ccelomic space. The enlargement of the myo-
tome partially obliterates the cavity of the somite in the dorsal
region, the small cavity remaining being termed the myoccel.
The larger cavity of the lateral plate is then distinguished from
the myocoel by the term splanchnoccel. Before the close of the
embryonic period the ventral walls of the more anterior somites
push completely around the enteron and meet in the mid-
ventral region, separating the enteron from contact with the
ectoderm. Presently the median walls of the splanchnoccels
for the most part disappear, and the splanchnoccels of each pair
of somites fuse more or less completely. Remnants of these
median partitions below the enteron appear to remain as the
rudiments of the subintestinal vein and branchial artery.
Finally the somite becomes divided by a horizontal partition
between the lateral plate and myotome, and the corresponding

32 OUTLINES OF CHORDATE DEVELOPMENT

cavities are completely separated. By the close of the embry-
onic period the anterior and posterior walls of the somites in the
region of the splanchnoccels also break through, leaving these
cavities continuous antero-posteriorly as well as transversely.
The unsegmented cavity thus formed is the ccelomic cavity of

up

FIG. 11. — Sections through young Amphioxus embryos showing the origin of
the anterior gut diverticula. After Hatschek. The cilia are omitted. A.
Frontal section through embryo with nine pairs of somites. (See Fig. 9, 5).
The dotted line marks the course of the gut wall ventral to the level of the section.
B. Optical sagittal section through anterior end of embryo with thirteen pairs
of somites, showing position of right anterior gut diverticulum. C. Same in
ventral view, c, Ccelomic cavity of somite; ch, notochord; csg, rudiment of
club-shaped gland; d, rudiment of anterior gut diverticula; ec, ectoderm; en,
endoderm; g, gut cavity (enteron, mesenteron); gsl, rudiment of first gill slit;
Id, left anterior gut diverticulum; n, nerve cord; np, neuropore; rd, right anterior
gut diverticulum; si, $2, sg, first, second, and ninth mesodermal somites.

the embryo and larva which is seen to be a true synccelom
(Fig. 19, A).

There remain to be described, in connection with the develop-
ment of the mesoderm, a pair of outgrowths from the anterior
end of the enteron in front of the first pair of mesodermal so-
mites. These cavities are known as the anterior gut diverticula

THE DEVELOPMENT OF AMPHIOXUS 33

and have been commonly regarded as endodermal derivatives
of peculiar character, but although their exact homologies
remain rather obscure it seems clear that they are essentially
a pair of mesodermal somites which develop late, on account
of the delayed forward extension of the whole anterior tip of
the body. The anterior gut diverticula first appear in the
embryo with seven pairs of somites, as a pair of narrow antero-
dorsal evaginations from an expanded anterior region of the
enteron (Figs. 9, B; 11, A, B). These push forward much
like the somites, and quickly pinch off from the enteron as
a pair of closed sacs (Fig. 11, C).

Although symmetrical in their origin they differ greatly in
their subsequent development. In the embryo with ten pairs
of somites the right diverticulum begins to grow forward and to
enlarge while its wall becomes very thin. Soon it extends
across the mid-line and finally, as a median structure, it occu-
pies the whole of the space below the chorda and from the en-
teron forward to the tip of the embryo. It remains wholly
in front of the first somite and forms what is known as the
preoral cavity or head cavity (Fig. 9, C). The left anterior gut
diverticulum differs widely from its antimere. It remains
quite small and unmodified throughout the embryonic period,
shortly after which it acquires an opening to the surface in the
left side of the head below the level of the chorda, and is then
known as the preoral pit (Fig. 9, C). Its history is quite com-
plicated and will be considered later.

4. The Enteron and its Appendages

After the wall of the archenteric cavity has lost successively
the mesoblast folds, notochord, and anterior gut diverticula, the
endodermal tube remains as the wall of the enteron or mesen-
teron. This gives rise to the epithelial lining of the alimentary
canal and related structures. After the time of hatching the
enteron elongates rapidly and, except at its anterior extremity,
narrows very markedly, differentiating in this way the posterior
stomach-intestine from the wide anterior pharyngeal region

34 OUTLINES OF CHORDATE DEVELOPMENT

opposite the first two somites (Fig. 9, C). Throughout the
embryonic period, as described above, the only opening to the
exterior is by way of the neurenteric canal, neuroccel, and neuro-
pore, the essential relations among which do not change during
this period. We may describe briefly the chief structures
arising in connection with the enteron during the embryonic
period.

A. THE CLUB-SHAPED GLAND AND ENDOSTYLE

In the floor of the enteron, just back of the anterior gut
diverticula, and therefore opposite the anterior margin of the
first somite, a transverse groove appears about the time nine
or ten somites are present (Figs. 9, B; 11). During the latter
part of the embryonic period this groove constricts off as a
narrow tube, separate from and below the gut, and acquires an
opening at its left end to the exterior in the region below the
preoral pit, while the right end dilates into a conspicuous sac,
closed at this time (Fig. 9, C).

Lying just in front of the grooved rudiment of the club-shaped
gland, is a strip of high ciliated cells which seems to be the first
indication of the endostyle. The later development of the
gland and endostyle is described in connection with the
history of the larval period.

B. THE MOUTH

The mouth, first gill slit, and anus develop almost simul-
taneously, toward the close of the embryonic period. At the
age of fourteen somites a large patch of ectoderm on the
left side of the head, along the margin of the first somite,
thickens considerably and with this thickened area the adjacent
wall of the enteron fuses. This fused region then becomes per-
forated by a small opening (Fig. 9, C), which rapidly enlarges
and becomes the relatively enormous mouth opening bordered
with elongated cilia (Fig. 12).

THE DEVELOPMENT OF AMPHIOXUS

35

C. THE FIRST GILL SLIT

At the same time the mouth is forming, the endoderm
pushes out ventrally, opposite the second somite, and fuses
with another thickened patch of ectoderm (Fig. 9, C). Per-
foration follows and forms the first gill slit which rapidly enlarges
and moves up on the right side of the head, nearly opposite

B

981

csg

FIG. 12. — Anterior ends of Amphioxus larvae, in optical section. A. One gill
slit stage, from right side. After Hatschek. B. Four gill slit stage, from left
side. After Lankester and Willey (mouth added). 6, Brain region; c, coelpm
(preoral head cavity); ch, notochord; csg, club-shaped gland; d, dorsal portion
of preoral pit (later forming the groove of Hatschek and Hatschek's nephridium) ;
e, rudiment of endostyle; gsl, first gill slit; Hn, Hatschek's nephridium; i,
intestine; ra, mouth; n, nerve cord; np, neuropore; o, external opening of club-
shaped gland; p, pigment; ro, Raderorgan; v, cerebral vesicle.

the mouth (Fig. 12, A). It remains smaller than the mouth
but is similarly bordered with long cilia.

D. THE ANUS

Very shortly after the mouth and first gill slit are formed the
wall of the narrow enteron, immediately below the neurenteric
canal, fuses with the ectoderm and the region is perforated as
the anus. At first this lies in the mid-line but later is displaced
toward the left, by the development of the provisional caudal

36 OUTLINES OF CHORDATE DEVELOPMENT

fin. Upon the formation of the anus the intestine is separated
from the neurenteric canal and this structure closes and gradu-
ually moves posteriorly, away from the anal region, as the tail
region grows out; but for some time the tip of the nerve
cord remains curved around toward the region of its original
connection with the enteron.

About the time the mouth and anus open, the alimentary
tract becomes ciliated and a small diverticulum forms in the
anterior part of the stomach-intestine; this is the rudiment of
the caecum or liver.

At the close of the embryonic period, which is arbitrarily
marked by the opening of the mouth, the embryo is about
1.0 mm. long and very slender (Fig. 9, C). Probably its actual
bulk is little greater than that of the egg. The embryo is
almost perfectly transparent, and swims about with the elon-
gated ectodermal cilia, accompanied by irregular muscular con-
tractions when strongly stimulated. The anterior end is di-
lated and prolonged forward into a rostrum, containing the
preoral head cavity and supported by the elongated notochord.
The external openings are, the mouth and first gill slit on
opposite sides of the head, above these the small median
neuropore, and near the posterior end the small ventral anus.
Posteriorly the tail is expanded into a provisional caudal fin
formed of elongated ectodermal cells. There are about fifteen
pairs of somites in every stage of development, from the com-
pletely undifferentiated condition of the posterior pairs of the
series, to the quite completely differentiated anterior pairs.
Anteriorly the nervous system shows the rudiment of the brain;
posteriorly it is no longer connected with the enteron on account
of the closure of the neurenteric canal. The notochord is com-
pletely established. In addition to the mouth and first gill slit
the enteron has formed the anterior gut diverticula and club-
shaped gland, all of which have become separate structures
and commenced their differentiation. In spite of its rather
complex structure all parts of the embryo are still of epithelial
character, though the epithelia now show some degree of
elementary cellular differentiation.

THE DEVELOPMENT OF AMPHIOXUS 37

III. THE LARVAL PERIOD

The duration of this period is roughly about three months,
during which the larva is free swimming but descends to deep
water. Development is very slow and consists largely in the
elaboration and modification or multiplication of structures
indicated at its beginning. Although up to this time devel-
opment has been simple and typical (primitive) in general,
now the anterior portion of the larva becomes highly modi-
fied through the development of characters not found in the
Craniata. These are, chiefly, the extensive asymmetry of the
pharyngeal and associated structures, and the development of
the atrium or peribranchial cavity — both to be regarded as
special adaptations to the habits of the larva. The close of
the larval period is marked by an extensive metamorphosis
which consists largely in a " symmetrization" of the anterior
end. At the close of this period the larva is said to be at the
''critical stage.7'

1. The Central Nervous System

Very soon after hatching the walls of the spinal cord thicken,
constricting the neuroccel, and becoming differentiated into
three regions. These are (a), a thin epithelial layer — the
ependyma, lining the neurocoel, (&), dorso-lateral and lateral
columns of nerve-cell bodies (gray substance] connecting re-
spectively with the dorsal and ventral spinal nerves, and (c)
ventral columns composed of nerve fibers (white substance).

In the brain region the walls become comparatively thin
and the cavity dilates considerably (Fig. 13). At first the
brain lies beneath the epidermis, and around the neuropore
its wall is directly continuous with the superficial ectoderm.
When the dorsal fin appears in the mid-line the neuropore is
pushed to one side, usually the left. Gradually the brain
sinks away from the epidermis, drawing down the neuropore
into a funnel-shaped depression, and at the same time drawing
out the antero-dorsal wall of the brain into a conical elevation,

38 OUTLINES OF CHORDATE DEVELOPMENT

the two remaining connected by a very small tube. Not
until after metamorphosis does this opening become entirely
closed and the neuropore then remains as a ciliated funnel
known as the olfactory pit, which retains an innervation from
the elevated region of the brain and becomes sensory in char-
acter, the assumption being that it functions as an olfactory

n

FIG. 13. — Median, sagittal sections through the brain of Amphioxus. After
Boeke. A. Of a larva with seven primary gill slits. B. Diagram of a section
through the brain of a larva of 2.25 mm., with five pairs of primary gill slits,
X 933. C. Same of a young specimen of 10 mm. X 233; c, Central canal of
cord; i, infundibulum; n, neuropore; p, cerebral pigment; op, olfactory pit;
v, cerebral vesicle; vd, postero-dorsal extension of cerebral vesicle.

organ. This antero-dorsal outgrowth of the brain may cor-
respond with the lobus olfactorius impar which marks the
morphologically anterior end of the brain of the Craniates.
Just in front of and below this is the large cranial pigment spot
(Fig. 13) in the general region from which the olfactory lobes
grow out in higher forms. Postero-dorsally the brain wall is

THE DEVELOPMENT OF AMPHIOXUS 39

thickened by an accumulation of ganglion cells, and in its
posterior part two important structures appear. Just in front
of the opening of the cavity of the cord the ependymal cells
elongate forming a small median pad which is regarded as the
infundibulum (Fig. 13). Posterior to the cerebral vesicle
proper is an extensive dorsal diverticulum of the neuroccel : this
has been compared with the IV ventricle of Craniates.

The simple character of the brain of Amphioxus is obviously
correlated with the general lack of special sense organs, par-
ticularly with the absence of the important optic and audi-
tory organs, and the feebly developed olfactory apparatus.

2. The Gill Slits

We may describe first the general morphological arrange-
ments of the developing gill slits: the development of the first
gill slit has already been mentioned.

Although finally symmetrical and paired organs the gill
slits of the right and left sides develop independently, those of
the left side first. These appear successively in the mid-
ventral line, posterior to the first gill slit, and as they form
they shift upward, on the right side of the pharynx (Fig. 14).
These are called the primary gill slits, and when twelve to
fifteen, typically fourteen, have appeared, their formation
ceases. At this time the more anterior slits are large ovoid
openings lying well up on the right side; posteriorly they
diminish in size and lie toward the mid-line. In all these
early stages they are metameric and correspond with the
somites, a correspondence which is entirely lost later on.
When the full number of fourteen primary gill slits has been
formed, the secondary gill slits, or those of the proper right
side, appear, also on the right side of the pharynx and dorsal
to the primary series. Their first indication is a longitudinal
ridge, in which appear six thickenings alternating with the
primary gill slits in the region between the third and ninth of
these (Fig: 14,* B).

The relations of these parts of the pharynx will become clear

40 OUTLINES OF CHORDATE DEVELOPMENT

if it be imagined that the formative centers located in the
most anterior region of the pharynx have been twisted out of
their normal positions, so that the morphological mid-ventral

en

gsl4

m rm

FIG. 14. — Anterior ends of Amphioxus larvae. A. Larva with eleven primary
gill slits, from left side. After Goodrich. B. Larva with eleven primary gill
slits, from right side showing metapleural fold and secondary gill slit rudiments.
After Willey. C. Larva with fourteen primary gill slits, from left side. After
Lankester and Willey. ao, Ventral aorta (branchial artery); at, atrial cavity;
ch, notochord; en, cranial nerve; csg, club-shaped gland; dn, dorsal spinal nerve;
e, end ostyle;gH, groove of Hatschek; gsl, gsll, gs!4, first, eleventh, and four-
teenth primary gill slits; H0s, rudiments of secondary gill slits; i, internal opening
of club-shaped gland; Im, lower margin of mouth; m, mouth; my, myotomes;
n, nerve cord; ne, nephridium; o, external opening of club-shaped gland; p,
pigment in nerve cord; r, renal cells in floor of atrial cavity; rm, edge of right
metapleural fold; ro, Raderorgan.

line becomes displaced to the topographical right side, and
structures morphologically of the right and left sides appear,
respectively, dorsally and ventrally on the right side alone.

THE DEVELOPMENT OF AMPHIOXUS 41

The rudiments of the secondary gill slits enlarge and become
perforated, and then an additional perforation appears at each
end of the series making eight in all. As these enlarge, chiefly
in the ventral direction, the primary gill slits below them are
moved down to the ventral side, and then over on the left side
of the pharynx to their proper position (Figs. 14, C; 15). As
a result of this migration the dorsal and ventral margins of the
primary gill slits are reversed, and it is evident that the mor-
phological ventral margins of these actually appeared first to
lie dorsally. As this migration is going on, first the secondary,
then the primary gill slits become divided by a downward
extension of a tongue-like process from the dorsal wall of
the slit which finally reaches the ventral side, divides the
originally simple opening into two, and forms the tongue bar
of the completed structure of the adult (Fig. 15). These
tongue bars appear in all the secondary slits except the first,
and in all of the primary slits except the first two and a vari-
able number of the last. As the primary gill slits approach
their final position the most anterior disappears completely
(Fig. 15) and soon after, the last five also disappear, reducing
the number in the primary series to eight, the same as the
number originally appearing in the secondary series. This is
the arrangement of the gill slits at the critical stage, the sym-
metrization of these structures being one of the important
phases of metamorphosis. After the reduction of the gill
slits to eight symmetrical pairs, arranged metamerically,
additional pairs form slowly, posterior to the primary and
secondary. These are the tertiary gill slits. They are not
metameric in their appearance and they displace anteriorly
the primary and secondary slits, so that the whole gill slit
series loses its metameric arrangement.

Regarding the actual details of the formation of the gill
slits little is known except in certain of the secondary series,
or those of the right side proper. In these, and presumably
in most of the primary series also, true gill pouches seem to be
formed first, purely of endodermal cells. These are drawn
out ventro-laterally into small tubes closed by a very thin

42 OUTLINES OF CHORDATE DEVELOPMENT

superficial layer of transparent ectoderm cells. The tongue
bar grows down like a stalactite from the roof of the gill pouch,
and just before it reaches the ventral side of the pouch the
ectoderm is perforated opposite the tongue bar. But by this
time the atrial cavity has formed in this region, as will be
described later, so that the gill slits never open directly to the

cv

dgsi

FIG. 15. — Anterior ends of Amphioxus larvae showing the migration of the
mouth, formation of tongue bars, reduction in primary gill slits, etc. After
Willey. A. Larva with fourteen primary gill slits nearly in their definitive posi-
tion on the left side. Oral hood in process of formation. B. Larva with nine
primary, and eight secondary gill slits. Mouth nearly in its definitive anterior
position and oral hood nearly completed. This larva has nearly reached the
"critical stage." at, Atrial cavity; 6, buccal (oral) cirri; be, buccal cavity (cavity
of oral hood); c, coelom; cv, cerebral vesicle; df, dorsal fin chambers; dgsl, dgs8,
first and eighth definitive gill slits (second and ninth of the primary series) ; dph,
dorsal wall of pharynx (region of epipharyngeal groove); e, endostyle; gsl, gs9,
gsl4, first, ninth, and fourteenth primary gill slits; h, hepatic caecum; i, intestine;
Im, lower margin of left metapleural fold; ra, mouth; nH, Hatschek's nephridium;
pb, peripharyngeal band; r, renal papilla in floor of atrial cavity; ro, Raderorgan.
tb, tongue bar; uh, upper margin of oral hood; v, velum.

outside; the more anterior primary gill slits apparently form
exceptions to the usual arrangement in opening directly for a
time (Fig. 17). As the external openings of the pouches en-
large, the tongue bars move to the surface and if it is true
that they are completely covered with endoderm, the atrial

THE DEVELOPMENT OF AMPHIOXUS 43

cavity on which they border must therefore to this extent be
lined with endoderm (Legros).

3. The Club-shaped Gland

The club-shaped gland lies far forward in the pharyngeal
region, and does not share in the shifting of the gill slits and
other derivatives of the pharynx with which it is at this time
connected only at a -single point. During the early larval
period its dilated right end narrows and acquires an opening
into the pharynx (Fig. 14, A). This " gland" now is in the
form of a narrow tube, opening at the right end into the
pharynx and at the left to the outside. It is of doubtful
significance, both functional and morphological; it has been
compared with a gill slit and may represent the antimere of the
first primary, which is otherwise entirely lacking. It soon
atrophies like this gill slit and disappears without leaving any
trace (Figs. 14, 15).

4. The Endostyk

This appeared as a transverse, ciliated thickening, in the
floor of the pharynx in front of the club-shaped gland. As a
thickening of the pharyngeal wall the endostyle is involved
in the general torsion of this region and passes over to the
right side (Fig. 12). There its middle region draws back above
the primary gill slits, i.e., in the morphological mid-ventral
line, converting the transverse £>and mto a > -shaped structure
with the apex directed posteriorly (Fig. 14). It continues to
extend backward, between the rows of primary and secondary
gill slits, while its limbs draw together coming into contact
and forming a double strip of cells, which in part become
differentiated as glandular cells. The endostyle is finally
carried back into a median ventral position by the time of the
critical stage (Fig. 15, B).

From the anterior end of the endostyle two narrow ciliated
bands — the rudiments of the peripharyngeal bands (Fig. 15,

44 OUTLINES OF CHORDATE DEVELOPMENT

B), pass around the pharyngeal wall to the dorsal side, and
there extend backward as a pair of ciliated bands which later
fuse into a single median structure — the epipharyngeal or
hyperbranchial groove.

5. The Mouth and Associated Structures

This opening on the left side of the head continues to en-
large during the early part of the larval period, and finally
extends from a point considerably in front of the first gill slit
to the region of the fifth gill slit (Fig. 14). When the second-
ary slits begin to develop and the pharynx rotates back to a
normal position, the mouth gradually shifts its position in a
horizontal plane, moving around to the anterior end: it finally
reaches an anterior median position at about the critical
stage (Fig. 15). As the mouth migrates its margin extends
inward as the velum, like that of Ammocoetes, finally reducing
the mouth opening to a small aperture. Later this becomes
fringed with outgrowths from the free margin of the velum—
the velar tentacles (Figs. 15, 16). From the base of the velum
the oral cirri grow out. These are first indicated about the
time the secondary gill slits appear, and by the time of the
critical stage they are well developed and their cartilaginous
supports have become differentiated. At the same time the
velum begins to form, folds of the integument, first above
and then below the mouth, grow out, the latter passing for-
ward toward the region of the snout. These folds are the
rudiments of the oral hood, and as the mouth passes forward
they enlarge and shift so as to form the left and right sides
respectively of the oral hood. The right fold becomes contin-
uous with the extremity of the dorsal fin as this turns the
anterior end of the larva (Figs. 15, 16).

6. The Preoral Pit and Its Derivatives

The preoral pit, the formation of which from the left anterior
gut diverticulum has been described, was left as a small sac

THE DEVELOPMENT OF AMPHIOXUS

45

(Fig. 9, C), opening upon the surface of the left side of the
head, in front of the mouth. When the rudimentary folds of
the oral hood appear, the dorsal fold develops just above the
opening of the preoral pit, which thereafter remains as a struc-

cr

vt

FIG. 16. — Ventral view of anterior end of adult Amphioxus. The buccal
cavity has been cut open along the mid- ventral line and spread out. After
Goodrich, b, Buccal skeleton; ch, notochord; cr, cirri; gH, groove of Hatschek;
h, oral hood, Hn, Hatschek's nephridium; m\t mz, first and third myotomes;
n, nerve coming from left side; o, pharyngeal opening of Hatschek's nephridium.
TO, Raderorgan; s, solenocytes; v, velum; vt, velar tentacles.

ture chiefly related with the buccal cavity. Early in the larval
period the preoral pit enlarges and then divides into a dorsal
and a ventral portion. The ventral or stomodceal portion, as it
is called, enlarges very considerably, moves to the surface, and

46 OUTLINES OF CHORD ATE DEVELOPMENT

spreads out over what is by that time the partly formed oral
hood. It forms here the irregularly lobed ciliated patch of
cells called the "Rdderorgan" (Figs. 12, 15, 16). The dorsal
portion of the preoral pit again divides into two parts, one
lying anteriorly and toward the right, the other posteriorly
and toward the left. The first of these remains on the right
side, in the roof of the buccal cavity, and forms there the
glandular "groove of Hatschek" leading to the oral aperture
(Figs. 14, 16). The second part remains toward the left side
and draws out into a long fine tube, extending back to the
pharynx, into which, by the time the larva has six gill slits, it
acquires an opening above the mouth, and loses its external
opening (Figs. 12, 15, 16). This part is sometimes called
" Hatschek' s nephridium": its final structure is that of a greatly
enlarged nephridium (Fig. 16). There seems to be little doubt
that the dorsal division of the preoral pit is homologous with
the hypophysis of the Craniates, and with the neural gland and
its duct of the Tunicates. Some would restrict this homology
to the anterior portion (groove of Hatschek) alone, others to
the posterior part alone (Hatschek's nephridium).

7. The Blood-vessels

The ventral blood-vessel which was formed from cells of
somewhat uncertain origin between the lower ends of the
lateral plates as they approached the ventral side, is formed
throughout the pharyngeal region during the larval period,
lying between the primary and secondary gill slits (Fig 14, B).
It first begins to show contractions about the time the first
gill slit is perforated.

8. The Atrium

The presence of the atrium is one of the two chief character-
istics wherein Amphioxus is essentially unlike other Chordates,
for a similar structure is found only among the Urochorda. It
is to be recognized in Amphioxus as a special adaptation to

THE DEVELOPMENT OF AMPHIOXUS

47

the burrowing habit, serving to protect the delicate and com-

plicated pharynx. The enclosure of the branchial region by the

atrium occurs early during the larval period. About the time

six or seven primary gill slits

are present, a pair of low folds

appears in the middle of the

body region, along the ventral

surface. These are the so-

called metapleural folds, at first

merely thickenings of the ecto-

derm, but later hollow ridges

of considerable size; their pri-

mary cavities are to be re-

garded as ccelomic in origin.

The metapleural folds lie close

together and gradually extend

forward, the right fold proceed-

ing rapidly in advance of the

left and passing far up on the

right side of the pharynx,

above the primary gill slits,

which it reaches about the

time ten are formed (Fig. 17,

A ) . Later the left fold reaches

the gill-slit region, diverges

widely from the right fold, and

, . , „ FIG. 17. — Diagrams of three larvae of

passes tO the Opposite Side Ot Amphioxus, viewed ventrally, showing

the Secondary gill slits, lying the, Rations of the metapleural folds

J . and the method of their closure. After

at first in the topographical Lankester and Willey. A. Folds still

i • / i i • i completely separate. B. Folds fused,

Ventral region (morphological andPatrial cavity thereby established!

left side) (FigS. 14 B; 17). from atriopore to posterior end of

.„. ' , , , „ , ! , pharynx. C. Folds fused throughout,

The metapleural folds enlarge except in the region of the first two

and new cavities of lymphatic

character appear within them, left metapleural fold; m, mouth; rm,
, . , T . , right metapleural fold.

which encroach upon the

original ccelomic space and lead to their obliteration.
From the inner face of each metapleural fold a horizontal

48 OUTLINES OF CHOKDATE DEVELOPMENT

ridge or shelf appears, just below the level of the body wall.
These are the subatrial ridges (Fig. 18, A); they grow toward
one another and fuse across the mid-line, enclosing between
themselves and the ventral body wall a small space lined with
ectoderm, which is the beginning of the atrial cavity (Fig. 18, B) .
The formation and fusion of the subatrial ridges occur first pos-

sa

FIG. 18. — Diagrams of transverse sections through Amphioxus larvae, showing
the formation of the atrial cavity. After Lankester and Willey. A. Section
through larva with eleven or twelve primary gill slits, showing subatrial ridges on
metapleural folds. B. Section through slightly older larva (Fig. 17, 5), showing
first fusion of subatrial ridges to form the rudiment of the atrial cavity. C.
Section through advanced larva showing enlargement of atrial cavity and the
method of its encroachment upon the coelom. a, Atrial cavity; ao, dorsal aorta;
c, ccelom (splanchnoccel) ; ch, notochord;/, dorsal fin cavity; i, intestine; ra, meta-
pleural fold containing ccelomic space; mt, myotome; my, myoccel; n, nerve cord;
sa, subatrial ridges; sc, sclerotome; v, subintestinal vein.

terior to the gill-slit region, and proceed thence forward, and by
the time the secondary gill-slit series is completed the bran-
chial region is completely covered. Anteriorly the subatrial
ridges merge with the body wall closing the cavity at this end,
but posteriorly the atrial cavity remains open to the outside as

THE DEVELOPMENT OF AMPHIOXUS 49

the atriopore (Fig. 17). The cavity, at first very small, gradu-
ally enlarges (Fig. 18, C) pushing 'upward each side of the
pharynx, ultimately surrounding it on all sides except the
dorsal, where alone the pharynx remains connected with the
body wall. The space occupied by the atrium was previously
the region of the general ccelom. The development of the
atrium therefore reduces the ccelom to a number of greatly
reduced and somewhat scattered spaces. The chief of these
are (a) the pair of dorsal coelomic canals along the dorso-lateral
regions of the pharynx, from which the atrium remains sepa-
rated by the suspensory folds or denticulate ligament; (b) the
endostylar ccelom in the ventral region below the endostyle;
and (c) the branchial ccelomic canals connecting the two pre-
ceding regions by way of very small canals in the primary
branchial arches. Posterior to the atriopore the ccelom remains
for a time in its normal relation, but later the atrial cavity
extends into this region on the right side nearly to the anus,
leaving the ccelom widely open only on the left side of the
intestine.

The atrial cavity is formed in the branchial region just before
the primary gill slits (except perhaps the more anterior) are
perforated, so that from the first these open into the atrial
cavity and never directly to the outside. From its mode of
formation the denticulate ligament or- suspensory fold is seen
to be a membrane equivalent to the body wall, and therefore
covered on its atrial surface with ectoderm. Of course the
remainder of the atrial cavity is lined with ectoderm, except,
as we have seen, that the endodermally covered tongue bars
line a small portion of it.

9. Larval Asymmetry

The nature and extent of the larval asymmetry of Amphioxus
represent the most important difference between the develop-
ment of this form and other Chorda tes. The asymmetry of
such structures as the neuropore and anus, which have merely
been displaced slightly by a later medially developing structure

50 OUTLINES OF CHORDATE DEVELOPMENT

(in these cases the median fins), is not unusual or of particular
importance. Nor is the alternation on opposite sides of the
body of the mesodermal somites and structures primarily re-
lated to them, such as the spinal nerves and gonads. The
asymmetry which is unique in Amphioxus concerns the for-
mation of the mouth, gill slits, and other organs connected with
the anterior end of the pharynx and with the oral hood. One
of the remarkable facts in this connection is that the asymmetry
is not indicated in early development and is wholly corrected
later in larval life, so that it is wholly limited to a comparatively
brief period during larval development. It is obviously a
purely secondary or ccenogenetic character, and must be ex-
plained as in some way adaptive either to present or past
conditions of development. We may mention but a single
explanatory hypothesis — that of Willey.

The starting point of this hypothesis is the assumption of a
primitively median dorsal position of the mouth, for which there
is some evidence. The second consideration is the extension of
the notochord forward to the tip of the snout, far in advance
of the central nervous system and enteron. So far as is known,
Amphioxus is the only form in which the chorda extends in
this way — in all Craniates it stops in the region of the mid-
brain. This anterior extension of the chorda, which is ob-
viously an adaptation to the burrowing habit assumed at the
close of the larval period, occurs very early in development
and necessarily prevents the mouth from appearing in the mid-
dorsal region. The net result of this is the shifting of the
formative centers of the mouth, and associated structures of
the oral hood, to one side, actually the left, and the correlated
shifting of the formative centers of other pharyngeal organs.
The whole rotation occurs in a counterclockwise direction,
throwing structures of the proper left side over to the median
line, or even to the right side, structures of the median line
up on the right side, and structures of the right side proper,
still higher up on the same side. The region of extreme torsion
is around the mouth so that posteriorly the amount of dis-
placement becomes less and less and in the posterior part of

THE DEVELOPMENT OF AMPHIOXUS 51

the pharynx the parts appear and remain in a normal
position.

Such an asymmetry is in itself obviously not advantageous
(adaptive) and during later development it becomes corrected
by a compensatory rotary growth of the pharyngeal structures
in the opposite direction, while the mouth and associated struc-
tures (Raderorgan, groove of Hatschek, etc.) move chiefly in
the anterior direction.

This explanation of the origin and correction of the larval
asymmetry may be accepted though its necessarily hypothet-
ical character should be clearly recognized.

10. The Mesodermal Somites

At the commencement of the larval period there were four-
teen or fifteen pairs of somites formed, and we have seen how
each of these divides into a dorsal myotome, with its small
myoccel and thickened muscular wall, and a ventral lateral
plate with thin walls and large splanchnoccel, and further how
the median, anterior, and posterior faces of the lateral plates
break through, forming a continuous ccelom, walled extern-
ally by somatic and internally by splanchnic mesoderm (Fig.
19, A). By the time three primary gill slits have been formed
the number of somites has more than doubled, and the full
adult number (sixty-one in the common species of Amphioxus,
Branchiostoma lanceolatum) is acquired by the time the series
of primary gill slits is completed. All of these additional
somites are formed from the rapidly elongating posterior
region of unsegmented mesoderm, which has been carried
backward past the neurenteric region by the outgrowth of the
tail.

During the later development of the somites their myoto-
mal region increases largely in vertical extent, and the nar-
rowed myoccel sends downward a thin-walled extension below
the myotome proper. This divides into two folds or out-
growths: one of these folds extends inward and upward, be-
tween the myotome or protovertebra as 'it is sometimes called,

52 OUTLINES OF CHORDATE DEVELOPMENT

and the axial structures — notochord and nerve cord, to the
region, of the dorsal fin (Fig. 19, B). This is the sclerotome; its
inner or axial layer is called the skeletogenous layer and gives
rise to dense fibrous connective tissue forming the notochordal
and neural sheaths; its outer or myotomal layer remains thin
and forms the fascia covering the muscular protovertebra :

<*/

FIG. 19. — Diagrams of transverse sections through Amphioxus larvse. A.
Through the body region of a larva with five gill slits, showing separation of
myocoel and splanchnocoel (coelom). B. Through the region between atriopore
and anus of young individual, shortly after metamorphosis, showing relations of
sclerotome. After Hatschek. o, Dorsal aorta; c, ccelom (splanchnocoel); ch,
notochord; d, dermatome; df, dorsal fin cavity; e, epidermis; i, intestine; me,
myocoel; mp, muscle plate (myotome); n, nerve cord; s, sclerotome; », sub-
intestinal vein; vf, ventral fin cavity.

the cavity between the two layers is soon obliterated by an
accumulation of connective tissue. There is no fascia on the
outer surface of the protovertebra or myotome such as is found
in Craniates. The second or dermal fold (dermatome) of the
myocoelic wall, extends downward and outward between the
somatic layer of the lateral plate and the ectoderm (Fig. 19, B),
where its inner and outer layers come into apposition and form

THE DEVELOPMENT OF AMPHIOXUS 53

the cutis layer of the integument. The blood cells and many
of the important blood-vessels appear to be derived from the
skeletogenous layer of the sclerotome.

In the adult the lateral plate forms only the lining membrane
of the ccelom, its somatic layer, the body wall, its splanchnic
layer, chiefly the wall of the gut outside the endodermal
epithelium. The ventral musculature develops later and
appears to be derived from the parietal (somatic) layer of the
lateral plate.

Among the Craniates the sclerotome is formed from a mass
of mesenchyme cells, a tissue which is noticeably lacking in
Amphioxus. It remains an open question whether in this
organism the formation of the sclerotome by a folding of the
myocoelic wall, and the correlated paucity of mesenchyme cells,
is a primitive or secondary character.

11. The Nephridia

The development of the nephridia is very incompletely
known (Legros, Goodrich). They appear in connection with
each gill pouch, as these are first marked out (Fig. 14, A), as
groups of mesoblast cells along the outer faces of the endo-
dermal gill pouches, lying at the base of a narrow ccelomic groove
in this region. These mesoblast cells soon form a definite
blind tube extending posteriorly and ventrally from the
coelom toward the gill pouch. The mesodermal cells compos-
ing the small nephridial rudiments become differentiated, for
the most part, as clear cubic cells, but a group of solenocytes
is distinguished as a small collection of elongated granular
cells in the neighborhood of the coelomic opening of the tubule.
Then the lower end of the nephridial tube fuses with the dorsal
wall of the gill pouch, just posterior to the region of the devel-
oping tongue bar. Finally it opens into the gill pouch, about
the time this becomes perforated externally, and at the same
time its coelomic opening is closed and the solenocytes elongate
into the coelom (Fig. 20).

The first formed nephridia apparently become functional

54 OUTLINES OF CHORDATE DEVELOPMENT

when four or five slits are formed. When the anterior and
posterior primary gill slits atrophy the associated nephridia
seem also to atrophy and later to be re-formed in connection
with the tertiary gill slits although actual details in the pro-
cess are unknown.

12. The Larva at the Critical Stage

We may now summarize briefly the most important char-
acters of the larva at the close of this period, in what is called
the critical stage, marked by the sym-
metrization of the mouth and pharynx,
and the reduction of the gill slits to eight
symmetrical pairs. The larva (Fig. 15, B)
is about 3.5 mm. in length and tapered
at each extremity. The only exter-
nal opening added during this period is
the atriopore, and the neuropore is about
to close. The mouth has assumed a
symmetrical anterior position, and in
front of it a buccal cavity has been es-
tablished by the outgrowth of the oral
hood, from the base of which the buc-
cal cirri have begun to grow out. The
fun number (61) of somites has been
formed for some time, and a definite tail
region has grown out posterior to the
anal opening. The provisional caudal

„ , , ,, , .

fin has been replaced by a permanent
caudal fin fold continuing anteriorly as
space; n, wall of nephri- the median dorsal and ventral fins, the
phridiZ0 former continuous with the right side of
the oral hood. The ventral fin has dis-
the anus to the left side. The atrium is a spacious
cavity receiving the external openings of the eight pairs of
gill slits, of which the anterior pair remains undivided by a
tongue bar, while the posterior one or two pairs are as yet in-

m

FIG. 20.— Portion of

a transverse section of

Amphioxus larva pass-

hridium. After Good-

rich, c, Coelom; e, bran-

chial epithelium; g, wall

placed

THE DEVELOPMENT OF AMPHIOXUS 55

completely divided. The liver or caecum is just beginning to
develop.

At this time the larva largely gives up its free swimming
habit, and assumes the adult habit of burrowing in the sand
or mud of the bottom, frequently remaining buried with
only the anterior end protruding. The cilia of this exposed
region, and of the pharynx in general, vibrate actively, carry-
ing into the pharynx a respiratory current containing small
nutritive organisms. The age of the larvae at the critical stage
varies greatly but three months may be taken as a rough
approximation.

IV. THE ADOLESCENT PERIOD

The larva now enters upon its long period of adolescence.
This is characterized by the very gradual assumption of adult
characteristics, chiefly through histological differentiations and
increasing complexity of many regions of the body. The devel-
opment of the brain and cord has been mentioned. In the
pharynx pairs of gill slits (tertiary) are slowly added and the
pharyngeal wall assumes the complex structure of the adult.
Apparently gill slits are added slowly throughout life, and
usually number upward of one hundred pairs in mature speci-
mens. The liver pushes forward as a simple blind sac, into the
atrial cavity on the right side, carrying before it a fold of fused
atrial and ccelomic walls; finally it extends far forward into the
pharyngeal region. The most important development of the
period is the formation of the gonads.

Gonads

In reality the gonads begin to develop before the end of the
larval period. They appear in the ninth or tenth segment and
continue to about the thirty-fifth. They are first indicated
as small groups of cells in the floor of the myocoel, in the re-
gion where the skeletogenous layer passes into the cutis layer.
This is the region of the nephrostome in the Craniates, and the

56 OUTLINES OF CHORDATE DEVELOPMENT

gonadial cavities which appear later have been compared
with the nephrostomes, or "gono-nephrostomes," of the higher
forms, and it seems likely that Amphioxus may be primitive
as regards the position and origin of the germ cells. At any
rate Amphioxus is primitive in that the gonads arise and
remain as metameric structures, entirely separate from the
excretory system.

Shortly after the completion of the larval period, in specimens
about 5 mm. long, these small groups of cells are found in the
ant ero- ventral region of the segment, toward its inner or atrial
surface, lying along the posterior face of the dissepiment sepa-
rating the surrounding myocoel from that next anterior. As
these cells slowly multiply they push forward into this next
anterior myocoel forming, in its postero-ventral region, a small
bud covered with a fold of the dissepiment. This dissepiment
soon becomes sac-like and remains attached by a short stalk
to the anterior face of the remainder. This solid gonadial rudi-
ment soon develops a cavity within its mass. When the larva
is about 12 mm. long, this general region of the myoccel becomes
cut off by a fold the outer myotomal wall, leaving the gonad
surrounded outside of its own wall by a portion of the general
myocoelic space; this is the perigonadial coelom or gonocoel (Fig.
21, A). In the base of this fold is a blood-.vessel — a branch of
the posterior cardinal vein, which extends through this entire
region.

Then the gonadial cells move toward the atrial side of the
original gonadial sac, leaving the dissepiment al wall as the
visceral wall of the gonocoel while its parietal wall is formed
by this latter downgrowth of the myotomal wall (Fig. 21, B).
The cavity of the gonad enlarges, as the primary gonadial
(ovarian or testicular) cavity, toward the outer or atrial side of
which the definitive germ cells are crowded and become covered
by a follicular epithelium, also formed from cells of the original
mass. The later history is more completely wrorked out in
connection with the ovary, although it is known that the
development of the testis is closely similar.

The outer (atrial) region of the gonocoel, lying between the

THE DEVELOPMENT OF AMPHIOXUS

57

pg

vg

FIG. 21. — Diagrams of sections through the gonads of Amphioxus in three
stages of development. After Cerfontaine. Atrial surface toward the right.
A. Early stage. B. Intermediate stage. C, Late stage showing definitive
arrangement. 6, Peribranchial (atrial) epithelium; c, cicatrix; /, true follicular
epithelium; fe, external layer of follicular epithelium; g, gonocoel; ge, germinal
epithelium; 01, primary ovarian cavity; 02, secondary ovarian cavity; pg, parietal
layer of gonocoel; v, cardinal vein; vg, visceral layer of gonocoel.

58 OUTLINES OF CHORDATE DEVELOPMENT

genital cells and the atrial epithelium, enlarges above and below
the region of the original stalk of attachment, which, by the
general growth of the gonad, is pushed from the myotomal to
the atrial surface. This cavity is now known as the secondary
gonadial (ovarian or testicular) cavity (Fig. 21, C). In the
outer wall of this, just above and below the stalk of attachment,
two specialized thickenings develop; these are the cicatrices.
As the gonadial cells multiply and enlarge they crowd upon
these cavities and nearly obliterate them, particularly those
toward the myotomal surface, but the essentially epithelial
arrangement is not lost, and as the ova develop, as described
at the beginning of this chapter, their polarity has a definite
relation to their position in the epithelium, such that the animal
pole is toward the free surface. When the germ cells are fully
developed the inner and outer gonadial envelopes contain
muscle fibers, the contractions of which appear to assist in
rupturing the visceral layer of the gonocoel in the region of
the secondary gonadial cavity, and force the germ cells into
this cavity, where they remain for some time before extrusion.
Sexual differentiation within the gonad appears in specimens
about 18 mm. in length.

When the fully formed germ cells, ready for laying, have
accumulated in the secondary gonadial cavity, strong contrac-
tions of the body wall and ventral musculature rupture the
outer membrane in the region of the cicatrices, and they are
forced into the atrial cavity, whence they are carried to
the outside through the atriopore by the respiratory current,
aided by continued muscular contraction. Individuals of the
common species of Amphioxus apparently first produce mature
germ cells, that is, become adult, when they reach a length of
about 2 cm.; the age of such specimens is unknown.

REFERENCES TO LITERATURE

CHAPTER I

The literature lists here and at the end of Chapters III, V and VI,
include only a few of the more important or more recent titles. Refer-
ences to the sources of borrowed figures are included, and a few works

THE DEVELOPMENT OF AMPHIOXUS 59

of historical importance, as well as articles containing extensive

literature references.

In each reference the author's name is followed by the title of the

work and the reference to the journal in which the article appeared,

or to the place of publication, in case the work appeared separately.

The number of the volume (Band, tome, etc.} is printed in black-face

Arabic numerals, followed by the year of its publication. References

to pages, parts, etc. are omitted except in a few instances where this

information is necessary.

The abbreviations of the journals more frequently referred to are as

follows :

Amer. Jour. Anat. American Journal of Anatomy. Baltimore and
Philadelphia.

Amer. Jour. Physiol. American Journal of Physiology. Boston.

Anat. Anz. Anatomischer Anzeiger. Jena.

Anat. Hefte. Anatomische He/te. Wiesbaden.

Anat. Record. Anatomical Record. Philadelphia.

Arch. Anat. u. Entw. Same as Arch. Anat. Physiol.

Arch. Anat. Physiol. Archiv fur Anatomic und Physiologic. Leipzig.

Arch. Biol. Archives de Biologic. Leipzig and Paris.

Arch. d'Anat. Micr. Archives dy Anatomic Microscopique. Paris.

Arch. Entw.-Mech. Archiv fur Entwickelungsmechanik der Organismen,
Leipzig.

Arch. mikr. Anat. Archiv fiir mikroscopische Anatomic undEntwicke-
lungsgeschichte. Bonn.

Arch. Naturgesch. Archiv fur Naturgeschichte. Berlin.

Arch. Zellf. Archiv fiir Zellforschung. Leipzig.

Arch. Zool. Exp. Archives de zoologie experimentale et general. Paris.

Biol. Bull. Biological Bulletin. Woods Hole, Mass.

Biol. Centr. Biologisches Centralblatt. Leipzig.

Bull. Acad. Sci. Cracovie. Bulletin de I 'Academic des sciences de
Cracovie.

Bull. Mus. Comp. Zool. Harvard Coll. Bulletin of the Museum of Com-
parative Zoology at Harvard College. Cambridge, Mass.

C. R. Acad. Sci. Paris. Comptes rendus hebdomaires des seances de V Aca-
demic de sciences. Paris.

C. R. Soc. Biol. Paris. Comptes rendus des seances et memoires de la
Societe de biologie. Paris.

Ergeb. Anat. u. Entw. Ergebnisse der Anatomic und Entwickelungs-
geschichte. Wiesbaden.

Intern. Monatsschr. Anat. Phys. Internationale Monatsschrift fiir
Anatomic und Physiologic. Leipzig.

Jena. Zeit. Jenaische Zeitschrift fiir Naturwissenschaft. Jena.

Jour. Anat. Physiol. Journal of Anatomy and Physiology. London.

60 OUTLINES OF CHORDATE DEVELOPMENT

Jour. Coll. Sci. Imp. Univ. Tokyo. Journal of the College of Science,

Imperial University of Tokyo.
Jour. Exp. Zool. Journal of Experimental Zoology. Baltimore and

Philadelphia.

Jour. Morph. Journal of Morphology. Boston and Philadelphia.
Mitt. Stat. Neapel. Mitteilungen aus der zoologischen Station zu

Neapel. Berlin.

Monit. Zool. Ital. Monitore Zoologico Italiano. Firenze.
Morph. Jahrb. MorphologischeJahrbuch. Leipzig.
Phil. Trans. Roy. Soc. Philosophical Transactions of the Royal Society

of London.

Proc. Roy. Soc. Proceedings of the Royal Society of London.
Q. J. M. S. Quarterly Journal of Microscopical Science. London.
Sitz.-Ber. Acad. Wiss. Wien. Sitzungsberichte der Kaiserlichen Akademie

der Wissenschaften zu Wien. Mathematisch-naturwissenschaft-

liche Klasse. Wien.

Zeit. wiss. Zool. Zeitschrift filr wissenschaftliche Zoologie. Leipzig.
Zool. Anz. Zoologischer Anzeiger. Leipzig.
Zool. Jahrb. Zoologische Jahrbilcher. Abteilung filr Anatomie und

Ontogenie der Tiere. Jena.

BOEKE, J., Das Infundibularorgan im Gehirne des Amphioxus. Anat.
Anz. 32. 1908.

CERFONTAINE, P., Recherches sur le deVeloppement de TAmphioxus.
Arch. Biol. 22. 1906.

GARBOWSKI, T., Amphioxus als Grundlage der Mesodermtheorie. Anat.
Anz. 14. 1898.

GOODRICH, E. S., On the Structure of the Excretory Organs of Amphi-
oxus. Q. J. M. S. 54. 1909.

HAMMAR, J. A., Zur Kenntnis der Leberentwickelung bei Amphioxus.
Anat. Anz. 14. 1898.

HATSCHEK, B., Studien iiber Entwicklung des Amphioxus. Arbeiten
a. d. Zool. Inst. Wien. 4. 1882. Ueber den Schichtenbau von
Amphioxus. Verh. d. Anat. Gesell. 2. Anat. Anz. 3. 1888.

KLAATSCH, H., Bemerkung liber die Gastrula des Amphioxus. Morph.
Jahrb. 25. 1897.

KOWALEWSKY, A., Entwickelungsgeschichte des Amphioxus lanceolatus.
Me"m. de 1'Acad. Impe*r. de St. Petersbourg. VII. 11. 1867.
Weitere Studien liber die Entwickelungsgeschichte des Amphioxus
lanceolatus, nebst einem Beitrage zur Homologie des Nervensystems
der Wlirmer und Wirbelthiere. Arch. mikr. Anat. 13. 1877.

LANKESTER, E. R. and WILLEY, A., The Development of the Atrial
Chamber of Amphioxus. Q. J. M. S. 31. 1890.

LEGROS, R., Sur quelques cas d'asyntaxie blastoporale chez P Amphioxus.
Mitt. Zool. Stat. Neapei. 18. 1907. Sur le developpement des

THE DEVELOPMENT OF AMPHIOXUS 61

fentes branchiales et des canalicules de Weiss-Boveri chez 1'Amphi-
oxus. Anat. Anz. 34. 1909. Published anonymously. Sur
quelques points de 1'anatomie et du developpement de PAmphi-
oxus. Notes preliminaires. 1. Sur le nephridium de Hatschek.
Anat. Anz. 36. 1910.

LWOFF, B., Ueber einige wichtige Punkte in der Entwicklung des
Amphioxus. Biol. Centralbl. 12. 1892. Die Bildung der pri-
maren Keimblatter und die Entstehung der Chorda und des
Mesoderms bei den Wirbelthieren. Bull. Soc. Impe"r. de Natural,
de Moscou. II. 8. 1894.

MAC BRIDE, E. W., The Early Development of Amphioxus. Q. J. M. S.
40. 1898. Further Remarks on the Development of Amphioxus.
Q. J. M. S. 43. 1900. The Formation of the Layers in Amphi-
oxus and its Bearing on the Interpretation of the Early Onto-
genetic Processes in Other Vertebrates. Q. J. M. S. 54. 1909.

MAR^CHAL, J., Sur Tovogenese des Selaciens et de quelques autres
Chordates. Premier memoire: morphologic de Pelement chromo-
somique dans Povocyte I chez les Selaciens, les Teleosteens, les
Tuniciers et 1'Amphioxus. Cellule. 24. 1907.

MORGAN, T. H. and HAZEN, A. P., The Gastrulation of Amphioxus.
Jour. Morph. 16. 1900.

SAMASSA, P., Studien liber den Einfluss des Dotters auf die Gastru-
lation und die Bildung der primaren Keimblatter der Wirbel-
thiere. IV. Amphioxus. Arch. Entw.-Mech. 7. 1898.

SOBOTTA, J., Die Reifung und Befruchtung des Eies von Amphioxus
lanceolatus. Arch. mikr. Anat. 50. 1897.

WILLEY, A., The Later Larval Development of Amphioxus. Q. J. M. S.
32. 1891. Amphioxus and the Ancestry of the Vertebrates.
Columbia Univ. Biol. Ser. II. New York. 1894.

WILSON, E. B., Amphioxus and the Mosaic Theory of Development.
Jour. Morph. 8. 1893.

ZIEGLER, H. E., Die phylogenetische Entstehung des Kopfes der
Wirbelthiere. Jena. Zeit. 43. 1908.

CHAPTER II
THE EARLY DEVELOPMENT OF THE FROG

PAGB
INTRODUCTION . . . . 62

I. OUTLINE OF THE LIFE HISTORY OF THE FROG .... 63

II. THE GERM CELLS AND THEIR PRODUCTION 68

A. THE EGG AND SPERM AT THE TIME OF SPAWNING . . 68

B. THE FORMATION OF THE GERM CELLS 71

1. The Reproductive Organs 71

2. Oogenesis 73

3. Spermatogenesis 77

C. SPAWNING 77

III. THE EMBRYONIC PERIOD 79

A. FROM FERTILIZATION THROUGH GASTRULATION .... 79

1. Fertilization and the Development of the Symmetry of

the Egg 79

2. The Symmetry of the Egg 83

3. Cleavage 91

4. The Blastula 94

5. Gastrulation and Notogenesis 98

6. The Mesoderm 107

7. The Medullary Plate 110

8. Summary and Comparisons with other Forms Ill

B. THE FORMATION OF THE EARLY EMBRYO 116

1. The Nervous System 116

2. The Notochord 121

3. The Enteron 122

4. The Mesoderm . 123

The frog (Rana, sp.) is important zoologically, not as a
central type representative of any large group of Chordates,
but as a transitional form connecting the lower and higher
groups of Craniata. This relation is no less apparent embryo-
logically than morphologically. For there are comparatively
few groups — Lampreys, Ganoids, Dipnoans — whose develop-
ment can be compared closely with that of the Amphibia, while
the types of development seen in the Cephalochorda (Amphi-

62

THE EARLY DEVELOPMENT OF THE FROG 63

oxus) and among the Elasmobranchs, Teleosts, and all of the
Amniota, are in various respects quite special. Many of these
special conditions may be more easily understood and com-
pared through common reference to the Amphibia so that as a
form transitional between the lower and higher Craniates the
frog is a type of great importance.

There are also practical and historical reasons for empha-
sizing the development of the frog. The size of the eggs and
their abundance at a season convenient for their study, the
hardiness of the embryos under laboratory conditions and
during experimental manipulation, and the ease with which
the eggs may be fertilized in the laboratory, all make the frog's
egg a particularly valuable laboratory subject. For such
reasons this egg has served as the basis for many of the great
embryological classics; in this respect the egg of the frog is
second only to that of the fowl. And much of the important
modern experimental embryology has had this same object
as its basis, so that a thorough knowledge of the development
of the frog is essential to the student of biology.

I. OUTLINE OF THE LIFE HISTORY OF THE FROG

It will prove advantageous to recall, at this point, the most
striking facts relating to the life history and development of
external characters of the frog. The later development of
this animal is marked by several abrupt changes in habit,
accompanied by pronounced external modifications, but the
earlier development is not so obviously divided into periods,
marked by striking changes in habit or structure. The whole
period of development may be subdivided as follows:

I. THE FORMATION AND PRODUCTION OF THE GERM CELLS. — This
period terminates with spawning.

II. THE EMBRYONIC PERIOD. — This is conveniently divided into:

A. From Spawning through Gastrulation and Notogenesis. —
This includes fertilization, cleavage, the formation of the
germ layers, the formation of the neural tube and noto-
chord, and the establishment of an early embryo.

B. From the Early Embryo to the Time of Hatching.

64 OUTLINES OF CHORDATE DEVELOPMENT

III. THE LARVAL PERIOD. — From hatching to metamorphosis. The
actual developmental processes of this and the latter part of the embry-
onic period (II, B.) are most conveniently described together.

IV. THE ADOLESCENT PERIOD. — From the beginning of metamorphosis
to sexual maturity.

The durations of these periods can be given only in the
roughest way since they vary with the species and particularly
with the temperature and food supply; to a lesser extent the
same is true regarding size. The ages and lengths given
below are to be regarded then as only approximations under
favorable conditions of development.

The period of formation of the germ cells occupies the long
interval between the annual spawning seasons. For the most
part the germ cells are formed during the summer so that in the
following spring only the final steps remain to be accomplished.
Fertilization is external and maturation of the egg is not com-
pleted until the entrance of the sperm cell. Spawning occurs
during the first warm days of spring in most species, although
some, like the bull-frog (R. catesbiana) may not spawn until
summer. The cleavage of the egg terminates with the forma-
tion of a fairly typical blastula, followed by gastrulation, which
is complicated during its later phases by the precocious proc-
esses of notogenesis and formation of the middle germ layer.
During these early phases of development, which usually
occupy about thirty-six hours, the spherical form of the egg is
retained (Fig. 22, B), though a slight enlargement may result
from the formation of internal cavities and the absorption of
water. As notogenesis is completed the embryo begins to
form, bent around the curved surface of the gastrula (Fig. 22,
C, D). Soon, however, the embryo becomes slightly elongated,
and shortly this elongation becomes quite marked chiefly as
the result of the enlargement of the head region and the growth
of the posterior part of the body (Fig. 22, E). Fig. 22, F,
shows an embryo of about two days (2.5 mm.), at the stage
which we may arbitrarily assume to represent the end of the
first division of the embryonic period.

The neural tube is entirely closed, the blastopore roofed over,

THE EARLY DEVELOPMENT OF THE FROG 65

FIG. 22. — Representative stages in the development of the frog. C-F, after
Keibel(Kopsch). G, H, from Ziegler's models. A. Unfertilized ovum. B. Fully
formed gastrula; posterior view. C. Early stage in the formation of the central
nervous system; dorsal view. D. Side view of young embryo showing the rudi-
ments of the visceral arches. E. Side view of an embryo with central nervous
system established, and optic vesicles indicated. F. Side view of ''early embryo,"
showing formation of head and tail regions. G. Side view of embryo just before
hatching. H. Fully formed tadpole, showing rudiments of hind-limbs, a,
Animal pole; b, blastopore containing yolk plug; ba, branchial arches; eg, rudi-
ments of external gills; hi, hind-limb bud; m, mouth; mh, mandibular and hyoid
arches; nf, neural folds; ng, neural groove; np, neural plate; o, olfactory and
stomodseal pit; op, rudiment of optic vesicle ; opr, right opening of opercular cavity,
just before its closure; p, proctodseum; pn, pronephric eminence; r, branchial
ridge (plate); s, oral sucker; t, rudiment of tail; tnf, transverse neural fold;
v, vegetal pole.

66 OUTLINES OF CHORDATE DEVELOPMENT

and in the head region are visible the rudiments of the man-
dibular and hyoid arches and the optic vesicle.

The influence of the yolk mass upon the form of the embryo
now diminishes rapidly, and during the next few days external
change consists largely in the appearance of a definite body
region, the elongation of the tail, and the enlargement of the
head upon which appear olfactory pits, stomodaBum, and
sucking disc, and just back of the head the rudiments of
external gills and the pronephric elevations (Fig. 22, G).

At about six days (5 mm.) the embryo begins to show muscu-
lar twitchings, and about one or two weeks after fertilization
the embryo wriggles its way out of the jelly and becomes a
free living larva or tadpole (Fig. 22, G). This marks the end
of the embryonic period. (In the higher temperatures of the
laboratory the larva? may hatch within five days after fer-
tilization.) For some days after hatching the larvse remain
comparatively inactive, sometimes attaching themselves by
their U-shaped suckers to the outside of the jelly mass, or to
other objects in the water and hanging thus, singly or in groups.
Or they may fall to the bottom and lie passively on one side.
During the days just after hatching the larva? are still depend-
ent for food upon the yolk contained within the wall of the
intestine, but about two to five days after hatching the mouth
opening is formed, and the tadpoles begin to take in food from
outside. As the tadpoles begin to feed they become active, the
sucker becoming functionless and diminishing; and soon they
are in almost constant motion searching for food over the bot-
tom, or in the surface film of the water. The mouth becomes
fringed with lips, covered with horny rasping papilla? and
furnished with a pair of horny beaks. Their food consists of
almost any kind of plant or animal debris and this is con-
sumed in immense quantities. In captivity tadpoles thrive
perfectly on a diet of any cereal, with the occasional sacrifice of
one of their own number. As the alimentary tract becomes
functional the digestive glands increase in size rapidly, and the
long intestine, coiled like a watch spring, can easily be seen
through the ventral body wall. This enlargement of the diges-

THE EARLY DEVELOPMENT OF THE FROG 67

live tract gives the body a well-rounded form, sharply marked
off from the narrow tail, upon which develop large dorsal and
ventral fin-like folds of skin; this is the only locomotor organ
in the tadpole. A period of rapid growth follows upon this
voracious feeding; the rate of growth depending upon tem-
perature and food supply.

Immediately after hatching external gills develop rapidly on
the sides just back of the head, and for a time these are the
only respiratory organs, but about the time the mouth opens
four pairs of gill slits successively perforate the pharyngeal
wall, and their borders become folded forming the true internal
gills: thereupon the external gills gradually diminish and after
a few days disappear completely. At this time the branchial
region becomes covered over externally by a protecting oper-
cular fold of integument, the opercular cavity thus formed
finally remaining open on the surface only by a single excur-
rent pore or " spiracle" on the left side.

During the next few weeks, while the tadpole continues to
feed almost incessantly, there are few external changes except
the general increase in size. About four or five weeks, ordi-
narily, after hatching (much sooner at room temperature) the
limb buds appear, first the anterior pair within the opercular
cavity and therefore not visible externally, and soon after the
posterior pair either side of the cloaca (Fig. 22, H). By the
end of the second month these have enlarged and become
jointed.

For some time previous to this the tadpoles have been coming
to the surface occasionally to expel small bubbles of air from
the slowly developing lungs, and to gulp down a fresh supply,
and as this aerial respiration increases the internal gills retro-
gress and the gill slits diminish.

If developmental conditions have been favorable and food
abundant, about the end of the third month the period of
metamorphosis commences during which, in the space of a few
days, the tadpole loses many of its characteristic structures
adapted to aquatic life and rapidly, almost suddenly, assumes
the characteristics of the amphibious frog. "The tadpole

66 OUTLINES OF CHORDATE DEVELOPMENT

and in the head region are visible the rudiments of the man-
dibular and hyoid arches and the optic vesicle.

The influence of the yolk mass upon the form of the embryo
now diminishes rapidly, and during the next few days external
change consists largely in the appearance of a definite body
region, the elongation of the tail, and the enlargement of the
head upon which appear olfactory pits, stomodaeum, and
sucking disc, and just back of the head the rudiments of
external gills and the pronephric elevations (Fig. 22, G).

At about six days (5 mm.) the embryo begins to show muscu-
lar twitchings, and about one or two weeks after fertilization
the embryo wriggles its way out of the jelly and becomes a
free living larva or tadpole (Fig. 22, G). This marks the end
of the embryonic period. (In the higher temperatures of the
laboratory the larvae may hatch within five days after fer-
tilization.) For some days after hatching the larvae remain
comparatively inactive, sometimes attaching themselves by
their U-shaped suckers to the outside of the jelly mass, or to
other objects in the water and hanging thus, singly or in groups.
Or they may fall to the bottom and lie passively on one side.
During the days just after hatching the Iarva3 are still depend-
ent for food upon the yolk contained within the wall of the
intestine, but about two to five days after hatching the mouth
opening is formed, and the tadpoles begin to take in food from
outside. As the tadpoles begin to feed they become active, the
sucker becoming functionless and diminishing; and soon they
are in almost constant motion searching for food over the bot-
tom, or in the surface film of the water. The mouth becomes
fringed with lips, covered with horny rasping papillae and
furnished with a pair of horny beaks. Their food consists of
almost any kind of plant or animal debris and this is con-
sumed in immense quantities. In captivity tadpoles thrive
perfectly on a diet of any cereal, with the occasional sacrifice of
one of their own number. As the alimentary tract becomes
functional the digestive glands increase in size rapidly, and the
long intestine, coiled like a watch spring, can easily be seen
through the ventral body wall. This enlargement of the diges-

THE EARLY DEVELOPMENT OF THE FROG 67

live tract gives the body a well-rounded form, sharply marked
off from the narrow tail, upon which develop large dorsal and
ventral fin-like folds of skin; this is the only locomotor organ
in the tadpole. A period of rapid growth follows upon this
voracious feeding; the rate of growth depending upon tem-
perature and food supply.

Immediately after hatching external gills develop rapidly on
the sides just back of the head, and for a time these are the
only respiratory organs, but about the time the mouth opens
four pairs of gill slits successively perforate the pharyngeal
wall, and their borders become folded forming the true internal
gills: thereupon the external gills gradually diminish and after
a few days disappear completely. At this time the branchial
region becomes covered over externally by a protecting oper-
cular fold of integument, the opercular cavity thus formed
finally remaining open on the surface only by a single excur-
rent pore or "spiracle" on the left side.

During the next few weeks, while the tadpole continues to
feed almost incessantly, there are few external changes except
the general increase in size. About four or five weeks, ordi-
narily, after hatching (much sooner at room temperature) the
limb buds appear, first the anterior pair within the opercular
cavity and therefore not visible externally, and soon after the
posterior pair either side of the cloaca (Fig. 22, H). By the
end of the second month these have enlarged and become
jointed.

For some time previous to this the tadpoles have been coming
to the surface occasionally to expel small bubbles of air from
the slowly developing lungs, and to gulp down a fresh supply,
and as this aerial respiration increases the internal gills retro-
gress and the gill slits diminish.

If developmental conditions have been favorable and food
abundant, about the end of the third month the period of
metamorphosis commences during which, in the space of a few
days, the tadpole loses many of its characteristic structures
adapted to aquatic life and rapidly, almost suddenly, assumes
the characteristics of the amphibious frog. "The tadpole

70 OUTLINES OF CHORDATE DEVELOPMENT

variable sizes. The egg of the frog is therefore markedly
telolecithal.

In the animal pole the nucleus is contained. At the time of
egg laying this is in the metaphase of the second polar division
(Fig. 26, /). The first polar body has already been extruded
and though very small, may be found near the light spot in
the flattened area at the upper pole.

FIG. 23. — Egg and spermatozoa of frog. A. Spermatozoon of Rana fusca.
After Broman. B. Spermatozoon of R. esculenta. After Broman. C. Section
through the fully formed ovarian egg of Rana sp. From Morgan (Development
of the Frog's Egg). The protoplasmic animal pole is covered with a thin layer
of pigment; vegetal pole filled with yolk bodies; other deutoplasmic granules are
distributed throughout the cell. The large nucleus, or germinal vesicle, sur-
rounded by a definite nuclear membrane, lies eccentrically toward the animal
pole, and contains the thread-like chromosomes and a group of nucleoli.

The specific gravity of the deutoplasm is slightly greater than
that of the protoplasm, and this brings about the assumption
of the definite position of the egg with the vegetal pole down-
ward. But at this time the egg membranes are so closely
adherent that its rotation to this position may be very slow.

At this time, i.e., preceding fertilization, the only symmetry
of the egg is that expressed by its polarity. That is to say it
has no single plane of symmetry, only an axis of symmetry
(polar axis); this is the primary egg axis passing through the
middles of the light and dark (vegetal and animal) poles.

THE EARLY DEVELOPMENT OF THE FROG 71

The spermatozoa of the frog are quite typical in size and
form (Fig. 23, A, B). They are about 0.1 mm. in length; the
head is comparatively long, in some species tapered and curved
at the apex with a laterally attached adhesive perforatorium
or in others, quite blunt with a small rounded perforatorium.
The anterior centrosome lies in the head, the posterior in the
middle piece.

B. THE FORMATION OF THE GERM CELLS
1. The Reproductive Organs

Before describing the formation of the ova and spermatozoa
it will be necessary to recall the essential arrangement of the
gonads and their ducts in the mature organism. The develop-
ment of the system will be described later.

The single parr of ovaries are proliferations of the cells form-
ing the longitudinal genital ridges. These project from the
body wall for some distance along either side of the dorsal
attachment of the mesentery (Fig. 24). Each is surrounded
by a peritoneal fold (mesovarium) , which also slings the organ
from the dorsal body wall and transmits its nervous and vas-
cular supplies. Each ovary is divided transversely into a
series of compartments. In each of these is a small internal
cavity the thick wall of which is formed by the germinal tissue
proper. After spawning the ovaries are left as small rudi-
ments, and during the following summer eggs are formed in
large numbers and their growth is practically completed be-
fore the beginning of the period of hibernation. The ova are
all formed from a few primitive ova which divide repeatedly,
forming small groups or nests of cells, one of which enlarges
becoming the ovum proper, while the others around it be-
come the nutritive follicle cells (membrana granulosa). As the
growth of the ova is completed, the ovaries are so enlarged
that they occupy a large part of the body cavity and crowd
upon the other viscera.

Loosely attached to the anterior ends of the ovaries are the
fat bodies — large masses of yellow streamers of lymphatic

72 OUTLINES OF CHORDATE DEVELOPMENT

tissue, filled with drops of fatty substance chemically similar
to the deutoplasm of the eggs. These are larger and more
abundantly supplied with fat just prior to the breeding season.
Their function seems, in part at least, to supply the material
used in the final stages of the growth and maturing of the eggs,
and also possibly, though doubtfully, for the nutrition of the

ao

f

ou

FIG. 24. FIG. 25.

FIG. 24. — Urinogenital system of the female frog. After Wiedersheim
(Ecker). c, Cloaca; /c, kidney; o, ovary; od, oviduct; oo, opening of oviduct
into cloaca; ou, opening of ureter into oviduct; ut, uterus.

FIG. 25. — Urinogenital system of the male frog. After Wiedersheim (Ecker).
ao, Dorsal aorta; c, cloaca; /, fat body; k, kidney; ou, opening of ureter into
cloaca; t, testis; u, ureter; v, vena cava.

animals themselves prior to and during the spawning season,
for usually no food is taken after the end of their period of
hibernation till after spawning is completed.

The remaining parts of the female reproductive system are
the oviducts (Miillerian ducts). These are a pair of very
long, much convoluted tubes, of small diameter but with
rather thick walls, suspended from the dorsal body wall by

THE EARLY DEVELOPMENT OF THE FROG 73

folds of peritoneum attached just along the outer sides of the
mesovaria (Fig. 24). Each oviduct opens directly out of the
body cavity at its upper end by a ciliated ostium, and at its
lower extremity it opens into the cloaca. The thickness of the
oviducal wall is due chiefly to the presence of glands secreting
the albuminous material which forms the outer egg membrane
or jelly; the lumen of the duct is lined with ciliated epithelium.
Both the length of the oviducts and the thickness of their
walls are subject to seasonal variation, the glands being
largest and the ducts most convoluted during the time of egg
laying. The lower extremities of the oviducts are thin walled
and easily dilatable forming the so-called "uteri," serving as
storage spaces for eggs ready to be laid.

In the male there is a single pair of ovoid testes (Fig. 25), in
a position corresponding to that of the ovaries, and similarly
suspended 'from the dorsal body wall by a peritoneal fold
(mesorchium). Each testis is drained by a variable number
(ten to twelve usually) of vasa efferentia which, after penetrat-
ing the kidney, open into a longitudinal collecting duct — the
vas deferens (Wolffian duct) which serves also as a ureter. Just
before the vasa deferentia open into the cloaca they are dilated
into the seminal vesicles, where mature sperm are stored just
previous to spawning. The testes are divided into lobes like
the ovaries and each lobe is further subdivided into lobules, in
the walls of which the sperm develop and mature. There are
fat bodies in the male similar to those in the female (Fig. 25).
The testes also show much the same seasonal variation in size
as the ovaries, in some species in which the formation of sper-
matozoa is seasonal, while in others, which form the sperm
continuously, there is less variation.

2. Odgenesis

During the later ovarian history of the eggs the maturation
processes are commenced and the deutoplasm or yolk material
is accumulated (growth period). The nucleus of the early
primary oocyte passes into synizesis on that side of the nucleus

74 OUTLINES OF CHORDATE DEVELOPMENT

toward the attraction sphere (Fig. 26, A). After synizesis the
chromosomes scatter through the nucleus as small feathery
bodies (Fig. 26, C), which stain lightly and become vacuolated,
finally losing their identity. Meanwhile small yolk particles
of mitochondrial nature appear in the cytoplasm, in the region
of the attraction sphere and apparently under its influence.
During the growth period the mitochondrial particles and
yolk bodies accumulate rapidly, especially around the attrac-
tion sphere giving it the appearance of a yolk nucleus, whence
they extend to other parts of the cell except in the region
immediately surrounding the nucleus. Finally the "yolk
nucleus" breaks down and the deutoplasm around it scatters
through the cytoplasm (Fig. 26, D, E).

Toward the close of this process the nucleus moves toward
one side of the cell, marking the polarity of the ovum, and
from the first the yolk accumulates in the side opposite the
nucleus or vegetal region, while around the nucleus in the
animal region the protoplasm contains much less deutoplasm;
the superficial protoplasm of the animal pole also contains
many pigment granules.

As the growth period of the primary oocyte is completed
the nucleus moves up to the surface of the cell which becomes
flattened or even depressed toward it; at the same time the
pigment over the nucleus is partially displaced or withdrawn
and the lighter fovea results. The nucleus is very large and
clear; no chromatin network is visible and the only chromatic
bodies in it are the nucleoli. The nucleoli are quite numerous
and apparently of two kinds — true nucleoli whose real nature
is doubtful, and chromatin nucleoli. The nucleus becomes
elongated parallel with the surface of the egg and pigment
accumulates around it, while the nucleoli become vacuolated
and much enlarged. Some of the nucleoli dissolve while
others fuse into large masses and the chromatin nucleoli collect
in a small group near the center of the nucleus.

While these events are occurring within the nucleus a pro-
nounced cytoplasmic modification has appeared. Along the
lower or inner side of the nucleus a small cytoplasmic area has

THE EARLY DEVELOPMENT OF THE FROG

75

G

II

FIG. 26. — Oogenesis in the frog (R. temporaria). A-E, After Lams. F-I,
After Lebrun. A. Primary oocyte in synizesis. B. Primary oocyte with vitel-
line substance of mitochondrial (chromidial) origin in the cytoplasm. C.
Primary oocyte showing feathery chromosomes and chromatin nucleoli. D.
Primary oocyte with ring-like vitelline mass. E. Primary oocyte showing cyto-
plasm in two zones. F. Nuclear region of primary oocyte after dissolution of
the nuclear membrane, showing the small chromosomes and large chromatin
nucleoli. Egg still in ovary. G. First polar spindle in primary position. From
egg in body cavity. H. First polar spindle in metaphase. From egg in uterus.
/. First polar body formed and second polar spindle forming. From egg in
uterus, a, Attraction sphere; c, chromosomes; /, follicle cells; g, contents of
germinal vesicle; n, chromatin nucleoli; fl, vitelline substance of mitochondria!
(chromidial) origin; y, yolk plates; /, first polar spindle (polar body, in /);
//, second polar spindle.

76 OUTLINES OF CHORDATE DEVELOPMENT

become differentiated and from it radiations begin to pass
downward into the cytoplasm. This area extends rapidly
and the radiations pass around the nucleus and up toward the
animal pole of the egg as well as centrally. Finally they ex-
tend even through the nuclear membrane and the nuclear
meshwork takes on the same radiational arrangement which
thus involves practically the entire animal pole. The nuclear
membrane dissolves as the radiations become complete and
the nucleoli are aggregated or dissolved, and just at this time
the egg follicle is ruptured in some way, and the egg escapes
freely into the body cavity surrounded only by its cho'rionic
and vitelline membranes (Fig. 23, C).

Certain areas of the peritoneum are covered with cilia
which beat in the direction of the oviducal ostia. These too
are abundantly ciliated, and as a result of the ciliary action
in both regions the eggs are soon carried to and into -the upper
ends of the oviducts. But by this time the first polar spindle
is already formed.

As the egg leaves the ovary the small group of chromatin
nucleoli becomes surrounded by a small spherical mass of
fibrillar plasma; the nucleoli become more or less fused and
vacuolated, and then give rise to the group of twelve small
rod-like chromosomes which soon become rings or crosses (Fig.
26, F). The fibrillar plasma draws out into the elongated
achromatic spindle, at first placed tangentially (Fig. 26, G), but
soon rotating and coming to the surface of the cell in the radial
position (Fig. 26, H). The spindle is quite blunt and no asters,
centrospheres, or centrosomes have been seen. The chro-
mosomes diverge as the egg is entering the oviduct, in the
upper part of which the very small first polar body is cut off
(Fig. 26,7).

The second polar spindle forms immediately, and by the
time the egg reaches the lower end of the oviduct the second
polar division has progressed as far as the mesophase or meta-
phase. In this condition the division is suspended, and pro-
ceeds considerably later and as a rule only after entrance of
the spermatozoon.

THE EARLY DEVELOPMENT OF THE FROG 77

Entrance of the eggs into the upper part of the oviduct
stimulates the jelly-secreting glands of its walls, and as the eggs
are carried along singly down the oviduct by the cilia of its
own walls, each is smeared over the surface of the chorion with
a thin coating of viscid albuminous material arranged in two
or three layers. About two hours are occupied in the passage
of an ovum down the duct. At the lower ends of the oviducts
the eggs collect in the uteri, where they remain stored, usually
for a day or two, pending the time of spawning.

3. Spermatogenesis

The formation and maturation of the spermatozoa is com-
pleted within the testes. Each lobule of the testis is composed
of a collection of tubules, in the walls of which the spermato-
gonia develop, surrounded by nutritive follicles the elements
of which become in part the basal cells or Sertoli cells. So
far as is known the formation of the spermatocytes and sper-
matids is fairly typical. The spermatid contains a large
nucleus and two peripheral centrioles. During the metamor-
phosis of the spermatid into the spermatozoon, the inner
centriole is taken into the nucleus while opposite the other the
flagellum grows out. The sphere of idioplasm remains on one
side of the anterior tip of the head, when this forms from the
nucleus, and a part of the cytoplasm flows down around the
base of the flagellum forming the middle piece; the remainder
of the cytoplasm appears to be thrown off.

In some species of Rana the sperm form continuously, in
others only seasonally, apparently just before hibernation
begins. As the breeding season approaches they are produced
more abundantly and collect in the dilated lower ends of the
vasa deferentia or seminal vesicles, ready for extrusion.

C. SPAWNING

In the more common species of Rana, spawning occurs
during the first warm days of early spring; some forms spawn

78 OUTLINES OF CHORDATE DEVELOPMENT

later in the spring, and in a few (e.g., R. catesbiana), breeding
occurs during early summer. In the first mentioned, spawning
follows immediately upon emergence from the period of hiber-
nation, when the frogs collect in small ponds or streams, or
about the margins of larger bodies of water. There is no true
copulation, the male merely seizing the female firmly around
the body dorsally, with the forelegs just behind those of the
female. This embrace or amplexus usually begins some hours,
even days, before the actual extrusion of the reproductive
products begins, and quite likely this affords the normal,
though not essential, stimulus to their discharge from the
ovaries and testes respectively. This amplexus continues
throughout the entire period of spawning of a single pair,
which may occupy several days or even weeks; the duration
depends upon the species and upon the temperature — colder
weather prolonging the period greatly.

Expulsion of the eggs usually occurs during the early morn-
ing hours and is an intermittent process. Apparently all the
eggs contained in the uteri are spawned at one time, and then
an interval of rest follows during which the uteri are again
slowly filled. As each mass of eggs is forced out of the cloaca
the male, at the same instant, expels quantities of seminal
fluid containing enormous numbers of spermatozoa which
mingle with the egg masses, insuring the fertilization of practi-
cally every egg. Fertilization is therefore strictly external.

In the common frogs there are no nursing habits so frequent
among other Anura (e.g., Alytes, Nototrema, Rhinoderma, etc.)
and the eggs are left to develop without further relation to the
parent organisms, which, upon the conclusion of spawning,
immediately leave the pools and scatter widely. The eggs
surrounded by the jellies remain in large masses which sink
to the bottow of the shallow water and there become loosely
attached to sticks or debris.

The total number of eggs laid by a single individual during
one season varies widely in different species, and seems to vary
conversely with the size of the eggs. The European grass-
frog (Rana temporaria) lays from one to two thousand large

THE EARLY DEVELOPMENT OF THE FROG 79

eggs (2-3 mm.), while the European water-frog (Rana escu-
knta) in which the eggs are small (1.5 mm.) lays from five to
ten thousand during each season.

III. EMBRYONIC PERIOD

A. FROM FERTILIZATION THROUGH GASTRULATION

1. Fertilization and the Development of the Symmetry of the Egg

During the first hour or two after the entrance of the sperm
several changes of great importance occur within the egg.
Although these are going on together and overlap to a certain
extent we shall have to describe them separately.

Entrance of the Spermatozoon. — Within a few moments after
ensemination, a sperm cell bores its way through the thin jelly
and the chorion, and enters the egg substance; in most cases
the entire spermatozoon enters. Although there is no micro-
pyle the sperm does not enter the egg at random, but normally
only in the pigmented hemisphere, more frequently about forty
degrees from the animal pole, and in any meridian (Brachet).
The meridian passing through both poles of the egg and the
point of entrance of the sperm is known as the fertilization
meridian.

Of course many sperm tend to enter the egg but the entrance
of the first seems to alter the chemical structure of the egg in
such a way that additional sperm are deterred from entering;
frequently many such sperm may be seen in the egg jelly.
Polyspermy, although not rare, is never normal in any of the
frogs, and should more than one sperm succeed in entering,
the development of the egg becomes abnormal.

Once within the egg substance the sperm head and middle
piece move rapidly inward, following approximately a radius
of the egg. The path of the sperm is marked by a distinct
trail of pigment, indicating unusual metabolic activity of the
region, which remains visible for some time, occasionally even
to the blastula stage. The first part of the sperm path is-
called the penetration path (Fig. 27, A, B). After the sperm
has travelled along this path for a short distance it rotates,

80 OUTLINES OF CHORDATE DEVELOPMENT

in the usual way, putting the middle piece with its centrosome
in advance of the head, which begins to dissolve and to form
a typical vesicular and enlarged nucleus. Then the sperm
changes its course, often abruptly, and moves toward the region
where the male and female nuclei will unite, unless, indeed,
the penetration path may have led in that direction (Fig. 27,

FIG. 27. — Sections through the egg of R. fusca, showing penetration and copu-
lation paths, and the symmetry of the first cleavage plane. After O. Schultze.

A. Sagittal section through the egg before the appearance of the first cleavage;

B. Frontal section of the same stage as A, showing the symmetrical distribution
of the egg materials. C. Frontal section through egg in two-cell stage, showing
the symmetry of the egg; the penetration path is not shown, a, Anterior;
cp, copulation path; I, left; p, posterior; pp, penetration path; r, right; s, remains
of first cleavage spindle; sp, superficial pigment; 1, first cleavage furrow.

A). This second part of the sperm path is known as the copu-
lation path and like the penetration path, it is marked by a
trail of pigment left in the cytoplasm.

Swelling of the Egg Membranes. — One result of the entrance
of the sperm is the withdrawal of fluid from the egg substance.
This fluid accumulates between the surface of the egg and the
chorion forming the perivitelline space. This leaves the egg free

THE EARLY DEVELOPMENT OF THE FROG

81

to rotate within its membranes, and in a few moments after
fertilization all the eggs are found with the pigmented pole
uppermost. In unfertilized eggs these membranes are more
adherent and while rotation occurs, it is very slow.

Probably some of the fluid in the perivitelline space is taken
in from the outside, for the egg membranes, particularly the
jelly, are extremely hydroscopic. The egg has been in the
water only one minute when the thin jelly has visibly com-
menced its absorption of water. When the eggs are extruded

FIG. 28. — Egg of frog a short time after laying and fertilization, showing the
swollen egg membranes. From Zieglec (Lehrbuch, etc.), after O. Schultze.
mb, The so-called vitelline membrane; p, pigmented penetration path of the
spermatozoon; r, polar bodies; 1, 2, 3, inner, middle and outer albumenous
membranes or layers of "jelly."

the thickness of the jelly is only about one-sixth the diameter
of the egg; after three minutes contact with the water this is
increased to one-half the diameter; and after ten to fifteen
minutes its thickness equals the diameter of the egg; The
swelling then becomes slower and unless fertilization has
occurred it may almost cease. Usually however the absorp-
tion of water continues for several hours and the thickness of
the jelly may equal twice the diameter of the egg proper.

As the jelly thickens it is seen to be arranged in definite
strata — a thin denser layer closely applied to the chorion, out-
side this a thick layer somewhat more fluid, and on the sur-

82 OUTLINES OF CHORDATE DEVELOPMENT

face a thick layer, rather firmer than the middle layer. The
two thick outer layers may, in some forms, be separate.d by a
narrow dense layer which is distinctly fibrous in structure
(Fig. 28).

The functions of the jelly are various. It serves to some
extent to attach the egg masses, but chiefly to protect the
eggs from pressure or mechanical injury, from being eaten by
other organisms, from infection of various kinds. It seems
likely, too, that the jelly assists in the elevation of the temper-
ature of the egg, for as a transparent sphere it condenses the
heat rays of sunlight which it allows to enter freely and at
the same time checks their radiation from the egg. The black
pigment of the upper pole seems to function toward the same
end by absorbing readily the heat rays, so that altogether the
temperature of the egg may be considerably higher than that
of the surrounding water. While the eggs, and the spermatozoa
also, are very resistant to cold, they are at the same time very
sensitive to warmth, so that this slight elevation of temperature
has the effect of hastening development — an effect that may
be quite important since the temperature of the water is often
quite low at the time the eggs are laid, and the ponds in which
the frogs spawn are quite likely to dry up during the summer,
so that each day gained in development toward metamorphosis
may mean much as regards survival.

Maturation. — Another effect of the entrance of the sperm is
the completion of the maturation process in the egg nucleus.
As the sperm enters, this is in the mesophase or metaphase of
the second polar division (Fig. 26, 7). This division is then
rapidly completed and the second polar body cut off; this
usually occurs about thirty minutes after entrance of the
sperm. The second polar body is of the same size as the first,
or smaller. The egg nucleus then reforms in the usual man-
ner. The polar bodies are only loosely attached to the sur-
face of the egg and frequently may be found floating in the
perivitelline space.

By the time the egg nucleus has reformed the sperm nucleus
Jias also become typical in form, and the two nuclei move

THE EARLY DEVELOPMENT OF THE FROG 83

toward the center of the egg, approach and meet in the usual
manner. The path of the egg nucleus is not marked by any
pigment, nor is it accompanied by any radiations such as were
connected with it during its maturation. The sperm centro-
some and centrosphere divide and form the poles of a small
but typical cleavage figure which is not located near the center
of the egg, but always toward the animal pole. The position
of the first cleavage spindle is not entirely undirected, but
before we can discuss this point we must consider some facts
regarding the structure of the egg itself after fertilization.

2. The Symmetry of the Egg

Before fertilization the egg has a well-marked polarity and is
radially symmetrical about its chief axis (Fig. 29, A). This
form of radial symmetry (not spherical) has been termed
11 rotatory," i.e., radially symmetrical in any plane at right
angles to the chief axis. The vegetal pole contains a large
proportion of yolk, while the animal pole is relatively free
from yolk and is covered externally by a thin but dense coating
of brown or black pigment; moreover, the nuclear structures
are hi the animal pole (Fig. 23, C). The specific gravity of
the lower pole is the greater, on account of the heavy yolk con-
tained in it, and therefore the pigmented animal pole is turned
upward when the egg is free to rotate. This rotation, however,
is not usually completed for some minutes after the spermato-
zoon has entered and the egg membranes are somewhat freed
from its surface.

But this radial or rotatory symmetry is not retained after the
entrance of the sperm, for this affords the stimulus which leads
to a rearrangement of the substance of the egg, accompanied
or followed by the rapid development of a bilateral symmetry
in the egg, with which that of the embryo tends strongly to
coincide. The factors determining the position of this new
plane of bilateral symmetry are really three-fold, one primary
and two secondary. The primary factor is the polar and
rotatory symmetry of the unimpregnated egg; the plane of

84 OUTLINES OF CHORDATE DEVELOPMENT

bilateral symmetry always passes through the chief egg axis.
The secondary factors then determine through what meridian
the plane will pass. One of the secondary factors is internal
and one external; the former is the point of entrance of the
spermatozoon together with the direction of its penetration
path, the latter is the direction of the action of gravity with
respect to the egg axis. These secondary factors alone cannot
direct the position of this plane, but each acts only in connec-
tion with the primary factor which is, in reality, the essential
structure or organization of the egg as expressed by its polarity
and rotatory symmetry.

We should recall that the sperm enters the upper pole in any
meridian (fertilization meridian) and that its penetration path
is first approximately radial, while the latter part of its path,
copulation path — along which it passes after the sperm head
has dissolved and become vesicular, may be at an angle with
the penetration path.

Immediately upon the entrance of the spermatozoon the
substance of the egg becomes more labile, and a sharper dif-
ferentiation and more pronounced segregation of the various
egg substances result. It is supposed that the influence of the
sperm is first exerted in the cytoplasm in its own immediate
neighborhood, and that the effects of its presence then spread
gradually to the more remote parts of the egg; and further,
that the influence of the sperm extends in a symmetrical wave
like those from a vibrating body. The result of this would
be that the rearrangement of the substances of the egg would
be symmetrical with reference to the point of origin of the
disturbance, namely, the sperm entrance point. Therefore the
plane of symmetry of the egg would be that plane containing
the three points: animal pole, vegetal pole, sperm entrance
point (Fig. 27, B). This would be at the same time the plane
containing the penetration path, and it would be marked
superficially as the fertilization meridian.

Whether or not this is a true description of the effects of the
sperm, the facts are that following impregnation there is a
streaming of the protoplasm upward and of the deutoplasm

THE EARLY DEVELOPMENT OF THE FROG

85

downward so that the animal pole is largely freed from yolk, the
vegetal pole composed more largely of it, and the polar dif-
ferentiation thus more marked than heretofore. The pigment
granules, whose specific gravity is really intermediate between
that of the yolk and of the protoplasm, show little disturbance
and redistribution except in one certain region. For some
reason which is not clear, the pigment granules located in a defi-
nite area at the lower margin of the pigmented pole, on the side

FIG. 29. — Frog's egg before and after fertilization, showing the formation of
the gray crescent. A. Unfertilized egg, from side. B. Unfertilized egg, from
vegetal pole. C. Fertilized egg before first cleavage, from side. D. Same from
vegetal pole, c, Gray crescent; p, pigmented animal pole; w, unpigmented
vegetal pole.

opposite that where the sperm has entered, and therefore in
the region presumably the last to be affected by the sperm, are
carried away from their original position leaving this region
lighter in color. This area is crescentic in outline, the crescent
extending one-half to two-thirds around the egg; it is known
as the gray crescent (Fig. 29) .

The rearrangement of substance which involves the forma-
tion of the gray crescent, is such that the center of the specif-
ically lighter substance of the egg is not located precisely in the
egg axis, toward the animal pole, but is displaced toward that

86 OUTLINES OF CHORDATE DEVELOPMENT

side on which the gray crescent appears, i.e., on the side of the
animal hemisphere farthest from the fertilization point. Nor-
mally this arrangement is sufficiently marked before the rota-
tion of the egg is completed, so that when the egg comes to a
position of rest the animal pole is not turned exactly upward.
In most species of frogs the egg axis is inclined out of the
vertical about thirty degrees; and of course at the same time
the margin of the pigmented area is similarly tilted out of the
horizontal and the gray crescent lies on that side which is the
higher (Fig. 29) . In the egg at rest, therefore, we may describe
a definite plane which is vertical and includes both the gravi-
tational and the polar axes; from the mode of determination
of the position of the gravitational axis this plane also includes
the fertilization point and meridian, and the penetration path.

While the egg is in this position the streaming and rearrange-
ment of its materials is completed, and since the specific gravity
of the different materials is concerned in. the rearrangement,
it takes place finally with reference to the direction of gravity
in the egg at rest. The final steps in the determination of
the structure of the unsegmented egg, therefore, take place
with reference to this gravitational plane, which thus becomes
the plane of bilateral symmetry of the egg structure. The
symmetry of the egg is expressed externally at this time only
by the gray crescent which is equally divided by the plane of
symmetry, but this is merely an indication of the really impor-
tant symmetry — that of the arrangement of the materials
within the egg, which is no longer rotatory about the egg axis,
but bilateral with reference to the gravitational plane.

The final development of the internal structure or organiza-
tion of the egg is completed (in Ranafusca) only shortly before
the first cleavage, or about an hour and a half after the
entrance of the sperm (Brachet). Before the end of the
first hour, the structure of the egg is gradually becoming
fixed and disturbances or artificial lesions are compensated, or
regulated, so that the final structure is not affected and later
development is not abnormal. But after this, by the time the
egg and sperm nuclei have fused, the egg structure becomes fixed

THE EARLY DEVELOPMENT OF THE FROG 87

and the egg is incapable of perfect regulation under abnormal
conditions imposed upon it, so that artificial lesions or other
disturbances result in abnormalities of its structure which lead
to abnormalities in cleavage or embryonic development.

To summarize, the bilateral symmetry of the egg is deter-
mined primarily by the polarity of the egg which has gradually
developed during its formation and maturation. How exten-
sive this essential bipolar structure is, we do not know, but it
is expressed visibly, and probably only in part, by the polar
arrangement of at least three different substances having dif-
ferent specific densities — protoplasm, pigment, deutoplasm.
Probably the arrangement of these is itself determined by
some fundamental structure of the egg, but this we cannot
observe directly. The bilateral symmetry is here only poten-
tial. It becomes actual only after ensemination when these
substances are rearranged, first under the influence of the en-
tering spermatozoon, which brings about the non-correspond-
ence of the egg axis and gravitational axis, and then through
the influence of gravity according to the plane fixed by these
two crossing axes. In other words the bilateral symmetry is
first determined by the egg structure as expressed through its
polar differentiation and then through that as the result of the
action of the entering spermatozoon and gravity, which latter
is able to act finally only after the entrance of the sperm.

The penetration path of the sperm is usually in the direction
of a radius of the egg from the entrance point, so that this
portion of the sperm path tends to lie in the plane of symmetry
to the same extent as, or even to a greater extent than the
entrance point itself, and it may be that we should express
the relation more truthfully by saying that the plane of sym-
metry tends to be directed first by the location of the pene-
tration path rather than the fertilization point, since the influ-
ence of the sperm is exerted as it passes all the way along this
portion of its course.

By placing the eggs under artificial conditions it has been
found that the action of both these secondary factors is not
essential, for normal development proceeds even when the di-

88 OUTLINES OF CHORDATE DEVELOPMENT

rective effect of gravity is removed; it is not known, however,
what the relation of the plane of symmetry to the fertilization
point is under such conditions. And further, by placing the eggs
in positions of constraint such that the sperm entrance point
cannot lie in the median gravitational plane, it is found that
the plane of symmetry is then that of the median gravitational
plane. The secondary factors may thus be independent in
their action, but in nature they usually tend to produce the
same effect. However, in nature, and this also indicates their
fundamental independence, there is some deviation between the
plane of symmetry and either the fertilization meridian or the
gravitational plane. The eggs in the interior of the mass are
subject to some constraint due to pressure, and unknown
factors may cause some variability in the effects of the factors
named in the determination of symmetry. It is possible that
the direction of the incident light (heat) rays plays some small
part in the determination of the position of this plane. So
that while the normal relation is that of coincidence of all
these, all other relations are possible (the plane symmetry of
course is always polar) and do occur with some frequency, and
all that can be said is, that on the whole the median plane of
the egg tends to coincide with the gravitational plane and with
the fertilization meridian.

One of the reasons why the position of the plane of symmetry
of the egg is of the greatest importance is that the plane of
bilateral symmetry of the embryo and adult is directly related
to it. Any factor which aids in the determination of the egg
symmetry is at the same time influencing the symmetry of the
developing embryo. By observing,, in a large number of speci-
mens, the relation between the symmetry of the egg and of the
embryo it is found that the tendency for the two to correspond
is very marked. And yet variations of any extent may and
do occur, showing that other factors may influence and devel-
opment of the embryo (Jenkinson). The symmetry of the
embryo and adult can be traced directly back into the gastrula
or blastula, and it seems, therefore, that whatever causes the
non-correspondence between these symmetries must operate

THE EARLY DEVELOPMENT OF THE FROG 89

during cleavage and not later, although there seems to be no
definite causal relation between the direction of the first cleav-
age plane itself and the symmetry of the embryo, although
there may be certain constancies in this relation.

We may finally mention briefly the relation between the
symmetry of the egg (and therefore in general of the embryo)
and the symmetry of cleavage, particularly the plane of the
first cleavage furrow. The position of the cleavage plane is of
course the direct result of the position of the cleavage spindle;
it is therefore the position of this latter which is essential. The
spindle always lies at right angles to the egg axis, in agreement
with the law of Hertwig. In such a plane the position of the
spindle is readily influenced by at least one external factor,
namely pressure, in such a way that it tends to lie at right
angles to the direction of the pressure, and the resulting cleav-
age would therefore occur in the direction of the pressure. In
a large mass of eggs this factor is probably one of considerable
importance, especially in affecting the direction of the first
cleavage in those eggs in the interior of the mass. The relation
between the direction of pressure and the symmetry of the egg
is purely accidental and consequently we find much variation
in the relation of these two planes.

When the egg is not subject to pressure there is a fairly
marked tendency for the spindle to lie either transversely to
the plane of symmetry or in that plane (Fig. 27, C). The
symmetrical structure of the egg is fairly well established by
the time the spindle forms, and there are only these two
positions which the spindle can occupy and yet retain sym-
metrical relations to the internal structure of the egg. The
former relation, in which the plane of the resulting cleavage
would coincide with the plane of egg symmetry, is the more
frequent and in approximately 25 per cent, of eggs the first
furrow deviates less than five degrees, plus or minus, from this
plane. The second relation, placing the first furrow at right
angles to the median plane (within five degrees, plus or minus)
is found in something like 10 per cent, of eggs (Jenkinson).

But the position of the spindle seems to be influenced quite

90 OUTLINES OF CHORDATE DEVELOPMENT

considerably by the direction of the copulation path of the
sperm nucleus, i.e., the direction of the plane passing through
the contact surface of the copulating egg and sperm nuclei,
and since this is subject to much variation with respect to the
median plane, and also since the postion of the spindle is easily
modified by external factors, we find that the relation between
the first cleavage and the median plane of the egg is not at
all regular, and deviations from the two relations mentioned
are very frequent and all relations occur. There is no direct
relation between the plane of the first furrow and the fertili-
zation meridian; whatever relation there is results from their
common relation to the plane of egg symmetry.

We may summarize briefly the relations of the plane of sym-
metry of the egg, the plane of symmetry of the embryo, and
the plane of the first cleavage furrow, in normally developing
eggs.

The position of the plane of bilateral symmetry of the egg is
determined primarily by the polarity and rotatory symmetry
of the unfertilized egg, in conjunction with the point of entrance
of the sperm or the direction of the penetration path, and the
direction of the action of gravity, in such a way that the
median plane tends to lie in the gravitation plane, which also
tends to coincide with the fertilization meridian. This determi-
nation, however, is not complete and variations may and do
occur.

The median plane of the bilaterally symmetrical embryo
tends to a marked degree to coincide with the plane of symmetry
of the fertilized egg, but all other relations in the same axis
are possible and actually occur.

The plane of the first cleavage furrow tends to lie either in
or at right angles to the plane of symmetry of the egg, primarily
on account of the tendency of the first cleavage spindle to
assume some symmetrical position with reference to the egg
structure.

There is, therefore, a tendency for the gravitational plane, the
point of entrance of the spermatozoon, the penetration path of
the spermatozoon, the median plane of the egg, the median

THE E1RLY DEVELOPMENT OF THE FROG 91

plane of the embryo, and the plane of the first cleavage furrow,
all to coincide, but all relations in the same axial plane are
possible among these and are actually found.

3. Cleavage

Cleavage of the frog's egg is total and unequal. The first
cleavage spindle lies in the direction of the greatest protoplasmic
extent, i.e., transversely to the egg axis, and in a position
determined by several different factors as described above (Fig.
27, C) . The first cleavage furrow becomes visible on the surface
first at the animal pole, and gradually extends thence as a
narrow groove around a meridian of the egg to the vegetal pole;
it is completed about two and one-half hours after ensemination,
or much sooner if the temperature is raised slightly. While this
furrow is meridional, we have seen that it may or may not
divide the gray crescent symmetrically. Throughout cleav-
age the blastomeres remain in close contact so that they are
separated superficially by only shallow narrow grooves (Fig. 30),
and do not become distinctly rounded and separate elements
as in Amphioxus or in other eggs containing less yolk.

The second cleavage appears about one hour after the first;
this is also meridional, at right angles to the first, dividing
the egg into four adequal blastomeres. Succeeding divisions
appear about an hour apart. The third cleavage is the first
to divide the egg unequally; in the typical form of cleavage
this appears similarly in all four quadrants, and is latitudinal
or horizontal, i.e., at right angles to the first two (Fig. 30, A).
Although this cleavage plane divides the protoplasmic material
of the egg about equally, the accumulation of yolk in the lower
pole actually displaces this middle plane above the equator of
the egg, so that the cleavage furrow appears about sixty
degrees from the animal pole, and the egg as a whole is divided
unequally. Of the eight resulting cells, the four upper are
small and richer in protoplasm, while the four lower are large
and richer in yolk. This typical relation of the third cleavage
is by no means invariable. A considerable proportion, in

92 OUTLINES OF CHORDATE DEVELOPMENT

some lots nearly one-half, of the eggs show some departure
from this arrangement, and the third cleavage may be horizon-
tal in only one, two, or three blastomeres, and vertical in the
remainder or, rarely, vertical in all four. These and also the
later vertical planes frequently do not pass actually to the upper
pole of the egg, and are therefore not strictly meridional,

FIG. 30. — Cleavage of the frog's egg. After Morgan. Animal pole upward
in all figures. (For earlier stages see Fig. 27.) A. Eight cells. B. Twelve cells
becoming sixteen. C. Thirty-two cells. D. Forty-eight cells, more regular than
usual. E, F. Posterior and anterior views of about 128 cell stage. G. Late
cleavage or early blastula. H. Commencement of gastrulation (cell outlines
indicated only in the region below the invaginating groove), i, Beginning of
invagination.

although there is a decided tendency for them to lie in me-
ridians. The location of the succeeding cleavages varies with
that of the third. Typically the fourth cleavages (Fig. 30, B)
are meridional forming eight small upper, and eight large lower
cells, and the fifth again latitudinal, forming thirty-two cells
arranged in four horizontal rows of eight cells each (Fig. 30, C).
But the atypical appearance of some of the third cleavages may
very early disturb this schema. With the appearance of the

THE EARLY DEVELOPMENT OF THE FROG 93

fifth cleavage the early, and brief, synchronism of the cleavages
has become lost, the small upper cells dividing more rapidly
than the large lower cells. Comparatively few eggs remain
regular up to this stage, for eggs which were regular at eight
cells usually become irregular at sixteen or thirty-two cells, and
after that all regularity is lost (Fig. 30).

Turning back now to notice some of the internal arrangements
of the cells during cleavage, we find that when four cells are
cut into eight these all round off somewhat internally, as in
Amphioxus, forming a small space among them, which is the
beginning of the segmentation cavity or Uastoccel, and which
from the position of the third cleavage has from the first an
eccentric position toward the animal pole. During subse-
quent cleavages the blastoccel enlarges but always retains this
eccentric location (Fig. 31, A).

After about thirty-two cells are formed not all of the sub-
sequent cleavages are visible on the surface, for these early
divisions, all passing through the axis of the egg, have formed
cells elongated in a radial direction, and in some of these the
cleavage spindles tend to take up a similar position* and the
resulting division occurs parallel with the surface of the mass,
forming a central cell bordering the segmentation cavity and
a superficial cell visible externally (Fig. 31, B). There is no
period at which such a delaminating cleavage occurs through-
out the cell group, but scattered cells show this arrangement,
first among the cells of the upper hemisphere and then later
in the lower cells, which are divided quite unequally in this
way. Many of these interior cells are formed by cleavages
that are not exactly tangential but considerably oblique to the
surface. By the time there are sixty-four or one hundred and
twenty-eight cells, approximately one-fourth of the cells are
interior, and line the blastocoel, so that at this stage the wall
of the blastocoel is two or more cells thick.

4. The Blastula

We may assume that the arrangement of the cells forming the
wall of the blastocoel as a more or less definite epithelium,

94 OUTLINES OF CHORDATE DEVELOPMENT

marks the end of the cleavage period and the formation of the
blastula. This arrangement is really definitely established
by the time thirty-two to sixty-four cells are formed, i.e., be-
fore many interior cells are present. The immediately sub-

Fio. 31. — Sections through the blastula of the frog. A, B, from Morgan
(Development of the Frog's Egg). C. After O. Schultze. A. Early blastula
showing wall of segmentation cavity only one cell in thickness. B. Later stage
showing multiplication of cells in wall of segmentation cavity. C. Late blastula
showing the thinning of the roof of the segmentation cavity and the beginning
of the germ ring, a, Animal pole; gr, germ ring; p, pigment; s, segmentation
cavity or blastocoel; SG, Same as s; v., vegetal pole.

sequent cleavages do not modify their essential relations; the
interior cells multiply rapidly and some cells migrate inward
from the surface. The early blastula is spherical and about
the diameter of the egg (Fig. 31, J3, C). The thinner roof and
lateral walls of the eccentric segmentation cavity, are formed

THE EARLY DEVELOPMENT OF THE FROG 95

of cells derived from the animal region of the egg; these vary
considerably in size and form, are irregularly and loosely ar-
ranged, and are roughly disposed in two sheets, one lining the
blastocoel and one covering the surface. The thicker floor
of the blastocoel is formed of the larger and less numerous
vegetative cells. As the number of cells continues to increase
several processes go on together. The small cells of the animal
region divide the more rapidly and as they multiply they move
gradually from the pole toward the equator, causing a thinning
of the roof and a thickening of the walls of the blastocoel.
This thickening toward the equator of the blastula is aug-
mented by the rapid multiplication of cells there so that sec-
tions soon show a thicker ring, not very definitely delimited,
of actively dividing cells forming what we may call the germ
ring or growth zone, such as that described in the blastula and
gastrula of Amphioxus (Fig. 31, C). This thinning of the
animal pole increases the eccentricity of the blastoccel, which
has meanwhile increased considerably in size. The later
blastula increases somewhat in diameter, and accompanying
this is the absorption or infiltration of water into the blastoccel,
a part of the fluid content of which is, however, the secretion
of its walls.

The germ ring is obviously formed of material from the
animal pole of the egg, and apparently the substance con-
tained in it can be distinguished at least as early as the eight
cell stage, where it forms the upper quartet (micromeres) and
the upper parts only of the lower quartet (macromeres) (Fig.
34). As the germ ring approaches the equator, one side (that
of the gray crescent) commences to extend downward faster
than the remainder; subsequent development proves this to
be the posterior side. Soon the entire germ ring passes the
equator, and by the time the blastula period is ended, it
reaches, on the posterior side, a point about half way between
the equator and the lower pole. These later phases in the
downward movement of the animal cells can be observed
externally, for these cells are easily distinguishable from the
true lower pole cells on account of their dense pigmentation-

96 OUTLINES OF CHORDATE DEVELOPMENT

Since the blastula retains its spherical form it is evident
that the downward extension of the germ ring must displace
the yolk cells in some direction, and as a matter of fact this
displacement is evidenced by the elevation of the floor of the
blastocoel. As the animal cells push downward the internal
yolk cells rise till the floor of the blastocoel becomes first flat,
and then convexly arched; at the same time the cavity widens
somewhat so that in section it appears broadly crescentic
(Fig. 32, A, B).

The first evidences of gastrulation now appear so that this
stage must be taken to mark the completion of the blastula.
We may state the characteristics of the fully developed blastula
as follows. The completed blastula is spherical, in volume
about one-fifth larger than the ovum, and bilaterally symmet-
rical; this bilaterality is accompanied by antero-posterior
differentiation, and is indicated by the greater thickness of
the anterior wall of the segmentation cavity, and by the more
ventral extension of the pigmented cells on the posterior side,
i.e., the side marked by the gray crescent in the egg. The
small cells of the upper pole form the thin roof and thicker
sides of the eccentric blastocoel; they are in two quite distinct
sheets — an outer layer of compactly arranged cells forming a
distinct epithelium known as the superficial or epidermal layer,
and, lining the blastocoel, a deeper or "nervous" layer of
irregularly and loosely arranged cells, gradually increasing in
thickness from the pole toward the base of the blastoccelic wall,
about at the level of the equator of the blastula. Just at and
below the equator actively dividing cells have accumulated
from the whole upper pole region. Since the fate of these
cells is to form the chief axial parts of the embryo this region
is called the germ ring, although it lacks the distinctness of the
germ ring as it is finally found in some other forms (e.g.,
Teleosts). This region seems comparable with a crescentic
group of actively dividing cells having a corresponding position
and function in the blastula of Amphioxus (Fig. 6). The floor
of the blastocoel is formed of the larger vegetative cells which
form practically the lower half of the blastula; these are com-

THE EARLY DEVELOPMENT OF THE FROG 97

pacted and show no definite arrangement, except that toward
the lower pole they gradually increase in size. Although some
yolk is contained in all the cells, the larger lower pole cells
are particularly rich in deutoplasm and are known as the yolk
cells. Immediately below the germ ring the cells are inter-
mediate in character and form what is known as the transitional
zone. The position of the polar axis in the blastula, with
respect to gravity, remains the same as in the egg or the cleav-
age period.

The pigment, while chiefly superficial and in the cells de-
rived from the animal pole, externally extends further toward
the lower pole than in the egg; it is also found to a limited
extent among the animal cells below the surface, and even in
the smaller vegetal cells lining the blastoccel, which resemble
closely the proper cells of the animal pole. This internal
pigment is not derived from that more superficially located
in the earlier stages, but it is deposited in situ as a by- or end-
product of metabolism. Pigment granules are laid down
wherever developmental processes, including cell division, are
in rapid progress. And since the smaller cells represent re-
gions where cell multiplication has been more active, such
cells contain relatively more pigment. This relation between
metabolic activity and the accumulation of pigment may
explain the pigmentation of the animal pole of the egg itself,
although it is customary to refer this to the adaptational
relation mentioned previously, a relation which need not be
negatived by this method of its formation. The dense pig-
mentation of the path of the sperm is also referable to an un-
usual degree of metabolic activity.

The blastula of the frog differs from that of Amphioxus
chiefly in that the blastocoel of the former is so decidedly eccen-
tric, relatively smaller, and its wall several cells thick, the
cells differing greatly in size, and already differentiated into
superficial and deeper layers, at least in the animal region.
The germ ring (growth zone in Amphioxus) extends completely
around the blastula of the frog. These differences for the most
part seem to be the direct results of the abundance of yolk in

98 OUTLINES OF CHORDATE DEVELOPMENT

F

FIG. 32. — Median sagittal sections through a series of gastrulas of the frog
(R. temporaria). After Brachet. The figures illustrate the change in position

THE EARLY DEVELOPMENT OF THE FROG 99

the frog egg, and its accumulation chiefly in one region. The
effect of the yolk in modifying the course of development be-
comes more marked in the immediately succeeding phases of
development, namely gastrulation and notogenesis; these
processes are not at all as simple and diagrammatic as in
Amphioxus.

5. Gastrulation and Notogenesis

The processes of gastrulation proper and of notogenesis
overlap to a more considerable extent in the frog, than in
Amphioxus, and are conveniently described together. Gas-
trulation results directly from a continuation of the downward
extension of the germ ring, together with the consequent
elevation of the yolk cells, which were such important features
in the development of the late blastula.

The first external indication of gastrulation is the appearance
of a slight irregular groove, approximately horizontal, lying
across the sagittal plane on the posterior side of the egg, just
at the lower margin of the germ ring, i.e., just below the
equator (Figs. 32, 35, A). Thus located, the groove lies just
between the animal cells and the yolk cells, and therefore
comes to be lined by both kinds of cells on its opposite faces.
From subsequent development we know that the formation
of this groove is the beginning of invagination, the groove
itself the beginning of the archenteron, its upper margin the
rim of the blastopore, and the cells lining it above and below,

of the whole gastrula, as well as the phenomena of gastrulation proper. A. Com-
mencement of gastrulation; earliest appearance of the dorsal lip of the blasto-
pore. Internally the gastrular cleavage is indicated. B. Invagination more
pronounced; beginning of epiboly. C. Invagination, epiboly and involution in
progress. The gastrular cleavage is now indicated on the side opposite the
blastopore. Rotation of the gastrula. D. Just before the ventral lip of the
'blastopore reaches the median line. The indentation of the wall of the segmen-
tation cavity is an artifact. E. Blastopore circular and filled with yolk plug.
Gastrula beginning to rotate back to its original position. Peristomial mesoderm
differentiating. F. Segmentation cavity nearly obliterated. Neural plate estab-
lished. G. Gastrulation completed, a, Archenteron; 6, blastopore; c, rudiment of
notochord; ec, ectoderm; en, endoderm; gc, gastrular cleavage; ge, gut endoderm;
m, peristomial mesoderm; np, neural plate; nt, transverse neural ridge;
s, segmentation cavity or blastoccel.

100 OUTLINES OF CHORDATE DEVELOPMENT

ectoderm and endoderm respectively. Hemisection of this
very early gastrula (Fig. 32, A), shows that the elevation of
the floor of the blastoccel is very rapid at this time, and one
of the first results of the arching up of the yolk cells (endoderm)
is the formation of a narrow groove all around the margin of
the blastocoel, between the base of its wall and its rising floor.
As the yolk continues to rise, this groove soon becomes quite
marked and compressed into a narrow slit which, though
originating in the manner just described, seems to be continued
ventrally all around the central cells as a definite splitting or
delamination (Fig. 33, A). In effect this narrow space sepa-
rates definitely the ectoderm and endoderm in the region
within (above) the restricted invaginating region, which of
course also gives rise to an ectodermal and an endodermal
layer. This original groove is called the gastrular groove,
and the delamination which extends it is the gastrular cleavage;
the formation of these is not limited to the region of the dorsal
lip of the blastopore, but extends entirely around the gastrula,
even to the side opposite that of invagination. It remains a
question whether the invagination process is the result of an
active inturning of the cells forming the lower margin of the
germ ring, or whether these cells are rather pulled inward by
the elevation of the yolk cells, which results from the com-
pression produced by the thickening and downgrowing germ
ring; perhaps both factors are involved. However this may be,
the invagination once begun continues rapidly, so that an
elongating tongue of inturned cells continually pushes up
under the superficial ectoderm which lies just above the
invaginating region. This tongue is the invaginated endoderm
derived from some of the cells of the animal pole and their
descendants; at its inner limit it becomes directly continuous
with the endoderm formed directly from the yolk cells, or
cells of the transitional zone which have become entitled to
the name endoderm, while still practically in situ, by the
appearance of the gastrular groove and cleavage.

Turning for a moment to the consideration of the external
modifications during gastrulation we see that the germ ring,

THE EARLY DEVELOPMENT OF THE FROG TO!

once having passed the equator begins to* rlarrow :as a 'whole
(i.e., diametrically), and this is chiefly accomplished by the
drawing in of its lateral regions toward the mid-line posteriorly.
This, together with the very active multiplication of its con-
stituent cells, causes this portion to push down more rapidly
than the remainder, carrying along the layer of invaginating
endoderm, and increasing considerably the vertical extent of
the archenteron. Surface views show that at the same time
the archenteric groove extends laterally, becoming first cres-
centic, then semicircular and finally circular (Fig. 35). That
is to say, the first invagination of the pigmented cells forms the
dorsal lip of the blast opore; then the invagination gradually
extends laterally in each direction forming the lateral lips of
the blast opore; and finally the process of invagination is carried
around to the side of the gastrula, almost diametrically oppo-
site to that where it began, and forms there the ventral lip of
the blastopore, and the circular blastoporal margin is thus
completed. During the completion of the blastoporal rim the
germ ring has continued to extend downward over the yolk on
all sides, so that by the time the rim is completed by the forma-
tion of the ventral lip, this is found at a level quite below that
at which invagination began on the dorsal side (Fig. 35). The
invagination involves the mturning of the cells transitional
between the animal and vegetal poles, so that the cells of the
pigmented and white areas are brought into sharp contrast.
The circle of white yolk cells left within the blastoporal rim is
called the yolk plug (Figs. 22, B; 32, E, F; 33, C). As the rim
draws together, i.e., as the blastopore closes, the yolk plug
appears gradually to diminish in size, while it really draws
within, or some would say that it is pushed within, by the over-
growing lips of the blastopore, until finally it is no longer visible
upon the surface (Fig. 38, B). The blastoporal opening then
remains as a narrow elongated slit leading directly into the
archenteron.

The precise way in which the germ ring narrows, or as we
might say, in which the blastopore closes, is a matter of some
importance. It has already been stated that the dorsal lip

102' OUTLINES OF CHORDATE DEVELOPMENT

.6

E

FIG. 33. — Frontal and transverse sections through gastrulas of the frog
(R. temporarid) of various ages. After Brachet. A. Frontal section through
gastrula of same age as Fig. 32, C. B. Frontal section through gastrula of
same age as Fig. 32, D. C. Frontal section through gastrula slightly older than
Fig. 32, F. D. Frontal section through gastrula of same age as Fig. 32, G.
E. Transverse section through gastrula slightly older than Fig. 32, D. F. Trans-
verse section through gastrula slightly older than Fig. 32, G. a, Archenteron;
b, blastopore; c, notochord; ge, gut endoderm; w, peristomial mesoderm; np,
neural plate; s, segmentation cavity or blastoccel.

THE EARLY DEVELOPMENT OF THE FROG 103

grows downward more rapidly than the remainder, due in part
to the inflowing of the lateral portions toward the mid-line.
This process is termed concrescence, or confluence, as in Amphi-
oxus. In this way the materials found in the lateral, as well
as posterior, regions of the germ ring are drawn to the median
region, and as the ring there extends backward or downward,
a thick median strand of tissue is left, from which are developed
later, when the embryo begins to form, the rudiments of many
of the important axial organs. The downward progress of the
lateral and ventral margins of the blastopore is quite slow
comparatively, so that the closure seems to occur mainly to-
ward the lower pole of the gastrula. That is, as the diameter
of the circular blastopore diminishes, its center, which is the
center of the yolk plug, moves toward the lower pole and may
finally reach this or even pass beyond it a short distance up on
the opposite side. The form of the blastopore changes mark-
edly during the later phases of its closure. The final rapid
approach of the lateral margins alters its outline from a circle,
so that it becomes ovoid and finally quite elongated and slit-
like, in the direction of the sagittal plane of the gastrula
(Figs. 35, 38, A). But before this occurs the blastopore is
carried back near its point of origin by the rotation of the whole
gastrula to be described shortly.

Sections through the gastrula during this period of closure of
the blastopore show that many important processes are going
on internally. Continuing from the stage described, where the
archenteron had become a curved crevasse putting the invagi-
nated and delaminated endoderm of its outer wall into connec-
tion, we find that the essential process of gastrulation is con-
tinued chiefly by the rising of the yolk cells from the floor of the
blastocoel in advance of the archenteron, so that the inner
limit of this cavity is carried upward under the animal pole
and then beyond, toward the side of the gastrula opposite that
of the first appearance of the archenteron (Fig. 32, C-F). The
yolk cells at the same time are carried around the front of the
advancing archenteron and form the outer wall of the primary
gut cavity. This rearrangement of the yolk cells, involving

104 OUTLINES OF CHORDATE DEVELOPMENT

their elevation in the dorsal or postero-dorsal region, draws
away the yolk cells from beneath the original segmentation
cavity so that as the archenteron advances the segmentation
cavity recedes. Meanwhile the archenteron enlarges over the
whole animal region and actually encroaches upon the blasto-

FIG. 34. — Diagrams of median sagittal sections through the frog's cleavage
and gastrula stages, showing the changes in position during gastrulation. From
Ziegler (Lehrbuch, etc.), after Kopsch. The arrow marks the vertical. (Accord-
ing to Morgan and others the figures of the first two stages should be rotated
about 15° in the counter-clockwise direction.)

coel, so that as the latter moves toward the anterior side of the
gastrula it diminishes in size and soon disappears (Figs. 32, 33).
In some cases the wall of yolk cells separating the archenteron
and blastoccel becomes thin and breaks through, before the
blastoccel has completely disappeared; in this case the remnant

THE EARLY DEVELOPMENT OF THE FROG 105

of the blastocoel is added to the archenteron and the endodermal
wall is completed by growth of the portion already formed.

The formation of the archenteric cavity in a region formerly
occupied by yolk cells, and the gradual enlargement and shift-
ing of this cavity as well as of the blastocoel, obviously alter the
position of the center of gravity of the gastrula as a whole, and
the extensive changes in the relative positions of yolk and
protoplasmic cells, whose specific gravities are unlike, contrib-
ute to the same alteration. This all results in a rotation of
the gastrula about a horizontal transverse axis (Fig. 34).
During the early phases of gastrulation, as just described, the
more rapid growth of the dorsal (posterior) lip of the blasto-

FIG. 35. — Diagrams of the frog's gastrula showing the position of the blasto-
pore at various ages. A. Posterior view. B. Lateral view. 1-5 indicate the
successive positions and forms of the blastopore. The change in position is due
both to the actual growth movements of the blastopore, and to the rotation of
the entire gastrula. Compare Figs. 32, 34.

pore carries this to or even past the lower pole of the gastrula,
even past the lower gravitational pole. Then as the blastopore
continues to narrow, the whole gastrula rotates slowly in the
opposite direction, carrying the blastopore back to the region
where the dorsal lip first appeared and then on dorsally some-
what above the equator, into a postero-dorsal position, where
it remains stationary for a time. Thus the shifting of the blas-
topore is the combined result of changes due to growth and to
rotation. On account of the localization of the growth processes
in the gastrula, which will be described presently, there is not
a complete correspondence between the chief axis of the bias-

106 OUTLINES OF CHORDATE DEVELOPMENT

tula or early gastrula and any single straight axis of the later
gastrula.

The description of gastrulation from observation of median
sagittal sections or hemisections does not give a complete idea of
this process. We may return now to a consideration of some of
the processes going on in the lateral parts of the gastrula. As
the dorsal lip of the blast opore becomes crescentic, the deepen-
ing archenteron pushes laterally around through the mass of
yolk cells (Fig. 33, B, C, D). But these have already become
separated from the ectoderm by the gastrular groove and cleav-
age, except only in the region of the lower pole just anterior to
the place where the anterior (ventral) lip of the blastopore will
form. So that by the time the blastoporal lip becomes circular,
i.e., by the time the ventral lip forms, this region has already
been divided into ectoderm and endoderm, and therefore the ex-
tent of invagination at the ventral lip is greatly limited. The
important result of this is that the actually invaginated endo-
derm is confined to a broad tongue of cells on the dorsal side
(roof of the archenteron) and a ring-like strip extending around
within the blastopore lip from the base of this tongue, nar-
rowing rapidly toward the ventral side. The archenteron itself
is at first a narrow slit, crescentic in cross section, but as it
grows up to the animal pole and enlarges, it grows farther lat-
erally so as to extend in a wide crescent (in transverse section)
about to the level of the equator of the gastrula (Fig. 33, E, F).
This leaves the yolk cells as a convex mass projecting into
the archenteron from its floor.

The frog illustrates very well the way in which the process of
gastrulation proper is complicated, in the Chordata, by the early
formation of certain of the important axial organs which are the
chief characteristics of the Chordate group; the formation of the
rudiments of these structures is termed notogenesis. Gastrula-
tion proper includes only those processes by which the single-
layered (monodermic) blastula is converted into the two-layered
(didermic) organism, with definitely established ectoderm and
endoderm — the gastrula. The method by which this is accom-
plished may vary in different groups of Chordates; in Amphi-

THE EARLY DEVELOPMENT OF THE FROG 107

oxus, we have seen, invagination is the chief process, while in
the frog this is less important, and the endoderm is more largely
the result of delamination or of a simple rearrangement of cells
forming different parts of the wall of the blastula. Among the
higher Chordates invagination may be entirely lacking and gas-
trulation may be entirely accomplished by other methods (in-
volution, epiboly, delamination). As a matter of fact, even in
the frog, invagination is concerned less with the formation of the
inner layer than with the establishment of the notochord and the
formation of the rudiment which gives rise hi part to the meso-
derm. It becomes necessary, therefore, to distinguish sharply
between gastrulation and notogenesis. In the frog the strictly
two-layered condition exists for a very brief period only, for the
earliest phases of notogenesis, namely the formation of the meso-
derm and chorda, occur quite precociously. The early forma-
tion of these structures may more conveniently be described
together, and for the first stages we must return to the early
gastrula.

6. The Mesoderm

In order to understand the origin of the mesoderm we must
examine the early gastrula at the time the gastrular groove and
cleavage extend down toward the incipient blastopore. Here
the inner region of the germ ring and the yolk cells lining the
blastocoel are continuous, and it is here that we find those cells
which are later to form the mesoderm, and although distin-
guishable at this time, they are not definitely delimited within
this zone which is transitional between the ectoderm and endo-
derm. On one side these cells are continuous with ectoderm
cells, on the other with endoderm or yolk cells (Figs. 32, A; 33, A).
As the lips of the blastopore extend laterally this mesoderm
rudiment forms pari passu, and when the blastopore rim becomes
circular the mesoderm rudiment can be distinguished in the
ventral lip (Figs. 32, F; 33, C) . We may say then that the rudi-
ment of the mesoderm appears first as a ring of cells just within
the margin of the blastopore. But by the time the ring is com-

108 OUTLINES OF CHORDATE DEVELOPMENT

pleted ventrally, its dorsal region, in the more rapidly develop-
ing dorsal lip, has broadened considerably so that its general
form might be compared with a signet ring.

As the blastopore is completed and begins to close, the con-
fluence of its lateral margins transports masses of the cells
toward the mid-line, and leaves them as a broad median band
extending upward from the dorsal lip of the blastopore. As a
result of the multiplication of these cells, and of the downward
extension of this lip, a considerable axial thickening is formed.
And at the same time the extension of the archenteron carries
the yolk cells, with which the mesoderm is closely related on one
side, upward toward the animal pole, so that altogether, even
in these comparatively early stages, the extent of the mesoderm
is nearly as great as that of the endoderm. And soon the meso-
derm is definitely delimited from the endoderm by a rearrange-
ment of cells giving the appearance of an irregular delamination
(Fig. 33, D). This delamination commences in the dorso-
lateral regions either side of the thickened axial mass and gradu-
ally extends thence anteriorly and laterally around the sides of
the archenteron separating a thin layer of definitive endoderm
walling the gut cavity, and a much thicker mass of mesoderm
between this and the superficial ectoderm (Fig. 44). In the
region of the lower pole of the gastrula, under the thickest mass
of yolk, the delamination comes to the surface of the yolk mass
forming a free circular margin of mesoderm. From this free
margin cells and groups of cells break or bud off passing farther
ventrally, and finally reaching the lower pole, completing thus
a fairly continuous layer between ectoderm and endoderm
(yolk) (Figs. 44, 61, 63). In the region of the dorsal axial
mass, particularly in the region of the blastopore, the de-
lamination is delayed and its course somewhat modified. In
these regions the cells concerned in mesoderm formation have
very different relations from the remainder, since throughout
they are the derivatives of cells which have been invaginated
from the outer layer. And here too the development of the
notochord complicates the matter somewhat.

Sections cut transversely through the blastopore and the

THE EARLY DEVELOPMENT OF THE FROG 109

region just in front of it, show that the rudiments of the chorda,
mesoderm, and dorsal endoderm are for a time not distinguish-
able (Fig. 33, E). Sections through the narrowed blastopore,
while it is still filled with the yolk plug, show that the rim of the
blastopore is composed of a thick undifferentiated mass of cells,
representing a part of the contracted germ ring. Farther
laterally the ectoderm is separated by a line or narrow space
which is formed in gastrulation ; the thin endoderm is separated
from the middle layer by a line or space which results from
delamination as described above. In front of the blastopore,
in the region formed by confluence, the arrangement of the
cells and germ layers is much the same, except that they are not
interrupted in the mid-line. The pigmentation of the inner
surface of the mass is an indication of the derivation of these
cells from the outer layer through invagination.

At a later stage, when the yolk plug has withdrawn from the
surface and the blastopore has become slit-like, transverse
sections show several important changes in this axial mass.
In front of the blastopore the separation between ectoderm and
mesoderm has extended, by delamination, toward the mid-
line, and just before reaching this, turns sharply downward
toward the line of delamination between the endoderm and
mesoderm, not, however, reaching quite to this, thus leaving in
the mid-line a narrow vertical ridge of cells. In the regions
where the endoderm and mesoderm remain continuous, a pair
of slight depressions appear as shallow grooves out of the
archenteron; these are continued into the cell mass a short
distance as virtual grooves, indicated only by the arrangement
of the pigmented cells. Further forward (Fig. 36) the lower
margins of these grooves become better marked, as low lip-like
structures approaching the mid-line, and the mesoderm in
these regions is more extensively separated from the lining of
the archenteron. Finally, still farther forward, the grooves
disappear and the extension vertically of the spaces separating
the mesoderm from the endoderm and ectoderm completely
delimits the pair of mesoderm masses. The cells left in the
mid-line between the proximal ends of the mesoderm sheets

110 OUTLINES OF CHORDATE DEVELOPMENT

form a wedge-shaped elevation continuous with the endoderm;
this is the rudiment of the notochord. In a still later stage
the chorda begins to be cut off from the endoderm by a narrow
split leaving the enteron roofed dorsally by a layer only one
cell thick (Fig. 44). Passing posteriorly from the first section
described above, into the region of the blastopore, we find the
grooves out of the archenteron better marked and the ventral
lip, as well as the dorsal, quite pronounced. These grooves
are apparently indications of the enterocoelic evaginations;

ec

FIG. 36. — Part of a transverse section through the young embryo of R. fusca,
showing traces of enteroccel formation. After O. Hertwig. a, Archenteron;
c, enteroccels; ec, ectoderm; en, endoderm; m, mesoderm; n, notochord; p, neural
plate; y, yolk cells.

this relation will be mentioned more fully at the close of the
description of notogenesis.

7. The Medullary Plate

The rudiment of another axial structure is developing at the
same time as the chorda and mesoderm; this is the medullary
plate. The medullary plate is formed in part from the median
band of cells extending from the region of the dorsal lip of the
blastopore nearly to the animal pole, and in part from the
axial thickening due to the confluence of the lateral portions
of the germ ring. In the former region the inner or nervous
layer of ectoderm begins to thicken and by the time the blasto-
pore has become circular and commenced to close, a thickened
medullary plate has formed over the whole dorsal surface of
the gastrula (Fig. 32, F). This is in the form of a broad plate,

THE EARLY DEVELOPMENT OF THE FROG 111

narrow just in front of the blast opore and widening gradually
as it extends up toward and beyond the upper pole. By the
time the yolk plug is withdrawn the margins of the medullary
plate are considerably thickened so that its outline is visible
externally; the median region has meanwhile become thinner
and a shallow groove results (Fig. 22, C). The thickened
margins are elevated slightly above the general surface of the
ectoderm and form the two lateral neural ridges, extending
from the sides of the blastopore along the dorso-lateral regions
of the embryo, widely separated, to a level about opposite the
blastopore, where they turn sharply and pass to the mid-line,
meeting and forming thus the transverse neural fold, which
marks the anterior limit of the medullary plate. The median
groove soon becomes quite pronounced and is known as the
neural groove.

Sections through the region just in front of the blastopore
(Figs. 32, G; 33, F) show that the neural plate early begins to
separate from the remainder of the ectoderm. Fig. 44 shows
how the medullary plate is cut away laterally and superficially
from the ectoderm by a narrow split resulting from cell re-
arrangements; we have already seen that a similar space sepa-
rates the medullary plate from the underlying notochord.

8. Summary and Comparisons with Other Forms

Before continuing our account of the development of the
rudiments whose formation has just been described, we should
summarize the events of notogenesis and then1 relation to
gastrulation. It is evident that the distinction between gas-
trulation and notogenesis is real, and essential to an under-
standing of this period in development. Gastrulation involves
only those processes which convert the monodermic embryo
into a didermic embryo; notogenesis includes those processes
involved in the formation of the medullary plate, notochord,
and mesoderm. Gastrulation is accomplished primarily by de-
lamination and the rearrangement of the yolk cells, and only
secondarily, and to a very slight extent, by invagination. In

112 OUTLINES OF CHORD ATE DEVELOPMENT

the frog the process of invagination is chiefly concerned in the
formation of the rudiments of the chorda and the mesoderm
of the dorsal and dorso-lateral regions, although these structures
are not formed wholly by invagination but also by the transport
of the materials of the germ ring to an axial position, and then
by delamination. In the development of the frog, therefore,
invagination is a process of minor importance.

The actual materials out of which the axial structures of the
embryo are formed are to be found in the animal half of the
blastula, that is, in the walls and floor of the blastocoel, and these
in turn are distinguishable in the eight cell stage, where they are
contained in the upper quartet and the upper parts of the lower
quartet; finally they can be traced back, approximately to the
animal half of the egg. The later localization of the greater
part of these materials in a true germ ring is an important
characteristic in the development of the frog, and makes pos-
sible a close comparison of the gastrula and early embryo of
this form, with the conditions in the lower as well as higher
forms. It is also important that accompanying the down-
growth and closure of the germ ring there is a true confluence
of its lateral margins, forming a thickened axial mass of cells,
gradually elongating posteriorly through continued confluence.
In this axial region the chief organs characteristic of the frog
as a Chordate animal, have their origin. These organs grad-
ually differentiate as the mass elongates posteriorly, and their
rudiments, though not individually differentiated as such, are
thus seen to form gradually from the cells contained laterally
in the roots of the axial thickening, that is, in the germ ring
itself. This germ ring is not so clearly indicated in Amphioxus,
although we have seen in that form a rapidly growing ring of
cells around the blastopore, wider on its dorsal side, from which
are differentiated gradually the rudiments of the chorda and
mesoderm, and a considerable part of the medullary plate. In
Amphioxus, however, gastrulation is more nearly completed
before notogenesis commences, so that while there is some
overlapping it is not so extensive as to cause confusion of the
two processes. In the frog not only does notogenesis commence

THE EARLY DEVELOPMENT OF THE FROG 113

so early as to obscure certain features of gastrulation, but these
processes are both highly modified by the presence of a large
mass of inert yolk cells. The presence of this rather immobile
mass results in the formation of the embryo as on the surface
of a sphere instead of as a simple elongated embryo, and such
processes as the formation of enterocoelic or notochordal evagi-
nations of the gut seem more or less abbreviated when com-
pared with such a form as Amphioxus, where the embryonic
layers are not impeded in their foldings by any such restraining
influence as the yolk mass in the frog. Were we to assume
that the development of Amphioxus represents truly primitive
processes of development among the Chordates, we might
describe the course of early development in the frog by saying
that it is directed toward the accomplishment of the final
result, rather than the carrying through of a definite program,
so that the formation of the chief axial structures is effected
more or less independently of the formal processes of develop-
ment, as illustrated by Amphioxus.

However, there is considerable doubt as to whether Amphi-
oxus does really represent, in these respects, conditions which
may be considered primitive for the Chordates, Opinion
remains quite divided upon the subject of the relation between
developmental processes in Amphioxus and in such forms as
the Amphibia. Some would point out that excepting only the
Protochordates, all of the lower vertebrates have large eggs,
containing a considerable quantity of yolk, definitely localized
in one pole; that, indeed, the Mammals are the only Craniates
which have small eggs, with little yolk, comparable with those
of the Tunicates and Amphioxus. These would maintain that,
while we may say that the presence of the yolk in the egg has
modified the form of early development, we cannot call this
modified development typical for the Chordata. It is quite
likely that while the development of Amphixous is simpler and
more diagrammatic than that of any Craniate, we. must after
all regard this as a secondary or acquired simplicity, and not the
simplicity of primitiveness. From the point of view of purely
comparative embryology, Amphioxus should be the first to be

114 OUTLINES OF CHORDATE DEVELOPMENT

considered; from the phyletic standpoint it should be consid-
ered after the more typically Chordate frog — not that the frog
is embryologically typical of all Chordates, merely that it rep-
resents that condition more truthfully than Amphioxus. On
the other side, some would hold that the embryological sim-
plicity of Amphioxus is that of true primitiveness, that Am-
phibian development is secondarily modified, and phyletically
a modification of that of the Protochordates, interpretable
only through the latter and not vice versa, and that many of the
differences are the result of the accumulation of yolk in the
Amphibia. We may mention from these two points of view
only the development of the mesoderm as one of the central
points.

Except in Amphioxus the Chordate embryo remains two
layered or didermic only a very short time, on account of the
very early development of the mesoderm in all other forms.
In the frog the mesoderm cells are found, soon after the endo-
derm begins to be formed, first all around the margin of the
blastopore forming an important part of the germ ring; that is,
the mesoderm is first all blast oporal or peristomial. Then con-
fluence begins and the lateral portions of the germ ring are car-
ried to the mid-dorsal region and poured into the posteriorly
elongating embryo, where they form the mesoderm bands; the
mesoderm of the germ ring thus becomes axial in position and
is known then as gastral mesoderm. The gastral mesoderm is
here derived from the peristomial through a change in position
due to confluence, and no essential distinction between the two
is to be drawn. Only in the posterior region of the frog embryo
immediately in front of the blastopore, are there traces of
evagination in connection with the formation of the mesoderm
in the form of a pair of slight grooves or slits. These may be
considered as due merely to the rapid, unilateral and localized
proliferation of the cells around the blastopore, such as often
leads to a grooving of the surface, and as having nothing to
do with the mesoderm folds and enterocoelic evaginations of
Amphioxus. Or, on the other hand, these grooves may be
regarded as vestiges of the enterocoelic grooves of a primitive

THE EARLY DEVELOPMENT OF THE FROG 115

Amphioxus-like embryo, which has been modified by the ac-
cumulation of yolk and the precocious formation of the meso-
derm before confluence. It might easily be supposed that the
formation of the mesoderm in advance of the definite establish-
ment of the gut cavity would result in the loss of function and
disappearance of the enteroccels. In Amphioxus the gastral
and peristomial mesoderms have unlike origins, because the
mesoderm is not formed until after gastrulation, and conse-
quently, that formed from invaginated endoderm (gastral or
axial) is unlike that (peristomial or blastoporal) formed from
the "germ ring" or growth zone, around the posterior end or
blastoporal region of the embryo.

While decisive evidence is perhaps lacking, and much may be
said on both sides, on the whole the evidence seems to favor the
first view; that the method of mesoderm formation in Amphi-
oxus is not wholly primitive, that primarily there is no distinction
between gastral and peristomial mesoderm, for all is first peristo-
mial or blastoporal, and that the mesoderm grooves of the frog
are not vestiges of enterocoelic evaginations, like those of Amphi-
oxus, but represent the primary mode of origin of the mesoderm
as a proliferation from the margin of the blastopore. This
would, of course, involve the conclusion that the ccelomic cavity
is not phylogenetically derived from the gut cavity among the
Chordata. In the frog the ccelom has no relation with the
mesoderm folds, as it would have if these are vestigial enterocoelic
grooves, and it will be recalled that in Amphioxus only the cav-
ities of the more anterior somites are ever connected, even as
grooves, with the gut cavity. And yet in some of the tailed
Amphibia the ccelom is apparently sometimes directly con-
nected with the grooves in the mesoderm folds.

Most of the differences in the arrangement of the mesoderm
rudiments in Amphioxus and the frog can be traced to this
difference: in the frog the mesoderm differentiates before gas-
trulation and confluence, in Amphioxus the mesoderm differ-
entiates after gastrulation and after confluence has begun.
Doubtless these unlike relations are largely the result of the
absence of the yolk mass in Amphioxus and the consequent

116 OUTLINES OF CHORDATE DEVELOPMENT

mobility of the blastomeres and the epithelia which they
compose.

We may assume that the stage in which the rudiments of the
central nervous system, notochord, mesoderm, and gut are all
definitely established, marks the end of notogenesis and the
beginning of the formation of a definite embryo in a restricted
sense.

B. THE FORMATION OF THE EARLY EMBRYO

We may close our account of the early embryonic period by
tracing briefly the further development of the rudiments
formed at the close of notogenesis, up to the time the neural
tube is closed. We have assumed arbitrarily to let this stage
(about two days after fertilization) represent an "early embryo"
(Fig. 22, E, F). At this time the embryo has elongated so that
its length is about one and one-half times its depth or the diam-
eter of the gastrula. The postero-dorsal region is narrowed and
drawn out slightly into the rudiment of the tail. The dorsal
surface is straight or even slightly concave and narrowed in
cross section, the ventral surface remains broadly convex. The
rudiments of several organs are visible externally as elevations
or depressions; these will be described in connection with the
internal structure. Externally the ectoderm alone still forms
the covering epithelium, for as yet no part of the mesoderm has
contributed to the formation of an integument. About the only
change in the character of the ectoderm is the development, on
some of its cells, o'f numerous short cilia. Just before the fusion
of the neural folds the cilia begin to appear first along their
margins. They extend rapidly more widely over the surface,
and by the time this early embryonic stage is reached they are
absent from only the ventral surface. A little later the ciliation
is completed. The cilia beat in the posterior direction and give
the embryo a slow rotary motion within the egg membranes.

1. The Nervous System

It is more convenient to describe the development of the
nervous system first, partly because many of the chief external

THE EARLY DEVELOPMENT OF THE FROG 117

characteristics of this period are associated with the develop-
ment of this system. The transverse neural fold, which marks
the anterior limit of the central nervous system (Figs. 22, C; 32,
G), forms from materials located in about the middle of the roof
of the blastoccel, while the posterior limit of the nervous system
is just above or in front of the dorsal lip of the blastopore. The
downward extension of the latter, on account of the confluence,
increases the length of the rudiment of the nervous system, so
that before the blastoporal margin or germ ring has fully con-
tracted, it extends nearly from pole to pole, around the posterior
side of the gastrula. The rotation of the gastrula then changes
the apparent, though not the true morphological, position of the
anterior margin of the medullary plate, so that when the trans-
verse neural fold actually appears, it is on the anterior side of
the gastrula, and the medullary plate itself occupies nearly the
whole dorsal surface of the early embryo (Fig. 32, G). We have
already described the formation of the neural or medullary-
plate, the neural groove, and the lateral and transverse neural
or medullary ridges.

The elevation of the neural ridges, particularly their anterior
portions, soon becomes very marked, and as it continues the
middle of the plate sinks downward and soon the ridges bend
over toward each other and meet along the mid-line, where they
fuse, transforming the neural plate into the neural tube contain-
ing the neural canal or neurocoel (Figs. 22, D, E; 38) . For a long
time after fusion a deep median groove marks the region where
the folds have come together. The fusion of the neural ridges
does not occur simultaneously throughout their extent, but
first in about their middle, then extending posteriorly and
anteriorly from this region (Fig. 38). This is approximately
the location of the future medulla (myelencephalon) ; from this
time, therefore, the spinal cord and brain are distinguishable
(Fig. 37). The narrower cord region closes before the much
wider brain. In the closure of the brain region the transverse
fold plays an important part; this extends backward, roofing the
expanded cavity of the brain, and meets the slowly fusing
lateral folds in the region between the future fore- and mid-

118 OUTLINES OF CHORDATE DEVELOPMENT

brain. This is, therefore, the last region of the neural tube to
close, and may consequently be termed the neuropore; in the
later embryo this is the region just posterior to the epiphysis or
pineal body (see next chapter). The neuropore has a very
transitory existence.

en

nc

b —

B

ms

ht

FIG. 37. — Diagrams of median sagittal sections of frog embryos. After
Marshall. A. Just before the closure of the blastopore. B. Just after the
closure of the blastopore. (See Fig. 38, D, E.~) a, Anal or cloacal aperture;
b, blastopore; e, epiphysis; ec, ectoderm; en, endoderm;/, fore-brain; g, mid-gut;
h, hind-brain; ht, rudiment of heart; hy, hypophysis; I, liver diverticulum ; m, mid-
brain; ms, mesoderm; w, notochord; nc, neurenteric canal; o, oral evagination;
p, proctodseum; ph, pharyngeal region of gut cavity; r, rectum; s, spinal cord;
y, yolk cells.

Those cells in the nervous layer of the ectoderm forming the
lateral margins of the neural plate, that is, the neural ridges
proper, do not themselves form an integral part of the neural
tube. When the margins of the neural plate fold together they
are left dorso-laterally, between the neural tube and the defini-
tive ectoderm. These ridges of cells become broken into cell
groups, lying along the lateral regions of the neural tube, forming

THE EARLY DEVELOPMENT OF THE FROG 119

the neural crests. These are concerned later in the development
of the nerves, which, together with some additional details of
this period, will be described in the next chapter.

At the posterior end of the embryo, the relations of the blasto-
pore (germ ring) and neural folds are of considerable importance
from a comparative point of view. We left the blastopore in
the form of an elongated slit on the postero-dorsal surface of the
embryo. The lateral walls then approach, about the middle of
the slit, and finally it is there constricted completely, so that the
blastopore is divided into two small openings, an upper and a
lower (Fig. 38, A, B). The medullary groove extends forward
from the upper opening, which remains open, leading directly
into the archenteron (Fig. 37). The lower opening is soon
closed by the fusion of its lips. The fusion involves only the
ectoderm and endoderm of the region, and occurs some distance
below the surface, so that a pit-like depression is left on the
surface, lined with ectoderm; this is the proctodceum. When the
posterior ends of the neural folds form, they extend into, or
rather out from, the middle regions which have fused, and as
they become elevated and form the neural tube they cover over
the upper blastoporal opening (Fig. 38, C) which thus becomes
the neurenteric canal, like that of Amphioxus or other Chordates,
and similarly formed, putting the neurocoel and gut into com-
munication. The lateral margins of the blastopore are formed
of the remains of the germ ring, and when they meet, dividing
the blastopore, they form a median cell mass in which ectoderm,
endoderm, and mesoderm are fused in a more or less undifferen-
tiated mass. This mass can no longer be called the germ ring,
although it is really equivalent to the lateral parts of this; it is
known as the primitive streak, and the groove that remains for
a time on its surface, indicating its origin from originally sepa-
rate lateral portions, is the primitive groove. The primitive
streak and groove of the frog are homologous with the similarly
named structures in Amphioxus and in the Amniota. The cells
of the primitive streak continue to multiply rapidly, and bud
forth strands of ectoderm into the neural folds and upon the
surface of the body, mesoderm into the lateral bands, and en-

120 OUTLINES OF CHORDATE DEVELOPMENT

doderm into the wall of the gut. This leads to the formation
of a postero-dorsal protuberance which is the rudiment of the

V

E

FIG. 38. — Posterior ends of a series of young frog embryos, showing the later
history of the blastopore, and the relation of the neural folds to it. The embryos
are viewed obliquely from the postero-lateral aspect. After F. Ziegler. A. Blas-
topore nearly closed; neural folds just indicated. B. Blastopore becoming di-
vided into neurenteric and proctodaeal portions; neural folds becoming elevated.
C. Neurenteric canal forming; neural folds closing together. D. Neural folds in
contact throughout. E. Neural folds completely fused; tail commencing to grow
out. b, Blastopore, containing yolk plug; 61, rudiment of neurenteric canal (dorsal
part of blastopore) ; 62, rudiment of proctodaeal pit (ventral part of blastopore) ;
60, branchial arches; g, neural groove; nf, neural folds; np, neural plate; p, proc-
todaeal pit; s, rudiment of oral sucker; t, rudiment of tail; x, neural folds roofing
the blastopore and establishing the neurenteric canal.

tail, but in the stage we are describing this is only just indicated
(Fig. 38, D, E).

THE EARLY DEVELOPMENT OF THE FROG 121

At the opposite end of the body the enlarged brain protrudes,
forming a head region faintly indicated externally. A sagittal
section (Fig. 37, A) shows that the future regions of the brain
are but faintly marked out. The chief characteristic of the
brain is its abrupt bending or flexure around the anterior tip
of the notochord; the region immediately in front of the chorda
is that of the future mid-brain, while the large fore-brain lies
entirely below the level of the chorda and the remainder of the
neural tube. In the mid-line, just beneath the end of the fore-
brain, a tongue-like proliferation of ectoderm cells extends
inward a short distance. This is the rudiment of the hypophysis.

The simple rudiments of the chief sense organs are also indi-
cated at this early stage. The eyes are distinguishable, even be-
fore the brain closes, as small patches of deeply pigmented ecto-
dermal epithelium in the antero-lateral regions of the medullary
plate. When the neural tube is completed, they form a pair of
hollow ventro-lateral outgrowths from the fore-brain to the
superficial ectoderm. Frequently they can be seen externally,
marked by a pair of slight darkened elevations, either side of the
fore-brain region (Fig. 22, E, F). The ears are indicated as a
pair of thickened patches of the inner or nervous layer of the
ectoderm opposite the hind-brain region. They are scarcely
visible externally at this time. The olfactory organs develop as
thickened circular patches of ectoderm below and in front of the
optic rudiments. At this stage a pair of slight depressions may
sometimes be detected on the surface, marking the future
olfactory pits.

2. The Notochord

By the time the neural tube is completed the chorda has
become completely delaminated from the outer surface of the
endoderm, except only in the region of the primitive streak
where its formation is still progressing posteriorly. The separa-
tion of the chorda from the endoderm, or rather the enteroderm
(see below), occurs in the posterior direction, beginning near
but not quite at the anterior tip.

122 OUTLINES OF CHORDATE DEVELOPMENT

3. The Enteron

At the close of gastrulation and notogenesis the archenteron
is a nearly hemispherical cavity on the dorsal side of the embryo,
open posteriorly through the blastoporal opening. Its roof
and sides are left as a thin layer of endoderm — the enteroderm —
after the chorda and mesoderm have been split off; its floor is
formed of the thick mass of yolk cells. By the time the neural
tube is completed and the embryo has elongated slightly, the
enteric cavity or mesenteron has enlarged considerably, chiefly
in front of the yolk mass, which retains a postero- ventral posi-
tion in the wall of the gut (Fig. 37). This anterior enlarged
region of the mesenteron is known as the fore-gut, the entire
wall of which is but one cell thick; this is the region of the
embryonic pharynx and later of the oesophagus and stomach
as well. At the posterior end of the mesenteron there is a slight
enlargement, just in front of the neurenteric canal, which is the
hind-gut or rectal portion of the intestine. Connecting these
two regions the narrow mid-gut or intestinal region proper, is
that containing the yolk cells, which are also to be regarded as
enteroderm.

In the fore-gut of this stage there is an antero-ventral out-
pocketing toward the ectoderm just below the fore-brain, indi-
cating the region where the mouth will form later. A postero-
ventral outgrowth beneath the anterior end of the yolk mass is
the rudiment of the liver. Sections passing through the sides
of the fore-gut show that even in this early stage the rudiments
of the first two or three visceral pouches are present in the form
of vertical outgrowths from the side walls of the pharynx to
the ectoderm, with which they fuse. Along the region of the
fusion the ectoderm is depressed so that these are externally
visible as vertical depressions just back of the head (Fig. 22, E,
F). Externally two of these are marked at this time as the
external branchial grooves, and the ridges left between and in
front of them are the rudiments of the second or hyoid, and first
or mandibular arches respectively. The hyoid arch is sometimes
known here as the "gill plate"; it extends dorsally nearly to

THE EARLY DEVELOPMENT OF THE FROG 123

the margin of the nervous system. The mandibular arches are
less marked; these appeared even before the medullary plate
became folded together, as a pair of low ridges diverging from
the antero-lateral regions of the plate and sometimes called
the " sense plates." They lie between the olfactory and optic
rudiments and form the antero-lateral regions of the embryonic
head.

4. The Mesoderm

The delamination of the mesoderm from the surface of the
endoderm commenced in the dorso-lateral regions anteriorly,
and spread thence posteriorly and ventrally. We have seen
that posteriorly the mesoderm finally passes into the region of
the germ ring, or what now represents a portion of that, the
primitive streak, where it continues to be formed and budded
off anteriorly as the primitive streak extends posteriorly. And
ventrally the delamination ceased in the ventro-lateral regions
of the endoderm, and the mesoderm then extended gradually
toward the ventral side through the multiplication of its own
cells and their downward extension, and through the splitting
off of scattered groups of cells from the endoderm toward the
ventral side. In this early embryo the mesoderm forms a
distinct layer separating ectoderm and endoderm throughout
(Fig. 44), except in the primitive streak and in the head region,
where the mesoderm is never in the form of a definite sheet, but
is represented by scattered cells filling the spaces between the
wall of the mesenteron and the nervous system and ectoderm
(Fig. 45). In the pharyngeal region the mesoderm becomes
interrupted by the extension of the gill pouches out to the ecto-
derm; between successive pouches groups of mesoderm cells
are enclosed which become the rudiments of the visceral arches
— mandibular, hyoid, and branchial.

Through the trunk region the typical mesodermal structures
develop rapidly. The axial region toward the chorda thickens
and becomes solid; this is the segmental plate or myotomal region
(Fig. 39) . Farther laterally the thinner layer is the lateral plate;

124 OUTLINES OF CHORDATE DEVELOPMENT

this splits into two more or less distinct sheets, the somatic
and splanchnic layers, in contact with ectoderm and endoderm
respectively. The space between these is the splanchnoccel,
the rudiment of the body cavity or coelom. In the stage we
are describing the coelom does not extend' completely through
the lateral plate as it does finally. The coelom does however
extend into the segmental plate, as the rudiment of themyocoels,

nc

so

ec

FIG. 39. — Part of a section through the anterior body region of an embryo of
R. sylvatica, just beginning to elongate, illustrating the differentiation of the
mesoderm. After Field, c, Coelom; ec, ectoderm; en, endoderm; g, gut cavity;
mp, medullary plate; my, myotome; n, notochord; nc, rudiment of neural crest;
so, somatic layer of mesoderm; sp, splanchnic layer of mesoderm.

appearing toward the surface of this thicker mass. As the
neural folds approach, the cells of this axial mesoderm are
rearranged in such a way that the longitudinal bands are cut
transversely into segments or somites. This process begins
just back of the pharynx and extends rapidly toward the
posterior ends of the bands (Figs. 44, E; 53). It is important
that the mesoblast of the head region is not clearly divided into
segments. By the time the neural tube is completed three or
four pairs of somites have been formed. At first these are

THE EARLY DEVELOPMENT OF THE FROG 125

continuous with the lateral plate but shortly after they are
marked out, the two regions become separate and the lateral
plate itself is never segmented but remains uninterrupted.
The coelomic spaces of the somites, the myocoels, then disappear
without leaving any trace. These processes are progressive
posteriorly, the formation of the coelom, somites, etc., con-
tinuing as the mesoderm forms from the primitive streak.

In the embryo of this period indications of two important
structures are present in connection with the mesoderm but
not as readily recognizable and definite rudiments; these are
the pronephros and the heart. The connections between the
second, third and fourth somites and the lateral plate remain as
small masses of cells, in close relation with the somatic layer
of the lateral plate. These are the cells forming the rudiments
of the pronephric tubules. The definite formation of these
rudiments and that of the pronephric duct must be left until a
later stage is described. Just below the pharynx and in
front of the liver, the mesoderm cells are arranged in somatic
and splanchnic layers, and between these the coelomic space is
well marked on either side, while elsewhere in the ventral region
it has not appeared (Fig. 37, B). Between the mesoderm and
the ventral side of the pharynx a few loose cells are scattered
along. This is the region where the heart is soon to appear
but this, too, must be described later.
(References to the literature will be found at the end of Chapter III.)

CHAPTER III

THE LATER DEVELOPMENT OF THE FROG:
ORGANOGENY

PAGE
INTRODUCTION 127

I. THE NERVOUS SYSTEM 128

1. The Central Nervous System 128

2. The Peripheral Nervous System 135

A. The Cranial Nerves 136

B. The Spinal Nerves 142

C. The Sympathetic System 143

II. THE SPECIAL SENSE ORGANS 144

1. The Eye 144

2. The Ear 149

3. The Olfactory Organ 153

4. The Sense Organs of the Lateral Line 156

III. THE ALIMENTARY TRACT AND ITS APPENDAGES . . 158

1. The Derivatives of the Fore-gut 159

2. The Derivatives of the Mid-gut 168

3. The Derivatives of the Hind-gut 169

IV. THE MESODERMAL SOMITES 170

V. THE VASCULAR SYSTEM 174

1. The Heart 174

2. The Origin of the Blood and Vessels 178

3. The Arterial System ' 179

4. The Venous System 185

5. The Lymphatic System and the Spleen 189

6. The Formation of the Septum Transversum 191

VI. THE URINOGENITAL SYSTEM 192

1. The Excretory System 192

A. The Pronephros and the Pronephric Duct 193

B. The Mesonephros (Wolffian Body) 198

2. The Reproductive System 201

A. The Gonoducts 202

B. The Gonads 203

3. The Adrenal Bodies 206

126

THE LATER DEVELOPMENT OF THE FROG 127

VII. THE SKELETON AND TEETH ....... .: ..„,. 207

1. The Vertebral Column 208

2. The Skull 210

A. The Cranium and Sense Capsules 210

B. The Visceral Arches 216

C. The Dermal Elements 219

3. The Teeth 220

4. The Appendicular Skeleton 221

IN this chapter we shall trace the chief events in the develop-
ment of the frog tadpole, from the stage described at the close
of the preceding chapter, i.e., just after elongation is inaugu-
rated by the enlargement of the head and the outgrowth of the
tail. The more important changes in external form and in
habit have been described in the introduction to the preceding
chapter, and we may turn at once to the description of the inter-
nal processes of development.

The developmental history of no single species of frog is
known with even fair completeness, and we should note that
this chapter presents a composite account of the development
of the genus Rana. No attempt has been made, save in occa-
sional instances, to distinguish the species serving as the basis
for different sections; these vary somewhat in details, but since
details are largely omitted, little confusion is likely to follow
such treatment. The species of Rana chiefly serving as the
material for this account are the American species, sylvatica,
palustris, and virescens, and the European temporaria, esculenta,
fusca, and muta.

While the early history of the frog embryo is fairly well
known, there are still many gaps in our knowledge of the later
development of the tadpole, gaps which sometimes seem of
remarkable proportions in view of the extent to which the frog
is used as an object of embryological study.

No accurate and convenient description of the age of the
frog larva has been determined, since the rate of development
varies so markedly with temperature changes before the opening
of the mouth, and afterward with the abundance of food. At
the time of hatching, which is usually between one and two
weeks after fertilization, the larvae of most species are approxi-

128 OUTLINES OF CHORDATE DEVELOPMENT

mately 6-7 mm. in total length. Another frequent reference
point is the time of the opening of the mouth, which usually
occurs in tadpoles of 9-10 mm., only a few days after hatching.
The limbs appear as small buds in tadpoles of 11-12 mm.; the
fore-limbs are of course concealed underneath the operculum,
but they develop at about the same time and rate as the hind-
limbs.

I. THE NERVOUS SYSTEM

1. The Central Nervous System

In the preceding chapter we described the formation of the
neural tube and noted the differentiation between the narrow
spinal cord and the dilated brain region. Posteriorly the cord
is bent downward toward the blastopore, and the cavity of the
cord is continuous with the archenteron by way of the neuren-
teric canal. Anteriorly the brain is strongly flexed around the
tip of the notochord. The neuropore, which is located ante-
riorly from the tip of the chorda, has just closed and remains
connected with the surface ectoderm by a broad cone of pig-
mented cells (Fig. 37, A).

The development of the brain from the stage described is
comparatively simple. In its early history it differs from most
other forms in two important respects; no neuromeres or brain
segments are indicated, and the division of the primitive brain
into its primary fore-, mid-, and hind-brain regions is incom-
pletely indicated and appears relatively late. The chief mor-
phological characteristics of the brain result largely from two
groups of processes, (a) thickenings and thinnings, (6) out-
growths and ingrowths of the wall. In describing these proc-
esses it is convenient to distinguish the roof, floor, and sides
of the brain tube.

One of the chief features of the brain is its well-marked
ventral flexure, the large anterior part of the brain lying below
the level of the notochord (Figs. 37, 40); this flexure remains
a permanent characteristic of the brain, although as we shall
see, it soon becomes masked by the unequal growth of the neigh-

THE LATER DEVELOPMENT OF THE FROG .129

boring regions. Just opposite the tip of the chorda the floor
of the brain becomes slightly thickened as the tuberculum poste-
rius, and in the roof, obliquely upward and forward from this.,
appears a rather extensive dorsal thickening (Fig. 41). With
the aid of these landmarks we may map out the location of the
future brain regions. A plane passing from the tuberculum
posterius in front of the dorsal thickening, marks approximately
the limit between the primary fore-brain or prosencephalon, and
the mid-brain or mesencephalon; while a plane passing from the
tuberculum posterius behind the dorsal thickening, marks the
limit between mesencephalon and the primary hind-brain or
rhombencephalon. The beginning of the rhombencephalon is
also indicated by a considerable transverse extension of the
brain tube; posteriorly the rhombencephalon passes insensibly
into the spinal cord.

We may now proceed to describe the more important events
in the development of each of these primary divisions of the
brain. We should note in advance that the prosencephalon
forms the olfactory lobes and cerebral hemispheres (tekncephalori)
and the between-brain (diencephalon) : the mesencephalon
forms the region of the optic lobes and chiasma: the rhomben-
cephalon forms the cerebellum (metencephalon) and the medulla
oblongata or spinal bulb (myelencephalon) .

The Prosencephalon. — The cells of the ectodermal cone
opposite the neuropore (Fig. 40) , soon scatter, as the tissues of
the head push out in advance of the brain, and no trace is
left of the original location of this structure, save a slight bay
or olfactory recess, which soon disappears. Below this level
the anterior wall of the fore-brain remains somewhat thick-
ened for a time, as the lamina terminalis. This extends to the
ventral side of the brain where the optic stalks extend out from
the fore-brain. These are hollow and their cavities are continu-
ous with the cavity of the prosencephalon. The regions of
the anterior and posterior borders of their attachment early
become considerably thickened as the torus transversus and
the rudiments of the optic chiasma and thalami, respectively
(Figs. 41, 42); the former becomes the seat of the anterior, and

130 OUTLINES OF CHORDATE DEVELOPMENT

certain other, commissures of the brain. The narrow depres-
sion between these two thickenings is the recessus options, i.e.,
the passage to the cavities of the optic stalks. The posterior
side of the prosencephalon extends backward beneath the tip
of the notochord forming a well-marked outgrowth, the
infundibulum.

FIG. 40. — Median sagittal section through the brain of an embryo R. fusca,
of 2.3 mm. From Von Kupffer (Hertwig's Handbuch, etc.). cd, Notochord;
d, superficial layer of ectoderm ("deckschicht") ; en, endodermal lining of
pharynx; g, inner or nervous layer of ectoderm; hy, hypophysis; J, infundibulum;
kg, conical proliferation of ectoderm cells at the point of closure of the neural
folds.

Somewhat later the entire dorsal wall of the prosencephalon
becomes thinner, and toward its posterior limit an evagination
appears which is the beginning of the epiphysis or pineal body
(Fig. 42). In front of this the roof ultimately becomes non-
nervous and forms a series of highly vascular folds projecting
down into the cavity of the brain; this is the choroid plexus of the
third ventricle. Later there develop, between this choroid
plexus and the epiphysis, the habenular ganglia and commissure,
and much later there develops, in front of this, a dorsal out-

THE LATER DEVELOPMENT OF THE FROG 131

growth of the wall, the paraphysis. That part of the prosen-
cephalon extending from the choroid plexus and epiphysis on
the dorsal side, to the inf undibulum on the ventral side, is known
as the diencephalon or between-brain, while the remaining ante-
rior portion is the telencephalon or secondary fore-brain.

Considerably later (about 7 mm. or time of hatching) the
rudiments of the cerebral hemispheres appear, growing outward

dw.

hy.

FIG. 41. — Median sagittal section through the brain of an embryo R. fusca,
of 2.3 mm. length, but in a more advanced stage than that of Fig. 40. From Von
Kupffer (Hertwig's Handbuch, etc.). cd, Notochord; cw, rudiment of optic
chiasma; dw, dorsal thickening; e, rudiment of epiphysis; en, endodermal lining
of pharynx; hy, hypophysis; /, inf undibulum; It, lamina terminalis; M, mesen-
cephalon; P, prose ncephalon; R, rhombencephalon; sk, rudiment of olfactory
placode; tp, tuberculum posterius; tr, torus transversus.

and forward from the sides of the telencephalon (Fig. 42, A).
These ultimately become very large and extend far in front of
the median region. They have thick inner and outer walls, and
contain extensions of the cavity of the telencephalon known as
the lateral or first and second ventricles, while the remaining
median cavity of the telencephalon and diencephalon is known
as the third ventricle. The ventricles of the cerebral hemi-
spheres are laterally compressed, and open out of the third
ventricle by a pair of openings known as the foramina of

132 OUTLINES OF CHORDATE DEVELOPMENT

Monro. The thickenings of these anterior extensions of the
telencephalon and of the regions of the optic thalami and ante-
rior commissure produce an apparent straightening of the origi-
nal ventral flexure of the brain; this does not really disappear,
however, and the infundibulum continues to extend below and
in front of the tip of the notochord.

The hypophysis, while originally not a part of the brain,
becomes intimately related with it. This forms very early as a
strand of cells extending inward from the inner layer of the sur-
face ectoderm (Figs. 37, 40), below the telencephalon and just
above the future mouth region (oral plate) . These cells multi-
ply and form a definite mass lying between the endoderm and
the infundibulum, just at the tip of the chorda. This rudiment
later cuts off from the ectoderm, and after fusing with the dorsal
wall of the pharynx, comes into intimate relation with the
lower surface of the infundibulum, forming the essential part
of the pituitary body.

The mesencephalon undergoes only slight modification during
the larval period. While its roof and floor remain thin, its
ventro-lateral walls thicken as the crura cerebri, connecting with
the prosencephalic wall: its dorso-lateral walls form the large
rounded optic lobes. In front of these the anterior limit of the
mid-brain is marked later by the posterior commissure. The
cavity of the mesencephalon is called the aqueduct of Sylvius; it
becomes narrow and connects the third ventricle with the cavity
of the rhombencephalon.

The rhombencephalon is an elongated part of the brain lying
wholly above the notochord. The usual division of this part of
the brain into an anterior metencephalon and a posterior myelen-
cephalon, is scarcely indicated in the frog. The wide cavity of
the rhombencephalon is known as the fourth ventricle; it is con-
tinuous anteriorly with the aqueduct of Sylvius and posteriorly
with the cavity of the spinal cord. The metencephalon is the
region of the cerebellum; this is very small in the frog, and
appears late in larval life, as a dorsal and dorso-lateral thicken-
ing. Ventrally the walls of the two regions are uniformly
continuous.

THE LATER DEVELOPMENT OF THE FROG 133

e.

hftr,

FIG. 42. — Median sagittal sections through the brain of the frog. From Von
Kupffer (Hertwig's Handbuch, etc.). A. Of a larva of R. fusca of 7 mm. in
which the mouth was open. B. R. esculenta at the end of metamorphosis.
c, Cerebellum; ca, anterior commissure; erf, notochord; ch, habenular commissure;
cp, posterior commissure; cpa, anterior pallial commissure; cq, posterior corpus
quadrigeminum; ct, tubercular commissure; cw, optic chiasma; d, diencephalon;
dt, tract of IV cranial nerve; e, epiphysis; hm, cerebral hemisphere; hy, hypophysis;
J, infundibulum; M, mesencephalon; Ml, myelencephalon; Mt, metencephalon;
p, antero-dorsal extension of diencephalon; pch, choroid plexus of third ventricle;
R, rhombencephalon; rm, recessus mammillaris; ro, optic recess; se, roof of
diencephalon; t, telencephalon; tp, tuberculum posterius; tr, torus transversus
(telencephali) ; vc, valvula cerebelli; vi, ventriculus impar (telencephali) (third
ventricle).

134 OUTLINES OF CHORDATE DEVELOPMENT

The broad roof of the myelencephalon is wholly non-nervous
and forms the folded choroid plexus of the fourth ventricle (Fig.
42, B). The floor and ventro-lateral walls of the rhomben-
cephalon become greatly thickened, forming chiefly the nervous
pathways extending between the cord and brain and the nuclei
of origin of most of the cranial nerves. Posteriorly the myelen-

W.

FIG. 43. — Transverse sections through the spinal cord of R. fusca. From Von
Kupffer (Hertwig's Handbuch, etc.). A. Through the anal region of a larva of
7 mm. B. Through the anterior body region of a larva during metamorphosis,
a, Spinal artery; c, central canal; d, dorsal column (white substance); dw, dorsal
root of spinal nerve; dz, atrophied dorsal cells; g, gray substance; vz, ventral
cells; w, dorso-lateral column (white substance).

cephalon narrows gradually and passes insensibly into the spinal
cord.

The spinal cord is at first flexed posteriorly toward the blasto-
pore (Fig. 37), but when the tail begins to grow out this flexure
disappears. The cavity of the cord is the central canal; it is
lined with a layer of non-nervous cells known as ependymal cells,
while the true nerve cells composing the greater part of its wall

THE LATER DEVELOPMENT OF THE FROG 135

are termed the germinal cells (Fig. 43). Part of the germinal
cells become the supporting or glia cells, while the remainder
become the functional nerve cells or neuroblasts. The closure of
the neural folds is complete and no dorsal fissure is left in the
cord.

The thickening of the walls of the cord begins dorsally and
dorso-laterally, so that the central canal is given a ventral loca-
tion, its floor formed only by a layer of ependymal cells. Later
the ventral wall thickens slightly and the ventro-lateral walls
extend below its level forming a shallow groove, the ventral
fissure. The central canal becomes compressed laterally, and
is later completely surrounded by neuroblasts (gray matter),
the outgrowths of which form a superficial layer known as the
white matter of the cord (Fig. 43).

2. The Peripheral Nervous System

We should recall in a few words the morphological arrange-
ment of the spinal and cranial nerves. The spinal nerves, of
which there are but ten pairs in the adult, although in the tad-
pole upward of forty pairs, arise from the cord by a dorsal or
afferent root, on which is located the spinal ganglion, and a
ventral or efferent root. These roots join to form the trunk of
the spinal nerve which is then divided into dorsal and ventral
rami and a ramus communicans which passes to the sympa-
thetic system (Fig. 46). Of the cranial nerves, connected
with the brain, there are commonly described ten pairs, con-
siderably varied in morphological, as well as in functional,
characteristics. Those regarded as the most typical are pri-
marily related with the gill clefts and are therefore known as the
branchiomeric nerves; these are the V, VII, IX, and X. Each
of these arises by a single, though in some cases compound,
root of mixed character, i.e., afferent and efferent, passes into
a large ganglion, beyond which it gives off a horizontal branch,
and then divides into two branches which pass anteriorly and
posteriorly to the gill cleft with which the nerve is associated.
The III, IV, and VI cranial nerves are simple, purely efferent,

136 OUTLINES OF CHORDATE DEVELOPMENT

supplying the muscles of the eye- ball. The development of the
nerves commonly described as I and II will be considered in
connection with the development of the olfactory and optic
sense organs.

Embryologically the rudiments of the cranial nerves are com-
posite structures, three elements entering into their formation.
These are, (a) cell masses derived from the neural crests, (&)
cells from ectodermal patches on the surface of the head, (c)
cell processes extending out from neuroblasts in the ventro-
lateral walls of the spinal cord. In the spinal nerves the ele-
ments from the surface ectoderm are lacking.

A. THE CRANIAL NERVES

The rudiments of certain of the cranial nerves appear very
early, and we may therefore describe them first although they
are more complicated than the later appearing spinal nerves.
While the central nervous system is still in the form of a flat plate
we have already seen that its margin is considerably thickened,
on account of the proliferation of the cells of the inner or ner-
vous layer there. These thickened margins are visible on the
surface of the embryo as the medullary ridges. Transverse
sections of this stage (Fig. 44) show that these thickened masses
of inner ectoderm become delaminated, both from the outer
stratum of ectoderm and from the medial portion of the medul-
lary plate which then goes to form the neural tube proper.
These lateral cell masses are the beginnings of the neural crests.
In the head region these masses become very large, and as the
neural plate begins to close each becomes transversely divided
into three masses. Posteriorly to the brain region the neural
crests are much smaller, but are typically formed. As the
neural tube closes these cell masses are left in situ along the
sides of the brain and cord (Corning, Brachet).

The three divisions of the head portion of each crest soon
become quite distinct. The anterior section, which begins in
the mid-brain region, is to be recognized as the rudiment of the
trigeminal ganglion (V nerve), the middle section as the rudi-

THE LATER DEVELOPMENT OF THE FROG 137

ment of the acustico-facialis ganglion (VIII and VII nerves),
and the posterior as the rudiment of the ganglion of the glosso-

FIG. 44. — Sections through young frog embryos (R. fused), illustrating the
development of the crest ganglia and placodes. After Brachet. A. Transverse
section through the neural plate of an embryo before elongation begins. B.
Sagittal section, to one side of the mid-line, through an embryo of the same age
as A. (This is also the stage of Fig. 32, G.) C. Sagittal section, to one side of
the mid-line, through an embryo just beginning to elongate. D. Transverse
section through, an embryo slightly older than that of A and B. E. Frontal
section through an embryo with three or four pairs of mesodermal somites.
F, G, H. Three transverse sections through an embryo just beginning to elongate
(same age as C), showing the trigeminal, acustico-facial and glossopharyngeal-
vagus crest ganglia, a/, Acustico-facialis ganglion; c, notochord; en, endoderm;
g, gut cavity; gl, glossopharyngeal ganglion; gv, glossopharyngeal-vagus ganglion;
I, liver diverticulum ; m, mesoderm; mp, primitive medullary plate; mpd, defini-
tive medullary plate; nc, neural crest; s, mesodermal somites; tg, trigeminal
ganglion; va, vagus (pneumogastric) ganglion.

pharyngeal (IX) and vagus (X) nerves. The delamination of
these rudiments from the medullary plate is not quite complete,

138 OUTLINES OF CHORDATE DEVELOPMENT

and when the neural tube is fully formed, each may be seen to
be' connected with the dorsal surface of the myelencephalon
by a slender chain of cells (Fig. 45).

Opposite each of these crest ganglia the cells of the inner or
nervous layer of the ectoderm very early (stage with 3-4
somites) proliferate and form a patch, in places three or four
cells deep (Fig. 45). These thickened patches are known as
placodes: they are undoubtedly to be interpreted as vestigial
sense organs. In each placode two separate elements are
distinguishable, a superficial sensory element, which usually
disappears (the exceptions will be noted below), and a deeper
ganglionic portion which is usually retained to a varying extent.
The ganglionic portion of the placode typically fuses with the
cells of the associated crest ganglion, and together they form
the rudiment of the chief sensory or afferent components of
the cranial nerve. From this point onward we may describe
separately the history of the chief cranial nerves. (Reference
is unavoidably made to the visceral arches and clefts whose de-
velopment must be described later, in connection with the
history of the pharynx).

The Trigeminal Nerve (V). — This is the chief nerve of the
mouth and mandibular arch. The trigeminal portion of the
neural crest is very large, extending from the eye to the hyo-
mandibular cleft (Fig. 44, C, E, F). The crest ganglion grows
downward and comes ventrally into contact with the mesoderm
of the mandibular arch. These ectodermal and mesodermal
cell groups then fuse, cells of the apposed surfaces intermingling,
and finally a cell mass is formed in which the two elements are
indistinguishable; this becomes the mesenchyme of the man-
dibular arch (Fig. 45, A, B).

The dorsal and superficial cells of the crest ganglion retain
their nervous character and come into relation with the large
placode of this region. The superficial or sensory portion of
this placode disappears, but its deeper or ganglionic portion
enlarges and divides into two parts. An anterior part separates
from the surface ectoderm as the ophthalmic ganglion of the
ophthalmic branch of the V nerve, whose fibers grow out ante-

THE LATER DEVELOPMENT OF THE FROG 139

eo

FIG. 45. — Portions of sections through the head of the frog (R. fused), illus-
trating the formation of the placodes and the history of the crest ganglia. After
Brachet. A. Transverse section through the trigeminal ganglion of an embryo
of 3 mm. B. Transverse section through the acustico-facialis ganglion of an
embryo with three or four pairs of mesodermal somites. C. Transverse section
through the facial ganglion and auditory placode of an embryo of 2.8 mm.
ei, inner or nervous layer of ectoderm; en, endoderm; eo, outer layer of ectoderm;
m, mesoderm; mpd, definitive medullary plate; n, nerve cord; pa, auditory pla-
code; pf, facial placode; ptg, trigeminal placode; r, spinal prolongation of ganglion;
tg, trigeminal ganglion.

140 OUTLINES OF CHORDATE DEVELOPMENT

riorly, through the dorsal head region, and also medially con-
necting with the medulla. The posterior part of the placode
ganglion then fuses with the crest ganglion and together they
form the trigeminal ganglion proper (Gasserian ganglion).
From the neuroblasts of this ganglion, cell processes extend
centripetally, entering the dorsal side of the medulla and form-
ing the sensory root of the V nerve, while centrifugal processes
rapidly grow out to the surface of the head (cutaneous branch of
the V nerve), and also in front of and behind the mouth
(mandibular and maxillary branches). These branches, as
indeed those of most of the other branchiomeric nerves as
well, are established before the time of the opening of the mouth.
The cells which formed the original attachment of the crest
ganglion with the medulla, appear to form the medullary sheath
cells of the root of this nerve, while the sheaths of the peripheral
branches are apparently derived from other migratory cells of
the crest ganglion itself.

The Facial and Auditory Nerves (VII and VIII). — It is con-
venient to describe these together, since both are derived from
the acustico-facialis crest ganglion and its associated placode.
The VII nerve is the nerve of the hyo-mandibular cleft, while
the VIII nerve is not one of the branchiomeric series, but is
purely sensory (auditory) .

The early history of these nerves is similar to that of- V; the
major part of the crest ganglion contributes to the mesenchyme
of the hyoid arch. The nervous part of the crest ganglion is
somewhat more extensive than that of the V nerve, i.e., a greater
part of the original ganglion remains of nervous function.
The first important distinctive character here, consists in the
fact that the sensory or superficial part of the placode does not
disappear, but, continuing to enlarge, gradually sinks below the
surface of the head, invaginates, and forms the rudiment of
the ear, the auditory sac (Fig. 45, (7). The deeper placode
ganglion cells in connection with this sensory epithelium remain
in close contact with the sac forming the rudiment of the VIII
nerve. From the neuroblasts of this rudiment processes grow
into the medulla forming the root of the VIII nerve.

THE LATER DEVELOPMENT OF THE FROG 141

The remainder of the placode ganglion joins with the nervous
portion of the crest ganglion, forming the ganglion of the VII
nerve, from which centripetal processes grow out connecting
the ganglion with the medulla, while centrifugal processes
extend into the hyoid arch and neighboring regions (hyoman-
dibular and palatine nerves).

The Glossopharyngeal and Vagus (Pneumogastric) Nerves
(IX and X). — These are the nerves of the remaining visceral
clefts, the first to fourth branchial clefts (third to sixth visceral
arches). The IX nerve is limited to the region of the first
branchial cleft, while the X nerve is distributed around the
remaining gill clefts, and is to be regarded as a compound nerve,
equivalent to several branchiomeric nerves. The crest gang-
lion of these nerves forms the large posterior section of the
crest in the head region (Fig. 44, E, H}. Essentially it resem-
bles that of V; it rapidly grows very large, extends farther
ventrally and posteriorly, and contributes to the formation of
mesenchyme to a considerably less extent than the ganglion of
the V nerve. The placode of the IX nerve develops typically;
its superficial sensory portion disappears, while its ganglionic
portion comes only slightly into relation with the crest ganglion.
Posterior to this, the large placode of the X nerve appears simul-
taneously and has a similar early history, save that it fuses
more extensively with the nervous portion of the crest ganglion.
When the fibers grow out from the IX and X ganglia they pass
together into the medulla as a single root. The IX ganglion
is only incompletely separated from that of X by the passage
of the anterior cardinal vein (see below). From the IX por-
tion of the ganglion, which is thus almost wholly placodal in
origin, fibers grow peripherally into the- usual relation with the
first branchial cleft, while from the mixed ganglion of the X
nerve, branches grow out with typical relations to all the remain-
ing clefts.

From the vagus ganglion certain other important processes
grow out posteriorly. From the placode a considerable tongue
of cells grows posteriorly, forming the rudiment of the sense
organs of the lateral line (see below), and accompanying this,

142 OUTLINES OF CHORDATE DEVELOPMENT

fibers grow out from the ganglion as the rudiment of the lateral
line nerves (Fig. 53), this branch is present throughout the tad-
pole stage but disappears at metamorphosis. The vagus gang-
lion also sends out processes which grow posteriorly, to the
thoracic and abdominal viscera; these form the visceral branch
of the X nerve.

The branchiomeric cranial nerves include, beside the afferent
or sensory components, whose development has just been out-
lined, efferent or motor fibers in varying numbers. These do
not arise by a morphologically separate root, but neuroblasts
in the wall of the medulla send out processes (axons), which
leave the cord in association with the afferent roots described
above. They are distributed with the branches which pass
posterior to the gill clefts.

The development of the III, IV, and VI cranial nerves is
incompletely known. They form, comparatively late, as out-
growths of neuroblasts located in the ventral parts of the med-
ulla. These processes extend through the mesenchyme of the
head into the orbit and innervate the muscles attached to the
eye-ball. The III nerve is the first to appear (Held) at a time
when 8-9 somites are present (5-6 mm.).

B. THE SPINAL NERVES

The spinal nerves differ from the cranial nerves in two
important respects: (a) they are related primarily with the
mesodermal somites instead of the visceral clefts, and (6) there
are no placodal elements connected with them.

The neural crests continue from the head region as much
smaller strands of cells; these become broken into segments
which are the rudiments of the spinal ganglia. From the neu-
roblasts of each ganglion, cell processes grow out, some centrip-
etally into the cord, forming the dorsal root of the spinal nerve,
others centrif ugally, forming the peripheral afferent fibers which
are distributed chiefly to the skin and other sensory surfaces
(Fig. 46) . The ventral root of the spinal nerve is formed by out-
growths (axons) from neuroblasts in the ventral side of the cord.

THE LATER DEVELOPMENT OF THE FROG

143

They first appear in the anterior part of the body in the larva
of about 4 mm. As they grow outward they meet the dorsal
root, just beyond the ganglion, and pass thence in part to the
mesodermal myotomes, and in part
are distributed with the sympathetic
system. The two most anterior
myotomes are without spinal nerves;
these are occipital in position and
later disappear.

C. THE SYMPATHETIC SYSTEM

The development of the sympa-
thetic system is very imperfectly
known in the frog. The first defi-
nite indication of it appears in the
embryo of about 6 mm., as slight
collections of cells on the spinal
nerves about the level of the dorsal
aorta. From what is known here
and to be inferred from the condi-
tions in other lower vertebrates, it
may be said that these cell groups
are composed of elements from the
spinal ganglia and certain of the
posterior cranial ganglia. These , FIG. 46.— Transverse section

r through 8.6 mm. larva of R.

Cells, COming from the ganglia, mi- esculenta, illustrating the rela-

grate ventro-medially and form a ^J^S^SfSt

pair of longitudinal Sympathetic COrds «• Dorsal aorta; c, spinal cord;

, , , . , .' , , , d, dorsal (sensory, afferent) root

along the Sides of the dorsal aorta Of spinal nerve; m, myotome;

(Fig. 46). From the Cells Of these n' notochord; r, ramus com-

mumcans; sc, sympathetic cord;
COrds processes appear to grOW back sg, spinal ganglion; sn, spinal

to the spinal ganglia forming the %££?* $%£££?*'
rami communicantes, and also* pe-
ripherally to the visceral organs and surfaces. Along the
paths thus marked out fibers grow out from other spinal gang-
lion cells, and quite likely other cells migrate from the cord

sc

144 OUTLINES OF CHORDATE DEVELOPMENT

forming additional sympathetic elements. From the sympa-
thetic cords, cells also migrate peripherally, forming the per-
ipheral sympathetic ganglia in connection with the great blood
vessels and the thoracic and abdominal viscera. The ganglion
of the III cranial nerve is also sympathetic in character, but
its origin is uncertain in the frog, as is also the origin of the sym-
pathetic fibers of the head region in general.

II. THE SPECIAL SENSE ORGANS

1. The Eye

In the preceding chapter we described the earliest traces of
the eyes. These consist of a pair of patches in the superficial
ectoderm of the medullary plate, before this has begun to fold

med-

FIG. 47. — Transverse section through the anterior part of the medullary plate
of an embryo of R. palustris, in which the medullary ridges are just forming.
From Froriep (Hertwig's Handbuch, etc.), after Eycleshymer. au, Optic grooves;
en, endoderm; ep, ectoderm (epidermis); med, medullary plate; ms, mesoderm.

together. The cells of these patches are distinguished by their
comparatively large size and by the presence of pigment in
their outer ends (Fig. 47). When the medullary plate folds
into a tube these patches are carried inward and are left toward
the antero-ventral border of the fore-brain (telencephalon).
Their pigment then gradually disappears, but it is clear that
their originally free ends now border the cavity of the brain.
Before the brain folds have entirely closed together, the regions
surrounding and including these patches have already evag-
inated and formed the pair of optic stalks and vesicles extending

THE LATER DEVELOPMENT OF THE FROG 145

quite to the surface of the head. The cavities of these struc-
tures are continuous with the brain cavity (third ventricle),
so that the relation of the optic cells to the optic vesicle is the
same as to the original cavity of the brain, and the free surfaces
of these cells are now turned away from the surface of the
head ; the true optic cells form the most distal part of the optic
vesicle.

The sensory, or recipient, and the nervous elements of the
eye (retina and optic nerve fibers), originally on the surface of
the head, are the essential parts of the eye; they now form the
optic vesicles, and are to be distinguished from the various
accessory parts (the choroid and sclerotic coats, the aqueous

FIG. 48. — Frontal section through the fore-brain and optic vesicle of an em-
bryo of R. fusca, in which the tail is just growing out. From Von Kupffer
(Hertwig's Handbuch, etc.). a, Optic vesicle; as, opening of optic stalk out of
fore-brain; J, posterior wall of infundibulum; I, rudiment of lens (placode) ;
P, wall of prosencephalon; r, rudiment of olfactory organ.

and vitreous humors, and the cornea), which are derived
chiefly from the mesoderm (mesenchyme) of the region, and
from the ectoderm outside of the optic vesicle (lens and cornea,
in part).

Upon reaching the surface of the head the optic vesicle is
converted into the optic cup. The peripheral part of the ves-
icle becomes flat and then folds into the proximal part, forming
a roughly hemispherical, two-layered cup, obliterating the
original cavity of the optic vesicle and establishing a new
cavity (Figs. 49, 50). The extent of the optic cup is increased

146 OUTLINES OF CHORDATE DEVELOPMENT

immediately by the outgrowth of its free margin, which
gradually draws partially together, leaving a small opening
toward the surface of the head; this is the rudiment of the pupil.
In the optic cup then we distinguish an inner and an outer layer,
and a central cavity; these are respectively, the rudiments of
the true retinal layer, the pigment layer, and the posterior
chamber of the eye.

During the growth and invagination of the optic cup the op-
tic stalk remains attached to its ventral side, so that the retinal

layer of the cup is continuous with
the lower side of the optic stalk
(Fig. 49). The infolding of the
retinal layer is not a simple in-
vagination, but, owing to this ven-
tral attachment of the optic stalk,
the infold is continued as a groove
from the middle of the vesicle to
the ventral border of the cup
where it joins the stalk. This
groove remains narrowly open for
a time and is known as the choroid
fissure, the pupil appearing as a
dilatation of its upper end in the
middle of the cup (Figs. 49, 128).
That part of the cup opposite the
pupil is referred to as the fundus
region.

While the vesicle is invaginating the rudiment of the lens is
formed as a thickening of the ectoderm opposite the pupillary
region (Figs. 48, 50). This thickening involves only the deeper
or nervous layer of the ectoderm and is, in all essential respects,
similar to the ganglionic portion of the ectodermal placodes
described in connection with the cranial nerves. This lens
placode is immediately anterior to the placode of the V cranial
nerve. By the time of hatching this forms a prominent rounded
thickening, which is cut off from the ectoderm as a solid
spheroidal cell mass (Fig. 50). After hollowing out internally

stalk of the frog. /, Choroid fis-
sure; I, lens; pc, posterior chamber
of eye; pi, outer or pigmented
layer of optic cup; rl, inner or reti-
nal layer of optic cup; s, optic
stalk; v, original cavity of optic
vesicle.

THE LATER DEVELOPMENT OF THE FROG 147

FIG. 50. — The development of the eye in the Urodele, Siredon pisciformis.
After Rabl. A. Of embryo with about twenty-five pairs of somites, showing the
thickening of the lens rudiment. B. Invagination of the lens and formation
of the optic cup. C. Lens separating from the superficial ectoderm in an embryo
of about thirty-five pairs of somites. D. Thickening of the inner wall of the lens.
E. Shortly before hatching; differentiation of the rods and cones in the retinal
layer, a, Anterior chamber of eye; c, cavity of primary optic vesicle; co, cornea;
e, ectoderm of head; /, choroid fissure; i, inner or retinal layer of optic cup;
tr, rudiment of iris; k, optic stalk; I, lens; o, outer or pigmented layer of optic
cup; p, posterior chamber of eye.

148 OUTLINES OF CHORDATE DEVELOPMENT

it again becomes solid through the elongation of the cells of its
inner side : the outer side remains as a thin epithelial layer over
the distal surface of the solid lens. When the pupil begins to
narrow the lens moves into the opening and finally remains
included just within it, in the cavity of the optic cup. (In
other vertebrates, except the Teleosts, the lens forms as a hollow
vesicle resulting from an invagination of the surface ectoderm.)

After hatching the cells of the optic cup layers begin to
differentiate into the histological elements characteristic of the
adult eye. The outer layer becomes very thin and pigmented,
while in the thick inner layer the characteristic cell layers of
the retina appear (Fig. 50, D, E). The cells in contact with
the pigment layer gradually differentiate as the rods and cones;
this process begins in the fundus region and spreads thence to
the more peripheral regions of the retina. Other cells of the
retina are neuroblasts and send out nerve processes; those from
the cells bordering the cavity of the optic cup (posterior
chamber) grow down, by way of the margins of the choroid
fissure, to the optic stalk. Entering the ventral and posterior
sides of this, they pass thence to the ventral wall of the fore-
brain, forming there the optic chiasma and optic thalami. The
cavity of the optic stalk is finally obliterated by the collection
of these fibers; in the brain the optic recess marks the region
of its original opening (Figs. 41, 42, 43). The component cells
of the stalk become largely non-nervous, forming the sup-
porting neuroglia cells. The optic stalks are commonly known
as the II pah- of cranial nerves, but it is evident from their
development that they are tracts of the brain, without any
similarities to the true cranial nerves.

The eye develops very slowly during the larval period after
hatching, but at the time of metamorphosis it is rapidly per-
fected. The details in the later development are not very well
known. The rudiment of the vitreous body, occupying the
posterior chamber of the eye, is of mixed origin, although
purely ectodermal. It arises from outgrowths of cells from
the inner surface of the lens placode and also from the retinal
layer of the cup. These elements intermingle and form the

THE LATER DEVELOPMENT OF THE FROG 149

stroma of the vitreous humor or body. In its essential com-
position it thus resembles a typical cranial nerve ganglion which
is derived from placode cells and neural crest; of course, in this
region, the neural crest is not typically present, but the retinal
cells have somewhat similar relations to the neural tube proper.
A day or two before hatching the choroid fissure of the optic
cup begins to close, first in the fundus region. Blood vessels
have already entered the posterior chamber and the margins of
the fissure embrace these. The region last to fuse, at the
margin of the cup, becomes enlarged as the ventral choroid
knot, and from this the iris develops, gradually extending
dorsally around the outer side of the pupil. The cornea and
outer coats of the eye-ball, as well as muscles are formed
from the mesenchyme around the optic cup.

2. The Ear

Like the eye this organ is a complex, derived from diverse
sources; the essential parts, composing the membranous laby-
rinth, are derived from the ectoderm of the surface of the head,
while the accessory parts, tubo-tympanic cavity and columella,
are of endodermal and mesodermal origin. We shall describe
first the formation of the membranous labyrinth or internal
ear.

We have already mentioned the first formation of the auditory
organ as the auditory placode, which appears just as the neural
folds close together (Fig. 45, C). As the embryo begins to
elongate each of these placodes becomes depressed below the
surface of the head and invaginates, forming the ovoid auditory
sac or otocyst, about 0.2 mm. in diameter (Fig. 51, A). For
a time this remains connected with the surface of the head by a
narrow tube of cells, but just before hatching it becomes com-
pletely closed and separates entirely from the surface ectoderm,
sinking in toward the lateral surface of the myelencephalon
(Fig. 51, B). The superficial layer of the ectoderm does not
share in the formation of the auditory sac but remains con-
tinued across the surface of the head outside the invaginating

150 OUTLINES OF CHORDATE DEVELOPMENT

aa

pa

VIII

FIG. 51. — The development of the auditory organ in the frog and toad. A,
B, F, after Krause; C, D, E, after Villy. A. Section through the auditory
vesicle of an embryo just beginning to elongate. B. Section through the audi-
tory vesicle that has very nearly separated from the' superficial ectoderm. C.
Transverse section, somewhat oblique, through the auditory organs of a 12 mm.
R. temporaria. D. Slightly more advanced stage than C. E. Section through
the auditory organs of a 25 mm. R. temporaria. F. Membranous labyrinth of
the toad (Bufo vulgaris). a, Auditory sac; aa, anterior ampulla; ac, anterior
vertical semicircular canal; 6, pars basilaris; d, dorsal outgrowth of primitive
auditory vesicle (rudiment of endolymphatic duct); e, endolymphatic duct;
g, ganglion of auditory (VIII) nerve; he, horizontal semicircular canal; I, lagena
or cochlea; pa, posterior ampulla; pc, posterior vertical semicircular canal:
s, saccule; ss, sinus superior; u, utricle; VIII, auditory nerve.

THE LATER DEVELOPMENT OF THE FROG 151

auditory epithelium. The wall of the auditory sac is only one
cell in thickness, except in its medio-ventral region where the
ganglionic portion of the placode is located. A small finger-
like outgrowth of the sac extends a short distance dorsally, from
its medio-dorsal region: this is the rudiment of the endolym-
phatic duct. From this condition the auditory sac changes very
little until after the opening of the mouth (10-12 mm.) when it
continues its development.

The next differentiations of the auditory sac result from the
formation of various ridges and septa extending into its cavity
(Fig. 51, C, D, E). The first of these appears obliquely along
the outer and posterior walls of the sac, and finally divides the
otocyst into two regions, an inner and upper part, known as
the utricle, and a lower and outer part, the saccule; these two
divisions remain connected by a small perforation in the septum.
The endolymphatic duct is connected with a dorsal extension
of the saccule, while from the utricle the three semicircular
canals grow out. These canals are formed first by the growth
of couples of ridges into the cavity of the utricle, approximately
in the relative positions of the future canals; the couples meet
and fuse save at their ends, so that the cavities enclosed by them
open directly into the utricle. Each rudiment then begins to
enlarge and pushes above the surface of the utricle, first as a
ridge, which becomes plate-like and then tunneled between
the canal and the wall of the utricle. The posterior canal is
formed somewhat later than the anterior and the horizontal
canals. The ampullae are added to the canals by additional con-
strictions of the wall of the utricle.

Shortly after the appearance of the semicircular canals, the
saccuie commences to differentiate. First there appears a
postero-ventral outpocketing, the rudiment of the lagena or
cochlea, which forms a simple sac of considerable size. Then
posteriorly to this appears a second ventral extension, the
basilar chamber (pars basilaris).

Upon the division of the auditory sac into utricle and saccule,
the endolymphatic duct remained in connection with the latter.
The duct slowly elongates dorsally, along the surface of the

152 OUTLINES OF CHORDATE DEVELOPMENT

hind-brain, on the dorsal side of which its tip forms an expan-
sion known as the endolymphatic sac. These sacs enlarge very
considerably, fuse together, and finally, after metamorphosis,
form a vascular structure, covering a large portion of the roof
and sides of the myelencephalon : they remain throughout
life, connecting with the saccule by the narrow endolymph-
atic ducts which pass through openings in the walls of the
auditory capsules (Fig. 51, F).

The epithelial lining of the membranous labyrinth becomes
truly sensory only in certain patches with which fibers of the
VIII cranial nerve are related. These patches are located
in the cochlea (3), utricle (1), saccule (1), and the ampulla
(3). The peril ymph and the cartilaginous and bony labyrinths
are laid down around the membranous labyrinth by the sur-
rounding mesenchyme.

The parts of the middle ear develop relatively late and are
not well differentiated until after metamorphosis. As in
other vertebrates the tubo-tympanic cavity is a derivative of
the pharynx, more precisely of the region of the first gill pouch
(the spiracular pouch, between the hyoid and mandibular
arches; see below). In the frog this gill pouch is vestigial:
it is never perforated, indeed does not contain a cavity, and is
represented only by a fold of the endodermal wall of the
pharynx which does not quite reach to the surface ectoderm.
From the dorsal end of this vestige a rod of cells grows out and
terminates as a solid knob, beneath the eye (Fig. 57). During
metamorphosis spaces appear in this rod and in the terminal
knob, and it moves back into the region of the ear, losing its
connection with the pharynx. After metamorphosis it ac-
quires a secondary connection with the pharynx, and its distal
portion enlarges very considerably, occupying the space be-
tween the ear and the integument of the side of the head:
the integument here later becomes the tympanic membrane,
the expanded cavity is the tympanic cavity, and the narrow
connection with the pharynx is the Eustachian tube.

In the adult the auditory capsule and the tympanic mem-
brane are connected by a rod, the columella, extending across

THE LATER DEVELOPMENT OF THE FROG 153

the tympanic cavity. This is the last part of the auditory
apparatus to be formed. • Its inner end is formed as a cartilage
(the operculum) appearing in the tissue plugging the large
foramen ovate in the outer side of the cartilaginous auditory
capsule. From this region another cartilage, the plectrum,
differentiates, toward the close of metamorphosis, along the
dorsal wall of the tympanic cavity, finally extending to the
tympanic membrane where it connects with a ring-like cartilage
developed from the palato-quadrate cartilage (see below) . The
elements of the columella are thus not genetically related with
the visceral skeleton (palato-quadrate cartilage). While the
opercular part of the columella is becoming chondrified, the
tympanic cavity extends dorsally and finally surrounds it
completely, leaving it in its definitive position crossing the
tympanic cavity.

3. The Olfactory Organ

The olfactory organs appear very early, before the brain
closes, as a pair of ectodermal thickenings either side of the
head, above and anterior to the future mouth region. Only
the deeper nervous layer of the ectoderm is involved in the
thickening, and the superficial layer disappears here, leaving
only its pigment scattered among the remaining cells. These
thickenings are immediately anterior to the lens placodes
and may be termed the olfactory placodes (Fig. 52, A): these
appear to have no relation to the median anterior ectodermal
thickening which is present at this time. These placodes
soon fold inward forming simple olfactory pits, the rudiments
of the true olfactory cavities, their walls becoming the olfactory
epithelium (Fig. 52, B). A few cells detach from the inner
surface of the olfactory placode and mingle with cells derived
from the surface of the telencephalon : these appear to be
equivalent to the crest ganglion, and from them are formed,
apparently, the sheath cells of the true olfactory nerve fibers,
which are outgrowths of the sensory cells of the olfactory
placode.

154 OUTLINES OF CHORDATE DEVELOPMENT

FIG. 52. — The development of the olfactory organ in R. fusca. After Hins-
berg. A, B, C. Sections through the olfactory groove and organ of 5 mm., 6 mm.,
and 11 mm. larvae, respectively. D. Lateral view of a model of the olfactory
organ of a 31 mm. larva. The dotted line marks the limit between the sensory
and non-sensory portions of the epithelial lining of the olfactory cavities, c,
Notochord; ch, internal nares (choanas); d, dorsal lumen; dc, dorsal sac; en, ex-
ternal nares; g, olfactory groove; i, cut edge of integument; in, internal nares
(choanae) ; Z, elongation toward the mouth; la, lateral appendix; m, mouth cavity;
n, inner or nervous layer of ectoderm; ns, part of chamber lined with non-sensory
epithelium; p, olfactory placode; r, ridge marking the limit between middle and
ventral chambers; s, superficial layer of ectoderm; se, part of chamber lined with
sensory epithelium; st, stomodaeum; t, telencephalon; v, thickened bands of super-
ficial ectoderm cells (possibly the vestige of a primitive sense organ) ; vc, ventral
sac; vg, ventral nasal gland attached to Jacobson's organ; x, elevation around
external nares; y, canal leading to olfactory cavity; z, fold around internal narial
opening.

THE LATER DEVELOPMENT OF THE FROG 155

About the time of hatching (6 mm.) a thick strand of cells
extends from each olfactory pit to the roof of the pharynx
just within the limit of the stomodseum (Fig. 52, B). Later
(9-12 mm.) each strand acquires a lumen which opens into the
olfactory sac, and also into the pharynx as the internal nares
or choance (Fig. 52, (7).

The extent of the olfactory cavity is increased by a cavity
formed in a dorsal cell proliferation of the olfactory epithelium.
This region soon forms a separate dorso-lateral lobe which
disappears entirely during metamorphosis.

The surface of the head pushes out above the olfactory sac so
that the duct leading to it is considerably elongated, and mean-
while, on account of the enlargement of the fore-brain and the
formation of the cartilage of the skull in this region, the
openings of the olfactory tubes or external nares are carried to
the dorsal side of the head, so that the entire olfactory organ
extends along a straight perpendicular axis (Fig. 52, D).

During metamorphosis the olfactory organ becomes con-
siderably complicated by the appearance of various foldings
and out-pocketings of its walls, and by a sharp flexure of its
axis. We may mention only the more important of these
outgrowths. The first is an extension from the ventral side
of the olfactory chamber; here a solid mass of cells prolifer-
ates, acquires a cavity, and, enlarging rapidly, turns trans-
versely toward the medial side. This is the rudiment of
Jacobson's organ; a large glandular mass develops upon its
medial end. Other outgrowths are formed from parts of the
olfactory sac that are non-nervous, i.e., lined with indifferent
cells. One of these appears opposite Jacobson's organ and soon
becomes a large sac whose cavity is added to the olfactory
chamber. Another appears anteriorly at the base of the
olfactory duct; this receives the ducts of the lachrymal glands.
Later a dorsal sac grows out from the medial and posterior
walls of the tube. During late metamorphosis the axis of the
olfactory organ is sharply bent on account of the posterior
shifting of the internal nares. In addition to the glands of
Jacobson's organ, other glands appear as outgrowths of the

156 OUTLINES OF CHORDATE DEVELOPMENT

olfactory chamber and in the posterior wall of the internal
nares.

4. The Sense Organs of the Lateral Line

As mentioned above, the sense organs of the lateral line
are derived from the placode of the X cranial nerve, and are
innervated by the ramus lateralis of this nerve. When the
embryo has elongated to about 4 mm. a small dorso-lateral
section of the vagus ganglion separates from the remainder
(Fig. 53, A, B) remaining closely in relation with the ecto-
dermal placode (Harrison). The placode now begins to
elongate posteriorly; the deeper cells multiply rapidly and
form a long narrow tongue which pushes along through the
epidermis just outside the basement membrane (Fig. 53, (7).
Finally, just before hatching, it reaches to the tip of the tail.
Differentiation of this cord progresses posteriorly commencing
in the older anterior part. The cells become grouped at inter-
vals, each group representing the rudiment of a sense organ
of the lateral line. In each rudiment a few central cells be-
come sensory and are surrounded by a layer of enveloping
cells (Fig. 53, D). These groups push up through the epidermal
layer to the surface of the body, and the sensory cells develop
hair-processes.

As the placodal rudiment grows posteriorly it is accompanied
by outgrowths (axons) from neuroblasts of the dorso-lateral
portion of the vagus crest ganglion. These processes lie within
the basement membrane of the epidermis, but when the defi-
nite sense organs develop the nerve fibers pass up among the
sensory cells. The cells forming the medullary sheaths of
these fibers appear to wander along the fibers from the vagus
ganglion.

Similar series of integumentary sense organs are formed in
definite rows on the head, and dorsally from the lateral line;
these are innervated by branches of the VII, IX, and X nerves.
The VIII nerve and the auditory organ also belong in this
group of sense organs. At metamorphosis they all disappear
save the auditory organ and nerve.

THE LATER DEVELOPMENT OF THE FROG

157

so si

FIG. 53. — The development of the lateral line organs in R. syhatica. After
Harrison. A. Part of a frontal section through the level of the notochord of a
3.3 mm. embryo. B. Part of a transverse section through the vagus region of a
4mm. embryo. C. Part of a frontal section through a 4 mm. embryo of R.
virescens. D. Section through the lateral line organ of a 15.5 mm. larva of
R. syhatica. a, Auditory vesicle (in A, its rudiment); 6, basement membrane
of epidermis; ch, notochord; g, gut; gV, trigeminal ganglion, of V cranial nerve;
gVIII, acoustic ganglion of VIII cranial nerve; gX, vagus ganglion; gXl, ganglion
of the lateral nerve (branch of the vagus) ; i, intersegmental thickenings of the
epidermis (ectoderm) ; I, rudiment of lateral line nerve; Ip, lateral plate of meso-
derm; my, myotomes; n, inner or nervous layer of epidermis (ectoderm); nc,
nerve cord; p, pigment in epidermis; s, superficial layer of epidermis (ectoderm) ;
si, inner sheath cells of lateral line organ; sn, sensory cells of lateral line organ;
so, outer sheath cells of lateral line organ.

158 OUTLINES OF CHORD ATE DEVELOPMENT

III. THE ALIMENTARY TRACT AND ITS APPENDAGES

In the preceding chapter we described the formation of the
enteron or gut cavity and its development up to the time the
embryo is just beginning to elongate (Fig. 37). We have de-
scribed, therefore, the formation of the fore-, mid-, and hind-
gut and have seen that up to this time the chief differen-
tiations are connected with the fore-gut. After the mesoderm
and the notochord have been split off from the endoderm, the
wall of the enteron is but one cell layer in thickness, excepting
the floor of the mid-gut which is occupied by the large yolk-
mass. The hind- and mid-gut cavities are narrow, while the
fore-gut expands widely in front of the yolk-mass, and in con-
nection with it we have described the first indications of the
mouth region, of two or three visceral pouches, and of the
liver.

We may proceed now to outline the further development
of each section of the alimentary tract. Before taking up the
history of the fore-gut we must notice the development of
certain structures associated with the mouth.

The stomodceum has already been mentioned as a shallow
median depression of the head, just below the olfactory and
fore-brain region. At hatching this is still rather shallow, but
its floor has come into contact with the wall of the enteron,
establishing a fusion known as the oral plate (Figs. 57, 58, A),
for this is the region where the mouth forms a few days after
hatching (9-10 mm.). In the older larvaB the inner bound-
ary of the stomodffial region is marked by the internal nares or
choanse, which lie just within the boundary between ec to-
dermal and endodermal territory. The formation of the oral
sucker, just below the stomodaeal invagination (Fig. 57), was
described in the previous chapter.

The margins of the stomodaeum are at first formed chiefly by
the mandibular ridges, but soon the integument above these
becomes drawn out in the form of lips. The mouth itself
remains small in the tadpole, but the lips, of which there are
an upper and a lower, soon project considerably in front of

THE LATER DEVELOPMENT OF THE FROG 159

the mouth, enlarging the stomodseal cavity; the lower lip is the
larger and is freely movable (Fig. 58, B). The lips form the
important feeding organs of the tadpole, and as such they
become furnished with various horny structures, described
as teeth and jaws (Fig. 58, B), but not at all to be compared
with the true teeth and jaws which develop later. These horny
structures are purely larval organs and are entirely lost at the
time of metamorphosis. The " teeth" develop from strands or
piles of cells of the deeper layer of the epidermis. Each cell,
as it nears the surface, undergoing cornification, becomes conical
in form, and pushes through the skin, soon to be replaced by the
next cell (" tooth") underlying it. The upper lip bears three
medially interrupted rows of these " teeth," the lower lip four
complete rows. Toward the base of each lip, near the mouth,
a closely set row of teeth, together with intermediate horny
cells, form a continuous ridge; these ridges, of which that of the
lower lip is the larger, form the "jaws" or beak of the tadpole.
During metamorphosis the horny teeth and jaws are lost, the
lips are retracted, and as the mouth rapidly enlarges the true
teeth and definitive jaws are formed.

1. The Derivatives of the Fore-gut

The organs derived from the fore-gut region that we shall
describe, are the pharynx, oesophagus, stomach, liver and pan-
creas; in connection with the pharynx we shall describe the
development of the visceral pouches and arches, the internal
and external gills, the thymus, the ultimo branchial bodies,
epithelioid bodies, the thyroid body, tongue, and the lungs.

In front of the yolk-mass the fore-gut is widely expanded
transversely as the pharyngeal cavity (Fig. 37) ; antero-ventrally
its wall is fused with the ectoderm as the oral plate, while
postero-ventrally the liver region is indicated as a small cavity
extending backward beneath the yolk. Dorsal to the yolk the
fore-gut is narrowed as the rudiment of the oesophagus. Along
the sides of the pharynx a series of vertically elongated ridges,
or solid outfoldings, appear and extend to the surface ectoderm

160 OUTLINES OF CHORDATE DEVELOPMENT

ol

with which they fuse (Figs. 54, 57). These are the visceral
pouches. They appear very early and the formation of the first
two or three pairs was mentioned in the preceding chapter.
Altogether six pairs are formed, decreasing in size and impor-

tance posteriorly. As these
pouches extend out to the ecto-
derm they divide the mesodermal
tissue lying between ectoderm and
endoderm, into a series of ver-
tical rods known as the visceral
arches. The most anterior visceral
pouch is the hyomandibular; in
front of it, between this and the
mouth, lies the mesodermal man-
dibular arch. The remaining
pouches are the first to fifth
branchial pouches. Between the
hyomandibular and first branchial
pouches is the hyoid arch, while
between successive branchial
pouches are the branchial arches.
Like the pouches these diminish
in size posteriorly until the last
is quite small and incompletely
marked. Some additional facts
FIG. 54.— Diagram of a frontal regarding the last branchial pouch

section of a frog larva at the time of ° r

hatching. After Marshall (modi- will be mentioned later in connec-
* tion with the ultimobranchial

lum; in, intestine; n, nephrostome; bodies.

o, base of optic stalk; ol, olfactory . .

pit (placode); p, pharynx; t, pro- About the time the mouth IS

nephric tubules; II, hyoid arch; nr,pr,Arl Qr»Qnmj arm^ar within *>ar>Vi

ni-vi, first to fourth branchial opened^ spaces appear witnm eacn

arches; 1, hyomandibular pouch; branchial pOUch; these Cavities
2-6, first to fifth branchial pouches. -, .. ..-, .-, •,

become continuous with the phar-

yngeal cavity, and soon perforate the area of ectodermal
and endodermal fusion, forming the branchial clefts or gill
clefts. The second and third clefts are perforated earliest,
and soon after, the first and fourth. The hyomandibular

THE LATER DEVELOPMENT OF THE FROG 161

pouch is never perforated; shortly before the opening of the
second and third clefts it loses its connection with the ectoderm
and gradually disappears. The formation, from the dorsal wall
of the hyomandibular pouch, of the rudiment of the tubo-
tympanic cavity of the ear, has already been described (Fig. 57).

The chief structures associated internally with the visceral
arches are the aortic arches and the visceral skeleton, the devel-
opment of which will be described in later sections. From the
external surface of certain visceral arches are developed the
gills, both external and internal. Reference has previously
been made to the external gills: these appear just before hatch-
ing, as small outgrowths from the outer surfaces of the dorsal
ends of the first and second branchial (second and third visceral)
arches (Fig. 22, G.) Later a small external gill appears on the
third branchial arch. The two anterior pairs grow very rapidly
and about the time the mouth opens -they form large branched
or lobed processes, extending out from the sides of the pharynx
(Figs. 64, 65). They become extremely vascular and are the
earliest respiratory organs of the tadpole. The posterior pair
remains small and comparatively simple.

After a few days the external gills become covered by the
operculum, and then they are gradually absorbed and finally
disappear completely. The operculum makes its first appear-
ance before the perforation of the mouth, as a pair of out-
growths from the posterior borders of the hyomandibular
arches. These folds grow backward rapidly, and just as the
external gills reach their maximum development, the operculum
extends to and outside of them, enclosing them in an opercular
cavity. This cavity finally becomes entirely enclosed on the
right side by the fusion of the posterior border of the right
opercular fold with the surface of the body; this fusion
extends across the ventral side also, and thus puts the right
cavity in connection with the left (Fig. 58, B). The left fold
remains partly free and the margins of the opening are drawn
out forming a short opercular tube or "spiracle."

The internal gills appear just after the gill clefts are perfo-
rated, about the time the mouth opens, as a series of small

162 OUTLINES OF CHORDATE DEVELOPMENT

elevations on the postero-external faces of the branchial arches
(Figs. 64, 65). Like the external gills, these are covered with
a thin layer of ectoderm cells which move in, covering their
original endodermal coat. These rudiments soon become
doubled on the first three branchial arches, but remain in a
single row on the fourth branchial arch. They enlarge rapidly
and form long branched processes or gill filaments, along the
whole border of the arch below the external gills. The fila-
ments become very vascular and project freely into the oper-
cular cavity, where they are bathed in the respiratory current
entering the mouth and passing out through the gill clefts and
opercular tube.

The inner borders of the branchial arches become serrated
by the formation of a series of papilla, forming a kind of filtering
organ (Fig. 64, D, E). The continued widening of the dorsal
part of the pharynx throws the branchial portion into a ventral
position, and then this whole region becomes partly separated
from the dorsal region by the anterior and posterior folds of
the pharyngeal floor; these are the velar plates (Fig. 64, D, E).

As the period of metamorphosis approaches, the opercular
cavity and the gill clefts become occluded by the rapid pro-
liferation of the cells lining these spaces, and of the gills them-
selves. The most of this solid mass of cells becomes completely
resorbed. Various structures of the young frog are derived
from vestiges of the gill clefts.

The thymus body appears just before hatching, as a solid
internal proliferation from the epithelium of the upper side of
the first branchial pouch (second visceral, or hyobranchial
pouch) (Fig. 56). A similar smaller proliferation from the
hyomandibular pouch has only a transitory existence. The
thymus rudiment enlarges slowly, separating from the wall of
the pouch at about 12 mm. After metamorphosis the thymus
bodies are seen toward the outer surface of the head, just back
of the auditory capsule and jaw articulation.

From the dorsal ends of the other branchial clefts somewhat
similar bodies are formed; these become lymphoid and appear
to have no correspondence with the thymus rudiments. From

THE LATER DEVELOPMENT OF THE FROG

163

ihe ventral ends of the anterior gill pouches additional epithelial
proliferations are formed about the time the internal gills

th

ub

FIG. 55.

FIG. 56.

FIG. 55. — Diagram of the branchial pouch derivatives in the frog. After
Maurer, with Greil's modification, eg, Carotid gland; e\, 62, ea, epithelioid bodies;
ih, thyroid body; tmi, tmz, thymus bodies; ub, ultimobranchial body; I-VI, first
to sixth visceral pouches. (/, hyomandibular; II-VI, first to fifth branchial
pouches.)

FIG. 56. — Diagrams of the derivatives of the visceral pouches and arches in
the frog. After Maurer, with Greil's modification. A. Lateral view, frog larva.
B. Lateral view, after metamorphosis. C. Transverse section through gill of frog
larva. D. Transverse section through gill region, just after metamorphosis;
the gills have not quite disappeared, a, Afferent branchial arteries; c, carotid
gland; d, dorsal gill remainder; e, epithelioid bodies; g, internal gills; m, middle
gill remainder; o, operculum; s, supr^apericardial or postbranchial body; t, thyroid
body; th, thymus bodies; v, ventral gill remainder; I-VI, visceral arches;
/, mandibular arch; II, hyoid arch; 1 1 I-VI, first to fourth branchial arches;
1-6, visceral pouches; 1, hyomandibular pouch; 2, hyobranchial pouch; 3-6,
first to fourth branchial pouches.

appear. Those derived from the first branchial pouch form the
carotid glands, while the others form the so-called epithelioid

164 OUTLINES OF CHORDATE DEVELOPMENT

bodies. These remain present throughout life, lying just
below the aortic arches (Fig. 56).

A body described as the pseudothyroid body appears in the
postero- ventral branchial region; this seems to have no relation
with the remains of the disappearing gill clefts. In addition to
the dorsal remains of the gill clefts, mentioned above, mid-

ep

FIG. 57. — Semi-diagrammatic optical section of the head of a 7.5 mm. larva
of R. temporaria, illustrating the relations of the visceral pouches and chondro-
cranium. After Spemann. The wall of the pharynx toward the observer has
been removed, so that the visceral arches are shown in section, a, Auditory
organ; ac, anterior ascending process of the palato-quadrate cartilage; e, eye;
E, rudiment of Eustachian tube; ep, epiphysis; h, hypophysis; hy, hyoid cartilage;
ra, oral membrane; md, mandibular cartilage; n, notochord; o, olfactory organ;
os, oral sucker (in section); p, pharyngeal cavity; pq, palato-quadrate cartilage;
s, stomodseum; t, trabecular cartilage; tc, trabecular cornu; th, rudiment of
thyroid body; ty, rudiment of thymus; 1-4, first to fourth visceral pouches.

die and ventral traces may be seen for some time after
metamorphosis.

A pair of ultimobranchial bodies, known also as post-branchial
or suprapericardial bodies, are found in the frog, lying posterior
to the fifth visceral pouch. These are formed as solid pro-
liferations from the pharyngeal wall just back of the fifth
visceral pouch (fourth branchial pouch). They clearly repre-

THE LATER DEVELOPMENT OF THE FROG 165

sent the vestiges of a sixth pair of visceral pouches, although
they never extend out as far as the surface ectoderm. They
soon separate from the pharyngeal wall and acquire internal
cavities, remaining in the floor of the pharynx, in a supraperi-
cardial position (Figs. 54, 55, 56).

The remaining structures of the pharyngeal region have no
genetic relationship with branchial structures. The thyroid
body appears just before hatching, as a median evagination,
narrow and elongated, from the floor of the pharynx (Fig. 57).
This slowly pinches off from the pharyngeal epithelium,
forming a solid rod of cells, and a few days after the opening of
the mouth it divides into a pair of bodies, which then enlarge
rapidly and become very vascular.

The lungs appear just before hatching as a pair of solid
proliferations from the ventral wall of the posterior part of the
fore-gut, between the yolk-mass and the heart. These rudi-
ments slowly extend posteriorly along the sides of the fore-gut,
and early acquire cavities proximally. Some time after the
opening of the mouth, the wall of the fore-gut between and
around the openings of these diverticula, becomes depressed
as a transverse groove, the laryngeal chamber (Fig. 58, B),
which is then partly constricted off from the alimentary tract;
the opening that remains is the glottis. The lungs now rapidly
elongate, pushing out into the body cavity and becoming very
vascular (Fig. 72); the mesodermal constituents surrounding
the endodermal lining of the lungs, are derived from the
splanchnic mesoderm.

The tongue appears very late, just before metamorphosis.
It is first indicated as an elevation in the floor of the anterior
part of the pharynx, just back of the region from which the
thyroid body was derived. In front of this elevation, between
it and the lower jaw, the floor of the pharynx is depressed and
glandular. During metamorphosis the rapid anterior extension
of the tongue carries this glandular area upward so that it
lies on the free anterior tip of the tongue.

The liver appears very early, even before the embryo begins
to elongate, as a postero-ventral extension of the cavity of the

166 OUTLINES OF CHORDATE DEVELOPMENT

ep

B

ht

I i PV o

FIG. 58. — Diagrams of median sagittal sections of the anterior ends of frog
larvae. After Marshall. A. Of a larva just before the opening of the mouth.
B. Of a 12 mm. larva (at the appearance of the hind-limb buds), a, Auricle;
ao, dorsal aorta; 6, gall bladder; bh, basihyal cartilage; ch, cavity of cerebral
hemisphere (lateral ventricle); e, epithelial plug closing the oesophagus; ep,
epiphysis; g, glottis; h, hypophysis; H, hind-brain; hr, cerebral hemisphere; ht,
horny "teeth"; hv, hepatic vein; i, intestine; if, infundibulum; /, lower jaw;
Z, liver; ly, laryngeal chamber; ra, mouth; M, mid-brain; mb, oral membrane (oral
septum); n, notochord; o, median portion of opercular cavity; oe, oesophagus;
p, pharynx; pb, pineal body; pc, pericardial cavity; pd, pronephric (mesonephric)
duct; pt, pituitary body; pv, pulmonary vein; pill, choroid plexus of third ven-
tricle; pIV, choroid plexus of fourth ventricle; r, rostral cartilage; ro, optic recess;
s, stomodseum; sv, sinus venosus; £,' thyroid body; ta, truncus arteriosus; tp, tuber-
culum posterius; v, ventricle; w, inferior (posterior) vena cava.

THE LATER DEVELOPMENT OF THE FROG

167

fore-gut, beneath the yolk-mass (Fig. 37). This rudiment
enlarges very slowly at first, the solidity of the yolk preventing
its penetration. The liver lies just posterior to the heart and
separated from it only by a mass of scattered mesoderm cells,
which come to be added to the anterior wall of the liver diver-
ticulum, forming its mesodermal components. Some of the
yolk cells adjoining the liver appear to be added to it, forming
true hepatic cells. After hatching, the wall of the anterior
part of the diverticulum
becomes folded, and later
forms the chief part of
the definitive liver (Fig.
58, A). The postero-
ventral extension of the
diverticulum is the rudi-
ment of the gall-bladder,
which becomes somewhat
separated from the ante-
rior hepatic portion; the
original opening of the
diverticulum out of the
fore-gut remains as the
bile-duct (Figs. 58, 59).

In later stages the liver

FIG. 59. — Models of the digestive tract
of frog embryos. After Hammar (Maurer.)
A. Lateral view of the tract of a 7 mm. larva.
The anterior portion has been opened by a
median sagittal section. B. Dorsal view of
the tract of an 8.5 mm. larva, d, Ductus
choledochus; g, gall bladder; h, liver; Z,
enlarges Very Considerably lung; m, mid-gut; p, pancreas; pd, dorsal
and Shifts its position pOS- rudiment of Pancreas; r, rectum.

teriorly; the gall-bladder also becomes very large in the
tadpole.

The pancreas develops in the region where the liver diver-
ticulum originally opens out of the fore-gut (Fig. 59). It
arises from three rudiments. A dorsal rudiment appears as a
solid outgrowth of the dorsal wall of the fore-gut, from which
it soon separates entirely. Right and left ventral rudiments
grow out from the fore-gut, just in the posterior margin of the
opening of the bile-duct. These ventral rudiments, retaining
a common connection with the gut, then enlarge and, passing
around the sides of the bile-duct, fuse together in front of it.

168 OUTLINES OF CHORDATE DEVELOPMENT

Later the dorsal rudiment unites with the fused ventral
parts, and the entire pancreas is then connected by the pan-
creatic duct with the ventral wall of the gut. The opening of
the pancreatic duct marks the boundary between the fore- and
mid-gut regions during these early stages; later the opening of
the duct shifts just within the margin of the bile-duct.

The chief steps in the differentiation of the oesophagus,
stomach, and intestines occur just after hatching. The region
between the lung rudiments and the openings of the hepatic
and pancreatic ducts, elongates as the region from which the
oesophagus and stomach are formed (Fig. 59). Shortly after
hatching (8 mm.) the anterior end of the oesophagus becomes
completely occluded by a proliferation of its wall just anterior
to the laryngeal opening (Fig. 58, A). The oesophagus remains
closed until shortly after the opening of the mouth (10-11 mm.)
when it reacquires cummunication with the pharynx. The
stomach appears as a dilation of the posterior portion of the
fore-gut. Its axis is at first longitudinal, but soon it becomes
bent so as to lie transversely. Throughout the larval period
the stomach remains comparatively small and not clearly
marked off from oesophagus and intestine.

2. The Derivatives of the Mid-gut

Up to the time of hatching the mid-gut remains as a narrow
opening, dorsal to the yolk-mass which forms the floor of this,
the intestinal region; its roof and sides are but one cell thick
(Fig. 37). After hatching, the yolk is rapidly absorbed and
the intestine begins to elongate. The process of yolk absorp-
tion is most rapid during the first week after hatching; in part
the yolk cells degenerate, and in part they become modified
into the glandular epithelium of the intestinal wall. Some of
the cells of the endodermal lining of the intestine seem to
wander outside the wall of the gut, into the mesentery (see
below) and contribute to the formation of lymphatic tissue.

As a result of the elongation of the intestine it becomes
thrown into a transverse or duodenal loop, extending across

THE LATER DEVELOPMENT OF THE FROG 169

the body cavity from the posterior end of the stomach (Fig. 59).
The elongation of the intestine continues rapidly, and soon it
becomes thrown into a double spiral which occupies the entire
ventral part of the body cavity. At its maximum length it is
about nine times the length of the body. The oesophagus
and stomach also elongate somewhat during this period, so
that the pancreas and liver are pushed back into the body
cavity. The relations of the mesentery are described below.
During the period of metamorphosis the entire digestive tract
shortens to about one-third its maximum larval length; this
shortening affects chiefly the intestine and stomach.

One structure developing in connection with the enteron
has not been mentioned as yet; this is the hypochordal rod.
This has no direct relation with the notochord. It appears
in tadpoles of about eight somites (3-4 mm.) as a median
ridge along the outer surface of the endodermal wall of the mid-
gut (Fig. 70, C). Later this ridge extends both anteriorly
and posteriorly, as the part first formed separates from the
enteric wall; it becomes entirely free at about 4.6 mm. Finally
it extends the entire length of the gut posterior to the dorsal
pancreas; through the tail it lies above the postanal gut. It
is a narrow rod, only two or three cells in diameter, lying be-
tween the dorsal aorta and the notochord. Shortly after
the opening of the mouth (13 mm.) it breaks into short pieces
and its cells either disappear or scatter; in the older larva no
traces remain.

3. The Derivatives of the Hind-gut

This is the smallest section of the enteron. We have de-
scribed, in the preceding chapter the formation of the neuren-
teric canal and proctodaBum, and the terminal dilation of the
enteron which becomes the rectal region (Fig. 37). Just after
the tail has begun to elongate (4 mm.) the fusion between the
rectal and proctodaBal walls becomes perforated by the anal
opening, so that the gut opens directly to the outside. The
proctocteal region becomes the cloaca of the tadpole and frog,

170 OUTLINES OF CHORDATE DEVELOPMENT

and receives not only the opening of the rectum, but the
openings of the excretory and reproductive ducts as well. The
urinary bladder is formed just before metamorphosis as a ven-
tral outgrowth from the cloaca.

As the tail grows out, the nerve cord and notochord extend
into it, while the true enteron remains limited to the body
region, and the neurenteric canal consequently is drawn out
posteriorly. It soon cuts, off from the nerve cord, but for a
time its antero- ventral limb remains open into the rectum and
is known as the postanal gut. This gradually closes, and by
the time of hatching it is represented only by a strand of cells
extending posteriorly from the rectum, nearly to the tip of
the tail; finally it disappears entirely. Throughout the larval
stage the rectum remains short and only slightly dilated;
during metamorphosis it enlarges and elongates, forming a
considerable terminal portion of the alimentary canal.

IV. THE MESODERMAL SOMITES

All of the remaining systems are primarily associated with
the mesoderm. In the preceding chapter we described the
early history of the mesoderm and in a few words we may re-
call its arrangement at the time the larva is about to commence
its elongation.

In the body region the mesoderm is already differentiated
into the thickened proximal portion along the chorda, known
as the segmental or vertebral plate, and the thinner peripheral
lateral plate, which passes around the sides of the yolk-mass
to the ventral surface. Dorso-laterally the lateral plate is
split into two sheets, the outer or somatic layer, and the inner
or splanchnic layer, separated by a narrow splanchnoccel or
rudimentary body cavity (Fig. 70, A). Through most of
the body region the vertebral and lateral plates are continuous
and the cavity of the lateral plate is continued into the verte-
bral plate as the myoccel At this stage, however, in the an-
terior body region, the vertebral plate is already transversely
divided into three or four pairs of somites, which have separated,
distally, from the lateral plate.

THE LATER DEVELOPMENT OF THE FROG 171

m

In the region of the head and pharynx the mesoderm is
in the form of scattered groups of cells, mesenchymal in charac-
ter, filling the irregular spaces among the organs of these
regions, brain, sense
organs, ganglia, gill-
pouches, etc. Some of
the details of the later
history of this mesoderm
have already been men-
tioned in connection
with the visceral
pouches, and others will
be considered with the
history of the vascular
and skeletal systems.
We may mention here,
however, the essential
facts regarding the
development of the
somites and lateral
plate.

The formation and
differentiation of the
somites and lateral plate
occur progressively in
the posterior direction,
so that in a young larva
all of the process may

* 4 *

be read in a Series Of

A , •

transverse Sections.

The Cavity Of the SO-

. ,.
mite, the myOCOel, lies

toward its surface; the
outer wall, only one cell thick, forms the cutis plate or derma-
tome, lying just beneath the surface ectoderm (Fig. 60).
The inner wall of the somite is much thickened as the
myotome or muscle plate; through the continued thickening

_ __ „,

FIG. 60. — Transverse section through the
sixth mesodermal somite of a 5 mm. larva of R.
temporaria, illustrating the arrangement of the
mesoderm. From Maurer (Hertwig's Hand-
buch, etc.). c, Cutis plate; Ch, notochord; D,
gut wall; m, myotome (muscle plate) ; we, nerve
cord; p, lateral plate ;», ventral process of my o-

torae and cutis plate'

172 OUTLINES OF CHORD ATE DEVELOPMENT

of the myotome the myocoel is early obliterated. The
myotomal cells or muscle cells, elongate antero-posteriorly
through the entire segment; the formation of muscle fibrillse
in these cells begins very early (5 mm.) on the side toward
the chorda (Fig. 53).

From the ventro-medial portion of the myotome, cells prolif-
erate and move downward below the chorda, and upward be-
tween the chorda and the myotome, forming the rudiment of
the sclerotome. The somite now separates entirely from the
lateral plate, and soon the sclerotome separates from the somite,
and extends dorsally around the nerve cord, forming a consider-
able mesenchymal mass surrounding this and the notochord.
This is the region where the cartilaginous vertebral column
forms later.

Just after the separation of the sclerotome (5 mm.) the
myotome and dermatome send down a ventro-lateral out-
growth, which soon separates from the myotome and forms
later the ventral musculature (Fig. 60); from the myotomes
of the limb regions these outgrowths extend into the rudiments
of the limbs, later giving rise to their voluntary musculature.

The cutis plate breaks into groups of branched mesenchyme
cells, some of which become applied to the inner surface of
the ectoderm and form the dermal layer of the dorsal half of
the embryo, while others pass in between the mytomes,
forming the connective-tissue septa or myocommata.
• In the trunk region of the frog, thirteen pairs of somites are
formed altogether, but the two anterior pairs disappear about
the time the limbs appear, leaving eleven in the adult. The
region of these two transitory somites later becomes incorpo-
rated into the head, as the occipital region. The accompanying
table, based upon the observations of Elliot, summarizes the
history of the somites and spinal nerves of the body region
of the embryo. In the tadpole there is, of course, a large, and
varying, number of somites in the tail region; Harrison has
counted about forty-five pairs in a 5.5 mm. larva of Rana
virescens. All posterior to the thirteenth (eleventh of the
adult series) disappear during metamorphosis.

THE LATER DEVELOPMENT OF THE FROG

173

TABLE OF SOMITES, VERTEBRA, AND RELATED NERVES OF
THE TADPOLE (ELLIOT)

Cartilaginous
elements in
sclerotome

Somites

Nerves

Rmbryo

Adult

Adult

Occipital
region of
skull

1

Absent (Disappears at forma-
tion of limbs)

Boot of vagus nerve

2

Absent (Disappears at forma-
tion of vertebrae)

No nerve. Ganglion
only

in embryo

3

1

Ganglion and nerve
Absent in adult

in embryo.

1 vertebra

4

2

1 spinal nerve ("hypoglossal")

2 vertebra

5

3

21
— f brachial plexus

3j

3 vertebra

6

4

4 vertebra

7

5

4

5 vertebra

8
9

6

5 !• to body wall

^J

6 vertebra

7

7 vertebra

10

8

7j

8 vertebra

11

9

8 [• sciatic plexus

•1

9 vertebra

r»

10

Part of uro-
style

[»

11

10 to pelvic region

Before the separation of the somites and lateral plate, the
latter shows traces of segmentation in the region adjoining the
somites, from which later the pronephros is formed (see below).
This region may therefore be termed nephrotome or intermediate
cell mass. These traces disappear, very quickly, and the lateral
plate itself is never segmented. The cavity of the lateral plate,
the general body cavity, gradually extends ventrally, and finally
divides the entire lateral plate into somatic and splanchnic
layers. Except in the extreme anterior and posterior ends of
the trunk, the cavities of the two sides meet and fuse across
the mid- ventral line, establishing a continuous body cavity and

174 OUTLINES OF CHORDATE DEVELOPMENT

completely separating the somatopleure , or body wall, consisting
of the somatic mesoderm and integument, from the splanchno-
pleure, or gut wall, consisting of splanchnic mesoderm and
enteric wall.

In the pharyngeal region, the layers of mesoderm remain
fused together medially, below the gut; consequently the
splanchnocoel is paired in this region, where the heart develops
later. The median fusion is a vestige of a ventral mesentery.
Along the dorsal side of the enteron, the splanchnic layers of
mesoderm push in between the chorda and the enteron, and
form the dorsal mesentery by which the gut remains connected
with the dorsal wall of the body cavity, and through which
later the vessels, nerves, etc., pass to and from the gut. When
the yolk is absorbed and the narrowed gut passes to the ventral
side of the body cavity, the mesentery forms a thin double
fold of membrane. Then as the intestine elongates the mesen-
tery is thrown into folds corresponding with those of the gut.

Through the absence of a ventral mesentery, save in the heart
region, the body cavity is continuous from side to side beneath
the gut; dorsally the mesentery interrupts such a communica-
tion. Later on, the body cavity becomes incompletely divided
transversely into anterior and posterior parts, but this and the
formation of the pericardial portion of the body cavity, are
more conveniently described in connection with the vascular
system.

V. THE VASCULAR SYSTEM

1. The Heart

The first parts of the vascular system to appear are the
heart and the large veins connected with its posterior .end.
We have already said that the cardiac region lies beneath the
hinder part of the pharynx, immediately anterior to the liver
and posterior to the thyroid body. In this region the somatic
and splanchnic layers of the lateral plate are separated by a
wide cavity which is the beginning of the pericardial cavity
(Fig. 61). This is at first directly continuous posteriorly with

THE LATER DEVELOPMENT OF THE FROG

175

the general body cavity, though we shall see that later it be-
comes completely closed off. Dorsally there is no definite
coelomic space in this, the pharyngeal region. The pericardial

FIG. 61. — Sections showing the formation of the heart in the frog. A-D.
Series of transverse sections through corresponding regions of a series of embryos
of R. temporaria. After Brachet. E. F. Sections through the same region in
older embryos of R. sylvatica. A. 2.6 mm. embryo. Mesoderm approaching
the mid-line; endothelium appearing. B. Older embryo of same length as A.
C. 3 mm. embryo showing enlargement of pericardial cavity and the begin-
ning of the folding of the somatic mesoderm. D. 3.2 mm. embryo. Endothelial
cells becoming arranged in the form of a tube. E. Embryo of about 3 mm.
F. Embryo of 5-6 mm. Heart tube established; dorsal mesocardium still
present, dm, Dorsal mesocardium; e, cardiac endothelial cells; en, endoderm;
g, wall of gut (pharynx); p, pericardia! cavity; so, somatic layer of mesoderm;
sp, splanchnic layer of mesoderm.

wall and the muscular wall of the heart are derived from the
lateral plate mesoderm, while the inner lining of the heart, the
endothelium, is derived from scattered mesoderm cells . lying

176 OUTLINES OF CHORDATE DEVELOPMENT

between the splanchnic mesoderm and the enteron, cells that
have been formed from the endoderm in the same way that
much of the lateral plate mesoderm has been, i.e., through a
splitting off of cell groups from the surface of the enteric wall
(Fig. 61). These scattered mesoderm cells are often regarded
as belonging primarily with the ventral ends of the hyoid
visceral arches. They become distinct by the time two
mesodermal somites are formed.

Fig. 61 shows how the layers of the lateral plate extend
beneath the pharynx, remaining fused in the mid-line as the

ra

FIG. 62. — Diagrams of frontal projections of the hearts of early frog embryos-
After Weber. A. Heart of an embryo of 2.7 mm. showing the median bulbus
arteriosus and the separate auricular and ventricular cavities. B, Heart of a
3.2 mm. embryo showing the fusion of the auricular and ventricular cavities.
The broken line marks the incomplete separation between the endothelial auri-
cular and ventricular regions. C. Heart of a 3.5 mm. embryo. At this stage the
ventricle is strongly looped ventrally. a, Auricle; ba, bulbus arteriosus; ra, roots
of aortic arches; s, incomplete septum between endothelial tubes of auricle and
ventricle; v, ventricle; vl, root of left vitelline vein; vr, root of right vitelline vein.

ventral mesocardium. The inner or splanchnic wall of the
pericardial cavity now folds together dorsally, enclosing the
endothelial cells, which have become arranged in the form of a
short tube. Finally the splanchnic folds meet and fuse dor-
sally, forming a tube outside of the endothelial tube and con-
nected with the dorsal wall of the pericardial cavity; this tube
forms the muscular wall of the heart and the connection is the
dorsal mesocardium.

The endothelial tube, which is to be regarded as the primary
rudiment of the heart, really consists of a pair of short tubes

THE LATER DEVELOPMENT OF THE FROG 177

(Weber); these very early fuse together anteriorly forming a
median region, the future bulbus aortce (Fig. 62). From the
antero-lateral margins of the bulbus, two short strands of cells
extend forward in the floor of the pharynx as the rudiments
of the bifurcated truncus arteriosus or ventral aortce. Posteriorly
the two endothelial tubes are only incompletely fused and are
asymmetrically developed. That of the right side forms a
dilated flexed tube which is the rudiment of the ventricle and
the right vitelline vein, while that of the left side is more elon-
gated and is dilated posteriorly as the rudiment of the auricle,
continuing posteriorly as the left vitelline vein (Fig. 62). Both
vitelline veins pass directly into the liver and yolk-mass. These
two cardiac tubes gradually fuse more extensively and their
cavities become somewhat confluent, so that the ventricular
region is in a small degree formed of the left tube also; the
more posterior auricle similarly receives a small addition from
the end of the right tube with which the right vitelline vein
is continuous.

The heart rudiment begins to elongate at once and is thrown,
by horizontal folds, into an S-form, whereupon the dorsal meso-
cardium disappears, leaving the heart tube attached to the peri-
cardial wall only at its ends. The posterior limb of the heart
lies toward the left side and abuts against the liver; this forms
the region of the sinus venosus and auricles. The anterior
section, and the right or middle section which is the region of
the ventricle, soon swing downward, becoming relatively
ventral in position, while the auricle then extends through nearly
the entire dorsal part of the pericardial cavity (Fig. 66).

These limbs of the heart tube are very early separated from
one another by constrictions. Shortly after the opening of the
mouth the auricle becomes divided into right and left auricles by
the downgrowth of the interauricular septum from its dorsal wall.
The sinus venosus remains connected with the right auricle.
The left auricle receives the pulmonary veins, but these are
only slightly represented during the tadpole stage. The wall
of the ventricle becomes much thickened by the ingrowth of
a muscular network from its inner surface. A few davs after

178 OUTLINES OF CHORDATE DEVELOPMENT

the mouth opens, the bulbus aortae becomes divided into the
anterior and posterior parts characteristic of the adult frog,
and in the former, now known as the truncus arteriosus, a
longitudinal fold appears separating its cavity into right and
left channels.

2. The Origin of the Blood and Vessels

Details regarding the exact method of origin of the blood
vessels of the frog are scanty. For the most part they seem to

FIG. 63. — Sections showing the formation of the blood islands in the frog.
After Brachet. A. Part of a transverse section through the middle of the yolk
region of a 2.8 mm. embryo of R. temporaries. B. Same of a 3.2 mm. embryo.
en, Endothelium; i, blood island; m, mesoderm.

arise (4-4.5 mm.) as irregular and often isolated lacunar spaces
in the mesenchyme and splanchnic mesoderm. The cells bor-
dering these spaces gradually form a definite boundary and the
sinuses thus formed are linked into continuous vessels. In

THE LATER DEVELOPMENT OF THE FROG 179

some cases the smaller vessels seem to be preformed as short
solid strands of cells, which become rearranged to form the
walls of hollow tubes.

At first these vessels, like the heart itself, are devoid of
cellular (corpuscular) elements. Some have described the
origin of blood corpuscles directly from the walls of the vessels,
but it seems doubtful whether such a process is at all common.
For the most part the blood corpuscles are formed from a large
group of blood islands, groups of cells occupying the ventral side
of the yolk-mass, between the liver diverticulum and the ventral
margin of the original blastoporal region (Fig. 63).

The ventro-lateral surfaces of the endodermal yolk-mass, as
we have seen, give off the mesoderm by delamination, but in
this ventral region the superficial cells of the yolk-mass split
off irregularly in groups. These cell groups are the blood islands
(Brachet). While some of these cells are converted into the
walls of the veins of the yolk, they are mostly transformed into
red blood corpuscles, which thus enter the circulation by way
of these veins. The corpuscles enter the circulation in Iarva3
of about 5 mm., and for some time their origin from the yolk
region is indicated by their abundant yolk content; not until
after hatching do they assume the histological characteristics
of the definitive corpuscles.

3. The Arterial System

The earliest arteries to appear (about 4 mm.) are .the paired
lateral dorsal aorta, dorsal to the pharyngeal region. At first a
series of separate spaces or lacunae in the mesenchyme of the
head, these soon connect forming definite vessels extending
forward into the cranial region. Posterior to the pharynx these
vessels unite forming the median dorsal aorta, which then
extends to the posterior extremity of the embryo.

The blood vessels of the visceral arches develop very early.
Those of all the branchial arches are essentially similar, while
the arteries of the hyoid and mandibular arches are consider-
ably modified from the branchial type and are largely vestigial

180 OUTLINES OF CHORDATE DEVELOPMENT

in character. There is some variation here among different
species of Rana; we shall outline the history of these vessels
in R. esculenta, as described by Maurer. Here, in each branchial

ab ig

FIG. 64. — Sections through the branchial region of tadpoles of R. esculenta,
showing the development of the gills and the history of the aortic arches. After
Maurer. A.^ 4 mm. larva showing the continuous first branchial aortic arch.
B. 5 mm. larva showing the anastomosis between the afferent and efferent
portions of the aortic arch. C. 6 mm. larva with vascular loops in the external
gills. D. 13 mm. larva. On the left the opercular cavity is closed and the
external gill is beginning to atrophy, while on the right this cavity is still open
and the external gill well developed and projecting through the opercular open-
ing. E. 17 mm. larva. Vessels of the second branchial arch. External gill
represented only by a minute pigmented vestige, cti, First branchial aortic
arch; ab, afferent branchial artery; ao, root of lateral dorsal aorta; au, auditory
organ; c, conus arteriosus; e, epithelioid body; eb, efferent branchial artery;
eg, external gill; i, internal (anterior) carotid artery; ig, internal gills; n, nerve
cord; o, operculum; p, pharynx; pc, pericardial cavity; r, gill rakers; s, oral
sucker; v, velar plate; x, anastomosis between afferent and efferent branchial
arteries.

arch a lacunar vascular space appears (about 4.5 mm.) which
early connects ventrally with the truncus arteriosus, and dor-

THE LATER DEVELOPMENT OF THE FROG

181

sally with the lateral dorsal aorta, forming thus, before the
gills appear, a continuous aortic arch in each branchial arch
(Fig. 64, A). There are, therefore, in the branchial arches, four
pairs of aortic arches; these are really the third to sixth pairs
of aortic arches, the first and second being formed in the
mandibular and hyoid visceral arches.

When the external gills appear an additional vessel develops
dorso-laterally to the aortic arch, along the base of the gill,
forming its supply. This vessel opens out of the ventral end

FIG. 65. — Diagrams of the aortic arch of the adult frog and tadpole. After
Maurer. A. The continuous aortic arch of the adult; showing the parts corre-
sponding with the larval vessels. B. First external gill and associated vessels
in young tadpole. C. Internal gill and associated vessels in the tadpole after
the disappearance of the external gills, ab, Afferent branchial artery; e, epi-
thelioid body; eb, efferent branchial artery; eg, external gill; ig, internal gill;
o, operculum; 'x, direct anastomosis between afferent and efferent branchial
arteries.

of the aortic arch and joins it again toward its upper end
(Fig. 64, B); the lower end of the aortic arch may then be
termed the afferent branchial artery, its dorsal end the efferent
branchial artery. The small vessels of the external gills form
loops connecting the dorsal and ventral parts of this second
vessel. Then as the external gills disappear and the internal
gills develop on the branchial arches, the direct ventral con-
nection between the original aortic arch and the second vessel,
becomes interrupted by the disappearance of a part of the
aortic arch, and the vascular networks of the internal gills
connect the two vessels. In this way the original aortic arch
becomes almost entirely the efferent branchial artery, while
the second vessel serves as the afferent branchial artery
(Figs. 64, 65).

182 OUTLINES OF CHORDATE DEVELOPMENT

When the internal gills disappear, during metamorphosis, the
lower end of the efferent branchial artery (original aortic arch)
reacquires a direct connection with the afferent branchial artery

ap

ao

FIG. 66. — Diagrams of the branchial blood vessels in frog larvae. After
Marshall. A. Of a 7 mm. larva (shortly after hatching). The vessels supplying
the external gills are removed, only their roots being indicated. B. Of a 12 mm.
tadpole. The vascular loops in the gills are omitted, a, Auricle; ac, anterior
(internal) carotid artery; am, anterior commissural artery; ao, dorsal aorta; apt
anterior palatine artery; 6, basilar artery; c, anterior cerebral artery; eg, carotid
gland; cv, posterior (inferior) vena cava; dC, ductus Cuvieri; g, pronephric
glomerulus; h, hepatic veins; hy, hyoidean vein; I, lingual artery; m, mandibular
vein; p, pulmonary artery; ph, pharyngeal artery; pm, origin of posterior oom-
missural artery; pp, posterior palatine artery; pv, pulmonary vein; s, vein of
oral sucker; t, truncus arteriosus; u, cutaneous artery; v, ventricle; 1-4, first to
fourth afferent branchial arteries; /, II, efferent arteries of the mandibular and
hyoid arches; III-VI, first to fourth efferent branchial arteries; VII, lacunar
vessel of the fourth branchial arch.

and the blood again passes directly from the truncus to the
dorsal aorta (Fig. 65, A). This connection enlarges as the gill
capillaries diminish, and finally these direct paths remain as
the only vessels of the branchial arches.

THE LATER DEVELOPMENT OF THE FROG 183

In the fourth branchial arch, which lacks external gills, the
history is essentially modified only to the extent of the omission
of the vessels related to these structures. The vessels of this
arch appear considerably later than in the anterior arches.

The development of the vessels of the mandibular and hyoid
arches seems to be quite variable among the different species
of Rana. The most consistent account is that of Marshall and
Bles, of R. temporaria. Here, in tadpoles of about 5 mm. a
lacunar vessel representing the aortic arch (the second of the
whole series) appears in the hyoid arch, and a small outgrowth
of the lateral dorsal aorta extends toward it, but never actually
joins it, disappearing about the time the mouth opens (Fig. 66,
A). At hatching a small outgrowth of the truncus arteriosus
may be seen extending into the lower end of the hyoid arch;
this has a very brief duration. At the same time the vestige
of the aortic arch has .divided into dorsal and ventral portions;
of these, the former soon disappears while the latter, now known
as the hyoidean vein, connects with a large vascular sinus in
the region of the oral sucker.

The vessels of the mandibular arch appear shortly before
hatching; these are, a lacunar vessel in the lower part of the
arch, representing the original aortic arch, and a small out-
growth of the lateral dorsal aorta into the dorsal part. Soon
these unite and also join the hyoidean vein. After the mouth
opens, the outgrowth from the lateral dorsal aorta separates
from the other vessels and grows forward as the pharyngeal
artery, while the hyoidean vein disappears with the oral sucker
(Fig. 66, B).

The continuations of the lateral dorsal aortse into the head
form the roots of the anterior or internal carotid arteries, whose
numerous branches supply the organs of the whole dorsal
part of the head; the internal carotids become connected by
two transverse commissural arteries passing anterior and post-
erior to the infundibulum (Fig. 66). The ventral part of the
head is supplied by the lingual or external carotid arteries; these
vessels appear, some time before the opening of the mouth,
as a pair of sinuses in the floor of the buccal cavity and

184 OUTLINES OF CHORD ATE DEVELOPMENT

pharynx. About the time the mouth opens, they extend back-
ward and connect with the ventral ends of the efferent bran-
chial arteries of the first branchial arch, in the region where
the carotid gland (see above) develops later.

About the time of hatching, outgrowths of the dorsal aorta,
just back of the pharyngeal region, extend laterally into the
region of the pronephros or head kidney (see below). These

later become very large and form
the vascular glomi of this kidney
(Figs. 66, 72); traces of these re-
main, long after the pronephros
*c itself has disappeared.

During metamorphosis, as the gills
disappear, the branchial blood ves-
sels are considerably modified. We
have seen that a continuous aortic
arch is reestablished in each of the
,ao four branchial arches by the fusion

FIG. 67.— Diagram of the of the afferent and efferent arteries.

aortic arches and their chief rrn n , v i_ • i ±' i/xi_'i

branches in an adult frog. The ^^ branchial aortic arch (third
Ventral view, ao, Dorsal aorta; of the whole series) remains as the

c, carotid artery; eg, carotid .

gland; cu, cutaneous artery; /, root of the anterior carotid artery,

and is known as the

subciavian artery; t, truncus (Fig. 67). The lateral dorsal aorta

arteriosus; v, vertebral artery. , , , ~ i i ALT • i

between the first and second (third

and fourth) aortic arches, becomes reduced to a solid strand
of connective tissue, and the second (fourth) pair of aortic
arches consequently become the roots of the dorsal aorta, and
are known as the systemic arches. The third (fifth) aortic arch,
after becoming a solid strand of tissue, disappears entirely.
The fourth (sixth) arch remains as the root of the pulmonary
and cutaneous arteries of the adult, and is known as the pulmo-
cutaneous arch.

The pulmonary arteries appear just after hatching as small
outgrowths from the upper ends of the efferent branchial
arteries of the fourth branchial arch. (Figs. 66, 67). They
extend backward to the lung rudiments, which they reach

THE LATER DEVELOPMENT OF THE FROG 185

before the vessels of this arch have acquired a connection
with the truncus arteriosus. Later the cutaneous arteries
leave the pulmonary, and extend dorsally, spreading over the
skin of the back and sides. Some time after metamorphosis
that part of the aortic arch between the origin of these vessels
and the lateral dorsal aorta, known as the ductus Botalli,
slowly atrophies and becomes a solid strand.

Longitudinal septa appear in the truncus arteriosus, dividing
it into three channels. One of these leads to the carotid arches,
and in the heart receives blood from the left side, i.e., fully
aerated blood which has been received through the left auricle
from the lungs and skin. Another channel leads from the
right side of the heart and carries the venous blood to the
pulmo-cutaneous arches. The remaining channel connects
with the systemic arches; in the heart its closer connection is
with the left side.

4. The Venous System

The large veins of the yolk-mass are in reality the first
parts of the vascular system differentiated. These are the
paired, but asymmetrical, omphalomesenteric veins (known
also as the vitello-intestinal or the vitelline veins) arising on the
ventral surface of the yolk, in the region of the blood islands
described above, and passing along the lateral surfaces of the
yolk and liver diverticulum, to enter the sinus venosus. This
posterior chamber of the heart appears to be formed chiefly
by the fusion of these large veins, although it receives later a
pair of large veins, the ductus Cuvieri or Cuvierian sinuses,
coming from the body wall opposite the sinus venosus. As
the liver develops, both of the vitello-intestinal veins break up
into capillary nets within its substance, and the parts of the
two veins between the liver and the heart fuse into a single
hepatic vein. Posteriorly from the liver the right vein seems to
disappear as a definite channel, while the left partly remains as
the root of the definitive hepatic portal vein, ultimately receiving
branches from the digestive tract and its appendages.

186 OUTLINES OF CHORDATE DEVELOPMENT

The ductfts Cuvieri pass from the sinus venosus obliquely
upward in a nearly vertical plane, to the body wall where they
divide, passing thence anteriorly and posteriorly. The anterior
branches are the anterior cardinal veins. These continue
forward as the superior jugular veins, receiving blood from the
brain and dorsal parts of the head, and from the region of the
eye and ear (facial branch). The inferior jugular veins, coming
from the region of the mouth, sucker, and ventral surface of the
head, open into the roots of the ductus Cuvieri, just before
these open into the sinus venosus.

The posterior branches of the ductus Cuvieri are the posterior
cardinal veins. These are primarily the veins of the body wall
and the excretory systems. They pass posteriorly through the
pronephric region, and thence along the medial side of the
pronephric ducts (see below) (Figs. 68, 72, 76) receiving blood
from the veins of the body wall (segmental veins). A median
caudal vein, passing forward through the entire length of the
tail, just ventral to the dorsal aorta or caudal artery, upon
reaching the body cavity divides above the cloacal region,
and its branches connect directly with the extremities of the
posterior cardinal veins, so that these receive blood from the
tail also. In the region of the head kidney or pronephros (see
below) each of these veins forms a large sinusoidal system
among the tubules of this excretory organ. Shortly after the
opening of the mouth, as the definitive kidney or mesonephros
(see below) commences to develop, the arrangement of the pos-
terior cardinal veins is profoundly modified. The hinder parts
of the two veins begin to fuse together at about 15 mm., and
ultimately form a median vessel, which may be termed the
median cardinal vein (Fig. 68). Anteriorly this vessel effects a
new and direct connection with the sinus venosus.

This connection is brought about by the development of the
posterior or inferior vena cava or postcaval vein. This important
vessel is first indicated by the marking out of a definite pathway
in the vessels of the dorsal side of the liver, vessels which are
branches of the left vitello-intestinal vein (Shore). This
vessel then leaves the surface of the liver and passes through

THE LATER DEVELOPMENT OF THE FROG

187

the suspensory fold of the liver (mesohepaticum) to the right
posterior cardinal vein, with which it connects, just in front of
the beginning of the median cardinal vein (i.e., immediately

w

lc

FIG. 68. — The development of the posterior part of the venpus system in the
frog. After Shore. A. Portion of a transverse section through the posterior
mesonephric region of an 18 mm. tadpole. B. Diagram of the veins of a 25-30
mm. tadpole. C. Diagram of the veins of the adult frog, a, Dorsal aorta; c,
vena cava; e, nuclei of the endothelial lining of the mesopheric sinus, continuous
with the vascular endothelium; /, femoral vein; i, iliac vein; lc, lateral mesone-
phric channel of the posterior cardinal vein; m, mesentery; ran, mesonephros;
n, mesonephric tubules; p, posterior cardinal veins (in C showing their original
location); pv, pelvic vein; rp, renal-portal vein; rr, revehent renal veins; sc,
sciatic vein; st, nephrostome; u, caudal vein; vcm, median mesonephric channel
of the posterior cardinal vein; W, Wolffian duct; x, connection between caudal
vein and the lateral mesonephric channels; 1-1, part of the renal-portal vein
formed from the lateral channel of the posterior cardinal; 2-2, part of the renal-
portal vein formed from the median channel of the posterior cardinal vein.

posterior to the pronephric region). This new channel en-
larges rapidly and ultimately becomes the largest blood vessel
of the body. Through the liver it passes directly to the sinus

188 OUTLINES OF CHORDATE DEVELOPMENT

venosus, and the hepatic vein comes to open directly into it
instead of into the sinus venosus.

As the pronephroi degenerate the pronephric sections of the
posterior cardinal veins diminish also, and by the time of
metamorphosis they have entirely disappeared. The ductus
Cuvieri consqeuently remain as the proximal parts of the
anterior cardinal veins only, and are sometimes known as the
anterior; or superior vence cavce or precaval veins. As the result
of these changes, all of the blood from the posterior parts of
the body wall, and from the tail, passes directly to the heart
through the median cardinal and postcaval veins (Fig. 68). '

The development of the mesonephroi, which begins as the
pronephroi diminish, entirely alters the relations of the median
cardinal vein. On each side the tubular components of the
mesonephros, whose development will be described below,
push into this vein, dividing it roughly into three parallel chan-
nels, one median and two lateral (Fig 68). The caudal vein
remains for a time, opening directly into the posterior end of
the median channel, while iliac veins, coming from the hind-
legs, open into the lateral channels. The caudal vein dis-
appears later, of course, while the iliac veins remain as the
chief vessels leading to the mesonephric region.

The arrangement of the vessels in the adult may now be
understood easily. The iliac veins and lateral channels of the
median cardinal vein, with which they are continuous, become
the afferent or advehent mesonephric veins or the renal portal
veins (Fig. 68, C). The small veins from the posterior body
wall (posterior vertebral veins) open into the renal portal veins.
The vascular spaces of the mesonephros remain connected,
by a series of short pathways — the revehent mesonephric or
renal veins, with the median channel of the median cardinal
vein, which therefore remains alone as the posterior continu-
ation of the postcaval vein.

Summarizing we may say that the inferior vena cava or post-
caval vein is composed of four different elements. An hepatic
section derived from the left vitelline vein, is followed by a
short section which represents a new structure; next comes a

THE LATER DEVELOPMENT OF THE FROG 189

very short region derived from the original right posterior
cardinal vein, and finally, the entire posterior section is formed
from the median channel, derived from the fused right and left
posterior cardinal veins. The renal portal veins consist of
two sections: a posterior part is derived from the iliac vein,
and an anterior part is formed from the lateral channel of the
median cardinal vein, which represents the hinder part of the
original posterior cardinal veins.

A pair of lateral veins develops late, in the ventral abdominal
wall, for a time opening directly into the sinus venosus. Pos-
teriorly these connect with the iliac veins, and then continue,
fusing together medially. The anterior portions of these ves-
sels then lose thair connection with the sinus venosus and the
anterior part of the right vessel disappears entirely, the left
vein forming a new connection with the hepatic portal vein,
when it is known as the anterior abdominal vein.

The rudiments of the pulmonary veins are indicated very
early (about 6 mm.) as proliferations of the endot helium on
the dorsal side of the sinus venosus (Federow). These cells
later form a definite tube opening proximally into the left side
of the auricle, and distally leaving the wall of the sinus venosus
and passing dorsally to the rudiments of the lungs. At the
base of the lung it bifurcates, each branch passing along the
medio-ventral side of each lung rudiment. Later, when the
lungs become functional the pulmonary veins discharge into
the left auricle.

5. The Lymphatic System and Spleen

The first indications of this system appear shortly before
hatching. In the larva of 6.5 mm. (Knower) a single pair of
anterior lymph hearts is present, as small sac-like outgrowths
of a pair (usually the fourth) of intersegmental veins (i.e., veins
running between the fourth and fifth myotomes, and opening
into the posterior cardinal veins at the posterior limit of the
pronephros). These hearts lie between the peritoneum and
the integument, below the level of the myotomes. The
endothelial wall of the lymph hearts is continuous with that

190 OUTLINES OF CHORDATE DEVELOPMENT

of the veins. Outside the endothelium is a syncytial layer
or network of striated muscle fibers, which commence rhythmic
contraction about the time the mouth opens.

Shortly after hatching (7.5-8 mm.) two lymphatic vessels
may be seen passing anteriorly and posteriorly from each
heart, along the lateral nerve, in the connective tissue beneath
the integument. The anterior vessel extends forward into the
head region, while the posterior vessel extends along the sides of
the trunk for a considerable distance. The openings of these

FIG. 69. — Dorsal, lateral and ventral views of the lymphatics in a 26 mm.
tadpole of R. temporaries. From Hoyer. For description see text.

vessels into the lymph hearts, and of the hearts into the veins,
are guarded by long valves. These vessels are formed as
blind tubular outgrowths from the endothelium of the lymph
heart; they grow rapidly and give off a rich network of fine
lymphatic capillaries and vessels which spread generally among
the other tissues and especially just beneath the skin.

In the older tadpole of about 26 mm. (Hoyer) the lymphatic
system is quite extensively developed. At this time the an-
terior vessel runs forward and downward, connecting with a
large lymph sinus around the mouth and heart and branchial
region (Fig. 69), while the posterior trunk passes to the base

THE LATER DEVELOPMENT OF THE FROG 191

of the tail, where it divides into dorsal and ventral branches.
The dorsal and ventral branches of each side then unite forming
two large vessels which extend through the tail, lying above
and below the myotomes (Fig. 69).

The large subcutaneous lymph sacs, so characteristic of
both the tadpole and the adult frog, are formed very early
from the network growing out from these vessels. The small
lymphatics in the subcutaneous connective tissue branch
abundantly and anastomose freely, forming a rich network;
their walls then disappear and the wide lymph sacs are left,
still connected with the lymph hearts by way of the lateral
trunks described.

The thoracic ducts also appear to arise from the anterior
lymph hearts, as a pair of outgrowths which extend poste-
riorly, between the dorsal aorta and the posterior cardinal
veins. When the hind-legs appear, from one to three pairs of
posterior lymph hearts develop in connection with the inter-
segmental veins of the region, in much the same way that the
anterior hearts developed. They open for a time into the pos-
terior cardinal veins, and later, therefore, into the renal-portal
veins, whether by the intersegmental veins or by the ischiadic
branch is not clear.

The spleen is first indicated in larvae of about 10 mm. by a
collection of mesenchymal lymphoid cells in the mesentery,
around the mesenteric artery, just dorsal and posterior to the
stomach (Radford). These cells multiply and in a 15 mm.
larva form a definite projection from the mesentery, covered
therefore, by a coelomic or peritoneal epithelium. During
this period of enlargement, the spleen appears to receive some
cells which wander out from the intestinal epithelium. Later
this organ becomes very vascular and in the 25-27 mm.
larva it forms a definite ovoid body, in the position where it is
found in the adult.

6. The Formation of the Septum Transversum

We have seen that the pericardial cavity is formed as a
median ventral section of the ccelom. This remains completely

192 OUTLINES OF CHOKDATE DEVELOPMENT

closed anteriorly and laterally, but posteriorly it is at first
directly, though incompletely, open into the general body
cavity or peritoneal cavity. During the early stages the liver
forms the hinder wall of the pericardial cavity, medially, but
it still remains open postero-laterally, either side of the liver,
and medio-ventrally, below it. When the ductus Cuvieri are
formed, passing from body wall to sinus venosus, they traverse
this region of the coelom and aid in establishing the hinder wall
of the pericardial cavity. Incomplete peritoneal folds from
the body wall accompany the ductus Cuvieri from the body wall
to the heart; these are known as the lateral mesocardia. Dor-
sally the lateral mesocardia remain incomplete for a long time,
but ventrally they gradually extend to the body wall entirely
across the coelom and form a complete ventral partition, be-
tween pericardial and peritoneal cavities. The transverse peri-
toneal fold thus formed is the pericardio-peritoneal septum, or
septum transversum. Its median ventral portion appears to be
formed by the peritoneum originally covering the anterior face
of the liver; this separates from the liver and becomes added
to the septum transversum. On the right side it becomes
continuous with the posteriorly directed suspensory fold of the
liver (mesohepaticum). Not until after metamorphosis is the
septum transversum fully united dorsally with the dorsal
mesentery, and the separation of the pericardial and peritoneal
cavities entirely completed.

VI. THE URINOGENITAL SYSTEM

The excretory and reproductive systems develop independ-
ently and at widely different times, but in their definitive
state they form a complex, in which structures orignally ex-
cretory, have assumed morphological and functional relations
with the reproductive system, while other parts function, at
different times, both as excretory and reproductive organs.

1. The Excretory System

A functional excretory system is already established, before
the rudiments of the reproductive system have more than made

THE LATER DEVELOPMENT OF THE FROG 193

their appearance. This is the embryonic or larval pro-
nephric system or larval kidney, known also as the head kidney.
This kidney is limited to early larval life and is replaced during
the tadpole stage by an excretory organ which remains the
definitive kidney of the adult; this is the mesonephros, which,
it should be noted, retains as its efferent duct, the duct of the
original pronephros . We have then to describe the development
of the pronephros and the pronephric duct, the development
of the mesonephros, and the disappearance of the pronephros.
We shall see how, during the later stages, the arrangement of
these parts is complicated by the relation between the excre-
tory and the reproductive systems. Since these organs are
symmetrically paired we may describe only the organs of one
side.

A. THE PRONEPHROS AND THE PRONEPHRIC DUCT

In a preceding section we described the position and rela-
tions of that part of the mesodermal somite known as the inter-
mediate cell mass or nephrotome, and said that this formed a
rudiment of the pronephric system. The first indication of the
pronephros is seen before the nephrotomal region has separated
from either the myotome or the lateral plate, as a solid thicken-
ing of the somatic mesoderm anteriorly (Fig. 70, B). This
thickening, which begins before the cavity (ccelom) of the
lateral plate and nephrotome appears, gradually extends
posteriorly along the nephrotomal level, and finally reaches to
the region opposite the cloaca, although this is not until the
anterior part of the rudiment has become quite markedly dif-
ferentiated. Anteriorly, in the region of somites 2-4, the
pronephros itself is formed, while the posterior remainder forms
the pronephric or segmental duct. As the thickening of the
anterior pronephric region becomes marked, the rudiment here
begins to extend ventro-laterally, like an epaulet, over the outer
surface of the dorsal margin of the lateral plate (Fig. 70, C).
Spaces appear in this cell mass, about the same time that the
ccelom appears in the lateral plate; in the lateral or distal part

194 OUTLINES OF CHORDATE DEVELOPMENT

of the thickening a continuous space is formed, from which
there extend medially or proximally, toward the lateral plate,
three small irregular canals which open into the upper margin

C

FIG. 70. — Sections through frog embryos (R. sylvatica) illustrating the forma-
tion of the pronephros. After Field. A. Through the anterior body region of an
embryo at the commencement of its elongation. B. Through the anterior end
of the pronephric rudiment of an embryo in which the neural folds are just
closed together. C. Through the second nephrostome of an embryo of about
3.5 mm. c, Ccelom; ca, rudiment of pronephric capusle; cc, communicating
canal; ec, ectoderm; en, endoderm; g, gut cavity; mp, medullary plate; my,
myotome; my 2, second myotome; n, notochord; nc, rudiment of neural crest;
si, 82, first and second pronephric nephrostomes; sc, spinal cord; sn, subnoto-
chordal rod (hypochorda) ; so, somatic layer of mesoderm (in A the reference
line points to the rudiment of the pronephros) ; sp, splanchnic layer of mesoderm;
t, pronephric tubule; v, vertebral plate of mesoderm.

of the coelom of the lateral plate opposite the middle of each of
the three pronephric somites (Field). From the posterior
end of this peripheral space or common trunk, the cavity leads

THE LATER DEVELOPMENT OF THE FROG

195

directly into the cavity of the pronephric duct, which is con-
tinuous posteriorly with this portion of the pronephric
rudiment.

There are now established the primary elements of the
pronephros. The three short canals with their cellular walls
are the rudiments of the three pronephric tubules, and their
openings into the coelom are the nephrostomes. The tubules
and also the proximal part
of the pronephric duct,
now elongate rapidly, and
as a consequence become
thrown into complicated
loops and folds (Figs. 71,
72) forming a conspicuous
mass whose position is
marked externally by a
slight elevation. The pro-
nephric duct gradually ac-
quires a lumen throughout
its extent; at about 4.5
mm. the duct effects a
connection with the wall
of the cloaca, and its
cavity then opens into the

Cbacal Chamber (Fig. 54). FlG. n._Total views of the pronephros

The nephrostomes become of the frog (R. sylvatica). After Field. A.

... ... , . , Right pronephros of an embryo of about 3.5

lined With large Cilia Which mm. The crosses mark the location of the
nrnrhipp f\ onrrpnt out of nephrostomes. B. Right pronephros of a

* larva of about 6 mm. First tubule dotted;

the COelom, passing by Way second white; third obliquely ruled; pro-
,. , , i • j nephric (segmental) duct shaded with lines.

of the pronephric duct to
the cloaca.

Meanwhile the pronephros acquires a rich vascular supply,
both arterial and venous. It will be remembered that the
posterior cardinal veins are passing along the pronephric ducts,
and in the region of the pronephros itself these veins become
greatly enlarged. As the pronephric tubules elongate, they
push up into the posterior cardinal sinus, which is ultimately

196 OUTLINES OF CHORDATE DEVELOPMENT

nearly filled by them. Each tubule carries around it a reflected
layer of the thin vascular wall and so is completely bathed in
the venous stream (Fig. 72).

cv

FIG. 72. — Sections through frog larvae illustrating the later development of
the pronephros. A. Through the first nephrostome of a larva of R. syhatica of
about 8 mm., with prominent external gills. After Field. B. Through the region
of the second nephrostome of a 12 mm. larva of R. temporaria. After Furbringer.
c, Coelom; cv, sinuses of posterior cardinal vein; eg, external glomerulus; g, gut
cavity; gX, ganglion nodosum (part of the ganglion of the vagus nerve) ; I, lung;
TO, mesenchyme; myz, second myotome; p, peritoneum; si, sz, first and second
pronephric nephrostomes; tr, common trunk; X, root of vagus nerve.

At the same time an arterial supply is derived from the
dorsal aorta. This is the pronephric glomus already mentioned.

THE LATER DEVELOPMENT OF THE FROG 197

The first indication of this is a horizontal fold of the splanchnic
or medial wall of the dorsal coelom just opposite the second
nephrostome. This fold appears at about 4.5 mm. and its
development is in general parallel with that of the pronephros.
It soon extends the entire length of the pronephric region and
becomes considerably elevated, projecting freely into the
coelom opposite the nephrostomes (Fig. 72). In it vascular
spaces soon appear, some of which form the long convoluted
vessels of the glomus proper, while others go to form a vessel,
connecting with a branch of the dorsal aorta, which is ap-
parently one of the segmental arteries passing ventrally from
the aorta. Later this section of the body cavity is cut off, as
the pronephric chamber, by the lateral projection of the lung
(Fig. 72, B) which carries a fold of peritoneum across to the
peritoneum covering the pronephros, with which it fuses. for a
short distance. This pronephric chamber remains open into the
body cavity both anteriorly and posteriorly to the lung region.

A definite pronephric capsule is formed early from two
sources. The ventro-lateral walls of the myotomes, which we
have seen give rise elsewhere to mesenchyme, here, in the pro-
nephric region, evaginate over the dorsal and lateral surfaces of
the pronephros, and meet folds coming up from the somatic
layer of the lateral plate (about 6 mm.). These folds form a
definite connective tissue layer enclosing the pronephros and
the pronephric sinus of the posterior cardinal vein.

The pronephros reaches its full development in the larva of
about 12 mm., when it consists of a large mass composed of the
coiled proximal end of the pronephric duct and the three
tubules, each of which has acquired blind tubular outgrowths,
the whole mass interpenetrated by the vascular sinus of the
posterior cardinal vein. In the larva of about 20 mm. the
pronephros commences to degenerate. At this time the pro-
nephric duct becomes closed just back of the pronephros; the
tubules become variously dilated and constricted, breaking
into irregular sections and gradually disappearing (Fig. 73, C).
The nephrostomes approach one another and finally meet,
opening into a common cavity known as the common nephro-

198 OUTLINES OF CHORD ATE DEVELOPMENT

stome, which is then closed, and the nephrostomes thus cut off
from the body cavity (Fig. 73, C). The glomus shrinks, and
by the time of metamorphosis only a few scattered traces of
the pronephros remain, although the glomus remains indicated
for some months after metamorphosis. The pronephric ducts
do not take part in this process of degeneration, posterior to
the pronephric region; they remain, closed anteriorly. The dis-
appearance of the pronephros is correlated with the develop-
ment of the second excretory system, the mesonephros, to the
formation of which we shall now turn.

B. THE MESONEPHROS OR WOLFFIAN BODY

This begins to develop in tadpoles of 8-10 mm. Its rudiment
is formed by the nephrotomes of the seventh to twelfth somites,
and it is consequently both somatic and splanchnic in origin.
The nephrotomes of these segments fuse into a continuous
longitudinal strip of irregularly arranged cells, lying between
the pronephric duct and the dorsal aorta, along the posterior
cardinal vein. In this mass, cell groupings appear, forming
definite swellings of the cord. These are the rudiments of the
mesonephric vesicles; they are not strictly metameric, but are
somewhat more numerous than the mesodermal segments.

All of these rudiments have essentially the same history
(Hall). First each becomes divided into a large ventral
chamber and a small dorsal one; the larger chamber is a primary
mesonephric unit, the smaller a secondary mesonephric unit (Fig.
73, B). The secondary units divide similarly, though much
later, into secondary units proper and tertiary mesonephric
units. All three series of units develop similarly though suc-
cessively, and we shall therefore describe only the history of
the primary series.

From the vesicular primary unit two outgrowths are formed
(Fig. 74). One, known as the inner tubule, extends dorso-
laterally to the pronephric duct and opens into it. The
other, the outer tubule, grows ventro-medially to the peritoneum
with which it fuses and opens into the body cavity. The

THE LATER DEVELOPMENT OF THE FROG 199

connections of the inner tubules with the pronephric duct
convert this into the mesonephric or Wolffian duct, which
remains as the ureter of the mesonephros or definitive kidney.
The inner tubules elongate and become coiled, forming the
tubular portion of the later kidney.

m

B

FIG. 73. — Sections through the developing mesonephros and the common
nephrostome of R. sylvatica. After Hall. A. Section through the eighth somite
of an 8.5 mm. larva. B. Section through the mesonephric rudiment of a 25 mm.
larva. C. Section through the common nephrostome of a 25 mm. larva, o,
Dorsal aorta; c, coelom; en, common nephrostome; g, germ cell; i, inner tubule;
m, mesonephric rudiment; my, myotome; o, outer tubule; p, remains of prone-
phros; pc, posterior cardinal vein; s, shelf cutting off the common nephrostome
from the remainder of the ccelom; so, somatic mesoderm; sp, splanchnic meso-
derm; W. Wolffian duct; /, primary mesonephric tubule; //, secondary meso-
nephric tubule.

Subsequently the outer tubules have a rather unusual history
in the frog. From the proximal portion an outgrowth appears,
which forms the capsule (Bowman's capsule) around the glo*

200 OUTLINES OF CHORDATE DEVELOPMENT

merulus associated with each tubule, the two forming the
Malpighian body. Each glomerulus is connected with a small

FIG. 74. — Series of diagrams illustrating the development of the primary
mesonephric tubules in R. sylvatica. After Hall. The Wolffian duct is drawn
in outline simply. The mesonephric vesicles are shaded; the somatic part of
the tubule is shaded by continuous lines, the splanchnic part by dotted lines.
A. Wolffian duct and simple mesonephric vesicle. B. Mesonephric vesicle
dividing into the large primary mesonephric unit and the small dorsal chamber.
The latter elongates antero-posteriorly and represents the rudiment of the
secondary and later mesonephric units. C. Formation of the rudiment of the
inner tubule. D. Inner tubule extending upward and toward the mesonephric
duct; formation of rudiment of outer tubule. E. Outer tubule fused with peri-
toneum and rudiment of nephrostome thus established. Bowman's capsule form-
ing. Commencement of differentiation of secondary mesonephric tubules. F.
Separation of nephrostomal rudiment from remainder of tubule. G. Connection
cf nephrostome with branch of posterior cardinal vein. Separation of secondary
tubule, and beginning of tertiary tubule indicated, c, Bowman's capsule; i, inner
tubule; n, nephrostome; o, outer tubule; p, peritoneum; v, branch of posterior car-
dinal vein; /, primary mesonephric tubule; //, secondary mesonephric tubule; ///,
tertiary mesonephric tubule.

twig derived from the dorsal aorta, and structurally resembles
essentially a miniature glomus like that of the pronephros.

THE LATER DEVELOPMENT OF THE FROG 201

This pare of the outer tubule now separates from the remainder,
retaining the connection with the inner tubule, while the distal
part retains its connection with the body cavity; this con-
nection now becomes ciliated and forms a typical nephrostome.
This nephrostomal region is short and effects a new connection
at its inner end, with the sinus of the posterior cardinal vein.
It will be remembered that, as the tubules of the mesonephros
enlarge (15 mm.) this body seems to extend freely into the
posterior cardinal vein, which has a sinusoidal character here
and interpenetrates the substance of the mesonephros, its walls
being closely reflected around the surfaces of the tubules.

During the later development of the mesonephros, the sec-
ondary and tertiary units acquire, similarly, connections with
the mesonephric duct, Malpighian bodies, and nephrostomal
connections with the body cavity and cardinal vein. Addi-
tional outer tubules and nephrostomes are formed later, but it
is not clear whether they form as independent evaginations
of the peritoneum or by splitting off from those previously
formed; perhaps both processes occur. The number finally
formed is very large (about two hundred according to Marshall
and Bles.)

Upon the development of the reproductive organs certain
of the mesonephric tubules become modified and take on new
functions; these processes will be described below.

Just before metamorphosis the urinary bladder appears as a
median ventral evagination of the wall of the cloaca, nearly
opposite the openings of the mesonephric ducts or ureters. The
rudiment forms just at the border between the ectoderm and
endoderm lining the cloaca. It is at first a long narrow sac,
directed anteriorly; later its diameter increases and as it
enlarges it becomes bifid at its extremity.

2. The Reproductive System

In order to make the devlopment of this system easier to
understand we may first repeat, very briefly, the arrangement
and composition of the adult system as described in the pre-

202 OUTLINES OF CHORDATE DEVELOPMENT

ceding chapter (Figs. 24, 25). In the male each of the paired
testes, suspended from the dorsal body wall by a double fold of
peritoneum, the mesorchium, is connected by a series of small
tubules, the vasa efferentia, with the upper end of the Wolffian
duct or mesonephric duct. The vasa efferentia are modified
mesonephric tubules, and the mesonephric duct therefore
functions here both as excretory (ureter) and reproductive
(vas deferens) duct, i.e., as a urinogenital duct. The homolog
of the oviduct or Mullerian duct of the female, is represented
in the male by a vestigial cord.

In the female the ovaries are similarly suspended by mes-
ovaria. They are not directly connected with the reproductive
ducts or oviducts, and consequently, in this sex the Wolffian
or mesonephric duct remains purely excretory in function
(ureter). The oviduct is a long convoluted tube which de-
velops from the peritoneal epithelium, quite independently of
the excretory ducts.

A. THE GONODUCTS

It will be convenient to describe the formation of the gono-
ducts first. The vas deferens of the male is the original meso-
nephric duct or ureter, and nothing need be added to the account
of its development given above, save to point out that in con-
nection with each duct a glandular seminal vesicle develops,
just in front of the opening of the duct into the cloaca. In the
female the mesonephric duct remains unmodified, and the
seminal vesicles are barely represented.

The Mullerian ducts for a long time develop similarly in both
sexes, although they become fully developed and functional, as
the oviducts, only in the female. The Mullerian duct appears
during the early stages of the degeneration of the pronephros,
just beneath the common nephrostome, the formation of which
has been mentioned. Here a peritoneal proliferation forms an
elongated thickening along the dorso-lateral wall of the body
cavity. From the dorsal border of this thickening a thin shelf
of cells forms and projects downward (Fig. 75), parallel with
the peritoneal thickening. The free lower margin of this shelf

THE LATER DEVELOPMENT OF THE FROG

203

or flap then fuses with the peritoneal wall forming a short
compressed tube open at both ends. This tube then extends
anteriorly and posteriorly: anteriorly it reaches to the anterior
end of the body cavity and then turns ventrally, stopping near
the base of the lung, where its open end forms, the rudiment
of the ostium or infundibulum of the oviduct. Posteriorly the
formation of the shelf and its closure continue parallel with
and just to the outer side of the mesonephric duct, and entirely

FIG. 75. — Sections through the developing Miillerian duct of a 34 mm. tadpole
of R. sylvatica. After Hall. A. Section passing through the beginning of the
Miillerian evagination. B< Section posterior to A. Duct established but still
connected with peritoneum. C. Section still farther posterior, showing the
separation of the duct from the peritoneum. M . Mtillerian duct; p, peritoneum ;
t, third pronephric tubule*

independent of it, until it reaches the cloaca, with which it
connects some time after metamorphosis.

In the male the development of the Miillerian duct ceases at
this stage, but in the female it continues to thicken and to
elongate, so that it becomes entirely free from the body wall,
though remaining suspended from it by a double fold of peri-
toneum; finally it acquires the characteristics described in the
beginning of the preceding chapter.

Bv THE .GONADS ,

The primitive germ cells are distiriguislia'ble quite early
(about 6 mm.) as a definite thotigh slight ''ridge along the

204 OUTLINES OF CHORDATE DEVELOPMENT

median dorsal side of the endodermal wall of the intestine.
The cells composing this ridge resemble closely the other cells
of this part of the enteric wall, and are to be distinguished
chiefly by their behavior (Fig. 76, A). The mesentery is formed
shortly after this stage, and when the mesodermal folds push

cv

sc

FIG. 76. — Sections showing the origin of the sex-cells (germ cells) in R.
sylvatica. After Allen. A, B, Sections of a 7.5 mm. larva showing (^4.) sex-cell
ridge of endoderm and (B) its separation as the sex-cell cord. C, Part of a section
of an 8.3 mm. larva showing the beginning of the migration of the sex-cells.
a, Dorsal aorta; ch, notochord; cv, posterior cardinal vein; e, endoderm cells;
g, gut cavity; I, lateral plate of mesoderm; m, mesentery; my, myotome; n, nerve
cord; sc, sex-cell cord; sch, subchordal rod (hypochorda) ; sr, sex-cell ridge;
W, Wolffian duct.

in toward the mid-line, above the gut, this ridge of primitive
germ cells seems to separate from the gut and to move dorsally,
so that when thfe mesentery is formed they are found in its
base, near the body wall (Fig. 76, B, C). Here they form a

THE LATER DEVELOPMENT OF THE FROG 205

definite median strand of cells between the posterior cardinal
veins (8-9 mm.) (Allen).

This germinal strand now divides longitudinally and the
halves move more laterally, projecting slightly into the body
cavity as the genital ridges, near the attachment of the mesen-
tery and just beneath the cardinal veins. The genital ridges
now become more conspicuous through the proliferation of the
primitive germ cells and the peritoneal cells covering them, to
which are added mesenchyme cells
from the body wall. In this cell mass
the mesenchyme elements are con-
cerned in the formation of the stroma
of the ridge. The peritoneum continues
to form a thin superficial covering and
later forms the suspensory folds (mes-
orchia, mesovaria) of the gonads, as the
ridges may be called when they pro-
ject freely into the body cavity. As
the primitive germ cells begin to
multiply, they form the nests of cells
described in the preceding chapter,
the further development of which
need not be repeated here.

Before metamorphosis begins the
anterior third or half of each genital pole of R. temporaria. After

. , -i j Bouin. /, Follicle cells; g,

ridge commences to degenerate and primitive germ ceU;m,mesen-
becomes converted into the fat body terv;. »• "nests" formed by

multiplication of the primitive
(see above). The posterior portion germ cells; s, genital strand

has previously acquired secondary (

connections with the mesonephric duct in the following man-
ner. From the stalks of a few (7-8, Nussbaum) of the Malpi-
ghian bodies of the posterior part of the mesonephros, there
grow out solid strands of cells known as the sexual cords.
These become tubular and gradually extend downward into
the substance of the gonad, either forming or connecting
with spaces within this organ (Fig. 77). From this point
onward their history is different in the two sexes. In the

206 OUTLINES OF CHORDATE DEVELOPMENT

male, the sexual cords, after metamorphosis, establish in-
timate connections with the cavities of the testis and form
the efferent ducts (vasa efferentia) by which the spermatozoa
are conducted from the gonad to the gonoduct (vas def-
erens). In the female, while the intragonadial portions of
the sexual cords may give rise to cavities there, the parts
connecting the gonad and the mesonephros undergo degenera-
tion and remain vestigial in the adult, forming what is known as
Bidder's organ.

The sexes are morphologically indistinguishable during the
early stages of development , and in R. temporaria it is not until
the -tadpole reaches a length of about 30 mm. (Bouin) that the
sex can be distinguished. About this time the ovary acquires
a central lumen; the sex cords appear larger in the male, and
trie form of the nests of germ cells can be distinguished, in that
in the testis groups of similar cells are formed while in the ovary
the cells become arranged as a follicle surrounding a large cen-
tral primitive ovum,

3. The Adrenal Bodies

The adrenal bodies of the adult frog consist of a thin layer of
irregularly distributed tissue on the ventral surface of the pel-
vic portion of the mesonephros and intimately connected with
it. Histological examination shows that the tissue consists
of a coarse network of cell strands with occasional groups of
darkly staining " phaBOchrome " tissue. The spaces within this
meshwork are occupied by sinusoids of the efferent renal (me-
dian posterior cardinal) vein. These two kinds of tissue are-
known respectively as the cortical and the medullary tissues,
not because they have such a relation here, but because the
corresponding elements of the adrenals in higher forms have
such a disposition.

The cortical substance of the adrenal appears first, in the
larva of about 12 mm. in the form of small cell groups along
either side of the wall o£ the median posterior cardinal vein
(Fig. 78, A). They lie below the level of the mesonephroi, and

THE LATER DEVELOPMENT OF THE FROG

207

beneath the peritoneal epithelium from which they appear to
have arisen. Just after metamorphosis these cell groups
separate from the peritoneum, and begin to send out branching
and anastomosing processes which soon form a network, like
that of the cortical substance of the adult.

The medullary or phaeochrome substance is derived originally
from ganglia of the sympathetic nervous system. After the
central network is established there appear within the sym-
pathetic ganglia of the mesonephric region groups of cells, the
precise origin of which is not clear, having the properties of

ct

am

m

FIG. 78. — Parts of sections through young R. temporaria, showing the origin
of the adrenal bodies. After Srdinko. A. Through 30 mm. tadpole. B.
Through 11 mm. frog after metamorphosis, a, Dorsal aorta; ac, cortical cells
of adrenal body; am, medullary cells of adrenal body; ct, connective tissue;
g, gonad; gs, sympathetic ganglion; m, mesentery; n, mesonephros; ro, revehent
renal vein; v, vena cava; x, point where ganglion cells enter mesonephros and
adrenal body.

these phseochrome cells. Some of these cell groups remain
in the sympathetic ganglia, while others appear to migrate into
the rudiment of the adrenal body, where they become scattered
through the cortical tissue (Fig. 78, B). The method by which
they extend into the adrenal is not clearly known in the frog.

VII. THE SKELETON AND TEETH

In describing the development of the skeletal system we
shall limit our account to the establishment of the essential

208 OUTLINES OF CHORDATE DEVELOPMENT

structures of the tadpole, merely indicating the trend of later
development. The later history of the skeleton falls largely
without our province.

1. The Vertebral Column

The formation of the notochord has been described pre-
viously, but its differentiation deserves a further word. The
chorda cells early become flattened
antero-posteriorly, and about the time
the embryo begins to elongate, vacuoles
appear within the protoplasm of the
cells and also between adjacent cells.
The chorda becomes surrounded by
three sheaths. The primary or elastic
sheath is formed on the surface of the
chorda by the action of the super-
ficial chorda cells. The secondary or
fibrous sheath is formed within the pri-
mary sheath by the chorda epithelium,
which is composed of a layer of cells
M within the primary sheath. Con-
column in the body region siderably later a skeletogenous sheath is

of a larva of Xenopus capen- -. . , -, , . •. ,-, . -. , -.

sis. After Schauinsiand. c, laid down outside the primary sheath;

Notochord; d, dorsal ver- fa^ jg formed by the Sclerotomal Out-

tebral cartilaginous arch; i,

inner chorda sheath of scle- growths of the SOmiteS, whose forma-

tion was described above (Fig. 79).
The skeletogenous layer is continued
dorsally around the nerve cord, and
it also extends a short distance later-
ally from the chorda, between successive myotomes.

The vertebral column is formed within this skeletogenous
layer. First there appears (about 15 mm.) a metameric series
of cartilages, along the dorso-lateral surfaces of the chorda
in the base of the neural arch. A metameric series of cartilages
appears also in the skeletogenous layer along the median ven-
tral surface of the chorda (Fig. 79). The cartilages of the
dorsal series become united on each side, so that a pair of con-

drial connective tissue; v,
ventral (hypochordal) ver-
tebral cartilage.

THE LATER DEVELOPMENT OF THE FROG . 209

tinuous strips extends along the entire chorda, while the
ventral elements similarly fuse forming a median ventral strip.

Separate vertebra now become marked out by the appearance,
in these continuous cartilages, of metameric rings of fibrous
tissue; these are the beginnings of the intervertebral ligaments.
They appear opposite the middle of each mesodermal segment,
consequently the segments of the vertebral column (vertebrae)
alternate with the muscle segments. Cartilage now begins to
form across the notochord, between successive vertebrae, so that
the notochord becomes completely segmented, remaining only
intravertebrally. In each of these transverse partitions appears
a curved split, concave anteriorly. The intervertebral carti-
lages then fuse with the adjoining vertebrae and thus determine
the procoelous character of the vertebral centra.

The ventral cartilages now grow up around the sides of the
chorda, meeting and fusing with the dorsal series. From the
former there extend outward short cartilaginous processes
which become the transverse processes of the vertebra. Later-
ally from these, bits of cartilage are formed later which repre-
sent ribs. These fuse with the tips of the transverse processes
so that no separate ribs are subsequently distinguishable.
In the meantime outgrowths from the dorsal elements have
extended inward beneath the nerve cord, as well as laterally
and dorsally to it (neural arch).

Bony tissue appears first, before the beginning of metamor-
phosis, in the region between the dorsal and ventral series of
cartilages. It soon invades the entire cartilaginous structure,
forming a complete shell around the intravertebral notochordal
remains, and dorsally around the nerve cord. In addition to
the articulation of the procoelous vertebral centra, intervertebral
articulations develop on short processies of the neural arches.

The foregoing description applies only to the nine vertebrae of
the body. In the greater part of the tal cartilage is not formed.
But in the region of the future urostyle three longitudinal strips
of cartilage are formed as in the trunk, but these fuse completely
enclosing the chorda in a cylinder of cartilage which is never
segmented into vertebrae.

210 OUTLINES OF CHORDATE DEVELOPMENT

2. The Skull

The fully formed skull is a complex organ formed by the
association, and more or less extensive fusion, of several diverse
elements; these are (a) the cranium, (6) the sense capsules, (c)
the visceral arches (in part), (d) the notochord (in part), (e)
vertebral elements, (/) membrane or derm bones. Before pro-
ceeding to describe the formation and association of these ele-
ments in the frog, we should note that here no embryologically
distinct vertebral elements are included in the skull; their
inclusion in the above list is based upon phyletic and compara-
tive grounds, and upon the behavior of the anterior somites.

A. THE CRANIUM AND SENSE CAPSULES

In tadpoles of about 7 mm. the first rudiments of the cranium
are formed as a pair of curved strands of dense tissue, soon
becoming cartilaginous, along the ventro-lateral surfaces of the
fore-brain. These are the rudiments of the trabeculce or tra-
becular cartilages (Fig. 80, A). They rapidly extend forward
and fuse across the mid-line between the olfactory organs,
forming there the rudiment of the internasal plate; each rod then
continues forward as the trabecular cornu, which expands
slightly, partly enclosing the olfactory organ and forming the
olfactory capsule. In front of the olfactory capsule the trabecula3
unite with the rudiments of a pair of labial or suprarostral
cartilages, lying in the extended upper lip. Posteriorly the
trabeculse extend beneath the mid-brain, embracing between
their ends the anterior extremity of the notochord, which it
will be recalled extends forward to the mid-brain region. Soon
similar tissue thickenings extend posteriorly each side of the
notochord in the hind- brain region; these are the indications
of the parachordce or parachordal cartilages. The rudiments of
the parachordals now fuse with the posterior ends of the tra-
beculaB, enclosing the tip of the chorda and forming a continuous
plate beneath the hind- brain, known as the parachordal plate
(Fig. 80, A).

THE LATER DEVELOPMENT OF THE FROG 211

In the tadpole at this stage (shortly after hatching) there are
present also rudiments of parts of the visceral arches; the general
development of these will be described below, but it is necessary
to mention here one of these elements, the palato-quadrate, since
from the beginning it takes part in the formation of the cranium.
The paired palato-quadrate rudiments are formed as short,

i r

ct

in

PP

c

FIG. 80. — Dorsal views of the chondrocranium of the frog larva. A. Chondro-
cranium of a 7.5 mm. larva of R. temporaries. After Gaupp, from Stohr-Ziegler
model. B. Chondrocranium of a 14 mm. larva of R. fusca. After Gaupp, from
Ziegler model, a, Auditory capsule; bp, basal plate; c, notochord; ct, trabecular
cornu; /, basicranial fontanelle; in, internasal plate; ir, infrarostral cartilage;
j, jugular foramen (for IX and X cranial nerves); m, muscular process; M,
Meckel's cartilage; mo, mesotic cartilage; o, occipital process; pa, anterior ascend-
ing process of palato-quadrate cartilage; pi, parachordal plate; pp, posterior
ascending process of palato-quadrate cartilage; pq, palato-quadrate cartilage;
sr, suprarostral cartilage; t, trabecular cartilage.

flattened, crescentic rods, lateral to the trabeculaB. They
soon connect with the trabeculaB by anterior ascending processes
a short distance back of the olfactory region, and by posterior
ascending processes opposite the extremity of the chorda. The
rudiments of the cranium thus marked out are now converted
into a continuous cartilaginous structure having the appearance
illustrated in Fig. 80, A . The large basi-cranial fontanelle in front
of the chorda is the seat of the inf undibulum and pituitary body.

212 OUTLINES OF CHORDATE DEVELOPMENT

Immediately subsequent events concern chiefly the posterior
part of the cranium. The auditory organ becomes partially
enclosed by a connective tissue capsule which is early chon-
drified, forming a cap open toward the mid-line (Fig. 80, B).
A cartilage (mesotic cartilage) then extends posteriorly and
laterally from the parachordal plate and becomes united
with the auditory capsule- by anterior and posterior ventral

sr

FIG. 81. — Chondrocranium of 29 mm. larva of R. fusca. After Gaupp, from
Ziegler. To the left, the ventral surface; to the right, the dorsal surface, o,
Auditory capsule; bp, basal plate; c, notochord; ct, trabecular cornu; /, basi-
cranial fontanelle; fa, foramen for carotid artery; fm, foramen magnum; fo,
foramen for olfactory nerve; ir, infrarostral cartilage; j, jugular foramen for
IX and X cranial nerves; I, perilymphatic foramina; ra, muscular process; M,
Meckel's cartilage; o, otic process of palato-quadrate; pf, palatine foramen;
pq, palato-quadrate cartilage; sr, suprarostral cartilage; t, trabecular cartilage;
v, secondary fenestra vestibuli.

connections, leaving between them a wide space. Posteriorly
to this mesotic cartilage the floor of the cranium is continued
as the occipital cartilage. This also fuses with the floor of
the auditory capsule leaving, however, a small space which
represents the jugular foramen transmitting the IX and X
cranial nerves. The floor of the posterior part of the cranium,

THE LATER DEVELOPMENT OF THE FROG 213

composed of the occipital and mesotic cartilages and the
parachordal plate, is known as the basal plate.

By the time the tadpole has reached a length of about 14
mm. the chondrocranium has acquired the form shown in
Fig. 80, B. A still later stage is illustrated in Fig. 81. Com-
parison of these two figures brings out most of the facts of
later development. We need therefore mention specifically
only a few details. No traces of the notochord finally remain;
it is partly replaced by, and partly converted into cartilage of
the basal plate. The occipital region slowly extends vertically
forming the hinder wall of the cranial cavity, and fuses exten-
sively with the auditory capsule. Finally the occipital cartilage
extends dorsally around the nerve cord, enclosing the foramen
magnum. In the frog the occipital cartilage shows no definite
indications of its vertebral origin.

The auditory capsule becomes more complete externally,
remaining open into the cranial cavity by a large foramen.
From the inner surface of the capsule cartilage grows in, sur-
rounding the elements of the membranous labyrinth previously
described. On the outer side of the capsule an opening is
formed, the secondary fenestra vestibuli, which becomes plugged
by the movable operculum. In connection with the ear we
described above the development of the plectrum or columellay
and its connection later with the annular cartilage in the
superficial tympanic membrane. We should repeat that the
columella is not related with the elements of the visceral
skeleton in the frog.

In the orbital region the trabeculaB gradually grow across
the basicranial fontanelle, closing it and forming the floor of
this part of the cranial cavity. They also extend vertically
forming the lateral walls of the cranial cavity, separating it
from the orbits; these walls are perforated only for the passage
of nerves and blood vessels. Anteriorly, cartilages from the
trabeculaB also extend dorsally across the mid-line forming a
narrow dorsal bridge. The large supracranial fontanelle
between this bridge and the supraoccipital region is not
closed by cartilage.

214 OUTLINES OF CHORDATE DEVELOPMENT

IV

art

FIG. 82. — A. Anterior portion of chondrocranium of R. fusca during meta-
morphosis. Lateral view. After Gaupp, from Ziegler. B. Skull of 2 cm.
R, fusca, after metamorphosis. Dorsal view. Membrane bones removed from
left side. After Gaupp, from Ziegler. a, Auditory capsule; am, anterior maxil-
lary process; an, annulus tympanicus; art, articular process of palato-quadrate
cartilage; eo, exoccipital bone; /, fronto-parietal bone; fpo, prootic foramen; mx,
maxillary bone; n, nasal bone; o, olfactory cartilages; on, orbito-nasal foramen;
pa, anterior ascending process of palato-quadrate; pg, pterygoid bone; pi,
plectrum; pm, posterior maxillary process; pp, posterior ascending process of
palato-quadrate; pq, palato-quadrate cartilage; pt, pterygoid process of palato-
quadrate; px, prem axillary bone; qj, quadrato-jugal bone; II, foramen for optic
nerve; ///, foramen for III cranial nerve; IV, foramen for IV cranial nerve.

THE LATER DEVELOPMENT OF THE FROG 215

The ethmoid region remains comparatively simple throughout
the tadpole stage; its extreme complication comes later.
During the larval period the internasal septum extends dorsally,
forming the anterior wall of the cranial cavity, perforated by
the olfactory nerves. The trabecular cornua remain separate
from the olfactory capsules and connect anteriorly with the
suprarostral or labial cartilages. During metamorphosis the
labial cartilages and the anterior ends of the cornua disappear
in front of the olfactory capsules (Fig. 82).

The formation of the bony elements of the skull occurs
relatively late in the frog. As a matter of fact, the derm or
membrane bones appear before those which are formed in the
cartilage cranium, but they will be described later. There
are, in the frog's skull the following elements formed as carti-
lage bones in the original cranium.

(a) The exoccipitals (lateral occipitals) which form from the
posterior parts of the occipital cartilage and auditory capsule;
the occipital condyles and the median dorsal and ventral parts
of the occipital region remain cartilaginous.

(6) The prootics, which form from the anterior parts of the
auditory capsules and the parts of the basal plate and orbital
region adjacent to the auditory capsules.

(c) The columellce, whose development has been described in
another place.

(d) The ethmoids which form as vertical elements in the
anterior part of the inner wall of the orbit; later the two eth-
moids unite above and below, forming a band-like element
around the cranium. This is often known as the sphenelhmoid
or orbito-sphenoid.

In the palato-quadrate cartilage, bone appears only in the
region of the articulation with the lower jaw (see below).
This region does not form a distinct element of the skull, how-
ever, but unites with a membrane bone, the two together
forming the quadrato-jugal.

With the exception of the ethmoids, these elements are all
present by the end of metamorphosis: the ethmoids form some
weeks later.

216 OUTLINES OF CHORDATE DEVELOPMENT

B. THE VISCERAL ARCHES

The elements of the visceral skeleton are formed in the
pharyngeal visceral arches, which are established by the fusion
of the serial gill pouches with the ectoderm. We have described
the formation of the mandibular, hyoid and four branchial
visceral arches. In each of these save the last branchial,
skeletal elements appear. The mandibular and hyoid skeletal
arches appear about the time the full number of visceral
pouches is established, as condensations in the mesenchyme of
the visceral arch regions, soon becoming cartilaginous. The
mandibular arch appears first as a short rod, lying transversely
to the axis of the embryo, in the floor and sides of the mouth
cavity (Fig. 57). It is very early divided into two parts, the
separation between them marking the jaw articulation. The
dorsal section, or upper jaw rudiment, known as the palato-
quadrate, has already been described; the ventral section, or
lower jaw rudiment, becomes subdivided into Meckel's cartilage,
or lower jaw proper, and the infrarostral cartilage. The last
two elements remain ventral to the olfactory region as small
relatively undifferentiated elements during early development,
but the palato-quadrate rapidly enlarges and grows backward,
becoming roughly parallel with the trabeculaB and fusing with
them at two points as described above. Later (about 21 mm.)
the posterior or quadrate portion of this cartilage forms a con-
nection with the auditory capsule. During metamorphosis,
as the mouth enlarges and extends far posteriorly, the arrange-
ment of the jaw elements is very considerably modified. The
upper end of Meckel's cartilage, which has been in the olfactory
region, rapidly extends posteriorly and reaches to the quadrate
cartilage, below and in front of the auditory capsule. The
quadrate, meanwhile, elongates ventro-laterally. That part of
the palato-quadrate lying in the orbital region, softens and
largely disappears, and the anterior connection with the tra-
becula is drawn back in its place and remains as the seat of the
future pterygoid and palatine regions. The jaw articulation
is thus carried rapidly from the anterior to the posterior region

THE LATER DEVELOPMENT OF THE FROG 217

of the cranium, and through the elongation of the quadrate,
also some distance laterally from the cranial wall (Fig. 82).

The infrarostral cartilages, which very early fuse across the
mid-line forming the apex of the lower jaw, also elongate at
this time, and now fuse with the Meckelian cartilages as the
mento-Meckelian cartilages. Later on each becomes bony and
fuses with the dentary, the chief membrane bone of the lower
jaw (see below). A small median element between the infra-
rostrals fuses with them.

ch

FIG. 83. — Hyoid and branchial arches of a 29 mm. larva of R. fusca. Ventral
view. After Gaupp, from Ziegler. 66, Basibranchial (first), or copula; bh,
basihyal; ch, ceratohyal; ho, hypobranchial plate; 1-4, first to fourth cerato-
branchials.

The annulus tympanicus surrounding the tympanic mem-
brane of the frog, forms as an outgrowth of the quadrate carti-
lage; it becomes separate and gradually extends to the surface
of the head, forming first a crescentic, then a circular cartilage,
and later bone, long after the completion of metamorphosis
(Fig. 82, B).

The development of the hyoid and branchial arches may
conveniently be described together. These all appear first as
paired rods of dense tissue, lying in the corresponding visceral
arches. The hyoid arch forms about the same time as the
mandibular, the first branchial just after hatching, the second
branchial at 9-10 mm., and the third and fourth branchials
shortly after.

218 OUTLINES OF CHORDATE DEVELOPMENT

On each side, the hyoid cartilage or ceratohyal, extends dor-
sally, connecting with the palato-quadrate just behind the jaw
articulation; ventrally it unites with its fellow (Fig. 83). The
first branchials also unite ventrally. The other branchial
cartilages do not reach the mid- ventral line, but the lower end
of each unites with that anterior to it; later they similarly
connect dorsally. In the ventral region of the pharynx a
median element, the copula (basibranchial) appears, between

ho

FIG. 84. — A. Hyobranchial apparatus of R. fusca, toward the end of meta-
morphosis. The left side is shown in a more advanced stage than the right, in
that less cartilage is present. The original cartilage is indicated by fine stipples.
The coarse stipples indicate the cartilage added during the early part of meta-
morphosis* After Gaupp, from Ziegler. B. Hyobranchial apparatus of a 2 cm.
R. fusca, after metamorphosis. After Gaupp, from Ziegler. a, Alar process;
ac, anterior process of hyoid cornu; 6, body of hyobranchial cartilage; bb, basi-
branchial (first)< or copula; ch, ceratohyal (hyoid cornu in B)\ ho, hypobranchial
plate; I, postero-lateral process of hyobranchial cartilage; m> manubrium;
2, remains of second ceratobranchial (postero-medial process of hyobranchial
cartilage).

tjie hyoid and the first branchial, connecting with the ventral
ends of both these arches. The basihyoid cartilage is repre-
sented only by a small median copula in front of the hyoid cartil-
age. The lower ends of the first branchials become flattened
and expanded as the hypobranchial plate, with which the ventral
ends of the other three branchials then fuse. Only the lateral
or middle sections of the branchial cartilages, between the

THE LATER DEVELOPMENT OF THE FROG 219

visceral pouches, then remain separate from one another as
the first to fourth ceratobranchials.

The arrangement of these arches is profoundly modified
during metamorphosis, when the gill slits close and the jaw
articulation moves backward. The hyoid bar, or ceratohyal,
loses its connection with the palato-quadrate, and becomes
considerably reduced in diameter. The copula becomes re-
duced and a pair of new cartilages develops each side of it,
connecting with the hypobranchial plate and hyoid elements;
these are the manubrial cartilages (Fig. 84, A).

The hyobranchial apparatus of the fully metamorphosed frog
consists of a broad median plate of cartilage formed of the fused
manubria, copula, and hyobranchial plate (Fig. 84, B). The
ceratohyals remain as slender processes of this, known as the
hyoid cornua. Other processes of the median cartilage develop
anew, and only the posterior processes formed from the
second branchials, represent primary elements of the branchial
series; the other elements disappear entirely.

C. THE DERMAL ELEMENTS

The derm bones of the skull begin to appear in the dermal
layer of the integument covering the head and lining the mouth
before any other bony elements of the skeleton are indicated.

The first derm bone to appear is the median parasphenoid, in
the roof of the mouth of the tadpole of about 20 mm. (shortly
after the hind-legs appear). This bone finally becomes dagger-
shaped and covers the large basicranial fontanelle of the chon-
drocranium. The paired f rentals and parietals appear some-
what later, roofing the cranium and covering the supracranial
fontanelle; these elements later unite forming the paired fronto-
parietals (Fig. 82, B). A pair of nasals roof the olfactory
capsules, while within the capsules appear the septo-nasals
(intranasals) .

During metamorphosis the dermal elements of the mandibu-
lar arch and the other bones of the mouth appear. Premaxillce
and maxillce form the margin of the upper jaw, connecting later

220 OUTLINES OF CHORDATE DEVELOPMENT

with the teeth (see below), while in the lower jaw MeckeFs
cartilage becomes surrounded by the dentary and angular; the
dentary then connects with the infrarostrals of Meckel's carti-
lage. Paired vomers beneath the olfactory capsules, and pala-
tines across the anterior margins of the orbits develop next.
The pterygoids develop along the inner faces of the palato-
quadrate cartilages, and the squamosals along their outer sur-
faces, finally extending back over the auditory capsules. The
quadrato-jugal represents a dermal element developed in con-
nection with the posterior angle of the palato-quadrate carti-
lage, and fused with the cartilage quadrate bone of the palato-
quadrate itself. With the exception of this element the derm
bones remain easily separable from the cartilage bones and the
remains of the chondrocranium, even in the skull of the fully
grown frog.

3. The Teeth

Teeth are present in the adult on the premaxillse, maxillae,
and vomers. During the larval period the teeth are function-
ally replaced by the horny "jaws" and "teeth," so that the
true teeth develop relatively late. They form independently
of the bones with which they are later associated. During
metamorphosis a series of dermal papillae forms around the
margin of the upper jaw and covering the vomers. These are
the tooth germs; they project into an associated thickening of
the epidermis. The Malpighian cells of the epidermis covering
each tooth germ become the enamel organ and secrete a layer
of enamel over the surface of the hollow cone of the dentine
which is formed by the surface of the dermal papilla. The
cellular core of the papilla remains as the pulp cavity of the
tooth. The teeth are elongated by the formation of bony
tissue at their bases, and they gradually push through the
epidermis. This basal mass of bony tissue serves also to attach
the teeth to the inner sides of the jaw, and to the surface of the
posterior part of the vomer; their attachment does not occur
until some time after metamorphosis.

THE LATER DEVELOPMENT OF THE FROG 221

The teeth are continually wearing away and dropping out of
the jaw; they are replaced by new teeth which develop similarly
deeper in the dermis. There are therefore always present in
the jaws, teeth in various stages of development.

4. The Appendicular Skeleton

The elements of the pectoral and pelvic arches and limbs do
not appear until just before metamorphosis. We shall make
only the briefest reference to these structures.

The pectoral arch appears as a pair of crescentic cartilages
around the lateral and ventral parts of the body, opposite the
anterior end of the vertebral column. Just below its middle
each rod forms an articulation (gknoid cavity) with the head of
the humerus. Above this are formed the bony scapula and the
cartilaginous terminal suprascapula. Below the glenoid cavity
the arch is divided into the posterior coracoid and the anterior
procoracoid elements. The coracoid becomes bony, while in
connection with the procoracoid a dermal element, the clavicle,
develops later. The lower ends of the coracoids and procora-
coids become united on each side by a cartilaginous epicora-
coid. Later the two epicoracoids fuse together in the mid-line.

Posterior to the epicoracoids a median cartilage develops
which is the rudiment of the sternum. Later this fuses with the
epicoraccids, and its proximal section becomes bony while
posteriorly it forms the cartilaginous xiphisternum. Anterior
to the epicoracoids a similar omosternum is formed.

The pelvic arch also appears first as a pair of cartilaginous
rods, but these are early in contact medio-ventrally, and soon
fuse together. These articulate with the femora, and the parts
dorsal to the articulations (acetabuld) form the ilia, which con-
nect with the transverse processes of the last or ninth vertebra
(sacral vertebra). The postero- ventral region of each arch
becomes the bony ischium, while the antero-ventral part
remains cartilaginous as the pubis.

While the pelvic arch is, like the pectoral, originally at right
angles to the vertebral column, after metamorphosis it rotates

222 OUTLINES OF CHORDATE DEVELOPMENT

so as to lie nearly parallel with the vertebral column and at the
same time the ilia elongate enormously, throwing the attach-
ment of the hind limbs far backward.

The details regarding the development of the elements of the
limb skeleton are outside our province. For information the
student may be referred to the papers of Zwick (1898), Tscher-
noff (1907), and Schmalhausen (1907, 1908), and to the litera-
ture there cited.

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224 OUTLINES OF CHORDATE DEVELOPMENT

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THE LATER DEVELOPMENT OF THE FROG 225

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KRAUSE, W., See Hertwig, Handbuch, etc.
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226 OUTLINES OF CHORDATE DEVELOPMENT

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THE LATER DEVELOPMENT OF THE FROG 227

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228 OUTLINES OF CHORDATE DEVELOPMENT

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wiss. Zool. 63. 1897.

CHAPTER IV

THE EARLY DEVELOPMENT OF THE CHICK
THE EMBRYONIC MEMBRANES AND APPENDAGES

PAGE
INTRODUCTION. . . 229

I. THE EGG AND ITS PRODUCTION 232

1. The Egg 232

2. The Reproductive Organs of the Fowl 234

3. The Formation of the Egg and its Early Development . . . 236

A. The History of the Ovarian Ovum to Ovulation . . 236

B. The Period from Ovulation through Fertilization . . 240

C. From the Beginning of Cleavage to the Time of Laying 241

D. Gastrulation . . 248

II. THE FORMATION OF THE EMBRYO 251

III. THE EARLY DEVELOPMENT OF THE EMBRYO .... 260

1. The Head-fold . . . 260

2. Mesoderm 262

3. Endoderm 267

4. The Nervous System 269

5. The Vascular System 271

IV. THE EMBRYO OF ABOUT THIRTY HOURS (10-12 PAIRS

OF SOMITES) 275

V. THE SEPARATION OF THE EMBRYO FROM THE EXTRA-

EMBRYONIC STRUCTURES 279

VI. THE ESTABLISHMENT OF THE EXTERNAL FORM OF THE
EMBRYO 282

VII. THE EMBRYONIC MEMBRANES AND APPENDAGES . . 286

1. The Yolk-sac 286

2. The Amnion 292

3. The Allantois 295

MANY of the great embryological classics are based upon the
development of the chick. The pioneer works of Harvey, of
Malpighi, of Wolff, Pander, and Von Baer, bear witness to the
fact that answers to many of the fundamental problems of the
science of embryology were sought in the development of Ihis

229

230 OUTLINES OF CHORDATE DEVELOPMENT

form; and from its study came many of the long dominant
conceptions of the process, as well as the morphology, of
development.

To-day, when the development of the chick is better known,
as a whole, than that of -perhaps any other vertebrate, it remains
an extremely important subject, not so much because of its
historical importance, nor because of its very great practical
convenience on account of its abundance, ease of manipulation,
and freedom from seasonal limitations in its use, as for other
more significant reasons.

The development of the chick is fairly typical of the develop-
ment of the members of the largest and most important Chor-
date division, the Sauropsida. And besides, it suggests inter-
pretations of many of the very special features of mammalian
development. The egg of the fowl represents the climax of
the process of yolk accumulation, which begins in Amphioxus
and steadily increases through the Ganoids, Amphibia, and
Elasmobranchs. Consequently we find here, in pronounced
form, many interesting phases of the influence of deutoplasm
upon development. Indeed so great is the accumulation of
yolk here, that it remains no longer contained within the limits
of the embryo proper, and instead of exercising a retardative
influence upon the rate of development, it becomes so related
to the embryo that development is greatly hastened. In this
form the presence of the great mass of yolk results chiefly in
an extensive modification of the external form of the embryo,
particularly during its early phases. The embryo develops
for some time as a flat disc, upon the surface of the yolk mass,
so that it gives a sort of map-like spherical projection of a
Chordate embryo. And the morphological separation of em-
bryo and yolk, freeing the former from the influence of the inert
deutoplasm, enables the young chick to proceed to a remarkably
advanced stage of development during the three weeks of its
brief embryonic life.

Moreover, the chick embryo possesses, in comparatively
simple form, certain embryonic membranes and appendages,
which, in the Mammal, are highly specialized and come to play

THE EARLY DEVELOPMENT OF THE CHICK 231

an important role in the modification of embryonic form, and
an essential role in relating the embryo to the walls of the mater-
nal cavity in which it develops, a relation that is singly the most
important distinction of Mammalian development.

As an introduction to the subject we may outline, in a few
words, the more striking points in the life of the young chick.
Fertilization is internal, following a process of copulation, and
after laying, the eggs are brooded by the mother during their
three weeks incubation. This ensures, besides protection, the
temperature necessary for development. Normally this is
about 38° C.; development ceases entirely at temperatures
above 41°, and becomes very slow when it falls to 25° or even
to 28°. Newly laid eggs may remain alive, however, without
undergoing any advance, for a considerable period at much
lower temperatures than these; development then proceeds when
the temperature is raised.

The processes of maturation, fertilization, cleavage, and
blastula formation are completed before the ovum leaves the
body of the parent, while the egg is passing down the oviduct.
Thus the hen's egg, as laid, may be roughly compared to the
seed of a plant, in which a simple embryo is already formed and
surrounded with nutritive material for its later development.

The chief steps in the formation of the definitive embryo,
occur during the first day of incubation, and during the second
day a complicated series of folds appear, which largely effect a
separation of the embryo from the yolk-mass, with which it then
remains in connection by a narrow stalk. At the same time a
very extensive circulatory system develops, putting the embryo
into relation with its outlying food supply (Fig. 118). Develop-
ment now becomes very rapid since, through the morphological
separation of embryo and yolk, the usual retardative effect of
the latter is obviated, while an efficient physiological connec-
tion is established through the precocious appearance of the
circulation.

During the second and third days of incubation, appear the
embryonic membranes and appendages, which provide for
respiration, extend the nutritive surfaces, and afford the spaces

232 OUTLINES OF CHORDATE DEVELOPMENT

within which the embryo may fully extend. In general the
development of the embryo occurs progressively from the
anterior end, posteriorly. Thus the brain and other structures
of the head are very large and in a fairly advanced stage of
development, while the posterior part of the trunk and the tail
are still in process of formation. The heart, which appears very
far forward, is also a very prominent feature of the early embryo.
From about the fifth day the development and enlargement of
the body region reduce the relative prominence of the head
region, and the typically bird-like form of the embryo is ac-
quired about the eighth day.

On the twentieth day, usually, the chick makes a small perfora-
tion through the shell and begins to breathe with its lungs, and
on the following day the young chick breaks entirely from the
shell. The chick is representative of those birds whose young
are " precocious," for it is able to run about actively, to pick up
food, and to lead a generally active life, within a few hours after
hatching.

I. THE EGG AND ITS PRODUCTION

1. The Egg

We shall find it convenient to describe first the general struc-
ture of the hen's egg in its newly laid condition, although this
is not the true ovum; for the "egg" is not laid for some time,
usually twenty-one to twenty-three hours, after fertilization,
and during these hours the process of cleavage is completed,
gastrulation and germ layer formation are well advanced, so that
the "egg" already contains a multicellular embryo.

The true ovum, or egg cell proper, is the large yolk, or
vitellus, surrounded by a thin but rather tough vitelline membrane
(Fig. 85). The extreme animal pole is nearly free from yolk and
appears at the time of laying as a circular whitish area, the
blastoderm, 3-4 mm. in diameter: this pole is the less dense and
is therefore turned upward when the vitellus is free to rotate.
The blastoderm of this stage will be fully described later, but we
may now distinguish in it two regions, a central translucent

THE EARLY DEVELOPMENT OF THE CHICK 233

area pellucida, and a whitish peripheral area opaca. The great
mass of the ovum or vitellus is composed of the deutoplasm or
"yolk," of which two forms are present, known as white and
yellow yolk. The white yolk occupies the region just beneath
the blastoderm, and extends thence as a flask-shaped mass, to

vm

ad

pv

FIG. 85. — Semidiagrammatic illustration of the hen's egg at the time of laying
A. Entire "egg." Modified from Marshall. B. Diagram of a vertical sec-
tion through the vitellus or ovum proper, showing the concentric layers of white
and yellow yolk, o, Air chamber; ac, chalaziferous layer of albumen; ad, dense
layer of albumen; a/, fluid layer of albumen; b, blastoderm; c, chalaza; I, latebra;
nl, neck of latebra; P, nucleus of Pander; pv, perivitelline space; smi, inner
layer of shell membrane; smo, outer layer of shell membrane; v, vitellus or "yolk" ;
vm, vitelline membrane; wy, layers of white yolk; yy, layers of yellow yolk.

the center of the whole vitellus; surrounding this the deuto-
plasm is arranged in several concentric layers, thick layers of the
yellow yolk alternating with thinner strata of white yolk (Fig.
85, B). These two forms of yolk differ in physical characteris-
tics other than color, and also in chemical composition; both are
made up of yolk spheres or plates, which in the white yolk are
smaller and quite variable in size and form.

234 OUTLINES OF CHORDATE DEVELOPMENT

Surrounding the vitellus or egg cell, are several nutritive and
protective egg membranes, all of the tertiary class, i.e., formed
by the accessory reproductive organs, the vitellus alone having
been formed within the ovary; there are no secondary or chori-
onic membranes. Immediately surrounding the vitellus is the
" white'7 or albumen. The chemical composition of this is
quite complex, various albumens forming the predominating
constituents. Two denser, opaque, twisted cords, the chalazce,
extend through the albumen from opposite sides of the vitellus,
toward the apices of the shell. These are continuous with a
very thin, dense layer of albumen surrounding the vitellus, the
chalaziferous layer. Outside of this the albumen forms a rather
thick dense layer, and superficially there is a still thicker layer of
more fluid albumen. In the hard-boiled egg the albumen can
often be seen to be laid around the vitellus in spiral sheets.

The entire ovum is enclosed in a definite ovoid shell, very
resistant to pressure applied gradually, though easily broken
by a sharp blow. The shell is covered superficially by a thin
structureless cuticle perforated by numerous pores. The
chief substance of the shell is composed of loosely arranged
particles of the carbonates and phosphates of calcium and
magnesium, in an organic matrix. The inner surface of the shell
is formed by a thinner but denser layer of inorganic salts.
The dried shell is very porous and affords an easy pathway for
the passage of gases and water vapor.

Lining the shell is the tough shell membrane. This is a
double sheet of fibrous connective tissue; at the blunter end of
the shell its two layers are separated by an air space, which is
often of considerable size in eggs that have been laid for some
time.

2. The Reproductive Organs of the Fowl

A better understanding of the structure of the egg can be had
from the study of its formation, but first we must review the
main facts regarding the re productive system of the fowl. These
organs are asymmetrically developed, those of the right side

THE EARLY DEVELOPMENT OF THE CHICK 235

ov

cl

FIG. 86.— The reproductive system of the fowl. After Duval (Coste). The
figure shows two eggs in the oviduct, whereas normally only one egg is in the
oviduct at a time, b, Blastoderm; c cicatrix; cl, cloaca; da, dense layer of
albumen;/, empty egg follicle from which the ovum has escaped; g, glandular por-
tion of oviduct; i, isthmus; m, mesovarium; 01-04, ovarian ova in various stages of
growth; O\, ovum in upper end of oviduct; Oz, ovum in middle portion of ovi-
duct (the oviduct has been cut open to show the structure of this ovum) ; os, os-
tium or infundibulum; ov, ovary containing ova in various stages of growth;
r, rectum; u, uterus; v, vitellus; w, ventral body wall, opened and reflected.

236 OUTLINES OF CHORDATE DEVELOPMENT

having degenerated to functionless vestiges; the left ovary and
oviduct correspondingly become very large.

The ovary (Fig. 86) appears to be composed of a mass of
globules of varying size, suspended from the dorsal abdominal
wall by a double peritoneal fold known as the mesovarium
(cf. mesentery). These globules are partly grown, immature
ova, and in the adult hen they vary in size from a simple cell up
to the full-sized vitellus. The oviduct is a large, rather thick-
walled, muscular tube, considerably convoluted and showing
a well-marked regional differentiation. Its upper end opens out
of the body cavity from the region of the ovary, while its lower
end discharges directly into the cloaca. Three general regions
are to be distinguished : the first, or oviduct proper, is the most
extensive and is itself divisible into three sections. The abdom-
inal opening of the oviduct is a wide, flaring, funnel-shaped
opening called the ostium, or infundibulum, or sometimes the
fimbriated opening, from its fringe-like margin; its walls are thin
and muscular, and it is lined internally with cilia. The ostium
leads directly into the long convoluted glandular portion, and
this is followed by the short third section of the true oviduct,
the isthmus. The second general region is the so-called uterus,
a dilated portion, also with glandular walls. The short terminal
region is a thin- walled vagina, which opens into the cloaca just
dorsally to the opening of the rectum. The functional charac-
teristics of these regions will be described in the following
paragraphs.

3. The Formation of the Egg and its Early Development

The early developmental history of the egg may conveniently
be described in three periods: (A) ovarian development to
the time of ovulation; (B) from ovulation through fertilization;
(C) from the beginning of cleavage to the time of laying.

A. THE HISTORY OF THE OVARIAN OVUM TO OVULATION

The rhythm of egg production in the domestic fowl is unusual
in that, as a rule, a long period of egg formation and laying,
extending over several months, is followed by a relatively

THE EARLY DEVELOPMENT OF THE CHICK 237

brief period of nearly or quite complete cessation. This is
quite in contrast to the great majority of animals, in which a
large number of ova are produced within a very brief period,
a condition probably correlated with the very large size of the
ova, for the formation of even a single egg requires a consider-
able expenditure of energy and substance. Moreover, there is
space in the organs of reproduction for but a very few ova of
such large dimensions. Such a succession in the formation of
the ova makes it possible to observe, in a single ovary, most of
the steps in the formation of the fully grown ovum.

The first phase of oogenesis, the multiplication of the oogonia,
occurs during the embryonic life of the chick, and is practically
completed by the time of hatching. All of the ova produced
later, during the period of adult life, are thus in the form of
primary oocytes at the "birth" of the chick. Surrounded by
the non-germinal cells of the "germinal" epithelium, the oogo-
nia or primitive ova multiply rapidly. Some of them leave the
epithelium and migrate into the stroma of the ovary where they
degenerate. The remaining oogonia, which commence to
enlarge while still continuing their multiplication, together with
the rapidly proliferating epithelial cells, then form elongated
strands or cords, extending from the epithelium into the stroma.
Soon these definitive oogonia cease multiplication and are then
to be termed primary oocytes (Fig. 87, A). The strands then
break up into cell groups or "nests," each consisting of a single
primary oocyte surrounded by a number of the original epithe-
lial cells; these latter take up a definite epithelial arrangement
around the oocyte, and thus form the primitive egg follicle
(granulosa cells). This arrangement of the cells occurs a few
days after hatching. The structure of the oocyte follicle at
this age is shown in Fig. 87, B.

The egg cell, both nucleus and cytoplasm, now begins to
enlarge and deutoplasmic granules are laid down all around the
centrally located nucleus, and throughout the cytoplasm, except
in its peripheral region which remains comparatively free from
yolk. This peripheral protoplasmic layer is definitely thickened
at one point, namely, toward the attached surface of the ovum

238 OUTLINES OF CHORDATE DEVELOPMENT

or follicle, forming there the germinal disc or spot. When the
ovum reaches a diameter of something more than 0.5 mm.
the nucleus migrates into the germinal disc, where it remains

FIG. 87. — Growth stages in the oogenesis of the hen's egg. After Sonnen-
brodt. A. Oocyte measuring 0.012 X0.016 mm., the nucleus of which is 0.006
mm. in diameter. B. Oocyte measuring 0.018 X0.028 mm., the nucleus of which
is 0.0105 X0.014 mm. Enclosed in follicle. C. Oocyte measuring 0.040 X0.045
mm., the nucleus of which is 0.020X0.022 mm. D. The nucleus only, of an
oocyte measuring 5.84 X 6. 16 mm., the nucleus itself measuring 0.214 X 0.238 mm.
Total view showing the small chromosomes in the midst of a collection of chro-
matin nucleoli. E. Vertical section through the nucleus only, of an oocyte, the
follicle of which measured 37 mm. in diameter. The nucleus itself is 0.455 mm.
in diameter and 0.072 mm. in greatest thickness, c, Chromosomes; cr, extra-
nuclear chromsome-like bodies; /, follicle; ra, nuclear membrane; mf, folds in
nuclear membrane; n, nucleus; nu, chromatin nucleolus; ps, pseud ochromosomes;
s, centrosphere; v, yolk nucleus or vitellogenous body.

throughout the remainder of its ovarian history (Fig. 88). It
should be noted that the eccentricity of the nucleus, which

THE EARLY DEVELOPMENT OF THE CHICK 239

marks the animal pole of the ovum, is toward the attached
surface.

The formation and accumulation of yolk now become more
rapid. The surface of the ovum is in the form of a zona radiata,
through the pores of which nutritive substances diffuse from

jr.*

FIG. 88. — Section through the pigeon's ovarian ovum, 1.44X1.25 mm. From
Lillie (Development of the Chick), /.s., Stalk of follicle; G.V., germinal vesicle
or nucleus; Gr., granulosa cells; I/., latebra; p.P., peripheral protoplasm; pr.f.,
primordial follicles; Th.ex., theca externa; Th. int., theca internal Y.Y., yellow
yolk; Z.r., zona radiata.

the follicle cells, which thus function as nurse cells (Fig. 88).
The rate of growth of the egg during its final stages may be
determined by the arrangement of the concentric layers of
white and yellow yolk (Fig. 85, B), which mark daily periodici-
ties in the formation of deutoplasm (Riddle) . Toward the close
of the growth period the follicle becomes more clearly mem-
branous, and along the side opposite its attachment, which is

240 OUTLINES OF CHORDATE DEVELOPMENT

comparatively non- vascular, a modified band appears; this
is the cicatrix, where the follicle ruptures when the ovum
escapes from the ovary.

Just before the egg leaves the ovary its nucleus, lying
flattened against the vitelline membrane, reaches the enormous
diameter of about 0.3 mm. It is now known as the germinal
vesicle, since the condensation of its small chromatin content
leaves the nucleus as a large clear spot (Fig. 87, D, E). The
last events before ovulation are the breaking down of the
nuclear wall and the formation of the first polar spindle. This
rotates into position and the primary oocyte, prepared for its
first maturation division, pauses to await ovulation.

B. THE PERIOD FROM OVULATION THROUGH FERTILIZATION

At the time a completed egg is laid, or very shortly thereafter,
the region of the ostium or infundibulum of the oviduct,
becomes very active and seems to grasp the ovarian follicle
containing the primary oocyte, through muscular or ciliary
action, or both. The follicle then becomes ruptured, appa-
rently by the pressure exerted by the contraction of the infun-
dibulum, or by its pulling away from the region of the ovary,
and the oocyte, contained within the infundibulum, is withdrawn
from the follicle, and ovulation is accomplished. In some cases
it may be that the follicle is ruptured before it can be grasped
by the infundibulum and the freed oocyte is subsequently
received by the fimbriated opening. The oocyte always enters
the infundibulum with its chief axis transverse to the long axis
of the oviduct, and this relation is retained during the entire
passage of the ovum down the oviduct.

The spermatozoa, after their receipt by the female, make
their way to the extreme upper end of the oviduct, where they
collect, remaining alive and capable of functioning for two
weeks or more. Upon its entrance into the oviduct, therefore,
the primary oocyte becomes bathed in a fluid containing sperm
cells, and fertilization immediately ensues. The details regard-
ing the penetration of the spermatozoa are not fully described,

THE EARLY DEVELOPMENT OF THE CHICK 241

but it is known that this occurs immediately after ovulation,
while the ovum is in the infundibulum. Polyspermy is normal,
five to twenty-four spermatozoa having been counted within
a single ovum (Patterson). Entrance of the spermatozoa
affords the stimulus to the completion of maturation, which
offers no unusual features. After the second maturation division
the egg nucleus unites with one of the sperm nuclei and the first
cleavage spindle is typically established.

C. FROM THE BEGINNING OF CLEAVAGE TO THE TIME
OF LAYING

Before continuing our account of the development of the
ovum we must outline the series of events occurring during
the passage of the egg down the oviduct; we shall follow the
accounts given by Patterson, and Pearl and Curtis.

The first cleavage furrow appears about three hours after
ovulation. During this interval the egg has traversed the
entire glandular portion of the oviduct, the walls of which have
secreted the denser layers of albumen and the chalazse (40 to
50 per cent, of the entire weight of albumen) . The egg is carried
along chiefly by peristaltic contraction of the oviducal wall,
and as it passes it is rotated about the long axis of the oviduct,
so that the germ disc describes a spiral path; this accounts for
the spiral arrangement of the albumen around the yolk. Dur-
ing the next hour or so (Pearl) the egg traverses the isthmus,
the walls of which secrete the shell membrane over the surface
of the dense albumen as the egg enters this region. The fluid
layer of albumen is added while the egg is traversing the isth-
mus and the upper part of the uterus. The formation of this
fluid albumen, which passes through the shell membrane
already laid down, is completed five to seven hours after the
egg enters the uterus (nine to eleven hours after entering the
oviduct). Before this the calcareous shell substance has begun
to be laid down on the shell membrane. The egg usually
occupies twelve to sixteen hours longer in completing its
passage through the uterus and vagina. At the end of this

242 OUTLINES OF CHORDATE DEVELOPMENT

time, twenty-one to twenty-seven hours after ovulation, gas-
trulation has begun and the egg is ready to be laid. If the
completely formed egg reaches the vagina during the middle of
the day (8 A. M. to 4 P. M.) it may be laid promptly; otherwise
it is retained within the vagina until the following day. In the
latter case, since development continues during the entire
period of its retention, which may be quite prolonged, the
embryo may be in a fairly advanced stage when the egg is
finally deposited. Thus, variation in the period of retention
accounts for the variation in developmental stages observed in
different eggs as laid.

TABLE SHOWING THE CHIEF EVENTS IN THE EARLY
HISTORY OF THE HEN'S EGG

Hours after
ovulation

Location in
oviduct

Action of oviduct

Action of germ
disc

0

Infundibulum

Reception of ovum

Maturation and fer-
tilization

0 to 3

Glandular por-
tion

Secretion of chala-
zae, chalaziferous,
and dense layers
of albumen

First cleavage fur-
row

3 to 4

Isthmus

Secretion of shell
membrane and
fluid albumen

Formation of eight
cells

4 to 21 (27)

Uterus and
vagina

Secretion of shell
and fluid albumen.
Retention prior to
laying

Gastrulation begun,
or completed if egg
is long retained

We may now return to describe the processes of development
occurring during the period prior to laying. The unicellular
germ disc consists of a quite definitely circumscribed area at
the animal pole of the vitellus. The disc is about 3 mm. in
diameter and less than 0.5 mm. in thickness. Beneath, the

THE EARLY DEVELOPMENT OF THE CHICK 243

protoplasm merges with a well-marked region of the white
yolk called the nucleus of Pander, which connects with the
central white yolk by a narrow stalk called the latebra (Fig.
85, A). In the disc itself two regions may be distinguished, a
large central area, which is to form the blastoderm proper, and
a narrow marginal area of denser appearance, known as the
periblast. Peripherally the periblast continues for some dis-
tance, perhaps completely, over the surface of the vitellus as
an extremely thin protoplasmic layer.

The first cleavage furrow appears as a short shallow groove,
near the middle of the germ disc, in length approximately one-
half the diameter of the disc (Fig. 89, A). Sections show that
this cleavage also fails to extend completely through the disc
vertically (Fig. 90, A). It is not known that the first cleavage
plane coincides with the median sagittal plane of the embryo:
indeed it seems probable that, as in other eggs of this extremely
meroblastic type, there is no correspondence between these
two planes. The position of the main embryonic axis is, how-
ever, fairly uniform, though not completely fixed. It lies
approximately at right angles to the long axis of the whole egg,
the anterior end of the embryo directed to the left, when the
sharper end of the egg is held pointing away from the observer.
In the few cases actually observed, the first cleavage plane
seems to have no definite relation to these axes.

The second cleavage is also vertical, and approximately at
right angles to the first, giving four adequal cells, all still in-
complete (Fig. 89, B) . About an hour after the first cleavage,
the third appears. Typically, though not in a majority of
instances, this is a fairly regular cleavage, parallel with the
first, and dividing the disc into two rows of four cells each.
Frequently this cleavage is more or less irregular in form, and
the synchronism of division is lost by this time (Fig. 89, C) .
The subsequent stage, consequently, may be said to consist
only approximately of sixteen cells. These are very irregular,
but the general tendency of the fourth plane is to separate each
of the eight cells into a central and a distal cell.

During the appearance of the third and fourth cleavages,

244 OUTLINES OF CHORDATE DEVELOPMENT

the central portion of the germ disc has become divided hori-
zontally by a cleavage plane, connecting the lower margins of

FIG. 89. — Cleavage in the hen's egg. Surface views of the blastoderm and
the inner part of the marginal periblast only. From Patterson. The anterior
margin of the blastodisc is toward the top of the page. A. Two-cell stage.
About three hours after fertilization. B. Four cells. About three and one-fourth
hours after fertilization. C. Eight cells. About four hours after fertilization.

D. Thirty-four cells. About four and three-fourths hours after fertilization.

E. One hundred and fifty-four cells upon the surface; the blastoderm averages
about three cells in thickness at this stage. About seven hours after fertiliza-
tion, ac, Accessory cleavage furrows; ra, radial furrow; p. inner part of marginal
periblast; sac, small cell formed by the accessory cleavage furrows.

the first and second planes. In this way a small group of
central cells become completely circumscribed, and are to be

THE EARLY DEVELOPMENT OF THE CHICK 245

distinguished from the marginal cells, which remain incomplete
both below and distally, retaining their connection with the
periblast (Fig. 90, B) . A definite though narrow space appears,
accompanying the horizontal cleavage, which separates the
superficial cellular elements from the underlying undivided

mp

FIG. 90. — Vertical sections through the chick blastoderm during the process
of cleavage. After Patterson. A. Section through the two-cell stage. B.
Median section through the thirty-two cell stage. C. Part of a longitudinal
section through the sixty-four cell stage, b, Blastoccel or segmentation cavity;
c, central cells; i, inner cell cut off by horizontal cleavage plane; I, neck of latebra;
m, marginal cell; mp, marginal periblast; n, nucleus; p, first cleavage; v, vitelline
membrane.

protoplasm. This space is the beginning of the segmentation
cavity or blastoccel; the protoplasm beneath it is termed the
central periblast. The original periblast region is now distin-
guished as marginal periblast. The two periblastic regions

246 OUTLINES OF CHORDATE DEVELOPMENT

retain their connection with one another peripherally, in the
deeper region of the marginal cells.

We should note here a few details regarding the history of the
accessory or supernumerary spermatozoa. During the period
intervening between fertilization and the early cleavages, these
form nuclei which migrate to the outlying portion of the blasto-
disc. There they may divide once or twice, forming small
groups of daughter nuclei. These divisions are sometimes
accompanied by slight indications of cytoplasmic division, and
the short superficial grooves thus formed are known as the
accessory cleavages (Fig. 89) . These are visible during the f our-
and eight-cell stages; they are usually radial in direction, lying
just across, or without, the margin of the blastodisc. No true
cells are formed by such cleavages. The accessory sperm
nuclei degenerate rapidly, the accessory cleavages fade out,
and by the time thirty-two cells are formed no traces of these
structures are left.

During subsequent cleavages the number of central cells
increases rapidly, by additions from the dividing marginal cells,
and through their own multiplication, which becomes very
rapid as the cells diminish in size. Additional horizontal cleav-
ages appear in the central cells, converting the roof of the
blastocoel into a layer several cells in thickness (Fig. 90, C).
No cells are added to the germ disc from the floor of the
segmentation cavity. The marginal cells become greatly
shortened through the continued cutting off of central cells,
and finally they are limited to the extreme margin of the
blastodisc.

About the time two or three hundred cells are formed, inter-
cellular furrows extend out into the marginal periblast (Fig. 89,
E). Up to this time both central and marginal periblast have
been entirely free from nuclei, but soon these areas, which are
still directly continuous, become converted into a nucleated
syncytium. The details of this process have not been described
for the chick, but are well known in the pigeon (Blount). In
the latter form, when the marginal cells have become reduced
to an approximately spherical form by the cutting off of central

THE EARLY DEVELOPMENT OF THE CHICK 247

cells, their nuclei continue to divide, while accompanying
cytoplasmic divisions are
either incomplete or en-
tirely lacking. A large
number of free nuclei is
thus formed in the margin
of the blastodisc. These
nuclei, continuing to mul-
tiply, wander out into the
marginal periblast, con-
verting this into a nu-
cleated though non-cellu-
lar tissue. From this re-
gion some of the nuclei
migrate inward below the
blastodisc, converting the
central periblast also into
a nucleated structure, ex-
cept in its middle area,
above the nucleus of
Pander, which appears to
remain free from nuclei.
The nucleated rim of the
periblast forms a part of
what is known later as the
germ wall.

The circular blastoderm
now begins to extend radi-
ally, partly on account of
the growth of its own cells,
and partly (continuing
Blount's account) by the
addition of cells from the
marginal periblast. The
region of the original blas-
todisc now becomes thin-
ner and more transparent, and is known as the area pellucida,

248 OUTLINES OF CHORDATE DEVELOPMENT

while its circular margin, apparently derived largely from the
periblast, is called the area opaca. The ring-like periblast
continues to grow and to become nucleated more peripherally,
at the same time that it is contributing cells to the blastoderm,
so that it steadily increases in diameter. The inner nucleated
margin of the periblast, which becomes of cellular composition
and contributes to the later extra-embryonic tissues, is known
as the germ wall (Fig. 91). Later the cells of the blastoderm
extend peripherally, overlapping the inner margin of the germ
wall, so that there is a narrow region transitional between pellu-
cid and opaque areas. We should not overlook the fact that
the lower surface of the periblast is directly continuous with the
yolk-mass, and is peripherally continuous with a very thin
superficial layer of protoplasm; this latter is sometimes re-
ferred to as a part of the germ wall. The thinning of the blasto-
derm, mentioned above, may be regarded as indicating the
completion of the blastula stage and the beginning of gastrula-
tion, to which we may next turn our attention.

D. GASTRULATION

In the chick the formation of the primary germ layers, ecto-
derm and endoderm, i.e., gastrulation proper, is quite easily
distinguished from the processes of notogenesis and mesoderm
formation. In the following account of gastrulation many
details are supplied from Patterson's account of this process in
the pigeon, for this period in the development of the chick is
incompletely known, although it is clear that the pigeon and
chick are in agreement as to essentials. The thinning of the
blastoderm through the rearrangement of its cells, continues
rapidly as the diameter of the area pellucida increases. It is
most marked in a wedge-shaped area in the posterior part of the
blastoderm, the most posterior portion of which may come to be
only one cell in thickness (Fig. 92, A). In this region the sub-
germinal or segmentation cavity increases in depth, and around
the hinder margin of the thinner area the germ wall (area opaca)
appears to be interrupted more or less completely, so that the
blastoderm cells border directly upon the yolk.

THE EARLY DEVELOPMENT OF THE CHICK 249

The first step in the real process of gastrulation is the turning
under of a few of the marginal cells in this posterior region of
the blastoderm, where it is free from the germ wall. As the
involution of superficial cells continues, this margin soon
becomes thickened, and since the involuted cells are the rudi-
ment of the endoderm, the thickening represents the lip of the

FIG. 92. — Diagrams of reconstructions of the pigeon's blastoderm. From
Lillie (Development of the Chick) after Patterson. A. Thirty-one hours after
fertilization. B. Thirty-six hours after fertilization. C. Thirty-eight hours after
fertilization. E, Gut endoderm; GW, germ wall; O, margin of overgrowth ; PA ,
outer margin of area pellucida; R, in B, margin of involution; in C, mass of cells
left after closure of the blastopore; S, beginning of yolk-sac endoderm; SG,
anterior part of subgerminal cavity (blastocoel), as yet free from endoderm; Y,
yolk zone; Z, zone of junction. The numbers 1-7 along the line C-D, in A,
indicate the number of cells in the thickness of the blastoderm in these regions.

blastopore, which is here reduced to a short crescent, between the
two free extremities of the germ wall (Fig. 92, B). Once
established, the endoderm rapidly grows forward between the
yolk and the ectoderm, as the upper cells of the blastoderm may
now be called, extending through the segmentation cavity

250 OUTLINES OF CHORDATE DEVELOPMENT

laterally as well as anteriorly (Fig. 91). During these early
stages the endoderm cells are considerably scattered, and are
arranged as a solid mass or definite layer only in the region of
the blastoporal margin. As the endoderm cells gradually ex-
tend across the segmentation cavity, two other processes become
apparent (Fig. 92, C). First, the free posterior extremities
of the germ wall approach, and finally meet and fuse; this proc-
ess, is known as the closure of the blastopore, the blastoporal
opening being present only virtually, and represented by the
region between the extremities of the germ wall. The second
process is the beginning of the extension of the blastoderm, or
gastrula, from every side save the region of the blastoporal
margin. The endoderm cells soon extend out to the margin of
the segmentation cavity in every direction except anteriorly.

The closure of the blastopore produces a small thickened
region, representing the contracted blastoporal margin, which
is left just within (anterior to) the germ wall, where this now
becomes continuous posteriorly. The process of extension of
the blastoderm now involves this region and leaves the con-
tracted blastoporal margin well within the area pellucida.

Normally the egg is laid twenty-two to twenty-three hours
after fertilization, in approximately this condition, with gastru-
lation not quite completed. The structure of the unincubated
blastoderm may therefore be described as follows. Three
general regions are to be distinguished. The original area pel-
lucida is surrounded by a complete area opaca, and beyond this
is a narrow margin where the blastoderm cells are extending
over the surface of the yolk. The pellucid area is formed by a
layer of ectoderm cells, slightly thickened toward the middle
of the area; posteriorly it includes also a sheet of endoderm
cells. The endoderm is in the form of a definite layer only
toward the posterior margin, elsewhere the endoderm cells are
scattered through the segmentation cavity, in the process of
migrating toward its anterior margin. A narrow space between
the endoderm and yolk, really the remains of the segmentation
cavity there, is the rudiment of the archenteron. The area
opaca, save in its posterior region, is formed by the thickened

THE EARLY DEVELOPMENT OF THE CHICK 251

margin of the blastoderm resting upon the germ wall and fusing
peripherally with it. Posteriorly, where the germ wall is nar-
rower, there is a thickened region of the cellular germ disc which
represents the contracted blastoporal margin. In this region
the ectoderm and endoderm are continuous.

During the first few hours of incubation, or even before lay-
ing in cases where the eggs have been retained for some time
longer than usual in the vagina, the endoderm extends com-
pletely across the segmentation cavity and becomes organized
into a fairly definite layer.

From the preceding description it will be seen that the
process of gastrulation in the chick is essentially a process of
involution. There is no true invagination, and the process of
epiboly is not immediately concerned in the establishment of
the primary inner layer. Moreover, the process of epiboly is
here greatly limited, being restricted to a narrow posterior
section of the blastoderm. In other words, the entire blasto-
poral region is greatly reduced, doubtless in correlation with the
excessive amount of yolk in the ovum.

The formation of the middle germ layer and the chief axial
structures of the embryo, is not intimately bound up with the
gastrulation process, as in the forms previously described. We
may now consider these processes in connection with the gen-
eral development of the whole embryonic region.

II. THE FORMATION OF THE EMBRYO

The earliest indication of the true embryo becomes visible
during the early hours of incubation, immediately after the
entire area pellucida has become two layered, through the com-
plete extension of the endoderm. It appears first as a slightly
thickened band, not very well marked, extending directly from
a point approximately in the middle of the area pellucida,
nearly to its posterior margin. This is called the primitive
streak; it is constituted at first solely by a thickening in the
ectodermal layer (Fig. 93). Once established, the primitive
streak grows very rapidly, chiefly through posterior elongation,

252 OUTLINES OF CHORDATE DEVELOPMENT

the anterior end remaining relatively fixed. The blastoderm,
too, shares in this elongation and becomes irregularly oval, and
then pear-shaped, the blunter end being anterior.

FIG. 93. — Total views of chick blastoderms. A. After Duval (modified) ;
B-D, after Lillie. A. Unincubated blastoderm, with primitive streak just form-
ing. B. Primitive streak formed, head process not yet indicated. C. Head
process formed; head-fold just commencing. D. Just before the establishment
of the first mesodermal somites, ac, Amnio-cardiac vesicle; cr, crescent-shaped
thickening at the posterior side of the blastoderm, in the region of endoderm
and mesoderm formation; g, primitive groove; hf, head-fold; hp, head process;
i, blood islands; m, axial thickening of mesoderm; mp, medullary plate; mr,
margin of mesoderm; n, Hensen's node; o, area opaca; p, area pellucida; pa,
proamnion; pi, primitive plate; pp, primitive pit; s, primitive streak; t, sinus
terminalis (marginal sinus); v, area vasculosa; vi, area vitellina interna.

As the primitive streak elongates a narrow transparent line
appears along its middle; this is the primitive groove. Anteriorly

THE EARLY DEVELOPMENT OF THE CHICK 253

the primitive groove terminates in a small depression, the
primitive pit, near the anterior end of the primitive streak, where
a slight thickening, known as the primitive knot or Hensen's
node, is visible (Fig. 97). In front of this another larger though
less definite thickening, known as the head process, soon may
be made out. Posteriorly the primitive streak is somewhat
transversely extended, just within the border of the area pel-
lucida, forming a more or less well marked crescentic area,
through which the primitive groove may be continued, giving
this a bifurcated appearance here. Between this broadened
hinder end of the primitive streak and the margin of the pellu-
cid area, a wide thickened region can sometimes be discerned;
this is known as the primitive plate.

Many important structural details of the primitive streak
region may be determined through the study of sections. Fig-
ures 94, 101 illustrate sections through representative regions
of an early primitive streak. The ectoderm is broadly thick-
ened as the rudiment of the medullary plate, and along the
mid-line is the primitive streak, soon marked by the rapid pro-
liferation of ectoderm cells, which are thrown off in the space
between ectoderm and endoderm. These cells are the rudi-
ment of the mesoderm. The endoderm forms a uniformly thin
sheet of cells across the entire blastoderm.

A little later (Fig. 94, B) the primitive groove is indicated,
bordered by a pair of primitive folds. Proliferation of mesoderm
cells from the inner surface of the ectoderm is now very rapid,
and these cells soon migrate distally throughout a large part of
the space between the two primary germ layers. Near the mid-
line they become intimately related with the endoderm, often
giving the misleading appearance of having been derived
directly from that layer (Fig. 101). Soon the cells along the
middle of the primitive streak have multiplied so extensively
that they form a dense mass, in which clearly marked limits of
the germ layers cannot be made out. More laterally, however,
the layers are completely distinct. The ectoderm extends out
over the germ wall and yolk; the endoderm, now more than one
cell thick, reaches only to the germ wall, with which it fuses,

254 OUTLINES OF CHORDATE DEVELOPMENT

the mesoderm forms a loosely arranged sheet of cells, thinning
peripherally and extending for a short distance between the
ectoderm and germ wall.

The conditions found near the extremities of the primitive
streak deserve special mention. Posteriorly, the primitive
plate shows a transversely extended region of mesoderm pro-

mp

en

FIG. 94. — Transverse sections through various levels of the blastoderm at
different ages. A. Through the head process of an embryo of about sixteen
hours. After Duval. B. Through the primitive streak of an embryo of seven-
teen and one-half hours. After Lillie. C. Through the primitive plate of an
embryo of about the same age as A. After Lillie. ec, Ectoderm; en, endoderm;
/, primitive folds; g, primitive groove; gw, germ wall; m, mesoderm; mp, medullary
plate; pp, primitive plate.

liferation, which continues across the posterior side of the
primitive plate, so that the pellucid area behind the primitive
streak is composed of all three germ layers (Fig. 94, C). In the
region of the head process, i.e., in front of the primitive pit
and streak, conditions are not essentially unlike those found
farther back. The primitive groove is absent, and the cells
of the three layers are more intimately fused. Relatively

THE EARLY DEVELOPMENT OF THE CHICK 255

little mesoderm is proliferated from the anterior part of the
head process, so that in front of this, the blastoderm is for a
considerable time composed of only the two primary layers.

Surface views of entire blastoderms now show considerable
modifications in the structure and relations of the primary
pellucid and opaque areas. The outline of the elongated pel-
lucid area becomes irregular; as a whole it is divisible into a
posterior darker region where all three layers are present, and an
anterior lighter area, crescentic in. form, composed of ectoderm
andendoderm only (Fig. 93, B). Later the irregular anterior
border of the mesoderm can be seen to advance along the sides
of the area pellucida, in front of the level of the head process
(Fig. 93, C). Finally the mesoderm extends completely around
the margin of the pellucid area, leaving only a small area
directly in front of the head process in the two layered condition ;
this area is known as the proamnion (Fig. 93, D).

Meanwhile the area opaca has been undergoing very marked
modifications. This has broadened rapidly, and in its lateral
and posterior regions, where the mesoderm has extended more
widely over the germ wall, it has assumed an irregularly mottled
appearance. Sections show this to be due to the formation of
differentiated cell groups known as blood islands, the beginning
of the vascular system. The presence of these blood islands
marks that portion of the opaque area known as the area vascu-
losa (Fig. 93, C, D). This appears first immediately behind the
embryo, but rapidly spreads laterally and anteriorly. Per-
ipherally it becomes bounded by a definite blood vessel known
as the sinus terminalis. Beyond this the opaque area is formed
only of ectoderm and endoderm, extending widely over the
yolk and known as the area vitellina. The blood islands are
formed of compact cell masses scattered through the deeper
portion of the germ wall. The cells composing them have
apparently, though not certainly, differentiated in situ; they
become covered superficially by a layer of scattered germ wall
cells, which comes to be known later as ccelomic "mesoderm"
(Fig. 95). While this layer, and the blood islands, early be-
come directly continuous with the mesoderm of the pellucid

256 OUTLINES OF CHORDATE DEVELOPMENT

area derived from the primitive streak, it is commonly supposed

that this relation is second-
ary. The blood islands later
become hollowed out, their
constituent cells forming
both the walls and the cor-
puscular contents of the ir-
regular vascular la ounce.
These soon anastomose with
one another forming a com-
plex network throughout the
area vasculosa; still later
this net connects with the
vascular structures of the
pellucid area and of the em-
bryo. The cellular portion
of the germ wall remaining
the ccelomic " meso-
derm" and the blood islands
forms the

§ | rudiment of the yolk-sac en-
3 | doderm, the development of
•3 1 1 1- which we shall describe pres-
§• ently.

At this point we should
consider briefly the relation
of the primitive streak and
associated structures to the
rudiments of the true em-
bryo. From what has been
£ said in the early part of this
^J chapter, we should not ex-
* | pect to find that all of the
§ a structures mentioned in the
® o> 1 * preceding paragraphs will be
43 ^ 8 ^ found to contribute to the
formation of the definitive embryo. As a matter of fact, of

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THE EARLY DEVELOPMENT OF THE CHICK 257

all the structures so far described, only those in the vicinity
of the head process, represent actual embryonic rudiments;
these are, that thickening of the ectoderm described as the
medullary (neural) plate, and the axial endoderm and meso-
derm lying directly beneath it. The substance of the primi-
tive streak, therefore, lies posterior to the embryo proper, and
the boundary between the two is indicated by the position of
the primitive pit;

As the embryo becomes more definitely established, it elon-
gates posteriorly, while the primitive streak correspondingly
shortens. The relation between the two structures is such
that the embryo draws its substance from the anterior end of
the primitive streak, or, we may say, the materials of the
anterior end of the primitive streak are slowly redifferentiated
and payed into the hinder end of the embryo. The region
where this process of redifferentiation is proceeding is indicated
as Hensen's node (primitive knot). Finally the primitive
streak is wholly transformed into embryonic structures, but
this is not fully accomplished until a relatively late stage in
development (second day of incubation). To the question as
to how much of the definitive embryo is formed of structures
primarily anterior to the primitive streak, no precise answer
can be given. In a general way, however, it may be said that
the region of the primary location of the primitive pit corre-
sponds roughly with the boundary between hind- and mid-
brain, and that structures developing anteriorly to this level
were related originally to the region of the head process, rather
than to the primitive streak.

We are now prepared to understand the essential homologies
of the primitive streak, having learned of its relation to the
embryo, on one hand, and to the structures of the gastrula, on
the other. Theoretically the primitive streak is to be inter-
preted as the result of a modified process of concrescence (con-
fluence). The chief alterations of the typical process of con-
crescence (confluence) are apparently due to the relatively
enormous mass of yolk, and the consequent modification of
the gastrula into a flat sheet, more or less intimately related to

258 OUTLINES OF CHORDATE DEVELOPMENT

the yolk through the germ wall. Thus the endoderm is in-
voluted from only a limited extent of the margin of the blas-
todisc. The region where ectoderm and endoderm become con-
tinuous is the rim of the blastopore; therefore we may say that

m.n.

FIG. 96. — Diagrams illustrating the idea of confluence (concrescence) as
applied to the chick. From Lillie (Development of the Chick). The central
area bounded by the broken line represents the area pellucida; external to this
is the area opaca, showing the germ wall (G.W.), zone of junction (Z.J.), and
margin of overgrowth (M.O). m.n., Marginal notch.

the rim of the blastopore here is a short crescent at the pos-
terior side of the blastula. The blastoporal opening is conse-
quently represented by a space, really only virtual, between
this and the contiguous periblast and yolk. Closure of this

THE EARLY DEVELOPMENT OF THE CHICK 259

vestigial blastopore occurs after the growth of the blastoderm
begins, so that when the lips of the blastopore approach and
fuse, in the typical manner of confluence, the region of their
fusion is limited to the posterior region of the blastopore
(Fig. 96). We recognize the primitive streak, therefore, as
the fused halves of the blastoporal margin; the primitive
groove is consequently to be interpreted as a vestige of the
blastopore itself. Later in development we know that the
anus develops at the posterior end of the remains of the
primitive streak, while from the beginning the primitive pit,
at its anterior end, represents the vestige of the neurenteric
canal, as described for Amphioxus and the frog.

The so-called head process thus represents, theoretically,
the earliest portion of the true embryo to be differentiated out
of the primitive streak. As a matter of fact, however, it is
difficult to observe a true genetic relation between the primitive
streak and the earliest portion of the head process, which
seems to form precociously. This theoretical distinction is
also the basis for the further distinction between gastral and
peristomial mesoderm in the chick. Really such a distinction
is not evident here, but it is sometimes useful to regard as
gastral, that mesoderm originating in the primary head proc-
ess, and as peristomial, that arising more posteriorly from the
primitive streak proper. Ultimately, of course, the " peristo-
mial" mesoderm becomes "gastral" in its relations to other
structures.

The fact that the whole process of gastrulation is itself ves-
tigial, to a certain extent, offers an interpretation of the hide-
pendent formation of the medullary plate, which occurs
unusually early, and of the mesoderm, which does not appear
until the primitive streak is largely established. This latter
fact, together with the development of the mesoderm from
cells of ectodermal character, are probably both related to the
marked restriction of the endoderm; this is reduced both in
extent and in importance, for most of the early functions of the
endoderm are here , in correlation with the extreme amount of
yolk, taken over by the periblast and the cells of the germ wall.

260 OUTLINES OF CHORDATE DEVELOPMENT

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III. THE EARLY DEVELOPMENT
OF THE EMBRYO

1. The Head-fold

In the stage we have just been des-
cribing, only the posterior limit of the
embryo is definitely marked; else-
where embryonic and extra-embry-
onic regions are directly continuous,
and no boundaries are indicated.
This remains the condition of affairs
for a long time in the lateral directions,
but anteriorly the limit of the embryo
becomes sharply marked out very
early. This is accomplished about the
twenty-second hour after fertilization,
by the formation of what is called the
head-fold, a transverse, crescentic fold
of both ectoderm and endoderm, ex-
tending nearly across the area pellu-
cida, a short distance in advance of
the head process (Fig. 97). At first a
shallow depression, bordered posteri-
orly by an elevation of the blastoderm,
this soon becomes a deep groove, as if
the blastoderm were being tucked in
under the anterior end of the med-
ullary plate. In longitudinal section
through the medullary plate and head
fold, the anterior part of the blasto-
derm has the appearance of a letter S
(Fig. 98). This folding is really due
chiefly, or wholly, to the rapid for-
ward growth of the medullary plate,
which carries with it the underlying
endoderm. Thus two cavities are
marked out; one occupies the dorsal
limb of the fold, is lined with endoderm,

THE EARLY DEVELOPMENT OF THE CHICK 261

and is an extension of the archenteric space between endoderm
and yolk; the other occupies the ventral limb, is lined with ecto-
derm, and is continuous with the space entirely outside the
embryo. The dorsal, endodermally lined cavity is the rudiment
of the fore-gut. The lower space is sometimes called the cavity
of the head-fold; it is merely an external space lying under the
head of the embryo. The boundary between embryonic and

® Q°> • ®

H.F.

or.pl

FIG. 98. — Median sagittal section through the head end of an embryo with
four pairs of somites (twenty-three to twenty-four hours). From Lillie (Devel-
opment of the Chick), a.i.p., Anterior intestinal portal; Ect. ectoderm; Ent.,
endoderm; F.G., fore-gut; H.F., head-fold; med. pi., anterior limit of medullary
plate; Mes., mesoderm; Mes. H.G., mesodermal head cavity; n. F., neural fold;
or. pi., oral plate (oral membrane).

extra-embryonic structures is just along the middle, i.e., most
posterior limit, of this latter fold or cavity; at this level the
morphologically anterior limit of the medullary plate passes
abruptly into the extra-embryonic ectoderm of the blastoderm,
in the region of the proamnion.

Laterally the head-fold and fore-gut narrow and finally dis-
appear into the flat blastoderm. The posterior curvatures of
the lateral extremities of the head-fold mark the lateral sur-

262 OUTLINES OF CHORDATE DEVELOPMENT

faces of the head, but otherwise the lateral limits of the embryo
proper are not definitely marked until twenty-two to twenty-
eight hours later, i.e.j forty-two to fifty hours after fertilization.
We may proceed, therefore, to describe the development of the
essential structures of the embryo, during the period from the
formation of the head-fold up to the time when the embryo
begins to be completely marked off from the extra-embryonic

FIG. 99. — Median sagittal section through the head end of a chick with eighteen
pairs of somites (about forty hours). From Lillie (Development of the Chick).
a.i.p., Anterior intestinal portal; Ao., dorsal aorta; Au., auricle; E.E.B.C.,
exocoelom (extra-embryonic body cavity); F.B., fore-brain; H.B., hind-brain;
H.F.Am., head-fold of amnion; Inf., infundibulum; Isth., isthmus; M.B., mid-
brain; N'ch., notochord; or.pl., oral plate (oral membrane); P.O., pericardial
cavity; Ph., pharynx; Pr'a., proamnion; pr'o.g., preoral gut; Rec.opt., optic
recess; S.V., sinus venosus; Tr.A., truncus arteriosus; Ven., ventricle.

region of the blastoderm. We shall describe the history of the
mesoderm first, not only because this seems the easiest method
of approach, but because the differentiations within the meso-
derm afford valuable landmarks in describing other structures.
Thus the age of the chick embryo is usually indicated by
reference to the number of pairs of mesodermal somites formed.

2. Mesoderm

While the head-fold is becoming well established (Fig. 100),
the mesoderm is in the form of a pair of sheets extending from
the sides of the primitive streak (peristomial) and head process
(gastral), across the whole extent of the area pellucida to the

THE EARLY DEVELOPMENT OF THE CHICK 263

germ wall, where it is continuous with the vascular area. The
inner or axial border of each sheet is considerably thickened, and
often distinguished as the vertebral plate, the remaining distal
portion being known as the lateral plate. The mesoderm also

FIG. 100. — Chick embryo of about twenty hours, showing first intersomitic
furrow. Dorsal view. From Lillie (Development of the Chick), a.c.v., Amnio-
cardiac vesicle; a.o., inner margin of area opaca; Ect., ectoderm; Ent. endoderm,
H.F., head-fold; i.a./.l., first intersomitic furrow; med.pl, medullary plate; Mes.,
mesoderm; n.gr., neural groove; Pr'a., proamnion; pr.gr., primitive groove.

extends posteriorly from the primitive streak, but at this time
there is none in the anterior part of the blastoderm in front of
the head process and head-fold (proamnion), although around
the margin of the pellucid area it is carried forward as a pair of
wing-like extensions, so that in surface view its anterior limit is
markedly concave (Fig. 93, D).

264 OUTLINES OF CHORDATE DEVELOPMENT

8!

In the vicinity of the head process (Fig. 101), the vertebral
plates at this stage rapidly lose their definite character and the
cells scatter throughout the region, combining with the cells
continually being budded off from the walls
of the fore-gut, to form the general mesen-
chyme of the head region. Later scattered
cells are added to the mesenchyme directly
from the ectoderm of the head region. The
history of the mesoderm farther back, just
in front of the end of the primitive streak,
is much the same as in the body region
proper, although all of the embryo thus
far developed out of the primitive streak
shares in the formation of the head only.
Here the vertebral plate thickens still more

I § and its cells become rearranged so as to
5 ^ form a short transverse break in the con-
Jg tinuity of the plate (Fig. 100). On each
i | side the cells immediately in front of this
3 | become grouped in a definite mass and
*> g form the first pair of mesodermal somites,
3 % continuous anteriorly with the forward ex-
3^ tensions of the vertebral plates (Figs. 100,
% *. 104). This rearrangement of cells con-
a ~ tinues posteriorly, and soon a second split

I 1 appears on each side, a short distance be-
c | hind the first, cutting out a definite block
i^. of the cells of the vertebral plate. This

is the second pair of somites. Additional
2 1 ^ pairs of somites are blocked out in regular
I ^ J fashion, as the embryonic region grows at
IJj I the expense of the primitive streak. The
5 ,2 formation of somites is not actually com-
pleted until about the fifth day of develop-
ment, by which time about fifty-two pairs
have been formed. The first somites formed remain the most
anterior in position. The first four pairs are ultimately in-

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03 fl

THE EARLY DEVELOPMENT OF THE CHICK 265

eluded in the hinder part of the head region of the embryo, and
although no other definite boundary of the head appears for
some time, its future limit may be marked by the position of
the fourth somites.

This division of the vertebral plate into somites expresses the
primary segmentation or metamerism of the body, and is funda-
mental, the metameric arrangement of other organs being
secondary and dependent upon this. Sections through the
somites (Fig. 102) show that their superficial cells are arranged

my

cr

so

FIG. 102. — Transverse section through the last somite of a chick of about
forty-eight hours (twenty-nine pairs of somites). After Lillie. a, Lateral dorsal
aorta; c, crelom; cr, neural crest; my, myotome; n, notochord; nc, nerve cord;
ne, nephrotome; so, somatic mesoderm; sp, splanchnic mesoderm; W, Wolffian
duct.

in the form of an epithelium, while the cells of the central parts
are loosely and irregularly arranged. This central portion,
although only virtually a cavity, is termed the myocoel; it cor-
responds, theoretically, with the region of the enterocoel of
other forms.

The more lateral portions of the mesoderm, the lateral plates,
remain unsegmented. They are connected with the somites by
an intermediate, transitional band, also unsegmented in the
chick, known as the nephrotome or intermediate cell mass.
The dorsal and ventral surfaces of the nephrotome are con-
tinuous with the corresponding surfaces of the somites, the
separation between the two bodies being indicated by a de-
pression resulting chiefly from the thickening of the somites.

266 OUTLINES OF CHORDATE DEVELOPMENT

The intermediate cell mass in part forms the rudiment of the
excretory system, and in part contributes to the formation of
mesenchyme: its history will be described in connection with
the later stages of development.

The lateral plate very early becomes separated into two dis-
tinct sheets by the development of a wide cavity within it.
This cavity is the coelom, which is here, as in the frog, to be
described as a schizocoel. The outer or upper sheet of lateral

op. Vea

FIG. 103. — Ventral views of the head ends of chick embryos. From Lillie
(Development of the Chick). A. Embryo with five pairs of somites (about
twenty- three hours). B. Embryo with seven pairs of somites (about twenty-
five hours), a.c.v., Amnio-cardiac vesicle; a.i.p., anterior intestinal portal;
End'c.s., endocardial septum; F.G., fore-gut; Ht., heart; My'C., myocardium;
N'ch., notochord; N'ch.T., anterior tip of notochord; n.F., neural fold; op.Ves.,
optic vesicle; p.C., parietal cavity (ccelomic); Pr'a., proamnion; s.2, s.4, second
and fourth mesodermal somites; V.o.m., omphalo-mesenteric vein.

plate cells is the somatic mesoderm; this unites with the overly-
ing ectoderm to form the somatopleure (Figs. 102, 105, 108).
The inner or lower sheet is the splanchnic mesoderm; this
unites with the underlying endoderm to form the splanchno-
pleure. The somatic and splanchnic layers of mesoderm
remain united proximally, in the region of the intermediate

THE EARLY DEVELOPMENT OF THE CHICK 267

cell mass. The somatopleure, splanchnopleure and coelorn,
later become separated into embryonic and extra-embryonic
regions, but during these early stages they form continuous
structures extending laterally out to the germ wall, and ante-
riorly into the head region. From the embryonic portions of
these structures develop, respectively, the body wall, the gut
wall and vascular organs, and the pericardial, pleural, and
peritoneal cavities: their extra-embryonic portions give rise
to the embryonic membranes and appendages, and to the
extra-embryonic portions of the vascular system and ccelom
(exocoelom).

The history of the mesoderm and coelom in the region of the
head-fold deserves a special word. The coelom very early
enlarges, either side of the head region, forming a pair of large
spaces called the ammo-cardiac vesicles. These grow inward
toward the head-fold, and by the time this is well established
(4-6 pairs of somites) they push into the lower limb of the head-
fold, between its ectodermal and endodermal layers (Fig. 105).
Here they finally meet and fuse, forming a median coelomic
space bounded, of course, by a mesodermal wall. This is the
rudiment of the pericardial cavity, and its formation and subse-
quent enlargement, bring about a wide separation of the ecto-
derm and endoderm, or as we may now say, of the somato-
pleure and splanchnopleure, of the head-fold, the latter being
carried much the farther posteriorly (Figs. 98, 99). The later
development of this region and of the vascular system in
general, may more conveniently be postponed, until after an
account of the history of the ectodermal and endodermal layers
during these early stages.

3. Endoderm

We left • the embryonic endoderm as a thin sheet of cells
extending forward from the primitive streak, and we had de-
scribed the important events connected with the formation of
the fore-gut from its anterior margin (Figs. 97, 98). In the
region between the fore-gut and the primitive streak, i.e., in the

268 OUTLINES OF CHORDATE DEVELOPMENT

remainder of the embryonic region thus far formed, the endo-
derm and mesoderm are united in a secondary median fusion
continuous with the cells of the primitive knot. Very soon
the mesoderm and endoderm separate again and the median

a.o.

F.G.

-pr.gr.

FIG. 104. — Chick embryo with three pairs of somites (about twenty-three
hours). Dorsal view. From Lillie (Development of the Chick), a.c.v., Amnio-
cardiac vesicle; a.o., inner margin of area opaca; F. G., fore-gut; N'ch., notochord;
n.F., neural fold; pr.gr., primitive groove; s.l, s.2, s.3, first, second and third
somites.

cells, then associated with the mesoderm, become arranged as
a small longitudinal rod, the notochord (Fig. 102). Since the
germ layers are fused in the primitive knot, and redifferen-
tiate anteriorly out of it, it is of little consequence whether
the notochord is regarded as of mesodermal or endodermal
origin; it is more closely associated with cells which later are

THE EARLY DEVELOPMENT OF THE CHICK 269

clearly mesodermal. As the primitive streak shortens and the
primitive knot moves posteriorly, the notochord continues to
differentiate, and so to elongate posteriorly.

The cavity of the fore-gut is the rudiment of the pharynx.
It remains a wide but shallow cavity throughout these early
stages, open posteriorly, by way of the anterior intestinal portal,
upon the surface of the yolk, where the endoderm remains
spread out as a thin flat sheet (Figs. 97, 98, 103). Near the
anterior extremity of the head-fold, the endoderm lining the
pharynx comes ventrally into contact with the ectoderm, and
later fuses with it. This forms the oral plate, which becomes the
inner wall of the stomodceum; it is perforated early the third
day of incubation. There is a pair of lateral extensions of the
fore-gut, where its walls come into contact with the ectoderm,
marking the positions of the future first gill pouches.

4. Nervous System

The rudiments of the central nervous system are the most
conspicuous structures of the chick embryo during its early
development. We have already noted the formation of the
medullary plate, a broad ectodermal thickening developing
precociously, before any other part of the embryo is definitely
established (Figs. 94, 101). The medullary plate is converted
into the medullary tube in the usual manner. A medullary
groove appears soon after the head-fold becomes marked; the
marginal medullary folds then become elevated and grow
rapidly so that they form a pair of high conspicuous ridges
on the surface of the anterior part of the blastoderm. They
extend posteriorly, gradually diminishing in height, until
finally they sink into the general level of the blastoderm in the
region of the primitive knot. The formation of the medullary
folds and central nervous system in general, as of the somites,
notochord, and other parts of the embryo, is progressive pos-
teriorly, so that steps in the formation of all these parts can be
read in any series of transverse sections extending from the
primitive knot anteriorly.

270 OUTLINES OF CHORDATE DEVELOPMENT

The elevated medullary folds, or neural folds, soon bend
over toward one another and first meet a short distance back
from the anterior limit of the head; this is known to be the
region of the future mid-brain (Fig. 105). Here the folds soon
fuse together forming a superficially continuous sheet of ecto-
derm, and an underlying medullary or neural tube. From this
point the fusion extends very rapidly posteriorly, very slowly
anteriorly. The point where the final closure occurs anteriorly,
and consequently the final separation from the superficial ecto-
derm, is known as the neuropore; it is the region later distin-
guished as the lamina terminalis, and is regarded as the mor-
phologically anterior limit of the brain. Topographically,
however, this is not the most anterior part of the central nerv-
ous system, for during these early stages the rudiment of the
brain grows forward and downward, in front of the fore-gut,
so that its anterior end becomes bent like a crook. Its floor
remains closely applied to the roof of the fore-gut, its extension
being due to the growth of the anterior and dorsal regions
chiefly (Fig. 99). Thus the morphologically anterior end of the
brain really comes to lie on its antero-ventral aspect.

Certain details in connection with the neural folds and their
closure deserve special mention. The actual crests of the
neural ridges are flattened, and when the ridges fold together
these flattened surfaces form a broad vertical contact. The
neural tube is formed by the fusion of the lower or inner
margins of these surfaces; the upper margins fuse across the
mid-line, restoring a continuous superficial ectoderm. The
cells left between the upper and lower margins, derived approxi-
mately from the very apices of the neural ridges, are thus left
between the neural tube and the surface ectoderm; these are
the neural crests (Fig. 102). They do not fuse across the mid-
line, but remain as a pair of longitudinal bands along the dorso-
lateral surfaces of the neural tube. The neural crests are the
rudiments of the ganglia of the cranial and spinal nerves; they
are not uniformly developed throughout their extent and may
be better marked in some sections than in others.

The anterior portion of the neural tube expands very con-

THE EARLY DEVELOPMENT OF THE CHICK 271

siderably. Its most anterior region expands transversely, the
lateral extensions thus formed representing the rudiments of
the optic vesicles (Figs. 106, 107). This is obviously, therefore,
the region of the primary fore-brain or prosencephalon, which
now includes the entire anterior portion of the nerve tube. Its
posterior limit is marked by a slight constriction just back of
the optic vesicle rudiments. A little later (9-10 pairs of so-
mites) another constriction appears marking the posterior limit
of the mid-brain or mesencephalon. The third section of the
brain, the hind-brain or rhombencephalon is much the longest
section of the brain (Fig. 107). It is marked by a series of
irregular constrictions, ultimately five in number forming six
segments, or neuromeres, in this region. No posterior limit of
the hind-brain can be made out in these early stages, but from
later development it is known that all in front of the fourth
mesodermal somites really belongs to the head, and conse-
quently this level may be taken to mark approximately the
posterior limit of the brain. The hind-brain narrows poste-
riorly and the remainder of the neural tube is the rudiment of
the spinal cord, which remains narrowed and approximately
uniform in diameter.

5. Vascular System

We may now return to a description of the formation and
development of the embryonic vascular system, postponed
from an earlier page. The formation of the vascular rudiments
in the area opaca continues, hi the manner already described
(Fig. 95), and when the extra-embryonic ccelom forms, dividing
the mesoderm into somatic and splanchnic layers, the blood-
vessels remain associated with the latter, i.e., with the splanch-
nopleure (Fig. 105, A). The vessels of the pellucid area
develop first from its margin, near the area opaca, and gradually
extend toward the embryo. • They first appear shortly after
the head-fold, just as the somites begin to be cut out. The
formation of the conspicuous blood islands does not occur in
the pellucid portion of the blastoderm; only the tubular vessels

272 OUTLINES OF CHORD ATE DEVELOPMENT

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THE EARLY DEVELOPMENT OF THE CHICK 273

develop here. Thus the cellular or corpuscular elements of
the early vascular system arise only in the area opaca, and
most extensively in its posterior region. Following Riickert,
we may say that the vessels of the pellucid area are formed by
the rearrangement of small groups of cells in the splanchnic
mesoderm of the area. These first form short sections of tubu-
lar vessels which very soon connect with the more peripheral
vessels of the opaque area. In this way a continuous vascular
network develops centripetally, finally reaching the embryo
about the time six pairs of somites are formed.

Soon after this, vessels appear in the embryo itself. The
first of these are the paired dorsal aortce of the body region
(Fig. 105). These are to be regarded as enlarged and straight-
ened inner (axial) margins of the vascular network of the pellu-
cid area. Posteriorly they diverge widely, passing as the
vitelline arteries, into the general vascular net (Fig. 107).
Anteriorly they become prolonged forward toward the head
region, where they connect with a pair of vessels differentiated
within the mesenchyme of the head.

The heart is clearly a specialized portion of the system of
vessels. Like the dorsal aortae, the rudiment of the heart is
paired. When the vessels grow into the head region, which is
now elevated above the level of the general splanchopleure,
they are related to the ventral, rather than to the dorsal region
(Fig. 105). The amnio-cardiac vesicles (see above) become
vascularized in the same manner as the rest of the pellucid
area, and a pair of ventral aortce is formed beneath the fore-gut
(Fig. 103). Posteriorly to the opening of the fore-gut (anterior
intestinal portal) these vessels diverge and pass into the vascu-
lar net as the rudiments of the vitelline veins. Reference to
the transverse section illustrated in Fig. 105, A, shows that
beneath the fore-gut the mesoderm has a considerable vertical
extent. This is commonly regarded as splanchnic mesoderm,
although it is a region where somatic and splanchnic layers
become continuous. The paired rudiments of the heart pass
along the inner or axial surface of this vertically extended
mesoderm, and thus come into close relation, shortly fusing

274 OUTLINES OF CHORDATE DEVELOPMENT

tfcfi.

•pr.str.

FIG. 106. — Chick embryo with seven pairs
of somites (about twenty-five hours). Dor-
sal view. From Lillie (Development of the
Chick), o.c.s., Anterior cerebral suture; ceph.
Mes., cephalic mesoderm; F.G., fore-gut; N'ch.,
notochord; n. T., neural tube; op.Ves., optic
vesicle; Pr'a., proamnion; pr. str., primitive
streak; s. 2, s. 7, pecond and seventh somites;
V.o.m.j omphalomesenteric vein.

together to form a me-
dian, thin-walled tube.
This becomes the endo-
thelial lining of the heart;
the muscular wall of the
heart is formed by the
addition of an external
layer of mesoderm; for
the splanchnic mesoderm
of each side forms a fold
around the endothelial
rudiment (Fig. 105, B).
These folds then ap-
proach and fuse across
the mid-line, both above
and below the endothe-
lial tube. For a brief
period after their fusion
they remain in the mid-
line forming a dorsal meso-
cardium, connecting the
heart with the tissues just
beneath the fore-gut, and
a ventral mesocardium,
extending from the heart
to the splanchnopleure.
The ventral mesocar-
dium breaks away almost
immediately after its for-
mation, while the dorsal
mesocardium remains for
a time, but then disap-
pears, except at the an-
terior and posterior ex-
tremities of the heart.
The heart is then left as
a short median tube con-

THE EARLY DEVELOPMENT OF THE CHICK 275

sisting of endothelial and rudimentary muscular layers, freely
suspended in a cavity which is the beginning of the pericardial
cavity. Anteriorly it is continuous with a short pair of vessels
extending into the head-fold; these are the ventral aortse men-
tioned above. Posteriorly the heart is directly continuous with
the vitelline veins.

The dorsal aortse have meanwhile extended forward into the
head, connecting with their cephalic sections which have
developed directly within the mesenchyme of the region.
These now unite with the ventral aortaa (Fig. 107, B) around the
sides of the anterior end of the fore-gut; these connections are
the rudiments of the first, or mandibular aortic arches. Thus
the embryonic circulatory system is established and connected
with the extra-embryonic vessels.

IV. THE EMBRYO OF ABOUT THIRTY HOURS (10-12
PAIRS OF SOMITES)

We may summarize, now, the events of this early period of
development by mentioning the structures of the chick embryo
at about its thirtieth hour of incubation, when it includes ten to
twelve pairs of mesodermal somites (Figs. 107, 108).

In the freshly opened egg of this age, the circular blastoderm
is seen to have extended approximately one-fourth of the way
around the vitellus (i.e., its diameter is roughly 25 mm.). The
embryo appears as a definite whitish streak, approximately 4
mm. in length, enlarged anteriorly, and posteriorly fading
gradually into the surrounding area. Thus by far the greater
part of the blastoderm is extra-embryonic. Three definite areas
may be distinguished in the extra-embryonic blastoderm (Fig.
108). (1) Immediately surrounding the embryo is the clear
area pellucida, now greatly restricted and not very distinct,
save in the head region which includes the proamnion. The
area opaca is now clearly divided into (2) the area vasculosa
and (3) the area vitellina. The vascular area, save for a slight
interruption anteriorly, has grown entirely around the embryo.
It has extended both peripherally, over the yolk, andce ntrally

276 OUTLINES OF CHORDATE DEVELOPMENT

B

"pr. sfa

FIG. 107. — Chick embryo with twelve pairs of somites (about thirty-three
hours). From Lillie (Development of the Chick). A. Dorsal view of entire
embryo. B. Ventral view of anterior end. A.C.S., Anterior cerebral suture;
a.i.p., anterior intestinal portal; Ao., dorsal aorta; F.G., fore-gut; H.B., hind-
brain; Ht., heart; M.B., mid-brain; op. Ves., optic vesicle; or.pl. , oral plate;
pr.str., primitive streak; s.2, s.12, second and twelfth somites; v.ao., ventral aorta;
V.o.m., omphalo-mesenteric vein.

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I s § g

11*1

THE EARLY DEVELOPMENT OF THE CHICK 277

encroaching upon the pellucid area. The broad area vitellina

is further separable into two regions,

an inner band, the vitellina in- \M I 'B § s §

Jr*.'!-* «\ ^ ^ M

terna, and a narrow area vitellina
externa.

The examination of sections
through the blastoderm shows that
the areas pellucida and vasculosa are
composed of the three germ layers,
the area vitellina of ectoderm and
endoderm only. Except in the re-
gion about the head of the embryo,
the area pellucida is extensively
vascularized, but the vessels are still
comparatively free from corpuscles.
The pellucid and opaque areas are
further characterized by the pres-
ence of extraembryonic coelom be-
tween the two sheets of mesoderm
(Fig. 108). The vascular area is
definitely limited peripherally by the
sinus terminalis. The area vitellina
externa is the region where the ex-
tension of the blastoderm is actually
being carried forward. Here are
found conditions similar to those de-
scribed in the early part of this
chapter. The extreme margin
("margin of overgrowth " — Lillie) is
formed by a single layer of super-
ficial cells called "ectoderm," while
between this margin and the area
vitellina interna is a band (" zone of
junction" — Lillie) which is the
equivalent of the marginal periblast,
where the processes of true blasto-
derm formation are chiefly localized,

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278 OUTLINES OF CHORDATE DEVELOPMENT

and where the extra-embryonic portions of the two primary
germ layers are being differentiated.

In enumerating the structures of the embryo itself (Fig. 107)
we may begin posteriorly and pass forward, since, read in this
direction, a series of transverse sections through a single embryo
roughly represents the steps in the development of most of the
parts fully formed at this time. Posteriorly there is a short
primitive streak region with thickened neural plate and primi-
tive groove. Passing anteriorly the neural folds rise and meet
forming the neural tube; the notochord becomes distinguishable,
and the mesoderm is differentiated into vertebral and lateral
plates connected by the intermediate cell mass; the lateral plate
is separated into somatic and splanchnic layers by the extra-
embryonic ccelom. In the trunk and hinder part of the head
ten to twelve pairs of mesodermal somites are formed.

The long head region extends forward from about the fourth
pair of somites (counting from the anterior end of the series).
The head is now almost completely separated from the yolk
ventrally, by the endodermal head-fold, while the ectodermal
head-fold, which also separates the lateral surfaces of the head
from the yolk and blastoderm, has more than half this extent.
The brain is the most prominent feature of the embryo, and its
primary divisions, fore-, mid-, and hind-brain, are well marked.
Neural crests are distinct in sections from the mid-brain poste-
riorly. The fore-gut, widely open posteriorly upon the yolk by
way of the anterior intestinal portal, is the only strictly endo-
dermal structure thus far differentiated. This is the pharyngeal
region, and the rudiments of the first or hyomandibular pair of
gill pouches are indicated laterally, while in its floor is the oral
plate.

The large vitelline veins unite in front of the level of the first
somites, forming the heart, which now has both endothelial and
muscular layers. The elongated heart lies in the pericardial
cavity and is bent to the right. Anteriorly it continues into
the diverging ventral aorta), which pass around the sides of the
head, dorsally, as the first or mandibular pair of aortic arches;
these are continuous with the wide lateral dorsal aorta? which

THE EARLY DEVELOPMENT OF THE CHICK 279

pass backward and become continuous posteriorly with the
extra-embryonic vascular network.

From this point onward we shall not attempt to continue
a description of the development of the embryo as a whole.
Next we shall outline the processes leading to the more complete
formation of the embryo, and to its well-marked separation
from the yolk and blastoderm on every side. Then, after a
consideration of the formation of the embryonic membranes
and appendages, we shall give, in the next chapter, a brief re-
sume of the more essential steps in the organogeny of the later
embryo. (Throughout this chapter, and more especially this
part of it, the student is referred for additional details to such
an account as Lillie's "Development of the Chick," and to the
literature there cited).

V. THE SEPARATION OF THE EMBRYO FROM THE
EXTRA-EMBRYONIC STRUCTURES

The remaining primitive streak region loses its typical
structure soon after the fortieth hour of incubation (about
18 pairs of somites) (Fig. 112), and thereafter it remains, as a
locus of continued cell proliferation known as the tail bud (Fig.
109, A). Shortly after this, about the forty-sixth hour (about
26 pairs of somites) a definite infolding of the blastoderm occurs
posteriorly, marking the hinder limit of the embryo. This fold
is the tail-fold, in many respects the counterpart of the head-
fold although appearing so much later. This fold, in which all
three of the germ layers are involved (Fig. 109, J5), slowly grows
forward forming a hind-gut, comparable with, though much
less extensive than, the fore-gut. The tail bud, thus separated
from the yolk beneath, continues to elongate slowly for a con-
siderable time. Mesodermal somites continue to be added pos-
teriorly, through the trunk region, which extends as far as the
thirty-fifth somite, formed about the seventieth hour, and finally
through the incurved tail region (Fig. 109, B). A total of
fifty-two pairs of somites have been counted, although some

280 OUTLINES OF CHORDATE DEVELOPMENT

X-

on.t.

Am.cev. Ect.

FIG. 109. — Sagittal sections through the posterior ends of chick embryos.
From Lillie (Development of the Chick). A. Median section through an embryo
with about twenty-one pairs of somites (about forty-four hours). B. Lateral
section through embryo with about thirty-five pairs of somites (about seventy-
two hours). All., allantois; Am., amnion; Am. cav., amnionic cavity; An. pi.,
anal plate; An. t., anal tube; Ao., dorsal aorta; Bl. v., blood-vessels in wall of
allantois; c.C., central canal of spinal cord; CL, cloaca; Ect., ectoderm; Ectam.,
ectoderm of amnion; E.E.B.C., exoccelom; Ent. endoderm; Mes., mesoderm;
Mesam., mesoderm of amnion; N'ch., notochord; n.T., nerve cord; p'a.G., post-
anal gut; p.i.p., posterior intestinal portal; s.A., segmental arteries, between the
somites; So'pl., somatopleure; Spl'pL, Sp'pl., splanchnopleure; T.B., tail bud;
t.f.So'pl., tail-fold in somatopleure; t f.Sp'pL, tail-fold in splanchnopleure.

THE EARLY DEVELOPMENT OF THE CHICK 281

ten of these disappear again during the eighth day of embryonic
life, leaving a total of forty-two pairs.

The formation of the tail-fold is but one phase in the general
process of the separation of the embryo from the remainder of
the blastoderm, and at the same time from the yolk. The for-
mation of the head-fold we have already described. We may
recall that this extended backward along each side of the head.
Posteriorly this now becomes continued either side of the trunk,
by a somewhat similar lateral fold, which finally reaches to the

la

ebc

vv

FIG. 110. — Diagrammatic transverse section through the region where the
gut is open out over the yolk (yolk-stalk umbilicus), in a chick of about forty-
eight hours (about twenty-eight pairs of somites). After Duval. a, Dorsal
aorta; c, ccelom; ebc, exocoelom; ig, intestinal groove; la, lateral folds of amnion;
vv, vitelline vein.

tail-fold. These folds involve both somatopleure and splanch-
nopleure (Fig. 110). The lateral folds gradually extend inward
toward the mid-line beneath the embryo, converting the flat
sheet of endoderm into a median fold above the yolk; this is
the intestinal groove, the rudiment of the true intestine (Fig.
110). The head- and tail-folds continue to extend posteriorly
and anteriorly, respectively, increasing the extent of the fore-
and hind-gut. These connect with the intestinal groove by
the anterior and posterior intestinal portals.

Gradually these folds all approach beneath the embryo, cut-
ting it off from the yolk, and marking a clear distinction
between embryonic and extra-embryonic regions. Finally,
about the fifth day, the lateral folds of the splanchnopleure fuse
together extensively, and the gut is entirely closed off except
in a restricted region in the hinder part of the trunk (Fig. 115).

282 OUTLINES OF CHORDATE DEVELOPMENT

This remains open to the yolk nearly throughout embryonic
life. The walls of this open portion of the gut elongate into
a tubular stalk known as the yolk stalk. In reality this is
double, composed of an outer wall of somatopleure, and an
inner tube of splanchnopleure; the former is sometimes known
as the somatic stalk, the latter as the splanchnic stalk or yolk
stalk proper. The splanchnic stalk is the pathway by which

FIG. 111. — Ventral view of the anterior end of a chick embryo with sixteen
pairs of somites (about thirty-eight hours). From Lillie (Development of the
Chick), a.i.p., Anterior intestinal portal; au.P., auditory pit; B.a., bulbus
arteriosus; F.B., fore-brain; Inf., infundibulum; op.Ves., optic vesicle; Or.pl.,
oral plate; Pr'am., proamnion; s.4, fourth somite; Tr.a., truncus arteriosus;
v.Ao., ventral aorta; Ven., ventricle; V.o.m., omphalo-mesenteric (vitelline)
vein; VII— VIII, acustico-facialis ganglion.

the blood-vessels pass between embryonic and extra-embryonic
structures. The narrow space between the two stalks is, of
course, ccelomic, connecting embryonic or true coelom, and
extra-embryonic coelom or exocoelom.

The inner limbs of the lateral folds of the somatopleure form
the body watt of the embryo, of which we may now describe
lateral and ventral surfaces, as well as the dorsal, which has
hitherto been the only free surface of the embryo, save in the
head and tail.

VI. THE ESTABLISHMENT OF THE EXTERNAL FORM
OF THE EMBRYO

Rapid growth and extensive changes in the external form of
the embryo have been proceeding, as the embryo has been

THE EARLY DEVELOPMENT OF THE CHICK

cf m

283

frstr

FIG. 112. FIG. 113.

FIG. 112. — Chick embryo with twenty pairs of somites (about forty-three
hours). Dorsal view. From Lillie (Development of the Chick). A.o.m.,
Vitelline artery; au.P., auditory pit; Cr.FL, cranial flexure; D.C., ductus Cuvieri;
Dienc., diencephalon; Mesenc., mesencephalon; Metenc., metencephalon; Myelenc.
1, and 2, anterior and posterior divisions of the myelencephalon; Op.Ves., optic
vesicle. Ph., pharynx; pr.str., primitive streak; s.2, s.5, etc., second, fifth, etc.,
somites; Telenc., telencephalon; Vel.tr., velum transversum; Ven., ventricle.

FIG. 113. — Chick embryo with twenty-seven pairs of somites (about forty-
eight hours). Viewed from above. After Lillie. a, Auricle; am, posterior
margin of amnionic folds; c, carotid loop; cf, cranial flexure; d, diencephalon;
dC, ductus Cuvieri; g\, g2, gs, first, second and third gill clefts; i, isthmus;
I, lens; ma, mandibular arch; ms, mesencephalon; mt, metencephalon; o, otocyst
(auditory sac); just to the right of the otocyst is a thickening representing the
ganglion of the VII and VIII cranial nerves; r, retinal layer; S2, sw, $20, second,
tenth, and twentieth somites; t, tail-bud; v, ventricle; va, vitelline artery; vv,
vitelline vein; 1, 2, 3, first, second and third aortic arches; V, ganglion of V
cranial nerve.

284 OUTLINES OF CHORDATE DEVELOPMENT

. folded off from the yolk and blastoderm. The embryo of
thirty hours was nearly straight and lay flat upon the yolk,
save that a simple flexure of the head was caused by the growth
of the fore-brain downward in front of the fore-gut. Continued
enlargement of the head (brain) leads to two important general
modifications of the form of the embryo, first, a twisting of the
embryonic body, and second, the formation of certain bendingg
or flexures in the axis of the head and trunk. As the cavities
of the brain enlarge, a sharp bending of the neural axis appears
between the fore- and mid-brain, soon involving the entire
mid-brain. The development of this cranial flexure (Fig. 112),
combined with the extensive enlargement of the fore-brain,
would force this region down into the yolk but for the fact that
the head now falls over upon one side, its left, which now comes
to lie over upon the yolk. The trunk retains for a time its
original position flat upon the yolk, and thus a twist appears
just back of the head. This change in the position of the head
begins about the thirty-sixth hour (15 pairs of somites), the
cranial flexure having appeared somewhat earlier, about the
thirtieth hour (10-12 pairs of somites). Gradually the region
of the twist moves posteriorly, leaving the more anterior parts
thrown over (Figs. 113, 114), and finally, about the close of
the fourth day, the entire embryo comes to lie upon its left side.
Long before this, about the end of the second day, another
flexure of the longitudinal axis appears; this is the cervical
flexure. A broad ventral sweep through the entire hind-brain
region, extending a short distance into the neck, results in the
more complete flexure of the fore-brain, which thus comes to
be directed posteriorly rather than ventrally, its true ventral
surface approximating the ventral surface of the pharyngeal
region. Later the entire trunk becomes arched dorsally,
bringing the head and tail fairly close together on the ventral
side (the morphologically ventral side now lies turned toward
what was the right side, previous to the torsion of the embryo).
During the later phases of embryonic development these last
flexures disappear to a considerable extent, leaving permanently
well-marked only the original cranial flexure.

THE EARLY DEVELOPMENT OF THE CHICK 285

ms-m

cewf/.

erf/

FIG. 114. — Chick embryo with adjacent portion of area vasculosa, with thirty-
five pairs of somites (about seventy- two hours). Dorsal view. From Lillie
(Development of the Chick), a. a., 1, 2, 3, 4, First to fourth aortic arches; Am.,
amnion; AT., branches of vitelline arteries; Atr., auricle; A.V., vitelline artery;
B.A., bulbus arteriosus; cere. Fl., cervical flexure; cr. FL, cranial flexure; D.C.,
ductus Cuvieri; D.V., ductus venosus; Ep., epiphysis; Gn. V., ganglion of V
cranial nerve; Isth., isthmus; Jug., external jugular vein; Md., mandibular arch;
M.M., maxillo-mandibular branch of V cranial nerve; Myel., myelencephalon;
olf.P., olfactory pit; Ophth. ophthalmic branch of V cranial nerve; Ot., otocyst;
8.2, s.10, s.20, etc., second, tenth, twentieth, etc., somites; V., branches of the
vitelline veins; V.c.p., posterior cardinal vein; V.umb., umbilical vein; V.V.,
vitelline vein; V.V.p., posterior vitelline vein; W.B., wing-bud.

286 OUTLINES OF CHORD ATE DEVELOPMENT

The general changes in form and the development of the
externally visible organs may best be appreciated by studying
such a series of embryos as that illustrated by Duval (Atlas
d'embryologie, Paris, 1889; Plates VII-X). We may merely
call attention to a few of the more striking features. The fore-
and hind-limbs appear, at approximately the same time, about
the eightieth hour, as bud-like outgrowths from the body wall
(Fig, 114). These enlarge rapidly; their segments are distin-
guishable at the beginning of the seventh day, and during the
eighth day they assume the outlines of the wings and legs,
During the eighth day too, the heart is drawn within the body
wall, the visceral arches and gill clefts disappear, save as they
remain represented in the adult by the jaws (mandibular arch)
and the external auditory meatus (hyomandibular gill cleft),
and the abdominal viscera are much enlarged. The following
day the facial portion of the head begins to enlarge, the feather
papillae become well marked, and the general musculature begins
to develop to such an extent as to affect the general contours
of the body.

VII. THE EMBRYONIC MEMBRANES AND
APPENDAGES

We have now to describe the development of certain ex-
tremely important structures which are primarily extra-em-
bryonic, and have to do with the protection, nutrition, and
respiration of the embryo, rather than with the actual forma-
tion of proper organs. These structures are the yolk-sac, the
amnion, and the allantois; strictly speaking the allantois arises
as an embryonic structure, but it soon becomes extra-embryonic
in position, and its functional value is derived from its later
relation. These three structures are all characteristic of the
embryos of the higher Craniates — Reptiles, Birds, and Mam-
mals, and consequently these classes are often grouped to-
gether under the term Amniota.

1. The Yolk-sac

We have seen that at the thirtieth hour of incubation the
blastoderm has extended over approximately one- fourth the

THE EARLY DEVELOPMENT OF THE CHICK 287

surface of the yolk. Throughout its pellucid and vascular areas
it is divided by the exocoelom, into somatopleure and splanchno-
pleure (Fig. 108). Its outlying area vitellina for the most part

111

-Ect.
-Mas

FIGS. 115, 116, 117. — Diagrams of the relations of the embryonic membranes
in the chick. Figures and description from Lillie (Development of the Chick).
The ectoderm and endoderm are represented1 by plain lines; the mesoderm by
a cross-hatched line or band. The yolk-sac is represented by broken parallel
lines. In Fig. 115 the allantois is represented as a sac. In Figs. 116 and 117,
where it is supposed to be seen in section, its cavity is represented by unbroken
parallel lines. The stalk of the allantois is exaggerated in all the diagrams to
bring out its connection with the embryo.

FIG. 115. — Fourth day of incubation. The embryo is surrounded by the amnion
which arises from the somatic umbilicus in front and behind; the sero-amniotic
connection is represented above the tail of the embryo; it consists at this time
of a fusion of the ectoderm of the amnion and chorion. The allantois is repre-
sented as a sac, the stalk of which enters the umbilicus behind the yolk-stalk;
the allantois lies in the extra-embryonic body-cavity (exoccelom), and itsmeso-
dermal layer is fused with the corresponding layer of the chorion above the embryo.
The septa of the yolk-sac are represented at an early stage. The splitting of
the mesoderm has progressed beyond the equator of the yolk-sac, and the un-
divided portion is slightly thickened to form the beginning of the connective-
tissue ring that surrounds the yolk-sac umbilicus. The ectoderm and endoderm
meet in the zone of junction, beyond which the ectoderm is continued a short
distance. The vitelline membrane is ruptured, but still covers the yolk in the
neighborhood of the yolk-sac umbilicus. The albumen is not represented in
this figure. (For explanation of lettering see Fig. 117.)

consists of ectoderm and endoderm only, and is bounded per-
ipherally by a region where the further extension of the blasto-
derm is being effected. The extension of the blastoderm con-

288 OUTLINES OF CHORDATE DEVELOPMENT

tinues in the manner previously described, the differentiation
of the mesoderm and the subsequent formation of exoccelom,
somatopleure, and splanchnopleure, slowly proceeding centri-
f ugally . During the fifth day the blastoderm extends completely
over the yolk, save for a narrow circular space, opposite the
embryo, which remains uncovered until toward the close of

FIG. 116. — Ninth day of incubation. The yolk-sac umbilicus has become
much narrowed, it is surrounded by the mesodermal connective-tissue ring,
and by the free edges of the ectoderm and endoderm. The vitelline membrane
still covers the yolk-sac umbilicus and is folded into the albumen. The allantoia
has expanded around the amnion and yolk-sac and its outer wall is fused with the
chorion. It has pushed a fold of the chorion over the sero-amniotic connection,
into which the mesoderm has penetrated, and thus forms the upper fold of the
albumen-sac. The lower fold of the albumen-sac is likewise formed by a dupli-
cation of the chorion and allantois; it must be understood that lateral folds are
forming also, so that the albumen is being surrounded from all sides. The stalk
of the allantois is exaggerated so as to show the connection of the allantois
with the embryo; it is supposed to pass over the amnion, and not through the
cavity of the latter, of course. (For explanation of lettering see Fig. 117.)

embryonic life (Fig. 115). The mesoderm and associated
structures of the blastoderm push around more slowly, but
finally arrive at the blastodermal margin, which becomes a
narrow ring called the yollt-sac umbilicus. The yolk-sac itself
is the splanchnopleural portion of the extra-embryonic blasto-
derm, one surface applied directly to the surface of the yolk, the

THE EARLY DEVELOPMENT OF THE CHICK 289

other forming the inner lining of the exoccelom (Fig. 115). The
lower pole of the yolk-sac is open at the yolk-sac umbilicus, and
the upper pole is of course directly continuous with the yolk
stalk or splanchnic stalk, and therefore with the embryonic mid-
gut (Fig. 115). While the yolk-mass is now practically enclosed
in a layer of endoderm (splanchnopleure) it cannot be said to be

All.+Am.

AI/.G

FIG. 117. — Twelfth day of incubation. The conditions represented in Fig
116 are more advanced. The albumen-sac is closing; its connection with the
cavity of the amnion by way of the sero-amniotic connection will be obvious.
The inner wall of the allantois has fused extensively with the amnion. The um-
bilicus of the yolk-sac is much reduced, and some yolk protrudes into the albu-
men (sac of the yolk-sac umbilicus). Alb., albumen; Alb.S., albumen-sac;
AIL, allantois; All.I., inner wall of allantois; All.C., allantoic cavity; AILS.,
allantoic stalk; All. -\- Am., fusion of allantois and amnion; Am., amnion;
Am.C., amnionic cavity; Chor., chorion; C.T.R., connective-tissue ling; Ect.t
ectoderm; E.E.B.C., exoccelom (extra-embryonic body-cavity); EnL, endoderm;
Mes., mesoderm; S.-Am., sero-amnionic connection; S.Y.S.U., sac of the yolk-
sac umbilicus; Umb., umbilicus; V.M., vitelline membrane; Y.S., yolk-sac,
Y.S.S., septa of yolk-sac.

included within the enteron, for it remains extra-embryonic in
position until the very close of embryonic life. The yolk is
never taken directly into the embryonic digestive cavity and
there absorbed. The endodermal lining of the yolk-sac early
becomes differentiated as a yolk-digesting and absorbing organ,

290 OUTLINES OF CHORDATE DEVELOPMENT

and the nutritive materials taken up by it are received into the
yolk-sac circulation and carried to the embryo.

The yolk-sac is characterized by a wealth of blood vessels.
The vessels of the vascular area, already mentioned, are the
beginnings of the yolk-sac circulation. In the rich network of
small vessels, larger pathways soon develop; the first of these are
the paired anterior vitelline veins, which pass from the anterior
margin of the blastoderm directly into the posterior end of the
heart (Fig. 118, A). Soon after these become well established,
the pair of vitelline arteries develop (about thirty-eight hours)
as lateral branches of the dorsal aorta in the middle trunk
region (Fig. 118, A, B). These arteries become distributed by
large trunks throughout the yolk-sac, and supply its abundant
capillaries. The blood re-collects into the marginal sinus or
sinus terminalis, and passes thence into the anterior vitelline
veins. By the end of the third day the two anterior vitelline
veins have fused, just within the sinus terminalis, and between
this point and the heart the right vein begins to disappear
(Fig. 118, B). Soon it disappears entirely, and for a time the
left anterior vitelline vein alone returns the blood to the heart,
but before long, venous trunks appear, parallel with the main
branches of the vitelline arteries, and by the end of the fourth
day (Fig. 118, C) the greater part of the blood returns to the
heart through these, the lateral vitelline or omphalo-mesenteric
veins, which unite into the ductus venosus immediately before
entering the heart. Thus both the supply and the return of
the yolk-sac circulation pass along the wall of the yolk stalk or
splanchnic stalk.

The digestive and absorptive surface of the yolk-sac becomes
enormously increased by a folding process, which begins at the
time the larger vessels begin to be marked out. The folding
(Fig. 116) finally comes to be very complicated, and accom-
panying the folds is a continuation of the network of large
capillaries which thus come to have an intimate and extensive
relation with the nutritive supply. The inner surface of the
yolk-sac finally acquires a structure not unlike that of the lung,
its spaces or meshes being filled with the yolk material.

THE EARLY DEVELOPMENT OF THE CHICK 291

FIG. 118. — Diagrams of the circulation in the chick embryo and area vas-
culosa. The vascular network of the area vasculosa is omitted for the most part.

A. Anterior and central parts of the embryo and vascular area at about thirty-
eight hours (sixteen pairs of somites). Viewed from beneath. After Popoff.

B. Median and anterior parts of vascular area and embryo at about seventy-two
hours (twenty-seven pairs of somites). Viewed from beneath. After Popoff.

C. The main vascular trunks of the fourth day. After Lillie (modified), a,
Dorsal aorta; aa, aortic arches (first and second in A, second, third and fourth
in C); ac, anterior cardinal vein; al, allantois; au, auricle; b, bulbus arteriosus;
dC, ductus Cuvieri; dv, ductus venosus; ec, external carotid artery; h, .heart;

292 OUTLINES OF CHORDATE DEVELOPMENT

The yolk-sac increases in complexity throughout the period
of embryonic development. About two days before hatching,
while still a comparatively large organ, it is pushed into the
body cavity of the embryo by way of the somatic stalk cavity
(coelom), apparently through the contraction of the walls of
the allantois and amnion. Its entrance is completed a day or
so before hatching, and a few days after hatching both the
yolk and the yolk-sac itself become completely absorbed into the
intestine of the young chick, and the yolk stalk is definitely
closed.

2. The Amnion

We must again return to the embryo of thirty hours to
describe the formation of the amnion, and the associated
chorion, which are derived from the somatopleural portion of
the extra-embryonic blastoderm. In a general way we may
say that these structures arise from the crests of the outer
limbs of those folds which cut the embryo off from the extra-
embryonic blastoderm. The first indication of the amnion is
in the blastoderm, just in front of the head of the embryo, in
the anterior region of the so-called proamnion, where, about the
thirtieth hour, a slight transverse thickening of the ectoderm
becomes apparent in sections. This thickening is the begin-
ning of the ectamnion, which plays an important role through-
out the formation of the true amnion. The proamnion,
it will be recalled, is that part of the blastoderm which for a
time remains mesoderm-free. Hence no coelom, somatopleure,
and splanchnopleure are present in the region where the amnion
makes its first appearance.

Just in front of the head, the region of the ectamnion, en-
doderm as well as ectoderm, becomes folded upward as the
head-fold of the amnion (Fig. 99). This begins to extend back-

ic, internal carotid artery; la, lateral dorsal aorta; h, left anterior vitelline vein;
p, anterior intestinal portal; pc, posterior cardinal vein; pv, posterior vitelline
vein; rv, right anterior vitelline vein; s, sinus venosus; t, sinus terminalis; tr,
venous trunks of the area vasculosajf, ventricle; va. vitelline artery; vv, vitelline
or omphalo-mesenteric vein.

THE EARLY DEVELOPMENT OF THE CHICK 293

ward over the head of the embryo, but before it has gone very
far the mesoderm, with the accompanying exoccelom, extends
into the fold, and the endodermal layer is withdrawn. The
lateral extremities of the head-fold of the amnion turn pos-
teriorly along the sides of the head, as the lateral folds of the
amnion. These are somatopleural from their beginning, and
may be described as elevations of the blastoderm in the region
where the outer limbs of the lateral embryonic folds pass into
the general surface of the blastoderm (Fig. 110).

As these folds of the amnion extend posteriorly, the ectam-
nion serves actively to draw the more lateral regions toward the
mid-line where they are fused together, and in this way the
lateral folds are gradually drawn up over the embryo (Lillie).
This process occurs progressively in a posterior direction.
About the time the embryo has thus become covered over as
far back as the level of the vitelline arteries (48 hours, 26-28
pairs of somites), a posterior tail-fold of the amnion appears,
(Fig. 109, A), similar to its head-fold save that it is somato-
pleural, i.e., contains coelom and mesoderm, from its com-
mencement. This tail-fold extends laterally and then ante-
riorly, and soon its extremities meet the lateral folds. About
the seventieth hour (35 pairs of somites) the amnionic folds
are completely closed together above the embryo; this closure
occurs about at the level of the hind-limb buds.

As the somatopleural amnion folds come together above the
embryo, the ectodermal and mesodermal layers of each side
fuse together and the original contact surfaces break through,
so that the ccelomic cavities of the amnionic folds become con-
tinuous across the mid-line. This results in the formation of
two complete membranes, each composed of two cell layers,
around the embryo. The inner of these, close to the embryo,
is the true amnion, and the space between this and the embryo
is the amnionic cavity (Figs. 119, 125). From the method of
its formation it will be seen that the amnion is continuous with
the somatic stalk, while the amnionic cavity is a space entirely
outside the embryo, and has no connection with any other
cavity. The outer membrane is now called the chorion. It is,

294 OUTLINES OF CHORDATE DEVELOPMENT

of course, the somatic portion of the blastoderm, and at this
time has no direct connection with any other structure. The
space between amnion and chorion is exoccelom. This cavity
and the amnionic cavity are filled with a watery fluid. Later
on, as we shall see, this space is largely occupied by the allan-
tois, which comes into intimate connection with the inner
surface of the chorion.

ch

FIG. 119. — Transverse section of chick embryo with thirty-five pairs of
somites (about seventy-two hours), passing through the region of the twenty-
third somite. After Lillie. a, Amnion; ac, amnionic cavity; ao, dorsal aortse;
c, embryonic ccelom; ch, chorion; d, dermatome; ebc, exocoelom; g, rudiment of
spinal ganglion; m, mesonephric tubules; my, myotome; p, posterior cardinal
vein; s, sclerotome; sa, sero-amnionic connection; sc, subcardinal vein; so,
somatic mesoderm; sp, splanchnic mesoderm; v, vitelline artery; TF.Wolffian duct.

One important fact has not been mentioned thus far. In
the region where the amnionic folds finally close together over
the embryo, the amnion and chorion remain firmly united
(Fig. 119). This forms the sero-amnionic fusion, which affects
in an important way the later arrangement of these mem-
branes, as well as the disposition of the allantois, when it
extends into this region (Figs. 115, 116).

The regular arrangement of the lateral folds of the amnion is
disturbed somewhat by the twisting of the embryo, which is
going on as these folds are becoming elevated and fused. As
the embryo turns upon its left side the amnionic folds do not
similarly alter their morphological relation to what was

THE EARLY DEVELOPMENT OF THE CHICK 295

originally the median plane. That is, they continue to close
together along what was originally marked out as the mid-line,
and they finally close immediately above the right hind-limb
bud. It follows from this that the left lateral fold becomes
much the more extensive, passing from the lower (left) side of
the embryo, around to the upper (right) side and thus covering
the whole morphologically dorsal surface of the embryo, while
the right lateral fold covers only a portion of the upper (morpho-
logically right) surface of the embryo. This is correlated with
the fact that the right fold is thicker than the left and is usually
thrown into irregular transitory folds or wrinkles.

Soon after the amnion is fully formed, muscle fibers are
differentiated in its mesodermal layer. Waves of contraction
then slowly pass along the amnion and keep up a movement of
the amnionic and coelomic fluids. It is also supposed that
they keep the embryo in slight motion, preventing adhesions
between the embryo and its appendages. The amnion also
serves, probably, as a water cushion, protecting the embryo
against deforming pressures. The later relations of the
amnion to the allantois and the albumen of the egg will be
mentioned below.

3. The Allantois

The allantois is an embryonic appendage of the greatest
importance. Unlike the yolk-sac, amnion, and chorion, it is
developed from the embryo itself, and not from -the extra-
embryonic structures. When fully developed it is the most
extensive of all these accessory organs, the arrangement of
which becomes considerably modified by its growth. Function-
ally, too, it is of the utmost importance, it is primarily the
embryonic respiratory organ, but it serves also as a reservoir
for excretory products, and through the development of muscle
fibers in its wall it effects certain movements of the embryo,
and assists in the final inclusion of the yolk-sac within the
embryonic body.

The morphological relations of the allantois to the embryo

296 OUTLINES OF CHORDATE DEVELOPMENT

will be better understood if we recall certain facts regarding the
development of the tail. The tail-fold of the blastoderm differs
essentially from the head-fold in that the blastoderm where it
appears includes mesoderm, and is already differentiated into
somatopleure and splanchnopleure (Fig. 109, A). Preceding
the formation of the tail-fold of the somatopleure, the splanch-
nopleure is folded forward beneath the posterior end of the
embryo, establishing a short hind-gut. Soon after, the true, or

somatopleural, tail-fold pushes
inward, a short distance be-
hind the splanchnic fold. The
embryonic region immediately
anterior (morphologically) to
the somatopleural tail-fold is
the rudiment of the tail, the
tail bud (Fig. 109, B). As this
elongates, a posterior extension

•r fi(^i ^^M ~r of the hmd~gut continues into

it, as the postanal gut, for the
anus is formed on the ventral
FIG. 120. — Model of part of the side of the base of the tail.

The anterior extent of the hind-

aiiantoic stalk. After Ravn ( modi- gut is increased by the forward

fied). The broken line marks the , ,. ,-, -, ,

cavity of the hind-gut and aiiantoic extension ot the splancnno-

stalk. a .Cut edge of amnion; Dalian- pleura! tail-fold. The region

toic stalk; ap, anal plate; hi, cut sur- f

face of hind-limb bud; o, viteiiine beneath the hind-gut, between

*"* <the ** *~ the spknchnopleural and somat-

opleural tail-folds, is mesoder-

mal and is in reality a deep ventral mesentery. The cavity of
the hind-gut now pushes downward into this ventral mesentery,
forming an elongated depression, just in front of the anal
region (Fig. 109, B). This groove-like outgrowth is the rudi-
ment of the allantois, which thus makes its appearance about
the commencement of the third day of incubation (about 28
pairs of somites). In front of this the hind-gut narrows again;
the dorsal portion of this expansion, and the region just posterior
to it, form the rudiment of the cloaca (Fig. 120).

THE EARLY DEVELOPMENT OF THE CHICK 297

The allantois is clearly an outgrowth or appendage of the
hind-gut, and consequently its cavity is directly continuous
with the enteron; it is lined with endoderm, and its outer wall
is mesodermal. Before the close of the fourth day (Fig. 121)
the allantois has extended for some distance out into the exo-
coelom, lying to the right of the tail. Its terminal portion has
enlarged into a dilated vesicle connected with the gut by a
narrow tubular allantoic stalk. It has an abundant blood
supply, derived from a pair of branches of the dorsal aorta,

FIG. 121. — Median sagittal section through posterior end of four-day chick.
After Gasser (Maurer). al, Allantois; am, amnion (tail-fold) ; c, cloaca; m, cloacal
membrane; n, notochord; r, rectum; s, spinal cord; y, wall of yolk-sac (endoderm
and splanchnic mesoderm).

the allantoic arteries; its blood collects into a single allantoic
'vein and is returned to the heart through the large left um-
bilical vein (Fig. 138).

Once established, the allantois grows very rapidly through
the exoccelom, between the chorion and the yolk-sac and
amnion (Figs. 115, 116). Its vesicle enlarges rapidly and by
the end of the sixth day has covered the entire embryo; two
days later it has passed nearly around the yolk-sac. As the
allantois enlarges it effects certain important fusions with
other structures. Superficially it fuses with the chorion, the
mesodermal layers of the two membranes uniting so intimately

298 OUTLINES OF CHORDATE DEVELOPMENT

that in effect the chorion forms a part of the outer membrane
of the allantois. Along the dorsal surface of the embryo the
inner wall of the allantois meets the amnion, and the apposed
mesodermal layers of these two membranes fuse together,
forming a layer of muscle fibers which function for a time
similarly to those of the amnion, and then disappear.

A modified region of the allantois should be mentioned here.
During the early days of incubation the albumen of the egg
condenses toward what may be described as the postero-
ventral side of the yolk, from which it is separated only by the
remains of the vitelline membrane, in the region where the
yolk-sac remains open (Fig. 116). About the ninth or tenth
day, the albumen, through continued loss of water, forms a
relatively small, dense mass, incompletely separated from the
yolk by the intervention of the yolk sac (Fig. 117). The
allantois reaches the albumen first from the lower side. It is
now fused with the chorion throughout its extent, and as it
pushes onward, it sends a short fold in between the albumen
and the yolk-sac, and a longer limb around the outer surface
of the albumen, almost covering it over. These folds of fused
chorion and allantois are the beginnings of the albumen sac.
The albumen sac is completed by the downgrowth of a
similar fold of fused chorion and allantois from the upper
side. These folds finally enclose the yolk completely (Fig.
117). The upper fold is not quite like the lower on account of
the obstruction offered to the progress of the allantois, by the
sero-amnionic fusion. When the rapidly extending allantois
reaches this area of fusion of the amnion and chorion, it pushes
the chorion out above the fused area, carrying a fold of the
chorion before it in its onward extension (Fig. 116). This
fold of the chorion, with the allantois within, is similar to the
outer limb of the ventral part of the albumen sac, but the
inner limb of the latter is consequently not represented on the
dorsal side. Dorsally the inner wall of the albumen sac is
formed only by the original chorion of the region, the sero-
•amnionic connection being included (Fig. 117). About the
time the albumen sac is completed, by the fusion of the mem-

THE EARLY DEVELOPMENT OF THE CHICK 299

branes forming its outer wall, the sero-amnionic fusion becomes
perforated, and the albumenous material partly passes into
solution in the amnionic fluid. For the most part, however,
the albumen is absorbed through the walls of the albumen sac.
This is fully accomplished toward the close of the embryonic
period, and the albumen sac then remains as an appendage of
the yolk-sac, with which it passes into the body of the embryo
at the end of incubation.

The most characteristic feature of the allantois is the extreme
vascularity of its outer wall. The withdrawal of the albumen
from the greater part of its surface leaves the fused chorion
and outer allantoic wall in direct apposition to the shell mem-
brane. The chorionic layers become extremely thin and
the shell membrane becomes very porous, so that there is an
easy exchange of gases between the outside air and the capil-
laries of the outer allantoic wall. These capillaries are very
wide and extremely abundant, so altogether the allantois is a
very efficient respiratory organ.

The inner wall of the allantois, as already mentioned, fuses
with the amnion in the region dorsal to the embryo, during the
second week of incubation. Here as elsewhere in the inner
wall, muscle fibers may develop. Later on, as the period of
incubation draws toward its close, it fuses also with the yolk-
sac. The cavity of the allantois remains connected with the
cloaca by the tubular allantoic stalk. It is filled with a fluid
containing the excretory products, received from the cloaca
where the excretory ducts discharge.

Von Baer's account of the principal events associated with
the hatching of the young chick, is summarized in the two
following paragraphs quoted from Lillie (" Development of the
Chick," p. 232).

" About the fourteenth day the growing embryo accommo-
dates itself to the form of the egg so as to lie parallel to the long
axis with its head usually toward the broad end near to the air-
chamber. Sometimes, however, the embryo is turned in the
reverse position (Von Baer). The head is bent toward the
breast, and is usually tucked under the right wing. Important

300 OUTLINES OF CHORDATE DEVELOPMENT

changes preparatory to hatching take place on the seven-
teenth to nineteenth days. The fluid decreases in the amnion.
The neck acquires a double bend so that the head is turned
forward, and, in consequence, the beak is toward that part
of the membranes next to the air-chamber. The intestine is
retracted completely into the body-cavity, and on the nine-
teenth day the yolk-sac begins to enter the body-cavity. On
the twentieth day the yolk-sac is completely included, and
practically all the amniotic fluid has disappeared. The chick
now occupies practically all the space within the egg, outside
of the air-chamber. The umbilicus is closing over. The
ductus arteriosi begin to contract, so that more blood flows
through the lungs. The external wall of the allantois fused
with the chorion still remains very vascular.

"Now, if the chick raises its head, the beak readily pierces
the membranes and enters the air-chamber. It then begins
to breathe slowly the contained air; the chick may be heard,
in some cases, to peep within the shell two days before hatch-
ing, a sure sign that breathing has begun. But the circulation in
the allantois is still maintained and it still preserves its respi-
ratory function. When the chick makes the first small opening
in the shell, which usually takes place on the twentieth day, it
begins to breathe normally, and then the allantois begins
to dr}' up and the circulation in it rapidly ceases. It then
becomes separated from the umbilicus, and the remainder of
the act of hatching is completed, usually on the twenty-first
day."

References to the literature are given at the end of Chapter V»

CHAPTER V

THE LATER DEVELOPMENT OF THE CHICK:
ORGANOGENY

PAGE

I. THE NERVOUS SYSTEM 302

1. The Central Nervous System 302

2. The Cranial and Spinal Ganglia 309

3. The Peripheral Nervous System 311

A. The Spinal Nerves and the Sympathetic System . . 311

B. The Cranial Nerves . 313

II. THE SPECIAL SENSE ORGANS . . . 316

1. The Eye v. 316

2. The Ear 321

3. The Olfactory Organ 325

III. THE ALIMENTARY TRACT AND ITS APPENDAGES . . 326

1. The Organs of the Fore-gut . , . 326

2. The Organs of the Hind-gut 334

3. The Mid-gut 334

IV. THE VASCULAR SYSTEM ' ' 336

1. The Heart i . . . 337

2. The Aortic Arches and the Arterial System 340

3. The Venous System 343

4. The Lymphatic System and Spleen 349

V. THE CAVITIES OF THE BODY 350

VI. THE LATER HISTORY OF THE MESODERMAL SOMITES . 352

VII. THE URINOGENITAL SYSTEM 354

1. The Excretory System 355

A. The Pronephros and the Pronephric Duct (Wolffian

Duct) 355

B. The Mesonephros 356

C. The Metanephros 358

2. The Reproductive System ...... 359

A. The Reproductive Ducts 360

B. The Gonads 361

3. The Adrenal Bodies .* . . 363

IT remains now for us to describe the chief events. in the
development of the systems and organs of the embryo, from the

301

302 OUTLINES OF CHORDATE DEVELOPMENT

condition at which we left them, for the most part about the
thirtieth hour. We shall limit this account to little more
than the bare mention of the more important morphological
alterations of structure, considering the systems separately.

I. THE NERVOUS SYSTEM

1. The Central Nervous System

We have already traced the development of the central
nervous system up to the formation of the spinal cord and

FIG. 122. — Neuromeres in the brain of the chick embryo. Dorsal views.
From Von Kupffer (Hertwig's Handbuch, etc.) after Hill. A. Embryo of
twenty-four hours; two pairs of somites. B. Embryo of twenty-four hours;
five pairs of somites. C. Embryo of twenty-five and one-half hours; six pairs
of somites. D. Embryo of twenty-six hours; seven pairs of somites, cp,
Posterior limit of prosencephalon; fr, posterior limit of mesencephalon; ps,
primitive streak; u, first somite; 1-11, neuromeres.

brain, and the establishment, in the latter, of the primary
hind-, fore-, and mid-brains. In connection with the pri-
mary fore-brain we noted the rudiments of the optic vesicles,
and in the primary hind-brain the series of six neuromeres,
or brain segments, which are clearly distinguishable at the
thirty-hour stage .described.

THE LATER DEVELOPMENT OF THE CHICK 303

In earlier stages neuromeres have made a brief, transitory
appearance in the fore- and mid-brains as well. Thus in the
embryo of about twenty-three hours (4 pairs of somites), Hill
has distinguished eleven neuromeres, all told. Of these three
are in the region of the future fore-brain: these disappear
about the twenty-sixth hour (7 pairs of somites). The mid-
brain includes only two neuromeres, which remain distin-
guishable until about the thirty-fifth hour (14 pairs of somites).
The six neuromeres of the hind-brain are the best marked, and
are visible for several days (Fig. 122).

The next important advance consists in the transverse con-
striction of the primary fore- and hind-brains each into two
sections, making in all five regions in the brain. The pri-
mary fore-brain, or prosencephalon, is divided into the anterior
telencephalon, or secondary fore-brain, and the posterior
diencephalon, or bet ween- brain. Then following the un-
divided mid-brain, or mesencephalon, come the two divisions
of the primary hind-brain, or rhombencephalon; the anterior
of these is known as the metencephalon, the posterior as the
myelencephalon. The myelencephalon continues directly into
the spinal cord.

We may now proceed to describe the principal structures
arising in connection with each of the secondary divisions of
the brain.

The telencephalon includes only the first neuromere. This
portion of the brain, it will be recalled, is directed backward
beneath the fore-gut, its morphologically anterior end actually
being directed postero-dorsally (Fig. 123). The telencephalon
expands vertically and the optic vesicles remain connected
with its ventral side. As the optic vesicles push out toward
the surface of the head, their connections with the brain
become narrowed as the optic stalks. The cavities of the
vesicles remain continuous, through the stalks, with the
cavity of the telencephalon (Fig. 127), and a median depression
in the floor of the telencephalon, between the openings of the
optic stalks, becomes well marked as the recessus options (Fig.
123). This optic recess, and a short stretch of the brain- wall

304 OUTLINES OF CHORDATE DEVELOPMENT

ao

A

sv

vt

am

ao

vt

am

FIG. 123. — Sagittal sections through the head of the chick. In A the heart
is shown in optical section. After Lillie. A. Of an embryo with twenty-two
or -three pairs of somites (about forty-four hours) . B. Of an embryo with thirty-
nine pairs of somites (end of the fourth day), o, Auricle; am, amnion; ao, dorsal
aorta; ba, bulbus arteriosus; cf, cranial flexure; D, diencephalon; dv, ductus
venosus; e, epiphysis; h, hypophysis; i, infundibulum; ip, anterior intestinal
portal; is, isthmus; I, rudiment of lung; li, liver; m, mandibular arch; Ms, mesen-
cephalon; Mt, metencephalon; My, myelencephalon; n, notochord (degenerating) ;
o, oral membrane (oral plate); oe, oesophagus; p.pharynx; P, parencephalon;
r, optic recess; S, Seessel's pocket (preoral gut); st, stomach; sv, sinus venosus;
Sy, synencephalon; T, telencephalon; th, rudiment of thyroid body; tp, tuber*
culum posterius; v, ventricle; vt, velum transversum.

THE LATER DEVELOPMENT OF THE CHICK 305

immediately in front of it, not now distinct but differentiating
later, together mark, morphologically, the true anterior end
of the central nervous system.

The anterior and lateral portions of the telencephalon now
begin to expand, giving the effect of a constriction at its
posterior limit. This apparent constriction of the dorsal wall
of the fore-brain is the velum transversum, which marks the
separation between telencephalon and diencephalon. In these

hnu

cd

hy.

FIG. 124. — Median sagittal section through the brain of the chick of twelve
to thirteen days. From Von Kupffer (Hertwig's Handbuch, etc.) ; c, Cerebellum;
ca, anterior commissure; cd, notochord; ch, habenular commissure; ci, infundi-
bular commissure; ck, central canal of spinal cord; cp, posterior commissure;
cpa, anterior pallial commissure; cs, spinal commissure; cv, cavum cerebelli;
cw, optic chiasma; dr, epiphysial gland; dt, decussation of the trochlear (IV)
nerve; e, epiphysis; ei, paraphysis; hm, cerebral hemisphere; hy, hypophysis;
J, infundibulum ; le, ependymal lamina of the roof of the fourth ventricle; lo,
olfactory lobe; Ip, posterior lobe of cerebral hemisphere; M, mesencephalon;
opt, optic chiasma; pch, choroid plexus third ventricle; pi, choroid plexus of fourth
ventricle; re, epiphysial recess; ro, optic recess; s, saccus of infundibulum; si,
posterior intracephalic furrow; tp, tuberculum posterius; <pi, tuberculum mam-
millare; tr, torus transversus; va, velum medullare anterius; vi, median ventricle
of telencephalon; vp, velum medullare posterius.

early stages no other sharp distinction between these two
regions can be determined.

Toward the close of the second day a pah- of lateral exten-
sions of the telencephalon push out rapidly and expand dor-
sally, anteriorly, and posteriorly; these are the rudiments of

306 OUTLINES OF CHORDATE DEVELOPMENT

the cerebral hemispheres. The cavity of the telencephalon is
continued into the cerebral hemispheres as the lateral ven-
tricles, known also as the first and second ventricles of the
brain. The reduced median cavity of the telencephalon re-
mains, forming the anterior portion of the third ventricle; the
openings of the lateral ventricles out of the third ventricle are
known as the foramina of Monro. The cerebral hemispheres
enlarge rapidly and soon grow out, either side of the mid-line,
far in front of, and above, the original extent of the telen-
cephalon, which remains limited to a narrow median strip dor-
sally and anteriorly (Fig. 124). The ventral and lateral walls
of the cerebral hemispheres soon become greatly thickened, as
the corpora striata, or basal ganglia, which finally become so
large that they nearly obstruct the lateral ventricles. Else-
where the walls of the hemispheres remain comparatively
thin.

The dorsal region of the original telencephalon remains em-
bedded between the hemispheres. On its dorsal surface,
immediately in front of the velum transversum, it becomes
invaginated as the paraphysis. That part of its walls in front
of the recessus opticus, as far as the level of the foramina of
Monro, forms the lamina terminalis; this remains very thin
except in its middle where the anterior commissure develops
later.

The diencephalon includes the second and third neuromeres.
Its antero-dorsal and antero- ventral limits are marked, re-
spectively, by the velum transversum and the recessus opticus.
Posteriorly it is marked off from the mesencephalon ventrally
by an elevation in the floor, the tuberculum posterius, and
dorsally by a broad depression of the wall (Fig. 123).

Like the telencephalon, this also is vertically extended. Its
cavity forms, together with the median cavity of the telen-
cephalon, the third ventricle. Just behind the recessus opticus
the ventral and ventro-lateral walls are thickened as the optic
chiasma, and just back of this is a well-marked evagination,
the rudiment of the infundibulum. The lateral walls of the
diencephalon remain thin for a time, but later become greatly

THE LATER DEVELOPMENT OF THE CHICK 307

thickened as the optic thalami. The roof remains thin and
considerably expanded; in the region of the velum transversum
the roof of the diencephalon and telencephalon becomes modi-
fied into the folded choroid plexus of the third ventricle (Fig. 124).
*Back of this the diencephalic roof is evaginated as the tubular
epiphysis or pineal body. Finally a thickening in the dorsal
wall marks the posterior dorsal limit of the diencephalon; this
is the rudiment of the posterior commissure.

The mesencephalon, or mid-brain, forms the topographically
anterior part of the brain, projecting considerably in advance
of all the other structures of the embyro (Figs. 113, 114, 123).
It includes the fourth and fifth neuromeres. It remains
relatively undifferentiated for a considerable period, but later
its dorsal and dorso-lateral walls evaginate and thicken, form-
ing the optic lobes, which include a part of the original cavity
of the mesencephalon. The central portion of its cavity, now
greatly restricted, remains as the aqueduct of Sylvius, or iter,
continuing posteriorly from the third ventricle. The ventral
and ventro-lateral walls of the mesencephalon thicken to form
the great nervous pathways from the optic lobes to other cen-
ters, known as the crura cerebri. Back of the optic lobes the
mesencephalon remains undilated as the isthmus, leading
directly to the metencephalon (Fig. 124).

The metencephalon, lying dorsal to the anterior tip of the
notochord, consists of only the sixth neuromere, and is thus
very short. The cavity of the metencephalon is not separable
from that of the succeeding section, the myelencephalon; to-
gether they are known as the fourth ventricle. The walls of the
metencephalon thicken slowly, though steadily, during the
early days of incubation. Later the dorsal and dorso-lateral
regions become very greatly thickened, forming the cerebellar
hemispheres, or cerebellum. The ventral and ventro-lateral
walls also thicken very considerably to form the pons Varolii.

The myelencephalon, the last division of the brain, includes
the seventh to eleventh neuromeres, indications of which re-
main visible, ventrally, until about the fourth day. Its cavity,
as said above, is the fourth ventricle. The roof of this section

308 OUTLINES OF CHORDATE DEVELOPMENT

remains thin and non-nervous, and ultimately forms the cho-
roid plexus of the fourth ventricle. The ventral and ventro-
lateral walls become greatly thickened as the medulla oblongata
or spinal bulb. This region becomes flexed ventrally forming
the pontine flexure (Fig. 124). The cervical flexure, previously,
mentioned, is gradually disappearing, but the original cranial
flexure of the mesencephalic region remains as a permanent
feature of the brain.

Posteriorly the elongated myelencephalon passes into the
spinal cord. This is of lesser diameter than the medulla, and
at first is vertically elongated with somewhat thickened lateral
walls. Its cavity, the central canal, continuous with the fourth
ventricle, is narrow but deep. The lateral walls continue to
thicken and finally the cord becomes approximately circular
in section, and its cavity is reduced to a very small tube by the
fusion of its dorsal walls. The median dorsal and ventral
walls of the cord remain thin. As the lateral walls begin to
thicken their constituent cells become highly differentiated.
The original epithelial elements of the neural tube become dif-
ferentiated as the ependymal cells; these are non-nervous, sup-
porting cells. The free ends of the ependymal cells, bordering
the central canal, become ciliated. The embryonic nerve cells,
or germinal cells, originally scattered through the epithelial
cells, multiply rapidly and form both neuroblasls, which give
rise to the gray matter of the cord, and non-nervous supporting
cells or glia cells. From the neuroblasts various processes grow
out, for the most part remaining within the central nervous
system and forming in part the white matter. Some of the
neuroblasts of the ventro-lateral regions (ventral cornua) send
out processes which leave the central system as the components
of the ventral or motor (efferent) roots of the spinal nerves.

From the functional standpoint the most important facts
concerning the development of the central nervous system
are the histogenetic processes going on in the different regions
of the walls of the brain and cord, especially the establishment
of the various centers (nuclei) and tracts. Although of the
greatest importance and interest, all such details lie without

THE LATER DEVELOPMENT OF THE CHICK 309

the scope of this work. (Further information on this general
subject is found, together with references to the literature,
in Johnston's " Nervous System of the Vertebrates/' Philadel-
phia, 1906.)

2. The Cranial and Spinal Ganglia

These structures are derived from the neural crests, whose
formation has already been described. The neural crests
finally extend the entire length of the nervous system. In
the trunk region they begin to extend laterally between the
ectoderm and the mesodermal somites. In the intervals
between successive somites the neural crest becomes inter-
rupted, the cells apparently, though not certainly, being
converted into mesenchyme. By this process each crest is
broken into a metameric series of cell-groups. These groups
are the rudiments of the spinal ganglia, and therefore also of
the dorsal (afferent) roots of the spinal nerves. Each group
contains neuroblasts as well as indifferent cells, and very
early comes into close relation with the cells of the adjoining
somite.

In the region of the somites of the head the neural crests are
poorly developed, in correlation with the absence of ganglia in
these segments. But throughout the remainder of the head
they are well developed and form the rudiments of the ganglia
and certain of the branches of the cranial nerves. As in the
trunk region, the continuous crests are broken up by the con-
version of certain regions into mesenchyme. The regions re-
maining form the rudiments of the ganglia of the X, IX, VIII,
VII, and V cranial nerves. The ganglia of the IX and X
nerves arise together and are divided, toward the close of the
second day into separate cell-groups by the formation of the
gill-pouches of the region (Fig. 130). Thus the ganglion of the
IX nerve, ganglion petrosum, is left just above the third visceral
arch, and that of the X nerve, ganglion jiigulare-nodosum, above
the fourth and fifth visceral arches. Each of these acquires a
connection with an ectodermal branchial sense organ, or

310 OUTLINES OF CHORDATE DEVELOPMENT

placode, just above the second and third visceral pouches.
These placodes are vestigial organs in terrestrial vertebrates,
and this connection, as well as the existence of the placodes
themselves, is of very brief duration.

The ganglia of the VII and VIII nerves arise in common,
from an enlarged part of the crest lying immediately in front
of the rudiment of the ear. This cell-group, the acustico-
facialis ganglion (Fig. 114), connects with the brain in the
region of the third neuromere of the myelencephalon. It also
connects (about the forty-eighth hour) with a well-marked pla-

Lens.

FIG. 125. — Transverse section, passing through the eyes and heart, of an
embryo with about thirty-five pairs of somites (about seventy-two hours).
From Lillie (Development of the Chick). Am., Amnion; Ao.t dorsal aorta;
Atr., auricle; B.A., bulbus arteriosus; Ch.Fis., choroid fissure; Chor., chorion;
D.C., ductus Cuvieri; Dienc., diencephalon; Lg., rudiment of lung;P.C., pericar-
dial cavity; p.Ch., posterior chamber; pl.gr., pleural groove; V.c., posterior car-
dinal vein; Y.S., yolk-sac.

code on the first visceral pouch. The ganglion of the V nerve,
trigeminal ganglion, is the most anterior of the series (Fig. 130).
It connects with the first neuromere of the myelencephalon and
sends outgrowths into the regions of both upper and lower
jaws, as the rudiments of certain branches of the V nerve. A
part of the mesenchyme of the mandibular and hyoid arches
is also formed from the cells of these rudiments, and especially
from the neural crest anterior to the V ganglion. During an
early stage in their formation from the crests, the rudiments
of the V and VII ganglia connect with the surface ectoderm

THE LATER DEVELOPMENT OF THE CHICK 311

around the first visceral pouch, and appear to receive cells pro-
liferated from this layer. This connection is not to be con-
fused with the much later connections established by the VII,
IX, and X ganglia with the epibranchial placodes.

3. The Peripheral Nervous System

We must distinguish here between the spinal and cranial
nerves. The spinal nerves, of which there are some thirty-
eight pairs distinguishable at certain stages, all develop essen-
tially alike, while the twelve pairs of cranial nerves may differ
widely form one another and from the spinal nerves, in their
development, as they do in morphology and in function.

A. THE SPINAL NERVES AND THE SYMPATHETIC SYSTEM

Each spinal nerve is a complex, including parts of unlike
function and relation to other structures. For our present
purposes it will be necessary to distinguish only the dorsal or
afferent and the ventral or efferent portions, and in each of these
the somatic (somatopleural) and splanchnic (splanchnopleural)
pathways. Brief reference to the sympathetic system may be
included here because it is obviously derived, to a certain
extent, from the same rudiments as are the spinal nerves.

The rudiments of the somatic afferent portions of the spinal
nerves are the cell-groups derived from the neural crests de-
scribed above, i.e., the spinal ganglia. During the third day
the neuroblasts of the spinal ganglia send out processes (axons,
axis cylinder processes) in two directions, centripetally into the
spinal cord, and centrifugally, meeting and joining the ventral
root; the cell bodies thus remain as the spinal ganglion cells.
The ventral root of each spinal nerve is efferent and is composed
of outgrowths (axons) from both somatic and splanchnic neuro-
blasts located in certain regions of the ventral cornua of the
spinal cord. The dorsal and ventral (afferent and efferent)
roots unite a short distance from the cord forming the spinal
nerve trunk. This trunk then immediately divides into three

312 OUTLINES OF CHORDATE DEVELOPMENT

main branches (Fig. 126); first is given off ventrally a large
branch to the sympathetic system, the ramus communicans (see
below). These fibers are finally distributed to splanchno-
pleural derivatives, and are derived from both dorsal and
ventral roots. The trunk then separates into dorsal and ventral
branches, each containing fibers from both roots, which are
distributed chiefly, though not wholly, to somatopleural struc-
tures, the integument and stri-
ated muscles. Opposite the limb-
buds the spinal nerves accom-
pany extensions of the somites
into the limbs and provide their
innervation, supplying the mus-
cles and integument.

Meanwhile the sympathetic
system has been forming. Dur-
ing the third day some of the
neuroblasts of the spinal ganglia
send out processes which extend
downward toward the aorta;

FIG. 126. — Diagram of the chief ., , .. . ,

elements of the sympathetic nervous then along the path&thus marked

SSS.^Ai.SSSf SToS out some of the neuroblasts of
aorta; ap, aortic plexus; d, dorsal the spinal ganglia, and others

(afferent) root of spinal nerve; g, /• ,-t - ^ •> •. -./.

spinal ganglion; t, intestine; m, from the Spinal COrd itself, mi-
mesentery ; n, notochordjfl, Remak's grate to a position ventral to the

ganglion; s, splanchnic plexus; sg, , r

sympathetic elements in intestinal Spinal COTO, around the dorsal

wall; t, mesonephric tubules; v, onrfo Thp^P Tniorfltnrv pplk

ventral (efferent) root of spinal * Ca- nigra

nerve; I, primary sympathetic cord; thus establish a pair of longi-

//, secondary sympathetic cord. i» -i

tudinal cords, the primary sym-
pathetic cords (Fig. 126). Other migratory neuroblasts from
the spinal ganglia then form somewhat similarly, a pair of
secondary sympathetic cords just above the primary cords.
The secondary cords then become connected segmentally with
the spinal ganglia, by processes from the secondary cord cells
which extend back into the ganglia and through the dorsal spinal
root into the spinal cord. The primary sympathetic cords give
rise to the prevertebral plexuses, but otherwise disappear en-

THE LATER DEVELOPMENT OF THE CHICK 313

tirely during the sixth and seventh days. The secondary sym-
pathetic cords are the rudiments of the major portion of the
definitive sympathetic cords of the adult, and the groups of
fibers connecting these cords with the spinal ganglia become
the rami communicantes. The secondary sympathetic cords
become ganglionated, and additional processes grow out, con-
necting with the ganglia derived from the primary cords,
whose cell processes are finally distributed in a complex man-
ner to the visceral surfaces. The cardiac plexus, and the
plexuses of the viscera, arise chiefly from neuroblasts migrating
along the X nerves from the hind-brain and X ganglion.

Two other important groups of fibers pass by way of the rami
communicantes; these are (1) the visceral afferent fibers be-
longing with the dorsal spinal root and ganglion, which pass
by way of the sympathetic trunks to their distribution in the
visceral sensory surfaces, and (2) the visceral efferent (motor)
fibers from the spinal cord and ventral root, to their distri-
bution in the visceral musculature. These latter fibers, al-
though arising in the cord and forming an important part of
the spinal nerve, are really to be regarded as components
of the sympathetic system.

B. THE CRANIAL NERVES

The cranial nerves exhibit in their development a variety that
parallels their diversity in morphology and in function. It is
possible, however, to relate many of them to parts of the typical
spinal nerves, and like these they have two sources, ganglia from
the neural crests, and neuroblasts within the spinal cord. The
details of their development are complicated and we may in-
clude here only a few of the more important facts in connection
with each nerve. The more posterior cranial nerves show
greater similarity to the spinal nerves, and as we pass forward
they diverge more and more widely from this type.

The XII Cranial Nerve (Hypoglossus) . — This is the nerve
associated with that part of the cord which has most recently
become included within the medulla, i.e., the region of the first

314 OUTLINES OF CHORDATE DEVELOPMENT

four mesodermal segments. It arises as two pairs of roots,
similar to the ventral spinal nerve roots, in the region of the
last two segments of the head. The two roots join and the
nerve then passes around, posteriorly to the last gill-pouch, to
the floor of the pharynx, where it is distributed to the muscles
of the tongue; it is thus visceral efferent.

The XI Cranial Nerve (Spinal Accessory). — The development
of this nerve in the chick is unknown. The XI nerve is to be
regarded as a separated caudal portion of the X nerve and
since it is visceral efferent (although supplying voluntary mus-
cles in the higher vertebrates), its development is probably not
unlike that of the visceral efferent elements of the X nerve.

The X Cranial Nerve (Vagus or Pneumogastric) . — This large
nerve is really a complex, consisting of the nerves associated
with the third and fourth visceral pouches. It is chiefly
visceral, both afferent and efferent, and in addition to its
visceral-pouch branches, it sends branches back to certain of
the viscera.

The formation of the primary vagus ganglion has been de-
scribed. This divides into two parts, one remaining in its
original position (ganglion nodosum), the other moving down
between the fourth and fifth visceral arches (ganglion jugulare).
Its ventral root is multiple, a large number of outgrowths from
the cells of the medulla converging to the ganglion nodosum,
from which connections are made with the sympathetic system.
From the ganglion jugulare branches grow out to the gill- pouch
region, and a large branch passes posteriorly to supply the
thoracic and abdominal organs. Neuroblasts accompany these
branches and later form the sympathetic ganglia of the organs
innervated.

The IX Cranial Nerve (Glossopharyngeal) . — This is to be re-
garded as a separate anterior portion of the vagus group. It
is the nerve of the second visceral pouch (first branchial pouch) .
Its development is essentially similar to that of the branchial
portions of the X nerve, with which it forms a connection.

The VIII Cranial Nerve (Auditory). — As already noted the
VIII nerve arises in common with the VII. A posterior part

THE LATER DEVELOPMENT OF THE CHICK 315

of the common acustico-facialis ganglion becomes intimately
related with the rudiment of the ear (auditory sac) and later
differentiates in situ. It has no efferent fibers equivalent to
the ventral spinal roots or to the efferent components of the
cranial nerves so far described.

The VII Cranial Nerve (Facial). — That portion of the acus-
tico-facialis ganglion remaining after the differentiation of the
VIII ganglion and nerve, remains as the geniculate ganglion
of the VII nerve. This connects with the medulla in the usual
fashion, and distally fibers grow out into the vicinity of the
first or hyomandibular visceral pouch (spiracle) with which
this nerve is primarily related. In the chick it is chiefly
visceral efferent, but the development of these motor compo-
nents is not known, although the cells composing its nuclei of
origin in the medulla, have the usual position relative to other
centers.

The V Cranial Nerve (Trigeminal) . — The trigeminal ganglion
derived from the neural crest connects with the medulla in the
usual way and early becomes partially divided. From the
smaller anterior portion (profundus ganglion) fibers grow for-
ward as the deep ophthalmic branch, while from the posterior
part (trigeminal ganglion proper) arise the branches distributed
to the upper and lower jaws. This nerve is chiefly somatic
afferent, its small efferent component developing typically,
during the fourth day.

The IV and VI Cranial Nerves (Trochlear and Abducent). —
These two nerves have many characteristics in common.
They are purely motor, distributed to muscles of the eye-ball
(superior oblique and external rectus, respectively), and con-
sequently have no ganglia outside the medulla. They appear
relatively late (fourth day), the IV from the dorsal surface of the
isthmus, the VI from the ventral side of the myelencephalon.

The III Cranial Nerve (Oculomotor). — This too is chiefly
motor, supplying the remaining muscles of the eye-ball. Its
fibers grow out from the ventral side of the mid- brain and
extend into the mesenchyme around the developing eye.
Associated with its motor elements are afferent components

316 OUTLINES OF CHORDATE DEVELOPMENT

growing out from the ciliary ganglion. The neuroblasts. form-
ing the ciliary ganglion appear to migrate from the neural
tube and from the profundus ganglion of the V nerve. These
afferent fibers seem to arise in the muscles of the eye-ball.

The so-called / (Olfactory) and II (Optic) cranial nerves will
be considered in connection with the development of the sense
organs with which they are associated.

II. THE SPECIAL SENSE ORGANS

1. The Eye

We have described in the preceding chapter the formation
of the optic vesicles from the primary fore-brain, and the
differentiation of the optic stalks, which remain related with
the ventral side of the diencephalon either side of and posterior
to the recessus opticus (Fig. 125). The optic stalks and vesicles
are the rudiments of only the essential, or sensory (recipient)
and nervous elements, of the eye. All of the other accessory
parts of this complex organ are differentiated from other tissues.

While the tubular optic stalk remains comparatively short,
the optic vesicle enlarges rapidly and soon (thirty hours)
reaches the surface ectoderm of the head. The continued dila-
tion of the vesicle occurs mostly above the level of the stalk,
-which therefore remains related with the ventral side of the
vesicle, as of the brain (Fig. 128). Now there appears a thick-
ening of the ectoderm opposite the optic vesicle; this is the
rudiment of the lens. Both the optic vesicle and the rudiment
of the lens then proceed to invaginate, independently, but in
the same direction (Figs. 127, 128).

The invagination of the optic vesicle, which converts it into
the two-layered optic cup, is not a simple hemispherical invagi-
nation. The irivaginating region begins about in the middle
of the outer wall of the vesicle and extends thence downward,
to the attachment of the optic stalk, as a vertical groove. The
distal wall of the vesicle rapidly folds in toward the proximal
wall and nearly obliterates the original cavity of the vesicle,
just as the invaginating endoderm of the Amphioxus gastrula

THE LATER DEVELOPMENT OF THE CHICK 317

obliterates the blastocoel. The result is the formation of a two-
layered optic cup; its inner layer, which may now be distin-
guished as the retinal layer is already quite thickened, while its

ir

FIG. 127. — Diagrams illustrating the development of the eye in the chick.
After Froriep (slightly modified). A. Transverse section through part of the
fore-brain and optic vesicles of a chick, late the second day of incubation. On
the left the section passes through the optic stalk, on the right to one side of it.
B. Transverse section through the optic vesicle and associated structures at the
end of the second day. C. Same, slightly later. D. Section through the pupil-
lary region of the eye, the latter part of the fifth day. a, Anterior chamber
of eye; ec, ectoderm of head (epidermis); eck, ectoderm of cornea; F, cavity (or
wall, in B) of fore-brain; i, inner or retinal layer of optic cup; ir, mesodermal
rudiment of iris; I, lens; m, mesoderm; mk, mesoderm of cornea; o, outer or pig-
ment layer of optic cup; t, optic stalk; v, cavity of primary optic vesicle (in C and
D nearly obliterated by the invagination of the optic vesicle to form the optic
cup).

outer layer has become quite thin (Figs. 127, 128). The new
cavity of the optic cup is the rudiment of the large posterior
chamber of the eye. The cavity of the cup is at first widely
open toward the lens and ectoderm, but its margin rapidly

318 OUTLINES OF CHORDATE DEVELOPMENT

draws together somewhat. In the middle of the cup, opposite
the lens, it remains open as the circular rudiment of the pupil.
Ventrally from this the rim draws together more closely,
leaving only a narrow slit-like opening extending from the
pupil to the attachment of the optic stalk; this is known as the
choroid fissure (Fig. 128). The choroid fissure remains open
for several days and takes an important part in determining
the course of the later development of the eye.

We must now return to trace the formation of the lens.
The ectodermal thickening mentioned above rapidly extends,

FIG. 128. — Diagrams of sections through the eye of the chick embryo at the
end of the second day. After Lillie. The dorsal margin is toward the top of the
page in A and B. A. Eye as viewed directly. B. Vertical section through the
line x-cf, in A. C. Horizontal section through the line y-y, in A. cf. Choroid
fissure; cv, cavity of primary optic vesicle; ec, superficial ectoderm of head; i,
inner or retinal layer of optic cup; I, lens; o, outer or pigmented layer of optic
cup; ol, opening of lens sac from surface of head; pc, posterior chamber of eye;
s, optic stalk, continuous with the floor and lateral wall of the diencephalon.

and proceeds to invaginate toward the invaginating retinal
layer. Its wall thickens as it invaginates simply, and soon
after the invagination of the retinal layer is completed, the
lens separates from the ectoderm, forming a flattened vesicle
lying in the cavity of the optic cup.

These events are completed during the third day, and now
the optic cup enlarges very rapidly for a time, forming a large
cavity (posterior chamber) still open through the pupil and
the choroid fissure. From the rudiments now established and
from the surrounding mesenchyme, the parts of the fully
formed eye are all derived. We may mention only a few of the

THE LATER DEVELOPMENT OF THE CHICK 319

more important events in the further history of the structures.

The optic cup extends ventrally as well as in other directions,
so that the attachment of the optic stalk appears no longer
connected with the ventral side, but rather with the middle of
the proximal hemisphere, nearly opposite the pupil and lens;
this is known as the fundus region. Associated with this
change is a decided alteration in the character and relations of
the choroid fissure, which will be described below.

About the sixth or seventh day the thick inner layer of the
optic cup becomes clearly differentiated into a proximal or
retinal zone, and a distal or lenticular zone. The former in-
cludes rather more than the proximal hemisphere, while the
latter forms a broad band bordering the pupil. The retinal
portion becomes transformed later into the sensory and nervous
parts of the eye; the thin outer layer in the retinal zone of the
cup is not sensory, but is transformed into the pigmented
layer of the retina. Both the inner and outer layers of the cup
in the lenticular zone share in forming the rudiments of the
iris and ciliary process. The separation between the retinal
and lenticular zones is marked in the developed eye by the
ora serrata.

In the lenticular zone the thin outer layer fuses with the
inner layer, becomes pigmented, and together with mesenchyme
cells of the region they form the iris (Fig. 127, D). The proper
muscles of the iris are not derived from the mesenchyme, but
from bud-like outgrowths of the lenticular zone (ectoderm).
The ciliary process is at first a series of folds of the lenticular
zone around the base of the iris, but soon these folds are
invaded by mesenchyme cells which form the muscles of the
ciliary process.

During the expansion of the optic cup the margins of the
choroid fissure have come into close apposition, nearly closing
the fissure. Owing to the originally ventral attachment of
the optic stalk the retinal layer is continuous, either side of the
fissure, with the lower side of the stalk, and the connection
extends through about one quadrant of the optic cup, i.e.,
from the fundus nearly around to the margin of the retinal

320 OUTLINES OF CHOHDATE DEVELOPMENT

zone. Some of the retinal layer cells form neuroblasts, and
from these nerve processes (axons) grow out. along the inner
surface of the retina toward the attachment of the optic stalk.
Finally they extend, by way of the margin of the choroid
fissure, into the stalk, from all parts of the retina, and thence
into the wall of the diencephalon (optic thalami) to the' optic
lobes. The consequent thickening of the ventral walls of the
optic stalks forming the optic tracts, leads to the disappearance
of the original cavity of the stalk. The solid stalks or optic
tracts, are commonly known as the // cranial or optic nerves
(Fig. 128).

In the meantime the free inner margins of the choroid
fissure have extended up into the cavity of the optic cup
(posterior chamber), and finally they fuse forming a low ridge,
the whole length of the original fissure, enclosing between
them a bit of mesenchyme which had extended into the fissure
from without. Finally the lips of the fissure fuse together
externally also, and the internal ridge is recognized as the
rudiment of the pecten of the eye. This enlarges rapidly and
ultimately forms a folded, fan-like organ, projecting some
distance upward into the posterior chamber.

The general content of the posterior chamber, known as the
vitreous humor, is formed from the innermost cells of the retinal
and lenticular zones. These cells send out branching processes
through the chamber and later add a secretion, the two materials
together making up the humor.

Just after the rudiment of the lens separates from the
surface ectoderm, its inner wall becomes thickened by the
elongation of its single layer of cells. Finally then* elongation
becomes so marked that the original cavity of the lens vesicle
is obliterated and the lens become solid. The epithelium on
its outer face remains simple. This primary lens vesicle forms
only the nucleus of the final structure, for around this are
laid down, beginning about the eighth day, a large number of
concentric layers of cells, derived from the periphery of the
lens region, where the thin outer lens epithelium becomes con-
tinuous with the thick inner layer. These cells are formed

THE LATER DEVELOPMENT OF THE CHICK 321

irregularly, but finally they assume a definite and regular
arrangement. Layers are formed during the entire growth
period of the organism and the number finally laid down is
very large. At first the lens is in contact with the surface
ectoderm, but it soon moves within the pupil, leaving a space
between itself and the ectoderm. This is the beginning of
the anterior chamber of the eye (Fig. 127, D); it extends beyond
the margin of the iris, and soon becomes invaded by mesen-
chyme cells, part of which are added to the iris; while others
form the larger part of the cornea.

The cornea is only to a slight degree formed by the surface
ectoderm without the iris and pupil; only its superficial epi-
thelium is thus derived. The major portion of the cornea is
derived from mesenchyme cells which first form a single layer
within the ectodermal epithelium (Fig. 127, D), and then later
enter in large numbers between these two epithelia, forming
layers of corneal cells. From the mesenchyme surrounding
the entire optic cup are derived the choroid and sclerotic coats
of the eye-ball.

2. The Ear

Like the eye, the fully formed ear is a complex, formed of
elements of diverse origin, which become morphologically and
functionally associated during development. The ear develops
somewhat later than the eye, in the region of the myelen-
cephalon. Making the customary distinction between the
primary or sensory, and the secondary or accessory portions,
we see that the true sensory portion is formed from the surface
of the head, rather than the wall of the nervous system. The
accessory parts are derived from the hyomandibular visceral
pouch and the mesenchyme of the region.

The first indication of the ear appears about the thirtieth
hour as a circular thickening in the ectoderm on the side of the
head, just in front of the level of the first mesodermal somite.
This patch enlarges, becomes depressed and invaginated, and
about the beginning of the third day it has formed a consider

322 OUTLINES OF CHORDATE DEVELOPMENT

able sac, the auditory sac or otocyst, connected with the surface
by a narrow canal. The otocyst very early becomes vertically
elongated and soon shows internally an oblique ridge on its
inner or medial surface, indicating its division into an upper
and inner part, and a lower and outer part, known respectively
as the superior and inferior chambers. The superior chamber
is extended vertically as a short tube with which the canal
leading to the surface is connected. This tube is the rudiment
of the endolymphatic duct (Fig. 129, A). On account of the
dorsal expansion of the superior chamber along the outer side

i

FIG. 129. — Two stages in the development of the auditory organ of the chick.
A. Hemiseoted model of the auditory sac (otocyst) just before its separation
from the superficial ectoderm of the head. After Krause. B. Median view
of a model of the left membranous labyrinth of an embryo of seven days and seven-
teen hours. After Rothig and Brugsch. a. Anterior vertical semicircular
canal; aa, ampulla of anterior vertical semicircular canal; ap, ampulla of poste-
rior vertical semicircular canal; d, ductus endolymphaticus; e, superficial ecto-
derm of head; I, lagena (cochlea); p, rudiment of posterior vertical semicircular
canal; s, rudiment of saccule; u, utricle; x, connection between auditory sac and
superficial ectoderm.

of the endolymphatic duct, the latter appears to open into
the inner side rather than into the apex of the superior chamber.
The narrow canal of the duct becomes closed during the fifth
day, and the otocyst soon thereafter loses all connection with
the surface ectoderm.

We may now mention the more important steps in the
development of each of these three primary regions of the
otocyst. The endolymphatic duct grows dorsally during the
seventh and eighth days, and its extremity dilates forming the

THE LATER DEVELOPMENT OF THE CHICK 323

endolymphatic sac. This finally extends above the central
nervous system, and lies embedded in the mesenchyme along
the dorso-lateral surface of the myelencephalon.

The superior chamber of the otocyst gives rise to the semi-
circular canals and the utricle. The semicircular canals are in-
dicated the fifth day, as three slight grooves in the wall of the
superior chamber, approximately in the relative positions of the
fully developed canals, save that the posterior canal is at first
oblique to the other two. These grooves deepen and their
margins meet converting them into canals, which remain open
into the chamber at their extremities. The canals push out
from the surface of the otocyst carrying a thin sheet of its
wall which becomes perforated between the body of the superior
chamber and the canals, leaving them free, except at their
attached ends. The cavity of the superior chamber remaining,
after the formation of the semicircular canals, is the utricle; this
receives also the opening of the endolymphatic duct, and
ventrally it opens into the inferior chamber of the otocyst.
The ampullce of the canals appear as dilations very early
(seventh day).

The inferior chamber of the otocyst is the seat of origin of
the saccule and the lagena or cochlea. The saccule appears
(seventh day) as a swelling on the inner or medial wall of the
extreme upper (dorsal) end of the inferior chamber. The
ventral end of this chamber pushes downward as the rudiment
of the lagena or cochlea, while the intermediate region remains
as the cochlear duct. The lagena grows out for some distance,
turning inward (medially) at its tip, forming as a whole a
hook-shaped structure (Fig. 129, B).

The epithelial lining of the otocyst has meanwhile become
thinner, except in certain patches which mark the location of
the maculce, cristce, and papillce of the fully formed ear. In
these regions the epithelium assumes the typical character-
istics of the acustic epithelium, and into each patch there
extend nerve fibers (axons) from the cells of the VIII nerve
ganglion, which is intimately fused with the antero-ventral
face of the otocyst.

324 OUTLINES OF CHOKDATE DEVELOPMENT

The mesenchyme surrounding the otocyst differentiates into
various structures during the development of the otocyst.
First is formed a membranous layer which fuses with the ex-
ternal surface of the complex otocyst and its derivatives,
forming the membranous labyrinth. Surrounding this the
mesenchyme forms a loose tissue which becomes the perilymph,
and around all of this comes finally a dense mesenchyme where
the cartilaginous and later the bony labyrinths are laid down.

We have thus far described only the structures of the internal
ear. It remains now to mention the chief facts regarding the
development of the middle and outer ears. These develop
partly from the pharyngeal cavity, and partly from the region
of the hyomandibular visceral pouch and the surrounding
mesenchyme. The hyomandibular pouch develops in two
parts, a large ventral portion corresponding in general with
the typical gill-pouch, and a smaller dorsal portion (Fig. 130,
B). The former is transitory and disappears without becoming
perforated, while the latter, which is perforated for a short
time only, enlarges and becomes differentiated as a part of the
middle ear or tympanic cavity. The major portion of this
cavity is, however, derived from the cavity of the pharynx
adjoining the dorsal portion of the hyomandibular pouch.
This part of the pharynx becomes incompletely cut off from
the remainder of the pharyngeal cavity by a horizontal shelf or
partition, a narrow slit remaining open in the mid-line. The
narrow pharyngeal space thus formed, and the dorsal portion
of the hyomandibular pouch, enlarge distally, between the
otocyst and the surface of the head, as the rudiment of the
tympanic cavity; the narrow medial portion of the pharyngeal
space becomes the Eustachian tubes, opening into the pharynx
by the slit mentioned.

The mesenchyme of the dorsal wall of the tympanic cavity
becomes differentiated into the two inner auditory ossicles.
The cavity then extends dorsally around either border of this
mesenchymal region, which is thus formed into a stalk contain-
ing the two ossicles and connecting the surface of the head
with the wall of the otocyst (twelve days).

THE LATER DEVELOPMENT OF THE CHICK 325

Meanwhile the external auditory meatus forms, as a depression
on the surface of the head between the dorsal and ventral
portions of the original hyomandibular pouch. This depres-
sion deepens and finally the tympanic cavity meets it; the
membrane separating the two cavities does not perforate, but
remains as the tympanic membrane or- ear-drum. In the in-
terior of this membrane, the mesenchyme which remains be-
tween its outer ectodermal and inner endodermal layers, dif-
ferentiates into the stapes, which comes into relation with the
malleus and incus, already marked out in the mesenchymatous
rod crossing the tympanic cavity.

3. The Olfactory Organ

This develops much later than the eye and ear, a fact which
is possibly correlated with the secondary importance of the
olfactory sense in the birds. Its appearance is made at the
close of the second day, as a pair of circular thickenings in
the superficial ectoderm just anterior to the eyes. These
thickenings are due to the elongation of the epithelial cells and
mark the primary differentiation of the olfactory epithelium.
Each patch soon becomes invaginated, forming an olfactory
pit, which remains open to the surface of the head. Out-
growth of the fore-brain produces an apparent shifting of the
external openings of the olfactory pits to the ventro-lateral
surfaces of the head in the margin of the stomodaBum. The
two pits are separated by a broad ridge, produced by the en-
largement of the fore- brain; this is the fronto-nasal process.
The outer border of the opening of the olfactory pit also
becomes elevated, and about the fifth day becomes joined
with the fronto-nasal process by a bridge of tissue, extending
across the olfactory opening and dividing it into upper and lower
portions. This bridge enlarges as the rudiment of a part of
the upper jaw, and the two openings thus have quite different
fates. The upper is carried outward and upward and forms
the external nares; the lower is carried downward and inward
(relatively) as the internal nares (choance).

326 OUTLINES OF CHORD ATE DEVELOPMENT

The olfactory pit has already begun to deepen before the
division of its external aperture. The true olfactory epithe-
lium, which is distinguished from the adjacent non-sensory
epithelium by the fact that the former remains only one cell
thick, is limited to the deeper part of the pit, so that the olfac-
tory and respiratory portions of the olfactory chamber are
sharply distinguished even in these early stages. During the
fourth to eighth days, the internal nares are carried farther
back by the development of the palate, and the three pairs of
turbinates make their appearance, growing in from the outer or
lateral wall of the chamber. The lower turbinate extends into
the respiratory portion, the middle and upper turbinates into
the olfactory portion; later, however, the epithelium covering
the middle turbinate loses its olfactory character and becomes
like that of the respiratory part.

The true olfactory epithelium contains neuroblasts as well as
ordinary epithelial cells. Superficially the former send out to,
or above, the surface of the epithelium, short processes which
are sensory or receptive in character. These same cells send
out also long processes (axons) which grow into the wall of
the adjacent telencephalon and form the true olfactory nerves.
The sensory epithelium of the olfactory organ is therefore a
neuro-epithelium. The I cranial nerve called the olfactory, is
composed of these fibers.

III. THE ALIMENTARY TRACT AND ITS APPENDAGES

We have already described the formation of the main divisions
of the embryonic gut; these are the fore-gut, with which we
described the pharynx and oral plate, the hind-gut with the
postanal gut, and the mid-gut connecting with the splanchnic
stalk. We shall now review the early development of the
various regions of the tract and of the appendages or derivatives
of each portion.

1. Organs of the Fore-gut

We left the fore-gut, at the thirtieth hour, as the short but
wide cavity of the head-fold, extending from the oral plate

THE LATER DEVELOPMENT OF THE CHICK 327

to the anterior intestinal portal (Fig. 99). Later we have seen
that, through the process of folding the embryo off the yolk,
the splanchnopleural gut is rapidly extended posteriorly from
the fore-gut and anteriorly from the hind-gut, and is closed
in entirely, save where it communicates with the yolk-sac by
way of the splanchnic stalk. That part of the gut which is thus
formed primarily by the approach of the lateral embryonic folds
is distinguished as the mid-gut, the definitive fore- and hind-
gut being formed primarily by the head- and tail-folds. Em-
bryologically the fore- and hind-gut are more important than
the mid-gut, for in connection with these regions develop all
of the important appendages of the alimentary tract.

In connection with the fore-gut we have to describe the for-
mation of the pharynx and visceral arches and pouches, the
thyroid, the thymus and post-branchial bodies, the whole res-
piratory tract, the oesophagus and stomach, the liver, and the
pancreas; in addition we must include the stomodseum and the
structures derived from it, the hypophysis and the organs of the
buccal cavity.

The stomodceum is an ectodermally lined depression on the
lower side of the head; the oral plate is at its bottom (Figs.
99, 123, A). The depth of the stomodseum is increased by the
formation and growth of the jaws. As previously noted, the
oral plate becomes perforated during the third day and then
gradually disappears, the stomodaBum itself, however, is the
seat of several important organs. The hypophysis appears
about the forty-fourth hour, as an elongated evagination from
its mid-dorsal wall, just in front of the oral plate (Fig. 123).
It grows directly toward the ventral surface of the diencephalon,
in the region of the infundibulum, which it reaches at about
the beginning of the third day. Later it becomes glandular,
loses its connection with the epithelium of the stomodaBum and
joins with the infundibulum to form the glandular portion of
the pituitary body.

The cavity of the stomoda3um and the future buccal cavity
are practically coincident, whether precisely or not can hardly
be said, on account of the disappearance of the oral plate

328 OUTLINES OF CHORDATE DEVELOPMENT

before the formation of any other landmark. The maxillary
and mandibular arches, whose formation is described below,
extend forward, around the sides of the stomodaeum forming
the rudiments of the jaws; the buccal cavity is considerably
enlarged by their formation and their enlargement as the beak.
An incomplete palate is formed later, above which the pharyn-
geal cavity extends. On the upper surface of the beak is
formed a superficial horny egg-tooth, which is used in perforat-
ing the shell and shell membrane at the close of incubation;
and on the margins of the jaws slight, transitory ridges appear,
representing the vestiges of the enamel organ — all that there
is left of the true teeth of other vertebrates. Although the
tongue extends forward into the buccal cavity, it is really a
pharyngeal derivative.

The pharynx is the most complicated region of the em-
bryonic gut. On account of the obliquity of the oral plate,
the antero-dorsal portion of the pharynx may be described as
pre-oral; this region is known as SeesseWs pouch, but when the
oral plate disappears this is indistinguishable (Figs. 123, A;
130). We have already described, in connection with the ear,
the separation of this antero-dorsal portion of the pharynx as
the rudiment of a part of the tympanic cavity and the Eusta-
chian tubes, which open into the pharynx through a median
fissure in the palate, the tubal fissure.

Beginning the second day there grow out from the walls of
the wide pharynx toward the surface of the head, a series of
paired, vertically elongated pouches, the visceral pouches (Fig.
130). Of these there are four pairs, diminishing in size and
importance posteriorly. The first and largest is the hyoman-
dibular pouch, the other three are the branchial or gill-pouches,
the last of which is very feebly developed. These visceral
pouches, containing extensions of the pharyngeal cavity, push
out to the surface ectoderm with which they fuse intimately,
dividing the body wall of the region into a series of vertical
sections between them; these are the visceral arches. The
visceral arches are composed chiefly of mesenchyme, in which
develop later the aortic arches and the cartilaginous visceral

THE LATER DEVELOPMENT OF THE CHICK- 329

ic

ao

FIG. 130. — Models of the pharynx and associated structures in the chick.
After Kastchenko. A. Ventro-lateral view of pharynx at the beginning of the
third day. B. Lateral view of the pharynx and associated nervous and vascular
structures, at the end of the third day. Nervous structures are left unshaded;
arteries in solid black; veins lightly stippled; pharyngeal structures darkly
stippled, a. Auditory sac; aa, aortic arches; ao, dorsal aorta; cf, choroid fissure;
cv, posterior cardinal vein; dC, ductus Cuvieri; ej, external jugular vein; gV,
Gasserian ganglion of V cranial nerve; gVII, geniculate ganglion of VII cranial
nerve; gVIII, acustic ganglion of VIII cranial nerve; glX, ganglion petrosum
of IX cranial nerve; gX, ganglion nodosum of X cranial nerve; h, hypophysis;
ic, internal carotid artery; j, internal jugular vein; I, rudiment of larynx; o, oral
evagination of fore-gut; oe,oesophagus; op, optic vesicle enclosing lens; p, pulmon-
ary artery; pIX, placode of IX cranial nerve; pX, placode of X cranial nerve;
s, stomach; S, Seessel's pocket (preoral gut); st, stomodaeum; t, rudiment of
trachea; 1-4, first to fourth visceral pouches (or their ventral portions, in B) ;
Id, 2d, dorsal portions of first and second visceral pouches; IX, glossopharyngeal
nerve; X, vagus nerve; XI, hypoglossal nerve.

330 OUTLINES OF CHORD ATE DEVELOPMENT

arches; each is covered externally by ectoderm, and internally
and laterally by endoderm. Five visceral arches are thus
marked out. The first is in front of the hyomandibular pouch,
between this and the mouth, and is known as the mandibular
arch. The second, or hyoid arch, lies between the hyoman-
dibular and the second visceral pouches, while the remaining
three branchial arches (third to fifth visceral arches) lie pos-
terior to the second, third, and fourth visceral pouches. Like
the pouches these diminish in size and importance posteriorly,
the last (fifth) being only a slight and transitory vestige.

The vertical fusions of ectoderm and endoderm along the
outer borders of the visceral pouches are interrupted just below
the upper ends of the pouches, so that dorsal and ventral
portions of each fusion are to be distinguished (Fig. 130, B).
The surface of the head becomes depressed in the lines of fusion,
so that a series of vertical grooves marks externally the dis-
position of the visceral arches and pouches.

The second visceral pouch (first branchial) is the best de-
veloped, and about the end of the second day both upper and
lower fusions are perforated as the vestiges of a gill cleft; these
perforations close during the fourth day without leaving any
trace. In the third pouch a gill cleft is similarly formed and
closed a little later. In the first pouch (hyomandibular) only
the dorsal fusion is perforated (spiracular cleft) shortly before
the perforation of the second pouch. No cleft appears in the
fourth pouch, only the dorsal portion of which fuses with the
ectoderm.

After the fourth day the visceral pouches become reduced.
The first undergoes a change in function and takes an essential
part in the formation of the tympanic cavity, as described
above. For the most part the other visceral pouches finally
disappear, but from parts of their epithelial walls the thymus
and the post-branchial bodies are derived. The thymus is
chiefly derived from part of the dorsal epithelium of the third
visceral pouch, but the fourth contributes to a small extent.
A transitory anterior portion of the thymus is derived
from the epithelium of the second pouch. The thymus be-

THE LATER DEVELOPMENT OF THE CHICK 331

comes a very considerable embryonic structure, extending
finally throughout the neck region. The post-branchial bodies
are epithelial buds connected with the fourth visceral pouches,
They are to be regarded as vestiges of a fifth pair of visceral
pouches and are thus serially homologous with the thymus
elements (Fig. 131).

The thyroid body also arises in connection with this part of
the pharynx. This appears during the middle of the second

FIG. 131. — Derivatives of the visceral pouches and associated organs, in the
chick. From Lillie (Development of the Chick). After Verdun (Maurer).
Combined from frontal sections. A. In embryo of seven days. B. In embryo
of eight days. Ep.3, EpA. Epithelioid bodies derived from third and fourth
visceral pouches; J, jugular vein; p'br., p'br. (V)., postbranchial bodies derived
from fifth visceral pouch; Ph., pharynx; Th.3., ThA., thymus bodies derived
from third and fourth visceral pouches; T'r., thyroid body; ///, IV, third and
fourth visceral clefts.

day as a thickened patch of cells in the floor of the pharynx,
between the lower ends of the second visceral pouches. This
plate of cells evaginates toward the close of the second day
(Fig. 123), and soon appears as an entirely closed sac below the
pharynx. Later (seventh day) it divides into a pair of vesicles
which enlarge and migrate a short distance posteriorly.

Finally we must describe, as an appendage of the pharynx,
the pulmonary tract. For a short distance behind the branchial
region the pharynx becomes narrower and is deepened by the
formation, late the second day, of a ventral groove (Fig. 130,

332 OUTLINES OF CHORDATE DEVELOPMENT

A). This groove is the beginning of the whole pulmonary
system. The depression becomes well marked early the third
day as the laryhgo-tracheal groove, and its posterior end
expands transversely forming the rudiments of the lungs. The
groove then becomes cut off from the pharyngeal cavity as 'the
rudiment of the trachea, remaining open out of the pharynx
only at its anterior end; this opening is the glottis, behind which
the larynx develops later. From the eighth to the eleventh
days the glottis and larynx are obstructed by a cell mass, and
the glottis itself remains closed for some time longer.

Just in front of the glottis, in fact both immediately behind
and in front of the thyroid rudiment, the floor of the pharynx is
elevated (fourth day), the two papillae thus formed representing
the beginning of the tongue. As these rudiments enlarge they
fuse together, the thyroid having been cut off meanwhile, and
grow forward into the buccal cavity, finally extending nearly to
the tip of the jaws.

The bifurcated posterior extremity of the laryngo-tracheal
groove or lung rudiment, grows backward through the sur-
roupding mesenchyme; the tubes thus formed are the rudiments
of the bronchi. By a sort of budding process they form the
bronchioles and terminal alveoli of the lung proper. The meso-
dermal parts of the entire pulmonary tract are derived from the
splanchnic mesoderm of the primary gut-wall. The air-sacs
are also formed from terminal dilations of branches of the
bronchial tubes.

Passing backward from the pharynx the gut is considerably
narrowed for a short distance as the cesophagus, but it soon
expands again as the rudiment of the stomach (third day).
Before these organs are differentiated, however, the liver
appears. This makes its appearance toward the close of the
second day, in the region where the fore-gut is at that time
open by the anterior intestinal portal, i.e., just back of the
future posterior limit of the stomach. Here two evaginations
of the ventral wall of the gut, or portal, push out, one above
the other in the mid-line ; they extend forward as pouch-like out-
growths, through the mesoderm of the ventral mesentery, below

THE LATER DEVELOPMENT OF THE CHICK 333

the stomach region. This is the region where the great veins
are converging toward the heart (ductus venosus, ductus
Cuvieri, see below). The anterior liver diverticulum appears
some hours before the posterior, and as it grows forward it lies
to the left, the later posterior diverticulum then extends
rather toward the right side, and although it becomes the
larger, it does not grow as far forward as the anterior diver-
ticulum. During the third and fourth days both diverticula
branch and anastomose, forming a network of liver tissue
(Fig. 123, B) around the large vein (ductus venosus). The
liver soon enlarges enormously and early becomes very vas-
cular, through the development of vessels connecting with
the ductus venosus, directly among the meshes of the liver
substance.

The bile duct and gall-bladder arise from the short ventral
region of the gut between the two liver diverticula; this re-
gion grows out carrying with it the openings of the diverticula,
which thus come to open into a common chamber, the ductus
choledochus or common bile duct. The gall-bladder develops
in connection with the duct of the posterior liver diverticulum.
The common bile duct is a transitory structure, and when it
disappears the two liver (bile) ducts again open separately into
the gut.

About the same time and in the same general region as the
liver, the pancreas develops, from three separate diverticula. A
dorsal median diverticulum grows out, directly opposite the pos-
terior liver diverticulum, about the end of the third day. Right
and left ventral pancreatic diverticula appear later, pushing
out from the walls of the ductus choledochus close to the gut-
wall. When the ductus choledochus disappears these pan-
creatic rudiments open separately into the gut. As these
diverticula enlarge they branch distally and by a budding proc-
ess form the glandular units of the organ. The bodies of the
three rudiments finally join, forming a common gland, al-
though their ducts remain opening separately near the two
bile ducts.

334 OUTLINES OF CHORDATE DEVELOPMENT

2. Organs of the Hind-gut

Embryologically the most important appendage of the hind-
gut is the allantois. In describing the formation of this organ
we mentioned the essential steps in the establishment of the
hind-gut itself, and described the formation of the postanal gut
and the beginning of the cloaca (Figs. 120, 121). On the ventral
side of the hind-gut, between the outgrowing allantois and the
base of the tail the ectoderm becomes pitted in toward the
cloaca forming the proctodceum. The ectodermal epithelium
of the proctodaeum fuses with the endodermal lining of the
cloaca forming the anal plate. This was originally toward the
dorsal surface of the embryo, but was pushed into a ventral
position by the formation and growth of the tail-bud (Fig. 121).

The cloaca becomes a deep but narrow cavity; it receives,
antero-dorsally, the opening of the terminal portion of the
intestine, and the allantoic stalk connects antero-ventrally.
Laterally, either side of the rectal opening, the urinogenital
ducts discharge into the cloaca. During the fifth and sixth
days the postero-ventral portion of the cloaca is temporarily
closed by the fusion of its walls. The cavity which re-forms
here is the rudiment of the bursa Fabricii, which acquires an
opening directly into the proctodseum just outside the anal
plate. Thus the embryonic cloaca gives rise chiefly to that
part of the adult cloaca into which the urinary and genital
ducts open. The anal plate finally becomes perforated early in
the third week of incubation.

3. The Mid-gut

The embryonic mid-gut gives rise to the intestinal tract ex-
tending from the hepatic and pancreatic diverticula to the cloaca.
Its establishment through the approach and fusion of the
lateral splanchnopleural folds has been described in the pre-
ceding chapter. 'It remains open by the splanchnic stalk to
the yolk-sac until toward the close of the embryonic period
(see above).

THE LATER DEVELOPMENT OF THE CHICK 335

Although really derived from the embryonic fore-gut, we
may include here certain details in the later development of
of the oesophagus and stomach, the formation of which was
mentioned above. The stomach and intestine extend through
the body cavity, from the dorsal wall of which they are suspended
by a double mesodermal fold, the dorsal mesentery and meso-
gastrium, which represents the original dorsal fusion of the lateral
splanchnopleural folds involved in the establishment of the
intestinal groove and tube. The similarly formed ventral

FIG. 132.— Partially dissected viscera of the chick, from the right side.
After Duval. A. Of a six-day chick, enlarged slightly less than six times.
B. Of a thirteen day chick, enlarged two and one-half times, showing the elon-
gated intestine and its extension into the umbilical stalk, a, Right auricle; aZ,
allantois; as, abdominal air sac; 6, bulbus arteriosus; c, caecal processes; d, loop
of duodenum; dj, duodenal-jejunal flexure (a relatively fixed point during the
elongation of the intestine) ; /, fore-limb bud (cut through) ; g, gizzard; go, gonad ;
A, hind-limb bud (cut through) ; i, loops of small intestine; I, liver; Ig, lung; II,
left lobe of liver; h, left ventricle; M, rudiment of Miillerian duct (tubal ridge) ;
p, pancreas; r, rectum; rl, right lobe of liver; rv, right ventricle; s, yolk stalk;
u, umbilical stalk; W, Wolffian body or mesonephros.

mesentery disappears immediately after its formation, save in
the region of the stomach and liver, where it forms the gastro-
hepatic ligament.

The oesophagus elongates with the neck, and during the
seventh to eleventh days is closed just back of the glottis by
cells proliferated from its wall. The crop appears as a posterior
dilation of the oesophagus just in front of the stomach. During
the fifth to seventh days the enlarging stomach becomes differ-

336 OUTLINES OF CHORD ATE DEVELOPMENT

entiated into the anterior proventriculus, with thick glandular
walls, and the posterior gizzard, with its thick muscular coats.
The horny lining of the gizzard is derived from the secretion of
specific glands in its own wall.

Beginning the third or fourth day of incubation the mid-gut,
including the stomach, commences to elongate, and as a result
the tract becomes first simply looped, and then complexly
folded (Fig. 132). First the stomach bends to the right, return-
ing to the median region near its opening into the intestine.
The first section of the intestine is the duodenum; this is a very
short section, receiving the ducts of the liver and pancreas.
The duodenum elongates very little and remains as a relatively
fixed region, closely attached to the dorsal body wall. Simi-
larly the terminal portion of the intestine, the rectum and large
intestine, elongates only slightly. Between the duodenum
and the large intestine the jejunum or vitelline portion of the
small intestine elongates considerably, and is consequently
thrown first into an S-shape. The yolk-sac connects with the
apex of the lower loop (Fig. 132). Later this whole section
shows secondary loops or twistings along each primary loop.
At the connection of the small and large intestines the two
intestinal cceca grow out during the second week.

IV. THE VASCULAR SYSTEM

The formation of the vascular system and its development up
to the thirtieth hour, we have already described; and we have
also mentioned the important steps in the development of the
extra-embryonic circulation (yolk-sac and allantois). We
must now trace the important steps in the development of the
true embryonic circulation, from the stage where we left it.
Let us recall that we left the heart as a bent tube, suspended in
the pericardial cavity; anteriorly it leads, by way of the first
or mandibular pair of aortic arches, into the dorsal aorta, the
chief branches of which (vitelline arteries) supply the extra-
embryonic organs. The embryonic venous system at that
time consisted only of the roots of the vitelline veins, returning

THE LATER DEVELOPMENT OF THE CHICK 337

the blood from the yolk-sac and opening directly into the pos-
terior end of the heart. The main vessels of the yolk-sac and
allantois are described in the preceding chapter, and we shall
need to add little to those accounts of the extra-embryonic
circulation.

1. The Heart

The sharp bending of the heart to the right divides it
roughly into anterior and posterior limbs (Fig. 133, A), and as
it continues to elongate an additional loop appears, directed
posteriorly from near the apex of the original loop. The entire
structure then swings underneath the pharynx and the loops
become less widely spread out (Fig. 133, B). The extent of the
heart is increased posteriorly by the addition of a region formed
by the fusion of the roots of the paired lateral vitelline or
omphalomesenteric veins; the chamber thus formed is the sinus
venosu's. •.

During the third day certain constrictions appear, dividing
the tube intd its primary chambers, and each of these shows
characteristic modifications in form, so that by the end of the
third day the following regions are distinctly marked. The
sinus venosus } formed by the confluence of the omphalomes-
enteric veins, is a wide triangular fc£vity with thin walls; it
receives also the embryonic veins, the duefrus venosus and the
paired ductus Cuvieri (see below). Its a^ex is anterior,
where it opens into the atrium or auricle bythe sinu-auricular
aperture; this opens into the postero-dorsal region of the auricle.
The auricle is formed from the originally posterior loop of the
heart tube, now dorsal in position. The auricle already shows
signs of its future division in that it is laterally expanded; the
sinus venosus is more directly connected with its right side and
its left side extends forward nearly to the limit of the peri-
cardial cavity. The wall of the auricle remains thin like that
of the sinus venosus; its cavity opens downward into the
dorsal region of the ventricle.

The ventricle is formed essentially from the secondary pos-

338 OUTLINES OF CHORDATE DEVELOPMENT

terior loop of the heart tube, and is now separated from the
auricle by the narrowed auriculo-ventricular aperture (Fig. 133).,
The ventricle occupies the ventral region of the pericardial

lit

FIG. 133. — The development in the heart of the chick. A, F, after Hoch-
stetter; B-E, after Greil. A-E, ventral views of the heart; A, of a forty-hour
embryo; B, of a 2.1 mm. embryo; C, of a 3.0 mm. embryo; D, of a 5.0 mm.
embryo; E, of a 6.5 mm. embryo. F. Frontal section through the heart of a 9
mm. embryo, a, Auricle; b, bulbus; d, roots of dorsal aorta; e, median endothelial
cushion; i, interventricular groove; la, left auricle; le, lateral endothelial cushion;
lv, left ventricle; om, vitelline artery; p, left pulmonary artery; ra, right auricle;
rv, right ventricle; s, interventricular septum, sa, interauricular septum; t,
roots of aortic arches; v, ventricle.

cavity beneath the auricle. The walls are already thickened
and spongy. Anteriorly a slight constriction separates the

THE LATER DEVELOPMENT OF THE CHICK 339

ventricle -from the bulbus arteriosus, the most anterior chamber
of the heart, formed from the anterior loop of the original heart
tube and now passing obliquely upward to the antero-dorsal
wall of the pericardial cavity, where it connects with the truncus
arteriosus in the floor of the pharynx. The wall of the bulbus is
also much thickened at this time.

Long before the end of the third day the heart is beating regu-
larly and rapidly. Its first irregular twitching begins toward
the middle of the second day and before the end of this day its
contraction becomes quite regular.

The later development of the heart may be sketched only
roughly. There are further changes in the position of the heart,
as the net result of which the ventricle assumes a posterior, and
the auricles an antero-dorsal, location; the auricles also grow
ventrally around the bulbus, which finally occupies a median
ventral position.

The bulbus arteriosus finally loses its identity as a separate
chamber. Three semilunar valves develop, about in its middle,
and its anterior section then becomes transformed into the proxi-
mal parts of the truncus arteriosus (finally the root of the dorsal
aorta) and the pulmonary artery, while its posterior section is
absorbed into the ventricles. Similarly the sinus venosus be-
comes incorporated into the right auricle, and the sinu-auric-
ular valves, which had developed from the wall of the sinu-
auricular aperture, entirely disappear. Thus of the original
four chambers of the heart only two remain separate. The
cavities of these two chambers, the auricle and ventricle, then
become secondarily divided longitudinally, so that the heart
may again be described as four-parted, though in a very
different sense.

From the postero-dorsal wall of the auricle, between the open-
ings of the sinus venosus and the pulmonary vein (see below) a
thin partition grows downward and forward, during the fourth
day, and soon reaches a thickened cushion of cells lying on the
upper and lower sides of the auriculo-ventricular aperture, thus
completely dividing the primary auricular cavity into right and
left cavities (Fig. 133, F). This interauricular septum early

340 OUTLINES OF CHORDATE DEVELOPMENT

becomes fenestrated and is not completely re-formed until after
hatching. At the same time the ventricle is becoming divided
into right and left portions by an interventricular septum.
This commences as an extension of the spongy wall of the ven-
tricle near its posterior apex; it becomes a thick partition,
rapidly extends anteriorly, meeting and fusing with the cushion
of the' auriculo- ventricular aperture, with which the interauricu-
lar septum has already connected. Finally the division of
the ventricle is completed save for a small antero- ventral aper-
ture, the interventricular foramen, by which the root of the
dorsal aorta later connects with the left ventricle.

The bulbus arteriosus too becomes divided before its fusion
with th3 ventricle, by a partition extending from the anterior
margin of the pulmonary aortic arch (see below) back to the
ventricles. The effect of this is to connect the pulmonary
aortic arches with the right ventricle and the systemic aortic
arch with the left ventricle. When this bulbus region is ab-
sorbed, as described above, the pulmonary arteries and the
dorsal aorta arise directly from the right and left ventricles,
respectively, and the separate blood streams are established.

2. The Aortic Arches and the Arterial System

At the thirtieth hour the heart is connected with the dorsal
aorta by a single pair of aortic arches running through the first
or mandibular visceral arch. Later an aortic arch forms in each
visceral arch, connecting the truncus arteriosus or ventral
aorta with the lateral dorsal aortas. The second or hyoid
aortic arch forms during the latter part of the second day and at
the end of that day the third aortic arch is completed. The
fourth is formed by the end of the third day and during the
fourth and fifth days fifth and sixth aortic arches are formed in
the tissues posterior to the last (fourth) visceral pouch (Fig. 134,
A ) . Of these arches the fourth and sixth are the best developed,
while the fifth is present only as a transitory and incompletely
developed vestige.

This embryonic aortic arch system is converted into the adult

THE LATER DEVELOPMENT OF THE CHICK 341

condition chiefly by a series of degenerations. During the
third and fourth days the first (mandibular) and second (hyoid)
arches disappear, leaving only their continuous ventral roots
as the root of the external carotid artery. The lateral dorsal
aortaB have meanwhile continued forward, as the internal ca-
rotid arteries, supplying the brain and other organs of the head.
These parts of the lateral dorsal aortae become separated, dur-
ing the sixth and seventh days from the remainder of the lateral
dorsal aortse by an interruption in these vessels just back of the
dorsal attachment of the third aortic arch; thus the internal
carotid arteries arise only from the third aortic arch, which is
consequently known as the carotid arch (Fig. 134, B). The

J^f^L^

A™- /*

FIG. 134. — Aortic arches of the chick. From Lillie (Development of the
Chick), A, after Locy. A. Of the left side of a chick of four and one-half days;
from an injection. B. Reconstruction from sagittal sections of an eight-day
embryo. Ao. A. Arch of the aorta (systemic arch) ; A.o.m., vitelline artery; Car.,
carotid artery; Car. ext., external carotid artery; Car. int., internal carotid artery;
D.a., ductus arteriosus; d.Ao., dorsal aorta; p.A., pulmonary artery; S'cL, sub-
clavian artery; 3-6, third to sixth aortic arches (first to fourth branchial aortic
arches).

ventral roots of the first and second arches (external carotids)
remain as branches from the bases of the carotid arch (roots of
the third arches), supplying the mandibular region.

The fourth, or systemic arch, is at first symmetrically devel-
oped like the others, but during the fifth and sixth days it
becomes reduced on the left side and correspondingly enlarged
on the right. Finally the left systemic arch wholly disappears,
and the anterior part of the left division of the truncus remains
only as the stem of the left carotid artery. Meanwhile, it will
be recalled, the right side of the truncus has connected with the

342 OUTLINES OF CHORDATE DEVELOPMENT

Concern

Au

left ventricle alone, so that the blood from this side of the heart
is now carried by the third arches to the carotids, and by the
right systemic or fourth arch to the general dorsal aorta.

The fifth aortic arches having already disappeared, .only the
sixth is left connecting now with the right ventricle. The
sixth arches ultimately form the roots of the pulmonary arteries,

but throughout embryonic
life they remain, on each
side connected with the
roots of the definitive dor-
sal aorta. The true pul-
monary arteries are small
vessels passing backward
from the upper ends of the
sixth or pulmonary arches
(Fig. 134). That part of
each arch between the
origin of the pulmonary
artery and the dorsal aorta
is known as the ductus
Botalli, and shortly after
hatching the two ductus
Botalli become closed as
strands of connective tissue,
turning the whole of the
blood stream of these

FIG. 135.— The heart and aortic arches flrrV,pS rominp1 from the
of a chick embryo the latter part of the aT< QS\

sixth day. From a dissection. From right side of the heart, into
Lillie (Development of the Chick) after , , ,u-^~

Sabin. Au. Auricles; Car. com., common tne pulmonary arteries,
carotid artery; S'cl.d., S.cl.s., primary and Thereupon the dorsal re-
secondary subclavian arteries; 3, 4, 6, third L

(carotid), fourth (systemic), and sixth mainder of the left lateral

(pulmonary) aortic arches. dorgal ^^ disappears and

leaves the dorsal aorta connected with the heart only by the
right systemic arch (Fig. 135).

Certain branches of the aortic arches and dorsal aorta deserve
a special word. The dorsal aorta gives off segment al branches
between the somites, known as the segmental arteries (Fig. 109,

d.Ao.

THE LATER DEVELOPMENT OF THE CHICK 343

B). Some of these become enlarged as the roots of the arteries
supplying the limbs, the subclavian and sciatic arteries. A
branch from the carotid artery grows out and connects with
the subclavian, finally forming its true root, its original root
from the aorta disappearing about the ninth day. The sciatic
artery gives off branches, the umbilical arteries, supplying the
allantois; the right umbilical artery is the smaller and finally
disappears.

During embryonic life the chief branches of the dorsal aorta,
and really those first formed, are the pair of large omphalo-
mesenteric or vitelline arteries, distributed to the yolk-sac by
way of the splanchnic stalk. The proximal parts of these be-
come fused as a single vessel from the base of which is derived
the anterior mesenteric artery. The posterior mesenteric and
coeliac arteries are derived directly from the dorsal aorta. The
dorsal aorta also gives off a series of small twigs supplying the
excretory organs, certain of which enlarge forming the renal
and genital arteries (Fig. 138).

3. The Venous System

We have thus far described only the veins of the extra-
embryonic circulation, for at the thirtieth hour the embryonic
veins are not developed. It will not be necessary to add any-
thing regarding the strictly extra-embryonic portions of these
vessels, but their intra-embryonic terminations take an im-
portant part in the formation of the definitive embryonic
circulation.

The first embryonic veins to appear, about the middle and
latter part of the second day, are the anterior cardinal veins.
Coming from the brain they extend along its ventro-lateral
walls, beneath the auditory sacs, receiving as they pass, branches
from the general head region, including the three anterior
somites. Just back of the head they also receive later, branches
from the floor of the pharynx (external jugular veins); the
anterior cardinals themselves become known as the internal
jugular veins. The proximal parts of the anterior cardinal

344 OUTLINES OF CHORDATE DEVELOPMENT

veins are considerably enlarged as the ductus Cuvieri, which
turn inward and downward and pass into the sinus venosus
(Fig. 137).

From the upper end of each ductus Cuvieri an outgrowth
extends posteriorly as the rudiment of the posterior cardinal
vein, which passes along the Wolffian duct (see below), finally
reaching nearly to the base of the tail. The posterior cardinal
veins receive the intersomitic or intersegmental veins, except
the first three, and the vessels of the nephros (mesonephros, see
below). The veins of the fore-limbs also discharge into the
posterior cardinals near the ductus Cuvieri. The anterior
and posterior cardinal veins are consequently the chief somatic
veins of the early embryo, and it should be noted that all of
the somatic veins connect with the heart by way of the ductus
Cuvieri.

The splanchnic veins of the digestive tract and its appendages
are primarily related with the intra-embryonic portions of the
great veins of the yol£-sac, the omphalomesenteric veins. We
have already seen how the proximal ends of these veins unite
to form the sinus venosus; they continue to fuse posterior to the
sinus venosus, and form thus the ductus venosus, around which,
as we have seen, the liver develops. The ductus venosus and
the ductus Cuvieri are the only vessels emptying directly into
the heart, until the time when the pulmonary veins appear.
The omphalomesenteric veins, entering the embryo, pass across
the body cavity to the mid-line, beneath the gut and between
the two liver diverticula.

It should be noted here that between each omphalomesenteric
vein and the dorsal body wall an extensive fusion occurs, form-
ing an incomplete oblique partition through that part of the
body cavity immediately posterior to the heart. These fusions
are known as the lateral mesocardia, and they are of considerable
importance in the later history of the cavities of the body (Fig.
139). The ductus Cuvieri pass from the dorsal body wall to
the sinus venosus through the anterior parts of the lateral
mesocardia.

Posterior to the ductus venosus the two omDhalomesenteric

THE LATER DEVELOPMENT OF THE CHICK 345

or lateral vitelline veins anastomose, at about the age of three
days, on the dorsal side of the intestine, posterior to the pan-
creatic rudiment (Fig. 136). Thereupon the base of the left

ul

FIG. 136. — Diagrams illustrating the formation of the omphalomesenteric
and umbilical veins, in the chick. After Hochstetter. A. At about fifty-eight
hours. B. At about sixty-five hours. Veins joined dorsal to the gut. C.
At about seventy-five hours. Veins again separate. D. At about eighty hours.
Secondary union of veins around the gut. E. At about one hundred hours.
Definitive arrangement of the vessels, c. Vena cava posterior (inferior) ; dC,
ductus Cuvieri; dv, ductus venosus; g, gut; hi, left hepatic vein; hr, right hepatic
vein; Z, liver; o, omphalo-mesenteric vein; p, anterior intestinal portal ; pa, rudi-
ment of pancreas; ul, left umbilical vein; ur, right umbilical vein; v, vitelline
vein; I, II, primary and secondary venous rings around the gut.

vein rapidly disappears, so that during the fourth day all of
the blood from the yolk-sac is returned to the heart by the right
vein, for it will be recalled that the original or anterior vitelline
veins have previously fused and connected with the right

346 OUTLINES OF CHORDATE DEVELOPMENT

omphalomesenteric vein; and now a large vein coming directly
from the posterior part of the yolk-sac similarly opens into the
same trunk.

By the end of the fourth day the two omphalomesenteric
veins again anastomose still farther back, and now the inter-
mediate portion of the right vein disappears. The embryonic
course of the omphalomesenteric veins may therefore be de-
scribed as follows (Fig. 136) ; they enter the body symmetrically,
passing directly to the ventral side of the intestine just in front
of the anterior intestinal portal; here they fuse into a single
vessel which passes anteriorly around the left side of the intes-
tine to its dorsal surface and thence across to the right side,
where it enters the liver.

This portion of the omphalomesenteric vein becomes the
trunk of the hepatic portal vein in the following manner. As
the vein passes through the liver to the ductus venosus, which
is now embedded in it, it branches abundantly supplying the
vascular spaces of the liver tissue, and soon the strands of liver
cells push into the large vessel so that it becomes entirely
broken up into small vessels and capillaries in the liver. The
ductus venosus then remains as the efferent vessel, or hepatic
vein, while the base of the omphalomesenteric vein itself be
comes the afferent hepatic vessel, the hepatic portal vein. This
arrangement is practically completed during the sixth day.
Before this time the veins of the digestive tract appear; these
collect into the mesenteric vein, which becomes the chief branch
of the hepatic portal. A typical subintestinal vein is indicated
the fourth day, coming from the tail and connecting with the
left omphalomesenteric vein; it soon disappears without taking
an essential part in the formation of any permanent venous
structure.

Veins of considerable phyletic importance are the umbilical
veins, which represent the lateral veins of the Elasmobranchs
and the abdominal vein of the Amphibia. These appear early
in the body wall, primarily as the veins of the limb-buds, open-
ing into the ductus Cuvieri (Fig. 137). During the fourth day
they connect with the veins of the allantois, and shortly there-

THE LATER DEVELOPMENT OF THE CHICK 347

after the right vein disappears, while proximally the connection
of the left vein with the ductus Cuvieri is lost, and this vessel
acquires a new connection with the intra-hepatic vessels and
ductus venosus. Through this pathway the veins of the
allantois then connect with the embryonic circulation.

The largest venous trunk of the fowl is the inferior vena cava
or postcaval vein. As in other forms, this vein is in part an

FIG. 137. — Injected chick embryo of the third day, showing the arrangement
of the cardinal veins and the formation of the umbilical vein from capillary
networks. From Evans. A.C.V., Anterior cardinal vein; P.C.V., posterior
cardinal vein; U.V., umbilical vein.

independent formation, and in part formed from the posterior
cardinal system. The first part of the vena cava appears
during the fourth day as a posterior outgrowth of the ductus
venosus, which connects with a series of venous spaces in the
dorsal wall of the liver, on the right side (Fig. 136). Soon this

348 OUTLINES OF CHORDATE DEVELOPMENT

vein connects with the right posterior cardinal vein. The
posterior cardinal veins pass along the dorsal side of the kid-
neys (mesonephroi, see below) receiving their vessels. But
during the fourth day a system of venous spaces appears on the
ventral side of the kidney; these vessels are known as the sub-
cardinal veins (Fig. 138). During the sixth day the inferior

pc dv

8V *t v

^^^€^ LJH^Vwa v a ™ -
aJ

FIG. 138. — Diagrammatic lateral view of the chief embryonic blood-vessels
of the chick, during the sixth day. After Lillie. a. Auricle; al, allantoic stalk;
ao, dorsal aorta; c, cceliac artery; ca, caudal artery; cl, cloaca; cv, caudal vein;
da, ductus arteriosus; dv, ductus venosus; ec, external carotid artery; ej, external
jugular vein; i, intestine; ic, internal carotid artery; ij, internal jugular vein;
I, liver; ra, mesonephros; ma, mesenteric artery; mv, mesenteric vein; p, pulmonary
artery; pc, posterior cardinal vein; pv, pulmonary vein; s, sciatic artery; sc,
subclavian artery; SCT, subclavian vein; st, yolk-stalk; sv, subcardinal vein;
ul, left umbilical artery; ur, right umbilical artery; uv, left umbilical vein; v,
ventricle; va, vitelline artery; vca, anterior vena cava (anterior cardinal vein);
vp, posterior vena cava; vv, vitelline vein; y, yolk-sac; 3, 4, 6, third, fourth, and
sixth aortic arches.

vena cava connects with the right subcardinal vein, the two
subcardinal veins anastomose posterior to this connection, and
the anterior parts of both posterior cardinal veins disappear.
The net result of these changes is that the hinder parts of the
posterior cardinals form the afferent renal trunks or renal portal
veins, the subcardinals form the efferent renal vessels leading into
the inferior vena cava, through which all of the blood from the
embryonic kidneys (mesonephroi) is returned directly to the

THE LATER DEVELOPMENT OF THE CHICK 349

heart. This arrangement continues until this embryonic
kidney is replaced by the definitive kidney of the adult (meta-
nephros), when the posterior cardinal veins, then the renal
veins, connect directly with the subcardinal veins and the vena
cava, and the renal portal system disappears. The subclavian
veins which originally opened into the proximal parts of the
posterior cardinals, acquire openings into the ductus Cuvieri
near the vertebral and external jugular veins.

4. The Lymphatic System and Spleen

The development of the lymphatic system is imperfectly
known in the chick. A pair of anterior or cervical lymph hearts
appears during the fifth day, and. from these lymphatic net-
works grow out extending posteriorly, parallel with the lateral
veins of the body; by the eighth day these nets are developed
into definite lymphatic vessels. A pair of posterior or caudal
lymph hearts appears early the seventh day as a series of lat-
eral outgrowths from the first five coccygeal veins (tributaries
of the posterior cardinal veins). These branches anastomose
with one another, forming an irregular sac or lymph heart, on
each side, which remains connected with the second, third, and
fourth coccygeal veins. The walls of the hearts become muscu-
lar and rhythmically contractile during the eighth and ninth
days.

During the ninth day the posterior lymph hearts connect
with a system of lymphatic spaces around the posterior section
of the dorsal aorta, and this space connects in turn with the
thoracic ducts. These lymphatic trunks are visible on the eighth
day, when they are described as two solid strands of mesen-
chyme, extending from the thyroid body to the roots of the
coeliac artery. They become hollowed out and connect with
the ductus Botalli, the dorsal aorta and the ductus Cuvieri.
These canals then approach and fuse, and about the twelfth
day connect with the posterior lymph hearts by way of the
lymphatic vessel around the posterior dorsal aorta. (It is
entirely probable that the connections between the thoracic

350 OUTLINES OF CHORDATE DEVELOPMENT

ducts and the blood-vessels represent the primarily formative
outgrowths of the ducts from the vascular endothelium, from
which the cords have extended and fused secondarily, but
direct observations to this effect are wanting.)

The anterior lymphatic hearts apparently disappear early.
The posterior lymph hearts attain their maximum development
during the fourteenth and fifteenth days, when they begin to
retrogress and disappear entirely ten to fourteen days after
hatching.

The spleen arises, during the fourth day, from a proliferation
of peritoneal cells in the base of the mesentery just above the
pancreatic region. It enlarges rapidly through continued cell
proliferation and the accumulation of a mesenchymatous
stroma. Its spaces, without definite endothelial walls, are
directly continuous with the sinusoidal origins of its efferent
vein, and from these spaces splenic cells enter the blood stream
and become converted into blood corpuscles.

V. THE CAVITIES OF THE BODY

The folding-off of the embryo from the yolk completes the
roughing-in of the body cavity. From the very beginning the
general embryonic body cavity shows signs of the differentiation
of the region surrounding the heart as the pericardial cavity.
We have already traced the origin of this part of the ccelom, in
describing the origin and formation of the heart. We have
also seen how the body cavity proper is formed and closed, and
how it is partially divided longitudinally by the dorsal mesen-
tery. It remains now for us to consider the essential steps
in the complete separation of the pericardial cavity and the
further subdivision of the primary body cavity.

Throughout the early stages of development the pericardial
cavity is only incompletely closed off from the body cavity,
since it is only partly closed posteriorly by the mesoderm in
the wall of the anterior intestinal portal, and the vessels which
are entering the heart from the yolk-sac. The formation of
the lateral mesocardia (see above) extends the separation of the,

THE LATER DEVELOPMENT OF THE CHICK 351

two cavities, but they still remain connected above and below

this partition. The pericardial cavity soon becomes restricted

to the median region of the body and the general body cavity

then pushes forward along the sides of the pericardial cavity.

These antero-lateral extensions of the body cavity are the rudi-

ments of the pleural cavity; they soon extend inward toward

the median line, dorsally

to the pericardial cavity

with which, however, they

still connect above the

lateral mesocardia. The

pericardial cavity still

connects with the general

body cavity beneath the

lateral mesocardia (Fig.

139).

The complete closure of
the pericardial cavity is
begun during the fourth
day, by the formation of
the septum transversum.
This partition is estab-
lished by the formation of
tissue connecting the
lateral mesocardia dorsally

FIG. 139. — Part of a transverse section
through the lateral mesocardia of a chick
with thirty-five pairs of somites (about
and Ventrallv Or ventro- seventy-two hours). Af ter Lillie. a, Auricle;

laterally,
11

wall.

, acm, accessory mesentery; am, amnion; ao,

With the body dorsal aorta; ba, bulbus arteriosus; ch, cho-

"U7i^'i j-V, ron; CD, posterior cardinal vein; dC, due-

While the septum tus ^ dwi> dorsal mesenter'y. ;liver.

tus

SOOn becomes Z™, lateral mesocardium; pc, pericardial
. cavity; pe, pulmo-enteric recess; pg, pleural
Complete between pen- groove; s, stomach; OT, sinus venosus; vm,

cardial and body cavities, ventral mesenterv-
it remains for a time incomplete between pleural and body
cavities. As the lungs begin to expand they push out into
the pleural cavities, the walls of which supply the greater
part of their mesodermal tissue. Finally the lungs extend
posteriorly as well as laterally and as they reach the region of
the septum transversum this gradually becomes completed

352 OUTLINES OF CHORD ATE DEVELOPMENT

(about the tenth day) as the pleuro-peritoneal membrane,
closing off the pleural cavity from the body cavity proper or
peritoneal cavity.

VI. THE LATER HISTORY OF THE MESODERMAL

SOMITES

In the chick of thirty hours we saw how the embryonic
mesoderm is divided into three general regions, (a) the axial
somites, (b) the intermediate cell mass or nephrotome, (c) the
distal lateral plate, continuous with the extra-embryonic meso-
derm (Fig. 102). We have already described the chief struc-
tures derived from the lateral plate — the vascular system and
the ccelom and its derivatives, and it remains now to describe
the structures derived from the somites and intermediate cell
mass.

The following table, quoted from Lillie (Development of the
Chick, pp. 184-185) gives a resume of the general disposition of
the somites.

"In an embryo of 42 somites (about ninety-six hours), the value of
the somites as determined by their relations and subsequent history is
as follows :

1 to 4. Cephalic; entering into the composition of the occipital re-
gion of the skull.

5 to 16. Prebrachial; i.e., entering into the region between the wing
and the skull.

17 to 19. Brachial.

20 to 25. Between wing and leg.

26 to 32. Leg somites.

33 to 35. Region of cloaca.

36 to 42. Caudal.

" More somites are formed later, the maximum number recorded being
52 (see Keibel and Abraham, Normaltafeln). In an eight-day chick
the number of somites is again about 42, including the four fused with
the skull. Thus the ten somites formed last are again lost."

The somites, excepting those at each end of the series, have
essentially a similar history, differing only in later details of
development (Fig. 119). Each gives rise to three structures:
(a) the musck plate or myotome, (b) the cutis plate or dermatome,

THE LATER DEVELOPMENT OF THE CHICK 353

(c) the sckrotome. The somites form as solid segmental cell
masses; their superficial cells are arranged as a rather dense
wall, epithelial in character, which encloses a loosely arranged
central mass of mesenchymal nature. The densely arranged
cells soon become limited to the dorsal and dorso-lateral
regions of the somites. The dorsal portion, in particular the
region toward the nerve cord, forms the rudiment of the
myotome or muscle plate, while the dorso-lateral region gives
rise to the cutis plate. In the more loosely arranged core, the
formation of intercellular substance begins very early, pro-
ducing a truly mesenchymatous structure. This part of the
somite then extends over toward the notochord and nerve
cord, as the rudiment of the sckrotome.

The myotome becomes thin and turns under the thicker
cutis plate, finally extending downward and outward entirely
beneath it, occupying a position between the spinal ganglion
and the cutis plate. The cells of the myotome elongate antero-
posteriorly, through the whole extent of the segment, and each
becomes converted into a striated muscle fiber. Later the
myotomes enlarge, as then- component cells multiply and grow,
and each extends down into the body wall. Opposite the limb-
buds, outgrowths of the myotomes extend into these, forming
their musculature. The entire voluntary musculature of the
chick develops from the myotomes; the involuntary muscula-
ture is mesenchymal in origin, chiefly splanchnic. The cutis
plate extends laterally, as the embryo grows, and after thinning
considerably, breaks up into a mesenchyme which spreads
underneath the ectoderm, forming the foundation of the thin
dermis layer of the integument.

The sclerotomal cells, multiplying and continuing the for-
mation of intercellular substance, extend dorsally, between
the nerve cord and the myotome, and ventrally, around the
notochord and dorsal aorta, and finally fill all the spaces around
these axial structures. Later the sclerotomes acquire a secon-
dary segmentation, in that each becomes transversely divided
opposite the middle of the somite; the posterior half of one
sclerotome then unites with the anterior half of the succeeding,

354 OUTLINES OF CHORDATE DEVELOPMENT

forming a sclerotomal segment. The sclerotome forms the
axial skeleton of the embryo (except the major portion of the
skull) and the segments are the rudiments of the vertebrte,
which thus alternate with the muscle segments, the arrange-
ment of which marks the primary segmentation of the embryo.
All details of the formation of the skeletal system lie without
the scope of the present chapter, and we shall merely call
attention to the fact that the skeleton arises in part from the
sclerotomes and in part from the general mesenchyme. The
vertebral column is the part derived from the sclerotomes.
These cells condense and the cartilaginous rudiments of the
vertebra begin to appear during the fifth day around the noto-
chord (centra) and nerve cord (neural arches). The sclero-
tomes of the head somites form the occipital region of the skull;
the remainder of the skull is formed from the mesenchyme
around the brain and sense capsules. Cartilage begins to
form in the skull during the sixth day. The visceral skeleton
forms from the mesenchyme of the visceral arches, cartilage
appearing here during the sixth day also. The skeleton of the
pectoral and pelvic arches and limbs is formed from the mesen-
chyme of these regions, cartilage appearing during the sixth
and seventh days. The clavicles, like the derm bones of the
skull and anterior visceral arches, ossify directly from mes-
enchyme, without being preformed in cartilage. (For simple
accounts of the development of the skeleton the student is
referred to Marshall, " Vertebrate Embryology/7 and Lillie,
"Development of the Chick," where full references to the lit-
erature will be found.)

VII. THE URINOGENITAL SYSTEM

In the chick, as in other vertebrates, the excretory and repro-
ductive sytems arise separately and come into relation only
secondarily. We may therefore begin with an account of the
origin of the excretory system, and through this lead to the
development of the reproductive system, and to an account of
their association.

THE LATER DEVELOPMENT OF THE CHICK 355

1. The Excretory System

The intermediate cell masses, or nephrotomes, form the
rudiments of the excretory system which, as in all Amniota, is
complicated by the succession of three nephric systems, pro-
nephros, mesonephros, and metanephros, of which the first two
are purely embryonic, only the last giving rise to the excretory
system of the adult. The nephroi develop only through the
neck and trunk regions, for in the head and tail no lateral plate,
nephrotome, and somite .are differentiated in the mesodermal
segment.

A. THE PKONEPHROS AND THE PRONEPHRIC DUCT
(WOLFFIAN DUCT)

The pronephros is wholly of vestigial character in the chick,
functionless even in the embryo. The pronephric duct, how-
ever, is retained as the duct of the embryonic kidney, and is
hence known as the mesonephric or Wolffian duct. On
account of its vestigial character the pronephros develops
variably, even in different regions in a single individual. It is
limited to the fifth to fifteenth or sixteenth somites, but
becomes typically developed only in the tenth to fifteenth.

In the latter region a small bud of cells grows upward from
the middle of the postero-dorsal surface of each nephrotome.
These buds, appearing about the middle of the second day, are
the rudiments of the pronephric tubules, so-called although they
remain solid here. The buds or tubules elongate gradually, and
their terminal portions bend over posteriorly, each uniting with
the next posterior tubule, forming thus a continuous longitudi-
nal strand, which is the rudiment of the pronephric or Wolffian
duct. Toward the close of the second day the duct becomes
hollow anteriorly. It pushes backward rapidly, above the
nephrotomes, growing independently, until about the sixtieth
hour it reaches the cloaca, with which it fuses; its lumen is
completed throughout at the end of the third day. In front
of the tenth somite no duct is formed and the tubules are re-

356 OUTLINES OF CHORDATE DEVELOPMENT

duced to small transitory buds entirely disappearing during the
latter part of the second day.

Soon after the tubule appears in each segment, the nephro-
tome is separated from the somite by the conversion of its
proximal part into mesenchyme, and the distal part then
appears added to the tubule. The only cavity of the pro-
nephric tubule is one sometimes appearing in this added por-
tion of the nephrotome, and is to be regarded as a continuation
of the ccelom of the lateral plate into the nephrotome region;
when present its opening to the coelom would therefore repre-
sent a nephrostome. No Malpighian bodies are developed in
connection with these tubules, and the whole pronephros
disappears by the end of the third day.

B. THE MESONEPHROS

The mesonephros is the functional embryonic kidney; its
duct is the original pronephric or Wolffian duct. The meso-
nephros begins to develop toward the end of the second day in
the region immediately posterior to the pronephros. Meso-
nephric tubules finally develop in all segments from the thir-
teenth or fourteenth to the thirtieth; the most anterior tubules
are thus present in segments developing pronephric tubules also.
In front of the twentieth segment, however, the mesonephros
remains rather vestigial and develops typically only from the
twentieth to the thirtieth segments.

In this latter region the narrow nephrotomal band widens,
separates entirely from the lateral plate and the somites, and
the original arrangement of its cells in dorsal and ventral layers
is lost. We should note that the Wolffian duct passes along,
between the nephrotomes and the somatic layer of the lateral
plate, while along the opposite sides of the nephrotomes is the
dorsal aorta; the posterior cardinal veins soon appear just
above the Wolffian ducts. On the ventral side of the nephro-
tome, about opposite the middle of the segment, its cells become
condensed into a spherical mass, in which a definite space
appears; this is the rudiment of the primary mesonephric tubule

THE LATER DEVELOPMENT OF THE CHICK 357

(Fig. 140). This rudiment then extends upward to the Wolffian
duct with which it communicates. On the side opposite this
extension another outgrowth appears which forms the Mal-
pighian body.

FIG. 140. — The development of the mesonephros. A, B. Transverse sections
through the mesonephric tubules of the duck embryo with forty-five pairs of
somites. After Schreiner. C. Transverse section through the middle of the
mesonephros of a chick of ninety-six hours. From Lillie (Development of the
Chick). Ao., Dorsal aorta; B., rudiment of Bowman's capsule; c., collecting
duct; Cad., ccelom; Col. T., collecting tubule; d., dorsal outgrowth of the Wolffian
duct; Glom., glomerulus; germ. Ep., germinal epithelium; M's't., mesentery;
n.t., nephrogenous tissue; r., rudiment of conducting portion of primary tubule;
T.I, 2, 3, primary, secondary, and tertiary mesonephric tubules; V.c.p., posterior
cardinal vein; W.D., Wolffian duct.

From the nephrotome, just above the primary tubule,
several additional secondary mesonephric tubules are formed,
and finally, other dorsal tertiary tubules are added, so that six

358 OUTLINES OF CHORD ATE DEVELOPMENT

or seven tubules are formed in each segment; all these tubules
develop similarly. No nephrostomes, or coelomic connections,
are formed save in the four or five most anterior tubules, which
are themselves transitory structures. The formation of the
mesonephric tubules is completed during the fourth and fifth
days, when they begin to elongate rapidly. During the next
three or four days they become convoluted and form altogether
a large mass, sometimes known as the Wolffian body, project-
ing from the dorsal body wall. The tubules of each segment
open into a common dilation of the Wolffian duct, distin-
guished as the collecting tubule.

The mesonephros becomes very vascular through the forma-
tion of abundant sinuses from the accompanying posterior
cardinal veins, which are its afferent vessels. The walls of
these sinuses are in direct contact with the tubules. The blood
collects along the ventral side of the mesonephros in the so-
called subcardinal veins, which connect, as we have seen, with
the inferior vena cava. The mesonephros begins to degenerate
the tenth or eleventh day, and by the time of hatching it has
completely disappeared, save in so far as parts of it remain con-
nected or associated with the reproductive system.

C. THE METANEPHROS

The metanephros is the permanent kidney of the adult, and it
also functions probably, together with the mesonephros, during
the latter part of embryonic life. Metanephric structures
appear toward the end of the fourth day as outgrowths from
each mesonephric or Wolffian duct, just as this turns to enter
the cloaca. Each outgrowth becomes a sac and then a tube,
turning anteriorly and rapidly growing forward along the inner
side of the posterior cardinal vein, and finally extending anteri-
orly, above the mesonephros, as far as the twenty-fifth somite.
This tube is the rudiment of the ureter and collecting tubules
of the metanephros; the latter are formed as the result of a com-
plicated system of branches of the original duct as it grows
forward (Fig. 141).

The secreting tubules or true metanephric tubules, are formed

THE LATER DEVELOPMENT OF THE CHICK

359

si

from the cells of the nephrotomes of the last two or three
segments of the body (31-33). In this region
the nephrotomal structure is not clearly differen-
tiated, and it is referred to simply as the meta-
nephrogenous tissue. As the metanephric diver-
ticulum grows out it is accompanied on its inner
face, throughout all its branching, by cells of this
tissue. During the seventh or eighth day typ-
ical nephric vesicles appear, like those of the
mesonephros, and acquire openings into each
branch of the collecting duct; Malpighian bodies
develop in the usual manner. During the next
three or four days the entire metanephros is
established, and the mesodermal cells surround-
ing the tubules and ducts form the stroma and
capsule of the kidney. During the fifth and
sixth days the terminal portions of the Wolffian
ducts and the metanephric diverticula become
absorbed into the wall of the cloaca so that the
ureters acquire openings separate from those of
the Woffian ducts; the latter are hence, after the
degeneration of the mesonephros, not at all ex-
cretory in function. No nephrostomes appear
in connection with the metanephros.

From the preceding description it will be seen
that the inner or medullary part of the defini-
tive kidney is derived from the branched out-
growth from the Wolffian duct, while the outer
cortical layer of secretory tubules and Malpig-
hian bodies is derived from the metanephro-
genous tissue (nephrotomes) of the last two
or three body somites, and is therefore homo-
logous with the glandular part of the meso-
nephros.

2. The Reproductive System

Before describing the development of this system it seems
necessary to recall, in a few words, the composition of the adult

FIG. 141.—
Diagram of the
arrangement of
the nephric ele-
m e n t s in the
chick. After
Felix. Proneph-
ric duct, and me-
tanephric ducts
(ureters) in
black; meso neph-
ric tubules cross
hatched; meta-
nephric tubules
in dotted out-
lines.

360 OUTLINES OF CHORDATE DEVELOPMENT

reproductive system in the Amniota. In these forms the
gonoducts are derived from the original mesonephric or Wolffian
duct, which is now represented by two longitudinal ducts, the
Wolffian duct, stricto sensu, and the Miillerian duct. As a
matter of fact, we shall see that the Miillerian duct develops
independently of the mesonephric duct, but phyletically it is
clear that both ducts are to be regarded as derivatives of a
common mesonephric duct. The mesonephros itself largely
degenerates, of course, but some part of it remains functionally
connected with the reproductive system in the male, and as a
purely vestigial structure in the female. Consequently in the
male Amniote the Wolffian duct proper is freed from excretory
function, and serves only as the gonoduct or vas deferens,
effecting a connection with the gonad through the remains of
certain mesonephric tubules; the Miillerian duct is either
vestigial or entirely wanting. In the female, on the contrary,
the Miillerian duct is the functional gonoduct, or oviduct, while
the Wolffian duct and mesonephros either disappear entirely
or remain as functionless vestiges.

A. THE EEPRODUCTIVE DUCTS

Nothing need be added to the account already given of the
development of the Wolffian duct. We shall see below how, in
the male, this connects with the testis; in the female the Wolffian
duct disappears along with the mesonephros.

The Miillerian ducts develop similarly in the male and female;
they appear during the fourth day. Each is formed as a
thickened longitudinal band in the peritoneum, along the outer
surface of the mesonephros, near its attachment to the body
wall, i.e., just along the outer side of the Wolffian duct. This
band invaginates, forming first a groove and then a tube, lying
just beneath the surface of the anterior end of the mesonephros.
The extreme anterior end of this canal remains open into the
body cavity, as the rudiment of the ostium or infundibulum.
The greater part of the Miillerian duct is formed by the backward
extension of the tube thus formed. It grows posteriorly as a

THE LATER DEVELOPMENT OF THE CHICK 361

solid rod, gradually becoming tubular, and reaches the cloaca
during the seventh day, although it does not acquire an opening
into the cloaca during embryonic life, indeed not until the fowl
is about six months old. The duct becomes surrounded by a
thick coat of mesenchyme cells and appears as a ridge on the
surface of the mesonephros.

After the eighth day, in the male both Miillerian ducts and
in the female the right duct, cease to develop and immediately
begin a series of degenerative changes. In the female the left
duct continues to enlarge, and as the mesonephros disappears,
it remains as a conspicuous organ, attached to the dorsal body
wall by a double fold of peritoneum, the mesovarium. Further
differentiation into the regions of the adult oviduct already
described, begins before the end of the second week of
Incubation.

B. THE GONADS

The early development of the gonads is alike in both sexes,
and it is not until the end of the first week that the sexes can be
distinguished. This early period is known as the indifferent
period. The gonads appear on the fourth day, as longitudinal
bands of thickened peritoneal epithelium, along the dorsal wall
of the body cavity, between the mesonephros and the attach-
ment of the mesentery. This band of " germinal epithelium"
later appears on the inner surface of the mesonephros, on
account of the enlargement of this organ. The germinal epithe-
lia develop symmetrically and extend through the posterior
half or third of the mesonephric region.

The peritoneal cells of the so-called " germinal epithelium"
are apparently not to be regarded as the true germ cells. As
in other groups, the primordial germ cells are differentiated very
early in development, and migrate into this peritoneal or germi-
nal epithelium, where they begin to multiply (Fig. 142). The
mesenchyme cells of the mesonephros, beneath the peritoneum,
become added to the developing gonad and later form its stroma
or connective tissues.

362 OUTLINES OF CHORDATE DEVELOPMENT

During the fifth day strands of cells appear, extending between
the substance of the gonad and the mesonephric tubules of the
region. These are the rudiments of the sexual cords (Fig. 142) .
While not definitely demonstrated as yet, it seems probable
that the sexual cords are outgrowths of the mesonephric tubules
(Malpighian bodies) which extend into the gonad. About the
end of the first week of development the sexes are distinguishable

FIG. 142. — Section through the gonad of a chick, the middle of the fifth day,
showing the sex cords reaching the germinal epithelium. After Semon. g,
Germinal epithelium; m, epithelium of the mesentery (peritoneum); o, primitive
ova; s, sex cords; t, connective- tissue stroma.

through the enlargement of the sexual cords in the male, and the
greater thickness of the germinal epithelium in the female.

Testis. — During the second week the primordial germ cells
appear all through the stroma, and even migrate into the sexual
cords, which continue to increase in size and number until they
form altogether a considerable bulk. While the greater part of
the mesonephros degenerates, a vestige remains as the para-
didymis, that part with which the sexual cords connect. The
tubules of this region become the vasa efferentia (epididymis)
through the formation, about the end of the third week,

THE LATER DEVELOPMENT OF THE CHICK 363

of a lumen in each sexual cord, which thus puts the cav-
ities of the testis into communication with the mesonephric
tubules. The sexual cords thus become the rete e/erentia.
The primordial germ cells, or spermatogonia as they may now
be called, lie in the walls of the dilated inner ends of the rete
efferentia (sexual cords), into the cavities of which their cell
products may be discharged and pass thence, by the vasa
efferentia and the vas deferens, to the cloaca. The original
"germinal epithelium" becomes converted into a flat covering
layer continuous with the peritoneal folds (mesorchia) slinging
the testis from the dorsal body wall.

Ovary. — The early development of the ovary parallels that
of the testis. Like the right oviduct, the right ovary, after
developing for a time, degenerates and disappears. In the
left or definitive ovary the primordial germ cells behave as in the
testis, at first, but after a brief period their migration ceases
and those which have left the primitive germinal epithelium
degenerate, together with the sexual cords. The epithelial
cells, and the primordial germ cells contained in the epithelium,
continue to multiply rapidly, and the mesenchymal stroma
becomes abundant. The inner surface of the germinal epi-
thelium forms strands of cells projecting into the stroma of the
ovary, and containing primordial germ cells or oogonia. These
strands segment into separate cell masses or nests, each includ-
ing an oogonial cell; the further growth and development of the
oogonia have been described in the beginning of the preceding
chapter.

The mesonephros thus has no share in the formation of the
reproductive system of the female; its posterior section may be
recognized in the vestigial paroophoron, while the homolog
of the epididymis of the male is to be seen in the parovarium.

C. THE ADRENAL BODIES

Brief reference to the development of the adrenal bodies may
be made here, although they are not a part of the renal system.
These bodies have a double origin, arising in part from periton-

364 OUTLINES OF CHORDATE DEVELOPMENT

eal proliferation and in part from sympathetic ganglion cells;
the part derived from the peritoneal cells effects secondary con-
nections with certain mesonephric components.

During the fourth day the peritoneal cells in front of the germi-
nal epithelia proliferate and extend through the mesenchyme
anterior to the mesonephroi and along the dorsal aorta. As
these cells multiply they become arranged in definite strands
or solid cords; these cords then connect with the renal vesicles
of the adjacent portion of the mesonephros. By the eighth day
a definite and highly vascular rudiment is established on each
side. About this time cells of a sympathetic ganglion located
on the antero-dorsal side of the adrenal rudiment, begin to
extend into it, penetrating among the primary cords. During
the later stages these peritoneal and sympathetic components
assume the relations found in the adult adrenal, forming then
the cortical and medullary cords respectively.

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nales chez les vertebres superieurs. Jour. anat. et physiol. Paris.

39. 1903.
TWINING, G. H., The Embryonic History of Carotid Arteries in the

Chick. Anat. Anz. 29. 1906.
VERDUN, M. P., Sur les derives branchiaux du Poulet. C. R. Soc. Biol.

Paris. X, 5. 1898.
VIRCHOW, H., Dottersyncytium, Keimhautrand und Beziehungen zur

Konkrescenzlehre. Ergeb. Anat. u. Entw. 6. 1896 (1897).
WILLIAMS, L. W., The Somites of the Chick. Amer. Jour. Anat. 11.

1910.

CHAPTER VI

THE EARLY DEVELOPMENT OF THE MAMMAL. THE

MAMMALIAN EMBRYONIC MEMBRANES AND

APPENDAGES

PAGE
INTRODUCTION 368

I. THE EGG AND ITS FORMATION 371

1. The Reproductive Organs of the Female 371

2. The Ovum and its Ovarian History 372

3. Maturation 376

4. Ovulation 377

II. FERTILIZATION AND THE EARLY PHASES OF DEVEL-

OPMENT 379

1. Fertilization 379

2. Cleavage 380

3. The Blastodermic Vesicle 383

A. The Growth of the Blastodermic Vesicle 384

B. The Formation of the Embryo and the Embryonic
Layers 384

III. THE DEVELOPMENT OF THE EXTERNAL FORM OF

THE HUMAN EMBRYO 399

IV. THE EMBRYONIC MEMBRANES AND APPENDAGES OF

THE EUTHERIAN MAMMALS . 417

1. Implantation . 421

2. The Amnion and Chorion 424

3. The Yolk-sac 431

4. The Allantois . . 434

5. The Placenta 437

WE shall not undertake, in the present chapter, to give an
account, however brief, covering the whole embryonic history
of a Mammal. We shall rather attempt to describe certain
phases or aspects of mammalian development, selected on
account of their interest or importance for the general student.
We shall give first a description of the mammalian ovum, its
formation, the early processes of cleavage and the formation

368

THE EARLY DEVELOPMENT OF THE MAMMAL 369

of the embryonic layers, and the formation of the embryo and
its chief rudiments. This will be followed by a brief account
of the development of external form of the human embryo.
Then in conclusion we shall outline the more salient facts
regarding the embryonic membranes and appendages, and the
establishment of those relations between the embryo and the
maternal organism which are such fundamental characteristics
of the true (Eutherian) Mammals. For the whole subject of
mammalian organogeny the student may be referred to the
excellent and recent accounts given in such texts as those of
0. Hertwig, Keibel-Mall, Minot, McMurrich, etc.

The whole life-history of the Mammal may be roughly
divided into four periods, each marked by one or two striking
characteristics, but often not otherwise clearly separated.
First is the true embryonic period or period of gestation, during
the greater part of which the organism is retained within the
uterine cavity of the mother, drawing its nourishment from the
uterine walls. This period extends from the time of fertiliza
tion to the time of birth, and its duration is widely variable ir
different species, though usually quite constant in any single
form, due, perhaps, in part, to the fact that conditions of tem-
perature, nutrition, etc., are subject to only slight variation. To
mention a few examples, the period of gestation is, in the mouse
twenty to thirty days (Daniel), rat about twenty-one days, in
the rabbit thirty to thirty-two days, guinea-pig sixty-four to
seventy days, cat about nine weeks, dog fifty-nine to sixty-
three days, sheep about twenty-one weeks, pig about four
months, cow about nine months, man about nine months
(270-280 days), deer ten months, horse about eleven months,
elephant about twenty months.

The time of birth, or parturition, marks the most abrupt
physiological and morphological transition in the entire life-
history. There is wide variation, among different forms, of
the comparative stage to which development has proceeded
when this event occurs. Some organisms, like the calf or the
colt, may be termed precocious, since they are able, within a
few hours after birth, to run about actively and to live with a

370 OUTLINES OF CHORDATE DEVELOPMENT

minimum of parental protection and care. Others, such as
the kitten or young rabbit, are born in a much less advanced
stage and, with unopened eyes and uncoordinated movements,
remain almost helpless for several days. Some of the marsu-
pial Mammals (Metatheria) are quite remarkable in that the
young are born after a very brief period of gestation (about
eight days in the opossum (Didelphys) and in Dasyurus), at a
relatively very early stage of development, not able even to
perform the simple act of sucking. In these forms there are
special adaptations to this condition, and the young are at
once transferred to a special external cavity of the mother, the
marsupium or pouch, where development proceeds.

In no case is the young Mammal entirely independent of the
maternal organism for some time after parturition, for there
follows the second general period in the life-history, that of
lactation, during which the young organism is wholly or partly
dependent for its nourishment upon the mammary secretion
of the mother'. During this period development continues, of
course, but at a slower rate, and toward its close there is a
gradual transition to conditions of complete independence,
save that some degree of parental care may be exercised for a
. time longer. The duration of the period of lactation is variable,
even in a given species.

Two other periods in the life-cycle of the Mammal need only
to be mentioned; these are the period of adolescence, during
which growth and development continue at a still slower rate,
and the period of adult life or sexual maturity. The transition
between these periods is often marked by a series of structural
and physiological alterations in characteristics other than those
of the reproductive system.

Embryologically as well as morphologically, the Mammalia
present many similarities to the Sauropsida. The mammalian
ovum is nearly yolkless, and yet in its development it exhibits
many of the phenomena of yolk-influence — characteristics of
eggs of the extreme telolecithal (meroblastic) type — such as
the formation of a modified germ disc, of a (yolkless) yolk-sac,
and other less striking characteristics. While the mammalian

THE EARLY DEVELOPMENT OF THE MAMMAL 371

egg resembles that of Amphioxus in size and deutoplasmic
relations, it exhibits almost none of the regularities of cleavage,
blastula formation, and gastrulation that we should expect to
be associated with a small, homolecithal ovum.

The origin of the most fundamental modifications of the
sauropsid type of development lies in the replacement of the
intra-oval yolk-mass by a source of food and energy lying out-
side of the ovum and embryo, i.e., the maternal uterine walls,
and in the early and extensive relation between the embryo
and this new source of nutrition.

In the following account of certain phases of mammalian
development, we shall not be limited to any single form through-
out, but shall describe in general, elementary terms, the mam-
malian type of development, using various forms as illustrations
of the topics considered.

I. THE EGG AND ITS FORMATION

1. The Reproductive Organs of the Female

In the Mammals there is always a single parr of ovaries, sus-
pended in the postero-dorsal region of the body cavity by
peritoneal mesovaria (Fig. 143). They are whitish, rounded
or ovoid bodies, of rather small dimensions (human, 3-4 cm.
long, by 2-3 cm. wide, by 0.7 — 1.2 cm. thick; rabbit, about
2 X 0.8 cm. The ovaries are not directly connected with the
gonoducts, although the openings of the oviducts are suspended
in the same peritoneal mesovaria, and are located very near to
the ovaries, so that the ova, when discharged from the ovary
pass only a short distance through the body cavity before
entering the oviduct (Fig. 143).

The Miillerian ducts, or oviducts in the broad sense, are
muscular tubes, highly differentiated into three regions. The
upper or anterior portion forms the Fallopian tube or oviduct,
stricto sensu (Fig. 143). The inner end of this, where it opens
out of the body cavity near the ovary, is expanded and its
margin is drawn out into finger-like or fringe-like processes;
this is the infundibulum, ostium or fimbriated opening. T\ie

372 OUTLINES OF CHORDATE DEVELOPMENT

second section is the uterus, thicker walled than the Fallopian
tube, and of greatly varying extent in different Mammals,
correlated with the number of young produced at one time,
for this is the part of the oviduct occupied by the developing
embryos. Lastly is the terminal vagina, which opens directly
to the outside in all placental Mammals.

The vaginal region is practically always a single, median
structure, formed by the fusion of the lower ends of the two

FIG. 143. — Diagrammatic representation of the human female reproductive
organs. Dorsal (posterior) view. From Quain's Anatomy. The posterior
walls of the uterus and vagina have been removed to show their cavities, c,
Cervix of uterus; fi, fimbriated opening or ostium of oviduct; h, hydatid; i,
wider distal part of oviduct; I, round ligament; II, the broad ligament; lo, liga-
ment of ovary; o, ovary (naturally the ovary has an oblique or nearly vertical
position); od, oviduct or Fallopian tube; po, parovarium; u, fundus of uterus;
v, upper part of vagina.

oviducts. Different groups of Mammals exhibit various
degrees in the extent of the fusion of the uterine sections also.
Thus in the Rodents the vaginae alone are fused, the uteri
remaining entirely distinct (uterus duplex), in the Garni vors and
most Ungulates the uteri are partly fused, partly free (uterus
bicornis), and in the Primates the uteri are completely fused
and only the Fallopian tubes remain paired (uterus simplex).

2. The Ovum and its Ovarian History

The ova of the placental Mammals are among the smallest
known. When fully formed they are usually 0.1-0.3 mm. in

THE EARLY DEVELOPMENT OF THE MAMMAL 373

diameter, although these limits are occasionally exceeded; for
example, the ovum of the mouse measures about 0.06 mm.,
deer 0.07-0 . 10 mm., guinea-pig 0.09 mm., dog about 0.18 mm.,
human 0.22-0.32 mm., cat 0.135-0.15 mm., rabbit 0.1 1-0. 12 mm.
The cytoplasm of the ovum ordinarily exhibits two general
regions, a clear exoplasm or cortical layer surrounding an opaque

FIG. 144. — Fully grown human oocyte just removed from the ovary. Out-
side the oocyte are the clear zona pellucida and the follicular epithelium (corona
radiata). The central part of the oocyte contains deutoplasmic bodies and the
eccentric nucleus (germinal vesicle). Superficially there is a well-marked exo-
plasm, or cortical layer. From Waldeyer (Hertwig's Handbuch, etc.).

endoplasm containing small granules of deutoplasmic material
(Figs. 144, 146). The nucleus or germinal vesicle of the fully
formed oocyte is relatively large, usually 0.025-0.040 mm. in
diameter; it is spherical, possesses a definite nuclear membrane,
a large nucleolus (karyosome), and has a slightly eccentric
position.

374 OUTLINES OF CHORDATE DEVELOPMENT

The presence of a vitelline membrane is not definitely known;
surrounding the ovum, however, is a thick transparent mem-
brane apparently of chorionic nature (i.e., of follicular origin
— secondary egg membrane), known as the zona pellucida. This
often has, either throughout or at least peripherally, the
appearance of being perforated by minute pores or canals, and
hence is often called the zona radiata. A micropyle is not
known. The zona pellucida is usually separated from the sur-
face of the fully grown egg by a narrow perivitelline space. In
many Mammals, at the time the ovum escapes from the ovary
it is, and for a time remains .surrounded by a few layers of
regularly arranged cells forming the corona radiata (Fig. 144).
This is a part of the ovarian egg follicle, and in order to under-
stand its relations we must outline the earlier ovarian history
of the ovum.

The formation of the ova begins in the ovary before the time
of birth, and in the case of the Mammals all of the ova which
are to be produced during the period of fertility, are at that
time definitely established, although only partly differentiated.
In other words the period of the multiplication of the oogonia
is completed during embryonic life. Subsequently there occur
the phases of oogonial growth and the maturation processes.
In the embryonic ovary the primordial germ cells divide
repeatedly and soon form large numbers of cells arranged in
small groups or " nests" (Fig. 145). The cells composing these
have all had a similar history, but are destined to have very
different fates. In each group one cell enlarges and becomes
a definitive ovum, while its sister cells and their descendants are
to form the egg follicle. All of the stages in the history of
the formation of the ovum and follicle can be found in the ovary
of a fertile individual.

The follicle appears first as a small group of flattened cells,
forming a single layer around the slightly enlarged central
oogonium (Fig. 145). As the follicle cells multiply they become
cubical and then columnar, forming a definite epithelium. As
the ovum increases steadily in size the follicle more than keeps
pace with it, so that as the follicular epithelium becomes three

THE EARLY DEVELOPMENT OF THE MAMMAL 375

to four cells deep, spaces begin to appear within the follicle,
usually toward one side. On the side opposite these spaces the
follicular cells multiply more rapidly and form a definite accu-

FIG. 145. — Section through part of the ovary of a dog. After Waldeyer. a.
"Germinal epithelium"; b, egg tubes; c, small ovarian follicles; d, older ovarian
follicles; e, ovum surrounded by discus proligerus; /, second ovum in follicle
with e. (Only rarely are two ova thus found in a single follicle.) g. Outer cap-
sule of the follicle; h, inner capsule of the follicle; i, membrana granulosa;
k, collapsed, degenerating follicle; I, blood-vesesls; m, sections through tubes
of the parovarium; y, involuted portion of superficial epithelium; z, transi-
tion to peritoneal epithelium.

mulation known as the discus proligerus, in the midst of which
the ovum is buried (Fig. 145). The follicle cells immediately
surrounding the ovum become markedly elongated forming the

376 OUTLINES OF CHORDATE DEVELOPMENT

corona radiata, mentioned above/ These cells appear to be
directly connected with the ovum by fine pseudopodial proc-
esses affording the pathways by which substances enter the
ovum, providing for its growth. The other cells of the follicle
form what is known as the stratum granulosum.

As the follicle and egg approach maturity the follicular cavity,
containing the liquor folliculi, becomes very large, and the whole
structure becomes enclosed in a definite capsule consisting
externally of connective-tissue fibers and cells formed from the
stroma of the ovary, and internally of a thick layer of cells,
blood-vessels, .and nerves. Within this lies the basement
membrane of the follicular epithelium (granulosa cells). At
the close of the oogonial growth period, the cells of the corona
radiata form a thick membrane (zona pellucida) around the
egg, and the protoplasmic processes remain only partially and
indistinctly (zona radiata). The full-grown follicle is very
large (9-14 mm. in man) forming a well-marked projection from
the surface of the ovary. The mammalian follicle is usually
known as the Graafian follicle. It was first described in 1677
by Regnerus de Graaf and was regarded as what we should
now call the ovum, until Von Baer's description in 1827 of
the true mammalian ovum.

As to the history of the egg itself during the growth stage,
little need be said here. A differentiated region around the
nucleus appears very early, before the follicle has definitely
formed. This becomes a sort of "yolk nucleus" giving rise
to the deutoplasmic content of the egg; it disappears while the
follicle is still single layered. During the growth period, which
is also a period of "organization" of the ovum, the nucleus
appears to give off chromatic substance into the cytoplasm. A
pair of small centrioles with surrounding centrosphere may be
seen during the early stages of growth.

3. Maturation

At the close of the growth period the nucleus forms a large
clear vesicle, with very little chromatin other than that of the

THE EARLY DEVELOPMENT OF THE MAMMAL 377

large chromatin reservoir or karyosome. It is now ready to
enter upon the period of maturation. As a rule, in the Mam-
mals, the first polar body is given off while the ovum is still
within the ovary (in the mouse about one hour before ovula-
tion), and the second polar spindle is established; the second
polar division is then completed only after fertilization, which
occurs, of course, in the oviduct. It is not necessary to describe
the details of the maturation process here, for in most respects
it offers nothing unusual. With respect to the size of the polar
spindles and polar bodies, however, the Mammals are rather
remarkable, for these, especially the first polar body, are very
large, often one-fourth the diameter of the ovum itself, and in
some cases even larger. Occasionally an abnormally large
first polar body may be formed so that the egg divides almost
equally; the later history of such cases is not known. The
first polar body usually divides soon after its formation;
amoeboid movements have been observed in the first polar body
of the mouse. Centrioles are distinctly present, but the asters
are only slightly indicated or absent.

A large second polar spindle is formed at once and moves
toward the surface of the egg (secondary oocyte,) when the
process of maturation is inhibited while the processes of ovula-
tion and fertilization occur. The second polar body is then
formed while the ovum is in the upper part of the oviduct; it
is smaller than the first. The polar bodies do not remain
attached to the surface of the ovum (Fig. 147) and are easily
lost sight of entirely. The number of chromosomes can be
most easily determined during these phases; some of the
somatic numbers determined are the following: man, twenty-
two in the male, twenty-four in the female (Guyer), mouse
twenty-four, cat between twenty-eight and thirty-two.

4. Ovulation

The escape of the ovum (secondary oocyte) from the Graafian
follicle and the ovary, is termed ovulation. The capsule of the
maturing follicle becomes very vascular, and at one place very

378 OUTLINES OF CHORDATE DEVELOPMENT

thin and easily ruptured; this is the cicatrix or stigma. It hag
been suggested that the rupture of the follicle may be due to
the continued accumulation of the liquor folliculi. However
this may be, when the follicle bursts the liquor flows out into
the periovarial cavity, carrying along the ovum, still surrounded
by the corona radiata. The fimbriaB of the oviduct are also
enclosed in this periovarial cavity, and through the ciliary
action of the epithelium covering these and lining the upper
part of the oviduct, and probably also through peristaltic con-
tractions of the oviducal walls, the ovum is carried through the
ostium and into the oviduct. During this passage the first
polar body frequently breaks through the chorion (zona pellu-
cida or radiata) and through the corona radiata as well, so that
it is entirely lost from the region of the ovum (mouse, Kirkham).

Returning to the history of the follicle itself, we find it
undergoing very important changes, as the result of which it is
converted into the corpus luteum. The emptied follicle soon
becomes a nearly solid mass of cells, known as lutein cells, large
rounded cells containing quantities of pigmented granules or
lutein. The origin of these cells is somewhat uncertain; they
appear to be derived from the stratum granulosum cells of the
follicle, although they may come from the inner capsule of the
follicle (stroma cells). Their pigment is yellowish in man,
hence the name corpus luteum; in other Mammals it may be
pinkish (pig, rabbit), red (mouse), brown (sheep), etc.

In cases of non-pregnancy following ovulation, the corpus
luteum is rapidly converted into fibrous connective tissue and is
absorbed, but when pregnancy follows, the corpus luteum
retrogresses very slowly and disappears only after parturition.
There is considerable evidence (Marshall, L. Loeb) that the
corpus luteum produces an internal secretion (hormone) of
great physiological importance in effecting the fixation of the
ovum to the walls of the uterus (implantation, see below).

The general conditions determining the occurrence of ovula-
tion are unknown in most instances. In the lower Mammals
it is associated with a general physiological condition known as
cestrus or heat, which may possibly itself be determined by

THE EARLY DEVELOPMENT OF THE MAMMAL 379

internal ovarian secretions (hormones). Usually, too, the
period of oestrus is preceded by a procestrus, or menstruation.
In man, however, these two conditions are more or less inde-
pendent, and no very constant relation is apparent. In the
rabbit, cat, and ferret, ovulation occurs only after coitus
(nine to ten hours after, in the rabbit, and usually within
fifty hours in the cat), while in the dog, rat, and mouse, and
in many Ungulates and Primates, it occurs independently of
coitus. In many cases ovulation follows upon parturition, in
the mouse about fourteen hours after the birth of a litter, and
in the rat within about eighteen hours.

II. FERTILIZATION AND THE EARLIER PHASES OF
DEVELOPMENT

1. Fertilization

In most of the Mammals fertilization occurs in the upper part
of the oviduct, almost immediately upon the entrance of the
ovum. After the introduction of the spermatozoa into the
vagina, they make their way to the upper ends of the oviducts,
where they may remain alive and capable of functioning for
several days or even weeks. Apparently the ovum too may
remain in the oviduct, alive and capable of development, for
several days or even a fortnight, in case fertilization does not
occur at once.

The details of the sperm entrance, the formation of the sec-
ond polar body, the establishment and fusion of the egg and
sperm pronuclei, and the formation of the first cleavage figure,
are not unusual and need not be described here (Fig. 146).
Monospermy is typical of the Mammalia, and since there is no
micropyle, the spermatozoon has to penetrate the zona pellucida
(radiata), as well as the corona radiata, which may remain
surrounding the egg during fertilization and even until a late
cleavage stage. Long before it finally breaks down it becomes
soft and easily penetrated (Fig. 146) . In the rat the vigorous
movements of the spermatozoa within and among the cells
of the corona tear this to pieces and leave the egg naked after

380 OUTLINES OF CHORDATE DEVELOPMENT

twenty to twenty-five minutes. In the mouse, at least, the
entire spermatozoon enters the ovum, but the tail soon disap-
pears. Some of the details of the process of fertilization in the
cat, are shown in Fig. 146.

II

Q7*^yf<>f'»l^7^

FIG. 146. — Reconstruction of four sections through the fertilized ovum of the
cat. From Longley (combined from two figures). No zona pellucida is visible
in these sections. The corona radiata is disintegrating, s, Remains of second
polar spindle; /, first polar body; //, second polar body; d", sperm pronucleus;
9 , egg pronucleus.

2. Cleavage

Before taking up the details of cleavage and early develop-
ment, we should say, in preface, that in the placental Mammals
these processes of cleavage, formation of the blastoderm and
early cell layers, are in many respects unique and often very
difficult of comparison with the corresponding processes in other
forms. As mentioned above, many of these peculiarities result
from the fact that the mammalian ovumwras originally markedly

THE EARLY DEVELOPMENT OF THE MAMMAL 381

telolecithal, probably like that of the Sauropsida, and we are
already familiar with the fact that the presence of a large yolk-
mass profoundly modifies the simple processes of cleavage,
gastrulation, etc. Accompanying the return of the mammalian
egg to the nearly alecithal condition, however, we do not find a
corresponding return to the simpler early developmental
processes characteristic of the primarily alecithal egg. On the
contrary these processes are modified in new directions, not
known elsewhere.

Added to these modifications is another series of alterations
resulting from the very early development of a mechanism by
which the segmenting ovum becomes intimately related with
the uterine walls. Altogether, then, we find conditions here
that are very special and not closely paralleled in other animals.
So profoundly have the early stages of development become
modified that there is sometimes difficulty in clearly identifying
and homologizing with other' types, certain structures of the
early mammalian embryo, such as the germ layers, primitive
streak, etc. In the following description we shall adopt the
convenient and more customary descriptive terms, but it
should be clearly recognized that there are possible contradic-
tions, and some students of mammalian embryology would say,
positive errors, in applying the customary terminology to the
early history of the mammalian embryo.

In most of the Mammals the early development is very slow.
The cleavage stages usually occur as the egg is passing slowly
down the oviduct. In the mouse the first and second cleavages
occur about twenty-four hours and forty-eight hours, respec-
tively, after coitus, and about eighty hours elapse before the
ovum reaches the uterus. In the rabbit the first cleavage
occurs fourteen to fifteen hours after ovulation, and nearly
four days are occupied in the passage to the uterus. In the
dog eight to ten days elapse before the ovum reaches the uterus.
A few instances are known, on the other hand, where the egg
arrives in the uterus just as cleavage begins (bat, hedgehog, and
other Insectivors). In the European roe-deer, where fertiliza-
tion occurs in the autumn, or perhaps in mid-summer, the ovum

382 OUTLINES OF CHORDATE DEVELOPMENT

develops only as far as a cleavage stage that season; its develop-
ment then continues the following spring.

There is considerable variation in the details of cleavage in
the Mammalia, and since we are not describing any single form,

FIG. 147. — Cleavage of the ovum of the rabbit. After Assheton. A. Two-
cell stage, twenty-four hours after coitus, showing the two polar bodies separated.
B. Four-cell stage, twenty-five and one-half hours after coitus. C. Eight-cell
stage, a, Albumenous layer derived from the wall of the oviduct; z, zona radiata.

we must be limited to very general terms; many of the details
may be learned from the accompanying figures (Figs. 147, 148).
Cleavage is total and at first adequal, very early becoming quite

FIG. 148. — Morula and early blastodermic vesicles of the rabbit. After
Assheton. The zona radiata and albumenous layer are not shown. A. Section
through morula stage, forty-seven hours after coitus. B. Section through very
young vesicle, eighty hours after coitus. Taken from uterus; ordinarily the ova
have not reached the uterus at this age. C. Section through more advanced
vesicle, eighty-three hours after coitus. Taken from uterus, c, Cavity of blas-
todermic vesicle; i, inner cell mass; w, wall of blastodermic vesicle (subzonal
layer, trophoblast).

unequal, and in many cases very irregular, so that stages of
three-, four-, five-cells, etc., may be found. The first cleavage
plane, and usually the second, pass nearly through the chief

THE EARLY DEVELOPMENT OF THE MAMMAL 383

egg axis, but the promorphological relations of these cleavages
are not known.

In a comparatively early stage the cells take on a fairly
definite arrangement. Thus on the surface of the cleavage
group we may see a regular and usually continuous, epithelium-
like layer, surrounding, or nearly surrounding, a central mass
of large, irregularly arranged cells (Fig. 148). The egg
usually remains closely surrounded by the zona pellucida dur-
ing these stages and the superficial cell layer is known as the
subzonal layer, the central mass as the inner cell mass.
This arrangement of cells forms what is known as the morula
stage, equivalent to the blastula stage of other forms. (The
identification of this stage as a gastrula ("metagastrula,"
Van Beneden) leads to some difficulties in the interpretation of
the homologies of the layers of later stages.) The fully formed
morula consists of thirty-six to seventy-two cells, of which
twenty-four to thirty compose the inner cell mass.

3. The Blastodermic Vesicle

As cleavage continues in the cells of the morula, vacuoles
appear among the cells of the inner cell mass, toward one side
of the morula only. These vacuoles rapidly enlarge and flow
together toward one pole, while the cells of the inner mass re-
main grouped together at the opposite pole (Fig. 148). The
structure thus formed is termed the blastodermic vesicle; the
fluid of the cavity is supposed to represent the yolk-mass of the
sauropsid blastula or gastrula.

In all cases the uterus is reached by the time the blasto-
dermic vesicle is formed, and the immediately subsequent
events in development may be described under two heads,
(a) the growth or enlargement of the blastodermic vesicle;
(6) the formation of the embryonic rudiment and its layers
(germ layers). The implantation or embedding of the vesicle
in the uterine wall will be described in connection with the
history of the foetal membranes. Although these processes
overlap to a considerable extent we may describe them sepa-
rately, as a matter of convenience.

384 OUTLINES OF CHORDATE DEVELOPMENT

A. THE GROWTH OF THE BLASTODERMIC VESICLE

The enlargement of the vesicle results from the flattening
of the cells of the subzonal layer, as well as from their multipli-
cation, and the wall of the vesicle thus becomes very thin
(Fig. 149). Growth of the vesicle is always rapid, and often it
becomes very large. In the rabbit the ovoid vesicle reaches
dimensions of about 4.5X3.5 mm. by the seventh day of de-

troyh

zp

FIG. 149. — Section through the fully formed blastodermic vesicle of the rabbit.
From Quain's Anatomy, after Van Beneden. fcm, Granular cells of the inner cell
mass; troph, trophoblast cell,s; zp, zona pellucida.

velopment (third day within the uterus), when implantation
commences. In the mouse the spherical vesicle is much
smaller when implantation begins. In the Ungulates the vesi-
cle becomes elongated and tapered at each end, and very large;
in the sheep the twelve-days vesicle (Bonnet) reaches a length
of more than 20 cm., its diameter being only 1-2 mm. Ulti-
mately the Ungulate vesicle may extend through the entire
uterus, and may even be folded, so that a total length of 1 m.
may be reached. In all these cases the embryonic portion of
the early vesicle is limited to a small, almost microscopic mass
about in its middle.

B. THE FORMATION OF THE EMBRYO AND THE EMBRYONIC

LAYERS

We may now return to a stage where the small blastodermic
vesicle is just established and consists of a single layer of

THE EARLY DEVELOPMENT OF THE MAMMAL 3&,

subzonal cells, with the inner cell mass suspended from its
inner surface like a hanging drop (Figs. 148, C; 149). The
first step in the differentiation of this structure consists in the
rearrangement of the cells of the inner mass so that those bor-
dering the cavity of the vesicle are formed into a definite, con-
tinuous layer, known as the embryonic endoderm (Figs. 152, 155).
The relative time at which the endoderm becomes distinct may
vary greatly. The endoderm cells multiply rapidly, and typ-
ically they spread distally over the entire inner surface of the
subzonal layer, converting the blastodermic vesicle into a two-

FIG. 150. — Diagrams of the formation of the amnion in the Insectivors. After
Keibel. Black, embryonic ectoderm; heavy stipples, trophoblast; light stipples,
endoderm; oblique ruling, mesoderm. A. Before the appearance of the amnionic
cavity. Inner cell mass differentiated into embryonic ectoderm and mesoderm;
endoderm extending completely around the wall of the vesicle. B. The amnionic
cavity (a) appearing in the ectoderm. C. Enlargement of the amnionic cavity.
Mesoderm expanded and split into somatic and splanchnic layers, separated by
the ccelom. s, Primitive streak.

layered structure, the gastrula (Figs. 150, 153, 155). In the
Primates, however, the formation of the endoderm does not
keep pace with the enlargement of the blastodermic vesicle,
so that the endoderm forms a smaller second vesicle suspended
below the inner cell mass (Fig. 161).

After the separation of the endoderm, the remainder of the
inner cell mass is known as the embryonic ectoderm. In most
instances this remains quite distinct from the original subzonal
layer, which, in view of its future function of attaching the
vesicle to the uterine mucosa, may now be termed the tropho-
blast (Hubrecht). The inner cell mass is now clearly differen-

386 OUTLINES OF CHORDATE DEVELOPMENT

tiated into embryonic ectoderm and endoderm, but before
we continue the later history of these layers, we must consider
briefly two other matters, (a) the relation between the ecto-
derm of the embryonic shield and the trophoblast cells

FIG. 151. — Sections through four stages in the early development of the
Insectivor, Tupaija javanica. From Hubrecht. A. Blastodermic vesicle com-
pletely closed; endoderm still continuous with the embryonic ectoderm. B, C.
Embryonic ectoderm split and folding out upon the surface of the vesicle,
pushing away the trophoblast cells. D. Embryonic ectoderm forming a flat disc
on the surface of the blastodermic vesicle. E. Inner cell mass ("ectodermal
shield"); ec, embryonic ectoderm; en, endoderm; tr, trophoblast.

(subzonal layer), and (6) the establishment of an important
cavity, the amnionic cavity, which first appears about this time.
There is a great deal of variation among the Mammals in the
details of these relations, and we shall attempt to give only a
very general statement of the more important conditions.

THE EARLY DEVELOPMENT OF THE MAMMAL 387

We may make a preliminary distinction between those in-
stances where the trophoblast is interrupted in a circumscribed
area, just above the embryonic ectoderm, the embryonic disc
then moving up and occupying this space, and thus acquiring a
superficial position; and others where the trophoblast remains

FIG. 152. — Three stages in the formation of the embryonic shield in the deer.
After Keibel. A. Spaces appearing in the inner cell mass. B. Fully formed
cavity (embryocyst) in the inner cell mass, which is still covered with a thin
trophoblast. C. Embryocyst opened out upon the surface, c, Ectoderm ; i, inner
cell mass; n, endoderm; s, embryonic shield; t, trophoblast; y, embryocyst.

continuous above the embryonic ectoderm, forming a complete
enveloping layer around the endoderm and embryonic shield.
The latter condition is known as the entypy of the germ.

Among the former instances we find again quite a variety of
methods by which the embryonic layers acquire their super-
ficial position. (1) In the Insectivor, Tupaija, the inner cell
mass forms a cup-shaped structure which opens out upon the
surface of the vesicle, pushing the trophoblast away (Fig. 151).
(2) More commonly, as in most Ungulates, in Tarsius, and the

388 OUTLINES OF CHORDATE DEVELOPMENT

opossum, the ectoderm moves up irregularly, gradually pushing
away the trophoblast cells (Figs. 152, 153, 157). (3) In the
rabbit, shrew, and probably in the dog, the trophoblast remains
for a time continued as a very thin layer (Rauber's layer) over

FIG. 153. — Transverse sections through the early blastodermic vesicle of the
hedgehog, Erinaceus. After Hubrecht. A. Embryonic ectoderm forming a solid
mass. Endoderm lining the entire trophoblast wall. Trophoblast becoming
trophodermic. B. Amnionic cavity established. Trophoderm formed com-
pletely around the blastodermic vesicle, a, Amnionic cavity; c, ectoderm;
d, trophoderm; n, endoderm; s, embryonic shield; t, trophoblast.

FIG. 154. — A. Section through part of the blastodermic vesicle of a six-day
rabbit. From Quain's Anatomy, after Van Beneden. B. Transverse section
through the embryonic shield of a dog of unknown age (between eleven and fifteen
days). After Bonnet, a, Trophoblast (in A, Rauber's layer); 6, embryonic
ectoderm; c, endoderm; s, embryonic shield (embryonic ectoderm); x, space in
embryonic shield.

the surface of the ectoderm of the embryonic region. Appa-
rently the thin cells of the trophoblast finally disappear, leaving
the ectoderm upon the surface, but it is possible that they mingle

THE EARLY DEVELOPMENT OF THE MAMMAL 389

indistinguishably with the cells of the ectoderm itself ; in either
case the trophoblast cells here disappear as such (Figs. 154,
157, G, H).

In the second condition mentioned, where the trophoblast
remains continuous above the embryonic layers (entypy), we
find a still greater variety in the details of the relations, which
may become very complicated. This general type of develop-
ment is found in many Primates (probably in man), many
Rodents including the mouse, rat, and guinea-pig, in the
Chiroptera (Fig. 155), and in some Insectivora including the
hedgehog (Erinaceus) Galeopithecus and Gymnura. In all these
forms a space appears in the ectoderm, known as the amnionic
cavity. This space may result from a definite splitting apart of
two cell masses (e.g., hedgehog), or it may result from the
gradual confluence of irregular spaces (e.g., bat, Fig. 155). It
is important to bear in mind that in these instances of entypy,
the true embryo develops only from the cells (ectoderm and
endoderm) lying in the floor of the amnionic cavity.

Very often the trophoblast in this region becomes thickened,
forming a trophoblastic knob ("trdger"), which enlarges and
pushes the embryonic shield down into the cavity of the blasto-
dermic vesicle (rat and mouse, for example). An additional
cavity, the false amnionic cavity, may develop within this
trophoblastic knob. This should not be confused with the
true amnionic cavity, which here forms a completely closed
vesicle, with ectodermal wall, entirely separate from the tro-
phoblastic knob, and often of considerable size, even in these
early stages (Fig. 156). A rather more special condition is
found in the guinea-pig, where the small amnionic vesicle
separates widely from the trophoblast, leaving a large space
known as the interamnionic cavity between the true and the
false amnionic cavities. The false amnionic cavity of the tro-
phoblastic knob becomes very large (Fig. 156, B), while during
these early stages the true amnionic cavity remains very small.

It is among these forms (e.g., rat, guinea-pig, etc.) that the
phenomenon of the so-called "inversion of the germ layers"
was described. It is now clear that no genuine inversion takes

390 OUTLINES OF CHORDATE DEVELOPMENT

c am a

FIG. 155. — Sections through the blastodermic vesicle, or its embryonic portion,
of the bat, Vespertilio, showing the formation of the amnionic cavity. After Van
Beneden (Brachet). A. Section passing through the inner cell mass showing the
very beginning of the amnionic cavity. B. Amnionic cavity clearly indicated as
irregular spaces. The endoderm is torn away from its normal position under
the embryonic ectoderm. C. Thickened trophoblast now a syncytiotrophoblast.
D. Amnionic cavity fully established. The endoderm is torn away from the
wall of the vesicle at its ends, a, Amnionic cavity; am, amnion; 6, capillaries of
the uterine wall; c, embryonic ectoderm; e, endoderm; i, inner cell mass; s,
syncytiotrophoblast; t, trophoblast; v, cavity of blastodermic vesicle.

THE EARLY DEVELOPMENT OF THE MAMMAL 391

place, but the basis of the phrase is clear. The enlargement of
the trophoblastic knob with its false amnionic cavity, pushes
the embryonic ectoderm cells far down within the cavity of the
blastodermic vesicle; this is especially marked in the guinea-
pig. Then as the endoderm cells spread out over the inner
surface of the embryonic ectoderm (Fig. 156) they may extend

FIG. 156. — Diagrams of the relations of the cavities and layers in the rat,
showing the "inversion" of the germ layers. After Selenka. Median sagittal
sections. Embryo and amnion, black; ectodermal knob or "trager" in light
tone; endoderm and mesoderm in darker tone. A. Early stage before the for-
mation of the false amnionic cavity. B. Late stage showing false and true
amnionic cavities and the interamnionic cavity, a, Amnion; ac, true amnionic
cavity; c, chorion; E, embryo (anterior end); ea, endodermal rudiment of
allantois; /, false amnionic cavity; i, interamnionic cavity; m, mesoderm; ma,
mesoderm of allantois; n, endoderm; o, trophoblast (ectoderm); p, anterior
intestinal portal; ra, rudiment of true amnionic cavity; rf, rudiment of false
amnionic cavity; s, marginal sinus; t, "trager" (ectoderm); y, yolk-sac; ye, yolk-
sac endoderm; x, amnionic folds.

over the walls of both the true and the false amnionic cavities,
so that the embryonic ectoderm appears to lie within an endo-
dermal sac (Fig. 156, A). When the embryo itself begins to
be differentiated in the floor of the true amnionic cavity it is
thus already surrounded by this endodermal layer, and the
appearance of an inversion of the layers is produced. Con-
sideration of the entire series of conditions mentioned above
demonstrates the absence of a true inversion of the germ
layers.

392 OUTLINES OF CHORDATE DEVELOPMENT

G

FIG. 157. — Diagrams of the formation of the amnion. After Keibel. A-F,
in Ruminants, pig, and Mammals, with entypy of the germ. G, H, in the Carniv-
ora. Black, embryonic ectoderm; heavy stipples, trophoblast; light stipples,
endoderm; oblique shading, mesoderm. A. Morula. B. Early blastodermic
vesicle; endoderm limited to embryonic region. C. Formation of cavity in the
embryonic ectoderm (embryocyst). Extension of the endoderm. D. Embryo-
cyst opening out; embryonic disc becoming superficial. Endoderm completely
lining the vesicle. E. Embryonic disc or shield superficial in position (compare
H). F. Formation of amnionic folds, primitive streak, and exocoelom. G. Early
carnivor blastodermic vesicle. H. Embryonic shield superficial in position (com-
pare Fig. 154, B.) A later stage would be identical with F. a, Amnionic folds;
c. embryocyst; e, exocoelom; p, primitive streak; s, embryonic shield.

THE EARLY DEVELOPMENT OF THE MAMMAL 393

An interesting condition, transitional between the two
general classes described above, is found in the mole. Here
spaces form between the ectoderm and the continuous tropho-
blast, which flow together as in the bat, forming a definite
amnionic cavity. This cavity is then obliterated by the re-
fusion of the ectoderm and trophoblast, resulting in a con-
dition similar to that of the shrew and rabbit. Then the
superficial cells of the trophoblast disappear, leaving the ecto-
derm on the surface of the blastodermic vesicle.

The formation of the amnionic cavity has not been mentioned
in forms where the embryonic disc becomes superficial in posi-
tion. In these instances the amnionic cavity is formed in a
manner entirely different from that described above. Here
a system of amnionic folds, much like those of the chick, appears
just outside the embryonic region proper. These folds grow
up over the embryo, establishing an amnionic cavity in which
the embryo is enclosed (Figs. 157, 176). The history of the
amnion will be taken up later, in connection with the other
embryonic membranes.

We may consider now the processes leading to the formation
of the definitive embryo. To give a comparative account of
these processes as they occur in the whole group of Mammals
would carry us far into details, as there is wide variation even
within this single class, and we shall, therefore, describe these
phenomena as they are found in such a form as the rabbit or
dog, forms whose early history is comparatively well known.

Of the entire blastodermic vesicle, with its complicated
associated structures, the only truly embryonic portion is
found in a restricted portion of the embryonic ectoderm and
endoderm known as the embryonic shield (Figs. 151-155, 157,
158, A). (We should note that in the rabbit the endoderm
does not come to line the entire blastodermic vesicle until a
relatively late stage, so that throughout early development
only the upper portion of the vesicle is two-layered.) In the
rabbit the embryonic shield first becomes visible about the
fifth day, when the blastodermic vesicle is still spherical and
only about 1.5 mm. in diameter. By the seventh day the

394 OUTLINES OF CHORDATE DEVELOPMENT

pr.s

B

FIG. 158. — A. Surface view of embryonic shield of a dog of thirteen to fifteen
days. B. Surface view of embryonic shield of dog showing medullary plate,
etc. From Minot (Laboratory Text-Book of Embryology), A, after Bonnet.
A.o., Area opaca; A. p., area pellucida; Kn., Hensen's knot or node; Md.,
medullary plate; md.F., medullary furrow; ps., pr.s., primitive streak; Sh.t
embryonic shield.

THE EARLY DEVELOPMENT OF THE MAMMAL 395

embryonic shield forms a well-marked oval thickening about
1.5X1.0 mm., the entire vesicle at this time measuring about
4.5X3.5 mm.

Sections through the embryonic shield show that it is formed
largely by a circumscribed thickening of the embryonic ecto-
derm, three or four cells deep, beneath which the endoderm
remains only one cell in thickness (Fig. 154). Over the surface
of the shield the original trophoblast cells (Rauber's layer) are
no longer distinguishable. Peripherally the shield passes into
the thinner extra-embryonic ectoderm, or trophoblast of these
forms.

The next phase of development is indicated (rabbit, about the
end of the seventh day, dog, about thirteen to fifteen days) by
the appearance of a slight opacity toward the middle of the em-
bryonic shield. This is known as the primitive knot or Hensen's
node. Usually the primitive knot is eccentric in position,
toward what proves to be the anterior margin of the shield.
At about this same time, or even before Hensen's node is dis-
tinctly visible, an opaque line appears across the shield, extend-
ing from the node to the posterior margin of the shield, where
it joins an opaque crescent-shaped region (Fig. 158, A). This
line is the primitive streak, and usually, along its middle can be
seen the clearer primitive groove (Figs. 157, F; 159). A little
later a less distinct opaque line may be seen extending a short
distance forward from Hensen's node; this is the head process.

These superficial appearances in the embryonic shield may be
understood only by the examination of sections. Sections
across the primitive streak of the rabbit or mole, for instance,
show that the opacity of the region is due to a very marked
thickening of the ectoderm, with which is associated the forma-
tion of the middle layer or mesoderm. A section like that
illustrated in Fig. 159, A, shows the primitive streak to be a
region of rapid cell proliferation in the ectoderm. From the
sides and inner surface of the primitive streak cells are given
off which gradually take on the arrangement of a definite layer
quite distinct from the ectoderm, and between the ectoderm
and endoderm. This is the mesoderm which here, therefore,

396 OUTLINES OF CHORD ATE DEVELOPMENT

as in the chick, is in its origin more closely associated with the
ectoderm than with endoderm. Sections through Hensen's
node show that this is a region of thickened ectoderm and
mesoderm, less clearly differentiated from one another than in
the primitive streak region. The endoderm, however, is not
fused with the other cells, as it is in the chick. And in front

FIG. 159. — A. Transverse section through the primitive streak of the mole.
J5. Transverse section through a human embryo of 1.54 mm. (Graf von Spec's
Embryo Gle.) From Minot (Laboratory Text-book of Embryology, after Heape
(A), and Graf von Spec (B). ch, Notochord; ct, somatic mesoderm; df, splanch-
nic mesoderm; EC, ek, ectoderm; en, En, endoderm;/, dorsal furrow; g, junction
of extra-embryonic somatic and splanchnic mesoderm; me, mes, mesoderm; p,
rudiment of embryonic ccelom; p.gr., primitive groove; Pr, primitive streak.

of Hensen's node, in the region of the head process, mesoderm
is present, though entirely separate from the ectoderm, indicat-
ing its origin from the region of Hensen's node and not directly
from the ectoderm of the head process region.

Later on conditions are found which make possible very close
comparison between the primitive streak and associated struc-
tures of the Mammal with those of the chick. Within the head
process, or in the region of Hensen's node, a rearrangement of

THE EARLY DEVELOPMENT OF THE MAMMAL 397

cells produces a small cavity known as the notochordal canal.
This varies greatly in extent. In such forms as the guinea-pig
and bat, the canal is comparatively long, extending from Hen-
sen's node, where it opens upon the surface by a definite per-

FIG. 160. — A. Sagittal section through the embryonic shield of the hedgehog,
showing the transitory blastopore. After Hubrecht. B. Posterior part of a
sagittal section through the embryonic disc of the mole. C. Diagram of a
aagittal section through the embryonic disc of the mole. From McMurrich
(Development of the Human Body), after Heape. am, Amnion; bl, blastopore;
ce, chorda endoderm; ec, ectoderm; en, endoderm; nc, neurenteric canal; prm,
prostomial mesoderm; ps, primitive streak; t, trophoderm.

foration through the ectoderm, anteriorly and ventrally;
finally either opening through the endoderm into the cavity
of the endodermal vesicle (Fig. 160, C), or simply ending blindly

398 OUTLINES OF CHORDATE DEVELOPMENT

'among the cells of the head process. In other forms, such as
the sheep, pig, or hedgehog, and in man, the notochordal canal
is simply a vertical perforation through the embryonic layers,
connecting the cavity of the endodermal vesicle directly with
the outside (amnionic cavity) (Figs. 160, A; 161, Z>). And in
still other forms the canal may never quite perforate the layers
of the shield (mole) ; or it may be reduced to a simple groove
on the lower surface of the shield (rabbit, Fig. 160, B).

Sections through the notochordal canal reveal an arrange-
ment of the germ layers which is practically that found around
the more typical blastopore of the yolk-filled egg. In this
region the layers are continuous with one another and the primi-
tive groove may be deepened into a sort of " primitive pit"
(compare chick). Altogether then we may recognize in the
primitive streak of the Mammal the essential equivalent of the
similarly named structure in the Sauropsida. The notochor-
dal canal therefore becomes the modified equivalent of the
blastoporal remains.

When the notochordal canal has the form of a simple perfora-
tion it may therefore correctly be termed the neurenteric canal,
marking the posterior limit of the embryonic rudiment. The
primitive streak, representing the modified and fused blasto-
poral lips, is here, as in the chick, a region from which the
structures of the embryo are derived and differentiated in the
antero-posterior direction, again much as in the chick.

All details regarding the formation of the embryonic layers
and organs are to be omitted from the present account. It
must suffice to say. that a typical medullary plate is formed,
medullary folds appear and fuse, forming a neural tube (Figs.
158, B; 159, B). A typical notochord is. differentiated, run-
ning forward from the primitive knot. The mesodermal layer
rapidly extends laterally from the axial region, finally passing
widely beyond the embryonic region and taking a very impor-
tant part in the development of the extra-embryonic structures.
The mesodermal sheet is very early split into somatic and
splanchnic layers by the appearance of a coelomic cavity; both
embryonic and extra-embryonic.

THE EARLY DEVELOPMENT OF THE MAMMAL 399

III. THE DEVELOPMENT OF THE EXTERNAL FORM
OF THE HUMAN EMBRYO

The earliest phases in the development of the human organ-
ism, up to the formation of the primitive streak, are not known
at all, and it is not until the medullary plate stage is reached
that the structure of the human embryo is fully known.
Scarcely half a dozen embryos younger than this have been
described. It is clear, however, that the processes leading to
the formation of the embryonic layers, the amnionic cavity,
etc., are in general similar to those found among the rat, mouse
and bat. That is, the amnionic cavity is formed by delamina-
tion, between the continuous trophoblast and the embryonic
ectoderm. The endodermal vesicle is much smaller than the
ectodermal trophoblastic vesicle, leaving a wide space between
the two layers (Fig. 161). When the mesoderm forms it ex-
tends rapidly through the extra-embryonic region of the blasto-
dermic vesicle, one layer (somatic) applied to the inner surface
of the trophoblast, the other (splanchnic) applied to the outer
surface of the endodermal vesicle, so that the large cavity of the
blastodermic vesicle becomes, in effect, an extra-embryonic
coelomic space. The layer of endoderm with the splanchnic
mesoderm is at first the yolk-sac, although of course entirely
yolkless, while the ectodermal trophoblast with the somatic
mesoderm forms the chorion. (Further reference to the chorion,
as well as to the amnion and the allantois, is deferred until a
later section.)

The reader should note that students of mammalian develop-
ment use the term "ovum" to designate any early stage in
development. In this connection the "ovum" includes not
only the embryo proper, but also all of the associated struct-
ures of the blastodermic vesicle.

As the embryo enlarges, its posterior end remains attached
to the inner surface of the trophoblastic wall by a mass of meso-
derm cells. This attachment is known as the body stalk or
belly stalk. Sections through an early embryo would give,
therefore, the appearance shown in Figs. 161, D; 179, A, B.

400 OUTLINES OF CHORDATE DEVELOPMENT

nc

FIG. 161. — Diagrams of sagittal sections through the human blastodermic
vesicle, showing the formation of the amnion and trophoderm. A-D, after
Keibei and Elze. E, From McMurrich (Development of the Human Body),

THE EARLY DEVELOPMENT OF THE MAMMAL 401

A slightly later stage is shown in sagittal section in Fig. 161, E.
At this time the embryo (Graf Spec's embryo Gle) measures
1.54 mm. in length by about 0.7 mm. in greatest breadth, while
the entire vesicle ("ovum") is approximately 10 mm. in di-
ameter. Its dorsal surface is occupied by the large neural
plate, with a distinct neural groove. Toward the posterior end

FIG. 162. — Young human embryos. After Keibel and Elze. A. Keibel and
Elze's Embryo Klb, X 25. B. Kollmann's Embryo Bulle, X 20. For de-
scription, see text.

is the small neurenteric canal, behind which may be seen a short
primitive streak and groove. A short thick body stalk attaches
the embryo to the chorionic wall of the blastodermic vesicle.
The wall of the ovoid yolk-sac, whose diameters are about
equal to the length of the whole embryo, is already quite

after Graf von Spee. In all the figures the anterior end is toward the left
Black, embryonic ectoderm; heavy stipples, trophoblast and trophoderm; light
stipples, endoderm; oblique ruling, mesoderm. A. Hypothetical early stage;
mesoderm a solid mass. B. Amnionic cavity and wide exoccelom established;
endoderm limited to a small vesicle beneath the embryonic ectoderm. The
exoccelom in reality contains scattered mesenchyme cells. C. Blastodermic vesi-
cle enlarged and covered with trophodermic villi, into which the mesoderm is ex-
tending. Endodermic vesicle (yolk-sac) very small (stage of Peter's ovum).
D. Embryonic portion only, of an older vesicle showing the neurenteric canal,
primitive streak (in the plane of the section), and body stalk. The mesoderm
of the yolk-sac is becoming vascular. E. Sagittal section through the human
embryo of 1.54 mm. (Graf von Spec's embryo Gle). a, Amnionic cavity; al,
allantois; am, amnion; B, body stalk; ch, chorion; e, exoccelom; h, heart region;
nc, neurenteric canal; V, chorionic villi; Y, yolk-sac.

402 OUTLINES OF CHORDATE DEVELOPMENT

vascular. The notochord is distinctly differentiated posteriorly,
and the embryonic mesoderm is only incompletely separated
into somatic and splanchnic layers (Fig. 159, B), although in
the extra-embryonic region there is a very wide coelom.

A sagittal section through this embryo shows that it is some-
what arched over the dorsal surface of the y oik-sac , and that an
endodermal outgrowth, the rudiment of the allantois, is extend-
ing into the mesoderm of the body stalk (Fig. 161, E).

Shortly after this, in an embryo measuring 1.8 X 0.9 mm.
(Keibel and Elze's embryo Klb.) the neural folds become very
prominently elevated and the head and tail regions project
slightly above the surface of the yolk-sac, as shown in Fig.
162, A. This figure shows also the persistent neurenteric
canal, and the very short primitive streak. Five or six pairs
of mesodermal somites are now present.

The head region now commences to enlarge rapidly although
the neural groove is still open. In an embryo of 2.36 mm.
length (Kollmann's embryo, Bulk) illustrated in Fig. 162, B,
the body is concavely arched toward the yolk-sac, while the
head and tail regions show distinct downward flexures. The
elementary divisions of the brain are already indicated, and the
fore-brain is protecting downward from the anterior end of the
neural axis. Though not shown in the figure the paired rudi-
ment of the heart is present. About fifteen pairs of somites
are visible externally.

As the embryo now begins to elongate rapidly it becomes
clearly folded off from the extra-embryonic structures, and the
opening of the yolk-sac out of the endodermal gut cavity of the
embryo becomes relatively, though not actually, narrower.
The yolk-sac thus appears to be attached to the embryo proper
by a narrow stalk, the yolk stalk, the connection of which, with
the embryo, is the yolk stalk umbilicus.

By the time the embryo reaches a length of. 2.5 mm. (Koll-
mann's embryo, 2.5 mm., age given as thirteen to fourteen days,
but probably much older) the high neural folds have begun to
close together posteriorly (Fig. 163). The head region is con-
siderably enlarged and extends downward in front of the heart,

THE EARLY DEVELOPMENT OF THE MAMMAL 403

which is now very large and clearly differentiated into regions
by the development of flexures.

The length of the embryo now affords a very unsatisfactory
index of the age or degree of development on account of the
considerable variability, and because of the bendings which
appear in the longitudinal axis. Apparently, shortly after
this time, the body becomes sharply bent downward into a
U-form just opposite the umbilicus, producing what has been
called the dorsal flexure. That this is entirely normal is,
however, still open to question.

Hfr

FIG. 163. — Human embryo of thirteen or fourteen days. From Minot
(Laboratory Text-book of Embryology), after Kollmann. Al, Body stalk;
Am, amnion; Ht, heart; Md, medullary groove; ST, seventh somite; Yks, yolk-

Figure 164 illustrates an embryo, enclosed in the amnion
and with yolk-sac attached, whose length, in a straight line, is
2.6 mm. and whose age was originally estimated at eighteen
to twenty-one days, though very probably it was approximately
one month (His's embryo, M). The entire blastodermic vesicle
or chorionic vesicle ("ovum") still measures approximately
10 mm. in diameter. This embryo shows many important
advances. No trace of the dorsal flexure remains, while both
the anterior and posterior extremities of the embryo are now
bent downward and inward. The body is also slightly twisted
so that the head lies toward the left, the tail toward the right
(the direction of this twisting is not fixed, for in other embryos
it may be in the opposite direction). The yolk-sac is some-

404 OUTLINES OF CHORDATE DEVELOPMENT

what shrunken and elongated, and the yolk stalk is clearly
distinguishable. Topographically the most anterior part of the
embryo is formed by the mid-brain, beneath which the fore-
brain is now folded back toward the heart. The heart is very
prominent and on the sides of the neck region three pairs of
gill clefts are indicated, decreasing in size posteriorly. Four
pairs of visceral arches (mandibular, hyoid, two branchial) are
thus marked out, and the most anterior (mandibular) already

FIG. 164. — Human embryo of 2.6 mm. From Minot (Laboratory Text-book
of Embryology), after His. The embryo is enclosed in the amnion and shows
the maxillary and mandibular processes, the rudiments of three gill clefts, and
the large heart. The large yolk-sac extends ventrally, while posterior to its origin
the root of the body stalk is shown turned dorsally.

shows signs of its transverse division into upper and lower
portions, the maxillary and mandibular processes. Later a
fourth cleft and fifth arch are indicated. Of course in the
Mammal actual gill clefts are not present as perforations; the
so-called clefts are vestigial structures and, excepting the first,
merely form superficial grooves, opposite corresponding pockets
out of the pharyngeal cavity. An anterior depression, the
oral sinus (stomodaBum) between the mandibular arches, marks
the position of the future mouth, which is perforated very
shortly after this time.

THE EARLY DEVELOPMENT OF THE MAMMAL 405

Just a few words may be added concerning the internal
structure of this embryo (Fig. 165). The slender notochord
extends the entire length of the body and tail. Optic vesicles
are distinct and the otocysts are entirely closed off below the
surface. The expanded pharynx shows an anterior hypo-
physial outgrowth, in addition
to the lateral branchial pockets.
A small rudiment of the lung
is indicated, and at the pos-
terior end of the narrowed
oesophagus the liver rudiment
is well marked. Posterior to
this the gut is open into the
yolk-sac by way of the yolk
stalk, and continuing poster-
iorly from this is the narrow
intestine, which, near its ex-
tremity, sends a small allan-
toic outgrowth into the body
stalk. Rudiments of the
mesonephros (Wolffian body)
and its duct are slightly in-
dicated.

The vascular system is very FlG- ^.—Reconstruction of a hu-

. man embryo of 2.6 mm. (See Fig.

Well developed. Opening into 164). From Minot (Laboratory Text-
ji ^ i f ji ^ i , book of Embryology), after His. A,

the posterior end of the heart Aortic limb of yhea£/' AUi body staik';

there are, the paired ductuS ^°> dorsal aorta; Au, umbilical arter-

~ . . ,. , , ies; Car, posterior cardinal vein; Jg, an-

LUVien, lormed by anterior terior cardinal vein (jugular vein). Om,

flnH nn^terinr oarHinal vpinq omphalomesenteric vein; op, optic ves-

an(1 P° lmal V€1QS> icle; ot, otocyst; Vh, right umbilical

the paired vitelline or omphalo- vein.
mesenteric veins, coming from

the yolk-sac by way of the yolk stalk, and the paired allantoic
or umbilical veins coming from the allantoie region by way of
the body stalk. Opening out of the anterior end of the heart
is the ventral aorta, which immediately divides into right and
left halves from each of which arise five aortic arches passing
through the visceral arches to the dorsal side of the pharynx,

Vh.

Car:

406 OUTLINES OF CHORDATE DEVELOPMENT

where they reunite into the dorsal aorta. A small anterior
carotid artery appears a little later. From the dorsal aorta is

given off a pair of small
mtelline arteries supply-
ing the yolk-sac, while
al posteriorly the dorsal
aorta divides into a pair
of umbilical or allantoic
arteries, passing through
the body stalk and sup-
plying the allantois.

As the head now en-
larges rapidly a well-
marked flexure (cervical
about n'exure) appears just back
of the gill cleft region,
while through the entire
body and tail a strongly
marked curvature ap-
pears, so that head and
tail are almost brought in contact, and the entire embryo is
almost circular in general
outline (Fig. 166). The fore-
and hind-limb buds have ap-
peared as low, extended ele-
vations, and the abdominal
region is becoming promi-
nent on account of the
growth of the liver and
other viscera. The ventral
body wall now becomes more
completely closed together,
and the tissues (somatopleu-
ral) at the base of the body
stalk grow forward enclosing

the root of the yolk Stalk for FIG. 167. — Human embryo of about 9.3
, -,. , ,, mm. After Hochstetter, X 6 2/3.

a Snort distance, SO that a For description see text.

B.S

FIG. 166. — Human embryo of
twenty-three days (4.0 mm.). From Minot
(Laboratory Text-book of Embryology),
after His (Embryo a), al, Fore-limb bud;
BS, body stalk; Op, optic vesicle; pi, hind-
limb bud; IV, fourth ventricle of brain; 1,
mandibular process; 2, hyoid arch; 3, 4, third
and fourth visceral arches.

THE EARLY DEVELOPMENT OF THE MAMMAL 407

single stalk from the embryo now carries both the yolk stalk
and the allantoic stalk. This is known as the umbilical stalk
or cord, and its attachment to the embryo is the umbilicus.
Ultimately the entire yolk stal£ becomes enclosed in the um-
bilical cord, and the yolk-sac itself is surrounded by the tis-
sues of the placenta as described below.

Up to this time the correlation between age and size of the
embryo is very uncertain. According to the careful studies of
Mall the ages of most of the early embryos have been under-
estimated, and it is very probable that the events thus far
described have occupied about the first month of development.
From this time on, however, the age of the human embryo is
more certainly determined.

During the sixth week of development the embryo measures
9.0-10.0 mm. in a straight line drawn from the apex of the
mid-brain to the sacral flexure or rump ("crown-rump"
length) (Fig. 167). The head, still the largest part of the
embryo, is beginning to be elevated on account of the straight-
ening out of the cervical flexure, and the whole body shows
considerably less curvature than before. A lense has been
formed opposite the small optic vesicle, and a pair of well-
marked olfactory pits has appeared on the under side of the
head, in front of the maxillary processes. Both maxillary and
mandibular processes are more prominent, while the posterior
visceral arches and clefts have become sunk in a depression,
the margins of which have nearly closed together forming a
cavity below the surface known as the cervical sinus. The
most anterior gill cleft (hyomandibular) is not included in this
cervical sinus, but in part remains on the surface of the neck, as
the rudiment of the external auditory meatus. The cervical sinus
later disappears entirely, along with the posterior gill clefts.

The ventral body region is still protuberant, and anteriorly
three elevations can often be observed, marking the under-
lying auricle, ventricle, and liver. The limbs are somewhat
elongated, and the fore-limbs, which are always in a more
advanced stage than the hind-limbs, show some indications of
differentiation of the hand. The umbilical cord is elongating

408 OUTLINES OF CHORDATE DEVELOPMENT

and the tail has reached nearly to the condition of its greatest
development.

The further development of the general bodily topography
may be sketched very briefly with the aid of the accompanying
figures (Figs. 168, 169, 170). During the latter part of the
second month (Fig. 169) the head continues to be elevated
rapidly, and the body to straighten. The head is now at its

FIG. 168. — Human embryo of 14.5 mm. (thirty-six days) showing thick um-
bilical cord, and yolk-sac at the end of the slender yolk stalk. After Minot.
X 4.3. For description see text.

greatest relative size, constituting about 45 per cent, of the
total weight of the embryo (Jackson). The pinna of the ear
is formed from elevations of the first and second visceral arches
around the external auditory meatus. The rudiments of the
eye are fully established and the eyelids are formed. The
ventral body wall still remains protuberant. The proximal
end of the umbilical cord becomes considerably expanded, and
into its extra-embryonic coelomic cavity extend several coils of
the embryonic intestine and even a portion of the liver. This
characteristic extension of the intestine (intestinal hernia)

THE EARLY DEVELOPMENT OF THE MAMMAL 409

reaches its maximum during the second month. The intestine
is rapidly withdrawn later and at about nine or ten weeks is
completely retracted into the embryonic body cavity. Beyond
this expanded region the umbilical cord is considerably elon-
gated and begins to show its characteristic spiral twisting. The
yolk stalk is correspondingly elongated and. now loses its
endodermal cavity.

FIG. 169. — Human embryo of 22.8 mm. (fifty-three days).
X4. For description see text.

After Minot,

The limbs grow rapidly during this month; they become dif-
ferentiated into their three chief regions, and in the hand and
foot the digits become clearly differentiated (Figs. 168, 169).
By the end of this month the limbs project beyond the outlines
of the body. The tail gradually recedes and by the time the
embryo is two months old is scarcely visible externally. The
structures of the facial region develop rapidly during this

410 OUTLINES OF CHORDATE DEVELOPMENT

month (see below), and at its close the embryo acquires a-
distinctly "human" aspect and is generally known as a "foetus"
in distinction from the earlier "embryo."

FIG. 170. — Outlines of human embryos of 106 to 110 days (118 to 120 mm.).
From Minot (Laboratory Text-book of Embryology). The figure to the left
shows the most frequent position of the embryo in utero; that to the right shows
the position assumed when removed from the embryonic membranes.

The external form changes now become relatively slower. The
outlines of the head become more rounded; the facial characters
are more fully established; the eyelids close together. The
abdominal region recedes, the limbs become slender, elongated,
and flexed. The foetus is in a position of constraint within the
uterus, as shown in Fig. 170 from Minot.

THE EARLY DEVELOPMENT OF THE MAMMAL 411

The general changes in size and weight of the embryo and
foetus during the entire intra-uterine period are summarized in
the accompanying table.

TABLE SHOWING THE AVERAGE WEIGHT AND LENGTH OF
THE HUMAN EMBRYO AND FCETUS.

Compiled from Jackson (weight) and Mall (length). (The column headed
CH gives the length as measured in a straight line from the crown of the head
to the heel; that marked CR gives the "sitting height," or length from the
crown to rump or sacral flexure.)

Length

Weight

CH

CR

Ovum (estimated).

0. 000004 grm.

28 days. .

0.04*

2.5 mm.

2.5 mm.

56 days.

3.0

30.0

25.0

84 days.

36.0

98.0

68.0

112 days.

120.0

180.0

121.0

140 days.

330.0

250.0

167.0

168 days.

600.0

315.0

210.0

196 days.

1000.0

371.0

245.0

224 days.

1500.0

425.0

284.0

252 days.

2200.0

470.0

316.0

270 days.

500.0

336.0

280 days.

3200.0

Before leaving the subject of the development of external
form we should add a few details regarding the development
of the facial characteristics and of the external genitalia.

THE DEVELOPMENT OF THE FACE

We may take as our starting point here, a stage of 2.6 mm.
(probably about thirty days) already described and figured
(Fig. 164). At this time the first gill cleft is unreduced, the
otocyst is not yet closed, and the optic vesicles are entirely lateral
in position. The fore-brain region hangs down over the deep

* Age probably underestimated.

412 OUTLINES OF CHORDATE DEVELOPMENT

oral sinus (stomodseum), the floor of which is still formed by
the im perforate oral membrane. Within the next few days this
membrane becomes perforated by the mouth opening. The
oral sinus is bordered posteriorly by the mandibular processes,
which do not quite meet in the mid-line, and antero-laterally
by the maxillary processes, which are widely separated medially,
the interval being occupied by the frontal process, a ridge over
the surface of the fore-brain.

FIG. 171. — Early stages in the development of the head and face. After
Rabl. A. Head of a human embryo of 8.3 mm., seen from in front (ventrally).
B. Head of human embryo of about 12 mm., seen from in front. For explanation
see text.

An important advance is to be seen in the development of
the olfactory pits, which appear at the ends of the frontal
process. Bordering the olfactory pits are inner or medial
and outer or lateral elevations or olfactory processes (Fig. 171,
A). The maxillary and mandibular processes are now closer
together so that the opening of the oral sinus (now called the
mouth) becomes a transversely elongated slit.

In the embryo of the fifth to sixth week (Fig. 171, B) the
olfactory pits have deepened and have moved in toward the
mid-line, thus separating the mouth from the fore-brain or
forehead region. At the same time the medial and lateral
olfactory processes become more prominent, and the former are

THE EARLY DEVELOPMENT OF THE MAMMAL 413

uniting with the maxillary processes of the first visceral arch
to form the rudiments of the upper jaw and lip. The man-
dibular processes are still separated medially by a groove.
During the sixth week the eyes become visible from in front,

FIG. 172. — The development of the face of the human embryo. After Retzius.
A. 18 mm. embryo, X4. B. 25 mm. embryo, X4. C. 42.5 mm. embryo, X2.
D. 117 mm. embryo, X4/5. For explanation see text.

the upper lip begins to enlarge though still indented medially,
the mandibular processes fuse completely forming the com-
pleted rudiment of the lower lip and jaw, and the chin appears.
The medial olfactory processes (globular processes) soon fuse
together forming the nasal septum (Fig. 172, A), and the nose
becomes slightly marked off from the forehead by a groove.

414 OUTLINES OF CHORDATE DEVELOPMENT

The chin gradually enlarges, and the lips, now both complete
medially, continue to enlarge (seventh week). At about eight
weeks (Fig. 172, B) the eyelids are forming, and the eyes, now
rapidly approaching one another, are separated from the fore-
head by oblique supraorbital folds. The ears now are marked
by well-developed pinnae, but still lie far down toward the neck,
below the level of the mouth. The mouth is less extended
transversely and the nose is completely separated from the
forehead.

During the next week or ten days (Fig. 172, C), the eyelids
close, the eyes move closer together, and the height of the fore-
head increases. The nose, though still very broad, begins to
project slightly, and the external nares become temporarily
closed by epidermal proliferations. The ear gains a somewhat
higher position. The mouth is smaller, the lips thinner, and
the lower jaw quite prominent. During the third month (Fig.
172, D), the pinna reaches nearly its adult position, the nose
projects markedly, the lips, especially the upper, become thin-
ner and protruded, and the essentials of the adult physiognomy
are fairly established.

THE DEVELOPMENT OF THE EXTERNAL GENITALIA

The end of the gut posterior to the origin of the allantois
(see below) forms the dilated cloaca, which is separated from
the surface of the body by a thin portion of the body wall
known as the cloacal membrane (Fig. 173, A). This membrane
is later depressed below the surface of the body, at the bottom
of a shallow depression (proctodseum). The cloacal cavity
becomes divided into a ventral portion, the urinogenital sinus,
receiving the openings of the excretory and reproductive ducts
and the allantois, and the rectal portion. The cloacal mem-
brane is correspondingly divided into the urinogenital mem-
brane and the anal membrane, the two being separated by a
narrow bridge of tissue forming the perineal rudiment.

In order to find the earliest traces of the external genitalia,
we must go back to the embryo of the early part of the second

THE EARLY DEVELOPMENT OF THE MAMMAL 415

month. Here we find a pair of ridges, either side of the cloacal
membrane (Fig. 173, A), which gradually fuse and enlarge
anteriorly, forming, toward the close of this month, a distinct
cloacal tubercle. The urinogenital membrane is perforated

ug

FIG. 173. — The development of the external genitalia. A, -After Keibel.
B-E, After Felix, from Meyer. A. Model of the cloacal region of a human
embryo of 3 mm. B. Ventral view of the caudal end of a human embryo of
18mm. C. Same of 28 mm. Indifferent stage. D. Same of 32.5 mm. Female.
E. Same of three and one-half months. Male, a, Anal opening; g, genital ridge;
gc, glans clitoridis; gp, glans penis; h, hind-limb; Im, labia majora; m, cloacal
membrane; ms, median scrotal rudiment; p, phallus; r, cloacal ridge; s, scrotal
ridge; t, coccygeal tubercle; u, umbilical cord (in A, umbilicus;) ug, urinogenital
aperture.

about this time by the urinogenital aperture. (The time at
which the anal opening is formed is quite variable, but usually
is also toward the close of the second month.)

Upon the cloacal tubercle, and toward its posterior or anal
side, there grows out quite rapidly a definitely circumscribed
process called, at this stage, the phallus (Fig. 173, B). The

416 OUTLINES OF CHORDATE DEVELOPMENT

remainder of the cloacal tubercle, at the base of the phallus and
mostly anterior and lateral to it, is now known as the genital
tubercle. The urinogenital aperture is continued forward upon
the posterior (ventral) surface of the phallus as a narrow groove,
the lateral margins of which are somewhat elevated as the
genital folds, which gradually enlarge and so reduce the urino-
genital aperture to a narrow elongated slit.

By the beginning of the third month (Fig. 173, C) the phallus
has enlarged considerably, and its extremity has dilated as the
rudiment of the glans. Lateral to each genital fold a second,
larger ridge, the genital swelling, has appeared. This marks the
end of the so-called indifferent period, during which there is
but very slight external differentiation between the sexes. As
a matter of fact, the sex of the individual is determined at the
time of fertilization, and even during the latter part of this
"indifferent period " the female embryo can be distinguished
by the presence of a groove around the base of the phallus,
which is lacking in the male.

The later development may be sketched very briefly. In
the female, where the modifications are less extensive, the
glans and the anterior (oral) portion of the phallus are trans-
formed into the clitoris (Fig. 173, D), while the posterior
(anal) portion of the phallus together with the lateral margins
of the urinogenital aperture, become the labia minora. The
labia major a are formed from the genital swelling and the
genital tubercle (basal portion of the cloacal tubercle).

In the male (Fig. 173, E), the entire phallus is transformed
into the penis, composed of the glans plus the shaft, the pos-
terior (anal) portion of which is therefore equivalent to the labia
minora. The anterior extension of the urinogenital aperture
upon the male phallus is enclosed by the fusion of the genital
folds and so added to the lower part of the urethra. The
genital swellings in part fuse and are transformed into the
scrotal sac, and in part disappear, to be replaced by other
scrotal swellings which form the remainder of the scrotal sac.
The essentials in the history of the external genitalia may be
summarized as follows

THE EARLY DEVELOPMENT OF THE MAMMAL 417

Indifferent Period

Female

Male

Early

Late

Urinogenital aperture

Vestibule

Terminal portion urethra

1 Anterior

In part, portion of

Ger

ital Genital ! portion

Mons Veneris 1

scrota! sat;

Scrotal

tub
Cloacal

ercle swelling f Lateral
J portions

Labia majora J

In part, replaced by
scrotal swellings

sac

tubercle

Glans

Glans and anterior

Phs

illus ' [ Anterior

Clitoris

portion shaft

e, ,, J portion I
Shaft } Posteriori

Penis

( portion }•
Genital folds J

Labia minora

Posterior portion
shaft J

IV. THE EMBRYONIC MEMBRANES AND APPEND-
AGES OF THE EUTHERIAN MAMMALS

Scattered references have been made in the preceding pages
to various details regarding the development of the amnion,
the chorion, the allantois, and yolk-sac, and we must now give,
possibly with some repetition, a more connected, though brief,
account of the development of these structures. There is in
general a remarkable similarity between the early history of
the embryonic appendages of the Mammals and those of the
Sauropsida, a similarity that is the more remarkable when the
eggs of the two groups are compared. As mentioned in the
introductory paragraphs of this chapter, these similarities are
to be explained upon an historical basis, that of relationship
through descent. But while there is, in the early stages, such
close agreement between Mammal and Sauropsid, in these re-
spects, during their later history, these mammalian membranes
undergo profound changes in function associated with the intra-
uterine development of the embryo and the consequent sub-
stitution, as a source of nutritive substance, of the maternal
tissues in place of the intra-oval yolk-mass or albuminous egg
membranes of the Sauropsida.

In the chick the amnion serves, among other functions, to
protect the embryo from drying and from the deforming pres-
sure of the rigid shell; the yolk-sac contains a large part of
the food substance for the developing embryo; the allantoic

418 OUTLINES OF CHORDATE DEVELOPMENT

wall is the embryonic respiratory organ, while its cavity serves
as an excretory reservoir; and the chorion (serosa) appears to
have little, if any, physiological importance. In the Mammal
this is all changed. The amnion is a membrane of secondary
protective importance; the yolkless yolk-sac is a vestigial organ,
often of little functional value; the allantois loses its respiratory
and excretory significance and is usually concerned in relating
the embryo to the source of its food supply; while the chorion,
either as a whole or in part, becomes the chief organ concerned
in the exchange of nutritive materials and excreted substances
between the embryo and the maternal uterine circulation.

These characteristic relations of the mammalian embryonic
membranes do not appear in this group in a fully established
condition; there is, on the contrary, a long series of intermediate
conditions, transitional in almost every respect, between the
Sauropsid condition and that found in the highest Mammals,
the Primates, where these relations are most highly developed.
It is a familiar fact that in the lowest Mammals, the Prototheria
(Monotremata or Ornithodelphia) including only the genera
Ornithorhynchus, Echidna, and Proechidna, essentially Sauropsid
conditions obtain here, as well as in so many morphological
and physiological characteristics of the adults. Here the de-
veloping embryo has no organic relation with the mother, for
the fully formed eggs are deposited outside the body of the
parent, either in an integumentary fold (Echidna), or in a
"nest" (Ornithorhynchus), where the young develop indepen-
dently, enclosed within a tough parchment-like egg shell. Usu-
ally only a single egg is produced at one time in Echidna, while
Ornithorhynchus normally produces two at a time. The eggs
too are reptilian in character, much larger than any other
mammalian egg, and yolk laden. As laid, they measure about
15-16.5X12-13 mm. (in Echidna); the egg cell proper, as it
leaves the ovary is, of course, smaller than this, but even so
is much larger than the egg cell of the higher Mammals, being
3.0-4.0 mm. in diameter in Echidna, 2.5 mm. in Ornithorhynchus.

Among the Metatheria (Didelphia or Marsupialia) many of
the typical mammalian conditions are found. The ova, though

THE EARLY DEVELOPMENT OF THE MAMMAL 419

commonly somewhat larger than in the higher Mammals, are
sometimes of no greater size. The embryo has a brief intra-
uterine period of development, during which nutritive relations
are established with the uterine wall by means of the surface of
the chorion, which, however, retains its originally smooth sur-
face and merely comes closely into contact with the vascular
uterine epithelium, without acquiring a close organic union.
The yolk-sac is very large in these forms and underlies nearly
•the entire chorion (serosa). Nutritive substances from the
maternal circulation may thus pass, with some difficulty,
through the chorion and the wall of the yolk-sac, into the blood
of the latter.

Conditions suggestive of the higher Mammals are by no means
lacking, however, for in Dasyurus (Hill) the yolk-sac in certain
areas becomes very vascular and forms a close relation with
the uterine wall. The ectoderm cells of the chorion, between
the two, aid in establishing this relation between the maternal
and the embryonic blood, a relation which is very different from
the mere contact relation of the typical Metatheria. And in
Perameks (Hill) the allantois takes up a similar relation with
the uterine mucosa, sending into the latter well-developed
vascular outgrowths (Fig. 174). We have here then, a con-
dition that in many respects resembles closely the relation
found in many of the "placental" Mammals. Indeed, these
structures are known as the " yolk-sac" and the "allantoic
placenta" respectively.

Among the remaining Mammalian orders, or Eutheria (Mono-
delphia or Placentalia), there is the greatest diversity in the
mode and degree of the relation between embryonic membranes
and appendages, and the uterine wall, or, in other words, in
the character of the placentation. In the simpler cases (pig,
horse, and many others) the relation is much like that described
in Perameks in its essentials, while in the more highly specialized
instances (apes and man) the relation becomes very complex,
involving considerable modification of what is regarded as the
typical arrangement of the embryonic appendages. Between
these two extremes there is the greatest variety of conditions

420 OUTLINES OF CHORDATE DEVELOPMENT

of placentation, which frequently do riot parallel the usual
ordinal classification, so that even within a single order (e.g.,
Ungulata, Primates) there may be divergences which con-
siderably exceed the range of the morphological traits upon
which the orders are based.

Before attempting to describe any of the actual details of the
structure and development of the placenta, we must give a

amn. coe.

vase, omp/i.

bH.omph,. y.spl

FIG. 174. — Diagram of the arrangement of the foetal membranes in the
Marsupial, Perameles. From Hill. The ectoderm is represented by a light con-
tinuous line, the endoderm by a dotted line, and the mesoderm by a heavy line.
amn, Amnion; all. c., allantoic cavity; all. mes., allanto-chorionic mesenchyme;
all. s., allantoic stalk; bil, omph.. ectodermal and endodermal wall of yolk-sac;
ch., margin of true chorion; cce., exocoelom; cce. w., inner wall of allantois; proa, r.,
persisting remnant of proamnion; s. t., sinus terminalis; vase, omph., three-layered
portion of yolk-sac wall; y. c., cavity of yolk-sac; y. spl., invaginated splanchno-
pleural wall of yolk-sac.

general outline of the ontogenetic history of the embryonic
membranes and appendages. We may consider first the
method by which the young embryo or "ovum" (blasto-
dermic vesicle) effects its primary relation with the uterine
wall. In the remaining pages it is understood that what is
said is limited to the Eutheria.

THE EARLY DEVELOPMENT OF THE MAMMAL 421

1. Implantation

Through the process of menstruation, or procestrous, its
equivalent in the lower Mammals, the mucous membrane
lining the uterus is kept in an active, wholly living condition,
and as the ovum or blastodermic vesicle enters this cavity it
almost immediately becomes attached or implanted upon the
wall. It may become superficially attached to the wall of
the main uterine cavity, so that as it grows it projects freely
into the lumen of the uterus; this is known as central implanta-
tion and is found in the Ungulates and Carnivors, the lower
Primates and some Rodents such as the rabbit. In other
forms the vesicle may come to lie in a furrow or groove in the
uterine wall, which is then closed off from the main cavity by
the fusion of the margins of the furrow, enclosing the vesicle.
This is eccentric implantation and is found in such forms as
the mouse and some Insectivors. Or the vesicle may burrow
into the substance of the mucous membrane lining the uterus,
the mucosa then closing together over the point of entrance,
as in man and some Rodents, such as the guinea pig and the
gopher. This type of implantation is known as interstitial.

The structure primarily concerned in effecting this early
connection between the vesicle and the uterine mucosa is the
trophoblast (Hubrecht). We have already described the forma-
tion of this superficial layer of ectoderm cells which covers the
entire blastodermic vesicle as this passes down the oviduct
and enters the uterus (Figs. 154, A; 175). The trophoblast
may remain for a short time the only component of the periph-
eral wall of the blastodermic vesicle. But extra-embryonic
mesoderm usually forms very early around the wall of the
vesicle, and the entire extra-embryonic wall may then be
known as the chorion; the trophoblast may then be called the
chorionic ectoderm.

It is convenient to distinguish two general types of behavior
on the part of the trophoblast or chorionic ectoderm. In
most instances of central implantation (e.g., pig, horse) it
merely forms an adhesive layer which comes closely into

422 OUTLINES OF CHORDATE DEVELOPMENT

contact, over practically its entire surface, with the uterine
mucosa. In other instances of central implantation and in
the eccentric and interstitial types, a part or even the whole of
the trophoblast becomes highly specialized, physiologically,
as the trophoderm (Minot), in which the cells proliferate rapidly
forming a layer of considerable thickness (Figs. 175, 176).
It is the function of the trophoderm to dissolve or digest the
uterine mucosa, with which it is in contact. The trophoderm,
probably through the action of specific enzymes, rapidly erodes
the uterine wall, and the blastodermic vesicle becomes either
partially or wholly embedded in the maternal tissue, so that
the embryo bears a relation to the maternal organism which
is quite that of an internal parasite.

In most cases a part of the trophoblast is thus specialized
as trophoderm. In the rabbit, for example, the trophoderm
forms a horse-shoe shaped area just around the embryonic
rudiment, lateral and posterior to it; this region alone becomes
embedded in the uterine tissue, while the remainder of the
blastodermic vesicle, projecting into the lumen of the uterus,
remains covered with the relatively unmodified trophoblast
(chorion). In the spermophile (Rejsek) the trophoderm
forms a thickened mass, in the wall of the vesicle, opposite the
inner cell mass or embryonic rudiment. As the trophoderm
erodes the mucosa, the vesicle is carried down and partially
embedded in the uterine wall (Fig. 175). In forms like the
hedgehog, apes, and man, the entire trophoblast becomes
trophodermal (Figs. 153, 161). Here, then, the maternal
tissues on all sides of the vesicle are eroded, and the "ovum"
becomes completely embedded and surrounded by a mass of
dissolved tissue.

The cells of the trophoderm very early begin to fuse together
forming either small masses, known as multinuclear giant cells,
or extensive protoplasmic masses known then as syncytia, or
better, the syncytiotrophoderm (syncytiotrophoblast) (Figs. 175,
184). In the trophoblast, which is less intimately associated
with the maternal tissues, the cell boundaries usually remain,
and this is then distinguished as the cytotrophoblast.

THE EARLY DEVELOPMENT OF THE MAMMAL 423

It is evident from this description that the trophoderm or
Syncytiotrophoderm, forms the boundary between the embry-
onic and the maternal tissues, and not only effects the implanta-
tion of the "ovum," but at the same time establishes the

FIG. 175. — Early stages in the implantation of the blastodermic vesicle of the
spermophile (Spermophilus citillus) . After Rejsek. A. Unattached vesicle. B.
Syncytiotrophoderm just penetrating the epithelium of the uterine mucous
membrane. C. Syncytiotrophoderm extending along the basement membrane
of the uterine epithelium. D. More highly magnified view of the Syncytio-
trophoderm after it has penetrated the basement membrane and entered the
connective tissue of the uterine mucosa. b, Basement membrane of uterine
epithelium; ct, connective tissue of the uterine mucosa; e, epithelium of the
uterine mucosa; en, endoderm; t, inner cell mass; s, Syncytiotrophoderm;
t, trophoblast.

primary element in the placenta. The trophoderm later
becomes vascularized from the mesoderm of the chorion or
allantois (yolk-sac in some cases), and acts as the chief absorp-

424 OUTLINES OF CHORD ATE DEVELOPMENT

tive or resorptive surface, taking in materials from the maternal
tissues and blood.

The extent to which the trophoderm erodes the uterine
lining varies greatly. Of course where no trophoderm is
differentiated, little or no actual erosion occurs. And when
the trophoderm is present, the erosion may affect only the
epithelium of the mucosa, or it may involve the connective-
tissue elements, or even the walls of the uterine blood-vessels.
The degree of erosion has been suggested as a basis for the
classification of the types of placentae (Grosser), but this and
many other facts regarding the later history of the trophoderm
are better considered later, in connection with the placenta
itself.

2. The Amnion and Chorion

Our description of the formation of these membranes may
be very brief on account of their general similarity to those
of the chick fully described in an earlier chapter (Fig. 178).

We must distinguish, at the very outset, between two
general types of amnion formation found among the Mammals,
a distinction that has already been noted above in describing
the formation of the embryonic disc and its relation to the
trophoblast. In the Carnivors, Ruminants, many Insectivors
and some Rodents, such as the rabbit, the amnion is formed
from a series of folds of the extra-embryonic somatopleure
(wall of the blastodermic vesicle) much as in the chick. In
other forms, such as the mouse, guinea-pig, bat, some Insecti-
vors, and many Primates, including man, the amnionic cavity
arises in situ (entypy), above the embryonic disc, through a
splitting of the ectoderm or through the confluence of gradually
enlarging spaces (Figs. 152, 153, 155).

The amnion and chorion of the rabbit may be described as a
fair representative of the first type. Here, as in the chick, the
mesoderm very early extends posteriorly and laterally from
the embryo, but immediately anterior to it the wall of the
blastodermic vesicle remains for a considerable period devoid

THE EARLY DEVELOPMENT OF THE MAMMAL 425

h ta

N

ex

pa

vb

FIG. 176. — Diagrams of the formation of the embryonic membranes and
appendages in the rabbit. After Van Beneden and Julin (partly after Marshall).
Sagittal sections. A. At the end of the ninth day. B. Early the tenth day.
C. At the end of the tenth day. Ectoderm black; endoderm dotted; mesoderm
gray, al, Allantois; as, allantoic stalk; b, tail bud; c, heart; d, trophoderm;
e, endoderm; ex, exocoelom; /, fore-gut; h, hind-gut; m, mesoderm; N, central
nervous system; p, pericardial cavity; pa, proamnion; s, marginal sinus (sinua
terminalis); /, trophoblast; ta, tail-fold of amnion; v, trophodermal villi; vb,
trophoblastic villi; y, cavity of yolk-sac; ys, yolk-stalk.

426 OUTLINES OF CHORD ATE DEVELOPMENT

of mesoderm, and therefore composed of ectoderm and endo-
derm only. This mesoderm-free region is called the proamnion
(Fig. 176). The amnionic folds appear, toward the end of the
ninth day, between the embryo and the horse-shoe shaped
implantation area described above. At this stage of develop-
ment the embryo is well established, its head- and tail-folds are
formed, and the head is beginning to enlarge. In the wall of

€ho.

FIG. 177. — Transverse section through the rabbit embryo of eight days and
two hours. From Minot (Laboratory Text-book of Embryology). Am, Am-
nion; Ao, lateral dorsal aorta; Ch, notochord; Cho, chorion; Cce, coelom; Ent,
endoderm; Md, medullary tube (nerve cord); Seg, myotome; Som. somato-
pleure; Spl, splanchnopleure.

the blastodermic vesicle the endoderm has extended nearly or
quite completely around the inside of the vesicle (trophoblast),
while the mesoderm with its exoccelom extends through only
the upper third of the vesicle, which is nearly as far as it ever
goes in the rabbit.

The tail-fold of the amnion appears first, composed of ecto-
derm and somatic mesoderm of the extra-embryonic region,
and therefore containing an extension of the exoccelom; the
mesodermal layer is unusually thick in the tail-fold. Later-
ally folds soon appear as anterior extensions of the extremities
of the tail-fold. The head of the embryo rapidly enlarges, and
as it sinks down into the proamnionic region this flows up to or

THE EARLY DEVELOPMENT OF THE MAMMAL 427

above the level of the surface of the embryo forming the rudi-
ment of the head-fold of the amnion, which is thus composed
at first of the ectodermal and endodermal wall of this part of
the vesicle. The posterior and lateral folds rapidly come to-
gether, close above the embryo, in the anterior direction (Fig.
177). Finally all four of the folds fuse together in front of the
middle of the embryo. The region of their fusion, the sero-
amnionic connection, is a small knot, quite in contrast to the
elongated seam of the chick; it should also be noted that the
direction of the closure of the folds is just the reverse of what
it is in the chick, for here the tail-fold, rather than the head-
fold, grows the more rapidly.

Following the complete fusion of the amnionic folds, occurs
the separation of the inner and outer layers of the folds, thus
establishing (1) an outer membrane, really an extension over
the embryo of the wall of the blastodermic vesicle, known as the
chorion; (2) an inner membrane, the amnion, separated from
the embryo itself by (3) the amnionic cavity; and (4) an ex-
tension completely around the dorsal and lateral sides of the
embryo, of the exoccelom (Fig. 176).

From the relation of these folds (Fig. 178), it is clear that the
chorion is ectodermal superficially, lined with extra-embryonic
somatic mesoderm, while the amnion is ectodermal internally
with its somatic mesodermal layer turned away from the em-
bryo. The exoccelom is of course entirely lined with meso-
derm, while the amnionic cavity is wholly lined with ectoderm,
embryonic and extra-embryonic. The amnion is a thin, semi-
transparent membrane, while the chorion is thicker and quite
opaque. The amnion is non-vascular, while the chorion is, in
the higher Mammals, often richly supplied with blood vessels.

As the embryo enlarges, the attachment of the amnion, and
therefore the region where the amnionic ectoderm becomes
continuous with the embryonic ectoderm, remains restricted to
the region just around the origin of the yolk stalk and allantois
or umbilicus (Fig. 176, B, C).

The proamnion finally becomes invaded by mesoderm, which
has from a very early stage been present in front of the pro-

428 OUTLINES OF CHORDATE DEVELOPMENT

amnion, and the entire amnion and chorion then have a meso-
dermal lining. In the rabbit the amnionic cavity remains
relatively small, while the exocoelom expands so as to fill the
cavity of the blastodermic vesicle, save for the space occupied
by the yolk-sac and allantois (Fig. 180). The tail- fold appears
extremely early in some forms, such as the mole (Talpa) and

FIG. 178. — Diagram of the embryonic membranes and appendages of the
Mammals in general. From Hertwig (Lehrbuch, etc.), after Turner. AC,
Amnionic cavity; al, allantois; ALC, allantoic cavity; am. amnion; E, embryonic
ectoderm; H, embryonic endoderm (the reference letter is placed in the gut
cavity); M, embryonic mesoderm; pc, trophoblast or trophoderm with villi;
sz, chorion; UV, yolk-sac.

in Tarsius, so that the point of the final closure of the amnionic
folds is far forward over the head. The extent of the proam-
nion is also extremely variable; in some forms (e.g., Ruminants,
bats, many Primates) it is nearly or quite absent, while in
the opossum it forms nearly the entire amnion.

Turning to the second type, where the amnionic cavity is
formed in situ, as a closed cavity from the very beginning, we
may describe the human amnion as an example. The earliest
stages in its formation have not been observed as yet, in man,

THE EARLY DEVELOPMENT OF THE MAMMAL 429

but a relatively early condition has been illustrated in Fig.
161, D. Here the embryo itself remains connected with the
wall of the blastodermic vesicle by the body stalk, described
above, and in this respect the human embryo is not a satis-
factory example of this type of amnion formation. Usually
this attachment represents the remains of a thickening in the
wall of the vesicle ("trager" see above), to which is added
later the definitive attachment of the allantois growing out
from the embryo through the cavity of the vesicle to the inner
surface of the chorion.

In the human vesicle, however, the amnionic cavity appears
directly above the embryo, so that the embryonic disc itself
forms its floor, while the body stalk bounds it posteriorly
(Figs. 161, 179). At first the roof of the amnionic cavity is
simply the trophoblast, but as the cavity enlarges it becomes
partly free, below the trophoblast, so that its roof is a separate
structure. The attachment of the amnion is around the mar-
gin of the embryonic disc (Fig. 162, A}] its roof and sides are
composed of a thin layer of ectoderm toward the embryo,
outside of which is a thin mesodermal layer, for the extra-
embryonic mesoderm has already been formed throughout the
entire vesicle. A proamnion is therefore lacking in forms whose
amnion is developed in this manner.

As the embryo enlarges and extends in every direction the
origin of the amnion appears to be carried ventrally, so that,
as in the rabbit, it connects with the embryo just around the
umbilicus. At the posterior end, however, it passes around
the sides of the body stalk, to its posterior surface, so that this
structure finally becomes wrapped in a part of the amnionic
membrane (Fig. 179) . In man the yolk stalk and sac, and the
allantois, are also bound up in this body stalk or umbilical
stalk (Fig. 179). The final disposition and character of the
amnion and chorion are thus essentially the same as when
formed from folds.

In man the amnionic cavity grows rapidly and by the third
month becomes so large as completely to fill the cavity of the
The exoccelom is thereby entirely obliter-

430 OUTLINES OF CHORDATE DEVELOPMENT

ated, the amnion and chorion being brought into contact with
one another over their mesodermal surfaces, and finally they
may fuse together. The amnionic cavity is filled with a fluid
known as the liquor amnii, now thought to be formed by the
amnionic epithelium. It contains solids, mostly albumins,
grape sugar, and urea, to the extent of about 1 per cent. The

FIG. 179. — Diagrams illustrating the formation of the umbilical cord and the
relations of the allantois and yolk-sac in the human embryo. From McMurrich
(Development of the Human Body). The heavy black line represents the
embryonic ectoderm; the dotted line marks the line of the transition of the body
(embryonic) ectoderm into that of the amnion. Stippled areas, mesoderm. Ac,
Amnionic cavity; Al, allantois; Be, exocoelom; Bs, body stalk; Ch, chorion;
P, placenta; Uc, umbilical cord; V, chorionic (trophodermic) villi; Ys, yolk-sac.

amount of the liquor amnii in man varies considerably, but usu-
ally between 0.5 and 1.0 liter at the period of its maximum
amount, which is some time before parturition. At parturition,
of course, both the amnion and chorion normally are ruptured
and the amnionic fluid escapes with or before the foetus.

The more important aspects of the chorion are those con-

THE EARLY DEVELOPMENT OF THE MAMMAL 431

cerned with placentation and will be considered in connection
with the development of the placenta.

3. The Yolk-sac

We may summarize what has already been said concerning
the yolk-sac and add a few facts of importance, chiefly from
the comparative standpoint. We are to think of the yolk-sac
of the Mammals as typically occupying the chief part of the
early blastodermic vesicle, its cavity opening widely into the
embryonic gut by the broad yolk stalk, and its wall separated

sh

FIG. 180. — Diagrammatic section through the fully formed blastodermic vesi-
cle of the rabbit, showing the reduced yolk-sac. From Hertwig (Lehrbuch,.eJc.)
after Bischoff. o, Amnion; al, allantois; ds, yolk-sac; e, embryo; ed, edf, ed"
yolk-sac endoderm; fd, vascular layer (mesoderm) of yolk-sac; pi, villi; r, exo-
ccelom; st, sinus terminalis; u, allantoic stalk.

from the chorion by the exoccelom (Figs. 161, 179). The yolk-
sac is thus a splanchnopleuric structure, in contrast to the
somatopleuric amnion and chorion. This typical relation, how-
ever, is subject to varied and often profound modification. In
the rabbit we have seen that the endodermal wall of the vesicle
develops slowly, so that for a considerable early period the yolk-
sac is incomplete ventrally. Finally the endoderm does form
a complete sac, in contact with the chorionic ectoderm; the

432 OUTLINES OF CHORDATE DEVELOPMENT

extra-embryonic mesoderm then develops very slowly pushing
down between the ectoderm and endoderm, but limited to the
upper half of the vesicle (Fig. 176). The yolk-sac in the rabbit
is therefore strictly splanchnopleural only in its upper half;
below this the chorionic ectoderm is in direct contact with the
yolk-sac endoderm. When the exoccelom expands so consider-
ably as it does in the rabbit, the yolk-sac is compressed and

va

FIG. 181. — Area vasculosa (yolk-sac circulation) of an eleven-day rabbit.
After Van Beneden and Julin. Veins black, arteries white, s, Marginal sinus
(sinus terminalis) ; va, vitelline artery; vv, vitelline veins.

reduced to an umbrella-shaped structure with a very narrow
cavity, connected with the embryonic gut by a long narrow
yolk stalk, the wall of which includes mesoderm as well as
endoderm (Fig. 180).

As in the chick the mesodermal wall of the yolk-sac becomes
very vascular. Its rich network of blood vessels is supplied
by the vitelline or omphalomesenteric arteries arising from the
dorsal aorta (Fig. 181) . After spreading over the surface of the
sac these collect into a well-marked sinus terminalis, which is a
complete ring in the rabbit, and from which the blood is re-
turned to the embryo through the vitelline or omphalomesenteric

THE EARLY DEVELOPMENT OF THE MAMMAL 433

veins. These empty into the posterior end of the heart after
penetrating the liver; later the extra-embryonic portions of
these veins disappear, while their embryonic portions are trans-
formed into the portal (hepatic portal) vein.

In the Carnivors the yolk-sac is very large and has a complete
mesodermal investment which is unusually vascular. At first
it is closely in contact with the chorion, and thus may have
temporarily a placental relation, but soon it is in part separated
from the chorion by the extension, between the two membranes,
of the allantois which then assumes the definitive placental rela-
tion. The primarily placental character of the yolk-sac in the
marsupial, Dasyurus, has been mentioned. In the mole, Talpa,
a similar relation has been described, the vascular mesoderm
of the upper part of the yolk-sac, with the endodermal wall of
its lower part, coming into close organic relation with the
chorion and uterine epithelium.

In many other Mammals the yolk-sac is from the beginning a
relatively small organ (Tarsius, hedgehog, Primates), or it may
early be reduced from an originally well-developed state (horse).
In man, which may be described as in a general way representa-
tive of this type, the yolk-sac at all stages comes far short of
filling the cavity (exocoelom) of the blastodermic vesicle. It
grows slowly out into the exocoelom during the first month or
more of development, its diameter about equal to the length of
the embryo. Its wall is richly vascular even in its very early
stages, the blood vessels producing a characteristic roughness
of its outer (mesodermal) surface (Fig. 164). After reaching
a size of about 11X7 mm. it begins to diminish in size. A
yolk stalk becomes clearly differentiated and elongates rapidly,
and we have already seen how it becomes enclosed proximally
within the umbilical stalk or cord. Finally the entire yolk stalk
is thus enclosed and, as the amnionic membrane expands, filling
the entire cavity of the "ovum," wiping out the exocoelom, the
yolk-sac itself disappears from view, embedded in the meso-
dermal tissues of the placental region (Fig. 179).

The greater part of the yolk stalk becomes a solid cord of en-
doderm during the latter part of the second month, and finally

434 OUTLINES OF CHORDATE DEVELOPMENT

it disappears entirely; its proximal end may occasionally remain
tubular as Meckel's diverticulum of the intestine. The yolk-
sac remains as a very small vestige, ordinarily 5 mm. or less in
diameter, even up to the the time of parturition.

4. The Allantois

The allantois is no less variable among the Eutheria, both
in its mode of development and in its definitive relations, than
are the other embryonic appendages. And again there is little
parallel between allantoic characters and the usual ordinal
classification of the Eutheria. Among the Carnivora and the
lower Primates (Lemurs) the allantois becomes very large and
fills the exocoelomic space, while, as an opposite condition,
among the other Primates it forms not even a free vesicle, but
remains as a vestigial structure, enclosed within the umbilical
cord. Between these two extremes there is a great variety of
conditions.

The earlier embryonic history of the allantois is considerably
less variable than its later history and final relations. At first
there is essential similarity to the condition already described
in the chick, so that the earlier phases in its development need
not be described here. Many of the later modifications of the
avian type of allantois are correlated with the fact that among
the Mammals the allantoic circulation functionally takes the
place of the avian yolk-sac circulation, or in other words, the
allantois takes an essential, though secondary, part in the
formation of the embryonic placental structures, indeed it may
even be limited to this relation, as in the rabbit. From the
functional relations of the allantois, among the Mammalia, it
is clear that its mesodermal structures, in particular its blood
vessels, are its most important elements, and there is relatively
slight variation in their arrangement.

As in describing the amnion we may consider two of the
important types of allantoic formation and history, and then
mention briefly a few comparative points of interest.

In the rabbit the allantois appears on the eighth day of de-
velopment, as a small mass of mesoderm cells extending into the

THE EARLY DEVELOPMENT OF THE MAMMAL 435

exoccelom opposite the posterior end (primitive streak) of the
embryo (Fig. 176, -A). At its base the tail-fold of the amnion
is just appearing, and there is already a slight indication of the
evagination of the endoderm into it. By the ninth day the
tail of the embryo has begun to grow out, and the allantoic
rudiment is forced into a ventral position; the amnion therefore
appears to arise posteriorly to the allantois, beneath the base
of the tail. By this day the allantois has enlarged and its
extremity has dilated forming a vesicle which extends freely
into the exoccelom, while the narrower allantoic stalk is
attached beneath the embryo, just back of the attachment of
the yolk-sac, from the cavity of which the allantoic cavity is
now clearly marked off.

As the allantois grows out it comes immediately into relation
with the inner surface of the chorion, in the region where the
chorionic ectoderm has become trophodermic (Fig. 176, 5), and
since the trophoderm is the beginning of the placental struc-
ture, the allantoic stalk thus becomes the direct pathway
between the embryo and the placental region.

During the tenth to twelfth days the allantois expands
rapidly beneath the chorionic trophoderm, its mesodermal wall
thickens and in it a rich vascular network is developed (Fig.
176, C). Blood vessels have been present in the allantoic meso-
derm from a very early period, and by the tenth day there are
present a pair of umbilical arteries, and a pair of umbilical veins,
having relations similar to those already described in the human
embryo. It is through the allantoic blood vessels, therefore,
that the embryonic circulation is related with the placental,
and in the rabbit this appears to be the only important function
of the whole allantoic structure.

In man the history of the allantois is a very different story.
Here, as in all Primates, the primitive connection of the hinder
end of the embryo with the chorion is never interrupted, and
this connection, known as the body stalk (see above), composed
of mesoderm, may be regarded as the modified equivalent of
the allantoic stalk of such a form as the rabbit. Into this body
stalk there early extends a small tubular outgrowth from the

436 OUTLINES OF CHORDATE DEVELOPMENT

endodermal lining of the yolk-sac, from which at this time the
hind-gut is not distinguishable (Fig. 161, D, E).

The essential relation thus established is never extensively
altered. When the hind-gut forms, it is dorsal or postero-
dorsal to the opening of the allantoic canal, and as the body
stalk elongates the allantoic canal continues to extend up
through it, finally reaching the region of the chorionic meso-
derm (Fig. 179). The allantois never expands into a free vesicle
in the exoccelom, but remains as a vestigial structure, wholly
embedded within the tissues of the body stalk, or of what is
later the umbilical stalk (see above). The endodermally lined
allantoic canal within the umbilical cord, remains present in
this condition throughout the foetal period. As the ventral
body wall of the embryo is formed it encloses the proximal
portion of the allantoic stalk, and this becomes enlarged,
forming the rudiment of the urino-genital sinus and the urinary
bladder; between this and the body wall it is reduced to a solid
strand of connective tissue called the urachus.

The blood vessels of the allantois (umbilical arteries and
veins) remain typically developed here, in spite of the
vestigial character of the endodermal portions of the allantois,
and as in the rabbit these are the only functional elements of
the whole allantoic structure. The vessels are very large and
form a very rich network in the placental region, beyond the
limits of which the chorion becomes almost non-vascular,
although in earlier stages the entire chorion is vascular.

Only among the higher Primates is the allantois vestigial to
such a degree; and it is not often that it has as limited an extent
as in the rabbit. In other forms, such as the Lemurs, Carnivors,
and Ungulates, the allantois extends completely around the
inner surface of the chorionic vesicle; among the Ungulates
this seems to be correlated with the simple type of placenta
(see below). In such cases, and in some other instances
where the allantois is more nearly limited to a definite placental
region, a definite allantoic cavity is present, small and com-
pressed in forms like the sheep and pig, or large and filling a
large part of the cavity of the entire vesicle.

THE EARLY DEVELOPMENT OF THE MAMMAL 437

5. The Placenta

Among the Eutherian Mammalia placentation may be de-
fined as an intimate relation between a portion of the uterine
mucosa and a part or the whole of the chorionic membrane
(trophoblast) of the blastodermic vesicle. This relation may
involve merely the close apposition of these two tissues, or their
actual fusion. Further, in order that this relation may be
effective in the nutrition of the embryo, which is in fact its
whole raison d'etre, the blood vessels of the allantois become
closely associated with the related chorionic and maternal
tissues.

All of the structures thus associated in effecting the nutritive,
respiratory and excretory interchanges between embryo and
maternal organism, may collectively be termed the placenta.
It is thus immediately evicbent that the placenta is a compli-
cated structure and one that is extremely variable, including
as it does, these several elements, themselves individually
variable.

Many of the essential facts regarding the establishment and
the grosser morphological relations of the placenta have been
mentioned in other connections. In the section on the im-
plantation of the "ovum" we have seen that the earliest step
in placentation is to be found in the relation established
between the chorionic ectoderm, whether trophoblast or tropho-
derm, and the uterine wall (Fig. 175). This is followed con-
siderably later by the vascularization of the chorion thus re-
lated to maternal tissues, by the blood vessels of the yolk-sac,
as in certain Marsupials (Fig. 174), or of the allantois, as in
the Ungulates and rabbit (Fig. 176), or by the vessels of the
chorionic mesoderm itself, as in man.

Upon the character and completeness of the relation between
chorionic ectoderm and the uterine tissues depends the funda-
mental character or type of the placenta developed later.
Among most of the Marsupial Mammalia the surface of the
chorion retains its smooth surface and is ordinarily not vascu-
larized, either by the yolk-sac or allantois, and since it forms

438 OUTLINES OF CHORDATE DEVELOPMENT

only simple contact with the uterine wall, nutritive inter-
changes between embryo and parent are carried on only with
some difficulty. These forms have been termed the achoria
or aplacentalia, although strictly speaking these terms are
misnomers, for a simple chorion is present and a placental
relation does exist, although to a very limited degree.

All of the Eutherian Mammalia may then be termed choriata
or placentalia, and it is characteristic of these forms that upon
the outer surface of the chorion there develop elevations or
papilla? known as the villi (Figs. 153, 161, 184).

The villi are the organs of primary importance in effecting
the nourishment of the embryo, and the essential characters,
as well as many of the minor characters of the placenta,
depend upon the form, mode of distribution, and other
characteristics of the villi.

The chief variations in the characteristics of the villi may be
enumerated as follows: they may be trophoblastic or tropho-
dermic in origin; they may be simple papilla? or complexly
branching, dendritic outgrowths; they may develop very early
in embryonic history or very late after a considerable period
of intra- uterine life; they may be almost non- vascular or very
highly vascularized from the embryonic circulation (umbilical
arteries and veins); they may be distributed quite uniformly
over the greater part of the chorionic surface or definitely
grouped and restricted to certain areas; when restricted they
may be grouped in definite patches or cotyledons, scattered
over the chorion, like polka-dots, or they may be restricted to
certain general zones or bands, or to single large circular areas,
or arranged in still other ways; they may be in contact with
the maternal mucous epithelium lining the uterine cavity, or
with its connective tissue stroma, or with the endothelium of
the uterine vessels, or actually bathed directly in the maternal
blood stream.

Several classifications of placenta? have been formulated;
based upon one or another of these conditions. While none of
these represents a natural classification, we may outline certain
of the more important, as a convenient way of stating the

THE EARLY DEVELOPMENT OF THE MAMMAL 439

essential facts of placental arrangement. The earlier classi-
fications, such as those of Owen, Huxley and Kolliker, based
upon the type of villous distribution and the degree of intimacy
between the villi and the uterine mucous membrane, may be
summarized as follows, following Hertwig in the main:

I. Achoria. Chorion with few or no villi. Monotremes and Marsupials.
II. Choriata. Chorion with many villi.

A. With uniformly distributed villi, not intimately related

-I

II

,j3 o3

f!
ii

with the maternal tissues. Most Ungulates except the
Ruminants (e.g., horse, pig, camel, deer, etc.),
B. With villi localized in definite areas, and more or less closely
related with maternal tissues. The true Placentalia.

1. Villi in numerous small patches or cotyledons. Cotyle-
donary placenta. Ruminants.

2. Villi in a band or zone around the chorion. Zonary
placenta. Carnivora.

3. Villi in a single large circular area. Discoid placenta.
Insectivors, Bats, Rodents, higher Primates including
man.

The terms deciduate and non-deciduate in the classification
above require a word of explanation. In several groups of
Mammals the epithelium of the mucous membrane lining the
uterine cavity becomes greatly thickened during pregnancy,
or preceding menstruation. This thickening during pregnancy
is termed the decidua, and usually the relations of the villi to
the decidua are such that the separation of the placenta at
parturition involves a certain loss of maternal tissue (de-
ciduata). In other forms, however, the uterine epithelium
shows no such proliferation, and the chorionic villi, at parturi-
tion are simply withdrawn from the pits in the mucosa where
they have been lodged, and no destruction of maternal tissues
results (non-deciduata). An intermediate condition, known as
contra-deciduate, is found in the mole where, although a decidua
is formed, the placental tissues are not lost at parturition, but
are absorbed by the walls of the uterus.

A more recent and more detailed classification of placental
arrangement, again based upon the morphological arrangement
of the villi, is that of Strahl, as follows:

440 OUTLINES OF CHORDATE DEVELOPMENT

I. Mammalia ovipara. Monotremata.
II. Mammalia vivipara.

A. Achoria (Aplacentalia) . Most Marsupialia (the exceptions
are Perameles, Dasyurus, and perhaps Phascolarctos) .

B. Choriata (Placentalia) .

1. Semiplacentalia (Partial placenta). Chorionic and
uterine structures in close apposition but not fused;
simple separation at parturition.

a. Semiplacenta avillosa. Chorion without villi. Pera-
meles, Dasyurus.

b. Semiplacenta diffusa. Simple villi uniformly dis-
tributed. Horse, pig, tapir, hippopotamus, camel,
deer, whale, Manis, Lemurs.

c. Semiplacenta multiplex. Villi in groups or cotyle-
dons. (Cotyledonary placenta.) Ruminants.

d. Semiplacenta zonaria. Villi in a zone or band
around the chorion. Only in the Dugong (Halicore) .

2. Placentalia vera (Complete placenta). More or less
complete fusion of chorionic and uterine tissues, in-
volving tissue destruction at parturition.

e. Placenta zonaria. Placental fusion in the form of a
broad band or zone, completely around the chorion.
Most Carnivora. In Hyrax and the elephant com-
bined with cotyledons.

f. Placenta zono-discoidalis. Placental fusion in the
form of an incomplete band or zone. Mustelidce
(e.g., marten, weasel, ferret, etc.).

g. Placenta discoidalis. Placental fusion in the form
of a circular disc, usually simple in outline, though
sometimes lobed. Insectivors, bats, Rodents, Tar-
sius, apes, man.

Of the many other classifications* of placental types we may
mention only one, that of Grosser, based upon an entirely
different relation, namely, the extent of the erosion of the
maternal uterine tissues effected by the trophodermal cells of
the chorion. From this point of view placentae are arranged
in four groups, as follows:

I. Placenta epitheliochorialis. All maternal tissues retained, un-
eroded. Chorionic epithelium (of the villi) in contact with the
uterine epithelium. Pig.

THE EARLY DEVELOPMENT OF THE MAMMAL 441

II. Placenta syndesmochorialis. Uterine epithelium nearly or
wholly eroded. Chorionic epithelium in contact with the con-
nective tissue of the uterine mucosa. Ruminants.

III. Placenta endotheliochorialis. Epithelium and connective tissue of
the uterine mucosa eroded. Chorionic epithelium in contact
with the endothelial walls of the uterine blood vessels. Carnivora.

IV. Placenta hcemochorialis. Uterine epithelium, connective tissue,
and vascular endothelium eroded. Chorionic epithelium in
contact with. maternal blood stream. Man.

Variation in the extent of the erosion of the maternal tis-
sues determines to some extent also the character of the
nutritive substances absorbed or resorbed by the chorionic
epithelium. The nutritive materials taken into the foetal
circulation are of two classes. (A) Food substances already
dissolved in the maternal blood. These, known as hcemotrophe,
may pass by diffusion or by active resorption directly into the
embryonic circulation. Obviously this process is easier, and
this type of nutritive substance more important, in those
placenta where the chorionic epithelium is more closely re-
lated with the maternal blood (Placenta endotheliochorialis and
PL risemochorialis) . (B) Products of the uterine mucous mem-
brane including the secretion of the uterine glands, the products
of the erosive or dissolving action of the trophoderm, and the
resultant extravasated blood. This is known as the ernbryo-
trophe or pabulum. Frequently these materials undergo a sort
of digestive process before their absorption into the embryonic
circulation. In forms whose chorionic (villous) epithelium is
less closely related to the maternal blood stream (PI. epithelio-
chorialis, PI. syndesmochorialis) the embryotrophe is the
more important source of nutrition. In the other types it
may be of great importance during the early period of devel-
opment, and gradually give place to the haBmotrophe as the
relation between the villous and uterine blood streams becomes
more intimate.

With these general facts regarding the variety of placental
arrangement in mind, we may describe the development and
structure of but a single type — the human placenta (Placenta
discoidalis, hamochorialis) . (For a description of the placental

442 OUTLINES OF CHORDATE DEVELOPMENT

relations in other forms, the student may be referred to Mar-
shall's " Physiology of Reproduction.")

The very early stages in the history of the human ovum are
not yet known, but from comparisons with other similar forms,
and from the conditions of the youngest embryos known (see
Peters, Bryce-Teacher) the characters of the early human
blastodermic vesicle may be inferred with a high degree of
probability. It is entirely probable that the entire tropho-
blastic surface of the vesicle becomes trophodermic (Fig. 161),
and digests or erodes the uterine mucosa all around itself, when
it becomes attached to the uterine wall after entering the uterine
cavity. This attachment and implantation of the "ovum'7
usually takes place on the anterior (upper) wall of the cavity,
between the openings of the oviducts, in what is known as the
fundus of the uterus. Attachments to other parts of the wall
are not infrequent, however, and do not affect the normality
of development.

The "ovum" or vesicle apparently eats its way a short
distance into the mucosa, which closes behind it, and by de-
stroying the adjacent tissues becomes surrounded by a narrow
space filled with fluid — extravasated blood and the products
of erosion (embryotrophe). This space is the rudiment of
what is later known as the intervillous cavity. The uterine
cells in this region then begin to proliferate rapidly, so that as
the blastodermic vesicle enlarges it remains covered with a
distinct layer of the uterine mucosa; this, as we shall see, is
the beginning of the decidua capsularis or reflexa. In some of
the Rodents the injury of the mucosa, when combined with
the presence of an internal secretion from the ovary (or corpus
luteum) serves as the stimulus to this proliferation (L. Loeb).

The chorionic villi are formed very early and at first develop
all over the surface of the vesicle. Some of the villi simply
extend freely into the intervillous cavity, while others grow
across it and reach the undisturbed tissues of the uterine
mucosa, to which they become definitely attached as the
fixation villi.

Before tracing further the history of the villi and the for-

THE EARLY DEVELOPMENT OF THE MAMMAL 443

mation of the placenta, we must consider some facts regarding
the general epithelial lining of the uterine cavity (Fig. 182).
During pregnancy this epithelium is not sloughed off as it is
during menstruation; on the contrary it thickens rapidly and
considerably, over the entire wall of the uterine cavity forming
the decidua. Its later history varies in different regions. That
part of the decidua not directly related with the blastodermic
vesicle, and therefore its greater part, is known as the decidua
vera. The region covering the vesicle and separating it from
the uterine cavity is the decidua capsularis or decidua reflexa;
while the portion beneath the vesicle, between it and the
muscular layer of the uterine wall, is the decidua basalis or
decidua serotina.

As the decidua vera thickens, during the early phases of
pregnancy, its vascularity increases and the uterine glands
within it elongate, becoming branched and anastomosing, ex-
tending down into the deeper layers of the mucosa. Toward
their openings upon the surface of the mucosa they dilate con-
siderably and the connective tissue matrix in which they are
embedded is correspondingly reduced, so that a superficial
layer of the decidua may be distinguished, as the spongy layer.
The deeper region is known as the compact layer; here the
glands do not dilate and the decidual cells multiply and en-
large. The decidua vera reaches its maximum development
during the second or third month of development, when it
may be 6-10 mm. in thickness; degenerative changes have
already begun at this time, however.

At first the structure of the decidua capsularis is not markedly
unlike that of the decidua vera, save where all its structure
has been destroyed by the entering vesicle, but its glands soon
atrophy. As the blastodermic vesicle rapidly enlarges the
decidua capsularis becomes extended, and by the fifth month
it is pushed out into contact with the decidua vera, and the
original cavity of the uterus is obliterated. The decidua
capsularis now becomes non-vascular, gradually thins out, and
finally disappears completely, leaving the chorionic surface of
the vesicle in contact with the decidua vera. But this too

444 OUTLINES OF CHORDATE DEVELOPMENT

FIG. 182. — Diagrammatic section through the gravid human uterus and the
embryo at the seventh or eighth week. From Quain's Anatomy, after Allen
Thomson, al, Allantois; am, amnion; c, c, openings of the oviducts (Fallopian
tubes) into the uterine cavity; c', cervix filled with mucous plug (the reference
letters c,c,c', are placed in the cavity of the uterus; ch, chorion with vascular
villi growing into the decidua capsularis and decidua basalis; in the decidua cap-
sularis the villi are becoming atrophied (chorion Iseve) ; dr, decidua capsularis;
ds, decidua basalis; dv, decidua vera; i, embryo; u, umbilical cord; y, yolk-sac;
yr, yolk-stalk;

THE EARLY DEVELOPMENT OF THE MAMMAL 445

has partly degenerated; it has become less vascular, its super-
ficial epithelium and spongy layer have disappeared, and there
remain only a part of its compact layer and the deeper portions
of the uterine glands.

The early history of the decidua basalis is not essentially
unlike that of the decidua vera, save that its glands disappear,
but later, instead of exhibiting any phenomena of atrophy its

FIG. 183. — Human embryo of the fourth month in utero, showing the arrange-
ment of the membranes and placenta. After Strahl. c, Chorion and amnion;
p, placenta; u, umbilical cord.

importance increases; its capillaries dilate, its decidual inter-
glandular cells continue to multiply, and it takes an essential
part in the formation of the placenta, forming in fact the
whole maternal portion of this organ. To understand the
origin and structure of the placenta we must return to the
early blastocyst, upon the surface of which the villi are forming.
The villi are formed at first wholly of the ectodermal tropho-

446 OUTLINES OF CHORD ATE DEVELOPMENT

derm, and as we have seen, extend into or across the inter-
villous cavity from all surfaces of the blastodermic vesicle.
As the vesicle enlarges the villi on the sides toward the decidua
capsularis disappear along with the capsularis itself, and the
smooth chorion thus left is the chorion Iceve, which then comes
into contact with the decidua vera on the opposite side of the
uterus (Figs. 182, 183). The villi in relation with the decidua
basalis alone remain, forming then the chorion frondosum;
this part of the chorion is in the region of the attachment of
the body stalk of the embryo, where the umbilical (allantoic)
blood vessels are distributed.

The villi of the chorion frondosum enlarge and branch, many
of them finally assuming a dendritic appearance, extending
irregularly through the intervillous cavity (Fig. 184). While
at first simply ectodermal, the mesoderm of the chorion soon
pushes out into them and becomes extremely vascular. Even
before this the superficial cells of the trophoderm (and villi)
have fused into a syncytial layer known as the syncytiotropho-
derm, which is lined internally, for a time, by a simple epithe-
lium of the cells of Langhans, also apparently derived from
the chorionic ectoderm. The vascular mesoderm then forms
the core of the villus (Fig. 184).

As the villi grow out they continue to erode the substance of
the decidua basalis, and the intervillous cavity is consequently
enlarged and filled with maternal blood from the opened
capillaries and vessels of the region. Finally the whole inter-
villous space is occupied by large vascular sinuses or lacunae,
and when the Langhans cells disappear, the embryonic and
maternal blood streams are separated only by the endothelium
of the villous capillaries and the syncytiotrophoderm covering
them (placenta haBmochorialis). Of course the two blood
streams are nowhere in direct communication.

The formation of the placenta has now been described. It
is a structure combined from two distinct sources, a maternal
portion, the decidua basalis, and an embryonic portion, the
chorion frondosum; the two are separated by the intervillous,
or as we may now say, intra-placental cavity, filled with maternal

THE EARLY DEVELOPMENT OF THE MAMMAL 447

m

FIG. 184. — Diagrams illustrating the development of the villi in the human
placenta. A. B, After Peters; C. after Bryce. A. Chorionic mesoderm just
beginning to extend into the villi. B. Mesoderm invading the villi which are
now branched. Layer of Langhans cells forming beneath the syncytiotro-
phoderm. C. Continued branching of the villi, all now covered only by the
syncytiotrophoderm and the single layer of Langhans cells, b, Decidua basalis;
cb, capillaries of the decidua basalis; cv, capillaries of the villi; e, endothelium of
the maternal capillaries; /, fibrin deposited at the junction of the trophoderm
and decidua basilis; i, intervillous cavity filled with maternal blood; L, Langhans
cells; m, chorionic mesoderm; s, syncytiotrophoderm; t, trophoderm; v, villi;
vf, fixation villi.

448 OUTLINES OF CHORDATE DEVELOPMENT

blood. The two regions are in actual connection only margin-
ally and through the fixation villi (Figs. 184, 185); later certain
septa afford additional connection (see below). From the
preceding description it is apparent that the human placenta is
at first of the diffuse type, later becoming discoid.

The fully formed placenta (i.e., at nine months) is an oval
or circular disc of irregular outline, roughly 16-20 cm. in
diameter, and about 3 cm. in thickness toward the middle,
gradually becoming thinner toward the margin. The umbilical
cord transmitting the umbilical arteries and veins, is attached
eccentrically; the cord itself measures, at full term, about
50-60 cm. in length and has a diameter of something over 1 cm.
The villous surface of the placenta is marked out in irregular
areas by partitions or septa, extending upward from the decidua
basalis, some of which, when the placenta is in situ, attach to
the chorion and so divide the intra-placental or inter villous
cavity into chambers. These areas are known as the loculi, or
sometimes as cotyledons, and they must not be confused with
the groups of villi of the cotyledonary placenta of the Rumi-
nants. The villi extend from the surface of the septa as well as
from the general chorionic surface.

Examination of Fig. 185, illustrating diagrammatically a
section through the placenta at its margin, will serve to make
clear the structure of the placenta. The embryonic surface of
the placenta, which is toward the top of the page, is seen to
be covered with the thin amnion; that is, the exoccelom has
been obliterated by the apposition of the amnion and chorion,
and the cavity of the embryonic vesicle is therefore the amnionic
cavity, filled with the amnionic fluid.

The chorion presents first a connective tissue membrane
(close vertical ruling) beneath which are the vascular villi
(horizontal ruling) which in reality form a dense spongy mass.
The vessels extend through the complexly branched villi,
both types of which are shown. Toward the close of gestation
the fixation villi become very loosely attached to the decidua
basalis, in preparation for the separation of the placenta at
parturition. The villi are for the most part freely suspended

THE EARLY DEVELOPMENT OF THE MAMMAL 449

in the intra-placental cavity filled with maternal blood (black
in Fig. 185). Beneath this are the greatly reduced layers of
the decidua basalis, traversed by the maternal blood vessels
communicating with the intra-placental cavity. In the deeper

S-ft

layer of the decidua basalis portions of the uterine glands
remain present. Finally the decidua basalis rests upon the
muscular layer of the uterine wall (oblique ruling).

Peripherally the irregular chambers of the intra-placental
cavity are nearly or quite free from villi, and form the marginal

450 OUTLINES OF CHORD ATE DEVELOPMENT

sinus. This is incompletely separated from the remainder of
the cavity by an irregular septum known as the closing plate.

At parturition, when the amnion has been ruptured and the
amnionic fluid and foetus have been expelled by the contrac-
tions of the uterine musculature, the arnnion itself and the
placenta and deciduse come away later. The decidua basalis
separates first through the spongy region, just outside the
glandular layer (Fig. 185, Tr-Tr). The decidua vera similarly
is divided through the remains of its spongy layer and comes
away with the placenta. The so-called " after-birth " therefore
includes amnion, chorion, decidua vera, placenta, and a por-
tion of the decidua basalis. The hemorrhage which follows this
separation of the maternal tissues is diminished by the general
contraction of the uterine walls. The entire uterine cavity is
then lined with the deeper decidual layer containing vestiges
of uterine glands, and from this tissue the decidua is formed
anew.

REFERENCES TO LITERATURE

CHAPTER VI

This list contains but a very few of the important works bearing
directly upon the topics of the chapter. For very full references to the
literature' of Mammalian development see especially the works in the
following list, by O. Hertwig, Handbuch, etc., 0. Hertwig, Lehrbuch,
etc., F. Keibel and F. P. Mall, Handbuch, etc., Hubrecht, Marshall, and
Minot, 1893.

ASSHETON, R., A Re-investigation into the Early Stages of the Develop-
ment of the Rabbit. Q. J. M. S. 37. 1894. On the Causes
which lead to the Attachment of the Mammalian Embryo to the
Walls of the Uterus. Q. J. M. S. 37. 1894. The Primitive
Streak of the Rabbit ; the Causes which may determine its Shape,
and the Part of the Embryo formed by its Activity. Q. J. M. S. 37.
1894. The Morphology of the Ungulate Placenta. Phil. Trans.
Roy. Soc. 198. 1906. The Segmentation of the Ovum of the
Sheep, with Observations on the Hypothesis of a Hypoblastic
Origin for the Trophoblast. Q. J. M. S. 41. 1898. The
Development of the Pig during the First Ten Days. Q. J. M. S. 41.
1898. Early Ontogenetic Phenomena in Mammals. Q. J. M. S.
54. 1909.

THE EARLY DEVELOPMENT OF THE MAMMAL 451

VAN BENEDEN, E., Recherches sur Tembryologie des mammiferes — La
formation des feuillets chez le Lapin. Arch. Biol. 1. 1880.
Recherches sur les premiers stades du developpement du Murin
(Vespertilio murinus). Anat. Anz. 16. 1899. (Brachet, ed.)
Recherches sur Fembryologie des Mammiferes. I. De la segmenta-
tion, de la formation de la cavit6 blastodermique et de 1'embryon
didermique chez le Murin. Arch. Biol. 26. 1911. II. De la ligne
primitive, du prolongement cephalique de la notochorde et du
mesoblaste chez la lapin et chez le murin. Arch. Biol. 27. 1912.

VAN BENEDEN, E. and JULIN, C., Observations sur la maturation, la
fe*condation et la segmentation de Tceuf chez les Cheiropteres.
Arch. Biol. 1. 1880.

BONNET, R., Beitrage zur Embryologie des Hundes. I. Anat. Hefte.
9. 1897. II. Anat. Hefte. 16. 1901. III. Anat. Hefte. 20.
1902.

BRYCE, T. H. and TEACHER, J. H., Contributions to the Study of the
Early Development and Imbedding of the Human Ovum. I . An
Early Ovum imbedded in the Decidua. Glasgow. 1908.

BURCKHARD, G., Die Implantation des Eies der Maus in die Uterus-
schleimhaut und die Umbildung derselben zur Decidua. Arch,
mikr. Anat. 57. 1901.

DANIEL, J. F., Observations on the Period of Gestation in White Mice.
Jour. Exp. Zool. 9. 1910.

ETERNOD, A.-C.-F., L'ceuf humain. Implantation et gestation, tropho-
derm et placenta. Geneva. 1909.

FELIX, W., See Keibel-Mall, Handbuch, etc.

GROSSER, O., Vergleichende Anatomic und Entwicklungsgeschichte der
Eihaute und der Placenta, mit besonderer Beriicksichtigung des
Menschen. Wien. 1909. See also Keibel-Mall, Handbuch, etc.

GUYER, M. F., Accessory Chromosomes in Man. Biol. Bull. 19.
1910.

HEAPE, W., The Development of the Mole (Talpa Europea). The For-
mation of the Germinal Layers, and Early Development of the
Medullary Groove and Notochord. Q. J. M. S. 23, 1883. 27.
1887.

HERTWIG, 0., Lehrbuch der Entwickelungsgeschichte des Mensch und
den Wirbeltiere. 9 Aufl. Jena. 1910. (Editor.) Handbuch
der vergleichenden und experimentellen Entwickelungslehre der
Wirbeltiere. Jena. 1906.

HILL, J. P., The Placentation of Perameles. (Contributions to the
Embryology of the Marsupialia.— I.) Q. J. M. S. 40. 1897. On
the Fcetal Membranes, Placentation and Parturition of the Native
Cat (Dasyurus viverrinus). Anat. Anz. 18. 1900.

His, W., Unsere Korperform und das physiologische Problem ihrer

452 OUTLINES OF CHORDATE DEVELOPMENT

Entstehung. Leipzig. 1874. Anatomie menschlicher Embryo-

nen. I-III. Leipzig. 1880-1885.
HOCHSTETTER, F., Bilder der ausseren Korperform einiger menschlicher

Embryonen aus den beiden ersten Monaten der Entwickelung.

Miinchen. 1907.
HUBRECHT, A. A. W., Early Ontogenetic Phenomena in Mammals and

their Bearing on our Interpretation of the Phylogeny of the Verte-
brates.. Q. J. M. S. 63. 1908.
JACKSON, C. M., On the Prenatal Growth of the Human Body and the

Relative Growth of the Various Organs and Parts. Amer. Jour.

Anat. 9. 1909.
KEIBEL, F., Zur Entwickelungsgeschichte des Rehes. Verh. Anat.

Gesell. Tubingen. 1899. Die Gastrulation und die Keimblatt-

bildung der Wirbeltiere. Ergeb. Anat. u. Entw. 10. 1900 (1901).

See also Hertwig's Handbuch, etc.
KEIBEL, F. and ELZE, C., Normentafeln zur Entwicklungsgeschichte

des Menschen. Jena. 1908.
KEIBEL, F. and MALL, F. P., (Editors and contributors). Handbuch

der Entwicklungsgeschichte des Menschen. Leipzig. 1910, 1911.

American Edition, Manual of Human Embryology. Philadelphia.

1910, 1912.
KIRKHAM, W. B., Maturation of the Egg of the White Mouse. Trans.

Connecticut Acad. Arts and Sciences. 13. 1907. (See also Biol.

Bull. 12. 1907.) Ovulation in Mammals, with Special Reference

to the Mouse and Rat. Biol. Bull. 18. 1910.
KOLLIKER, A. VON, Entwicklungsgeschichte des Menschen und der

hoheren Thiere. 2 Aufl. Leipzig. 1876, 1879. Grundriss der

Entwicklungsgeschichte des Menschen und der hoheren Thiere.

2 Aufl. Leipzig. 1884.
KOLLMANN, J., Die Korperform menschlicher normaler und patholog-

ischer Embryonen. Arch. Anat. Physiol. Suppl. 1889. Hand-
atlas der Entwickelungsgeschichte des Menschen. Jena. 1907.
KOLSTER, R., Weitere Beitrage zur Kenntnis der Embryotrophe. IV.

Zur Kenntnis des Chorionepithels. Anat. Hefte. 40. 1909.
LANE-CLAYPON, J. E., On the Origin and Life-history of the Interstitial

Cells of the Ovary of the Rabbit. Proc. Roy. Soc. B. 77. 1905.
LOEB, L., Beitrage zur Analyse des Gewebwachstums. III. Die Erz-

eugung von Deciduen in dem Uterus des Kaninchens. Arch.

Entw.-Mech. 27. 1909. The Function of the Corpus Luteum,

the Experimental Production of the Maternal Placenta, and the

Mechanism of the Sexual Cycle in the Female Organism. Medical

Record. 77. 1910.
LONG, J. A., The Living Eggs of Rats and Mice, etc. Univ. of California

Publications in Zool. 9. 1912.

THE EARLY DEVELOPMENT OF THE MAMMAL 453

LONG, J. A. and MARK, E. L., The Maturation of the Egg of the Mouse.
Publ. Carnegie Institution. Washington. No. 142. 1911.

LONGLEY, W. H., The Maturation of the Egg and Ovulation in the
Domestic Cat. Amer. Jour. Anat. 12. 1911.

McMuRRiCH, J. P., The Development of the Human Body. 3rd. ed.
Philadelphia. 1909.

MALL, F. P., Early Human Embryos and the Mode of their Preservation.
Bull. Johns Hopkins Hospital. 4. 1893. See also Keibel-Mall,
Handbuch, etc.

MARSHALL, F. H. A., The Physiology of Reproduction. London. 1910.

MELISSINOS, K., Die Entwickelung des Eies der Mause von den ersten
Furchungs-Phsenomen bis zur Festsetzung der Allantois an der
Ectoplacentarplatte. Arch. Mikr. Anat. 70. 1907.

MINOT, C. S., Human Embryology. New York. 1892. A Bibliog-
raphy of Vertebrate Embryology. Mem. Boston Soc. Nat. Hist.
4. 1893. A Laboratory Text-Book of Embryology. 2nd. ed.
Philadelphia. 1911.

NAGEL, W., Das menschliche Ei. Arch. mikr. Anat. 31. 1888.

NEWMAN, H. H., The Ovum of the Nine-banded Armadillo. Growth
of the Ovocytes, Maturation and Fertilization. Biol. Bull. 23.
1912.

PETERS, H., Ueber die Einbettung des menschlichen Eies und das frii-
heste bisher bekannte menschliche Placentationsstadium. Leip-
zig and Wien. 1899.

RABL, C., Die Entwickelung des Gesichtes. Das Gesicht der Sauge-
thiere. Leipzig. 1902.

REJSEK, J., Anheftung (Implantation) des Saugetiereies an die Uterus-
wand, insbesondere des Eies von Spermophilus citillus. Arch,
mikr. Anat. 63. 1904.

RETZIUS, G., Weitere Beitrage zur Kenntniss der Spermien des Menschen
und einiger Saugethiere. Biol. Unters. N. F. 10. 1902. Zur
Kenntnis der Entwicklung der Korperform des Menschen wahrend
der fotalen Lebensstufen. Biol. Unters. N. F. 11. 1904.

ROBINSON, A., Observations upon the Development of the Segmentation
Cavity, the Archenteron, the Germinal Layers, and the Amnion in
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RUBASCHKIN, W., Ueber die Reifungs- und Befruchtungs-prozesse des
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SCHOENFELD, H., Contribution & PEtude de la Fixation de 1'ceuf des
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454 OUTLINES OF CHORDATE DEVELOPMENT

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INDEX

(Pages 1 — 61 refer to Amphioxus : 62-228 to the frog: 229-367 to the
chick: 368-454 to the Mammal. Page numbers in heavy-face type refer to
illustrations.

Accessory cleavage furrows, 244, 246
Achoria, 438, 439, 440
adolescence, 370
adrenal bodies, 206-207, 207: 363-

364

after-birth, 450
age, frog, estimation of, 64, 127-128;

of human embryos, 403, 407

air, chamber, 233, 234; sacs,

332, 335
albumen, 233, 234, 241, 288, 289;

formation, 241; later

history, 298 ff.;
289, 298 ff.

sac, 288,

alimentary canal, 33: 158 ff.: 269,
326 ff., 335

allantois, 280, 287, 288, 289, 291, 295
ff., 296, 297, 335: 400, 402, 428,

430, 431, 434 ff.; at hatching,

300; blood vessels of, 299:

435, 436; functions of, 295:

434; fusions of, 297-298;

human, 400, 430, 435-436,

444; later history, 430, 431,

434 ff.; mammalian com-
pared with avian, 435; rela-
tion with chorion, 430, 431, 435;

stalk of, 287, 288, 289, 296,

297,297, 348:430, 431

Allen, 205

ammo-cardiac vesicles, 252, 263,
266, 267, 268, 272, 273

amnion, 280, 287, 288, 289, 292 ff.,

296, 310, 351: 444, 445;

cavity, 280, 287, 288, 289, 293,
294: 385, 386, 388, 389, 390, 390,
391, 391, 392, 393, 399, 400, 424,

444, 445; cavity, false, 389,

391, 391; cavity, formation

in man, 428 ff., 430; folds,

262, 283, 292 ff.: 391, 392, 393,

396, 425, 426 ff., 426, 427;

folds, closure of, 293, 296, 297:

425, 426, 427; folds, head,

262, 292: 425, 427; later

history, 424 ff., 428, 430

Amphioxus, outline of life-history, 3

amplexus, 78

ampulla, 150, 151: 322, 323

anal, membrane, 414, 415;

opening, 415, 415; plate,

280, 296, 296, 297, 334
annulus tympanicus, 214, 217
anterior, chamber (eye), 317, 321;

gut diverticula, 25, 32-33,

32, 35 ; intestinal portal,

261, 262, 266, 269, 272, 276, 278,

282, 291, 304, 345

anus, 35: 118, 169: 296: 415, 415
aorta, dorsal, 179, 182, 184, 184:
273, 275, 276, 278, 281, 291, 294,
329, 341, 342, 342, 348: 406;

lateral dorsal, 179, 180, 182 :

272, 291, 292, 341; ventral,

177:273,275,278,282
aortic arches, 180, 181, 181, 184:

283, 285, 291, 329, 338, 340 ff.,

341, 342, 348: 405, 405;

carotid, 184, 184: 283, 341, 342;

hyoid, 179, 183: 340, 341;

mandibular, 179, 183: 275,

278; pulmo-cutaneous, 184,

184; pulmonary, 184: 342,

342; systemic, 184, 184:

341, 342

aperture, auriculo-ventricular, 338;

sinu-auricular, 337;

urinogenital, 415 ff., 415

Aplacentalia, 438, 440
appendicular skeleton, 221—222
aqueduct of Sylvius, 132: 307

arch, see aortic; branchial, 120,

123, 160, 163, 164: 330: 404, 404,

406, 407, 408; hyoid, 66,

122, 160, 160: 330; man-
dibular, 122, 160, 160, 163, 164,

216: 283, 286, 304, 330;

pectoral, 221; pelvic, 221;

visceral, 120, 123, 160, 160,

163, 164 : 286, 328 ff.; 404 ff., 404,
406, 408; visceral, cartilagi-
nous, 211, 216 ff., 217, 218
archenteron, 15 ff., 16, 21 : 98, 101,
102,106:250

455

456

INDEX

(Amphioxus, pages 1-61; frog, 62-228

area, opaca, 233, 248, 252, 275: 394;
— pellucida, 233, 247, 252, 255,

275: 394; vasculosa, 252,

255, 256, 256, 275-277, 277,

291: 432; vitellina, externa

and interna, 262, 255, 275-277,
277

arterial system, 179 ff., 180, 181,
182, 184: 291, 340 ff., 341, 348:
405

artery, allantoic, 297; see aorta;

basilar, 182 ; branchial,

40: 179 ff., 180, 181, 181, 182;

carotid, external and in-
ternal, 180, 182, 183: 291, 329,

341, 341, 342, 348; caudal,

348 ; cerebral, 182 ; coe-

liac, 343, 348; commissural,

182, 183; cutaneous, 182,

185; genital, 343; inter-

somitic, 280; b'ngual, 182,

183; mesenteric, 343, 348;

of mandibular and hyoid

arches, 179, 182, 183: 275, 278,

340, 341; omphalomesenteric,

343: 432, 432; - — palatine, 182;

; chick, 229-367; mammal, 368-454.)

basilar chamber, 150, 151

bat, amnion, 424; blastodermic

vesicle, 390; cleavage, 381; noto-

chordal canal, 397; placentation,

439, 440; trophoblast, 389
beak, 159: 328
beating, of heart, commencement of,

339

belly stalk, 399, 400, 429, 430, 446
between-brain, 129, 131, 133: 283,

303, 304, 306 ff., 310
Bidder's organ, 167
bile duct, 167: 333;

common, 333

birth, 369
bladder, gall 166, 167, 167: 333;

urinary, 170, 201

blastocoel, 14, 16 : 93, 94, 96, 98, 102 :

245, 245, 247, 248
blastoderm, 238, 239, 240, 242-243;

at 30 hours, 275; at

time of egg laying, 232, 233 ;

growth of, 247 ff.: unincu-

bated, 250
blastodermic vesicle, 382, 383 ff.,

384, 385, 386, 390, 399;

pharyngeal, 182,183; growth of, 384; : hu-
man, 399

blastopore, 16, 18 ff.; 98, 101 ff.,
102, 118, 119, 120: 249 jf., 249,

258, 258: 397-398; closure

of, 103, 120; position of,

105, 105

pulmonary, 182, 184, 184: 329,

338, 339, 341, 342, 348;

renal, 343; sciatic, 343, 348;

segmental, 280, 342;

subclavian, 184: 341, 342, 343,

348; umbilical, 343, 348:

435, 436; vertebral, 184;

vitelline, 273, 283, 285, 290,

291, 294,338,343:432,432

articulation, jaw, 216

asymmetry, of Amphioxus larva,
49 jf.

atrial cavity, 46 ff., 47, 48

atriopore, 47, 49

atrium, see atrial cavity, auricle

auditory, capsule, 2.11 ff., 212, 214;

organ, rudiment, 121: 282,

283, 285, 321; organ, later

history, 149 ff., 150: 322 ff., 322;

ossicles, 324-325; pit,

282, 283; sac, 140, 149,

160: 321 jf., 322, 322,329

auricle, 176, 177: 283, 285, 291, 310,
337, 339, 342, 348, 355

auriculo-ventricular aperture, 338

axis, of chick embryo, 243

axons, of retinal cells, 320; of

spinal nerves, 311

von Baer, 299 : 376

basal, ganglia, 306; plate, of

cranium, 211, 212, 213;

of placenta, 449

blastula, 12, 14, 16: 92, 93 ff., 94,
96, 247, 247, 248: 383; sym-
metry of, 96

blood, cells, 256, 273; corpus-
cles, 179: 350; islands, 178,

179: 252, 255, 256, 271, 272, 277;

origin, 178-179, 178;

vessels, 46: 271 jf., 273, 277;

vessels, allantoic, 280, 299: 435,

436; branchial, 179 .ff.,

180; origin, 178-179;

oxus, 31;

rudiments in Amphi-
yolk-sac, 290,

291 : 432-433, 432 ; see also artery,
vein

Blount, 246, 247

body, cavity, 124, 170, 173: 350 jf.,

352; see also caelom; form

of human embryo, 399 ff.;

Malpighian, 200, 201, 205: 356,

357, 359, 362; pineal, 130:

307; pituitary, 132: 327;

post-branchial, 331, 331 ;

pseudothyroid, 164; supra-

pericardial, 163, 164; ultimo-
branchial, 163, 164; vitreous,

148: 320; wall, 282;

INDEX

457

(Amphioxus, pages 1-61; frog, 62-228;

body, Wolffian, 198 ff., 199, 200:

335, 357, 358, 359, 360
bone, angular, 220; dentary,

217, 220; dermal, of skull,

214, 219-220; exoccipital,

214,215; frontal, 219;

fronto-parietal, 214, 219;

lateral occipital, 215; maxil-
lary, 214, 219; nasal, 214,

219; orbito-sphenoid, 215;

palatine, 220; para-
sphenoid, 219; parietal, 219;

premaxillary, 214, 219;

prootic, 215; pterygoid, 214,

220; quadrato-jugal, 214,

215, 220; septo-nasal (intra-

nasal), 219; sphenethmoid,

215; squamosal, 220;

vomer, 220

Bonnet, 384

Bouin, 206

Bowman's capsule, 199, 200: 357

Brachet, 79, 86, 136, 179

brain, 25, 28: 118, 121, 166: 262,
266, 271, 278, 303 ff.; 402 ff.
See also, flexure, nervous system,
prosencephalon, etc.

branchial, arches, 120, 123, 160, 160,
163, 164: 330: 404, 404, 406, 407,

408; blood vessels, 179 ff.,

180 ; clefts, see gill, clefts;

grooves, 65, 122; pouches,

41: 122, 158, 160, 160, 163, 164:
269, 278, 328 ff., 329

branchiomeric nerves, 135

bronchi, 332

buccal cavity, 42, 45 : 327-328;

cirri, 42, 44, 45

bulbus aortse, 177, 178; ar-

teriosus, 176: 282, 286, 291, 304,
310, 335, 338, 339, 340

bursa Fabricii, 334

Bryce-Teacher, 442

Caecal process, 335

caecum (caeca), 36, 42, 55;

intestinal, 335.

camel, placentation, 439, 440

canal, central, 134: 280, 305, 308;

neurenteric, 16, 21, 25, 28 : 118,

119, 120: 259: 397, 398, 400, 401;

not9chordal, 397-398, 397;

semicircular, 150, 151: 322,

323

capsule, auditory, 211 ff., 212, 214;

Bowman's, 199, 200: 357;

olfactory, 210, 211, 212, 214,

215; ovarian, follicular, 376;

pronephric, 194, 197;

sense, 210 ff.

chick. 229-367; mammal, 368-454.)

Carnivora, allantois, 434, 436; am-
nion, 392, 424; implantation, 421;
placentation, 439, 440, 441; uteri,
372; yolk-sac, 433

carotid, arch, 184, 184: 283, 341,

342; gland, 163, 163, 182,

184, 184

cartilage, annular, 213, 217;

basibranchial, 217, 218, 218 ;

basihyoid, 218; branchial,

217 ff., 217, 218; cerato-

branchial, 217, 218, 219;

ceratohyal, 217, 218, 218, 219;

hyoid, 217 ff., 217, 218;

infrarostral, 211, 212, 216,

217; intervertebral, 209;

labial, 210, 211, 212, 215;

mandibular, 164;

Meckel's, 211, 212, 216, 217, 220;

mento-Meckelian, 217;

mesotic, 212; occipital, 212;

palato-quadrate, 164, 211,

211, 212, 214, 215, 216 ff.;

parachordal, 210; quadrate,

216; suprarostral, 210, 211,

212, 215; trabecular, 210,

211, 212, 213; vertebral, 208-

209, 208

cat, chromosomes, 377; fertilized
ovum, 380; gestation, 369; ma-
turation, 380; ovulation, 379

cavity, amnionic, see amnion; — —

body, 124, 170, 173: 350 ff.;

buccal, 42, 46: 327-328;

gonadial, 56, 67, 58; inter-

amnionic, 389, 391; inter-

villous, 442, 447, 449; intra-

placental, 446, 449; opercu-

lar, 161, 163; • • parietal, see

exoccelom; pericardial, 166,

174, 176, 180, 192 : 262, 267, 275,

310, 350 ff., 361 ; perigona-

dial, 56; peritoneal, 352;

pleural, 351; preoral,

26, 32, 33; segmentation,

14, 16 : 93, 94, 96, 99, 102 : 245,

246, 247, 248 ; subgerminal,

245, 245, 248; tubo-tym-

panic, 152; tympanic, 152:

324, 328

central, canal, 134: 280, 306, 308;

cells, 244, 244, 246;

nervous system, see nervous system

cerebellum, 129, 132, 133: 306, 307
cerebral, hemispheres, 129, 131, 133:

306, 306: suture, 274, 276;

vesicle, 26, 36, 38

cervical sinus, 406, 407
cervix, uteri, 444
chalazse, 233, 234, 241

458

INDEX

(Amphioxus, pages 1-61; frog, 62-228;

chamber, air, 233, 234; anterior

(eye), 317, 321; basilar, 160,

151; laryngeal, 165, 166;

posterior (eye), 146, 147:

317, 318 ; pronephric, 196, 197

chiasma, optic, 129, 131, 133, 148:
306

chick, embryo at 30 hours, 275 ff.;

formation of embryo, 251 ff.,

262, 256 #., 268, 260, outline

of developmental history, 231;
position in egg, 243, 299

Chiroptera, see bat.

choanse, 154, 155, 158: 325

chondrocranium, 210 ff.

chorda, see notochord.

Choriata, 438, 439, 440

chorion, 69: 287, 288, 289, 292 ff.,
294, 310, 361: 399, 400, 421, 438,

439, 444, 446, 449; ectoderm

of, 421 ; frondosum, 446;

human, 399, 400, 444, 446, 449;

Iseve, 444, 446; later

history, 424 ff., 426, 428, 430;

relation to allantois, 430, 431,

435; villi of, 438 ff.; see also

villi.

choroid, fissure, 146, 146, 147: 310,

SISff., 318, 329; knot, 149;

plexus, of III ventricle, 130,

133: 305, 307; of IV

ventricle, 134:306, 308
chromosomes, number in Mammals,

377
cicatrix (cicatrices), 7, 67, 58: 236,

240: 378

cilia, superficial, 26: 116
ciliary process, 319
circulation, allantoic, 299: 435, 436;

yolk-sac, 290, 291 : 432-433,

432

cirri, buccal, 42, 44, 46
clavicle, 221
cleavage, 10, 11 ff., 12: 80, 91

92: 243 ff., 244, 246 : 380 ff., 3i

accessory, 244, 246;

delaminating, 93, 94; first,

plane of, 11: 89 jf.; 243: 382;

gastrular, 99, 100; pores, 14

cleft, see gill.

clitoris, 416, 416, 417

cloaca, 169: 280, 296, 297, 334, 348-.

414
cloacal, membrane, 297: 414 ff.,

415; tubercle, 415, 416, 417

closing plate, 449, 450

club-shaped gland, 26, 32, 34, 35,

40,43

coccygeal tubercle, 416
cochlea, 160, 151:322,323

chick, 229-367; mammal, 368-454.)

cochlear duct, 323

coelogastrula, 17

ccelom, 31, 32, 47, 62 : 124: 256, 265,

266-267, 294: 398, 402;

branchial, 49; dorsal, 49;

endostylar, 49

coitus, relation to ovulation, 379

collecting tubule, mesonephric, 367,
358; metanephric, 358

columella, 152: 213, 215

commissure, anterior, 129, 133 : 306,

306; habenular, 130, 133:

305; pallial, 305;

posterior, 132, 133: 306;

spinal, 306 ; tubercular, 133

common trunk, pronephric, 194

concrescence, 103: 257 ff., 268

condyles, occipital, 215

confluence, 103, 112: 257 ff., 258

contra-deciduata, 439

copula, 217, 218, 219

copulation path, 80, 80

coracoid, 221

cord, sex, 204, 204, 205: 362, 362;

spinal, 37: 117, 118, 134, 134 :

308; sympathetic, 143, 143:

312-313, 312 ; umbilical, 406,

407, 408, 430, 444, 445

cornea, 147, 149: 317, 321

Corning, 136

cornu (cornua), hyoid, 218, 219;
trabecular, 210, 211,212, 215

corona radiata, 373, 376, 379, 380

corpora quadrigemina, 133;

striata, 306

corpuscles, blood, 179: 350

corpus luteum, 378

cotyledons, 438, 448

cow, gestation, 369

cranium, 210 ff.

crescent, gray, 85, 86

crest, neural, 119, 124, 136, 137, 139,
142, 194:266,270, 309

cristae, auditory, 323

critical stage, 4, 54

crop, 335

crown-rump length, 407, 411

crura cerebri, 132: 307

cup, optic, 145, 146, 147: 316 ff.,
317, 318

cushion, endothelial, 338

cutis, 53; plate, 171-172, 171:

352-353

Cuvierian sinus, see ductus Cuvieri

cytotrophoblast, 422 ff.

Daniel, 369

Dasyurus, embryonic membranes,

419; gestation, 370; placentation.

419, 439, 440

INDEX

459

(Amphioxus, pages 1-61; frog, 62-228;

decidua, 439, 443; basalis, 443,

444, 445, 447, 449, 450; capsu-

laris, 442 ,443, 444 ; compact

layer, 443; reflexa, 442, 443;

serotina, 443; spongy

layer, 443; vera, 443, 444, 450

deciduata, 439

"Deckschicht," 130

deer, cleavage, 381 : embryocyst,
387: embryonic shield, 387; fer-
tilization, 381; gestation, 369;
ovum, 373; placentation, 439, 440

denticulate ligament, 49

dermal, bones, of skull, 214, 219-220;
fold, 52

dermatome, 52, 62: 171-172, 171:
294, 352-353

deutoplasm, 4, 5: 69, 74, 75: 230;
see also yolk.

Didelphia, ova, 418-419; embryonic
period, 419

Didelphys, blastodermic vesicle, 388;
gestation, 370

diencephalon, 129, 131, 133: 283,
303, 304, 306 ff., 310

digestive tract, see alimentary canal.

discus proligerus, 375

diverticulum, gut, anterior, 25, 32-33,
32, 35 ; Meckel's, 434

dog, cleavage, 381: embryo, 394;
embryonic shield, 393, 394 ; for-
mation of embryo, 393 ff.; gesta-
tion, 369; oogenesis, 375; ovary,
375; ovulation, 379; ovum, 373;
trophoblast, 388, 388

dorsal aorta, see aorta

dorsal, coelomic canal, 49;

thickening (brain), 129, 131

duct, bile, 167: 333; cochlear,

323; mesonephric (Wolffian),

199, 199, 202 ff.; 265; 294, 355 ff.,

357, 358, 359, 360; meta-

nephric, 359, 359 ; Miillerian, 202 ff.,

203 : 335, 360-361 ; pancreatic,

168; pronephric (segmental),

193 ff., 194, 195, 196, 198;

reproductive, 202 ff.; 360^.,

thoracic, 191: 349; urino-

genital, 202 ff.

ductus, arteriosus, 341, 348;

Botalli, 185: 342; chole-

dochus, 167: 333; Cuvieri,

185 ff., 192: 283, 285, 291, 310,
329, 337, 344, 345, 351; —
endolymphaticus, 150, 151: 322,

322 ; venosus, 285, 291, 304,

333, 337, 344, 345, 348

dugong, placentation, 440

duodenal loop, 168

duodenum, 335, 336

chick, 229-367; mammal, 368-454.)

Ear, 149 ff., 150, 211 ff.t 212, 214:

321 ff., 322; internal, 324;

middle, 152-153: 324;

outer, 324; see also auditory.

Echidna, ovum, 418

ectoderm, 15, 16: 98 ff., 98, 100:
247, 249 ff., 249, 253, 280: 385 ff.,
386, 391, 395 ff.

egg, see ovum; membranes, 4,

5, 8, 9, 10: 69, 80, 81, 82: 233, 234:

373, 374, 376, 380, 382;

membranes, functions, 82;

tooth, 328

"egg," of fowl, 231 ff., 233, 242

elephant, gestation, 369; placenta-
tion, 440

Elliot, 172, 173

embryo, axis of, 243; formation

of, 251 ff., 252, 256 jf., 258, 260:

384 ff.;

position in "egg,1

243, 299; see also human.

embryocyst, 387, 392

embryonic, membranes, 286 ff., 287,
288, 289: 417 ff., 425, 428, 430;

see also amnion, chorion etc.;

comparison of mammalian

and sauropsidan, 417;

functions, 290, 295: 417-418;

shield, 387, 388, 392, 393 ff.t
394

embryotrophe, 441, 442

enamel organ, 220: 328

endocardial septum, 266

endoderm, 15, 16 : 98, 100, 102 : 247,
249 ff., 249, 253, 267 ff.; 385, 386,

390, 391, 391, 392, 395, 396;

yolk-sac, 256, 272, 277, 289-290:
390, 391, 425, 431

endolymphatic, duct, 150, 151: 322,
322; sac, 152:323

endostyle, 34, 35, 40, 42, 43

endothelial cushion, 338

endothelium, 175-176, 175, 178, 187:
256, 272, 274

enteroccel, 21, 24, 26, 29, 30

enterocoelic grooves, 110, 110, 114

enteroderm, 121, 122

enteron, 26, 29, 33 ff.: 122-123, 158
ff.: 326 ff.

entoderm, see endoderm.

entypy, 387, 389

ependyma, 37

ependymal cells, 134: 308

epiblast, see ectoderm.

epiboly, 15 ff.: 98, 99: 251

epicoracoid, 221

epididymis, 362, 363

epipharyngeal groove, 44

epiphysis, 118, 118, 130, 131, 133:
285, 304, 306, 307

460

INDEX

(Amphioxus, pages 1-61; frog, 62-22J

epithelioid bodies, 163, 163: 331

epithelium, acustic, 323; folli-

cular, 373, 374 ff., 376; ger-
minal, 361, 362; neuro-, 326;

olfactory, 326

Erinaceus, see hedgehog.

erosion, of uterine wall, 422, 424;
in classification of pla-
centae, 440-441

ethmoid region, 215

Eustachian tube, 152: 324, 328

Eutheria, embryonic membranes,
419 ff.; placentation, 437$".

excretory system, 53: 192 ff.: 355 ff.

exocoelom, 262, 266, 267, 272, 278,
280, 281, 282, 287, 287, 288, 289,
294: 427, 428; human, 400

external, form, chick embryo, es-
tablishment of, 282 ff.; —
human embryo, 399 ff., 400, 401

ff.; genitalia, 414 ff., 415;

- gills, 65, 161

extra-embryonic ccelom, see exo-
coelom.

eye, 65, 121, 144 ff., 144, 145 : 316 ff .,

317, 318; see also optic;

muscles, innervation, 315

Face, development in human embryo,
411 ff., 412, 413

Fallopian tube, 371, 372

false amnionic cavity, 389, 391, 391

fascia, 52

fat bodies, 71, 72, 205

feather papillae, 286

Federow, 189

fenestra vestibuli, 213

ferret, ovulation, 379; placentation,
440

fertilization, 6, 9: 78, 79 ff., 80, 85:
240-241 : 379-380, 380 ; merid-
ian, 79, 84

Field, 194

filtering organ, 162

fimbriated opening, 311; during

ovulation, 378

fissure, choroid, 146, 146, 147 : 310,
318 jf., 318, 329; tubal, 328;

ventral, 135

fixation villi, 442, 447, 448, 449
flexures, of brain, 270, 283, 284: 404;

cervical, 284, 285, 308: 405,

406, 406; cranial, 284, 285,

304, 308; pontine, 308; -

ventral, 128, 130; of head and

tail, 402 ff.

folds, amnionic 262, 283, 292 ff.:-
391, 392, 393, 396, 425, 426 ff.,
426, 427; — — amnionic, closure
of, 293, 296, 297: 425, 426, 427;

chick, 229-367; mammal, 368-454.)

folds, genital, 415, 416, 417;

medullary (neural), 16, 21, 22, 23:
261, 266, 268, 269, 270, 278: 398;

mesoderm, 21, 24; meta-

pleural, 40, 47, 47, 48; prim-
itive, 253, 254; supraorbital,

413, 414; suspensory, 49; —

tail, 280, 293, 296, 296, 297 ff., 297

follicle, Graafian, 375, 376;

ovarian, 56, 57: 206, 235, 236,
238, 239: 373, 374, 375, 376, 378;

ovarian rupture of, 378

follicular epithelium, 373, 374 ff.,

375
fontanelle, basicranial, 211, 211,

212; supracranial, 213

foramen (foramina), interventricular

340; - - jugular, 211, 212, 212;

magnum, 212, 213; of

Monro, 131-132: 306;
153

ovale,

fore-brain, 129, 131, 131: 262, 271,

282, 302, 303 ff., 317
fore-gut, 122, 159 ff.; 260, 261, 261,

262, 268, 274, 276, 278, 326 ff.,

329

fovea, 69, 74
frog, age, at maturity, 68; age,

estimation of, 64, 127-128;

" early embryo/' 64, 65, 116, 120;
— metamorphosis, 67-68;

outline of life history, 63 ff.
frontal process, 412, 412
fronto-nasal process, 325
fundus, eye, 146: 319; uterus,

372, 442
furrow, intersomitic, 263

Gall bladder, 166, 167, 167 : 333
ganglion (ganglia), acustico-facialis,
136, 137, 157: 282, 283, 310, 329;

basal, 306; ciliary, 316;

cranial, 309; crest, 136,

137,138;

facialis;

facial, see acustico-

Gasserian, 140: 329;

- geniculate, 315, 329;

glossopharyngeal, 136, 137; —

habenular, 130; jugulare,

314; jugulare-nodosum, 309;

— nodosum, 196 ; 314, 329 ;

ophthalmic, 138; petro-

sum, 309, 329 ; pneumogas-

tric, 137, 137; profundus,

315; Remak's, 312;

spinal, 135, 142, 143: 294, 309,

311; sympathetic, 144, 207,

207: 364; trigeminal, 136,

137, 138, 139, 140, 157: 283, 285,

310, 315; vagus, 137, 137,

157

INDEX

461

(Amphioxus, pages 1-61; frog, 62-228;

gastro-hepatic ligament, 335
gastrula, 16, 17, 19-20: 65, 99 ff.,

98, 102, 104, 105: 249, 252, 257

ff.; 385; rotation of, 98, 104,

105 ff., 105

gastrular cleavage (groove), 98, 100.

gastrulation, 15 ff., 16, 17 : 99 ff., 98,
102, 106, 111 ff.: 248 ff., 249,
251, 259; - — comparisons, Am-
phioxus, 113 ff.; - frog,

111 ff.; chick, 259

genital, folds, 416, 416, 417;

ridge, 415; ridge (sex-cell),

204, 204, 205; swelling, 415,

416, 417; tubercle, 415, 416,

417

genitalia, external, 414 ff.

germ,cells, 4, 5, 6: 65, 68 ff., 70, 81,

85 : 232 ff., 233 : 372 ff., 373, 383 ;

— formation of, 64, 71 ff.,

199, 205: 361, 362, 363: 375,

— — disc, see blastoderm;

layers, 15 ff., 16, 21, 24 ff.: 98 ff.,

99, 102, 107 ff., 110, 111 ff.: 247,
248 ff., 249, 252, 254, 254, 260,
264, 272, 280: 385, 385, 390, 391,
392, 395 ff., 396, 397, 398, 399;

— layers, inversion of, 389, 391 ;
see also ectoderm, endoderm, meso-

derm; ring, 16, 18, 24: 94,

95, 96, 101, 112; - - wall, 247,

247, 248, 254, 256, 258, 264, 272

germinal, cells (nervous), 134: 308;

— epithelium, 361, 362
gestation, duration of, 369
gill, clefts (slits), 32, 35, 35, 39 ff.,
40, 41, 42, 55 : 160: 283, 286 : 404 ff.,

404 ; first, 35, 40 ; —

- primary, 32, 35, 39 ff., 40, 42 ;

secondary, 39 ff., 40 ;

tertiary, 41, 55;

vestiges of, 162, 163, 164:

330, 331 ; filaments, 162;

plate, 65, 122; pouches, 41:

122, 158, 160, 160, 163, 164: 269,
278, 328 jf., 329; rakers, 180

gills, external and internal, 65, 161,
180, 181

gizzard, 335, 336

gland, carotid, 163, 163, 182, 184,

184; club-shaped, 25, 32,

34, 35, 40, 43 ; uterine, 443,

445

glans clitoridis, 415; penis,

415, 416, 417

glia ceUs, 134: 308

globular process, 413, 413

glomerulus, 182, 184, 196-197, 196,
198, 199, 200

glottis, 165, 166: 332

chick, 229-367; mammal, 368-454.)

gonad, 6, 55 ff., 57: 71-73, 72, 203
ff., 204, 205: 335, 361 ff., 362.
See also ovary, testis.

gonadial cavities, 56, 57, 58

gonoccel, 7, 56, 57

gonoducts, see ducts, reproductive.

gono-nephrostome, 56

Goodrich, 53

Graafian follicle, 375, 376

Graf von Spec's Embryo Gle, 400, 401

granulosa cells,71 : 237, 239 : 375, 376

gravitational plane, 86

gravity, as a factor in determining
symmetry, 86 ff.

gray crescent, 85, 85

groove, branchial, 65, 122;

enteroccelic, 110, 110, 114; •

epipharyngeal, 44; — - hyper-
branchial, 44; interventricu-

lar, 338; intestinal, 281, 281;

laryngo-tracheal, 332;

medullary (neural), 65, 111, 117,

120: 263, 269: 401; of Hat-

schek, 35, 40, 45, 46; olfac-
tory, 154; pleural, 310, 351;

primitive, 119,120: 252,252,

253, 254, 263, 268: 395, 396, 398,
401

Grosser, 424, 440

•guinea-pig, amnionic cavity, 389,
424; gestation, 369; implantation,
421; notochordal canal, 397; ovum
373; trophoblast, 389

gut, 25, 29, 33 ff.: 122, 158 ff.: 326 jf.:
402 ff.; - — diverticula, anterior,

25, 32-33, 32, 35; postanal,

170: 280, 296, 296, 334;

preoral, 262, 304, 328, 329

Guyer, 377

Hsemotrophe, 441

Halicore, placentation, 440

Hall, 198

Harrison, 156

hatching, 26:66:299-300

Hatschek's groove, 35, 40, 45, 46;
nephridium, 35, 42, 45, 46

head, cavity, 25, 32, 33; fold,

252, 260, 260, 261, 262, 263, 278,

281; fold, of amnion, 262,

292: 425, 427; kidney, 193;

process, 252, 253, 259: 395

heart, 118, 125, 166, 174 ff., 175, 176,
182: 262, 266, 273 ff., 276, 278',
286, 291, 304, 337 ff., 338, 342,

351: 402 ff.; commencement

of beating, 339; lymph, 189,

191:349-350

heat, effect upon symmetry, 88; see
also oestrus.

462

INDEX

(Amphioxus, pages 1-61; frog, 62-228; chick, 229-367; mammal, 368-454.)

hedgehog, blastodermic vesicle, 388 ;
cleavage, 381; notochordal canal,
398; trophoblast, 389; trophoderm,
422; yolk-sac, 433

Held, 142

hemispheres, cerebral, 129, 131, 133 :
305, 306

Hensen's node (knot), 262, 253, 257,
260:394,395, 396

hernia, intestinal, 408

Hertwig, 439

Hill, 303:419

hind-brain, 129, 131, 132, 133: 262,

271, 276, 303; gut, 122, 169-

170: 279, 296, 296, 327, 334

hippopotamus, placentation, 440

His's Embryo M, 403, 404

horse, gestation, 369; implantation,
421; placentation, 439, 440; yolk-
sac, 433

Hoyer, 190

Hubrecht, 385, 421

human embryo, early development,
399, ff., 400, 401; ex-
ternal form, 399, ff.;

face, 411, ff., 412, 413;

measurement of, 407;

structure at 2.6 mm., 405 ff.,

406. See also man.

humor, vitreous, 148: 320

Huxley, 439

hydatid, 372

hyobranchial, apparatus, 217, 218,
218, 219; pouch, 162

hyoid arch, 65, 122, 160, 160: 330;
cornu, 218, 219

hyomandibular pouch, 160, 160, 161,
162:324,330

hyperbranchial groove, 44

hypoblast, see endoderm.

hypobranchial plate, 217, 218, 218

hypochordal rod (hypochorda), 169,
194, 204

hypophysis, 118, 121, 130, 131, 132,
133, 166: 304, 305, 327, 329

Hyrax, placentation, 440

Ilium, 221

implantation, 378, 421 ff.;

central, eccentric, interstitial, 421;

of human "ovum," 442

incubation, 231

incus, 325

indifferent period, genitalia, 416;

gonad, 361-362

infundibulum (brain), 38, 39: 130,

130, 131, 133, 145, 160: 262, 282,

304, 305, 306; of oviduct, 203 :

235, 236, 360: 371, 372 ;

during ovulation, 378

inner cell mass, 382, 383, 384, 385,

386, 390

Insectivora, amnion, 385, 424; blas-
todermic vesicle, 385, 386, 387;

cleavage, 381; germ layers, 385;

implantation, 421 ; placentation,

440; trophoblast, 389
integumentary organs, 156
interammonic cavity, 389, 391
interauricular septum, 177: 338, 339
intermediate cell mass, 173, 193 : 265-

266,265:355
internasal plate (septum), 210, 211,

215

intersomitic furrow, 263
interventricular, foramen, 340;

septum, 338, 340
intervillous cavity, 442, 447, 449
intestinal, caeca, 336; groove,

281, 281; hernia, 408;

portal, anterior, 261, 262, 266, 269,

272, 276, 278, 282, 291, 304, 345 ;

posterior, 280

intestine, 122, 168-169: 335 ff., 335,

348

intra-placental cavity, 446, 449
imagination, 15 ff.: 99 ff., 98, 107,

111 ff-
inversion, of germ layers, 389, 391

involution, 15 ff.: 249

iris, 147, 149: 317, 319, 321

ischium, 221

isthmus (brain), 262, 283, 285, 304,

307; (oviducal), 235, 236

iter, 307

Jackson, 408, 411

Jacobson's organ, 154, 155

jaws, 325, 327, 328: 412, 412, 413,

413; articulation, 216;

horny, 159, 166
jejunum, 329, 336
Jenkinson, 88, 89
junction, zone of, 247, 258, 277, 277

Keibel and Elze's Embryo, Klb., 401,

402

kidney, 359; head, 193

Kirkham, 378

knot, choroid, 149; Hensen's

(primitive), 252, 253, 257, 260:

394, 395, 396
Knower, 189
Kolliker, 439
Kollmann's Embryo, Bulle, 401, 402;

2.5 mm., 402

Labia, majora and minora, 415, 416 ,
417

INDEX

463

(Amphioxus, pages 1-61; frog, 62-

labyrinth, 152: 324; bony,

cartilaginous, membranous, 324
lactation, 370
lagena, 160, 151:322, 323
lamina terminalis, 129. 131 : 270, 306
Langhans, cells of, 446, 447
larva, Amphioxus at the critical

stage, 4, 54

laryngeal chamber, 165, 166
laryngo-tracheal groove, 332
larynx, 329, 332
latebra, 239, 243, 245
lateral, dorsal aorta, 179, 180, 182 :

272, 291, 292, 341; folds, 281,

281; of amnion, 293;

line nerve, 142, 156, 157;

line organs, 141, 156, 167;

mesocardia, 344, 350 ff., 361;

plate, 31: 123-124, 170, 171,

194 : 263, 278
Legros, 53
Lemurs, allantois, 434, 436; placen-

tation, 440

length, of human embryos, 407, 411
lens, 146 -148, 146, 147 : 283, 316, 317,

318, 318, 320-321; placode,

146

lenticular zone, 319
life history, Amphioxus, 3;

chick, 231; frog, 63 ff.;

Mammal, 369 ff.
ligament, denticulate, 49; gas-

tro-hepatic, 335; interverte-

bral, 209; uterine, 372

Lillie, 277; quoted, 299-300, 352
limbs (and buds), 65, 128: 285, 286,

347 : 406, 406, 409
lips, 158, 159, 166 : 413, 413

liquor, amnii, 430; folliculi, 376

liver, 36, 42, 55: 118, 122, 159, 165,

166, 167 : 304, 332-333, 335, 345,

348, 351
lobe, olfactory, 129: 305 ; optic,

129, 132:307

lobus olfactorius impar, 38
loculi, placental, 448
Loeb, L., 378, 442
lung, 67, 165, 167: 304, 310, 332,

335, 351

lutein, 378; cells, 378

lymphatic, hearts, 189, 191: 349-350;

sacs, 191; sinuses, 190-

191, 190; system, 189-191,

190 ; tissue, 168

Maculae, acustic, 323
Mall, 407, 411
malleus, 325

Malpighian bodies, 200, 201, 205 : 356,
357, 359, 362

228; chick, 229-367; mammal, 368-454.)

Mammal, outline of life history,
369 #.

man, allantois, 435 ff.; amnion
formation, 428 ff., 430 ; amnionic
cavity, 399, 400, 424, 444, 445;
blastodermic vesicle, 399, 400 ;
chorion, 444, 446, 446; chromo-
some number, 377; embryo, early,

399, 400, 401 ; development

of external form, 399 ff.; in

utero, 445; exoccelom, 429, 433;
germ layers, 396 ; gestation, 369 ;
lutein, 378; mesoderm, 399, 400;
notochordal canal, 398; ovary, 371,
372 ; oocyte, 373 ; placenta, 442 jf.,
444, 446; placentation, 439, 440,
441; proamnion, 429; reproductive
system, female, 372 ; trophoblast,
389; trophoderm, 422; uterus,
gravid, 444; yolk-sac, 433 ff.;
yolk-stalk, 444, 446

mandibular arch, aortic, 179, 183:

275, 278; cartilaginous,

164, 216; visceral, 122,

160, 160, 163: 283, 286, 304, 330;

process, 404, 404, 406, 407,

412, 412 ; ridge, 158

Manis, placentation, 440

marginal, cells, 244, 245-246, 246;

notch, 268 ; sinus, 252, 262,

255, 290: 431, 432, 432, 449, 449

margin of overgrowth, 247, 249, 258,
277, 277

Marshall, 378, 442; quoted, 67-

68; — and Bles, 183, 201

Marsupialia, embryonic membranes,
419; gestation, 370, 419; ova, 418-
419; placentation, 419, 437, 439,
440

marten, placentation, 440

mass, inner cell, 382, 383, 384, 385,

386, 390; intermediate cell,

173, 193: 265-266, 266, 355

maturation, 6, 8, 9: 73 ff., 76, 82 ff.;
240, 340, 341:374, 376-377

Maurer, 180

maxillary process, 404, 406, 407, 412,
412

measurement of human embryos, 407,
411

meatus, 325

Meckel's diverticulum, 434. See
also cartilage

medulla (oblongata), 117, 129: 308

medullary folds, 16,21, 22, 23: 261,

266, 268, 269, 270, 278: 398;

furrow (groove), 269 : 394, 396, 398,

401 ff., 401 ; plate, 21, 22, 23:

110-111, 110, 117, 120, 124, 137,
194: 252, 253, 260, 261, 263, 264,

464

INDEX

(Amphioxus, pages 1-61; frog, 62-238;

medullary furrow, 269; tube,

270, 278. See also, neural.

membrana granulosa, 71 : 237, 239 :
375, 376

membrane, anal, 414, 415 ;

cloacal, 297: 414 ff., 415;

embryonic, 286 ff., 287, 288, 289,
290, 295: 417 ff.; - - of egg, 4, 5,
8, 9, 10: 69, 80, 81, 82: 233, 234:
373, 374, 376, 380, 382 ; - - of
egg, functions of, 82 ; — — of egg,
swelling of, 81; — — oral, 132, 158,
159, 164: 261, 262, 269, 276, 282,
394, 327: 412, 412; - - peri-

vitelline, 5, 9; pleuro-perito-

neal, 352; shell, 233, 234, 241 ;

tympanic, 152, 213: 325;—

urinogenital, 414 ff.: 415;

vitelline, 4, 5, 8: 69: 232, 233, 245,
247,287:374

menstruation, 379, 421

meridian, fertilization, 79, 84

mesencephalon, 129, 131, 132, 133:
262, 270, 271, 283, 303, 304, 305,
307

mesenchyme, 138, 139, 140, 141, 171,
172: 264, 309, 353

mesenteron, 25, 29: 118, 122 ff.:
334 #.

mesentery, dorsal and ventral, 174,
204, 204 : 335, 351

mesocardium, dorsal and ventral,

175, 176, 192: 272, 274;

lateral, 344, 350 ff ., 351

mesoderm, 21, 24, 25, 29 ff. : 99, 102,
107, ff., 123, 137, 170, 194: 252,
253 ff., 254, 256, 262 ff., 263, 272,
278, 294: 395, 396, 398, 399, 402;

bands, 24; ccelomic, 255,

256 ; folds, 21, 24; - — formation
in frog compared with Amphioxus,

114 ff.: gastral, 24,26: 114-

115: 259, 262; lateral plate of,

31: 123-124, 170, 171, 194: 263,
278; - - peristomial, 26: 114-

115: 259, 262; somatic and

splanchnic, 31: 124, 124, 170: 256,
265, 266-267, 272, 277 ; yolk-
sac, 425, 432

mesogastrium, 335

mesohepaticum, 187, 192

mesonephros, 193, 198 jf., 199, 200:
335, 348, 355, 356 ff., 357, 359;

disappearance of, 358; —

duct of, 199, 199, 202^.: 265, 294,
355 ff., 357, 358, 359, 360; -
tubules of, primary, secondary,
tertiary, 294, 356-357, 357, 359,
362; - -units, 198 #., 199, 200;
vestiges of, 360

chick, 229-367; mammal, 368-454.)

mesorchium, 202, 205 : 363

mesovarium, 71, 202, 205: 235, 236,
361: 371, 372

metagastrula, 383

metamerism, 265

metamorphosis of tadpole, 67-68

metanephrogenous tissue, 359

metanephros, 355, 358 ff.; duct

of, 359, 359 ; tubules of, 358-

359, 359

metapleural folds, 40, 47, 47, 48

Metatheria, gestation, 419; ova,
418-419

metencephalon, 129, 132, 133 : 283,
303, 304, 307

micropyle, 9: 79: 374

mid-brain, 129, 131, 132, 133: 262,
270, 271, 276, 283, 303, 304, 305,
307; gut, 167, 169: 327, 334

Minot, 422

mole, amnion cavity, 293; amnion
folds, 428; germ layers, 396; noto-
chordal canal, 397, 398; primitive
streak, 396 ; yolk-sac, 433

Monodelphia, embryonic mem-
branes, 419 ff.

Monotremata, ova, 418; placenta-
tion, 439, 440

Monro, foramina of, 131-132: 306

mons veneris, 417

morula, 382, 383

mouse, amnion folds, 424; blasto-
dermic vesicle, 384; chromosomes,
377; cleavage, 381; false amnionic
cavity, 389; gestation, 369; im-
plantation, 421; lutein, 378; ovu-
lation, 379; ovum, 373; polar
bodies, 377, 378; sperm entrance,
380; Trager, 389; trophoblast, 389

mouth, 34, 35, 40, 42, 44, 47 : 65, 118,
122, 128, 158, 166: 269, 304, 327:
404, 412, ff., 412

mucosa, uterine, 443

Mullerian duct, 202 ff., 203: 335,
360-361

muscle, fibrillse, 172 : 353; of eye-
ball, innervation, 315; plate,

171, 171: 352-353

musculature, ventral, 53

Mustelidse, placentation, 440

myelencephalon, 117, 129, 132, 133,
134:283, 285, 303,304,307

myoco3l, 31, 48, 52 : 124, 125, 170 : 265,
295

myocardium, 266, 272

myocommata, 172

myotome, 31, 48, 51, 52: 123, 171,
171, 194 : 294, 352-353

Nares, 154, 155: 325-326

INDEX

465

(Amphioxus, pages 1-61; frog, 62-228; chick, 229-367; mammal, 368-454.)

nasal septum, 413, 413
nephridia, 40, 53, 54
nephridium of Hatschek,35, 42, 45, 46
nephrostome, mesonephric, 201: 358;

metanephric, 359; pro-

nephric, 194, 195, 195, 196, 198;

common, 197, 199

nephrotome, 173, 193: 265, 265, 355,

356
nerve, branchiomeric, 135;

cranial, 135, 136 ff.: 313, ff.;

abducent (vi), 142: 315;

auditory (viii), 140, 157 :

314; facial (vii), 140,

141: 315; glosso-

pharyngeal (ix), 141: 314, 329;

hypoglossus (xii), 313;

lateral line, 142, 156,

157; oculomotor (iii),

142: 315; olfactory (i),

316, 326; optic (ii), 316,

320; pneumogastric (x),

141: 314, 329; - spinal

accessory (xi), 314, 329 ;

trigeminal (v), 138, 140: 285, 315;

trochlear (iv), 142: 315;

vagus (x), 141: 314,

329; vagus, visceral

branch, 142; spinal, 135, 142-

143, 173: 311 ff., 312; -

axons of , 311; roots of,

142, 143: 311, 312;

table of arrangement, 173
nervous system, central, 20-23, 21,
27-28, 37-39, 38: 116 ff., 128 ff.:
269 ff., 302 ff., 302; -
peripheral, 135 ff.; 311 ff.;

sympathetic, 143-144, 143:

312-313, 313

"nests," of ovarian cells, 205, 206:
237 363' 374

neural, crest, 119, 124, 136, 137, 139,

142, 194: 265, 270, 309; folds

(ridges), 16, 21, 22, 23: 261, 266,

268, 269, 270, 278: 398; folds,

lateral, 65, 111, 117, 120;

folds, transverse, 65, 99, 111, 117;

groove, 65, 111, 117, 120:

263, 269: 401; plate, 21, 22:

65, 110-111, 110, 117, 124: 269,

270, 278; sheath, 52;

tube, 21, 27: 270, 274, 278: 398

neurenteric canal, 16, 21, 25, 28: 118,
119, 120: 259: 397, 398, 400 ,401

neuroblasts, 135: 308

neurocoel, 21, 27

neuro-epithelium, 326

neuromeres, 128: 271, 302-303, 302

neuropore, 22,25, 32, 35, 38 : 118, 128:
270

node, Hensen's, 252, 253, 257, 260 :

394, 395, 396
non-deciduata, 439
notch, marginal, 258
notochord, 16, 21, 23, 25, 28-29: 121

ff., 208-210, 213: 260, 262, 264,

265, 266, 268, 268, 278, 304: 398,

402
notochordal, canal, 397-398, 397;

— sheath, 52:208, 208
notogenesis, 99 ff., 98, 106, 112 ff.
nuclei, of periblast, 246-247
nucleus, of Pander, 243, 247;

volk, 74, 75:376
Nussbaum, 205

Occipital condyles, 215

oesophagus, 159, 166, 168, 169: 304,
329, 332, 335

osstrus, 378; relation to ovula-

tion, 379

olfactory, capsule, 210, 211, 212, 214,

215; epithelium, 326; -

groove, 154 ; lobes, 129: 305 ;

organ, 145, 153 ff., 154: 325

ff.; pit, 38, 38: 153, 154, 160:

325 : 407, 412, 412 ; placode,

131, 153, 154; process, 412,

412 ; recess, 129

omosternum, 221

oocytes, 74, 75 : 237, 238

oogenesis, 7: 73 ff., 75: 237, 238:
374 ff.

oogonia, 7: 237, 363

opercular cavity, 161, 163

operculum, 67, 161, 163, 180;

(auditory), 153, 213

optic, chiasma, 129, 131, 133, 148:

305, 306; cup, 145, 146, 147,

148: 316 ff., 317, 318 ; lobes,

129, 132: 307; recess, 130,

133, 148: 262, 303, 304, 305, 306;

stalks, 129, 144, 145, 147,

148, 160: 303, 316, 317, 318, 320;

thalami, 129, 148: 307, 320;

vesicles^ 144, 145, 147 : 266,

271, 274, 276, 282, 283, 316 ff.,
317, 318, 329 ; vesicle, ante-
rior chamber, 317, 321;

posterior chamber, 146, 147: 310,
317, 318

opossum, blast odermic vesicle, 388;
gestation, 370

oral, cirri, 44, 45 ; hood, 42, 44,

45; membrane (plate), 132,

158, 159, 164: 261, 262, 269, 276,
282, 304, 327: 412, 412; -

sinus, 404, 412 ; sucker, 66,

66, 120, 164, 180

or a serrata, 319

466

INDEX

(Amphioxus, pages 1-61; frog, 62-228

organs, of lateral line, 141, 156, 167

Ornithodelphia, ova, 418

Ornithorhynchus, ova, 418

ossicles, auditory, 324-325

ostium (oviducal), 72, 73, 203: 236,

236, 360: 371; during ovula-

tion, 378

otocyst, 140, 149, 160: 283, 285, 322,
322

ovary, 6, 7, 56 ff., 67: 71, 72: 235,

236, 363: 371, 372; follicular

capsules of, 56, 67: 206: 235, 236,
238, 239: 373, 374, 376, 376, 378;
stroma of, 205: 361, 362

overgrowth, margin of, 247, 249, 268,
277, 277

oviduct, 72, 202, 203 : 235, 236, 360
ff .: 371, 372

ovulation, 78: 240 ff.: 377-379;

relation to coitus and parturition,
379

ovum, 4, 6, 6, 10, 17: 66, 68 ff., 70:
232 ff., 233: 372 ff., 373, 376;

at time of laying, 70: 232 ff.,

233; formation of, 236 ff.;

human, 373, 373 ; lon-
gevity of, 379; number

formed, 78; polarity of, 4, 5,

6, 10, 11, 17: 69, 70, 83;

production of, 236-237, 242;

sizes, 373; symmetry, 4, 6,

10, 11, 17:70, 80, 83 jf., 87, 88 #.

"ovum," the mammalian blastoder-
mic vesicle and ovum, 399

Owen, 439

Pabulum, 441

pancreas, 167, 167: 333, 336, 346

pancreatic duct, 168

Pander, nucleus of, 243, 247

papillae, acustic, 323; feather

286

parachordse, 210
paradidymis, 362
paraphysis, 131 : 305, 306
parencephalpn, 304
parietal cavity, see exoccdom
paroophoron, 363
parovarium, 363 : 372, 375
pars basilaris, 160, 151
parturition, 450; relation to

ovulation, 379
Patterson, 241, 248

Pearl, 241; and Curtis, 241

pecten, 320

pectoral and pelvic arches, 221

penetration path, 79, 80, 81, 84

penis, 415, 416, 417

Perameles, embryonic membranes,

419, 420; placentation, 419, 439

„• chick, 229-367; mammal, 368-454.)

periblast, 243; central, 245, 246 ;

marginal, 244, 245, 246, 277;

nucleation, 246-247

pericardial cavity, 166, 174, 176, 180,
192: 262, 267, 275, 310, 350 ff.,
351

pericardio-peritoneal septum, 191-
192

perigonadial cavity, 56

perilymph, 152: 324

perineum, 414

peripharyngeal bands, 42, 43

peripheral nervous system, 135 ff:
311 #.

peritoneal cavity, 352

perivitelline, membrane, 6, 9;

space, 4, 5, 9, 10:80, 81:374

Peters, 442

phseochrome tissue, 206-207, 207

phallus, 415 ff., 415

pharynx, 33: 118, 159, 160: 262, 269,
272, 278,304, 328 #.,329

Phascolarctos, placentation, 439

pig, allantois, 436; amniqn, 392;
gestation, 369; implantation, 421;
lutein, 378; notochordal canal,
398; placentation, 439, 440

pigeon, gastrulation, 248 ff.; oocyte,
239 ; nucleation of periblast, 246-
247

pigment, of ovum, 66, 69, 80, 85, 85 ;
of blastula, 97

pineal body, 130: 307

pinna, 413, 414

pit, auditory, 282, 283; ol-
factory, 38,38: 153, 164, 160: 325:

407, 412, 412 ; preoral, 25, 32,

33, 44 jf.; primitive, 262, 253,

257, 260: 398

pituitary body, 132: 327

placenta, 391, 425, 430, 437 ff.,
444, 445, 447, 448 #.,449; -
basal plate of, 449; classifica-
tion, 438 ff.; cotyledonary,

439; discoid, 439; dis-

coidalis, 440, 441 ff.; endo-

thelipchorialis, 440; epithelio-

chorialis, 440-441; hsemocho-

rialis, 441 ff., 446; human, 441

ff., 444, 445, 448 ff., 449 ; loculi

of, 448; partial, 440;

syndesmochorialis, 441; zo-

naria, 440; zonary, 439;

zono-discoidalis, 440

Placentalia, 438, 439, 440;

vera,

440; embryonic mem-
branes of, 419 ff.

placentation, defined, 437

placode, 138, 139 : 310; auditory

139, 149; facial, 139;

INDEX

467

(Amphioxus, pages 1-61; frog, 62-228; chick, 229-367; mammal, 368-454.)

placode, glossopharyngeal, 329 ;

lateral line, 156;

lens, 146;

olfactory, 131, 153, 154;
vagus, 329

plane, first cleavage, 11: 89 ff.; 243:

382; gravitational, 86;

of symmetry of ovum, 4, 6, 10, 11,

17: 70, 80, 83 ff., 87, 88 ff.;

of blastula, 96

plate, anal, 280, 296. 296, 297, 334;

basal, placental, 449;

basal, cranial, 211, 212, 213;

closing, 449, 450; cutis,

171-172, 171: 352-353; gill,

65, 122; hypobranchial, 217,

218, 218 ; internasal, 210, 211, 215;

lateral, 31: 123-124, 170, 171,

194: 263, 278; medullary

(neural), 21, 22: 65, 110-111, 110,

117, 124: 269, 270, 278;

parachordal, 210, 211 ; primi-
tive, 247, 262, 253, 254 ; sense

123; velar, 162, 180;

vertebral, 170, 194: 263, 278

plectrum, 153, 213, 214

pleural, cavity, 351; groove,

310, 361

pleuro-peritoneal membrane, 352

plexus, choroid, of iii ventricle, 130,

133: 306, 307; of iv

ventricle, 134: 305, 308; pre-

vertebral, 312; splanchnic,

312

plug, yolk, 66, 99, 101, 102, 120

polar bodies, 6, 8, 10: 70, 75, 81, 82:
340,341:377,378,380

polarity, of ovum, 4, 5, 6, 10, 11, 17:
69,70,83:232-233

polyspermy, 79: 241

pons Varolii, 307

pore, cleavage, 14

portal, intestinal, anterior, 261, 262,
266, 269, 272, 276, 278, 282, 291,

304, 346 ; posterior, 280 ;

see also vein.

position of embryo in "ovum," 243;
' change in, 284

postanal gut, 170: 280, 296, 296, 334

postbranchial bodies, 331, 331

pouch, branchial (gill), 41, and see

pouch, visceral; hyobranchial,

162; hyomandibular, 160,

160, 161, 162: 324, 330;

Seessel's, 304, 328, 329; vis-
ceral, 41: 122, 158, 160, 160, 163,
164: 269, 278, 328 ff., 329

preoral, cavity, 25, 32, 33; gut,

262, 304, 328, 329 ; pit 26, 32,

33, 44 ff.

pressure, effect upon symmetry, 88

Primates, allantois, 434, 436; am-
nion formation, 424; endoderm
formation, 385; implantation, 421;
ovulation, 379; placentation, 439,
440; proamnion, 428; trophoblast,
389; trophoderm, 422; uteri, 372;
yolk-sac, 433

primitive, folds, 253, 264;

groove, 119, 120: 252, 252, 253,
254, 263, 268: 395, 396, 398, 401;

knot, 252, 253, 257, 260 : 394,

395, 396; 200 : 398; plate,

247, 252, 253; 254; streak,

119, 120: 251 ff., 252, 254, 268,
260, 274: 394, 395, 396, 398, 401;

streak, relation to embryo,

256 ff., 258, 260

proamnion, 252, 255, 260, 262, 263,
263, 266, 274, 282, 292: 426 ff.

process, ascending, of palato-quad-

rate, 211, 211, 214; csecal,

335 ; ciliary, 219 ; frontal,

412, 412; fronto-nasal, 325;

globular, 413, 413 ; head,

252, 253, 259: 395; mandib-

ular and maxillary, 404, 404, 406,

407, 412, 412; olfactory, 412,

412 ; transverse, 209

procoracoid, 221

proctodseum, 65, 118, 119, 120, 169:
334: 414

Proechidna, ova, 418

pronephric, capsule, 194, 197;

chamber, 196, 197; duct, 160,

193 ff.: 355 ff.; see also duct,
Wolffian; tubules, 160, 194,

195, 195, 196: 355
pronephros, 65, 125, 193 J"., 194, 195,

196, 199 : 355 ff.; degenera-
tion of, 197-198, 199

prooestrus, 379

prosencephalon, 129, 131, 131 : 262,

271, 282, 303, 317
Prototheria, ova, 418
protovertebra, 51
proventriculus, 336
pseudothyroid body, 164
pubis, 221

pulmo-cutaneous arch, 184, 184
pulmo-enteric recess, 361
pulmonary, arch, 184: 342, 342 ;

tract, 331-332
pupil, 146:318,318

Rabbit, allantois, 425, 431, 434 ff.;
amnion, 424 ff., 426, 426; amnion
cavity, 428,'431 ; blastodermic vesi-
cle, 382, 384, 384, 426 ; chorion,426,
426, 431 ; cleavage, 381, 382 ; em-
bryonic shield, 393; endoderm, 393;

468

INDEX

(Amphioxus, pages 1-61; frog, 62-228;

rabbit, exocoelom,431, 432; formation
of embryo, 393 ff.; gestation, 369;
implantation, 421, 422; lutein,
378; morula, 382; notochordal
canal, 398; ovary, 371; ovulation,
379; ovum, 373; proamnion, 425,
426; trophoblast, 388, 388, 425;
trophoderm, 422, 425 ; villi, 425 ;
yolk-sac, 431, 431

"Raderorgan," 35, 40, 42, 45, 46

Radford, 191

ramus, communicans, 135, 143, 143:

312, 312, 313; lateralis, x

cranial nerve, 156

rat, false amnion cavity, 389, 390;
gestation, 369; inversion of germ
layers, 389, 390; ovulation, 379;
trager, 389, 390 ; trophoblast, 389,
390

Rauber's layer, 388, 388, 395

recessus, mammillaris, 133 ;

olfactorius, 129; opticus, 130,

133, 148: 262, 303, 304, 305, 306;
pulmo-entericus, 351

rectum, 118, 167, 170: 297, 335, 336

regulation, in ovum, 86 ff.

Rejsek, 422

reproductive, ducts, 2Q2 ff.: 360^.;

system (organs), 55 ff., 57:

71 ff., 72, 201 ff., 203, 205: 234-
236, 235, 359 ff.: 371-372

rete efferentia, 363

retinal, layer, 146, 146, 147, 148:317,

317, 318 ;{ zone, 319

rhombencephalon, 129, 131, 132, 133 :

262,271,276,303
ribs, 209
Riddle, 239
ridge, genital, 415 ; mandibular,

158; neural, 16, 21, 22, 23:

261, 266, 268, 269, 270, 278: 398;

sex-cell (genital), 204, 204,

205; sub-atrial, 48, 48

rod, hypochordal (subnotochordal),

169, 194, 204
Rodents, amnion, 424 ff.; decidua,

442; implantation, 421; placenta-

tion, 439, 440; uteri, 372
roots, of spinal nerves, 135, 142, 143 :

311, 312
rotation, of gastrula, 98, 104, 105 jf.,

105 ; of ovum, 81, 83, 86, 89

Riickert, 273

Ruminants, amnion, 392, 424; pla-

centation, 439, proamnion, 428

Sac, albumen, 288, 289, 298 ff.;

endolymphatic, 152: 323; -
lymphoid, 191; scrotal, 416,

chick, 229-367; mammal, 368-454.)

saccule, 150, 151:322,323

sacrum, 221

scapula, 221

sclerotome, 48, 52, 52, 53: 172, 208:

294, 353, 354
scrotal, sac, 416/417; swellings,

415, 416, 417

Seessel's pouch, 304, 328, 329
segmental, duct, 193, ff., 194, 195,

196, 198; plate, 123, 170

segmentation, 265; cavity, 14,

16 : 93, 94, 96, 98, 102 : 245, 245,

247, 248
semicircular canals, 150, 151: 322,

323

semilunar valves, 339
seminal vesicles, 73 : 202
semiplacenta (semiplacentalia), 440
sense, capsules, 210 ff.; plate,

123
septum (septa), 172; endo-

cardial, 266 ; interauricular,

177 : 338, 339; internasal, 210,

211, 215; interventricular,

338, 340; nasal, 413, 413 ;

pericardio-peritoneal, 191-

192; transversum, 191-192:

351; — yolk-sac, 287, 288, 289,
290

sero-amnionic fusion, 287, 288, 289,
294, 294 : 427

sex, cells, 204, 204 ; cords, 204,

204, 205: 362, 362; distinc-
tion of, 206: 362: 416

sheath, notochordal, 52: 208, 208;
neural, 52

sheep, allantois, 436; blastodermic
vesicle, 384; gestation, 369; lutein,
378; notochordal canal, 398

shell, 233, 234, 241; membrane,

233, 234, 241

shield, embryonic, 387, 388, 392, 393,
ff-, 394

Shore, 186

shrew, trophoblast, 388

sinu-auricular aperture, 337;

t valves, 339

sinus, cervical, 406, 407; Cuvier i

see ductus; lymphoid, 190-

191, 190; superior, 150;

terminalis (marginal), 252, 252,
255, 290: 431, 432, 432, 449, 449;

urinogenital,414^.,415,416;

venosus, 177: 291, 304, 337,

339, 351

sitting height, human embryo, 411
size, of human embryo, 407, 411
skeletogenous layer, 52

skeleton, 207 ff.: 354; appen-

dicular, 221-222

INDEX

469

(Amphioxus, pages 1-61; frog, 62-228;

skull, 164, 210, ff.: 354; bony

elements of, 215; cartilag-
inous, 210 ff.

solenocytes, 45, 53

somatic stalk, 282

somatopleure, 174: 266-267, 280

somites, 21, 25, 26, 29 ff., 30, 32, 51
f.: 124, 170 #., 171: 264 ff.,

66, 268, 274, 278: 352 ff.: 401,

402 ff.; number of, 51: 172:

264, 352; of head, 264-265;

table of, 173

space, perivitelline, 4, 5, 9, 10: 80,
81 : 374

spawning, 8, 58: 64, 71, 77 jf.

spermatogenesis, 77

spermatogonia, 7

spermatozoon, 5: 70, 71; lon-
gevity of,379; supernumerary,

246

spermophile, implantation, 422, 423

spinal, bulb, 129: 308; cord, 37:

117, 118, 134, 134: 308; -
ganglia, 135, 142, 143: 309, 311;
- nerves, 135, 142-143, 143,

173: 311 jr., 312; nerves,

axons of, 311

spiracle, 67, 161:315, 330

splanchnic stalk, 282, 289, 327, 334

splanchnoccel, 25, 31, 52 : 124,124, 170

splanchnopleure, 174: 266-267, 280

spleen, 191: 350

stalk, allantoic, 287, 288, 289, 296,

297, 297, 348: 430, 431;

body (belly), 399, 400, 429, 430,

446; optic, 129, 144, 145, 147,

148, 160: 303, 316, 317, 318, 320;

somatic, 282 ; splanchnic,

282, 289, 327, 334

stapes, 325

sternum, 221

stigma, follicular, 378

stomach, 168, 169: 332, 335, 351

stomach-intestine, 33

stomodseum, 158, 164, 166 : 269, 327,
329 : 404, 412, 412

Strahl, 439

stratum granulosum, 375, 376

streak, primitive, 119, 120: 251 ff.,
252, 254, 258, 260, 274: 394, 395,

396, 398, 401; relation

to embryo, 256 JT., 258, 260

stroma, ovarian, 205: 361, 362

subatrial ridges, 48, 48

subgerminal cavity, 245, 246, 248

subnotochordal rod, 169, 204

subzonal layer, 382, 383, 385, 385

sucker, oral, 65, 66, 120, 164, 180

supra-orbital folds, 413, 414

suprapericardial body, 163, 164

chick, 229-367; mammal, 368-454.)

suprascapula, 221

suspensory fold, 49

suture, cerebral, 274, 276

swelling, genital, 415, 416, 417

Sylvius, aqueduct of, 132: 307

symmetry, of blastula, 96; of

ovum, 4, 6, 10, 11, 17: 70, 80, 83
#., 87, 88 ff.

sympathetic, cords, 143, 143: 312-

313, 313; ganglia 144: 207,

207: 364; nervous system,

143-144, 143:312-313,313

synccelom, 32

syncytia, trophodermal, 422 ff.

syncytiotrophoblast, 390, 422 ff.,
423

syncytiotrophoderm, 422 JT., 423

synencephalon, 304

systemic arch, 184, 184: 341, 342

Tadpole, 63 ff.; - — metamor-
phosis of, 67-68

tail, 65, 120, 120: 404, 406, 406, 408,

408, 409, 409 ; bud, 279, 280,

283, 296, 296, 297 ; fold, 280,

293, 296, 296, 297 ff., 297

Talpa, see mole.

tapir, placentation, 440

Tarsius, amnion folds, 428; embry-

. onic shield, 387; placentation, 440;
yolk-sac, 433

teeth, 220; vestiges, 328

"teeth" (horny), 159, 166

telencephalon, 129, 133: 283, 303 jf.,
304

temperature, of incubation, 231

tentacles, velar, 44, 45

terminal sinus, see sinus.

testis, 6: 72, 73, 77: 362

thalami, optic, 129, 148: 307, 320

thoracic duct, 191: 349

thymus, 162,163:330,331

thyroid body, 163, 165, 166 : 304, 331,

tongue, 165: 332; bar, 41, 42

torus transversus, 129, 131, 133 : 305
trabeculse, 210, 211, 212, 213
trabecular cornu, 210, 211, 212, 215
trachea, 329
"Trager," 389, 391, 429
transverse process, 209
trophoblast, 382, 384, 385 ff., 385,

386, 388, 390, 421, 423 ; knob,

389
trophoderm, 397, 422, 447;

functions of, 422-423; - - syn-

cytium, 422 ff.; vasculari-

zation of, 423
truncus arteriosus, 177, 178, 184, 185:

282,338,339

470

INDEX

(Amphioxus, pages 1-61; frog, 62-228; chick, 229-367; mammal, 368-451.)

trunk, common pronephric, 194

tubal fissure, 328

tube, Eustachian, 152: 324, 328;

Fallopian, 371, 372; medul-
lary (neural), 21 ; 27: 270, 274, 278:
398

tubercle, cloacal, 415, 416, 417;

coccygeal, 415; genital, 416,

416, 417

tuberculum posterius, 129, 131, 133 :
304, 306, 306

tubo-tympanic cavity, 152

tubule, mesonephric, 294, 356-357,

367, 359, 362; collecting,

367, 358; inner and

outer, 198-201, 199, 200;

metanephric, 358-359, 359;

collecting, 358; pro-
nephric, 160, 194, 195, 195, 196

Tupaija, blastodermic vesicle, 386,

387

turbinates, 326
tympanic, cavity, 152: 324, 328;

membrane, 152, 213: 325

Ultimobranchial body, 163, 164

umbilical cord and stalk, 335 : 406,
407, 408, 430, 444, 445

umbilicus, 287, 288, 289:407;

yolk-sac, 287, 288, 288, 289 ;

yolk-stalk, 402

Ungulates, allantois, 436; blasto-
dermic vesicle, 384; embryonic
shield, 387; implantation, 421;
ovu'ation, 379; placentation, 439;
uteri, 372

urachus, 436

ureter, 199, 202: 358

urethra, 416

urinogenital, aperture, 415 ff., 416;

ducts, 202 ff.; mem-
brane, 414 jf., 416 ; sinus, 414

ff., 415, 436; system, 192 ff.:

354 jf.

urostyle, 209

uterus, 236, 236: 372, 372, 444 ;

bicornis, duplex, simplex, 372;

cervix of, 444 ; f undus of,

372, 442; glands of, 443, 445;

human, gravid, 444;

ligaments of, 372 ; mucosa,

443

"uterus" of frog, 72, 73
utricle, 150, 151: 322

Vagina, 236, 236:372, 372
valves, semilunar, sinu-auricular, 339
valvula cerebelli, 133
Van Beneden, 383

vasa efferentia, 73, 202, 206 : 362

vascular, area, see area; lacunae,

256, 256; system, 174 ff.:

271 ff.: 336 ff.: 405-406, 406

vas deferens, 202, 206: 360

vein, abdominal (anterior), of

Amphibia, 189, 346; allan-

toic, 297; cardinal (anterior

and posterior), 56, 67 : 186 ff., 187,
196, 201: 285, 291, 294, 310, 329,

343 ff., 347, 348, 357, 358;

cardinal, median, 186 ff., 187;

caudal, 186, 187 : 348 ;

caval, see postcaval, precaval;

coccygeal, 349; Cuvierian,

see ductus Cuvieri; femoral,

187; hepatic, 182, 185: 346,

346; hepatic portal, 185:

346: 433; hyoidean, 182, 183;

iliac, 187, 188; interseg-

mental (intersomitic), 189: 280,
344; jugular (external, in-
ternal, superior, inferior), 186 ff.:

285, 329, 343, 348 ; lateral,

189; lateral, of Elasmo-

branchs, 346; mesenteric, 346,

348 ; mesonephric (advehent,

revehent), 188; omphalomes-

enteric, 185: 274, 276, 282, 290,
291, 337, 344 ff.: 432, 432;

Jelvic, 187 ; postcaval, 166,
86 ff.t 187: 345, 347-348, 348;
precaval, 188; pulmon-
ary, 177, 182, 189: 339, 348;

renal, 187, 188: 348, 349;

renal portal, 187, 188: 348, 349;

segmental, 186: 280;

somatic, 344; splanchnic, 344;

subcardinal, 294, 348, 348,
358; subclavian, 348;

ff ,/T A4 K • «JC/<J • DUfc/*/Ut T ACMM W^w •

mrn^ subintestinal, 48, 52: 346;

umbilical, 286, 297, 346, 346, 347,
348 : 405, 405, 435, 436; verte-
bral, 188; vitelline, 176, 177,

185: 273, 278, 281, 282, 283, 285,
290, 291, 345-346, 345, 348 : 405,

406, 432, 432 ; vitello-intesti-

nal, 185

velar, plate, 162, 180; tentacles,

44,45

velum, 42, 44, 45 ; medullare,

305; transversum, 283, 304,

305, 306

vena cava; see vein, postcaval.

venous system, 185 ff.: 343 ff.

ventral, aorta, 177: 273, 275, 278,
282 ; fissure, 135; mus-
culature, 53

ventricle (cardiac), 176, 177: 282,
283, 304, 336, 337 ff., 338;

INDEX

471

(Amphioxus, pages 1-61; frog, 62-228

ventricle (cerebral), 131, 132, 133:

304, 306, 306, 307
vertebrae, 208-209: 354; table

of, 173
vertebral plate (mesoderm), 170,

194:263, 278
vesicle, amnio-cardiac, 252, 267, 273;

blastodermic, 382 383 ff., Xiphisternum, 221

chick, 229-367; mammal, 368-454.)

whale, placentation, 440
Willey, quoted, 2, 50
Wolffian, body, 198 ff., 199, 200:
336, 357, 358, 359, 360; duct,

199, 199, 202 ff.: 265, 294, 355,
356 ff, 357, 369, 360

384, 385, 386, 390, 399;

cerebral, 25, 35, 38; meso-

nephric, 198 ff., 199, 200 ;

optic, 144, 146, 147 : 266, 271, 274,
276, 282, 283, 303, 316 jf., 317, 318,
329 ; seminal, 73 : 202

villi, 400, 438 ff., 442, 444, 445 ff.,

447, 448, 449 ; fixation, 442,

447, 448, 449; of human

placenta, 442, 444, 445 ff., 449

visceral, arches, 120, 123, 160, 160,
163, 164 : 286, 328 ff. : 404 jf., 404,

406, 408 ; cartilaginous,

211, 216 ff., 217, 218 ; clefts,

see gill defts; pouches, 122,

158, 160, 160, 163, 164 : 269, 278,
328 jf., 329

vitelline membrane, 4, 5, 8: 69: 232,
233,245,247,287: 374

vitellus, 232, 233

vitreous body, 148: 320

Wall, body, 282

weasel, placentation, 440

Weber, 177

weight, of human embryo, 411

Yolk, influence upon development,

230; mass, later history, 289

ff.; -• white and yellow, 233,

233, 239, 239, nucleus, 74, 76 :

376; plug, 65, 99, 101, 102,

120; sac, 286 ff., 287, 288,

289, 310, 348: 428, 430; sac,

circulation, 290, 291 : 432-433,432 ;

disappearance of, 292,

300; endoderm, 256, 272,

277, 289-290: 390, 391, 425, 431;

human, 399, 400, 402

ff., 444 ; later history of,

292, 300: 431 ff.; meso-
derm of, 426, 432; septa

of, 287, 288, 289 ; um-
bilicus, 287, 288, 288, 289 ;

stalk, 282, 287, 288, 289, 289, 335,

348 : 402, 408 ; human,

431,433,444; umbilicus,

402

Zona, pellucida, 373, 374, 376, 384 ;

radiata, 239, 239 : 374, 376

Zone of junction, 247, 258, 277, 277

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