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THE DEVELOPMENT OF THE’ CHICK 
AN INTRODUCTION TO EMBRYOLOGY 


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THE DEVELOPMENT 
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AN INTRODUCTION TO EMBRYOLOGY 


IB Ye 


FRANK R® LILLIE 


PROFESSOR IN THE UNIVERSITY OF CHICAGO 


NEW YORK 
HENRY HOLT AND COMPANY 
1908 


CopyrRIGHT, 1908, 
BY 
HENRY HOLT AND COMPANY 


PREEBACH 


Tuts book is a plain account of the development of the never- 
failing resource of the embryologist, the chick. It has been neces- 
sary to fill certain gaps in our knowledge of the development 
of the chick by descriptions of other birds. But the account 
does not go beyond the class Aves, and it applies exclusively 
to the chick except where there is specific statement to the 
contrary. Projected chapters on the integument, muscular sys- 
tem, physiology of development, teratology, and history of the 
subject have been omitted, as the book seemed to be already 
sufficiently long. The account has been written directly from 
the material in almost every part, and it has involved some 
special investigations, particularly on the early development 
undertaken by Doctor Mary Blount and Doctor J. T. Patterson, 
to whom acknowledgments are due for permission to incor- 
porate their results before full publication by the authors. As 
the book is meant for the use of beginners in embryology, refer- 
ences to authors are usually omitted except where the account 
is based directly on the description of a single investigator. A 
fairly full list of original sources is published as an appendix. 

Figures borrowed from other publications are credited in 
the legends to the figures. The majority of the illustrations are 
from original preparations of the author: Figures 46, 48, 50, 51, 
20S, 09;'60,61). 62,63; 64,65, 66, 67.271.-72.0 730 14. 75290: 
105 and 106 were drawn by Mr. K. Hayashi; the remainder of 
the original drawings were executed by Mr. Kenji Toda. The 
photographs in Figures 118, 119, 120, 168, 181, 182, 189, 194, 197, 
and 231 are the work of Mr. Willard C. Green. Some of the 
figures may be studied with advantage for points not described 
in the text. 

Acknowledgments are also due my colleague, Professor W. L. 
Tower for much assistance, and to Doctor Roy L. Moodie for 
special work on the skeleton, and photographs of potash prep- 
arations reproduced in Figures 242, 246, 249 and 250. 

The best introduction to the problems opened up by the study 


lll 


lv PREFACE 


of embryology is a careful first-hand study of some one species. 
It is in this sense that the book may serve as an introduction to 
embryology, if its study is accompanied by careful laboratory 
work. In some respects it is fuller, and in others less complete, 
than other books with which it might be compared. On its 
comparative and experimental sides, embryology is the only key 
to the solution of some of the most fundamental problems of 
biology. The fact that comparative and experimental embry- 
ology receive bare mention is not due to any lack of appreciation 
of their interest and importance, but to the conviction that the 
beginner is not prepared to appreciate these problems at the 
start; to the behef that our teachers of embryology are com- 
petent to remedy omissions; and finally to the circumstance 
that no one book can, as a matter of fact, cover the entire field, 
except in the most superficial way. 

The development before laying and the first three days of 
incubation are treated by stages as far as possible, and this mat- 
ter constitutes Part I of the book. It involves the study of the 
origin of the primordia of most of the organs. The matter 
concerning the later development is classified by the organs 
concerned, which seems to be the only possible way, and _ this 
constitutes Part II. The first part is complete in itself, so far 
as it goes, and no doubt it will be the only part consulted by 
some students. 

The attempt to present a consecutive account of the develop- 
ment of the form on which so many classics in the history of 
embryology have been based is no slight undertaking. The 
author can hardly hope that he has avoided omissions and errors, 
and he will be sincerely grateful to those who call such to his 
attention. 


CONTENTS 


INTRODUCTION 


I. Tse CeLtt THEORY ; 
Il. Tue RecaPiTuLATION THEORY 
Ill. Tue PuystotoGy or DrvELOPMENT coh ale: 
IV. Empryonic PrrmorpiA AND THE LAW OF Gunntic Reeate 
TION Ve 
V. GENERAL Gunmionnes OF Cae CELLS 
The Spermatozoon 
The Ovum 
Comparison of the Ger m- tells 
VI. PowuaRiITy:AND ORGANIZATION OF THE OVUM 


PARE al 


PAGE 


THE EARLY DEVELOPMENT TO THE END OF THE 


TER DAY. 


CHAPTER I. THE EGG 
Chemical Composition oj the Ter n’s ne 
Formation of the Egg 
Abnormal Eggs 
Ovogenests 


CHAPTER II. THE DEVELOPMENT PRIOR TO LAYING 
I. MATURATION 
II. FERTILIZATION . : 
Ill. CLEAVAGE OF THE OvUM 
The Hen’s Egg 
The Pigeon’s Egg abit te A te ee 
IV. ORIGIN OF THE PERIBLASTIC oer EI, soneloton OF THE 
GERM-WALL 
V. ORIGIN OF THE ECTODERM AND iinaeouen 


CHAPTER III. OUTLINE OF DEVELOPMENT, ORIENTA-— 
TION, CHRONOLOGY 
Orientation : 
Chronology (¢ Tasereeanien of Senge) 
Tables of the Development of the Chick 
. 


68 


vl CONTENTS 


PAGE 
CHAPTER IV. FROM LAYING TO THE FORMATION OF 
THE FIRST SOMITE... . i) Gl Rao 
STRUCTURE OF THE UNINCUBATED BLASTODERM. . . . 69 
II.. Tee PRIMITIVE STREAK. 3. 9. (2) 4) 5. 9S ee ee 
Potal Views. ae ae Se We 5 cee ep ee 
Sections — . b - so sB, Sy. Gs 9 ee ee 74 
The Head-process ; «Ue edt ge aa 
Interpretation of the Pr inne Str aE . 6 eke Sees 
III. THe MrsopERM OF THE OpaQuE AREA . ... . . 86 
TV. Tae GerRM-wWabh - . *s 6s iy ow ww oe oe 1 ee 
CHAPTER V. HEAD-FOLD TO TWELVE SOMITES 
(From about the twenty-first to the thirty-third hour of incu- 
bation) er Ee SS ade A. ae ee 
I. ORIGIN OF THE Aire AD-FOLD 9." 2 2» <) » 0» . 9 seme 
II. FoRMATION OF THE FoRE-GUT. . . . ... . . 98 
Ill. OriGciIn oF THE NEURAL TUBE bus eh a a ey Cag 
The Medullary_Plate. . . . . . «1 . . « « 
The Neural Groove and Folds. . . . . . . 97 
Primary Divisions of the Neural Tube... - £05 
Origin of the Primary Divisions of the Embryonic Bram 108 
IV. Tue MESoBLAST . . . «© « w 2 Se Beg 
Primary Structure of ile See Sg a “eS le Ce ie 
The Nephrotome, or Intermediate Cell-mass (Middle 
‘Plate Fe ee eles 
The Lateral Plate. . . oe ee SES 
Development of the Body-c Piva or Chisme « fe oe ie a ID 
Mesoblast of the Head . . . . . . . . . . 42116 
Vascular System .9. : 2. 2 & % .« = «» 4 ~ ig 
Origin ofthe Heart . . . . .... . . «. JY 
The Embryonic Blood-vessels 5. ow « fe ae 
V. DESCRIPTION OF AN EMBRYO WITH 10 Somme » 4 oe alee 
The Nervous System . . . . . . .. . . . 4124 
Alimentary Canal > as Vo Se 8 A 
Vascular System™, > G.8e_« % we elo 
General : : Se bape Se he ogee A Voller 
Zones oj the Blesindoem oes & We 2 eae 


CHAPTER VI. FROM TWELVE TO THIRTY-SIX SOMITES. 
THIRTY-FOUR TO SEVENTY-TWO HOURS . 1380 

I. D&rVELOPMENT OF THE EXTERNAL FORM, AND TURNING OF 
THE EMBRYO . . 2 oe Us OU SO 
Separation of the Embryo on the Blasters . » ay dO 


CONTENTS vil 


PAGE 

The Turning of the Embryo and the Embryonic Flexures 133 

Il. Origin or THE Empryronic MEMBRANES. . . . . . 185 
Origin of the Amnion and Chorion. . . . .  «  TB9 

The Y olk-sac Sea eee eee GAS ale, oud, aS 

Origin of the Wllarines mn & . 1438 
Summary oj Later History oj He Binbr Yonic Me eae anes. 145 

fie (Rum NERVOUS SYSTEM . 9. «2 «= « 5 «2 «14% 
The Brain : 147 

The Neural Gres oe the Coe We cine Garona 156 

IV. Tue OrGANS oF SpeciAL SENSE (Ey, Ear, NOSE) 5 alo! 
Meshes We os. <7 wl. OA ee ee Oe 

The Auditory Sac a, So teh oo eee ges. OS 

The Nose (Olfactory Pits) tp Paty ity 28 oY a. ota eee el OD 

V. Tue ALIMENTARY CANAL AND ITS aeae ES med en 0, 
The Stomodeum .. Bo be ee ole ase Flite 

The Pharynx and V sheet ieahes Ag Pie a weg ie ee te alee 
(Esophagus and Stomach a ee aes, A, ole Lee 
ipowivberge. 2-66 ye © ee ce alle ce ee aes bin’, 

The Pancreas rere Sarr, 9M a ME Pay | 

Pee NageGl fs. on | ms ee Gee eee ee Ee OL 

Anal Plate, Hind-qut, Post-anal gut and Allantois 182 

VI. History oF THE MESODERM ee ee eo 
Somites : PO ate Ln Pen ae 

The lieeeaediate Cell- GSS 3). Ls ee, at LOU 

The Vascular System aso se ih gata © aR - on 

VII. Tue Bopy-caviITy AND Teo eee FR ie ee RA ene LO 


PART. It 
THE FOURTH DAY TO HATCHING, ORGANOGENY, 
DEVELOPMENT OF THE ORGANS 
CHAPTER VII: THE EXTERNAL FORM OF THE EM- 
BRYO AND THE EMBRYONIC MEMBRANES 211 


I. Tue ExTerRNAL Form Pr ee es et en) oe ma 
Genicraie 92, a. &, 00S Pe, Seats Oe cea ee a eee Oa eee tee 

Head i jm Ape ote MO ee PR A th ZS. 

II. Embryonic NiGueerns A Oe Bae, ) CS age a we 
Concrie COU, CE a) ees es ee 7s, SO 

The Allantois ae ee es fe Sek ae ee 0, 

The Y olk-sac yn i a 
ThevAmnion 24 nanan cee Tee ee Ber OL 

Hatching 232 


vill CONTENTS 


CHAPTER VIII. THE NERVOUS SYSTEM 
I. THe NEUROBLASTS 
The Medullary Newroblass 
The Ganglionic Neuroblasts ; 
II. THe DEVELOPMENT OF THE SPINAL Corp 
Central Canal and Fissures of the Cord 


Neuroblasts, Commissures, and Fiber Braces 6 the Cord 


III. THe DrvetopMeNT OF THE BRAIN. 
The Telencephalon 
The Diencephalon 
The Mesencephalon 
The Metencephalon 
The Myelencephalon 
Commissures of the Brain 

IV. Tur PertpHERAL NERVOUS SYSTEM 
The Spinal Nerves 
The Cranial Nerves 


CHAPTER IX. ORGANS OF SPECIAL SENSE 
I. THe Eye 
The Optic Cup 
The Vitreous Humor . 
The Lens . 
Anterior Chamber oe Cornea 
The Choroid and Sclerotic Coats 
The Eyelids and Conjunctival Sac 
Choroid Fissure, Pecten and Optic Nerve 
Il. THe DEVELOPMENT OF THE OLFACTORY ORGAN 
Ill. THe DEVELOPMENT OF THE EAR 
Development of the Otocyst and Assoc nee Bis 


The Development of the Tubo-tympanic Cavity, EB. ae 


Auditory Meatus and Tympanum 


CHAPTER X. THE ALIMENTARY TRACT AND ITS AP- 


PENDAGES 
I. Moutu AND ORAL CAVITY 
Beak and Egg-tooth 
The Tongue 
Oral Glands eee 
Il. Derivatives oF THE IEMBRYONIC PHARYNX 
Fate of the Visceral Clejts 
Thyroid 


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CONTENTS 


Visceral Pouches . 
The Thymus 
Epithelial Vestiges ; 
The Postbranchial Bodies in ae 
III. Tue (Esopuacus, STOMACH AND INTESTINE 
(Hsophaqus 
Stomach Be 0 
Large Intestine, Cloaca, and Anus bie} 
IV. Tue DeEvVELOPMENT OF THE LIVER AND PANCREAS . 
The Liver 
The Pancreas ; 
V. Tue Resprrarory TRActT 
Bronchi, Lungs and Air-sacs 
The Laryngotracheal Groove . 


CHAPTER XI. THE BODY-CAVITIES, MESENTERIES AND 
SEPTUM TRANSVERSUM Se eee 
I. THe SEPARATION OF THE PERICARDIAL AND PLEUROPERI-— 
TONEAL CAVITIES . 
Septum Transversum . 
Closure of the Dorsal Opening or the Perenan : 
Establishment of Independent Pericardial Walls 
Derivatives of the Septum Transversum ad, «eae 
II. SEPARATION OF PLEURAL AND PERITONEAL CAVITIES; OR- 
IGIN OF THE SEPTUM PLEURO-PERITONEALE 
Ill. THe M&sSENTERIES 
The Dorsal Mesentery 
The Origin of the Omentum 
Origin of the Spleen 


CHAPTER XII. THE LATER DEVELOPMENT OF THE 
VASCULAR SYSTEM 
I. Toe Hearr. 

The Tene opinent * he E Peinul Form a} ihe Rear 
Division of the Cavities of the Heart 
Fate oj the Bulbus 
The Sinus Venosus 

Il. Tue ArTerRIAL SYSTEM 
The Aortic Arches 
The Carotid Arch . 
The Subclavian Artery 
The Aortic System 


1x 


PAGE 
307 
308 
309 
309 
309 
312 
Bolles} 
314 
319 
319 
323 
325 
325 
331 


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x CONTENTS 


lil. Tur Venous System ae) Est ttnar cis “oheane oS. § pete 
The Anterior Venw Cave se 2 ats 2 
The Omphalomesenteric Veins. . 
The Umbilical Veins . , aes 
The System of the Inferior Vena Cc i) ee ei 
IV. THe Empryonic CrrcULATION 


CHAPTER XIII. THE URINOGENITAL SYSTEM 
I. THe Larer History oF THE MESONEPHROS . 


Il. Tue DEVELOPMENT OF THE METANEPHROS OR Pantene 


KIDNEY . oe 

The Metanephric iver alii 2S) ge ; 

The Nephrogenous Tissue of the Meionepiras 
HI. THe Orcans or REPRODUCTION 

Development of Ovary and Testis 

Development of the Genital Ducts 
IV. Tur SuPRARENAL CAPSULES 

Origin of the Cortical Cords 

Origin of the Medullary Cords 


CHAPTER XIV. THE SKELETON 

I. GENERAL ee 

Il. THe VERTEBRAL Conn MN ; 
The Sclerotomes and Vertebral S Pena 
Membranous Stage of the Vertebriv 
Chondrification 
Atlas and Axis Capit i 
Formation of Vertebral Articulations 


Ossification 


Tl. DevVELOPMENT OF THE eee AND STERNAL APPARATUS. 


IV. DEVELOPMENT OF THE SKULL 


Development oj the Cartilaginous or Prmorare ranium. 


Ossification of the Skull 
V. APPENDICULAR SKELETON 
The Fore-limb : 
The Skeleton of the Eine one 


APPENDIX 
GENERAL LITERATURE 
LITERATURE — CHAPTER I 
LITERATURE — CHAPTER II 
LITERATURE — CHAPTER III Pre: 
LITERATURE CHAPTERS IV AND V 


PAGE 
363 
363 
364 
367 
368 
372 


378 
378 


384 
384 
387 
390 
391 
401 
403 
405 
406 


407 
407 
411 
412 
414 
418 
420 
42] 
421 
424 
427 
428 
432 
454 
454 
438 


CONTENTS 


LITERATURE — CHAPTER VII 
LITERATURE — CuHapPTER VIII 
LITERATURE — CHAPTER IX 
LITERATURE — CHAPTER X 
LITERATURE — CHAPTER XI 
LITERATURE — CHAPTER XII 
LITERATURE — CHAPTER XIII 
LITERATURE — CHAPTER XIV 


INDEX 


THE DEVELOPMENT OF THE CHICK 


INTRODUCTION 


J. Tuer CeLtt THEORY 


Tue fundamental basis of the general conceptions of embry- 
ology, as of other biological disciplines, is the cell theory. The 
organism is composed of innumerable vital units, the cells, each 
of which has its independent life. The life of the organism as a 
whole is a product of the combined activity of all the cells. New 
cells arise always by subdivision of pre-existing cells, and new 
generations of the organism from liberated cells of the parental 
body. The protozoa, however, have the grade of organization 
of single cells, and the daughter-cells arising by fission constitute 
at the same time new generations. In some metazoa new gen- 
erations may arise asexually by a process of budding, as in Hydra, 
or of fission, as in some Turbellaria; such cases constitute excep- 
tions to the rule that new generations arise from liberated cells 
of the parental body, but the rule holds without exception for 
all cases of sexual reproduction. 

The body consists of various functional parts or organs; each 
of these again consists of various tissues, and the tissues are com- 
posed of specific kinds of cells. The reproductive organs, or 
gonads, are characterized by the production of germ-cells, ova 
in the female gonad or ovary, and spermatozoa in the male gonad 
or testis. However large the ovum may be, and in the hen it 
is the part of the egg known as the yolk, it is, nevertheless, a 
single cell at the time that it leaves the ovary in all animals. 
Similarly the spermatozo6n is a single cell. An ovum and sper- 
matozoon unite, in the manner to be described later, and con- 
stitute a single cell by fusion, the fertilized ovum or oosperm. 
This cell divides and forms two; each of the daughter-cells divides, 
making four, and the number of cells steadily increases by suc- 
cessive divisions of all daughter-cells, so that a large number 
of cells is rapidly produced. Organs are formed by successive 

1 


He THE DEVELOPMENT OF THE CHICK 


and orderly differentiation among groups of these cells. Among 
these organs are the gonads, consisting of cells which trace a 
continuous lineage by cell-division back to the fertilized ovum, 
and which are capable of developing into ova or spermatozoa 
according to the sex of the individual. 

The lives of successive generations are thus continuous because 
the series of germ-cells from which they arise shows no break in 
continuity. All other kinds of cells composing the body finally 
die. In view of this contrast the non-germinal cells of the body 
are known collectively as somatic cells. In some way the germ- 
cells of a species maintain very constant properties from gen- 
eration to generation in spite of their enormous multiplication, 
and this furnishes the basis for hereditary resemblance. 

The establishment of the fact that in all animals the ovum is 
a single cell, and that the cells of all tissues of the body are derived 
from it by a continuous process of cell-division, completes the 
outline of the cycle of the generations, and furnishes the basis 
for a complete theory of development. The full significance 
of this principle can only be appreciated by learning the condition 
of embryology before the establishment of the cell-theory in the 
eighteenth century. The history of our knowledge of the devel- 
opment of mammals is particularly instructive in this respect: 
some knowledge had been gained of the anatomy of the embryos, 
mostly relatively advanced, of a few mammals; but the origin 
of the embryo was entirely unknown; the ovum itself had not 
been discovered; the process of fertilization was not understood. 
In the knowledge of the cycle of generations there was a great 
gap, and the embryo was as much a mystery as if it had arisen 
by a direct act of creation. To be sure Harvey in 1651 had 
propounded the theorem, omne vivum ex ovo, but no one had 
ever seen the egg of a mammal, and there was no clear idea in 
the case of other forms what the ege@ signified. 

In 1672, de Graaf (who died in 1673 at the age of 32) published 
a work, “de mulierum organis generationis inservientibus,”’ in 
which he attempted to show that the vesicles seen on the surface 
of the ovaries were the female reproductive material. But he 
could not reconcile the view that the Graafian follicle is the mam- 
malian egg with the fact that the earllest embryos discovered 
by him were smaller than the follicles. For this reason his views 
were opposed by Leeuwenhoek and Valisnieri; and the later re- 


INTRODUCTION 3 


searches of Haller and his pupil Kuhlemann seemed to establish 
a view which banished all possibility of a rational explanation 
of development, viz., that, in the highest group of animals (the 
mammalia) the embryo arose after fertilization out of formless 
fluids. 

In 1827 vy. Baer discovered the mammalian ovum within the 
Graafian follicle. But no correct interpretation of this discovery 
was possible until the establishment of the cell-theory by Theo- 
dore Schwann in 1839; Schwann concluded as the result of his 
investigations that there was one general principle for the forma- 
tion of all organisms, namely, the formation of cells; that “the 
cause of nutrition and growth resides not in the organism as a 
whole, but in the separate elementary parts, the cells.”’ He 
recognized the ovum as a single cell and the germinal vesicle as 
its nucleus. But on account of his erroneous conception of the 
origin of cells as a kind of erystallization in a primordial sub- 
stance, the cytoblastema, he was unable to form the conception 
of continuity of generations which is an essential part of the 
modern cell-theory. 

Schwann’s theory as regards the ovum was not at once ac- 
cepted. Indeed, for a period of about twenty years some of 
the best investigators, notably Bischoff, opposed the view that 
the ovum is a single cell, and the so-called germinal vesicle its 
nucleus. It was not, indeed, until 1861 that Gegenbaur deci- 
sively demonstrated that the bird’s ovum is a single cell. Even 
after that it was maintained for a long time by His and his fol- 
lowers that all the cells were not derived from the ovum directly, 
but that certain’ tissues, notably the blood and connective tissues, 
were to be traced to maternal leucocytes that had migrated into 
the ovum while it was yet in the follicle. This view was decisively 
disproved in the course of time. 


Il. Tuer RecaAPITuLATION THEORY 


Haeckel’s formula, that the development of the individual 
repeats briefly the evolution of the species, or that ontogeny is 
a brief recapitulation of phylogeny, has been widely accepted by 
embryologists. It is based on a comparison between the embry- 
onic development of the individual and the comparative anatomy 
of the phylum. The embryonic conditions of any set of organs 
of a higher species of a phylum resemble, in many essential par- 


4 THE DEVELOPMENT OF THE CHICK 


ticulars, conditions that are adult in lower species of the same 
phylum; and, moreover, the order of embryonic development 
of organs corresponds in general to the taxonomic order of organ- 
ization of the same organs. As the taxonomic order is the order 
of evolution, Haeckel’s generalization, which he called the funda- 
mental law of biogenesis, would appear to follow of necessity. 

But it never happens that the embryo of any definite species 
resembles in its entirety the adult of a lower species, nor even 
the embryo of a lower species; its organization is specific at all 
stages from the ovum on, so that it is possible without any diffi- 
culty to recognize the order of animals to which a given embryo 
belongs, and more careful examination will usually enable one 
to assign its zodlogical position very closely. 

If phylogeny be understood to be the succession of adult 
forms in the line of evolution, it cannot be said in any real sense 
that ontogeny is a brief recapitulation of phylogeny, for the 
embryo of a higher form is never like the adult of a lower form, 
though the anatomy of embryonic organs of higher species re- 
sembles in many particulars the anatomy of the homologous 
organs of the adult of the lower species. However, if we conceive 
that the whole life history is necessary for the definition of a 
species, we obtain a different basis for the recapitulation theory. 
The comparable units are then entire ontogenies, and these re- 
semble one another in proportion to the nearness of relationship, 
just as the definitive structures do. The ontogeny is inherited 
no less than the adult characteristics, and is subject to precisely 
the same laws of modification and variation. Thus in nearly 
related species the ontogenies are very similar; in more distantly 
related species there is less resemblance, and in species from 
different classes the ontogenies are widely divergent in many 
respects. 

In species of lower grades of organization the ontogenetic 
series is a shorter one than in species of higher grades, so that 
the final stages of the organs of a lower species become inter- 
mediate or embryonic stages in species of higher rank. But the 
stage of the lower species does not appear in all the organs of the 
higher species simultaneously. Thus the chick never exhibits 
the grade of organization of a fish throughout; while its pharynx, 
for instance, is in a fish-like condition with reference to arches 
and clefts, the nervous system is relatively undifferentiated, and 


INTRODUCTION 5 


it has no vertebrae; on the other hand, it has a heart of an am- 
phibian rather than of a fish type. 

Some of these considerations may be represented graphically 
as follows: let us take a species D that has an ontogeny A, B, C, D, 
and suppose that this species evolves successively into species 
EK, F, G, H, ete. When evolution has progressed a step, to E, 
the characters of the species established develop directly from 
the ovum, and are therefore, in some way, involved in the com- 
position of the latter. All of the stages of the ontogeny leading 
up to E are modified, and we can indicate this in the ontogeny 


LAB CD of FE. as in line 2; similarly, when evolu- 
2a Ae BSCE DME tion has progressed to species I, seeing 
Bie Vase Bil Os Dies Deal th that the characters of F now develop 
4A" BC? D? b? EUG directly from the ovum, all the onto- 


5. A* Bt Ct D* E? F? GH genetic stages leading up to F are modi- 
fied, line 3. And so on for each successive advance in evolution, 
lines 4 and 5. It will also be noticed that the terminal stage D of 
species 1, becomes a successively earlier ontogenetic stage of species 
2, 3, 4, 5, etc., and moreover it does not recur in its pure form, 
but in the form D' in species 2, D? in species 3, etc. Nowif the 
last five stages of the ontogeny of species 5 be examined, viz., 
D*, KE, F?, G', H, it will be seen that they repeat the phylogeny 
of the adult stages D, E, F, G, H, but in a modified form. 

This is in fact what the diagram shows; but it is an essential 
defect of the diagram that it is incapable of showing the character 
of the modifications of the ancestral conditions. Not only is each 
stage of the ancestral ontogenies modified with each phylogenetic 
advance, but the elements of organization of the ancestral stages 
are also dispersed so that no ancestral stage hangs together as a 
unit. The embryonic stages show as much proportional modi- 
fication in the course of evolution as the adult, but this is not 
so obvious owing to the simpler and more generalized character 
of the embryonic stages. 

The recapitulation theory as outlined above is obviously a 
corollary of the theory of organic descent; it was in fact developed 
in essentially its present form, soon after the publication of the 
“Origin of Species,” by Fritz Muller and Ernst Haeckel. But 
the data on which it was based were known to the earlier embry- 
ologists; and Meckel, for instance, insisted very strongly on the 
resemblance between the ontogenetic and the taxonomic series 


6 THE DEVELOPMENT OF THE CHICK 


(1821). vy. Baer opposed Meckel’s view that higher organisms 
pass through the definitive stages of the lower organisms, and 
formulated his conclusions on the subject in 1828 in the following 
theses : 

1. “The more general features of a large division of animals 
arise in the embryo earlier than the more special features.” 

2. “From the most general features of structure arise those that 
are less general, and so on until the most specific features arise.” 

3. “The embryo of any definite species tends away from the 
specific forms of other species instead of passing through them.” 

4. “Fundamentally, therefore, the embryo of any higher 
species is never like a lower species, but only like its embryo.” 

Some embryologists profess to prefer the laws of v. Baer to 
the recapitulation theory as a formulation of the actual facts. 
But it is obvious that the only possible explanation of the facts 
is found in the theory of descent, and that therefore they must 
be formulated in terms of this theory. The method of formula- 
tion will depend on the conception of the nature of the factors 
of organic evolution. Haeckel stated his theory in Lamarckian 
terms, which renders it inacceptable in many places to those 
who cannot accept the Lamarckian point of view. But as the 
basis of any theory of descent is heredity, and it must be recog- 
nized that ontogenies are inherited, the resemblance between the 
individual history and the phylogenetic history necessarily fol- 
lows. If one holds, as does the present writer, that phylogenetic 
variations are germinal in their character, then one must admit 
that every phase of development of every part has two aspects, 
viz.: the modern, specific, or coenogenetic, and the ancestral or 
palingenetic aspect. The latter aspect may be more or less com- 
pletely obscured in the course of evolution, but it can never 
entirely vanish because it is the original germ of the specific 
form acquired. It is not correct from this point of view to classify 
some features of development as coenogenetic and others as palin- 
genetic, though it is obvious that some characters may exhibit 
the ancestral conditions in more apparent and others in less 
apparent form. 


II. THe Puysrotocy or DEVELOPMENT 
To explain how a germ possessed the potency of forming an 
adult, the preformationists of the eighteenth century assumed 


INTRODUCTION i 


that it contained a miniature adult, and that the process of 
development consisted essentially in enlargement and completion 
in detail of that which was already preformed. They solved the 
problem of development, therefore, by denying its existence: 
In the begininng the Creator had not only made all species of 
animals and plants in essentially their present forms, but had 
at the same time created the germs of all the generations that 
were ever to come into existence. The ovum of any species, 
therefore, contained encapsuled the germ of the next generation; 
this, likewise encapsuled, the germ of the generation next follow- 
ing, and so on to the predetermined end of the species. This 
was known as the doctrine of evolution or preformation. In 
opposition to this conception, those of the same period who be- 
lieved in epigenesis maintained the apparent simplicity of the 
germ to be real, and development to be actual. But, as there 
was no conception of the continuity of generations, the adherents 
of this point of view had to assume the spontaneous generation 
of the embryo. 

A great advance over the preformation theory of develop- 
ment was made in the modern theory of determinants. This 
conception, which forms the basis of Darwin’s theory of pan- 
genesis as well as of Weismann’s germ-plasm theory of develop- 
ment, is, essentially, that all the diverse components of the 
organism are represented in the germ by distinct entities (pangens 
of Darwin, determinants of Weismann) which are germs of the 
parts that they represent, and which are so distributed in the pro- 
cess of development that they produce all the parts of the embryo 
in their proper sequence and relations. This is not the place 
to enter into the numerous and diverse variations of the deter- 
minant hypothesis. It was an advance over the preformation 
theory of development in so far as it was reconcilable with the 
cell and protoplasm theories of organization, but it has a real 
relationship to the preformation theory inasmuch as it denies 
the simplicity of the germ and avoids any real explanation of 
the modus eperandi of development. 

Development is as truly a physiological process as secretion, 
and as such is to be studied by similar methods, mainly experi- 
mental. The limits of pure observation without experiment are 
soon reached in the analysis of such a complex subject as the 
physiology of development; experiment then becomes necessary 


S THE DEVELOPMENT OF THE CHICK 


to push the analysis of the subject farther, and to furnish the 
true interpretation of the observations. In some cases experi- 
ments have confirmed the physiological deductions of pure ob- 
servation, and in many cases have decided between conflicting 
views. Not all embryological experiments, however, are essays 
in the direction of a physiology of development; some are directed 
to the solution of morphological problems, as, for instance, the 
origin of the sheath cells of nerves, or the order of origin of so- 
mites, or the relation of the primitive streak to the embryo. 
Experimental embryology is, therefore, not synonymous with 
physiology of development. 

Physiology of development must proceed from an investiga- 
tion of the composition and properties of the germ-cells. It 
must investigate the role of cell-division in development, the 
factors that determine the location, origin, and properties of the 
primordia of organs, the laws that determine unequal growth, 
the conditions that determine the direction of differentiation, 
the influence of extraorganic conditions on the formation of the 
embryo, and the effects of the intraorganic environment, 7.e., 
of component parts of the embryo on other parts (correlative 
differentiation). Each of these divisions of the subject includes 
numerous problems, which have attracted many investigators, 
so that the materials for a consistent exposition of the physiology 
of embryonic development are being rapidly accumulated. This 
direction of investigation is, however, one of the youngest of 
the biological disciplines. It will be seen how far it is removed 
from attempts to explain embryonic development by a single 
principle. 


IV. Empryonic PRIMORDIA AND THE Law or GENETIC RE- 
STRICTION 

In the course of development the most general features of 
organization arise first, and those that are successively less general 
in the order of their specialization. For every structure, there- 
fore, there is a period of emergence from something more general. 
The earhest discernible germ of any part or organ may be called 
its primordium. In this sense the ovum is the primordium of 
the individual, the ectoderm the primordium of all ectodermal 
structures, the medullary plate the primordium of the central 
and part of the peripheral nervous system, the first thickening 


INTRODUCTION 9 


of the ectoderm over the optic cup the primordium of the lens, 
etc. Primordia are, therefore, of all grades, and each arises 
from a primordium of a higher grade of generality. 

The emergence of a primordium involves a limitation in two 
directions: (1) it is itself limited in a positive fashion by being 
restricted to a definite line of differentiation more special than 
the primordium from which it sprang, and (2) the latter is limited 
in a negative way by losing the capacity for producing another 
primordium of exactly the same sort. The advance of differen- 
tiation sets a limit in all cases, in the manners indicated, to sub- 
sequent differentiation, a principle that has been designated by 
Minot the law of genetic restriction. 

This law has not been sufficiently investigated in an experi- 
mental fashion to demonstrate its universal validity, but enough 
is known to establish its general applicability. A very impor- 
tant property of primordia in many animals is their capacity 
for subdivision, each part retaining the potencies of the whole. 
Thus, for instance, in some animals two or several embryos may 
be produced from parts of one ovum. Similarly two or more 
limbs may be produced in some forms by subdividing a limb- 
bud, ete. 


V. GENERAL CHARACTER OF GERM-CELLS 


As already remarked the ovum and spermatozo6n have the 
character of single cells in all animals. They are, however, 
specialized for the performance of their respective functions. 
The ovum is relatively large, inert, and usually rounded in form. 
Its size is due to the presence of a sufficient quantity of proto- 
plasm to serve as the primordium of an embryo, and of a greater 
or less amount of yolk for its nutrition. The spermatozoén, 
on the other hand, is relatively minute and capable of locomotion. 
It contains no food substances, and only sufficient protoplasm 
to serve as transmitter of paternal qualities and for organs 
of locomotion. 

The Spermatozoon. The spermatozodn (Fig. 1) is an elon- 
gated flagellated cell in which three main divisions are distin- 
guished, viz., head (caput), neck (collum) and tail (eauda). The 
head contains the nucleus, and the neck the centrosomes of the 
sperm mother-cell or spermatid. The tip of the head is often 
transformed into a perforatorium. Three parts may be recog- 


10 THE DEVELOPMENT OF THE CHICK 


nized in the tail, viz., the connecting piece (pars conjunctionis) 
next to the neck, the main piece (pars principalis) and the end- 
piece or terminal filament (pars terminalis). The entire tail is 
traversed by an axial filament; in the region of the connecting and 

f main pieces the axial filament is surrounded by 
a protoplasmic sheath (involucrum) which may 
be variously modified in different animals. The 
end-piece is made up of the axial filament 
alone. 

The Ovum. The ova of different phyla and 
classes of animals vary greatly in size, in or- 
ganization, and in the nature of their enve- 
lopes. In considering these variations we shall 
limit ourselves to the vertebrates. Within the 
ovary the ovum receives two envelopes, viz., a 
primary envelope, the so-called vitelline mem- 
brane, which is supposed to be secreted by the 
ovum itself, and a secondary or follicular mem- 
brane, which is secreted by the follicular cells. 
(See Chap. I). Theoretically the distinction be- 
tween vitelline membrane and _ follicular mem- 
brane (primary and secondary egg-membranes) 


is perfectly clear; but practically it is impossi- 
] ble in most cases to make such a distinction. 
\ Therefore the membrane that surrounds the 
/ Ovarian ovum will be termed the vitelline mem- 
Ku brane or zona radiata without reference to its 


Fic. 1. —Sperma- theoretical mode of origin. 
tozoon of the pig- The ovum escapes from the ovary (ovula- 


eon from the vas tion) by rupture of the wall of the follicle, and, 
deferens. (After 


in most vertebrates, is taken up by the oviduct 
Ballowitz. ) ; 


through which it passes on its way to the ex- 
terior. Within the oviduct it may become surrounded by tertiary 
membranes secreted by the wall of the oviduct itself. Tertiary 
membranes are lacking in some vertebrates, in others they are 
of great importance. Thus in birds the albumen, the shell- 
membrane and the shell itself are tertiary membranes. 
The principal differences to be emphasized in the ova of ver- 
tebrates are, however, in the amount and arrangement of the 
yolk contained within the ovum proper. All ova contain more 


INTRODUCTION 11 


or less yolk. In the case of mammals (excepting the monotre- 
mata: Ornithorhynchus, Echidna, ete., which have large ova) 
the yolk is scanty in amount, and quite uniformly distributed 
in the form of fine granules; the ovum is, therefore, relatively 
very small (mouse, 0.059 mm.; man, 0.17 mm.). Such ova are 
often termed alecithal, which means literally without yolk. In 
the literal sense, however, no ova are entirely alecithal, so that 
it will be better to use the term of Waldeyer, isolecithal. In the 
amphibia the yolk is much greater in amount and it is centered 
towards one pole of the ovum; the germinal vesicle (nucleus of 
the egg-cell), which occupies the center of the protoplasm of the 
ovum, is therefore displaced towards the opposite pole of the 
ovum. Such ova are termed felolecithal. In the ova of Selachia, 
reptiles and birds, the yolk is very much greater in amount and 
in consequence the protoplasm containing the germinal vesicle 
appears as a small disc, the germinal disc, on the surface of the 
huge yolk-mass. 

But no matter how large the ovum may become by deposi- 
tion of yolk, its unicellular character is not altered. The deposi- 
tion of yolk is simply a provision for the nutrition of the embryo. 
In the mammals the nutrition of the embryo is provided for by 
the placenta; therefore yolk may be dispensed with. In the 
absence of such provision the amount of yolk is a measure of the 
length of the embryonic period of development. In the amphibia, 
for instance, this is relatively brief, for the yolk is soon used up, 
and the larva must then depend on its own activities for its nutri- 
tion. Therefore the development involves a metamorphosis: the 
embryo is born in a very unfinished condition, as a larva (the 
tadpole in the case of amphibia), which must undergo an exten- 
sive metamorphosis to reach the adult condition. In the reptiles 
and birds, however, the amount of yolk is sufficient to carry the 
development through to a juvenile condition, before an extrane- 
ous food-supply is necessary. The metamorphosis, therefore, 
which takes place in free life in amphibia, goes on within the egg 
in reptiles and birds. The first form of development is known 
as larval, the second as foetal. 

The amount and arrangement of yolk also influences very 
profoundly the form of the early stages of development. Ova 
are Classified in this respect as holoblastic and meroblastic. Holo- 
blastic ova are those in which the process of cell division (cleav- 


12 THE DEVELOPMENT OF THE CHICK 


age or segmentation of the ovum), with which development 
begins, involves the entire ovum. This occurs where the amount 
of the yolk is relatively small and where it is completely inter- 
penetrated by sufficient protoplasm to carry the planes of divi- 
sion through the inert yolk. But where the amount of yolk 
becomes very large, or where it is not interpenetrated sufficiently 
by the protoplasm, the division planes are confined to the proto- 
plasmic portion of the ovum, and the yolk remains undivided. 
Such ova are known as meroblastic. In these ova the cellular 
part of the ovum forms a blastodise (germinal disc) on the surface 
of the yolk. The ova of Amphioxus, Petromyzontidxe, Ganoi- 
dea, Dipnoi, Amphibia, Marsupialia, and Placentalia are holo- 
blastic; those of Myxinoidea, Teleostei, Selachia, Reptilia, Aves, 
and Monotremata are meroblastic. 

It is obvious that transitional conditions between holoblastic 
and meroblastic ova may occur; such are in fact found among 
the ganoids. In Lepidosteus, for instance, the quantity of proto- 
plasm in the lower hemisphere is so sight that the division planes 
form with extreme slowness. On the other hand, it should be 
emphasized that the distinction between holoblastic and mero- 
blastic ova is not so much due to amount of yolk as to the defi- 
niteness of its separation from the protoplasm. Thus the ova 
of some teleosts, particularly of the viviparous forms described 
by Eigenmann, are many times smaller than the ova of Necturus 
or Cryptobranchus among amphibia. Yet the teleost ovum is 
meroblastic, because the protoplasm does not penetrate suffi- 
ciently into the yolk, and the amphibian ovum is holoblastic. 

Comparison of the Germ-cells. Although it is not within the 
province of this book to enter fully into a discussion of this ques- 
tion, vet it should be pointed out that, in spite of the extreme 
differences in the structure of the germ-cells, they are exactly 
equivalent in hereditary potency, as is proved by the similar 
nature of reciprocal crosses. Their resemblances are in_ fact 
fundamental and their differences must be regarded as adapta- 
tions to secure their union. The comparative history of the 
germ-cells, that is a comparison of ovogenesis and spermato- 
genesis, brings out their fundamental similarity as germ-cells. In 
both the ovogenesis and spermatogenesis three periods are clearly 
distinguishable, viz.: a period of multiplication, a period of growth, 
and a period of maturation. In the period of multiplication 


INTRODUCTION 15 


the primordial germ-cells, known as ovogonia and spermatogonia 
are very similar in their morphological characters; both kinds 
are small, yolkless cells containing the typical or somatic number 
of chromosomes; they multiply rapidly by karyokinetic division. 

At the end of this period multiplication ceases and the germ- 
cells increase in size (period of growth). They are now known 
as ovocytes and spermatocytes of the first generation. The 
growth of the ovocyte is much greater than that of the sperma- 
tocyte; deposition of yolk occurs in the ovoecyte during this 
period; and in some animals a small quantity of yolk-granules 
may be found even in the spermatocytes. Another character- 
teristic feature of the period of growth is the reduction of the 
number of chromosomes to one half of the typical number, which 
takes place, according to the current conception, by union of the 
chromosomes in pairs (synapsis) forming one half of the somatic 
number of chromosomes, which are, however, bivalent and are 
known as tetrads. 

At the end of the period of growth the ovocyte of the first 
generation is usually many times larger than the spermatocyte, 
owing mainly to the amount of yolk formed. But the two kinds 
of cells are precisely alike in nuclear constitution. Then comes 
the period of maturation, which is the same in both kinds of cells 
with reference to the nuclear phenomena, but very different as 
regards the behavior of the cell-body. The maturation consists 
of two rapidly succeeding karyokinetic divisions: in the case of 
the spermatocyte the first division results in the formation of 
two similar cells, the spermatocytes of the second order, and the 
second maturation division divides each of these equally, forming 
two similar spermatids, so that four equal and similar spermatids 
arise from each spermatocyte of the first order. Each spermatid 
then differentiates into a single spermatozoon. In the case of 
the ovocyte of the first order, the first maturation division is 
exceedingly unequal; the smaller cell is known as the first polar 
body, but both cells are ovocytes of the second order. The second 
maturation division usually involves only the large secondary 
ovocyte; it is as unequal as the first division and results in the 
formation of a second polar body. The division of the first polar 
body, where it occurs, is equal. Thus the net result of the matu- 
ration division of the ovum is the production of three cells (four 
if the first polar body divides), viz., the two (or three) polar bodies 


14 THE DEVELOPMENT OF THE CHICK 


and the ovum. The size of the polar globules is usually so small 
that their elimination makes no appreciable difference in the 
size of the ovum proper, but they have, nevertheless, the same 
nuclear constitution as the ovum. 

The mature ovum (o6tid) and the polar bodies are the precise 
equivalent of the four spermatids, but whereas each of the latter 
becomes a functional spermatozoon, only the ovum on the female 
side is functional; the polar bodies lack the necessary protoplasm 
and yolk for development, and they therefore die. The polar 
bodies must be regarded as abortive ova; and a teleological ex- 
planation of the form of maturation of the ovum is afforded by 
the consideration that equal maturation divisions would reduce 
the amount of protoplasm and yolk in the products below the 
minimum desirable for perfect development. 

Although the maturation divisions of the ovum and sperma- 
tozoon are so dissimilar externally, yet the nuclear phenomena 
are exactly alike. The net result of the maturation divisions is 
to produce definitive germ-cells containing one half of the somatic 
number of chromosomes owing to the reduction by pairing (syn- 
apsis) that occurs in both at the beginning of the period of growth. 
The somatic number is again restored when the sperm-nucleus 
and the egg-nucleus unite in fertilization. Questions of funda- 
mental importance for the problems of heredity arise in connec- 
tion with the phenomena of maturation and fertilization, but 
their consideration hes without the scope of the present book. 


VI. POLARITY AND ORGANIZATION OF THE OvuM 


Although the ovum is morphologically a single cell, yet, as 
the primordium of an individual, it has certain specific properties 
that predelineate or foreshadow the main structural features of 
the embryo. Polarity is the most general of these features: all 
the axes of the ovum are not similar, though they may be equal; 
there is one axis around which the development centers; the ends 
of this axis are known as the animal and the vegetative poles of 
the ovum, and the hemispheres in which they le are named 
correspondingly. In telolecithal ova the yolk is centered in the 
vegetative hemisphere, the protoplasm in the animal hemisphere; 
even in ova which are called isolecithal there is a tendency for 
the yolk to be more abundant in the vegetative hemisphere. 
The polar globules are formed at the animal pole; hence their 


INTRODUCTION 15 


name; they often furnish the only clear indication of polarity 
before cleavage begins. 

With reference to the heteropolar ovic axis a series of meridia 
may be defined, drawn from pole to pole over the surface; likewise 
an equator and a series of horizontal zones parallel to the equator. 
Thus directions on the surface of the ovum may be defined as 
meridional, equatorial, or oblique. 

Cleavage takes place with reference to the axis of the ovum. 
Thus in holoblastic vertebrate ova the first and second cleavage 
planes are meridional, and the third usually equatorial. The 
mammalian ovum may form an exception to this rule, though 
little is known, as a matter of fact, about the polarity of the mam- 
malian ovum. The cleavage of meroblastic ova takes place 
likewise with reference to the polarity (see Chap. II); and the 
location of the primary germ-layers is determined by the polarity. 

Not only is the ovum heteropolar, but in many bilateral 
animals, and perhaps in all, it is bilaterally symmetrical before 
cleavage begins; that is to say, one of the meridional planes 
defines the longitudinal axis of the future embryo, and the direc- 
tion of anterior and posterior ends is also predetermined in this 
meridian, so that halves of the egg corresponding to future right 
and left sides of the embryo may be distinguished. In the frog’s 
egg the plane of symmetry is marked by a gray crescent that 
appears above the equator on the side of the egg that corresponds 
to the hinder end of the embryo. This crescent is bisected by 
the meridional plane of symmetry. In the hen’s egg the plane 
of symmetry of the embryo appears on the surface of the yolk 
in a line at right angles to the axis of the shell, and the left side 
of the embryo is turned towards the broad end, the right side 
towards the narrow end of the shell. The same plane of sym- 
metry must exist in the ovum prior to cleavage for reasons ex- 
plained beyond, although there is no morphological differentiation 
in the ovum proper, 7.e., the germinal disc or yolk, that indicates it. 

This predelineation of embryonic areas within the unseg- 
mented ovum has led to the idea that the ovum contains various 
materials, so-called formative stuffs, in typical arrangement, that 
determine in some physiological way the formation of specific 
structures. 


PA a on 


LHE EARLY DEVELOPMENT TO THE END OF 
THE THIRD “DAY 


CHAPTER I 


THE EGG 

THe parts of a newly laid hen’s egg are the shell, shell-mem- 
brane, albumen, and yolk. In an egg that has been undisturbed 
for a short time the yolk floats in the albumen with a whitish 
disc, the blastoderm about 4 mm. in diameter, on its upper sur- 
face. If the yolk be rotated, it will return to its former position 
in a few minutes, owing to the slightly lower specific gravity of 
the hemisphere containing the blastoderm. The blastoderm is 
the living part of the egg, from which the embryo and all its 
membranes are derived. It is already in a fairly advanced stage 
of development when the egg is laid. The yolk and blastoderm 
are enclosed within a delicate transparent membrane (vitelline 
membrane) which holds the fluid yolk-mass together. We may 
now consider some details of the structure and composition of 
the parts of the egg. 

The shell is composed of three layers: (1) the inner or mam- 
millary layer, (2) the intermediate spongy layer, and (8) the 
surface cuticle. The mammillary layer consists of minute cal- 
‘rareous particles about 0.01—0.015 mm. in diameter welded to- 
gether, with conical faces impinging on the shell-membrane; the 
minute air-spaces between the conical inner ends of the mammillz 
communicate with the meshes of the spongy layer, which is sey- 
eral times as thick, and which is bounded externally by the ex- 
tremely delicate shell cuticle. The spongy layer consists of 
matted calcareous strands. The shell cuticle is porous, but 
apparently quite structureless otherwise. The cuticular pores 
communicate with the mesh-work of the spongy layer; thus the 
entire shell is permeable to gases, and permits of embryonic 
respiration, and evaporation of water. 

17 


18 THE DEVELOPMENT OF THE CHICK 


The shell-membrane consists of two layers, a thick outer 
layer next to the shell and a thinner one next the albumen. Both 
are composed of matted organic fibers (more delicate in the inner 
than in the outer layer), crossing one another in all directions. 
At the blunt end of the ege the two layers are separated and 
form a chamber containing air that enters after the egg is laid 
(Fig. 2). 

The physical characteristics of the albumen are too well 
known to require description. A dense layer immediately next 


Bf LVLs 


Fig. 2. Diagram of the hen’s egg in section to show relations of the parts. 

A. C., Air chamber. Alb., Albumen. BI., Blastoderm. Chal., Chalaza. 
[. S. M., Inner layer of the shell membrane. L., Latebra. N. L., Neck of 
Latebra. N.P., Nucleus of Pander. O.S. M.. Outer shell membrane. Dp Vass 
Perivitelline space. S., Shell. V.M., Vitelline membrane. W. Y., White 
yolk. Y. Y., Yellow yolk. 


to the vitelline membrane is prolonged in the form of two spirally 
coiled opalescent cords towards the blunt and narrow ends of 
the egg respectively; these are the chalaze, so called from a 
fanciful resemblance to hail stones. The two chalaze are twisted 
in Opposite directions. In a hard-boiled egg it is possible to strip 
off the albumen in concentric spiral layers from left to right from 


the broad to the small end of the ege. 


THE EGG 19 


The yolk and blastoderm are enclosed within the delicate 
vitelline membrane; the yolk is a highly nutritious food destined 
to be gradually digested and absorbed by the living cells of the 
blastoderm and used for the growth of the embryo. It is not 
of uniform composition throughout, but consists of two main 
ingredients known as the yellow and the white 
yolk. The yellow yolk makes up the greater 
part of the yolk-sphere; the main part of the 
white yolk is a flask-shaped mass, the bulb of 
which, known as the latebra, is situated near 
the center of the whole yolk, the neck rising 
towards the surface and expanding in the form 
of a dise (nucleus of Pander) situated imme- 
diately beneath the blastoderm (Fig. 2); at its 
margin this disc is continuous with a thin peri- 
pheral layer of white yolk that surrounds the 
entire mass. In addition there are several thin A 


concentric layers of white yolk concentric to the 
inner bulb-shaped mass.’ If an egg be opened, 
a delicate hair inserted in the blastoderm to 
mark its position, and then boiled hard, a sec- 
tion through the hair and center of the yolk 
will show the above relations quite clearly. The 
white yolk does not coagulate so readily as the 
vellow yolk, and it may be distinguished by this 


B 


Higseoy— Yuowl kk 


: ; spheres of the 
property as well as by its lighter color. Hens cee highly 


Both kinds of yolk are made up of innumer- magnified. (After 
able spheres which are, however, quite different Foster and Bal- 
in each (Fig. 3). Those of the yellow yolk are four.) 
on the whole larger than those of the white ee eee 
yolk (about 0.025—-0.100 mm. in diameter) with B. Yellow yolk- 
extremely fine granular contents. There is no “Phere: 
fluid between the spheres. Those of the white yolk are smaller 
and more variable in size, ranging from the finest granules up to 


1 The assertion that the thin layers that define the concentric stratifica- 
tion of the yellow yolk are of the nature of white yolk is traceable to Meckel 
V. Hemsbach, Leuckart, and Allen Thomson. His was not able to satisfy 
himself that the characteristic elements of the white yolk occur within these 
thin concentric lamellae (Untersuchungen ueber die erste Anlage des Wir- 


beltierleibes, p. 2). 


20 THE DEVELOPMENT OF THE CHICK 


about 0.07 mm. The larger spheres of the white yolk contain 
several highly refractive granules of relatively considerable size 
as compared with those of the yellow spheres (lig. 3), and such 
granules may have secondary inclusions. As we shall see later, 
the smaller granules of the white yolk extend into the germinal 
dise (forerunner of the blastoderm) and grade into minute yolk- 
granules contained within the living protoplasm. 


The earlier investigators from the time of Schwann regarded the 
white yolk-spheres as actual cells (Schwann, Reichert, Coste, His). 
His especially laid great stress on this interpretation; he believed that 
they were derived from the cells of the ovarian follicle which migrated 
into the ovum in the course of ovogenesis, that they multiplied like other 
cells, and took part in the formation of certain embryonic tissues. Sub- 
sequently he abandoned this position as untenable. The white yolk 
spheres are now universally regarded as food matters of a particular sort. 


The yolk and albumen are complex mixtures of many different 
substances, organic and inorganic, containing all the elements 
necessary for the growth of the embryo. Very little is known 
concerning the series of chemical changes that go on in them 
during incubation. 

Chemical Composition of the Hen’s Egg. — The following data 
on the chemical composition of the hen’s egg are taken from 
Simon’s Physiological Chemistry. For details and literature the 
student is referred to the standard text-books of physiological 
chemistry. 


GENERAL COMPOSITION OF THE YOLK 
PER CENT. 


A225) ae ee ee ee eee ee 47.19-51.49 
elolbte kin Reis Ga ean a aan anes cae 17 OYE oe Se 48.51-42.81 
Fats (olein, palmitin, and stearin) ................. . 21.30-22.84 
Vitelline and other albumens ....... eer 15.63-15.76 
eGrGhint wegen tee es 8.43-10.72 
Cholesterin ....... meee Sonat Ae le 0.44— 1.75 
Cerebrin ........... ha a S Gt are 0.30 
Mineral salts ....... , on fh 3.33- 0.36 
Coloring matters | ce 
be Weenehe epee hee Ment oye ORE) Sees semen aiteee ra tee Lente 0.553 


Glucose 


ANALYSIS OF THE MINERAL SALTS 

Jee see ee 5.12— 6.57 

«ante ee ca aT 2a, ae ee eine 8.05— 8.93 
ee tge 6 ects Be eee ae setcwenss “LAZINESS 


Sodium (NasO) ... 
Potassium (KK,Q) . . 
Caleium (CaO) 


THE EGG 21 


PER CENT. 


Malomesiunre (Mig @))teerewpetsrcise.g20s + sisve voters ielaverevcusyciate ahoteretere tere 2.07— 2.11 
ico rns (es Os) Mere eA etree pe cesar aac Sets ae CAR AMEN toy oe eae 1.19- 1.45 
hospnoric*acid, tree: (P2O-)i ts sys... ete ace tin wie te oie ove oe eye. 5.72 
Bhospionricracid «combined esc. emi etter eerie eine cies 63.81-66.70 
SHUNGVO-BXCITO ER sts ats coke etd, actore soma OA ics Sorin Penis mined eneS 0.55— 1.40 
(Cin Orinie wesc ces seer aes etey sails iar aaei ss RUIN Shower he usta as are Traces. 


GENERAL COMPOSITION OF THE ALBUMEN 


VAY Save Eh 2 eager aR ey RE NS eng Re Pec Ree te? OY nk rane NRE S0.00-86.68 

(SOIC ISS x. cx: BEEN, GRR CEN ERM a NON Oe CR ARS OT UE Dice wa 13.22—20.00 
PAU UITIGTIS WR oii eon cole mene ty Uns, Se ea ear ag ae 11.50-12.27 
RGA CELVIOS erry cae Fees oles BN cee oe eee ee ee 0.38— 0.77 
(GUYS ey 5 le. 5 cae earl ee ee eee oe a AO ee oe 0.10— 0.50 
HartsiamGh SOAP Stas devs croc vt ious te eu sherds nebo ens eye eet et el ss teeter Traces 
Mimeralesalittsurrtemccra ich ttre sc te a nee ete ee Ree 0.30— 0.66 
eciuhinsrandiCholesterimy s+. .ca0..srecicras ¢ aera eee ecene Traces. 


ANALYSIS OF THE MINERAL ASH 


Socata ya AO) marae toe xe Yao clede ee. drag So ee eae Ce epee 23.56-32.93 
BOCAS SUITING CeO) Arann csih “lcs osnd acer tava aasralearee neetcks Ponce eettoaers neta ne 27.66-28.45 
Gx Curr (al ON erect es ene Gusts tee nteisiteisiincat adc sy eset tes Gpastensron A Ry cheeenses 1.74— 2.90 
Micrearesnumman (NICO NN i wk, Bits k Read leis! dda beatae ce tatg thn eaters catks 1.60-— 3.17 
HAG TM ULSS Oe eee sts tae ee hua esa Shi tacate een ecu Aaa i ape oe eae 0.44— 0.55 
@inlonime nC lth see cpeec st Satys Chk 5 BANG See eke eee pee: 23.84-28.56 
HBOS POMC COCIAN Ea.) wccss ghalienn bdo oie 4 Ree ead ea ape erene ey ae 3.16— 4.83 
Warhoniceacidn (OOS) 2545, d24 Jssths else chet, eee setae 9.67-11.60 
SO MMIICMACICE (Oa) his to. 5.a.2080 & shame stot deem aida het atauers 1.32— 2.63 
SUC CEACIGA( SIO) s )UEseyaetins tran este eaeth tie eee treet ere eee ee: 0.28— 0.49 
ulworinen(h ye. 2 ee aie his, herd tro dee Menard Ghats to erence rer tape me ns Traces. 


The shell consists of an organic matrix of the nature of keratin 
impregnated with lime salts: calctum and magnesium carbonates 
about 97%, calcium and magnesium phosphates about 1%, 
keratin and water about 2%, trace of iron. 

The shell-membrane and the vitelline membrane are stated 
to consist of keratin or a closely allied substance. 

Formation of the Egg. The organs of reproduction of the 
hen are the ovary and oviduct of the left side of the body.  Al- 
though the right ovary and oviduct are formed in the embryo 
at the same time as those of the left side, they degenerate more 
or less completely in the course of development (see Chap. XIII), 
so that only functionless rudiments remain. This would appear 
to be correlated with the large size of the egg and the delicate 


22 THE DEVELOPMENT OF THE CHICK 


Hic. 4. — Reproductive organs of the hen. (After Duval, based on a figure 
by Coste.) The figure is diagrammatic in one respect, namely, that two 


THE EGG 23 


nature of the shell, as there is not room for two eggs side by side 
in the lower part of the body-cavity. 

The ovary hes at the anterior end of the kidney attached 
by a fold of the peritoneum (mesovarium) to the dorsal wall of 
the body-cavity. In a laying hen ova of all sizes are found from 
microscopic up to the fully formed ovum ready to escape from 
the follicle. Such an ovary is shown in Figure 4; the gradation 
in size of the ova will be noticed up to the one fully formed and 
ready to burst from its capsule. At 5 in this figure is shown a 
ruptured follicle, and the ovum which has escaped from this 
follicle is shown in the oviduct at 8. It will be seen that the part 
of the definitive hen’s egg produced in the ovary is the so-called 
yolk. The blood-supply of the very vascular ovary is derived 
from the dorsal aorta, and the veins open into the vena cava 
inferior. 

The oviduct is a large coiled tube (Fig. 4) which begins in a 
wide mouth with fringed borders, the ostiwn tube abdominale 
(funnel or infundibulum) opening into the body-cavity near the 
ovary. It is attached by a special mesentery to the dorsal wall 
of the body-cavity, and opens into the cloaca. The following 
divisions are usually distinguished: (1) the oviduct s. s., (2) the 
uterus, (3) the vagina (Fig. 4). The oviduct includes the entire 
tube from the funnel to the dilated uterus. The vagina is the 
short terminal portion opening into the cloaca (Figs. 4 and 5). 
In the oviduct proper we distinguish the funnel, the main glandu- 
lar part, and the isthmus. 

The formation of an egg takes place as follows: the yolk, or 
ovum proper, escapes by rupture of the follicle along a preformed 
band, the stigma (Fig. 4-4), into the infundibulum which swallows 
it, so to speak, and it is passed down by peristaltic contractions 


ova are shown in the oviduct at different levels; normally but one ovum 
is found in the oviduct at a time. 
1, Ovary; region of young follicles. 2 and 38, Successively larger follicles. 
4, Stigmata, or non-vascular areas, along which the rupture of the follicle 
takes place. 5, Empty follicle. 6, Cephalic lip of ostium. 7, Funnel of 
oviduct (ostium tubs abdominale). 8, Ovum in the upper part of the ovi- 
duct. 9, Region of the oviduct in which the albumen is secreted. 10, Albu- 
men surrounding an ovum. 11, Ovum. 12, Germinal dise. 13, Region 
of the oviduet in which the superficial layers of albumen and the shell-mem- 
brane are formed. 14, Lower part of the oviduct (‘‘uterus,” shell-gland). — 15, 
Rectum. 16, Reflected wall of the abdomen. 17, Anus, or external opening 
of cloaca. 


24 THE DEVELOPMENT: OF THE CHICK 


of the oviduct. The escape of the ovum from the follicle is known 
as the process of ovulation. During its passage down the ovi- 
duct it becomes surrounded by layers of albumen secreted by 
the oviducal glands. The shell- 
membrane is secreted in the 
isthmus and the shell in the 
uterus (Fig. 5). The ovum is 
fertilized in the uppermost part 
of the oviduct and the cleavage 
and early stages of formation of 
the germ-layers take place be- 
fore the egg is laid. The time 
occupied by the ovum in tra- 
versing the various sections of 
the oviduct is estimated by 
Ixolliker as follows: Upper two 
thirds of the oviduct about 
three hours (formation of al- 
bumen), isthmus about three 
hours (secretion of shell-mem- 
brane), uterus twelve to twenty- 
four hours (formation of shell 
and laying). These figures 
are only approximate and it is 
obvious that they are likely to 


vary considerably in different 


Fig. 5. — Uterus (shell-gland) of the 
hen cut open to show the fully 
formed egg. (After Duval.) Some of the details of these 


1, Cut surface of oviduct, region of remarkable processes deserve 


breeds of hens. 


isthmus. 2, Reflected flap of uterus. 
3, Egg ready to be laid. 4, Lower ; 
extremity, or vaginal portion, of the several naturalists demonstrate 
oviduct. 5, Rectum. 6, Opening of t ee eee BATTS . 

: : - at ; ollicle is - 
the oviduct into the cloaca. 7, Open- that the ripe ; follic le » ee 
ing of the rectum into the cloaca. 8, braced by the funnel of the ovi- 


Cloaca. duct before its rupture so that 


attention: the observations of 


the ovum does not escape into the body-cavity, but into the 
oviduct itself. Coste describes the process in the following 
way: “In hens killed seventeen to twenty hours after laying I 
have observed all the stages of this remarkable process. In 
some the follicle, still intact and enclosing its egg, had already 
been swallowed, and the mouth of the oviduct, contracted 


THE EGG 25 


around the stalk of the capsule, seemed to exert some pressure 
on it, in other cases the ruptured capsule still partly enclosed 
the egg which projected from the opening; in others finally 
the empty capsule had just deposited the egg in the entrance of 
the oviduct.” 

The existence of double-yolked eggs renders it probable that 
the oviduct can pick up eggs that have escaped into the body- 
cavity. But in some cases ova that escape into the body-cavity 
undergo resorption there. 

Immediately after the ovum is received by the oviduct. it 
appears to become softer and more flexible (Coste). The upper- 
most portion of the oviduct then secretes a special layer of albu- 
men which adheres closely to the vitelline membrane and _ is 
prolonged in two strands, one extending up and the other down 
the oviduct; these strands become the chalazze; the layer to which 
they are attached may, therefore, be called the chalaziferous 
layer (Coste) of the albumen. The ovum then passes down the 
oviduct, rotating on the chalazal axis, and thus describing a 
spiral path; the albumen which is secreted abundantly in advance 
of the ovum is therefore wrapped around the chalaziferous layer 
and chalaze in successive spiral layers and the chalaze are re- 
volved in spiral turns. The main factor in propulsion of the 
ovum along the oviduct appears to be the peristaltic movements 
of the latter; it is probable that the cilia which line the cavity 
have something to do with the rotation of the ovum on its chalazal 
axis. 

The line joining the attachments of the chalaze is at right 
angles to the main axis of the ovum (that passing through the 
germinal disc); it is obvious, therefore, that there must be some 
antecedent condition that determines the position of the ovum 
in the oviduct; probably the position of the ovum in the follicle, 
7.e., the relation of the germinal dise to: the stigma, for the fol- 
licular orientation is apparently preserved in the oviduct. The 
question is of considerable importance because, as we shall see, the 
axis of the embryo is later bisected by a plane passing through 
the chalaze, and is therefore certainly determined at the time 
that the chalaze are formed. Is the embryonic axis determined 
before or after ovulation, and how is it determined in either event ? 
This question, to which there is at present no answer, furnishes 
an interesting problem for investigation. 


26 THE DEVELOPMENT OF THE CHICK 


Abnormal eggs are of two main kinds: those with more than 
one yolk, and enclosed eggs (ovum in ovo). Double-yolked eggs 
are obviously due to the simultaneous, or almost simultaneous, 
liberation of two yolks, and their incorporation in a single set of 
egg-membranes. The two yolks are usually separate in such 
cases and are derived, presumably, from separate follicles. But 
two yolks within a single vitelline membrane have been observed; 
such are in all probability products of a single follicle. Cases of 
three yolks within a single shell are extremely rare. The class 
of enclosed eggs includes those in which there are two shells, 
one within the other. There are different cases: (1) those in 
which the contents of the enclosed and the enclosing eggs are 
substantially normal, though of course the enclosing shell is 
abnormally large. (2) the enclosed egg may be abnormal as to 
size (small yolk), or contents (no yolk). In all cases described, 
the enclosing egg possesses a yolk (Parker). Abnormal eggs of 
these three classes are of either ovarian or oviducal origin; double- 
yolked eggs and eggs with abnormal yolks are due to abnormal 
ovarian conditions; enclosed eggs to abnormal ovidueal condi- 
tions, or to both ovarian and oviducal abnormalities. Assuming 
the normal peristalsis of the oviduct to be reversed when a fully 
formed egg is present, the egg would be carried up the oviduct 
a greater or less distance and might there meet a second yolk. 
If the peristalsis became normal again, both would be carried 
to the uterus and enclosed in a common shell. (For a fuller 
discussion of double eggs see G. H. Parker.) 

Ovogenesis. The ovogenesis, or development of ova, may 
be divided into three very distinct stages. The first stage, or 
period of multiplication, is embryonic and ends about the time 
of hatching (in the chick); it is characterized by the small size of 
the ova and their rapid multiplication by division. The multi- 
plying primitive ova are known as ovogonia. At the end of this 
period multiplication ceases and the period of growth begins. 
The ova, known as ovocytes of the first order, become enclosed 
in follicles; the size of the ovum constantly increases and the 
yolk is formed. The third period, known as the period of matura- 
tion, is characterized by two successive exceedingly unequal 
divisions of the egg-cell, producing two minute cells, the polar 
globules, that take no part in the formation of the embryo, but 
die and degenerate. The process of maturation begins in the 


THE EGG 27 


fully ripe follicle and is completed after ovulation in the oviduct, 
while the ovum is being fertilized. 

The origin of the primitive ova, their multiplication and 
the formation of the primordial follicles is described in Chapter 
XIII. In the young chick all the cell cords and cell nests (de- 
scribed in Chapter XIII) become converted into primordial 
follicles. During the egg-laying period there is a continuous 
process of growth and ripening of the primordial follicles, which 
takes place successively; the immense majority at any given 
period remain latent, so that at any time all stages of growth 
of egg follicles may be found in a laying hen. 

A primordial follicle consists of the ovum surrounded by a 
single layer of cubical epithelial cells (granulosa or follicle cells) ; 
the fibers of the adjacent stroma have a concentric arrangement. 
around the follicle forming the theca folliculi (Fig. 6 Str.). The 
ovum itself is a rounded ceil with 
a large nucleus which may be 
central in position or slightly ex- 
centric. In the protoplasm on 
one side of the nucleus is a con- 
centrated mass of protoplasm 
from which rays extend out into 
the protoplasm. This is the so- 
‘alled yolk-nucleus; it probably 
corresponds morphologically to 
the attraction sphere of other 
cells. FG. 6.— Primordial follicle from the 

Holl derives the follicular cells Creer pe ae (After Hol) 

: ; ; Gr., Granulosa. N., Nucleus. Str. 
in birds from the stroma, but on stroma. Y. N., Yolk nucleus. : 
insufficient grounds. The most re- 

cent and, in many respects, the best account is that of D’Hollander. 
According to this author they are derived, like the primitive ova, from 
the germinal epithelium, in which he agrees with the majority of his 
predecessors. He states that the period of multiplication of the ovo- 
gonia ends about the time of hatching; that the period of growth of the 


ovocytes begins at about the fourteenth day of incubation (seven days 
before hatching), and before the formation of the primordial follicle, 
which begins on the fourth day after hatching. Thus the periods of 
multiplication and growth overlap. He gives a detailed and well-illus- 
trated account of the nuclear changes accompanying the first stages of 
growth (synapsis, etc.) 


28 THE DEVELOPMENT OF THE CHICK 


Although the nuculeus (germinal vesicle of authors) may 
be excentriec in position in the youngest ovocytes, it always 
occupies an approximately central position in those slightly 
older. The nucleus increases in size with the growth of the 
cell-body; in the youngest ovocytes its diameter is about 9 ». and 


Ne Ros sy oes 
Iie. 7. — Section of an ovarian ovum of the pigeon; drawn from a prepara- 
tion of Mr. J. T. Patterson. The actual dimensions of the ovum are 1.44 


x 1.25 mm. 

f. s., Stalk of follicle. G. V., Germinal vesicle. Gr., Granulosa. L., 
Latebra. p. P., Peripheral protoplasm. pr. f., Primordial follicles. Th. ex., 
Theca externa. Th. int., Theca interna. Y. Y., Yellow yolk. Z.r., Zona 
radiata. 


in the ripe ovum it is flattened and measures about 117 x 
315 p. It retains its central position until the ovum is about 
0.66 mm. in diameter, and then moves to the surface where 
it hes almost in contact with the vitelline membrane (Fig. 
7). It becomes elliptical, and later the outer surface is flat- 


THE EGG 29 


tened against the vitelline membrane, the inner surface re- 
maining convex (Fig. 8). The point on the surface to which 
the germinal vesicle migrates is situated away from the surface 
of the ovary, and thus in the position of the pedicle of the 
follicle, when the latter projects from the surface of the ovary 
(Sie Oe 

The formation of the yolk has not received the attention that 
the subject deserves; and it is possible to give only a very general 
outline. While the nucleus is still in the center of the egg a 
very dense deposit of extremely fine granules is formed around 
it, and gradually extends out towards the periphery of the cell, 
but does not involve the peripheral layer of protoplasm, which 
is shghtly thicker at the innermost side of the follicle correspond- 
ing to the stalk. When the ovum has reached a size of approx- 
imately 0.66 mm, the nucleus moves towards the thickening 
of the peripheral layer and enters it, lying very close to the vitel- 
line membrane. 

The very finely granular central aggregation of yolk-granules 
represents the primordium of the latebra or central mass of the 
white yolk. After the nucleus has reached the periphery, or 
while it is still on its way, the yellow yolk begins to be formed 
by the peripheral layer of protoplasm. Small yolk-granules 
arise near the inner margin of the peripheral layer of protoplasm 
and increase in size; each becomes enclosed in a vacuole which 
grows to a considerable size, so that the accumulation of vacu- 
oles on the inner surface of the peripheral protoplasm soon 
produces a kind of emulsion; this appears in section like a 
reticulum, the spaces of which are the sectioned vacuoles, and 
the strands the remains of the protoplasm in which the 
vacuoles are embedded (fig. 7). This layer lies between the 
peripheral unmodified protoplasm and the white yolk. <A sim- 
ilar process is going on at the same time in the central pri- 
mordium of the white yolk, but the vacuoles and the granules 
are smaller, and the contrast between the white and yellow yolk 
is obvious (Fig. 7). 

Successive layers of yellow yolk are deposited around the 
central mass of white yolk by the activity of the peripheral layer 
of protoplasm. Thus one can understand in general how the 
concentric arrangement of the yellow yolk is produced. But the 
alternation of layers as seen in a section of the hardened yolk 


30 THE DEVELOPMENT OF THE CHICK 


implies a certain periodicity in the deposition of the yolk that 
is not understood.! 

The germinal vesicle lies in a thickening of the peripheral 
layer of protoplasm known as the germinal disc, which is con- 
tinuous, like the remainder of the peripheral protoplasm, with 
the protoplasmic reticulum that forms the walls of the yolk- 
vacuoles. The protoplasmic reticulum gradually disappears as 
the vacuoles are completely converted into yolk-granules. In 
the last stages of growth a peripheral layer of white yolk is formed 
around the entire yolk-mass, presumably by the peripheral proto- 
plasmic layer. The germinal disc increases in extent and thick- 
ness; but whether this takes place by inflowing of the peripheral 
protoplasm, or growth of the original disc, is not known. It is 
certain that the peripheral protoplasm disappears over most of 
the yolk when the external layer of white yolk is formed. An 
inflow of the peripheral protoplasm into the disc appears very 
probable by analogy with the bony fishes where this process can 
be studied with great ease. The alternative assumption would 
be the complete utilization of the peripheral protoplasm in form- 
ing the superficial layer of white yolk. 

The method of formation of the neck of the latebra and the 
so-called nucleus of Pander, or peripheral expansion of the neck, 
follows more or less directly from the preceding account: As the 
circumference of the ovum enlarges, the germinal disc is carried 
out and leaves behind it a trail in which yellow yolk is not formed. 
When the ovum is fully grown, the exact boundaries between the 
protoplasmic germinal dise and the yolk are not determinable. 
The dise itself is charged with small yolk-granules which grade 
off very gradually into the white yolk lying around and beneath 
the disc. 

The mode of nutrition of the ovum and the formation of the 
vitelline membrane remain to be considered. The nutrition is 
conveyed from the highly vascular theca folliculi by way of the 
follicular cells, or membrana granulosa, to the ovum. The nutri- 
ment enters by diffusion; at no stage is there any evidence of 


' Since the above was written, observations and experiments of Dr. Oscar 
Riddle have demonstrated that the periodicity is daily, and is correlated 
with the daily physiological rhythm of vitality of the hen. Acknowledgment 
is due Dr. Riddle for permission to make this statement in advance of his 
own publication. 


THE EGG ol 


immigration of solid food particles, let alone entire cells, into 
the growing ovum. At an early stage a definite membrane is 
formed between the ovum and the follicular cells, the zona radiata 
or primordium of the vitelline membrane (Fig. 7). This is 
pierced by innumerable extremely minute pores which become 
narrow canals as the zona radiata increases in thickness. The 
follicular cells and the peripheral layer of protoplasm of the ovum 
are connected by extremely delicate strands of protoplasm that 
pass through the pores (Holl). In some way the nutriment of 
the ovum is conveyed through these strands. 

The discussion as to whether the zona radiata is a product of 
the ovum itself or of the follicular cells seems to me to be largely 
academic and will not be summarized here. There seems to be 
sufficient evidence of a primary true vitelline membrane secreted 
by the ovum itself, though this may not represent the entire 
zona radiata of older ova. 

The third phase of ovogenesis, maturation or formation of 
the polar globules, is transferred to the next chapter, because it 
is overlapped by the process of fertilization. It is not definitely 
known if maturation in birds may be completed without fertiliza- 
tion, but it seems probable that, as in many other animals, the 
completion of maturation is dependent on the stimulus of fertiliza- 
tion. It is, however, essentially a process absolutely distinct 
from fertilization, and in some animals (e.g., echinids) is com- 
pleted without fertilization. 


CHAPTER II 
THE DEVELOPMENT PRIOR TO LAYING 


I. MatTURATION 


Tue phenomena of the maturation and fertilization of the hen’s 
ege are almost entirely unknown. The observations of Holl 
demonstrate only that the wall of the germinal vesicle tends to 
disappear when the follicle is nearly ripe. He also doubtfully 
identified six rod-shaped bodies at the margin of the germinal 
vesicle as the chromosomes of the maturation spindle (Fig. 8). 


5 Bh YY pits a 
3) (Dew " 


ALTE PRO ORE EOC ICOMOS 
DS BIO Me S 9,8 [ls by SES gal oy Gr 
1 GRRE Nel a 


sees 7" 


Raat SESS AS 


lia. 8. — Section of the germinal vesicle and surrounding parts 
of an ovarian ovum of the hen measuring 40 x 85 mm. (after 
Holl). 
Chr., Chromosomes. Gr., Granulosa. G. V., Germinal vesi- 
cle. Z.r., Zona radiata. 


But we have fortunately a very good account of the maturation 
and fertilization of the pigeon’s egg by E. H. Harper, which fur- 
nishes the basis of the following description: 

The wall of the germinal vesicle begins to break down in ovarian 
eges of about 18.75 mm. diameter, the full size of the egg of the 
pigeon being about 25 mm. Part of the fluid contents of the 
germinal vesicle flows out and forms a layer outside the disinte- 


32 


DEVELOPMENT PRIOR TO LAYING 30 


grating wall (Fig. 9). The chromosomes and nucleoli form a 
group near the center of the upper plane surface of the germinal 


Fig. 9. — Vertical section of the germinal vesicle and part of the germinal 
disc of an ovarian ovum ? inch in diameter; pigeon. x 385. (After 
Harper.) 


Chr., Chromosomes. Gr., Granulosa. G. V., Wall of germinal vesicle. 
? bf 5 


vesicle. The first maturation spindle is formed before ovulation, 
containing eight quadruple chromosomes (tetrads). The spindle 
is still in the equatorial plate 


stage when the ovum is 2 OS Se 

grasped by the mouth of the | is Ys N ok, 

oviduct (Fig. 10). The bulk | S/, Tit 2 7 Spl 
of the substance of the ger- | o Os abe 
minal vesicle soon forms a NE Was 

yolk-free cone extending | on BRK 

from the maturation spin- , Pes aN 

dle deep into the superficial, _ 4 

yolk. The outer end of the Fria. 10.— Vertical section of the germinal 
spindle is in almost imme- dise of the pigeon’s egg showing the 


F . irs aturation spi . The egg was 
diate contact with the sur- first maturation spindle le egg was 


clasped by the funnel of the oviduct. 
face of the ovum. In the : . 


: : 8.50 p.M. x 2000. (After Harper.) 
later stages of formation of m. Sp. 1, First maturation spindle. Tetr., 


the first polar body each Tetrad. 

tetrad, or quadruple chromosome, separates into two dyads or 
double chromosomes, and the members of each pair of dyads 
separate and approach opposite ends of the spindle (anaphase). 


34 THE DEVELOPMENT OF THE CHICK 


Thus at each end of the spindle there are eight dyads. Those at 
the outer end then enter a little bud of protoplasm projecting 
above the surface of the germinal disc, and this bud with the 
dyads is cut off as the first polar body, which hes in a depression 
of the germinal dise beneath the vitelline membrane (Fig. 11). 
Right dyads, therefore, remain within the germinal disc. 

A second maturation spindle is then formed almost imme- 
diately, apparently without the intervention of a resting stage 
of the nucleus, and takes a radial position similar to that occupied 
by the first, with the dyads forming an equatorial plate (Pig. 11). 


Fie. 11. Second maturation spindle and first polar body of the pigeon’s 
egg; a combination of two sections. 8.15 p.m. x 2000. (After Harper.) 


m. Sp. 2, Second maturation spindle. p. b. 1, First polar body. v. M., 
Vitelline membrane. 


ach dyad then divides along the preformed plane of division, 
and the daughter-chromosomes diverge towards opposite poles 
of the spindle. The outer end of the second maturation spindle 
then enters a superficial bud of the protoplasm of the germinal 
dise similar to that of the first maturation spindle; and this bud 
together with the contained chromosomes becomes cut off as the 
second polar body. 

The result of these processes of maturation is the formation 
of three cells, viz., the two polar bodies and the mature egg. 
The polar bodies are relatively very minute and soon degenerate 
completely. 

After the formation of the second polar body there remain 
in the egg eight chromosomes, each of which represents one 


> 


quarter of an original tetrad. These form a small resting nucleus 
known as the egg-nucleus or female pronucleus. It is many 
times smaller than the original germinal vesicle (Fig. 12), and 


DEVELOPMENT PRIOR TO LAYING 35 


it rapidly withdraws from the surface of the egg to a deeper 
position near the center of the germinal disc. (Concerning the 


| ec a Na Oa ss ET PUM aes aS Sake a est sed 


Fria. 12.— Egg nucleus (female pronucleus) and polar bodies 
of the pigeon’s egg. (After Harper.) 8.30 p.m. x 2000. 


E. N., Egg nucleus. p.b.1, First polar body. p. b. 2, 
Second polar body. p’v.8., Perivitelline space. v. M., Vi- 
telline membrane. 


general theory of the maturation process see E. B. Wilson, “The 
Cell in Development and Inheritance,” the Macmillan Company, 
New York.) 


Il. FERTILIZATION 


The spermatozoa traverse the entire length of the oviduct 
and are found in the uppermost portion in a fertile hen. The 
period of life of the spermatozoa within the oviduct is considerable, 
as proved by the fact that hens may continue to lay fertile eggs 
for a period of at least three weeks after isolation from the cock. 
After the end of the third week the vitality of the spermatozoa 
is apparently reduced, as eggs laid during the fourth and fifth 
weeks may exhibit, at the most, abnormal cleavage, which soon 
ceases. Eggs laid forty days after isolation are certainly unfer- 
tilized, and do not develop (Lau and Barfurth). The so-called 
parthenogenetic cleavage of such eggs is merely a phenomenon 
of fragmentation of the protoplasm; there is no true cell-division. 

The ovum is surrounded immediately after ovulation, that is 
in the infundibulum, by a fluid containing spermatozoa in suspen- 
sion. In the egg of the pigeon a certain number of spermatozoa 


36 THE DEVELOPMENT OF THE CHICK 


immediately bore through the egg-membrane and enter the ger- 
minal dise, within which the heads, which represent the nuclei of 
the spermatozoa, enlarge and become transformed into sperm nuclei 
(Fig. 13). The fate of the middle piece and tail of the sperma- 
tozoa is not known in birds, but it is improbable that they furnish 
any definitive morphological element of the 
fertilized egg. At the time of entrance of 
the spermatozoa the first maturation spin- 
dle is in process of formation; it hes in the 
center of a group of granules at the sur- 
face of the egg, which is bounded by a 
non-granular zone of protoplasm, called by 
Harper the polar ring, in which the sperm- 
nuclei accumulate. External to the polar 
ring the protoplasm is granular again (Fig. 
14). 
The sperm-nuclei remain quiescent while 
the polar bodies are being formed, and, 
Spemnine icnmeene when the egg nucleus is reconstituted, one 
sperm nuclei fromthe Of them, which may be called the male pro- 
ovum of the pigeon. nucleus or primary sperm nucleus, moves 
x 2000. (After Har- inwards and comes into contact with the 
per.) The order of Goo nucleus (Fig. 15). The opposed faces 
stages is indicated by oa . : p 
fhe letrerala as of the conjugating nuclei become flattened 
together, until the contours form a single 
sphere, the first segmentation nucleus, in which a partition sep- 
arates the original components, viz., the sperm and egg nucleus. 


Fig. 138.—Stages in 
the transformation of 


The partition apparently disappears. However, it 1s very un- 
likely that a complete intermingling of the contents of the two 
germ-nuclei takes place, because in other groups of animals where 
the processes have been more fully studied, it has been determined 
that each germ-nucleus forms an independent group of chromo- 
somes of the same number in each. 

Shortly after its formation, the first segmentation nucleus 
prepares for division in the usual karyokinetiec way. The first 
segmentation (or cleavage) spindle thus formed lies near the 
center of the germinal dise a short distance beneath the surface 
and its axis is tangential to the surface, or, in other words, at 
right angles to the axis of the egg. The fertilization may be 
considered to be completed at this stage. 


DEVELOPMENT PRIOR TO LAYING 37 


The entrance of several spermatozoa appears to be character- 
istic of vertebrates with large ova; thus for instance, it has been 
described in selachii, some amphibia, reptiles, and birds. Such 
a condition is known as polyspermy; it is normal in the forms 
mentioned, but occurs only under abnormal conditions in the 


Fic. 14. — Horizontal section of the germinal disc of a pig- 
eon’s ovum immediately after ovulation. x 125. (After 
Harper.) 


N., Nucleus, probably first maturation spindle. p. r., 
Polar ring. Sp. N., Sperm nuclei. 


= 


Fig. 15. — Vertical section of the pigeon’s egg showing germ nuclei 
(pronuclei) in the center of the dise. x 2000. 10.40 p.m. (After 
Harper.) 


38 THE DEVELOPMENT OF THE CHICK 


great majority of animals. Harper observed that the number 
of sperm-nuclei formed in the pigeon varied from twelve to twenty- 
five in different cases. Only one of these serves as a functional 
sperm-nucleus; the remainder or supernumerary sperm-nuclei 
migrate, as though repelled, from the center towards the margins 
and deeper portions of the germinal disc, where they become 
temporarily active, dividing and furnishing a secondary area of 
small cells (accessory cleavage) surrounding the true cleavage- 
cells produced by division of the central portion of the dise around 
the descendants of the segmentation nucleus. It has been sup- 
posed by some authors who studied the selachi that the de- 
scendants of the supernumerary sperm-nuclei form functional 
nuclei of the so-called periblast, but this view has been disproved 
for the pigeon (Blount), in which it can be demonstrated that 
the supernumerary sperm-nuclei have but a brief period of 
activity, and then degenerate. 


Ill. CLEAVAGE OF THE OvuM 


The fertilized ovum is morphologically a single cell, with a 
single nucleus, the first segmentation nucleus. The living proto- 
plasm is aggregated in the germinal disc, and the remainder of 
the ovum is an inert mass of food material destined to be assimi- 
lated by the embryo which arises from the germinal disc. The 
first step in the development is a series of cell-divisions of the 
usual karyokinetic type, restricted to the germinal dise, which 
rapidly becomes multicellular. As the early divisions take place 
nearly synchronously in all the cells, there is a tendency for the 
number of the cells to increase in geometrical progression, fur- 
nishing 2-, 4-, 8-, and 16- ete., celled stages; but sooner or later 
the divisions cease to be synchronous. All of the cells of the 
body are derived from the germinal disc, and the nuclei of all 
cells trace their lineage back to the first segmentation nucleus. 
The supernumerary sperm-nuclei do not take part in the forma- 
tion of the embryo. 

Cell-division is the most conspicuous part of the early de- 
velopment; hence this period is known as the cleavage, or 
sezmentation, period. But it should be remembered first, that 
cell-division is as constant a process in later embryonic stages as 
in the cleavage period, and second, that it is probable, though 
little is known yet about this subject in the bird’s egg, that 


DEVELOPMENT PRIOR TO LAYING 39 


other important phenomena are going on during the cleavage 
period. 

The type of cleavage exhibited by the bird’s egg is known 
as meroblastic, for the reason that only a part of the ovum is 
concerned, viz., the germinal disc. This is obviously due to the 
great amount of yolk (see Introduction, pp. 11 and 12). 

To understand the form and significance of the cleavage of 
the bird’s egg, it is necessary first of all to gain a clear idea of the 
structure of the germinal dise and its relations to the yolk. At 
the time of the first cleavage the germinal disc is round in surface 
view and about 3 mm. in diameter; the center is white and is 
surrounded by a darker margin about 0.5 mm. wide. These 
two zones have been compared to the pellucid and opaque areas 
of later stages, but it is certain that the correspondence is not 
exact. We shall call the outer zone the periblastic zone, or simply 
periblast. In section, the germinal disc is biconvex, but the 
outer surface which conforms to the contour of the entire egg 
is much less arched than the inner surface. The dise is every- 
where separated from the yellow yolk by a layer of white yolk 
(Fig. 2); on the other hand, there is no sharp separation between 
the dise and the white yolk. The granules of the latter are largest 
in the deeper layers and there is a gradual transition from them 
to the smaller yolk-granules with which the disc is thickly charged 
(Fig. 19). It is practically impossible in a section to say where 
the protoplasm of the disc ceases; it is indeed probable that it 
extends some distance into the white yolk both beneath and 
around the margins of the disc. Thus in Figure 21 a cone, ap- 
parently of protoplasm, extends into the neck of the latebra a 
considerable distance. In other cases it does not extend so far. 

The Hen’s Egg. The form of cleavage of the hen’s egg is 
illustrated in Fig. 16, A-E. The first cleavage appears in surface 
view as a narrow furrow extending part way across the germinal 
dise (Fig. 16 A). According to Coste the furrow is central in po- 
sition, but Kolliker describes it as excentric. Probably both con- 
ditions may be found in different eggs. While the ends of the 
first cleavage furrow are still extending towards the periblast, the 
second division begins. It is a vertical division in each cell like 
the first and the two furrows meet the first cleavage furrow at 
right angles. They may meet the first furrow at approximately 
the same point, in which case they form an approximately straight 


40) 


THE DEVELOPMENT OF THE CHICK 


Kia. 16. — Five stages of the cleavage of the hen’s egg. (After 

Kolliker.) 

A. First cleavage furrow (x 14). The egg came from the 
lower end of the oviduct. 

B. Four-celled stage (x 17); from the uterus. 

C. Ten central and eleven marginal cells (x about 16). 

D. Nine central and sixteen marginal cells (x about 16). 

IX. Late cleavage stage (x about 22). 


DEVELOPMENT PRIOR TO LAYING 41 


line (Fig. 16 B), or they may meet the first cleavage furrow at 
separate points, in which case the intervening part of the first 
furrow becomes bent at an angle, forming a cross furrow. The 
third cleavage of the hen’s egg has not been figured or described 
by any author, so faras I know. But it is probable from analogy 
with other similar forms of cleavage that in each of the four 
cells a furrow arises approximately at right angles to the second 
furrow and parallel to the first, thus producing eight cells in 
two parallel rows of four each. But the variable forms of the 
succeeding cleavage stages indicate a probable considerable 
variation in the eight-celled stage. 

Before describing the later cleavage stages, we should note 
certain important relations of the first four or eight cells: First, 
these are not complete cells in the sense that they are separate 
from one another. They are, indeed, areas with separate nuclei 
marked out by cleavage furrows in a continuous mass of proto- 
plasm. The furrows do not cut through the entire depth of 
the germinal disc, and the cells are therefore connected below 
by the deeper layer of the protoplasm; nor do the furrows extend 
into the periblast, and all the cells are therefore united at their 
margins by the unseginented ring of periblast. Second, accord- 
ing to several observers, the center of the cleavage, 7.e., the place 
where the first two cleavage furrows cross, is excentric. It is 
believed by those who emphasize this point, that the displace- 
ment is towards the posterior end of the blastoderm; but Coste, 
for instance, failed to note any excentricity. The number of 
observations is still too few to admit of a safe conclusion on this 
point; in the pigeon, according to Miss Blount’s observations 
recorded below, excentricity appears to be exceptional; more- 
over, the excentric area may bear any relation whatever to the 
future hind end of the embryo, so that in the pigeon it will not 
bear the interpretation that has been placed on it in the hen’s 
egg. 

The following cleavages (after the eight-celled stage) in the 
hen’s egg are very irregular, but two classes of furrows may be 
distinguished in surface view: (1) those that cut off the inner 
ends of the cells, and (2) those that run in a radial direction. 
The furrows of the first class produce a group of cells that are 
bounded on all sides in surface view, but these are, at first, still 
connected below by the deeper protoplasm. They may be called 


42 THE DEVELOPMENT OF THE CHICK 


the central cells. These are bounded by cells that are united 
in the marginal periblast, and thus lack marginal boundaries as 
well as deep boundaries; these may be called the marginal cells 
(Fig. 16C). The distinction between central and marginal cells 
is one of great importance which should be clearly grasped. 

In the surface views of later cleavages the following points 
should be noted: (1) the group of central cells increases by the 
addition of cells cut off from the inner ends of the marginal cells, 
and by the multiplication of the central cells themselves; (2) the 
marginal cells increase by the formation of new radial furrows. 
The increase of the central cells is much more rapid than that of 
the marginal cells, and the cells themselves are much smaller than 
the marginal cells, both because of their mode of origin and also 
because of their more rapid multiplication. The area of the 
central cells is also constantly increasing, with consequent. re- 
duction of the marginal zone (Fig. 16 E). emphasis has been 
laid by several authors on the excentric position of the smallest 
cells, and the inference has been drawn that these represent the 
hinder end of the blastodise. Similar excentricity in the pigeon’s 
egg is without reference to the future embryonic axis (see Fig. 18). 

But the surface views do not show what is going on in the 
deeper parts of the germinal disc. Sections show that after 
about the 16- or 32-celled stage an entirely new class of cleav- 
age planes arises in the central cells. These planes are parallel to 
the surface, and the superficial cells arising from such a division 
are therefore completed below. Of the two daughter-nuclei 
produced by such a division, one remains in the superficial cell 
and the other in the unsegmented deep layer of the germinal 
dise, which thus becomes nucleated. After this the nuclei mul- 
tiply in this deeper layer and cells are constantly being produced, 
which bud off from it and become added to the segmented part 
of the germinal dise above. 

In this way the entire thickness of the central part of the 
germinal disc becomes gradually converted into cells. A cavity 
arises between the cellular dise and the white yolk below, the seg- 
mentation cavity, often called the subgerminal cavity. It is first 
formed in the center of the central group of cells and extends out 
gradually towards the margin, but it never cuts under the mar- 
ginal cells, which remain united below and at their margins by the 
periblast. 


DEVELOPMENT PRIOR TO LAYING 43 


Duval interprets a narrow space observed by him between the single 
superficial layer of cells and the deeper cells of the germinal dise as the 
segmentation cavity; it is thus entirely distinct from the subgerminal 
cavity which arises much later, according to his conception. Apart 
from the fact that his figures appear to represent the merely virtual 
space between the superficial cells and the underlying cells in an exag- 
gerated form, the interpretation appears to me to be incorrect. It is 
based on the theory that the deeper cells represent the primary entoderm, 
a view which I cannot accept; the interpretation of this space as cleavage 
ravity fails if it be shown (see beyond) that the underlying cells are not 
entoderm. 

The account given above of the deeper cleavages, those seen in 
section, is the conventional one, based on the observations of Kolliker, 
Duval, and others. The account, that follows, of the corresponding 
cleavages in the pigeon’s egg, is different in some important respects, 
that bring it into agreement with the best known meroblastic eggs, 
those of the bony fishes. I have, however, allowed the above account 
to stand, though I consider it probable that a careful re-examination 
would bring the cleavage of the hen’s egg into line with that of the pigeon 
and the teleost. 


The Pigeon’s Egg. The cleavage of the pigeon’s egg has 
been worked out in more detail than that of the hen’s egg (Blount) ; 
as it offers some interesting features that have never been de- 
scribed for the hen’s egg, and must be made the basis of the 
description of the formation of the germinal wall and the germ- 
layers in the absence of any consistent account for the hen’s egg, 
it will next be described. The fundamental features of the cleav- 
age are the same as in the hen’s egg, so that the description need 
not be repeated. 

The feature to be particularly emphasized in the cleavage 
of the pigeon’s egg is the occurrence of a secondary or accessory 
cleavage in the marginal zone or periblast (Figs. 17 and 18 A). 
When the origin of these cells is traced it is found that they arise 
around the supernumerary sperm-nuclei, which accumulate and 
multiply in the periblast. The complete history of these nuclei 
has been worked out by Harper and Blount, so that there 
‘an be no doubt as to their derivation. Another interesting 
point illustrated by the figures is that the marginal cells have 
a peripheral wall wherever the accessory cleavage occurs, but 
between the groups of accessory cleavage cells the marginal cells 
are continuous with the periblast (Figs. 17 and 18 A), as they are 


dt THE DEVELOPMENT OF THE CHICK 


everywhere in the hen’s egg. In a section of a germinal disc, 
showing the accessory cleavage (lig. 20), it is seen that the 
peripheral boundary of the marginal cells cuts under the margin 
for a considerable distance. 

The accessory cleavage becomes manifest at the time of 
appearance of the first cleavage plane, and increases in amount 


Fic. 17. — Photograph of an eight-celled pigeon ovum 
(after Mary Blount). 2.45 a.m. Accessory cleavage 
(ac. el.) in the marginal zone bounding the segmented 
area. Vesicles, appearing black in the photograph, 
are seen on the surface of the yolk beyond the mar- 
ginal zone of the germinal dise. Orientation as in 
Fig. 18. 


up to about the 32-celled stage,and thereafter gradually decreases 
until it completely disappears (Figs. 18 B, C, and D). The 
peripheral boundaries of the marginal cells disappear pari passu, 
and, when the accessory cleavage is finally wiped out, the mar- 
ginal cells are everywhere continuous with the periblast, as in 
the hen’s egg (Figs. 18 B and C). In some eggs the accessory 
cleavage is much more extensive than in others; indeed, in some 
it appears to be entirely absent, but this is relatively rare. In 
the stage shown in Fig. 18 B, for instance, there is usually con- 
siderable accessory cleavage; but in this egg there is none. The 
variation is obviously due to variations in the number of super- 
numerary spermatozoa, such as may readily occur. 


DEVELOPMENT PRIOR TO LAYING 45 


The question arises whether the disappearance of the cell- 
walls around the sperm-nuclei is caused by degeneration of the 
latter, or is simply a later syncytial condition in the periblast in 


Cc D 


Fic. 18. — Photographs of the cleavage of the pigeon’s ovum (after Mary 
Blount). The figures are so arranged that the axis of the shell is across 
fan) t 
the page with the large end to the left. The future axis of the embryo 
is therefore inclined 45° to the margin of the page with the anterior end 
to the right above. 

A. A very regular sixteen-celled stage; accessory cleavage well shown; 
though not well focused on the lower margin. 3.45 A.M. 

B. Approximate thirty-two celled stage. There is no accessory cleavage 
in this ease. The formation of the central from the marginal cells may be 
readily observed in this figure. 5.15 A.M. 

C. Later stage of cleavage. 7.10 A.M. 

D. Cleavage at 9.30 a.m. The marginal cells are now becoming separated 
peripherally from the periblast which has received its nuclei from them. 


which the sperm-nuclei are embedded. There can be little doubt 
that the former alternative is correct. While in the stages of 
the accessory cleavage, sperm-nuclei are readily found both in 


16 THE DEVELOPMENT OF THE CHICK 


the accessory cleavage-cells and also in the unsegmented periblast 
(Figs. 19 and 20), they decrease in number as the accessory 
cleavage planes disappear, and when the latter are entirely lost 


i d Cc b a 2 


Pia. L9.— Transverse section of the blastoderm of a pigeon’s egg about 
S} hours after fertilization (4.45 a.m.). (After Blount.) 
_1, Accessory cleavage. 2, Migrating sperm-nuclei. a,b, ec, d, Cells of 
primary cleavage. 


the periblast is absolutely devoid of nuclei. Fragmentation of the 
sperm-nuclei is a frequent accompaniment of their disappearance. 

Thus the accessory cleavage is a secondary and _ transient 
feature of the cleavage of the pigeon’s egg due to polyspermy. 
After it has passed, the ovum is in precisely the same condition 


Kia, 20. — Transverse section of the blastoderm of a pigeon’s egg at the end 
of the period of multiplication of sperm-nuclei, about 10 hours after fertil- 
ization (6.380 a.m.). (After Blount.) 

1, Accessory cleavage around the sperm-nuclei. 2, Marginal cells; sharply 
separated from the sperm-nuclei. 3, Central cells. 4, Sperm-nuclei. 


as the hen’s ovum of the same stage of development. It is doubt- 
ful whether the absence of accessory cleavage in the hen’s egg 
should be taken as evidence that the fertilization is monospermic. 
It may well be that supernumerary sperm-nuclel are present 
without producing the appearance of accessory cleavage, owing, 
perhaps, to a deeper situation in the periblast. This point 
requires investigation. 

Another feature brought out by these photographs requires 
emphasis. The periblast ring shows no definite outer margin, 


DEVELOPMENT PRIOR TO LAYING 47 


but beyond the zone of the accessory cleavage there may occur 
two or three concentric circles variously indicated (lig. 17). 
Vacuoles, appearing black in the photographs, are very common 
in the outer zones. These appearances indicate that the peri- 
blastic protoplasm extends farther out in the superficial white 
yolk than is usually believed to be the case; and this suggests an 
interesting comparison with the teleost ovum, where the peri- 
blastic protoplasm surrounds the entire yolk as a very thin layer. 
Sections confirm the idea that the periblastic protoplasm has an 
extension beyond the so-called margin of the blastodise. Some 
eggs show a more definite margin than others; it may be that 
there is a periodic heaping of the periblast at the margins, for 
which again an analogy may be found in teleosts. 

Although the smallest cells may be more or less excentric in 
the segmented germinal dise of the pigeon, their position bears 
no constant relation to the future embryenic axis. They may 
lie in this axis in front of or behind the middle, or to the right or 
left of it (ef. Fig. 18 A-D). 

At the eight-celled stage a horizontal cleavage plane begins to 
appear beneath the central cells (ig. 19). This marks the full 
depth of the blastoderm at all stages, and the several-layered 
condition arises by horizontal cleavages between this and the 
surface. Comparison of Figs. 19, 20, and 22, drawn at the same 
magnification, will show that the depth does not increase by addi- 
tion of cells cut off from below, as is usually supposed to be the 
‘ase in the bird’s ovum. The first horizontal cleavage plane not 
only marks the full depth of the blastoderm, but it also indicates 
the site of the segmentation cavity which arises gradually by aceu- 
mulation of fluid between the cells and the underlying unseg- 
mented protoplasm and yolk. The segmentation cavity gradually 
extends towards the margin of the blastoderm, but it is bounded 
peripherally by the zone of junction between the marginal cells 
and the periblast. 


IV. ORIGIN OF THE PERIBLASTIC NUCLEI, FORMATION OF THE 
GERM-—W ALL 

Our knowledge of this part of the subject in the hen’s egg is 

very incomplete, and the various accounts are contradictory. 

The reason for this is the great difficulty of securing a complete 

series of stages, and of arranging them in proper sequence. There 


48 THE DEVELOPMENT OF THE CHICK 


is no way of timing the development, so that one has to judge 
the sequence of the stages, all of which come from the uterus, by 
the degree of formation of the shell, by the size of the cells and 
by the appearance of the sections. This can be at best only 
approximate; and, as the securing of any given stage is largely 
a matter of chance, no one has, as a matter of fact, secured a 
complete series. In the pigeon, on the other hand, the time 
since laying the first egg is a fairly exact criterion of the stage 
of development of the second egg. It has, therefore, been pos- 
sible to secure a complete series, and the subject has been worked 
out by Miss Blount, whose preliminary communication in Vol. 
XII of the Biological Bulletin furnishes the basis of the following 
account. 

The periblast ring is entirely devoid of nuclei after the super- 
numerary sperm-nuclei have degenerated. The marginal cells 
become greatly reduced in size owing to multiplication and > 
continuous production of central cells, and their nuclei thus 
approach more and more closely to the periblastie ring. The 
scene then changes; the marginal cells cease to produce central 
cells; when their nuclei divide the peripheral daughter-nuclei 
move out into the periblast, which is thus converted into a nu- 
cleated syncytium. The periblastic nuclei multiply rapidly and 
invade all portions of the periblastic ring, which maintains its 
original connection with the white yolk. Not only do the peri- 
blastic nuclei invade the periblastic ring, but some of them also 
migrate centrally into the protoplasm forming the floor of the 
segmentation cavity. They do not, however, reach the center, 
but leave a non-nucleated sub-germinal area, corresponding 
approximately to the nucleus of Pander, free from nuclei. The 
subgerminal syncytium may be known as the central periblast 
to distinguish it from the marginal periblast. They are, of 
course, continuous. In sections one has the appearance of nuclei 
in the yolk, for there is no sharp boundary between periblast 
and yolk (Fig. 22). The syncytium, which has received its nuclei 
from the marginal cells, is the primordium of the germ-wall (Figs. 
21, 22, 23, 24). 

There is a snarp contrast between the segmented blastoderm 
and the syneytial periblast not only in structure but also as 
regards fate. The marginal cells constitute a zone of junction be- 
tween blastoderm and periblast. Thus in Fig. 22 it will be ob- 


DEVELOPMENT PRIOR TO LAYING 49 


served that the large marginal cells on each side are continuous 
with the periblast, and nuclei are found in the periblast both 
central and peripheral to the zone of junction. The latter forms 


3 


a ater ae | 


es nn ees ae 

Fic. 21. — Longitudinal section of the blastoderm of a pigeon’s egg at the 

time of disappearance of the sperm-nuclei. On the left (anterior) margin, 

the marginal cells have become open, that is, continuous with the peri- 

blast, as contrasted with Fig. 20. About 11 hours after fertilization (7.00 
A.M.). (After Blount.) 


1, Marginal cells. 2, Cone of protoplasm. 3, Marginal periblast. 4, Neck 
of latebra. 5, Yellow yolk. 


Fic. 22. — Transverse section through the center of the blastoderm of a 
pigeon’s egg, 144 hours after fertilization (10.30 a.m.). (After Blount.) 


1, Marginal cells. 2, Marginal periblast. 3, Nuclei of the subgerminal 
periblast. 


a0 THE DEVELOPMENT OF THE CHICK 


a ring around the blastoderm. It persists during the expansion 
of the blastoderm over the surface of the yolk. 

The blastoderm now begins to expand, owing largely, at first, 
to additions of cells to its margin cut off from the germ-wall. 
The central as well as the marginal periblast contributes to the 
blastoderm, but the former appears to be rapidly used up. The 
marginal periblast on the other hand grows at its periphery while 
it adds cells to the blastoderm centrally, and thus it moves out 
in the white yolk, building up the margin of the blastoderm at 
the same time. The original group of central cells appears to 
correspond approximately to the pellucid area; the additions from 
the germ-wall would thus constitute the opaque area. 


Fia. 23. — Posterior end of a longitudinal section through the blastoderm 
of a pigeon’s egg about 25 hours after fertilization (8.50 p.M.). (After 
Blount.) 

1, Nests of periblast nuclei. 2, Periblast nucleus in marginal position. 

3, Syneytial mass derived presumably from the periblast, in process of or- 

ganization into cells. 4, Vacuoles. 


Some phases of these processes are illustrated in Figs. 23 and 
24. In the vertical section, Fig. 23, the surface of the germ- 
wall next the blastoderm is indented as though for the formation 
of superficial cells. Along the steep central margin of the germ- 
wall groups of cells are apparently being cut off and added to 
the cellular blastoderm. In the horizontal section, Fig. 24, the 
process of cellularization at the central margin of the germ-wall 
is apparently proceeding rapidly. 

The superficial cells thus added to the margin of the cellular 
blastoderm become continuous with the ectoderm, and_ the 
deeper layers later form the yolk-sae entoderm which becomes 
continuous with the embryonic entoderm secondarily. The term 
verm-wall is usually applied to the primordium of the yolk-sae 


DEVELOPMENT PRIOR TO LAYING ol 


entoderm and the periblast proper as well. We shall follow this 
usage and distinguish two parts of the germ-wall. 


Fig. 24. — Part of the margin of a horizontal section 
through the blastoderm of a pigeon’s egg about 25 hours 
after fertilization (8.50 p.m.). (After Blount.) 


1, Periblast nuclei. 2,3, Cells organized in the periblast. 
4, A cell apparently added to the blastoderm from the 
periblast. 5, Vacuoles. 


In later stages the inner margin of the periblast becomes much 
less steep, owing apparently to active proliferation of cells. This 
is illustrated in the outline drawings of Fig. 25. Later yet the 


A 


Fiq. 25. — Outlines of the margins of transverse sections 
of the blastoderm of pigeon’s eggs; 26 (A), 28 (B), and 
32 (C) hours after fertilization. (After Blount.) 


o2 THE DEVELOPMENT OF THE CHICK 


marginal cells extend out peripherally and form a short project- 
ing shelf beyond the zone of junction, appearing wedge-shaped 
in section (Figs. 28 A, etc.). This we shall call the margin of 
overgrowth. 

Thus we may distinguish the following zones: (1) margin of 
overgrowth; (2) zone of junction; (3) the inner zone of the germ- 
wall, and (4) the original cellular blastoderm (pellucid area) Fig. 29. 


V. ORIGIN OF THE ECTODERM AND ENTODERM 


The ectoderm and entoderm are the primary germ-layers, 
out of which all organs of the embryo differentiate; hence great 
importance attaches to the mode of their origin. But up to the 
present it has not been possible to decide between three con- 
flicting views. These are: (1) The theory of delamination, viz., 
that the superficial cells of the segmented blastoderm form the 
ectoderm and the deeper cells the entoderm; in other words, that 
the blastoderm splits into the two primary germ-layers. This 
is the oldest view, but it has not lacked support in recent times, 
e.g., by Duval. (2) The theory of invagination, viz., that the 
primary entoderm arises as an ingrowth from the margin of the 
blastoderm. This view, which was supported by Haeckel, Goette, 
Rauber, and some others, brings the mode of gastrulation in the 
bird into line with lower vertebrates. (3) A third and relatively 
recent point of view is that the primary entoderm arises as an 
ingrowth of cells from the germ-wall, more particularly from 
the posterior portion. This view, put forward by Nowack, has 
been adopted in substance by O. Hertwig (Handbuch der vergl. 
u. exp. Entwickelungslehre der Wirbeltiere). 

The reason for the conflict of opinion appears to lie mainly 
in the fact that the critical stages occur prior to laying, and no 
one has investigated a complete series of stages. For this reason 
the subject was reinvestigated in the Zodlogical Laboratory of 
the University of Chicago, by Mr. J. Thomas Patterson, at the 
suggestion of Prof. C. O. Whitman. A very complete series of 
stages of the pigeon’s ovum was studied, with results that are 
consistent in themselves and that agree with the principles of 
formation of the primary germ-layers in the lower vertebrates. 
The author has had the opportunity of following the work step 
by step, and is convinced of its accuracy. It is therefore made 
the basis of the following account: 


DEVELOPMENT PRIOR TO LAYING as) 


The first step in the process of gastrulation, or formation of 
the primary entoderm, is a thinning of the blastoderm, which 
begins slightly posterior to the center and rapidly involves a 
sector of the posterior third of the blastoderm. This process 
occurs between the twenty-first and tenth hours prior to laying. 
It is due apparently to the gradual rearrangement of the cells 
in asingle layer. A late stage of this process is shown in Figure 
26, which represents a complete longitudinal section through the 
blastoderm ten hours before laying. It will be observed that the 
anterior portion of the blastoderm is many cells thick (26 A), 
but as one passes towards the posterior end the number of layers 
becomes less, and is reduced to a single layer at the extreme pos- 
terior end. Here and there, ¢.g., at X, the arrangement of the 
cells indicates that cells of the lower layer are entering the upper 
layer. It is obvious that such a process must result in increase 
of the diameter of the blastoderm, and Patterson states that the 
average diameter twenty hours prior to laying is 1.915 mm. and 
2.573 mm. ten hours later. The thinning also involves enlarge- 
ment of the segmentation cavity, which may now be known 
as the subgerminal cavity. 

Hand in hand with the thinning out there takes place an 
interruption of the germ-wall at the posterior end, so that in this 
region the margin no longer enters a syncytium but rests directly 
on the yolk (ef. anterior and posterior ends of Fig. 26). 

Figure 27 is a reconstruction of the stage in question. The 
germ-wall, represented by the parallel lines, is absent at the 
posterior end. Here the cells of the blastoderm rest directly 
on the yolk. The sector bounded by this free margin and the 
broken line represents the area of the blastoderm that is 
approximately one cell thick. The figures 2 to 7 indicate 
regions approximately two to seven cells thick. 

Gastrulation begins by an involution or rolling under of the 
free margin, as though the free edge were tucked in beneath the 
blastoderm. The involuted edge then begins to grow forward 
towards the center of the blastoderm, and thus establishes a lower 
layer of cells, the primary entoderm. As soon as this process 
is started the margin of the blastoderm begins to thicken, and 
thus the inner layer of cells (entoderm) and the outer layer of 
cells (ectoderm) are continuous with one another in a marginal 
thickening (Fig. 28). 


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DEVELOPMENT PRIOR TO LAYING 59 


The margin of invagination is known as the lip of the blasto- 
pore or primitive mouth; the space between this margin and 
the yolk is the blastopore, and the space between the entoderm 
and yolk, derived from part of the subgerminal cavity, is the 
archenteron or primitive intestine. 


Fig. 27. — Diagrammatic reconstruction of the blasto- 
derm of which a longitudinal section is shown in 
Fig. 26. 


C-D., Plane of Fig. 26. 

G. W., Germ-wall. 1, 2, 3, 4, 5, 6, and 7 indicate 
regions of the blastoderm which are approximately from 
1 to 7 cells deep respectively. The broken line around 
1 indicates the region where the blastoderm is approxi- 
mately one cell deep. x 27.2. (After Patterson.) 


The first stage in the formation of the entoderm is interpreted 
as involution of the free margin, and this view is supported by 
the fact, determined by Patterson, that the antero-posterior 
diameter of the blastoderm is shorter than the transverse diameter 
during this process, whereas previously the blastoderm was 
approximately circular. An even stronger support of this view 
is furnished by experiments which demonstrate that injuries to 
the margin made just prior to gastrulation appear later in an 


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DEVELOPMENT PRIOR TO LAYING OW 


anterior position in the entoderm (Patterson). But after the 
margin has thickened the farther extension of the entoderm is 
due, largely at least, to ingrowth from the marginal thickening. 

Patterson also believes that the thickening of the margin is 
due not so much to multiplication of cells 7 situ as to immigration 
of cells from the sides. This view is also supported by experi- 
ments. 


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Fic. 29. — Diagrammatic reconstruction of the blastoderm of a 
pigeon’s egg, 36 hours after fertilization; from the same series as 
Fig. 28. x 27.2. (After Patterson.) 

E., Invaginated or gut entoderm. O., Margin of overgrowth. 
PA., Outer margin of pellucid area. R., Margin of invagination 
(dorsal lip of blastopore). 8., Beginning of yolk-sac entoderm. 
Y., Yolk zone. Z., Zone of junction. 

The arrows at the posterior margin indicate the direction of 
movement of the halves of the margin. The circles in the pellucid 
area indicate yolk masses in the segmentation cavity. 


Figure 29 is a reconstruction of a blastoderm in the stage of 
Fig. 28, that is at the height of gastrulation. The margin: of 
overgrowth (cf. Fig. 28 O) is represented by the area O; the 
zone of junction by the ruled area Z; the inner portion of the 


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DEVELOPMENT PRIOR TO LAYING 59 


germ-wall by the area with large granules Y. These zones con- 
stitute the opaque area. The circles in the pellucid area represent 
megaspheres, that is yolk-masses cut off from the floor of the 
subgerminal cavity and lying in the latter (cf. Fig. 28 M). The 
invaginated entoderm is represented by the crossed area E; 
the lip of the blastopore, where ectoderm and entoderm are 
continuous, by the region R. 


Fig. 31. — A diagrammatic reconstruction of the blastoderm repre- 
sented in Fig. 30. (After Patterson.) 
R., Mass of cells left after closure of blastopore. S.G., Anterior 
portion of subgerminal cavity not yet crossed by the entoderm. Other 
abbreviations as in Fig. 29. 


The last three or four hours prior to laying witness the closure 
of the blastopore. A comparison of Figs. 27 and 29 will show 
that the blastopore has become considerably narrower in the 
later stage. It will be observed that the posterior ends of the 
germ-wall are approaching. Finally they come into contact, and 
the blastopore is closed. During this process the lip of the 
blastopore is not cut off externally, but on the contrary comes 


60 THE DEVELOPMENT OF THE CHICK 


to lie within the germ-wall at the posterior margin of the pellucid 
area. 

This is illustrated by Figs. 30 and 31, representing a longi- 
tudinal section and a reconstruction of a blastoderm three hours 
before laying. Considering the reconstruction first, it will be 
noted that the lip of the blastopore, R, now lies within the blasto- 
derm at the posterior margin of the pellucid area. The greater 
portion of the pellucid area is now two-layered owing to the 
continued expansion of the entoderm KE, which has met and 
united with the germ-wall at the sides. The section (Fig. 30) 
passes longitudinally through the center of the blastoderm. The 
mass of cells at D represents the original lip of the blastopore. 
It is continuous with the germ-wall behind and with the ento- 
derm in front. The latter is not a continuous layer (Fig. 30 A), 
and the cells are not coherent. It is probable that the extension 
of the entoderm is due largely to independent migration of the 
cells. Subsequently the entoderm cells unite to form a coherent 
layer of flattened cells. (See Chap. IV.) 

In some cases the closure of the blastopore takes place in 
such a way as to produce a marginal notch, which is. referred 
to again in connection with the primitive streak (Chap. IV). 


CHAPTER III 


OUTLINE OF DEVELOPMENT, ORIENTATION, CHRO- 
NOLOGY 


THE preceding chapters have traced the development up to 
the time of laying. The formation of the germ-layers has begun; 
and the stage of development is fairly definite, though not abso- 
lutely constant. When the egg cools, after laying, the develop- 
ment ceases, but is renewed when the temperature is raised to 
the required degree by incubation. 

On the surface of the yolk is a whitish dise about 4 mm. in 
diameter, known as the blastoderm. Edwards gives the average 
diameter of the unincubated blastoderm (59 eggs) as 4.41 mm., 
of the area pellucida (50 eggs) as 2.51 mm. The central part 
of the blastoderm is more transparent and is hence known as 
the area pellucida; beneath it is the subgerminal cavity. The 
less transparent periphery is known as the area opaca. In the 
course of development the embryo and the embryonic mem- 
branes, which serve for the protection, respiration, and nutrition 
of the embryo, arise from the blastoderm. 

The embryo proper arises within the area pellucida, which 
becomes pear-shaped as the embryo forms; the remainder of the 
blastoderm beyond the embryo is extra-embryonic. From it 
arise the embryonic membranes known as the amnion, chorion, 
and yolk-sac. The allantois (Fig. 33 B) arises as an outgrowth 
from the hind-gut of the embryo, and spreads within the extra- 
embryonic body-cavity; it thus becomes an extra-embryonic 
membrane secondarily. The growth of the embryo and of the 
extra-embryonic blastoderm are distinct, though interdependent, 
processes going on at the same time. 

During the first four days of development the blastoderm 
spreads very rapidly (Figs. 32 and 33). ‘Thus on the fourth day 
(Fig. 33 A) the greater portion of the yolk is already covered. 
Thereafter the overgrowth of the yolk proceeds much more slowly 
(ef. Fig. 33 B). In the opaque area there arise,as concentric zones, 
the area vasculosa distinguished by its blood-vessels and the area 

61 


62 THE DEVELOPMENT OF THE CHICK 


vitellina, which may be divided into inner and outer zones 
(Figs. 32 and 33). The development of the embryo during the 
same period is indicated in the same figures. 


Fig. 82. — A. Hen’s egg at about the twenty-sixth hour of incubation, to 
show the zones of the blastoderm and the orientation of the embryo with 
reference to the axis of the shell. (After Duval.) 


B. Yolk of hen’s egg incubated about 50 hours to show the extent of 
overgrowth of the blastoderm. (After Duval.) 

A.C., Airchamber. a.p., Area pellucida. a.v., Area vasculosa. a. v.e., 
Area vitellina externa. a. v. i., Area vitellina interna. Y., Uncovered 
portion of yolk. 


The blastoderm early becomes divided in two layers as far 
as the margin of the vascular area. The outer layer, known 
as the somatopleure, is continuous with the body-wall, which is 
open ventrally in the young embryo. The inner one, known as 
the splanchnopleure, is continuous with the wall of the intestine 
which is likewise open ventrally. The space between these two 
membranes, the extra-embryonic body-cavity, 1s continuous 
with the body-cavity of the embryo. Ultimately, the splitting 
of the blastoderm is carried around the entire yolk, so that 
the latter is enclosed in a separate sac of the splanchnopleure, 
the yolk-sac, which is connected by a stalk, the yolk-stalk, to the 
intestine of the embryo. This stalk runs through an opening 
in the ventral body-wall, the umbilicus, where the amnion, which 
has developed from the extra-embryonic somatopleure, joins the 
body-wall (Fig. 33 B). 


About the nineteenth day of incubation the yolk-sae is drawn 


OUTLINE OF DEVELOPMENT, CHRONOLOGY 63 


into the body-cavity through the umbilicus, which thereupon 
closes. The young chick usually hatches on the twenty-first day. 

Orientation. It is an interesting and important fact that 
the embryo appears in a definite relation to the line drawn through 
the axis of the entire egg, or to the line joining the bases of the 
two chalaze, which is usually the same thing. If the egg be 
placed as in Fig. 32 A, with the blunt end to the left, the head 
of the embryo will be found directed away from the observer 
when the blastoderm is above; the left side of the embryo is 
therefore towards the broad end, and the right side towards the 
narrow end of the egg. According to Duval this orientation is 


Fie. 33. — A. Yolk of hen’s egg incubated 84 hours. (After Duval.) 


B. Embryo and membranes of the hen’s egg on the seventh day of incu- 
bation. (After Duval.) 

Al., Allantois. Am., Amnion. a. v., (in B) Area vitellina. E., Embryo. 
S.t., Sinus terminalis. Other Abbreviations as in Fig. 32. 


found in about 98.5 % of eggs: of 166 eggs observed, in which 
the embryo was formed, Duval found 124 oriented exactly in 
this manner, 39 in which the axis of the embryo was slightly 
oblique, 2 in which the head was towards the broad end, and 1 
in which the usual position was completely inverted. In the 
pigeon’s egg the orientation of the embryo is equally definite, but 
shghtly different. The axis of the embryo cuts the axis of the 
entire egg at an angle of about 45°, the head of the embryo being 


64 THE DEVELOPMENT OF THE CHICK 


directed away from the observer to the right, when the broad 
end of the egg is to the observer’s left as in Fig. 32 A. 

The definiteness of orientation of the embryo with reference 
to the axis of the egg enables one to distinguish anterior and 
posterior ends of the blastoderm before there is any trace of an 
embryo; and while there is no possibility of orientation by 
examination of the blastoderm itself, or when such orientation is 
otherwise extremely difficult. By the method of orienting the 
blastoderm with reference to the axis of the shell, observers have 
been able to discover important features of the early development 
which would otherwise, no doubt, have escaped observation 
The relation is of interest in other respects discussed in their 
appropriate places. (See p. 15.) 

Chronology (Classification of Stages). The development of 
an animal is an absolutely continuous process, but for purposes 
of description it is necessary to fix certain stages for comparison 
with those that precede and those that follow. Each stage has 
a certain position in the continuous process, and the correct ar- 
rangement of stages is therefore a sine qua non for their correct 
interpretation. This may seem a very simple matter seeing that 
development is in general from the more simple to the more 
complex. And it would be so if it were not for the fact that 
embryonic stages, like the adult individuals of a species, vary 
more or less, so that no one embryo is ever exactly like another. 
These embryonic variations involve (1) the rate of development 
of the whole embryo, so that at a given time in the process no 
two embryos are in exactly the same stage; (2) the relative rates 
of development of different organs; (3) the size of the embryo, 
for embryos of the same stage of development may vary some- 
what in size. 

Although the total period of incubation is fairly constant in 
the hen’s egg, about twenty-one days, yet there is great variation 
in the grade of development of embryos of the same age, especially 
during the first week. This is due to two main factors: first, 
variation in the latent period, that is the time necessary to start 
the development of the cooled blastoderm after the egg is put 
into the incubator, and second, to variation in the temperature 
of incubation. Individual eggs may vary in rate of develop- 
ment when these two factors are constant, but this difference is 
relatively shght. Other things being equal, the latent period 


OUTLINE OF DEVELOPMENT, CHRONOLOGY 65 


varies with the freshness of the egg; it is relatively short in eggs 
that are newly laid, and long in eggs that have remained qui- 
escent some time after laying. It is obvious that the latent 
period will form a more considerable portion of the entire time 
of incubation in early than in late stages. Hence the difficulty 
of classifying embryos, particularly in the first four or five 
days of incubation, by period of incubation. Eggs procured from 
dealers usually show such great variations in degree of develop- 
ment, at the same time of incubation, that it is quite impossible 
to grade them with any high degree of accuracy by time of incu- 
bation. It is stated also that the rate of development varies 
considerably at different seasons, other factors being constant. 
But this has not been found to be a serious matter in my own 
experience. 

Variations in temperature, either above or below the normal, 
also seriously affect the rate of development, and produce abnor- 
malities when extreme. If the temperature be too low, the rate 
is slower than normal; if too high, the rate increases up to a 
certain point, beyond which the egg is killed. 

The physiological zero, that is the temperature below which 
the blastoderm undergoes no development whatever, has been 
estimated differently by different authors. Some place it at 
about 28° C., others at about 25°; Edwards places it as low as 
20-21°C. At the last temperature, apparently, a small percent- 
age of eggs will develop in the course of several days to an early 
stage of the primitive streak, but most eggs show no perceptible 
development. In very warm weather, therefore, the atmos- 
pheric temperature may be sufficient to start eggs. The follow- 
ing table is given by Davenport based on Féré’s work: 


Temperature 34° 35° = 386° 87° 338° 39° = 40° 41° 
Index of Development 0.65 0.80 0.72 1:00) 1-06 1225, Arb 


The index of development represents the proportion that the 
average development at a given temperature in a given time 
bears to the normal development (7.e., development at the normal 
temperature for the same time). There is an increase in the rate 
up to 41°; a maximum temperature, which cannot be much 
above 41°, causes the condition of heat-rigor and death. 

There would seem to be no better way to determine the normal 
temperature for incubation than by measuring the temperature 


66 THE DEVELOPMENT OF THE CHICK 


of eggs incubated by the hen throughout the entire period of 
incubation. This has been done very carefully by Eycleshymer, 
who finds the internal temperature of such eggs to be as follows: 


Day of incubation 1 2 3 4 5 
Temperature of hen 102.2 103.0 103.5 104.0 103.8 
Temperature of egg 98.0 100.2 100.5 100.5 100.4 
Day of incubation 6 7 8 9 10 
Temperature of hen 105.0 104.6 104.5 105.0 105.0 
Temperature of egg 101.0 1OL.S 102.5 101.6 102.0 
Day of incubation ala i 13 14 15 
Temperature of hen 104.8 105.2 104.5 105.0 105.2 
Temperature of egg 101.8 102.2 102.0 102.5 102.0 
Day of incubation 16 17 18 19 20 
Temperature of hen 105.0 104.6 104.8 104.5 104.5 
Temperature of egg 103.0 102.4 103.0 103.0 103.0 


The temperature of the hen is seen to be somewhat higher 
than that of the eggs. In an artificial incubator where 85 % of 


the fertile eggs hatched on the twentieth and twenty-first days, 
the temperatures were as follows: 


Day of incubation 1 2 3 4 5 
Temperature of incubator 102.0 102.0 103.0 102.0 102.5 
Temperature of egg 99.5 100.0 101.0 100.5 100.5 
Day of incubation 6 7 8 9 10 
Temperature of incubator 103.0 102. 5 102.0 103.0 103.5 
Temperature of egg 101.0 100.0 100.0 101.0 101.5 
Day of incubation ala 12 13 14 15 
Temperature of incubator 103.0 103.5 104.0 103.5 104.0 
Temperature of egg 101.5 101.8 102.0 102.5 103.0 
Day of incubation 16 17 18 19 20 
Temperature of incubator 104.5 104.0 103.5 104.0 104.5 
Temperature of egg 103.0 103.0 102.5 102.5 103.5 


It would be possible then to establish a normal rate of develop- 
ment, by using perfectly fresh eggs incubated at a normal tem- 
perature. In practice I have found that the times given in Duval’s 
atlas are approximately normal, and these are, therefore, adopted 
so far as given. But even under the best conditions the varia- 
tions are sufficient to prevent close grading of stages by time of 
incubation in the first three days. This may be due to differences 
in the grade of development at the time of laying, owing to varia- 


OUTLINE OF DEVELOPMENT, CHRONOLOGY 67 


tions in the time of development in the oviduct and uterus, or 
to slow development before incubation in warm weather, or to 
individual variation. It becomes necessary, therefore, to find 
some other system. The method followed by a considerable 
number of investigators, namely to classify by the number of 
somites, has been found to be best between about the twentieth 
and ninety-sixth hours of incubation. In the table which follows, 
therefore, this method of classification is used. For the sake 
of brevity throughout the book a stage reckoned by the number 
of somites will be written 1s, 2s, 3s, etc. It is true that the rela- 
tive rate of the development of organs varies slightly. Never- 
theless, classification by number of somites is unquestionably 
the most exact method up to the end of the fourth day at least. 
Beyond this stage the method is difficult to apply, and after 
about the sixth day the number of somites becomes constant. 
After the fourth day the time of incubation is usually a suffi- 
ciently exact criterion for most purposes: the latent period has 
become a relatively inconsiderable fraction of the whole time 
of incubation, and the embryos that survive, assuming fresh eggs 
and normal temperature of incubation, are in about the same 
stage of development. 

Classification of embryos by length is a favorite method 
particularly in Germany, and it offers many advantages in the 
‘ase of some animals; under many conditions it is the only avail- 
able method. But it offers considerable difficulties, the most seri- 
ous of which come from the varying degrees of curvature of the 
embryo. In early stages of the chick, for instance, up to about 
12 s, the total length of the embryonic axis may be measured, 
for the embryo is approximately straight. The cranial flexure 
then begins to appear, and slowly increases to a right angle; 
during this period there may be an actual reduction in length 
of the embryo (cf. table, 14-16s). Conditions are also compli- 
‘ated by the fact that the head of the embryo is turning on its 
left side at the same time. The cervical flexure then appears 
and causes a second reduction of the total length (ef. table 29— 
32s). Later still the curvature of the trunk and particularly 
of the tail develops in somewhat varying degrees and makes 
bad matters worse. After these flexures are formed, let us say 
at about eighty hours in the chick, it is customary to take the 
so-called neck-tail measurement, that is, from the cervical flexure 


6S THE DEVELOPMENT OF THE CHICK 


to the apex of the tail flexure. But even then it is questionable 
if this measurement is as accurate a means of Classification as 
the age of normally incubated embryos; particularly as the cer- 
vieal flexure is secondarily eliminated by raising of the head. 
It is probable that the measurement from the tip of the head to 
the apex of the cranial flexure (head-length) would be best for 
classification of chick-embryos by measurement. This dimen- 
sion may be readily taken, after the cranial flexure begins, 
throughout the entire period of incubation. However, it has 
been relatively little used up to the present time. 

The following tables give the chronology of development up 
to the end of the fourth day, the period usually covered in labo- 
ratory courses. For the later chronology the student is referred 
to Keibel and Abraham’s Normaltafeln zur Entwickelungsge- 
schichte des Huhnes (Gallus domesticus), Jena, Gustav Fischer, 
1900. In the various chapters of Part II, the later chronology 
of the various organs is given here and there throughout the text. 
It is believed that these references will be sufficient on the whole 
to enable the student to determine what embryos to select for 
the desired stage of most organs. The tables have been made 
practically continuous from 1s up to 41s, because these cover 
the period of development in which the primordia of most organs 
are formed. They have been constructed mostly from entire 
mounts. The corresponding tables in Keibel and Abraham’s 
work are noted by number in the right-hand column. 


CHRONOLOGICAL TABLES OF THE DEVELOPMENT OF THE CHICK 

I. Before Laying: 
1. Maturation and fertilization; found in the oviduct above the 

isthmus. 

2. Early cleavage up to about 44 superficial cells found in the isth- 
mus of the oviduct during the formation of the shell-membrane 
(Kolhiker). 

. Later cleavage, formation of periblast and entoderm, etc., found 


Ww 


in the uterus up to time of laying. 
Data for the pigeon given in Chapter II; see legends to figures. 
II. Incubation to Formation of the First Somite: 

The period may be divided in three parts: (1) before the appearance 
of the primitive streak; (2) primitive streak formed but no head process ; 
(3) after the appearance of the head-process. These stages may be sub- 
divided by time or by length of the primitive streak. 


hava 1 
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Dips 362mm. areten least 


(6.6 mm. greatest length 


7 mim. greatest Jength 


(6.x mm. greatest length 


7-4 mm, greatest mens! 
‘urement 


6.6 mm, greatest length 


gt S |6.6.mm. neck-tail 


ps 


2.6 mm.|About 72 
hours 


53 mm. necktail 2.2) 
mom, foresmid brain 


\. neck-tall, 3.23 About 
tall. 3.23 * 


‘Lelt-turned to 29 somit 
‘Granial exure about 
angle, cer. ex 


anal mn 
tha & right 


Increase of cephalic flex 
tres urs fore bai 
directly back 


[Cephalic fexures sli 
ee eocotae | 


[Cervical flexure _ mare) 
‘Pronounced; rounded 


Like 28S 


nd 
approach « Might angle! 
Cervical flexure full) 
Fight angle 


Slight increase of cervical 
feure is 


Prolomgation of fore: mid 
rain, Nine ‘cuts fore) 
limb’ buds 


Uke 15S. Uke 158 


eo 


Onis ia ul) erm Saralopeset 
ver relortshape 10 


off tail bud) Like a1 S. 
seal \al 


—— 


Aicated. Tahun very 
sharply marked 


(Cerebral hemispheres 
‘clearly Indicated 


[Cerebral hemlapheres 
early indicated | 


Cerebral hemispheres 
“ronly todicated 


Cerebral hemlapheres 
‘Gearly tolled | 


Cerebral hemiey 
renuy tollesied™ 


Mouth, fue void Thhenng 
t < 
pracy derm. No 
Closed invasion: 
toa 
Like 28S |LiteayS |Uke shS 
Constrictlon of sthmus! Thickening 
‘becoming pronounced | of retinal] 
layer of 
cup 
opening 
ar 
ba 
More constriction of lth-| Retina layer|Otlc_ vesicle! Sight Invag 
mus thicker, closed nation 
Lene cof olfng 
opeting tony 
Cerebral hemispheres {i Stight inves: 
Ticated Same, a iS, ax 31) oa 
olfactory 
fat (les 
than gr) 
Cerebral herlapheces in Same as 31 |Shallow pit 


Pearshaped Pit barely: 
Pear ae diated 


Beginning off Lateral 
‘endl. 
ducts ol 


Pearaba| Lateral 
Pearsbaped oundary 


ning of Pit ly henw 
egaaiym | tspbera) 
haa | 
ar | toe 
Endol. doct.| Like 37 
forms 
hemi 


seo 
reo) 

duct} Deep. 
rte elr| pocket 
fe feo" 


Bebe | forme ight, 


No epiphysis 


|Small epiphysis 


‘Small epiphysis 
Small epiphysis 


Hemiapherical epiphysis 


Like 335 


Very alight distal en: 
‘argement 


peacoat slighly 
bs mr a re 


Kyagination is turned! 
‘Pachovards daca ad 


slignly enlarged a 


Hemisy cal | 
es Se 


‘Same as 97 S sscera 

bbs oe ten 

‘Same as 27 Like 28. Oral memby 
‘unsken 


dis he -| 
rege, Serer ta ca 
disally thin.) 


Brave of 
tea eabeane, er 
thin 
Hypepha igagan 
ae a ea 
fn 
fundibular ‘region 
Same os 31 ‘Same as 32 
Same as 31 [Same aa 32 
Dignal ol] Oral membrane i 
Ly A oS Talay com of ornare EA 
Ultr Mepresion cleasl;} raid diveniculum clos 
ween 


Stalk of hypophyxissbort|Oral_ membrane further 
ting et 200 care Thor 


seers 
Seal membrane "| Sertiealum 
co 
oe 
teriorly, 
Rupture of oral mem-| Fourth pouch clearly seen) 
causes upper wall] 
Pea Es 
pocket (preoral gut) 
[Shorteni mem! 


of Invagina.|Oral 


brane gone 
‘ion ol byp. owing ta) Fourth visceral 
sistppearane of eral) esl en 
ment 
Ra Sadry 
{ofundibuluma strongly 
marked 

poued] 


Infundibalum strongly 
marked 


‘Same asp 


‘Same as 


"eat 


Head-fold covers to» 
somite. Small till) 


Oval opening into aroni 

Vile casts exten 
from 80h to. just be) 
‘hind 31st somi 


Amnlotie wba 
inwidina 5 site} 


[Same as 32 S| Amniotie umbilicus equal! 
to diametre of 4, 
somites: 

|About samme) Aim pletely 

8 | oe 
lat round 

‘ed bods 

Cloned 

Like 36 | Closed 
Axis of 

a 

" 1 

bread, 


\: “ ” 
Uke 08'S 

Allantole extending Late 

‘veolral mesenlery ams 
Same as 30 46 ey 


” 


ow 
Uke 32 Curetog of tall bocun | 48 aie] 9us 
Codi staan epits|Cureing of tall “ sone 
orelliog 

2 


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CHAPTER IV 


FROM LAYING TO THE FORMATION OF THE FIRST 
SOMITE 


I. STRUCTURE OF THE UNINCUBATED BLASTODERM 

THERE is more or less variation in the stage of development 
of unincubated blastoderms; in exceptional cases these variations 
may be extreme. However, the usual condition may be described 
very briefly as follows (see Fig. 34): Beneath the pellucid area 
is the subgerminal cavity bounded marginally by the germ-wall. 
The posterior part only of the pellucid area is two-layered. The 
lower layer or gut-entoderm terminates posteriorly at the germ- 
wall, with which, however, it is not united. It is composed of 
spindle-shaped cells which form a coherent layer, perforated by 
numerous small openings that appear as breaks in the layer 
in section. In front of the gut-entoderm a few scattered cells 
appear in the subgerminal cavity. The gut entoderm does not 
reach the germ-wall either laterally or anteriorly, but in the 
course of a few hours’ incubation it spreads so as to unite with 
the germ-wall around the entire margin of the pellucid area. 

The germ-wall is slightly thicker at the posterior than at the 
anterior end, that is to say, that the nuclei extend deeper into 
the yolk (Fig. 34). There is a broad zone of junction and beyond 
this the margin of the blastoderm overlaps the yolk a short dis- 
tance. The germ-wall has not yet become organized as a layer 
separate from the yolk. 

The ectoderm is thicker in the region of the area pellucida 
than in the area opaca; and slightly thicker in the center than 
at the margin of the area pellucida. This thickening is in part 
the forerunner of the medullary plate. 


Il. Tue PRIMITIVE STREAK 
Total Views. The primitive streak appears early on the first 
day of incubation as an elongated slightly opaque band occupying 
69 


Kk 


CHIC 


NT OF THE 


DEVELOPME 


7) 
= 


TE 


70 


use “OW 


ayy ul yy 


S 
oO 


: 


I oy} 07 


$s 


t pu 


“][B MUL! 


c 


) 


) 


‘uornount jo ou0g “pf Zz ‘eyed aatqruntd ‘id cad -ao1taysog ‘4S0q "YI MOIB.IBA0 jo 
SMH ‘UepoyUy “JURE “Uepojod “Jou “AYLARO [BUIULIESGNY “SqNs “ABY “AOLOJUY “YU 
‘UOISTAIP JOMOT OY} UL Joy OY} 0} pus AOLIoJUT IY} saINSY oy} JO UOISTATP aoddn 
Jolweysod ay, “Ue ey} JO WepoysET poyRqnouluN UB JO WOTI0S [BUIPNSUOT uLIpe| — “PE “PT 


m8) = 32 ses 
STEEN SI eis 


he, 


We wie s. _ 
NST epee att tee or 
eee Se re ‘ eed 


=e Sons Ae) 


FROM LAYING TO FORMATION OF FIRST SOMITE rip 


the posterior half or two fifths of the circular pellucid area (Fig. 
35 B). It is relatively narrow in front and widens posteriorly, 
where it is at the same time less dense. Its anterior end usually 
does not quite reach the center of the pellucid area. It rapidly 
increases in length; the anterior end appears to be practically a 
fixed point, and growth takes place posteriorly probably not by 
addition, but between the two ends. The posterior half of the 
pellucid area elongates simultancously, keeping pace with the 


Fic. 35. — Surface views of two stages of the blastoderm of the egg of 


the sparrow. (After Schauinsland.) 


A. Before the appearance of the primitive streak. 

B. The first appearance of the primitive streak. 

a. o., Area opaca. a. p., Area pellucida. Ent. Th., Thickening of en- 
toderm. pr. str., Primitive streak. 


primitive streak which lies entirely within it in the chick and 
most other birds. Thus the area pellucida becomes oval, then 
pear-shaped, and the primitive streak bisects the greater part of 
its length (Figs. 35, 36, 44, etc.). 


According to Koller the primitive streak takes its origin from a 
erescentic area at the posterior margin of the pellucid area, which he 
terms the sickle. The primitive streak appears as a process extending 
forward from the center of the sickle, and, as it grows forward, the 
lateral horns of the sickle are gradually taken into its posterior end. 
Koller’s observations and interpretations have not, however, been con- 
firmed by subsequent investigators and they would appear to rest on 
rather exceptional and inessential conditions. 


72 THE DEVELOPMENT OF THE CHICK 


Fia. 36. — A. Intermediate stage of the formation 
of the primitive streak of the sparrow. (After 
Schauinsland. ) 

B. Fully formed primitive streak of the spar- 
row. (After Schauinsland.) 

a.o., Area opaca. a. p., Area pellucida. Ent. 
Th., Thickening of entoderm. Mes., Mesoderm. 
pr. f., Primitive fold. pr. gr., Primitive groove. 
pr. p., Primitive pit. pr. str., Primitive streak. 
s. gr., Sickle groove. 


At first the surface of the primitive streak is even, but, as 
it elongates, a groove appears down its center. This groove is 
known as the primitive groove; it is bounded by the primitive 
folds and terminates abruptly in front in a pit, the primitive 
pit, which corresponds to the neurenteric canal of other verte- 


FROM LAYING TO FORMATION OF FIRST SOMITE 73 


brates (Figs. 35, 36, 44, etc.). The primitive groove does not 
involve the extreme anterior end of the primitive streak, which 
forms a little knot in front of it, the primitive knot (‘“ Hen- 
sen’s knot”’). The posterior end of the primitive streak termi- 
nates In an expansion which is not very obvious in surface view, 
and hence is not usually described; it may be called the primitive 
plate (Figs. 36, 44 A, 44. B, etc). In some cases the primitive 
streak and groove are bifurcated at the posterior end (Fig. 44 B). 
The primitive streak is the first clear indication of the axis of the 
embryo. 


The neurenteric canal is a canal that connects the posterior end of 
the central canal of the neural tube with the intestine. It arises from 
the anterior end of the primitive mouth, and is typically developed in 
Selachia, Amphibia, reptiles, and some birds (e.g., duck, goose, Sterna, 
etc.). It begins in the primitive pit and extends forward into the head- 
process (p. SO). Subsequently the primitive pit becomes surrounded by 
the medullary folds, and thus opens into the neural canal. An opening is 
later formed through the entoderm so that the definitive canal connects 
neural tube and hind-gut. In the chick the neurenteric canal is never 
typically developed. Usually it is represented only by the primitive pit. 
In exceptional cases I have found traces of it in the head-process. 


The so-called head-process appears in front of the primitive 
knot (Figs. 36 Band 44 B). In surface view it appears not unlike 
the primitive streak itself, but is fainter and less clearly defined. 
It is continuous with the primitive streak at the primitive knot, 
but its axis is usually a little out of line with the axis of the primi- 
tive streak. 

Figs. 35 and 36 exhibit four stages of the development of 
the primitive streak of the sparrow (after Schauinsland). The 
darker area in the anterior part of the area pellucida is caused 
by a thicker region of the entoderm which in the course of time 
becomes of uniform thickness with the remainder. It will be ob- 
served that the primitive streak arises entirely within the area 
pellucida (Fig. 35 B). In later stages its posterior end is bifureated 
(Figs. 36 A and B), and we have the appearance of a sickle some- 
what similar to Ixoller’s description for the chick. The primitive 
groove begins near the anterior end of the primitive streak in an 
especially deep pit just behind the primitive knot, and extends 
back the entire length of the primitive streak into the horns of 
the sickle. The head-process is barely indicated in Fig. 36 B. 


74 THE DEVELOPMENT OF THE CHICK 


The later history of the primitive streak is illustrated in Figs. 
44, 51, 61, 65, ete.: the embryo arises in front of it around the 
head-process as a center; the anterior end of the primitive streak 
marks the hind end of the differentiated portion of the embryo. 
As the embryo grows in length the primitive streak decreases (cf. 
measurements in table), until finally, when the completion of the 
embryo is indicated by the formation of the tail-fold, the primi- 
tive streak disappears. The primitive knot and primitive pit 
occupy its anterior end at all stages, and, as the embryo differen- 
tiates from the anterior end of the primitive streak, the primitive 
pit must be regarded as moving back along the line of the primi- 
tive groove, always representing its anterior end. 

Sections. The preceding sketch of the superficial appearance 
of the primitive streak must now be followed by a careful exami- 
nation of its structure and réle in the development. 
aD oe ae pire: Be 


e ee ee 


B \epeer oss Bape rae 


es EWR; 
tS) oe 
‘Fo 
a ote ni aatae ae 
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Fic. 37. — Three sections through the pene streak of a sparrow at a 
stage intermediate between Figs. 35 and 36. x 230. (After Schauinsland.) 
A. In front of the primitive streak. 
B. Through the anterior end of the primitive streak (primitive knot). 
About through the center of the primitive streak. 


All recent authors are agreed that the primitive streak owes 
its origin to a linear thickening of the ectoderm, from which cells 
are proliferated between the ectoderm and the entoderm, forming 
a third layer, the mesoderm. Figs. 37 A, B, C show three trans- 
verse sections through a blastoderm of the sparrow shghtly more 
advanced than the stage shown in Fig. 35 B. The first section 
is just in front of the primitive streak. The ectoderm is thick 
in the center and thins gradually toward the margin of the area 
pellucida, becoming decidedly thin in the region of the area opaca 
The thin entoderm of the area pellucida unites peripherally with 
the thick yolk-sae entoderm of the area opaca. The second 


FROM LAYING TO FORMATION OF FIRST SOMITE 75 


section passes through the anterior end of the primitive streak ; 
the ectoderm is greatly thickened (primitive knot); the base- 
ment membrane is interrupted below, and the lowermost. cells 
are becoming loose. The third section is through a more pos- 
terior portion of the primitive streak. The proliferation from 
the ectoderm is more extensive, the cells are looser and are begin- 


Fic. 38. — Transverse sections through a very short primitive streak of the 
chick. Incubated 174 hours; no head-process. 


A. Through the anterior end of the primitive streak (primitive knot). 
Mesodermal cells are being proliferated from the ectodermal thickening; 
some are scattered between the two primary germ layers. The entoderm 
shows no proliferation, though some mesoderm cells are adhering to it. 

B. Fourteen sections posterior to A. (Entire length of the primitive 
streak is 80 sections.) The mesoblast wings are forming; the primitive 
groove and primitive folds are indicated. The entoderm is free from the 
mesoderm. 

Ect. Eetoderm. Ent., Entoderm. Mes., Mesoderm. pr. f., Primitive 
fold. pr. gr. Primitive groove. pr. kn., Primitive knot. 


ning to spread out laterally. The entoderm is a continuous 
membrane without any connection with the primitive streak, 
and there are no cells between ectoderm and entoderm save those 
derived from the primitive streak. 

Figs. 88 A and B show the structure of the primitive streak 


76 THE DEVELOPMENT OF THE CHICK 


of the chick at a more advanced stage, but before the formation 
of the head-process. Sections in front of the primitive streak 
show no cells between ectoderm and entoderm. In the region 
of the primitive knot (A) the ectoderm is greatly thickened, 
forming a projection above and below. Cells become detached 
from the lower surface of the ectoderm, and are converted into 
migratory cells between the two primary layers. Immediately 
behind the primitive knot the primitive groove begins abruptly; 
it is the seat of active proliferation from the lower layer of the 
ectoderm, and the cells migrate out laterally forming wings of 
cells, which do not, however, reach the area opaca (Fig. 38 B). 
Conditions are very similar along the entire length of the primitive 
streak at this time; but near the posterior end a few cells of the 
mesoderm reach the area opaca and begin to insinuate themselves 
between the ectoderm and the germ-wall. There is no evidence 
at any place that any of the mesoderm cells are derived from the 
entoderm. The axial thickening of the primitive groove comes in 
contact with the entoderm and appears in places fused to it. 

ligures 39 A~E represent five sections through the head-process 
and primitive streak of a chick embryo at a time when the head- 
process is still very short. The first section through the head- 
process is described beyond. B is through the primitive knot; 
the ingrowth of cells is more extensive than in the preceding 
stage and it will be observed that they are now fused with the 
entoderm, so that the latter no longer appears as a distinct layer. 
C is through the primitive groove near its anterior end. D is a 
little behind the center of the primitive groove, and E is through 
the primitive plate. Behind the center of the primitive streak 
the entoderm is again free (D). It will be observed that the 
area of proliferation in the primitive plate is very wide. 


lig. 39. — Five sections through the head-process and primitive streak of a 
chick embryo. The head-process is very short. 

A. Through the head-process, now fused to the entoderm. 

B. Through the primitive knot. 

C. Through the anterior end of the primitive groove. 

D. A little behind the center of the primitive streak. 

Kk. Through the primitive plate. 

The total number of sections through the head-process and primitive 
streak of this series is 102. B. is 4 seetions behind A. C. is 12 sections behind 
A. D. is 59 sections behind A. E. is 87 sections behind A. 

Eet., Ectoderm. Ent., Entoderm. G. W., Germ-wall. H. Pr., Head- 
process. med. pl, Medullary plate. Mes. Mesoblast. pr. f. Primitive fold 
pr. gr., Primitive groove. — pr. kn., Primitive knot. pr. pl., Primitive plate. 


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78 THE DEVELOPMENT OF THE CHICK 


The mode of origin of the mesoderm of birds has been a very puzzling 
question as is proved by the numerous views that have been in vogue 
from time to time. One of the earliest views was that the mesoderm 
arose by splitting of the primary entoderm (Remak). This view sur- 
vives in part even at the present time (mesoblast of the opaque area). 
Balfour believed that the mesoblast in the region of the embryo “ ori- 
ginates as two lateral plates split off from the primitive hypoblast,” and 
that the primitive streak mesoblast is extra-embryonic, or at most enters 
into the formation of mesoblast of the extreme hind end of the embryo 
(allantois mesoblast in part). This view is found in the “ Elements of 
Embryology” of Foster and Balfour. A third view, now of historical 
interest only, was that the mesoblast cells arose peripherally and mi- 
grated between the two primary germ-layers (Peremeschko, Goette). 
The latter author even attempted to derive the primitive streak from 
an aggregation of such inwandering cells. The view that the primitive 
streak arises as a thickening of the ectoderm and that it is the source 
of all the mesoderm was first stated by Iolliker, and has been accepted 
by Hertwig, Rabl, and many others. It may, indeed, be regarded as 
definitely established for the embryonic mesoblast. Others, however, 
believe with His that the mesoblast of the opaque area arises by delam- 
ination from the germ-wall; this question is discussed beyond. It should 
also be noted that it is probable that the primitive embryonic mesoblast 
is supplemented in certain regions at later stages by cells proliferated 
from both entoderm and ectoderm, particularly in the region of the 
head. (See pp. 116, 117.) 

In early stages oi the primitive streak the mesoblast cells 
are relatively sparse and bear every appearance of migrating 
separately. But as the ingrowth progresses and the cells become 
more numerous, the mesoderm becomes converted into coherent 
plates. These are wedge-shaped, the central broad ends fused 
with the primitive streak and the narrow margins extending 
laterally (Figs. 40 A, B,C). They soon overlap the margin of 
the opaque area and thus is produced a three-layered portion of 


Fig. 40. — Three transverse sections of a late stage (corresponding to about 
Fig. 44 B), through the head-process and primitive streak of a chick embryo. 


A. Near the hind end of the head-process. 

B. Through the primitive pit. 

©. A short distance behind the center of the primitive streak. The region 
between the lines A~A and B~-B is represented under a high magnification 
in Fig. 41. 

Bl. I.. Blood island. coel. Mes., Coelomie mesoblast. Eet., Eetoderm. 
Ent., Entoderm. G.W., Germ-wall. med. pl., Medullary plate. Mes., Meso- 
derm. N’ch., Notochord. pr. f., Primitive fold. pr. gr., Primitive groove. 
pr. p.. Primitive pit. 


79 


F FIRST SOMITE 


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SO THE DEVELOPMENT OF THE CHICK 


the latter which corresponds to the future vascular area. The 
mesoblast grows out, not only from the sides of the head-process 
and primitive streak, but also from the hind end of the latter, 
that is from the primitive plate. The mesoblast thus extends into 
the opaque area behind the embryo at a very early stage (Figs. 
42 and 44). This part of the mesoblast is homologous with the 
mesoblast of the ventral lip of the blastopore of reptiles and 
amphibia, and, like it, is the first place of formation of blood. 

The primitive groove must be regarded as an expression of 
the forces of invagination of the mesoblast, and the primitive 
folds as the lips of this invagination. 


Fria. 41. — The part of the section shown in Fig. 40 C, between A—A and 
B-B more highly magnified. 
Abbreviations same as Fig. 40. 


The Head-process. ‘Two stages of the head-process are shown 
in tranverse section a short distance in front of the primitive 
knot in Figs. 39 A and 40 A. It consists of a thicker central 
mass of cells with lateral wings; the central part, or primordium 
of the notochord, is continuous posteriorly with the axis of the 
primitive streak (Fig. 42); the lateral wings are mesoblast and 
they are continuous posteriorly with the mesoblast wings of the 
primitive streak. The head-process becomes inseparably fused 
with the entoderm in the middle line immediately after its forma- 
tion; and this fusion is continued back along the axis of the 
primitive streak (Figs. 39 and 40). The fusion is particularly 
intimate and persistent at the extreme anterior end of the head- 
process; behind this point the notochord and entoderm soon sepa- 
rate again in the course of development. But the anterior end 


SI 


FROM LAYING TO FORMATION OF FIRST SOMITE 


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82 THE DEVELOPMENT OF THE CHICK 


a 


of the notochord remains attached to the entoderm for a consid- 
erable period after the formation of the head-fold. A longitudinal 
section shows the head-process as an appendage to the anterior 
end of the primitive streak, or the primitive knot (Fig. 42). 


m.n. 
Fig. 43.— Diagrams to illustrate the theory of concrescence as applied to 
the primitive streak of the bird. The central area bounded by the broken 
line represents the pellucid area; external to this is the area opaca, showing 
as concentric zones the germ-wall (G. W.), the zone of junction (Z. J.), 
and the margin of overgrowth (M. O.). m.n., Marginal notch. For de- 


scription see text. 


The most obvious interpretation of the head-process is as 
an outgrowth from the primitive knot. But another, and more 
probable interpretation in view of all the facts, is that the head- 
process is a later stage of the anterior end of the primitive streak; 


FROM LAYING TO FORMATION OF FIRST SOMITE 83 


that a gradual separation of the ectoderm takes place in the 
axis of the primitive streak beginning at the anterior end, and 
progresses posteriorly. That part in which the ectoderm is 
separated represents the head-process; it has therefore the same 
composition as the primitive streak, except that the ectoderm 
has become independent. 

Interpretation of the Primitive Streak. The discussion of the 
significance of the primitive streak involves two parts: (1) its 
morphological significance, and (2) its réle in the formation of the 
embryo. The first question involves knowledge of comparative 
embryology, which is not assumed for the purposes of this book, 
and it will therefore be considered very briefly. The fundamental 
relations of the primitive streak must define its morphological 
interpretation; the first thing to be noted is that the germ-layers, 
more especially the ectoderm and mesoderm, are fused in the 
primitive streak; second, the differentiated part of the embryo 
is formed in front of it; third, the neurenteric canal occupies the 
anterior end of the primitive streak; fourth, the anus forms at its 
posterior end. Now these characters are exactly those of the 
blastopore or primitive mouth of lower vertebrates, that is of the 
aperture of invagination of the archenteron. For these reasons, 
and because in all other essential respects the primitive streak 
corresponds to the blastopore, it must be interpreted as the homo- 
logue of the latter. It is to be regarded, therefore, as an elongated 
blastopore, and the primitive groove as a rudimentary archenteric 
invagination. 

This interpretation raises the question as to its relation to 
the original marginal area of invagination of the entoderm. Can 
these two things be really different stages of the same thing? 
The concrescence theory gives a theoretical basis for their iden- 
tification. It will be remembered that the margin of invagina- 
tion represents a small section of the margin of the primitive 
blastoderm in the pigeon, and, by inference, in the chick also. 
The remainder of the margin where the zone of junction persists 
is the margin of overgrowth. Now we assume that the closure 
of the original marginal area of invagination proceeds by con- 
crescence or coalescence of its lips, beginning in the middle line 
behind, thus producing a suture which is the beginning of the 
primitive streak. Let the above circles (Fig. 48) represent the 
blastoderm in four stages of closure of the original area of invag- 


S4 THE DEVELOPMENT OF THE CHICK 


ination. The shaded margin represents the zone of Junction, the 
unshaded portion of the margin represents the area of invagina- 
tion of the entoderm. The dotted contour represents the margin 
of the pellucid area. In A the middle of the area of invagination 
is marked 1, and corresponding points to the right and left 2, 3, 
and 4. In diagram B it is supposed that the margin of invagina- 
tion is turned forward at 1, and that the lateral portions are 
brought together as far as 2, thus producing a suture in the middle 
line 1-2 continuous with the margin 3-4. The zone of invagina- 
tion is correspondingly reduced in extent and the zone of junction 
increased. In diagram C the lateral lips of the zone of invagina- 
tion are represented as completely concresced, thus producing a 
median suture 1, 2, 3, 4, extending through the posterior half 
of the area pellucida to the margin. The zone of Junction is 
on the point of closing behind the line of concrescence which is 
the primordium of the primitive streak. In diagram D, finally, 
the opaque area has closed in behind the line of concrescence 
which occupies the hinder half of the pellucid area. 

To apply this theory to the actual data of the development, 
it is only necessary to assume that the entoderm separates from 
the ectoderm along the line of concrescence, and that the primi- 
tive streak arises subsequently along the same line. The actual 
demonstration of the truth of this conception cannot be furnished 
by observation alone, however detailed. It is, however, possible 
to test it by experiment, though difficult because the concrescence 
must take place, if at all, prior to laying. The strong support 
of the theory lies at present in the data of comparative embry- 
ology; in the lower vertebrates the mesoderm and entoderm 
are both formed from the margin of invagination. 

Summarizing the matter, we may say that in the chick gastru- 
lation is divided into two separate processes: the first is the in- 
vagination of the entoderm from the margin, and the second is 
the ingrowth (or invagination) of mesoblast and notochord from 
the primitive streak, which represents the coalesced lips of the 
margin of invagination; the primitive groove is therefore the 
expression of a second phase of invagination. 

The genetic relation of the primitive streak to the margin of 
the blastoderm is well illustrated by an abnormal blastoderm 
described by Whitman in which the primitive groove was con- 
tinued across the area opaca to a marginal notch at the posterior 


FROM LAYING TO FORMATION OF FIRST SOMITE 85 


end. <A similar marginal notch at the hinder end of the blasto- 
derm in the line of prolongation of the primitive streak has been 
described also by His and Rauber, but in the cases observed 
by them there was no connection with the primitive groove. 
It suggested to them, however, the idea of genetic connection 
between the two, and was used as argument for the derivation 
of the primitive streak from the margin by concrescence. 

The second question concerning the primitive streak, its rdéle 
in the formation of the embryo, may be answered very briefly 
by saying that it is itself the primordium of the greater portion 
of the axis of the embryo; some indeed maintain that it represents 
the entire embryonic axis excepting the short pre-chordal part 
(Kkopsch). The view of Balfour and Dursy that it takes no essen- 
tial part in the formation of the embryo, but atrophies as the 
embryo forms, is now of historical interest only. The question 
is how much of the embryo is represented by the primitive streak. 
But this question is by no means easy to answer, and there is 
no complete agreement in regard to it. The one point that is 
definitely settled is that the anus arises at the hinder end of the 
primitive streak; but what point in the embryo corresponds to 
the anterior end of the primitive streak, or, in other words, how 
much of the embryo is laid down in the blastoderm in front of 
the primitive streak, is a disputed question. The attempt has 
been made to solve the problem by destroying the anterior end 
of the primitive streak by a hot needle, or by electrolysis, then 
sealing up the egg and permitting it to develop farther and finally 
locating the resultant injury in the embryo. But, while one 
worker finds the injury at the anterior end of the notochord 
(Kopsch), that is in the region of the fore-brain, another finds it 
in the region of the heart, that is in the hind-brain (Peebles). 
The reasons for this discrepancy in results are two: (1) the methods 
employed are not sufficiently exact, and (2) it is difficult in the 
living egg to determine the exact location of the anterior end of 
the primitive streak, and sometimes even to distinguish it from 
the head-process. Owing to the extremely rapid growth of all 
parts of the embryonie axis, a minute division of the primitive 
streak becomes a relatively long part of the embryonic axis in a 
very short time. It is obvious, therefore, that the slightest 
deviation of the injury from the point aimed at may lead to 
considerable error in the results. Until embryologists operate 


S6 THE DEVELOPMENT OF THE CHICK 


with instruments of greater precision one cannot feel certain of 
the results of such experiments. 


Ill. Tue MrsopERM OF THE Opaque AREA 


We have seen that the mesoderm arises from the sides of the 
head-process and the primitive streak, and grows out between 
the ectoderm and the entoderm to the margin of the pellucid 
area; it then begins to overlap the opaque area at first behind, 
later at the sides, appearing between the ectoderm and the germ- 
wall. Figs. 44 A, B, C, and 45 illustrate its peripheral extension; 
at first it spreads most rapidly behind the embryo, but soon ex- 
tends with equal speed opposite the primitive streak, and thus 
a considerable portion of the area opaca becomes three-layered, 
consisting of ectoderm, mesoderm, and germ-wall (Figs. 40 C 
and 41). The contour of the anterior margin of the mesoderm 
it as first rounded, convex anteriorly (Figs. 44 A and B). Then 
the antero-lateral angles of the mesoblast begin to extend forward 
so that the anterior boundary becomes concave (Fig. 44 C); the 
lateral horns thus established continue to grow forward and 
ultimately meet in front of the head (Mig. 45); they thus bound a 
mesoblast-free area in front of and beneath the head, known 
as the proamnion, into which the mesoderm does not penetrate 
until a relatively late stage of development. 

Blood-islands (Figs. 44 C and 45) develop early in the three- 
layered part of the opaque area; appearing first behind the em- 
bryo, they rapidly differentiate forward opposite the sides of 
the embryo and follow the expansion of the mesoblast. This 
three-layered portion of the opaque area is known as the vascular 
area (area vasculosa) after the appearance of the blood-islands. 
It soon acquires a very definite peripheral boundary by the forma- 
tion of the vena (sinus) terminalis at its margin (Fig. 45). The 
two-layered peripheral portion of the opaque area is known as 
the vitelline area (area vitellina), and here again we distinguish 
two zones, an outer including the zone of junction,and an inner 
one (Figs. 32, 33). 

The first blood-islands are masses of cells lying on the germ- 
wall behind the embryo; the first blood-cells (erythrocytes) and 
blood-vessels arise from them, hence their name. Soon after 
their origin the blood-islands appear red owing to the formation 
of hemoglobin. Between the blood-islands and the eetoderm 


87 


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FROM LAYING TO FORMATION OF FIRST SOMITE 


ae 


88 THE DEVELOPMENT OF THE CHICK 


is a layer of the mesoderm (Fig. 41). If the blood-islands be 
reckoned as mesoderm we must distinguish two layers of the 
latter, viz., a deep or vascular layer (angioblast) lying next the 
germ-wall, and an upper layer next the ectoderm, which may 
be called the coelomic mesoderm, inasmuch as the body-cavity 
(ecelome) develops within it later. 


ies 2 =n 6 A eA) 
ee Nes easier Sees SR. CES Se os Sea Shae peers Vai 2 | 
Pia. 45. — Blastoderm and embryo at the stage of four- 


teen somites. The horns of mesoblast are on the point 
of meeting in front of the head. 


a. p., Area pellucida. a. vase., Area vasculosa. a. V. i.. 
Area vitellina interna. Ht., Heart. n. F., Neural folds. 
pr’a., Proamnion. pr. str., Primitive streak. S. t., Sinus 
terminalis. 


There are two sharply contrasted views concerning the origin 
of the mesoblast in the area opaca. According to the one point 
of view it is simply a peripheral extension of the primitive streak 
mesoblast with which as a matter of fact it is continuous (Hert- 
wig, Rabl, and others). According to the other point of view 


FROM LAYING TO FORMATION OF FIRST SOMITE 89 


it is split off from the germ-wall (His and others). One thing 
is perfectly clear, viz., that the mesoderm of the opaque area 
arises in continuity with the primitive streak mesoderm; the 
second view would therefore be better expressed, as Riickert 
states it, that the primitive streak mesoderm grows in the region 
of the area opaca at the expense of elements of the germinal wall. 

If the cells of the primitive streak mesoblast be compared 
with the cells of the forming blood-islands a sharp contrast is 
observed; the mesoblast cells of the area pellucida are devoid of 
yolk-granules; young blood-islands on the other hand contain 
yolk-granules of precisely the same character as those of the 
germ-wall (Fig. 41), which must have been derived from the latter. 
If the origin of the blood-islands be carefully traced, they are 
found to be rooted in the protoplasm of the germ-wall; and prior 
to the appearance of the blood-islands proper, protoplasm and 
nuclei of the germ-wall aggregate superficially in a manner that 
appears to foreshadow the blood-islands. Therefore, either the 
blood-islands are derived from the celis of the germ-wall, or 
cells of the mesoderm growing over the germ-wall burrow into 
the latter, engulf yolk-spheres, and reappear in masses as blood- 
islands. We shall not attempt to decide between these pos- 
sibilities. 

Another question concerns the origin of the layer of ecelomic 
mesoblast that overlies the blood-islands: is it derived from the 
primitive streak mesoblast, or is it split off from the blood-islands ? 
When the latter first appear, in the periphery of the vascular 
area at least, there is no ccelomic mesoblast above them. It 
appears later, at first not as a coherent layer, but as scattered 
cells that rapidly unite to form a layer. In many places the 
microscopical appearances indicate strongly that the cells are 
split off from the surface of the blood-islands; but, as they are 
usually not far from the edge of the advancing ccelomic meso- 
blast, it may be that they are derived from the latter. Riickert 
states, however, that, in the case of some isolated blood-islands 
behind the embryo, a layer of mesoblast is formed over them 
while they are still isolated. This would render the derivation 
from the blood-islands probable in such cases. It is possible, 
therefore, that the caelomic mesoblast grows partly, at least, at 
the expense of the superficial cells of blood-islands. 

As rapidly as they are formed the various blood-islands con- 


90 THE DEVELOPMENT OF THE CHICK 


nect and anastomose with one another, forming a vascular net- 
work lying between the coelomic mesoblast and the remains of 
the germ-wall. This network spreads throughout the vascular 
area, and appears later in the pellucid area, and communicates 
with the blood-vessels of the embryo (Figs. 44 and 45). In the 
next chapter we shall consider the manner in which the extension 
takes place, and the origin of the blood-vessels and blood-cells. 


IV. THe GERM-WALL 

The germ-wall arises, as we have seen, through infiltration 
of the superficial white yclk by the periblast. These cells mul- 
tiply and anastomose and form a multinucleated syncytium with 
the yolk-granules in its meshes. By degrees the protoplasm itself 
takes up the yolk-granules, which are gradually digested, and the 
germ-wall thus becomes organized as a coherent layer. It then 
separates from the underlying yolk. The next period in the 
history of the germ-wall is its differentiation, which takes place 
in the vascular area concomitantly with the formation of the blood- 
islands: a considerable proportion of the protoplasm and nuclei 
of the germ-wall accumulates at the surface and forms the vascu- 
lar mesoderm in the manner already described. The part of the 
germ-wall that remains after the separation of the mesoderm then 
differentiates into the characteristic entodermal epithelium of the 
opaque area, which is known as the yolk-sac epithelium (ento- 
derm) because it is destined to form the lining of the volk-sac. 

After the formation of the vascular area the term germ-wall 
must be restricted to the lower layer of the vitelline area, because 
within the vascular area it has already differentiated into the 
mesoderm and = yolk-sac entoderm. The development of the 
germ-wall takes place in a centripetal direction; at any period 
during the overgrowth of the yolk the three stages of the germ- 
wall may be found in the concentric zones. The first stage, 
that of periblast, is found in the zone of junction (area vitellina 
externa); the second stage, that of organization of the germ- 
wall, is found in the area vitellina interna; and the third stage, 
that of differentiation, is found at the margin of the area vascu- 
Josa. Within the latter area the differentiation is completed. 


CHAPTER V 


HEAD-FOLD TO TWELVE SOMITES 


(From about the twenty-first to the thirty-third hour of incubation) 


I. ORIGIN OF THE HEAD-FOLD 


At the end of the period described in Chapter IV, the embryo 
is represented by a central differentiated area of the blastoderm, 
lying within the area pellucida, distinguished anteriorly by the 
medullary plate and head-process, and posteriorly by the primitive 
streak. The layers of the embryonic area are everywhere continu- 
ous with the corresponding layers of the extra-embryonic blasto- 
derm, with no clear line of division between the two. In the course 
of the second and third days the embryo becomes clearly defined 
by its own growth, and by the formation of bounding folds. 

The delimitation of the embryo from the blastoderm begins 
immediately after the formation of the head-process by the for- 
mation of a fold at the anterior end of medullary plate known as 
the head-fold (Fig. 42). Seen from the surface, this fold has a 
semicircular outline, the concavity of which is directed posteriorly 
(Fig. 44). It involves both the ectoderm and entoderm. A later 
stage is shown in sagittal section in Figs. 46 and 47: the ecto- 
derm and entoderm immediately in front of the medullary plate 
make a sharp bend downwards and backwards, and then turn 
forward again. The head-fold thus produces an internal bay in 
the entoderm, the beginning of the fore-gut. There is similarly an 
external bay, the posterior angle of which is the head-fold proper, 
lying beneath the projecting head. These bays are of course 
turned in opposite directions, the internal one opening into the 
subgerminal cavity posteriorly, and the external one opening 
anteriorly on the surface of the blastoderm. 

The transition from the ectoderm of the medullary plate into 
that of the under surface of the head and the proamnion is a grad- 
ual one. The difference is, however, very strongly marked (Tig. 
47). The formation of the head-fold is due to the more rapid 

91 


92 THE DEVELOPMENT OF THE CHICK 


ke S E's growth of the medullary plate, 
<< S Se which causes the latter to extend 
N g & forward above the thinner and more 
-* ce pliable membrane in front. The 
,X & iv entoderm is attached to the inner 

= 


surface of the anterior end of the 
medullary plate (Fig. 47), and is 
apparently carried forward with the 


med. pl. 


\ 

it latter to form the anterior portion 
+ : ; 

<7 of the fore-gut. The actual form of 


Owing to the bending of the primi- 


the fold depends upon the mechani- 
eal properties of the membranes 


NM 


pr. p., Primitive pit. 


pl., Medullary plate. 


x concerned, especially the unequal 
~ +3 ae 
we =e thickness of their parts produced 
; Be ¢~ by unequal growth. 
S SS S ; 
xs CO, 25s Although the head-fold thus ap- 
& 5 : : : ‘ 
Q tees pears to be a single fold involving 
OF eee i 
& z ae the two primary layers, it 1s con- 
Ke © ams = = . . ; J . . at . 
N Sot, venient, for purposes of description, 
io.) 0 a 
Eee. to consider it as two separate folds, 
2A ectodermal and entodermal. The 


deepening of these folds takes place 
at the same rate up to the time 
when four somites are formed (Fig. 
49). At about this time the paired 
primordia of the parietal cavity 


Germ-wall. 


Pr’a., Proamnion. 


(amnio-cardiae vesicles), which ap- 
pear in the mesoblast in the lateral 


W., 


Stage of the first inter 
t. 


tive streak the section passes to one side of the middle line posteriorly. 


extensions of the head-fold (Fig. 
50), push in towards the mid- 
dle line so as to separate the ecto- 


.. Fore-gut. 


dermal and entodermal limbs (Figs. 
52 and 58). When = six somites 


G 


nt., Notochord and entoderm. 


fF, 


are formed, these cavities fuse in 
the middle line, thus effecting a 
complete separation of the two 
limbs. The further progression of 
the head-fold, after this union, 
takes place separately in the two 


Y.S. Ent., Yolk sae entoderm. 


Eetoderm. 


46. — Median sagittal section. 
E 


Bets 
» streak. 


limbs. 


Fic. 
N’ch.4 
tive 


HEAD-FOLD TO TWELVE SOMITES 93 


II. ForMATION OF THE FORE-GUT 

The extension of the amnio-cardiac vesicles between the 
ectodermal and entodermal layers of the head-fold introduces a 
section of the body-cavity (pericardium) between these layers 
and at the same time converts the ectodermal limb into a portion 
of the somatopleure, and the entodermal limb into a portion of 
the splanchnopleure. (See p. 115.) The splanchnopleuric 
head-fold extends posteriorly very rapidly after the invasion 
of the body-cavity, while the somatopleuric fold apparently 
remains fixed for some time, though the head-fold appears to 


magnified. 
For abbreviations see Fig. 46. 


become deeper, owing to the forward extension of the head 
above the blastoderm. The posterior extension of the splanch- 
nopleuric head-fold lengthens the floor of the fore-gut; it is 
‘aused by the median growth and conerescence of folds of the 
splanchnopleure (Fig. 53). Along with this process is involved 
the development of the heart described farther on. The growth 
in length of the fore-gut may be realized by a comparison of 
Pies. 50, 52, 62, etc. 

Thus by the 12s stage a considerable section of the fore-gut 
is already established (Fig. 63); this is the pharyngeal division; 
from the first it is extremely broad, and lunate in cross-section 
(Fig. 54), the floor being composed of columnar cells, and the roof 


94 THE DEVELOPMENT OF THE CHICK 


of very flat cells. The lateral extensions may be regarded as 
diverticula; subsequently these grow more rapidly at four places 
along their length, and come in contact with the ectoderm. Thus 
four pouches are established on each side as described in detail 


sis ee ee 
/ 
/ } - \ 


ne a 
ees 
Via. 48. — Stage of first intersomitie groove 


drawn from an entire mount in balsam by 
transmitted light. 

a.c. v., Amnio-eardiae vesicle. a. o., In- 
ner margin of Area opaca. Ect., Eetoderm. 
Ent., Entoderm  H. F., Head-fold.  i.s.f.1., 
First intersomitic furrow. med. pl., Medullary 
plate. Mes., Mesoderm. n. gr., Neural groove. 
pr. gr., Primitive groove. Pr’a, proamnion. 


in the next chapter. At the 12s stage one such place of contact 
is already formed, lying a short distance in front of the thickened 
ectoderm destined to form the auditory pit. 


HEAD-FOLD TO TWELVE SOMITES 95 


Another place of fusion between the fore-gut and the ecto- 
derm is the so-called oral plate (pharyngeal membrane), which 
occupies a mid-ventral position at the extreme anterior end. 
The parietal cavities meet posterior to the oral plate (Figs. 67 
and 75). Transverse sections show the oral plate to be depressed 
beneath the level of the ventral surface of the head at the stage of 
10 somites (Fig. 55), a condition that increases, as development 


g 


‘ HID 
<f ENCE sie eam 
IG RABE aAT a7 
O'S) > 


=, — 
Oxy L£3R> “TES 
Fig. 49. — Median sagittal section of the head at the stage of 4s. 
a. i. p., Anterior intestinal portal. F.G., Fore-gut. Ect., Eetoderm. 


Ent., Entoderm. H.F., head-fold. Mes., Mesoblast. n. F., Neural fold. 
or. pl., Oral plate. 


proceeds, by the formation of the cranial flexture, and by the up- 
growth of the tissues behind and at its sides; thus will be estab- 
lished a deep depression lined by ectoderm, the floor of which is 
formed by the oral plate, and which is destined to form a large 
part of the mouth. The depression is known as the stomodeum. 


III. Oricin or THE NEURAL TUBE 
The Medullary Plate. The medullary plate is the primordium 
of the central nervous system. At the time of formation of the 
head-fold it is broad in front and narrower posteriorly, ending 
opposite the posterior end of the primitive streak. Its central 
portion is not a separate plate of cells in the region of the primi- 


96 THE DEVELOPMENT OF THE CHICK 


tive streak, but this part becomes distinct as the primitive streak 
splits into its derivatives. It is therefore only when the latter 
is entirely used up that the entire length of the medullary plate 
is established. However, long before this time the greater por- 
tion has become converted by folding into the neural tube, a 
process that proceeds in general from in front backwards. Thus 


o.0. 


Fic. 50. — Embryo of 3s from above, drawn in bal- 
sam with transmitted light. 

a.c. v., Amnio-ecardiae vesicle. a. o., inner margin 
of Area opaca. IF. G., Fore-gut. N’ch., Notochord. 
n. I’., Neural fold. pr. gr., Primitive groove. s.1,s. 2, 
s. 3, First, second and third somites. 


successive stages may be studied in serial sections of the same 
embryo; an anterior section, for instance, showing the completed 
tube, one farther back, the folded medullary plate, and yet more 
posteriorly the central part of the medullary plate disappears in 


HEAD-FOLD TO TWELVE SOMITES 97 


the undifferentiated mass of the primitive streak. These condi- 
tions must be born in mind in the following description. 

The Neural Groove and Folds. Shortly after the formation of 
the head-fold the center of the medullary plate becomes sunk in 
the form of a deep groove beginning a short distance behind the 


DCE - 


wi 
sie 


iB 


Fic. 51. — Embryo of 4s from above, drawn in alcohol by reflected light. 

a. c. v., Amnio-cardiae vesicle. a.p., Area pellucida. a. v.i., Inter- 
nal vitelline area. med. pl., Medullary plate. n.F., Neural fold. Pr’a 
Proamnion. pr. str., Primitive streak. s. 1, s. 3, First and third 


oe) 


somites. 


9S THE DEVELOPMENT OF THE CHICK 


anterior end of the plate (Fig. 48) (the neural groove); the mar- 
gins of the anterior portion of the medullary plate then become 
elevated somewhat above the surrounding blastoderm, forming 


Fig. 52.— The same embryo from beneath. 


a.ec. v., Amnio-eardiac vesicle. 
Sl the ad-fold. r’a., Proamnion. 
H. F., Head-fold. Pr’ P 


a. i. p., Anterior intestinal portal. 
the neural folds (Figs. 51 and 56). The latter rise very rapidly, 
thus deepening the neural groove, and bend in towards the middle 
line (Figs. 53,54, ete.,) meeting, by the time four or five somites are 


HEAD-FOLD TO TWELVE SOMITES 99 


formed, a short distance back of the anterior end of the medullary 
plate (Figs. 50 and 51). The posterior ends of the neural folds 
do not, at this time, reach the region of the first somite. The 
region where the neural folds first come in contact corresponds 
approximately with the region of the future mid-brain, or ante- 
rior part of the hind-brain. 


L£nt. & 


Fic. 52 A. — Median longitudinal section of the head, stage of 4s. The sec- 
tion passes through the length of one of the neural folds just behind the 


anterior end. (Cf. Fig. 51.) 


a. i. p., Anterior intestinal portal. Ect., Eetoderm. Ent., Entoderm. 
F. G., Fore-gut. H. F., Head-fold. Mes., Mesoderm. Mes. H. C., Meso- 
blastic head cavity. n. F., Neural fold. or. pl., Oral plate. 


The process of closure itself is essentially the same in all 
regions of the neural tube. Each neural fold has two limbs: an 
inner thick limb, belonging to the medullary plate, and an outer, 
thin limb, continuous with the general ectoderm (cf. Fig. 68 B). 
When the folds of opposite sides come in contact, the inner limbs 
of the two sides become continuous with one another, and also 
the outer limbs, the ectoderm then passing continuously over a 
closed neural tube. 

Certain cells in the suture and in the walls of the tube next 


Kx 


1 
J 


‘HIC 


( 


7 
4 


TELOPMENT OF THE 


DEV 


THE 


100 


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‘poyBAySN][L OSTR St SoaTey [esoyey Jo uorun Aq yauvoYy oy} JO UOIVUIIO}, OY, ‘SPIOF | 


SI 4nd oY} YOryM utr ABM oY} MOYS 07 ‘S J Jo 95RYS OYA YB TeVLod JBUTQSOZUT AOI 


I 


0yUB oy} party, 


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eq ysnf uoy 


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‘Oo pug 


OSLOASUBA], — 


‘Ayavo peyoueg “9 ‘d 


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“AYLABO 
“Soy “XB “BSOTNOSVA Bol “OSBA “B 


B19}B] JO dUBISaIOUOD AG Paulo} 
tae] 


3) A | 


HEAD-FOLD TO TWELVE SOMITES 101 


the ectoderm are destined to form the neural crest, a structure 
of great significance, inasmuch as the series of cranial and spinal 
ganglia is derived from it. (See following chapter.) 


x 


SS 
N=) sompi 


Fig. 54. — Transverse section through the same embryo a short distance 
in front of the anterior intestinal portal. For explanation of letters see 
preceding figure; in addition: Ph., Pharynx. Som/’pl., Somatopleure. 
Spl’pl., Splanchnopleure. v. M., Ventral Mesentery. 


Fic. 54 A.— Transverse section through the head of a 10s embryo. The 
region of the section is near the center of the hind brain. 
Ao., Aorta. End’ec., Endoecardium. End’e. S., Endocardial septum. 
H. B., Hind brain. My’e., Myocardium. p.C., Parietal cavity. Ph., pharynx. 
So’pl., Somatopleure. Spl’pl., Splanchnopleure. v. M., Ventral mesentery. 


The Neuropore. [rom the place where the neural folds first 
meet, the elevation and fusion proceed both forwards and back- 
wards in a continuous fashion (ef. Figs. 59, 61, 65, ete.). Although 
the open anterior stretch of the neural tube is very short in com- 
parison to the posterior open part, it is not until about the 12s 


102 THE DEVELOPMENT OF THE CHICK 


stage that the former closes completely (cf. Fig. 64). The final 
point of closure at the anterior end, known as the neuropore, 1s 
supposed by some to be a point of great morphological signifi- 
cance, and to mark the extreme anterior end of the original neural 


4 “ 
% 


\" 


f 


: _ VAo. On d/. 


a 
ye A 
Fig. 55. — Transverse section through the head immediately behind the 
optic vesicles; stage, 10s. 
Ao., Aorta. ax. Mes., Axial mesoblast. Eet., Ectoderm. Ent., Entoderm. 


F. B., Fore-brain. Mes., Mesoderm. or. pl., Oral plate. p’a.c., Periaxial cord. 
p. C. Parietal cavity. Pr’a., Proamnion. Ph., Pharynx.  v. Ao., Ventral aorta. 


axis. It is identified by these writers with the permanent neuro- 
pore of Amphioxus. However, this is open to question. Poste- 
riorly the closure of the neural tube proceeds much more rapidly, 
though, of course, it is not fully completed until after the disap- 
pearance of the primitive streak. 


ec 


Le 


Fic. 56. — Early stage of the neural folds. Transverse section through a 
4-5 s embryo between the last somite and the anterior end of the primitive 
streak. 

Eet., Eetoderm. Ent., Entoderm. n. F., Neural fold. N’ch., Noto- 
chord. med. pl., Medullary plate. Mes., Mesoderm. 


The question as to the position of the anterior end of the 
original neural axis is one of great morphological significance. 
Accompanying the closure of the neural tube in this region the 


HEAD-FOLD TO TWELVE SOMITES 103 


Lele 


THER: 


- | 
a<f\G o> te 
BSero he. 
a ©: 
on LG 


 \WSe ue oe 
Resresanee 


Coat 


Fic. 57. — Later stage of the neural folds. Section through the head of an 
embryo of 2-3; corresponding to about the future mid-brain region. 
Coel., Coelome. g. C., Germinal cells. med. pl., Medullary plate. Mes., 

Mesoblast. n. F., Neural fold. n. Cr., Neural crest. N’ch., Notochord. som. 

Mes., Somatic layer of mesoblast. spl. Mes., Splanchnie layer of mesoblast. 


anterior end rapidly grows forward beyond the anterior end of 
the fore-gut. The floor of the neural tube does not, however, 
take part in this extension, the consequence being that the sum- 
mits of the neural folds form 
arching knees extending in front 
of the original anterior end of 
the medullary plate (Figs. 51 
and 52). The extreme anterior 
end of the neural tube formed 
in this way has a ventral as well 
as a dorsal defect, and when it 
closes there is a ventral as well 
as a dorsal suture. The ventral 
end of this suture marks the 
original anterior end of the me- 
dullary plate, and this hes at 
the stage of 10 somites a short 


distance in front of the ante- Fic. 58. — Ventral view of the head 


rior end of the oral plate in region of an embryo of 5 somites, 


the region of the future re- re in eas with transmitted 
: a8 ie ’ ight. x 30. 

cessus opticus (Fig. 62). (Go- a. @. v., Amnio-cardiae vesicle. 

ronowitsch calls the anterior a. i. p., Anterior intestinal portal. 

F.G., Fore-gut. My’e., Myocardium. 

es N’ch., Notochord. n.I*., Neural fold. 

rior; His divided it into twos 2,s 4, Second and fourth somites. 


fissure, sutura cerebralis  ante- 


104 


THE DEVELOPMENT OF THE CHICK 


Fig. 59. — Embryo of 7s from above drawn 


in balsam with transmitted light. x 30. 

a.c.s., Anterior cerebral suture. ceph. 
Mes., Cephalic Mesoblast. EF. G., Fore-gut. 
N’ch., Notochord. n.'T., Neural tube. op. 
Ves., Optie vesicle. Pr’a., Proamnion. — pr. 
str., Primitive streak. s 2, s 7, Second and 
seventh somites. V. 0. m., Omphalo-mes- 
enteric vein. 


HEAD-FOLD TO TWELVE SOMITES 105 


parts, sutwra neurochordalis seu ventralis and sutura terminalis 
anterior.) 

The neuropore question resolves itself into this: What part 
of the sutura cerebralis anterior is to be called neuropore? As 
the suture extends from near the infundibulum to the pineal 
region at least, there is a wide range of choice. However, there 
is a point in the suture near its dorsal end where the separation 
of the ectoderm from the neural tube takes place later than 
elsewhere. This may be regarded as the equivalent of the 
neuropore. The suture is the site of formation of the lamina 
terminalis (Chap. VIII). 


Neh.T. 


DELP: 
Fic. 60. — The head of the same embryo from 

below x 30. 

a. i. p., Anterior intestinal portal. Kinde. s:, 
Endocardial septum. F. G., Fore-gut. Ht., Heart. 
N’ch. T., Termination of Notochord. op. Ves., 
Optic vesicle. p. C., Parietal cavity. Pra. ero- 
amnion. V. 0. m., Omphalo-mesenteric vein. 


It will be seen that according to this account most of the 
primary fore-brain includes no part of the original floor of the 
neural tube. 

Primary Divisions of the Neural Tube. The neural tube is the 
primordium of the brain and spinal cord. Its cavity becomes the 
ventricles of the brain and the central canal of the cord. There 


THE DEVELOPMENT OF THE CHICK 


op. Ves. 
: \ 


ceph. Mes. 
£6. 


PESETS. 


Fig. 61. — Embryo of 9 s from above drawn 
as a transparent object with transmitted 
hight. x 30. 

Abbreviations same as before: in addi- 
tion: H. B., Hind brain. M. B., Mid brain. 

n. 8., Neural suture. 


HEAD-FOLD TO TWELVE SOMITES 107 


Fig. 62.— The head of the same embryo from beneath more 
highly magnified. In this drawing an attempt is made to 
show different levels of the embryo superposed: thus the 
heart is uppermost in the figure, beneath this the fore-gut 
(F.G.), beneath this the notochord, and at the lowest level, 
the neural tube. 


a.¢.s., Anterior cerebral suture. Inf., Infundibulum. p.C., 
represents the anterior boundary of the parietal cavity. or. pl., 
Oral plate. v. Ao., Ventral aorta. Other abbreviations as 
before. 


is no clear distinction between brain and cord at. first, the one 
passing without any anatomical landmark into the other. Now 
the brain is the central nervous system of the head, so it is not 
until one can determine the posterior boundary of the embryonic 
head that it becomes possible to determine the hind end of the 


108 THE DEVELOPMENT OF THE CHICK 


brain. The first clear landmark is given by the mesoblastic so- 
mites, because it is known that the four anterior somites are 
cephalic. All of the neural tube in front of the fifth somite is 
therefore cranial. What a large proportion of the neural tube 
this is in early stages may be seen by comparison of figures of 
embryos in the period covered by the chapter (cf. Fig. 61). Be- 
fore the appearance of the first somite the entire medullary plate 
in front of the primitive streak is in fact cranial. 

Origin of the Primary Divisions of the Embryonic Brain. The 
embryonic brain is divided into three divisions of unequal length, 
viz., the fore-brain (prosencephalon), mid-brain (mesencephalon), 
and hind-brain (rhombencephalon). The first division is character- 
ized in the period we are considering by its very considerable 
lateral expansions, the rudiments of the optic vesicles (Figs. 59, 
61, 63, ete.), and also by the fact that there is a suture in the 
anterior portion of its floor owing to the mode of its origin (Tig. 
62). A definite constriction between it and the following division 
first appears in embryos with six or seven somites (Fig. 59). At 
the stage of 9-10 somites the next division (mid-brain) becomes 
clearly marked off by a constriction from the hind-brain (Fig. 
61). The latter is relatively very long, and its anterior half is 
characterized in the 12-somite stage by the existence of five divi- 
sions (neuromeres) separated by constrictions (Fig. 63). 

It will be noted that the first neuromere of the hind-brain appears 
about twice as large as the succeeding ones; it really includes two neuro- 
meres according to some authors. Similarly, it is maintained that the 
mid-brain includes two neuromeres and the fore-brain three. 

According to Hill’s account the entire brain of the embryo chick 
is composed of eleven neuromeres or neural segments, which are formed 
even in the 1s stage. The first three enter into the composition of the 
fore-brain; the next two, viz., 4 and 5, form the mid-brain, and the last 
six the hind-brain. 

The three that enter into the composition of the primary fore-brain 
have the following fate according to Hill: the first forms the telen- 
cephalon, the second the anterior division (parencephalon) and the third 
the posterior division (synencephalon) of the diencephalon. The cere- 
bellum arises from the first neuromere of the hind-brain, sixth of the 
series. This question is more fully discussed in Chapter VI. (See 
Fig. 83.) 


HEAD-FOLD TO TWELVE SOMITES 109 


Embryo of 12 s, from above, drawn 


Fia. 63. 
as a transparent object with transmitted 
light. x 30. Abbreviations as before. 


IV. Tue MESOBLAST 


The changes in the mesoblast during this period are of great 
importance. At the time of appearance of the head-fold it con- 
sists of two great sheets of cells between ectoderm and entoderm 


110 THE DEVELOPMENT OF THE CHICK 


beginning on each side of the head-process and primitive streak, 
and extending laterally and posteriorly to the margin of the 
vascular area. The lateral margins at this time extend anterior to 
the embryonic axis, so that the anterior margin of the mesoblast 
forms a curve with the concavity directed forward. 


ap. 


Fic. 64. — Head of the same embryo from 
below. x 30. Abbreviations as before. 


The mesoblast in the region in front of the primitive streak 
is known as gastral mesoblast, and in the region of the primitive 
streak as prostomial mesoblast; the latter is fused with the primi- 
tive streak. However, the distinction between the gastral and 
prostomial mesoblast is not of permanent significance, because 
the latter is being continually converted into the former as the 
primitive streak undergoes separation into ectoderm, notochord, 
and mesoderm. 

Confining our account now to the gastral mesoblast: a trans- 
verse section across an embryo in which the head-fold is forming 
shows a sheet of cells lying on each side of the notochord between 
the ectoderm and entoderm. It is several cells deep near the 
notochord, and thins gradually peripherally (ef. Fig. 56). The 
thicker portion next the notochord is distinguished as the paraxial 
mesoblast (vertebral plate) from the more peripheral portion or 
lateral plate. The mesoblast is sparser, the cells more scattered, 


HEAD-FOLD TO TWELVE SOMITES vt 


and the whole tissue of much looser texture in the more anterior 
portions of the embryo. 

The paraxial mesoblast increases rapidly in thickness and 
thus becomes clearly distinguishable from the lateral plate. 
Shortly after the formation of the head-fold a transverse split 
appears in the paraxial mesoblast a short distance in front of the 
anterior end of the primitive streak (Fig. 48). This is soon fol- 
lowed by a second split, a very short distance behind the first, 
and thus a complete mesoblastic somite is established. The split- 
ting is accomplished rather by segregation of the cells than by 
an actual folding. The mesoblast cells immediately in front of 
the first split aggregate so as to form a somite continuous 
anteriorly with the mesoblast of the head and thus lacking an 
anterior boundary; this is the first somite, and the one formed 
between the first two splits in the mesoblast is the second. 

The first somite established is first, not only in point of time, 
but also in position, all the remainder forming in succession behind 
this (cf. Figs. 48, 50, 51, 59, 61, etc.). As this is a point of con- 
siderable importance for understanding the topography of the 
embryo, and as previous text-books have a different account of 
it, it is worth while to give the evidence for this position in some 
detail. It has been believed up to a very recent time that from 
two to four somites were formed in front of the first one. This 
belief was due very largely to a misconception of the nature of 
the primitive streak, which was believed by some to be extra- 
embryonic, that is to he behind the embryo and not to be a part 
of the embryo itself. The first somite hes so near to the anterior 
end of the primitive streak that it was difficult to believe that 
room could be made by growth between it and the primitive 
streak with sufficient rapidity to accommodate the rapidly form- 
ing somites. In the entire absence of differentiated organs it was 
impossible to find landmarks by which to distinguish the first 
somite among the first five or six; hence it was natural to suppose 
that a certain number of somites arose in front of the first, espe- 
cially as it was not known how much of the anterior portion of 
the embryonic axis represented the head. However, in the 
absence of natural landmarks identifying the first somite formed, 
it is quite possible to create artificial ones, and in this way to 
identify it in later stages. This has been done by one of my 
students, Miss Marion Hubbard, in the following manner: In the 


112 THE DEVELOPMENT OF THE CHICK 


first place the position of the first somite was marked with a 
delicate electrolytic needle which left a permanent sear. The 
eges thus operated on were closed up and permitted to develop 
to a stage of 10-12 somites or more; and then the mark was found 


Fig. 65. — Embryo of 12s, from above, drawn in alcohol with re- 
flected light. 
au. ep., Auditory epithelium. Other abbreviations as before. 


to coincide with the first somite of the series. In the next place 
it was possible by similar means to mark out the topography of 
the embryonic head in the stage of one or two somites. Thus 
it was determined that a mark made immediately in front of the 
first somite formed appeared later in the region of the otocyst; 


HEAD-FOLD TO TWELVE SOMITES 113 


but this arises normally at the stage of 12-14 somites, a very 
short distance in front of the first somite of the series, which is 
thus shown to have the same position as the first somite formed. 
On the other hand, if one assumed that the first somite formed 


TLE 
L 


2.0. ps 


Fic. 66. — The same embryo from beneath, drawn in alcohol with 
reflected light. Abbreviations as before. 


became the third or fourth of the series, it is clear that one would 
have to make a mark some distance in front of the first somite 
formed, to strike the place of origin of the otocyst. Marks made 
on this theory were always found a considerable distance in 
front of the otocyst. Altogether a large number of experiments 


114 THE DEVELOPMENT OF THE CHICK 


was made, the concurrent testimony of which was_ perfectly 
conclusive.! 

We shall then proceed on the assumption that the first somite 
formed is also the first of the series, and that the remainder arise 
in succession behind it as transverse sections of the paraxial 
mesoblast. 

There is always a stretch of unsegmented paraxial mesoblast 
between the last somite and the anterior end of the primitive 
streak. 

The first four somites belong to the head, and enter into the 
composition of the occipital region. The more anterior part of 
the mesoblast of the head never becomes segmented in the chick. 
In the anamniote vertebrates, segmentation of the mesoblast 
extends farther forward, and there is a greater number of cephalic 
somites. This may be taken as evidence that a large part, at 
least, of the head was primitively segmented like the trunk. 
As we shall see later, the primitive metamerism of the head is 
also expressed in other ways: neuromeres, branchiomeres, etc. 

The segmentation of the mesoblast finally extends to the 
hind end of the tail, new segments being continually cut off 
from the anterior end of the paraxial mesoblast until it is all used 
up. This is not complete until the fifth day. The number of 
somites thus formed is perfectly constant, as is also the fate of 
the individual somites. 

Primary Structure of the Somites. Hach somite is primarily 
a block of cells arranged in the form of an epithelium around a 
small central lumen, towards which the inner ends of all the cells 
converge (Fig. 68 B). The central cavity (myoccele) is, however, 
filled with an irregularly arranged group of cells, and, though 
the cavity must be regarded as part of the primitive body-cavity, 
or ccelome, it has no open communication with it. After the 
somites are formed they rapidly become thicker so that their 
lateral boundary becomes very sharply marked; this is not due 
to a longitudinal constriction external to the paraxial mesoblast, 
as usually stated. Each somite has six sides, of which five are 
free, viz., dorsal, ventral, anterior, posterior, and median. The 
sixth or lateral side is continuous with the nephrotome. 

The Nephrotome, or Intermediate Cell-mass (Middle Plate). 


1Sinece the above was written, J. T. Patterson has obtained the same 
results (Biol. Bull. XIII, 1907). 


HEAD-FOLD TO TWELVE SOMITES £5 


The somites and the lateral plate are not in immediate contact 
but are separated by a short stretch of cells continuous with 
both, known as the nephrotome or intermediate cell-mass or 
middle plate. The intersegmental furrows do not extend into 
the intermediate cell-mass, and the latter therefore remains 
unsegmented like the lateral plate. It consists fundamentally 
of two layers of cells, dorsal and ventral, of which the former 
is continuous with the dorsal wall of the somite and the somatic 
layer of the lateral plate, and the latter with the ventral wall 
-of the somite and the splanchnic layer of the lateral plate (Fig. 
68 B). Thus if the two layers of the intermediate cell-mass 
were separated the space between them would be continuous 
with the coelome that arises secondarily in the lateral plate. This 
condition actually exists in some of the Anamnia (Selachii, for 
instance) in which the intermediate cell-mass is also segmented. 

The Lateral Plate. This name is given to the lateral meso- 
blast within which the body-cavity arises. It is separated from 
the somite by the nephrotome and its lateral extension coincides 
with the margin of the vascular area. 

Development of the Body-cavity or Celome. The cclome 
or body-cavity arises within the lateral plate as a series of sep- 
arated small cavities, distributed throughout its whole extent, 
which appear first in the anterior portion (1-38 s stage). By 
successive fusion of these cavities and their extension centrally 
and laterally, there arises a continuous cavity, the ccelome, 
which extends from the nephrotome to the margin of the vascular 
area (Fig. 68), and which becomes the pleuroperitoneal and per- 
icardial cavities in the embryo, and the extra-embryonic body- 
cavity beyond the boundaries of the embryo. 

Of the two layers of the lateral mesoblast thus established, 
the external is known as the somatic and the internal as the 
splanchnic layer. In the course of development the somatic 
layer becomes closely bound to the ectoderm, thus constituting 
the somatopleure, and the splanchnic layer becomes similarly 
united to the entoderm, thus establishing the splanchnopleure. 
The somatopleure is destined to form the body-wall and the 
extra-embryonic membranes known as the amnion and chorion; 
from the splanchnopleure is derived the alimentary canal with 
all its appendages, and the yolk-sac. As described in detail in the 
next chapter, this splitting of the mesoblast progresses with 


116 THE DEVELOPMENT OF THE CHICK 


the overgrowth of the yolk until it extends completely around 
the latter 

Returning now to the first stages in the formation of the coe- 
lome. In the 35s stage it undergoes a precocious expansion in 
the region lateral to the head of the embryo (Figs. 51, 52, etc.), 
forming a pair of large cavities known as the amnio-cardiac 
vesicles, because they participate in the formation of the amnion 
and pericardium. These cavities extend in rapidly towards the 
middle line, and enter the head-fold in the 4-5 s stage (Figs. 52, 
58). At the stage of 6-7 s they meet in the floor of the fore-gut 
immediately behind the oral plate and fuse together, thus divid- 
ing the head-fold into somatic and splanchnic limbs, as previously 
described. A median undivided portion of the body-cavity 
known as the parietal cavity (forerunner of the pericardium) 
is thus established beneath the fore-gut; and it extends back- 
ward with the elongation of the fore-gut in the manner already 
deseribed. <A pair of blind prolongations of this cavity extends 
a short distance forward at the sides of the oral plate at the 10-12 s 
stage (cf. Fig. 62), lying lateral and ventral to the ventral aorte. 

The median angle of the body-cavity, where the somatic 
and splanchnic layers meet, is a point of fundamental morpho- 
logical importance. In the region of the somites the nephrotome 
is attached here, and in the head the wing of cells leading to the 
axial mesoblast (cf. Figs. 68 B, 538, and 54). In an embryo 
with ten somites this angle may be traced forward to near the 
hinder end of the oral plate, lying beneath the lateral angles of 
the pharynx. 

Mesoblast of the Head. Mesoblast exists in two forms in 
the embryo: (1) in the form of epithelial layers or membranes 
(mesothelium), and (2) in the form of migrating cells which 
usually unite secondarily to form a syncytium in the form of a 
network, the meshes of which are filled with fluid; the nuclei 
lie in the thickened nodes. This form of the mesoblast is known 
as mesenchyme. It is always derived from a pre-existing epl- 
thelial layer, usually, but not necessarily, mesothelium, for, as 
we shall see, parts of it are derived from ectoderm and entoderm; 
on the other hand, mesenchyme may secondarily take on an 
epithelial arrangement (endothelium). The terms mesothelium 
and mesenchyme have therefore merely descriptive significance 
in the early embryonic stages. The mesenchyme has no single 


HEAD-FOLD TO TWELVE SOMITES C7, 


embryonic significance either as to origin or fate, but is to be 
regarded as a mixed tissue. 

The mesoblast of the head is derived from several sources: 
(1) from a continuation forward of the paraxial mesoblast; (2) 
by proliferation from the fore-gut; and (3) from proliferations of 
ectoderm. 

(1) The axial mesoblast of the head is an anterior continua- 
tion of that of the trunk; it terminates at the anterior end of the 
fore-gut with which it is continuous from the stage of the head- 
process up to about the 6s stage (Figs. 48 and 49). In the 
anterior part of the head it is mesenchymal in its general struc- 
ture, grading posteriorly: into the mesothelial paraxial mesoblast 
of the hinder part of the head and trunk. It is continuous at 
first with the lateral mesoblast in which the amnio-cardiae 
vesicles are forming; but this connection is lost in the anterior 
part of the head that projects forward above the blastoderm; 
that is, in front of the head-fold. 

(2) The anterior end of the fore-gut proliferates mesenchyme 
from the time of its first formation to about the 6s stage (Fig. 
49). The proliferation is so rapid that it may give rise to the 
appearance of diverticula. The extreme anterior end of the floor 
forms a sac which lies just in front of the oral plate at the 4s 
stage (Fig. 52 A), but soon after breaks up into mesenchyme. 
There is a considerable mass of mesenchyme formed from this 
source in the space bounded by the anterior end of the fore-gut, 
the neural tube and the ectoderm; at the 4s stage this appears 
fused with the floor of the neural tube and the surface ectoderm, 
and probably receives cells from both; the anterior end of the 
notochord also disappears in this mass (cf. Fig. 67). 

(3) Ectodermal proliferations forming mesenchyme in the 
head. (This subject is discussed in the next chapter.) 

Vascular System. The origin of the blood-islands in the 
opaque area was described in the preceding chapter. They lhe 
between the ccelomic mesoblast and the yolk-sac entoderm de- 
rived from the germ-wall. When the somatopleure and splanch- 
nopleure are formed the blood-islands lie between the two layers 
of the latter, and the somatopleure is entirely bloodless. About 
the stage of 1 somite a vascular network continuous with the 
original network of the opaque area begins to appear in the 
pellucid area, at first at the margin of the opaque area, but by 


118 THE DEVELOPMENT OF THE CHICK 


degrees nearer and nearer to the embryo, until, by the 7 or 8s 
stage, blood-vessels begin to appear in the embryo itself. It is 
important to note that the order of appearance of the vascular 
primordia is first in the area opaca in the order previously de- 
scribed, then in the pellucid area and finally in the embryo itself. 
Moreover, the parts appearing later are, usually at least, in con- 
tinuity with those first formed. 

Before discussing the way in which the blood-vessels arise 
in the pellucid area and in the embryo, we should consider the 
first differentiation within the original, or peripheral, blood- 
islands. Between the 3 and 5s stage it may be noticed in 
sections that vacuoles are forming within the peripheral blood- 
islands near the entodermal surface. The expansion of these 
vacuoles carries the peripheral layer of cells away from the main 
mass of cells composing the blood-islands, and by degrees the 
process is carried completely around the blood-island, so that 
the peripheral layer becomes entirely separated from the central 
mass and encloses it (See Fig. 68 C.). The enclosing cells become 
flattened during this process to form an endothelium; inasmuch 
as the blood-islands are not separate, but anastomose to form a 
network, the process results in the formation of a network of 
endothelial tubes enclosing cell-masses. Thus arise the first 
blood-vessels. The enclosed masses of cells rapidly acquire 
hemoglobin, become separated from one another, and form 
blood-cells. 

There is a great difference in the relative amounts of blood- 
cells formed in different regions. Thus in the anterior part of 
the opaque area and in the pellucid area the original blood- 
islands are relatively small (Figs. 44 and 45), and furnish material 
sufficient only for the formation of the blood-vessels. On the 
other hand, in the peripheral part of the vascular area, especially 
towards its posterior end, the largest masses of blood-cells are 
found; and these conditions grade into one another. In other 
words, the formation of blood-cells is restricted at this time to 
the opaque area, and is most abundant posteriorly. In the 
pellucid area only empty blood-vessels are formed. Similarly 
the blood-vessels of the embryo itself are at first empty; they 
become filled secondarily from the opaque area when circulation 
begins. 

The appearance of blood-vessels within the pellucid area 


HEAD-FOLD TO TWELVE SOMITES 119 


and the embryo has been interpreted in two principal ways: 
(1) that they are an ingrowth from the original vascular primor- 
dium of the opaque area; and (2) that they arise by differentia- 
tion in situ. The first view was originally stated by His, and 
has been supported by Ixolliker and others. The second is sup- 
ported by Rickert, P. Mayer and others. The observations, 
on which the ingrowth theory of His were based, were made 
originally on whole blastoderms of the chick, and concerned 
primarily the order of origin of the blood-vessels, which is cen- 
tripetal. But it is obvious that such observations do not in 
themselves demonstrate the existence of an independent ingrow- 
ing primordium; they are not in the least inconsistent with the 
view that the blood-vessels differentiate from the cells im situ. 
Within the embryo itself parts of certain vessels appear to arise 
separately, and form secondary connections with the vessels 
formed at an earlier time; this is the case for instance with the 
dorsal aorta in the region of the head. The histological appear- 
ances accompanying the first origin of blood-vessels in the pel- 
lucid area appear to favor the view that they arise from detached 
cell-groups of the splanchnic mesoderm. It would, however, be 
going too far to assert that the embryonic blood-vessels have no 
independent power of growth; certain appearances cannot be 
satisfactorily explained in any other way. 

Origin of the Heart. The embryonic heart possesses two 
layers: an internal delicate endothelium, the endocardium, and 
an external strong muscular layer, the myocardium. The endo- 
cardium arises in continuity with the blood-vessels of the pellucid 
area, and is in no wise different from them; the myocardium, on 
the other hand, arises from the splanchnic mesoblast. The heart 
is thus to be regarded as a portion of the embryonic vascular 
system, specially provided with a muscular wall for the propul- 
sion of the blood. The first indication of the heart is a thicken- 
ing of the splanchnopleure of the amniocardiac vesicles, which 
forms the primordium of the myocardium. This is situated a 
short distance lateral to the hind-brain region of the embryo, and 
makes its appearance between the stage of 3 and 5 somites. 

The endocardium soon appears between the thickened ento- 
derm and the myocardium, in the form of a delicate endothelial 
vessel on each side, continuous with the extra-embryonic blood- 
vessels. This is, indeed, the place where the blood-vessels first 


120 THE DEVELOPMENT OF THE CHICK 


reach the embryo. The myocardium then becomes arched 
towards the body-cavity and includes the endocardium in its 
concavity (Fig. 53). The heart thus comes to consist of two 
parts on each side: a myocardial gutter semicircular in cross 
section, open towards the entoderm, and an endothelial tube 
lying in the gutter, and in contact with the entoderm. At this 
time the lateral limiting sulci appear in the splanchnopleure 
just central to the endocardium on each side, and, as the fore- 
gut closes from in front backwards, the following changes take 
place (Figs. 54 and 54 A): (1) the entoderm withdraws completely 
from the fused apices of the lateral folds in the splanchnopleure, 
and thus a wide separation is made between the floor of the pharynx 
and the splanchnopleure below; (2) the right and left endocardial 
tubes come into immediate contact in the floor of the pharynx; 
(3) the two myocardial gutters coming together form a single 
tube around the endocardium, suspended by a double mesoder- 
mal membrane (mesocardium or dorsal mesentery of the heart) to 
the floor of the pharynx, and attached by a similar mesentery 
(ventral mesentery of the heart) to the splanchnopleure beneath 
(Fig. 54). The latter connection is ruptured almost as soon as 
formed, so that the floor of the myocardium becomes complete 
(Fig. 54 A). Soon after the completion of the floor of the phar- 
ynx the two endocardial tubes press together until the common 
wall becomes reduced to a vertical partition, which then ruptures; 
and finally (10-12 s) all traces of the original duplicity of the 
heart disappear (Figs. 60, 62, 64). 

The heart thus arises from two lateral halves which fuse sec- 
ondarily to form a single tube. This fusion takes place from 
in front backwards, hence the anterior end of the heart is formed 
first. Indeed, the full length of the cardiac tube is not formed 
in the period covered by this chapter; the definitive hindermost 
division is established by concrescence after the 12s stage. But 
the actual hind end is always continuous with the extra-embryonic 
network of blood-vessels and this connection develops into the 
main splanchnic veins. 


As a rare abnormality the lateral primordia of the heart may meet 
and fuse dorsal to the embryo, instead of in the floor of the pharynx. 
This condition is known as omphalocephaly ; in other rare cases the lateral 
halves may fail to unite, and two hearts may be formed. 

There are three views concerning the origin of the endocardium: 


HEAD-FOLD TO TWELVE SOMITES 121 


(1) that it is an ingrowth of the extra-embryonic vessels, (2) that it arises 
from the mesoblast 7n situ, (3) that it arises from the entoderm in situ. 
Appearances such as that shown in Fig. 53 favor the last view. 

The heart is then a double-walled tube attached to the floor 
of the pharynx. The posterior end rests squarely against the an- 
terior intestinal portal and is continuous with the rudiments of 
the splanchnic veins running in the diverging folds of the portal; 
the anterior end of the heart is continued as a simple endothelial 
tube (ventral aorta) as far forward as the oral plate, where it is 
divided in two (Figs. 62, 64, etc.). 

This primitive simplicity of the cardiac tube continues through- 
out the period considered in this chapter without substantial 
alteration. The heart increases in length with considerable 
rapidity, but being attached at its anterior and posterior ends by 
the aortic and venous roots respectively, it is forced to bend, 
nearly always to the right, so that a convexity of the heart 
appears to the right of the embryonic head, at about the 11-12 s 
stage (Figs. 63, 64). About this time the mesocardium (dorsal 
mesentery of the heart) disappears except at the posterior end, 
and the cardiac tube thus becomes free except at its two ends. 

The Embryonic Blood-vessels. The dorsal aorta arises from 
the median edge of the vascular network, which extends across 
the pellucid area in the splanchnopleure. At the stage of 7-9 
somites, it has reached the nephrotomic level. The marginal 
meshes gradually straighten themselves out into a longitudinal 
vessel, continuous with the net-work at the sides and behind. 
Only the trunk part arises in this manner. The cephalic part 
arises by forward growth of the trunk part or from mesenchyme 
in situ. In some embryos the most anterior portions of the 
cephalic aorte are much better developed than the posterior por- 
tion; indeed, in places there appears to be a complete hiatus 
between cephalic and trunk aorte. The impression gained is that 
a large part of the cephalic aorte arises in situ. Some series of 
sections are practically conclusive in this respect (8-9 somites). 
A connection is then formed around the anterior end of the fore- 
gut with the ventral aorte (Fig. 55), and an arterial pathway is 
thus established from the heart by way of the ventral and dorsal 
aorte to the vascular network of the splanchnopleure. 

The arterial system consists at thirty-three hours (12s stage) 
of the following parts: (1) ventral aorta; (2) first visceral or 


122 THE DEVELOPMENT OF THE CHICK 


mandibular arteries connecting 1 and 3; (3) dorsal aorte; (4) seg- 
mental branches of the dorsal aorte. The ventral aorta is, as 
we have seen, the anterior prolongation of the endocardium 
extending between the extreme anterior end of the heart proper 
and the oral plate. At the oral plate it divides into two branches, 
right and left mandibular arteries or arches, that surround the 
anterior end of the fore-gut, and arch over to be continued into 
the two dorsal aortee. The tissue in which these arches run is 
destined to form the mandibular arch or lower jaw. The two 
dorsal aorte are very large vessels running above the roof of the 
pharynx near its lateral angles. They give off no branches in 
the head. In the trunk they pass backwards in the splanchno- 
pleure beneath the somites (Fig. 68 B), and are connected at 
intervals with the extra-embryonic blood-vessels. These con- 
nections are more important in the region of the primitive streak 
(Fig. 63) where the dorsal aortz disappear in the general extra- 
embryonic network. Shght diverticula of the dorsal aorte 
ascend in the interspaces between successive somites (segmental 
arteries). 

Concerning the veins in the period under consideration there 
is nothing additional to be said. 


V. DESCRIPTION OF AN EMBRYO WITH 10 SOMITES 


It will now be in place to describe rather fully the anatomy 
of the stage at which we have arrived; this will serve as a point 
of departure for the next chapter. 

The blastoderm is a circular membrane covering a consider- 
able portion of the yolk (ef. Fig. 32 A). The embryo appears 
to the naked eye as a whitish streak in the central pear-shaped 
pellucid area. The surface views and the two views of the em- 
bryo viewed as a transparent object show the topography of the 
various parts of the embryo (Figs. 63-66). 

A section across the entire blastoderm at the stage of 10s, 
through the sixth somite (Fig. 68), shows the following parts: 

The ectoderm bounds the section above; it is thickened in the 
angle between the neural tube and the somites, and becomes 
thinner as it is traced peripherally; at the extreme periphery of 
the blastoderm it merges into a mass of cells that interpenetrate 
the yolk. Ventrally the boundary of the section is formed by 
the entoderm which is slightly arched upwards in the middle line. 


HEAD-FOLD TO TWELVE SOMITES 12 


In the region of the area pellucida the entoderm is very thin; at 
its boundary it passes rather abruptly into the large rounded vesi- 
cular cells of the yolk-sac entoderm, which becomes continuous 
at the margin of the vascular area with the germ-wall; the 
latter continues to the periphery where it merges in the undifferen- 
tiated cell-mass (zone of junction) (Figs. 68 A-68 E). The large 
neural tube is not yet closed. Beneath the neural tube is a sec- 
tion of the solid rod-like notochord. 


Fic. 67. — Median longitudinal section of the head of an embryo of 13 s. 

Ectam., Ectamnion. F. B., Fore-brain. H. B., Hind-brain. Inf., In- 
fundibulum. M. B., Mid-brain.  pr’e. pl., Precardial plate. T. p., Tuber- 
culum posterius. Other abbreviations as before. 


The mesoderm (Fig. 68 A, B, C) lies between the parts already 
named; it consists on each side of the middle line of the following 
parts: (1) the mesoblastic somite, a block of cells that radiate 
from a central cavity filled with irregularly disposed cells; (2) the 
intermediate cell-mass or nephrotome, forming a narrow connect- 
ing bridge between the somite and the lateral plate; (3) the 
lateral plate, split into two layers, external, known as the somatic 
layer, and internal or splanchnic layer. The cavity between the 
two layers is the celome or body-cavity; it is very narrow next the 
nephrotome, but widens as it extends laterally to the margin 
of the vascular area, and is divided by various strands of cells 
extending from somatic to splanchnic layers, thus indicating its 
origin by fusion of ccelomic vesicles. 

The ectoderm plus the somatic layer constitute the somato- 
pleure, from which the body-wall, amnion, and chorion are derived, 
and the entoderm plus the splanchnic layer form the splanchno- 


124 THE DEVELOPMENT OF THE CHICK 


pleure, from which arises the intestine and all its appendages, 
including the allantois and the yolk-sac. Blood-vessels lie be- 
tween the splanchnic mesoblast and the entoderm. The large 
vessels beneath the somite and nephrotome are the dorsal aorte; 
small vessels are present in the area pellucida, and there are 
many large ones in the area vasculosa. The walls of the vessels 
are constituted of a single layer of flat endothelial cells bulging 
in the region of the nuclei; in the vascular area are true blood- 
islands with embryonic blood-cells more or less fully filling the 
cavity. 

In a median sagittal section (Fig. 67) the following points 
should be noticed: (1) the neural tube is enlarged in the region of 
the head to form the brain, more fully described below; (2) the 
entoderm forms a tube in the head known as the pharynx or 
cephalic enteron (cephalic part of the fore-gut), opening behind 
the heart into the space between the entoderm and yolk. The 
floor of the anterior end of the fore-gut is fused to the ectoderm 
in the middle line forming the oral plate. The entoderm forming 
the floor of the fore-gut turns forward around the hind end of 
the heart, and beneath the anterior part of the head forms part 
of the proamnion or mesoderm-free region of the pellucid area; 
(3) the large pericardial (parietal) cavity lies beneath the floor 
of the fore-gut. Attached to the posterior wall of the pericar- 
dium one sees the hind end of the heart with its two walls, the 
endocardium and the myocardium a fold of the mesoblastie lin- 
ing of the pericardium. Between the anterior end of the pericar- 
dium and the oral plate is seen the endothelial ventral aorta; (4) 
the notochord les between the fore-gut and neural tube and ends 
anteriorly in a mass of mesenchyme lying between the infundib- 
ulum and fore-gut. 

The Nervous System. The neural tube is closed at the 12s 


Fic. 68. — A. Transverse section across the axis of the embryo and the en- 
tire blastoderm of one side. The section passes through the sixth somite 
of a 10 s embryo, and is intended to show the topography of the blastoderm. 
The regions B, C, D, E are represented under higher magnification in the 
Hiss: B,C, Dy E. 

a.v.e., Area vitellina externa. a.v.i,Area vitellina interna. BI. i., Blood 
island. Bl. v., Blood vessel. Coel., Coelome. G. W., Germ-wall. M. O., 
Margin of overgrowth. N’ph., Nephrotome. $., Somite. Som’pl. Soma- 
topleure. Spl’pl.,Splanchnopleure. Som. Mes., Somatie layer of mesoblast. 
spl. Mes., splanchnic layer of the mesoblast. 5S. T., Sinus terminalis. Y. 5. 
Ent., Yolk-sac entoderm. Z. J., Zone of junction. 


area pellucida ave. | 


oe 
Pow 


Oe, ) 


ONO" 5. Ent. 
as 


126 THE DEVELOPMENT OF THE CHICK 


stage (Figs. 63 and 65) to a point a little behind the last meso- 
blastic somite; beyond this the medullary folds diverge and are 
lost to view towards the hind end of the primitive streak. We 
may distinguish a cephalic portion (brain or encephalon) and a 
trunk portion (spinal cord or myelon) of the neural tube; the 
boundary lies between the fourth and fifth somites, for the first 
four somites enter into the composition of the head. The brain 
is thus at this time about as long as the portion of the cord formed 
or indicated by the medullary folds. For description, see p. 108. 

Alimentary Canal. The alimentary canal and its appendages 
exist only potentially in this embryo in the form of the splanchno- 
pleure, except in the head. The cephalic enteron of this stage 
corresponds to a large part of the pharynx. The oral plate has 
already been described in connection with the sagittal section 
(Fig. 67). In transverse section the extreme anterior end of the 
fore-gut is quite narrow, elsewhere it is very wide laterally, and 
in one place its lateral expansions come in contact with the 
ectoderm on each side and fuse to it, thus indicating the hyoman- 
dibular cleft. The floor and lateral walls of the pharynx are com- 
posed of columnar cells, the roof of flattened squamous cells 
(Fig. 54). 

Vascular System. The heart lies in the parietal cavity be- 
neath the pharynx; it is bent near its middle to the right. It is 
an undivided double-walled tube, the internal wall or endocardium 
being a continuation of the blood-vessels, and the external wall, 
myocardium or muscular heart, being a duplication of the wall 
of the pericardium. It has not yet reached the stage of regular 
contraction, though it may be observed to twitch from time to 
time. The chambers of the heart are indicated, but not clearly 
defined at this time; one can only say that the posterior end is 
the venous end from which the sinus and auricles are to form, 
and the anterior two thirds, the arterial end, destined to form the 
ventricles and bulbus. 

The endocardium is continued anteriorly into the ventral 
aorta, which divides on each side of the oral plate (Fig. 64), to 
form the mandibular arches that describe a loop around the 
anterior end of the fore-gut and are continued posteriorly as 
the dorsal aorte, which run above the roof of the pharynx, lateral 
to the notochord, into the trunk, where they lie ventral to the 
nephrotome, and send off short blind branches (segmental arteries) 


HEAD-FOLD TO TWELVE SOMITES 127 


between the somites. Near the primitive streak they disappear 
by merging in the vascular network of the blastoderm. 

The posterior end of the endocardium divides in two branches 
that pass out along the postero-lateral margins of the fore-gut 
into the general vascular network of the blastoderm (Fig. 64). 
This connection constitutes the beginning of the vitelline veins 
through which the blood from the yolk-sac enters the posterior 
end of the heart. 

General. The elongated form of the entire embryo and the 
preponderance of the head are marked features of this stage. 
The latter condition is largely due to the order of origin of parts: 
the anterior parts preceding the more posterior in their appear- 
ance. The head is really, therefore, in a more advanced stage 
of development than the trunk, hence larger. The elongated 
condition of the head and the arrangement of all its organs in 
longitudinal sequence, however, are probably conditions of 
phylogenetic significance, and point towards an ancestral con- 
dition. The topographical values of the divisions of the em- 
bryonic head are very different from those of the adult, to attain 
which certain regions develop to a relatively enormous extent, 
and others comparatively little. 

A number of features in the anatomy of the 12s stage are 
purposely omitted from this description, as they represent the 
primordia of structures described more fully beyond; such, for 
instance, are the neural crest, the pronephros, ete. 

Zones of the Blastoderm. ‘The following zones may be recog- 
nized in the blastoderm : (1) the pellucid area surrounding the 
embryo; (2) the vascular zone of the opaque area; (3) area vitel- 
lina interna; (4) area vitellina externa. The pellucid area is 
readily defined by its transparency and by the existence of the sub- 
germinal cavity beneath it. The vascular zone is most readily 
defined by the extension of the blood tissue which has a very 
definite margin, coincident with the extension of the mesoblast. 
The area vitellina includes all of the blastoderm peripheral to the 
vascular area, and it is characterized by the presence of two 
layers only, ectoderm and entoderm (germ-wall). It is again 
divided into two concentric zones, internal and external. The 
internal is much the wider (Fig. 32 A), and is characterized by 
the existence of a perilecithal space, 7.e., a slight fluid-filled 
‘avity between the entoderm and yolk continuing the subgerminal 


128 THE DEVELOPMENT OF THE CHICK 


cavity peripherally. The external vitelline area is_ relatively 
narrow, and consists (1) of the zone of junction adjoining the 
internal vitelline area, and (2) a free margin separate from the 
yolk (margin of overgrowth). The zone of junction is the per- 
sistent embryonic or formative part of the blastoderm from 
which the extra-embryonic ectoderm and entoderm arises. Thus 
as it spreads peripherally over the surface of the yolk, it leaves 
on its central margin the differentiated extra-embryonic ecto- 
derm and entoderm; in other words, the zone of junction is the 
youngest part of the blastoderm, and the concentric zones that 
may be drawn within it represent successively older stages in a 
centripetal direction. Therefore in a transverse section through 
the entire blastoderm successive stages of differentiation of the 
ectoderm and particularly of the entoderm are met as one passes 
from the zone of junction towards the center. 

The free margin arises from the zone of Junction in the manner 
already described in Chapter II. It may be considered as a part 
of the ectoderm and it terminates in a row of enlarged cells that 
often exhibit amoeboid prominences on their margins. It would 
appear that these cells have the function of a marginal wedge 
that separates the vitelline membrane and yolk. 

The germ-wall has been the subject of many extended re- 
searches, but a definitive solution of its origin and function has 
not hitherto been obtained, mainly on account of the incomplete 
knowledge of its early history. The ground here taken is in some 
respects different from that of the various authors, but it is based 
on a study of its early history given in Chapter II. There is no 
deviation from the mode of formation of the zone of junction in 
the stage under consideration from what was found in earlier 
stages, and there is no reason to believe that its subsequent history 
varies in any important respect. It appears to be produced by 
continuous proliferation of the cells in the yolk as in earlier stages 
(see Fig. 68 E). These cells actively engulf the large yolk gran- 
ules, and the histological structure becomes in consequence diffi- 
cult of analysis. The cells lose their individuality and constitute 
an extended syncytium, the protoplasm of which is packed with 
yolk-granules. In removing the blastoderm from the egg in salt- 
solution one finds always, after removing the yolk that may be 
washed off, a narrow submarginal zone of adherent yolk that is 
not readily removed, and this is the site of the zone of junction. 


HEAD-FOLD TO TWELVE SOMITES 129 


Centrally to the zone of junction we have the differentiated 
ectoderm and germ-wall sharply separated from the yolk by the 
perilecithal space. The ectoderm of the inner zone of the vitelline 
area requires no extended notice; it consists at this time of a sin- 
gle layer of flattened cells. The germ-wall next to the zone of 
junction consists of two or three layers of large, more or less 
rounded, cells with definite boundaries, each of which contains 
one or more yolk-spheres and smaller yolk-granules (Fig. 68 E). 
We may say roughly that whereas in the zone of junction we 
have cells in the yolk, in the vitelline area we have yolk in the 
cells. This may indicate sufficiently the way in which a several 
layered epithelium becomes differentiated from the zone of junc- 
tion. As this epithelium is traced centrally we find usually a 
short distance from the zone of junction a thinner area (Fig. 
68 D), and beyond this again the several layers of cells even 
more laden with yolk-spheres and granules than previously; so 
that it would appear that these cells may actively engulf yolk- 
granules. At the margin of the vascular area the entoderm be- 
comes one-layered, and is composed of columnar cells with swollen 
free margins turned towards the yolk and still containing some 
yolk-granules and spheres (Fig. 68 C). At the margin of the 
pellucid area there is a rather sudden transition to the flat ento- 
dermal epithelium characteristic of this area. 


CHAPTER VI 


FROM TWELVE TO THIRTY-SIX SOMITES. THIRTY- 
FOUR TO SEVENTY-TWO HOURS 


I. DEVELOPMENT OF THE EXTERNAL FORM, AND TURNING OF 
THE EMBRYO 


In the embryo of twelve somites only the head is distinctly 
separated from the blastoderm; and there is no sharp boundary 
between the embryonic and extra-embryonic portions of the 
blastoderm in the region of the trunk; but this changes very 
rapidly. The progress of the developmental processes, that have 
marked out an embryonic axis in the blastoderm, produces in 
the course of about eighteen hours a sharp distinction everywhere 
between embryo and extra-embryonic blastoderm. The latter, 
together with an outgrowth of the embryonic hind-gut (allantois), 
then constitute the so-called embryonic membranes, which become 
very complicated, and which provide for the protection, respira- 
tion, and nutrition of the embryo. We shall consider the forma- 
tion of the embryonic membranes separately in order not to 
confuse the account of the development of the external form of 
the embryo. 

In considering the development of the external form of the 
embryo, we must distinguish between those processes that sepa- 
rate it from the extra-embryonic blastoderm, and those that occur 
within its own substance leading to various characteristic bend- 
ings and flexures; we may consider them separately, although 
they are going on at the same time. 

Separation of the Embryo from the Blastoderm. ‘The separa- 
tion of the embryo from the blastoderm takes place by the 
formation of certain folds or sulci that may be named: (1) the 
head-fold or anterior limiting sulcus; (2) the lateral limiting sulci, 
appearing as prolongations of the head-fold along the sides of the 
embryonic axis; and (3) the tail-fold or posterior limiting sulcus. 

The head-fold has been described in detail in the preceding 

130 


FROM TWELVE TO THIRTY-SIX SOMITES 131 


chapter. The lateral limiting sulci are a continuation of the 
lateral limbs of the head-fold; they owe their origin to the folding 
of the splanchnopleure and somatopleure adjacent to the embryo 
towards the yolk, at the line of junction of embryonic and extra- 
embryonic parts. The tail-fold arises about the stage of 26 to 
27 somites (Fig. 93), and is similar to the head-fold, except that 
it is turned in the opposite direction. The sulci combine to form 
a continuous ring around the embryo and gradually pinch it off, 
so to speak, from the extra-embryonic blastoderm. 

In the splanchnopleure the limiting sulci (Fig. 69) come to- 


Fic. 69. — Transverse section through the fifth somite of the 23 s stage. 

Amn., Amnion. <Ao., Aorta. a. i. p., Anterior intestinal portal. Coel., 
Coelome. Chor., Chorion. Ectam., Ectamnion. E. E. B. C., Extra-embry- 
onic body-cavity. Int., Intestine. 1. 1. s., Lateral limiting sulcus. My., 
Myotome.  s. a., Segmental artery. So’pl., Somatopleure. Spl’pl., Splanch- 
nopleure. s., Somite. s. 5, Fifth somite. V.O.M. R. and L., Right and left 
omphalo-mesenteric veins. V. V., Vitelline vein. 


gether and fuse both in a caudal direction from the fore-gut, and 
subsequently in a cephalic direction from the hind-gut (see below), 
so as to convert the splanchnic gutter into a tube (the alimentary 
canal). There is thus a ventral suture along the alimentary 
canal in which the entoderm of the alimentary canal becomes 
separated from the extra-embryonic entoderm, thus leaving a 
double layer of the splanchnic mesoblast (ventral mesentery) 
connecting the alimentary canal with the extra-embryonic splanch- 
nopleure; but this disappears everywhere as soon as formed, 
except in the region of the posterior part of the heart and the 
liver where it forms the dorsal mesocardium and gastro-hepatic 
ligament (Fig. 118), and in the region of the neck of the allantois. 


132 THE DEVELOPMENT OF THE CHICK 


The fore-gut is thus being continually lengthened backwards 
by fusion of the lateral limbs of the splanchnopleure. At the 
31s stage this has proceeded about to the fourteenth somite. 
At about the 26 s stage the tail-fold appears in the splanchno- 
pleure, thus establishing the hind-gut (Fig. 70) which gradually 


Ect. 


LAS 


SEO o 
© 


Fig. 70. — Median longitudinal section through the hind end of an embryo 
of about 21 s. 
an. pl., Anal plate. an. t., Anal tube. _ p. i. p., Posterior intestinal portal. 
T. B., Tail-bud.  t.f. So’pl., Tail fold in the Somatopleure.  t. f. Sp’pl., Tail 
fold in the splanchnopleure. Other abbreviations as before. 


elongates forwards. There remains then an open portion of the 
alimentary tract, where its walls are continuous with the extra- 
embryonic splanchnopleure or yolk-sac. This is known as the 
yolk-stalk. The entrance from the yolk-sac into the fore-gut 
is known as the anterior intestinal portal, and that from the 
volk-sae into the hind-gut as the posterior intestinal portal (Fig. 
70). At the 27s stage the yvolk-stalk is long and narrow (Fig. 
106); the stems of the splanchnic (omphalo-mesenteric) veins run 
to the heart in its anterior portion, and the omphalo-mesenteric 
arteries pass out about its center. As it gradually closes, the 
stems of the omphalo-mesenteric arteries and veins are brought 
closer together. At about five days it becomes a tubular, thick- 
walled stalk, connecting intestine and yolk-sac, and so remains 
throughout embryonic life. 

The limiting sulci in the somatopleure lead to the formation 
of the body-wall. In the trunk the somatopleure is separated 
from the splanchnopleure by the ccelome (Fig. 69), and the folds 
in the somatopleure take the same general direction as those in 
the splanchnopleure; they thus lead to the formation of a tube 
(body-wall) outside of a tube (alimentary canal), the intervening 


FROM TWELVE TO THIRTY-SIX SOMITES 133 


cavity being the body-cavity. The unclosed part of the body- 
wall is continuous with the extra-embryonic somatopleure, more 
specifically the amnion (see below), and this connection is known 
as the somatic stalk or umbilicus. The yolk-stalk and neck of the 
allantois pass out of the body-cavity through the somatic stalk, 
which therefore remains open until near the end of incubation. 

The Turning of the Embryo and the Embryonic Flexures. 
We have described the separation of the embryo from the extra- 
embryonic blastoderm without reference to its turning from a 
prone to a lateral position or to the formation of the flexures 
of the entire head and body that are so characteristic of amniote 
embryos generally. These changes begin about the 14s stage 
and are first indicated by a slight transverse bending of the origi- 
nally straight axis of the head in the region of the mid-brain 
(Fig. 67). By means of this bending, known as the cranial flex- 
ure, the fore-brain is directed toward the yolk; but almost simul- 
taneously another tendency manifests itself, viz., rotation of the 
head on its side, at first affecting only the extreme end. (See 
Figs. 71, 73, 99, etc.) By the 27s stage these two processes 
have resulted in the conditions shown in Fig. 105: by the cranial 
flexure the fore-brain is bent at right angles to the axis of the 
embryo, and owing to the rotation the head of the embryo lies 
on its left side. But inasmuch as the trunk is still prone on the 
surface of the yolk the axis of the embryo is twisted in the inter- 
mediate region. This twist is transferred farther and farther 
backwards as the turning of the head gradually involves the 
trunk, until finally, at about ninety-six hours, the embryo lies 
entirely on its left side. 

Exceptionally the rotation may be in the inverse direction 
(heterotaxia); in such cases it is often associated with situs in- 
versus viscerum. Heterotaxia has been produced experimentally 
(Fol and Warynsky). 

After the appearance of the cranial flexure a second trans- 
verse flexure appears in the embryo, this time at about the 
junction of head and trunk, hence known as the cervical flexure 
(Figs. 73, 99, etc.). This flexure gradually increases in extent 
until the head forms a right, or even smaller, angle with the 
trunk; thus the fore-brain is turned to such an extent that its 
anterior end points backwards and its ventral surface is opposed 
to the ventral surface of the throat (Fig. 117). 


134 THE DEVELOPMENT OF THE CHICK 


Pr. str-——_ ——— 


Fig. 71.— Entire embryo of 16s, drawn 
from above as a transparent object. Note 
the cranial flexure, also the rotation of the 
head on its left side. 

au. P., Auditory pit. F. B., Fore-brain. 

H. B. 1, First division of the hind brain. 

H.F. Am., Head-fold of theamnion. Hm.F., 

Hyomandibular furrow.  Pr’am., Proam- 

nion. M. B., Mid-brain. op. Ves., Optic 

vesicle. pr. str., Primitive streak. s 2, s 4, 

s 16, Second, fourth, and sixteenth somites. 

V.o.m., omphalo-mesenteric vein. VII-VIII, 

The acustico-facialis primordium. IX—X, 

Primordium of the glossopharyngeus and 

vagus. 


The entire trunk tends also to bend ventrally, 7.e., to develop 
a dorsal convexity, and this approximates its posterior end to the 
tip of the head. These flexures are characteristic of amniote 


FROM TWELVE TO THIRTY-SIX SOMITES 135 


vertebrate embryos; the cause appears to lie in the precocious 
development of the central nervous system, of which more here- 
after. Only the cranial flexure remains as a permanent con- 
dition. 

II. OrIGIN OF THE EMBRYONIC MEMBRANES 


The period from about 12 to 36 somites also includes the early 
history of the embryonic membranes, amnion, chorion, yolk-sac 
and allantois. The first three arise from the extra-embryonic 
blastoderm, and the allantois arises as an outgrowth of the ven- 
tral wall of the hind-gut. 


OL. 


Fic. 72. — The head of the same embryo from 
below. 


a. i. p., Anterior intestinal portal.  B. a., 
Bulbus arteriosus. Inf., Infundibulum. or. pl., 
Oral plate. Tr. a., Truncus arteriosus. 
Ven., Ventricle. v. Ao., Ventral aorta. 


Origin of the Amnion and Chorion. The amnion is a thin 
membranous sac, forming a complete investment for the embryo 
and continuous with the body-wall at the umbilicus; it lies beneath 
the chorion to which it remains attached throughout incubation 
by a plate of tissue (sero-amniotie connection), and it arises in 
common with the chorion from the extra-embryonic somatopleure. 
The entire somatopleure external to the embryo is used up in 
the formation of these two membranes. The amnion arises from 
a portion immediately adjoining the embryo itself; the remainder 
of the somatopleure peripheral to the amniogenous part forms 
the chorion. Thus the extra-embryonic somatopleure may be 
divided into two zones; an ammniogenous zone immediately adja- 


156 THE DEVELOPMENT OF THE CHICK 


pienc. 
Mesenc.  / Waren 


— 


Sy Zelenc 


FL = 
Metenc. f= —Op. Ves. 
Myelenc./ 
au. P ae Ni Ph. 
Myelenc.2.“* DiC. 
5.2.- 4 


\ 


Pr str <=" 


Fic. 73. — Entire embryo of 20s, viewed 
as a transparent object from above. 
The cranial flexure and the rotation of 
the head of the embryo have made 
considerable progress. 

A. o. m., Omphalo-mesenteric artery. 
Cr. FL, Cranial flexure. D.C., Duct of 
Cuvier. Diene., Diencephalon. Mesenc., 
Mesencephalon. Metene., Metencepha- 
lon. Myelene. 1, and 2, Anterior and 
posterior divisions of the myelencepha- 
lon. Telene., Telencephalon. Vel. tr., 
Velum transversum. Other abbrevia- 
tions as before. x 30. 


cent to and surrounding the embryo, and a choriogenous zone, 
comprising the remainder. 
The method of formation of amnion and chorion is as follows: 


“FROM TWELVE TO THIRTY-SIX SOMITES 137 


(a diagrammatic outline is first given and a detailed description 
follows). The somatopleure becomes elevated in the form of 
a fold surrounding the embryo; this fold begins first in front of 
the head of the embryo as the head-fold of the amnion, which 


Fic. 74. — Head of the same embryo 
from the ventral side. Abbreviations 
as before. 


Fic. 75. — Median sagittal section of the head of an embryo of 18 s. 

H. F. Am., Head-fold of the amnion. Ph., Pharynx. Isth., Region of 
the isthmus, pr’o. g., Preoral gut. or. pl., Oral plate. Rec. opt., Recessus 
opticus. S. v., Sinus venosus. Other abbreviations as before. 


immediately turns backwards over the head, forming a complete 
cap (Figs. 67, 71, 75, ete.); the side limbs of the head-fold are 
then elongated backwards, and are here known as the lateral 


folds of the amnion; these rise up and arch over the embryo 


138 THE DEVELOPMENT OF THE CHICK 


(Figs. 109 and 110). In each fold one can distinguish an amniotic 
or internal limb, and a chorionic or external limb meeting at or 
near the angle of the folds, the line of junction being marked 
by an ectodermal thickening, the ectamnion. Fusion of the 
right and left lateral folds begins at the head-cap, and progresses 
backwards in such a way that the right and left amniotic limbs 
become continuous with one another, similarly the right and 
left chorionic limbs; and, when fusion is complete, the amnion 
and chorion become separate continuous membranes. In this 
way the amnion extends, by the 27 s stage, back to the seventeenth 
somite (Fig. 105). At this time a new fold arises behind the 
rudimentary tail-bud and covers the tail precisely as the head- 
fold covers the head (Fig. 105); the tail-fold of the amnion then 
apparently is prolonged forward a short distance and soon meets 
the anterior lateral folds, forming a continuous lateral fold. Fu- 
sion continues until, about the 31s stage, the opening into the am- 
niotic cavity is reduced to a small elliptical aperture lying above 
the buds of the hind-limbs (Fig. 99). This then rapidly closes, 
but a connection, sero-amniotic connection, remains at the place 
of final closure. Elsewhere the separation of chorion and amnion 
is complete. 

The formation of the amnion is an extremely interesting 
process from the standpoint of developmental mechanics, and 
involves a number of details that are best understood after such 
a general review of the process as has been given in the preceding 
paragraphs. Returning then to the 12s stage for consideration 
of these details, we must first note that the extension of the meso- 
blast prior to this period has left an area situated in front of 
the head free from mesoblast (Figs. 65, 67, 71, 75, ete.). This 
area, in which the ectoderm and entoderm are in contact, is 
known as the proamnion. The formation of the amnion begins 
within this area by a thickening in the ectoderm (ectamnion) 
near the anterior boundary of the proamnion at a stage with 
about eight or nine somites. The thickening, which is very 
narrow, extends right and left, and turns backwards along the 
sides of the head to about the region of the middle of the heart, 
gradually becoming more peripheral in position and fading out 
(Fig. 76). It represents the junction of the amniogenous and 
choriogenous somatopleure and thus corresponds to the angle 
of the future amniotic folds. The head of the embryo lies in a 


FROM TWELVE TO THIRTY-SIX SOMITES 139 


depression bounded in front by the ectamnion, and on the sides 
by the amnio-cardiac vesicles of the body-cavity (Fig. 65). The 
floor of the depression is the proamnion. Just before the for- 
mation of the head-fold proper, the ectamnion in front of the 
head becomes irregularly thickened to 
such an extent as sometimes to present 
an actually villous surface (Fig. 77; cf. 
Fig. 67). 

The head-fold of the amnion begins 
to form at about the same time as the 
cephalic flexure. The great expansion 
of the body-cavity on each side of the 
head (amnio-cardiac vesicles) causes an 
elevation of the anterior angle of the 
ectamnion, and a pocket is formed by 
fusion of its lateral limbs. This slips 
over the head of the embryo with aid 
of the ventral flexure of the head just 
developing. Inasmuch as the anterior 
angle of the ectamnion is in the pro- 
amnion, where there is no mesoderm, 
and where the ectoderm is in immediate | 
contact with the entoderm, the ento- s 
derm as well as the ectoderm of the pro- Fic. 76.— Entire embryo 
amnion is drawn into the head-fold, so of 15s, to show the rela- 
that the latter is not at first a fold’ of  “0?sOtthe ectamnion- 

; ; a. ¢., Inner margin of 
the-somatopleure. But im. the chick the. amacenrdinc vesicles: 
proamniotic part of the head-fold is & ae eae ae 
never very extensive and does not at any topleure destined to form 
time extend back of the beginning of the body-wall. 

: : She: ae: B. Amniogenous soma- 
the mid-brain. Moreover, it is soon in-  topleure. 
vaded (Fig. 75) by the body-cavity, and C. Choriogenous soma- 

. i ae ‘ topleure. 

then the entoderm is withdrawn and 
becomes part of the general splanchnopleure. The proamnion 
ventral to the head is not invaded by mesoderm until a much 
later period. 

The ectodermal thickening marking the junction of amniotic 
and chorionic somatopleure extends backwards very rapidly and 


~— 


always precedes the origin of folds in any region. The lateral 
folds themselves appear to owe their origin to the progressive 


140 THE DEVELOPMENT OF THE CHICK 


fusion of the ectodermal thickenings of the opposite sides, 
beginning at the posterior angle of the head-fold and proceeding 
backwards. The energy of fusion is sufficient in itself to lift the 
somatopleure up in the form of a fold around the body of the 
embryo. Thus new parts of the ectodermal thickening are con- 
stantly being brought together and the fusion progresses steadily, 
and this in its turn prolongs the lateral amniotic folds. These 
possess no independent power of elevation of any considerable 
amount, for, when the initial fold of one side is destroyed by 
cauterization, the fold of the opposite side remains as an insig- 
nificant elevation in the somatopleure a long distance lateral to 
the embryo. 


ia. 77. — Transverse section through the anterior angle of 
the ectamnion a few sections in front of the tip of the head. 
Stage of 14-15 s. 
b. e., Extra-embryonie body-cavity. c¢., Cavity in the 
entoderm. e. a., Eetamnion. 


The tail-fold arises in an analogous manner to the head-fold, 
except that there is no proamnion here. The progress of the 
various folds and their final fusion follows from what has already 
been said. 

Practically all of the somatopleure of the pellucid area is 
amniogenous with the exception, naturally, of that part internal 
to the limiting sulei that forms the body-wall. What effect has 
the turning of the embryo on its left side on the amniogenous 
somatopleure? We will suppose that the latter is primitivelv 
of equal width on both sides and that the notochord represents 
approximately the axis of rotation. During the process of rota- 
tion, the embryo sinks and the lateral limiting sulci become deeper. 
A direct consequence of the rotation must be, therefore, a strong 
tension on the somatopleure belonging to the under (left) side, 
a—b, and practically none on the upper (right) side, c-d. (See 
Fig. 78 A, B). 


FROM TWELVE TO THIRTY-SIX SOMITES 141 


Even though the difference may be partly compensated by 
drawing of the embryo to the left, the tendency would be to 
stretch a—b. If there were no such compensation and a and b 
were practically fixed points, the length of a—b at the conclusion 
of the rotation would much exceed that of c-d (Fig. 78 B), and 


Fia 78. A, B, and C. Diagrams to represent the effect of 
rotation of the embryo on the amniogenous somatopleure. 
a represents in all figures the position of the ectamnion on 
the left (lower) side; d represents in all figures the position 
of the ectamnion on the right (upper) side. 6 and c¢ repre- 
sent the junction of amnion and body-wall on left and right 
sides respectively. In Fig. A, a-b and c-d are equal. In 
Fig. B, rotation of the embryo is assumed to have taken 
place without formation of the amnion; the distance a—b has 
become greater than c-d. In Fig. C is represented rotation 
of the embryo with synchronous formation of the amniotic 
folds, as is actually the case; c-d is inevitably thrown into 
secondary folds. The vertical lines at the extreme right 
and left represent the margins of the pellucid area. 


if, during this process, there were actual independent growth 
of a-b and c-d, the latter would of necessity be thrown into folds, 
but not the former. Finally, if the amniotie folds were forming 
at the same time (as is actually the case), the right one would 


142 THE DEVELOPMENT OF THE CHICK 


inevitably be thrown into secondary folds by the approximation 
of points ¢ and d (Fig. 78 ©). 

Study of the fusion of the amniotic folds in actual sections 
shows, that the line of fusion of the opposite amniotic limbs is 
over the dorsal surface of the embryo only so long as the latter 
lies flat on the yolk; it does not follow the turning of the embryo 
on to its left side, and the consequence is that, after rotation of 
the embryo, the line of fusion lies over the upper (right) side of 
the embryo, often opposite the horizontal level of the intestine 
(Fig. 79). Thus one fold of the amnion passes all the way from 
the under side over the back of the embryo and around on the 
other side to the line of fusion, and thus is several times as long 
as the opposite limb. Moreover, the amniotic fold of the right 


Fia. 79. 
ondary fold (s. f.) of the amnion on the right side. 
e. a., Eetamnion.  s. f., Secondary fold. 1., Left. r., Right. 


Section of an embryo of about 60 hours to show the sec- 


side is invariably thicker than that of the left side, and is always 
thrown into secondary folds at the place of turning (lig. 79). 
These conditions are satisfactorily explained, as noted above, by 
the mere turning of the embryo on its side. 

One must therefore distinguish in the upper limb of the am- 
nion two kinds of folds: (1) The ordinary amniotic fold induced 
by the fusion of the right and left folds, and (2) secondary folds 
formed simply by the process of twisting of the embryo. 

These secondary folds of the amnion are very transitory, 
except in two regions: (1) Above the hind end of the heart (apex 
of ventricle), and continuing a short distance behind it; (2) in 
the region immediately in front of the allantois, at sixty to seventy 
hours, thus in the neighborhood of the final closure of the amniotic 


FROM TWELVE TO THIRTY-SIX SOMITES 143 


folds. The former are of very constant occurrence and _ persist 
a long time (Fig. 93). 

Elsewhere the effect of the twisting of the embryo is rapidly 
compensated so that the secondary folds of the right half of the 
amnion do not persist long. 

The subsequent history of the amnion and chorion is given 
in another place. It should be noted here that the chorion, at 
the stage of seventy-two hours, is continuous peripherally with 
the splanchnopleure at the margin of the vascular area, and that 
it becomes separate from it only as the body-cavity extends 
more and more peripherally. The sero-amniotic connection 
remains throughout the entire embryonic period and modifies in 
an important fashion the subsequent history of the membranes. 

The yolk-sac is the name given to the extra-embryonic 
splanchnopleure, because in the course of expansion of the blasto- 
derm and extension of the extra-embryonic body-cavity over the 
surface of the yolk, it finally becomes a separate sac enclosing 
the yolk. It remains connected by the yolk-stalk with the intes- 
tine until finally, some time after hatching, it is absorbed com- 
pletely. The yolk is absorbed by the entodermal lining and is 
carried to the embryo in solution by means of the vitelline veins. 

Origin of the Allantois. The allantois arises as a diverticulum 
of the hind-gut soon after the formation of the latter by the tail- 
fold. It is not indicated before the formation of the tail-fold as 
stated by some authors, but the tube identified by them as the 
primordium of the allantois at this early stage is really the in- 
testinal diverticulum leading to the anal plate (Fig. 70). At the 
stage of twenty-eight somites the allantois is indicated by the 
depth of the hind-gut, the ventral portion of which in front of 
the anal plate soon becomes constricted from the upper portion, 
and forms the primordium of the allantois. In longitudinal sec- 
tions of an embryo of about thirty-five somites it can be seen to 
include nearly the entire floor of the hind-gut between the anal 
plate and the posterior intestinal portal (Fig. 80). It is lined 
with entoderm and has a thick mesodermal floor in which numer- 
ous small blood-vessels are already present. A transverse section 
(Fig. 81) shows that the thick mesodermal wall is broadly fused 
with the somatopleure in the region of the neck. In other 
words, the allantois is developed within the ventral mesentery. 
It will also be seen by comparing these figures that the amnion 


144 THE DEVELOPMENT OF THE CHICK 


arises from the neck of the allantois both behind and also at the 
sides. (cf. Fig. 82.) 

During the fourth day the distal portion of the allantois 
pushes out into the portion of the extra-embryonic body-cavity 
beneath the hind end of the embryo and rapidly expands to form 
a relatively large sac. But the neck of the allantois remains 
embedded in the ventral mesentery and does not expand; the 
terminal portion of the intestine has in the meantime formed 


Am. Amesy. Ect. 


ie 2 


eel } 
av 


£etam. 
Mesam. 
Fic. 80. — Sagittal section through the tail of an embryo of about 35 s. 


All., Allantois. An. pl., Anal plate. ¢. C., Central canal of the neural 
tube. Cl, Cloaca. Ectam., Eetoderm of the amnion. Mesam., Mesoderm 
of the amnion. _p’a. G., Post-anal gut. p. i. p., Posterior intestinal portal. 
s. A., Segmental arteries. Other abbreviations as before. 


the primordium of the cloaca, from which, therefore, the neck of 
the allantois appears to arise (Fig. 183); at all stages of incuba- 
tion the neck of the allantois forms an open connection between 
the cloaca and the allantoic sac. 

The Umbilicus. The closure of the body-wall progressively 
reduces the communication between the embryonic and extra- 
embryonic body-cavity to a narrow chink between the yolk-stalk 


FROM TWELVE TO THIRTY-SIX SOMITES 145 


and allantoic stalk on the one hand and the attachment of the 
amnion on the other. The umbilical cord thus consists of an 
outer tube continuous with the body-wall, enclosing the yolk- 
stalk and the stalk of the allantois, together with the arteries 
and veins of yolk-sac and allantois. It is important to bear in 
mind that in the region of the neck of the allantois the amnion 
is attached to the latter at the sides and behind; only the anterior 
wall of the allantoic stalk is free (Fig. 82). In other words, the 
somatic umbilical stalk is fused with the lateral and caudal wall 
of the neck of the allantois, a relation that is common to all 
amniota. 


Fic. 81. — Transverse section through the hind-gut and allantois of an em- 
bryo of 35s; the section passes through the thirtieth somite. Details 
diagrammatic. 

All., Allantois. H. G., Hind-gut. L. B., Leg bud. v. M., Ventral 
mesentery. W. D., Wolffian duct. Other abbreviations as before. 


Summary of Later History of the Embryonic Membranes. 
The full history of the embryonic membranes will be given later 
(Chap. VII), but it seems desirable to give an outline here in order 
to avoid repeated recurrence to this subject. The extension of 
the body-cavity in the blastoderm is at first very rapid, but about 
the fifth day it becomes slow, and the yolk-sac is never com- 
pletely separated from the chorion. The allantois extends out 
into the extra-embryonic body-cavity as a small pear-shaped 
vesicle by the end of the fourth day. It then enlarges very 
rapidly and extends in the form of a flattened sac over and around 
the embryo immediately beneath the chorion with which it forms 


146 THE DEVELOPMENT OF THE CHICK 


an inseparable union. As the extra-embryonic body-cavity 
extends, the allantois continues its expansion between the chorion 
and the yolk-sac, and finally wraps itself together with a duplica- 
tion of the chorion, completely around the albumen of the egg, 
which has become very viscid, and aggregated in a lump opposite 
to the embryo. The allantois is very vascular from the start, 
and serves as an embryonic organ of respiration. It also receives 
the excretion of the embryonic kidneys and absorbs the albumen. 


Fig. 82. — Model of the caudal end of a four-day chick 


to show the relations of the amnion to the allantois 
and umbilicus. (After Ravn.) 


All., Neck of the Allantois. Am., cut surface of 
the amnion. <A. 0. m., Omphalo-mesenteric artery. 
an. pl., Anal plate. L. B., cut surface of leg bud. 
ey vail, 


The yolk-sac becomes much shriveled during incubation owing 
to absorption of its contents, and on the last day of incubation 
is withdrawn into the body-cavity through the umbilicus, which 
finally closes. The chorion, amnion, and allantois shrivel up 
when the chick begins to breathe air, and are cast off with the 
shell at hatching. 


FROM TWELVE TO THIRTY-SIX SOMITES 147 


Ill. THE Nervous SystEmM 

The Brain. The description of the nervous system in the pre- 
ceding chapter forms our starting-point. During the period now 
under consideration the foundation of the main parts of the adult 
brain are laid down, and its five chief divisions become sharply 
characterized. It is important to correlate these with the earliest 
morphological characters (original anterior end of medullary 
plate, neuromeres, etc.) in order to trace these fundamental 
landmarks through to definitive structures. 

As we have already seen, the primary fore-brain includes the 
first three neuromeres, the mid-brain the fourth and fifth, and 
the hind-brain the sixth to the eleventh, as well as the region 
opposite to the first four mesoblastic somites. It is clear that a 
second point of fundamental morphological significance is the 
original anterior end of the medullary plate which would naturally 
form the center for a description of the anterior part of the neural 
axis, if recognizable throughout the development. This point 
may be recognized for a considerable period after the closure of 
the anterior part of the neural tube, as the ventral end of the 
anterior cerebral fissure (ig. 62), opposite the center of the 
primary optic vesicles, thus in the region of the recessus opticus 
(Figs. 87 and 88), which is to be regarded as marking the original 
anterior end of the neural axis. Even after closure of the anterior 
cerebral fissure a connection remains at its dorsal end between 
the ectoderm and the neural tube. To this we may apply the 
name neuropore, though no actual opening is found here at this 
time. The median stretch of tissue between the recessus opticus 
and the neuropore constitutes the lamina terminalis which remains 
as the permanent anterior wall of the neural tube. It must not 
be forgotten that the original anterior end of the medullary plate 
lies at the ventral end of the lamina terminalis, 7.e., in the re- 
cessus opticus. <A third landmark of fundamental morphogenic 
significance is the infundibulum, which coincides in position, as 
we have seen, with the anterior end of the notochord. Thus we 
may distinguish prechordal and suprachordal portions of the neu- 
ral axis (cf. Fig. 67). 

Dorsal and Ventral Zones in the Wall of the Brain. The con- 
ception of His, that the walls of the neural tube may be consid- 
ered as formed of four longitudinal strips, viz., floor, roof, and 


148 THE DEVELOPMENT OF THE CHICK 


Fig. 83. — Five stages in the history of the neuromeres of the brain of the 
chick. (After Hill.) All figures drawn from preparations of the embryonic 
brain dissected out of the embryo. 


A. Neural groove in an embryo with 4 somites. Right profile view. x 44. 

B. Brain of a 7s embryo, 26 hours old. Dorsal view; the three anterior 
neuromeres are practically obliterated. x 44. 

C. Brain of 14s embryo. Dorsal view. x 44. The neuromeres have 
now disappeared in the mid-brain region. 

D. Right side of the brain of a chick embryo, 47 hours old. x 44. 

Ki. Right side of the brain of an embryo, 80 hours old. x 17. 

1-11, Neuromeres 1 to 11. III, V, VII, interneuromeric grooves. A't., 
toot of acustico-facialis (seventh and eighth cranial nerves). au. vs., Audi- 
tory pit. ep., Epiphysis. r., Groove between the tel- and diencephalon. 
s., Groove between the par- and synencephalon. Tr., Root of trigeminus. 


FROM TWELVE ‘TO THIRTY-SIX SOMITES 149 


two lateral walls, is a useful one. Each lateral wall may also 
be divided into a dorsal and ventral zone, the former of which 
is related to the sensory nerve roots and the latter to the motor. 

Cerebral Flexures. The cerebral flexures correspond to the 
cranial and cervical flexures of the entire head already described. 
Their form and rate of progress may be more readily learned 
from the figures (Figs. 67, 73, 83, etc.) than from any verbal 
description. Only the cranial flexure is permanent, and the angle 
thus formed ventrally in the floor of the mid-brain is known as 
the plica encephali ventralis. A third flexure is formed later in 
the anterior portion of the hind-brain, by a ventral bending of 
the floor which is barely indicated in the period now under de- 
scription, but becomes much more pronounced later; this is known 
as the pontine flexure. 

We may now take up separately the changes in each of the 
primary cerebral vesicles. 

The Prosencephalon. The principal events in the early de- 
velopment of the prosencephalon are: (a) the separation of the 
optic vesicles; (b) the delimitation of the tel- and diencephalon; 
(c) special differentiation of the walls. 

(a) A section across the optic vesicles of the 12s chick shows 
the prosencephalon as a central division with its cavity widely 
confluent with the cavities of the optic vesicles. This wide com- 
munication is rapidly narrowed by a ventrally directed fold of the 
roof at the line of junction of the optic vesicles and prosencephalon 
proper (Fig. 84); the fold also involves to a certain extent the 
anterior and posterior line of junction. In the 20s embryo the 
connection of the optic vesicles and prosencephalon has been re- 
duced in this way to about one third of its original diameter 
(from actual measurements), forming a narrow tubular stalk, the 
optic stalk, attached to the ventral portion of the fore-brain 
(Figs. 73 and 74); the cavities of the optic vesicles are still con- 
tinuous through the stalk with the cavity of the prosencephalon, 
dipping into the recessus opticus; the ventral wall of the optic 
stalk thus becomes continuous with the floor, and the dorsal wall 
with the lateral wall of the prosencephalon (Fig. 84). Growth 
of the mesenchyme situated above the original optic stalk appears 
to be an active factor in the separation; at least it grows at a 
rate sufficient to fill in the space produced by the constriction. 
At the same time there is a slight increase in the dorso-ventral 


150 THE DEVELOPMENT OF THE CHICK 


diameter of the fore-brain itself, though this is relatively slight 
up to twenty somites, but it enhances the general effect of the 
change in position of the optic stalk. The subsequent history 
of the optic vesicles is given beyond. 

(b) The delimitation of the tel- and diencephalon is initiated 
by a forward expansion of the anterior end of the primary fore- 
brain, which becomes the telencephalon or secondary fore-brain, 
the remainder being then known as the diencephalon or ’tween 
brain. The expansion proceeds very rapidly from the 145 stage, 
and it is probable that it involves only the dorsal zones. It is, 


L£elam 


4 ee omg / 


e3e2: ea a 


2G) 
Pa 


250995 


Ae 
see 


E 


Fia. 84. — Transverse section through the fore-brain and optic vesicles of a 
16-s embryo. 
Am. F., Amniotie fold. Ectam., Ectamnion. L., Left side. op.st., 
Optic stalk. R., Right side. Other abbreviations as before. 


however, difficult to establish an exact line of demarcation be- 
tween the two subdivisions of the primary fore-brain, until about 
the 18 to 20s stage, when a slight transverse fold or indentation 
in the roof (velum transversum) gives a dorsal landmark (Figs. 
73, 85); the recessus opticus forms the ventral boundary between 
the two. The velum transversum lies a considerable distance 
above the dorsal end of the lamina terminalis, but it is difficult 
to say just how far, owing to the indefiniteness of this point for 
some time after the disappearance of the neuropore. <A line 
drawn between the velum transversum and the recessus opticus 
may be taken as the boundary between the two divisions of the 


FROM TWELVE TO THIRTY-SIX SOMITES 1ot 
primary fore-brain; but, owing to the simultaneous lateral expan- 
sion of the telencephalon, the line of separation in the lateral 
walls forms a curve with the convexity directed posteriorly 
(Figs. 83 E and 86). 

(c) The next stage in the differentiation of the telencephalon 
(20 s to 36s) is characterized by a rapid expansion and evagina- 
tion of its lateral walls, while the entire median strip extending 
from the velum transversum to the recessus opticus remains prac- 


Fic. 85. — Optical sagittal section of the head of an embryo of 22-23 s. 
The heart is represented entire. 


Atr., Atrium. Hyp., Hypophysis. Inf., Infundibulum. Md., Man- 
dibular arch. or. pl., Oral plate.  Pr’o. G., Preoral gut. Th., First in- 
dication of thyroid. T. p., Tuberculum  posterius. V. tr., Velum 
transversum. Other abbreviations as before 


tically unaltered; and thus 
the surface between these 
form a pair of outgrowths 
anteriorly, and posteriorly 


acts like a rigid band stretched over 
two points. The effect of this is to 
that soon begin to project dorsally, 
(Fig. 83 E); these are the primordia 


of the cerebral hemispheres, the cavities of which thus appear 
as lateral diverticula of the median cavity of the telencephalon 
(Fig. 86). The central part of the telencephalon may be called 
the telencephalon medium, and the lateral outgrowths the hemi- 
spheres. The walls of the hemispheres become considerably 
thicker in this period, but quite uniformly at first, so that the 
distinetion between mantle and basal ganglia is indicated only 


(See Chap. VIII.) 


by position. 


152 THE DEVELOPMENT OF THE CHICK 


The median strip includes the tela choroidea, beginning at 
the diencephalon, and the lamina terminalis, which ends at the 
recessus opticus. These divisions are of great prospective signifi- 
‘ance, though at the stage of 36s they are but slightly differen- 
tiated, save by their position. A slight thickening of the lamina 
terminalis just in front of the recessus opticus marks the site of 
the future anterior commissure (Figs. 87 and 88). 


a / He Metene. 
th 


MeSCNC — ieee | / \ Myelenc 


. — ™ , > 
—— ~/ ene V .: » 


a = 
= te 
x - 


Jil SS 


7 Ch opt. 


Dienc. -jaees 


7 Frec ofl 


| 


jf 
Fig. 86. — Inner view of the brain of a chick of about 82 hours, drawn from 


a dissection. 

Ch. opt., Chiasma opticus. Ep., Epiphysis (pineal gland). Isth., Isth- 
mus. Pl.enec. v., Plica encephali ventralis. Ree. opt., Recessus opticus. 
V. tr., Velum Transversum. Other abbreviations as before. 


The Diencephalon. The portion of the primary fore-brain pos- 
terior to the telencephalon is known as the diencephalon. — It in- 
cludes the second and third neuromeres and probably also the 
ventral zones and floor of the first (Fig. 83). A slight constriction 
in the roof that appears about the 18 to 20s stage near the Junc- 
tion of the middle and last third may represent the boundary be- 
tween the second and third neuromeres; this persists for a long 
time and may be traced in the lateral walls to the region of the 


FROM TWELVE TO THIRTY-SIX SOMITES 158 


infundibulum (Fig. 83 E); thus the diencephalon may be divided 
into an anterior and posterior division, parencephalon and synen- 
cephalon (Kupffer) (Fig. 87). The optic stalks are attached to 
the floor and ventral zones at the extreme anterior end. The 
diencephalon includes part of the roof, floor, and dorsal and ven- 
tral lateral zones of the original neural tube. These may be de- 
scribed as follows (Figs. 87 and 88): 


Myelenc. 


MeESENC. 


— Zp. 


7 Symenc 


FParerne 


Fig. 87. — Optical longitudinal section of the head of an embryo of 30s. 

The heart is represented entire. 

Atr., Atrium (auricles). B.a., Bulbus arteriosus. D. v., Ductus venosus. 
Lg., Laryngo-tracheal groove. Oeces., Oesophagus. or. pl., Oral plate, which 
has begun to rupture. Parenc., Parencephalon. Ph., Pharynx. Stom., 
Stomach. Synene., Synencephalon. Th., Thyroid. 8S. v., Sinus venosus. 
Ven. R., Right ventricle. Other abbreviations as before. 


The roof rises quite sharply from the velum transversum, and 
is indented between the parencephalic and synencephalic divi- 
sions as already noticed. It is relatively thin. About the 30- 
35s stage the epiphysis (pineal body) begins to form as an 
evagination from about the middle, and by the 36s stage is a 
small hemispherical protuberance (Figs. 86 and 88). The floor 
becomes extremely thin in the center of the recessus opticus, which 
marks its anterior end; immediately behind this is a sudden and 


154 THE DEVELOPMENT OF THE. CHICK 


conspicuous thickening, the optic chiasma, which is continued 
as a ridge in the lateral ventral zones on each side (Fig. 86). 
The infundibulum follows just behind this, and constitutes a 
considerable pouch-shaped depression from which the saccus 
infundibuli grows out later. The posterior wall of this depression 
rises sharply and joins the thickened tuberculum posterius which 
is the end of the floor of the diencephalon. The diencephalon is 
compressed laterally (Fig. 97); the dorsal zones are slightly 
thickened, indicating the future thalami optici. 


spoFenc- 
Me Lé 


es 


pent SD posse 
3 Mesenc 


Synenc 


PATONC. 


LD. 


Fig. 88. — Optical longitudinal section of the head of an embryo of 39 s. 
Abbreviations as before. 


The hypophysis should be mentioned here, although it is not 
embryologically a part of the brain. It arises as a median tubu- 
lar invagination of the ectoderm of the ventral surface of the 
head immediately in front of the oral plate at about the 20s 
stage (Fig. 85), and grows rapidly inward in contact with the 
floor of the diencephalon. At about the 30s stage its end 
reaches nearly to the infundibulum (Fig. 87). At first part of 
its wall is formed by the oral plate, and when this ruptures the 
effect is to shorten the apparent length of the hypophysis (Fig. 
SS). At about the 36s stage its distal portion flattens laterally 


FROM TWELVE TO THIRTY-SIX SOMITES 155 


and shows indication of branching. Subsequently it becomes 
much branched and quite massive and unites with the infun- 
dibulum to form the pituitary body. (See Chap. VIII.) 

The Mesencephalon. This portion of the brain comes to 
occupy the summit of the cranial flexure, which indeed owes its 
origin largely to the rapid growth in extent of the roof of the 
mesencephalon. In longitudinal section it thus appears wedge- 
shaped, with short floor and long arched roof (Figs. 87 and 
88). Its walls remain of practically uniform thickness up to 
the seventy-second hour. The lateral walls expand more rapidly 
than the roof and thus form the optic lobes. But these are 
barely indicated at the 36s stage. 

Isthmus. The great expansion of the mesencephalon does 
not involve the portion immediately adjacent to the hind-brain, 
which is henceforth known as the isthmus (Figs. 87, 88). 

The Rhombencephalon (Primary Hind-brain). Two divisions 
of the embryonic brain arise from the rhombencephalon, viz., 
the metencephalon and the myelencephalon; the former becomes 
the region of the cerebellum and pons of the adult brain, 
and the latter the medulla oblongata. The metencephalon is a 
relatively short section of the original rhombencephalon, and 
includes only the most anterior neuromere of the rhomben- 
cephalon or the sixth of the series (Fig. 83 D, KE). It may be 
distinguished at the beginning of the period under consideration 
by the fact that its roof remains as thick as that of the mesen- 
cephalon. At the end of this time, 7.e., seventy-two hours, the 
roof in sagittal sections appears to rise sharply from the isthmus 
and thins towards the summit, where it passes into the thin epi- 
thelial roof of the myelencephalon (Figs. 87 and 88). The rudi- 
ment of the cerebellum is slightly thicker on each side of the 
middle line at seventy-two hours. 

The myelencephalon becomes sharply characterized by the 
thinness of its roof and thickening of ventral lateral zones and 
floor. The epithelial roof has a triangular form, the base resting 
against the metencephalon. The neuromeres remain very distinct 
(Figs. 83, 89), but change their form. Up to about twenty-three 
somites they still form external expansions, but as the wall 
thickens the external surface becomes smooth, and the neuro- 
meres may now be recognized as a series of concavities in the 
lateral wall, with intervening projections (Fig. 89). The arrange- 


156 THE DEVELOPMENT OF THE CHICK 


ment of the nuclei leaves thin non-nucleated strips (septa) be- 
tween adjacent neuromeres. The interneuromeric projections are 
most pronounced laterally and fade out dorsally and ventrally. 

Behind the neuromeric portion of the hind-brain is a portion 
extending to the posterior end of the fourth mesoblastic somite 
from which the twelfth cranial nerve arises. 

The Neural Crest and the Cranial and Spinal Ganglia. The 
cranial and spinal ganglia owe their origin to a structure known 
as the neural crest, which is a practically continuous cord of cells, 
lying on each side in the angle between the neural tube and 
the ectoderm, extending from the extreme anterior to the pos- 
terior end. Like other meristic structures the anterior portion 


Vy 


Am V4 VL. 


t 


Chor __ 


1 
| 
t 


Wil MONS yg Gr ae 


YS. 


Fic. 89. — Frontal section of the hind-brain region of an embryo of about 
36s. 

Ot., Otocyst... N.°6, N.. 7,..N. 8, .N, 9, Ne 10; N. 11, Neuromeres, 6 to 11, 
according to Hill’s enumeration. s. 1, s. 2, s. 3, First, Second, and third 
somites. V, Primordium of the trigeminus. VII-VIII, Primordium of the 
acustico-facialis. 


of the neural crest is the first to arise (at about 6—-7s stage), 
and the remainder appears in successive order during or shortly 
after the closure of the neural tube in each region; thus it is not 
until after the completion of the neural tube that the last portion 
of the neural crest is established. 

But before this time successive enlargements of the cranial 
part of the crest have formed the primordia of the cerebral gan- 
elia, and similar successively arising enlargements of the parts 
of the crest opposite the mesoblastic somites form the rudiments 
of the spinal ganglia. The intervening portions of the crest form 
the so-called interganglionic commissures, which subsequently 


FROM TWELVE TO THIRTY-SIX SOMITES 157 


appear to form mesenchyme. The formation of mesenchyme 
from certain parts of the neural crest is most marked in the 
region of the brain. 

The primordia of the ganglia contain the cells (neuroblasts) 
which form the dorsal root fibers of the spinal nerves and parts 
of certain cranial nerves. They also appear to contain the cells 
from which the sheaths of the nerve fibers are formed; thus 
three kinds of cells at least are found in the neural crest, viz., 
mesenchyme forming cells, neuroblasts, and sheath cells. 

The Cranial Neural Crest and its Derivatives. The neural 
crest in the head may be divided into pre- and post-otic divisions, 
and these arise at different times. 


Fic. 90. — Transverse section of the fore-brain, and optic 
vesicles at the stage of 7 s. 

M’ch., Mesenchyme. n.Cr., Neural crest. Ph., Phar- 
ynx. Sut. cer., Anterior cerebral suture. X., Mass of cells 
in which the anterior end of the intestine, the neural tube 
and the notochord fuse. 


(1) The pre-otie division, which extends from the extreme 
anterior end of the neural tube to about the center of the audi- 
tory pit, is well developed at a stage of 7-8 somites, but it is not 
found at the 5s stage. The origin is everywhere the same, viz., 
from the dorsalmost cells of the medullary plate and the ecto- 
derm immediately adjacent; it arises at the time of contact of 
the medullary folds and is thus thickest in the region of the 
suture. Fig. 90 is a section through the developing optic vesicles, 
and shows the neural crest continuous with the tube and ectoderm 


158 THE DEVELOPMENT OF THE CHICK 


in the neural suture; it is separated from the mesenchyme in the 
region of the fore-gut by a considerable space. (We shall call 
the latter portion of mesenchyme the axial mesenchyme of the 
head, to distinguish it from the mesenchyme derived from the 
neural crest, which later hes lat- 
eral to it, and which may thus 
be known as the periaxial layer.) 
The crest may be followed ante- 
riorly to the extreme tip of the 
neural tube, and posteriorly to 
the region of the anterior intesti- 
nal portal, which hes at about the 
transverse level of the future au- 
ditory pit (cf. Fig. 91). In the 
region of the mid-brain it spreads 


( (c3> VI. V1. ae 
eee out laterally until its peripheral 


cells reach the axial mesenchyme. 


Goronowlitsch divides the pre-otic 
portion of the neural crest into pri- 
mary and secondary ganglionic crests, 
the post-otic portion being the terti- 
ary crest. According to his account 
there is a decided difference in time 


of origin of the primary and second- 
ary crests; the primary, involving the 


Fig. 91. — Diagram of the cephalic 
neural crest of a chick of about Yregion of fore- and mid-brain, aris- 
12s. (After Wilhelm His.) ing before the secondary which in- 


cludes the region of the trigeminus 
and acustico-facialis. I have not, however, found such a difference in 
my preparations. 


At the stage of 10 somites the cells of the pre-otic neural 
crest have lost their connection with the neural tube. Behind 
the optic vesicles they have spread out laterally between the 
axial mesenchyme and the ectoderm, where they form a_prac- 
tically continuous periaxial layer, distinguishable from the axial 
mesenchyme by its greater density, and hence deeper stain; 
but apparently mingling with it at the surface of contact. 

In the stages immediately following (10-20 s), the portions 
of the periaxial layer lying above the mandibular and the hyoid 
arches condense and thicken, and form strong cords extending 


FROM TWELVE TO THIRTY-SIX SOMITES 159 


from the superior angles of the neural tube into the arches in 
question; here they form connections with the ectoderm of the 
arches, which proliferates so as to contribute to their substance 
(Fig. 92). Elsewhere the periaxial layer gradually merges with 
the axial mesenchyme. The periaxial cords are the primordia 
of the trigeminus and acustico-facialis ganglia, and mark the 
paths of the trigeminal and facial nerves. Their connection with 


Fic. 92. — Transverse section immediately be- 
hind the first visceral pouch of a chick 
embryo of thirteen somites. (After Gorono- 
witsch.) Note connection of the periaxial 
cord with the ectoderm of the visceral arch. 


Ad., Aorta descendens. ec. Rounded me- 
senchyme cells. g. Place where cells derived 
from neural crest unite with the mesenchyme 
cells of the periaxial cord. f. Fusion. —p. Spin- 
dle-shaped peripheral mesenchyme cells. 


the ectoderm in the neighborhood of the first visceral pouch 
must not be confused with the so-called branchial sense-organs, 
for the primary connection is soon lost, and secondary connec- 
tions arise at about the 27 s stage, and constitute the true branchial 
sense-organs of these arches. 


160 THE DEVELOPMENT OF THE CHICK 


The acustico-facial periaxial cord attains definiteness some 
time before the trigeminal (ef. Fig. 71), and indeed appears almost 
from the first as a specially strong part of the periaxial layer: 
whereas in the region of the trigeminus the cells of this layer are 
first widely dispersed and secondarily aggregate, between the 
stages of 14 and 18 somites. Both cords are attached to the 
brain, the trigeminus to the first neuromere of the myelencepha- 
lon, and the acustico-facialis to the third (Fig. 83 E). 

The trigeminal and facial periaxial cords are supplemented, 
as we have seen, by proliferations of the ectoderm on each side 
of the first visceral pouch; the trigeminal cord then enters the 
mandibular arch, and the facial the hyoid arch, and in the stages 
between 20 and 27 somites form at least part of the mesenchyme 
of these arches. The axial mesoblast likewise contributes to the 
mesenchyme of these arches, and it becomes impossible in later 
stages to separate these two mesenchymal components. The 
gangha proper differentiate from the upper portions of the cords. 
The trigeminal periaxial cord divides over the angle of the mouth 
and sends out a process into the rudimentary manillary process. 
A third projection of the same cord towards the eye forms the 
path of the ophthalmic division of the trigeminus (Fig. 117). 

At the stage of about 27s the trigeminus forms a connection 
with a thickening of the ectoderm (placode of the trigeminus) 
situated in front of and above the first visceral cleft; and the 
facial connects similarly with a larger ectodermal thickening 
(placode of the facialis) situated on the posterior margin of the 
uppermost part of the first visceral furrow. These ectodermal 
thickenings are rudimentary structures of very brief duration, 
representing parts of the sensory canal system of the head of 
aquatic vertebrates. Their occurrence in the chick is an interest- 
ing example of phylogenetic recurrence. <A third and fourth 
like organ arises in connection with the post-otie ganglia. 

At the stage of 72 hours there are two ectodermal thicken- 
ings (placodes) in connection with the trigeminus, one in front 
of the other, derived probably by division of the original first. 
The facialis placode is more fully developed. 

(2) The post-otie ganglionic crest is a direct continuation of 
the pre-otic behind the ear, and it is at first difficult to make an 
exact boundary between them. At the stage of 13s the pre-otic 
crest extends beneath the auditory epithelium nearly to its middle 


FROM TWELVE TO THIRTY-SIX SOMITES 161 


in the form of a thick mass of cells in the roof of the neural tube. 
Towards the posterior end of the auditory epithelium the crest 
becomes smaller, and this is the beginning of the post-otic crest. 
Behind the ear the crest becomes larger again and extends later- 
ally so as to form a periaxial layer between the ectoderm and 
the axial mesoblast which extends back, above the first, second, 
and third somites to the middle of the fourth. The part between 
the ear and the first somite is, however, by far the best developed, 
the continuation behind being a relatively slight cord of cells. 

At about the stage of 17 somites the anterior part of the crest 
condenses to form a well-defined periaxial cord, which arises 
from the neural tube above the middle of the auditory pit, arches 
back behind its posterior margin and extends down into the 
third visceral arch, where it enlarges. This is the glossopharyn- 
geal periaxial cord. There is an enlarged portion of the crest 
just behind this overlying the site of the future fourth and fifth 
arches, but its substance is not yet condensed to form a distinct 
periaxial cord. 

At the stage of 20 somites the anterior cardinal vein and the 
duct of Cuvier form the posterior boundary of the enlarged por- 
tion of the post-otic crest (Fig. 73). The part of the periaxial 
layer immediately in front of this is somewhat condensed to 
form the periaxial cord of the vagus, and this is only indistinctly 
separated from that of the glossopharyngeus. 

The formation of the third visceral cleft definitely splits the 
periaxial layer into the periaxial cords of the glossopharyngeus 
and vagus (25s). This division is carried up indistinctly, at 
first, into the roots which occupy the space between the auditory 
sac and the first somite. The formation of the fourth visceral 
pouch similarly divides the distal portion of the vagus cord, 
so that part of it lies in front of the pouch and part behind. 

At the stage of seventy-two hours the ganghon petrosum 
glossopharyngeus) is definitely formed by an enlargement of 
the cord just above the third visceral arch, and the ganglion 
nodosum (vagus), similarly formed from the vagus cord, hes 
above the fourth visceral pouch, thus extending over the fourth 
and fifth arches. Branchial sense organs are formed at the dorsal 
angles of the second and third visceral furrows in connection 
with the IX and X nerves respectively. 

It would appear that the neural crest in the head is the 


162 THE DEVELOPMENT OF THE CHICK 


source of much of the mesenchyme, and it is an interesting ques- 
tion whether or not such mesenchyme has a different fate from 
that of different origin. Nothing definite, however, is known in 
regard to this, owing to the impossibility of separating the various 
kinds after they have once merged. 

The Neural Crest in the Region of the Somites. The neural 
crest is very slightly developed in the region of the first five so- 
mites, which is correlated with the fact that these somites are 
devoid of gangla. But the mode of origin is the same through- 
out the somitic region. Shortly after the closure of the neural 
tube in any region the neural crest forms an aggregation of cells 
in the roof, more or less sharply separated from the remainder 
of the tube both by the arrangement of the cells and also by their 
lighter stain (Figs. 107, 109, 112, 113). The early history may be 
followed in a single embryo, by comparing the conditions opposite 
the last somite with that of more anterior somites where develop- 
ment is more advanced. Figs. 107, 108, 109, 110 represent 
transverse sections through the twenty-ninth, twenty-sixth, 
twentieth, and seventeenth somites of a 29s embryo. In Fig. 
107 the cells of the crest are extending towards the upper angle 
of the somite, with which they are connected by protoplasmic 
strands. The aggregation in the roof of the neural tube is thus 
decidedly diminished; the lateral wings of the crest lie in the angle 
between the neural tube and the ectoderm. In the twenty-sixth 
somite (Fig. 108) the lateral wings extend farther from their point 
of origin, and appear to have a more intimate connection with 
the myotome. In the more anterior and older somites, twenty 
and seventeen (Figs. 109 and 110), the process has progressed 
much farther and the neural crest cells are completely expelled 
from the neural tube, which closes after them (Fig. 110). A yet 
later stage is shown in Fig. 111, through the twenty-third somite 
of a 35s embryo. 

The dorsal commissure uniting the right and left sides of the 
crest ruptures, and the cells of the crest aggregate so as to form 
a pair of ganglia in each somite. Thus, although the neural crest 
is primarily a median structure, it becomes divided into two 
lateral halves, and although it is primarily a continuous structure 
it becomes divided into a series of pairs of metamerice ganglia. 
The fate of the interganglionic commissures is conjectural. The 
ganglia are ill-defined from the mesenchyme when they are first 


FROM TWELVE TO THIRTY-SIX SOMITES 163 


Metenc Isth. crf]. Mesenc. 


Fic. 93. —Entire embryo of 27s viewed as a 
transparent object from above. 
a.a.1,a.a.2,a.a.3, First, second, and third 
aortic arches. Car., Carotid loop. Ret., Retina. 
v. C. 1, v. C. 2, First and second visceral clefts. 
Other abbreviations as before. x 20. 


164 THE DEVELOPMENT OF THE CHICK 


formed, but they rapidly become well differentiated. (See Chap. 
VIII.) 


IV. THE ORGANS OF SPECIAL SENSE (Eye, Ear, Nose) 


Kmbryologically a sharp distinction must be drawn between 
the essential percipient part of the organs of sense (retina of the 
eye, olfactory epithelium, and epithelium of the membranous laby- 
rinth) and the parts formed for protection and for the elaboration 
of function. The sensory part proper is the first to arise in the 
embryo, and is protected later by modifications of surrounding 
tissues or parts. We may thus distinguish between primary and 
secondary parts in the case of all organs of sense. Only the early 
history of the primary parts falls within the period covered by 
this chapter, except the formation of the lens in the case of the 
eye. 

The Eye. The primary optic vesicles arise, as we have seen, 
as lateral expansions of the anterior end of the neural tube; 
their position is indicated by an enlargement of the neural tube 
even before the meeting of the medullary folds in this region. 
The shape and relations of the early optic vesicles have already 
been described and figured. The origin of the optic stalk by 
constriction of the base of the vesicle was described in a preced- 
ing section of this chapter (p. 149). The stalks remain attached 
to the ventral end of the lateral walls of the diencephalon in 
the region of the recessus opticus, and constitute tubular con- 
nections between the vesicles and the brain, in the walls of which 
the optic nerve develops later (I*ig. 84). 

Locy found six pairs of “ accessory optic vesicles ’’ occurring in series 
immediately behind the true optic vesicles; they form low rounded 
swellings of the side-walls of the neural folds before the true brain 
vesicles are indicated, and last only about three hours in the chick 
(twenty-fourth to twenty-seventh hours of incubation). ‘‘ Their exist- 
ence supports the hypothesis that the vertebrate eyes are segmental, and 
that the ancestors of vertebrates were primitively multiple-eyed.”’ (Locy.) 

The external surface of the optic vesicle early reaches the 
ectoderm, to which it appears to be cemented at the 10s stage. 
In the 17-18 s stage, the optic vesicles project decidedly behind 
the attachment of the optic stalk, and the external wall is slightly 
thicker than that next the brain. The ectoderm then becomes 
thickened over a circular area in contact with the optic vesicle 


FROM TWELVE TO THIRTY-SIX SOMITES 165 


and this constitutes the primordium of the lens (Fig 94). The 
thickening of the external wall of the optic vesicle and of the 
lens primordium now proceed rapidly, and soon an invagination 
is formed in each (Fig. 95). 


Fic. 94. — Section through ~~ Fia. 95. — Section through the 
the primordium of the eye primordium of the eye of a 
of a chick embryo of 21 s. chick embryo at the end of 
(After Froriep.) the second day of incubation. 

d., Distal wall of optic (After Froriep.) 


vesicle. p., Proximal wall 
of optic vesicle. 


It is probable that a stimulus is exerted by the optic vesicle on the 
ectoderm with which it is in contact, causing it to thicken and become 
the primordium of the lens. This has been demonstrated experimentally 
to be the case in the embryo of the frog, and the morphological rela- 
tions are the same in the chick. The invagination of the primary optic 
vesicle to form the secondary optic vesicle is not mechanically produced 
by the growth of the lens, as some have supposed, for it has been shown 
(see Fol and Warynsky) that the secondary optic vesicle is formed in 
the absence of the lens. 


We may now consider the formation of the optic cup and of 
the lens separately. 

The Optic Cup. The invagination of the outer wall of the 
primary optic vesicle gradually brings this wall into contact 
with the inner wall and obliterates the primary cavity. Thus 


166 THE DEVELOPMENT OF THE CHICK 


is established the secondary optic vesicle or optic cup. Special 
attention must be given to the form of the invagination, for this 
determines relations of fundamental importance. The invagina- 
tion may be stated to consist of two parts. The first is directly 
internal to the lens primordium, and the second, which is continu- 
ous with the first, involves the ventral wall of the primary optic 
vesicle as far as the optie stalk. The secondary optic vesicle 
established by these invaginations thus has two openings into 
its cavity, (1) the external opening, which becomes the pupil 
of the eve, and (2) the ventral opening, continuous with the 
pupil, which is known as the choroid fissure. Figs. 96 A, B, and 
C exhibit these relations better than a detailed description. 

The choroid fissure is a transitory embryonic structure, sub- 
sequently closing by fusion of its lips. However, it establishes 
a relation of fundamental importance in that the ventral wall 
of the optic-stalk is kept continuous in this way with the inner 
or retinal layer of the secondary optic vesicle (Figs. 96 B, and 97), 
and thus a path is provided for the development of the optic 
nerve (see Chap. IX). It also provides an aperture in the wall 
of the optie cup for the entrance of the arteria centralis retine. 

The optic primordium at the 36s stage, with the omission of 
the lens, is composed as follows: 

(1) Optie-stalk attached to the floor of the brain; this is 
still tubular. 

(2) The optic cup or secondary optic vesicle consisting of 
two layers, viz., (a) a thick internal or retinal layer continuous 
at the pupil and choroid fissure with (6) the thin external layer. 
The cavity of the cup is the future posterior chamber of the eye; 
it has two openings, viz., the pupil filled by the primordium of 
the lens, and the slit-like choroid fissure extending from the pupil 
to the optic stalk along the ventral surface. The retinal layer 
is continuous with the floor of the optic-stalk, and thus with the 
diencephalon. 

The optie cup expands with extreme rapidity between the 
stages of 26 and 36 somites, as may be seen from the figures by 
comparing the relative size of the lens and optic cup at different 
stages. 

The Lens. The invagination of the thickened ectoderm 
external to the optie vesicle soon leads to the formation of a deep, 
thick-walled pit which rapidly closes (26-28 somites) and thus 


FROM TWELVE TO THIRTY-SIX SOMITES 167 


forms an epithelial sac, which at first practically fills the cavity 
of the optic cup. However, it very soon becomes detached from 
the posterior wall of the optic cup, which expands with great 
rapidity, and the lens is left at the mouth of the cup. The walls 


yer of optic 
mber of the 


alls of the optic 
y; the lens-sac is 


The w 
op. c. i., Inner la 


93). 


ao C 
gf. 


ral wall of diencephalon. 


p. Ch., Posterior cha 


‘i 


DMs Wate 


op. St., Optic stalk. 


w of the head (compare I 
; but the lens is represented as a solid bod 


ctoderm of the surface of the head. 


ch. Fis., Choroid fissure. 


Fic. 96. — Semi-diagrammatic representation of the eye of an embryo of about 27-30 s. 


ot 
oo 
Onn fo! 
Z of of = 
) ae =! 
= 4 Sc 5) 
S38 nel 
= o 
on | — 
Cian WKS. aoa 
~~ oO ata ia! > 
mG Qy 
CFR rN fx) O 
~ | = 
Qr -—O4 a 
= 8 : ee) 
e e 
o ada © =. 
Sem VYORnR OO 
= Sa Ag Y 
a = S of ¢ 
qe Ser ict 
SG) —=— fant 
Sees or) 
meee Lael 
Sed ams 
Doo Cea gy 
o.4 Oom & & 
[eb) =< ©) 
o = 2) 
Ro — oc. ~ 
S ~ ate 
word) OS = 
28 34 tO 
ao IS) a er 
Lan! orm omy — 
Sept a 5 ~ 
nm Cd . 
Ss. wn Se-s5o$o 
a aa ae) 
nao Qo ne 4 
@ + SOoOHRR., 
= SO OD 5 
os FS emt 
© Og Ree 
ot ene ieee . 
— 4 & OgomM ~ 6 
eS O72 ae 8 = 
do mt 
S OO SO 
— =~ © 
Puli spcaeye 
~ a a] 
ae EL) Sacee 
HS a 
—_— OO — O 
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a ae ie 
CR Pat 


7) 
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TM 

Se 


of the lens sac are at first of practically even thickness (2 
but by the 35s stage a great difference has arisen by the elonga- 
tion of the cells of the inner wall, which are destined to form 
lens fibers: the cells of the anterior (outer) wall elongate much 


168 THE DEVELOPMENT OF THE CHICK 


less during this period, and are destined to form the epithelium 
of the lens (Fig. 97). Intermediate conditions are found around 
the equator of the lens. The subsequent history is given in 
chapter IX. 

The Auditory Sac. At about the 12s stage the first evidence 
of the auditory sacs is found in the form of a pair of circular 
patches of thickened ectoderm situated on the dorsal surface of 
the head opposite to the ninth, tenth, and eleventh neuromeres, 
and thus a short distance in front of the first mesoblastic somite; 


it lies between the rudiments of the acustico-facialial and glosso- 
pharyngeal ganglia. In the 14s stage the auditory epithelium 


la 4S, 


(@) 


Lens . =G 
Fig. 97. — Transverse section through the eyes and heart of an embryo of 
about 35s. The plane of the section will be readily understood by com- 
parison of Fig. 117. 
ch. Fis., Choroid fissure. D. C., Duet of Cuvier. Lg., Lung. pl. gr., 
Pleural groove. V. ¢., Posterior cardinal vein. Y. 8., Yolk-sae. Other 
abbreviations as before. 


is slightly depressed, and in the 16s stage it forms a wide-open 
pit. At about the 20s stage the mouth of the pit narrows slightly, 
and gradually closes (28-30 s), thus forming the auditory sac or 
vesicle (otocyst) (ef. Figs. 71, 73, 89, and 93). 

The method of closure of the pit, which is of interest, may 
readily be observed in mounts of entire embryos; at first the 
lips fold over most rapidly from the anterior and posterior mar- 
gins; thus the mouth of the pit becomes elliptical with the long 
axis vertical (stage of 22 somites) and extending from the apex 
nearly to the base. The ventral lip then begins to ascend (stage 
of 24 somites) and the closure gradually proceeds towards the 


FROM TWELVE TO THIRTY-SIX SOMITES 


169 


apex, so that by the stage of 29 somites the opening is reduced 
to a minute ellipse situated on the external side of the dorsalmost 


portion of the otocyst (see Fig. 93). 
now begins to form a small conical 
elevation, and the final closure takes 
place on the external side of this 
elevation, which is destined to 
form the endolymphatic duct. The 
latter remains united to the epi- 
dermis at this point for a consid- 
erable period of time by a strand 
of cells which preserve a 
lumen up to 104 hours (Fig. 98). 
The final point of closure of the oto- 
cyst is thus very definitely placed, 
and it coincides with the middle of 
the endolymphatic duct, that is, 
with the junction of the later formed 
saecus and ductus endolymphaticus. 
In the Selachia this duct remains 
in open communication with the 
exterior throughout life; the rela- 
tively long persistence of its con- 
nection with the epidermis in the 
chick may thus be interpreted as ¢ 
phylogenic reminiscence of the an- 
cestral condition. 

The Nose (Olfactory Pits). At 
about the 28s stage, the ectoderm 
on the sides of the head a short dis- 
tance in front of the eyes appears 
thickened. Two circular patches of 
ectoderm are thus marked off, the 
beginning of the olfactory epithe- 
lium; at first this grades almost im- 
the 


may 


perceptibly into neighboring 


ectoderm. 


This portion of the otocyst 


Fig. 98. — Section of the otocyst 
of an embryo of 104 hours. The 


original opening of the otocyst 
is drawn out into a narrow ca- 
nal which connects with the 
endolymphatic duct (recessus 
labyrinthi). 

a., Ball of cells in the otocyst 
(otolith?). b., Canal leading from 
the surface to the otocyst. D. 
end’]., Endolymphatie duct. D., 
Dorsal. Ect., Eetoderm of the 
surface of the head. Gn., Audi- 
tory ganglion. L., Lateral. M., 
Median. V., ventral. 


In the stages immediately following the olfactory 


plates appear to sink down towards the ventral surface of the 


head, due no doubt to more rapid growth of the dorsal portion 


of the head. 


Thus they appear at the ventro-lateral angles of 


170 THE DEVELOPMENT OF THE CHICK 


the anterior part of the head at the stage of 36 somites. During 
the displacement a depression appears in the center of each olfac- 
tory plate, and as this becomes deeper, the olfactory pits are 
formed (Figs. 99 and 117). At the stage of 36 somites each is 
a deep pit situated at the junction of the sides and ventral sur- 
face of the anterior portion of the head, with the wide mouth 
opening outwards and ventrally. 

The olfactory epithelium now becomes sharply differentiated 
from the ectoderm of the head, owing to the formation of a super- 
ficial layer of cells (teloderm, see p. 285) above the columnar cells 
in the ectoderm, but not in the region of the sensory epithelium, 
where the cells still form a single layer. In the center of the 
olfactory pit the epithelium is very much thickened owing to 
elongation of the cells, and the nuclei lie in five or six layers; 
there is a gradual thinning of the epithelium to the lips of the 
pit and then a sudden, but graduated, decrease to the general 
ectoderm. The line of junction of olfactory epithelium and 
indifferent ectoderm of the head is a little distance beyond the 
margin of the pit, as may be determined by the edge of the telo- 
dermice layer; in other words, all of the olfactory epithelium is 
not yet invaginated. 

It is probable that the invagination of the olfactory plates is 
due mostly, up to this time, to the processes of growth within 
the plates themselves, although there has been considerable 
accumulation of mesenchyme in this region. But the subsequent 
deepening of the pits appears to be due largely to the formation 
of processes around the mouths of the primary pits. (See 


Chap. IX.) 


V. Tue ALIMENTARY TRACT AND ITS APPENDAGES 

We have already learned that the main portion of the alimen- 
tary tract arises from the splanchnopleure; a portion of the mouth 
cavity is, however, lined with ectoderm and arises from an inde- 
pendent ectodermal pit, the stomodeum, which communicates 
only secondarily with the entodermal portion; similarly the last 
portion, external to the cloaca, arises from an ectodermal pit, 
the proctodeum, which communicates only secondarily with the 
entodermal part. We shall thus have to consider the origin of 
the stomodeum and the proctodeum in connection with the 


alimentary tract. 


FROM TWELVE TO THIRTY-SIX SOMITES eA 


CELL: 


Ol. VeVi =~ Nim V. Mefenc. Is th. 


Fic. 99. — Entire embryo of 31 somites viewed as a 
transparent object. 


am. Umb., Amniotic umbilicus. B. a., Bulbus 
arteriosus. cerv. Fl., Cervical flexure. ch. Fis., Cho- 
roid fissure. er. Fl., Cranial flexure. D.C., Duct of 
Cuvier. ex. 0. c., External layer of the optic cup. 
int. o. c., Internal layer of the optic cup (retina.) 
N’m., Neuromere of myelencephalon. olf., Olfactory 
pit. pe. W., Line of attachment of amnion to peri- 
eardial wall. V.C.1, 2, 3, First, second, and third 
visceral clefts. Other abbreviations as before. 


172 THE DEVELOPMENT OF THE’ CHICK 


From the embryological point of view the alimentary tract 
may be divided into fore-, mid-, and hind-gut. The fore-gut 
includes the anterior portion as far back as the liver diverticulum, 
the mid-gut extends from here to the ccecal appendages, and the 
hind-gut includes the remainder. From each division there 
arise certain outgrowths which may be termed collectively 
appendages of the alimentary tract, and these will also be 
considered here, so far as they arise within the period covered 
by this chapter. Thus from the fore-gut there arise the visceral 
pouches, the thyroid and thymus glands, the postbranchial 
bodies, the respiratory tract, and the liver and pancreas; from 
the mid-gut the yolk-sac, and from the hind-gut the ccecal 
appendages and allantois. 

The enlargement of the body-cavity towards the middle line 
gradually reduces the broad mesodermal septum situated between 
its inner angles to a relatively narrow plate, which forms the dor- 
sal mesentery of the intestine (Figs. 107, 109, 110, and 111). This 
elongates in the course of development and forms a sheet of tissue 
suspending the intestinal tube to the mid-dorsal line of the body- 
cavity. It is composed of two layers of mesothelium (peritoneum) 
continuous with the lining of the body-cavity and enclosing a 
certain amount of mesenchyme; the dorsal mesentery extends 
along the entire length of the intestinal canal. 

A ventral mesentery uniting gut and yolk-sac is also estab- 
lished by the meeting of the limiting sulci in the splanchnopleure. 
When the body-wall closes, the ventral mesentery consists of 
two layers of mesothelium attaching the intestinal canal to the 
mid-ventral line of the body-wall. The dorsal and ventral mesen- 
teries, together with the alimentary canal, thus constitute a 
complete partition between the right and left halves of the body- 
cavity. However, the ventral mesentery is a very transient 
structure except in the region of the fore-gut and liver, and in 
the extreme end of the hind-gut. In these places it is persistent 
and is the seat of formation of important organs. 

The wall of the intestine contains three embryonic layers: 
viz., entoderm, mesenchyme, and mesothelium. The first forms 
the lining epithelium of the intestine, and of all glandular attach- 
ments, as well as of the respiratory tract and allantois; the last 
forms the serosa; and the mesenchyme the intermediate layers. 

We shall now consider the development of each region of the 


FROM TWELVE TO THIRTY-SIX SOMITES 173 


alimentary tract and the appendages proper to each in the follow- 
ing order: (1) Stomodzum, (2) Pharynx, (3) Ctsophagus, (4) 
Stomach, (5) Hepato-pancreatic division of the fore-gut, (6) Mid- 
gut, (7) Hind-gut. 

The stomodeum owes its origin to an expansion of the em- 
bryonic parts surrounding the oral plate, and it gives rise to a 
large part of the buccal cavity, which is therefore lined by ecto- 
derm. (See Chap. X.) It will be remembered that at the 12s 
stage the oral plate lies between the pericardium and the head- 
fold (Fig. 67), and that it consists of a fusion between the 
ectoderm of the ventral surface of the head and the entoderm 
composing the floor of the anterior end of the fore-gut. It lies 
in a slight depression on the under surface of the head which 
is the beginning of the oral cavity. This small beginning owes 
its enlargement (1) to the cranial flexure, by which the ventral 
surface of the head becomes bent at right angles to the oral 
plate instead of forming a direct continuation of it, and (2) to 
the formation and protrusion of the mandibular arches and 
maxillary processes at the sides and behind. (See fuller account 
in Chap. VII.) In this way it becomes a deep cavity closed 
internally by the oral plate. The series of figures of sagittal 
sections through the head illustrates very well the gradual deep- 
ening of the stomodeum by these processes (Figs. 75, 85, 87, 88). 

The oral plate thins gradually from the 12 to the 30s stage 
when it breaks through (Figs 87 and 88), thus establishing an 
opening into the alimentary tract. The remnants of the oral 
membrane then gradually disappear and leave no trace. The 
subsequent extension of the maxillary region to form the upper 
jaw greatly enlarges the extent of the ectodermal portion of the 
buceal cavity. It will have been noted (Figs. 85 and 87) that 
the hypophysis opens in front of the oral plate on the ectodermal 
side, and this constitutes a most important landmark for deter- 
mining the limit of the ectodermal portion of the buccal cavity 
in later stages. 

The Pharynx and Visceral Arches. The pharynx may be briefly 
defined as the alimentary canal of the head. It is the most 
variable part of the alimentary canal in the series of vertebrates. 
Modified, as it is in all vertebrates, for purposes of respiration, 
the transition from the aquatic to the terrestrial mode of respira- 
tion brought about great changes in it. It is thus marked em- 


174 THE DEVELOPMENT OF THE CHICK 


bryologically first by the development of structures, the viscera! 
arches and clefts, whose primary function was aquatic respira- 
tion, and second by the development of the air-breathing 
lungs. Such fundamental changes in function have left a deep 
impression, not only on the embryonic history of the pharynx 
itself, but also on the development of the nervous and vascular 
systems. 

The extreme anterior end of the pharynx extends at first 
some distance in front of the oral plate, and may hence be called 
the pre-oral gut (Figs. 75, 85, etc.). After the rupture of the 
oral plate, the pre-oral gut appears like an evagination of the 
pharynx immediately behind the hypophysis and is now known 
as Seessel’s pocket (Fig. 87), but it gradually flattens out and 
disappears (lig. 88). 

The form of the pharynx at thirty-three hours has been 
already described; briefly, it is much expanded laterally, exhibiting 
a crescentic form in cross-section (Fig. 54 A). The horns of the 
crescent are in contact with the ectoderm in front of the auditory 
pit, marking the site of the future hyomandibular cleft, which 
arises by perforation in the fused area at about forty-six hours. 
A second pair of lateral expansions brings about a second fusion 
of the lateral wings of the pharynx just behind the auditory pit 
at about the stage of 19-20 somites. This is followed by the 
formation of a third and a fourth pair of lateral evaginations of 
the pharynx which reach the ectoderm at about 23s and 35s 
respectively. The walls of the pharynx appear considerably 
constricted between the evaginations which are known as vis- 
ceral pouches (Figs. 100 and 101). 

Corresponding to each visceral pouch there is formed an 
ectodermal invagination of much lesser extent, which may be 
known as the visceral furrow. The furrows do not form directly 
opposite the pouches, but slightly behind them so as to overlap 
the margins of the latter (Fig. 101). The ectoderm of the visceral 
furrows forms a close union with the entoderm of the pouches, 
and openings arise within these areas, excepting the fourth, 
forming transitory visceral cle/ts. 

There are thus four pairs of visceral pouches and furrows, 
known as the first, second, third, and fourth; the first 1s some- 
times called the hyomandibular. 


According to Kastschenko, there are evidences of three pairs of 


FROM TWELVE TO THIRTY-SIX SOMITES 175 


visceral furrows in front of the first at the 14-16s stage. These he in- 
terprets as phyletic rudiments. It is certain that the lower vertebrates 
had pouches posterior to the fourth. The post-branchial bodies (see 
p. 309) are probably rudiments of a fifth pair of pouches. 

The tissue between the visceral pouches thickens, by acecumu- 
lation of mesenchyme, to form the visceral arches, of which there 
are five, viz.: (1) the mandibular in front of the first pouch, form- 
ing also the posterior boundary of the oral cavity, (2) the hyoid 
between the first and second pouches, (8) the third visceral arch 
between the second and third pouches, (4) the jfowrth viscerat 
arch between the third and fourth pouches, and (5) the fijth 


vy P/ vo~0/ vP2 yC.aé 


aN 7 me v rte VPS 
3 ~~ y ye ae 
TOO ae Ries / ~ ho a 
Nes / > 
he —? “ ff 
“C— ae lg AS 1 
\ 3/74 aN \ \ 
\ / | Ome \ 0es 
v.C. ve \ ay NE x 
cee we ‘ va J \ 
ve ML af Stom. 
LG. 
Fig. 100. — Reconstruction of the fore-gut of a chick of 72 hours. 


(After Kastschenko.) 

Hyp., Hypophysis. lar-tr. Gr., Laryngotracheal groove.  Lg., 
Lung. Md.a., Mandibular arch. Oeces., Oesophagus.  pr’o. G., Preoral 
gut. Stom., Stomach. Th., Thyroid. v.C.d, 1, 2, Dorsal division of 
the first and second visceral clefts. v.C. v. 2, Ventral division of the 
second visceral cleft. v. P. 1, 2, 3, 4, First, second, third, and fourth 
visceral pouches. 


visceral arch behind the fourth pouch. Each arch is bounded 
internally by entoderm, externally by ectoderm. The main portion 
of its substance is formed of mesenchyme; each contains also a 
branch of the ventral aorta (aortic arch) and a branch of a cranial 
nerve. Understanding of their relations is therefore essential to 
knowledge of the development of the nervous system, vascular 
system, and skull. 

We shall now consider the history of each visceral pouch 
and arch separately: 

The first visceral pouch becomes adherent to the ectoderm 
of the first visceral furrow at its dorsal and ventral ends, leaving 


176 THE DEVELOPMENT OF THE CHICK 


an intermediate free portion. At about the 26s stage an opening 
(cleft) forms at the dorsal adhesion, but none at the ventral; 
thus the first visceral cleft is confined to the dorsalmost portion 
of the pouch (Fig. 100). This opening closes about the end of 
the fourth day; the ventral portion of the pouch then flattens 
out, and the dorsal portion expands upwards towards the otocyst 
(Fig. 102). 

The first visceral (mandibular) arch thickens greatly between 
the 14 and 35s stages, the ventral ends project a little behind 
the oral invagination, and subsequently meet to form the primor- 
dium of the lower jaw (Figs. 125 and 126, Chap. VII). A pro- 


ules VP. P, 
A ee 


UAL | UPF 
28) IAATCT. of, 


} 


Fic. 101. — Frontal section through the pharynx of a 35s embryo. 

a.a. 1, 2, 3, 4, First, second, third, and fourth aortic arches. Hyp., Hypo- 
physis. J., Jugular vein. lar-tr. Gr., Laryngotracheal groove. or., Oral 
cavity. Ph., Pharynx. Th., Thyroid. v. A. 1, 2, 3, First, second, and third 
visceral arches. v. C. 1, First visceral cleft. v. F. 2, 3, Second and third 
visceral furrows. v. P. 2, 3, 4, Second, third, and fourth visceral pouches. 

IH, Third cranial nerve. 


jection of the upper anterior border just behind the eye is 
the beginning of the maxillary process, or primordium of the 
maxillary portion of the upper Jaw. 

The second visceral pouch likewise becomes adherent to the 
ectoderm of the second visceral furrow at its dorsal and ventral 
ends, and openings are formed in each adhesion by the 35s stage 
(Fig. 190); the dorsal opening is small and oval (later becoming 
more elongated) while the ventral one is a long, narrow fissure; 
they are separated only by a narrow bridge of tissue, and close 
during the fourth day. 

The third visceral pouch behaves like the second, forming a 


FROM TWELVE TO THIRTY-SIX SOMITES LATE 


small round dorsal, and long fissure-like ventral cleft at about 
the 40s stage (Fig. 102). These close during the fifth day. 


The significance of the separate dorsal and ventral divisions of the 
visceral clefts is an interesting question. It is probable that the dorsal 
division had a special function, as they have a special connection with 
the branchial sense organs. 


Fic. 102. — Reconstruction of the pharyngeal organs of the chick 
at the end of the fourth day of incubation. (After Kastsch- 
enko.) 


a.a. 3, a. a. 4, a. a. 6, Third, fourth, and sixth aortic arches. 
Car. e., External carotid. Car. i., Internal carotid. G. Gn., Ge- 
niculate ganglion. G.n. X.,Ganglion nodosum. G. pr., Gan- 
glion petrosum. ot., Otocyst. p. A., pulmonary artery. Th., 
Thyroid. v. P. 1, 2, 3, 4, First, second, third, and fourth visceral 
pouches. 


V, VU, VII, IX, X, XII, Cranial nerves and ganglia. 


The fourth visceral pouch connects with the ectoderm at its 
dorsal end, about the 35s stage, but no cleft develops. Its pos- 
terior wall develops an evagination (postbranchial body) which 
by some is considered to be a rudimentary fifth pouch, and 
which contributes to the formation of the thymus. (See 


Chap. X.) 


178 THE DEVELOPMENT OF THE CHICK 


The second visceral arch is the largest of the arches and over- 
laps both the first and third. See Figs. 117 and 125 in place of 
description. All of the arches are wedge-shaped, corresponding 
to the wedege-like form of the hind-brain region. The fourth 
arch is small and incomplete ventrally; the fifth a mere transitory 
rudiment. The greatest development of the arches is at about 
the end of the fourth day. 


According to Kastschenko the closure of the visceral clefts takes 
place external to the meeting-place of the visceral furrows and clefts, 
and in this way some of the ectoderm of the furrows remains attached 
to the visceral pouches. 


The thyroid arises as a small, spherical evagination of the 
epithelium of the floor of the pharynx situated between, and a 
little in front of, the ventral ends of the second pair of visceral 
pouches (Figs. 85, 87, 88, 101). In the 18-20 stage, it is repre- 
sented by a sharply defined plate of high, columnar cells in the 
same situation, which may be recognized even at the stage of 
12s. At the stage of 26s this plate forms a deep, saucer-shaped 
depression, and at the 30s stage it is a well-developed sae with 
wide-open mouth which gradually closes, thus transforming the 
sac into a small spherical vesicle lying beneath the floor of the 
pharynx (Hig. 102). 

The Pulmonary Tract. The portion of the pharynx that 
includes the visceral pouches may be called the branchial portion, 
because it is homologous to the gill-bearing portion in fishes and 
amphibia, and because the visceral pouches are phylogenetic 
rudiments of branchial clefts. The larnyx, trachea, and lungs 
develop from the ventral division of the postbranchial portion 
of the pharynx. At about the 23s stage a reconstruction shows 
this respiratory division of the pharynx slightly constricted from 
the broader branchial portion, enlarged on each side at its pos- 
terior end and with a ventral depression; the latter rapidly 
deepens to form a narrow groove, the primordium of the larynx 
and trachea, while the posterior lateral expansion begins to form 
outgrowths, the primordia of the lungs and air-sacs. By the 
stage of 35s (Fig. 100) the postbranchial portion of the pharynx 
has become narrow transversely and its ventral half is a deep 
groove (laryngotracheal groove) leading back to the lung pri- 
mordia. A true median sagittal section at this time shows the 


FROM TWELVE TO THIRTY-SIX SOMITES 179 


floor of the laryngotracheal groove directly continuous with the 
floor of the branchial portion of the pharynx at its hind end; the 
former bends up at about right angles to enter the narrow 
oesophagus (Figs. 87 and 88). 

Thus the whole pulmonary tract communicates widely with 
the pharynx at the 35s stage. Its complete delimination falls 
within the period covered by Chapter X. The continuity of 
the expansions that form the lung primordia, with the series of 
visceral pouches as shown in Fig. 100, is especially noteworthy 
as suggesting a theory of the phylogenetic derivation of the lungs. 


Fig. 103.— Reeconstructions of the liver diverticula of the chick. 


(After Hammar.) 

A.On the third day of incubation; from the left side; the divertic- 
ula arise from the anterior intestinal portal. 

B. Beginning of the fourth day; from the left side. 

a. i. p., Anterior intestinal portal. D. V., Indicates position of 
ductus venosus. g. b., Gall bladder. 1. d. d. (er.)., Dorsal or era- 
nial liver diverticulum. 1. d. v. (eaud.), Ventral or caudal liver 
diverticulum. pe. d., Dorsal pancreas. X., Marks the depression in 
the floor of the duodenum from which the common bile duct. is 
formed. 


Csophagus and Stomach. Immediately behind the pharynx, 
at the stage of 36s, the intestine narrows suddenly (primordium 
of cesophagus) and enters a small, spindle-shaped enlargement, 
the primordium of the stomach (Figs. 87, 88, 100). 

The liver arises in the chick as two diverticula of the entoderm 
of the anterior intestinal portal, one situated immediately above 
and the other below the posterior end of the ductus venosus, or 
fork of the omphalomesenteric veins (Fig. 103 A). This portion 


180 THE DEVELOPMENT OF THE CHICK 


of the anterior intestinal portal becomes incorporated in the 
floor of the intestine as the anterior intestinal portal retreats 
backwards, and the original dorsal liver diverticulum therefore 
becomes anterior or cephalic and the ventral becomes posterior 
or caudal (Fig. 103 B). Before this transposition occurs, how- 
ever, the diverticula have grown forward towards the sinus 
venosus in the ventral mesentery of the stomach, the anterior 
diverticulum above and the posterior diverticulum below the 
ductus venosus. The stretch of entoderm between the two liver 
diverticula thus lies in the angle made by the union of the two 
omphalomesenteric veins. At the stage of 26 somites, the anterior 
diverticulum has grown forward above the ductus venosus 
to the level of the Cuvierian veins and is large and flattened 
laterally. The posterior diverticulum is barely indicated at this 
time. 


The anterior diverticulum was originally described as left and the 
posterior as right (Goette, 1867), and this description was taken up 
by Foster and Balfour. This was corrected by Felix (1892). Subse- 
quent writers do not agree exactly as to the time or precise relations 
of the diverticula; however, it is generally agreed that the two diver- 
ticula are subdivisions of a common hepatic furrow, inasmuch as the 
entoderm between them lies below the level of the entoderm in front 
and behind (Fig. 103 B). Brouha maintains that at first the hepatic 
furrow lies in front of the anterior intestinal portal, and that the latter 
secondarily moves forward so as to include the hepatic furrow, which 
later again comes into the floor of the intestine with the definitive retreat 
of the anterior intestinal portal. This view does not rest on very secure 
evidence, and is probably based on interpretation of slight individual 
variations as successive stages of development. Choronschitzky places the 
time of appearance of the hepatic diverticula at about the thirty-sixth 
hour. It is probable, however, that this is too early. I have found the 
first unmistakable diverticulum at a stage of 22 somites, a slight rudi- 
ment of the anterior diverticulum in the anterior intestinal portal. 


At the 30s stage the anterior or dorsal diverticulum has ex- 
panded much more, mainly to the left of the middle line, as though 
to embrace the ductus venosus, and the posterior or ventral 
diverticulum has an even greater development and embraces 
the right side of the ductus venosus, but it does not extend as 
far forward as the anterior diverticulum. Both diverticula 


now branch rapidly and profusely, forming secondary anasto- 


x 
“ 


FROM TWELVE TO THIRTY-SIX SOMITES 181 


moses where branches meet, so that a complete ring of anas- 
tomosing columns of hepatic cylinders is rapidly formed around 


the center of the ductus venosus 
(Figs. 103 B and 104, ef. also Figs. 
119 and 120). But the anterior 
and posterior ends of the ductus 
venosus are not yet completely 
surrounded by the basket-work of 
liver substance, owing to the ab- 
sence of any part of the posterior 
diverticulum in its anterior por- 
tion, and of the anterior divertic- 
ulum in its posterior portion. 

The floor of the intestine be- 
tween the anterior and posterior 
liver diverticula is depressed; later 
it becomes separated from the 
intestinal cavity to form a tem- 
porary common bile-duct; which 
then receives the two primary di- 
verticula (Figs. 103B, 104 and 
187). 

The pancreas arises from a dor- 
sal and a pair of ventral primordia. 
The former is an outgrowth of 
the dorsal wall of the intestine 
immediately above the posterior 
liver diverticulum (Figs. 103 B 
and 104). At the 35s stage it is 
a solid thickening of the dorsal 
wall of the intestine of consider- 
able extent; a little later the base 
of the thickening is hollowed out, 
and the free margin sends off solid 
buds into the dorsal mesentery 


Fig. 104. — Reconstruction of the 
liver of the chick at the end of 


the fourth day of incubation. 

(After Hammar. ) 

du., Duodenum. L., Substance 
of liver. Other abbreviations as 
before. 


just behind the stomach. The ventral primordia arise from the 
posterior liver diverticulum in a manner to be described later 


(Chap. X). 


Mid-gut. At the 35s stage the mid-gut is still open to the 
yolk-sac. Its subsequent history is given in Chapter X. 


182 THE DEVELOPMENT OF THE CHICK 


Anal Plate, Hind-gut, Post-anal Gut, and Allantois. At about 
the 14s stage a thickening of the ectoderm in the middle line 
just behind the primitive streak extends towards the entoderm 
which is folded up so as to nearly meet it, thus cutting off the 
extra-embryonic mesoblast from the primitive streak. The ecto- 
derm and the entoderm then come into contact here, and form 
a firm union, the anal plate (Fig. 70), which is subsequently 
perforated to form the anus. At first, however, the anal plate les 
entirely behind the embryo, and the post-anal portion of the 
embryo arises from the thickened remnant of the primitive streak 
(tuil-bud) which grows backwards over the blastoderm beyond 
the anal plate. Even before this, however, the hind-gut begins 
to be formed by a fold of the splanchnopleure directed forwards 
beneath the tail-bud, and the hind end of the tube thus formed 
ends at the anal plate (Fig. 70). The entoderm in front of the 
anal tube is fused with the substance of the tail-bud, and as the 
latter grows backwards beyond the anal plate it carries with it 
a pocket of the hind-gut, and this forms the post-anal gut (Fig. 
80). 

The formation of the tail brings the anal plate on to the ven- 
tral surface of the embryo at the junction of tail and trunk, and 
the post-anal gut then appears as a broad continuation of the 
hind-gut extending behind the anal plate, and ending in the tail 
at the hind end of the notochord (Fig. 80). The further elonga- 
tion of the tail draws out the post-anal gut into a narrow tube 
lying beneath the notochord in the substance of the tail; it 
then gradually disappears and leaves no trace. 

The formation of the hind-gut takes place prior to the for- 
mation of the embryonic body-cavity at this place. It thus 
happens that the splanchnic mesoderm, forming the floor of the 
hind-gut, is directly continuous with the somatic mesoderm. 
When the body-cavity does penetrate this region it is without 
direct lateral connections with the extra-embryonic body-cavity, 
so that the connection of the splanchnic and somatic mesoderm 
persists, forming the ventral mesentery of the hind-gut (Fig. 81). 
This is a thick mass of mesoblast binding the hind-gut to the 
somatopleure. The hind-gut is deep from the first, and its ven- 
tral division soon begins to extend into the ventral mesentery 
as a broad evagination, the allantois (see p. 148). 


FROM TWELVE TO THIRTY-SIX SOMITES 183 


VI. History or THE MESODERM 


The history of the extra-embryonic mesoderm is considered 
sufficiently in the first part of this chapter. The history of the 
embryonic mesoderm will be considered under the following 
heads: (1) Somites, (2) Intermediate Cell-mass, (3) Vascular 
System, (4) Lateral Plate and Body-Cavity, (5) Mesoblast of 
the Head. 


WS 


Bytes 
Oe 


Fig. 105. — Embryo of about 27 somites drawn in aleohol by re- 
flected light; upper side. x 10. 
Am., Amnion. ot., Otoecyst. t. F. Am., Tail fold of amnion. 


(1) Somites. The rate of formation of the somites from the 
segmental plate and their number at different times is given in 
the normal table of embryos (p. 68), and may be seen in various 


184 THE DEVELOPMENT OF THE CHICK 


figures of entire embryos. The formation of new somites con- 
tinues after the end of the period discussed in this chapter, 
up to about the sixth day. Each somite has a definite value in 
the developmental history. 


Ses Sasi 


Fig. 106. — The same embryo from beneath. x 10. 
a. i. p., Anterior intestinal portal. A. V., Vitelline artery. 
Int., Intestinal groove. 


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: 

Lto 4. Cephalic; entering into the composition of the occipital region 
of the skull. 

5to 16. Prebrachial; “e., entering into the region between the wing 
and the skull. 

17 to 19. Brachial. 

20 to 25. Between wing and leg. 


FROM TWELVE TO THIRTY-SIX SOMITES 185 


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. This points 
towards a long-tailed ancestry for birds. 

Each somite is composed of an epithelial wall of high, columnar 
cells, enclosing a core of cells that nearly fills the cavity (Iigs. 
112, 113, etc.). From each somite there arise three parts of 
fundamental significance, viz., the sclerotome, the muscle plate, 
and the cutis plate (dermatome), the primordium of the axial 


Fic 107. — Transverse section through the twenty-ninth somite of a 29s 
embryo. 


n. Cr., Neural crest. Neph., Nephrotome. W. D., Wolffian duct. Other 
abbreviations as before. 


skeleton, the voluntary muscles (excepting those of the head), 
and derma respectively. The manner of origin of these parts 
may be studied fully in an embryo of 25 to 30 somites, by com- 
paring the most posterior somites, in which the process is begin- 
ning, with somites of intermediate and anterior positions in the 
series, which show successively later stages. 

Figs. 107, 108, 109, and 110 represent transverse sections 
through the twenty-ninth, twenty-sixth, twentieth, and seven- 
teenth somites of a 29s embryo. In the twenty-ninth somite 


186 THE DEVELOPMENT OF THE CHICK 


(Fig. 107) the primitive relations of the parts are still preserved. 
In the twenty-sixth somite (Fig. 108) it will be seen that the 
cells of the core and of the ventral and median wall of the somite 
extending from the nephrotome to about the center of the neural 
tube are becoming mesenchymal; they spread out towards the 
notochord and the space between the latter and the dorsal aorta. 
These cells constitute the sclerotome. The muscle plate extends 
from the dorsal edge of the sclerotome to the dorso-median angle 
of the wall of the somite, and the dermatome from this point 
to the nephrotome. 


Fic. 108. — Transverse section through the twenty-sixth somite of a 29s 
embryo. (Same embryo as Fig. 107.) 


Derm., Dermatome. My., Myotome. Scler., Sclerotome. V. ¢. p., Pos- 
terior cardinal vein. Other abbreviations as before. 


Fig. 109 is a section through the twentieth somite of the same 
embryo. The sclerotome is entirely mesenchymal, and its cells 
are extending between the notochord and aorta, and along the 
sides of the neural tube. The muscle-plate has now bent over 
so that its inner surface is being applied against the dermatome, 
but there is still a considerable cavity (myoccele) between the 
two, at the lateral angle of the dermo-myotomic plate. The 
lateral edge of the dermatome is freed from the nephrotome, and 
turns in to a slight extent. Other details are readily understood 
from the figure. 

The growth of the free edge of the muscle-plate towards the 
free lateral edge of the dermatome continues as illustrated in 


FROM TWELVE TO THIRTY-SIX SOMITES 1 


Peay 
3S x 
= 
a 
Oe 
s 
ae, 
suo: 
— 
ae 
Bans 
n 
Oo g 
ae) 
wes 
ai as 
Os 
GS 
oo ed 
S| 
o 5 
o R 
an 
= 2 
8 8 
are 
ey 
ro) 
= 
La 
~_ 
o~ 
eS) 
oO 
= 
=) 
mM 


is 


Neph. T., Nephrogenous t 


My’c., Myoccel. 


Fic. 109. — Transverse section through the twentieth somite of a 29s embryo. 
Am. F., Amniotie fold. 


188 THE DEVELOPMENT OF THE CHICK 


Figs. 109 and 110, until complete union of the two takes place 
(Fig. 111) and there is established a complete dermo-myotomic 
plate in each somite. This is usually known as the myotome, 
which therefore includes two layers; the external cutis-plate 
or dermatome, and the internal muscle-plate. With the eleva- 
tion of the axis of the body, the myotome gradually assumes 
a nearly vertical position. 


Fic. 110. — Transverse section through the seventeenth somite of a 29s 
embryo. (Same embryo as Fig. 107.) 
am. Cav., Amniotic cavity. E. E. B. C., Extra-embryonic body-cavity. 
Gn., Ganglion. mes’n. V., Mesonephric vesicle. $8.-Am., Sero-amniotic con- 
nection. Other abbreviations as before. 


Other details concerning the early history of the sclerotome 
are given in Chapter XIII, and it remains to add here only a short 
description of certain changes in the cells of the myotome (myo- 
blasts). In longitudinal sections the cells of the myotome are 
seen to become spindle-shaped soon after the folding towards 
the dermatome begins. The nuclei of the myoblasts are large 
and stain less deeply than those of adjoining tissues. They 
become elliptical in correspondence with the form of the cell- 
bodies. Each myoblast soon stretches from anterior to pos- 
terior faces of the somite, and this represents the first stage in 
the differentiation of the voluntary muscles. 

In later stages the myotomes send outgrowths into the limb- 
buds and ventral body-wall for the formation of the voluntary 


189 


TO 
) 


4 


FROM TWELVE TO THIRTY-SIX SOMITI 


‘A1OJod SB SUOTVIABIQGe JaYJQ ‘“UleA [RUTpavo-qng “d,s "A 


‘ i 


‘OAIQUIA SEE B JO opWUOS PALy}-AjUOM oY YFno«y, wuoyoos osdoasuvay, — “TET “Py 


RU ey 
ge Ce’ 
99 Me P94 g Dh, 


¢ 


190 THE DEVELOPMENT OF THE CHICK 


muscles of these parts. The voluntary muscles of the head, on 
the other hand (excepting the hypoglossus musculature), arise 
in front of the somites; the mesoblast from which they arise is, 
however, part of the original paraxial meroblast, in large part 
at least. It is important to note that the voluntary muscles 
are epithelial in origin. The involuntary, or smooth, muscle 
fibers, on the other hand, are mesenchymal in origin. 

The dermatome remains epithelial in all the somites well 
into the third day; the cells then begin to separate and form 
mesenchyme; this process begins at the anterior somites and 
proceeds backwards. The mesenchyme thus formed is the 
foundation of the derma. 

The Intermediate Cell-mass. This is the cord of cells uniting 
somite and lateral plate; it reaches its typical development only 
from the fifth to the thirty-third somites, in which it contributes 
to the development of the excretory system. Behind the cloaca, 
that is in the region of the tail, there is no lateral plate and no 
nephrotome. 

Origin of the Excretory System. The history of the excretory 
system in Amniota is of particular interest, because it shows a 
succession of three separate organs of excretion or kidneys, the 
first of which is a mere functionless rudiment, the second is the 
principal organ of excretion during embryonic life (at least in 
reptiles and birds), and the third finally becomes substituted 
for the second, which degenerates and is mostly absorbed; 
however, parts of the second remain and contribute to the 
formation of the organs of reproduction. The first, known as 
the head kidney or pronephros, is probably homologous to the 
permanent kidney of Amphioxus; the second or mesonephros, 
is the homologue, in part, of the permanent kidney of Anamnia, 
and the third or metanephros is the permanent kidney. The 
secreting parts of all arise from the intermediate cell-mass, though 
not in the same manner. The development of the metanephros 
does not begin until the fourth day; it is therefore not considered 
in this chapter. 

Pronephros and Wolffian Duct. The pronephros extends 
over only eleven or twelve somites, viz., from the fifth to the 
fifteenth or sixteenth inclusive; it consists originally of as many 
parts or tubules as the somites concerned. Each tubule arises 
as a thickening of the somatic layer of the intermediate cell- 


FROM TWELVE TO THIRTY-SIX SOMITES 191 


mass, which grows out towards the ectoderm in the form of a 
blind, solid sprout. The distal end of each turns backwards 
and unites with the one behind so as to form a continuous cord 
of cells, which is thus united with the intermediate cell-mass in 
successive somites by the original outgrowths. This cord of 
cells is the beginning of the Wolffian duct. Behind the sixteenth 
somite, the latter grows freely backwards just above the inter- 
mediate cell-mass until it reaches the cloaca with which it unites 
about the 31s stage. 


LG 
a7 
her 
Pats 
en 
tis = a 
_ Soil Ys LF ee 
CRT Fn Pre p “2 


Fig. 112. — A. Transverse section through the twelfth somite of a 16s em- 

bryo. 

B. Three sections behind A to show the nephrostome of the same pro- 
nephric tubule. 

V. ce. p., Posterior cardinal vein. c. C., Central canal. Ms’ch., mesen- 
chyme. n. Cr., Neural crest. N’st. Nephrostome. n. T., Neural tube. 
pr’n. 1, 2, Distal and proximal divisions of the pronephric tubule. 


The primary pronephric tubules are originally attached to 
the nephrotome opposite the posterior portion of the somite, 
about half-way between the somite and the lateral plate (Iigs. 
112 and 113). The part of the nephrotome between the attach- 
ment of the primary tubule and the lateral plate is continuous 
with the primary tubule and forms a supplementary part of the 
complete pronephric tubule; the remainder of the nephrotome 
then becomes converted into mesenchyme and the connection 
with the somites is lost (Figs. 112 and 113). Thus each pro- 
nephrie tubule forms a connection between the Wolffian duct 


192 THE DEVELOPMENT OF THE CHICK 


and the angle of the body-cavity; it consists of two parts, viz., 
the primary tubule and the supplementary part. It never pos- 
sesses a continuous lumen, though there is often a cavity in the 
supplementary part, which opens into the body-cavity through 
the nephrostome (ig. 112 B). 

The pronephros of the chick is a purely vestigial organ, of 
no apparent functional significance. Its development is accord- 
ingly highly variable, and it often happens that the nght and 
left sides of the same embryo do not correspond. It is also of 
very short duration and is usually completely lost on the fourth 
day. The tubules in the fifth to the tenth somites, moreover, 


SAT 


VWistverar vy Leh cee (15) 
a) 


Fig. 113. — Transverse section through the fifteenth somite of the same 
embryo. 
pr’n. (14), (15), Pronephrie tubules of the fourteenth and fifteenth somites, 
respectively. 


hardly pass the first stage when they appear as thickenings of the 
somatic layer of the somitie stalk; thus the Wolffian duct does 
not extend into this region, and the best developed pronephrie 
tubules are confined to the tenth to the fifteenth somites. 

The pronephric tubules do not form Malpighian corpuscles; 
but glomeruli develop as cellular buds at the peritoneal orifices 
of the posterior tubules, projecting into the calome near the 
mesentery. Curiously enough these do not form at the time of 
greatest development of the tubules, but subsequently to this 
when the tubules themselves are in process of degeneration. 
Moreover, they are extremely variable as to number, and degree 
of development. They appear to be best developed on the third 
and fourth days. They agree in many respects with the so-called 
external glomeruli of the pronephros of Anamnia, and should be 


FROM TWELVE TO THIRTY-SIX SOMITES 193 


homologized with these. On the other hand, they appear at the 
same time as the first glomeruli of the mesonephros (q. v.) and 
possess, by way of the intermediate tubules, undeniable resem- 
blance to the latter. 


At the stage of 10 somites the pronephros is represented by a series 
of thickenings of the somatic layer of the intermediate cell-mass extend- 
ing from the fifth somite backward to the segmental plate. In an embryo 
of 13 somites the connection between the somite and nephrotome is lost, 
and the pronephric tubules from the ninth to the thirteenth somites 
have united to form the beginning of the Wolffian duct. 

In an embryo of 16 somites a single pronephric tubule was found 
at the level of the hind end of the fifth somite, and was very distinct 
on one side but hardly discernible on the other. Its posterior continua- 
tion was soon lost, and the next distinct tubules were between the ninth 
and tenth somites; from here back there was a tubule opposite the hind 
end of each somite to the fifteenth, which was the last, and the duct was 
continuous. 

In an embryo of 21 somites, one finds only isolated remnants of the 
pronephros in front of the eleventh somite; from here to the fifteenth 
the tubules are well developed and retain their connection both with 
the Wolffian duct and the lateral plate. The Wolffian duct extends 
back of this place to the region of the posterior half of the segmental 
plate. 

At the 35s stage the pronephric tubules are much degenerated, 
but the nephrostomes usually remain. In one embryo there was found a 
well-developed pronephric tubule on each side in the thirteenth somite. 
That of the left side had a wide nephrostome, the lumen of which stopped 
short of the tubul ; the nephrostome of the right side was rudimentary. 
On the right side the Wolffian duct extended no farther forward, but 
on the left side it was continued to the eleventh somite, and rudimentary 
pronephric strands uniting it to the ccelomic epithelium existed in both 
eleventh and twelfth somites. Here the Wolffian duct stopped. But 
isolated pronephric rudiments and minute nephrostomes were found on 
both sides as far forward as the tenth somite. 


The Wolffian Duct. The Wolffian duct consists according to 
the foregoing account of two parts, (1) an anterior division formed 
by the union of the pronephric tubules, and (2) a posterior divi- 
sion that arises as an outgrowth of the anterior part. The latter 
grows backward above the intermediate cell-mass as a_ solid 
cord (Fig. 107), apparently by active multiplication of its own 
cells, without participation of the neighboring mesoderm or 


194 THE DEVELOPMENT OF THE CHICK 


ectoderm, until it reaches the level of the cloaca at about the 
sixtieth hour (30-318). It acquires a narrow lumen anteriorly 
at about the 25s stage; but the remainder is solid. At about 
the sixtieth hour the ends of the ducts fuse with broad lateral 
diverticula of the cloaca, and the lumen extends backwards 
until the duet becomes viable all the way into the cloaca (at 
about seventy-two hours, 35s stage). 

The Mesonephros or Wolffian Body. The mesonephros de- 
velops from the substance of the intermediate cell-mass between 
the thirteenth or fourteenth somites and the thirtieth somite. 
There are slight local differences in the relations of the tubules 
in front and those behind the nineteenth and twentieth somites, 
but in general the tubules may be stated to arise as epithelial 
vesicles derived from the intermediate cell-mass, which become 
transformed into tubules, one end of which unites with the Wolfhan 
duct and the other forms a Malpighian corpuscle in the manner 
described below. It will be seen that the anterior mesonephric 
tubules which are relatively rudimentary and of brief duration 
overlap the posterior pronephric tubules; they may possess neph- 
rostomes, whereas the typical mesonephric tubules formed behind 
them, which constitute the main bulk of the mesonephros, never 
possess peritoneal connections. 

An embryo with 29-30 somites is in a good stage for consid- 
ering the early development of the mesonephric tubules. If 
one examines a section a short distance behind the last somite, 
one finds that the intermediate cell-mass is a narrow neck of 
cells uniting the segmental plate and the lateral plate, and that 
the cells composing it are arranged more or less definitely in a 
dorsal and ventral layer, though some occur between. The 
primordium of the Wolffian duct occurs in the angle between 
the somatic mesoblast and the intermediate cell-mass, and the 
aorta lies in the corresponding angle of the splanchnic mesoblast. 
In the last somite (Fig. 107) one finds two important changes: 
(1) the intermediate cell-mass is much broader owing to multi- 
plication of its cells, and as a consequence the two-layered arrange- 
ment is lost; (2) whereas the cells of the intermediate cell-mass 
in the region of the segmental plate could not be delimited accu- 
rately from either the segmental or lateral plate, it is now easy 
in most sections to mark its boundary on both sides. It now 
constitutes, therefore, a rather well-defined but unorganized mass 


FROM TWELVE TO THIRTY-SIX SOMITES 195 


of cells between the somite and lateral plate, aorta and Wolffian 
duct; the posterior cardinal vein appears above the Wolfhan duct. 

The next change, found to begin in about the twenty-sixth 
somite, is a condensation of a portion of the cell-mass lying 
median to and below the Wolffian duct (Fig. 108), rendered evi- 
dent by the deeper stain in this region; the condensed portion 
of the original intermediate cell-mass is not, however, sharply 
separated from the remainder, but shades gradually into it both 
dorsally and ventrally, so that it can be seen to represent 
approximately the central part of the original middle plate. In 
view of its prospective function it may be called the nephrogenous 
tissue. Following it yet farther forward one finds that it is a 
continuous cord of cells with alternating denser and less dense 
portions, until in the twentieth somite (Fig. 109), the denser 
portions become discrete balls of radially arranged cells. In 
the eighteenth and seventeenth somites (Fig. 110) these become 
small thick-walled vesicles, which are situated median and ventral 
to the duct. Each vesicle is the primordium of a complete 
mesonephric tubule. Farther developed tubules are found in the 
fifteenth and sixteenth somites, and it is probable that the 
nephrogenous tissue forms mesonephric tubules in the four- 
teenth, thirteenth, and perhaps yet more anterior segments. 

The formation of the tubules proper from the vesicles may 
be studied satisfactorily in a 35s embryo (seventy-two hours). 
In the twenty-third somite of such an embryo the nephrogenous 
tissue and the nascent tubules he lateral to the Wolffian duct 
and below the median margin of the cardinal vein (Fig. 111). 
The Wolffian duct is triangular in cross-section with its longest 
and thinnest side next the ccelome. The most advanced vesicle 
in this region possesses a hollow sprout extending laterally to the 
Wolffian duct with which it is in close contact; this is the pri- 
mordium of the tubular part of the mesonephric tubule (ef. Fig. 
114 A and B). In more anterior somites it is found that such 
sprouts have fused with the wall of the duct in such a manner that 
the lumen of the tubule now communicates with that of the duct. 

Simultaneously the median portion of the original vesicle 
has been transformed into a small Malpighian corpuscle in the 
following manner: it has first become flattened so that the lumen 
is reduced to a narrow slit; then this double-layered disc becomes 
concave with the shallow cavity directed posteriorly and dorsally; 


196 THE DEVELOPMENT OF THE CHICK 


at the same time the convex wall becomes thin, and the concave 
thick. The entire tubule thus becomes S-shaped. Figs. 114 A, 
B, C, D illustrate the corresponding processes in the duck, which 
are similar in all essential respects to the chick. 


Fic. 114. — From a transverse series through a duck embryo of 45s, to 
show the formation of the mesonephric tubules. (After Schreiner.) 
Fig. 218 shows the position of the sections A, B, and C. 


V.c. p., Posterior cardinal vein. W. D., Wolffian duct. 
A. and B. represent tubules of the twenty-ninth segment. 
C. of the twenty-seventh segment. 

D. of the twenty-fourth segment. 


In the chick embryo of 35 somites the only differentiated 
tubules are in front of the twentieth somite, a region of the 
mesonephros that never develops far, and such tubules do not 
appear ever to become functional. In the region of the subse- 
quent functional mesonephros (twentieth to thirtieth somites) the 
development has not progressed beyond the stage of the vesicles 
showing the first indications of budding. 


FROM TWELVE TO THIRTY-SIX SOMITES 197 


The main part of the mesonephros is thus between the twen- 
tieth and thirtieth somites. In the anterior half of this region 
three or four rudiments of tubules are formed in each somite by 
the seventy-second hour. Subsequently five or six tubules are 
formed in each segment between the twentieth and thirtieth. 
Tubules are formed first from the ventral portions of the neph- 
rogenous tissue (see Fig. 111); those formed later arise from 
the unused portions. There is no evidence that they ever arise 
in any other way. The tubules may thus be divided according 
to the time of origin into primary, secondary, tertiary, etc., sets, 
but there is no morphological or functional distinction between 
the successive sets. (See Chap. XII.) 

The collection of tubules causes a projection or fold on each 
side of the mesentery into the body-cavity, known as the Wolffian 
body, the detailed history of which is given in Chapter XII. 


In conclusion it should be noted that the most anterior tubules 
of the Wolffian body possess peritoneal funnels like the pronephric 
tubules. Thus in an embryo of 30 somites I have noticed open perito- 
neal funnels in the eighth, ninth, twelfth, thirteenth, fourteenth, fifteenth, 
sixteenth, and seventeenth somites. It seems quite certain that the 
last of these belong to the mesonephros, though the most anterior are 
undoubtedly pronephric rudiments. In the eighteenth, nineteenth, 
twentieth, and twenty-first somites, small depressions of the peritoneum 
were noticed opposite tubules, but not communicating with them. 


The Vascular System. Soon after the thirty-third hour the 
heart begins to twitch at irregular intervals, and by the forty- 
fourth hour its beatings have become regular and continue unin- 
terruptedly. The contraction proceeds in the form of a rapid 
peristaltic wave from the posterior to the anterior end of the 
cardiac tube, and the blood, already present, is forced out in 
front. Through the aortic arches it reaches the dorsal aorta 
which distributes part to the body of the embryo, but most of 
the blood enters the vascular network of the yolk-saec. It is 
returned to the heart by various veins in the yolk-sac and em- 
bryo, and recommences the circuit. 

The development cf the vascular system will be more readily 
understood if we preface the account with a brief description of 
the anatomy of the system early in the fourth day (Fig. 115, 
ci. also Mies: 135 and: 136): 

The heart consists of four chambers, viz., the sinus venosus, 


198 THE DEVELOPMENT OF THE CHICK 


the atrium, the ventricular loop, and the bulbus arteriosus (Fig. 
116). 

The truncus arteriosus les in the floor of the pharynx and 
gives off the following vessels: (1) a short branch, the external 
carotid, extending into the mandibular arch; (2) complete arches 
in the second, third, and fourth visceral arches which join the 


elas taen Wee 


Via. 115. — The circulation in the embryo and yolk-sac between the eightieth 
and ninetieth hours of incubation, drawn from a photograph by A. H. Cole. 
The arteries are represented in solid black; the veins in neutral tint. A 
fold of the yolk-sac covers the fore part of the head. 

a. a. 2, 3, 4, Second, third, and fourth aortic arches. Ao., Aorta. Atr., 
Atrium. B. a., Bulbus arteriosus. Car. ext., External carotid. Car. int., 
Internal carotid. D. C., Duct of Cuvier. D. V., Duetus venosus. J., Jugu- 
lar vein (anterior cardinal). 1. a. V., Left anterior vitelline vein. p. V., 
Posterior vitelline vein. S. V., Sinus venosus. V. e. p., Posterior cardinal 
vein. Ven., Ventricle. V.O.M. L., Left omphalomesenteric vein. 


FROM TWELVE TO THIRTY-SIX SOMITES 199 


dorsal aorta; these are known as the second, third, and fourth 
aortic arches; the third arch is the largest. 


The original mandibular aortic arches unite with the anterior ends 
of the dorsal aorte, forming a loop on each side at the base of the fore- 
brain (Fig. 93), and they have, therefore, a different relation from the 
other aortic arches; it seems probable also that they have a different 
morphological value. The ventral limb of this loop disappears in its 
pre-oral part after this stage and a new vessel is formed entirely within 
the mandibular arch, bearing the same relation to the visceral arch as 
the other aortic arches. At the stage of 35 somites it is a complete arch, in 
some embryos at least (Fig. 117), though of very small caliber and very 
transitory, possibly sporadic, in its occurrence. It is possible that this 
is the true mandibular arch, and the pre-oral portion of the original 
mandibular arch should have another interpretation. Kastschenko 
suggests that it may have been related to lost pre-mandibular gill- 
clefts. 


The roots of the dorsal aorta above the pharynx receive the 
aortic arches and are continued forward as the internal carotid 
arteries, branching in the fore part of the head. Posteriorly the 
right and left aortic roots unite just behind the fourth visceral 
pouch to form the dorsal aorta, and this continues as an undi- 
vided vessel to about the level of the twenty-second somite, 
where it divides into right and left dorsal aorte, and at the 
same time sends out a large omphalomesenteric artery into the 
yolk-sac on each side, and these branch as shown in Figure 115 into 
the capillary network of the yolk-sac. The dorsal aorte, now 
much diminished in size, continue back into the tail where they 
are known as the caudal arteries. The dorsal aorta also sends off 
a pair of segmental arteries into each intersomitic septum, and a 
pair of small allantoic arteries into the primordium of the allantois. 

The veins enter the heart through three main trunks: (1) the 
ductus venosus, (2 and 3) the paired ducts of Cuvier. These 
are made up as follows: (1) the ductus venosus is formed at the 
level of the posterior liver diverticulum by the right and left 
omphalomesenteric veins, which arise in the yolk-sac by union 
of the capillaries of the vascular area; the right vitelline vein 
also receives two veins coming directly from the anterior and 
posterior ends respectively of the sinus terminalis, the anterior 
of these is frequently partly double owing to its mode of origin. 
(See beyond, Chap. VII.) The vascular area in the yolk-saec thus 


200 THE DEVELOPMENT OF THE CHICK 


appears strikingly bilateral at this time. (2 and 3) The ducts of 
Cuvier are made up by the union of all the somatic veins. Each 
is formed primarily by the union of the anterior and posterior 
cardinal veins. The anterior cardinal vein receives all the blood 
of the head, and thus includes the first three segmental veins. 
It also receives at its point of Junction with the posterior cardinal 
vein a branch from the floor of the pharynx, the external jugular 
vein. The posterior cardinal vein receives (1) all the segmental 
veins of the trunk, of which there are twenty-nine pairs, running 
in the intersomitic septa between the fourth and thirty-third 
somites, and the veins of the Wolffian body of which there are 
several to each somite concerned, as described in the account 
of that organ. 

The development of the vascular system up to the stage just 
described will now be taken up. 

Development of the Heart. (a) Changes in the External Form. 
In the last chapter we traced the origin of the heart up to the 
time when it is a practically straight, undivided, somewhat 
spindle-shaped tube lying below the floor of the pharynx, to which 
it is attached by its dorsal mesentery (mesocardium). Posteriorly 
its cavity divides into the omphalomesenteric veins which run 
in the side-walls of the anterior intestinal portal. The heart is 
lengthened backwards by the conecrescence of the omphalo- 
mesenteric veins and the most posterior division of the heart 
(the sinus venosus) is established in this way between the stages 
of 12 and 18 somites; it is marked by a broad fusion with the 
somatopleure (mesocardia lateralia) through which the ducts of 
Cuvier enter the heart. 


At the stage of sixteen somites the duct of Cuvier lies opposite 
the hind end of the second somite on the right side, and a little farther 
back on the left side; and the somato-cardiac fusion (mesocardium 
laterale) in which it lies is of the width of about one and a half somites. 
On the right side the duct of Cuvier lies a little in front of, and on the 
left side a little behind, the point of union of the omphalomesenteric 
veins; thus the posterior end of the heart is not fully formed at the 
stage of 16s, but is at the stage of 18s. The subsequent fusion of the 
omphalomesenteric veins produces the so-called ductus venosus, or 
main splanchnic vein, which is therefore a posterior continuation of the 
sinus venosus. 


The cardiac tube proper lies between the origin of the aortic 


FROM TWELVE TO THIRTY-SIX SOMITES 201 


arches at the anterior end and a point little behind the entrance 
of the ducts of Cuvier into the heart at the posterior end. 

Two main changes characterize the development of the heart 
in the period under consideration: (1) folding of the cardiac tube 
and (2) differentiation of its walls in successive regions to form 
the four primary chambers of the heart, viz. (from behind for- 
wards), the sinus venosus, the auricular division (atrium), the 
ventricular division and the bulbus arteriosus. 

The folding of the heart is caused by the rapid growth between 
its anterior and posterior fixed ends, and the places of folding 
are determined largely by differences in the structure of the walls 
at various places. The folding begins by a curvature to the 
right, and this proceeds until the tube has an approximately 
semicircular curvature (Fig. 72). At a certain place in the 
curved tube a very pronounced posterior projection takes place 
(Figs. 73 and 74), and at the same time this bent portion turns 
ventrally; the apex of the bend represents the future apex of the 
ventricles. The continuation of these two directions of folding 
then brings the ventricular division of the heart immediately 
beneath the sinu-auricular division which is attached dorsally 
by the somato-cardiac connections; further continuation brings 
the apex of the heart a little behind the auricular portion (Figs. 
85, 87, 88, 93, 99). During all this period the distance between 
the two fixed ends has remained practically constant. 

During the process of folding, constrictions have arisen 
between successive portions of the cardiac tube, owing to expan- 
sion of intervening portions, and thus at the stage of seventy-two 
hours the heart shows the following divisions and form. From 
the dorsal surface (in a dissection, Fig. 116) one sees (1) the sinus 
venosus, broad behind and narrow in front where it joins the 
auricular division; it receives three veins: (a) the large ductus 
venosus, appearing as a direct posterior continuation of the sinus, 
and separated from it by only a slight constriction; and (b and c) 
the right and left ducts of Cuvier entering the sinus laterally 
and dorsally near its enlarged posterior end; (2) the sinus enters 
the atrium through the dorsal wall; the atrium shows two lateral 
expansions, the future auricles, of which the left is much the 
more expanded at this time; the sinus appears partly sunk in 
the right auricle. (3) Only the right limb of the ventricular 
loop is visible from the dorsal surface at this time, and is separated 


202 THE DEVELOPMENT OF THE CHICK 


from (4) the bulbus arteriosus by a slight constriction. The 
bulbus thus lies on the right side; it sweeps around the atrium 
anteriorly to the middle line and then bends up to enter the floor 
of the pharynx. 

From the ventral side one sees the looped ventricular division 
behind, in which we distinguish 
right and left limbs, the former 
of which enters the bulbus in 
front, and the latter the auricles. 
These two limbs represent ap- 
proximately the future right 
and left ventricles (Fig. 198, 
Chap: X11). 

In an ordinary entire mount 
of this stage the heart is seen 
from the right side, and the dis- 
position of the parts may be 
readily understood by reference 
to Fig. 117, and the preceding 


description. 


Fria. 116 .— Heart of a chick embryo i ; Hae Suen 
- other change that s 

of 72 hours, dissected out and drawn Another ¢ 1aee sie saan 

fromm therdareal cuviace: be noted here is the disappear- 


Aur. 1, Left auricle. Aur.r., Right ance of the mesocardium during 
sume a US grea the folding of the cardiae tube, 
Cuvier. D. V., Ductus venosus. Du Vep TE XCept in the region of the 
Sins venowic Tr runes arte sinus venosus where it remains 

permanently and becomes much 
broadened (seventy-two hours). 

(b) Changes in the Internal Structure of the Heart. We have 
already seen that the heart consists of two primary layers, viz., 
the endocardium, which is endothelial in nature, and the myo- 
eardium, which is derived from the splanchnic mesoblast. The 
distinction between the sinu-auricular and the bulbo-ventricular 
divisions of the heart is indicated internally at about the time 
the first external evidence is seen, by the fact that the endocar- 
dium is more closely applied to the myocardium in the former 
than in the latter division. In the sinus and atrium but little 
change takes place in the period under consideration. In the 
ventricle, on the other hand, and especially in the right limb, 
the wide space originally existing between endocardium and 


FROM TWELVE TO THIRTY-SIX SOMITES 203 


myocardium becomes more or less filled by multiplication of 
the endocardial cells. On the side of the myocardium there is 
first a thickening, and then anastomosing processes are sent out 
towards the endocardium. Cavities also arise within the thick- 
ened myocardium and all communicate. The endocardial cells 
then form a covering to all myocardial processes and cavities, 
and the cavities thus lined communicate with the main endo- 
cardial cavity. Thus the wall of the ventricles becomes spongy 
and all the cavities in it are lined by a layer of endocardium 
and communicate with the endocardial cavity. In the bulbus 
finally there is a great thickening of the endocardium produced 
by multiplication of its cells, but no corresponding change in 
the myocardium; thus the bulbus at seventy-two hours shows 
a thin myocardial and a thick endocardial wall. The later 
development is described in Chapter XIT. 

The Arterial System. The description of the development of 
the arterial system proceeds from the stage of 12 somites described 
in the last chapter. 


The following should be added to the account there given. At this 
stage Kastschenko finds three pairs of small arterial vessels in front of 
the first visceral pouch running from the dorsal towards the ventral 
aorta, which, however, they do not meet. At about forty-six hours 
the first two of these have disappeared. The third, however, has become 
almost as large as the hyoid aortic arch. Kastschenko thinks it prob- 
able that this is the true mandibular arch. Though he did not find it 
in connection with the ventral aorta, he thinks it may form such a union 
of short duration. I have actually found such a vessel joining the man- 
dibular arch to the dorsal aorta in an embryo of 35 somites. On the 
other hand, what we have previously called the mandibular arch may 
be the true one displaced in the course of phylogeny. 


The Aortic Arches. An arch of the aorta is formed in each vis- 
ceral arch; they arise successively as buds from the roots of the dor- 
sal aorta in the order and time of formation of the visceral arches. 
Thus the first or mandibular aortic arch is formed at the stage of 
9-10 somites; the second or hyoid aortic arch arises from the dor- 
sal aorta at about the stage of 19s and joins the ventral aorta at 
about the 24s stage. The third is completely formed at the stage 
of 26 somites. The fourth is completely formed at the stage of 36 
somites; and the fifth and sixth arise during the fourth and fifth 
days. (See Chap. XII for account of the fifth and sixth arches.) 


204 THE DEVELOPMENT OF THE CHICK 


The first aortic arch loses its connection with the dorsal aorta 
at about the stage of 30 somites, and the second arch similarly 
during the fourth day; the ventral ends of these arches retain 
their connection with the ventral aorta and constitute the begin- 
ning of the external carotid. Thus the third, fourth, fifth and 
sixth aortie arches remain. Their transformation belongs to the 
subject-matter of Chapter XII. 

The pulmonary artery appears as a posterior prolongation of 
the ventral aorta on each side at about the 35s stage. It thus 
appears successively in later stages as a branch from the base of 
the fourth and sixth aortic arches. 

The Internal Carotids. The loop where the mandibular arch 
joins the dorsal aorta may be called the carotid loop; it is situated 
in front of the oral plate at the base of the fore-brain on each 
side (Fig. 93). It enlarges to form a sac, and when the connec- 
tion with the mandibular arch is lost, sends out branches into 
the tissue surrounding the brain. These are of course a direct 
continuation of the dorsal aorta on each side. 

The segmental arteries are paired branches of the dorsal aorta 
in each intersomitic septum. They pass dorsally to about the 
center of the neural tube and arch over laterally to enter the 
segmental veins, and thus unite with the cardinal veins. 

The Development of the Venous System. The main outlines 
of the development of the venous system have been already 
considered. 

The somatic veins, 7.e., the anterior and posterior cardinal 
veins and their branches, enter the sinus venosus through the 
ducts of Cuvier. The original position of this duct as we have 
seen is about the level of the second somite. The formation of 
the cervical flexure, however, carries a number of somites forward 
above the heart. so that at about the stage of 32s it comes to 
lie in the region of the eighth and ninth somites. The relation 
between the somatopleure and the heart in this region has been 
already described. 

The anterior cardinal veins are the great blood-vessels of the 
head, and become the internal jugulars in the course of develop- 
ment. Owine to the order of development of the body, the 
anterior cardinals are formed before the posterior cardinals. At 
the 15-16s stage they lie at the base of the brain, dorsal and 
lateral to the dorsal aorte, and extend forward to the region of 


FROM TWELVE TO THIRTY-SIX SOMITES 205 


the diencephalon. They le internal to the cranial nerves and 
pass just beneath the auditory pits. 

As the brain develops many branches of the anterior cardinal 
veins arise, the most conspicuous of which at seventy-two hours 
are a large branch just behind the auditory sac, one between the 
auditory sac and the trigeminal ganglion, an ophthalmic branch 
extending along the base of the brain to the region of the optic 
stalks and a network of vessels on the lateral surfaces of the 
fore-brain. The other branches of the anterior cardinal vein 
are the three anterior intersomitic veins (Fig. 115); the external 
jugular from the floor of the pharynx enters the duct of Cuvier 
just beyond the union of the anterior and posterior cardinal veins. 

Up to about forty-eight hours the anterior cardinal veins lie 
median to the cranial nerves, but between this time and seventy- 
two hours the facial and glossopharyngeal nerves cut completely 
through the vessel and thus come to lie median to it; the trigem- 
inus and vagus continue to lie lateral to it. 

The posterior cardinal arises as a posterior prolongation from 
the duet of Cuvier and grows backward above the Wolffian duct, 
keeping pace with the differentiation of the intermediate cell- 
mass, as far as the thirty-third somite. It does not enter the 
caudal region of the body. As already described it receives 
twenty-nine intersomitic veins and the veins of the Wolffian 
body. At first its connection with the duct of Cuvier is by 
means of a network of vessels, which gradually gives place to a 
single trunk (cf. Fig. 117). 

The Splanchnic Veins. The ductus venosus is the unpaired 
vein immediately behind the sinus venosus, formed by fusion of 
the two omphalomesenteric veins. It is fully formed at the stage 
of 27 somites. Its relations to the liver have already been de- 
scribed in connection with that organ. Its subsequent changes 
are described in Chapter XII. 

The vitelline veins are united at about the stage of seventy- 
two hours by a loop passing over the intestine immediately 
behind the pancreas. (See Chap. XII.) 


VII. Tue Bopy-caviry AND MESENTERIES 
The origin of the dorsal and ventral mesenteries was con- 
sidered in the section of this chapter dealing with the ali- 
mentary canal. As noted there, the dorsal mesentery extends 


206 THE DEVELOPMENT OF THE CHICK 


Li Crk 
ae Gah as 


ae 
(his C7, A H 


Z Gig. K 
If WY eK AAW Z 
(ee 


SE a 


fp & a, ] 
ss Se 


Tia. 117. — Entire embryo of 35s, drawn as a transparent object. 
a.a. 1, 2, 3, 4, First, second, third, and fourth aortie eae Ar., 
Artery. A. V., ¥ itelline artery. cerv. Fl., Cervical flexure. wot ie 


Cranial flexure. D. C., Duct of Cavicn DV: Ductus venosia! 
Ep., Epiphysis. Gn. V., Ganglion of trigeminus. Isth., Isthmus. 
Jug. ex., External jugular vein. Md., Mandibular arch. M. M., 
Maxillo-mandibular branch of the trigeminus. — olf. P., Olfactory pit. 
Ophth., Ophthalmic branch of the trigeminus. Ot., otoeyst.  V., 
vein. W. B., Wing bud. V. c. p., Posterior cardinal vein. V. 
umb., Umbilical vein. V. V., Vitelline vein. VY. V. p., Posterior vitel- 
line vein. 


FROM TWELVE TO THIRTY-SIX SOMITES 207 


the entire length of the alimentary canal, while the ventral 
mesentery persists only in the region of the fore-cut and the 
cloaca. 

The embryonic body-cavity shows two divisions from a very 
early stage, viz., (1) the large cephalic or parietal cavity situated 
in the pharyngeal region of the head and containing the heart, 
and (2) the general ccelomic cavity of the trunk. After 
the heart is established in the middle line the parietal cavity 
is bounded posteriorly by the wall of the anterior intestinal portal 
(Figs. 75, 85, ete.), but it communicates with the pleuroperi- 
toneal cavity around the sides of the portal, in which the vitelline 
veins run. Laterally the parietal cavity communicates with the 
extra-embryonic body-cavity. 

The mesocardia lateralia are also an important landmark in 
the embryonic bedy-cavity because from them proceed the par- 
titions that subsequently separate the pericardial and pleural 
eavities on the one hand, and the pleural and peritoneal body- 
cavities on the other. (See Chap. XI.) The primordium of the 
lateral mesocardia may be recognized in the 10s stage: just behind 
the heart the median portion of the body-cavity is thick-walled, 
the peritoneal cells being actually columnar. At this place, a 
short distance lateral to the median angle of the body-cavity, 
and at the junction of the cylindrical and flat mesothelium, a 
fusion of considerable longitudinal extent is formed between 
the somatopleure and the proximal portion of the vitelline veins, 
projecting up from the splanchnopleure; this fusion is the begin- 
ning of the lateral mesocardium. It separates a more median 
portion of the body-cavity from a more lateral, and in it the 
duct of Cuvier soon develops. 

When this portion of the body of the embryo becomes ele- 
rated (forty to fifty hours) the portion of the body-cavity lateral 
to the mesocardia lateralia comes to le ventrally to the median 
portion (cf. Fig. 69), and at the same time the lateral mesocardia 
rotate around a longitudinal axis through an angle of about 
90°, so that the original median border becomes dorsal, and the 
original lateral border becomes ventral. The dorsal divisions, 
right and left, of the pleuroperitoneal cavity may now be called 
the pleural grooves. Inasmuch as the parietal cavity has receded 
considerably at the same time into the trunk with the elongation 
of the fore-gut, it comes to lie beneath the pleural grooves 


208 THE DEVELOPMENT OF THE CHICK 


instead of in front of them as before. Therefore in cross-sections, 
in front of the lateral mesocardia, the pleural grooves appear as 
dorsal projections of the parietal cavity, separated from one 
another in the middle line by the caesophagus (Fig. 118). 

The relations of the three divisions of the embryonic body- 
cavity thus established may be described as follows: the parietal 
cavity contains the heart, and is therefore the prospective peri- 


Fic. 118. — Transverse section of an embryo of 385s, imme- 
diately in front of the lateral mesocardia. 
Ao., Aorta. Atr., Atrium. B.a., Bulbus arteriosus. D.C. 
r., and l., Right and left duets of Cuvier. Lg., Lung. m’s’e. 
dors., Dorsal mesocardium. m’s’t. dors., Dorsal mesentery. 
P.C., Pericardial cavity. pl. gr., Pleural groove. Ree. pul. 
ent., Recessus pulmo-entericus. 5. V., Sinus venosus. 


cardial cavity. It is not, however, a closed cavity, but ecommuni- 
cates in front of the lateral mesocardia with the pleural grooves 
(Fig. 118), and by way of the latter above the lateral mesocardia 
with the peritoneal cavity (Figs. 119 and 120); a second communi- 
cation of the parietal cavity with the peritoneal cavity is beneath 
the lateral mesocardia around the sides of the anterior intestinal 
portal, now being converted into the septum transversum (cf. 


FROM TWELVE TO THIRTY-SIX SOMITES 209 


Fig. 120). A more complete description of the cavities is given 
in Chapter XI. 

The median wall of the pleural grooves forms much mesoblast 
during the formation of the lung diverticula, and thus initiates 
the formation of lobes enclosing the lungs (Figs. 118 and 119). 
These lobes descend ventrally and unite with the septum trans- 
versum (see below), thus producing blind bays of the ccelome 


Fia. 119. — Transverse section of the same embryo through the 
lateral mesocardia. 

Liv., Liver. m/’s’e. lat., Lateral mesocardium. m/’s’t. access., 
Accessory mesentery. m’s’t. ven., Ventral mesentery. Other 
abbreviations as before. 

at the sides of the oesophagus, known as the superior recesses 
of the peritoneal cavity or pulmo-enteric recesses. 

The ventral mesentery extends from the anterior end of the 
sinus venosus to the hind end of the fore-gut, where it unites 
with the ventral body-wall. It includes the sinus venosus and 
the ductus venosus, together with the hepatic diverticula. The 
median and lateral mesocardia, together with the ventral mesen- 
tery of the fore-gut, form a mass known as the septum transversum. 


210 THE DEVELOPMENT OF THE CHICK 

At the stage of seventy-two hours, then, the pleural, pericar- 
dial and peritoneal divisions of the body-cavity are indicated, 
but all are in communication. The pleural cavities connect 
with the peritoneal cavity posteriorly, and with the pericardial 
cavity anteriorly in front of the lateral mesocardia (Figs. 118, 
119, 120); and the pericardial cavity communicates with the 


St. yey 


S-Qm ._ 


Viumb-. 


Lire ——<T 


Fia. 120. — Transverse section of the same embryo immediately 
behind the lateral mesocardia. 
ant. hep. Div., Anterior hepatic diverticulum. Duod., Duo- 
denum. End’e., Endoeardium. D.V., Ductus venosus. My’e., 
Myocardium. Pl. m’s’g., Plica mesogastrica. S-am., Sero-am- 
niotie connection. ven. r., l., Right and left limbs of the ven- 
tricle. V. umb., Umbilical vein. 


peritoneal cavity beneath the lateral mesocardia around the 
roots of the vitelline veins (sides of the anterior intestinal portal). 
Thus the ducts of Cuvier and the vitelline veins are the agencies 
that introduce the separation of the body-cavities. 

The tail-fold forms blind caelomic pockets in the region of 
the hind-gut, which end in the region of the thirty-third somite. 


(Cf. Fig. 81.) 


PART Il 


THE FOURTH DAY TO HATCHING 
ORGANOGENY, DEVELOPMENT OF THE ORGANS 


CHAPTER VII 


THE EXTERNAL FORM OF THE EMBRYO AND THE 
EMBRYONIC MEMBRANES 


I. THe EXTERNAL FoRM 
General. The development of the external form of the em- 
bryo is conditioned by the order of development of the organs. 
The early form is thus given by the nervous system, somites 


ae et / 


A B 
Fig. 121.— A. Embryo of 3 days’ and 16 hours’ incubation. x 5. 
B. Embryo of 5 days’ incubation. x5. (After Keibel and Abra- 
ham.) 


and viscera. The development of muscles, bones, limbs, etc., that 
define the form of the fowl, begins relatively late, and only gradu- 
ally conceals the outlines of the internal parts. 
Figs. 121 to 124 illustrate the development of the external 
PA 


212 THE DEVELOPMENT OF THE CHICK 


form from three days sixteen hours to ten days. In Fig. 121 A 
(three days sixteen hours) the form of the head is defined by 
the brain, eves, and visceral arches. The cervical flexure is 
strongly marked. There is no neck. The heart makes a large 
protuberance immediately behind the head. The limb-buds are 
rounded swellings. In Fig. 121 B (five days one hour) the cer- 
vical flexure is less marked; the enlargement of the mid-brain 


Fig. 122. — Embryo of 7 days’ and 7 hours’ 
incubation x 5. (After Keibel and Abra- 
ham.) 


makes a more pronounced protuberance of the head in this region; 
the heart has retreated farther back into the thorax, and the 
neck is thus indicated. The main divisions of the limbs are 
beginning to appear. In Fig. 122 (seven days seven hours) 
there are marked changes: The cervical flexure is practically 
lost. The elevation of the head and retreat of the heart into 
the thorax have produced a well-marked neck. The upper 


EMBRYO AND EMBRYONIC MEMBRANES 213 


portion of the first visceral cleft alone is visible as the external 
auditory meatus; the other visceral arches and clefts have prac- 
tically disappeared, excepting the mandibular arch, forming the 
lower jaw. The abdominal viscera begin to protrude. In the 
next stage, Fig. 123 (eight days), the contours of the body are 
decidedly bird-like; feather germs have appeared in definite 


Fig. 123.— Embryo of 8 daysx 5. (After Keibel and Abrabam.) 


tracts; the fore-limbs are wing-like. The contours of the head 
are much smoother, and determined more by the development 
of the facial region and skull than by the brain. The protuber- 
ance of the ventral surface caused by the viscera is strongly 
marked. Fig. 124 finally shows a ten-day embryo. 

Head. The embryonic development of the head depends on 
the changes in three important classes of organs, together with 


214 THE DEVELOPMENT OF THE CHICK 


their supporting and skeletal structures and accessory parts: 
(a) the central nervous system, (6) the organs of special sense, 
and (ce) the visceral organs, mouth and pharynx. The origin of 
all these parts has been considered, and it is proposed to take 


Kia. 124. — Embryo of 10 days and 2 hours x 5. (After Keibel and Abraham.) 


up here only the development of the external form of the head. 
The preceding section gives an account sufficient for cur present 
purposes, except in the ease of the facial region. At four days 
this region appears as follows (Fig. 125): the mouth is a large, 
‘-defined opening, bounded behind by the mandibular arches, 


EMBRYO AND EMBRYONIC MEMBRANES 215 


at the side by the maxillary processes, and in front by the naso- 
frontal process, which is a broad projection below the cerebral 
hemispheres overhanging the mouth. On each side of the naso- 
frontal process are the olfactory pits, the cavities of which are 
continuous with the oral cavity. Lateral to the olfactory pits 
are the external nasal processes, abutting against the eye and 
separated from the maxillary process by the lachrymal groove. 
The portion of the naso-frontal process bounding the olfactory 
pits on the median sides may be called the internal nasal process. 


Fig. 125. — Head of an embryo of 4 days’ in- 
cubation, from the oral surface (N. L. 6 
mm.) 


Ep., Epiphysis. Hem., Cerebral hemi- 
sphere. Hy., Hyoidarch. 1. nas. pr., Lateral 
nasal process. Md., Mandibulararch. Mx., 
Maxillary process. nas. fr., Naso-frontal pro- 
cess. Olf., Olfactory pit. Or., Oral cavity. 
Ph., Pharynx. v. A. 3, Third visceral arch. 


During the fourth and fifth days a fusion is gradually formed 
between the internal nasal process on the one hand, and the 
external nasal and maxillary processes on the other (Fig. 126), 
thus forming a bridge across the open mouth of the olfactory 
pits and dividing the openings in two parts, one within the oral 
cavity, which becomes the internal nares or choane, and one 
without, which becomes the external nares or nostrils. During 
the same time the whole naso-frontal process begins to project 


216 THE DEVELOPMENT OF THE CHICK 


forward to form the tip of the upper jaw. The two mandibular 
arches have also fused in the middle line and begin to project 
forward to form the lower jaw. This projection of upper and 
lower jaw causes a great increase in the depth of the oral cavity 
(Fig. 147). 

The upper jaw is thus composed of three independent parts: 
viz., the median part formed from the naso-frontal process and 


Fic. 126. — Head of an embryo of about 5 days 
from the oral surface. (N. L. 8 mm.) 
ch. F., Choroid fissure. E. L., Eye-lid (nie- 
titating membrane). ex. nar., External nares. 
1. Gr., Lachrymal groove. Other abbreviations 
as before. 


the two lateral parts formed from the maxillary processes. The 
former becomes the intermaxillary and the latter the maxillary 
region. 
Il. Empryronic MEMBRANES 

General. The extension of the blastoderm over the surface 
of the yolk goes on very rapidly up to the end of the fourth day 
of incubation (Fig. 33), at which time there is left a small cir- 
cumseribed area of uncovered yolk, that may be called the 
umbilicus of the yolk-sac, which remains uncovered for a long 
time. Its final closure is associated with the formation of the 
albumen-sac. 


EMBRYO AND EMBRYONIC MEMBRANES 217 


The splitting of the mesoblast is never complete; but on the 
contrary the undivided margin begins to thicken after the fourth 
day, and gradually forms a ring of connective tissue that surrounds 
the umbilicus of the yolk-sac (Figs. 128 and 129). When this 
ring closes, about the seventeenth day, it forms a mass of con- 
nective tissue uniting the yolk-sac and albumen-sac. (See 
below). 

During the first few days of incubation the albumen loses 
water rapidly, and becomes more viscid, settling, as this takes 
place, towards the yolk-sac umbilicus. Thus the amniotic sac 
containing the embryo lies above; beneath the amniotic sac comes 
the yolk, and the main mass of the albumen lies towards the 
caudal end of the embryo (Figs. 128 and 129). 

The allantois expands very rapidly in the extra-embryonic 
body-cavity, and the latter extends by splitting of the mesoblast 
into the neighborhood of the yolk-sac umbilicus. When the 
allantois in its expansion approaches the lower pole of the egg, 
it begins to wrap itself around the viscid mass of the albumen 
accumulated there. In so doing, it carries with it a fold of the 
chorion, as it must do in the nature of the case, and thus the 
albumen mass begins to be surrounded by folds of the allantois 
with an intervening layer of the duplicated chorion. These 
relations will be readily understood by an examination of the 
accompanying diagrams (Figs. 128 and 129). In this way an 
albumen-sac, which rapidly becomes closed, is established out- 
side of the yolk-sac, and the two are united by the undivided 
portion of the mesoblast around the yolk-sac umbilicus. This 
connection is never severed, and in consequence the remains of 
the albumen-sac is drawn with the yolk-sac into the body-cavity 
towards the end of incubation. 

The sero-amniotic connection, which persists throughout incu- 
bation, has an important effect on the general disposition of the 
embryonic membranes. It is formed, as we have seen, in the 
closure of the amnion, by the thickened ectoderm of the suture; 
this ectodermal connection is, however, absorbed and replaced 
on the fifth to the seventh days by a broad mesodermal fu- 
sion, which maintains a permanent connection between amnion 
and chorion. One important result of this relation is that the 
albumen-sac, which is formed by the duplication of the chorion, 
is prolonged by a tubular diverticulum to the sero-amniotie 


218 THE DEVELOPMENT OF THE CHICK 


plate (see Figs. 128 and 129). The latter becomes perforated 
after the eleventh day, and there is thus direct communication 
between the albumen-sac and the amniotic cavity. Hirota 


Fras. 127, 128, and 129. — Diagrams of the relations of the embryonic mem- 
branes of the chick, constructed from preparations, and from figures and 
descriptions of Duval, Hans Virchow, Hirota and Fiulleborn. In these 
figures the ectoderm and entoderm are represented by plain lines: The 
mesoderm by a cross-hatched line or band. The yolk-sac is represented 
by broken parallel lines. In Fig. 127 the allantois is represented as a sac. 
In Figs. 128 and 129, 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 em- 
bryo. The actual relations of the stalk is shown in Figures 33 and 82. 

Alb., Albumen. Alb. S., Albumen-sac. All., Allantois. All. 1, Inner 
wall of the allantois. All. C., Cavity of allantois. All. S8., Stalk of allantois. 

All. + Am., Fusion of allantois and amnion. Am., Amnion. Am. C., 

Amniotic cavity. Chor., Chorion. C. T. R., Connective tissue ring. Eet., 

Jetoderm. E. E. B. C., Extra-embryonie body-cavity. Ent., Entoderm. 

Mes., Mesoderm. S.-Am., Sero-amniotic connection. S. Y. 8S. U., Sae of 

the yolk-sae umbilicus. Umb., Umbilicus. V. M., Vitelline membrane. 

Y.S.8., Septa of the yolk-sac. 

Fic. 127. — 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 represented as a sac, the stalk of which enters the umbilicus 
behind the yolk-stalk; the allantois lies in the extra-embryonic body-cavity, 
and its mesoblastic 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 undivided portion is slightly thickened to form 
the beginning of the connective tissue ring that surrounds the yolk-sae 
umbilicus. The ectoderm and entoderm 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. 

Fig. 128. — Ninth day of incubation. The yolk-sae umbilicus has become 
much narrowed; it is surrounded by the mesodermal connective tissue 
ring, and by the free edges of the ectoderm and entoderm. The vitelline 
membrane still covers the yolk-sac umbilicus and is folded into the albumen. 
The allantois 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-sae is likewise formed by a duplication of the chorion and allan- 
tois: 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. 


EMBRYO AND EMBRYONIC MEMBRANES 


219 
| {Chor 
ae = a — “Unb 


nt 


ye 
EA 
‘S) 


i 


220 THE DEVELOPMENT OF THE CHICK 


states that, after this connection is established, the amniotic 
fluid coagulates in alcohol, “just like the fluid in the albumen- 
sac; owing, presumably, to the presence of albumen which has 
found its way through the perforations into the amniotic fluid.” 
This observation is confirmed by Fulleborn. 

The Allantois. The part of the wall of the allantois that 
fuses with the chorion may be called the outer wall; the remainder 
of the sae of the allantois constitutes the inner wall. The distal 
intermediate part of the allantois is specialized as the wall of the 
albumen-sac. 


All+Am, 


Fig. 129. — Twelfth day of incubation. The conditions 
represented in Fig. 128 are more advanced. The albu- 
men-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 umbilicus of 
the yolk-sae is much reduced, and some yolk protrudes 
into the albumen (sae of the yolk-sae umbilicus). 


In the outer wall there are three layers, viz., an internal epi- 
thelial layer, formed by the entoderm of the allantois; a thick 
very vascular middle or mesodermal layer, formed by fusion of 
the mesoblast of allantois and chorion; and a thin, outer, ecto- 
dermal layer derived from the chorion. 


EMBRYO AND EMBRYONIC MEMBRANES 221 


Rate of Growth of the Allantois. As the embryo lies on its 
left side, the allantois grows out on the right side of the embryo 
(Figs. 127 and 130 A) and unites with the chorion about the 
one hundredth hour. It then spreads rapidly as a flattened sac 
over the embryo, increasing the extent of the fusion with the 


77. C—-- 


ALE 


Fic. 130. — Diagrams showing the relations of the allantois, 
represented by the tinted area, at different ages. (After 
Hirota.) 


Alb., Albumen. Alb. S., Edge of albumen-sac. All. V., 
Allantoic vein. am. C., Amniotic cavity. S.-Am., Sero-amni- 
otic connection. Y.S., Yolk-sac. 

A. At uel hours showing only the amniotic cavity and al- 
lantois x ‘ 

B. At 44 hours, showing only the amniotic cavity and al- 
lantois x 1.2. 

C. At 192 hours; the entire yolk x .66. The dotted out- 
line represents the amniotic cavity. 

D. At214hours. The entire egg after removal of the shell, 
x .66. The albumen mass is at the left; the albumen-sac is be- 
ginning to form. 


chorion, hence of its outer wall pari passu. At the end of the 
fifth day it covers more than half of the embryo (Fig. 130 A); 
at the end of the sixth day the embryo is entirely covered by 


222 THE DEVELOPMENT OF THE CHICK 


the allantois (Fig. 130 B); at the end of the eighth day the allan- 
tois has covered half of the yolk-sac (Fig. 130 C). At the end 
of the ninth day, the formation of the albumen-sac is begun 
(fig. 130 D). At the end of the eleventh day, the albumen-sae 
is practically closed at the lower pole. On the twelfth day, the 
albumen-sac is closed, and on the sixteenth day the contents 
are practically entirely absorbed. 

blood-supply of the Allantois. There are two allantoic arteries 
and one allantoic vein. (See Chap. XII). Both arteries persist 
throughout the period of incubation, but the left is much the 
best developed. It passes out along the stalk of the allantois 
to the inner wall of the allantoic sac, where it divides in two 
strong branches, one running cephalad and the other caudad to 
the margins of the sac where they pass over to the outer wall; 
The allantoic vein runs in the inner wall and passes over to the 
outer wall near the sero-amniotic connection. Both arteries and 
veins inhibit the expansion of the allantoic sac where they sur- 
round the margin; but the vein has by far the greatest effect, 
as its action is supplemented by the sero-amniotic connection. 
Thus indentations, gradually growing deeper, are established 
along the margins of the allantoic sac, and the outgrowth of the 
latter on each side of the indentations produce overlapping lobes 
(Figs. 1380 C and D). 

The arrangement of the smaller vessels and capillaries is 
very different in the outer and inner walls. In the outer wall 
the arteries and veins branch and interdigitate in the deeper 
portions of the mesoblast, and end in an extraordinarily fine- 
meshed capillary network situated immediately beneath the thin 
ectoderm. “The capillaries form such narrow meshes, and have 
relatively so wide a lumen, that they can be compared only with 
those of the lungs of higher animals, and of the choroidea of 
the eye; indeed, instead of describing it as a vascular network 
embedded in tissue, one could as well describe it as a great 
blood-sinus interrupted by strands of tissue’? (Fiilleborn.) This 
‘apillary network of the outer wall constitutes the respiratory 
area of the allantois. At the margins it passes gradually into 
the incomparably wider meshed capillary network of the inner 
wall. An extensive system of lymphatics is developed, both 
in the outer and inner walls of the allantois, accompanying all 
the blood-vessels, even to their ultimate terminations. 


EMBRYO AND EMBRYONIC MEMBRANES 223 


Structure of the Allantois. (1) Inner wall. The inner wall 
of the allantois consists primarily of two layers, an inner ento- 
dermal and outer mesodermal layer. The latter soon becomes 
differentiated into two layers, an external, delicate, limiting layer 
of flat polygonal cells, with interlocking margins, and an inter- 
mediate layer of star-shaped cells embedded in a homogenous 
mucous ground substance. Parts of the inner wall become 
extremely thin, and in these regions the intermediate layer may 
become entirely absent. Elsewhere, particularly around the 
larger arteries and veins, the intermediate layer may attain 
considerable thickness. The entoderm becomes reduced to a 
layer of flat, interlocking cells. On the eighth day, spindle- 
shaped muscle cells begin to appear in the mesoderm of the 
inner wall, and undergo rapid increase in numbers. Their dis- 
tribution is somewhat irregular; in certain places they may even 
form several layers, and in others are practically wanting. 

On the seventh day the inner wall of the allantois begins 
to fuse with the amnion in the neighborhood of the sero-amniotic 
connection, and this fusion rapidly extends over the area of 
contact between the two membranes. Within the area of fusion 
the muscle layers of the allantois and amnion mutually reinforce 
each other, and in places no boundary can be found between 
them (Filleborn). But during the latter half of incubation the 
musculature of the fused area of allantois and amnion degener- 
ates almost completely. 

Towards the end of incubation, part of the inner wall of the 
allantois fuses also with the yolk-sac, and is therefore carried 
with the latter into the body-cavity of the chick. 

(2) The Outer Wall of the Allantois. As already noted, the 
outer wall of the allantois fuses with the chorion. The compound 
membrane, which is respiratory in function, must be considered, 
therefore, as one. Over the entire respiratory area the ectoderm, 
belonging primarily to the chorion, which is elsewhere two layers 
of cells in thickness, becomes reduced to an exceedingly thin 
layer in direct contact with the walls of the capillaries internally 
and the shell membrane externally. According to Fulleborn, 
the ectoderm cannot be distinguished as a separate layer in the 
latter half of incubation, and the capillaries appear to be in 
immediate contact with the shell-membrane. No muscular 
tissue appears to develop in the outer wall of the allantois. 


224 THE DEVELOPMENT OF THE CHICK 


(3) The Albumen-sac. The allantois in the course of its 
expansion over the embryo, between amnion and chorion, reaches 
the sero-amniotic connection; it must then either divide and 
grow round on each side of the connection, or evaginate the 
chorion above the connection and carry it as an overlapping 
fold on beyond. The latter is what actually happens, and there 
is established as a consequence an overlapping fold of the chorion 
containing an extension of the allantois (Fig. 128); the space 
beneath this fold terminates, naturally, at the sero-amniotic 
connection. In the meantime the cleavage of the mesoblast 
has separated chorion and yolk-sac as far as the neighborhood 
of the yolk-sac umbilicus, where the viscid albumen has accumu- 
lated. The latter is situated not opposite to the yolk-stalk, 
but near the posterior pole of the yolk-sac, with reference to 
the embryo, 7.e., usually towards the narrow end of the shell. 
Now the allantois growing around the yolk-sac from all sides 
reaches the neighborhood of the albumen and enters an evagina- 
tion of the chorion that wraps itself around the albumen, thus 
initiating the formation of a double sac of the chorion enfolding 
the albumen and containing between its two layers an extension 
of the allantois. The latter is therefore separated everywhere 
from the albumen by the thickness of the chorion. The superior 
fold of the albumen-sac is the same fold that overgrows the 
sero-amniotic connection, and the albumen-sac is therefore pro- 
longed beneath this fold to the sero-amniotic connection itself, 
which, as we have seen, becomes perforated, thus admitting 
albumen into the amniotic cavity. 

The ectoderm lining the albumen-sac is two-layered, and the 
cells next the albumen tend to be cubical or swollen, and fre- 
quently vesicular, owing apparently to absorption of albumen. 
In the neighborhood of the yolk-sac umbilicus, papilla-like pro- 
jections of the ectoderm into the albumen are common (Fig. 129). 
But these do not occur over the remainder of the albumen-sac 
of the chick, as described by Duval for the linnet; nor do they 
possess a mesodermal core. 

Prior to the union of the mesoderm over the yolk-sac umbili- 
cus, the yolk forms a hernia-like protrusion into the albumen- 
sac (sac of the yolk-sac umbilicus, see Fig. 129), which is, however, 
retracted as the mesoderm ring closes over the yolk-sac umbilicus. 
The vitelline membrane ruptures at an early period of the incu- 


EMBRYO AND EMBRYONIC MEMBRANES 225 


bation over the embryonic pole and gradually slips down over 
the yolk, and is finally gathered together in the albumen-sac. 

(4) The allantois also serves as a reservoir for the secretions 
of the mesonephros, and subsequently the permanent kidney, 
which reach it by way of the cloaca and neck of the allantois. 
The fluid part of the embryonic urine is absorbed, but the con- 
tained salts are deposited in the walls and cavity of the allantois. 
If the connection between the Wolffian ducts and cloaca be inter- 
rupted, the former become enormously extended by the secre- 
tions of the mesonephros. 

The Yolk-sac. The yolk-sac is established in the manner 
already described; it is constituted by the extra-embryonic 
splanchnopleure, and is permanently united to the intestine by 
the yolk-stalk. A narrow lumen remains in the stalk of the 
yolk-sac throughout and even after incubation, but the yolk 
does not seem to pass through it into the intestinal cavity. The 
walls of the yolk-sac, excepting the part derived from the pellucid 
area, are lined with a special glandular and absorbing epithelium, 
which digests and absorbs the yolk and passes it into the vitel- 
line circulation, through which it enters the hepatic portal circu- 
lation and comes under the influence of the hepatic cells. The 
yolk-sac is thus the primary organ of nutrition of the embryo, 
and it becomes highly elaborated for the performance of this 
function. Contrary to the statements found in many text-books, 
it does not reach its maximum development until the end of 
incubation. Throughout incubation it steadily increases in 
complexity and efficiency so as to provide for the extremely 
rapid growth of the embryo. 

The functions of the yolk-sac manifestly require a large sur- 
face area, which is provided for by foldings of the wall projecting 
into the yolk. At the height of its development the inner surface 
of the yolk-sac is covered with numerous folds or septa projecting 
into the yolk, which are highest at the equator and decrease in 
both directions away from the equator. In general, these folds 
follow the direction of the main arteries, z.e., they run in a 
meridional direction, repeatedly bifurcating distally (Fig. 132). 
Moreover, each one is perforated by numerous stomata, and the 
yolk-sac epithelium covers all free surfaces, and a capillary net- 
work is found in every part. So far do they project into the 
interior towards the close of incubation, that those of opposite 


226 THE DEVELOPMENT OF THE CHICK 


sides may be approximately in contact, and the cavity of the 
yolk-sac is thus broken up into numerous connecting compart- 
ments filled with yolk. The outer wall of the yolk-sac is smooth 
and not involved in the folds. The beginning of the folds of the 
yolk-sac may be found at the time of appearance of the vascular 
area of the blastoderm, and they develop pari passu, with the 
vessels of the yolk-sae (Fig. 131). 

Fig. 131 shows the appearance of the folds at the stage of 
twelve somites. It is a view of the blastoderm from below, 


Fie. 13: 
the lower surface of the blastoderm at the 
stage of 12s. (After Hans Virchow.) 

m. R., Marginal ridge of entoderm overly- 
ing the sinus terminalis. 


Septa of the yolk-sac as seen on 


drawn as an opaque object, and it shows the incipient folds of 
the yolk-sae in an arrangement that corresponds roughly, but 
not accurately, with that of the blood-islands, which lie in large 
part in the bases of the folds. The site of the vena terminalis 
is marked by a circular fold of the entoderm. The folds of the 
yolk-sae thus coincide in their distribution with the vascular area 
and are so limited at all times, being absent in the vitelline area. 
There is thus a close connection between the vitelline blood- 


EMBRYO AND EMBRYONIC MEMBRANES 227 


vessels and the folds of the yolk-sac, which will be considered 
more fully beyond. 

The interior of the yolk-sac is lined with entoderm which 
differs in its structure in different regions: In the area pellucida 
the cells are flattened; in the vascular zone of the area opaca 
are found the columnar cells with swollen ends described pre- 
viously. After the third or fourth day these are found filled 
with yellow fatty droplets, which give a yellow tone to the interior 
of the living yolk-sac, and which are so abundant in later stages 
as to render the layer perfectly opaque. These cells do not con- 


Fic. 152. — Part of the interior of the yolk-sae of a 
duck at the time of hatchng. In the upper part of 
the figure the septa are seen from the side showing 
the stomata. In the lower part they are seen on 
edge. Note the sinuous course of the arteries along 
the free edges of some of the septa. (After H. 
Virchow.) 


tain entire yolk-granules; apparently, then, the yolk-granules are 
digested before absorption in this region. In the region of the 
inner zone of the vitelline area, the entoderm is composed of 
several layers of large cells containing yolk-granules, and in 
the outer vitelline zone we come to the germinal wall. The 
germinal wall and inner zone of the vitelline area represent 
the formative region of the yolk-sac epithelium in the manner 
already described (Chap. V). 

Blood-vessels of the Yolk-sac. The development of the circu- 


228 THE DEVELOPMENT OF THE CHICK 


lation in the yolk-sae may be divided into the following stages 
(following Popoff): 

1. Indifferent network bounded peripherally by the vena 
terminalis, connected by two anterior vitelline veins with the 
heart; no arterial trunks. 

2. Origin of an arterial path in the network; the right anterior 
vitelline vein begins to degenerate. 

3. Origin of intermediate veins; the (left) posterior vein 
begins to develop. 

4. Development of collateral veins; further degeneration of 
the right anterior vein; complete formation of the posterior vein. 

5. Further branching; development of a rich venous network; 
the vena terminalis begins to degenerate. 

6. Definitive condition; development of a rich venous net- 
work in the folds or septa of the volk-sac; anastomosis of vessels 
of the yolk-sae and allantois. 

The changes can be followed only in outline. The earliest 
condition has been described in Chapters IV and VY. Fig. 133 
shows a condition intermediate between stages 1 and 2 above. 
The network is entirely arterial, except towards the anterior 
end, 7.e., the blood flows outwards away from the heart. It 
enters the vena terminalis and is returned by right and left an- 
terior vitelline veins to the heart. The beginning of arterial 
trunks in the network is indicated particularly on the left side 
(right side of the figure). The connection of the arterial network 
with the dorsal aorta is still net-like. 

Fig. 134 shows an advance of the same processes. The trunks 
of the vitelline arteries are better differentiated from the network, 
and the blood is still returned to the heart entirely by way of 
the vena terminalis and the right and left anterior vitelline veins, 
which have come in contact distally, circumscribing in their 
proximal parts the mesoderm-free area of the blastoderm. The 
beginning of the lateral vitelline veins is indicated, particularly 
on the right side (left of the figure). 

Fig. 135 represents a great advance. The vitelline arteries 
arise from the dorsal aortze as single trunks, and branch in the 
vascular network, some of them reaching as far as the vena 
terminalis. The two anterior vitelline veins have fused in front, 
and the right anterior vein is reduced in size so that most of the 
blood reaches the heart through the left anterior vein. But the 


Fic. 133. — Circulation in the embryo and the yolk-saec. Stage of about 
16s; from below. ‘The vitelline arteries are beginning to differentiate out 
of the vascular network particularly on the left side. (Observer’s right.) 
Injected. (After Popoff.) 


1, Marginal vein. 2, Region of venous network. 3, First and second 
aortic arches. 4r, 41, Right and left anterior vitelline veins. 5, Heart. 
6, Anterior intestinal portal. 7, Aorts. 8, Vitelline arteries in process of 
differentiation. 9, Blood islands. 


. = 
vo. SatiTe 


eared) 
4. Oo ME s 


Fic. 134. — Circulation in the embryo and the yolk-sac at the stage of about 
22s, drawn from below. Note differentiation of branches of the vitelline 
arteries. Injected. (After Popoff.) 


1, Marginal vein. 2, Region of venous network. 3, Carotid loop. 4r, 
41, Right and left anterior vitelline veins. 5, Heart. 6, Anterior intes- 
tinal portal. 7, Dorsal aorta. 8, Branches of vitelline arteries. 


EMBRYO AND EMBRYONIC MEMBRANES 229 


most striking change is the transformation of part of the vascular 
network into channels in which the blood flows towards the heart. 
Of these there may be recognized the following: 1. Intermediate 
veins arising from the vena terminalis at various places and 
gradually losing themselves centrally in the vascular network. 
2. The vascular network immediately behind the embryo has 
assumed a venous character and likewise a large part of the 
network immediately surrounding the embryo. 3. Lateral vitel- 
line veins are beginning to develop from the anterior intestinal 
portal backwards. 

Fig. 136, representing the circulation at a stage of about 40 
somites, shows the completion of the primary circulation in the 
yolk-sac. The vitelline arteries branch richly, and end in a 
capillary network; very few arterial branches reach the vena 
terminalis as such, and then only very fine ones. The vena 
terminalis itself is relatively reduced; the lateral vitelline veins 
have absorbed the network between themselves and the inter- 
mediate veins, which now appear as prolongations of the lateral 
veins. The right anterior vitelline vein has disappeared almost 
entirely and the posterior vitelline vein is well developed, empty- 
ing into the left lateral vein. 

The lateral vitelline arteries and veins are superposed as 
far peripherally as the original intermediate veins, which lie 
between the arterial trunks. Wherever there is superposition 
of arteries and veins, the latter are superficial and the former 
deep in position as seen from above. The figure also shows the 
vascular network in the budding allantois, and some of the em- 
bryonic blood-vessels. 

In the later stages of development the arteries are carried in 
by the septa of the yolk-sac and he near their free edges; the 
veins, on the other hand, remain superficial in position. The 
terminal vein becomes progressively reduced in importance up 
to about the tenth day, and then gradually disappears as such, 
being taken into the terminal capillaries. After the tenth day 
the anterior and posterior vitelline veins decrease in importance 
and finally become almost unrecognizable. The lateral veins, 
on the other hand, increase in importance and return all of the 
blood to the embryo. 

The rich network of venous capillaries in the septa of the 
yolk-sac is shown in Fig. 137. It lies immediately beneath the 


230 THE DEVELOPMENT OF THE CHICK 


epithelium over the entire extent of the septa and forms loops 
along the free border. The arteries do not communicate directly 
with this network according to Popoff, and the course of the 
circulation from arteries to veins is not clearly described by this 
author. 

The allantois fuses with the yolk-sac in the region of the 
yolk-sac umbilicus, and anastomoses arise between the veins of 
the allantois and those of the yolk-sac. 

Ultimate Fate of the Yolk-sac. On the nineteenth day of 
incubation, the yolk-sae slips into the body-cavity through the 
umbilicus; which thereupon closes. The mechanism of this 
process is of considerable interest. The yolk-sac is still a volu- 
minous organ, and equal to about one sixth the weight of the 
embryo. It is therefore inconceivable that it could be “drawn 
into” the body-cavity by means of its stalk, which has only the 
intestine for attachment. The process is much more complex 
and may be briefly described as follows: We have already seen 
that the inner wall of the allantois fuses with the amnion on the 
one hand; distally it is connected with the yolk-sac. Now this 
wall of the allantois is muscular, and it is probable that its con- 
traction is the first act in the inclusion of the yolk-sac within the 
body-wall. It is aided in this, however, by the inner wall of 
the amnion, 7.e., that part of the amnion arising from the umbili- 
cus and not fused with the allantois. This part of the amnion 
surrounds the yolk-stalk, and is itself richly provided with muscle 
cells, forming a crossing and interlacing system. It is carried 
down and over the volk-sac to about its equator by the allantois, 
and when the yolk-sac is half taken into the body-cavity, it reaches 
its distal pole and fuses there. Now if the egg be opened at 
this stage in the process and this wall of the amnion cut through, 
it contracts rapidly to a fraction of its former area (Virchow). 
It is apparent, then, that the tension of this membrane on the 
yolk-sac must exert a continuous pressure that tends to force it 
into the body-eavity. It is in this way, then, by contraction 
of the inner walls of the allantois and of the amnion, that the 
yolk-sac is pressed into the body-cavity. 

The umbilicus is therefore closed by the mere act of inclusion 
of the yolk-sac, for the inner amniotic wall is attached on the 
one hand to the body-wall, and on the other to the distal pole 
of the yolk-sac. A minute opening is left in the center of the 


aes 

Os ws ane ‘ 
2 > ~ 
S SS = 


Fig. 135. — Circulation in the embryo and yolk-sac after 74 hours’ incuba- 
tion. Stage of about 27s from below. Injected. (After Popoff.) 

1, Marginal vein. 2r, 21, Right and left anterior vitelline veins sur- 
rounding the mesoderm-free area. 3, Anterior intestinal portal. 4, In- 
termediate veins connecting with the venous network centrally. 5, Right 
dorsal aorta. 6, Posterior vitelline vein in process of formation. 7, Vitel- 
line arteries. 

Note that the right anterior vitelline vein (2 r) is much atrophied. 


Lt 
26. 
Ors ATS 


Ros 
2 


¢ 


Fie. 136. — Circulation in the embryo and yolk-sac of an embryo of about 
40 s, showing the later development of the lateral and intermediate vitel- 
line veins. Reduction of vena terminalis (marginal vein). Almost com- 
plete atrophy of the right anterior vein. Injected. (After Popoff.) 

1, Marginal vein. 2r, 21, Right and left anterior vitelline veins. 3, 

Arch of aorta. 4, Left posterior cardinal vein. 5r, 51, Right and 


left omphalomesenteriec veins. 6, Aorta. 6a, Left dorsal aorta. 7, 
Vitelline artery. 8, Posterior vitelline vein. 9, Vascular network in the 


allantois. 


EMBRYO AND EMBRYONIC MEMBRANES 231 


umbilical field, through which dried remnants of the inner wall 
of the allantois, which is likewise attached to the distal pole of 
the yolk-sac, protrude for a short time. On the inner side the 
yolk-sac is attached to the umbilicus by its distal pole, and by 
its stalk to the intestine. The absorption of the yolk-sac then 
goes on with great rapidity, being reduced from a weight of 
5.34 gr. twelve hours after hatching to 0.05 gr. on the sixth day 
after hatching, according to a series of observations of Virchow. 

The Amnion. The amnion invests the embryo closely at the 
time of its formation, but soon after, fluid begins to accumulate 
within the amniotic cavity, which gradually enlarges so that the 
embryo les within a considerable fluid-filled space, which in- 
creases gradually up to the latter part of the incubation, and 
then diminishes again, so that the embryo finally occupies most 
of the cavity. The connections of the amnion with the chorion, 
and later with the allantois, albumen-sac, and yolk-sac, have 
been already described. 

Muscle fibers appear in the walls of the amnion on the fifth 
or sixth day and gradually increase in number; though they 
subsequently degenerate over the area of fusion with the allan- 
tois. They persist elsewhere, however, and are active in the 
inclusion of the yolk-sac in the manner already described. Shortly 
after the appearance of the muscle fibers slow vermicular or 
peristaltic contractions of the amnion begin, and the embryo is 
rocked within the amniotic cavity. Apparently, adhesions are 
thus prevented, but they are sometimes formed and lead to various 
malformations of the embryo. In some cases the amnion fails 
to develop; in such cases, the embryo usually dies at a relatively 
early stage, though Dareste records an anamniotic embryo of 
thirteen days, apparently full of life and vigor. 

The amnion apparently acts first as a protection against all 
mechanical shocks and jars which are taken up by the fluid; 
second, by protecting the embryo against the danger of desicca- 
tion; third, by protecting it against adhesions with the shell- 
membrane and embryonic membranes, and lastly by providing 
space for the expansion of the allantois and consequent increase 
of the respiratory surface. It also has secondary functions in 
the chick in connection with the absorption of the albumen and 
the inclusion of the yolk-sac. It will be readily understood, 
then, why anamniotic embryos usually do not develop far. 


232 THE DEVELOPMENT OF THE CHICK 


Hatching (ajter von Baer). About the fourteenth day the 
erowing embryo accommodates itself to the form of the egg so 
as to lie parallel to the long axis with its head usually towards 
the broad end near to the air-chamber. Sometimes, however, 
the embryo is turned in the reverse position (von Baer). The 
head is bent towards the breast, and is usually tucked under 
the right wing. Important changes preparatory to hatching 
take place on the seventeenth to the 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 towards that part of the membranes next to the air-chamber. 
The intestine is retracted completely into the body-cavity, and 
on the nineteenth 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 
breath slowly the contained air; the chick may be heard, in some 
cases, to peep within the shell two days before hatching, a sure 
sign that breathing has begun. But the circulation in the allan- 
tois is still maintained and it still preserves its respiratory func- 
tion. 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 dry 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. 


oA gi Ler 


SF 


a W 


 . « fae Foe, et eg Ce Se one ‘ 


Fic. 137. — Part of a septum of the yolk-sac. Injected. 20 days’ incuba- 
tion. The free edge is above. (After Popoff.) 


Ar., Artery. St., Stomata. V.an., Longitudinal anastomoses of venous 
network. V., vein. 


CHAPTER VIII 
THE NERVOUS SYSTEM 


I. Tor NEUROBLASTS 


THE account given in Chapters V and VI outlines the origin 
of the larger divisions of the central nervous system and ganglia. 
The subsequent growth and differentiation is due to multiplica- 
tion of cells, aggregation of embryonic nerve-cells, or neuro- 
blasts, in particular regions or centers, the formation and growth 
of nerve-fibers which combine to form nerves and tracts, and 
the origin and differentiation of nerve-sheaths, and the support- 
ing cells, neuroglia, of the central system. The most important 
factors are the origin of the neuroblasts and of nerve-fibers in 
connection with them; these fibers form the various nerve-tracts 
and commissures within the central nervous system and the 
system of peripheral nerves. The origin of neuroblasts and the 
development of fibers is the clue to differentiation in all parts 
of the nervous system. 

Neuroblasts are found in two primary locations in the embryo; 
(1) in the neural tube, and (2) in the series of ganglia derived 
from the neural crest; these are known as medullary and gang- 
lionic neuroblasts respectively.' 

The Medullary Neuroblasts. In the neural tube of the chick, 
up to about the third day, there are present only two kinds of 
cells, the epithelial cells and the germinal cells (Fig. 138). 

The epithelial cells constitute the main bulk of the walls, 
and extend from the central canal to the exterior; their inner 
ends unite to form an internal limiting membrane lining the 
central canal, and their outer ends to form an external limiting 
membrane. Each cell in the lateral walls of the tube is much 
elongated and usually shows three enlargements, viz., at each 
end and in the region of the nucleus, the cell being somewhat 
constricted between the nucleus and each end. In different 


1 Neuroblasts arise also in the olfactory epithelium. (See Chap. IX.) 
233 


234 THE DEVELOPMENT OF THE CHICK 


cells the nuclei are at different levels; thus in a section several 
layers of nuclei appear. These cells are not closely packed 
together, except at their outer ends, but are more or less separated 
by intercellular spaces that form a communicating system of 
narrow channels. 


PS Fe) 


~ 


ins ch. 


(rs ows! 


I'ig. 138. —Structure of the wall of the neural tube. Trans- 
verse section through the region of the twenty-first somite 
of a29sembryo. Drawn with Zeiss 2 mm. oil-immersion. 

e.C., Central canal. ep. C., Epithelial cells. g. C., Ger- 
minal cells. Ms’ch., Mesenchyme. 


The germinal cells are rounded cells situated next the central 
canal between the inner ends of the epithelial cells; karyokinetie 
figures are very common in them. According to His the germinal 
cells are the parent cells of the neuroblasts alone; it is probable, 
however, that they are not so limited in function, and that they 
represent primitive cells from which proceed other epithelial 
cells and embryonic neuroglia cells as well as neuroblasts. 


THE NERVOUS SYSTEM 230 


A narrow non-nucleated margin, known as the marginal 
velum, appears in the lateral walls of the neural tube external 
to the nuclei (Fig. 188). This is occupied by the outer ends of 
the epithelial cells. At this time, therefore, three zones may 
be distinctly recognized in the walls of the neural tube, viz., 
(1) the zone of the germinal cells, including also the inner ends 
of the epithelial cells, (2) the zone of the nuclei of the epithelial 
cells, (8) the marginal velum. No distinctly nervous elements 
are yet differentiated. 

Such elements, however, soon begin to appear: Fig. 139 repre- 
sents a section through the 
cord of a chick embryo of 
about the end of the third day; 
it is from a Golgi preparation 
in which the distinctly nervous 
elements are stained black, and 
the epithelial and germinal 
cells are seen only very indis- 
tinctly. The stained elements 
are the neuroblasts, and it will 
be observed that they form a 
layer roughly intermediate in 
position between the marginal 


Fia. 139.— Transverse section through 
the spinal cord and ganglion of a 


velum and the nuclei of the chick about the end of the third 
epithelial cells. They are day; prepared by the method of 


usually regarded as derived Golgi. (After Ramon y Cajal.) 
i C., Cones of growth. Nbl.1, 2, 3, 4, 


from germinal cells that have  Neuroblasts of the lateral wall’ (1 and 
migrated from their central 2); of the spinal ganglion (3); of the 
es es ventral horn (motor neuroblasts) (4). 
position outwards; but it is 
possible that some of them may have been derived from epithelial 
cells. However this may be in such an early stage, it is certain 
that the neuroblasts formed later are derived from germinal cells. 
It will be observed that each neuroblast consists of a cell- 
body and a process ending in an enlargement. The process 
arises as an outgrowth of the cell-body, and forms the axis cylin- 
der or axone of a nerve-fiber; the terminal enlargement is known 
as the cone of growth, because the growth processes by which 
the axone increases in length are presumably located here. It 
may be stated as an invariablerule that each axone process of a 
medullary neuroblast arises as an outgrowth, and grows to its 


236 THE DEVELOPMENT OF THE CHICK 


final termination without addition on the part of other cells. 
The body of the neuroblast forms the nerve-cell, from which, 
later on, secondary processes arise constituting the dendrites. 

The view that each nerve-cell with its axone process and 
dendrites is an original cellular individual, is known as the neurone 
theory. For the central nervous system this view is generally 
held, but its extension to the peripheral system is opposed by 
some on the ground that the axone in peripheral nerves is formed 
within chains of cells, and is thus strictly speaking not an original 
product of the neuroblast, though it may be continuous with the 
axis cylinder process of a neuroblast. This view is discussed 
under the peripheral nervous system. 

‘ach medullary neuroblast is primarily unipolar and the 
axone is the original outgrowth. 
Soon, however, secondary  proto- 
plasmic processes arise from the 
body of the nerve-cell and form the 
dendrites. These appear first in 
certain neuroblasts of the ventro- 
lateral portion of the embryonic 
cord, whose processes enter into the 
ventral roots of spinal nerves (Fig. 
140). The extent and kind of de- 
velopment of these dendritic pro- 


Fic. 140.— Transverse section cesses of the nerve-cells varies 
through the spinal cord of a extraordinarily in different regions; 
chick om the fourti) day ‘of “Wigs. 139,140) and 141 give amaded 
incubation; prepared by the Lana Ae ie ~ fama 

‘1s heir rar velo nt 4 
method of Golgi. (After Ra- © SE ee ee oy = 
mon y Cajal.) motor neuroblasts up to the eighth 
©. a., Anterior commissure. day. 

D., Dendrite. d. R., Dorsal root. The Ganglionic Neuroblasts. The 

ip. Z., Ependymal zone. W., ee 

White matter (marginal velum). ganglionic neuroblasts are located, 

Nbl. 4, Neuroblast of the ventral 


as the name implies, in the series of 
horn (motor). 


ganglia derived from the neural 
crest. It must not be supposed, however, that all of the cells 
of the ganglia are neuroblasts, for the ganglia contain, in all 
probability, large numbers of cells of entirely different function. 
(Sheath-cells, see peripheral nervous system.) It is probable 
also that the neuroblasts of the spinal ganglia and some cranial 
ganglia, at least, are of two original kinds, viz., the neuroblasts of 


THE NERVOUS SYSTEM 237 


the dorsal root and of the sympathetic system. The first kind 
only is considered here, and they are usually called the gan- 
glionic neuroblasts s.s., because they alone remain in the spinal 
ganglia. Like the medullary neuroblasts these neuroblasts form 
outgrowths that become axis cylinder processes; but they differ 
from the latter in that each ganglionic neuroblast forms two 
axones, one from each end of the spindle-shaped cells, which are 
arranged with their long axis parallel to the long axis of the 
ganglion (Fig. 139). Thus we may distinguish a central process 
and a peripheral process from each neuroblast, the former grow- 
ing towards and the latter away from the neural tube (Fig. 139). 
In other words each ganglionic neuroblast is bipolar, as contrasted 
with the unipolar medullary neuroblasts. The central axone 
enters the dorsal zone of the neural tube, and the peripheral one 
grows out into the surrounding mesenchyme. 


Ol. 


Fig. 141. — Transverse section through the spinal 
cord of a 9-day chick, prepared by the method 
of Golgi. (After Ramon y Cajal.) 

Col., Collaterals. d.R., Dorsal root. G., Gray 
matter. Gn., Ganglion. Nbl. 4, Neuroblast of the 
ventral horn (motor). v. R., Ventral root. W., 
White matter. 


In the course of the later development the cell-body moves 
to one side so that the central and peripheral branches appear 
nearly continuous (Fig. 141). Farther shifting of the cell-body 
produces the characteristic form of the ganglionic nerve-cell with 
rounded body provided with stem from which the central and 
peripheral branches pass off in opposite directions. The central 
process enters the marginal velum near its dorsal boundary and 


238 THE DEVELOPMENT OF THE CHICK 


there bifurcates, producing two branches, one of which grows 
towards the head and the other towards the tail in the dorsal 


mils) 


\ 


ae: 
S 

Ee 

~ 


mG 
aa 
5 


Fig. 142. — Six centripetal axones of the dorsal 
root, rigorously copied from a good preparation 
prepared according to the method of Golgi. 
From a longitudinal and tangential section of 
the dorsal column of the spinal cord of an 8- 
day chick. (After Ramon y Cajal.) 

Col., Collaterals. 1, 2, 3, 4, 5, 6, the axones 
entering the cord. 


column of the white matter. The ascending and descending 
branches send off lateral branches, collaterals, which pass deeper 
into the cord, and ramify in the gray matter of the dorsal horn. 


THE NERVOUS SYSTEM 239 


Fig. 142 represents six central processes of ganglionic neuroblasts 
entering the cord and branching as described. 

After this preliminary account of the neuroblasts we may 
take up the development of the spinal cord, brain, and peripheral 
nervous system. 


II. THrt DEVELOPMENT OF THE SPINAL CoRD 


We have seen that the epithelial cells of the neural tube 
stretch from the lumen of the central canal to the exterior, and 
that the nuclei are arranged so as to leave the outer ends free, 
thus forming the marginal velum. 

In the roof and floor the epithelial cells are relatively low, 
and in the lateral zones much elongated. The epithelial cells 
are added to at first by transformation of some of the germinal 
cells; but they do not appear to multiply by division, and as 
development proceeds they become more and more widely sep- 
arated, the interstices being filled up by neuroblasts, embryonic 
glia cells, and fiber tracts. As the wall of the neural tube grows 
in thickness, the epithelial cells become more and more elongated, 
seeing that both external and internal connections are retained; 
and, as the growth takes place mainly external to their nuclear 
layer, the latter becomes reduced, relative to the entire thickness 
of the neural tube, to a comparatively narrow zone surrounding 
the central canal, and is now known as the ependyma (Fig. 143). 
Cilia develop on the central ends of the ependymal cells in the 
central canal, and from the outer end of each a branching process 
extends to the periphery anastomosing with neighboring epen- 
dymal processes so as to form a skeleton or framework enclosing 
the other cellular elements and fibers of the central system. 

Beginning with the third day a new layer appears between 
the nuclei of the epithelial cells and the marginal velum. This 
layer, known as the mantle layer, is composed of neuroblasts 
and embryonic glia cells, and represents the gray matter (Figs. 
139 and 140). The white matter of the cord is laid down in 
the marginal velum. The sources of the cells composing the 
mantle layer may be twofold, viz., from the young epithelial 
cells or from the germinal cells. According to some authors 
young epithelial cells may be transformed into either neuroblasts 
or neuroglia cells. Thus the form of the youngest neuroblasts 
in Fig. 139 indicates derivation from epithelial cells, but this 


240 THE DEVELOPMENT OF THE CHICK 


cannot be regarded as proved. Similarly intermediate stages 
between epithelial and true gla cells are apparently shown in 
Fig. 148. However, there can be but little doubt that the prin- 
cipal source of the neuroblasts of the mantle layer is the germinal 
cells, that migrate outwards between the bodies of the epithelial 
cells. The germinal cells continue in active division up to at 
least the eleventh day, and their activity seems sufficient to 
provide for all the cellular elements of the mantle layer, whereas 
the epithelial cells apparently do not divide at all. Moreover, 
mitoses are not infrequent in some cells of the mantle layer itself. 


Fig. 148. — Transverse section of the cord of a 
nine-day chick to show neuroglia and ependymal 
cells; prepared by the method of Golgi. (After 
Ramon y Cajal.) 

D., Dorsal. Ep., Ependymal cells. N’gl., Neu- 
roglia cells. V., Ventral. 


The form of the gray matter in the cord in successive 
stages is shown in Figs. 144, 145, and 146, representing sections 
of the cord at five, eight, and twelve days. It will be seen that 
the gray matter gains very rapidly in importance between the 
fifth and the eighth days. 


Attention should be directed to a group of neuroblasts situated at 
the external margin of the white matter just above the ventral roots. 
This is known as Hoffmann’s nucleus; it extends the entire length of the 
cord (Fig. 146, twelve days). 


The white matter of the cord gains in importance at an equal 
rate (Figs. 144, 145, 146). Its production is due to ascending 


THE NERVOUS SYSTEM 241 


and descending tracts of fibers derived from medullary and 
ganglionic neuroblasts. The dorsal and ventral roots of the 
spinal nerves divide it on each side into three main columns, 
viz., dorsal situated above the dorsal root, lateral situated be- 
tween dorsal and ventral roots, and ventral situated below the 


Fic. 144. — Transverse section through the cervical swelling 
of the spinal cord of a chick, middle of the fifth day. (After 
v. Kupffer.) 

bl. V., Blood vessel. C.a., Anterior commissure. C., Cen- 
tral canal. d., Group of axones at the level of the dorsal root. 

Ep., Ependyma. N’bl., Neuroblasts. V. Ventral column of 

white matter. 


ventral roots. The dorsal column begins first as a bundle of 
fibers at the entrance of the fibers of the dorsal root (Fig. 144). 
Subsequently, other fibers come in this region and gradually 
extend towards the dorsal middle line, displacing the ependyma 


242 THE DEVELOPMENT OF THE CHICK 


and gray matter (Fig. 145, eight days), but the dorsal columns 
of the two sides are still separated in the median line by a broad 
septum of ependymal cells. Later (Fig. 146, twelve days) this 
septum becomes very narrow, and the accumulation of fibers in 
the dorsal columns causes the latter to project on each side of 
the middle line, thus forming an actual fissure between them. 


Fic. 145. — Transverse section through the spinal cord, and the eighteenth 
spinal ganglion of an eight-day chick. 

Centr., Centrum of vertebra. d.R., Dorsalroot. Ep., Ependyma. Gn., 
Spinal Ganglion. Gn. symp., Sympathetic ganglion. Gr. M., Gray matter. 
m. N., Motor nucleus. R.com., Ramus communicans. R. d., Ramus dor- 
salis. R. v., Ramus ventralis. Sp., Spinous process of vertebra. v. R., 
Ventral root. Wh. M., White matter. 


Central Canal and Fissures of the Cord. The central canal 
passes through a series of changes of form in becoming the prac- 
tically circular central canal of the fully formed cord. Up to 
the sixth day it is elongated dorso-ventrally, usually narrowest 
in the middle with both dorsal and ventral enlargements. About 


THE NERVOUS SYSTEM 243 


the seventh day the dorsal portion begins to be obliterated by 
fusion of the ependymal cells, and is thus reduced to an epen- 
dymal septum. On the eighth day this process has involved the 
upper third of the canal; the form of the canal is roughly wedge- 
shaped, pointed dorsally and broad ventrally (Fig. 145). The 
continuation of this process leaves only the ventral division as 
the permanent canal. 

At the extreme hind end of the cord the central canal becomes 
dilated to form a relatively large pear-shaped chamber with thin 
undifferentiated walls (Fig. 148); the terminal wall is still fused 
with the ectoderm at eight days, and the chamber appears to 
have a maximum size at this time. At eleven days the fusion 
with the ectoderm still exists, and the cavity is smaller. 


Fic. 146. — Transverse section through the 
cervical swelling of the spinal cord of a 
12-day chick. (After v. Kupffer.) 

C., Central canal. d. H., Dorsal horn of 
the gray matter. Ep., Ependyma. N. H., 
Nucleus of Hoffmann. - s. d., Dorsal fissure. 
s. v., Ventral fissure. v. H., Ventral horn 
of the gray matter. 


The development of the so-called dorsal and ventral fissures 
is essentially different. The entire ventral longitudinal fissure 
of the cord owes its origin to growth of the ventral columns of 
gray and white matter which protrude below the level of the 
original floor (Figs. 145 and 146), and the latter is thus left be- 
tween the inner end of the fissure and the central canal. The 
dorsal longitudinal fissure on the other hand is for the most part 


244 THE DEVELOPMENT OF THE CHICK 


a septum produced by fusion of the walls of the intermediate 
and dorsal portions of the central canal; there is, however, a true 
fissure produced by protrusion of the dorsal columns of white 
matter (Fig. 146). This is, however, of relatively slight extent. 
The original roof of the canal is therefore found between the 
dorsal septum and the fissure. 

Neuroblasts, Commissures, and Fiber Tracts of the Cord. The 
medullary neuroblasts may be divided into four groups: (1) The 
first group, or motor neuroblasts, form the fibers of the ventral 
roots of the spinal nerves. These are situated originally in the 
ventro-lateral zone of the gray matter (Figs. 144, 145, 146); 
they are relatively large and form a profusion of dendrites (Figs. 
140, 141). As they increase in number and size they come to 
form a very important component of the ventral horn of the gray 
matter and contribute to its protrusion. (2) The second group 
may be called the commissural neuroblasts. These are situated 
originally mainly in the lateral and dorsal portions of the mantle 
layer, but are scattered throughout the gray matter, and their 
axis cylinders grow ventrally and cross over to the opposite side 
of the cord through the floor (Figs. 139 and 140), and thus form 
the anterior or white commissure of the cord. (3) The cells of the 
fiber tracts are scattered throughout the gray matter, and are 
characterized by the fact that their axis cylinders enter the white 
matter of the same side; here they may bifurcate, furnishing 
both an ascending and a descending branch, or may simply turn 
in a longitudinal direction. (4) Finally there are found certain 
neuroblasts with a short axis cylinder, ramifying in the gray 
matter on the same side of the cord. These are found in the 
dorsal horn of the gray matter and develop relatively late (about 
sixteen days, Ramon y Cajal). 


Ill. Tur DEVELOPMENT OF THE BRAIN 


Unfortunately the later development of the brain of birds 
has not been fully studied. The following account is therefore 
fragmentary. It is based mainly on a dissection and sections of 
the brain of chicks of eight days’ incubation. 

Fig. 147 is a drawing of a dissection of the brain of an eight- 
day embryo. The left half of the brain has been removed, and 
the median wall of the right cerebral hemisphere also. The 
details of the cut surfaces are drawn in from sections. Figs. 148 


THE NERVOUS SYSTEM 245 


and 150 show median and lateral sagittal sections of the same 
stage. 

The flexures of the brain at this stage are: (1) the cranial 
flexure marked by the plica encephali ventralis on the ventral 
surface, (2) the cervical flexure at the junction of myelencephalon 
and cord, somewhat reduced in this stage, and (3) the pontine 
flexure, a ventral projection of the floor of the myelencephalon. 


| Comant. pac op 
Ze mee 


Fig. 147. — Dissection of the brain of an 8-day chick. For description see 
text. The arrows shown in the figure lie near the dorsal and ventral boun- 
daries of the foramen of Monro. 

ch. Pl., Choroid plexus. Com. ant., Anterior commissure. Com. post., 

Posterior commissure. CC. str., Corpus striatum. Ep., Epiphysis.  H., 

Hemisphere. Hyp., Hypophysis. L. t., Lamina terminalis. Myel., Myel- 

encephalon.  olf., Olfactory nerve. op. N., Optie chiasma. op. L., Optic 

lobe. Par., Paraphysis. Paren., Parencephalon. pl. enc. v., Plica en- 
cephali ventralis. pont. Fl., Pontine flexure. Ree. op., Recessus opticus. 

S. Inf., Saceus infundibuli. Tel. med., Telencephalon medium. Th., Tha- 

lamus. T. tr., Torus transversus. Tr., Commissura trochlearis. 

The lines a—a, b-b, e-e, d-d, e-e, f-f, represent the planes of section A, 

Bw. Dib rand: PofsHios) 15k 


Telencephalon. The telencephalon is bounded posteriorly, 
as noted in the last chapter, by the line drawn from the velum 
transversum to the recessus opticus. The telencephalon medium 
has grown but little since the fourth day, but the hemispheres 


246 THE DEVELOPMENT OF THE CHICK 


I'ia. 148. — Median sagittal section of an embryo of eight days. 

a. A., Aortic arch. All., Allantois. An., Anus. A. o. m., Om- 
phalomesenteric artery. B. F., Bursa Fabricii. b. P., Basilar plate. 
C. A., Anterior commissure. ec. C., Central canal. Ch. op., Optie 
chiasma. C. p., posterior Commissure. Cl, Cloaea. Cr., Crop. 
d. Ao., Dorsal aorta. D. Hyp., Duet of the hypophysis. Ep., Epi- 
physis. Fis. Eus., Fissura Eustachii. Hem., Surface of hemisphere 
barely touched by section. Hyp., Hypophysis. L. t., Lamina ter- 
minalis. mn. A. 8, neural arch of the eighth vertebra. Nas., Nasal 


THE NERVOUS SYSTEM 247 


have expanded enormously, particularly anteriorly and dorsally, 
and their median surfaces are flattened against one another in 
front of the lamina terminalis, which forms the anterior boundary 
of the telencephalon medium (Figs. 148, 149). Posteriorly the 
cerebral hemispheres extend to about the middle of the dien- 
cephalon and their lateral faces are rounded. The lateral walls 
of the hemispheres have become enormously thickened to form 
the corpora striata (Figs. 147 and 151 A), and the superior and 
lateral walls have remained relatively thin, forming the mantle 
of the cerebral hemispheres (pallium). Thus the cavity of the 
lateral ventricle is greatly narrowed. 

The dissection (Fig. 147) shows the corpus striatum of the 
right side forming the lateral wall of the hemisphere, and extend- 
ing past the aperture (foramen of Monro) between the lateral 
and third ventricles towards the recessus opticus, where it comes 
to an end. 

The olfactory part of the hemispheres is not well differen- 
tiated from the remainder in the chick embryo of eight days. 
There is, however, a slight constriction on the median and ventral 
face (Fig. 147) which may be interpreted as the boundary of the 
olfactory lobe. 

The telencephalon medium is crowded in between the hemi- 
spheres and the diencephalon; its cavity forms the anterior end 
of the third ventricle, and communicates anteriorly through two 
slits, the foramina of Monro, with the lateral ventricles in the 
hemisphere. In Fig. 147, the upper and lower boundaries of 
the foramen of Monro, are indicated by the grooves on either 
side of the posterior end of the corpus striatum. A hair intro- 
duced from the third ventricle into the lateral ventricle through 
the foramen of Monro in the position of the arrow in Fig. 147, 
‘an be moved up and down over the whole width of the striatum. 
The lateral walls of the telencephalon medium are formed by 
the posterior ends of the corpora striata and are therefore very 
thick. 

The lamina terminalis passes obliquely upwards and forwards 


cavity. Oes., Oesophagus. p. A., Pulmonary arch. par., Paraphysis. P.C., 
Pericardial cavity. Rec. op., Recessus opticus. R., Rectum. 3. Inf., Saccus 
infundibuli. T., Tongue. Tel., Med. Telencephalon medium. Tr., Trachea. 
V. 1, 10, 20, 30, First, tenth, twentieth and thirtieth vertebral centra.  r. A., 
right auricle. Vel. tr., Velum transversum.  V. 0. m., Omphalomesenteric 
vein. V.umb., Umbilical vein. 


248 THE DEVELOPMENT OF THE CHICK 


from the recessus opticus to the region between the foramina of 
Monro. It is very thin, excepting near its center, where it is 
thickened to form the torus transversus, containing the anterior 
commissure. At its dorsal summit it 1s continuous with the 
roof of the telencephalon medium, which has formed a pouch- 
like evagination, the paraphysis. Just behind the paraphysis 


Fig. 149. — Median sagittal section of the brain of a chick embryo of 7 
days. (After v. Kupffer.) 

c., Cerebellum. ca., Anterior commissure. ed., Notochord. ch., Pro- 
jection of the optic chiasma. ep., Posterior commissure. e., Epiphysis. 
e’., Paraphysis. hy., Hypophysis. I., Infundibulum. It., Lamina termi- 
nalis. Lop., Optie lobe. M., Mesencephalon. Mt., Metencephalon. 
opt., Chiasma of the optic nerves. p., Parencephalon. ro., Recessus 
opticus. s., Saccus infundibuli. se., Synencephalon. tp., Mammillary 
tubercle. tp., Tuberculum posterius.  tr., Torus transversus. Tr., De- 
cussation of the trochlear nerves. Va., Velum medullare anterius. Vi., 
Ventriculus impar telencephali. vp., Velum medullare posterius. 


is the velum transversum, where the roof bends upwards sharply 
into the roof of the diencephalon. The epithelial wall around 
the bend is folded to form the choroid plexus of the third ven- 
tricle, which is continued forward into the lateral ventricle along 


THE NERVOUS SYSTEM 249 


the median wall of the hemisphere, ending anteriorly in a free 
branched tip (Fig. 147, ch. Pl.) 

The principal changes in the telencephalon since the third 
day comprise: (1) great expansion of the hemispheres and 
thickening of the ventro-lateral wall to form the corpora striata; 
(2) origin of the paraphysis which arises as an evagination of the 
roof just in front of the velum transversum about the middle of 
the fifth day; (8) formation of the choroid plexus; (4) origin of 
the anterior commissure within the lamina terminalis; (5) develop- 
ment of the olfactory region. The general morphology of the 
adult telencephalon is thus well expressed at this time. 

The Diencephalon has undergone marked changes since the 
third day. The roof of the parencephalic division has remained 
very thin, and has expanded into a large irregular sac (Figs. 
147 and 148), situated between the hinder ends of the hemispheres. 
The attachment of the epiphysis has shifted back to the indenta- 
tion between parencephalic and synencephalic divisions, and the 
epiphysis itself has grown out into a long, narrow tube, dilated 
distally, and provided with numerous hollow buds. In the roof 
of the synencephalic division the posterior commissure has de- 
veloped (Fig. 147). In the floor the chiasma has become a thick 
bundle of fibers, and the infundibulum a deep pocket, from the 
bottom of which a secondary pocket (saccus infundibuli) is grow- 
ing out in contact with the posterior face of the hypophysis. 
Following the posterior wall of the infundibulum in its rise, we 
come to a slight elevation, the rudiment of the mammillary 
tubercles; just beyond this is a transverse commissure (the in- 
ferior commissure); and the diencephalon ends at the tuberculum 
posterius. 

The hypophysis has become metamorphosed into a mass of 
tubules enclosed within a mesenchymatous sheath; the stalk is 
continuous with a central tubule representing the original cavity 
from which the other tubules have branched out (Fig. 148), and 
it may be followed to the oral epithelium from which the whole 
structure originally arose. 

The lateral walls of the diencephalon have become immensely 
thickened, both dorsally and ventrally, and a deep fissure (Fig. 
147) is found on the inner face at the anterior end, between the 
dorsal and ventral thickenings. The deepest part of the fissure 
is a short distance behind the velum transversum; from this a 


250 THE DEVELOPMENT OF THE CHICK 


Gn.l3. 
LECCE 


F.thl 


Fia. 150. — Lateral sagittal section of an embryo of 8 days. Right side of 
the body. 
All. N., Neck of the allantois. Cbl., cerebellum. Cr., Crop. E. T., Egg 


THE NERVOUS SYSTEM 251 


short spur runs forward, a still shorter one ventrally, and the 
longest arm extends backwards, gradually fading out beyond 
the middle of the diencephalon. This fissure is not a continuation 
of the sulcws Monroi, or backward prolongation of the foramen 
of Monro, but is, on the contrary, entirely independent. 

The lateral thickenings of the diencephalon constitute the 
thalami optici, each of which may be divided into epithalamic, 
mesothalamic, and hypothalamic subdivisions. In the chick at 
eight days there is a deep fissure between the epi- and meso- 
thalamic divisions (the thalamic fissure, Fig. 147). The substance 
of the epithalamus forms the ganglion habenule. The meso- 
thalamic and hypothalamic divisions are not clearly separated. 
The transition zone between the diencephalon and mesencephalon 
is sometimes called the metathalamus. 

The mesencephalon has undergone considerable changes since 
the third day. The dorso-lateral zones have grown greatly in 
extent, at the same time becoming thicker, and have evaginated 
in the form of the two large optic lobes. Hence the median 
portion of the roof is sunk in between the lobes (Fig. 147), and is 
much thinner than the walls of the lobes. The dorso-lateral 
zones and roof thus form a very distinct division of the mesen- 
cephalon, known as the tectum lobi optici. The ventro-lateral 
zones and floor have thickened greatly and form the basal divi- 
sion of the mesencephalon. The ventricle of the mesencephalon 
thus becomes converted into a canal (aqueduct of Sylvius), from 
which the cavities of the optic lobes open off. 

In the metencephalon likewise there is a sharp distinction 
between the development of the dorso-lateral zones and roof, 
on the one hand, and the ventro-lateral zones and floor on the 
other. From the former the cerebellum develops in the form 
of a thickening overhanging the fourth ventricle. This thick- 
ening is relatively inconsiderable in the middle line (cf. Figs. 148 
and 150). Thus the future hemispheres of the cerebellum are 


tooth. Eust., Eustachian tube. Gn. 1, 13, First and thirteenth spinal 
ganglia. Gon.,Gonad. Hem., Hemisphere. Lag., Lagena. Lg., Lung. M., 
Mantle of Hemisphere. Msn., Mesonephros. Olf. L., Olfactory lobe. Olf. 
N., Olfactory nerve. P. C., Pericardial cavity. Pz. 5, The fifth post-zyga- 
pophysis. R.C. 1, 2, Last two cervical ribs. R. th. 1,5, First and fifth tho- 
racic ribs. S. pe-per., Septum pericardiaco-peritoneale. S’r., Suprarenal. 
Symp., Main trunk of the sympathetic. Str., Corpus striatum. V. 1, 10, 
20, 30, First, tenth, twentieth and thirtieth vertebral arches. V.C. I., Vena 
cava inferior. V. L. L., Ventral ligament of the liver. 


252 THE DEVELOPMENT OF THE CHICK 


indicated. The surface is still smooth at the eighth day, but 
on the tenth and eleventh days folds of the external surface 
begin to extend into its substance, without, however, invaginat- 
ine its entire thickness. These are the beginnings of the cere- 
bellar fissures. 

The floor and ventro-lateral zones of the metencephalon enter 
into the formation of the pons. 

In the roof of the isthmus, or constricted region between 
cerebellum and mesencephalon, is found a small commissure 
produced by decussation of the fibers of the trochlearis (Fig. 147). 

In the wall of the myelencephalon the neuromeres have dis- 
appeared. The thin epithelial roof has become more expanded 
in the anterior part (Figs. 147 and 148). Floor and sides have 
become greatly thickened. 

Commissures. The brain commissures existing at eight days 
are the anterior, posterior, inferior, and trochlearis (ig. 149). 
In the next four or five days two more appear, viz., the com- 
missura pallii anterior (tupffer), corresponding to the corpus 
callosum of mammalia and the commissura habenularis. 

The development of the various: nuclei and fiber tracts of 
the bird’s brain is entirely unknown and affords an interesting 
topic for research. 


IV. Tur PERIPHERAL NERVOUS SYSTEM 


The peripheral nervous system comprises the nerves which 
span between peripheral organs and the central nervous system. 
There are fifty pairs in a chick embryo of eight days, of which 
twelve innervate the head, and thirty-eight the trunk, distin- 
guished respectively as cranial and spinal nerves. It is con- 
venient for purposes of description to consider cranial and spinal 
nerves separately, and to take up the spinal nerves first because 
they are much more uniform in their mode of development 
than the cranial nerves, and also exhibit a more primitive or 
typical condition, on the basis of which the development of the 
cranial nerves must be, in part, at least, explained. 

The Spinal Nerves. Each spinal nerve may be divided into 
asomatic portion related primarily to the somatopleure and axis of 
the embryo, and a splanchnic portion related primarily to the 
splanchnopleure and its derivatives. In each of these again a 
motor and sensory component may be distinguished. Thus each 


THE NERVOUS SYSTEM 253 


Tel med) 


Fig. 151. — Six transverse sections through the brain of an 8-day chick in 
the planes represented in Fig. 147. 
Cbl., Cerebellum. F.M., Foramen of Monro. Gn. V., Ganglion of the 
trigeminus. Isth., Isthmus. It. d., Diverticulum_ of the iter. at. V-; 
Lateral ventricle. Other abbreviations as before (Fig. 147). 


254 THE DEVELOPMENT -OF THE CHICK 


spinal nerve has four components, viz., somatic motor, somatie 
sensory, splanchnic motor, and splanchnic sensory, the two latter 
constituting the so-called sympathetic nervous system. It is 
obvious, of course, that the splanchnic components must be 
missing in the caudal nerves. The somatic and splanchnic com- 
ponents will be considered separately. 

Somatic Components. ach spinal nerve arises from two roots, 
dorsal and ventral (Fig. 145). The fibers of the former arise from 
the bipolar neuroblasts of the spinal ganglia; the fibers of the ven- 
tral root, on the other hand, arise from a group of neuroblasts in 
the ventral portion of the cord. The roots unite in the interver- 
tebral foramen to form the spinal nerve. Typically, each spinal 
nerve divides almost immediately into three branches, viz., a dor- 
sal branch, a ventral branch, and a splanchnic branch to the sym- 
pathetic cord; the last is known as the ramus communicans. 

Fig. 145 represents a section passing through the twentieth 
spinal nerve of an eight-day chick. The dorsal and ventral roots 
unite just beneath the spinal ganglion; fibers are seen entering 
the sympathetic ganglion (ramus communicans); the ventral 
branch passes laterally a short distance where it is cut off; 
beyond this point it can be traced in other sections in the 
next posterior intercostal space more than half-way round the 
body-wall; that is, as far as the myotome has extended in its 
ventral growth. The dorsal branch arises at the root of the 
ventral and passes dorsally in contact with the ganglion to 
branch in the dorsal musculature. This nerve may be regarded 
as typical of the spinal nerves generally. 

There are thirty-eight spinal nerves in an embryo of eight 
days. The first two are represented only by small ventral roots. 


The first two spinal ganglia are rudimentary in the embryo and 
absent in the adult, hence the ganglion illustrated in Fig. 145 is the 
eighteenth of the functional series (see Fig. 149); it lies between the 
nineteenth and twentieth vertebra. 


The fourteenth, fifteenth, and sixteenth are the principal 
nerves of the brachial plexus, and have unusually large ganglia. 
The twenty-third to the twenty-ninth are the nerves of the leg 
plexus, the thirtieth to the thirty-second innervate the region 
of the cloaca and the remainder are caudal. The special mor- 
phology of the spinal nerves does not belong in this description. 


THE NERVOUS SYSTEM 255 


There are one or two vestigial ganglia behind the thirty-eighth nerve, 
evidently in process of disappearance at eight days. 

The early history of the spinal nerves is as follows: The axis 
cylinder processes of the fibers begin to grow out from the neuro- 
blasts about the third day (ef. p. 235). At this time the myo- 
tomes are in almost immediate contact with the ganglia; thus 
the fibers have to cross only a very short space before they enter 
the myotome. The further growth is associated with the growth 
and differentiation of the myotome between which and _ the 
embryonic nerve there is a very intimate relation of such a sort 
that the nerve follows the myotome and its derivatives in all 
changes of position. Thus nerves do not need to grow long 
distances to establish their connections, but these are formed 
at a very early period. This accounts for the motor fibers; the 
way in which the sensory fibers, that arise from the spinal ganglia, 
reach their termination is not known. 

Sheath-cells and Cell-chain Hypothesis. No embryonic nerve 
consists entirely of axones, but, from the start, each nerve trunk 
contains numerous nuclei. The latter belong to cells which have 
been given two radically different interpretations, corresponding 
to two distinct theories concerning the neuraxone. 

(1) The first theory, known as the neurone theory, is the one 
tacitly followed in the preceding description and may be stated 
as follows: the nerve-cell, dendrites and axone, including the 
terminal arborization, constitute a single cellular individual or 
unit, differentiated from the neuroblast alone. The nuclei in 
the embryonic nerves therefore belong to cells that are foreign 
to the primary nerve. Their function is to form the various 
sheaths of the nerves, viz., the sheaths of the individual axones 
and the endo-, peri-, and epineurium. The sheath of Schwann 
arises from such cells that envelop the individual fibers at suitable 
distances and spread longitudinally until neighboring sheath cells 
meet; each such place of meeting constitutes a node of Ranvier. 
Until recently it has been universally believed that the sheath 
cells arose from the mesenchyme; but recent observations on Am- 
phibia and Selachia have shown that they arise from the gangha 
in these forms; their original source is therefore the ectoderm. It 
is probable that they have the same origin in the chick, though this 
has not been demonstrated by direct observation or experiment. 

(2) The second theory is known as the cell-chain hypothesis. 


256 THE DEVELOPMENT OF THE CHICK 


According to this the axones of peripheral nerves arise as differ- 
entiations of the sheath-cells in situ; continuity of the axone is 
established by arrangement of these cells in rows, and union 
with the neuroblast is essentially secondary. The entire axone 
is thus by no means an outgrowth of the neuroblast; at most its 
proximal portion is. 

Bethe (1903) expresses the idea thus: “ Between the cord of 
the embryo and the part to be innervated there is formed primarily 
a chain of nuclei around which the protoplasm is condensed. 
This is fundamentally an extended syncytium in which the nuclei 
of the neuroblasts and of the nerve-primordium he. Within 
the denser protoplasm which appears as the body of the nerve- 
cells, axones differentiate by condensation, and these extend 
from one cell to the next, and so on to the condensations which 
are called neuroblasts. The differentiated axones tend more 
and more to occupy the center of the embryonic nerve, where 
they appear to lie free, though as a matter of fact they are still 
embedded in the general plasma which is no longer distinctly 
visible on account of its lesser density. Since the axones remain 
in firm connection with the neuroblasts, it appears in later stages 
as if they were processes of these and had nothing to do with 
their original formative cells.” 

This view is essentially that of Balfour, Beard, and Dohrn; 
the neurone hypothesis was first clearly formulated in embryo- 
logical terms by His, and has been supported by the investiga- 
tions of a considerable number of observers, notably Ramon y 
Cajal, Lenhossek and Harrison. 

The neurone hypothesis has far stronger embryological sup- 
port than the cell-chain hypothesis so far as peripheral nerves 
are concerned; moreover, it is the only possible hypothesis of 
the development of nerve tracts in the central system, because 
cell-chains are entirely lacking here during the formation of these 
tracts, in which axones may have as long a course as in most 
peripheral nerves. It still remains to be seen whether the neurone 
hypothesis will be modified in any important way by observa- 
tions on the development of peripheral nerves. 

Splanchnic Components (Sympathetic Nervous System). Two 
views have been held concerning the origin of the sympathetic 
nervous system: (a) that it is of mesenchymal origin, its elements 
arising in situ; (b) that it is of ectodermal origin, its elements 


THE NERVOUS SYSTEM 257 


migrating from the cerebro-spinal ganglia to their definitive 
positions. The first view was held by the earlier investigators 
and was originally associated with the extinct idea that the 
spinal ganglia were mesenchymal in origin; the view has been 
largely, but not entirely, abandoned. The second view was 
partly established with the discovery that the spinal ganglia are 
of ectodermal origin, and that the ganglia of the main sym- 
pathetic trunk arise from the spinal ganglia; but there is some 
difference of opinion yet in regard to the peripheral ganglia 
of the sympathetic system, and especially the plexuses of 
Meissner and Auerbach in the walls of the intestine. However, 
the preponderance of evidence and logic favors the view of the 
ectodermal origin of the entire sympathetic nervous system. 

The first clear evidences of the sympathetic nervous system 
of the chick are found at about the end of the third or the begin- 
ning of the fourth day; at each side of the dorsal surface of the 
aorta there is found in cross-section a small group of cells massed 
more densely than the mesenchyme and staining more deeply. 
Study of a series of sections shows these to be a pair of longi- 
tudinal cords of cells beginning in the region of the vagus, where 
they lie above the carotids, and extending back to the beginning 
of the tail; the cords are strongest in the region of the thorax, 
and slightly larger opposite each spinal ganglion. Cells similar 
to those composing the cords are found along the course of the 
nerves up to the spinal ganglia, and careful study of earlier stages 
indicates that the cells composing the cords have migrated from 
the spinal ganglia. The two cords constitute the primary sym- 
pathetic trunks. 

Fig. 152 is a reconstruction of the anterior spinal and sym- 
pathetic ganglia of a chick embryo of four days. The primary 
sympathetic trunk is represented by a cord of cells enlarged 
opposite each ganglion and united to the spinal nerve by a cellu- 
lar process, the primordium of the ramus communicans. — In the 
region of the head the segmental enlargements are lacking. 

No other part of the sympathetic nervous system is formed 
at this time with the exception of a group of cells situated in the 
dorsal mesentery above the yolk-stalk; these are destined to 
form the ganglion and intestinal nerves of Remak. They have 
not been traced back to the spinal ganglia, but it is probable 
that such is their origin. 


258 THE DEVELOPMENT OF THE CHICK 


In the course of the fourth and fifth days aggregations of 
sympathetic ganglion cells begin to appear ventral to the aorta, 
and in the mesentery near the intestine. The connection of these 
with the primary cord is usually rendered evident by agreement 
in structure, and by the presence of intervening strands of cells; 
moreover, in point of time they always succeed the primary cord, 
so that their origin from it can hardly be doubted. 

About the sixth day the secondary or permanent sympathetic 
trunk begins to appear as a series of groups of neuroblasts situ- 
ated just median to the ventral roots of the spinal nerves. They 


| 
Z a = | 
PS eee gam ets. 
a 
Sey aera SP, 
= Ga 


Soar 


Fic. 152.— Reconstruction in the sagittal plane 
of the anterior spinal and sympathetic gan- 
glia of a chick embryo of 4 days. (After 
Neumayer.) 


Ceph. 8., Cephalic continuation of the sym- 
pathetic trunk. $8. C., Sympathetic cord. Sg 


o*,) 
Sympathetic ganglion. sp., Spinal nerve. spg., 
Spinal ganglion. R.C., Ramus communicans. 


are thus separated from the spinal ganglia only by the fibers 
of the ventral roots between which neuroblasts may be found, 
caught apparently in migration from the spinal to the sympa- 
thetic ganglion. The number of these secondary sympathetic 
ganglia is originally 30, one opposite the main vagus ganglion, 
and each spinal ganglion to the twenty-ninth (Fig. 150). Soon 
after their origin they acquire three connections by means of 
axones, viz., (a) central, with the corresponding spinal nerve- 


THE NERVOUS SYSTEM 259 


root by means of strong bundles of fibers; (b) peripheral, with 
certain parts of the original primary sympathetic cord; (c) longi- 
tudinal, the entire series being joined together by two longitudinal 
bundles of fibers uniting them in a chain. The central connec- 
tions constitute the rami communicantes, and are as numerous as 
the sympathetic ganglia themselves; but so close is the approxi- 
mation of the sympathetic ganglion to the roots of the spinal 
nerves that they are not visible externally, the ganglion appear- 
ing to be sessile on the root (Fig. 145); sections, however, show 
the fibers. The peripheral connections constitute the various 
nerves of the abdominal viscera; these are not metameric; 
their number and arrangement is shown in Figure 153. 

In the period between the fourth and the eighth day the pri- 
mary sympathetic cord becomes resolved into the various ganglia 
and nerves constituting the aortic plexus, the splanchnic plexus, 
and the various ganglia and nerves of the wall of the intestine. 
Remak’s ganglion has grown and formed connections with the 
splanchnic plexus, and other parts of the primary sympathetic 
cord. The details of these various processes are too complex 
for full description; they are included in part in Figs. 153 and 154. 

Ganglia and Nerves of the Heart. The development of the 
cardiac nerves is of special interest on account of its bearing on the 
physiological problem of the origin of the heart-beat. The heart 
of the chick begins to beat long before any nervous connections 
with the central system can have been established; indeed, the 
rhythmical pulsation begins at about the stage of 10 somites 
when the neural crest is yet undifferentiated, and no neuroblasts 
are to be found anywhere. Either, then, the heart-beat is of mus- 
cular origin (myogenic), or, if of nervous origin, the nerve-cells 
concerned must exist in the wall of the cardiae tube ab initio. 

The first trace of nerve-cells is found in the heart of the chick 
about the sixth day. These cells are at the distal ends of branches 
of the vagus, with which they have grown into the heart. Pre- 
vious to this time these neuroblasts are found nearer to the vagus 
along the course of the arteries. There can be but little doubt 
that they have arisen from the vagus ganglion and that they 
reach the heart by migration. Such an origin has been demon- 
strated with great probability for all the known nervous elements 
of the heart of the chick. (See Wilhelm His, Jr., Die Entwickelung 
des Herznervensystems bei Wirbelthieren.) 


THE CHICK 


DEVELOPMENT OF 


THE 


260 


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THE NERVOUS SYSTEM 261 


If any cardiac nervous elements arise in situ, they certainly 
remain undifferentiated until those that have a ganglionic origin 
have already entered the heart. 

The Cranial Nerves. The nerves of the head exhibit a much 
greater degree of heteronomy than the spinal nerves, and, in 
spite of much study, knowledge of their embryonic development 
is still in a very unsatisfactory condition. The same principles, 
however, apply to the development of both cranial and spinal 
nerves; the axones of the former like those of the latter arise 
either from medullary or ganglionic neuroblasts which are re- 
spectively unipolar and bipolar; but the cranial ganglionic and 


Fig. 154. — Diagram of the relations of the 
parts of the sympathetic nervous system 
as seen in the cross-section. (After His, 
Jr) 


M., mesentery. Msn., Mesonephros. 
Other abbreviations same as Fig. 153. 


medullary nerve-nuclei are not similarly segmented, as in the 
‘ase of the spinal nerves, and hence the axones are not related 
as dorsal and ventral roots of single nerve trunks; nor has the 
attempt to interpret the cranial nerves as homologues of dorsal 
and ventral roots respectively been successful in the case of the 
most important nerves. Moreover, the olfactory and optic nerves 
differ from the spinal type even more fundamentally. The olfac- 
tory is a sensory nerve that arises apparently from the olfactory 


262 THE DEVELOPMENT OF THE CHICK 


epithelium, and the optic is really comparable to an intramedul- 
lary nerve tract, seeing that its termination lies in a part of the 
original wall of the neural tube, viz., the retina. 

Groups of medullary neuroblasts giving rise to axones of 
motor cranial nerves are located in the brain as follows, according 
to His: 

Oculo-motor nucleus in the mid-brain. 

Trochlearis nucleus in the isthmus. 

Motor trigeminus nucleus in the zone of the cerebellum, including 
the descending root. 

Abducens and facialis nuclei, beyond zone of greatest width 
of the fourth ventricle (auditory sac zone). 

Glossopharyngeus, vagus, in the region of the calamus_ scrip- 
torius. 

Accessorius and hypoglossus, in the region extending to the 
cervical flexure. 

These constitute the cranial motor nerve nuclei, and are more 
or less discontinuous. 

The ganglionic nerves or nerve-components of the head arise 
from the following primitive embryonic ganglion-complexes: 

1. Complex of the trigeminus ganglia. 

2. Complex of the acustico-facialis ganglia. 

3. Complex of the glossopharyngeus ganglia. 

4. Complex of the vagus ganglia. 

The early history of these ganglion-complexes has already been 
considered; they are called complexes because each forms more 
than one definitive ganghon. It is probable also that each con- 
tains sympathetic neuroblasts, which may separate out later as dis- 
tinct ganglia, thus resembling the spinal sympathetic neuroblasts. 

There is no close agreement in the segmentation of the motor 
neuroblasts within the brain and that of the ganglion complexes. 
For instance, in the region of the trigeminal ganglionic complex, 
the motor nuclei of the oculo-motor, trochlearis, and trigeminus 
are found, and in the region of the vagus ganglionic complex, 
the motor nuclei of vagus, accessorius, and hypoglossus. Thus 
the medullary and ganghonic nerves of the head are primitively 
separate by virtue of their separate origins. They may remain 
entirely so, as in the case of the olfactory, trochlearis, and abdu- 
cens, or they may unite in the most varied manners to form 


mixed nerves. 


THE NERVOUS SYSTEM 263 


The motor nuclei of the oculo-motor, trochlearis, abducens, 
and hypoglossus nerves lie in the same plane as the motor nuclei 
of the spinal nerves, 7.e., in the line of prolongation of the ventral 
horns of the gray matter. The motor nuclei of the trigeminus, 
facialis, glossopharyngeus, vagus, and spinal accessory on the 
other hand lie at a more dorsal level, and the roots emerge there- 
fore above the level of origin of the others. It will be noted that 
these are the nerves of the visceral arches, whereas those cranial 
nerves that continue the series of spinal ventral roots innervate 
myotomic muscles, like the latter. Similarly the ganglia of the 
pharyngeal nerves (V, VII, LX, and X) differ from spinal gangliz 
in certain important respects: the latter are derived entirely 
from the neural crest, whereas a certain portion of each of the 
primary cranial ganglia is derived from the lateral ectoderm of 
the head, as noted in the preceding chapter. Thus the pharyn- 
geal nerves form embryologically a class by themselves, both 
as regards the medullary and also the ganglionic components. 

1. The Oljactory Nerve. The embryonic origin of the olfactory 
nerve has been a subject of much difference of opinion: thus it 
has been maintained by a considerable number of workers that 
it arises froma group of cells on each side situated between the 
fore-brain and olfactory pits; some of these maintained that 
these cells arose as an outgrowth from the fore-brain, others 
that they came from the epithelium of the olfactory pit, and 
yet others that this group of cells, or olfactory ganglion, was 
derived from both sources. This group of cells was supposed 
by some to include a large number of bipolar neuroblasts, one 
process of which grew towards the olfactory epithelium and 
the other towards the fore-brain, entering the olfactory lobe 
and ending there in terminal arborization. This view is, however, 
in conflict with the ascertained fact that the fibers of the fully 
formed olfactory nerve are centripetal processes of olfactory 
sensory cells situated in the olfactory epithelium. 

The most satisfactory account of the origin of the olfactory 
nerve in the chick is that of Disse. This author finds two kinds 
of cells in the olfactory epithelium of a three-day chick, viz., 
epithelial cells, and germinal cells which become embryonic 
nerve-cells or neuroblasts. At this time the olfactory epithelium 
is separated from the wall of the fore-brain by only a very thin 
layer of mesenchyme. Early on the fourth day axones arise 


264 THE DEVELOPMENT OF THE CHICK 


from the central ends of the neuroblasts and grow into the 
mesenchyme towards the fore-brain. At the same time groups 
of epithelial cells free themselves from the inner face of the 
olfactory epithelium, and come to lie between this and the fore- 
brain. The axones of the neuroblasts grow between these cells 
until they reach the base of the fore-brain over which they spread 
out, entering the olfactory lobe about the sixth day (Figs. 155 
and 156). In the meantime the peripheral ends of the olfactory 
neuroblasts have extended out as broad protoplasmic processes 
to the surface of the olfactory epithelium, and thus form the per- 
cipient part of the olfactory sense-cells. 


Iria. 155. — Olfactory epithelium of a chick embryo of 5 


days, prepared by the method of Golgi. (After Disse.) 
a, b, and e indicate different forms of neuroblasts in the 
olfactory epithelium. 


The epithelial cells between fore-brain and olfactory pit, through 
which the axones of the olfactory neuroblasts grow, are for the 
most part supporting and sheath-cells of the nerve, but they in- 
clude a few bipolar neuroblasts (ig. 156). The latter are to 
be considered as olfactory neuroblasts with elongated protoplas- 
mic processes. 


Rubaschkin finds a ganglion, which he ealls ganglion olfactortum 
nervi trigemini, situated beneath the olfactory epithelium in a nine- 
day chick. The bipolar cells send out processes peripherally which end 
in fine branches between the cells of the olfactory mucous membrane, 
and centrally, which go by way of the ramus olfactorius nervi 


trigemini towards the Gasserian ganglion. 


2. The Second Cranial or Optic Nerve. The course of this 


THE NERVOUS SYSTEM 265 


nerve is entirely intramedullary, the retina being part of the 
wall of the embryonic brain; its development will therefore be 
considered in connection with the development of the eye. 


Fic. 156. — Sagittal section through the head of a chick embryo of 5 days, 


showing the floor of fore-brain, olfactory pit, and developing olfactory 

nerve between. (After Disse.) 

a., Unipolar neuroblasts near the olfactory epithelium. b., Bipolar cell 
in the olfactory nerve. c¢., Unipolar cell near the brain. F. B., Floor of 
fore-brain. N’bl., Neuroblast in the olfactory epithelium. olf. Ep., Olfac- 
tory epithelium. olf. N., Olfactory nerve. olf. P., Cavity of olfactory pit. 


D) 


3. The third cranial or oculo-motor nerve arises from a group 
of neuroblasts in the ventral zone of the mid-brain near the median 
line, and appears external to the wall of the brain at about sixty 
hours (about 28-30 somites). At this time it appears as a small 
group of axones emerging from the region of the plica encephali 


266 THE DEVELOPMENT OF THE CHICK 


ventralis, and ending in the mesenchyme a short distance from 
its point of origin. At seventy-two hours the root is much 
stronger, interpenetrated with mesenchyme and ends between 
the optic cup and floor of the brain behind the optic stalk (ef. 
Fig. 101). At ninety-six hours the root is broad and fan-shaped, 
the nerve itself is comparatively slender, and passes downwards 
and backwards behind the optic-stalk where it enters a well- 
defined ganglion situated just median to the ophthalmic branch 
of the trigeminus; this is the ciliary ganglion; beyond it the 
fibers of the oculo-motor turn forward again to enter the region 
of the future orbit. 

According to Carpenter (1906) the ciliary ganglion arises 
from two sources: (@) migrant medullary neuroblasts that pass 
out into the root of the oculo-motor, and follow its course to 
the definitive situation of the ciliary ganglion, and (b) a much 
smaller group of neuroblasts that migrate from the ganglion of 
the trigeminus along the ophthalmic branch, and by way of a 
ramus communicans to the ciliary ganglion. The adult ciliary 
ganglion shows correspondingly two component parts: (a) a 
larger ventral region composed of large bipolar ganglion cells, 
and (6b) a smaller dorsal region containing small ganglion cells 
with many sympathetic characters. It is probable that the 
medullary fibers of the oculo-motor nerve are distributed entirely 
to the muscles innervated by it, viz., the superior, inferior, and 
internal rectus and inferior oblique muscles of the eye. The 
fibers arising from the neuroblasts of the ciliary ganglion ter- 
minate peripherally in the intrinsic muscles of the eye-ball, and 
centrally (in the case of the bipolar cells) in the brain, which 
they reach by way of the medullary nerve. The motor branches 
leave the trunk of the nerve a short distance centrally to the 
ciliary ganglion. 

4. The trochlearis or fourth cranial nerve is peculiar inas- 
much as it arises from the dorsal surface of the brain in the 
region of the isthmus. It arises entirely from medullary neuro- 
blasts and innervates the superior oblique muscle of the eye. 
Marshall states that it may be readily seen in a five-day embryo; 
in an embryo of eight days it is a slender nerve arising from the 
dorsal surface of the isthmus immediately in front of the cere- 
bellum; the fibers of the two sides form a commissure in the roof 
of the isthmus (Fig. 148). 


THE NERVOUS SYSTEM 267 


5. The trigeminus or fifth cranial nerve consists of motor 
and sensory portions. The latter arises from the trigeminal 
ganglion, the origin of which has already been described. The 
ganglionic rudiment appears roughly Y-shaped even at an early 
stage (cf. Figs. 105 and 117), the short stem lying against the 
wall of the brain and the two branches diverging one in the direc- 
tion of the upper surface of the optic cup (ophthalmic branch) 
and the other towards the mandibular arch. The original con- 
nection of the ganglion with the roof of the neural tube is lost 
during the second day and permanent connection is established 
during the third day, presumably by growth of axones into the 
wall of the brain. The new connection or sensory root of the 
trigeminus is attached to the myelencephalon in the region of 
greatest width of the fourth ventricle near the ventral portion 
of the lateral zone. 

During the fourth day the peripheral axones follow the direc- 
tion of the ophthalmic and mandibular branches of the ganglion 
and grow out farther as the ophthalmic and mandibular nerves; 
the former passes forward between the optic vesicle and the wall 
of the brain; the latter runs ventrally towards the angle of the 
mouth, over which it divides, a smaller maxillary branch entering 
the maxillary process of the mandibular arch, and a larger one, 
the mandibular nerve, runs into the mandibular arch. (For an 
account of the branchial sense organ of the trigeminus, see Chap. 
VI.) 

A medullary component of the trigeminal nerve arises from 
the wall of the brain just median to the ganglionic root during 
the fourth day; it runs forward parallel to the ganglionic ophthal- 
mic branch, and sends a twig to the ciliary ganglion. Beyond 
this point it unites with the ganglionic branch. 

A connection of the trigeminus with the olfactory sensory 
epithelium is described under the olfactory nerve. 

6. The sixth cranial or abducens nerve is stated to arise about 
the end of the fourth day. It is a purely motor nerve, and has 
no ganglion connected with it; it innervates the external rectus 
muscle of the eye. At 122 hours it arises by a number of slender 
roots attached to the myelencephalon near the mid-ventral line, 
beneath the seventh nerve. Its roots unite into a slender trunk 
that runs directly forward beneath the base of the brain to the 
region of the orbit. The sixth nerve thus corresponds more 


268 THE DEVELOPMENT OF THE CHICK 


nearly than any other cranial nerve to a ventral spinal nerve- 
root. 

7 and 8. The Facial and Auditory Nerves. The ganglia of 
these nerves at first form a common mass, the acustico-facialis. 
But during the course of the fourth day the anterior and ventral 
portion becomes distinctly separated from the remainder and 
forms the geniculate ganglion; the remainder then forming the 
auditory ganglia (cf. Fig. 102). The acustico-facialis ganglion 
complex moves from its original attachment to the dorsal surface 
of the brain and acquires a permanent root during the third day, 
attached ventrally just in front of the auditory sac. 

(a) The seventh cranial or facialis nerve arises during the 
fourth day from the geniculate ganglion which is situated just 
above the second or hyomandibular branchial cleft. It grows 
first into the hyoid arch (posttrematic branch), but towards 
the end of the fourth day a small branch arises just above the 
cleft and arches over in front of it and runs down the posterior 
face of the mandibular arch (pretrematic branch). The origin of 
the motor components is not known. 

(b) The further history of the auditory nerve is considered 
with the development of the ear. 

9. The ganglion of the ninth cranial or glossopharyngeal nerve 
eanglion petrosum ef. Fig. 102) arises from the anterior part of 
the postotie cranial neural crest as already described. Early on 
the fourth day the ganglionic axones enter the base of the brain 
just behind the auditory sac and establish the root, which con- 
sists of four or five parts on each side. From the ganglion which 
is situated at the summit of the third visceral arch a strong 
peripheral branch develops on the fourth day, and extends into 
the same arch; a smaller anterior branch develops a little later 
which passes over the second visceral pouch and enters the 
second visceral arch. About the same time an anastomosis is 
formed with the ganglion of the vagus. 

10. The tenth cranial or vagus (pneumogastric) nerve is very 
large and complex. Its ganglion very early shows two divisions, 
one near the roots (ganglion jugulare) and the other above the 
fourth and fifth visceral arches (ganglion nodosum cf. Fig. 102). 
It arises by a large number of fine rootlets on each side of the 
hind-brain behind the glossopharyngeus, and the roots converge in 
a fan-like manner into the proximal ganglion; from here a stout 


THE NERVOUS SYSTEM 269 


nerve passes ventrally and enters the ganglion nodosum situated 
above the fourth and fifth visceral arches. Branches pass from 
here into the fourth and fifth arches, and the main stem is con- 
tinued backward as the pneumogastric nerve s.s.. From the hinder 
portion of the spreading roots a strong commissure is continued 
backward parallel to and near the base of the neural tube as far 
as the fifth somite; this is provided with three small ganglion-like 
swellings. This condition is found about the end of the fourth 
day. Later this commissure unites with the main sympathetic 
trunk, and part of the vagus ganglion separates from the remain- 
der as the ganglion cervicale primum of the sympathetic trunk. 

During the fifth and sixth days the main stem of the vagus 
grows farther back and innervates the heart, lungs, and stomach. 
Neuroblasts of the sympathetic system accompany the vagus 
in its growth, and form the various ganglion cells of the heart, 
and other organs innervated by the vagus. 

During che fifth and sixth days the ganglion nodosum, which 
originally lay at the hind end of the pharynx, is carried down 
with the retreat of the heart into the thorax, and on the eighth 
day it is situated at the base of the neck in close contact with 
the thymus gland. 

11. The Eleventh Cranial or Spinal Accessory Nerve. No ob- 
servations on the development of this nerve in the chick are 
known to me. 

12. The tweljih cranial or hypoglossus nerve appears on the 
fourth day as two pairs of ventral roots opposite the third and 
fourth mesoblastie somites; each root is formed, like the ventral 
roots of the spinal nerves, of several bundles that unite in a com- 
mon slender trunk; ganglia are lacking, as in the first and second 
cervical nerves. The roots of the hypoglossus are a direct con- 
tinuation of the series of ventral spinal roots, and as they are 
related to somitic muscle plates in the same way as the latter, 
there can be no doubt of their serial homology with ventral roots 
of spinal nerves. The first four mesoblastic somites are subse- 
quently incorporated in the occipital region of the skull, and 
thus the hypoglossus nerve becomes a cranial nerve. No nerves 
are formed in connection with the first and second mesoblastic 
somites. As the occipital region of the skull forms in the region 
of the occipital somites, two foramina are left on each side for 
exit of the roots of the hypoglossus (Figs. 150 and 244). 


270 THE DEVELOPMENT OF THE CHICK 


During the fourth and fifth days the nerve grows back above 
the roof of the pharynx, then turns ventrally behind the last 
visceral pouch and forward in the floor of the pharynx. 


According to Chiarugi minute ganglia are formed in the second, 
third, and fourth somites: but they soon degenerate (fourth day) without 
forming nerves. 


CHAPTER IX 
ORGANS OF SPECIAL SENSE 


I. Toe Ey 

THE development of the eye up to the stage of 36 somites has 
been already described. We shall now consider the subsequent 
changes in the following order: (1) optic cup, (2) vitreous body, 
(3) lens, (4) anterior chamber, cornea, iris, ete., (5) choroid and 
sclerotic, (6) the conjunctival sac and eyelids, (7) the choroid fis- 
sure and the optic nerve. 

1. The optic cup at the stage of 36 somites is composed of 
two layers, an inner, thicker layer, known as the retinal layer, 
and an outer, thinner layer, known as the pigment layer; these 
are continuous with one another at the pupil and choroid fissure. 
The inner and outer layers come into contact first in the region 
of the fundus, and the cavity of the original optic vesicle is gradu- 
ally obliterated. The choroid fissure is in the ventral face of 
the optic cup; it is very narrow at this time, and opens distally 
into the pupil; centrally it ends at the junction of optic stalk 
and cup, not being continued on the stalk as it isin mammals (Fig. 
157). 

The walls of the optic cup may be divided into a lenticular 
zone (pars lenticularis or pars caca) and a retinal zone; the former 
includes the zone adjacent to the pupil, not sharply demarcated 
at first from the remainder or retinal zone, but later bounded dis- 
tinctly by the ora serrata. The retinal zone alone becomes the 
sensitive portion of the eye; the lenticular zone develops into the 
epithelium of the iris and ciliary processes. 

In the lenticular zone the inner and outer layers become actu- 
ally fused, but in the retinal zone they may always be separated; 
indeed, in most preparations they are separated by an actual 
space produced by unequal shrinkage. 

The differentiation of the lenticular from the retinal zone 
begins about the seventh day, when a marked difference in thick- 


271 


272 THE DEVELOPMENT OF THE CHICK 


ness appears. The transition from the thinner lenticular to the 
thicker retinal zone soon becomes rather sudden in the region of 
the future ora serrata. About the eighth or ninth day a further 
differentiation arises within the lenticular zone, marking off the 
regions of the iris and ciliary processes (Fig. 159). The region 


eo Mes RT 


157 158 
Fig. 157. — Section through the eye of a chick embryo at the 
beginning of the fourth day of incubation. (After Froriep.) 
ch. Fis. 1., Lip of the choroid fissure. Di., Lateral wall of the 
diencephalon. 1’, 1”, Distal and proximal walls of the lens. — st., 
Optic stalk. 
Fic. 158. — Section of the distal portion of the eye of a chick, 
second half of the fifth day of incubation. (After Froriep.) 
ce. ep. int., Internal epithelium of the cornea. Corn. pr., Cornea 
propria. Ect., Eetoderm. ep., Epidermis ir., Iris. mes., Meso- 
derm. p., Pigment layer of the optic cup. r., Retinal layer of 
the optic cup. 


of the iris is a narrow zone bounding the pupil in which the two 
layers of the optie cup become blended so that pigment from 
the outer layer invades the inner layer; the epithelia are decidedly 


ORGANS OF SPECIAL SENSE 273 


T2715 


ab. CH. 


Corn. — 


Fie. 159. — Frontal section of the eye of an eight day chick. 

ant. ch., Anterior chamber of the eye. ch., Choroid coat.  cil., Ciliary 
processes. Corn., Cornea. 1. e. 1., Lower eyelid. n. m., Nictitating mem- 
brane. olf., Olfactory sac. op. n., Optic nerve. o. s., Ora serrata. p., 
Pigment layer of the optic cup. post. ch., Posterior chamber of the eye. 
ret., Retina. scl., Sclerotic coat. sel. C., Sclerotice cartilage. u.e. 1., Upper 
eyelid. 


thinner than in the ciliary region. The mesenchyme overlying 

the iris early becomes condensed to form the stroma of the iris; 

the epithelia form the uvea of the developed iris (Fig. 159). 
The muscles of the iris (sphincter pupille) are stated by 


274 THE DEVELOPMENT OF THE CHICK 


Nussbaum, Szily, and Lewis to arise from epithelial buds of the 
pupillary margin and the adjacent portion of the pigment layer 
of the iris. The marginal buds (Fig. 160) begin to form during 
the seventh day, the more peripheral ones somewhat later; the 
former are less numerous and larger than the latter. The 
observations are well supported, and appear to leave no doubt 
that the specificity of the ectoderm cells of the iris are not fixed. 
According to Lewis the wandering pigmented cells of the ante- 
rior portion, at least, of the choroid also arise from the pigment 
laver of the optic cup. 

The ciliary processes begin to form from the ciliary region 
of the lenticular zone on the eighth day (Fig. 159); the epithelium 


A 


Via. 160.—Two sections of the pupillary margin of the eye of a chick of 13 
days’ incubation. <A., X 260. B., 130. (After Lewis.) 
ce. P., Ciliary process. E. B., Epithelial bud. P., Margin of pupil. p. L., 
Pigment layer of Iris. r. 1., Retinal layer of iris. Sph., Bud for the forma- 
tion of the sphineter muscle of the iris, derived from the margin. Sph.’, 
Sph.”, Submarginal buds of the sphincter. 


becomes thrown into folds projecting towards the posterior cham- 
ber, the cavity of the folds being filled by the mesenchyme of the 
developing choroid coat. The muscles of the ciliary body de- 
velop from the mesenchyme of the processes, which acquire a 
connection with the lens through a special differentiation of the 
vitreous body, the zonula ciliaris (zonula Zinnii). 

In the retinal portion of the optic cup the inner layer forms 
the entire retina proper from the internal limiting membrane 
to the rods and cones inclusive. The outer layer forms the pig- 


ORGANS OF SPECIAL SENSE 275 


ment layer of the retina. About the middle of the fourth day 
pigment begins to develop in the outer layer and extends through- 
out it, even to the distal portion of the optic-stalk at first (Ucke, 
91). The histogenesis of the retina of the chick has been de- 
scribed by Weysse (1906). 

2. The Vitreous Humor (Corpus Vitreum). Until compara- 
tively recently embryologists have adhered to the view stated 
by Schoeler (1848) and Ixolliker (1861) that the vitreous body 
arises from mesenchymal cells that enter the eyeball through 
the choroid fissure. The fact that the embryonic vitreous humor 
of birds is almost entirely devoid of cells was a serious difficulty. 
The cells are in fact so scanty as to be absent in many entire 
sections. Moreover, in character they resemble embryonic 
blood-cells and not mesenchyme, and disappear entirely by the 
eighth day. It seems impossible that they should play any 
important part in the origin of the massive vitreous body. Re- 
searches of the last few years have demonstrated that the vitreous 
body is primarily of ectodermal origin, its fibers arising as processes 
of cells of the inner layer of the optic cup and the matrix as 
secretion. According to some the cells of the lens are responsible 
wholly (Lenhossek) or in part (Szili) for the fibers; this view, 
however, has been strongly combatted (Ix6lliker and Rabl) and 
requires further evidence to substantiate it. 

Both retinal and czecal parts of the cup take part in the forma- 
tion of the fibers of the vitreous body; the retinal part is at first 
the most important, and the primary vitreous body is almost 
entirely retinal in its origin. But after the cxeal part is differ- 
entiated the activity of the retinal part becomes less, and the 
greater part of the fibers of the vitreous body appears to be 
formed from cells of the cawcal part, that send out branching 
and anastomosing processes into the posterior chamber. There 
is no sharp boundary between the fibers that form the vitreous 
body and those that form the zonula; and the fibers of the latter 
may be regarded as homologous to those of the former. The 
matrix of the embryonic vitreous body may be regarded as a 
secretion of the walls of the optic cup. Later, the secretion 
appears to be confined to the ciliary processes. It is possible 
that the mesenchyme plays some part in the formation of the 
vitreous body after the formation of the pecten begins; but there 
is no evidence that it does so at first. 


276 THE DEVELOPMENT OF THE CHICK 


3. The Lens. The account of the development of the lens is 
mainly after Rabl. The wall of the lens-sac is everywhere a sin- 
ele-layered epithelium, though the nuclei are at different levels in 
the cells. 

Shortly after the lens-sac has become separated from the ecto- 
derm the proximal wall (that next the cavity of the optic cup) 
begins to thicken by elongation of the constituent epithelial cells 
(Figs. 157 and 158). During the fourth day the elongation of the 
cells increases greatly as the first step in the formation of the lens 
fibers, while those of the distal wall remain practically unchanged, 
being destined to form the epithelium of the lens. Between the 
cells of the proximal and distal walls are found cells of an inter- 
mediate character, bounding the equator of the lens (Fig. 158). 

During the fifth day the elongation of the cells of the proximal 
wall proceeds apace; those in the center of the wall are most 
elongated and there is a gradual decrease towards the equator 
of the lens. In this way the face of the proximal wall gradually 
approaches the distal wall and meets it on the fifth day, thus 
obliterating the central part of the lens cavity, though the periph- 
eral part remains open for a considerably longer time (Fig. 158). 
The nuclei of the lens fibers occupy approximately their center, 
and thus form a fairly broad curved band, concave towards the 
optic cup. At the same time the lens is increasing very rapidly 
in size. 

During the sixth, seventh, and eighth days the same processes 
continue and the elongation of the lens fibers makes itself felt 
on the inner face of the lens which becomes convex. The form 
and arrangement of the parts is shown in Figure 159. The fibers 
already present are destined to form only the core of the adult 
lens; and a new process begins at this time, leading to the forma- 
tion of fibers that wrap themselves around this core in a merid- 
ional direction and form many concentric layers (666 according 
to Rabl). These new concentric fibers proceed from cells situated 
between the core fibers and the lens epithelium, that is, around 
the equator of the lens. There is a very rapid multiplication of 
cells here; those next the core transform into fibers arranged 
meridionally on the surface of the core; others develop over these 
and thus the original fibers come to be surrounded by more and 
more concentric layers. At first these are disposed rather irregu- 
larly, but soon the arrangement becomes extraordinarily regular. 


ORGANS OF SPECIAL SENSE 


This process is kept up not only 
during embryonic life, but dur- 
ing the entire growth of the 
fowl; thus the thickness of the 
superimposed lamelle is only 
0.60 mm. at hatching, but is 
2.345 mm. in the adult (Rabl). 

In the fowl the lens includes 
three concentric layers of fibers: 
(1) the central mass or core 
formed by the proximal wall of 
the original lens-sac; this has 
the same diameter (0.80 mm.) 
as the entire fiber mass at eight 
days. Nuclei are entirely ab- 
sent. (2) An intermediate layer 
of meridional rows of fibers 
rather irregularly arranged, 
which shade gradually into the 
fibers of the core and into those 
of (8) the radial lamelle, which 
form the greater part of the 
substance of the adult lens. 
The meridional rows and the 
radial lamelle proceed from the 
cells of the intermediate zone 
of the original lens-sac. Fig. 
161 shows a sector of an equa- 
torial section through the lens 
of a chick. The three zones 
are well marked; the extraordi- 
nary regularity of the super- 
imposed layers of the radial 
lamella is well shown. 

The lens epithelium of birds 
and reptiles also produces a 
peculiar structure which may be 
called the equatorial ring (Ring- 
wulst, Rabl). 

It will be seen in the figures 


eu) 
ert 


esasassecqes] 


1. 
< 
pecmeaSens: 
sy Gass cate etacsseesess 
ene gers 
JO ee anes ee Cease ercee ere ars 
CEE SOE PLR EAE AS 
COPE A p< oR 
Reet rer Be S 
ay BS Ot Casares ee. 
ES Teo 
oy VIP OTe 
a HS were 
pale stamseese: 
SER 
aS oy LP 
Svar taeisok 
pen 
Beene: 
=) 
pepeanan 
a, fo) She 


Fia. 161.— Equatorial section through 
the lens of a chick embryo of eight 
days. The main mass of the entire 
lens is represented by irregularly 
arranged central fibers. Towards 
the surface (above) the fibers are 
arranged in rows and are quite 

regularly six sided. (After Rabl.) 


278 THE DEVELOPMENT OF THE CHICK 


that the epithelium is originally thinnest distally and thickens 
towards the equator. This condition increases up to the eighth 
day, at which time the thickening increases more a short distance 
from the equator, so that there is a broad ring-shaped thickening 
of the anterior epithelium separated by a narrow thinner zone 
from the cells of the equatorial zone (cf. Fig. 159). This ring 
increases in thickness during the greater part of the period of 
incubation, and its cells become fibers arranged in a radial direc- 
tion. The meaning of this curious structure is somewhat obscure, 
but from the fact that it shows on its surface the impression of 
the ciliary processes, Rabl was of the opinion that it served in 
accommodation of the eye as an intermediary between the ciliary 
processes and the true lens-fibers. 

4. Anterior Chamber and Cornea, etc. When the optic vesicle 
is first formed it is in immediate contact with the ectoderm. 
After its invagination the lips of the optic cup withdraw a short 
distance from the surface. At the same time the lens invagi- 
nates and is cut off from the ectoderm, but remains in contact 
with it during the third day. There is thus a ring-shaped space 
between the lens and optic cup on the one hand and the ectoderm 
on the other, which is the beginning of the anterior chamber of 
the eye (ef. Fig. 96 C). With the formation of the cornea the 
lens withdraws somewhat from the surface and the space spreads 
over the whole external surface of the lens; at first it Is very 
narrow, but increases in size by the formation of the iris and 
the bulging of the cornea. 

The cornea itself develops from two sources: (1) the external 
epithelium is derived from the ectoderm overlying the anterior 
chamber, (2) the cornea propria and the internal epithelium 
lining the anterior chamber develop from the surrounding mesen- 
chyme but in somewhat different ways. 

The cornea propria appears on the fourth day as a deli- 
cate structureless membrane beneath the corneal epithelium. 
During the fifth day it increases to about the thickness of 
the overlying ectoderm (Fig. 158). About this time mesen- 
chyme cells from the margin of the optic cup begin to migrate 
between the cornea propria and lens, and soon form a single 
complete layer of cells on the inner face of the cornea propria; 
this layer becomes the inner epithelium of the cornea (Fig. 158). 
The cornea propria is still devoid of cells, but on the sixth and 


ORGANS OF SPECIAL SENSE 279 


seventh days the mesenchyme surrounding the eyeball begins 
to penetrate it from all sides in the form of a compact wedge, 
which, advancing in the substance of the cornea propria, soon 
meets in the center. These cells form the so-called corpuscles 
of the cornea. They appear arranged in strata from a very 
early period. 

The anterior chamber is bounded by the cornea externally; 
its margins, which are at first coincident with the lips of the optic 
cup, soon extend peripherally over the iris (Fig. 159). The inner 
epithelium ceases at the margin of the cavity or is continuous 
with the cells of the sclerotic; it does not appear, in an eight-day 
chick at any rate, to be reflected over the iris, but the epithelium 
of this structure next the anterior chamber appears to be simply 
a special differentiation of its own superficial cells. The anterior 
chamber is closed centrally by the lens, but communicates more 
or less for a considerable period around its margin with the pos- 
terior chamber. This is at least the appearance in good sections; 
it seems probable, though, that in life there is contact between 
the optic cup and lens. 

The stroma of the iris proceeds from that portion of the 
mesenchyme left in association with the pars iridis retine after 
the peripheral extension of the anterior chamber. It becomes 
very vascular at an early stage. The canal of Schlemm arises 
as aseries of vacuoles just peripheral to the margin of the ante- 
rior chamber about the eighth day. These soon run together 
to form a ring, which is separated from the anterior chamber 
by the ligamentum pectinatum tridis. 

5. The choroid and sclerotic coats are differentiations of the 
mesenchyme surrounding the optic cup. But little is known 
concerning the details of their development in the chick. A 
figure of Kessler’s shows chromatophores developed in the choroid 
coat at twelve days; I find a very few already formed at eight 
days. Cartilage begins to appear in the sclerotic at eight days, 
the forerunner of the sclerotic ossicles (Fig. 159). 

6. The Eyelids and Conjunctival Sac. The integument over 
the embryonic eyeball remains unmodified until about the 
seventh day. At this time a circular fold of the integument 
forms around the eyeball with the pupil as its center. At the 
same time a semi-lunar fold develops within the first on the side 
of the eyeball next the beak. (See Figs. 122-124.) From the 


280 THE DEVELOPMENT OF THE CHICK 


first fold the upper and lower eyelids are developed, and from the 
second the third eyelid or nictitating membrane. The area bounded 
by the outer ring-shaped fold becomes the conjunctival sac. 

From their place of origin the free edges of these folds then 
erow towards the center, and thus a cavity, the conjunctival 
sac, is formed between the folds and the integument over the eye- 
ball (conjunctiva sclerz). The outer fold grows more rapidly 
above and below than at the sides and the opening narrows, 
becoming, therefore, gradually elliptical and finally somewhat 
spindle-shaped. Thus the upper and lower eyelids are established. 
The semi-lunar fold of the embryonic nictitating membrane also 
grows towards the pupil, most rapidly in its center. The con- 
junctival sac also expands peripherally, especially at the inner 
angle of the eye, and thus accommodates itself to the increasing 
size of the eyeball (Fig. 159). 

The Harderian gland is visible on the eighth day as a solid 
ingrowth of ectodermal cells of the conjunctival sac at the inner- 
most angle of the nictitating membrane. 

Feather germs develop on the outer surface of both upper 
and lower lids especially at their edges. The ectoderm covering 
the inner faces of the upper and lower lids, both faces of the nic- 
titating membrane and the remainder of the conjunctival sac 
becomes modified into a moist mucous membrane. Over the 
cornea the ectoderm is especially modified as already noted. 

Papille Conjunctiva Sclere. On the seventh day of incubation 
papille begin to appear on the surface of the conjunctiva sclerz 
and soon form a ring surrounding the iris at some distance periph- 
eral to its margin (Figs. 122, 123 and 124). The number of these 
papille appears to be quite constantly fourteen. They are at first 
fully exposed owing to the undeveloped condition of the eyelids, 
but the latter overgrow them about the eleventh or twelfth days. 
Degeneration of the papille begins about this time, and on the 
thirteenth day they have entirely disappeared. In section they 
are found to be thickenings of the ectoderm, produced by multi- 
plication of the cells. They may rise above the surface; but more 
frequently project inwards towards the connective tissue. There 
is apparently no accompanying hypertrophy of the latter. Thus 
they differ quite essentially from feather germs with which it 
seems natural to compare them; and their significance is entirely 
problematical (see Nussbaum). 


ORGANS OF SPECIAL SENSE 281 
7. Choroid Fissure, Pecten, and Optic Nerve. The pecten of 
the hen’s eye is a pigmented vascular plate inserted in the depres- 
sion occupying the center of the elongated blind spot, or entrance 
of the optic nerve, which extends meridionally from the fundus 
nearly to the ora serrata. The pecten projects a considerable 
distance into the posterior chamber and its free edge is much 
longer than its base, being consequently folded like a fan; hence 
the name. The optic nerve runs along the base of the pecten, 
its fibers passing off on either side into the retina; thus it con- 
tinually diminishes in size until it disappears. The pecten is 
consequently separated from the choroid coat by the optic nerve. 
It is supposed to function as a nutrient organ for the layers of 
the retina, by means of lymph channels that pass off from its 
base into the retina. There is no arteria centralis retinz in the 
bird’s eye. 

These structures develop in connection with the choroid 
fissure as follows: On the fourth day the choroid fissure has be- 
come a very narrow slit, and by the middle of the day its edges 
are in apposition in the pars ceca of the bulbus. Proximally, 
however, the meeting of the lips of the fissure is prevented by the 
mesoblast, in which the basal blood-vessel runs along the entire 
length of the open portion of the fissure. During the fourth 
day this blood-vessel enters the posterior chamber with its en- 
veloping mesenchyme along the entire length of the open portion 
of the choroid fissure, and forms a low mesenchymal ridge con- 
nected by a narrow neck of mesenchyme in the fissure with the 
mesenchyme outside. During the fifth day the ridge becomes 
higher and keel-shaped, and a thickening appears along part of 
its free edge above the blood-vessel. During this day also fusion 
of the lips of the choroid fissure has taken place in the pars cca. 
At the same time an important change begins in the proximal 
portion of the choroid fissure that leads to the formation of the 
pecten proper. This is an involution of the lips of the optic cup 
bounding the choroid fissure on each side of the mesodermal 
keel, and their continuous ingrowth until they meet over the 
keel and fuse above it in a mass in which the outer and inner 
layers of the retina are indistinguishably fused. Thus the proxi- 
mal portion of the mesodermal keel is enclosed in a kind of tunnel 
composed of the involuted edges of the optic cup. The forma- 
tion of this tunnel progresses gradually from the fundus towards 


282 THE DEVELOPMENT OF THE CHICK 


the ora serrata by the same process of involution, until on the 
eighth day the mesodermal keel is completely covered up. 

Fig. 162 gives a diagrammatic view of the condition of the 
pecten in the middle of the seventh day of incubation. Figs. 
163 and 164 show sections through this at the points a, b, c¢, d, e, 
indicated in the figure. The formation of the tunnel will be 
readily understood by study of the figures. It will be seen that 
the major portion of the embryonic pecten is of ectodermal origin, 
and that the mesoderm forms a relatively inconspicuous part 
of it. Later, on the same day, it becomes increasingly difficult 


C [4 g : 

op a Mes. Db. C. e 

Fia. 162. — Diagrammatic reconstruction of the pecten of the 
eye of a chick embryo of 74 days’ incubation. (After Bernd.) 

Ch. fis. l., Lip of the choroid fissure. Ch. fiss., Choroid fis- 
sure. Mes., Mesoblast. Mes. b., Boundary of the mesoblast 
within the choroid fissure. Mes. KX., Thickening of the meso- 
blastic keel. op. C., Optic cup. O.St., Optic stalk.  P., Pec- 
ten. P. B., Base of the pecten. 

The arrow indicates the direction of growth of the ecto- 
dermal tunnel. 

The lines a, b, ce, d, e show the planes of the sections re- 
produced in Fig. 163 (a, b, ¢, e) and in Fig. 164 (d). 


to distinguish ectodermal and mesodermal portions of the pecten, 
and thereafter it is quite impossible to say which parts of it are 
of ectodermal and which are of mesodermal origin. During the 
eighth and ninth days the pecten increases greatly in height, 
and becomes relatively very much narrower. 

The folds of the pecten now begin to develop and, by the 
seventeenth day their number is 17-18, the same as in the adult. 
The pigment does not begin to appear until about the twelfth day. 
The details of the development of the blood-vessels are not known. 


ORGANS OF SPECIAL SENSE 283 


The Optic Nerve. Owing to the relations established by the 
choroid fissure, the floor of the optic stalk is continuous from the 
first with the inner layer of the retina (Fig. 96 B), and it furnishes 
the path along which the optic nerve grows. The axones of the 
optic nerve originate, for the most part, from the retinal neuro- 
blasts, composing the layer next to the cavity of the optic cup, 
and their growth is thus centripetal. They are first formed in 
the fundus part of the retina, and grow in the direction of the 


Fic. 163. — Outlines of sections in the planes a, b, ¢, e, of 
Fig. 163. (After Bernd.) 


bl. v., Blood vessel. i. 1., Inner or retinal layer of the 
optic cup. o.1., Outer or pigment layer of the optie cup. 
P. inv., Angle of invagination of the pecten. Other ab- 
breviations as before. (Fig. 162.) 


optic stalk between the internal limiting membrane and the neu- 
roblast layer (ganglion cell layer), thus forming a superficial layer 
of axones; their formation begins on the fourth day, and there is 
a period about the end of this day when axones are found in the 
distal part of the optic stalk, next to the bulbus oculi, but not 
in the proximal part, next to the brain. This observation affords 
conclusive proof of the retinal origin of the fibers of the optic 


284 THE DEVELOPMENT OF THE CHICK 


nerve; moreover, at an early stage of their differentiation it is 
possible to trace their connection with retinal neuroblasts. 

The first fibers of the optic nerve are formed, as already 
stated, from the fundus part of the retina; the fibers, therefore, 
pass directly to the floor of the optic stalk; but on the fifth day 
the formation of fibers begins from more distal portions of the 
retina and these do not grow towards the insertion of the optic 
stalk, but towards the choroid fissure; arrived there, they bend 
centrally and run in a bundle on each side along the floor of the 
bulbus oculi to the optic stalk, where they join with the fibers first 
formed. The later formed fibers pass to still more distal portions 


Fic. 164. — Section in the plane of d of Fig. 162, to 
show the histological structure. (After Bernd.) 
Abbreviations as before. 


of the choroid fissure, and, as the pecten forms in the manner 
already described, the fibers of the optic nerve all unite beneath 
it on their way to the original optic stalk. Thus, the optic nerve 
obtains an insertion coincident in length with the base of the 
pecten, and its fibers, radiating off into the retina on each side 
of the pecten, separate the latter completely from the choroid 
coat of the eyeball. 

The optic stalk is at first a tubular communication between 
the optic vesicle and the fore-brain, and its walls are an epithelial 
layer of the same thickness throughout. The fibers of the optic 


ORGANS OF SPECIAL SENSE 285 


nerve grow into its ventral wall exclusively, between its epithelial 
cells, which gradually become disarranged and irregular. Thus 
the ventral wall becomes increasingly thick and the lumen excen- 
tric. By the sixth day the lumen appears in cross-section as a 
narrow lenticular space with an epithelial roof, above the large 
optic nerve. Soon after, the lumen disappears entirely; no trace 
of its former existence is to be found on the eighth day. 


Il. THE DEVELOPMENT OF THE OLFACTORY ORGAN 


The origin of the olfactory pit, external and internal nares, and 
olfactory nerve, has already been considered (pp. 169,215, and 263). 
Before the formation of the internal and external nares, not only 
has the entire olfactory epithelium become invaginated, but, owing 
to the elevation of internal and external nasal processes, the pit 
has become so deepened that the margin of the olfactory epithe- 
lium proper now lies a considerable distance within the cavity. 
That part of the nasal cavity thus lined with indifferent epithelium 
is known as the olfactory vestibule. After the fusion of the 
internal nasal process with the external nasal and maxillary 
processes, the cavity deepens still more. 

The choane lie at first just within the oral cavity, but the 
palatine processes of the maxillary process, growing inwards 
across the primitive oral cavity (pp. 298, 299), unite on the sixth 
or seventh day at their anterior ends with the internal nasal 
processes, and thus cut off an upper division of the primitive 
oral cavity at its anterior end from the remainder; in this way 
the internal openings of the nasal cavities into the oral cavity 
are carried back of the primitive choan; they are henceforward 
known as the secondary choane. Further growth of the palatine 
processes brings them nearly together in the middle line along 
the remainder of their length, about the eleventh day; but fusion 
does not take place, the birds possessing a split palate. Thus 
the superior division of the primitive oral cavity is added to the 
respiratory part of the nasal passages. 

The nasal cavity is further elaborated between the fourth 
and eighth days by ingrowths from the lateral wall (turbinals) 
and by the formation of the supraorbital sinus as an evagination 
that grows outwards above the orbit. Three turbinals are formed 
in the nasal cavities, viz., the superior, middle, and inferior tur- 
binals. These arise as folds of the lateral wall projecting into 


286 THE DEVELOPMENT OF THE CHICK 


the lumen, the superior and middle from the olfactory division 
proper, and the inferior from the vestibulum; on the middle 
turbinal, however, the sensory epithelium gradually flattens out 
to the indifferent type. The middle turbinal appears first in 
the ventral part of the olfactory division, about the beginning 
of the fifth day, and the superior somewhat later, immediately 
above the former, the two being separated by a deep groove 
(Fig. 165). The vestibular turbinal arises still later, and is well 
formed on the eighth day. 

Fig. 166 shows a reconstruction of the nasal cavity, seen from 
the lateral side, of an embryo of about seven days. It is a re- 
construction of the epithelium, and thus practically a mold of the 
cavity; therefore projections into the cavity appear as depressions 
in the model, and the grooves and outgrowths of the external 
wall as projections. The superior turbinal has an oval shape with 
the long axis in an apical direction; it is bounded by a fairly deep 
depression, the elevated margin of the model, from the lower end 
of which the supra-orbital sinus (8. s’0.) passes off ventrally and 
externally. The deep depression immediately below the superior 
turbinal lodges the median turbinal. A fairly long passage leads 
off from its neighborhood to the choanz and a shorter one, the 
vestibulum, to the external nares. The depression in the wall of 
the vestibulum is caused by the vestibular or inferior turbinal. 
The palatine and maxillary sinuses are not yet formed. 

The external nares are closed during the greater part of the 
period of incubation by apposition of their walls. The form 
and dimensions of the nasal cavities change greatly during incu- 
bation, owing to shifting in the original positions of the turbinals, 
outgrowth of the facial region, and development of sinuses. The 
details are not very well investigated, and an examination of 
them would lead too far. 

There has been a good deal of discussion as to the existence 
of an organ of Jacobson in the nose of birds; it has usually been 
assumed that it is entirely absent even in the embryo. Others 
have identified the ducts of nasal glands as a modification of this 
organ. Recently, however, Cohn has described a slight evagi- 
nation in the median wall of the primary olfactory pit, that 
agrees precisely in its form and relationship with the first rudi- 
ment of the organ of Jacobson in reptiles. Although it persists 


only from the stage of about 5.3 mm. to about the stage of 


ORGANS OF SPECIAL SENSE 287 


5.9 mm. head-length, he identifies it positively as a rudimentary 
organ of Jacobson. 

The septal gland arises on the eighth day from the inner 
wall of the vestibulum, opposite the base of the vestibular tur- 


PF coe 


° prc 


2 
eo seses 
ar 


a2 
22 


Fic. 165. — Transverse section of the olfactory organ of a 
chick embryo, of 7.5 mm. head length. (After Cohn.) 


f., Line of fusion. e.n., External nasal process. 1. n., 
Internal nasal process. T. 1, T. 2, Intermediate and supe- 
rior turbinals. 


binal, as a solid cord of cells. This grows backwards in the nasal 
septum and passes to the outer side and branches, subsequently 
acquiring a lumen. 


288 THE DEVELOPMENT OF THE CHICK 


Ill. THe DEVELOPMENT OF THE EAR 

The ear develops from two entirely different primary sources, 
viz.,the otocyst,and the first visceral or hyomandibular cleft: The 
former furnishes the epithelium of the membranous labyrinth; the 
entodermal pouch of the latter becomes the tympano-eustachian 
eavity; and part of the external furrow forms the external audi- 
tory meatus; the tissue between the internal pouch and the ex- 
ternal furrow develops into the tympanum. The mesenchyme in 
the neighborhood of each of these primordia becomes modified, 


ia. 166. — Reconstruction of the nasal cavity of a chick 


embryo of about 7 days; lateral view. (After Cohn.) 
Ch., Choane. e. N., External nares. 38. s’o., Supraor- 
bital sinus. T. 1, 'T. 2, T.3, Intermediate, superior and in- 
ferior (vestibular) turbinals. 


(1) to form the bony labyrinth, perilymph, and other mesenchymal 
parts of the internal ear, and (2) to form the auditory ossicles of 
the middle ear. Thus the ear furnishes a striking example of the 
combination of originally diverse components in the formation 
of a single organ. The course of evolution of this complex sense- 
organ is thus illustrated in the embryonic development; in the 
Selachia the hyomandibular cleft is a communication between 
pharynx and exterior, like the branchial clefts, and still preserves 
to a certain extent the respiratory function. The embryonic 
history furnishes a summary of the way in which it was gradually 


ORGANS OF SPECIAL SENSE 289 


drawn into the service of the otocyst in the course of evolu- 
tion. 

Development of the Otocyst and Associated Parts. In the pre- 
ceding chapter we took up the formation of the otoeyst and the 
origin of the endolymphatic duct. The latter is at first an apical 
outgrowth from the otocyst, but its attachment soon becomes 
shifted to the median side of the otocyst, owing to the expansion 
of the dorsal external wall of the 
latter (Fig. 167). Three divisions 
of the otocyst may now be distin- 
euished: (a) ductus endolymphaticus 
or recessus labyrinthi; (b) pars su- 
perior labyrinthi; (¢) pars inferior 
labyrinthi. The boundary between 
the two latter is rather indistinctly 
indicated at this stage by a shallow 
groove on the median face of the 
otocyst. The development of these 


parts may now be followed separately. 


(a) The Development of the Ductus F ee ae Ee a of te oe 
= é . of a chick embryo short e= 
Endolymphaticus. It was noted in : So eieraae 
z fore its separation from the 
} 


Chapter VI that the ductusendolym- gctoderm. (After Krause.) 

phaticus is united to the epidermis D. e., Endolymphatic duct. 
Ect., Ectoderm. p. v., Pocket 
for formation of vertical semicir- 
lumen up to the stage of 104 hours eular canals. X indicates the 


at least (Fie. 98). Shortly after. this Strand of cells uniting the endo- 
Cat enone , lymphatic duct to the ectoderm. 


by a strand of cells that preserves a 


connection is entirely lost. 

The opening of the endolymphatic duct into the otocyst 
appears to be shifted more and more ventrally along the median 
surface, with the progress of differentiation of the other parts 
of the otocyst, until it lies in the region of communication of 
the utriculus, sacculus and lagena (Figs. 168 and 171). This is 
brought about by the various foldings and expansions of the 
wall of the otocyst described in b and c. In the meantime the 
endolymphatic duct has increased in length with the growth of 
the surrounding parts, and on the sixth day the distal half begins 
to expand to form the saccus endolymphaticus, lying between 
the utriculus and the hind-brain. The elongation of the entire 
endolymphatic duct and the enlargement of the saceus continue 
during the seventh day, and on the eighth day the saccus overtops 


290 THE DEVELOPMENT OF THE CHICK 


the hind-brain and bends in above it towards the middle line (Fig. 
168). The right and left sacci are, however, still separated by 
a considerable space. The walls of the saccus already form a 
large number of low folds, presumably glandular, the first begin- 


OX CTL LE ass 


ia. 168. — Transverse section through the head of a chick embryo of eight 
days in the region of the ear (photograph). 

C. a., Anterior semicircular canal. C. h., Horizontal semicircular canal. 
Caps. aud., Auditory capsule. Cav. Tymp., Tympanic cavity. Col., Colu- 
mella. Duet end., Endolymphatie duct. ex. au. M., External auditory 
meatus. Fis. Tub., Tubal fissure. Lag., Lagena. M. C., Meckel’s cartilage. 
Myel., Myelencephalon. N’ch., Notochord. p’l., Perilymph. Sac., Saceu- 
lus. Sae.end., Endolymphatie sac. Tub. Eust., Eustachian tube. Tymp., 
Tympanum. Utr., Utriculus. X., Sac derived from the inner extremity 
of the tympanic cavity. 


nings of which were visible on the sixth day. The form of the 
saccus and ductus endolymphaticus at a somewhat later stage 
is shown in the reconstruction (Fig. 173). 


ORGANS OF SPECIAL SENSE 291 


It is interesting to note that the epidermic attachment to the endo- 
lymphatic duct is about at the junction of the saccus endolymphaticus 
and ductus endolymphaticus s.s. If this may bear a phylogenetic inter- 
pretation, it would seem that the saccus should be regarded as an addi- 
tion to the primitive ductus of Selachii, which opens on the surface. 


(b) Development of the Pars Superior Labyrinthi; Origin of the 
Semicircular Canals. We have already seen that the shifting 
of the ductus endolymphaticus to the median surface of the 
otocyst is brought about by a vertical extension of the superior 
lateral wall of the otocyst, which forms a shallow pocket opening 
widely into the otocyst (Fig. 167). Shghtly 
later a second pocket is formed by a horizon- 
tally extended evagination of the lateral wall 
of the pars superior directed towards the 
epidermis. These two pockets, known as the 
vertical and horizontal pockets, are the fore- 
runners of the semicircular canals: the vertical 
of both anterior and posterior, and the hori- 
zontal of the horizontal semicircular canal. Fie. 169.— Model of 
The horizontal pocket forms at about the mid- the auditory laby- 
dle of the external surface on the fifth day; mth (otocyst) of 
immediately above it is a roughly triangular, eniek emery e oF 

. ; , ee undetermined age ; 
pear-shaped depression in the wall of the oto- — yjew from behind. 
cyst, bounded by the vertical pocket on the (After Réthig and 
other two sides. Thus the vertical pocket con- — Brugsch.) 
sists of two divisions, anterior and posterior, C. 1., Pocket for 

: : Y ; the formation of the 
meeting at the apex of the otocyst (Fig. 169). lateral (horizontal) 

The pockets gradually deepen; and the eens Re 
semicircular canals arise from them by the fu- mation of vertical 
sion of the walls of the central part of each Ss Rae 
pocket, thus occluding the lumen except at of ductus cochlearis 


the periphery (Fig. 170). The fused areas 224 lagena. D. e., 
: 7 endolymphatic duct. 


subsequently break through. The peripheries 
thus form semicircular tubes communicating at each end with 
the remainder of the superior portion of the otocyst, or utriculus, 
as it may now be called. Three semicircular canals are thus 
formed, one from each division of the original vertical pocket 
and one from the horizontal pocket. The upper ends of the an- 
terior and posterior semicircular canals, formed from the anterior 
and posterior divisions of the vertical pocket, open together into 


292 THE DEVELOPMENT OF THE CHICK 

the apex of the utriculus; and the horizontal canal formed from 
the external pocket extends between the separated lower ends 
of the other two. 

We must now proceed to a more detailed examination. In 
point of time the anterior (sagittal) 
semicircular canal is the first to be 
formed (Fig. 171); the external (hori- 
zontal or lateral) canal comes next, 
and considerably later the posterior 
(frontal). Thus the anterior canal 
is at first the largest, the external 
next, and the posterior the smallest. 
These differences however, 
largely compensated in the course 
of the embryonic development. The 
ampullze appear as dilations in the 
pockets even before the canals are 


are, 


Fic. 170. — Model of the auditory 
labyrinth of a chick embryo of 6 
days and 17 hours; external view. 
(After R6éthig and Brugsch.) 


formed, and are conspicuous dila- 
tions by the time that the central 
parts of the pockets have broken 
through (Fig. 172). 


C. a., Poeket for formation of 
anterior semicircular canal. C. 1., 
Pocket for formation of lateral 


Figs. 170-173 show the pockets 
a and canals at six days seventeen 
semicircular canal. C. p., Pocket ; 
for formation of posterior semicir- hours, seven days seventeen hours, 
cular canal. D. ¢., Duetus eoch- 
learis. D.e., Endolymphatie duct. 
La., Lagena. 


eight days seventeen hours, and 
eleven days seventeen hours. It 
will be seen that, whereas the an- 
terior and lateral canals are formed from the start in planes at 
right angles to one another, viz., the sagittal and horizontal, the 
posterior canal is not at first in the third or frontal plane, but 
gradually assumes it. 

The form of the utriculus is gradually assumed during the 
formation of the semicircular canals; it becomes drawn out into 
a roughly triradiate form, so that it consists of a central cavity 
and three sinuses, viz., the median sinus which receives the end 
of the anterior and posterior semicircular canals, the posterior 
sinus situated above the ampulla of the external semicircular 
canal, and the anterior sinus in the region of the ampull of the 
horizontal and sagittal semicireular canals (ef. Fig. 173). A short 
distance in front of the posterior sinus on the median face of 


ORGANS OF SPECIAL SENSE 293 


the utriculus occur the openings of the ductus endolymphaticus, 
sacculus, and ductus cochlearis; the two latter derived from the 
pars inferior of the otocyst, to the development of which we 
now turn. 

(c) Development of the Pars Inferior Labyrinthi; Lagena, 
Ductus Cochlearis, and Sacculus. During the changes described 
in the pars superior labyrinthi, the pars inferior has developed 
into the ductus cochlearis and lagena on the one hand, and the 
sacculus on the other. Throughout the series of the vertebrates 


Tic. 171.— Model of the auditory labyrinth of the left side of a chick 
of 7 days and 17 hours. A. Median view. B. External view. 
(After Réthig and Brugsch.) 

A.a., Ampulla of the anterior semicircular canal. A. p., Ampulla 
of the posterior semicircular canal. C. a., Anterior semicircular 
eanal. C.1., Pocket for formation of the lateral semicircular canal. 
C. p., Pocket for formation of the posterior semicircular canal. Sa., 
Saeculus. Other abbreviations as before. 


the structure of the pars superior is very uniform; the pars inferior, 
on the other hand, has a characteristic structure in each class 
and exhibits in general a progressive evolution. The condition 
in the chick is characteristic on the whole for the class of birds. 

At six days the lower division of the otocyst has grown out 
ventralward into a deep pouch which is curved posteriorly and 
towards the middle line (Fig. 170); the terminal portion is the 
rudiment of the lagena, and the intermediate portion of the ductus 


294 THE DEVELOPMENT OF THE CHICK 


cochlearis; the tip of the lagena in its growth ventralward has 
reached the horizontal level of the notochord. The sacculus is 
barely indicated yet, but is clearly seen on the seventh day as 
a slight protuberance on the median surface of the uppermost 
part of the pars inferior; it lies in front of the lower end of the 
endolymphatic duct at a slightly lower level and is separated by 
two depressions above and below, from the anterior ampulla 
and the ductus cochlearis respectively. The furrows above the 
sacculus and below the ampulla of the frontal semicircular canal 
mark the boundary between the pars superior and inferior. 


lic. 172. — Model of the auditory labyrinth of the 
right side of a chick embryo of 8 days and 17 
hours; external view. (After R6thig and Brugsch.) 
A.a., Ampulla of the anterior semicircular canal. 
A.1., Ampulla of the lateral semicircular canal. A. 
p., Ampulla of the posterior semicircular eanal. C. 
a., Anterior semicircular canal. C. 1., Lateral semi- 
circular canal. C. p., Posterior semicircular canal. 
Sa.e., Endolymphatie sac. U., Utriculus. Other 
abbreviations as before. 


A day later (ig. 172), these furrows have cut in deeper and 
have become continuous on the median surface; the lagena has 
enlarged distally, and the sacculus is a hemispherical protuber- 
ance. The tip of the lagena lies beneath the hind-brain (Fig. 


ORGANS OF SPECIAL SENSE 295 


168). The condition shown in Fig. 173, at eleven days seven- 
teen hours is substantially the same as in the adult. 

(d) Development of the Auditory Nerve and Sensory Areas of the 
Labyrinth. During the changes in the form of the labyrinth 
described in the preceding section, the lining epithelium has 
become thin and flattened except in eight restricted areas: viz., 
the three criste acusticw, one in each of the ampulle of the semi- 
circular canals, the macula utriculi, the macula saccult, the papilla 


Fia. 173. — Model of the auditory labyrinth of 
the right side of a chick embryo of 11 days 
and 17 hours; external view. (After Réthig 
and Brugsch.) Abbreviations as before. 


lagene, the papilla basilaris and the macula neglecta. Fach of 
these contains sensory cells ending in fine sensory hairs project- 
ing into the endolymph, or fluid of the labyrinth, and receives a 
branch of the auditory nerve proceeding from the acustie ganglia. 

Returning to an early stage to follow the development of sen- 
sory areas and nerves, we note first that the acustic ganglion from 
which the auditory nerve arises takes its origin from the acustico- 


296 THE DEVELOPMENT OF THE CHICK 


facialis ganglion which hes in front of and below the center 
of the auditory pit. During the closure of the latter, the acustic 
ganglion becomes fused with part of the wall of the otocyst in 
such a way that it becomes impossible to tell in ordinary sec- 
tions where the epithelial cells leave off and the ganglionic cells 
begin. This fused area may be called the auditory neuro-epi- 
thelium. At the 36 somite stage the neuro-epithelium is confined 
to the lower (ventral) fourth of the otocyst, covering the entire 
tip, the anterior face, and a small portion of the median face 
(cf. Fig 98). The neuro-epithelium is the source of all the sen- 
sory areas, which arise from it by growth and subdivision. The 
branching of the auditory nerve follows the subdivision of the 
neuro-epithelium. 

The exact manner in which the changes take place has not 
been made a subject of special investigation in the chick, so far 
as the author knows. However, it can be said in general that 
there is first a partial division of the neuro-epithelium into a 
pars superior and a pars inferior, and that the former divides 
into the criste acustice (sensory areas of the three ampullz) 
and the macula utriculi, while the latter furnishes the macula 
sacculi, papilla basilaris and papilla lagene. 

The sensory cells differentiate from the epithelium of the 
labyrinth, and the nerve fibers from the bipolar neuroblasts of 
the acustic ganglion, the peripheral process growing into the 
epithelium and branching between the sensory cells, while the 
central process grows into the brain. 

(e) Bony Labyrinth, Perilymph. etc. The loose mesenchyme 
that entirely surrounds the otocyst, differentiates in the course 
of development into the membrana propria and perilymphatie 
tissue of the membranous labyrinth, the perilymph and the bony 
labyrinth in the following manner; on the sixth day a single layer 
of mesenchyme cells in contact with the cells of the otocyst are 
arranged with their long axes parallel to the wall, and show 
already in places a slight fibrous differentiation. These gradually 
form the membrana propria, which appears on the eighth day 
as an extremely thin adherent layer with protruding nuclei at 
intervals. The mesenchyme external to this delicate layer is 
already differentiated on the sixth day into a_perilymphatic 
and a procartilaginous zone; in the former the mesenchyme is 
of loose consistency, and in the latter zone it has become dense 


ORGANS OF SPECIAL SENSE 297 


as a precursor to chondrification. The distinction between the 
perilymphatic and cartilaginous zones is most distinct (on the 
sixth day) on the median surface of the ductus cochlearis and 
lagena. The differentiation proceeds rapidly, however, and on 
the eighth day the entire membranous labyrinth is surrounded 
by a mass of embryonic cartilage, the foundation of the bony 
labyrinth, excepting around the endolymphatic duct (Fig. 168). 
Between the bony and membranous labyrinths is a thick layer 
of perilymphatic tissue composed of very loose-meshed mesen- 
chyme, which in the course of the subsequent development 
breaks down to form the perilymphatic space. Portions of the 
perilymphatic tissue, however, remain attached to the mem- 
branous labyrinth and form a support for its blood-vessels and 
nerves. 

The Development of the Tubo-tympanic Cavity, External 
Auditory Meatus and Tympanum. These structures develop 
directly or indirectly from the first or hyomandibular visceral 
cleft and the adjacent wall of the pharynx. In a_ preceding 
chapter the early development of this cleft was described; we 
saw that the pharyngeal pouch forms two connections with the 
ectoderm, a dorsal one corresponding to a pit-like depression of 
the ectoderm, and a ventral one corresponding to an ectodermal 
furrow. The latter connection is soon lost, the ectodermal fur- 
row slowly disappears, and the ventral portion of the pouch 
flattens out. In the dorsal connection, however, an opening is 
formed which closes on the fourth day, and the dorsal division 
of the pouch then frees itself from the ectoderm and expands 
dorsally and posteriorly until it les between the otocyst and the 
ectoderm, still preserving its connection with the pharynx (Fig. 
102). 

(a) The Tubo-tympanic Space. The dorsal portion of the 
first visceral pouch forms the lateral part of the tubo-tympanic 
space, but the greater portion of the latter is derived from the 
lateral wall of the pharynx itself, immediately adjacent to the 
entrance into the first visceral pouch; the region concerned 
extends from near the anterior edge of the second visceral pouch 
forwards, and ends a short distance in front of the first pouch. 
The original transverse diameter of the pharynx in this region 
increases in the course of development, and a frontal partition 
grows across the pharynx forming a dorsal median chamber into 


298 


which the two tubo-tympanic cavities open. 


THE DEVELOPMENT OF THE CHICK 


The median cham- 


ber communicates by a longitudinal slit (tubal fissure) in the 


Fig. 174. — A. Head of a chick embryo of 
4 days, halved by median section and 
viewed from the cut (After 
Moldenhauer.) 

B. Internal view of the pharynx of a 
pigeon embryo, corresponding in develop- 
ment to a chick of 10 days. (After Mol- 
denhauer. ) 

Col. 1., Colliculus lingualis. 
Colliculus palato-pharyngeus. 


surface. 


Col. p. p., 
Crea Crus 


inferior. Cr. s., Crus  superius.  Hyp., 
Hypophysis. Mx., Maxilla. N’ch., No- 
tochord. O. Ph. T., Ostium tubze phar- 


ynge. §. P., Seessell’s pocket. 2, 3, 4, 
Seeond, third, and fourth visceral arches. 


roof of the pharynx with the 
oral cavity (Figs. 168 and 
175). 

The frontal partition in 
question is a posterior pro- 
longation of the palatine 
processes of the maxillary 
arch, and forms as follows: 

If the head of a four-day 
chick be halved by a sagit- 
tal plane, and the interior 
of the pharynx and mouth 
‘avity be then viewed by 
reflected light, an elongated 
lobe will be seen on the me- 
dian surface of the mandib- 
ular arch and maxillary 
process (Fig. 174 A). This 
lobe begins far forward on 
the median surface of the 
maxillary process and may 
be followed posteriorly over 
the median surface of the 
mandibular arch to the first 
visceral pouch, where it 
ends with a free rounded 
extremity. The lobe itself 
is called by Moldenhauer 
the colliculus palato-phar- 
yngeus; it is bounded above 
and below by depressions, 
viz., the sulcus tubo-tym- 
the 
sulcus ventrally, 
both of which end behind 


panicus dorsally and 


lingualis 


in the first visceral pouch; 


anteriorly the ventral furrow disappears at the margin of the 


mouth, and the dorsal furrow near Seessel’s pocket. 


The maxil- 


ORGANS OF SPECIAL SENSE 299 


lary portion of the colliculus palato-pharyngeus corresponds to 
the palatine processes of mammals; the mandibular portion is 
peculiar to Sauropsida. 

If the interior of the pharynx and oral cavity of a ten-day 
chick be examined (Fig. 174 B), it will be found that the col- 
liculus has undergone important changes. Its maxillary or an- 
terior division divides in two limbs, crura superior and inferior, 
diverging anteriorly and separated by a depression which con- 
tinues the nasal cavity backward; its free posterior end extends 
farther backwards than before, and is more elevated. The 
bounding sulci are both deeper than before. The sulcus tubo- 
tympanicus, with which we are specially concerned, now extends 
on to the median surface of the hyoid arch. Subsequently, the 
crura superiores of the opposite side meet in the middle line and 
fuse together; in a similar fashion the posterior ends of the col- 
liculi fuse; thus the sulci tubo-tympanici open into a dorsal 
chamber common to both, which communicates with the ventral 
division of the pharynx by a slit remaining between the two 
fused areas. The crura inferiores also approach one another 
in the middle line but do not fuse, thus leaving the typical split 
palate of birds in front of the fused lower ends of the crura super- 
iores. In this way the typical adult condition of the bird’s 
palate is established. 

From this description it will be seen that only the most lateral 
portion of the tubo-tympanic cavity is directly derived from 
the first visceral pouch. In later stages it is quite impossible 
to say exactly what part, but it is quite certain that it lies within 
the tympanic part of the cavity. About the end of the fifth 
or the beginning of the sixth day the tubo-tympanic canal begins 
to enlarge distally to form the tympanic cavity proper (ef. Fig. 
168); the auditory ossicles (see chapter on skull) are beginning 
to form just above its dorsal extremity, and as the tympanic 
‘avity enlarges it expands around them, displacing the mesen- 
chyme, and finally meets above the auditory ossicles, so that 
these appear to he within it, though as a matter of fact the rela- 
tion is analogous to that of the entodermal alimentary tube to 
the body-cavity. The process of inclusion of the auditory ossicles 
is not, however, concluded until about the twelfth day. The 
blind end of the tympanic cavity attains a level dorsal to the 
external auditory meatus. (See below.) 


300 THE DEVELOPMENT OF THE CHICK 


During the seventh and eighth days the enlarging cartilaginous 
labyrinth presses down on the Eustachian tube and hinders its further 
enlargement. On the eighth day the tube is a wide but narrow slit 
which appears crescentic in a sagittal section of the head (Fig. 150). 

Some rather obscure details about the formation of the tubo-tym- 
panic canal are mentioned here as suggestions for further work on the 
subject. On the sixth day almost the entire roof is composed of flat- 
tened cells similar to the roof of the pharynx; the floor, however, is lined 
with a columnar epithelium which extends out to and surrounds the 
distal extremity; it seems probable that this terminal chamber lined 
on all sides by columnar epithelium represents the first visceral pouch 
proper. On the eighth day the cavity of this distal chamber is com- 
pletely constricted off from the main tympanic cavity, though it is still 
connected with the latter by a solid rod of cells, which gives unequivocal 
evidence of its origin. I do not know what becomes of this separated 
cavity later. (See Fig. 168 X.) 

(b) The Haternal Auditory Meatus and the Tympanum. We 
have already seen that on the ectodermal side there are originally 
two depressions corresponding to the first visceral pouch, viz., 
a dorsal round one in which a temporary perforation is formed, 
and an elongated ventral furrow. Between these is a bridge of 
tissue within which the external auditory meatus arises as a new 
depression, first clearly visible on the sixth day, when it is sur- 
rounded by four shg¢ht elevations, two on the mandibular and 
two on the hyoid arch. The meatus gradually becomes deeper 
and tubular, mainly owing, I think, to the elevation of the sur- 
rounding tissue, the bottom of the meatus, or tympanic plate, 
being held in position by the forming stapes. The meatus is 
directed in a general median direction with a slight slant dorsally 
and posteriorly, and the tympanic plate is placed obliquely, not 
opposite the lateral extremity of the tympanic cavity, but ven- 
trally to this (ef. Fig. 168). 

Even on the sixth day the position of the head of the stapes 
may be recognized by the density of the mesenchyme internal to 
the bottom of the meatus. During the seventh and eighth days 
the stapes becomes sharply differentiated, and the internal face 
of the tympanum is established in proportion as the tympanic 
cavity expands around the cartilage (cf. Fig. 168). Thus the 
tympanum is faced by ectoderm externally, by entoderm inter- 
nally, and includes an intermediate mass of mesenchyme, which 
differentiates by degrees into the proper tympanic substances. 


CHAPTER X 


THE ALIMENTARY TRACT AND ITS APPENDAGES 


Tue origin of the alimentary canal and of its various main 
divisions and appendages has been considered in preceding chap- 
ters. The subsequent history will now be taken up in the fol- 
lowing order: 

1. The mouth and oral cavity. 

2. The pharynx and its derivatives. 

3. The cesophagus, stomach and intestine. 

4. The liver and pancreas. 

5. The respiratory tract. 
The history of the yolk-sac and allantois was considered with the 
embryonic membranes (Chap. VII); the detailed history of the 
mesenteries will be taken up in connection with the body cavities 
(Chap. XI). 

I. MoutH AND ORAL Cavity 

The oral cavity may be defined embryologically as that part 
of the alimentary canal formed on the outer side of the oral plate. 
Anatomically, however, such a definition is unsatisfactory both 
because it is impossible to determine the exact location of the 
oral plate in late stages, and also because of the difference in 
extent of the ectodermal component in roof and floor of the 
mouth; the definitive mouth cavity includes part of the floor of 
the embryonic pharynx. It is, however, of interest to determine 
as nearly as possible the limits of the ectodermal component 
of the oral cavity. In the roof this is not difficult because the 
hypophysis, which arises just in front of the oral plate, retains 
its connection with the mouth cavity until definitive landmarks 
are formed. The median sagittal section of an eight-day chick 
(Fig. 148) shows that this point is situated almost immediately 
opposite to the glottis, that is, between the palatine and tubal 
fissures in the roof (ef. Fig. 175). In the floor the extent of 
the ectodermal component is much less. If the tongue is entirely 

301 


302 THE DEVELOPMENT OF THE CHICK 


a pharyngeal structure (in the embryological sense) the limit 
of the ectoderm would lie near the angle between the tongue 
and the floor of the mouth. In the side walls the boundary must 


be near the lines uniting the dorsal and ventral points as thus 


determined. 


Tongue 


Fig. 175. — Floor and roof of the mouth of the hen. The jaw muscles were 
cut through on one side, the lower jaw disarticulated and the entire floor 
drawn back. 

Corn. H., Cornu of the hyoid. Fis. pal., Palatine fissure. Fis. Tub., 

Tubal fissure. Mu., cut surface of Jaw muscles. 


We have already considered the formation of the boundaries 
of the mouth (Chap. VI and Chap. VII), and of the palate (Chap. 
IX, page 299). These data need not be repeated, so we have 
left to consider only the development of the beak, egg-tooth, 
tongue, and oral glands. 

Beak and Egg-tooth. The beak is a horny structure formed 
by cornification of the epidermal cells around the margins of 


ALIMENTARY TRACT AND ITS APPENDAGES 


303 


the mouth: the egg-tooth is a mammiform hard structure with 
pointed nipple (Figs. 176 and 177) situated on the dorsum of the 


upper jaw hear its tip (ef. Fig. 150). 
Its function is to aid in breaking 
the shell-membrane and the shell it- 
self at the time of hatching; shortly 
afterwards it is lost. It is, there- 
fore, an organ concerned with a sin- 
gle critical event in the life of the 
individual; nevertheless fully de- 
veloped like the instinct of its use, 
needed only for the same critical 
event. Though its structure is dif- 
ferent from that of the beak, it de- 
velops in connection with the latter, 
and the two will, therefore, be con- 


m2 


 ° nae | 


co 


» 


\ 


Lgr 


Fic. 176. — Outline of the up- 
per jaw of a chick embryo 
of 18 days’ incubation. (After 
Gardiner. ) 

EK. T., Ege tooth. 


ne rs 


L. gr., Lip 


sidered together. 


groove. 


The formation of the egg-tooth begins on the sixth day from 
an area situated in the middle line near the tip of the upper jaw, 
distinguishable in the living embryo by its opacity, which con- 


Fic. 177.— Transverse section through 
the upper jaw of a chick embryo of 
11 days. (After Gardiner.) 


EK. T., Egg tooth. H.Horn. L.gr., 
Lip groove. Pd., Periderm. T. R., 
Tooth ridge. 


the act of hatching. 


trasts with the translucency of 
the surrounding parts; in pro- 
file view, the area is seen to be 
shightly elevated. In sections 
the appearance is found to be 
due to an accumulation of 
rounded ectodermal cells lying 
between a superficial layer of 
periderm of several layers of 
cells, and the subjacent mucous 
layer of the epidermis (Tig. 
177)... Wathout their 
rounded shapes this mass of 
cells gradually the 
form of the egg-tooth by the 
fourteenth day. The overlying 
layer of periderm is lost during 


losing 


assumes 


During their differentiation the cells of the 


egg-tooth secrete an intercellular substance of horny consistency 


in which intercellular protoplasmic connections are found. 


The 


304 THE DEVELOPMENT OF THE CHICK 


protoplasm of the cell-bodies themselves becomes densely packed 
with granules, apparently also of a horny nature, and the boun- 
daries of the cells and outlines of the nuclei become indistinct. 

Reptiles with a horny egg-shell are provided with a true dentinal 
tooth on the premaxilla, which has the same function as the egg-tooth 
of birds and of those reptiles that have a calcareous shell (crocodiles, 
turtles, and Trachydosaurus). The latter is, however, as we have 
seen, a horny structure, and therefore not a tooth morphologically. 
Rose therefore proposes the term “ Eischwiele”’ for the horny tooth- 
like structure, to distinguish it sharply from the real egg-tooth. 

The formation of the upper beak begins in the neighborhood 
of the egg-tooth and spreads towards the tip and the angle of 
the mouth. Similarly, in the lower Jaw the differentiation begins 
near the tip. It is a true process of cornification, that takes 
place beneath the periderm and involves many layers of cells. 
It is therefore preceded by a rapid multiplication of cells of the 
mucous layer of the epidermis. Soon after the appearance of 
the horn a groove appears a little distance above and parallel to 
the margin of the upper beak, extending from the anterior end a 
short distance backwards (Fig. 176). In sections, this appears 
as an invagination of the epidermis; a similar but shallower 
invagination appears on the lower beak. In the upper beak the 
lips of the invagination fuse together and thus close the groove; 
in the lower beak the groove flattens out and disappears. These 
grooves correspond in many respects to the grooves that form 
the lips of other vertebrates, and they may be interpreted as a 
phylogenic reminiscence of lip-formation. 

Teeth. All existing species of birds are toothless, but some 
of the most ancient fossil birds possessed well-developed teeth; 
it is natural, therefore, to expect that rudiments of teeth might 
be found in the embryos of some existing birds. In the early 
part of the nineteenth century some observers interpreted papillie 
on the margin of the jaws of certain young birds as rudimen- 
tary teeth; these were, however, shown to be horny formations, 
and therefore not even remotely related to teeth. Gardiner was 
one of the first to call attention to a thickening of the ecto- 
derm forming a ridge projecting slightly into the mesenchyme, 
just inside the margin of the jaw of chick embryos about. six 
days old (Fig. 177). The ridge disappears shortly after cornifica- 
tion sets in. Gardiner discussed the possibility of this represent- 


ALIMENTARY TRACT AND ITS APPENDAGES 305 


ing a stage in tooth formation, and rejected the interpretation. 
Rose, however, has found the same ridge still better developed 
in embryos of the tern and ostrich, and identifies it very posi- 
tively with the tooth-ridge or first step in the formation of the 
enamel organ of other vertebrates. It seems probable that this 
is the case, and that in this ridge we have the very last stage 
of the disappearance of teeth. 

The Tongue. The tongue develops from two primordia in 
the floor of the embryonic pharynx, one situated in front of, and 
the other behind the thyroid diverticulum. The former, or 
tuberculum impar, becomes manifest on the fourth day as a 
slight rounded swelling situated between the lower ends of the 
first and second visceral arches. The swelling is bounded behind 
by a groove that has the ductus thyreoglossus for its center, and 
in front by a shallow groove, that represents the frenulum, on 
the posterior margin of the mandibular arches. The second 
primordium, or pars copularis, arises just behind the thyroid 
and includes the lower ends of the second visceral arches, a small 
part of the lower ends of the third, and the region between these 
arches. According to WKallius the tuberculum impar forms only 
the center of the fore part of the tongue, and the lateral parts 
arise from two folds that form right and left of it (lateral tongue- 
folds). The tuberculum impar thus expanded and the pars copu- 
laris constitute two very distinct components in the development 
of the tongue. 

Soon after the closure of the thyroid duct the two tongue 
components become confluent, but the zone of junction remains 
visible for a long time as a groove (ef. Fig. 148). Moreover 
the epithelium of the forward component soon becomes thick- 
ened and stratified, while in the pars copularis the epithelium 
remains thin and simple for a long time. With the elongation of 
the jaws the tip of the tongue grows forward above the frenulum 
(Fig. 148) and the shape of the entire organ conforms itself to 
the shape of the mouth cavity. 

Figure 175 shows the tongue of the adult fowl. ‘The anterior 
half is pointed and horny and is bounded from the posterior half 
by a double crescent whose posterior convexity is beset with horny 
spines. It seems probable that the anterior portion is derived 
from the precopular part, though this has not been demonstrated 
by continuous observation. Cornification of the precopular part 


306 THE DEVELOPMENT OF THE CHICK 


sets in about the eighth day, and the early thickening of the 
epithelium of this part already referred to is undoubtedly the 
first stage in the process. 

The development of the musculature of the tongue has not 
been followed. The development of the skeletal parts is con- 
sidered under the head of the skeleton. 

Oral Glands. The following oral glands occur in the hen: 
1, lingual glands; 2, mandibular glands; 3, glands opening at 
the angle of the mouth; 4, palatine glands in the neighborhood 
of the choanz. The only account of their development known 
to me is the brief one of Reichel. All the glands begin as solid 
ingrowths of the mucosa, which may branch more or less, and 
secondarily acquire a lumen. Their development begins relatively 
late. The mandibular glands appear first on the eighth day as 
a series of solid ingrowths of the mucosa extending on both sides 
of the base of the tongue forward to near the mandibular sym- 
physis. They are still mostly solid on the eleventh day, and 
very slightly branched, if at all. The lingual glands arise beneath 
the lateral margin of the tongue and grow up on each side of the 
lingual cartilage towards the upper surface where they branch 
out. They begin to form on the eleventh day. No glands form 
on the upper surface of the tongue. The glands of the angle of 
the mouth appear on the eleventh day, in situ, as slight epithelial 
ingrowths. Their further history has not been followed. An- 
terior and posterior palatine glands can be distinguished; the 
first in front of the choanz, the latter at the sides of and behind 
the choane. They begin to appear after the eleventh day. 


II. DrrRIVATIVES OF THE EMBRYONIC PHARYNX 

The pharynx, which is such an extensive and important region 
of the early embryo owing to the development of the visceral 
arches and clefts, becomes relatively much reduced in the process 
of development, though of course it becomes much larger abso- 
lutely. In the adult it is a somewhat ill-defined cavity from 
which the cesophagus leads away posteriorly, and which is con- 
fluent with the mouth anteriorly. The tubal fissure opens in 
its roof and the glottis in its floor. During the course of develop- 
ment, however, certain more or less persistent structures form 
from its walls, or from the epithelium of the pouches. Although 
these are relatively inconspicuous organs in the adult, they are of 


ALIMENTARY TRACT AND ITS APPENDAGES 307 


considerable morphological importance, being of very ancient 
origin and common to the whole series of vertebrates. They are 
the thyroid body or gland, the thymus, the postbranchial or 
suprapericardial bodies, and certain epithelial vestiges. 

Fate of the Visceral Clefts. The times of opening and closing 
of the visceral clefts have been already given (pp. 176 and 177). 
The later history of the first visceral pouch has been described 
(p. 297). The second, third, and fourth pouches retain their 
connections with the corresponding ectodermal grooves for a 
long time during the thickening of the visceral arches. The con- 
sequence is, that not only the pouches, but also the ectodermal 
furrows, are drawn out into long epithelial tubes, and the original 
closing plate is thus deeply invaginated. In the case of the 
second cleft the tube ruptures and begins to degenerate on the 
sixth day, leaving no remnants. In the case of the third and 
fourth clefts the ectodermal components become solid on the 
sixth day, and form strands (juniculi precervicales) connecting 
the entodermal pouches with the sinus cervicalis. These strands 
are subsequently broken through and disappear. Parts of the 
entodermal pouches, however, persist in the thymus, supraperi- 
cardial bodies and other epithelial remains. (See below.) 

Thyroid. The thyroid sac (median thyroid of authors) loses 
all connection with the pharyngeal epithelium on the fourth day, 
and on the seventh day it becomes divided in two massive lobes 
placed bilaterally (see Fig. 178). These then migrate backwards 
on each side of the trachea towards the hinder end of the deriva- 
tives of the third visceral pouch (Verdun) and become lodged 
in the junction of the subclavian and common carotid arteries, 
where they are found in the adult just internal to the jugular vein. 

The so-called lateral rudiments of the thyroid, or post branchial 
bodies, are histologically entirely different from the thyroid proper. 
They are described below. 

Visceral Pouches. The second visceral pouch leaves ino 
derivatives in the adult; during the fourth day, however, a con- 
siderable thickening of the epithelium appears on its dorsal and 
posterior aspect, near its Opening into the pharynx; though this 
disappears very soon, it may be considered to represent the 
thymus IT of Selachia and Anura. 

The third visceral pouch loses its connection with the pharynx 
by atrophy of its internal portion between the seventh and eighth 


308 THE DEVELOPMENT OF THE CHICK 


days, and its intermediate portion persists as an epithelial pocket 
on the ventral face of the jugular vein (Fig. 178). This pocket 
soon divides into dorsal and ventral moities of which the former 
develops into the chief part of the thymus (thymus III) and the 
latter into the so-called epithelial vestige III. (See below.) 

The fourth visceral pouch likewise separates from the pharynx 


on the seventh day, and furnishes from its dorsal portion the 
thymus IV, and from its ventral portion epithelial vestige IV. 
(See below.) 


Fria. 178. — The derivatives of the embryonic pharynx of the chick. (After 
Verdun from Maurer.) 


A. Of 7 days’ incubation. 

B. Of 8 days’ incubation. 

Ep. 3, Ep. 4, Epithelial bodies derived from the third and fourth visceral 
pouches. J., Jugular vein. p’br (V)., Postbranchial bodies derived from 
the fifth visceral pouch. Ph., Pharynx. Th. 38, Th. 4, Parts of the thymus 
derived from the third and fourth visceral pouches respectively. T’r., Thy- 
roid. III, [V, third and fourth visceral clefts. 


The fifth pouch (postbranchial body) likewise becomes iso- 
lated on the seventh day as a closed vesicle; its differentiation is 
considered below. 

The Thymus. According to the above, the thymus of the 
chick has a double origin on each side; the main portion (thymus 
III) is derived from the dorsal wall of the intermediate part of 
the third visceral pouch. This soon elongates to form an epi- 
thelial cord extending along the jugular vein; a smaller portion 
(thymus IV) of the thymus is derived from a corresponding part 
of the fourth visceral pouch, and fuses with thymus IIT (Fig. 178). 


ALIMENTARY TRACT AND ITS APPENDAGES 309 


In the young chick the thymus forms a voluminous tract of lobu- 
lated aspect, extending the entire length of the neck; later it 
atrophies and in old subjects one finds only traces of it. (Verdun.) 

Epithelial vestiges are formed from the ventral wall of the 
intermediate portions of the third and fourth visceral pouches; 
these come to lie together at the hinder end of the thymus in the 
base of the neck. They are found in the adult near the lower 
pole of the thyroid (Fig. 178). 

The postbranchial bodies have been called lateral rudiments 
of the thyroid; in their differentiation, however, they do not form 
thyroid tissue, but two main kinds of epithelial tissues similar 
to the tissues of the thymus and epithelial vestiges respectively. 
They are to be regarded, therefore, as a fifth pair of visceral 
pouches, for which there are other reasons, as we have seen before. 
The constituent elements, however, do not separate as in the case 
of the third and fourth visceral pouches, but form a rather ill- 
defined mass situated a short distance behind the thyroid (Fig. 
178). 

The epithelial derivatives of the embryonic pharynx in the 
chick are, therefore; 1. thyroid; 2. thymus (from III, IV); 
3. epithelial vestiges (from III, IV); 4. postbranchial bodies, 
including thymus V and epithelial vestiges V. The thyroid 
develops in essentially the same manner in all vertebrates. In 
the case of the thymus it may be said in general that more visceral 
pouches are concerned in the lower than in the higher vertebrates. 


Ill. THe Csopuaaus, STOMACH AND INTESTINE 


During the third and fourth days a very pronounced lateral 
curvature of the alimentary canal develops, the convexity being 
turned to the left and the concavity therefore to the right. The 
part involved extends from the posterior portion of the cesopha- 
gus to the end of the duodenum. As the duodenum is at first 
very short, the stomach is the part principally affected at the 
start. The depth of the mesogastrium (dorsal mesentery of 
the stomach) is considerably increased by the displacement; in the 
region of the greatest curvature it descends directly in the middle 
line, then bends sharply to the left and is attached to the dorsal 
wall of the stomach; the accessory mesentery arises at the bend. 
(See Chap. XI.) The stomach does not rotate on its long axis so 
as to carry the attachment of the mesogastrium to the extreme 


310 THE DEVELOPMENT OF THE CHICK 


left, as in mammals; in the chick the lateral bending of the 
stomach appears to be uncomplicated by any such rotation. The 
curvature leaves a large space within it to the right containing 
the meatus venosus and liver, in short, the entire median mass 
of the septum transversum. 

The main divisions of the intestine are marked out by their 
position, size-relations and structure before the closure of the 
yolk-stalk; thus on the third day the cesophagus appears as a 
constricted portion immediately behind the pharynx, and the 
stomach as a spindle-shaped enlargement behind the cesophagus; 
the duodenum is indicated at the same time by the hepatic and 


Fic. 179. — Viscera of a chick embryo of 6 


days, seen from the right side. (After 
Duval.) 


All., Allantois. Au. r., Right auricle. 
B.a., Bulbus arteriosus. ¢. pr., Ceeeal pro- 
cesses. D. L., Loop of the duodenum. Giz., 
Gizzard. Lg. r:, Right lung. Li., Liver. 
R., Reetum. t. R., Tubal ridge. V., Ven- 
tricle. W.B., Wolffian body. Y.St., Yolk 
stalk. X., Duodeno-jejunal flexure. 


pancreatic outgrowths. The form of the intestine on the sixth 
day is illustrated in Figure 179. Behind the stomach, the intes- 
tine forms two loops descending ventrally. The first or duodenal 
loop is relatively slightly developed at this time, and forms an 
open curve Just beneath the right lobe of the liver. Its ascend- 
ing limb rises to a high dorsal position just behind the liver, and 


ALIMENTARY TRACT AND ITS APPENDAGES oll 


bends sharply to enter the descending limb of the second loop. 
This bend or duodeno-jejunal flexure (X, Fig. 179) is a relatively 
fixed point in the growth of the intestine, and marks the bound- 
ary between the duodenum and succeeding parts of the small 
intestine. The second loop descends deep into the umbilical 
cord, and the yolk-stalk is attached to its lowermost portion. 
A bilateral swelling at the upper end of its ascending limb is the 
primordium of the cecal processes, and marks the anterior end of 
the large intestine, which passes in a slight curve to the cloaca. 

In the subsequent growth of the intestine the fixed point 
referred to above at the hinder end of the duodenum is held in its 
place, and the duodenal loop in front of it simply becomes longer 


Fic. 180. — Viscera of a chick embryo of 17 days’ 
incubation from the right side. (After Duval.) 


Am., Attachment of amnion to umbilical stalk. 
Li. r.,]., Right and left lobes of the liver. Pe., Pan- 
creas. U.St., Umbilical stalk. Other abbreviations 
same as Fig. 179. 


without forming secondary convolutions; the pancreas comes to 
lie in this loop. The second loop, on the other hand, forms 
numerous secondary convolutions (Fig. 180) which lie at first in 
the umbilical cord, but which are gradually retracted (seven- 
teenth to eighteenth day) into the abdominal cavity. 

The two intestinal ceca begin to grow out as finger-shaped 
processes from the swelling already referred to, about the seventh 
day, and rapidly attain considerable length. The large intestine 
elongates only about in proportion to the growth of the entire 
embryo. 

Having thus noted the general gross anatomy of the embry- 


312 THE DEVELOPMENT OF THE CHICK 


onic intestine, we may next note a few details concerning some 
of its divisions. The history of the mesenteries is considered in 
Chapter XI). 

(Esophagus. Owing to the rapid elongation of the neck the 
cesophagus quickly becomes a long tube. On the sixth day its 
lumen becomes very narrow, and on the seventh day completely 
occluded immediately behind the glottis, owing to proliferation 
of the lining cells. On the eighth day the occluded portion 


Fig. 181. — Photograph of a transverse section through the cesopha- 
gus and trachea of an 8-day chick. 
Cop. H., Copula of the hyoid. Qés., Gisophagus. Tr., Trachea. 
Ven. jug., Jugular vein. 


extends only a short distance behind the glottis: it is com- 
pressed dorso-ventrally and extended laterally throughout the 
occluded region (Fig. 181). On the eleventh day it is open again 
along its entire length. The crop arises as a spindle-shaped dila- 
tation of the cesophagus at the base of the neck; on the eighth 
day it is about double the diameter of the parts immediately 


ALIMENTARY TRACT AND ITS APPENDAGES 313 


in front of and behind it (Fig. 150). No detailed account of its 
development exists. 

Stomach. It is well known that the stomach of birds exhibits 
two successive divisions, the proventriculus and the gizzard, 
the former of which has a digestive function and is richly pro- 
vided with glands, while the latter has a purely mechanical fune- 
tion, being provided with thick muscular walls, within which is 
the compressed cavity lined on each side by tendinous plates. 

On the third day of incubation, the divisions of the stomach 
are not recognizable, either by the form of the entire organ or by 
the structure of the walls. On the fifth day, however, the first 
indications of the formation of the compound glands of the 
proventriculus may be seen in the cardiac end; the posterior or 
pyloric end occupies the extreme left of the gastric curve and 
forms the rudiment of a blind pouch projecting posteriorly, that 
develops into the gizzard. On the sixth and seventh days this 
pouch expands farther in the same direction (ef. Fig. 179), and a 
constriction forms between the anterior portion of the stomach, 
or proventriculus, and the gizzard, as thus marked out. The 
gizzard grows out farther, to the left and posteriorly, at the same 
time undergoing a dorso-ventral flattening, owing to the forma- 
tion of the large muscle-masses. According to this account, 
therefore, the greater curvature of the gizzard would represent 
the original left side of the portion of the embryonic stomach 
from which it is derived, and the original right side would be 
represented by the lesser curvature. 

The large compound glands of the proventriculus are indi- 
cated on the fifth or sixth days as slight depressions of the ento- 
derm towards the mesenchyme; on the seventh day these become 
converted into saccular glands with narrow necks (Fig. 182). 
Each sacculus becomes multilobed about the twelfth or thirteenth 
days, and each lobulus includes a small number of culs-de-sac, 
lined with a simple epithelium. The last subsequently become 
tubular, and the original sacculus then represents the common 
duct of a large compound gland. (See Cazin.) 

The simple, tubular glands of the gizzard begin to form about 
the thirteenth or fourteenth day, and the lining of the gizzard 
is simply the hardened secretion of these glands; it is thus essen- 
tially different from cuticular and corneous structures of the sur- 
face of the body. According to Cazin, the glands of the gizzard 


314 THE DEVELOPMENT OF THE CHICK 


are formed as folds and culs-de-sac excavated in the thickness of 
the original epithelial wall, by elevations of the subjacent con- 
nective tissue. It should be noted finally, that from the eighth 
day on, the surface of the mucosa, both in the proventriculus and 
in the gizzard, is covered with a thick layer of secretion; subse- 
quently replaced in the gizzard by the corneous lining. 


Fic. 182. — Photograph of a transverse section of an 8-day chick through 
the region of the proventriculus and tip of the heart. 


A. coel., Coeliac artery. A. o.m., Omphalomesenteric artery. Cav. om., 
Cavum omenti. Cav. pe., Pericardial cavity. Coel., Coelome. Gon., Gonad. 
Lig. g-h., Gastro-hepatie ligament. M.D., Miillerian duct. Mtn., Metaneph- 
ros. p’e., Membranous pericardium. Pr’v., Proventriculus. S’r., Supra- 
renal. V.c.i., Vena cava inferior. Ven., Ventricle of heart. V. h. 1., Left 
hepatic vein. V. s’e., Subeardinal vein. V. umb., Umbilical vein. 


Large Intestine, Cloaca, and Anus. The cloaca of the adult 
is a large chamber opening to the exterior by the anus; it consists 
of three divisions: the proctodseum or terminal chamber is capable 
of being closed by the sphincter muscle, the bursa Fabricii opens 
into its dorsal wall, and it is separated by a strong circular fold 


ALIMENTARY TRACT AND ITS APPENDAGES 315 


from the intermediate section of the cloaca or urodseum: this is 
a relatively short division of the cloaca which receives the renal 
and reproductive ducts in its dorsal wall by two pairs of openings: 
it is bounded from the larger anterior division, coprodeum, by 
a rather low circular fold; the coprodzeum passes gradually, with- 
out a sharp line of division, into the rectum. 

The early embryological history of these parts has been con- 
sidered in the preceding chapters. The condition on the fourth 
day is shown in the accompanying figure (Fig. 183) representing a 


mates QUSSLECLIZER Esse ese 
qmat elittiegs 


we tes eth Gir 
rs TT 7 
Re LE enEs S 
SS Ss one Oa 


Fig. 183. — Median sagittal section of the hind end of a chick embryo 
on the fourth day of incubation. (After Gasser from Maurer.) 


All., Allantois. Am., Tail fold of amnion. el. M., Cloacal mem- 
brane. Cl.,Cloaca. N’ch., Notochord. n. T., Neural tube. R., Rec- 
tum. Y.S., Wall of yolk-sac. 


sagittal section of the hind end of the embryo. The cloaca is the 
large terminal cavity of the intestine, closed from the exterior 
by the cloacal membrane, in which the entoderm of the floor of 
the cloaca is fused to the superficial ectoderm at the base of the 
tail. The line of fusion is a long, narrow median strip, extending 
from just below the neck of the allantois to the hinder end of the 
cloaca. Leading out from the cloaca ventrally, in front of the 


316 THE DEVELOPMENT OF THE CHICK 


cloacal membrane, is the neck of the allantois, and dorsal to this, 
the large intestine. Though not shown in the figure, it may be 
noted that the Wolffian ducts open into the cloaca behind and 
dorsal to the opening of the rectum. 

The appearance of the cloaca in a longitudinal section does 
not, however, give an adequate idea of its form. The anterior 
portion of the cloaca which receives the rectum, stalk of the 
allantois and Wolffian ducts is expanded considerably in the 
lateral plane, and thus possesses a large cavity. The posterior 


2 
Bireo 
aed S009. 905% 


PLT R 
Hg teary SAS to 
fabar 


s 
RS 6 070: 
ey rete 
artact oh Shadi, 


Fig. 184. — Frontal section through the region of the 
cloaca of a 54-day chick embryo. 
an. F., Anal fold. B. F., Bursa Fabrici. Cl., Cloaca. 
Coel., Coelome. Reet., Rectum. W. D., Wolffian duct. 
X., Posterior angle of the body-cavity; the epithelium 
is invaginated and folded so as to simulate a glandular 
structure. 


portion, on the other hand, is greatly compressed laterally and 
the cavity is extremely narrow. During the fifth day the walls 
of this part of the cloaca become actually fused together, and 
its cavity obliterated, or rendered virtual only (Fig. 184). Thus 
the anterior part of the cloaca is prolonged backwards by 


ALIMENTARY TRACT AND ITS APPENDAGES 317 


median plate which is continuous ventrally with the cloacal mem- 
brane. 

This plate was interpreted by all the earlier observers (up to Wenck- 
ebach) as the hypertrophied cloacal membrane. It is, however, not 
difficult to demonstrate in good series of sections, that this is not the 
‘ase; the cloacal membrane forms only a small part of this plate, and 
its ectodermal component is thin. 

During the fifth and sixth days, vacuoles appear in the pos- 
terior and dorsal part of the fused portion of the cloaca, and 
these soon run together in the uppermost part, but remain as a 
chain of vacuoles ventrally (Fig. 184). The vacuolated portion 
is the primordium of the bursa Fabricii and its duct. Its cavity, 
which is extremely narrow and ill-defined at this time, may be 
regarded as a re-establishment of the cavity of the posterior 
division of the embryonic cloaca; its communication with the 
anterior portion of the cloacal cavity is soon closed. 

At this stage the lining epithelium of the rectum is much 
thickened, and the lumen has therefore become narrow (Fig. 184). 

During the seventh day the conditions change very rapidly 
and on the eighth day the relations are as shown in Figure 185. 
The anterior portion of the original cloaca, or urodzeum, has 
become compressed in an antero-posterior direction; the allantois 
leads off from it anteriorly and ventrally, and the rectum with 
its cavity now obliterated is attached to its anterior face; the dor- 
sal extension, above the rectum (see Fig. 185), is related to the 
urinogenital ducts. The bursa Fabricii has now a well-defined 
cavity that no longer communicates with the urodeum. The 
tissues surrounding the cloacal membrane have grown out to 
form a large perianal papilla, and the cloacal membrane is 
therefore invaginated; its direction also is so altered that the 
invaginated cavity or proctodzeum now hes behind it; the bursa 
‘abricii is on the point of opening into the highest point of the 
proctodeum. Vacuolization of the tissue between the cloacal 
membrane and the urodzum indicates its subsequent dis- 
appearance. 

At eleven days (Fig. 186) the general arrangement is essen- 
tially the same, but there are important differences in detail. 
The bursa Fabricii has now become a long-stalked sac, opening 
into the proctodeum at the level of the urodzal membrane. 
The latter is still quite a thick plate, but the vacuoles in it fore- 


318 THE DEVELOPMENT OF THE CHICK 


shadow its final rupture. The lower end of the large intestine 
is perfectly solid, and higher up, somewhat vacuolated. (The 
solid stage begins on the seventh day.) The urinogenital ducts 
open into the urodzum above the solid end of the large intestine. 
It will be seen, therefore, that the urodzum is transformed into 
a passageway between the urinogenital ducts and the allantois, 
being closed anteriorly by the solid large intestine and posteriorly 
by the urodieal (cloacal) membrane. 


Fig. 185. — Photograph of the region of the cloaca in a median sagittal 
5 5 5D 
section of an 8-day chick. 
All., Allantois. An., Anus. B. F., Bursa Fabricii. caud. A., Caudal 
artery. Int., Intestine. N’ch., Notochord. p. P., Perianal papilla. Rect., 
Rectum. Ur’d., Urodzeum. 


During the twelfth and thirteenth days, the vacuoles in the 
upper part of the large intestine flow together and re-establish 
the cavity, but the lower end still remains closed by a solid plug 
of cells; immediately anterior to the latter the large intestine is 
dilated, and this apparently corresponds to the coprodzeum of 


ALIMENTARY TRACT AND ITS APPENDAGES 319 


the adult cloaca. Even on the seventeenth day the large intes- 
tine appears to be still closed at its lower end, and the urodeal 
membrane still persists as a plug of vacuolated cells. (Gasser.) 
Both plugs must, however, disappear soon after. 

It would thus appear that the urodzeum only of the adult 
cloaca corresponds to the embryonic cloaca; the proctodzeum is 
certainly derived from an ectodermal pit, and it is probable that 


Fia. 186. — Chick embryo of 11 days, sagittal section 
through the region of the cloaca. Reconstructed from 
several sections. (After Minot.) 


All’., Ascending limb of the allantois. AIl”., Descend- 
ing limb of the allantois. An., Analinvagination. An. pl., 
Urodeal membrane. Art., Umbilical artery. B. F., 
Bursa Fabricii. b. f., Duct of the bursa. Clo., Cloaeca. 
Ee., Ectoderm. Ent., Entoderm of the rectum.  Ly., 
Nodules of crowded cells, probably primordia of lym- 
phoid structures in the wall of the large intestine. W. D., 
Wolffian duct. 


the coprodeum represents the enlarged lower extremity of the 
embryonic large intestine. The bursa Fabricii is an entodermal 
structure derived from the posterior portion of the embryonic 
cloaca. 


IV. Tuer DEVELOPMENT OF THE LIVER AND PANCREAS 
The Liver. The anterior and posterior liver diverticula, de- 
scribed in Chapter VI, constitute the rudiments from which the 


320 THE DEVELOPMENT OF THE CHICK 


substance of the liver is derived. <A third diverticulum is dis- 
tinguished by Brouha as the right posterior diverticulum; this is 
an early outgrowth of the posterior diverticulum. Hepatic cylin- 
ders arise from both primary diverticula at an early stage, and 
these, branching and anastomosing, soon form a basket-work of 
liver tissue around the intermediate portion of the meatus venosus. 
The anterior diverticulum alone extends forward to the anterior 


Fia. 187. — Reconstruction of gizzard, duodenum, 
and hepato-pancreatie ducts of a chick embryo 
of 124 hours. (After Brouha.) 


D.ch., Ductus choledochus. D. ey., Ductus cys- 
ticus. D.h.ey., Ductus hepato-eysticus. D-h.d., 
Dorsal or hepato-enteric duct. Du., Duodenum. 
G. bl., Gall bladder. Giz., Gizzard. Pa. d., Dor- 
sal pancreas. Pa. v. d., Right ventral pancreas. 
Pa. v. s., Left ventral pancreas. 


end of the meatus, and it even encroaches on the sinus venosus, as 
we have already seen; in the posterior part of the meatus venosus, 
on the other hand, the liver tissue is derived entirely from the 
posterior diverticulum. The mesenchyme in the interstices of 
the hepatic framework is replaced almost immediately by blood- 


ALIMENTARY TRACT AND ITS APPENDAGES 321 


vessels that empty into the meatus, and thus appear as branches 
of the latter. 

The gall-bladder is a very early formation, arising from the 
hindermost portion of the posterior hepatic diverticulum, as a 
distinct bud about the stage of 68 hours (Fig. 103), and forming 
a pyriform appendage at 84 hours. It may reasonably be re- 
garded as derived from the most posterior portion of the prim- 
itive hepatic gutter, an interpretation that agrees with the 
condition found in more primitive vertebrates. 

At the stage of 68 hours (cf. Fig. 103B), the anterior and 
posterior diverticula proceed from a common depression of the 
ventral wall of the duodenum, the ductus choledochus. By 
means of an antero-posterior constriction, the latter becomes 
much more clearly defined as development proceeds (Fig. 187); 
there arise from it also the right and left ventral primordia of 
the pancreas (see below), so that it receives at this stage four 
main ducts, viz.: the right and left ventral pancreatic diverticula 
and the cephalic and caudal hepatic diverticula. On the sixth 
day these four ducts obtain independent openings into the duo- 
denum and the common bile duct thus ceases to exist. The 
relations thus established are practically the same as in the 
adult. 

As the caudal hepatic diverticulum grows out it carries the 
attachment of the gall-bladder with it, so that the latter is then 
attached to the caudal diverticulum, which is thus divided in 
two parts, a distal or ductus hepato-cysticus, and a proximal or 
ductus cystico-entericus. That portion of the liver arising from 
the cephalic diverticulum is thus without any connection with 
the gall-bladder. There seem, however, to be anastomoses 
between the ductus hepato-cysticus and the original cephalic 
duct (ductus hepato-entericus) in the adult, lying in the com- 
missure of the liver; the embryological origin of these appears, 
however, to be unknown. In the course of the development, 
the openings of the two original ducts into the duodenum come 
to lie side by side instead of one behind the other, and the original 
cephalic duct (ductus hepato-entericus) appears to be derived 
maimy from the left lobe, and the ductus cystico-entericus mainly 
from the right lobe of the liver. The actual distribution is, how- 
ever, by no means so simple; the mode of development of the 
lobes of the liver (see below) would explain a preponderant dis- 


322 THE DEVELOPMENT OF THE CHICK 


tribution of the cephalic duct to the left, and the caudal duct to 
the right lobe. 

The liver is primarily an unpaired median organ. Its division 
into right and left lobes is therefore secondary and has no funda- 
mental embryological significance. The factors that determine 
its definitive external form are the following: (a) the relative 
power of growth of its various parts; (b) limitation of its exten- 
sion to the septum transversum and its connections; (¢) the limi- 
tations of space in the eccelome. 

Bearing these principles in mind, the growth of the liver 
may be described as follows: three primary divisions succeed- 
ing one another in a cranio-caudal direction, may be distinguished 
at an early stage, viz., an antero-dorsal division, abutting on the 
postero-dorsal part of the sinus venosus, formed by the anterior 
end of the cephalic hepatic diverticulum; an intermediate division, 
surrounding the meatus venosus in which both cephalic and 
caudal hepatic diverticula are concerned; and a postero-ventral 
division, beneath the posterior end of the meatus venosus and the 
right omphalomesenteric vein, formed exclusively by the caudal 
diverticulum. 

The growth of the liver causes expansion of the median mass 
of the septum transversum in all directions, excepting anteriorly, 
and the substance of the liver extends more or less into all the 
connections of the latter, viz., the lateral mesocardia, the lateral 
closing plates associated with the umbilical veins, the primary 
ventral ligament, the mesentery of the vena cava, the gastro- 
hepatic ligament, and that part of the hepatic portal vein formed 
by the right omphalomesenteri¢ vein. 

At the stage of 96 hours the anterior division spreads 
out in the lateral mesocardia behind the Cuvierian ducts nearly 
to the lateral body-wall on each side. The intermediate division, 
on the other hand, lies largely on the right side of the middle 
line, owing to the displacement of the stomach to the left and the 
meatus venosus to the right. A small lobe is, however, pushing 
itself to the left beneath the gastro-hepatic ligament. The pos- 
terior division lies entirely on the right ventral side of the hinder 
end of the meatus venosus and right omphalomesenteric vein, 
as far back as the dorsal anastomosis. There are, of course, 
no sharp lines of demarcation between the divisions, so that in 
general it may be said that the liver substance tends more and 


ALIMENTARY TRACT AND ITS APPENDAGES 323 


more to the right side of the body from its fairly symmetrical 
anterior end backwards. 

The lines of development of the liver are thus marked out. 
On the sixth day the anterior division is larger on the left than 
on the right side, owing no doubt to the incorporation of the sinus 
venosus into the right auricle, thus leaving more room for the 
liver on the left side. Passing backwards in a series of sections 
to the region of the center of the meatus venosus, we find the liver 
larger on the right than on the left side, being centered around 
the meatus, but a small lobe extends over to the left side ventral 
to the stomach. The posterior division, again, is confined to 
the right side and ends in a free right lobe projecting caudally to 
the region of the umbilicus. The division of the liver into right 
and left lobes thus takes place on each side of its primary median 
ligaments, dorsal or gastrohepatic, and primary ventral; expan- 
sion being inhibited in the median line by the stomach above and 
heart below, it takes place on both sides, but particularly on the 
right side where there is more space. 

The reader is referred to Chapter XI for description of the 
origin of the ligaments of the liver and the relations of the liver 
to the pericardium and other structures; also to Chapter XII for 
description of its blood-vessels. 

The histogenesis of the liver should be finally referred to. 
This organ is remarkable in possessing no mesenchyme in the 
embryonic stages (Minot, 1900); but from the start the hepatic 
cylinders are directly clothed with the endothelium of the blood- 
vessels, so that only the thickness of the endothelial wall separates 
the hepatic cells from the blood in the sinusoids. The hepatic 
cylinders have been described as arising in the form of solid buds 
from the primary diverticula; the buds first formed branch 
repeatedly, forming solid buds of the second, third, ete., orders, 
and wherever buds come in contact they unite, forming thus a 
network of solid cylinders of hepatic cells. The solid stage does 
not, however, last very long, for on the fifth day it can be seen 
that many of them have developed a small central lumen by dis- 
placement of the cells. Thus there gradually arises a network 
of thick-walled tubes instead of solid cylinders, and the whole 
system opens into the primary diverticula from which it arose. 

The Pancreas. The pancreas arises as three distinct entodermal 
diverticula, the origin of which has been already described, and 


324 THE DEVELOPMENT OF THE CHICK 


has correspondingly in the adult three separate ducts opening 
into the duodenum. (Two pancreatic ducts is the rule in Gallus, 
according to Gadow in Bronn’s Thierreich.) Of the three pan- 
creatic diverticula, the dorsal one arises first (about 72 hours) 
then the right ventral slightly earlier than the left ventral 
(about 96 hours). The two latter arise from the common 


£2 g 

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Fic. 188. — Transverse section through the duodenum and hepato- 

pancreatic ducts of a chick embryo of 5 days. (After Choronschitzky.) 

Ao., Aorta. cav. F., Caval fold. Coel., Coelome. D. hep. 2, 2a, 
2b, Posterior hepatic diverticulum and branches of same. Du., Du- 
odenum. Li., Substance of liver. M/’st., Dorsal mesentery. Pa. d., 
Dorsal pancreas. Pa. v. d., Right ventral pancreas. Pa. v. s., Left 
ventral pancreas. Spl., Spleen. V. e. p., Posteardinal vein.  V. I.., 
Vena lienalis. V.o.m.d., Right omphalomesenteric vein. V.o.m.s., 
Left omphalomesenteric vein. 


hepatie diverticulum near its Junction with the duodenum (Fig. 
ISS). The differentiation of the three parts is essentially similar, 
and proceeds naturally in the order of their origin. Solid buds 
arise from the ends of the diverticula, and these branch repeatedly 
in the surrounding mesenchyme, but do not anastomose; the 


ALIMENTARY TRACT AND ITS APPENDAGES 320 


final terminations of the buds form the secreting and the inter- 
mediate portions the various intercalated and excretory ducts 
that form a branching system opening into the main ducts. 

The successive stages in the development of the pancreas 
may be stated thus (following Brouha): At 124 hours the two 
ventral pancreatic ducts pass anteriorly and a little to the left, 
crossing the cephalic hepatic duct which les between them. 
They are continued into ramified pancreatic tubes which already 
form two considerable glandular masses. The right ventral 
pancreas is united by a very narrow bridge to the dorsal pancreas, 
and the latter is moulded on the left wall of the portal vein, 
while its excretory duct has shifted on the left side of the duo- 
denum nearer the ductus choledochus. At 154 hours the duct. of 
the dorsal pancreas is still nearer to the others, and the three pan- 
creatic ducts enter a single glandular mass, the dorsal portion of 
which, derived from the primitive dorsal pancreas, is moulded on 
the left wall of the portal vein, and is continued into a smaller ven- 
tral portion formed by the fusion of the two ventral pancreases. 

Subsequently, the pancreatic lobes fill up the duodenal loop 
(Figs. 179 and 180), and elongate with this so as to extend from 
one end of it to the other in the adult; the three ducts open 
near the termination of the duodenum (end of distal limb) 
beside the two bile ducts. 


V. Tue Resprratory TRAcT 

The origin of the laryngotracheal groove and the paired 
primordia of the lungs was described in Chapter VI. At the stage 
of 36 somites the laryngotracheal groove includes the ventral 
division of the postbranchial portion of the pharynx, which is 
much contracted laterally so as to convert its cavity into a deep 
and narrow groove. This communicates posteriorly with right 
and left finger-shaped entodermal diverticula (the entodermal 
lung-primordia) extending into the base of the massive pear- 
shaped mesodermal lung-primordia attached to the lateral walls 
of the cesophagus. The mesodermal lung-primordia are con- 
tinuous with the accessory mesenteries,as described in Chapter XI; 
and by them attached to the septum transversum. 

Bronchi, Lungs and Air-sacs. The primitive entodermal 
tubes form the primary bronchi, in which two divisions may be 
distinguished on each side, viz: a part leading from the end of 


326 THE DEVELOPMENT OF THE CHICK 


the trachea to the hilum of the lung (extra-pulmonary bronchus) 
and its continuation within the lung, extending its entire length 
(mesobronchus). The secondary air passages and chambers 
of the lung (ecto- and entobronchi, parabronchi, canaliculi and 
terminal alveoli) and the air-sacs arise from the mesobronchi 
by a process of budding and branching and enlargement of ter- 
minal twigs. The mesobronchi are surrounded from the first 
by a thick mass of mesenchyme, covered of course towards the 
body cavity by a layer of mesothelium. In the early develop- 
ment the mesenchyme of the lung-primordia expands so rapidly 
as to provide adequate space for the branching of the mesobronchi 
entirely within the mesenchymal tissue. 

Although the development of the lungs of the chick has been 
studied by several investigators (Rathke, Goette, Selenka, Ber- 
telli) there has been no complete study made with the resources 
of modern technique, and our knowledge is therefore defective 
in many important respects. 

We may note the general topographical development as 
follows: The expansion of the lungs takes place into the pleural 
cavities; they therefore raise themselves from their surfaces of 
attachment, oesophagus and pleuroperitoneal membrane, and 
project in all directions, but especially dorsally and anteriorly 
(Fig. 189). We may thus distinguish free and attached surfaces; 
the latter is nearly a plane surface and on the whole ventral in 
position, and the free arched surfaces are dorsal. However, it 
should be remembered that the pleuroperitoneal membrane 
which forms the attached surface, lies at first in a sagittal plane, 
and only secondarily becomes frontal. In successive stages, the 
attached surface of the lung (pleuroperitoneal membrane) 
rotates from a sagittal to an approximately frontal plane (Chap. 
XI). An anterior lung lobe grows out in front and dorsal to the 
mesobronchus, beginning at six days, and the extra-pulmonary 
bronchus thus acquires a ventral insertion into the lung. 

Stages in the development may be described as follows: 
At 96 hours, the bronchi arise from the end of the trachea, ven- 
tral to the cesophagus and pass back on either side of the latter, 
describing near their centers a rather sharp curve that brings 
the dorsal ends to a higher level than the cesophagus. A very 
slight dilatation at the extreme end of the mesobronchus is usually 
interpreted as the beginning of the abdominal air-sac. 


ALIMENTARY TRACT AND ITS APPENDAGES 327 


At six days the mesobronchus within the lung describes a 
course nearly parallel to the cesophagus as far as the middle of 
the lung; in this part of its course it les near the median sur- 
face and ascends very slightly. About the middle of the lung 
it makes a sharp bend, almost at right angles, and passes 
towards the lateral and dorsal surface of the lung; here it enters 


a considerable thin-walled dilatation from which it is con- 


Fig. 189. — Photograph of transverse section through the lungs of an 8-day 
chick embryo. 

A. A. d., Right aortie (systemic) arch. D. art. d.,s., Right and left ductus 
arteriosi. Ent’b.1., Branches of first entobronchus. M. pl. pe., Pleurope- 
ricardial membrane. Mes’b. d., s., Right and left mesobronchia. (Es., 
(Esophagus. Pc., Pericardial cavity. pl. Cav., Pleural cavity. Rec. p. e.s., 
Left pneumato-enteric recess. V.c. a., Anterior ven cave. 


tinued straight backwards by means of a second curve, and 
ends in the same slight thick-walled dilatation that we noted 
on the fourth day. There are thus three very distinct divisions 
of the mesobronchus which we may name the anterior (or ven- 
tral) the middle (or ascending) and the posterior (or dorsal). 
Three evaginations arise from the dorsal wall of the anterior 


328 THE DEVELOPMENT OF THE CHICK 


division of the mesobronchus, which is otherwise unbranched. 
These represent the three anterior entobronchi; the first or 
anterior one is the largest, and the third or posterior the smallest. 
Their direction of growth is, on the whole, dorsal, with an inclina- 
tion anteriorly and towards the middle line. It is evident that 
the part of the mesobronchus from which they arise will form 
the vestibulum of the adult lung. 

On the eighth day the fourth entobronchus is formed, 
extending posteriorly from the hind end of the vestibulum in the 
ventral wall of the lung; it gives off a couple of latero-ventral 
small branches. The first entobronchus is now much subdivided 
in the anterior lobe of the lung, and two of its terminal twigs, 
one in the antero-dorsal, the other in the antero-ventral tip of 
the lung, are slightly dilated and project as primordia of the 
cervical and interclavicular air-sacs respectively. The second 
entobronchus is also subdivided several times; its terminal 
branches extending to the dorsal surface of the lung. The third 
entobronchus similarly branches dorsally and posteriorly, and 
from its base a narrow canal extends into the pleuroperitoneal 
membrane, where it expands into the anterior thoracic air-sac, 
which is much the largest of the air-sacs at this time. 

Behind the vestibulum, the mesobronchus ascends towards 
the dorsal surface of the lung, remaining unbranched, then turns 
posteriorly and gives off five or six branches, presumably the 
ectobronchi. — It terminates posteriorly in the small abdominal 
air-sac, which is still contained within the lung substance. Just 
anterior to this is a slight diverticulum, possibly the primordium 
of the posterior thoracic air-sae. The parabronchi or tertiary 
bronchi are not yet formed. 

Between the eighth and eleventh days, numerous tertiary 
bronchi (parabronchi) arise from the ento- and ectobronchi 
(Fig. 190). These are considerably smaller than the tubes from 
which they arise, and are extremely numerous, radiating from all 
parts of the secondary bronchi towards the free surfaces of the 
lungs, and ending always in slight enlargements. They do not 
appear to anastomose, though they are known to do so later. 
They are embedded in the mesenchyme of the lung, which is 
already marked out into areas hexagonal in cross-section, with 
the parabronchi in the centers, by the developing pulmonary 
blood-vessels. The canaliculi and alveoli arise later, and it 1s easy 


ALIMENTARY TRACT AND ITS APPENDAGES 329 


to imagine the manner in which they must form, from the anatomy 
of the adult lung; small branches must arise radially around the 
central parabronchi and penetrate to the margins of each hexagonal 
area, branching on the way and terminating in the final alveoli. 


Fic. 190. — Transverse section through the lungs of a chick embryo of 11 days. 
a. th. A. 8., Anterior thoracic air-sac. Ao., Aorta. Aur. d.,s., Right and 


left auricles. B. d., s., Right and left ducts of Botallus. F., Feather germs. 
Li., Liver. P. C., Pericardial cavity. p. p. M., Pleuroperitoneal membrane. 
P. V., Pulmonary vein. Par’b., Parabronchi. Pl. C., Pleural cavity. ~Pts Ce 
Peritoneal cavity. R., Rib. Se., Scapula. V.d.,s., Right and left ventri- 
cles. 


The expanding lungs nearly fill the pleural cavities on the 
eleventh day. Subsequently, the pleural cavity is obliterated 
by fusion of the free surfaces of the lungs with the wall of the 
pleural cavities. Thus it happens that the dorsal surfaces of the 


330 THE DEVELOPMENT OF THE CHICK 


lungs of the adult ‘“‘have no peritoneal covering,” although this 
is denied by other authors. 

The air-sacs are terminal expansions of entobronchi or of the 
mesobronchus (Fig. 191). Some details of their later history 
may be noted as follows: The 
abdominal air-sacs are, accord- 
ing to all authors, the first to 
appear. It seems to me, how- 
ever, doubtful that the slight 
terminal expansion at the hin- 
der end of the mesobronchus 
should be regarded at its first 
appearance as the primordium 
of the posterior air-sac. How- 
ever this may be, they do not 
undergo any considerable ex- 
pansion until after the eighth 
day (cf. Fig. 191). Then they 
push through the hinder end of 


the pleuroperitoneal membrane, 
now fused with the lateral body- 


Fic. 191. — Lungs and air-sacs of a 
chick embryo of about 10 days. wall, and penetrate the latter 
(After Selenka.) just beneath the peritoneum. 


1, Cervical air-sac. 2 and 2’, inter- 
clavicular air-saec. 3, Anterior thoracic : ; 
air-sac. 4, Posterior thoracic air-sac. to expand into the abdominal 


5, Abdominal air-sac. ‘avity just behind the liver, 
thus evaginating the peritoneum. The enlarged sac is connected 
by a narrow tube with the hind end of the mesobronchus. The 
left sac is somewhat larger than the right. The expansion goes 
on rapidly and by the thirteenth to the fifteenth day they have 
reached the hinder end of the body cavity, and have already ex- 


About the tenth day they begin 


panded into it so far as to form fusions with the mesentery. 
According to Bertelli, the rudiments of the cervical sacs appear 
on the fifth day, but I doubt that they are distinguishable from 
the first entobronehus so early. They push forward first into 
the pleural cavity, afterwards entering the mediastinal tissue 
and so reach the neck. The interclavicular sac, which is single in 
the adult, arises on the sixth day as a pair of evaginations of the 
first entobronchus (according to Bertelli from the cervical sacs); 


they undergo fusion secondarily. 


ALIMENTARY TRACT AND ITS APPENDAGES 331 


The anterior thoracic sac forms about the seventh day as a 
dilatation of the ventral wall of the third entobronchus pro- 
jecting into the pleuroperitoneal membrane near its median 
edge; it thus lies just lateral to the pneumato-enteric recesses. 
From this position it expands laterally and posteriorly in the 
pleuroperitoneal membrane! and thus gradually splits it in two 
layers (Fig. 190, 11 days); the original connection with the pul- 
monary tube does not expand much, and thus gradually forms 
a constricted neck. 

The posterior thoracic air-sac arises from the mesobronchus 
near its hind end somewhat later than the others, and grows 
at first through the hinder portion of the pleuroperitoneal 
membrane to enter the lateral body wall. In its subsequent 
expansion, it splits the posterior portion of the pleuroperitoneal 
membrane, as the anterior thoracic air-sac does the anterior 
portion of the same membrane. Anterior and posterior thoracic 
air-sacs then come into contact, forming a septum. 

The lower layer of the pleuroperitoneal membrane, split. off 
from the upper layer by expansion of anterior and posterior 
thoracic air-sacs, constitutes the oblique septum. The most 
posterior portion of the oblique septum, however, is derived from 
the peritoneum of the lateral body wall by expansion of the 
posterior thoracic air-sacs behind the pleuroperitoneal mem- 
brane. 

Like the abdominal air-saes, ‘the remainder expand rapidly, 
particularly from the fourteenth day on, among the thoracic 
viscera, and fuse intimately with these and the walls of the body 
cavity in a few days, the ccelomatie fluid being in the meantime 
absorbed. The interclavicular air-sac grows out to form the 
subscapular air-sac and at the time of hatching has approached 
close to the humerus. But more time is required to enable it to 
enter the humerus through the foramen pneumaticum; certainly 
more than twenty-two days, that is after the bone is nearly full- 
grown. The marrow, rich in blood-vessels, makes room for the 
air, as soon as the bone is fully formed.’’ (Selenka.) 

The Laryngotracheal Groove. ‘The embryonic primordium 
of the larynx and trachea communicates at first along its entire 
length with the postbranchial division of the pharynx (72 hours). 
At 96 hours the hinder portion of the groove is already converted 


1A small projection also grows forward. 


332 THE DEVELOPMENT OF THE CHICK 


into a tube lying beneath the anterior end of the cesophagus; this 
is the beginning of the trachea; the anterior part of the original 
groove represents the larynx, and its opening into the pharynx 
the glottis. It is not clear whether the trachea arises as an out- 
growth of the hinder end of the laryngotracheal groove, or from 
the hinder portion of the groove itself, by constriction from the 
pharynx. At 96 hours the lumen of the lower end of the trachea 
and adjoining portion of the two bronchi is obliterated by thicken- 
ing of the walls; this is, however, a very transitory condition. 

The growth of the trachea in length is extremely rapid, keep- 
ing pace, of course, with the elongation of the neck. At six 
days the trachea is a long epithelial tube with thick walls branch- 
ing into the two bronchi at its lower end (cf. Fig. 191). At its 
cephalic end the lumen opens into a considerable cavity, repre- 
senting the larynx; the glottis appears to be closed by a plug of 
epithelial cells continuous with the solid wall of the cesophagus. 
At eight days the lumen of both larynx and glottis is completely 
closed by the thickened epithelium; at eleven days the cavity 
of the lower end of the larynx is re-established, and the 
cell mass at the upper end is converted into a mesh-work by 
vacuolization; the lips of the glottis still show a complete epi- 
thelial fusion. Thus it is apparent that the cavity of the larynx 
is established by the formation of vacuoles within the solid cell- 
mass, and by their expansion and fusion. I cannot say how 
soon the glottis becomes open. 

The development of the laryngotracheal apparatus, includ- 
ing the cartilages and muscles, has not been specially investi- 
gated in the chick. In general, it can be said that the parts 
external to the epithelium arise from the mesenchyme which be- 
gins to condense around the epithelial tube on the fifth day. 
On the eighth day the glottis forms a decided projection into the 
pharynx. Distinct cartilaginous rings in the trachea are not 
visible on the eighth day, but are well formed on the eleventh 
day. As regards the syrinx it has been established by Wunder- 
lich for Fringilla domestica that the tympanic cartilage arises 
from the lower tracheal rings. The origin of the musculature 
of the syrinx is not known. 


CHAPTER XI 


THE BODY-CAVITIES, MESENTERIES AND SEPTUM 
TRANSVERSUM 


Tue development of these parts is one of the most difficult 
subjects in embryology, involving, as it does, complex relations 
between the viscera, vascular system, and primitive body-cavity, 
on which the definitive relations of the body-cavities and mesen- 
teries depend. 

The pericardial and pleuroperitoneal cavities are completely 
separated in all vertebrates excepting Amphioxus, cyclostomes 
and some Selachii and ganoids, in which narrow apertures exist 
between the two. The pleural and peritoneal divisions of the 
ccelome of the trunk communicate widely in amphibia; among 
reptiles completely closed pleural cavities are found apparently 
only in Crocodilia; in birds and mammals they are completely 
closed. 

As we have seen, in the early embryo of the chick there is 
free communication between all parts of the body-cavity. We 
have to consider, therefore, (1) the separation of the pericardial 
and pleuroperitoneal cavities, (2) the separation of pleural and 
peritoneal cavities, and (3) development of the mesenteries. 


I. THe SEPARATION OF THE PERICARDIAL AND PLEUROPERI- 
TONEAL CAVITIES 

The pericardial cavity proceeds from the cephalic division of 
the primitive ecelome (parietal cavity of His). We may review 
its primitive relations as follows (stage of 10 somites; see Chap. 
V): it contains the heart which divides it into right and left 
parts so long as the dorsal and ventral mesocardia persist; these, 
however, disappear very early. Laterally, the parietal cavity 
communicates with the extra-embryonic body-cavity (Figs. 53 
and 54); posteriorly it is bounded by the wall of the anterior 
intestinal portal (Fig. 67), on which the heart is seated like a 

333 


3354 THE DEVELOPMENT OF THE CHICK 


rider in his saddle, the body of the rider being represented by 
the heart, and his legs by the omphalomesenteric veins. On 
each side of this posterior wall the parietal cavity communicates 
with the ccelome of the trunk. The floor of the parietal cavity 
comprises two parts meeting at the head-fold, the anterior part 
being composed of somatopleure, and the posterior part of 
splanchnopleure; the former is part of the definitive pericardial 
wall, the latter, known as the precardial plate, is provisional 
(Fig. 67). 

The lateral mesocardia also take part in bounding the parietal 
cavity. It will be remembered that these arise as a fusion on 
each side between the somatopleure and the primitive omphalo- 
mesenteric veins, and that the ducts of Cuvier develop in them. 
As the blastoderm is spread out flat at the time that they form, 
they constitute at first a lateral boundary to the posterior part 
of the parietal cavity; but as the embryo becomes separated from 
the blastoderm they assume a frontal position between the sinus 
venosus and body-wall, the criginal median face becoming dorsal 
and the lateral face ventral. Thus they come to form a dorsal 
wall for the posterior part of the parietal cavity (Fig. 119). The 
communication of the parietal cavity with the coelome of the 
trunk is thus divided into two, known respectively as the dorsal 
parietal recess and the ventral parietal recess. The former is 
a passageway above the lateral mesocardia, communicating in 
front with the parietal (pericardial) cavity and behind with the 
trunk cavity; the latter is a communication on each side of the 
wall of the anterior intestinal portal ventral to the lateral meso- 
cardia, 

The completion of the posterior wall of the pericardium is 
brought about by the formation and development of the septum 
transversum., 

Septum Transversum. The septum transversum arises from 
three originally distinct parts, viz., (1) a median mass, (2) the 
lateral mesocardia, and (38) lateral closing folds arising from 
the body-wall between the umbilicus and the lateral mesocardia. 

1. The median mass proceeds from the ventral mesentery 
of the fore-gut. The location of the heart and liver in the ventral 
mesentery divides it in three parts, viz., (@) a superior part, 
comprising the mesocardium and dorsal ligament of the liver 
(gastrohepatie ligament), uniting the floor of the fore-gut and 


THE BODY-CAVITIES 330 


the heart and liver, (b) a median portion comprising the sinus 
venosus, ductus venosus and liver, and (¢) an inferior portion. 
The superior part persists in the region of the sinus venosus and 
liver, and the inferior part only as the primary ventral ligament 
of the liver. 

The median mass of the septum transversum thus includes 
the sinus venosus, liver, and dorsal and ventral ligaments of the 
liver. 

At sixty hours the median mass includes chiefly the sinus 
and ductus venosus and their mesenteries. At eighty hours 
(Fig. 192) a constriction begins to appear between sinus and 


Fia. 192. — Reconstruction of the septum transversum and 
associated mesenteries of a chick embryo of 8O hours. (After 
Ravn.) 


Ao., Aorta. Int., Intestine. Liv., Liver. Pl. m’g., Plica 
mesogastrica. §.V., Sinus venosus. 


ductus venosus, and the walls of the latter are expanded by the 
formation of liver tissue, so that the cylindrical form charac- 
teristic of sixty hours is lost, and the lateral walls of the ductus 
venosus bulge considerably. The continued growth of the liver 
causes a rapid lateral expansion of this portion of the septum 
transversum (Fig. 193 A). 

The primary ventral ligament of the liver is included within 
the wall of the anterior intestinal portal up to about eighty hours. 
But, as the yolk-sac shifts farther back, this hgament appears 
as a separate membrane (inferior part of the primary ventral 


336 THE DEVELOPMENT OF. THE CHICK 


Fia. 193. — Reconstruction of the septum transversum and asso- 
ciated mesenteries of a chick embryo of 5 to 6 days. (After 
Ravn.) 


A. Entire. 

B. After removal of the liver. 

A., Aorta. ac. M., Accessory mesentery. cav. F., Caval 
fold. ecoel. F., Ccaehae fold. Her., Hiatus communis reces- 
sum. Int., Intestine. Lg., Lung. Liv., Liver. pvl., Primary 
ventral ligament of the liver. Sv., Sinus venosus. 


mesentery), uniting the ventral and posterior face of the liver 
to the body-wall just in front of the umbilicus (Fig. 193 A, pvl.). 

lor the purposes of these figures the body-wall is cut away. 
Nevertheless, it can be seen that the pericardial cavity communi- 


THE BODY-CAVITIES 337 


cates with the peritoneal cavity around the median mass of the 
septum transversum beneath the lateral mesocardia. 

2. The lateral mesocardia constitute the second component 
of the septum transversum. At the stage of sixty hours they 
are nearly round in section. At eighty-six hours the substance 
posterior to the duct of Cuvier begins to thicken (Fig. 192) so 
that the section is no longer round but elongated towards the 
umbilicus. They still extend almost transversely to the lateral 
body-wall. However, the retreat of the heart backwards soon 
changes their direction (Fig. 193 A) so as to form a long oblique 
partition between the pericardium and the dorsal parietal recess, 
the direction of the ducts of Cuvier being changed at the same 
time. The lateral mesocardia are directly continuous with the 
anterior portion of the median mass of the septum transversum. 

3. The lateral closing folds arise as ridges of the lateral body- 
wall extending obliquely from the primary ventral ligament of 
the liver upwards and forwards to the lateral mesocardia. They 
arise along the course of the umbilical veins which open at first 
into the ducts of Cuvier. As the lateral closing folds develop 
first at their anterior ends, they appear as direct backward 
prolongations of the lateral mesocardia. They fuse with the 
lateral ventral surface of the liver (median mass of the septum 
transversum), and when they are completed back to the primary 
ventral ligament of the liver, they completely close the ventral 
communication of the pericardium with the peritoneal cavity. 
They mark out a triangular area on the cephalic face of the liver 
with postero-ventral apex and antero-dorsal base, which forms 
the median portion of the posterior wall of the pericardium (cf. 
Fig. 193 A). At six days the ventral communication of the 
pericardium is reduced to a very small opening, and at eight days 
it is entirely closed. 

Closure of the Dorsal Opening of the Pericardium. As already 
noted the pericardial cavity communicates with the peritoneal 
cavity above the lateral mesocardia by way of the dorsal 
parietal recesses, which are destined to form a large part of the 
pleural cavities. We have, therefore, to consider next the closure 
of the aperture between the pleural and pericardial cavities. 
We have already seen that the heart shifts backwards very rapidly 
between the third and sixth days, and this draws out the lateral 
mesocardia in an oblique plane directed from dorsal anterior to 


338 THE DEVELOPMENT OF THE CHICK 


ventral posterior (Fig. 193); the ducts of Cuvier thus become 
oblique also, and the lateral mesocardia become converted into 
an oblique septum between the posterior parts of the incipient 
pleural cavities and the pericardial cavity (pleuro-pericardial 
membrane). In front of the sinus venosus, however, the pleural 
and pericardial cavities communicate with one another between 
the ducts of Cuvier, which form a projection from the lateral 
body-wall, and the bronchi which project laterally beneath the 
cesophagus. These apertures are gradually closed by fusion of 
the walls of the bronchi with the projecting duct of Cuvier, begin- 
ning in front and extending back to the sinus venosus. Thus the 
incipient pleural cavities come to end blindly in front, though 
they still communicate widely behind with the peritoneal cavity. 
The membrane thus established between pleural and pericardial 
cavities is known as the pleuropericardial membrane. 
Establishment of Independent Pericardial Walls. With the 
formation of the ventral body-wall the precardial plate (a portion 
of the splanchnopleure, which at first forms part of the floor of 
the pericardial cavity) is gradually replaced by the ventral body- 
wall. The pericardial cavity is thus bounded ventrally and 
laterally by the body-wall and posteriorly by the median mass 
of the septum transversum. It has no independent walls at 
first. The definitive pericardium is, however, a membranous 
sac, and this is formed by two main processes: in the first place 
the membrane of the anterior face of the liver (median mass of 
the septum transversum) which forms the posterior boundary 
of the pericardium becomes much thickened, and gradually 
splits off from the liver (ef. Figs. 148 and 150), the peritoneal 
cavity extending pari passu between the liver and the membrana 
pericardiaco-peritoneale thus formed. The suspensory ligament 
of the liver, however, remains in the middle line, and the mem- 
brane is also directly continuous with the liver dorsally around 
the roots of the great veins. Thus a membranous wall is estab- 
lished for the posterior part of the pericardium. In the second 
place the peritoneal cavity extends secondarily into the body- 
wall bounding the pericardium ventrally and laterally, and thus 
splits a membranous pericardial sac off from the body-wall. In 
this process the liver appears to play an active role. At least 
its anterior lobes oceupy the peritoneal spaces thus established 
(Fig. 194). In the mammals, on the other hand, it is the ex- 


THE EODY-CAVITIES 339 


tension of the pleural cavities ventrally that splits the mem- 
branous pericardium from the body-wall. 

Derivatives of the Septum Transversum. [rom the preceding 
account it will be seen that the following are derivatives of the 
septum transversum: (1) The posterior part of the pericardial 
membrane. (2) The pleuro-pericardial membrane. (38) The liver 
with its vessels and gastro-hepatic and primary ventral ligaments. 


Fic. 194. — Photograph of a transverse section of an 8-day chick. 

abd. A. S., Abdominal air-sac. A. coel., Coeliac artery. <Ao., Aorta. 
A. o. m., Omphalomesenteric artery. Aur. d., Right auricle. Cav. pe., 
Pericardial cavity. M. D., Miillerian duct. M. pe., Membranous pericar- 
dium. Msn., Mesonephros. Pr’v., Proventriculus. $S., Septum ventricu- 
lorum. V. c. i., Vena cava inferior. V. h.d., Right hepatic vein. V. d., 
Right ventricle. V. s., Left ventricle. 


(4) A small part of the heart (the sinus venosus). As regards 
the last, it should be noted that the anterior portion of the original 
septum transversum is gradually constricted from the major 
posterior portion and becomes established as the sinus venosus; 


340 THE DEVELOPMENT OF THE CHICK 


this subsequently becomes incorporated in the right auricle of 
the heart. (See Chap. XII). 


II. SEPARATION OF PLEURAL AND PERITONEAL CAVITIES; ORIGIN 
OF THE SEPTUM PLEURO-PERITONEALE 


The pleuro-peritoneal septum arises from the so-called acces- 
sory mesenteries, the origin of which must now be described. 
At first the septum transversum has only a median dorsal mesen- 
tery, viz., the superior part of the primary ventral mesentery 
that unites the septum transversum to the floor of the fore-gut, 
and so by way of the dorsal mesentery of the latter to the dorsal 
body-wall. Subsequently, however, there arises a pair of mesen- 
teries extending from the lateral wall of the cesophagus to the 
septum transversum. These are the accessory mesenteries, and 
they arise as follows: about the sixtieth hour they appear as 
mesenchymatous outgrowths, forming elongated lobes, projecting 
from the side walls of the cesophagus opposite the hind end of 
the lung rudiments. The right and left lobes are practically 
the same size at first and they bend over ventrally and soon fuse 
with the median mass of the septum transversum, represented 
at this time by the sinus and meatus venosus (cf. Figs. 118-120, 
Chap. VI). Thus are produced a pair of bays of the peritoneal 
‘avity ending blindly in front, bounded laterally by the accessory 
mesenteries, and in the median direction by the intestine and 
its mesenteries. These are the pneumato-enteric recesses. 

These bays have received different names from the various authors: 
thus His named only the right one as recessus superior sacci omenti; 
the left one being practically absent in mammals; Stoss called both re- 
cessus pleuro-peritoneales; Mall called them gastric diverticula; Hoch- 
stetter, recessus pulmo-hepatici; Maurer, bursa hepatico-enterica; Ravn, 
recessus superior for the right one and recessus sinister for the left. We 
may callthem the pneumato-enteric recesses (recessus pneumato-entericl), 
following Broman. 

At seventy-two hours the entodermal lung-sacs extend to 
the base of the accessory mesenteries, ending at the anterior 
end of the pneumato-enteric recesses. On the left side at this 
time the recess is fully formed back to near the anterior end of 
the cephalic hepatic diverticulum, on the right side considerably 
farther back; that is, the accessory mesentery is already longer 
on the right than on the left side, and the mesenchymatous lobe 


THE BODY-CAVITIES 341 


from which it arises (plica mesogastrica, Broman) can be traced 
back, shifting its attachment to the dorsal mesentery, as far as 
the anterior intestinal portal and a little farther (Fig. 192, ef. 
also Fig. 120). 

At ninety-six hours the entodermal lung-saes extend far into 
the accessory mesenteries, and thus lie laterally to the pneumato- 
enteric recesses. On the left side the accessory mesentery ceases 
opposite the tip of the lung, but on the right side it is continued 
back by the mesentery of the vena cava as far as the middle of 
the stomach, and in this region its ventral attachment is to the 
superior lateral angle of the liver. 

The growth of the lung-sacs into the accessory mesenteries 
divides the latter into three parts, viz., a superior portion uniting 
the lung to the dorsal mesentery, a median portion enclosing the 
lung, and an inferior portion uniting the lung-sacs to the median 
mass of the septum transversum. Now, as the liver expands 
laterally the ventral attachment of the accessory mesentery is 
‘arried out towards the lateral body-wall, inasmuch as its attach- 
ment is to the lateral superior face of the liver (cf. Fig. 231, Chap. 
XII). Thus the accessory mesenteries are gradually shifted 
from their original almost sagittal plane to a plane that is approxi- 
mately frontal. The developing lungs project dorsally from the 
accessory mesenteries, which may now be called the pleuro- 
peritoneal membranes, into the pleural cavities (Fig. 189); and 
the latter communicate with the peritoneal cavity only laterally 
to the liver. These communications are then soon closed by a 
fusion between the lateral edges of the pleuro-peritoneal mem- 
brane and the lateral body-wall; this fusion is not completely 
established on the eighth day, but it is on the eleventh day. 


In reptiles and mammals the so-called mesonephric mesentery plays 
an important part in the closure of the pleural cavities. It arises from 
the apex of the mesonephros at its cephalic end, and fuses with the septum 
transversum. It thus forms a partition between the hinder portion 
of the pleural cavity and the cranio-lateral recesses of the peritoneal 
cavity. Subsequently, in mammals, its posterior free border fuses with 
the caudal bounding folds of the pleural cavity that arise as forwardly 
directed projections from the accessory mesentery on the right side 
and the wall of the stomach on the left. Hochstetter states that such 
a mesonephric fold is found in the chick but that it does not appear to 
play any essential part in the formation of the septum pleuro-peritoneale. 


342 THE DEVELOPMENT OF THE CHICK 


I find it in the chick as a very minute vestige at the cranial end of the 
mesonephros associated with the funnel of the Mullerian duct. It aids 
in the final closure of the pleural cavity by bridging over the narrow 
chink between the lateral angle of the pleuro-peritoneal membrane and 
the lateral body-wall. (See Bertelli, 1898.) 


The oblique septum of birds arises as a layer split off from 
the septum pleuro-peritoneale (pulmonary aponeurosis or pul- 
monary diaphragm of adult anatomy) by the expansion of the 
anterior and posterior thoracic air-sacs within it. This mode 
of formation is clearly seen, particularly on the right side, in a 
series of transverse sections of a chick embryo of eleven days 
(Fig. 190). Thus the cavity between the oblique septum and the 
pulmonary diaphragm (cavum sub-pulmonale of Huxley) is not 
a portion of the body-cavity and bears no relation to it. The 
ingrowth of muscles into the pulmonary diaphragm can be 
observed in the same series of sections. It begins on the tenth 


day according to Bertelli. 


III. Tar MrsentTerius 


The dorsal mesentery is originally a vertical membrane 
formed by redupliecation of the peritoneum from the mid-dorsal 
line of the body-cavity to the intestine; mesenchyme is contained 
from the outset between its peritoneal layers, and serves as the 
pathway for the development of the nerves and blood-vessels 
of the intestine. In the course of development, its lower edge 
elongates with the growth of the intestine, and is thrown into 
folds, or twisted and turned with the various folds and turnings 
of the intestine. Detailed studies of its later development in the 
chick have not been published, but the principal events in its 
history are as follows: For convenience of description the dorsal 
mesentery may be divided into three portions corresponding to 
the main divisions of the alimentary tract, viz., an anterior 
division belonging to the stomach and duodenum, sometimes 
known as the mesogastrium; an intestinal division belonging to 
the second loop of the embryonic intestine that descends into 
the umbilicus; and a posterior division belonging to the large 
intestine and rectum. Inasmuch as the duodeno-jejunal flexure 
(igs. 179 and 180, X) retains from an early stage a short 
mesenterial attachment, there is quite a sharp boundary in the 
chick between the first and second divisions of the dorsal 


THE BODY-CAVITIES 343 


mesentery. The mesogastrium becomes modified by the dis- 
placement of the stomach, the outgrowth of the duodenal loop, 
the formation of the omentum, and by the development of the 
pancreas and spleen in it. (See below.) 

The second division of the mesentery is related to the longest 
division of the intestine, but as this arises from a relatively very 
small part of the embryonic intestine, its dorsal attachment. is 
short and the roots of the mesenteric arteries are grouped 
together. The third division is relatively long and not very 
deep; at its base it approaches near to the mesogastrium, to 
which it is attached by the root of the intermediate division. 

The Origin of the Omentum (mainly ajter Broman). In a 
preceding section we saw that the accessory mesentery is con- 
tinued back on the right side (at the stage of seventy-two hours) 
by a fold of the dorsal mesentery of the stomach known as the 
plica mesogastrica (ig. 120). The stomach is already displaced 
somewhat to the left, hence the dorsal mesentery is bent also, 
and the plica mesogastrica arises from the angle of the bend 
(Fig. 120). The ventral mesentery of the stomach, including 
the meatus venosus and liver, remains in the middle line. Thus 
the body-cavity on the right of the stomach is divided into two 
main divisions, viz., the general peritoneal cavity lateral to the 
plica mesogastrica and liver, and another cavity between the 
plica mesogastrica and liver on the one hand, and the stomach 
on the other; the latter cavity has two divisions, a dorsal one 
between the plica mesogastrica and upper half of the stomach 
(recessus mesenterico-entericus) and a ventral one between the 
liver (meatus venosus) and stomach (recessus hepatico-entericus), 
which are continued anteriorly into the pneumato-enteric recesses. 
Subsequently, they become entirely shut off from the peritoneal 
cavity, but at present (stage of Fig. 120) they communicate 
with it by a long fissure bounded by the accessory mesentery in 
front, by the plica mesogastrica above, and the meatus venosus 
below; this opening may be called the hiatus communis recessum ; 
it corresponds to the foramen of Winslow of mammals (cf. Fig. 
193 A). 

As development proceeds, a progressive fusion of the right 
dorsal border of the liver with the plica mesogastrica takes place 
in a cranio-caudal direction, thus lessening the extent of the 
hiatus. 


344 THE DEVELOPMENT OF THE CHICK 


At about ninety-six hours, the plica mesogastrica divides to 
form two longitudinal folds, in the lateral one of which the vena 
cava inferior develops (cf. Fig. 193 B); it is hence known as the 
‘aval fold; the more median division is the coeliac fold including 
the coeliac artery. Between them is a subdivision of the recesses 
known as the cavo-cceliac recess, which corresponds to the atrium 
bursee omentalis of mammals. The fusion of the right lateral 
border of the liver continues along the course of the caval fold, 
and the vena cava inferior is soon completely enveloped in liver 
tissue. Behind the point where the vena cava inferior enters 
the liver, the latter fuses with the ventral edge of the right meso- 
nephros, thus progressively diminishing the opening of the collec- 
tive recesses into the peritoneal cavity. At about the one hun- 
dred and sixtieth hour, the fusion reaches the portal vein, and the 
recesses are thus completely shut off from the peritoneal cavity. 
Thus a lesser peritoneal cavity is completely separated on the 
right side of the body from the main cavity; and from the former 
both lesser and greater omental spaces develop on the right and 
left sides respectively of the coeliac fold. (Bursa omenti minoris 
and bursa omenti majoris of the bursa omentalis dextra.) 

The communication of the lesser and greater omental spaces 
in front of the cceliac fold is closed by fusion of the latter with 
the right side of the proventriculus at about the one hundred 
and sixtieth hour, though it remains open throughout life in some 
birds. The two omental spaces are also elongated in a posterior 
direction by the caudal prolongation of the right lobe of the liver 
and of the gizzard respectively (Fig. 195). The lateral wall of 
the omentum minus is attached to the lateral dorsal border of 
the right lobe of the liver as already described, and it is therefore 
carried back by the elongation of this lobe; but as the vena cava 
inferior is inserted about the middle of this wall and cannot be 
drawn back, it results that there is a deep median indentation 
of the lateral wall of the omentum minus, at the bottom of which 
lies the vena cava inferior. 

The condition of both right and left omental spaces at 154 
hours is shown in Figures 195 and 196. Subsequently, about the 
eleventh day, the mesogastrium behind the spleen becomes per- 
forated, and the greater omental space thus opens secondarily 
into the left side of the body-cavity. A true omental fold exists 
only for a short time in the development of the chick, and is 


THE BODY-CAVITIES 345 


soon taken up by the caudal elongation of the stomach. Oblitera- 
tion of the cavity of the omentum by fusion of its walls takes 
place at its caudal end. (Broman.) 

Spaces corresponding to the omental cavities are also formed 
on the left side of the body, but they are of much less extent. 
(See Fig. 196.) The communication of these spaces with the 
greater peritoneal cavity is not, however, shut off as on the right 
side. However, a secondary and later fusion of the left lobe 
of the liver with the lateral body-wall, and of the gizzard with 


Her ---- 


Fic. 195. — Reconstruction of the omental space of a chick embryo of 154 
hours from the right side. (After Broman.) 


Bomaj., Bursa omenti majoris. Bomin., Bursa omenti minoris. Du., 
Duodenum. Giz., Gizzard. Her., Hiatus communis recessum.  oe., (Esoph- 
agus. rBr., Right bronchus. Rpedx., Right pneumato-enteric recess. 


the ventral body-wall does isolate a portion of the peritoneal 
cavity from the remainder on the left side. Into this the pneu- 
mato- and hepato-enteric cavities of the left side open; however, 
it is obvious that this space is not analogous to the omental 
spaces on the right. 

Origin of the Spleen. ‘The spleen arises as a proliferation from 
the peritoneum clothing the left side of the dorsal mesentery 
just above the extremity of the dorsal pancreas. This prolifera- 
tion forms the angle of a cranio-caudal fold of the dorsal mesen- 
tery which is caused by the displacement of stomach and intestine 


346 THE DEVELOPMENT OF THE CHICK 


to the left side of the body-cavity (Fig. 188), and which is 
exaggerated by the rapid growth of the dorsal pancreas (Choron- 
schitzky). The spleen is thus genetically related to the wall of 
the great omentum, and hes outside the cavity of the latter. 
The cells of the spleen are proliferated from a peritoneal thicken- 
ing, Which may be compared in this respect to the germinal 
epithelium. It is recognizable at ninety-six hours, and the mass 
formed by its proliferation grows rapidly, forming a very consid- 
erable projection into the left side of the body-cavity above 
the stomach, at six days (cf. Fig. 197). 


Bomin 


~~--~Bomay 


Fig. 196. — The same model from the left side. (After Broman.) 


Hrpesin., Hiatus recessus pneumato-entericus sinister. 1. Br., 
Left bronchus. Pr’v., Proventriculus. Rhesin., Recessus hepato- 
entericus sinister. Rpesin., Right pneumato-enteric recess. Other 
abbreviations as in Fig. 195. 


According to Choronschitzky, the peritoneal cells invade the 
neighboring mesenchyme, and, spreading through it, form an ill- 
defined denser area, the fundamental tissue of which is therefore 
mesenchymal. The meshes of the latter are in immediate con- 
tinuity with the vena lienalis, but the vascular endothelium is 


THE BODY-CAVITIES 347 


not continued into these meshes. Thus free embryonic cells 
of the primordium of the spleen enter the venous circulation 
directly, and become transformed into blood-corpuscles. 


On account of the intimate relation between the pancreas and spleen 
in early embryonic stages, certain authors (see esp. Woit) have asserted 
a genetic connection, deriving the spleen from the pancreas. There 
is, however, no good evidence that the relation is other than that of 
propinquity. 


Fig. 197. — Photograph of transverse section through a chick embryo of 

8 days. 

A.o. m., Omphalomesenteric artery. Du., Duodenum. Giz., Gizzard. 
Gon., Gonad. IIL., Ilium. M.D., Miillerian duct. Pe., Pancreas. V. umb., 
Umbilical vein. 

It should also be noted that the absence of rotation of the 
chick’s stomach (as contrasted with mammals) and the lesser 
development of the great omentum appear to be the causes of 
the more primitive position of the spleen in birds as contrasted 
with mammals. 


CHAPTER XII 


THE LATER DEVELOPMENT OF THE VASCULAR 
SYSTEM 


I. Tae Heart. (For an account of the earlier development, 
see Chapters V and VI.) 


At the stage of seventy-two hours (lig. 198), the ventricle 
consists of a posterior transverse portion and two short parallel 
limbs; the right limb is continuous with the bulbus arteriosus 
from which it may be distinguished by 
a slight constriction, and the left limb 
with the atrium. The constriction be- 
tween the latter is the auricular canal. 
Between the two limbs in the interior 
of the ventricle is a short bulbo-auricu- 
lar septum separating the openings of 
Fic. 198. — Ventral view of Dulbus and atrium into the ventricle. A 


the heart of a chick em- slight groove, the interventricular sulcus, 

bryo of 2.1 mm. head that extends backwards and to the right 

length. (After Greilfrom  f.4m) the bulbo-auricular angle, marks 

Hochstetter.) ; ra : : ; 

Age Mi Bebe the line of formation of the future inter- 
Bulbus cordis. b. V., The ventricular septum (Fig. 199). 
ronserictign between bulls The Development of the External 
riculo-ventricular canal. V., Form of the Heart. We have seen that 
Ventricle. in the process of development the heart 
shifts backwards into the thorax. The ventricle undergoes the 
greatest displacement, owing to its relative freedom of move- 
ment, and thus comes to lie successively to the right of, and then 
behind the atrium. <A gradual rotation of the ventricular division 
on its antero-posterior axis accompanies its posterior displacement; 
and this takes place in such a way that the bulbus is transferred 
to the mid-ventral line, where it lies between the auricles (Figs. 
199 and 200). 

The auricles arise as lateral expansions of the atrium, the 

348 


LATER DEVELOPMENT OF VASCULAR SYSTEM 349 


left one first at an early stage and the right one later. The left 
auricle is thus larger than the right for a considerable period of 
time in the early development. When the right auricle grows 
out it passes above the bulbus, which is already in process of 
rotation, and the two auricles then expand ventrally on each 
side of the bulbus. The apex of the ventricle belongs primarily 
to the left side and this remains obvious as long as the external 
interventricular groove exists. In the adult the apex of the 
heart belongs to the left ventricle. 


Fic. 199.— Ventral view of the heart of a 


chick embryo of 5 mm. head-length. 
(After Masius.) 


Atr. d., s., Right and left auricles. 
B. Co. Bulbus cordis. V. Ventricle. 


The varying positions occupied by the chambers of the heart in rela- 
tion to the body axes constitute a serious difficulty in describing the 
development. For instance, the auricular canal is at first in front of 
the atrium (before any bending of the heart takes place). As the ven- 
tricular loop turns backward and beneath the atrium, the auricular 
‘anal is ventral to the atrium; and finally, as the ventricles assume their 
definitive position behind the auricles, the derivatives of the auricular 
canal (auriculo-ventricular openings) come to lie behind the atrium. In 
other words, the atrium rotates around a transverse axis through nearly 
180 degrees in such a way that its original anterior end becomes succes- 


390 THE DEVELOPMENT OF THE CHICK 


sively ventral and posterior. The definitive ventral surface of the heart 
is a cranial rather than a ventral surface during the critical period of 
development described below, up to eight days (cf. Figs. 148 and 150). 
In other words, the apex of the heart is directed ventrally rather than 
posteriorly, though it has a posterior inclination. For simplicity of de- 
scription, however, it seems better to use the definitive orientation in the 
following account; that is, to regard the apex of the heart as posterior 
instead of ventral, and the bulbus face of the heart as ventral instead 
of cranial, in position. 


Fig. 200. — Ventral view of the heart of a 


chick embryo of 7.5mm. head-length. (After 
Masius. ) 


Atr. d., s., Right and left auricles. B. Co., 
Bulbus cordis. V., Ventricle. 


Division of the Cavities of the Heart. The embryonic 
heart is primarily a single continuous tube; during development 
a complex series of changes brings about its complete division 
into right and left sides, corresponding to the pulmonary and 
systemic circulations. Partitions or septa arise independently 
in each primary division of the cardiac tube, excepting the sinus 
venosus, and subsequently these unite in such a way as to make 
two independent circulatory systems. During this time the 


LATER DEVELOPMENT OF VASCULAR SYSTEM dol 


appropriate valves are formed. We have thus to describe the 
origin of three primary septa, viz., the interauricular septum, 
the interventricular septum, and the septum of the truncus and 
bulbus arteriosus. These do not, however, themselves unite 
directly, but are joined together by the intermediation of a fourth, 
large, cushion-like septum formed in the auricular canal, 7.e., in 
the opening between the primitive atrium and ventricle. 

In general it may be said that the development of the three 
primary septa takes place from the periphery towards the center, 
7.e., towards the cushion-septum of the auricular canal, and that 
it is practically synchronous in all three, though there is a slight 
precedence of the interauricular septum. During the same time 
the cushion-septum of the auricular canal is formed. We may 
then consider first the origin of these septa separately, and second 
their union. 

(a) The Septum Trunci et Bulbi Arteriosi (Septum Aortico- 
Pulmonale). This septum divides the truncus and bulbus arte- 
riosus into two arteries, the aorta and pulmonary artery. Three 
divisions may be distinguished, viz., a part in the truncus arte- 
riosus, a part in the distal division of the bulbus extending to 
the place of formation of the semilunar valves, and a part in the 
proximal portion of the bulbus, which subsequently becomes 
incorporated in the ventricles. In mode of formation these are 
more or less independent, though they unite to form a continuous 
septum. 

The septum of the truncus arteriosus arises on the fifth day 
as a complete partition extending from the cephalic border of 
the two pulmonary arches into the upper portion of the bulbus 
arteriosus; the blood current flowing through the bulbus that 
passes behind this partition enters the pulmonary arches exclu- 
sively, that passing in front enters the two remaining pairs of aortic 
arches. During the latter half of the fifth day and on the sixth 
day the septum of the truncus is continued into the proximal por- 
tion of the bulbus and divides it in two stems. Here, however, 
it co-operates with three longitudinal ridges of the endocardium 
of the bulbus, one of which is in the direct line of prolonga- 
tion of the septum of the truncus, which therefore is continued 
along this one and between the other two as far as the place of 
formation of the semilunar valves (Fig. 201). The entire septum 
thus formed has a slightly spiral course, of such a nature that 


302 THE DEVELOPMENT OF THE CHICK 
the pulmonalis, which les dorsal to the aorta distally, is gradually 
The third division of the aortie- 


pulmonary septum arises near the opening of the bulbus into 


transposed to its left side. 


the ventricle in the form of two ridges of the endocardium on 
the right and left sides respectively of the bulbus, the pulmonary 

division lying ventral and the 
division the 
partition. A third 
slight endocardial ridge of the 
proximal part of the bulbus is 
described (Hochstetter, Greil) 
at this stage, but it soon dis- 
The proximal bulbus 


aortic dorsal to 


incipient 


Fia. 201. — A. Section through the appears. 


truncus arteriosus of an embryo of 5 
mm. head-length. 
B. Section through the distal por- 


ridges may be seen on the fifth 
day; on the sixth day they are 
well formed; on the seventh day 


tion of the bulbus arteriosus of the 
same embryo. (After Greil.) 

A., Aorta. P., Pulmonalis. A.S. ao. 
p., Plane of the septum aortico-pulmo- 
nale. 1, 2, and 3, Ridges prolonging 
the septum aortico-pulmonale. 


they have united to form a par- 
tition which becomes continu- 
ous with the partition in the 
distal 
Thus the separation of the aor- 


portion of the bulbus. 


tic and pulmonary trunk is completed down to the ventricle. 

The semilunar valves arise by excavation of three endocar- 
dial thickenings in each trunk formed at the caudal end of the 
distal division of the bulbus (Hochstetter, Greil). The origin 
of these thickenings is as follows. Both the aortic and pulmonary 
trunks receive one each of the original endocardial ridges of the 
distal portion of the bulbus owing to the course of the aortic- 
Mach also receives half of the ridge along 
A third ridge 
A cavity then 


pulmonary septum. 
which the septum of the truncus is prolonged. 
arises subsequently in each between these two. 
arises in each ridge and opens distally into the aorta and pul- 
monary artery respectively, thus forming pockets open in front. 
These valves are fully formed at eight days. 

The aortic-pulmonary septum becomes thick early in its 
history and the muscular layers of the vascular trunks, which 
at first form a common sheath for both, gradually constrict into 
the septum, and separate when the constriction brings them 
together, so that each vessel obtains an independent muscular 


wall. Subsequently, a constriction extends from the outer layer 


LATER DEVELOPMENT OF VASCULAR SYSTEM 3093 


of the truncus and bulbus along the entire length of the septum, 
and thus completely separates the aorta and pulmonary arteries 
from each other. On the eighth day each vessel has independent 
muscular walls, and the external constriction has made some 
progress. 

(b) The Interventricular Septum. As noted before, the inter- 
ventricular sulcus that extends from the bulbo-auricular angle 
towards the apex of the heart marks the line of development of 
the interventricular septum. The right division of the primitive 
ventricle is therefore continuous with the bulbus and the left 
with the atrium. However, the partition, bulbo-auricular sep- 
tum, which at first separates the primitive right and left limbs 
of the ventricle, undergoes rapid reduction and becomes a mere 
ridge by the stage of ninety-six hours. Thus the opening of the 
bulbus and the auricular canal lie side by side, separated only 
by this shght ridge. The rotation of the ventricle brings the 
bulbus from the right side into the mid-ventral line so that the 
opening of the bulbus comes to lie ventral to the auricular canal 
on its right side (cf. Figs. 199 and 200). 

In the interior of the heart the development of the inter- 
ventricular septum is associated with the formation of the tra- 
beculee or ramified and anastomosing processes of the myocardium 
that convert the peripheral part of the ventricular cavity into a 
spongy mass at an early stage. Along the line of the interven- 
tricular sulcus these trabecule extend farther into the cavity 
than elsewhere, and become united together at their apices by a 
shght thickening of the endocardium, which clothes them all, 
thus originating the interventricular septum (lig. 202). This 
process begins at the apex of the ventricle, and extends towards 
the base, the fleshy septum becoming gradually higher and thicker 
and better organized. It thus has a concave free border, directed 
towards the bulbo-auricular ridge and continued along both the 
ventral and dorsal surfaces of the ventricle. The septum develops 
more rapidly along the dorsal than the ventral wall and on the fifth 
day reaches the neighborhood of the auricular canal on this side, 
and unites with the right side of the fused endocardial cushions 
which have in the meantime developed in the latter. (See below.) 
Thus the interventricular foramen, or communication between 
the ventricles, is gradually reduced in extent and limited to the 
ventral anterior portion of the septum. It is never completely 


354 THE DEVELOPMENT OF THE CHICK 


closed, but, as we shall see later, the interventricular foramen 
is utilized in connecting up the aorta with the left ventricle. 

It will be seen that if the original direction of this septum, 
as indicated by the interventricular groove on the surface, were 
preserved (Fig. 199), the interventricular septum would fuse 
with the bulbo-auricular ridge and the right ventricle would then 
be continuous with the bulbus only, and the left ventricle with 
the atrium, and circulation of the blood would be impossible. 
The avoidance of this condition is due to the rotation of the bul- 
bus by which it is brought beneath the auricular canal, and by 
widening of the auricular canal to the right. Thus the inter- 


Fig. 202. — Frontal section of the heart of a chick 
embryo of 9 mm. head-length. (After Hochstet- 
ter.) 


E. C., Median endothelial cushion. 1. E. C., Lat- 
eral endothelial cushion. $8. Atr., Septum atriorum. 
S. V., Septum ventriculorum. 


ventricular septum meets the right side of the cushion-septum 
and divides the auricular canal, though the opening of the bulbus 
remains on its right. 

(c) The interauricular septum forms at the same time as the 
septum between the ventricles, as a thin myocardial partition 
arising from the vault of the atrium between the openings of the 
sinus venosus and pulmonary vein; it extends rapidly with con- 
cave free border towards the auricular canal, and soon fuses 


LATER DEVELOPMENT OF VASCULAR SYSTEM 300 


completely along its entire free border with the endothelial 
cushions of the latter. It would thus establish a complete par- 
tition between the two auricles were it not for the fact that 
secondary perforations arise in it before its free edge meets the 
endothelial cushions (Fig. 203). These have the same physio- 
logical significance as the fora- 
men ovale in the mammalian 
heart, and persist through the 
period of incubation, closing 
soon after hatching. 

(d) TheCushion-septum (Sep- 
tum of the Auricular Canal). 
This septum completes the en- 
tire system by uniting together 
the three septa already consid- 
ered. It forms as two cushion- 
like thickenings of the endothe- 
lium in the floor and roof  re- 
spectively of the auricular canal 
(ef. Figs. 202, 203 and 204). 
These cushions rapidly thicken 
so as to restrict the center of Fra. 203. — Reconstruction of the 


the atrioventricular aperture, heart of a chick embryo of 5.7 mm. 
and finally, fusing together, di- head-length, seen from right side. 


widelthe latter into two verti Part of the wall of the right auricle 
is cut away. (After Masius.) 


vally-elonge apertures, right ‘ 
cally elong ited apertures, right B. Co., Bulbus cordis. D.C., Duct 
and left respectively. The time of Cuvier. E. C. d., v., Dorsal and 

, : 2 : ventral endothelial cushions. O.S.v., 

“mé his large endo- . 
of 101 on on of this large endo Opening of the sinus venosus into the 
cardial cushion dividing the au- right auricle. O.1,0.2, Primary and 
ricular canal is coincident with secondary ostia or inter-auricular con- 
: nections. 
the formation of the other septa. 

(e) Completion of the Septa. Thus by the end of the fifth 
or the beginning of the sixth day of incubation, the heart is 
prepared for the rapid completion of a double circulation. The 
embryonic circulation is never completely double, however, for 
the reason that the embryonic respiratory organ (allantois) 
belongs to the aortic system, and full pulmonary circulation does 
not begin until after hatching. However, between the sixth 
and eighth days the right and left chambers of the heart become 
completely separated, except that the interauricular foramina 


306 THE DEVELOPMENT OF THE CHICK 


remain until hatching, and serve as a passageway of blood from 
the right side to the left side. 

The completion of the cardiac septa takes place in such a 
way that the aorta becomes connected with the left ventricle, 
the pulmonary artery remaining in connection with the right. 
To understand how this occurs it is necessary to remember that, 
although the bulbus arteriosus is primitively connected with the 
right side of the ventricle, the revolution of the latter has trans- 
ferred the bulbus to the middle line where it les to the right of 


Fic. 204. — Reconstruction of the heart of a 
chick embryo of 5.7 mm. head-length. Ven- 
tral face removed; interior of the dorsal 
half. (After Masius.) 

Atr.d.,s., Right and left auricles. D.C. 
d.,s., Right and left duets of Cuvier. E.C., 
Endothelial cushion. i. A.S., Interauricu- 
lar septum. M. V., Opening of the meatus 
venosus into the sinus. 8S. V., Sinus venosus. 
V.d.,s., Right and left ventricles. 


the interventricular septum, and ventral to the right division of 
the auricular canal. The bulbo-auricular ridge thus forms the 
floor of this side of the auricular canal. The interventricular 
septum is attached to the right side of the cushion-septum and 
its foramen and the aperture of the bulbus le side by side. It 
will also be remembered that the proximal portion of the bulbus 
is divided by a partition formed by right and left endocardial 


LATER DEVELOPMENT OF VASCULAR SYSTEM 307 


ridges, and that the aortic division of the bulbus lies above the 
pulmonary division, that is, next the bulbo-auricular ridge. 
The left bulbus ridge is thus continuous with the interventricular 
septum immediately beneath the foramen of the latter, and the 
right bulbus ridge lies on the opposite side. 

The bulbus septum now becomes complete by fusion of the 
right and left sides. The blood from the left ventricle is then 
forced in each systcle through the interventricular foramen and 
along a groove in the right side of the cushion-septum into the 
aortic trunk. This groove, however, is open to the right ven- 
tricle also above the septum of the bulbus; but it is soon bridged 
over by an extension of the cushion-septum along the bulbo- 
auricular ridge as far as the right side of the septum of the bulbus; 
in this way the space existing between the interventricular sep- 
tum and the opening of the aorta is converted into a tube, and 
thus the aorta is prolonged through the cushion-septum, and 
by way of the interventricular foramen into the left ventricle. 

Fate of the Bulbus. The distal portion of the bulbus is con- 
verted into the proximal parts of the aorta and pulmonary artery. 
The part proximal to the semilunar valves is gradually incor- 
porated into the ventricles, owing to extension of the ventricular 
cavities into its wall, and subsequent disappearance of the inner 
wall of the undermined part. 

The Sinus Venosus. (lor earlier development see Chap. VI; 
relation to septum transversum, Chap. XI.) 

In the course of development, the sinus venosus gradually 
separates from the septum transversum, though always connected 
with the latter by the vena cava inferior. In early stages (up to 
about 24 somites) it is placed quite symmetrically behind the 
atrium, and extends transversely to the entrance of the ducts of 
Cuvier on each side. The sinu-auricular aperture is approximately 
in the median line at first, so that the right and left divisions of 
the sinus are nearly symmetrical. The condition of approximate 
bilateral symmetry of the sinus is, however, rapidly changed 
by shifting of the sinu-auricular aperture to the right side with 
the outgrowth of the right auricle (24-36 somites); thus the left 
horn of the sinus becomes elongated; moreover, the main expan- 
sion of the sinus takes place in the region of the sinu-auricular 
aperture, and thus the left horn appears relatively narrow in diam- 
eter. The interauricular septum forms to the left of the sinu- 


308 THE DEVELOPMENT OF THE CHICK 


auricular aperture (Fig. 204). At the stage of ninety-six hours the 
general form of the sinus is that of a horseshoe situated between 
the atrium and the septum transversum; the ends of the horse- 
shoe, or horns of the sinus venosus, are continued into the ducts 
of Cuvier. The sinu-auricular aperture les on the right, and 
here the cavity of the sinus is largest; the right horn of the sinus 
is relatively short and the left horn forms a transverse piece on 
the anterior face of the septum transversum, which gradually 
curves dorsally and enters the left duct of Cuvier. 

The right and left boundaries of the sinu-auricular aperture 
project into the cavity of the right auricle as folds that meet 
below the aperture and diverge dorsally (ig. 204), thus forming 
sinu-auricular valves; a special development of the muscular 
trabecule running along the roof of the right auricle from the 
angle of these valves corresponds to the septum spurium of mam- 
malia. The sinus septum arises as a fold of the roof of the sinus 
between the entrance of the left horn and the vena cava inferior; 
it grows across the sinus into the sinu-auricular aperture and 
thus divides the latter (ef. Fig. 231). Subsequently, the sinus 
becomes incorporated in the right auricle, and the systemic 
veins thus obtain independent openings into the latter (see account 
of development of the venous system). The sinu-auricular 
ralves disappear during this process. 


Il. Tuer ARTERIAL SYSTEM 


The Aortic Arches. In the Amniota six aortic arches are 
formed connecting the truncus arteriosus with the roots of the 
dorsal aorta. The first four le in the corresponding visceral 
arches; the fifth and sixth are situated behind the fourth visceral 
pouch; the fifth is a very small and transitory vessel, the exist- 
ence of which was not suspected until comparatively recently 
(v. Bemmelen, Boas), and the sixth or pulmonary arch was pre- 
viously interpreted as the fifth. The discovery of the fifth arch 
has brought the Amniota into agreement with the Amphibia 
as regards the number and significance of the various aortic arches. 

The fate of the aortic arches in the chick is as follows (see 
Figs. 205, 206): the first and second arches disappear as already 
described (Chap. VI), and the anterior prolongation of the dorsal 
aorte in front of the third arch constitutes the internal carotid; 
the ventral ends of the first and second arches form the external 


LATER DEVELOPMENT OF VASCULAR SYSTEM 309 


carotid. The third arch on each side persists as the proximal 
portion of the internal carotids; and the dorsal aorta ruptures 
on each side between the dorsal ends of the third and fourth 
arches. The fourth arch and the root of the dorsal aorta dis- 
appear on the left side, but remain on the 
right as the permanent arch of the aorta. 
The fifth arch disappears on both sides; 
the sixth arch persists throughout the 
period of incubation and forms an im- 
portant arterial channel of the systemic 
circulation until hatching. Then the 
dorsal portion (duct of Botallus or duc- 
tus arteriosus) becomes occluded, and 
the remainder of the sixth arch becomes 
the proximal portion of the pulmonary 
arteries. 

The details of these changes are as 
follows: On the third and fourth days of 
incubation the first and second aortic 
arches disappear (Fig. 102). The lower 


ends of these arches then appear as a Fig. 205. — Diagram of 
branch from the base of the third arch the aortic arches of birds 
on each side, extending into the mandi- and their fate. (After 


Boas. ) 


es ae i Car. com., Common ca- 
tery. The dorsal aorta in front of the rotid. Car. ext., External 
third arch constitutes the beginning of carotid. Car. int., Internal 
: ; : : is earotid. D.a., Ductus ar- 
the internal carotid. During the fourth  teriosus. L., Left. p. A., 
: : 3 : ‘ > PS ESP aoe 
day the sixth pair of aortic arches is SS apa artery. R., 
cae P : : ight. 
formed behind the fourth cleft, and the 1, 2, 3, 4, 5, and 6, First, 
origin of the pulmonary arteries is trans- second, third, fourth, fifth, 
ar, a : ma es : and sixth aortic arches. 
ferred to them (Fig. 102). The fifth pair 


of aortic arches is also formed during the fourth day (Fig. 206.) 


ble and forming the external carotid ar- 


It is a slender vessel passing from near the base to near the 
summit of the sixth arch. As it has been entirely overlooked 
by most investigators, it is certain that it is of very brief duration. 
and it may even be entirely absent in some embryos. Apparently 
it has no physiological importance, and it can be interpreted only 
as a phylogenic rudiment. 

Thus at the beginning of the fifth day the entire series of 
aortic arches has been formed, and the first, second, and fifth 


300 THE DEVELOPMENT OF THE CHICK 


have entirely disappeared. The surviving arches are the third 
or carotid arch, the fourth or aortic arch, and the sixth or pul- 
monary arch. Up to this time the development is symmetrical 
on both sides of the body. 
During the fifth and = sixth 
days the two sides become 
asymmetrical, the fourth arch 
becoming reduced on the left 
side of the body and enlarged 
on the right. Fig. 207 shows 


the condition on the two sides 
Fig. 206. — Camera sketch of the aortic of the body on the sixth day. 
arches of the left side of a chick em- [Tf the fourth arch of the two 
bryo 44 days old. From an injected sides be compared it will be 
specimen. (After Locy.) : ; 
Abbreviations as in Fig. 205. seen that the left one is re- 
duced to a very narrow rudi- 

ment which has lost its connection with the bulbus arteriosus, 
while on the right side it is well developed. Another important 
change illustrated in the same figure is the reduction of the dorsal 
aorta between the upper ends of the carotid and aortic arches to 


& narrow connection. Two factors co-operate in the diminution 


Car ext 


Car com 


A 


Kia. 207. — Reconstruction of the aortic arches of a 6-day 
chick embryo from a series of sagittal sections. 
A. Left side. 
B. Right side. 
Car. com., Common earotid. Car. ext., External carotid. 
Car. int., Internal carotid. D.a., Duetus arteriosus. 


3, 4, and 6, Third, fourth, and sixth aortie arches. 

and gradual disappearance of this part of the primitive dorsal 
aorta, viz., the elongation of the neck and the reduction of the 
blood current. It will be seen that relatively little circulation 


is possible in this section, because the current up the carotid 


LATER DEVELOPMENT OF VASCULAR SYSTEM 361 


arch turns forward and that up the aortic arch turns backward, 
hence there is an intermediate region of stagnation, and here 
the obliteration occurs. 

On the eighth day the changes indicated on the sixth day 
are completed. The left aortic arch has entirely disappeared, 
and the connection between the upper ends of the carotid and 
aortic arches is entirely lost on both sides (Fig. 208), though lines 
of apparently degenerating cells can be seen between the two. 
On the other hand, the upper end of the pulmonary arch (duct 
of Botallus) is as strongly developed on both sides as_ the 
right aortic arch itself. The pulmonary artery proper is rela- 
tively very minute (Fig. 208), and it can transmit only a small 


C4, 


Fic. 208. — Reconstruction of the aortic arches of an 8-day embryo from 

a series of sagittal sections. 

A. Left side. 

B. Right side. 

A. o. m., Omphalomesenteric artery. Ao. A., Aortic (systemic) arch. 
Car., Carotid. D.a., Ductus arteriosus. d. Ao., Dorsal aorta. p. A., Pul- 
monary artery. S’cl., Subclavian artery. V., Valves of the pulmonary 
artery. 


quantity of blood; the principal function of the pulmonary arch 
is obviously in connection with the systemic circulation. In 
other words, both sides of the heart pump blood into the aorta 
during embryonic life; after hatching, the duct of Botallus be- 
comes occluded as already noted, and the pulmonary circulation 
is then fully established. 

The Carotid Arch. With the retreat of the heart into the 
thorax, the internal and external carotids become drawn out into 
lone vessels extending through the neck region. The internal 
carotids then become approximated beneath the vertebral centra. 
The stem of the external carotid forms an anastomosis with the 
internal carotid in the mandibular region, and then disappears, 


362 THE DEVELOPMENT OF THE CHICK 


so that its branches appear secondarily as branches of the inter- 
nal carotid. The common carotid (car. communis) of adult 
anatomy is derived entirely from the proximal part of the inter- 
nal carotid. 

The Subclavian Artery. The primary subclavian artery 
arises on the fourth day from the fifteenth (eighteenth of entire 
series) segmental artery of 
the body-wall when the 
wing-bud forms, and grad- 
ually increases in import- 
ance with the growth of the 
wing. During the fifth day 
a small artery that arises 
from the base of the carotid 
arch grows backwards and 
unites with the primary sub- 
clavian at the root of the 
wing. Thus the subclavian 
artery obtains two roots, a 
primary one from the dorsal 
aorta and a secondary one 
from the carotid arch (Fig. 
209). As the latter grows 
in importance the primary 
root dwindles and _ finally 
disappears (about the ninth 
day). Apparently the Cro- 
codilia and Chelonia agree 
with the birds in this re- 


Fic. 209. — Dissection of the heart and 
aortic arches of a chick embryo in the ; 
latter part of the sixth day of incuba- Spect, while the other ver- 
tion. (After Sabin.) tebrates retain the primary 

Au., Auricle. Car. com.,Common car- oot, 


otid. Sel. d., s., primary and secondary : 5 
subclavian artery. The Aortic System in- 


3, 4, 6, Third (carotid), fourth (system- cludes the aortic arch and 
ic), and sixth (pulmonary) arches. Sia Pea 
the primitive dorsal aorta 
with its branches (Fig. 216). 

The segmental arteries belong to the primitive dorsal aorta; 
originally there is a pair in each intersomitic septum, but their 
fate has not been thoroughly worked out in the chick. At six 
days the cervical segmental arteries are united on each side by 


LATER DEVELOPMENT OF VASCULAR SYSTEM 363 


a longitudinal anastomosis communicating with the internal 
carotid in front. 

The two omphalomesenteric arteries are originally independent 
(Chap. V), but as the dorsal mesentery forms, they fuse in a 
common stem extending to the umbilicus. The anterior mesen- 
teric artery arises from this. The coeliac and posterior mesen- 
teric arteries arise independently from the dorsal aorta (Fig. 216). 

Mesonephric arteries arise from the ventro-lateral face of the 
dorsal aorta and originally supply the glomeruli; they are very 
numerous at ninety-six hours, but become much reduced in 
number as the renal portal circulation develops; some of them 
persist as the definitive renal and genital arteries. 

The umbilical arteries arise from the same pair of segmental 
arteries that furnishes the primitive artery of the leg. Thus 
on the fourth day the umbilical arteries appear as branches of 
the sciatic arteries; but later the umbilical arteries become much 
larger than the sciatic (Fig. 216). The right umbilical artery is, 
from the first, smaller than the left. On the eighth day its inter- 
mediate portion in the region of the neck of the allantois is much 
constricted, and it gradually disappears. The caudal artery is 
the narrow posterior extremity of the dorsal aorta behind the 
umbilical arteries. 

I do not find a stage in the chick when the umbilical arteries unite 
directly with the dorsal aorta by way of the intestine and dorsal mesen- 
tery, though no doubt indirect connections exist at an early stage. In 
mammals (Hochstetter) the primitive umbilical artery has such a 
splanchnic course, but a secondary connection in the somatopleure soon 
replaces the primary splanchnic path. 


Il]. THe Venous System. (See Chapter VI for origin of the 
first venous trunks) 


We shall take up the development of the venous system in 
the following order: (a) the system of the anterior vene cave 
(venz cave superiores); (b) the omphalomesenteric and um- 
bilical veins and the hepatic portal system; (c) the system of the 
inferior vena cava. 

The anterior vene cave are formed on each side by the 
union of the jugular, vertebral, and subclavian veins. The jugular 
is derived from the anterior cardinal veins, which extend down 
the neck in close proximity to the vagus nerves. The embryonic 


364 THE DEVELOPMENT OF THE CHICK 


history of its branches is not known in detail (see Chap. VI and 
Fig. 162 for the first branches). The history of the vertebral 
veins, which open into the jugular veins near the base of the 
neck, formed by union of anterior and posterior branches, is 
likewise unknown. Presumably they are formed in part by 
anastomoses between segmental veins. The subclavian vein 
arises primitively as a branch of the posterior cardinal vein; 
it receives the blood from the wing and walls of the thorax. The 
part of the posterior cardinal behind the entrance of the sub- 
clavian vein disappears on the sixth day, and its most proximal 
part represents then the anterior continuation of the subclavian 
vein (Fig. 216). The part of the superior vena cava proximal 
to the union of jugular and subclavian veins is derived from the 
duct of Cuvier, and on the left side also from the left horn of 
the sinus venosus. 

The primitive omphalomesenteric veins unite behind the 
sinus venosus to form the meatus venosus, around which the 
substance of the liver develops as described in Chapters VI and 
X; the union extends back to the space between the anterior 
and posterior liver diverticula, where the omphalomesenteric 
veins diverge and pass out to the yolk-sae along the margins 
of the anterior intestinal portal (Fig. 210 A). In the latter part 
of the third day (84-36 somites) an anastomosis forms between 
the right and left omphalomesenteric veins above the intestine 
just behind the dorsal pancreas, and thus establishes a venous 
ring around the intestine, the upper portion of which is formed 
by the anastomosis, the lower portion by the meatus venosus, 
and the sides by the right and left omphalomesenteric veins 
respectively (Fig. 210 B). Even during the formation of this 
first venous ring it can be seen that its left side is becoming nar- 
rower than the right side, and in less than a day it disappears 
completely (Fig. 210C). Thus the blood brought in by the 
left omphalomesenteric vein now passes through the dorsal 
anastomosis to the right omphalomesenteric vein, and the latter 
alone connects with the meatus venosus. 

While this:is taking place (seventy-two to ninety-six hours) 
the intestine has elongated, the anterior intestinal portal has 
shifted backwards, and a second anastomosis is formed between 
the two omphalomesenteric veins ventral to the intestine and 
immediately in front of the intestinal portal (Fig. 210 D). Thus 


LATER DEVELOPMENT OF VASCULAR SYSTEM 365 


a second venous ring is established around the alimentary canal, 
the lower portion of which is formed by the second anastomosis, 


Fig. 210. — Diagrams illustrating the development of the hepatic 
portal circulation. (After Hochstetter.) 


A. About the fifty-eighth hour. 

B. About the sixty-fifth hour; first venous ring formed around 
the intestine. 

C. About the seventy-fifth hour; the left limb of the first ve- 
nous ring has disappeared. 

D. About the eightieth hour; the second venous ring is estab- 
lished. 

E. About the one hundredth hour; the right limb of the second 
venous ring has disappeared. 

F. Hepatic circulation about the one hundred and _ thirtieth 
hour, immediately before the disappearance of the intermediate 
portion of the meatus venosus. 

a.i.p., Anterior intestinal portal. D.C., Duct of Cuvier.  int., 
Intestine. M. V., Meatus venosus. (Es., (Esophagus. Pe., Pan- 
creas. St., Stomach. S. v., Sinus venosus. V. c¢. i., Vena cava 
inferior. V.h., Hepatic veins. V.o.m., Omphalomesenteric vein. 
v. r. 1, First venous ring. v.r. 2, Second venous ring. V. u. d., 
Right umbilical vein. V. u. s., Left umbilical vein. 


366 THE DEVELOPMENT OF THE CHICK 


the upper portion by the first anastomosis, and the sides by the 
right and left omphalomesenteric veins respectively. This ring 
is also soon destroyed, this time by the narrowing and disappear- 
ance of its right side (Fig. 210 E). 

Thus at about 100 hours the condition is as follows (Fig. 210 
Ek): the two omphalomesenteric veins unite to form a single trunk 
in front of the anterior intestinal portal and ventral to the intes- 
tine (second anastomosis), the single trunk then turns to the left 
(left side of second ring), passes forward and above the intestine 
to the right side (first or dorsal anastomosis), and then farther 
forward on the right side of the intestine (right side of first venous 
ring) to enter the liver, where it becomes continuous with the 
meatus venosus. 

The Hepatic Portal Circulation becomes established in the 
following manner: The meatus venosus is primarily a direct 
passageway through the liver to the sinus venosus (Fig. 210 C); 
but, as the liver trabeculz increase, more and more of the blood 
entering the meatus venosus is diverted into the vascular chan- 
nels or sinusoids that occupy the spaces between the trabecule. 
By degrees these secondary channels through the liver substance 
form two sets of vessels, an afferent one, branching out from 
the caudal portion of the meatus venosus, in which the blood 
is flowing into the hepatic sinusoids, and an efferent set branch- 
ing from the cephalic portion of the meatus venosus in which 
the blood is flowing from the hepatic sinusoids into the meatus 
(210 D and E). By degrees the circulation through the liver 
substance gains in importance, and liver trabeculze grow across 
the intermediate portion of the meatus venosus (six to seven 
days ef. Fig. 216), thus gradually occluding it as a direct path 
through the liver (Fig. 210 F). 

In this way there arises a set of afferent veins of the liver, 
branches of the omphalomesenteric or hepatic portal vein, and 
a set of efferent vessels which unite into right and left hepatic 
veins opening into the cephalic portion of the original meatus 
venosus. These veins begin to be differentiated after the one 
hundredth hour of incubation, and the disappearance of the 
intermediate portion of the meatus venosus as a direct route 
through the liver is completed on the seventh day. 

The original hepatic portal circulation is thus supplied mainly 
with blood from the yolk-sac. But on the fifth day the mesen- 


LATER DEVELOPMENT OF VASCULAR SYSTEM 367 


teric vein begins to form as a small vessel situated in the dorsal 
mesentery and opening into the omphalomesenteric vein behind 
the dorsal pancreas. This vein increases in importance as the 
development of the viscera proceeds, and becomes the definitive 
hepatic portal vein; it receives branches from the stomach, in- 
testine, pancreas, and spleen. The development of these branches 
proceeds pari passu with the development of the organs from 
which they arise, and does not require detailed description. It 
should be noted, however, that part of the veins from the giz- 
zard and proventriculus form an independent vena porta sinistra 
which enters the left lobe of the liver. 


A distinct subintestinal vein extends forward from the root of the 
tail at the stage of ninety-six hours to the posterior intestinal portal, 
where it opens into the branch of the left omphalomesenteric vein, 
that extends forward from the posterior end of the sinus terminalis. 
This vein appears to take up blood from the allantois at an early stage. 
However, it disappears at about the time when the umbilical vein be- 
comes the functional vein of the allantois. Originally it appears to 
open into symmetrical right and left branches of the omphalomesen- 
teric vein that encircles the splanchnic umbilicus. The right branch 
is, however, much reduced at ninety-six hours (ef. Hochstetter, 1888). 


The Umbilical Veins. The umbilical veins appear as vessels 
of the lateral body-wall opening into the ducts of Cuvier (Fig. 
210 C; ef. Fig. 117); at first they show anastomoses with the 
latter, which, however, soon disappear. They are subsequently 
prolonged backwards in the somatopleure along the lateral closing 
folds of the septum transversum (Chap. XI). Up to the end of 
the third day of incubation they have no direct connection with 
the blood-vessels of the allantois,and function only as veins of the 
body-wall. 

However, they obtain connection with the efferent vessels 
of the allantois during the fourth day, apparently by widening 
of parts of an intervening vascular network, and then the allan- 
toic blood streams through them to the heart. The right um- 
bilical vein disappears on the fourth day, and the left one alone 


persists. 
In the meantime the central ends of the umbilical veins have 
acquired new connections. (Middle of third day, Fig. 210 D.) 


This takes place through the formation of anastomoses, especially 
on the left side, between the umbilical vein and the hepatic 


368 THE DEVELOPMENT OF THE CHICK 


vessels. (On the right side similar connections appear, according 
to Brouha, but as the entire right umbilical vein soon degenerates 
they need not be considered farther.) The blood of the left um- 
bilical vein thus divides and part flows into the duct of Cuvier by 
way of the original termination, and part flows through the liver 
into the meatus venosus. The original connection is then lost 
and all of the blood of the umbilical vein flows through the liver 
into the meatus venosus. Although the intrahepatic part is 
at first composed of several channels, yet the blood of the um- 
bilical vein flows fairly directly into the meatus venosus, and 
thus takes no part in the hepatic portal circulation. On the 
eighth day the entrance of the umbilical vein into the cephalic 
part of the meatus venosus is still broken into several channels 
by liver trabecule (Fig. 182); these, however, soon disappear, 
and the vein then empties directly into the meatus venosus, which 
has in the meantime become the terminal part of the inferior 
vena cava. As the ventral body-wall closes, the umbilical vein 
comes to lie in the mid-ventral line, and in its course forward it 
passes from the body-wall in between the right and left lobes 
of the liver. The stem of the umbilical vein persists in the adult, 
as a vein of the ventral body-wall opening into the left hepatic 
vein. 

The System of the Inferior Vena Cava (Post-cava). The 
post-cava appears as a branch of the cephalic portion of the meatus 
venosus, and in its definitive condition the latter becomes its 
cephalic segment; thus the hepatic and umbilical veins appear 
secondarily as branches of the post-cava. The portion of the 
post-cava behind the liver arises from parts of the posteardinal 
and subeardinal veins, and receives all the blood of the posterior 
portion of the body and viscera, that does not flow through the 
hepatic portal system. The history of the development of this 
vein, therefore, involves an account of (1) the origin of its proxi- 
mal portion within the liver, and (2) of the transformation of the 
posteardinals and subeardinals. 

The proximal portion of the post-cava arises in part from 
certain of the hepatie sinusoids in the dorsal part of the liver 
on the right side at about the stage of ninety hours, and in part 
from a series of venous islands found at the same time in the 
caval fold of the plica mesogastrica (Figs. 211 and 212. See 
Chap. XI). As the caval fold fuses with the right dorsal lobe of 


LATER DEVELOPMENT OF VASCULAR SYSTEM 369 


the liver, the venous islands flow together and establish a venous 
trunk extending along and within the right dorsal lobe of the 
liver, and opening anteriorly into the meatus venosus. At first 
the connection with the meatus venosus lies near the sinus veno- 
sus, but in later stages is some distance behind the latter. Behind 
the liver the dorsal attachment of the caval fold is to the ventral 
surface of the right mesonephros, and at this place the vena cava 
enters the mesonephros and connects with the subcardinal veins 
(cf. Fig. 182). 

The latter vessels arise as a series of venous islands on the 
median surface of the mesonephros and lateral to the aorta on 
each side. Such disconnected primordia are first evident at 


Dic:s: 
V.us 
Fig. 211. — A drawing of a wax reconstruction of 


the veins in the region of the liver of a sparrow 
embryo. Outline of the liver represented by 
broken lines. Dorsal view. (After Miller.) 
D. C. d., s., Right and left ducts of Cuvier. 
D. V., Duetus (meatus) venosus. 5S. V., Sinus 
venosus. V.c.i., Vena cava inferior. V.u.d.,s., 
Right and left umbilical veins. 


about the seventieth hour, and soon they run together to form 
a longitudinal vessel on each side, which has temporary direct 
connections with the postecardinals (Fig. 212), replaced after- 
wards (fifth day) by a renal portal circulation through the sub- 
stance of the mesonephros. As the subeardinal veins enlarge, 
they approach one another just behind the omphalomesenteric 
artery beneath the aorta and fuse together (sixth day, Fig. 213). 
In the meantime, the post-cava has become continuous with the 
anterior end of the right subeardinal (Fig. 213). 

The venous circulation is then as follows: The blood from 


370 THE DEVELOPMENT OF THE CHICK 


LATER DEVELOPMENT OF VASCULAR SYSTEM By At 


¢. Usc.d 
Nai V3.5. 


Fia. 213.— Reconstruction of the venous system of 

a chick of 5 days. Ventral view. (After Miller.) 

a., Mesonephric veins. <Ao., Aorta. A. se. s., Left 
sciatic vein. Other abbreviations as before. 


the right and left posteardinal veins passes through the vas- 
cular network of the mesonephros, and empties into the sub- 
cardinal veins, from which it flows into the vena cava inferior, 
and so through the meatus venosus to the heart. Prior to the 
sixth day, however, the greater portion of the blood in the pos- 


Fic. 212. — Reconstruction of the venous system of a chick of 90 hours, 
ventral view. (After Miller.) 
A. o. m., Omphalomesenterie artery. a. sc. s., Left sciatic artery. A. 
u. s., Left umbilical artery. b., Vessels enclosed within ventral side of meso- 
nephros. V.c. p. d., s., Right and left posterior cardinal veins. YV. c¢. 1., 
Vena cava inferior. V. sc. d., s., Right and left subeardinal veins. 


3/2 THE DEVELOPMENT OF THE CHICK 


terior cardinals passes forward to the ducts of Cuvier without 
entering the mesonephric circulation. On the fifth and sixth 
days the cephalic ends of the posteardinals gradually dwindle 
and disappear (cf. Fig. 216); thus all of the blood entering the 
posteardinals must pass through the mesonephros to the sub- 
‘ardinals, which thus become efferent vessels of the mesonephros; 
and a complete renal-portal circulation is established. 

This form of circulation continues during the period of func- 
tional activity of the mesonephroi, and as the latter gradually 
atrophy, the portions of the subeardinals posterior to the anas- 
tomosis gradually disappear. A direct connection between the 
post- and subcardinals is then established on each side, by way 
of the great renal veins, which have in the meantime formed in 
connection with the development of the kidney (Fig. 214). 

The crural and ischiadic veins have, in the meantime, developed 
in connection with the formation of the hind limbs, as branches 
of the posteardinals. Thus the hinder portion of the latter be- 
comes transformed into the common iliac veins, and at the hinder 
end the posteardinals form an anastomosis (Tig. 214). 


IV. THe EMBRYONIC CIRCULATION 


On the fourth day the blood is driven into the roots of the 
dorsal aorta through three pairs of aortic arches, viz., the third 
or carotid, the fourth or aortic, and the sixth or pulmonary. The 
fifth pair of aortic arches is also functional for a time during this 
day, but soon disappears. The blood passing up the third or 
carotid arch is directed forward through the internal and external 
carotid arteries to the head; that passing up the fourth and 
sixth arches turns backwards to enter the dorsal aorta, so that 
there is an intermediate area of stagnation in the roots of the 
dorsal aorta between the carotid and aortic arches; though this 
is more or less problematical, the arrangement of the vessels ren- 
ders such a condition very probable. A very small proportion of 
the blood enters the rudimentary pulmonary arteries from the 
sixth arch. The blood in the dorsal aorta passes backwards and 
enters (1) the segmental arteries, (2) the omphalomesenteric 
arteries, (3) the (rudimentary) umbilical arteries, and behind 
the latter passes into the narrow continuation of the dorsal aorte, 
still separate in this region, known as the caudal arteries. 

The blood is returned to the heart through the sinus venosus 


LATER DEVELOPMENT OF VASCULAR SYSTEM 373 


— VPNs. 


Files, 


~ KC ps.(V22) 


Fic. 214. — Reconstruction of the venous system of a sparrow embryo, 
corresponding to a chick of about 14 days. (After Miller.) 
V. e.1. H., Intra-hepatie part of the vena cava inferior. V. e. i. SC 
Part of the vena cava inferior derived from the subeardinal vein. V. v. g 


Bo.) 
Genital veins. V.i. e. d., s., Right and left vena iliaca externa. V. i. 1, 
Vena iliaca interna. V.i. 1. d., s., Right and left vena intervertebralis lum- 


balis. V.r.m.d.,s., Right and left great renal veins. 


>) 


almost exclusively, the pulmonary veins being very rudimentary 
at this stage. The veins entering the sinus venosus are the ducts 
of Cuvier, and the meatus venosus. The former are made up 
on each side by (1) the anterior cardinal vein, returning blood 
from the head, (2) the posterior cardinal vein returning blood 
from the veins of the Wolffian body, and the intersomitie veins, 
(3) the umbilical veins returning blood mainly from the body- 


374 THE DEVELOPMENT OF THE CHICK 


wall, inasmuch as direct connection with the veins of the allantois 
is not yet established. The meatus venosus receives the omphalo- 
mesenteric veins, and the blood of the allantois by way of the 
subintestinal vein (the latter arrangement of very brief duration). 

Thus at this time all of the blood is mixed together in the 
sinus venosus, viz., that re- 
ceived through the ducts of 
Cuvier, presumably venous, 
and that received through 
the meatus venosus, pre- 
sumably arterial, owing to its 
circulation in the superficial 
vascular network of the yolk- 
sac. Apparently there is no 
arrangement for separation 
or discrimination in the re- 
distribution of the blood. 
But on the other hand it 
should be noted that most 


ric. 215. — Region of the bifureation of of the blood comes from the 
the post-cava in the adult fowl. Ven- 
tral view. (After Miller). 

A.m.s.(A. 0.m.), Omphalomesenteric ; ek 
artery. A.i.s., Left internal iliac artery. of the embryo at this time; 
Le i. Vena cava inferior. V. 1. ¢. d.. ond that the blood of the 
Right common iliac vein. V.i.e.d., Right ; 
external iliac vein. V.i.i.d., Right inter- embryo itself cannot be 
nal iliac vein. YV.i. Ll. s., Left vena in- hiplaree . 

' ; ughly venous owing to th 
tervertebralis lumbalis.  V. sr. s., Left aa s . ee the 
suprarenal vein. Vv. g., Genital veins. shortness of the circuit and 
Vy.r.m., Great renal veins. 


yolk-sac, owing to the slight 
development of the vessels 


the delicate nature of the 
embryonic tissues, which, no doubt, permit direct access of oxygen. 

On the sixth day the embryonic circulation enters on a second 
phase, owing to the changes in the structure of the heart and 
arrangement of the vessels described in detail in the preceding 
part of this chapter. 

On the eighth day the circulation is as follows: The right 
and left ventricles are completely separate, and the former 
pumps the blood into the pulmonary trunk, the latter into the 
aortic trunk. The carotid arteries arise from the base of the 
aortic arch and convey the blood to the head, and also, by way 
of the subelavians, to the walls of the thorax and to the wing. 
The left aortic arch has disappeared, and the right arch is con- 


LATER DEVELOPMENT OF VASCULAR SYSTEM 379 


tinuous with the dorsal aorta. The pulmonary trunk divides into 
right and left arches from which the small pulmonary artery is 
given off on each side, and the arch is continued without per- 
ceptible diminution in size as the ductus Botalli (ductus arteri- 
osus) to the dorsal aorta. Thus the greater quantity of blood 
pumped by both sides of the heart passes into the dorsal aorta 
by way of the right aortic arch, and the right and left ductus 
Botalli; but part of the blood from the left ventricle passes into 
the carotids. The main branches of the dorsal aorta are (1) 
ceeliac, distributed to stomach and liver mainly, (2) omphalo- 
mesenteric to the yolk-sac and mesentery, (3) right and left 
umbilical arteries (of which the left is much more important, the 
right soon disappearing), to the allantois and leg, (4) segmental 
arteries to the body-wall, (5) the caudal arteries. 

The anterior vene cave (former ducts of Cuvier) return the 
blood from the head, wing, and walls of the thorax to the right 
auricle; but owing to the formation of the sinus septum, the left 
vena cava opens directly into the right auricle to the left of the 
sinus valves, and the right one, also independently, to the right of 
the sinus valves. The proximal portion of the vena cava 
inferior is the original meatus venosus, and it receives the 
right and left hepatic veins, the last of which receives all the 
blood from the allantois through the umbilical vein (original 
left). 

There is also an hepatic portal and a renal portal circulation. 
The hepatic portal system is supplied with blood mainly from 
the yolk-sac, but also from the veins of the alimentary canal by 
the mesenteric vein; the latter is a relatively unimportant vessel 
at eight days, but grows in importance and becomes the entire 
hepatic portal vein after absorption of the yolk-sac. The hepatic 
portal vein branches within the liver into a system of capillaries 
which reunite to form the right and left hepatic veins. Thus 
all the absorbed nutrient material passes through the capillaries 
of the liver, where certain constituents are no doubt acted on 
in some important, but little understood, way. 

The renal portal circulation persists through the period of 
functional activity of the mesonephros. The afferent vein is 
the posterior cardinal which is supplied by the segmental veins 
and the veins of the leg and tail. The blood flows through the 
capillaries of the mesonephros into the subeardinal veins, and 


376 THE DEVELOPMENT OF THE CHICK 


hence to the vena cava inferior. With the degeneration of the 
mesonephros, the subeardinals disappear in large part and the 
posteardinals then empty directly into the vena cava inferior 
by way of the renal veins, which have formed in the meantime. 
The embryonic renal portal system of birds is similar in all essen- 
tial respects to the permanent system of amphibia and consti- 
tutes a striking example of recapitulation. The left auricle of 
the heart receives the small pulmonary veins. 

Thus practically all of the blood is returned to the right auricle 
of the heart; a considerable part of it is diverted into the left 
auricle through the foramina in the septum atriorum, and thus 
the blood reaches both ventricles. Complete systems of valves 
prevent its regurgitation in any direction. 

It is an interesting question to what extent the different kinds 
of blood received by the right auricle remain separate and receive 
special distribution through the body. The blood poured in by 
the anterior ven cave is purely venous, and it seems probable 
from the arrangement of the sinus valves that it passes into the 
ventricle of the same side, and so into the pulmonary arch and 
through the ductus Botalli into the dorsal aorta, and thus in part 
at least to the allantois where it is oxygenated. The blood coming 
in through the posterior vena cava is purified and rich in nutrition, 
for part of it comes from the allantois, where it has been oxygen- 
ated, and part has passed through the renal portal circulation, 
where, no doubt, it has been purified of nitrogenous excretory 
matter, and the remainder is mostly from the yolk-sac and hence 
laden with nutrition. This blood appears to be diverted through 
the foramen of the septum atriorum into the left auricle, and 
thence to the left ventricle, and so out into the carotids and 
aortic arch. It would seem, therefore, to be reasonably certain 
that the carotids receive the purest and most nutritious blood, 
for the blood in the dorsal aorta is mixed with the blood from 
the right ventricle. There can be no reasonable doubt that the 
heart is a more effective organ for separate and effective distribu- 
tion of the various kinds of blood received by it than this account 
would indicate. But further investigation is necessary to deter- 
mine in what ways and to what extent this takes place. 

At the time of hatching the following changes take place: 
the umbilical arteries and vein are obliterated in the allantois, 
owing to drying up of the latter; their stems remaining as relatively 


Fig. 216. — Diagram of the relations of the main splanchnic blood vessels 


on the sixth day of incubation. 


A. c., Coeliac artery. Adv., Vena advehens. All., Allantois. A.m., Mes- 
enteric artery. <Ao., Aorta. A. o. m., Omphalomesenteric artery. A. p., 
Pulmonary artery. A.sc., Sciatic artery. A.u. d., Right umbilical artery. 
A. u. s., Left umbilical artery. A. V., Vitelline arteries. Car. int., Internal 
carotid. Car. ext., External carotid. Cl., Cloaca. D.a., Ductus arteriosus. 
D. V., Ductus (meatus) venosus. Int., Intestine. J. e., External jugular 
vein. J. i., Internal jugular vein. Li., Liver. Scl., Subclavian artery. V. 
ce. a., Anterior vena cava. V. c. i., Inferior Vena cava. V. c. p., Posterior 
cardinal vein. V.m., Mesenteric vein. V. 0. m., Omphalomesenteric vein. 
Vp., Pulmonary vein. V.s’c., Subeardinal vein. V. s’cl., Subclavian vein. 
V. u. (s.), Umbilical vein (left). V. V., Vitelline vein. W. B., Wolffian 
body. Y.S., Yolk-sac. Y. St., Yolk-stalk. 


LATER DEVELOPMENT OF VASCULAR SYSTEM 377 


insignificant vessels. The veins of the yolk-sac likewise disap- 
pear. The ductus arteriosus (Botalli) is obliterated on both 
sides, and becomes a solid cord uniting the pulmonary arteries 
and arch of the aorta. Thus the blood from the right ventricle 
is driven into the lungs, and the pulmonary artery enlarges. 
The foramina in the septum atriorium gradually close, and so a 
complete double circulation is established. The right auricle 
receives all the systemic (venous blood), which is then driven 
through the lungs by way of the pulmonary artery, and returned 
in an oxygenated condition through the pulmonary veins to 
the left auricle; thence to the left ventricle and out through the 
aorta into the systemic circulation again. 


CHAPTER XIII 
THE URINOGENITAL SYSTEM 


Tue history of the pronephros and the origin of the meso- 
nephros have been already described (Chap. V). We have now 
to consider (1) the later history of the mesonephros, (2) the 
development of the metanephros or permanent kidney, (3) the 
development of the reproductive organs and their ducts, and 
(4) the development of the suprarenals. All these organs form 
an embryological unit, by virtue of their mode of origin and their 
interrelations. Thus we find that the intermediate cell-mass is 
significant for the development of all: its growth causes the forma- 
tion of the Wolffian body, on the median face of which the gonads 
arise. The secreting tubules and renal corpuscles of the perma- 
nent kidney are also derivatives of the intermediate cell-mass. 
The Wolffian duct is derived from the same source, and by change 
of function becomes the vas deferens, after functioning for a while 
as the excretory duct of the mesonephros. Certain parts of the 
mesonephros also enter into the construction of the testis. And 
the Millerian duct, which forms the oviduct of the female, is 
derived from the epithelium covering the Wolffian body. 


I. Tuer Larter History oF THE MESONEPHROS 


In Chapter VI we traced the origin of the nephrogenous 
tissue, and the differentiation of the first mesonephric tubules 
within it. We saw that in each of the segments concerned a 
number of balls of cells arises by condensation within the neph- 
rogenous tissue, and that these become converted into vesicles. 
We saw also that each vesicle sends out a tubular sprout from 
its lateral side to the Wolffian duct, with which it unites; and 
that its median face becomes converted into a renal corpuscle. 
These processes take place sucessively in antero-posterior order 
within the somites concerned, so that a series of stages in the 
development of the tubules may be studied in the same embryo. 
Moreover, all the tubules of a given somite do not develop simul- 

378 


THE URINOGENITAL SYSTEM 379 


taneously: primary tubules are formed in each somite from the 
most ventral portion of the nephrogenous tissue; then secondary 
tubules later from an intermediate portion, and tertiary tubules 
later yet from the dorsal portion. 

Fig. 217 represents a transverse section through the middle 


7S. 


Ze Vm. 


Fic. 217. — Transverse section through the middle of the 
Wolffian body of a chick embryo of 96 hours. 


Ao., Aorta. Coel., Coelome. Col. T., Collecting tubule. 
Glom., Glomerulus. germ. Ep., Germinal epithelium. M_’s’t., 
Mesentery. n.t., Nephrogenous tissue. T. 1, 2,3, Primary, 
secondary, and tertiary mesonephric tubules. V. ce. p., Pos- 
terior cardinal vein. W. D., Wolffian duct. 


of the Wolffian body at the stage of ninety-six hours, showing a 
primary, secondary, and tertiary tubule. The primary tubule 
is typically differentiated; the secondary has formed the secreting 
tubule and the rudiment of the renal corpuscle, but the tubule 
does not yet open into the Wolffian duct, though it is connected 
with it; the tertiary tubule is still in the vesicular stage. Some 
undifferentiated nephrogenous tissue remains above the rudi- 
ment of the tertiary tubule, which makes it possible that quar- 
ternary tubules may be formed later. 

Referring still to the same figure, it will be noted that the 
Wolffian duct itself has formed a considerable evagination dorso- 
medially (collecting tubule), with which both secondary and 
tertiary tubules are associated as well as the undifferentiated 
nephrogenous tissue. Similar evaginations are formed along 
the entire length of the functional portion of the mesonephros. 


380 THE DEVELOPMENT OF THE CHICK 


Higs. 218 and 219 illustrate the form of these evaginations in 
duck embryos of 40 and 50 somites respectively, as they appear 
in reconstructions of the posterior portion of the mesonephros. 


It will be seen that they gradually 
form sacs opening into the Wolffian 
duct. Subsequently, by elongating, 
these sacs form collecting tubules 
that gather up the secretions of the 
mesonephric tubules proper and con- 
duct them to the Wolffian duet. 
These conducting tubules are stated 
to branch more or less; it is also 
said that they are more highly de- 
veloped in the duck than in the chick. 
Felix proposes to call them meso- 
nephrie ureters. 

In the case of the secondary and 
tertiary tubules, three parts may be 
distinguished: parts one and two (de- 
rived from the nephrogenous tissue) 
are the renal corpuscle and secreting 
tubule respectively; the third part is 
the collecting tubule derived by 
evagination from the Wolffian duct. 
In the case of the primary tubules, 
a conducting part appears to be 
formed secondarily, though in what 
Way is not clear. 

The formation of new tubules 
ceases on the fifth day, all the ne- 
phrogenous tissue being then used 
up. Up to the eighth day at least 
the tubules grow rapidly in length 
and become more differentiated. The 
result is a relatively enormous  pro- 
trusion into the body-cavity on each 
side of the dorsal mesentery.  De- 
generation of the tubules sets in 
about the tenth or eleventh days, 
and the tissue is gradually absorbed; 


THE URINOGENITAL SYSTEM dsl 


this process extends over the whole of the latter period of incu- 
bation, and is completed at hatching. Parts, however, remain 
in the male in connection with the testis; non-functional remnants 


Kia. 219. — Profile reconstruction of part of the 
mesonephros and diverticulum of the ureter of 
aduck embryo of 50 somites. (After Schreiner.) 

Cl., Cloaca. Int., Intestine. Mn. T., Meso- 
nephric tubules. n. T., Nephrogenous tissue. 

Ur., Ureter. W. D.. Wolffian duct. 

XXXII, XX XIII, XXXIV, Somites of the 


same number. 


may also be detected in the female (p. 401). It is difficult to 
state the exact period of beginning and cessation of function of 
the mesonephric tubules. Judging from the histological appear- 


Fic. 218. — Profile reconstruction of part of the Wolffian duet and primordia 
of mesonephric tubules (represented by circles) of a duck embryo of 45 
somites. (After Schreiner.) 


XXIV, XX/V, ete., position of the corresponding somites. Lines 114 A, 
114 B, 114, represent the positions of the sections shown in these figures. 


382 THE DEVELOPMENT OF THE CHICK 


ances, however, it is probable that secretion begins in the tubules 
on the fifth day and increases in amount up to the eleventh day 
at least, when signs of degeneration become numerous. Presuma- 
bly the functional activity diminishes from this stage on, being 
replaced by the secretion of the permanent kidney. 


Fig. 220. — Transverse section through the mesonephros 
and neighboring parts of a 6-day chick, in the region of 
the spleen. 

Ao., Aorta. bl. V., Blood vessels (sinusoids). Caps., Cap- 
sule of renal corpuscle. Coel., Coelome. col. T., Collecting 
tubule. D., Dorsal.  Giz., Gizzard. Glom., Glomerulus. 
Gon., Gonad. L., Left. Spl., Spleen. Sr. C., Cortical sub- 
stance of the suprarenal. s. t., Seereting tubule. T. R., 
Tubal ridge. V., Ventral. V. e. p., Posterior cardinal vein 
V.s’e. 1., Left subeardinal vein. W. D., Wolffian duct. 


Figs. 220 and 221 represent sections through the mesonephros 
on the sixth and eighth days respectively (see also Vig. 222, 
eleven days). The renal corpuscles show the typical capsule 
and glomerulus, and relation to the secreting tubules. The latter 
are considerably convoluted on the sixth day, much more so on 
the eighth day. The conducting tubules can usually be distin- 
guished by their smaller caliber and thinner walls. The Wolffian 


THE URINOGENITAL SYSTEM 383 


duct is situated near the dorso-lateral edge of the mesonephros, 
and the opening of a collecting tubule into it is shown in Figure 
220. The renal corpuscles are situated next the median face of 
the Wolffian body. The space between the tubules is occupied 


LOZ. 


Fic. 221.— Transverse section through the metanephros, mesonephros, 
gonads and neighboring parts of an 8-day chick. 


bl. v., Blood vessels (sinusoids). B. W., Body-wall. col. T. M’t’n., 
Collecting tubules of the metanephros. M. D., Miillerian duct. M’s’t., Mesen- 
tery. n. t. 1. z., Inner zone of nephrogenous tissue (metanephric). n. t. o. 
z., Outer zone of the nephrogenous tissue. Symp. Gn., Sympathetic gang- 
lion of the twenty-first spinal ganglion. V.C., Centrum of vertebra. Other 
abbreviations as before. 


almost entirely by a wide vascular network of sinusoidal char- 
acter; that is, the endothelial walls of the vessels are moulded 
directly on the basement membrane of the tubules without any 
intervening connective tissue. The circulation is described in the 
chapter on the vascular system. 


384 THE DEVELOPMENT OF THE CHICK 


Il. Tue DEVELOPMENT OF THE METANEPHROS OR PERMANENT 
KIDNEY 


The metanephros or permanent kidney supplants the meso- 
nephros in the course of development. It is derived from two 
distinct embryonic primordia: (1) the nephrogenous tissue of 
the two or three posterior somites of the trunk (31 or 32 to 33), 
which furnish the material out of which the renal corpuscles 
and secreting tubules develop; and (2) a diverticulum of the 
posterior portion of the Wolffian duct (Fig. 219), which develops 
by branching into the collecting tubules and definitive ureter. 
The development of the kidney takes place in a mass of mesen- 
chyme, known as the outer zone of the metanephrogenous tissue, 
that furnishes the capsule and connective tissue elements of 
the definitive kidney, in which also the vascular supply is developed 
(Figs. 221 and 222). The cortical tubules of the kidney are 
thus derived mainly from the nephrogenous tissue, and the medul- 
lary tubules and ureter from the metanephric diverticulum. 

Thus the definitive kidney is analogous in mode of develop- 
ment to the mesonephros, and is best interpreted as its serial 
homologue. This point of view may be regarded as definitely 
established by the work of Schreiner, to which the reader is re- 
ferred for a full account of the history of the subject. 

The metanephric diverticulum, or primordium of the ureter 
and collecting tubules, arises about the end of the fourth day as 
a rather broad diverticulum of the Wolfhan duct at the convexity 
of its terminal bend to the cloaca (Fig. 219). It grows out 
dorsally, forming a little sac, which, however, soon begins to grow 
forward median to the posterior cardinal vein and dorsal to the 
mesonephros (Fig. 224); by the end of the fifth day its anterior 
end has reached the level of the czecal appendages of the intes- 
tine, and on the eighth day its anterior end has reached its defin- 
itive position at the level of the vena cava inferior, near to the 
anterior end of the mesonephros (twenty-first definitive somite or 
twenty-fifth of the entire series; cf. Fig. 150). 

It should be noted that the metanephric diverticulum is similar 
in its mode of origin to the so-called mesonephric ureters. It 
may in fact be regarded as the posterior member of this series, 
but it is separated from those that form the collecting tubules of 
the mesonephros by at least two somites in which no diverticula 


THE URINOGENITAL SYSTEM OSD 


of the mesonephros are formed (Fig. 219). During its growth 
forward a series of small diverticula arise from its wall and extend 
dorsally (Fig. 223); these branch secondarily in a generally dichot- 


t 


oe Pi > 


ole as 
Ke) 
WV, 


Fig. 222.— Transverse section through the metanephros, mesonephros, 
gonads and neighboring structures of an 11-day male chick. 

a. A.S., Abdominal air-sac. Ao., Aorta. B. W., Body-wall. Coel., Coe- 
lome. Giz., Gizzard. I]., ium. M. D., Remains of degenerating Miillerian 
duct. M/’s’t., Mesentery. M’t’n., Metanephros. Sp., Spine of neural arch. 
tr. Pr., Transverse process of the neural arch. V. ¢. i., Vena cava inferior. 
W. D., Wolffian duct. Other abbreviations as before. 


386 


THE DEVELOPMENT OF THE CHICK 


Via. 223. — Profile reconstruction of the Wolffian 
duct and primordium of the metanephros of a 
chick embryo of 6 days and 8 hours. (After 
Schreiner.) 

XXV to XXXIII, twenty-fifth to thirty-third 
somites. Al. N., Neck of allantois. Cl., Cloaea. 
Int., Intestine. M’s’n., Mesonephros. n. T., 
Nephrogenous tissue of the metanephros include: 
within the dotted lines. W. D., Wolffian duct. 
Ur., Ureter. 


THE URINOGENITAL SYSTEM 387 


omous manner, and it is from them that the collecting tubules 
of the kidney arise; the posterior unbranched portion of the meta- 
nephric diverticulum represents the definitive ureter. 

The following data concerning these branches should be noted: 
(1) the first ones are formed from the posterior portion of the 
metanephric diverticulum, and the process progresses in an 
anterior direction. This is the reverse direction of the usual order 
of embryonic differentiation, but the reason for the order is the 
same, viz., that differentiation begins in the first formed parts. 
(2) A posterior, smaller group of collecting tubules is separated 
at first by an unbranched portion of the ureter from an anterior 
larger group (Fig. 223). The unbranched region corresponds to 
the position of the umbilical arteries which cross here. (3) During 
the fifth and sixth days the terminal portion of the Wolffian 
duct common to both mesonephros and metanephros is gradually 
drawn into the cloaca, and thus the ureter obtains an opening 
into the cloaca independent of the Wolffian duct and_ posterior 
to 1 (Mig. 223). 

The Nephrogenous Tissue of the Metanephros. The nephro- 
genous tissue of the thirty-first, thirty-second, and thirty-third 
somites is at first continuous with the mesonephros (Figs. 218 
and 219), but on the fourth and fifth days that portion situated 
immediately behind the mesonephros degenerates, thus leading 
to a complete separation of the most posterior portion situated 
in the neighborhood of the metanephric diverticulum. This con- 
stitutes the metanephrogenous tissue proper (inner zone). It is 
important to understand thoroughly its relations to the metane- 
phric diverticulum. ‘This is indicated in Fig. 219, which repre- 
sents a graphic reconstruction of these parts in a duck embryo 
of 50 somites. It will be seen that the metanephrogenous tissue 
covers nearly the entire metanephric diverticulum; a transverse 
section (Fig. 224) shows that it lies on its median side. The 
outer dotted line (Fig. 219) gives the contour of a dense portion 
of mesenchyme related to the diverticulum and nephrogenous 
tissue proper. In section this forms a rather ill-defined area 
shading into the nephrogenous tissue on the one hand and into 
the surrounding mesenchyme on the other. 

Fig. 224 shows the relations of the three constituent elements 
of the kidney at the end of the fifth day, as seen in a transverse 
section. The metanephric diverticulum lies on the median side 


388 THE DEVELOPMENT OF THE CHICK 


of the cardinal vein, and is in contact, on its median face, with 
the proper nephrogenous tissue (inner zone); the latter shades 
into the outer zone, the cells of which are arranged concentrically 
with reference to the other parts. The relations subsequently 
established may be summarized in a few words; the inner zone 
of tissue grows and branches part passu with the growth and 
branching of the metanephric diverticulum, so that the termina- 
tion of every collecting tubule is accompanied by a portion of 


mete te 
y Cru 
ON 


Fic. 224.— Transverse section through the 
ureter and metanephrogenous tissue of a 
5-day chick. 

A.umb., Umbilical artery. Coel., Coelome. 
M’s’t., Mesentery. n.t.i.z., Inner zone of the 
nephrogenous tissue. n. t. 0. z., Outer zone of 
the nephrogenous tissue. Ur., Ureter. V.c.p., 
Posterior cardinal vein. W.D., Wolffian duct. 


the inner zone, which is, however, always distinct from it. This 
conclusion is established by the fact that from the start the two 
elements, collecting tubules and inner zone, are distinct and 
may be traced continuously through every stage. The outer 
zone differentiates in advance of the two more essential con- 
stituents at all stages, and thus forms a rather thick investment 
for them. 

The formation of the secreting tubules from the inner zone 


THE URINOGENITAL SYSTEM 389 


Via. 225. — Sections of the embryonic metanephros of the chick 
to show developing tubules. (After Schreiner.) 


A. Nephric vesicle or primordium of secreting tubule (ur. t.) 
and collecting tubule (col. T.); 9 days and 4 hours. 

B. Elongation of nephrie vesicle; same embryo. 

C. Indication of renal corpuscle at the distal end of the 
forming tubule. 

D. The secreting tubule appears S-shaped. 

E. Secreting tubule well formed; 9 days and 21 hours. 

I’. Secreting tubule opening into collecting tubule; 11 days. 


390 THE DEVELOPMENT OF THE CHICK 


of the metanephrogenous tissue takes place in essentially the 
same manner as the formation of the mesonephric tubules. The 
first stages may be found in seven and eight-day chicks in the 
portion of the kidney behind the umbilical arteries. The inner 
zone tissue begins to arrange itself in the form of minute balls 
of cells in immediate contact with the secreting tubules; a small 
lumen then arises within the ball, transforming it into a thick- 
walled epithelial vesicle with radially arranged cells. The vesicle 
then elongates away from the collecting tubule and gradually 
takes on an S-shape. The distal end of the S becomes con- 
verted into a renal corpuscle as illustrated in Figure 225, 
and the proximal end fuses with the wall of the collecting tubule; 
an opening is then formed between the two. 

On the eleventh day of incubation, secreting tubules are thus 
formed throughout the entire length of the kidney; but the histo- 
logical structure does not yet give the effect of an actively secret- 
ing gland, although degeneration of the mesonephros has already 
begun. The full development of the nephric tubules in the 
chick has not been studied. 

At all stages in its development the kidney substance is 
separated from the mesonephros by a distinct layer of undiffer- 
entiated mesenchyme, which is, however, at certain times ex- 
tremely thin. But there is no evidence that at any time elements 
of the mesonephros, e.g., undifferentiated nephrogenous tissue, 
extend up into the metanephric primordium which so closely 
overlies it (ef. Figs. 221 and 222). 

The kidney is entirely retroperitoneal in its formation, and 
its primary capsule is established by differentiation of the periph- 
ery of the outer zone. This may be seen in process at eleven 
days (Fig. 222): the primary capsule is definitely established on 
its median and lateral sides; but is defective dorsally and at the 
angle next the aorta. With the subsequent degeneration of the 
mesonephros, and projection of the kidney into the ccelome, 
its ventral surface acquires a secondary peritoneal capsule. 


III]. Tur OrGans or REPRODUCTION 


The gonads are laid down on the median surface, and the 
ducts on the lateral surface of the Wolffian body, which thus 
becomes converted into a urinogenital ridge. The composition 
of the urinogenital ridge is at first the same in all embryos, whether 


THE URINOGENITAL SYSTEM 391 


destined to become male or female. It has three divisions: 
(1) the anterior or sexual division, containing the gonad, involves 
about the anterior half of the Wolffian body; (2) a non-sexual 
region of the Wolffian body occurs behind the gonad, and 
(3) behind the Wolffian body itself the urinogenital ridge con- 
tains only the Wolffian and Miillerian ducts. A transverse sec- 
tion through the anterior division shows the following relations 
(Fig. 221): on the median surface the gonad, on the lateral sur- 
face near the dorsal angle of the body-cavity the Wolffian and 
Miillerian ducts, the latter external and dorsal to the former: 
between the gonad and ducts lie the tubules of the Wolffian 
body destined to degenerate for the most part. 

There is an indifferent stage of the reproductive system 
during which the sex of the embryo cannot be determined, either 
by the structure of the gonad or the degree or mode of develop- 
ment of the ducts. In those embryos that become males the 
gonad develops into a testis, the Wolffian duct becomes the vas 
deferens, the tubules of the anterior part of the Wolffian body 
become the epididymis, those of the non-sexual part degenerate, 
leaving a rudiment known as the paradidymis, and the Miullerian 
duct becomes rudimentary or disappears. In embryos that be- 
come females, the gonad develops into an ovary; the Wolffian duct 
disappears or becomes rudimentary, the Miullerian duct develops 
into the oviduct on the left side and disappears on the right side, 
and the tubules of the Wolffian body degenerate, excepting that 
functionless homologues of the epididymis and paradidymis per- 
sist, known as the epodphoron and paroophoron respectively. 

It is not correct to state, as is sometimes done, that the 
embryo is primitively hermaphrodite, for, though the ducts char- 
acteristic of both sexes develop equally in all embryos, the primi- 
tive gonad is, typically, only indifferent. Nevertheless, if the 
gonad be physiologically as well as morphologically indifferent 
in its primitive condition, the possibility of an hermaphrodite 
development is given. The primitive embryonic conditions 
appear to furnish a basis for any degree of development of the 
organs of both sexes. 

Development of Ovary and Testis. Indijjerent Period. The 
reproductive cells of ovary and testis alike arise from a strip 
of peritoneal epithelium, known as the germinal epithelium, 
which is differentiated on the fourth day by its greater thickness 


392 THE DEVELOPMENT OF THE CHICK 


and absence of a basement membrane from the adjacent peri- 
toneum (Fig. 217). The germinal epithelium les between the 
base of the mesentery and the mesonephros at first, but as the 
latter grows and projects into the body-cavity the germinal 
epithelium is drawn on to its median surface. It is difficult to 
determine its antero-posterior extent in early stages; it begins 
near the point of origin of the omphalomesenteric arteries, and 
its posterior termination is indefinite, but it certainly extends 
over seven or eight somites. 

Two kinds of cells are found in the germinal epithelium, viz., 
the ordinary peritoneal cells and primitive ova. The latter are 
typically round, and several times as large as the peritoneal 
cells (Figs. 226 and 227); the cytoplasm is clear and the nucleus 
contains one or two nucleoli; they are sharply distinguishable 
from the peritoneal cells in most cases, and they may be traced 
through a continuous series of later developmental stages into 
the ova and spermatozoa. The origin of these primitive ova is 
therefore a matter of considerable interest. 

Two views have been held: (1) that they are derived from 
the peritoneal cells, and (2) that they have an independent history 
antecedent to the differentiation of a germinal epithelium, repre- 
senting in fact undifferentiated embryonic cells that reach the 
germinal epithelium by migration from their original source. In 
support of the latter hypothesis the observations of Hoffmann may 
be cited, who has found cells indistinguishable from primitive ova 
in embryos of Hzematopus, Sterna paradisea, and Gallinula, at 
a stage of 23 somites, embedded in the mesoderm, mesenchyme, 
and even the entoderm of the splanchnopleure. (See also Nuss- 
baum, 1901.) Transitional cells were not found. On the other 
hand, in the germinal epithelium itself, transitional stages between 
the primitive ova and the ordinary peritoneal cells are frequent 
in jater stages (Semon). The embryos of birds are not well 
adapted for the solution of this puzzling question; but in some 
reptiles and selachia and other vertebrates primitive ova have 
been traced from a very early stage of the embryo through various 
migrations to the germinal epithelium. On comparative and 
theoretical grounds, the view of the independent origin of the 
primitive ova is preferable; but the origin of some at least from 
the peritoneal epithelium cannot be disproved for the chick. 

Two other constituents enter into the composition of the 


THE URINOGENITAL SYSTEM 393 


indifferent gonad, viz., the stroma cells and the sexual cords 
(segmental or genital cords). The stroma is formed from mesen- 
chyme situated internal to the germinal epithelium. It is a 
very narrow layer at first, and is formed, in part at least, by pro- 
liferation of the germinal epithelium itself, in the same manner 
as mesenchyme is formed elsewhere by proliferation from the 
mesoderm. The stroma of the gonad is separated from the tubules 


Fig. 226. — Cross-section through the genital primordium of Limosa xgo- 
cephala. (After Hoffmann, from Felix and Bihler.) 
The stage is similar to that of a chick embryo of 44 days. 
Germ., Germinal epithelium. Mst., Mesentery. 8. C., Sexual cords. 
V., Posterior cardinal vein. W..D., Wolffian duct. 


of the Wolffian body by the numerous blood-vessels on the me- 
dian aspect of the latter. Up to the middle of the period of 
incubation, and a little later, it is extremely sparse; it increases 
subsequently as a result of ingrowth of the blood-vessels and 
accompanying connective tissue. 


394 THE DEVELOPMENT OF THE CHICK 


The sexual cords appear within the gonad on the fifth day; 
they are solid cords of epithelial cells that fill up the interior 
of the gonad and cause it to protrude from the surface of the 
Wolffian body (Fig. 226); the cords extend from the germinal 
epithelium, with which they may be in contact, towards the hilum 
of the gonad (represented at this time by the broad surface 
opposed to the Wolffian body), and into the Wolffian body where 
they enter into close connection with the renal corpuscles. In 
the Wolffian body and intermediate zone they are very irregular 
in their course and connected by numerous anastomoses, corre- 
sponding to the rete region of the future testis. Strands of these 
cells pass dorsally, and, according to some authors, form the 
cortical cords of the suprarenal capsules (Fig. 226). 

The following views of the origin of the sexual cords in birds 
have been held: (1) That they arise as outgrowths of the capsules 
of renal corpuscles (Hoffmann, Semon) and the neck of the 
Wolffian tubules also (Semon); (2) that they are ingrowths of 
the germinal epithelium (Janosik); (3) that they differentiate 
from the stroma (Prenant). The subject is a somewhat difficult 
and complicated one, but the view that the sexual cords arise 
as outgrowths of the capsules of renal corpuscles appears to be 
the best substantiated, and brings the birds into line, in this 
respect, with the reptiles and amphibia. Hoffmann’s observa- 
tion that the sexual cords le at first on the lateral side of the 
blood-vessels intervening between the germinal epithelium and 
the Wolffian body, and that the cells of the sexual cords are 
directly continuous with those of the capsules, should be con- 
clusive. If the cords arose from the germinal epithelium and 
grew secondarily through the stroma into the Wolfhan body, 
there should be a stage when they occur exclusively median to 
the blood-vessels intervening between the germinal epithelium 
and the Wolffian body; but such does not appear to be the case. 
The relation of the sexual cords to renal corpuscles, germinal 
epithelium, and suprarenal capsules in Limosa eegocephala is well 
shown in Fig. 226. 

Sexual Differentiation. The period of morphological indiffer- 
ence of the gonad is relatively long and the actual sexual differ- 
entiation appears slowly. It manifests itself (1) in differences in 
the behavior of the germinal epithelium; (2) of the sexual cords; 
(3) larger size of the left ovary and ultimate disappearance of the 


THE URINOGENITAL SYSTEM 3995 


right one; (4) behavior of the stroma, particularly the albuginea. 
According to Semon the nature of the gonad may be detected on 
the fifth, or, at the latest, on the sixth day, by the fact that the 
right ovary is already much smaller than the left, owing to the 
more rapid growth of the latter. Although the right testis 
frequently develops more slowly than the left, the difference is 
not so great as in the case of the ovary. In Grallatores and Nata- 
tores, according to Hoffmann, retrogression of the right ovary 
does not begin until shortly before hatching. 

Histological differentiation manifests itself first in the ger- 
minal epithelium and sexual cords. In the males the germinal 
epithelium never attains as great thickness as in the females, 
and the sexual cords are much better developed and the stroma 
therefore less abundant than in the females. It is impossible 
to tell from the literature just how early these differentiating 
characters become decisive; but it is between the sixth and 
eighth days. 

Development of the Testis. We have seen that, during the 
indifferent period, the primitive ova multiply in the germinal 
epithelium; small groups may thus be formed, and such groups, 
or single primitive ova, soon appear in the stroma and in the 
sexual cords (Fig. 227). Their appearance in these situations 
is attributed to migration, and not neo-formation in situ for 
the following reasons: (1) The primitive ova are found in the 
germinal epithelium before they appear either in the stroma or 
sexual cords; (2) the boundary between the germinal epithelium 
and the stroma is not sharp, and both ordinary epithelial cells 
and primitive ova are found in intermediate positions before 
they appear in the stroma and sexual cords; (3) the primitive 
ova in the stroma and in the sexual cords are precisely like those 
originally found in the germinal epithelium; (4) the sexual cords 
have no basement membrane in early stages, and primitive ova 
may be found in the margin of the cords. 

By this process of migration. then, the primitive ova leave 
the germinal epithelium and pass either directly or through the 
stroma into the sexual cords, which thus come to be composed 
of two kinds of cells, viz., the epithelial cells and the primitive 
ova (Fig. 227). This process appears to go on until about the 
end of the second week of incubation. The sexual cords increase 
in number very rapidly and become closely pressed together so as 


396 THE DEVELOPMENT OF THE CHICK 


to almost eliminate the stroma, a condition that lasts up to the 
twelfth day, at least, after which the quantity of the stroma 
increases again with the ingrowth and enlargement of the 
blood-vessels. 

As the testis increases in size it projects more from the surface 
of the Wolffian body, and folds arise above and below it as well 
as in front and behind, that progressively narrow the surface 


Fig, 227. — Section through the gonad of a chick in the middle of the fifth 
day. Indifferent stage. The sexual cords have reached the germinal 
epithelium; the primitive ova are appearing in the cords. (After Semon.) 


e T, Connective tissue. germ. Ep., Germinal epithelium. M. ep., 
Epithelium of the mesentery. pr. O., Primitive ova. s. C., Sexual cords. 


of apposition, which in this way becomes gradually reduced to 
form the hilum of the testis, through which the sexual cords pass 
to the neighboring renal corpuscles (ef. Figs. 221 and 222). 

As the testis is attached to the anterior portion of the Wolffian 
body, the latter may be divided in two portions, an anterior 


THE URINOGENITAL SYSTEM 397 


sexual and a posterior non-sexual portion. In the latter part of 
the period of incubation the non-sexual portion undergoes absorp- 
tion while the anterior portion becomes converted into the epididy- 
mis. 

The increase of primitive ova in the germinal epithelium and 
their migration into the sexual cords continues until about the four- 
teenth day. In the meantime the stroma has increased notably 
in amount; it constitutes a considerable layer between the cords, 


Fic. 228. — Cross-section through the periphery of the testis of a 
just hatched chick. (After Semon.) The sexual cords have 
acquired a lumen, and the walls of the canals are formed of the 
primitive ova and the cells of the sexual cords, or supporting 
cells. The connective tissue forms septulze, connecting with the 
albuginea; the remains of the germinal epithelium form the serous 
covering of the testis. 

Alb., Albuginea. ce. T., Connective tissue of the septule testis. 
1., Lumen of the sexual cords. pr. O., Primitive ova. - s. C., Sexual 
cord. 
and begins now to form a layer between the germinal epithelium 
and the distal ends of the sexual cords. This layer forms the 
albuginea of the testis, and with its establishment the production 
of the primitive ova from the germinal epithelium ceases, and the 
latter becomes reduced to an endothelial layer (Fig. 228). 


398 THE DEVELOPMENT OF THE CHICK 


During this period the sexual cords become converted into 
the semeniferous tubules, rete, and vasa efferentia; and the 
sexual tubules of the Wolffian body into the epididymis. About 
the end of the third week the sexual cords obtain a lumen, owing 
to rearrangement of the cells; at the same time a basement mem- 
brane appears over the outer ends of the cells, and the semenif- 
erous tubules are definitely established (Fig. 228). In these 
one can easily recognize the descendants of the primitive ova 
which may now be called spermatogonia, and the epithelial or 
supporting cells. The irregularly anastomosing sexual cords in 
the region of the hilus become the rete cords, which acquire a 
lumen shortly after hatching. The rete cords are united to the 
neighboring renal corpuscles by the original strands and these 
form the vasa efferentia. 

As regards the formation of the epididymis: the renal corpuscles 
of the Wolfhan tubules concerned diminish in size, the glom- 
erulus disappears and the cells of the capsule become cylindrical. 
These changes progress from the lateral side of the Wolffian 
body towards the testis; that is to say, the more lateral corpuscles 
are first affected. A rudiment of the non-sexual part of the 
Wolffian body persists in the mesorchium of the male, between 
testis and kidney. It is known as the paradidymis. 

Development of the Ovary. (There is no complete account of 
the development of the ovary in the chick; the following account 
is based on Hoffmann’s description of Grallatores and Natatores.) 

The right ovary may attain a considerable size; but sooner 
or later it degenerates and is never functional; moreover, its 
growth does not follow a normal course of differentiation. The 
description applies, therefore, only to the left ovary. 

In the indifferent gonad, primitive ova leave the germinal 
epithelium and enter the stroma and sexual cords at corresponding 
stages of development whether the organ is to become ovary or 
testis. Such, however, in the case of the ovary, are destined to 
degenerate, along with the sexual cords. The definitive ova 
are derived from primitive ova that have remained within the 
germinal epithelium. 

The characteristic feature of the development of the ovary 
is, then, a cessation of migration of primitive ova from the 
germinal epithelium after a certain stage and a multiplication 
in situ. The epithelial cells of the germinal epithelium share in 


THE URINOGENITAL SYSTEM 399 


this multiplication and the consequence is a great increase in 
thickness. At the same time the sexual cords cease to grow, 
and become converted into tubes with a wide lumen, and low 
epithelium; and the stroma increases notably in amount. The 
inner surface of the germinal epithelium, or ovigerous layer of 
the ovary, then begins to form low irregular projections into the 
stroma, or the latter begins to penetrate the ovigerous layer at 
irregular distances so as to produce elevations. This condition 
is well illustrated in Fig. 229. 


Fic. 229. — Cross-section of the ovary of a young embryo of Numenius 
arcuatus. (After Hoffmann.) 


bl. v., Blood-vessel. germ. Ep., Germinal epithelium. r., Mesonephric 
canals (rete ovarii). s.¢., Sexual cord. 


In the course of development the ovigerous layer continually 
increases in thickness, and the projections into the stroma form 
veritable cords of ovigerous tissue, which correspond to the 
cords of Pfliiger in the mammalian ovary. The cords carry 
the primitive ova with them. The surface of the ovary also 
begins to become lobulated by the extension of the stroma tra- 
becule. Successive stages in the growth and differentiation of 
the primitive ova occur from the surface towards the inner ends 
of the ovigerous strands. Fig. 230 represents a section through 
the ovary of a fledgling of Numenius acuatus three or four days 


400 THE DEVELOPMENT OF THE CHICK 


old. The germinal epithelium covers the surface and is continu- 
ous with the ovigerous strands projecting far into the stroma. 
The strands are broken up in the stroma into nests of cells; 
next the germinal epithelium are found characteristic primi- 
tive ova, but in deeper situations the primitive ova are larger 
and each is accompanied by a group of epithelial cells, which are 
distinctly differentiated as granulosa cells of young follicles in 


Car Li 7.) 


Fig. 230. — Cross-section of the ovary of a fledgling of Numenius ar- 
cuatus 3-4 days old. The germinal epithelium is below. (After 
Hoffmann. ) 

s. ¢., Sexual cords. 


the deepest. Thus the young follicles arise by separation of 
nests of cells from the ovigerous strands within the stroma; 
each nest includes a young ovocyte and a group of epithelial 
cells which arrange themselves in a single layer of cuboidal cells 
around the ovocyte. On each side of the free border of the ovary 
the embryonic state persists, and it is not known whether this 


THE URINOGENITAL SYSTEM 401 


condition is maintained permanently, as in some reptiles, or 
not. 

The atrophy of the Wolffian body is much more complete in 
the female than in the male; no part of it remains in a functional 
condition, but the part corresponding to the epididymis of the 
male remains as a rudiment, known as the epodphoron. It has 
almost the same structure in young females as in young males, 
but the sexual cords uniting it with the ovary do not become 
tubular, nor does the rete ovarii. A rudiment of the non-sexual 
part of the Wolffian body is also found in the hen between ovary 
and kidney in the lateral part of the mesovarium; it has been 
named the paroophoron. 

Development of the Genital Ducts. Vhe Wolffian Duct. The 
origin and connections of the Wolffian ducts have been already 
sufficiently described. In the male they are connected with the 
semeniferous tubules by way of the rete, vasa efferentia, and 
epididymis, and function as vasa deferentia exclusively, after 
degeneration of the mesonephros. Subsequently they become 
somewhat convoluted, acquire muscular walls and a slight ter- 
minal dilatation. The details of these changes are not described in 
the literature. In the female the Wolffian duct degenerates; at 
what time is not stated in the literature, but presumably along 
with the Wolffian body. 

The Miillerian Duct. The Miullerian duct, or oviduct, is laid 
down symmetrically on both sides in both male and female em- 
bryos; subsequently both right and left Millerian ducts degen- 
erate in the male; in the female the right duct degenerates, the 
left only remaining as the functional oviduct. We have now to 
consider, therefore, (1) the origin of the ducts during the in- 
different stage, and (2) their subsequent history in the male 
and in the female. 

The origin of the Millerian duct is preceded by the formation 
of a strip of thickened peritoneum on the lateral and superior 
face of the Wolffian body extending all the way to the cloaca 
(cf. Fig. 220). This strip, which may be called the tubal ridge, 
appears first at the anterior end of the Wolffian body on the 
fourth day, and rapidly differentiates backwards; it lies imme- 
diately external to the Wolffian duct. The anterior part of the 
Miillerian duct arises as a groove-like invagination of the tubal 
ridge at the cephalic end of the Wolffian body immediately 


402 THE DEVELOPMENT OF THE CHICK 


behind the external glomeruli of the pronephros. The lips of 
this groove then approach and fuse on the fifth day, so as to form 
a tube which soon separates from the ridge. This process, how- 
ever, takes place in such a way as to leave the anterior end of 
the tube open and this constitutes the ccelomic aperture of the 
oviduct, or ostium tube abdominale. Moreover, the closure of 
the groove does not take place uniformly, and one or two open- 
ings into the Millerian duct usually occur near the ostium on 
the fifth day. Typically, however, these soon close up, though 
persistence of one of them may lead, as a rather rare abnormality, 
to the occurrence of two ostia in the adult. There is no ground 
for the view (see Balfour and Sedgwick) that the two or three 
openings into the anterior end of the Miillerian duct correspond 
to nephrostomes of the pronephros; they are situated too far 
posteriorly and laterally to bear such an interpretation. 

The anterior part of the Millerian duct is thus formed by 
folding from the epithelium of the tubal ridge; it constitutes a 
short epithelial tube situated between the Wolffian duct and the 
tubal ridge, ending blindly behind. The part thus formed is rela- 
tively short; the major portion is formed by elongation of the 
anterior part, which slowly grows backwards between the Wolffian 
duct and the tubal ridge, reaching the cloaca on the seventh day. 
The growing point is solid and appears to act like a wedge sepa- 
rating the Wolffian duct and the tubal ridge, being thus closely 
pressed against both, but apparently without receiving cells from 
either. Balfour’s view, that it grows by splitting off from the 
Wolffian duct or at the expense of cells contributed by the latter, 
has not been supported by subsequent investigators. A short 
distance in front of the growing point the Miillerian duct receives 
a lumen, and mesenchyme presses in from above and_ below, 
and forms a tunic of concentrically arranged cells around it 
(Fig. 221). 

The Miillerian duet thus begins to project above the surface 
of the Wolffian body, and, as it does so, the thickened epithelium 
of the tubal ridge becomes flat and similar to the adjacent peri- 
toneum; whether it is used up in the formation of the mesen- 
chymatous tunie of the epithelial Millerian duct is not known. 
Up to this time the development is similar in both sexes and on 
both sides of the body. 

In the male development of these ducts ceases on the eighth 


THE URINOGENITAL SYSTEM 403 


day; retrogression begins immediately and is completed, or at 
any rate far advanced, on the eleventh day. In this process the 
epithelial wall disappears first, and its place is taken by cells 
of mesenchymatous appearance, though it is not known that 
transformation of one kind into the other takes place. Retro- 
gression begins posteriorly and proceeds in the direction of the 
head; the ostium is the last to disappear. The mesenchymatous 
tunic shares in the process, so that the ridge is no longer found 
(see Fig. 222). In the male the Miillerian ducts never open into 
the cloaca. 

In the female the development of the right Miillerian duct 
ceases after the eighth day, and it soon begins to degenerate. Its 
lumen disappears and it becomes relatively shorter, so that its 
anterior end appears to slip back along the Wolffian body. On 
the fifteenth day slight traces remain along its former course and 
a small cavity in the region of the cloaca. It never obtains an 
opening into the cloaca (Gasser.) 

With the degeneration of the anterior end of the Wolffian 
body the ostium tubz abdominale comes to be attached by a 
ligament to the body-wall (Fig. 231); farther back the ligamen- 
tous attachment is to the Wolffian body. 

The fimbriz begin to develop on the eighth day on both 
sides in both sexes. It is only in the left oviduct of the female, 
however, that development proceeds farther, and differentiation 
into ostium, glandular part, and shell gland takes place. This 
appears distinctly about the twelfth day. The lower end ex- 
pands to form the primordium of the shell-gland at this time, 
but does not open into the cloaca. Indeed, the opening is not 
established until after the hen is six months old (Gasser.) 


IV. THe SUPRARENAL CAPSULES 


The suprarenals of the hen are situated medial to the anterior 
lobe of the kidney, in the neighborhood of the gonad and vena 
cava inferior. They have a length of about 8-10 mm. The 
substance consists of two kinds of cords of cells, known respect- 
ively as cortical and medullary cords, irregularly intermingled; 
the so-called cortical cords make up the bulk of the substance, 
and the medullary cords occur in the meshes of the cortical cords. 
The terminology does not, therefore, describe well the topo- 
graphical arrangement of the components; it was derived from 


404 THE DEVELOPMENT OF THE CHICK 


the condition found in many mammals, the cortical cords of the 
birds corresponding to the cortical substance, and the medullary 
cords to the medullary substance of mammals. The medullary 
cords are often called phaochrome or chromaffin tissue on account 
of the specific reaction of the constituent cells to chromic acid, 
and their supposed genetic relation to tissue of similar composition 
and reaction found in the carotid glands and other organs asso- 
ciated with the sympathetic system. 


hig. 231. — Photograph of a cross-section of an embryo of 8 days through the 


ostia tubs abdominalia. 


a. ALS., Neck of abdominal air-sac. O. T. a., Ostium tube abdominale. 
M’s’t. uc., Accessory mesentery. pl. C. r., 1., Right and left pleural cavities. 
Rec. pn. ent. r., Right pneumato-enteric recess. V. ¢e. a. 1., Left anterior 
vena cava. R., rib. Other abbreviations as before. 


The embryonic history has been the subject of numerous 
investigations, and has proved a particularly difficult topic, if 
we are to judge from the variety of views propounded. Thus 
for instance it has been maintained at various times: (1) that 


THE URINOGENITAL SYSTEM 405 


cortical and medullary cords have a common origin from the 
mesenchyme; (2) that they have a common origin from the 
peritoneal epithelium; (3) that the origin of the cortical and 
medullary cords is absolutely distinct, the former being derived 
from the sexual cords by way of the capsules of the renal cor- 
puscles and the latter from the sympathetic ganglia; (4) that 
their origin is distinct, but that the cortical cords are derived 
from ingrowths of the peritoneum, and the medullary cords from 
sympathetic ganglia. The first view may be said now to be 
definitely abandoned, and no one has definitely advocated a 
common epithelial origin since Janosik (1883). Thus it may 
be regarded as well established that the two components have 
diverse origins, and it seems to the writer that the fourth view 
above is the best supported. (See Poll and Soulié.) The com- 
parative embryological investigations, strongly support this view. 

Origin of the Cortical Cords. According to Soulié, the 
cortical cords arise as proliferations of a special suprarenal zone 
of the peritoneum adjacent to the anterior and dorsal part of 
the germinal epithelium. This zone is distinguishable early on 
the fourth day, and begins about half a millimeter behind the 
glomeruli of the pronephros, extending about a millimeter in a 
‘caudal direction. Proliferations of the peritoneal epithelium are 
formed in this zone, and soon become detached as groups of epi- 
thelial cells lying in the mesenchyme between the anterior end 
of the Wolffian body and the aorta. Such proliferation continues 
up to about the one hundredth hour or a little later, and a second 
stage in the development of the cortical cords then begins: The 
y and fill the space on the medio-dorsal aspect 
of the Wolffian body, and then come secondarily into relation 


cords grow rapid 


with the renal corpuscles of the latter and the sexual cords. 

According to Semon and Hoffmann the relation thus estab- 
lished is a primary one, that is to say, that the cortical cords 
arise from the same outgrowths of the capsules of the renal cor- 
puscles that furnish the sexual cords. Rabl agrees essentially 
with Soulié, and it seems probable that Semon and Hoffmann 
have overlooked the first stages in the origin of the cortical cords 
of the suprarenal corpuscles. 

During the fifth, sixth, and seventh days there is a very 
rapid increase of the cortical cords accompanied by a definite 
circumscription of the organ from the surrounding mesenchyme ; 


406 THE DEVELOPMENT OF THE CHICK 


however, no capsule is formed yet. The topography of the organ 
on the eighth day is shown in Figs. 150 and 182... Whereas during 
the fourth, fifth, and sixth days the arrangement of the cortical 
cells is in masses rather than in cords, on the eighth day the 
cords are well developed, in form cylindrical with radiating cells, 
but no central lumen. The organ has become vascular, and the 
vsesels have the form of sinusoids, ¢.e., they are moulded on the 
surface of the cords with no intervening mesenchyme. 

Origin of the Medullary Cords. The medullary cords take 
their origin unquestionably from cells of the sympathetic ner- 
vous system. During the growth of the latter towards the mesen- 
tery, groups of sympathetic cells are early established on or near 
the dorso-median surface of the cortical cords (Fig. 226). The 
ingrowth of the sympathetic medullary cords does not, however, 
begin until about the eighth day. At this time there is a large 
sympathetic ganglionic mass on the dorso-median surface of the 
anterior end of the suprarenal, and stands of cells characterized 
sharply by their large vesicular nuclei and granular contents 
can be traced from the ganglion into the superficial part of the 
suprarenal. These cells are precisely like the specific cells of 
the ganglion, perhaps a little smaller, and without axones. On 
the eleventh day these strands have penetrated through a full 
third of the thickness of the suprarenal, and are still sharply 
characterized, on the one hand by their resemblance to the sym- 
pathetic ganglion cells, and on the other by their clear differen- 
tiation from the cells of the cortical cords. These occupy the 
relations characteristic of the differentiated medullary cords, and 
there can be little doubt that they develop into them. 


CHAPTER XIV 
THE SKELETON 


I. GENERAL 


From an embryological point of view, the bones of the body, 
their associated cartilages, the ligaments that unite them together 
in various ways, and the joints should be considered together, 
as they have a common origin from certain aggregations of 
mesenchyme. The main source of the latter is the series of 
sclerotomes, but most of the bones of the skull are derived from 
the unsegmented cephalic mesenchyme. 

Most of the bones of the body pass through three stages in 
their embryonic development: (1) a membranous or prechondral 
stage, (2) a cartilaginous stage, (8) the stage of ossification. 
Such bones are known as cartilage bones, for the reason that 
they are preformed in cartilage. Many (see p. 433 for list) of 
the bones of the skull, the clavicles and the uncinate processes of 
the ribs do not pass through the stage of cartilage, but ossifica- 
tion takes place directly in the membrane; these are known as 
membrane or covering bones. The ontogenetic stages of bone 
formation parallel the phylogenetic stages, membrane preceding 
cartilage, and the latter preceding bone in the taxonomic series. 
Thus, in Amphioxus, the skeleton (excluding the notochord) 
is membranous; in the lamprey eel it is partly membranous and 
partly cartilaginous; in the selachia it is mainly cartilaginous; in 
higher forms bone replaces cartilage to a greater or less degree. 
The comparative study of membrane bones indicates that they 
were primitively of dermal origin, and only secondarily grafted 
on to the underlying cartilage to strengthen it. Thus the ear- 
tilage bones belong to an older category than the membrane 
bones. 

The so-called membranous or prechondral stage of the skeleton 
is characterized simply by condensation of the mesenchyme. 
Such condensations arise at various times and places described 

407 


408 THE DEVELOPMENT OF THE CHICK 


beyond, and they often represent the primordia of several future 
bony elements. In such an area the cells are more closely aggre- 
gated, the intercellular spaces are therefore smaller, and the 
area stains more deeply than the surrounding mesenchyme. 
There are, of course, stages of condensation in each case, from 
the first vague and undefined areas shading off into the indifferent 
mesenchyme, up to the time of cartilage or bone formation, 
when the area is usually well defined. In most of the bones, 
however, the process is not uniform in all parts; the growing 
extremities may be in a membranous condition while cartilage 
formation is found in intermediate locations and ossification has 
begun in the original center of formation; so that all three stages 
may be found in the primordium of a single bone (e.g., scapula). 
Usually, however, the entire element is converted into cartilage 
before ossification begins. 

The formation of cartilage (chondrification) is brought about 
by the secretion of a homogeneous matrix of a quite special char- 
acter, which accumulates in the intercellular spaces, and thus 
gradually separates the cells; and the latter become enclosed in 
separate cavities of the matrix; when they multiply, new deposits 
of matrix form between the daughter cells and separate them. 
As the original membranous primordium becomes converted into 
‘artilage, the superficial cells flatten over the surface of the 
‘artilage and form a membrane, the perichondrium, which be- 
comes the periosteum when ossification takes place. 

The process of ossification in cartilage involves the following 
stages in the chick: 

(1) Formation of Perichondral Bone. The perichondrium 
deposits a layer of bone on the surface of the cartilage near its 
center, thus forming a bony ring, which gradually lengthens into 
a hollow cylinder by extending towards the ends of the cartilage. 
This stage is well illustrated in Fig. 231 A and in the long bones 
of Fig. 242; the bones of the wing and leg furnish particularly 
good examples; the perichondral bone is naturally thickest in 
the center of the shaft and thins towards the extremity of the 
cartilages. 

(2) Absorption of Cartilage. The matrix softens in the 
center of the shaft and becomes mucous, thus liberating the 
cartilage cells and transforming the cartilage into the funda- 
mental tissue of the bone marrow. This begins about the tenth 


THE SKELETON 409 


day in the femur of the chick. The process extends towards the 
ends, and faster at the periphery of the cartilage (7.e., next to 
the perichondral bone) than in the center. In this way there 
remain two terminal, cone-shaped cartilages, and the ends of the 
cones project into the marrow cavity (Fig. 231 A). 

(3) Calcification of Cartilage. Salts of lime are deposited in 
the matrix of the cartilage at 
the ends of the marrow cavity; 
such cartilage is then removed VEN 
by osteoclasts, large multinu- poze 
cleated cells, of vascular en- 
dothelial origin, according to 
Brachet (seventeenth or eigh- 
teenth day of incubation). 

(4) Endochondral Ossifica- 
tion. Osteoblasts within the 
marrow cavity deposit bone on 
the surface of the rays of cal- 
cified cartilage that remain 
between the places eaten out 
by osteoclasts, and on the 
inner surface of the perichon- 


erie 0852 oats = oft Cort. 


dral bone. Fic. 231 A. — Longitudinal section of 
f le 96 ae) Shae 

These processes gradually the femur of a chick of 196 hours’ in 
cubation; semi-diagrammatic. (After 


extend towards the ends of 
Peat 1 tl Hi Brachet.) 
the bone, and there 1s never art. Cart., Articular cartilage. C.C., 


any independent epiphysial Calcified cartilage. end. B., Endochon- 
Pentortor Gscification anslonc dral bone. M., Marrow cavity. P’ch., 

Saabs Y“o  Perichondrium. P’os., Periosteum. 
bones of birds, as there is in p’os. B., Periosteal bone. Z. Gr., Zone 
of growth. Z. Pr., Zone of proliferation. 


mammals. The ends of the 7 R., Zone of resorption 
ane s : 


bones remain cartilaginous 
and provide for growth in length. Growth in diameter of the 
bones takes place from the periosteum, and is accompanied by 
enlargement of the marrow cavity, owing to simultaneous ab- 
sorption of the bone from within. It is thus obvious that all of 
the endochondral bone is removed from the shaft in course of 
time; some remains in the spongy ends. 

The details of the process of ossification will not be described 
here, and it only remains to emphasize a few points. At a stage 
shortly after the beginning of absorption of the cartilage in the 


410 THE DEVELOPMENT OF THE CHICK 


center of the shaft, the perichondral bone is invaded by capillary 
vessels and connective tissue that break through into the cavity 
formed by absorption; it 1s supposed by many that osteoblasts 
from the periosteum penetrate at the same time. The marrow 
of birds is derived, according to the best accounts, from the 
original cartilage cells, which form the fundamental substance, 
together with the intrusive blood-vessels and mesenchyme. The 
endochondral osteoblasts are believed by some to be of endo- 
chondral origin (7.e., derived from cartilage cells), by others of 
periosteal origin. For birds, the former view seems to be the 
best supported. | 

In birds. calcification does not precede absorption of the 
‘artilage, as it does in mammals, until the greater part of the 
marrow cavity is formed. The cones of cartilage, referred to 
above, that are continuous with the articular cartilages, are 
absorbed about ten days after hatching. 

On the whole, perichondral ossification plays a more extensive 
role in birds than in mammals. The endochondral bone forma- 
tion begins relatively much later and is less extensive. The 
bodies of the vertebrae, which ossify almost exclusively in an 
endochondral fashion, form the main exception to this rule. 

Ossification in membrane proceeds from bony spicules de- 
posited between the cells in the formative center of any given 
membrane bone. It spreads out from the center, the bony 
spicules forming a network of extreme delicacy and beauty. 
After a certain stage, the membrane bounding the surface becomes 
a periosteum which deposits bone in dense layers. Thus a mem- 
brane bone consists of superficial layers of dense bone, enclosing 
a spongy plate that represents the primitive bone before the 
establishment of the periosteum. 

The formation of bones proceeds from definite centers in all 
three stages of their formation; thus we have centers of mem- 
brane formation, centers of chondrification and centers of ossifi- 
cation. Membranous centers expand by peripheral growth, 
cartilage centers expand by the extension of cartilage formation 
in the membrane from the original center of chondrification, and 
bony centers expand in the original cartilage or membrane. 
Several centers of chondrification may arise in a single primitive 
membranous center; for instance, in the membranous stage, the 
skeleton of the fore-limb and pectoral girdle is absolutely con- 


THE SKELETON 411 


tinuous; cartilage centers then arise separately in different parts 
for each of the bones: similarly for the hind-limbs and _ pelvic 
girdle, etc. Separate centers of ossification may likewise appear 
in a continuous embryonic cartilage, as for instance, in the base 
of the skull or in the cartilaginous coraco-scapula, or ischio- 
ilium. Such centers may become separate bones or they may 
subsequently fuse together. In the latter case, they may repre- 
sent bones that were phylogenetically perfectly distinct elements, 
as for instance, the prootic, epiotic, and opisthotic centers in 
the cartilaginous otie capsule; or they may be of purely func- 
tional significance, as for instance, the separate ossifications in 
the sternum of birds, or the epiphysial and diaphysial ossifica- 
tions of the long bones of mammals. It is usually possible on 
the basis of comparative anatomy to distinguish these two cate- 
gories of ossification centers. 

Phylogenetic reduction of the skeleton is also usually indi- 
‘ated in some manner in the embryonic history. Where elements 
have completely disappeared in the phylogenic history, as for 
instance, the missing digits of birds, they often appear as mem- 
brane formations in the embryo, which then fade out without 
reaching the stage of cartilage; if the latter stage is reached the 
element usually fuses with some other and is therefore not really 
missing, e.g., elements of the carpus and tarsus of birds (though 
not all). But the ontogenetic reduction may go so far that 
the missing elements are never distinguishable at any stage of 
the embryonic history; thus, though the missing digits of birds 
are indicated in the membranous stage, their component phalanges 
are not indicated at all. 


Il. THE VERTEBRAL COLUMN 


The primordia of the vertebral column are the notochord 
and sclerotomes. The former is the primitive axial support of 
the body, both ontogenetically and phylogenetically. In both 
components, notochord and sclerotomes, we may recognize a 
cephalic and trunk portion. The notochord, as we have seen, 
extends far into the head, and the sclerotomes of the first four 
somites contribute to the formation of the occipital portion of 
the skull. The cephalic parts are dealt with in the development 
of the skull. The history of the notochord and sclerotomes will 
be considered together, but we may note in advance that the 


412 THE DEVELOPMENT OF THE CHICK 


notochord is destined to be completely replaced by the bodies of 
the vertebra, derived from the sclerotomes. 

The Sclerotomes and Vertebral Segmentation. The vertebral 
segmentation does not agree with the primitive divisions of the 
somites, but alternates with it; or in other words, the centers 
of the vertebrae do not coincide with the centers of the original 
somites, but with the intersomitiec septa in which the segmental 
arteries run. Thus each myotome extends over half of two 
vertebral segments, and the spinal ganglia and nerves tend to 
alternate with the vertebra. It therefore happens that each myo- 
tome exerts traction on two vertebra, obviously an advantageous 
arrangement, and the spinal nerves lie opposite the intervertebral 
foramina. 

This arrangement is brought about by the development of 
each vertebra from the caudal half of one sclerotome and the 
cephalic half of the sclerotome immediately behind; parts of 
two somites enter into the composition of each vertebra, as is 
very obvious at an early stage: Fig. 232 represents a section 
through the base of the tail of a chick embryo of ninety-six hours; 
it is approximately frontal, but is inclined ventro-dorsally from 
behind forwards. The original somites are indicated by the 
myotomes and the segmental arteries. In the region of the 
notochord one can plainly distinguish three parts to each 
sclerotome, viz., (1) a narrow, median, or perichordal part 
abutting on the notochord, in which no divisions occur either 
within or between somites; (2) a caudal lateral division distin- 
guished by the denser aggregation of the cells from (3) the cephalic 
division. Between the caudal and cephalic divisions of the sclero- 
tome is a fissure (intervertebral fissure) which marks the boundary 
of the future vertebre. Each vertebra in fact arises from the 
caudal component of one sclerotome and the cephalic component 
of the sclerotome immediately behind. Between adjacent sclero- 
tomes is the intersomitie septum containing the segmental artery. 
If one follows these conditions back into successively earlier stages, 
one finds that the intervertebral fissure arises from the primitive 
somitie cavity, and that the distinction between caudal and 
cephalic divisions of the sclerotome is marked continuously from a 
very early stage by the presence of the intervertebral fissure and 
the greater density of the caudal division, 7.e., the cephalic com- 
ponent of each definitive vertebra. 


THE SKELETON 


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Fic. 232.— Frontal section through the base of the tail of a chick 


embryo of 96 hours. The anterior end of the section (above 
in the figure) is at a higher plane than the posterior end. 


caud. Sel., Caudal division of the sclerotome. ceph. Sel., Ce- 
phalie division of the sclerotome. Derm., Dermatome. Ep., Epi- 
dermis. Gn., Ganglion. int’s. F., Intersomitic fissure. int’v. F., 
Intervertebral fissure. My., Myotome. N’ch., Notochord. N. Rs 


Neural tube. per’ch. Sh., Perichordal sheath. s. A., Segmental 
artery. 


413 


414 THE DEVELOPMENT OF THE CHICK 


Now, if one follows these components as they appear at suc- 
cessively higher levels in such a frontal section as Fig. 232, one 
finds that the perichordal layer disappears in the region of the 
neural tube, and that the spinal ganglia appear in the cephalic 
division of the sclerotome, and almost completely replace it. 
Thus the caudal division of the sclerotome is more extensive, as 
well as denser, than the cephalic division. 

In transverse sections one finds that the sclerotomic mesen- 
chyme spreads towards the middle line and tends to fill all the 
interspaces between the notochord and neural tube, on the one 
hand, and the myotomes on the other. But there is no time at 
which the sclerotome tissue of successive somites forms a con- 
tinuous unsegmented mass in which the vertebral segmentation 
appears secondarily, as maintained by Froriep, except in the thin 
perichondal layer; on the contrary, successive sclerotomes and 
vertebral components may be continuously distinguished, except 
in the perichordal layer; and the fusion of caudal and cephalic 
sclerotome halves to form single vertebree may be continuously 
followed. Thus, although the segmentation of the vertebre is 
with reference to the myotomes and ganglia, it is dependent 
upon separation of original sclerotome halves, and not secondarily 
produced in a continuous mass. 

Summarizing the conditions at ninety-stx hours, we may say 
that the vertebre are represented by a continuous perichordal 
layer of rather loose mesenchyme and two mesenchymatous 
arches in each segment, that ascend from the perichordal layer 
to the sides of the neural tube; in each seement the upper part 
of the cephalic selerotomic arch is occupied almost completely 
by the spinal ganglion, but the caudal arch ascends higher, though 
not to the dorsal edge of the neural tube. The cranial and caudal 
arches of any segment represent halves of contiguous, not of the 
same, definitive vertebra. 

Membranous Stage of the Vertebrae. In the following or 
membranous stage, the definitive segmentation of the vertebre 
is established, and the principal parts are laid down in the 
membrane. These processes are essentially the same in all the 
vertebrae, and the order of development is in the usual antero- 
posterior direction. As regards the establishment of the verte- 
bral segments: Figs. 233 and 234 represent frontal sections 
through the same vertebral primordia at different levels from 


THE SKELETON 415 


the thoracic region of a five-day chick. The notochord is 
slightly constricted intervertebrally, and the position of the 
intersegmental artery, of the myotomes and nerves, shows that 
each vertebra! segment is made up of two components repre- 
senting succeeding sclerotomes. In the region of the neural 
arches (Fig. 234) the line of union of cranial and caudal vertebral 
components is indicated by a slight external indentation at the 
place of union, and by the arrangement of the nuclei on each 
side of the plane of union. 


coud Sel. = 2s: 
SA Fs 


ESS 


nt oe 
er ee) 
Ree) 


x 
Pest 


pal 


v 
bore @ paeee 
HOE CITRATE pate 
A 
a 


= 
ole ; & 
2 57, O_O Pate Oia Odie o Be 2882 


Fic. 233. — Frontal section through the notochord and _pri- 
mordia of two vertebre of a 5-day chick; thoracic region. 
Note intervertebral constrictions of the notochord. The 
anterior end of the section is above. 


N., Spinal nerve. Symp., Part of sympathetic cord. v.C., 
Region of pleurocentrum, in which the formation of cartilage 
has begun. Other abbreviations as in Fig. 282. 


The parts of the vertebrae formed in the membranous stage 
are as follows: (1) The vertebral body is formed by tissue of 
both vertebral components that grows around the perichordal 
sheath; (2) a membranous process (neural arch) extends from 
the vertebral body dorsally at the sides of the neural canal; but 
the right and left arches do not yet unite dorsally; (3) a lateral 
or costal process extends out laterally and caudally (Fig. 233) 
from the vertebral body between the successive myotomes. 

The union of the right and left cephalic vertebral components 


416 THE DEVELOPMENT OF THE CHICK 


(caudal sclerotome halves) beneath the notochord is known as 
the subnotochordal bar (Froriep). It forms earler than the 
remainder of the body of the vertebra and during the membranous 
stage is thicker, thus forming a ventral projection at the cephalic 
end of the vertebral body that is very conspicuous (lig. 235). 


‘8 
Gn ty 
rg 
coud. Sel, 
3A 
ceph Sel. 
Gn 
My 


caud Se/ ~Ft 


sA 
ceph, Jel 


2 Z Poy? « 
My A We <a 
a , 8 
AN) ot 
Peeters Nt by 


o & 
" 


mordia as Fig. 233, at a higher level through the neural arches. 
a. C., Anterior commissure of the spinal cord. v. R., Ven- 


tral root of spinal nerve. Other abbreviations as before (Fig. 
929 


404 


Ne 


It chondrifies separately from the vertebral body and earlier. 
Except in the case of the first vertebra it fuses subsequently 
with the remainder of the vertebral body, and disappears as 


THE SKELETON 417 


a separate component. Schauinsland has interpreted it as the 
homologue of the hemal arches of reptilia (e.g., Sphenodon). 
The membrane represents not only the ftiture bony parts 
but the ligaments and periosteum as well. Hence we find that 
the successive membranous vertebre are not separate structures 
but are united by membrane, 7.e., condensed mesenchyme, and 
are distinguishable from the future ligaments at first only by 
greater condensation. In the stage of Fig. 233, chondrification 
has already begun in the vertebral body, hence there is a sharp 


0 


the end of the sixth day of incubation. (After Froriep.) x 40. 
b. C., Basis cranii. i’v. L.1,2,3, First, second, and third 
intervertebral ligaments. s. n. b. 1, 2,3, 4, First, second, third, 
and fourth subnotochordal bars (hypocentra). v. C. 3, 4, 
Pleurocentra of third and fourth vertebre. 


distinction in this region between the vertebral body and inter- 
vertebral dises. The centers of chondrification, however, grade 
into the membranous costal processes and neural arches. 

The vertebral seementation has now become predominant as 
contrasted with the primitive somitic. 

The development of the vertebree during the fifth day com- 
prises: (1) Fusion of successive caudal and cephalic divisions of 


418 THE DEVELOPMENT OF THE CHICK 


the sclerotomes to form the definite vertebrae; (2) union of the 
cephalic vertebral arches beneath the notochord to form the 
subnotochordal bar; (3) origin of the membranous vertebral 
bodies and of the neural arch and costal processes. 

Chondrification, or development of cartilage, sets in from the 
following centers in each vertebra: (1) the cephalic neural arches 
and subnotochordal bar, forming a horseshoe-shaped cartilage 
at the cephalic end of each vertebra; (2) and (3) right and left 
centers in the body of each vertebra behind the subnotochordal 
bar, which soon fuse around the notochord; (the subnotochordal 
bar probably corresponds to the hypocentrum, and the lateral 
centers (2 and 3) to the pleurocentra of paleontologists); (4) and 
(5) centers in each costal process (Figs. 235 and 236). These 
centers are at first separated by membrane, but except in the 
case of the costal processes, which form the ribs, the cartilage 
centers flow together. The neural arches end in membrane 
which gradually extends dersally around the upper part of the 
neural tube, finally uniting above with the corresponding arches 
of the other side to form the membrana reuniens. The chondri- 
fication follows the extension of the membrane. During this 
time the transverse processes of the neural arch and the zygo- 
pophyses are likewise formed as extensions of the membrane. 

The distinction that some authors make between a primary 
vertebral body formed by chondrification within the perichordal 
sheath, and a secondary vertebral body formed by the basal 
ends of the arches surrounding the primary, is not a clear one 
in the case of the chick. 

On the seventh and eighth days the process of chondrifica- 
tion extends into all parts of the vertebra; the entire vertcbra 
is, in fact, laid down in cartilage on the eighth day, although the 
neural spine is somewhat membranous. Fig. 237 shows the 
right side of four trunk vertebrie of an eight-day chick, prepared 
according to the methylene blue method of Van Wijhe. The 


Fic. 236. — Frontal seetion of the vertebral column and neighboring strue- 
tures of a 6-day chick. Upper thoracic region. Note separate centers 
of chondrifiecation of the neural arch, centrum, and costal processes. An- 
terior end of section above. 

B. n. A.. Base of neural arch. br. N. 1, 2, 3, First, second, and third 
brachial nerves. Cp. R., Capitulum of rib. iv. D., Intervertebral dise. 

Mu., Muscles. N. A., Neural arch. T. R., Tubereulum of rib. VY. C., Cen- 


trum cf vertebra. Other abbreviations as before. 


THE SKELETON 419 


ae 
eye Chie 
cavoansee ge 


‘A 
a 


Oe. 
ea 


0? dp 
ary I) 

° 

Fo00 AP 


a0 


420) THE DEVELOPMENT OF THE CHICK 


notochord runs continuously through the centra of the four 
vertebree shown. It is constricted intravertebrally and expanded 
intervertebrally, so that the vertebral bodies are amphiccelous. 
The intervertebral discs are not shown. Each vertebral centrum 
consists of united cephalic and caudal parts; the arches arising 
from the centra are likewise double, but the caudal component 
diminishes posteriorly and is incomplete in the last vertebra 
shown. <A pre- and postzygapophysis is formed on each arch. 
As it is possible to follow the sclerotomal components of the 
primitive vertebre up to this stage continuously, there can be 
no reasonable doubt that they correspond to the divisions shown 


oie 


by the staining in the cartilaginous vertebre of Fig. 237. The 


ceph vA. 


CaUL VA 


Fic. 237.— The right side of four bisected vertebrie of the trunk 
of an 8-day chick. (After Schauinsland.) 
eaud. v. A., Caudal division of vertebral arch. ceph. v. A., 
Cephalie division of vertebral arch, N’ch., Notochord. 


successive vertebra have persistent membranous connections in 
the regions of the neural spines, zygapophyses and centra. These 
are shown in Figs. 238 and 239 (cf. also Fig. 150); they are con- 
tinuous with the perichondrium and all are derived from unchon- 
drified parts of the original membranous vertebre. 

Atlas and Axis (epistropheus). The first and second verte- 
bre agree with the others in the membranous stage. But, when 
chondrification sets in, the hypochordal bar of the first vertebra does 
not fuse with the body, but remains separate and forms its floor 
(Figs. 238 and 239). The body of the first vertebra chondrifies 
separately and is attached by membrane to the anterior end of 
the body of the second vertebra, representing in fact the odon- 
toid process of the latter. It has later a separate center of ossi- 
fication, but fuses subsequently with the body of the second 
vertebra, forming the odondoid process (Fig. 240). 


THE SKELETON 421 


Formation of Vertebral Articulations. In the course of develop- 
ment the intervertebral dises differentiate into a peripheral inter- 
vertebral ligament and a central suspensory ligament which at first 
contains remains of the notochord. There is a synovial cavity 
between the intervertebral and suspensory ligaments. This dif- 
ferentiation takes place by a process of loosening and resorption 


Fic. 238. — Median sagittal section of the basis 
cranii and first three vertebral centra of an 
8-day chick. 

B.C., Basi-eranial cartilage. iv. D. 1, 2, 3, 4, 
First, second, third, and fourth intervertebral 
discs. N.T., Floor of neural tube. s.n.b. 1, 2, 
First and second subnotochordal bars. VY. C. 
1, 2, 3, First, second, and third pleurocentra. 


of cells just external to the perichordal sheath (Fig.241). The in- 
tervertebral ligament takes the form of paired, fibrous menisci, or, in 
other words, the intervertebral ligaments are incomplete around 
the bodies of the vertebre dorsally and ventrally (Sechwarck). 
Ossification is well advanced in the clavicles, long bones, 


422 THE DEVELOPMENT OF THE CHICK 


and membrane bones of the skull before it begins in the vertebra. 
It takes place in antero-posterior order,so that a series of stages 
may be followed in a single embryo (cf. Fig. 242). There are 
three main centers for each vertebra,.viz., one in the body and 
one in each neural arch. The ossification of the centrum is almost 


eA 4 


ptoute . 
Wage’ 
aoe 


1 Poe 
a5, 


Iria. 239. — Lateral sagittal section of the same vertebre (as in Fig. 
238). 

At. 1,2, Floor and roof of atlas. B.C., Basiscranii. Cerv.n. 1, 2, 
First and second cervical nerves. Med. Obl., Medulla oblongata. 
R. V. 2,3, 4, Ribs of the second, third, and fourth vertebra. YV. A. 
2, 3, Arches of the second and third vertebree. 

XII 2, Second root of hypoglossus. 


entirely endochondral, though traces of perichondral ossification 
may be found on the ventral and dorsal surfaces of each centrum 
before the endochondral ossification sets in. The perichondral 
centers soon cease activity. The endochondral centers arise 
just outside the perichordal sheath near the center of each ver- 
tebra on each side of the middle line, but soon fuse around the 


THE SKELETON 423 


notochord, and rapidly spread in all directions, but particularly 
towards the surface, leaving cartilaginous ends (Fig. 241). The 
notochord is gradually reduced and exhibits two constrictions 


Fic. 240. — The first cervical vertebre of a young 
embryo of Haliplana fuliginosa. (After Schauins- 
land.) 


s.n.b.1,2, First and second subnotochordal bars. 
R. 3, 4,5, 6, Ribs of the third, fourth, fifth, and sixth 
cervical vertebrie. 


and three enlargements within each centrum. The main en- 
largement occupies the center and the two smaller swellings the 
cartilaginous ends, the constriction occurring at the junction of 
the ossified areas and cartilaginous ends (Fig. 241). 


Fig. 241. — Section through the body of a cer- 
vical vertebra of a chick embryo of about 12 
days. (After Schwarck.) 

1, Endochondral ossification. 2, Articular 
cartilages. 3, Notochord. 4, Loosening of cells 
of the intervertebral dise, forming a synovial 
cavity. 5, Periosteum. 6, Ligamentum  sus- 
pensorium surrounding the notochord. 


424 THE DEVELOPMENT OF THE CHICK 


The centers of ossification in the neural arches arise from 
the perichondrium a short distance above the body of the ver- 
tebra, and form bony rings about the cartilaginous arch. They 
gradually extend into all the processes of the neural arch. Thus 
the neural arches are separated from the vertebral centra by a 
dise of cartilage which is, however, finally ossified, fusing the 
arches and centra. At what time this occurs, and at what 
time endochondral ossification begins in the arches, is not 
known exactly for the chick. 

The vertebral column of birds is characterized by an extensive 
secondary process of coalescence of vertebre. Thus the two 
original sacral vertebre coalesce with a considerable number of 
vertebre, both in front and behind, to form an extensive basis 
of support for the long iliac bones. The definitive sacrum may 
be divided into an intermediate primary portion composed of 
two vertebrae, an anterior lumbar portion, and a posterior caudal 
portion. The development of these fusions has not been, appar- 
ently, worked out in detail for the chick. The bony centers are 
all separate on the sixteenth day of incubation (ef. Fig. 249). 
Similarly, the terminal caudal vertebra fuse to form the so-called 
pygostyle, which furnishes a basis of support for the tail feathers. 


Ill. DeVELOPMENT OF THE RIBS AND STERNAL APPARATUS 


In the membranous stage of the vertebral column, all of the 
trunk vertebra possess membranous costal processes the subse- 
quent history of which is different in different regions. In the 
cervical region these remain relatively short, and subsequently 
acquire independent centers of chondrification and ossification. 
The last two cervical ribs, however, acquire considerable length. 
In the region of the thorax, the membranous costal processes 
grow ventralward between the successive myotomes and finally 
unite in the formation of the sternum (q.v.). In the lumbar and 
sacral regions the membranous costal processes remain short. 
The primary costal process is an outgrowth of the membranous 
centrum, corresponding in position to the capitulum of the 
definitive rib. The tubereulum arises from the primary costal 
process while the latter is still in the membranous condition and 
crows dorsalward to unite with the neural arch in the region of 
the transverse process. (See Fig. 256.) 

The centers of chondrifieation and ossification of the typical 


THE SKELETON 425 


ribs (cervical and thoracic) arise a short distance lateral to the 
vertebral centers, with which they are connected only by the 
intervening membrane, which forms the vertebro-costal liga- 
ments. Chondrification then proceeds distally. 

The cervical ribs chondrify from a single center. The thoracic 
ribs have two centers of chondrification; a proximal one, corre- 
sponding to the vertebrai division of the rib, and a distal one 
corresponding to the sternal division. The lumbar and sacral 
membranous costal processes do not chondrify separately from 
the vertebral bodies; if they persist at all, therefore, they appear 
as processes of the vertebra, and are not considered further. 


In the fowl the atlas does not bear ribs, and in the embryo the primary 
costal processes of this vertebra do not chondrify. The second to the 
fourteenth vertebrae bear short ribs, with capitulum and tuberculum 
bounding the vertebrarterial canal. The fourteenth is the shortest of 
the cervical series. The fifteenth and sixteenth vertebrie bear relatively 
long ribs, but, as these do not reach the sternum, they are classed as 
cervical. The entire embryonic history, however, puts them in the 
same class as the following sternal ribs; on an embryological basis they 
should be classed as incomplete thoracic ribs. They possess no sternal 
division, but the posterior one has an uncinate process like the true tho- 
racal ribs. The following five pairs of ribs (vertebrae 17-21) possess 
vertebral and sternal portions, but the last one fails to reach the sternal 
rib in front of it. 


The vertebral and sternal portions of the true thoracal ribs 
meet at about a right angle in a membranous joint. This bend 
is indicated in the membranous stage of the ribs. 

The membranous ribs growing downwards and backwards 
in the wall of the thorax make a sudden bend forward, and their 
distal extremities fuse (seven and eight days) in a common mem- 
branous expansion (primordium of the sternum), which, however, 
is separated from the corresponding expansion of the opposite 
side by a considerable area of the body-wall. 

The vertebral and sternal portions of the ribs ossify separately ; 
the ossification of the ribs is exclusively perichondral up to at 
least the sixteenth day (cf. Fig. 242). 

The uncinate processes were not formed in any of the embryos 
studied. Apparently they arise as separate membranous ossi- 
fications after hatching. 

The sternum takes its origin from a pair of membranous expan- 


426 THE DEVELOPMENT OF THE CHICK 


sions formed by the fusion of the distal ends of the first four 
true thoracal ribs; the fifth pair of thoracal ribs does not take 
part in the formation of the sternum. The sternum thus arises 
as two distinct halves, which he at first in the wall of the thorax 
at the posterior end of the pericardial cavity (eight days). The 
greatest extension of the sternal primordia is dorso-ventral, the 


Kia. 242. — Photograph of the skeleton of a 15-day 
chick embryo. Prepared by the potash method. 
(Preparation and photograph by Roy L. Moodie.) 

1, Premaxilla. 2, Nasal. 3, Lachrymal. 4, Para- 
sphenoid. 5, Frontal. 6, Squamosal. 7, Parietal. 


8, Exoccipital. 9, Cervieal rib. 10, Coracoid. 1 
Seapula. 12, Humerus. 18, Ilium. 14, Ischium. 1: 
Pubis. 16, Metatarsus. 17, Tibiofibula. 18, Pal 
tine. 19, Jugal. 20, Maxilla. 21, Clavicle. 


l 


), 
L- 
ventral extremities corresponding to the anterior end of the defini- 


tive sternum, which is formed by concrescence of the lateral halves 
in the middle line beginning at the anteriorend. The concrescence 


THE SKELETON 427 


then proceeds posteriorly, as the dorsal entls of the primordia 
rotate backwards and downwards towards the middle line. 

Although there are two lateral centers of chondrification, 
these soon fuse. The carina arises as a median projection very 
soon after concrescence in any region, and progresses backwards, 
rapidly following the concrescence. There is, therefore, no stage 
in which the entire sternum of the chick is ratite, though this 
condition exists immediately after concrescence in any region. 
The various outgrowths of the sternum (episternal process, antero- 
lateral and abdominal processes), arise as processes of the mem- 
branous sternum and do not appear to have independent centers 
of chondrification. 

The sternum ossifies from five centers, viz., a median anterior 
center and paired centers in the antero-lateral and abdominal 
processes. The last appear about the seventeenth day of incu- 
bation. On the nineteenth day a point of ossification appears 
at the base of the anterior end of the keel. At hatching centers 
also appear in the antero-lateral processes. The centers gradually 
extend, but do not completely fuse together until about the third 
month. The posterior end of the median division of the sternum 
remains cartilaginous for a much longer period. In the duck 
and many other birds there are only two lateral centers of ossifi- 
cation: the existence of five centers in the chick is, therefore, 
probably not a primitive condition. 


IV. DEVELOPMENT OF THE SKULL 


The skull arises in adaptation to the component organs of 
the head, viz., the brain, the sense organs (nose, eye, and ear) 
and cephalic visceral organs (oral cavity and pharynx); it thus 
consists primarily of a case for the brain, capsules for the sense 
organs, and skeletal bars developed in connection with the mar- 
gins of the mouth and the visceral arches. In the chick, 
the primordia of the auditory and olfactory capsules are con- 
tinuous ab initio with the primordial cranium; the protecting coat 
of the eye (sclera) never forms part of the skull. Therefore, we 
may consider the development of the skull in two sections, first 
the dorsal division associated with brain and sense organs (neuro- 
cranium), and second, the visceral division or splanchnocranium. 
Although the investment of the eyes forms no part of the skull, 
yet the eyes exert an immense effect on the form of the skull. 


428 THE DEVELOPMENT OF THE CHICK 


Development of the Cartilaginous or Primordial Cranium. 
(1) The Neurocranium. The neurocranium is derived from the 
mesenchyme of the head, the origin of which has been described 
previously. The mesenchyme gradually increases in amount and 
forms a complete investment for the internal organs of the head. 
It is not all destined, however, to take part in the formation of 
the skeleton, for the most external portion forms the derma and 
subdermal tissue; and, internal to the skeletogenous layer, the 
membranes of the brain and of the auditory labyrinth, etc., are 
formed from the same mesenchyme. 

The notochord extends forward in the head to the hypophysis 
(Figs. 67, 88, ete.), and furnishes a basis for division of the 
neurocranium into chordal and prechordal regions. Within the 
chordal division again, we may distinguish pre-otic, otic, and 
post-otie regions according as they are placed in front of, around, 
or behind the auditory sac. The part of the postotic region 
behind the vagus nerve is the only part of the neurocranium 
that is primarily segmental in origin. The sclerotomes of the 
first four somites (Figs. 63 and 117) form this part of the skull; 
and at least three neural arches, homodynamous with the verte- 
bral arches, are formed in an early stage, but fuse together while 
still membranous, leaving only the two pairs of foramina of the 
twelfth cranial nerve as evidence of the former segmentation. It 
is also stated that membranous costal processes are found in 
connection with these arches, but they soon disappear without 
chondrifying. 

The primordial neurocranium is performed in cartilage and 
corresponds morphologically to the cranium of cartilaginous 
fishes. However, it never forms a complete investment of the 
brain; except in the region of the tectum synoticum it is wide 
open dorsally and laterally. It is subsequently replaced by 
bone to a very great extent, and is completed and_ reinforced 
by numerous membrane bones. 

The neurocranium takes its origin from two quite distinct 
primordia situated below the brain, viz., the parachordals and 
the trabeculae. The former develop on each side of and around 
the notochord, being situated, therefore, behind the cranial 
flexure and beneath the mid- and hind-brain; the trabecule are 
prechordal in position, being situated beneath the twixt-brain 
and cerebral hemispheres, and extending forward through the 


THE SKELETON 429 


interorbital region to the olfactory sacs. It is obvious, therefore, 
that the parachordals and trabeculae must form with relation to 
one another the angle defined by the cranial flexure. 

The parachordals appear in fishes as paired structures on 
either side of the notochord, uniting secondarily around the 
latter; but in the chick the perichordal portion is formed at the 
same time as the thicker lateral portions, so that the parachordals 
exist in the form of an unpaired basilar plate from the first. The 
trabecule are at first paired (in the earliest membranous condi- 
tion), but soon fuse in front, while the posterior ends form a pair 
of curved limbs (fenestra hypophyseos) that surrounds the infun- 
dibulum and hypophysis, and joins the basilar plate behind the 
latter. At the same time that the parachordals and trabecule 
are formed by condensations of mesenchyme, the latter con- 
denses also around the auditory sacs and olfactory pits in direct 
continuity with the parachordals and trabecule respectively; so 
that the auditory and olfactory capsules are in direct continuity 
with the base of the neurocranium from the beginning. 

Chondrification begins in the primordial cranium about the 
sixth day; it appears first near the middle line on each side, and 
extends out laterally. Somewhat distinct centers corresponding 
to the occipital sclerotomes may be found in some birds, but 
they soon run together, and the entire neurocranium forms a 
continuous mass of cartilage (sixth, seventh, and eighth days). 

During this process the trabecular region increases greatly in 
length simultaneously with the outgrowth of the facial region, 
and the angle defined by the cranial flexure becomes thus appar- 
ently reduced. The posterior border of the fenestra hypophyseos 
marks the boundary between the basilar plate and trabecular 
region. 

In the region of the basilar plate the following changes take 
place: (1) in the post-otic or occipital region a dorso-lateral 
extension (Fig. 244) fuses with the hinder portion of the otic 
capsule, thus defining an opening that leads from the region of 
the cavity of the middle ear into the cranial cavity (fissure met- 
otica). This expansion is pierced by the foramina of the ninth 
tenth and eleventh nerves. (2) The otic region becomes greatly 
expanded by the enlargement of the membranous labyrinth. The 
cochlear process grows ventrally and towards the middle line and 
thus invades the original parachordal region (Fig. 168). The 


430 THE DEVELOPMENT OF THE CHICK 


posterior region of the otic capsule expands dorsally above the 
hind-brain, and forms a bridge of cartilage extending from one 
capsule to the other, known as the tectum synoticum (Fig. 244, 
33). (3) The preotic region expands laterally and dorsally in 
the form of a wide plate (alisphenoidal plate) which is expanded 
transversely, and thus possesses an anterior face bounding the 
orbit posteriorly and a posterior face forming part of the anterior 
wall of the cranial cavity. This plate arises first between the 
ophthalmic and maxillo-mandibular branches of the trigeminus, 
and subsequently sends a process over the latter that fuses with 
the anterior face of the otic capsule, thus establishing the foramen 
prooticum. 


For an account of numerous lesser changes, the student is referred 
to Gaupp (1905), and the special literature (especially Parker, 1869). 
The various foramina for the fifth to the twelfth cranial nerves are 
defined during the process of chondrification; the majority of these are 
shown in the figures. 

The trabecular region may be divided into interorbital and 
ethmoidal (nasal) regions. The basis of the skeleton in this 
region is formed by the trabecule already described. The median 
plate formed by fusion of the trabeculee extends from the pituitary 
space (fenestra hypophyseos) to the tip of the head; a high median 
keel-like plate develops in the interorbital and internasal regions 


Fig. 243. — Skull of an embryo of 65 mm. length; right side. Membrane 
bones in yellow. Cartilage in blue. (Drawn from the model of W. Tonkoff; 
made by Ziegler.) 

Fic. 244. — View of the base of the same model. 

243-244. — 1, Squamosum. 2, Parietale. 3, Capsula auditiva. 4, Cap- 
sula auditiva (cochlear part). 5, Fissura metotica. 6, Epibranchial cartilage. 
7, Sphenolateral plate. 8, Foramen proédticum. 9, Columella. 10, Otie pro- 
cess of quadratum. 11, Basitemporal (postero-lateral part of the parasphenoid). 
12, Articular end of Meckel’s cartilage. 13,Angulare. 14, Supra-angulare. 15, 
Dentale. 16,Skeleton of tongue. 17,Pterygoid. 18, Palatine. 19, Rostrum 
of parasphenoid. 20, Quadrato-jugal. 21, Jugal (zygomaticum). 22, Vomer. 
23, Maxilla. 24, Premaxilla. 25, Anterior turbinal. 26, Posterior turbinal. 
27, Nasale. 28, Prefrontal (lachrymale). 29, Antorbital plate. 30, Interor- 
bitalforamen. 31, Interorbital septum. 32,Frontale. 33,Tectum synoticum. 
34, Foramen magnum. 35, Prenasal cartilage. 36, Orbital process of quad- 
rate. 37, Articular process of Quadrate. 38, Fenestra basicranialis posterior. 
39, Chorda. IX, Foramen glossopharyngei. X, Foramen vagi. XII, Fora- 
mina hypoglossei. 

Fic. 245. — Visceral skeleton of the same model. 

1, Dentale. 2, Operculare. 3, Angulare. 4, Supra-angulare. 5, Meckel’s 
cartilage. 6, Entoglossum — (cerato-hyal). 7, Copula (1). 8, Pharyngo- 
branchial (1). 9, Epibranchial. 10, Copula (2). 


THE SKELETON 431 


and fuses with the trabecule, forming the septum interorbitale 
and septum nasi (Fig. 243). The free posterior border of this 
plate lies in front of the optic nerves; an interorbital aperture 
arises in the plate secondarily (Fig. 243). 

In the ethmoidal region the septum nasi arises as an anterior 
continuation of the interorbital plate; and the trabecular plate 
is continued forward as a prenasal cartilage in front of the olfac- 
tory sacs. Curved, or more or less rolled, plates of cartilage 
develop in the axis of the superior, middle, and inferior turbinals 
(see olfactory organ), and these are continuous with the lateral 
wall of the olfactory capsules, which in its turn arises from the 
dorsal border of the septum nasi (Figs. 248 and 244). 

(2) The Origin of the Visceral Chondrocranium (Cartilaginous 
Splanchnocranium). The visceral portion of the cartilaginous 
skull arises primarily in connection with the arches that bound 
the cephalic portion of the alimentary tract, viz., oral cavity 
and pharynx. In the chick, cartilaginous bars are formed in 
the mandibular arch, hyoid arch, and third visceral arch. In 
fishes, the posterior visceral arches also have an axial skeleton, 
but in the chick the mesenchyme of these arches does not develop 
to the stage of cartilage formation. The elements of these arches 
are primarily quite distinct. The upper ends of the mandibular 
and hyoid skeletal arches are attached to the skull; and the lower 
ends of the three arches concerned meet in the middle line. Two 
medial elements or copule are formed in the floor of the throat, 
one behind the angle of the hyoid arch, and one behind the 
third visceral arch (Fig. 245). 

Mandibular Arch. Two skeletal elements arise in the man- 
dibular arch on each side, a proximal one (the palato-quad- 
rate) and a distal one (Meckel’s cartilage). The former is 
relatively compressed, and the latter an elongated element (Fig. 
243, 10). The palato-quadrate lies external to the antero-ver- 
tral part of the auditory capsule, and soon develops a triradiate 
form. The processes are: the processus oticus, which applies 
itself to the auditory capsule, the processus articularis, which 
furnishes the articulation for the lower jaw, and the processus 
orbitalis, which is directed anteromedially towards the orbit. 
A small nodule of cartilage of unknown significance lies above 
the junction of the processus oticus and otic labyrinth. Meckel’s 
cartilage is the primary skeleton of the lower jaw, corresponding 


432 THE DEVELOPMENT OF THE CHICK 


to the definitive lower jaw of selachians. It consists of two 
rods of cartilage in the rami of the mandibular arch, which articu- 
late proximally with the processus articularis of the palato- 
quadrate cartilage, and meet distally at the symphysis of the 
lower jaw. The form of the articulation of the lower jaw is early 
defined in the cartilage (seven to eight days). 

Hyoid Arch. The skeletal elements of the hyoid arch consist of 
proximal and distal pieces (with reference to the neurocranium) 
which have no connection at any time. The former are destined to 
form the columella, and the latter parts of the hyoid apparatus. 
The columella apparently includes two elements (in Tinnunculus 
according to Suschkin, quoted from Gaupp): a dorsal element, 
interpreted as hyomandibular, in contact with the wall of the 
otic capsule, and a small element (stylohyal) beneath the former. 
The two elements fuse to form the columella, the upper end of 
which is shown in Fig. 168. The stapedial plate (operculum of 
the columella) is stated to arise in Tinnunculus from the wall 
of the otic capsule, being cut out by circular cartilage resorption 
and fused to the columella. 

The distal elements of the hyoid arch consist of (1) a pair 
of ceratohyals, which subsequently fuse in the middle line to 
form the entoglossal cartilage, the proximal ends remaining free as 
the lesser cornua of the hyoid, and (2) a median unpaired piece 
(copula I or basihyal) behind the united ceratohyals (Fig. 245). 

First Branchial Arch. The skeletal elements of the third visceral 
(first branchial) arch are much more extensive than those of the 
hyoid arch. They are laid down as paired cerato- and epi-branchial 
cartilages on each side, and an unpaired copula IL (basibranchial I) 
in the floor of the pharynx, in the angle of the other elements 
(Fig. 245). The cerato- and epibranchials increase greatly in 
length, and form the long curved elements (greater cornua) of the 
hyoid, which attain an extraordinary development in many birds. 

Ossification of the Skull. The bones of the skull are of two 
kinds as to origin: (1) those that arise in the primordial cranium, 
and thus replace cartilage (cartilage bones or replacement bones), 
and (2) those that arise by direct ossification of membrane (mem- 
brane or covering bones). 

The cartilage bones of the bird’s skull are: (a) in the occipital 
region; the basioccipital, two exoccipitals, and the supraocci- 
pitals; (b) in the otie region: proGtic, epiotic, and opisthotic; 


THE SKELETON 433. 


(c) in the orbital region: the basisphenoid, the orbitosphenoids, 
the alisphenoids and ossifications of the interorbital septum; (d) in 
the ethmoidal region the bony ethmoidal skeleton; (e) the palato- 
quadrate cartilage furnishes the quadrate bone; (/) a proximal 
ossification, the articulare, arises in Meckel’s cartilage and fuses 
later with membrane bones; (g) the upper part of the hyoid arch 
furnishes the columella, and the ceratohyals the os entoglossum; 
(h) the cerato- and epibranchials ossify independently, as also 
do the two copule. (See Figs. 243, 244 and 245.) 

The membrane bones of the skull are: (a) in the region of the 
cranium proper: parietals, frontals, squamosals; (6) in the facial 
region: lachrymals, nasals, premaxille, manille, jJugals, quad- 
rato-jugals, pterygoids, palatines, parasphenoid, and vomer; (c) 
surrounding Meckel’s cartilage and forming the lower Jaw: angu- ¢ 
lare, supra-angulare, operculare, and dentale. (See Figs. 243, 244 
and 245.) 

The embryonic bird’s skull is characterized by a wealth of 
distinct bones that is absolutely reptilian; but in the course of 
development these fuse together so completely that it is only in 
the facial and visceral regions that the sutures can be distinguished 
readily. 

In order of development the membrane bones precede the 
cartilage bones, though the latter are phylogenetically the older. 
Thus, about the end of the ninth day, the following bones are 
present in the form of delicate reticulated bars and plates: all 
four bones of the mandible, the faint outline of the premaxille, 
the central part of the maxilla, the jugal and quadratojugal, the 
nasals, the palatines and pterygoids. The base of the squamosal 
is also indicated by a small triangular plate ending superiorly in 
branching trabecule, delicate as frost-work. A faint band of 
perichondral bone is beginning to appear around the otic process 
of the quadrate, the first of the cartilage bones to show any 
trace of ossification. These ossifications. appear practically 
simultaneously as shown by the examination of the earlier stages. 

On the twelfth day these areas have expanded considerably, 
and the frontals and prefrontals (lachrymals) are formed; the 
rostrum of the parasphenoid is also laid down, and the exoccipi- 
tals appear in the cartilage at the sides of the foramen magnum. 
The parietals appear behind the squamosal (Fig. 242) about the 
thirteenth day; the basioccipitals soon after. The supraoc- 


434 THE DEVELOPMENT OF THE CHICK 


cipital appears as a pair of ossifications in the tectum synoticum 
on each side of the dorsal middle line, subsequently fusing 
together. 

A detailed history of the mode of ossification of all the various 
bones of the skull would be out of place in this book. The figures 
illustrate some points not described in the text. The reader is 
referred to W. Ix. Parker (1869) and to Gaupp (1905). 


V. APPENDICULAR SKELETON 


The appendicular skeleton includes the skeleton of the limbs 
and of the girdles that unite the limbs to the axial skeleton. The 
fore and hind-limbs, being essentially homonymous structures, 
exhibit many resemblances in their development. 

The Fore-limb. The pectoral girdle and skeleton of the 
wing develop from the mesenchyme that occupies the axis and 
base of the wing-bud, as it exists on the fourth day of incuba- 
tion. It is probably of sclerotomic origin, but it is not known 
exactly how many somites are concerned in the chick, nor which 
ones. After the wing has gained considerable length (fifth day) 
it can be seen from the innervation that three somites are prin- 
cipally involved in the wing proper, viz., the fourteenth, fifteenth, 
and sixteenth of the trunk. But it is probable that the mesen- 
chyme of the base of the wing-bud, from which the pectoral 
girdle is formed, is derived from a larger number of somites. 

It is important, then, to note first of all that the scapula, 
coracoid, clavicle, humerus, and distal skeletal elements of the 
wing are represented on the fourth day by a single condensation 
of mesenchyme, which corresponds essentially to the glenoid 
region of the definitive skeleton. From this common mass a 
projection grows out distally in the axis of the wing-bud, and 
three projections proximally in different directions in the body- 
wall. These projections are (1) the primordium of the wing- 
skeleton, (2) of the scapula, (8) of the coracoid, (4) of the 
clavicle. 

The Pectoral Girdle. The elements of the pectoral girdle are 
thus outgrowths of a common mass of mesenchyme. The scapula 
process grows backward dorsal to the ribs; the coracoid process 
grows ventralward and slightly posterior towards the primordium 
of the sternum, thus forming an angle slightly less than a right 
angle with the scapular process; and the clavicular process grows 


THE SKELETON 435 


out in front of the coracoid process ventrally and towards the 
middle line. These processes are quite well developed on the 
fifth day, and increase considerably in length on the sixth day, 
when the hind end of the scapula nearly reaches the anterior end 
of the ilium, and the lower end of the ccracoid is very close to 
the sternum. The elements are still continuous in the glenoid 
region. 

About the end of the sixth day independent centers of chon- 
drification appear in the scapula and coracoid respectively near 
their union; these spread distally and fuse centrally, so that 
on the seventh day the coraco-scapula is a single bent cartilagi- 
nous element. In the angle of the bend, however (the future 
coraco-scapular joint), the cartilage is in a less advanced condi- 
tion than in the bodies of the two elements. The clavicular 
process, on the other hand, never shows any trace of cartilage 
formation, either in early or more advanced stages, but ossifies 
directly from the membrane. It separates from the other ele- 
ments of the pectoral girdle, though not completely, on the eighth 
day. 

The scapula and coracoid ossify in a perichondral fashion, 
beginning on the twelfth day, from independent centers, which 
approach but never fuse, leaving a permanent cartilaginous 
connection (Fig. 242). The clavicle, on the other hand, is a 
purely membrane bone; bony deposit begins in the axis of the 
membranous rods on the eighth or ninth days, soon forming 
fretted rods that approach in the mid-ventral line by enlarged 
ends, which fuse directly without the intervention of any median 
element about the twelfth to thirteenth day, thus forming the 
furcula or wish-bone (Fig. 246). 


The nature of the clavicle in birds has been the subject of a sharp 
difference of opinion. On the one hand, it has been maintained that it 
is double in its origin, consisting of a cartilaginous axis (procoracoid) 
on which a true membrane bone is secondarily grafted (Gegenbaur, Fur- 
bringer, Parker, and others) ; on the other hand, all cartilaginous preforma- 
tion in its origin has been denied by Rathke, Goette, and Kulezycki. After 
careful examination of series of sections in all critical stages, and of 
preparations made by the potash method, I feel certain that in the chick 
at least there is no cartilaginous preformation. It is still possible (in 
deed probable on the basis of comparative anatomy) that the theory 
of its double origin is correct phylogenetically; but it is certain that the 


456 THE DEVELOPMENT OF THE CHICK 


procoracoid component does not develop beyond the membranous stage 
in the chick. It is interesting that the clavicle is the first center of ossi- 
fication in the body, though perichondral ossification of some of the 
long bones begins almost as soon. 

The Wing-bones. The primordium of the wing-bones_ is 
found in the axial mesenchyme of the wing-bud, which is origi- 
nally continuous with the primordium of the pectoral girdle, and 
shows no trace of the future elements of the skeleton. The 
differentiation of the elements accompanies in general the external 
differentiation of the wing illustrated in Figs. 121 to 124, Chapter 
VII. The humerus, radius, and ulna arise by membranous differ- 
entiation in the mesenchyme in substantially their definitive 
relations; they pass through a complete cartilaginous stage and 


Fig. 246. — Photograph of the pectoral 
girdle of a chick embryo of 274 hours; 
prepared by the potash method.  (Prep- 
aration and photograph by Roy L. 
Moodie. ) 

1, Coracoid. 2, Clavicle. 3, Scapula. 

4, Humerus. 


then ossify in a perichondral fashion (see Fig. 242). In the 
carpus, metacarpus, and phalanges, more elements are formed 
in the membrane and cartilage than persist in the adult. Elimi- 
nation as well as fusion takes place. These parts will therefore 
require separate description. 

As birds have descended from pentadactyl ancestors with 
subsequent reduction of carpus, metacarpus, and phalanges, it 
is naturally of considerable interest to learn how much of the 
ancestral history is preserved in the embryology. The hand is 
represented in the embryo of six days by the spatulate extremity 
of the fore-limb, which includes the elements of carpus, meta- 
carpus, and phalanges. From this expansion five digital rays 
grow out simultaneously, the first and fifth being relatively 


THE SKELETON 437 


small; the second, third, and fourth represent the persistent digits. 
In each ray is a membranous skeletal element, which, however, 
soon disappears in the first and fifth. Thus there are distinct 
indications of a pentadactyl stage in the development of the 
bird’s wing. 

In the definitive skeleton there are but two carpal bones, 
viz., a radiale at the extremity of the radius, and an ulnare at 
the extremity of the ulna. In the embryo there is evidence of 
seven transitory pieces in the carpus arranged in two rows, proxi- 
mal and distal (Fig. 247). In the proximal row only two car- 


Fic. 247. — Skeleton of the wing of a chick embryo of 8 days. (After W. 
K. Parker.) 


Cp. 2, 3, and 4, Second, third, and fourth carpalia. -C. U., Centralo- 
ulnare. H., Humerus. I. R., Intermedio-radiale. M’c. 2, 3, 4, Second, 
third, and fourth metacarpalia. P’ch., Perichondral bone  R., Radius. 
UU; Ulna. 


tilages appear, viz., the radiale and ulnare; but in earlier stages 
each appears to be derived from two centers: the radiale from a 
radiale s.s. and an intermedium, the ulnare from an ulnare s.s. 
and a centrale. Evidence of such double origin of each is found 
also in the eartilaginous condition (v. Parker, 1888). Four 
elements in all enter into the composition of this proximal row. 
In the distal row there are three distinct elements corresponding 
to the three persistent digits, and representing, therefore, carpalia 
II, Ill, and IV. These subsequently fuse with one another, 
and with the heads of the metacarpals to produce the carpo- 
metacarpus. 

On the seventh day the metacarpus is represented by three 
cartilages corresponding to the three persistent digits, viz., II, 


438 THE DEVELOPMENT OF THE CHICK 


Ill, IV. Metacarpal I is only about one third the length of IIT. 
Metacarpal IV is much more slender than III, and is bowed out 
in the middle, meeting III at both ends. The elements are at 
first distinct, but II and III fuse at their proximal ends in the 
process of ossification. Cartilaginous rudiments of metacarpals 
Land V have also been found by Parker, Rosenberg, and Leighton. 

As to the phalanges, Parker finds two cartilages in II, three 
in III, and two in IV on the seventh day; but already on the 
eighth day the distal phalanges of III and IV have fused with 
the next proximal one. 


As regards the homology of the digits of the wing, the author has 
adopted the views of Owen, Mehnert, Norsa, and Leighton, that they 
represent numbers II, HI, and IV, which seem to be better supported 
by the embryological evidence than the view of Meckel, Gegenbauer, 
Parker, and others, that they represent I, II, and III. 


The Skeleton of the Hind-limb. The skeleton of the hind- 
limb and pelvic girdle develops from a continuous mass of mesen- 
chyme situated at the base of the leg-bud. The original center 
of the mass represents the acetabular region; it grows out in four 
processes: (1) a lateral projection in the axis of the leg-bud, the 
primordium of the leg-skeleton proper, (2) a dorsal process, the 
primordium of the ilium; and two diverging ventral processes, 
one in front of the acetabulum (3) the pubis, and one behind 
(4) the ischium. In the membranous condition the elements are 
continuous. The definitive elements develop either as separate 
‘artilage centers in the common mass (usually), or as separate 
centers of ossification in a common cartilaginous mass (lium 
and ischium). 

The Pelvic Girdle. The primitive relations of the elements of 
the pelvic girdle in Larus ridibundus is shown in Fig. 248, which 
represents a section in the sagittal plane of the body, and thus 
does not necessarily show the full extent of any of the cartilagi- 
nous elements, but only their general relations. The head of the 
femur is seen in the acetabulum, the broad plate of the ilium 
above and the pubis and ischium as cartilaginous rods of almost 
equal width below, the pubis in front and the ischium behind 
the acetabulum. In this stage the pelvic girdle, in this and 
many other species of birds, consists of three separate elements 
on each side in essentially reptilian relations. 


THE SKELETON 439 


In the chick at a corresponding age the ilium is much more 
extensive, and the ischium is united with it by cartilage; the 
pubis, however, has only a membranous connection with the 
ilium (contra Johnson). In the course of development the distal 
ends of the ischium and pubis rotate backwards until the two 
elements come to lie substantially parallel to the ilium (Figs. 
242 and 249). The displacement of the ischium and pubis may 


Fic. 248. 


Sagittal section of the right half of the body 
of Larus ridibundus, to show the composition of the pel- 
vie girdle; x 35. Length of the leg-bud of the embryo, 
0.4mm. (After Mehnert.) 


F., Femur. cr.N., Crural nerve. II., Ilium. I. s., Is- 
chium. Is. N., Ischial nerve. ob. N., Obturator nerve. 
Pi Pubis: 


be associated with the upright gait of birds; it is fully established 
on the eighth day in the chick. The mode of ossification, which 
is perichondral, is shown in Fig. 249. 

Later, the illum obtains a very extensive pre- and_post- 
acetabular union with the vertebre. I have found no evidence 
in a complete series of preparations (potash) of attachment by 
ribs arising as independent ossifications. The ischium also fuses 


440) THE DEVELOPMENT OF THE CHICK 


with the ventral posterior border of the ilium, and the pubis, 
except at its anterior and posterior ends, with the free border 
of the ischium. 

The spina iliaca, a pre-acetabular, bony process of the ilium, 
requires special mention in- 
asmuch as it has been inter- 
preted (by Marsh) as the 
true pubis of birds, and the 
element ordinarily named 
the pubis as homologous to 
the post-pubis of some rep- 
tiles. There is no evidence 
for this in the development. 
The spina iliaca develops as 
a cartilaginous outgrowth of 
the ium and ossifies from 
the latter, not from an inde- 
pendent center (Mehnert). 

The Leg-skeleton. The 
skeleton of the leg develops 
from the axial mesenchyme, 
which is at first continuous 
with the primordium of the 


pelvic girdle. In the process 
Fia. 249. — Photograph of the skeleton of chondrification it seg- 
of the leg of a chick embryo of 15 days’ ments into 4 larger number 
1 > ‘ 1 IpaANnara r » Qe 7 » . 
incubation. Pre pared by the potash of elements than: 4ounaen 
method. (Preparation and photograph 
by Roy L. Moodie.) ; 
1, Tibia. 2, Fibula. 38, Patella. 4, suppressed and others fuse 


Femur. 5, Ilium. 6, Pleurocentra of toeether. The digits erow 
sacral vertebrie. 7, Ischium. 8, Pubis. Le: ; a 
9, Tarsal ossification. 10, Second, third, out from the palate-like eX- 


the adult, some of which are 


and fourth metatarsals. 11, First meta- pansion of the primitive 
tarsal. I, IH, III, IV, First, second, third, ; ; : : 
and fourth digits. limb in the same fashion as 
in the wing. In general the 

separate elements arise in the proximo-distal order (Figs. 242 and 
249). 

The femur requires no special description; ossification begins 
on the ninth day. 

The primordium of the fibula is from the first more slender 
than that of the tibia, though relatively far larger than the adult 


THE SKELETON 44] 


fibula. The fibular cartilage extends the entire length of the crus, 
but ossification is confined largely to its proximal end; on the 
fourteenth day its lower half is represented by a thread-like fila- 
ment of bone. 

No separate tarsal elements are found in the adult; but in the 
embryo there are at least three cartilages, 
viz., a fibulare, tibiale and a large distal 
element opposite the three main metatar- 
sals. In the course of development, the 
two proximal elements fuse with one 
another, and with the distal end of the 
tibia. The distal element fuses with 
the three main metatarsals, first with the 
second, then with the fourth, and lastly 
with the third (Johnson). 

Five digits are formed in the mem- 
branous stage of the skeleton. In the 
‘ase of the fifth digit, only a small nodule 
of cartilage (fifth metatarsal) develops and 
soon disappears. The second, third, and 
fourth are the chief digits; the first is 


relatively small. Metatarsals 2, 3, and 4 Fic. 290. — Photograph 
of the skeleton of the 
foot of a chick embryo 
of 15 days’ incubation. 


are long and ossify separately in a peri- 
chondral fashion. They become applied 


near their middle and fuse with one (Preparation and pho- 
another and with the distal tarsal element tograph by Roy L. 
to form the tarso-metatarsus of the adult Moodie.) 


Ne oe OR n : 1, 2,3, 4, First, second 
No 25( st, atarsal is s 5 1) 459545) , Second, 
(Fig. 250). The first metatarsal is short, thied. Ane fourth deite 


lying on the preaxial side of the distal end M2, M 3, M 4, Second, 
of the others (Fig. 249); it ossifies after ee a oe 
the first phalanx. The number of pha- a 
langes is 2, 3, 4, and 5 in the first, second, third, and fourth digits 
respectively (ig. 249). 

The patella is clearly seen in potash preparations of thirteen-day 
chicks. At the same time there is a distinct, though minute, separate 
center of ossification in the tarsal region (Fig. 249). 


APPENDIX 


GENERAL LITERATURE 


y. Barr, C. E., Ueber Entwickelungsgeschichte der Tiere. Beobachtung 
und Reflexion. Kéonigsberg, 1828 u. 1837. 

id., 2. Teil — Herausgegeben von Stieda. Konigsberg, 1888. 
Duvat, Marnias, Atlas d’embryologie. (With 40 plates.) Paris, 1889. 
Foster, M., and Batrour, F. M., The Elements of Embryology. Second 

Edition revised. London, 1883. 

Gapow, Hans, Die Vogel, Bronn’s Klassen und Ordnungen des Thier-Reichs, 
Bd. VI, Abth. 4, 1898. 

Handbuch der vergleichenden und experimentellen Entwickelungslehre der 
Wirbeltiere. Edited by Dr. Oskar Hertwig and written by numerous 
collaborators. Jena, 1901-1907. 

His, W., Untersuchungen tiber die erste Anlage des Wirbeltierleibes. Die 
erste Entwickelung des Hiihnchens im Ei. Leipzig, 1868. 

Kersex, F., and Asranam, K., Normaltafeln zur Entwickelungsgeschichte 
des Huhnes (Gallus domesticus). Jena, 1900. 

v. Kéuurker, A., Entwickelungsgeschichte des Menschen und der héheren 
Thiere. Zweite Aufl. Leipzig, 1879. 

MarsHatt, A. M., Vertebrate Embryology. A Text-book for Students and 
Practitioners. (Ch. IV, The Development of the Chick.) New York 
and London, 1893. 

Minor, C. 8., Laboratory Text-book of Embryology. Philadelphia, 1903. 

Panper, Beitriige zur Entwickelungsgeschichte des Hithnchens im Ei. | Wiirz- 
burg, 1817. 

Prevost ET Dumas, Mémoire sur le développement du poulet dans lceuf. 
Ann. Se. Nat., Vol. XII, 1827. 

Preyer, W., Specielle Physiologie des Embryo. Leipzig, 1885. 

Remak, R., Untersuchungen tiber die Entwickelung der Wirbelthiere. Ber- 
lin, 1855. 


LITERATURE — CHAPTER I 


Costr, M., Histoire générale et particuliére du développement des corps 
organisés, T. I. (Formation of Egg in Oviduct, see Chap. VI). Paris, 
1847-1849. 

D’Houuanper, F., Recherches sur l’oogenése et sur la structure et la signi- 
fication du noyau vitellin de Balbiani chez les oiseaux. Archiv. d’anat. 
micr., I. VII, 1905. 

GEGENBAUR, C., Ueber den Bau und die Entwickelung der Wirbeltiereier 
mit partieller Dottertheilung. Archiv. Anat. u. Phys., 1861. 

443 


444 APPENDIX 


v. Hemspacu, Mecket, Die Bildung der fiir partielle Furchung bestimmten 
Kier der Vogel im Vergleich mit den Graafschen Follikel und der Decidua 
des Menschen. Zeitschr. wiss. Zool., Bd. III, 1851. 

Hou, M., Ueber die Reifung der Eizelle des Huhnes. — Sitzungsber. Akad. 
Wiss. Wien, math.-nat. Kl., Bd. XCIX, Abth. III, 1890. 

vy. Kouurmker, ALBERT, Entwickelungschichte des Menschen und der héheren 
Thiere. Zweite ganz umgearbeitete Auflage. Erste Halfte (Bogen 1-25). 
(See pp. 59-83, segmentation of hen’s egg.) Leipzig, 1879. 

Lanpors, H., Die Eierschalen der Vo6gel in histologischer und genetischer 
Beziehung. Zeitschr. wiss. Zool., Bd. XV, 1865. 

MirropHanow, P., Note sur la structure et la formation de Venveloppe du 
jaune de l’oeuf de la poule. Bibliog. anat., T. VI. Paris, 1898. 
v. Naruusius, W., Zur Bildung der Eihiillen. Zool. Anz. Bd. XIX, 1896. 
Die Entwickelung von Schale und Schalenhaut des Hiihnereies im 
Ovidukt. Zeitschr. wiss. Zool., Bd. LV, 1893. 
Parker, G. H., Double Hen’s Eggs. American Naturalist, Vol. XL, 1906. 
{1zz0, A., Sul numero e sulla distribuzione dei pori nel guscio dell’ ovo di 
gallina. Ricerche fatte nel Laborat. di Anat. normale, Univ. di Roma ed 
in altri Laborat. biol., Vol. VII, 1899. 

Waxupryer, W., Die Geschlechtszellen. Handbuch der vergl. und exper. 
Entwickelungslehre der Wirbeltiere. Bd. I, T. 1, 1901. 


LITERATURE — CHAPTER II 


AnpbreEws, E. A., Some Intercellular Connections in an Ege of a Fowl. The 
Johns Hopkins University Circular. Notes from the Biological Lab- 
oratory, March, 1907. 

Barrurtu, D., Versuche tiber die parthenogenetische Furchung des Hiithner- 
eles. Arch. Entw.-mech., Bd. 2, 1895. 

Biount, Mary, The Early Development of the Pigeon’s Egg with Especial 
Reference to the Supernumerary Sperm-nuclei, the Periblast and the 
Germ-wall. Biol. Bull., Vol. XIII, 1907. 

Duvat, M., De la formation du blastoderm dans l’ceuf d’oiseau. Ann. Se. 
Nat. Zool., Sér. 6, T. XVIII, 1884. 

Gasspr, E., Der Parablast und der Keimwall der Vogelkeimscheibe.  Sit- 
zungsber. der Ges. zur Beférd. d. ges. Naturwiss. zu Marburg, 1883. 

Eierstocksei und Hileiterei des Vogels. bid, L884. 

Gorter, A., Beitrige zur Entwickelungsgeschichte der Wirbeltiere, IIT. Die 
Bildung der Keimblitter und des Blutes im Hiihnerei. Archiv. mikr. 
Anat., Bd. X, 1874. 

Harrrer, E. H., The Fertilization and Early Development of the Pigeon’s 
Ege. Am. Jour. Anat., Vol. III, 1904. 

Kronka, H., Die Furchung des Hiihnereies. Anat. Hefte, Bd. III, 1894. 

Lau, H., Die parthenogenetische Furchung des Hiihnereies. Inaug. Dissert. 
Jurjew — Dorpat., 1894. 

OxELLAcHER, J., Untersuchungen iiber die Furehung und Blitterbildung im 
Hiihnerei. Studien tber experimentelle Pathologie von Stricker, Bd 
I, 1869. 


APPENDIX 445 


OELLACHER, J., Die Verinderungen des unbefruchteten Keimes des Hiihnereies 
im Hileiter und bei Bebriitungsversuchen. Zeitschr. wiss. Zool., Bd. XXII, 
1872. 

Patterson, J. THos., On Gastrulation and the Origin of the Primitive Streak 
in the Pigeon’s Egg. Preliminary Notice. Biol. Bull., Vol. XIII, 1907. 

PeREMESCHKO, Ueber die Bildung der Keimblitter im Hiihnerei. Sitzungs- 
ber. Wiener Akad. der Wiss. math.-nat. Kl., Bd. LVII, 1868. 

Rauser, A., Ueber die Stellung des Hiihnchens im Entwicklungsplan. 
Leipzig, 1876. 

Sopotra, J., Die Reifung und Befruchtung des Wirbeltiereies. Ergeb. 
Anat. u. Entwickelungsgesch., Bd. V, 1895. 


LITERATURE — CHAPTER III 


Epwarps, C. L., The Physiological Zero and the Index of Development for 
the Egg of the Domestic Fowl, Gallus Domesticus. Am. Journ. Physiol., 
Vol. VI, 1902. 

Eyciesuymer, A. C., Some Observations and Experiments on the Natural 
and Artificial Incubation of the Egg of the Common Fowl. Biol. Bull., 
Vol. XII, 1907. 

Frere, Cu., Note sur l’influence de la température sur incubation de l’ceuf 
de poule. Journ. de l’anatomie et de la physiologie, Paris, T. XXX, 
1894. 

LITERATURE — CHAPTERS IV AND V 


ASSHETON, R., An Experimental Examination into the Growth of the Blasto- 
derm of the Chick. Proce. Roy. Soe., London, Vol. LX, 1896. 
Batrour, F. M. The Development and Growth of the Layers of the Blas- 
toderm. Quar. Jour. Micr. Se., Vol. XIII, 1873. 
On the Disappearance of the Primitive Groove in the Embryo Chick. 
Thid. 
Batrour, F. M., and Derauron, A Renewed Study of the Germinal Layers 
of the Chick. Quar. Jour. Micr. Se., Vol. XXII, 1882. 
Dissz, J., Die Entwickelung des mittleren Keimblattes im Hiihnerei. Arch. 
mikr. Anat., Bd. XV, 1878. 
Drascu, O., Die Bildung der Somatopleura und der Gefiisse beim Hiithnchen. 
Anat. Anz., IX, 1894. 
Dursy, Emin, Der Primitivstreif des Hiihnchens. Lahr, 1866. 
Duvat, Marutas, Etudes sur la ligne primitive de l’embryon du_poulet. 
Ann. Se. Nat. Zool., Sér. 6, T. VII, 1878. 
De la formation du blastoderm dans l’ceuf d’oiseau. Ann. Se. Nat. 
Zool., Sér. 6, T. XVIII. Paris, 1884. 
Fox, H., Recherches sur le développement des protovertébres chez l’embryon 
du poulet. Arch. se. phys. et nat. Genéve, T. II, 1884. 
Gasser, Ueber den Primitivstreifen bei Vogelembryonen. Sitz.-Ber. d. Ges. 
z. Beford. d. ges. Naturw. z. Marburg, 1877. 
Der Primitivstreif bei Vogelembryonen (Huhn w. Gans). Schriften 
d. Ges. z. Beford. d. ges. Naturw. z. Marburg, Bd. XI, Suppl. Heft 1, 
1879. 


446 APPENDIX 


Gasser, Beitriige zur Kenntnis der Vogelkeimscheibe. Arch. Anat. u. 
Entw., 1882. 

Der Parablast und der Keimwall der Vogelkeimscheibe. Sitz.-Ber. 
d. Ges. z. Beférd. d. ges. Naturw. z. Marburg, 1883. 

GorettrE, A., Beitrige zur Entwickelungsgeschichte der Wirbeltiere. IT. 
Die Bildung der Keimblitter und des Blutes im Hiithnerei. Arch. mikr. 
Anat., Bd. X, 1874. 

Herrwia, O., Die Lehre von den Keimblittern. Handbuch der vergl. und 
exper. Entwickelungslehre der Wirbeltiere. Vol. I. Jena, 1903. 
His, W., Der Keimwall des Hithnereies und die Entstehung der para- 

blastisehen Zellen. Arch. Anat. und Entw., Bd. I, 1876. 

Neue Untersuchung tiber die Bildung des Hitthnerembryo. Arch. 
Anat. und Entw., 1877. 

Lecithoblast und Angioblast der Wirbelthiere. Histogenetische 
Studien. Abh. der math.-phys. Klasse der Kénigl. Sachs. Ges. der 
Wissenschaften, Bd. XXVI. Leipzig, 1900. 

Die Bildung der Somatopleura und der Gefisse beim Hithnchen. 
Anat. Anz., Bd. XXI, 1902. 

HorrMmann, C. K., Die Bildung des Mesoderms, die Anlage der Chorda dor- 
salis und die Entwickelung des Canalis neurentericus bei Vogelembry- 
onen. Ver6dffentl. d. kgl. Akad. d. Wiss. zu Amsterdam, 1883. 

Janosik, J., Beitrag zur Kenntnis des Keimwulstes bei Végeln.  Sitz.-Ber. 
Akad. Wiss. Wien, math.-phys. Kl., Bd. LXXXIV, 1882 

Kouuer, C., Beitrige zur Kenntnis des Hiihnerkeimes im Beginne der Be- 
briitung. Sitzungsber. Wien. Akad. Wiss., math.-nat. Kl., 1879. 

Untersuchungen tiber die Blitterbildung im Hihnerkeim. Arch. 
mikr. Anat., Bd. XX, 1881. 

v. Kéuumker, A., Zur Entwickelung der Keimblitter im Hihnerei. Verh. 
phys.-med. Ges. Wirzburg, Bd. VIII, 1875. 

Entwickelungsgeschichte des Menschen und der héheren Thiere. Zweite 
Auflage, erste Halfte. Leipzig, 1879. 

Korscu, Fr., Ueber die Bedeutung des Primitivstreifens beim Hiihnerembryo, 
und ber die ihm homologen Theile bei den Embryonen der niederen 
Wirbeltiere. Intern. Monatschr. f. Anat. u. Phys., Bd. XIX, 1902. 

MirrorpHanow, P. J., Teratogene Studien. II. Experimentellen Beo- 
bachtungen iiber die erste Anlage der Primitivrinne der Végel. Arch. 
Entw.-mech., Bd. VI, 1898. 

Beobachtungen iiber die erste Entwickelung der Vogel. Anat. 
Hefte, Bd. XII, 1899. 

Nowack, K., Neue Untersuchungen iiber die Bildung der beiden priméren 
Keimblitter und die Entstehung des Primitivstreifen beim Hihner- 
embryo. Inaug. Diss. Berlin, 1902. 

Parrerson, J. THos., The Order of Appearance of the Anterior Somites in 
the Chick. Biol. Bull., Vol. XIII, 1907. 

PrEBLES, FLORENCE, Some Experiments on the Primitive Streak of the 
Chick. Arch. Entw.-mech., Bd. VII, 1898. 

A Preliminary Note on the Position of the Primitive Streak and its 
Relation to the Embryo of the Chick. Biol. Bull., Vol. IV, 1903. 


APPENDIX 447 


PreErBes, FLORENCE, The Location of the Chick Embryo upon the Blasto- 
derm. Journ. Exp. Zool., Vol. I, 1904. 

PrreMEScHKO, Ueber die Bildung der Keimblitter im Hiihnerei.  Sitz.- 
ber. Wien. Akad. d. Wiss. math.-nat. KI., Bd. LVII, 1868. 

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

Rabu, C., Theorie des Mesoderms. Morph. Jahrb., Bde. XV und XIX, 
1889 and 1892. 

Rauser, A., Primitivstreifen und Neurula der Wirbelthiere, in normaler 
und pathologischer Beziehung. Leipzig, 1877. 

Ueber die embryonale Anlage des Hiihnchens. Centralb. d. med. 
Wiss., Bd. XII, 1875. 

Ueber die erste Entwickelung der V6gel und die Bedeutung der Primi- 
tivrinne. Sitz.-ber. d. naturf. Ges. zu Leipzig, 1876. 

Rex, Huao, Ueber das Mesoderm des Vorderkopfes der Ente. Archiv. 
mikr. Anat., Bd. L., 1897. 

Rickert, J., Entwickelung der extra-embryonalen Gefiisse der Vogel. Hand- 
buch der vergl. w. exp. Entw.-lehre der Wirbelthiere, Bd. I, T. 1, 
1906. 

Ueber die Abstammung der bluthaltigen Gefiissanlagen beim Huhn, 
und tuber die Entstehung des Randsinus beim Huhn und bei Torpedo. 
Sitzungsber. der Bay. Akad. Wiss., 1903. 

ScHAUINSLAND, H., Beitrige zur Biologie und Entwickelung der Hatteria 
nebst Bemerkungen iiber die Entwickelung der Sauropsiden. Anat. 
Anz. XV, 1899. 

VIALLETON, Développement des aortes chez Vembryon de poulet. Journ. 
de l’anat. T. XXVIII, 1892. See also Anat. Anz., Bd. VII, 1892. 
VircHow, H., Der Dottersack des Huhns. Internat. Beitrige zur wiss. 

Med., Bd. I, 1891. 

Wavpryer, W., Bemerkungen tiber die Keimblitter und den Primitivstreifen 
bei der Entwickelung des Htthnerembryo. Zeitschr. rationeller Medicin, 
1869. 

Wuirman, C. O., A Rare Form of the Blastoderm of the Chick and its Bearing 
on the Question of the Formation of the Vertebrate Embryo. Quar. 
Journ. Mier. Se., Vol. XXIII, 1883. 


Literature to Chapter VI included in following chapters. 


LITERATURE — CHAPTER VII 


CHARBONNEI-SALLE et Pursaurx, De |’évolution postembryonnaire du 
sac vitellin chez les oiseaux. C. R. Acad. Se., Paris, 1886. 

DareEste, C., Sur l’absence totale de l’amnios dans les embryons de poule. 
C. R. Acad. Sce., Paris, T. LX XXVIII, 1879. 

Duvat, M., Etudes histologiques et morphologiques sur les annexes des 
embryons d’oiseau. Journ. de l’anat, et de la phys., T. XX, 1884. 

Ktude sur Vorigine de l’allantoide chez le poulet. Rev. se. nat., 

Paris, 1877. 


448 APPENDIX 


DuvatL, M., Sur une organe placentoide chez V’embryon des oiseaux. C. R. 
Acad. Se., Paris, 1884. 

FROMANN, C., Ueber die Struktur der Dotterhaut des Huhnes.  Sitz.-ber. 
Jen. Ges. Medizin u. Naturw., 1879. 

FULLEBORN, F., Beitrige zur Entwickelung der Allantois der Végel.  Diss., 
Berlin, 1894. 

Gasser, E., Beitrige zur Entwickelungsgeschichte der Allantois, der Miiller- 
schen Ginge und des Afters. Frankfurt a. M., 1874. 

Gorrr, A., Beitraige zur Entwickelungsgeschichte des Darmkanals im Hiihn- 
chen. Tiibingen, 1867. 

Hirora, S., On the Sero-amniotie Connection and the Foetal Membranes in 
the Chick. Journ. Coll. Se. Imp. Univ. Japan, Vol. VI, Part IV, 1894. 

Linuir, Frank R., Experimental Studies on the Development of the Organs 
in the Embryo of the Fowl (Gallus domesticus): 1. Experiments on the 
Amnion and the Production of Anamniote Embryos of the Chick. Biol. 
Bull., Vol. V, 1908. 2. The Development of Defective Embryos and 
the Power of Regeneration. Biol. Bull., Vol. VII, 1904. 

Mertens, H., Beitrige zur Kenntniss der Fétushiillen im Vogelei. Meckels 
Archiv, 1830. 

MirrorHanow, P. J., Note sur la structure et la formation de l’enveloppe 
du jaune de l’ceuf de la poule.  Bibliogr. Anat., Paris, 1898. 

Poporr, Demerrius, Die Dottersackgefiisse des Huhnes. Wiesbaden, 1894. 

Port, R.,and Preyer, W., Ueber den Gaswechsel und die echemischen Verinder- 
ungen des Htthnereies wiihrend der Bebriitung. Archiv. ges. Phys., 1882. 

Preyer, W., Specielle Physiologie des Embryo. Leipzig, 1885. 

Ravn, E., Ueber die mesodermfreie Stelle in der Keimscheibe des Hithner- 
embryo. Arch. Anat. u. Entw., 1886. 

Ueber den Allantoisstiel des Hiihnerembryo. Verh. Anat. Ges., 1898. 

SCHAUINSLAND, H., Die Entwickelung der Hihiute der Reptilien und der 
Vogel. Handbuch der vergl. und exp. Entw.-lehre der Wirbeltiere. Bd. 
Tele 2 1902: 

Beitrige zur Entwickelungsgeschichte der Wirbeltiere. II. Beitrage zur 
Entwickelungsgeschichte der Eihiute der Sauropsiden. Bibliotheca 
Zoologica, 1903. 

ScHENK, 5S. L., Beitriige zur Lehre vom Amnion. Archiv. mikr. Anat., Bd. 
VII, 1871. 

Ueber die Aufnahme des Nahrungsdotters wiihrend des Embryonal- 
lebens.  Sitz.-ber. Akad. Wiss. Wien, math.-nat. K1., 1897. 

SHore, T. W., and Pickerina, J. W., The Proamnion and Amnion in the 
Chick. Journ. of Anat. and Phys., Vol. XXIV, 1889. 

SoBOLEFF, Die Verletzung des Amnions wiihrend der Bebriitung. Mittheil, 
embryolog. Inst., Wien, 1883. 

SprRAHL, H., Kihiute und Placenta der Sauropsiden. Ergeb. Anat. u. Entw.- 
gesch., Bd. I, 1891. 

Sruart, T. P. A., A Mode of Demonstrating the Developing Membranes in 
the Chick. Journ. Anat. and Phys., London, Vol. XXV, 1899. 

Vircnow, H., Beobachtungen am Hiihnerei; tiber das dritte Keimblatt 
im Bereiche des Dottersackes. Virehow’s Arch., Bd. LXII, 1874. 


APPENDIX 449 


Vircuow, H., Ueber das Epithel des Dottersackes im Hiihnerei. Diss., Berlin, 
1875. 
Der Dottersack des Huhnes. Internat. Beitrige zur wissenschaft. 
Medizin, Bd. I, 1891. 
Das Dotterorgan der Wirbeltiere. Zeitschr. wiss. Zool., Bd. LIIT, 
Suppl., 1892. 
Das Dotterorgan der Wirbelthiere. Arch. mikr. Anat., Bd. XL, 1892. 
Dottersyneytium, Keimhautrand und Beziehungen zur Koncrescenz- 
lehre. Ergeb. Anat. u. Entw., Bd. VI, 1897. 
Ueber Entwickelungsvorginge, welche sich in den letzten Bruttagen 
am Hiihnerei abspielen. Anat. Anz., Bd. IV, Berlin, 1889. 
Vurran, La physiologie de l’amnios et de l’allantoide chez les oiseaux. 
Mém. soe. biol., Paris, 1858. 
Wevpon, W. F. R., Prof. de Vries on the Origin of Species. (Includes experi- 
ments on amnion.) Biometrica, Vol. I, 1902. 


LITERATURE — CHAPTER VIII 


Bearp, J., Morphological Studies, II. The Development of the Peripheral 
Nervous System of Vertebrates. Pt. I. Elasmobranchs and Aves. 
Quar. Journ. Mier. Se., Vol. X XIX, 1888. 

Breraneck, E., Etudes sur les replis médullaires du poulet. Recueil Zool. 
Suisse, Vol. IV, 1887. 

Berne, ALtBRecut, Allgemeine Anatomie und Physiologie des Nervensys- 
tems. Leipzig, 1903. 

Branpis, F., Untersuchungen iiber das Gehirn der Vogel. Arch. mikr. 
Anat., Bd. XLI, 1893; Bd. XLIII, 1894; Bd. XLIV, 1895. 

Bumm, A., Das Grosshirn der Vogel (Anat.). Zeitschr. wiss. Zool., Bd. 
XXXVIII, 1883. 

Casa, S. R. y., Sur lorigine et les ramifications des fibres nerveuses de la 
moelle embryonnaire. Anat. Anz., Bd. V, 1890. 

A quelle époque aparaissent les expansions des cellules nerveuses de 
la moelle épiniére du poulet. Anat. Anz., Bd. V, 1890. 

Froriep, A., Ueber Anlagen von Sinnesorganen am Facialis, Glossopha- 
ryngeus und Vagus, tiber die genetische Stellung des Vagus zum Hypo- 
glossus, und itiber die Herkunft der Zungenmuskulatur. Arch. Anat. 
u. Entw., 1885. 

CARPENTER, FREDERICK WALTON, The Development of the Oculomotor Nerve, 
the Ciliary Ganglion, and the Abducent Nerve in the Chick. Bull. 
Mus. Comp. Zool. Harv. Vol. XLVIII, 1906. 

Dissz, J., Die erste Entwickelung des Riechnerven. Anat. Hefte, Abth. I, 
Bas dX 1897, 

Go ovine, E., Sur le développement du systéme ganglionnaire chez le poulet. 
Anat. Anz., Bd. V, 1890. 

Goronowitscu, N., Die axiale und die laterale (A. Goette) Kopfmetamerie 
der Végelembryonen. Anat. Anz., Bd. VII, 1892. 

Untersuchungen tiber die Entwickelung der Sogenannten ‘* Ganglien- 
leisten im Kopfe der Végelembryonen. Morph. Jahrb., Bd. XX, 1893. 


450 APPENDIX 


Hernricnw, Grora, Untersuchungen tiber die Anlage des Grosshirns beim 
Hiithnehen. Sitz.-ber. d. Ges. f. Morph. u. Phys. in Miinchen, Bd. XII, 
1897. 

Hitt, Cuaries, Developmental History of the Primary Segments of the 
Vertebrate Head. Zool. Jahrbiicher, Abth. Anat. Bd. XIII, 1900. 
His, W., Die Neuroblasten und deren Entstehung im embryonalen Mark. 
Abh. math.-physik. Klasse, Koénigl. Sachs. Ges. Wiss., Bd. XV, 1889. 
Histogenese und Zusammenhang der Nervenelemente. Arch. Anat. 

u. Entw., Suppl., 1890. 

Ueber das frontale Ende des Gehirnrohres. Arch. Anat. u. Entw., 1893. 
Ueber das frontale Ende und iiber die natiirliche Eintheilung des 
Gehirnrohres. Verh. anat. Ges., Bd. VII, 1893. 

His, W. (Jr.), Ueber die Entwickelung des Bauchsympathicus beim Hiihn- 
chen und Menschen. Arch. Anat. u. Entw., Suppl., 1897. 

v. Kouuiker, Ueber die erste Entwickelung der Nervi olfactorii. Sitz.-ber. 
phys. med. Ges. zu Wiirzburg, 1890. 

v. Kuprrer, K., Die Morphogenie des Centralnervensystems. Handbuch der 
vergl. und exp. Entwickelungslehre der Wirbeltiere, Kap. VIII, II’, 1905. 

MarsHati, A. M., The Development of the Cranial Nerves in the Chick. 
Quar. Journ. Micr. Se., Vol. XVIII, 1878. 

The Segmental Value of the Cranial Nerves. Journ. Anat. and Physiol., 
Vol. XVI, 1882. 

v. Minatcovics, V., Entwickelungsgeschichte des Gehirns. Leipzig, 1877. 

Munzer und Wiener, Beitrige zur Anatomie und Physiologie des Central- 
nervensystems der Taube. Monatschr. Psych. u. Neur., Bd. III, 1898. 

Onopi, A. D., Ueber die Entwickelung des sympathischen Nervensystems. 
Arch. mikr. Anat., Bd. XX VI, 1886. 

Ras, C., Ueber die Metamerie des Wirbelthierkopfes. Verh. anat Ges., 
VI, 1892. 

RuBAScCHKIN, W., Ueber die Beziehungen des Nervus trigeminus zur Riech- 
schleimhaut. Anat. Anz., Bd. XXII, 1903. 

SCHAPER, ALFRED, Die friihesten Differenzirungsvorgiinge im Centralnerven- 
system. Arch. Entw.-mech., Bd. V, 1897. 

Weser, A., Contribution A l’étude de la métamerism du cerveau antérieur 
chez quelques oiseaux. Arch. d’anat. microse., Paris, T. III, 1900. 
Van Wuue, J. W., Ueber Somiten und Nerven im Kopfe von Végel- und 

Reptilien-embryonen. Zool. Anz. Bd. IX, 1886. 
Ueber die Kopfsegmente und das Geruchsorgan der Wirbelthiere. 
Zool. Anz., Bd. IX, 1886. 


LITERATURE — CHAPTER IX 


ORGANS OF SPECIAL SENSE 


A. The Eye 


Appario, C., Sulla struttura del vitreo embryonale e de’ neonati, sulla ma- 
trice del vitreo e sull’ origine della zonula. Ann. Ottalmol., Anno 30, 
1901-1902. 


APPENDIX 451 


Apparto,C., Ueber die Matrix des Glaskérpers im menschlichen und thierischen 
Auge. Vorlaiuf. Mitth. Anat. Anz., Bd. XXI, 1902. 

AGABABOW, Untersuchungen iiber die Natur der Zonula ciliaris. Arch. 
mikr. Anat., Bd. L, 1897. 

AnGeE.tucctl, A., Ueber Entwickelung und Bau des vorderen Uvealtractus der 
Vertebraten. Arch. mikr. Anat., Bd. XIX, 1881. 

ARNOLD, J., Beitrage zur Entwickelungsgeschichte des Auges. Heidelberg, 

1874. 

ASSHETON, R., On the Development of the Optic Nerve of Vertebrates, and 
the Choroidal Fissure of Embryonic Life. Quar. Journ. Micr. Se., Vol. 
XXXIV, 1892. 

Bernp, ApotpH Huao, Die Entwickelung des Pecten im Auge des Hiihn- 
chens aus den Blattern der Augenblase. Bonn, 1905. 

Casa, S. R. y., Sur la morphologie et les connexions des éléments de la rétine 
des oiseaux. Anat. Anz. Bd. IV, 1889. 

Sur la fine structure du lobe optique des oiseaux et sur l’origine réelle 
des nerfs optiques. Int. Monatschr. Anat. u. Phys., Bd. VIII, 1891. 

CrrRINCIONE, G., Ueber die Entwickelung der Capsula perilenticularis. Arch. 
Anat. u. Entw., Suppl. Bd., Jahrg. 1897. 

Zur Entwickelung des Wirbeltierauges. Ueber die Entwickelung 
des Capsula perilenticularis. Leipzig, 1898. 

Ueber die Genese des Glaskérpers bei Wirbelthieren. Verh. Anat. 
Ges., 17. Versamml. in Heidelberg, 1903. 

CoLuIn, R., Recherches sur le développement du muscle sphincter de Viris 
chez les oiseaux. Bibliog. Anat., T. XII, fase. V. Paris, 1903. 

Froriep, A., Ueber die Entwickelung des Sehnerven. Anat. Anz., Bd. VI, 
1891. 

Die Entwickelung des Auges der Wirbeltiere. Handb. der vergl. u. 
exp. Entw.-l. der Wirbeltiere, Bd. IT, 1905. 

Huscuke, E., Ueber die erste Entwickelung des Auges und die damit zusam- 
menhiingende Cyklopie. Meckel’s Arch., 1832. 

Kessuer, L., Untersuchungen iiber die Entwickelung des Auges, angestellt 
am Hiihnchen und Tauben. Dissertation. Dorpat, 1871. 

Die Entwickelung des Auges der Wirbelthiere. Leipzig, 1877. 

v. Kouurker, A., Ueber die Entwickelung und Bedeutung des Glaskérpers. 
Verh. anat. Ges., 17. Vers. Heidelberg, 1903. 

Die Entwickelung und Bedeutung des Glaskérpers. Zeitschr. wiss. 
Zool., Bd. LX XVII, 1904. 

v. Lenuossek, M., Die Entwickelung des Glaskérpers. Leipzig, 1903. 

Lewis, W. H., Wandering Pigmented Cells Arising from the Epithelium of 
the Optic Cup, with Observations on the Origin of the M. Sphincter 
Pupille in the Chick. Am. Journ. Anat., Vol. II, 1903. 

Locy, W. A., Contribution to the Structure and Development of the Ver- 
tebrate Head. Journ. Morph., Vol. XI. Boston, 1895. 

Accessory Optic Vesicles in the Chick Embryo. Anat. Anz., Bd. XLV, 
1897. 

Nusssaum, M., Zur Riickbildung embryonaler Anlagen. (Corneal papillee 

of chick embryos.) Archiv. mikr. Anat., Bd. LVII, 1901. 


452 APPENDIX 


NusspauM, M., Die Pars ciliaris retina des Vogelauges. Arch. mikr. Anat., Bd. 
LVII, 1901. 

Die Entwickelung der Binnenmuskeln des Auges der Wirbeltiere. 
Arch. mikr. Anat., Bd. LVIII, 1901. 

Rast, C., Zur Frage nach der Entwickelung des Glaskérpers. Anat. Anz., 
Bd. XXII, 1903. 

Ueber den Bau und die Entwickelung der Linse. II. Reptilien und 
Vogel. Zeitschr. wiss. Zool., Bd. LXV, 1899. 

Ropinson, A., On the Formation and Structure of the Optic Nerve, and its 
Relation to the Optie Stalk. Journ. Anat. and Phys. London, 1896. 

Szit1, A.V. Beitrag zur Kenntniss der Anatomie und Entwickelungsgeschichte 
der hinteren Irisschichten, ete. Arch. Opthalm., Bd. LIIT, 1902. 

Zur Anatomie und Entwickelungsgeschichte der hinteren Irisschich- 
ten, ete. Anat. Anz., Bd. XX, 1901. 
Zur Glaskoérperfrage. Anat. Anz. Bd. XXIV, 1904. 

TorNaToua, Origine et nature du corps vitré. Rev. génér. d’opthalm. Année 
14, 1897. 

Ucke, A., Epithelreste am Opticus und auf der Retina. Arch. mikr. Anat., 
Bd. XXXVIII, 1891. 

Zur Entwickelung des Pigmentepithels der Retina. Diss. aus Dorpat. 
Petersburg, 1891. 

Vircuow, H., Facher, Zapfen, Leiste, Polster, Gefiasse im Glaskérperraum 
von Wirbelthieren, sowie damit in Verbindung stehenden Fragen. Er- 
gebn. Anat. u. Entw., Bd. X. Berlin, 1900. 

Weyssk, A. W., and BurGrss, W. 38., Histogenesis of the Retina. Am. 
Naturalist, Vol. XL, 1906. 


B. The Nose 


Born, G., Die Nasenhéhlen und der Thriinennasengang der amnioten Wir- 
belthiere II. Morph. Jahrb., Bd. V, 1879; Bd. VIII, 1883. 

Coun, Franz, Zur Entwickelungsgeschichte des Geruchsorgans des Hiihn- 
chens. Arch. mikr. Anat., Bd. LXI, 1903. 

DiruLarr, Leon, Les fosses nasales des vertébrés (morphologie et embry- 
ologie). Journ. de Vanat. et de la phys., T. 40 and 41, 1904 and 1905. 
(Translated by Hanau W. Loeb: Ann. of Otol., Rhin. and Laryng., Mar., 
June and Sept., 1906.) 

Disse, J., Die erste Entwickelung des Riechnerven. Anat. Hefte, Bd. IX, 
1897. 

GANIN, M., Einige Thatsachen zur Frage iiber das Jacobsohn’sche Organ der 
Vogel. Arb. d. naturf. Ges. Charkoff, 1890 (russisch). Abstr. Zool. 
Anz., 1890. 

vy. Kéuurker, A., Ueber die Entwickelung der Geruchsorgane beim Menschen 
und Hiihnehen. Wirzburger med. Zeitschr., Bd. I, 1860. 

vy. Minarkovics, V., Nasenhéhle und Jacobson’sche Organ. Anat. Hefte, 
I. Abth., Bd. XI, 1898. 

Perer, Karu, Entwickelung des Geruchsorgans und Jakobson’sche Organs 
in der Reihe der Wirbeltiere. Bildung der fiusseren Nase und des 


APPENDIX 453 


Gaumens. Handbuch der vergl. und experiment. Entwickelungslehre 
der Wirbeltiere. II’, 1902. 
PREOBRASCHENSKY, L., Beitrage zur Lehre tiber die Entwickelung des Ge- 
ruchsorganes des Huhnes. Mitth. embryol. Inst. Wien, 1892. 
Purevu, F., Ueber das Verhalten der Zellen der Riechschleimhaut bei 
Hiihnerembryonen friiher Stadien. Mitth. embr. Inst. Wien, 1889. 


C. Phe Ear. 


Hasse, C., Beitrage zur Entwickelung der Gewebe der hiautigen Vogel- 
schnecke. Zeitschr. wiss. Zool., Bd. XVII, 1867. 

Huscuke, Ueber die erste Bildungsgeschichte des Auges und Ohres beim 
bebriiteten Hiihnchen. Isis von Oken, 1831. 

KastscHENKO, N., Das Schlundspaltengebiet des Hiihnchens. Arch. Anat. 
u. Entw., 1887. 

KeEIBEL, Ueber die erste Bildung des Labyrinthanhanges. Anat. Anz., Bd. 
XVI, 1899. 

Krause, R., Die Entwickelung des Aqueeductus Vestibuli, s. Ductus endo- 
lymphaticus. Anat. Anz., Bd. XIX, 1901. 

Die Entwickelungsgeschichte des hiutigen Bogenganges. Arch. mikr. 

Anat., Bd. XX XV, 1890. 

MotpEnHAuER, W., Die Entwickelung des mittleren und des iiusseren Ohres. 
Morph. Jahrb., Bd. III, 1877. 

Pout, C., Sviluppo della vesicula auditiva; studio morphologico. Genoa, 
1896. 

Zur Entwickelung der Gehérblase bei den Wirbeltieren. Arch. mikr. 

Anat., Bd. XLVIII, 1897. 

Rerzius, G., Das Gehérorgan der Wirbelthiere. II. Theil, Reptilien Vogel, 
Saéuger. Stockholm. 1881-1884. 

Roruic, P., und Bruescu, THEeopor, Die Entwickelung des Labyrinthes 
beim Huhn. Archiv. mikr. Anat., Bd. LIX, 1902. 

Rupincer, Zur Entwickelung des haiutigen Bogenganges des inneren Ohres. 
Sitzungsber. Akad. Miinchen, 1888. 


LITERATURE — CHAPTER X 


THe ALIMENTARY TrRAcT AND Its APPENDAGES 


A. The Oral Cavity and Organs 


FratssgE, P., Ueber Zihne bei Végeln. Vortrag, geh. in der phys.-med. 
Ges. Wiirzburg, 1880. 

GARDINER, E. G., Beitriige zur Kenntniss des Epitrichiums und der Bildung 
des Vogelschnabels. Inaug. Dissert. Leipzig, 1884. Arch. mikr. Anat., 

Bd. XXIV, 1884. 

Gaupp, E., Anat. Untersuchungen itiber die Nervenversorgung der Mund- 
und Nasenhohledriisen der Wirbeltiere. Morph. Jahrb., Bd. XIV, 1888. 

Giacomini, E., Sulle glanduli salivari degli uecelli. Richerche anatomico- 
embrologiche. Monit. zool. Ital., Anno 1, 1890. 


454 APPENDIX 


Gorrert, E., Die Bedeutung der Zunge fiir den secundiren Gaumen und den 
Ductus naso-pharyngeus. Beobachtungen an Reptilien und Vé6geln. 
Morph. Jahrb., Bd. XX XI, 1903. 

Katurus, E., Die mediane Thyreoideaanlage und ihre Beziehung zum Tuber- 
culum impar. Verh. anat. Ges., 17. Vers., 1903. 

Beitrige zur Entwickelung der Zunge. Verh. anat. Ges., 15. Vers. 
Bonn, 1901. 

Manno, ANpREA, Sopra il modo onde si perfora e scompare le membrana 
faringea negli embrioni di pollo. Richerche Lab. Anat. Roma, Vol. 
IX, 1902. 

Opret, A., Lehrbuch der vergleichenden mikroskopischen Anat. der Wir- 
beltiere. Jena, 1900. 

Reicuer, P., Beitrag zur Morphologie der Mundhohlendriisen der Wirbel- 
thiere. Morph. Jahrb., Bd. VIII, 1885. 

Rosp, C., Ueber die Zahnleiste und die Eischwiele der Sauropsiden. Anat. 
Anz., Bd. VII, 1892. 

Sturrer, C. P., Ueber den Eizahn und die Eischwiele einiger Reptilien. 
Morph. Jahrb., Bd. XX, 1893. 

Yarrevi, W., On the Small Horny Appendage to the Upper Mandible in 
Very Young Chickens. Zool. Journal, 1826. 


B. Derivatives of the Embryonic Pharynx 


van BemME.eN, J. F., Die Visceraltaschen und Aortenbogen bei Reptilien 
und Végeln. Zool. Anz., 1886. 
His, W., Ueber den Sinus praecervicalis und die Thymusanlage. Arch. 
Anat. u. Entw., 1886. 
Schlundspalten und Thymusanlage. Arch. Anat. u. Entw., 1889. 
Der Tractus Thyreoglossus und seine Beziehung zum Zungenbein. 
Arch. Anat. u. Entw., 1891. 
KastscHenko, N., Das Schlundspaltengebiet des Hiithnchens. Arch. Anat. 
und Entw., 1887. 
Liessner, E., Ein Beitrag zur Kenntniss der Kiemenspalten und ihrer An- 
lagen bei amnioten Wirbelthieren. Morph. Jahrb., Bd. XIIT, 188s. 
Matu, I’. P., Entwickelung der Branchialbogen und Spalten des Htthnchens. 
Arch. Anat. und Entw., 1887. 

pe Meuron, P., Recherches sur le développement du thymus et de la glande 
thyreoide. Dissertation, Genéve, 1886. 

Mtuier, W., Ueber die Entwickelung der Schilddriise. Jen. Zeitschr., Bd. 
VI, 1871. 

Sresset, A., Zur Entwickelungsgeschichte des Vorderdarms. Arch. Anat. 
und Entw., 1877. 

Verpun, M. P., Sur les dérivés branchiaux du poulet. Comptes rendus 
Soc. Biol., Tom. V. Paris, 1898. 

Dérivés branchiaux chez les vertébrés supérieurs. Toulouse, 1898. 


APPENDIX 455 


C. Esophagus, Stomach, Intestine 


Bornuavrt, TH., Untersuchungen tiber die Entwickelung des Urogenital- 
systems beim Hiihnchen. Inaug. Diss. Riga, 1867. 

CarraNneo, G., Intorno a un recente lavoro sullo stomaco degli uccelli. Pavia, 
1888. 

Istologia e sviluppo del apparato gastrico degli uccelli. Atti della 
Soe. Ital. di Se. Nat., Vol. XX VII, Anno 1884. Milano, 1885. 

Cazin, M., Recherches anatomiques, histologiques et embryologiques sur 
Vappareil gastrique des oiseaux. Ann. Se. Nat. Zool. 7 sér., Tom. IV, 
1888. 

Sur le développement embryonnaire de l’estomac des oiseaux. Bull. 
de la société philomathique de Paris. 7 sér., Tom. XI, Paris, 1887. 

Développement de la couche cornée du gesier du poulet et des glandes 
qui la séerétent. Comptes rendus, T. CI, 1885. 

Ciortta, M., Beitrage zur mikroskopischen Anatomie des Vogeldarmes. 
Archiv. mikr. Anat., Bd. XLI, 1893. 

FLEISCHMANN, ALBERT, Morphologische studien tiber Kloake und Phallus der 
Amnioten. III. Die Végel, von Dr. Carl Pomayer. Morph. Jahrb., 
Bd. XXX, 1902. 

Gasser, E., Beitrage zur Entwickelungsgeschichte der Allantois, Miiller- 
schen Giinge und des Afters. Frankfurt a. M., 1893. 

Die Entstehung der Kloakenéffnung bei Hiihnerembryonen. Arch. 
Anat. u. Entw., 1880. 

Maurer, F., Die Entwickelung des Darmsystems. Handb. d. vergl. u. 
exp. Entw.-lehre der Wirbeltiere. II', 1902. 

v. Mrnaucovics, V., Untersuchungen tiber die Entwickelune des Harn- und 
Geschlechtsapparates der Amnioten. Internat. Monatschr. Anat. u. 
Phys., Bd. II, 1885-1886. 

Minot, C.S8., On the Solid Stage of the Large Intestine in the Chick. Journ. 
Bos. Soc. Med. Se., Vol. IV, 1900. 

PomMayeEr, Carb. See Fleischmann. 

Rerrerer, E., Contributions a l’étude du cloaque et de la bourse de Fabricius 
chez des oiseaux. Journ. de l’anat. et de la phys. 21 An. Paris, 1885. 

SEYFERT, Beitrige zur mikroskopischen Anatomie und zur Entwickelungs- 
geschichte der blinden Anhiainge des Darmeanals bei Kaninchen, Taube 
und Sperling. Inaug. Diss. Leipzig, 1887. 

Scuwarz, D., Untersuchungen des Schwanzendes bei den Embryonen der 
Wirbeltiere. Zeitschr. wiss. Zool., Bd. XLVIII, 1889. 

Stiepa, L. Ludwie, Ueber den Bau und die Entwickelung der Bursa Fabricii. 
Zeitschr. wiss. Zool., Bd. XXXIV, 1880. 

SWENANDER, G., Beitriige zur Kenntniss des Kropfes der Vogel. Zool. Anz., 
Bd. XXII, 1899. 

Weser, A., Quelques faits concernant le développement de l’intestin moyen, 
et de ses glandes annexes chez les oiseaux. C. R. Soc. Biol., T. LIV. Paris, 
1902. 

WENCKEBACH, K. F., De Ontwikkeling en de bouw der Bursa Fabricii. In- 
aug. Dissert. Leiden, 1888. 


456 APPENDIX 


D. Liver and Pancreas 


Bracuet, A., Die Entwickelung und Histogenese der Leber und des Pancreas. 
Ergebnisse d. Anat. u. Entw.-gesch., 1896. 

Brouna, M., Recherches sur le développement du foie, du pancréas, de la 
cloison mesentérique et des cavités hepato-entériques chez les oiseaux. 
Journ. de l’anat. et phys., T. XXXIV. Paris, 1898. 

Sur les premiéres phases du foie et sur l’évolution des paneréas ven- 
traux chez les oiseaux. Anat. Anz., Bd. XIV, 1898. 

CHoronscuirzky, B., Die Entstehung der Milz, Leber, Gallenblase, Bauch- 
speicheldriise und des Pfortadersystems bei den verschiedenen Abthei- 
lungen der Wirbelthiere. Anat. Hefte, Bd. XIII, 1900. 

Fenix, W., Zur Leber und Pancreasentwickelung. Arch. Anat. u. Entw., 1892. 

FROBEEN, F., Zur Entwickelung der Vogelleber. Anat. Hefte, 1892. 

Gorrr, ALEX., Beitriige zur Entwickelungsgeschichte des Darmeanals im 
Hiihnehen. Tiibingen, 1867. 

Hammar, G. A., Ueber Duplicitit ventraler Pancreasanlage. Anat. Anz., 
Bd. XIII, 1897. 

Ueber einige Hauptziige der ersten embryonalen Leberentwickelung. 
Anat. Anz., Bd. XIII, 1897. 

Hinige Plattenmodelle zur Beleuchtung der friiheren embryonalen 
Leberentwickelung. Arch. Anat. u. Entw., 1893. 

Minot, C. S., On a Hitherto Unrecognized Form of Blood-Cireulation without 
Capillaries in the Organs of Vertebrata. Proce. Boston Soe. of Nat. 
Hist., Vol. NXIX, 1900. 

ScHREINER, K. E., Beitrige zur Histologie und Embryologie des Vorder- 
darms der Vogel. Zeitsehr. wiss. Zool., Bd. LX VIII, 1900. 

SHore, T. W., The Origin of the Liver, Journ. of Anat. and Phys., Vol. XXV, 
1890-91. 

Saint-Remy, Sur le développement du pancréas chez les oiseaux. Rey. 
biol. du Nord de la France. Année VY, 1893. 


EK. The Respiratory Tract 


Bar, M., Beitriage zur Kenntniss der Anatomie und Physiologie der Athem- 
werkzeuge bei den Végeln. Zeitschr. wiss. Zool., Bd. LXI, 1896. 
Berrevur, D., Sviluppo de sacchi aeriferi del pollo. Divisione della cavita 
celomatiea degli uecelli. Atti della Societa Toscana di scienze naturali 

residente in Pisa. Memorie, Vol. XVII, 1899. 

BLUMSTEIN-JUDINA, Berita, Die Pneumatisation des Markes der Vogelkno- 
chen. Anat. Hefte, Abth. I, Bd. XXIX (Heft 87), 1905. 

Campana, Recherches d’anatomie de physiologie, et d’organogénie pour la 
détermination des lois de la genése et de Vevolution des espéces ani- 
mals. I. Mémoire. Physiologie de la respiration chez les oiseaux. 
Anatomie de l’appareil pneumatique pulmonnaire, des faux diaphragmes, 
des séremus et de Vintestin chez le poulet. Paris, Masson, 1875. 

Gorprert, E., Die Entwickelung der luftfithrenden Anhinge des Vorder- 
darms. Handbuch d. vergl. u. exp. Entw.-lehre der Wirbeltiere, Bd. 
IL, Te 1, 1902. 


APPENDIX 457 


Raruke, M. H., Ueber die Entwickelung der Atemwerkzeuge bei den Vogeln 
und Siugetieren. Nov. Act. Acad. Caes. Leop. Car., T. XIV. Bonn, 1828. 

SeLenka, E., Beitrage zur Entwickelungsgeschichte der Luftsiicke des 
Huhnes. Zeitschr. wiss. Zool., Bd. XVI, 1866. 

Srrasser, H., Die Luftsiicke der Vogel. Morph. Jahrb., Bd. III, 1877. 

Weser, A., et BuviGNier, A., Les premiéres phases du développement du 
poumon chez les embryons de poulet. Comptes rendus hébd. des séances 
de la société de Biologie, Vol. LV. Paris, 1903. 

Wonper.icu, L., Beitrage zur vergleichenden Anatomie und Entwickelungs- 
geschichte des unteren Kehlkopfes der Vogel. Nova Acta Acad. Caes. 
Leop. Carol. Germanicae, Bd. XLVIII, 1884. 

ZuMSTEIN, J., Ueber den Bronchialbaum der Siuger und Vogel.  Sitz.-ber. 
Ges. z. Beford. d. ges. Naturwiss. Marburg, 1900. 


LITERATURE — CHAPTER XI 


Bepparp, F. E., On the Oblique Septa (“ Diaphragm’ of Owen) in the Pas- 
serines and some other Birds. Proce. Zool. Soe. London, 1896. 

Berteu, D., Sullo sviluppo del diaframma dorsale nel Pollo. Nota pre- 
ventiva. Monit. Zool. Ital., Anno IX, 1898. 

Contributo alla morfologia ed allo sviluppo del diaframma._ ornitico. 
Ibid., 1898. 

Bracuet, A., Die Entwickelung der grossen Kérperhéhlen und ihre Tren- 
nung von einander, etc. Ergebnisse d. Anat. u. Entw.-gesch., Bd. VII, 
1897. 

Broman, Ivar, Die Entwickelungsgeschichte der Bursa omentalis und &hn- 
licher Recessbildungen bei den Wirbeltieren. Wiesbaden, 1904. 

Brouna, M. See Chap. X. 

Butter, G. W., On the Subdivision of the Body Cavity in Lizards, Croco- 
diles and Birds. Proc. Zoél. Soc. London, 1889. 

Cuoronscuitzky, B. See Chap. X. 

Darestr, C., Sur la formation du mésentére et de la gouttiére intestinale 
dans V’embryon de la poule. Comptes rendus, T. CXII, 1891. 

Hocustetrer, F., Die Entwickelung des Blutgefiisssystems. Handbuch 
der vergl. und exp. Entw.-lehre der Wirbeltiere. III”, 1903. 

Janosik, J., Le pancréas et la rate. Bibliographie Anat. Année 3. Paris, 
1895. 

Lockwoop, C. B., The Early Development of the Pericardium, Diaphragm 
and Great Veins. Phil. Trans. Roy. Soc., London, Vol. CLXXIX, 1889. 

Matt, F. P., Development of the Lesser Peritoneal Cavity in Birds and 
Mammals. Journ. Morph., Vol. V, 1891. 

Maurer, F., Die Entwickelung des Darmsystems. Handbuch d. vergl. u. 
exp. Entw.-lehre d. Wirbeltiere, Vol. II, 1906. 

PreremMescuko, Ueber die Entwickelung der Milz. Sitzungsber. d. Akad. d. 
Wiss. in Wien, math., naturwiss. Klasse, Bd. LVI, Abth. 2, 1867. 
Ravn, E., Die Bildung des Septum transversum beim Hithnerembryo. Arch. 

Anat. u. Entw., 1896. See also Anat. Anz., Bd. XV, 1899. 


458 APPENDIX 


Reicuert, Entwickelungsleben im Wirbeltierreich. Berlin, 1840. 

Remak, Untersuchungen tiber die Entwickelung des Wirbeltierreichs, p. 60, 
1850-1855. 

Usxow, W., Ueber die Entwickelung des Zwerchfells, des Pericardium und 
des Coeloms. Arch. mikr. Anat., Bd. XXIT, 1883. 

Worr, O., Zur Entwickelung der Milz. Anat. Hefte, Bd. IX, 1897. 


LITERATURE — CHAPTER XII 


vy. Barr, K. E., Ueber die Kiemen und Kiemengefisse im den Embryonen 
der Wirbeltiere. Meckel’s Archiv., 1827. 

vAN BeMMELEN, J., Die Visceraltaschen und Aortenbogen bei Reptilien und 
Vogeln. Zool. Anz., 1886. 

Boas, J. E. V., Ueber die Aortenbogen der Wirbeltiere. Morph. Jahrb., 
Bd. XIII, 1887. 

Brounwa. See Chap. X. 

Hocusterrer, I., Die Entwickelung des Blutgefiisssystems (des Herzens 
nebst Herzbeutel und Zwerchfell, der Blut- und Lymphgefisse, der 
Lymphdriisen und der Milz in der Reihe der Wirbeltiere). Handbuch 
der vergl. und exp. Entwickelungslehre der Wirbeltiere. III’, 1903. 

Beitriige zur Entwickelungsgeschichte des Venensystems der Amnioten. 
I. Hiihnehen. Morph. Jahrb., Bd. XIII, 188s. 

Ueber den Ursprung der Arteria Subclavia der Végel. Morph. Jahrb, 
Bd. XVI, 1890. 

Entwickelung des Venensystems der Wirbeltiere. Ergeb. der Anat. 
u. Entw., Bd. III, 1893. 

Huscuke, E., Ueber die Kiemenbogen und Kiemengefiisse beim bebriiteten 
Hiihnehen. Isis, Bd. XX, 1827. 

Lanaer, A., Zur Entwickelungsgeschichte des Bulbus cordis bei Végeln und 
Sdiugetieren. Morph. Jahrb., Bd. XNXIT, 1894. 

Linpes, G., Ein Beitrag zur Entwickelungsgeschichte des Herzens. Disser- 
tation. Dorpat, 1865. 

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

Mackay, J. Y., The Development of the Branchial Arterial Arches in Birds, 
with Special Reference to the Origin of the Subeclavians and Carotids. 
Phil. Trans. Roy. Soc., London, Vol. CLA XIX, 1889. 

Mastus, J., Quelques notes sur le développement du cceur chez le poulet. 
Arch. Biol., T. IX, 1889. 

Miutter, W. 8., The Development of the Postcaval Veins in Birds. Am. 
Journ. Anat., Vol. II, 1903. 

Pororr, D., Die Dottersackgefiisse des Huhnes. Wiesbaden, 1894. 

2aruKeE, H., Bemerkungen tiber die Entstehung der bei manchen Voégeln 
und den Krokodilen vorkommenden unpaaren gemeinschaftlichen Carotis. 
Arch. Anat. u. Phys., 1858. 

Roser, C., Beitrige zur vergleichenden Anatomie des Herzens der Wirbel- 


tiere. Morph. Jahrb., Bd. XVI, 1890. 


APPENDIX 459 


Ross, C., Beitrige zur Entwickelungsgeschichte des Herzens. Inaug. Dissert. 
Heidelberg, 1888. 

Tonaer, Morris, On the Development of the Semilunar Valves of the Aorta 
and Pulmonary Artery of the Chick. Phil. Trans. Roy. Soc., London, 
Vol. CLIX, 1869. 

TWINinGc, GRANVILLE H., The Embryonic History of the Carotid Arteries 
in the Chick. Anat. Anz., Bd. XXIX, 1906. 

VIALLETON, L., Développement des aortes postérieures chez l’embryon de 
poulet: C2 R:iSoc. Biol. i. Til Paris, is9r. 

Développement des aortes chez Vembryon de poulet. Journ. de 
Vanat. et phys., T. XXVIII, 1892. 

ZUCKERKANDL, E., Zur Anat. und Entwickelungsgeschichte der Arterien des 
Unterschenkels und des Fusses. Anat. Hefte, Bd. V, 1895. 

Zur Anatomie und Entwickelungsgeschichte der Arterien des Vor- 
derarmes. Anat. Hefte, Bd. IV, 1894. 


LITERATURE — CHAPTER XIII 


ABRAHAM, K., Beitrige zur Entwickelungsgeschichte des Wellensittichs. 
Anat. Hefte, Bd. XVII, 1901. 

Barrour, F. M., On the Origin and History of the Urogenital Organs of 
Vertebrates. Journ. of Anat. and Physiol., Vol. X, 1876. 

Batrour and Sepa@wick, On the Existence of a Rudimentary Head Kidney 
in the Embryo Chick. Proc. R. Soc., London, Vol. XX VII, 1878. 

On the Existence of a Head Kidney in the Embryo Chick and on 
Certain Points in the Development of the Millerian Duet. Quar. Journ. 
Micr. Sc., Vol. XIX, 1879. 

Bornuaupt, TuH., Zur Entwickelung des Urogenitalsystems beim Hiihnchen. 
Inaug. Diss. Dorpat, 1867. 

Branpt, A., Ueber den Zusammenhang der Glandula suprarenalis mit dem 
parovarium resp. der Epididymis bei Hithnern. Biolog. Centralbl., 
Bd. IX, 1889. 

Anatomisches und allgemeines tiber die sog. Hahnenfedrigkeit und 
uber anderweitige Geschlechtsanomalien der Vogel. Zeitschr. wiss. Zool., 
Bd. XLVIII, 1889. 

Erzoip, F., Die Entwickelung des Testikel von Fringilla domestica von der 
Winterruhe bis zum Eintritt der Brunst. Zeitschr. wiss. Zool., Bd. 
LII, 1891. 

Feuix, W., Zur Entwickelungsgeschichte der Vorniere des Hiihnchens. 
Anat. Anz., Bd. V, 1890. 

Frevuix und Bunter, Die Entwickelung der Harn- und Geschlechtsorgane. 
I. Abschnitt — Die Entwickelung des Harnapparates, von Prof. Felix. 
Handbuch der vergl. u. exper. Entw.-lehre der Wirbeltiere, IIT', 1904. 

FUrBRINGER, M., Zur vergleichenden Anatomie und Entwickelungsgeschichte 
der Excretionsorgane der Vertebraten. Morph. Jahrb., Bd. IV, 1878. 

Fusart, R., Contribution a l’étude du développement des capsules surré- 
nales et du sympathétique chez le poulet et chez les mammiféres. Ar- 
chives. Ital. de biologie, T. XVI, 1892. 


460 APPENDIX 


Gasser, E., Beitrige zur Entwickelungsgeschichte der Allantois, der Miiller- 
schen Giinge und des Afters. Frankfurt a. M., 1874. 
Die Entstehung des Wolff’sechen Ganges beim Huhn. Sitz.-ber. 
Naturf. Ges., Marburg, Jahre. 1875. 
Beobachtungen wber die Entstehune des Wolff’schen Ganges bei 
Embryonen von Hiithnern und Giinsen. Arch. mikr. Anat., Bd. XIV, 1877. 
Gasser, E., und SrEMMERLING, Beitriige zur Entwickelung des Urogenitalsys- 
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Geruarpt, U., Zur Entwickelung der bleibenden Niere. Arch. mikr. Anat., 
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Hocusterrer, I*., Zur Morphologie der Vena cava inferior. Anat. Anz., Bd. III, 
ISSS. 
HOFFMANN, 


1 


KX., Etude sur le développement de l’appareil urogenital des 
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Janosik, J., Bemerkungen tiber die Entwickelung der Nebennieren. Archiv. 
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Histologisch-embryologische Untersuchungen iiber das Urogenital- 
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3. Abth., 1885. 

Kose, W., Ueber die Carotisdriise und das ‘‘Chromaffine Gewebe’’ der Vogel. 
Anat. Anz., Bd. XXV, 1904. 

JIkowauevsky, R., Die Bildung der Urogenitalanlage bei Hiihnerembryonen. 
Stud. Lab. Warsaw Univ., II, 1875. 

Kurrrer, C., Untersuchungen tiber die Entwieckelung des Harn- und Ge- 
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v. Minaucovics, V., Untersuchungen tiber die Entwickelung des Harn- 
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Minervint, R., Des capsules surrénales: Développement, structure, fone 
tions. Journ. de l’anat. et de la phys, An. XL. Paris, 1904. 

Nussspaum, M., Zur Differenzierung des Geschlechtes im Thierreich. Arch. 
mikr. Anat., Bd. XVIII, 1880. 

Zur Entwickelung des Geschlechts beim Huhn. Verh. anat. Ges., Bd 
XV, 1901. 

Zur Riackbildung embryonaler Anlagen. Arch. mikr. Anat., Bd 
LVII, 1901. 

Zur Entwickelung des Urogenitalsystems beim Huhn. C. R. Ass. 
d. An. Ses3., 5. Liége, 1903. 

Pout, H., Die Entwickelune der Nebennierensysteme. Handbuch der 
vergl. und exper. Entwickelungslehre der Wirbeltiere. IIT, 1906. 
PrENANT, A., Remarques A propos de la constitution de la glande génitale 
indifférente et de Vhistogénése du tube séminifére. C. R. Soe. biol., 

Sér. 9, T. IT, 1890. 

Rasy, H., Die Entwickelung und Struktur der Nebennieren bei den Vo6geln. 
Arch. mikr. Anat., Bd. XX XVIII, 1891. 

Renson, G., Recherches sur le rein céphalique et le corps de Wolff chez les 
oiseaux et les mammiféres. Arch. mikr. Anat., Bd. XXII, 1883. 


APPENDIX 461 


Rickert, J., Entwickelung der Excretionsorgane. Ergebnisse der Anat. 
u. Entw.-gesch., Bd. I, 1892. 

ScHMIEGELOW, E., Studien iiber die Entwickelung des Hodens und Neben- 
hodens. Arch. Anat. u. Entw., 1882. 

Scuretner, K. E., Ueber die Entwickelung der Amniotenniere. Zeitschr. 
wiss. Zool., Bd. LX XI, 1902. 

Sepewick, A., Development of the Kidney in its Relation to the Wolffian 
Body in the Chick. Quart. Journ. Mier. Se., Vol. XX, 1880. 

On the Early Development of the Anterior Part of the Wolffian Duct 
and Body in the Chick, together with Some Remarks on the Excretory 
System of Vertebrata. Quart. Journ. Micr. Se., Vol. XXI, 1881. 

Semon, Ricuwarp, Die indifferente Anlage der Keimdriisen beim Hiihnechen 
und ihre Differenzierung zum Hoden. Jen. Zeitschr. Naturwiss., Bd. 
XXI, 1887. 

SIEMERLING, E., Beitrige zur Embryologie der Excretionsorgane des Vogels. 
Inaug. Dissert. Marburg, 1882. 

Souuiz, A. H., Recherches sur le développement des capsules surrénales 
chez les vertébrés supérieurs. Journ. de Vanat. et phys., Paris, An. 
XXXIX, 1903. 

VALENTI, G., Sullo sviluppo delle capsule surrenali nel pollo e in aleuni mam- 
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Wa.LpeEyer, W., Eierstock und Ei. Ein Beitrag zur Anatomie und Ent- 
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WELDON, On the Suprarenal Bodies of Vertebrates. Quar. Journ. Micr. 
Se., Vol. XXV, 1884. 


LITERATURE — CHAPTER. XIV 


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BLUMSTEIN-JUDINA, Berta, Die Pneumatisation des Markes der Vogelkno- 
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Bracuet, A., Etude sur la resorption de cartilage et le développement des 
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Braun, M., Entwickelung des Wellenpapageis. Arb. Zool. Zoot. Inst. Wiirz- 
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Bru.tuiké et Huaureny, Développement des os des oiseaux. Ann. Se. Nat., 
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Bunae, A., Untersuchungen zur Entwickelungsgeschichte des Beckengiirtels 
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462 APPENDIX 


Urwirbel und Neugliederung der Wirbelsiiule. Sitzungsber. d. k. 
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Frorrer, A., Zur Entwickelungsgeschichte der Wirbelsiiule, insbesondere 
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Gaupp, E., Die Entwickelung des Kopfskelettes. Handbuch der verel. u. 
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Die Entwickelung der Wirbelsiule. Zool. Centralbl., Jahrg. III, 1896. 
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GeGEenBAuR, C., Untersuchungen zur vergl. Anat. der Wirbelsiiule bei 
Amphibien und Reptilien. Leipzig, 1864. 

Beitrige zur Kenntniss des Beckens der Végel. Eine vergleichende 
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Die Metamerie des Kopfes und die Wirbeltheorie des Kopfskelettes, 
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Gorrrr, A., Die Wirbelsiiule und ihre Anhinge. Arch. mikr. Anat., Bd. 
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Herpurn, D., The Development of Diarthrodial Joints in Birds and Mam- 
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Jager, G., Das Wirbelkérpergelenk der Vogel. Sitzungsber. Akad. Wien, 
Bd. XXXIII, 1858. 

Jounson, Auice, On the Development of the Pelvie Girdle and Skeleton 
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Kunezycext, W., Zur Entwickelungsgeschichte des Sehultergiirtels bei den 
Vogeln mit besonderer Beriicksichtigung des Schliisselbeines (Gallus, 
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Leiauton, V. L., The Development of the Wing of Sterna Wilsonii. Am. 
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Ltuper, W., Zur Bildung des Brustbeins und Schultergiirtels der Vogel. 
Journ. Ornith., 1871. 

MAnnicu, H., Beitrage zur Entwickelung der Wirbelsiiule von Eudyptes 
chrysocome. Inaug. Diss. Jena, 1902. 

MexNnert, HMrnst, Untersuchungen tiber die Entwickelung des Os Pelvis 
der Vogel. Morph. Jahrb., Bd. XIII, 1887. 

Kainogenesis als Ausdruck differenter phylogenetischer Energieen. 
Morph. Arb: Bab VIL. 1897. 

Morsg, E. 8., On the Identity of the Ascending Process of the Astragalus 
in Birds with the Intermedium. Anniversary Mem. Boston Soc. Nat. 
Hist., 1880. 

Norsa, E., Aleune richerche sulla morphologia dei membri anteriori degli 
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T. XXII, 1894. 

Parker, W. Ix., On the Structure and Development of the Skull of the Com- 
mon low! (Gallus domesticus). Phil. Trans., Vol. CLIX, 1869. 


APPENDIX 463 


Parker, W. K., On the Structure and Development of the Birds’ Skull. 
Trans. Linn. Soc., 1876. 

On the Structure and Development of the Wing of the Common Fowl. 
Phil. Trans., 1888. 

Remak, R., Untersuchungen tiber die Entwickelung der Wirbeltiere. Berlin, 
1850-1855. 

Rosensera, A., Ueber die Entwickelung des Extremitiitenskelets bei einigen 
durch die Reduction ihrer Gledmaassen charakteristischen Wirbeltiere. 
Zeitschr. wiss. Zool., Bd. X XIII, 1873. 

ScHAUINSLAND, H., Die Entwickelung der Wirbelsiiule nebst Rippen und 
Brustbein. Handbuch der vergl. und exper. Entw.-lehre der Wirbel- 
tiere, Bd. III, T. 2, 1905. 

ScHENK, F., Studien iiber die Entwickelung des knéchernen Unterkiefers 
der Vogel. Sitzungsber. Akad. Wien, XXXIV Jahrg., 1897. 

ScuutrzeE, O., Ueber Embryonale und bleibende Segmentirung. Verh. 
Anat. Ges., Bd. X. Berlin, 1896. 

Srricut, O. vAN DER, Recherches sur les cartilages articulaires des oiseaux. 
Arch. de biol., T. X, 1890. 

SuscHkIn, P., Zur Anatomie und Entwickelungsgeschichte des Schiidels der 
Raubvégel. Anat. Anz., Bd. XI, 1896. 

Zur Morphologie des Vogelskeletts. (1) Schiidel von Tinnunculus. 
Nouv. Mém. Soc. Imp. des Natur. de Moscow, T. XVI, 1899. 

ScHwarck, W., Beitrige zur Entwickelungsgeschichte der Wirbelsiiule bei 
den Végeln. Anat. Studien (Herausgeg. v. Hasse), Bd. I, 1873. 

WiepeErRSHEIM, R., Ueber die Entwickelung des Schulter- und Beckengiirtels. 
Anat. Anz., Bd. IV, 1889, and V, 1890. 

Wuue, J. W. van, Ueber Somiten und Nerven im Kopfe von Voégel- und 
Reptilienembryonen. Zool. Anz., Jahrg. IX, 1886. 


IN 


Atrium burs omentalis, 344 


DEX 


Abducens nerve, 267 Auditory nerve, 295; ossicles, 299, 
Abducens nucleus, 262, 263 432; pit, 168 
Abnormal eggs, 25 Auricular canal, 354 
Accessory cleavage of pigeon’s egg, | Auriculo-ventricular canal, 348; di- 
38, 48, 44 vision of, 355 
Accessory mesenteries, 340, 341 Axis, development of, 420 
Acustico-facial ganglion complex, 159 | Axones, origin of, 235 
160, 262, 268 
Air-sacs, 326,a30n0a1 Basilar plate, 429 
Albumen, 18 Beak, 302, 304 
Albumen-sac, 217, 224 Biogenesis, fundamental law of, 4 
Albuginea of testis, 397 Blastoderm, 17; diameter of unin- 
Alecithal ova (see isolecithal) cubated, 61; expansion of, 50, 53, 
Allantois, blood-supply of, 222; gen- 61 
eral, 217; inner wall of, 220: neck Blastopore, 55, 82 
of, 148, 144, 316; origin of, 143, | Blood-cells, origin of, 118 
144; outer wall of, 220; rate of | Blood-islands, origin of, 86, 89 
growth, 221; structure of inner | Blood-vessels, origin of, 118 
wall, 223; structure of outer wall, Body-cavity, 115, 205-210, 333 
223 Bony labyrinth, 296 
Amnion, effect of rotation of em- | Brain, primary divisions of, 108; 
bryo on, 140, 141, 142; functions early development of, 147, 156; 
of, 231; head fold of, 137, 139; later development of, 244-252 
later history of, 231; mechanism Branchial arch, first, skeleton of, 432 
of formation, 139, 140; muscle | Bronchi, 325, 326 
fibers of, 231; origin of, 135; see- | Bulbus arteriosus, 198, 201, 202, 348; 
ondary folds of, 142 fate of, 357 
Amnio-cardiae vesicles, 92, 116 Bursa Fabricii, 314, 317, 319 
Ampulle of semicircular canals, 291 Bursa omenti majoris, 344 
Anal plate, 143, 182 Bursa omenti minoris, 344 
See also cloacal membrane 
Angioblast, 88 Canal of Schlemm, 279 
Anterior chamber of eye, 278 Cardinal veins, anterior, 200, 204, 
Anterior commissure of spinal cord, 205, 363; posterior, 200, 204, 205, 
origin of, 244 368 
Anterior intestinal portal, 95 (Fig. | Carina of sternum, 427 
49), 121, 132 Carotid arch, 361 
Anterior mesenteric artery, 363 Carotid, common, 362; external 359, 
Aortic arches, 198, 199, 203, 358- 361; internal, 359-361 
362; transformations of, 359-361 Carpus, 436, 437 
Appendicular skeleton, 434 Cartilage, absorption of, 408; bones, 
Aqueduct of Sylvius, 251. definition, 407; calcification — of, 
Archenteron, 55 409 
Area opaca, 39, 50, 61, 86; pellu- | Caval fold, 344 
cida, 39, 50, 61; vasculosa, 61, 86; | Cavo-caliace recess, 344 
vitellina, 61, 62, 86 Cavum sub-pulmonale, 342 
Arterial system, 121, 126, 198, 199, | Cell-chain hypothesis, 255 
203, 204, 228, 358-363 Cell theory, 1 
Atlas, development of, 420 Central and marginal cells, 41, 42 


Central canal of spinal cord, 242 
465 


466 


Cerebellum, 155, 251 

Cephalic mesoblastie 
269, 428 

Cerebral flexures, 149, 245 

Cerebral ganglia, 157-162, 262 

Cerebral hemispheres, origin of, 151; 
(see telencephalon) 

Cervical flexure, 1338, 245 

Chalazee, 1S 

Chemical composition of 
hen’s egg, 20, 21 

Chiasma opticus, 154, 249 

Choane, 215, 285 

Chondrification, 408 

Chorion, 135, 217, 218, 220 

Choroid coat of eye, 279; fissure, 
166, 281; plexus, 248 

Chromaffin tissue, 404 

Chronology, 64 

Cilary processes, 272, 274 


somites, 108, 


of 


parts 


Cireulation of blood, 121, 122, 197- 
200, 372-376 

Cireulation of blood, changes at 
hatehing, 3876; completion — of 


double, 355 

Classifieation of stages, 64-67 

Clavicle, 434, 435 

Cleavage of ovum (hen), 39-43 

Cleavage of ovum (pigeon), 43-47 

Cloaeca, 314-319; (see hind-gut) 

Cloneal membrane, 315, 318; (see 
also anal plate) 

Coeliac artery, 363 

Coelome (see body-cavity) 

Ccenogenetic aspects of 
ment, 6 

Collaterals, origin of, 238 

Collecting tubules of mesonephros, 
379, 380 

Colliculus palato-pharyngeus, 398 

Commissura anterior, 252; inferior, 
252; posterior, 252; trochlearis, 252 

Concrescence, theory of, 82, 84 

Cones of growth, 235 

Conjunctival sac, 279 

Coprodeum, 315, 318, 319 

Coracoid, 484, 455 

Cornea, 278 

Corpus striatum, 247 

Corpus vitreum, 275 

Cortical cords of suprarenal] 
sules, 405 

Cranial flexure, 133, 245; nerves, 261 

Cristee acusticw, 295 

Crop, 312 

Crural veins, 372 

Cushion septum, 355 

Cuticle of shell, 17 

Cutis plate, 185, 188 


develop- 


cap- 


INDEX 


Delimitation of embryo from  blas- 
toderm, 91 

Dendrites, origin of, 236 

Determinants, 7 

Diencephalon, early development. of, 
152; later development of, 249 

Dorsal aorta, origin of, 121 

Dorsal longitudinal fissure and sep- 
tum of spinal cord, 248, 244 

Dorsal mesentery, 172, 342 

Duct of Botallus, 359, 361, 376 

Ducts of Cuvier, 200, 204, 207, 364 

Duetus arteriosus (see duct of Bo- 
talus); choledochus (common. bile- 
duct), 181, 321; cochlearis, 293; 
cystico-entericus, 321; endolymph- 
aticus, 169, 289; hepato-cysticus, 
321; hepato-entericus, 321; veno- 
sus {see meatus venosus) 

Duodenum, 310, 311 


Ear, later development of, 288 

Eetamnion, 138 

Eetoderm and entoderm, origin of, 52 

Eetoderm of oral cavity, limits of, 
301 

Ege, formation of, 22, 

EKee-tooth, 302, 308 

Imbryonic circulation, on the fourth 
day, 372-374; on the sixth day, 
374; on the eighth day, 374-376 

Embryonic membranes, diagrams of, 
219, 220; general, 216; origin of, 
135; summary of later history, 145 

Endocardium, origin of, 119 

Endolymphatic duct (see 
endolymphaticus) 

Endolymphatic sac (see saccus endo- 
lymphaticus) 

Entobronchi, 327, 328 

Entoderm, origin of, 52 

Ependyma, origin of, 239 

Epididymis, 391, 398 

Epiphysis, 153, 249 

Epiphyses (of long bones), 409 

Epistropheus, development of, 420 

Epithalamus, 251 

Epithelial cells of neural tube, 233, 
234 

Epithelial vestiges of visceral pouches 
309 

Epodphoron, 401 

Equatorial ring of lens, 277-278 

Excentricity of cleavage, 41, 47 

Excretory system, origin of, 190 

External auditory meatus, 297, 3800 

Iexternal form of the embryo, 211 

Eye, early development of, 164; 
later development of, 271 

Kyelids, 279-280 


24, 25 


ductus 


INDEX 


Facial region, development of the, 
214, 215, 216 

Facialis nerve, 268 

Facialis nucleus, 262, 263 

Femur, 440 

Fertilization, 35 

Fibula, 440 

First segmentation nucleus, 36 

Fissura metotica, 429 

Foetal development, 11 

Fold of the omentum, 344, 345 

Follicles of ovary, 22, 26, 27, 28, 30, 
400 

Follicular cells, origin of, 27, 400 

Foramen, interventricular, 353, 354; 
of Monro, 247; of Winslow, 343; 
ovale, 355 

Foramina, interauricular, 355 

Fore-brain, origin of, 108 

Fore-gut, 91, 93, 172 

Formative stuffs, 15 

Funiculi precervicales, 307 


Gall-bladder, 321 

Ganglia, cranial and spinal, 156; 
cranial, 157, 158, 159, 262; spinal, 
later development of, 254, 257 

Ganglion, ciliare, 266; geniculatum, 
268; jugulare, 268; olfactorium 
nervi trigemini, 264; nodosum, 
161, 268; petrosum, 161, 268; of 
Remak, 257 

Gastric diverticula of body-cavity, 
340 

Gastrulation, 53, 84 

Genetic restriction, law of, 8 

Genital ducts, development of, 401 

Germ-cells, general characters of, 
9-12; comparison of, 12-14 

Germ-wall, 47, 48, 69, 90, 128, 129 

Germinal cells of neural tube, 233, 
234 

Germinal dise, 11, 12, 35, 37, 39 

Germinal epithelium, 391, 392, 399 

Germinal vesicle, 27, 28 

Gizzard, 313, 314 

Glomeruli of pronephros, 192 

Glossopharyngeus, ganglion complex 
of, 161, 262, 268; nerve, 268; nu- 
cleus, 262, 263 

Glottis, 332 

Gray matter of spinal cord, develop- 
ment of, 240; origin of, 239 


Heemal arch of vertebrae, 416, 417 
Harderian gland, 280 

Hatching, 282 

Head, development of, 213 
Head-fold, origin of, 91 

Head process, 73, 80 


467 


Heart, changes of position of, 348, 
349; development on second and 
third days, 200-203; divisions of 
cavities of, 350; ganglia and nerves 
of, 259; later development of, 348; 
origin of, 119 

Hensen’s knot, 73 

Hepatic veins, 366 

Hepatic portal circulation, 366, 375 

Hermaphroditista of embryo, 391 

Heterotaxia, 133 

Hiatus communis recessum, 348 

Hind-brain, origin of, 108 

Hind-gut, 143, 172 

Hind-limbs, origin of skeleton, 438 

Hoffmann’s nucleus, 240 

Holoblastic ova, 11, 12 

Humerus, 436 

Hyoid arch, 175: skeleton of, 432 

Hyomandibular cleft, 174, 297 

Hypoglossus nerve, 269 

Hypophysis, 154, 249 

Hypothalamus, 251 


Tlium, 438, 439 

Incubation, normal temperature for, 
65, 66 

Indifferent stage of sexual organs, 
391 

Infundibulum (of brain), 154, 249 

Infundibulum (of oviduct). See os- 
tium tubs abdominale 

Interganglionic commissures, 156 

Intermediate cell-mass, 114, 190 

Interventricular suleus, 348, 353 

Intervertebral fissure, 412 

Intestine, general development of, 
S10)31il 

Tris, 272; muscles of, 273, 274 

Ischiadie veins, 372 

Ischium, 438, 489 

Tsolecithal ova, 11 

Isthmus, of brain, 155; of oviduet, 22 


Jacobson, organ of, 286 
Jugular vein, 363 


Kidney, capsule of, 390; permanent, 
384-389; secreting tubules of, 390 


Lagena, 298 

Lamina terminalis, 105, 152, 247, 248 

Larva, 11 

Laryngotracheal groove, 
302 

Larynx, 332 

Latebra, 19 

Lateral plate of mesoblast, 

Lateral tongue folds, 305 

Lens, 166, 276-278 


178, 331, 


115 


468 


Lenticular zone of optie cup, 271 

Lesser peritoneal cavity, 344 

Ligamentum pectinatum iridis, 279 

Limiting sulci, 130 

Lingual glands, 306 

Lip-grooves, 304 

Liver, histogenesis of, 323; later de- 
velopment of, 319-323; origin and 
early development of, 179, 180, 
ISL; origin of lobes of, 322; pri- 
mary ventral ligament of, 335 

Lungs, 178, 326 


Maeula utriculi, saceuli, ete., 295 

Malpighian corpuscles (mesonephric) 
origin of, 195 

Mammillie of shell, 17 

Mandibular aortic arch, 
203, 204 

Mandibular arch, skeleton of, 431 

Mandibular glands, 306 

Mantle layer of spinal cord, origin 
of, 239 

Margin of overgrowth, 52, 57 

Marginal notch, 60, 84, 85 

Marginal velum, 235 

Marrow of bone, origin of, 410 

Maturation of ovum, 82 

Meatus venosus, 199, 364, 366, 368 

Medullary cords of suprarenal cap- 
sules, 405, 406 

Medullary neuroblasts of brain, 262 

Medullary plate, 95; position of an- 
terior end of, in neural tube, 102, 
103 

Megaspheres, 59 

Membrana reuniens, 418 

Membrane bones, definition of, 407 

Membranes of ovum, !0 

Membranous labyrinth, 289 

Meroblastic ova, 11 

Mesencephalon, LOS, 155, 251 

Mesenchyme, definition of, 116 

Mesenteric artery, 363 

Mesenteric vein, 366, 367 

Mesenteries, 333 

Mesentery, dorsal, 172, 342; of the 
vena cava inferior, 341 

Mesoblast, gastral, 110; of the head, 
origin of, 116, 117; history of be- 
tween | and 12 somites, 109; lat- 
eral plate of, 110, 115; of opaque 
area, origin of, 86, 8S; origin of, 
74, 78; paraxial, 110; prostomial, 
110; somatic layer of, 115; splanch- 
nic layer of, 115 

Mesobronchus, 326, 327 

Mesoeardia lateralia, 200, 207, 334, 
Sot 


Mesoeardium, origin of, 120 


121, 


122 


INDEX 


Mesogastrium, 309, 342, 343 

Mesonephrie arteries, 363 

Mesonephric mesentery, 341 

Mesonephric tubules, formation of, 
195 

Mesonephric ureters, 380 

Mesonephros, later history of, 378; 
origin and early history of, 194— 
197; see Wolffian body 

Mesothalamus, 251 

Mesothelium, definition of, 116 

Metacarpus, 486, 487, 488 

Metamorphosis, 11 

Metanephros, 384-389 

Metatarsals, 441 

Metathalarus, 251 

Metencephalon, 155, 251 

Mid-brain (see Mesencephalon) 

Mid-eut, 172, 181, 310 

Mouth, 301 

Millerian duets, 391; degeneration 
in male, 402, 403; origin of, 401, 
402, 403 

Muscles of iris, 274 

Muscle plate, 185, 186 

Myelencephalon, 155, 252 

Myoeardium, origin of, 119 

Myotome, L188 


Nares, 286 

Nephrogenous tissue, 195, 378; of 
metanephros, 384, 387 

Nephrotome, 114, 190 

Neural erest, 156 

Neural folds, 97, 99 

Neural groove, 97 

Neural tube, 95, 105 

Neurenteric canal, 73, 82 

Neuroblasts, 233-239; classes of, in 
spinal cord, 244 

Neurocranium, 427, 428 

Neuroglia cells, origin of, 239, 240 

Neuromeres, LOS, 148, 152, 155 

Neurone theory, 256, 255, 256 

Neuropore, 101, 105 

Notochord, later development of, 
411 ff; origin of, 80; in the region 
of the skull, 428 


Oblique septum, 331, 342 

Oculo-motor nerve, 265; nucleus, 
262, 263 

Odontoid process, origin of, 420 

Q£sophagus, 179, 310, 312 

Olfactory lobe, 247 

Olfactory nerve, 263 

Olfactory pits, 169, 285 

Olfactory vestibule, 285 

Omentum, development of, 343 


| Omphalocephaly, 120 


INDEX 


Omphalomesenterie arteries, 199,363 ; 
veins, 364-366 

O6tid, 14 

Opaque area, see area opaca 

Optie cup, 165, 271; lobes, 251; nerve, 
283, 284, 285; stalk, 149, 164, 284, 
285; vesicles, accessory, 164 

Optic vesicles, primary, 108, 
secondary, 166 

Ora serrata, 272 

Oral cavity, 215, 216, 301 

Oral glands, 306 

Oral plate, 95, 173 

Orientation of embryo on yolk, 25, 63 

Ossification, 408-411; endochondral, 
409; perichondral, 408 

Ostium tubze abdominale, 23; devel- 
opment of, 402, 403; relation to 
pronephros, 402 

Otocyst, 168; later development. of, 
289; method of closure, 168 

Ovary, 22, 398-401; degeneration of 
right, 398 

Oviducal membranes of ovum, 10 

Oviduct, 22; later development. of, 
403 

Ovocyte, 13, 26, 27 

Ovogenesis, 12, 26 

Ovogonia, 12, 26 

Ovum, 2, 10; bilateral symmetry of, 
15; follicular membrane of, 10; or- 
ganization of, 14; polarity of, 14 


164; 


Palate, 285, 299 

Palatine glands, 306 

Palingenetic aspects of development, 
6 

Pancreas, 181, 323-325, 347 

Pander’s nucleus, 19 

Papillzee conjunctive 

Parabronchi, 328 

Parachordals, 428, 429 

Paradidymis, 391, 398 

Paraphysis, 248 

Parencephalon, 108, 153, 249 

Parietal cavity, 92, 116, 207, 208, 
303, 334 

Paroéphcron, 401 

Pars copularis (of tongue), 305 

Pars inferior labyrinthi, 289, 293 

Pars superior labyrinthi, 289, 291 

Parthenogenetice cleavage, 35 

Patella, 441 

Pecten, 281, 282 

Pectoral girdle, 434-436 

Pellucid area (see area pellucida) 

Pelvie girdle, 488-440 

Periaxial cords, 158, 159, 161 

Pericardiaco-peritoneal © membrane, 
338 


scleree, 280 


469 


Pericardial and pleuroperitoneal cay- 
ities, separation of, 333 

Pericardium, closure of dorsal open- 
ing of, 337; formation of mem- 
branous, 338; see parietal cavity. 

Periblast, 38, 43, 47; marginal and 
central 48; nuclei, origin of, 47, 48 

Perichondrium, 408 

Periderm, 304 

Perilymph, 296, 297 

Periosteum, 409 

Peripheral nervous system, develop- 
ment of, 252 

Pfliiger, cords of, 399 

Pheeochrome tissue, 404 

Phalanges, 436, 438; of foot, 441; of 
wing, 438 

Pharynx, derivatives of, 306; early 
development of, 93-95, 173; post- 
branchial portion of, 178 

Phylogenetic reduction of skeleton, 
411 

Physiological zero of development, 65 

Physiology of development, 6 

Pineal body, 153, 249 

Placodes, 160, 161 

Pleural and peritoneal cavities, sep- 
aration of, 340 

Pleural grooves, 208, 209 

Pleuro-pericardial membrane, 338 

Pleuroperitoneal membrane, 326; 
septum, 340, 341 

Plica encephali ventralis, 149, 245 

Plica mesogastrica, 341, 344, 368 

Pneumato-enteric recesses, 209, 340 

Pneumatogastriec nerve, 268 

Polar bodies, 13, 34 

Polyspermy, 35, 36, 37 

Pons, 252 

Pontine flexure, 149, 245 

Postanal gut, 182 

Postbranchial bodies, 307, 309 

Posterior intestinal portal, 132 

Postotie neural crest, 160, 161 

Precardial plate, 334, 338 

Preformation, 6 

Pre-oral gut, 174 

Pre-oral visceral furrows, 174, 175 

Preotic neural crest, 158 

Primitive groove, 72 

Primitive intestine, 55 

Primitive knot, 73 

Primitive mouth, 55, 82 

Primitive ova, 26, 392, 399 

Primitive pit, 73 

Primitive plate, 73 

Primitive streak, 69; interpretation 
of, 82; origin of, 74; relation to 
embryo, &5 

Primordia, embryonic, 8 


470 


Primordial cranium, development of, 
428 

Primordial follicle, 27 

Proamnion, 86, 138 

Procoracoid, 435 

Proectodzeum, 170, 314, 319 

Pronephros, 190-195 

Pronucleus male and female, 34, 36 

Prosencephalon, LOS, 149 

Proventriculus, 313 

Pubis, 488, 489 

Pulmo-enteric 
mato-) 

Pulmonary arteries, 359 

Pupil of eye, 166, 272 


recesses (see pneu- 


Radius, 436 

Ramus communieans, 254, 257, 259 

Reeapitulation theory, 3; diagram 
of, 5 

Recessus hepatico-entericus, 343; re- 
eessus mesenterico-entericus, 343; 
recessus opticus, 155;  recessus 
pleuro-peritoneales, 340; recessus 
pulmo-hepatici, 340; recessus  su- 
perior sacci omenti, 340 

Rectum, 317 

Renal corpuscles, 378, 385 

Renal portal circulation, 369, 372, 
375 

Renal veins, 372 

Reproduction, development of or- 
gans of, 390-405 

Respiratory tract, 178, 325 

Rete testis, 398 

Retina, 274, 275 

Retinal zone of optic cup, 271 

Rhombencephalon, 108, 155 

Ribs, development of, 424, 425 


s (abbreviation for somites), 67 

Sacrum, 424 

Sacculus, 2938, 294 

Sacecus endolymphaticus, 169, 
290 

Saceus infundibuli, 249 

Seapula, 434, 455 

Sclerotic cout of eye, 279 

Sclerotomes, and vertebral segmenta- 
tion, 412; components of, 412; oc- 
cipital, 428; origin of, 185, 186 

Seessell’s pocket, 174 

Segmental arteries, 122, 199, 362 

Segmentation cavity, 43, 47, 55 (see 
also subgerminal cavity) 

Semeniferous tubules, 398 

Semicireular canals, 291 

Semi-lunar valves, 352 

Sensory areas of auditory labyrinth, 
origin of, 296 


289, 


‘ 


INDEX 


Septa of heart, completion of, 355, 
300; 350 

Septal gland of nose, 287 

Septum aortico-pulmonale, 351, 352; 
of auricular canal, 355; bulbo- 
auricular, 353; cushion, 351, 355; 
interauricular, 351, 354; interven- 
tricular, 351, 358, 354; of sinus 
venosus, 358 

Septum transversum, 208, 209, 334; 
derivatives of, 339; lateral closing 
folds of, 334, 337; median mass of, 
Soo 

Septum trunci et bulbi arteriosi, 351 

Sero-amniotic connection, 138, 143, 
Bld 

Sexual cords, 393, 394;. of ovary, 398; 
of testis, 395 

Sexual differentiation, 394, 395 

Sheath cells, 255 

Shell, structure of, 17 

Shell membrane, 18 

Sickle (of Koller), 71 

Sinu-auricular aperture, 357, 358 

Sinu-auricular valves, 358 

Sinus terminalis 86 (see also vena 
terminalis) 

Sinus venosus, 197, 200, 201, 357; 
horns of, 358; relation to septum 
transversum, 559 

Skeleton, general statement 
cerning origin, 407 

Skull, echondrification of, 429-4382: de- 
velopment of, 427; ossification of, 
432, 433, 434 

Somatopleure, 62, 115 

Somite, first, position in embryo, [11 

Somites, of the head, 1t4; meso- 
blastic, origin of, 110, 111; meso- 
blastic, metameric value of, 1LS4; 
primary structure of, 114 

Spermatid, 13 

Spermatocyte, 15 

Spermatogenesis, 12 

Spermatogonia, 15 

Spermatozoa, period of life 
oviduet, 385 

Spermatozoon, 9 

Spina iliaca, 440 

Spinal accessory nerve, 269 

Spinal cord, development of, 239 

Spinal nerves, components of, 254; 
development of, 252, 255; somatic 
components of, 254; splanchnic 
components of, 256 

Splanchnocranium, 427 

Splanchnopleure, 62, 115 

Spleen, 345-347 

Spongy layer of shell, 17 

Stapes, 500 


con- 


within 


INDEX 


Sternum, development of, 425-427 

Stigma of follicle, 25 

Stomach, 179, 313 

Stomodieum, 170, 173 

Stroma of gonads, 393; of testis, 397 

Subeardinal veins, 368, 369 

Subelavian artery, 362 

Subclavian veins, 363, 364 

Subgerminal cavity, 53, 61, 69 

Subintestinal vein, 367 

Subnotochordal bar, 416, 418 

Sulcus lingualis, 298 

Suleus tubo-tympanicus, 298 

Supraorbital sinus of olfactory cav- 
ity, 285 

Suprarenal capsules, 403-406 | 

Sutura cerebralis anterior, 103-105; | 
neurochordalis seu ventralis, 105; 
terminalis anterior, 105 

Sympathetic nervous system, 
261; relation to suprarenals, 

Sympathetic trunks, primary, 
secondary, 258 

Synencephalon, 108, 153, 249 

Syrinx, 332 


256- 
406 


PASI (S 


Tables of development, 68 
Tail-fold, 131 

Tarsus, 441 

Tectum lobi optici, 251 
Teeth, 304 

Tela choroidea, 152 


Telencephalon and diencephalon, 


origin of, 150 

Telencephalon, later development of, | 
245-249; medium, 151, 245 

Telolecithal, 11 

Ten somite embryo, description of, 
122 

Testis, 395-398 

Tetrads, 33 

Thalami optici, 154, 251 

Thymus, 308 

Thyroid, 178, 307 

Tongue, 305 

Torus transversus, 248 

Trabecule, of skull, 428, 429: of 
ventricles, 353 

Trachea, 331, 332 

Trigeminal ganglion complex, 160, 
267 

Trigeminus nerve, 267; nucleus (mo- 
tor), 262, 263 

Trochlearis nerve, 266; nucleus, 262, 
263 

Truncus arteriosus, 198 

Tubal fissure, 298, 301 

Tubal ridge, 401 

Tuberculum impar (of tongue), 305 

Tuberculum posterius, 249 


Tubo-tympanie cavity, 297-300 

Tubules of mesonephros, degenera- 
tion of, 380-882; formation of, 
195-196; primary, secondary, ter- 
tiary, 379, 380 

Turbinals, 285, 286, 431 

Turning of embryo, 133 

Tympanum, 297, 300 


Ulna, 436 

Umbilical arteries, 
368 

Umbilieus, 144: of 

Unincubated 
of, 69 

Ureter, origin of, 384 

Urinogenital ridge, 390, 391; system, 
later development of, 378, ete. 

Urodeum, 314, 319 

Uterus, 22 

Utriculus, 291, 292 

Uvea, 273 


363; veins, 367, 


yolk-sac, 216 
blastoderm, structure 


Vagina, 22 

Vagus, ganglion complex of, 161; 
nerve, 268; nucleus, 262, 263 

Variability, embryonic, 64 

Vas deferens, 401 

Vasa efferentia, 398 

Vascular system, anatomy of, on 
fourth day, 197-200; origin of, 117 

Venous system, 127, 199, 204, 205, 
228, 363-372 

Velum transversum, 150, 248 

Vena cava, anterior, 363, 364; in- 
ferior, 368-372 

Vena porta sinistra, 367 

Vena terminalis, 228; see also 
terminalis 

Ventral aorta, 121 

Ventral longitudinal fissure of spinal 
cord, 243 

Ventral mesentery, 131, 182, 343 

Vertebree, articulations of, 421; co- 
alescence of, 424; costal processes 
of, 418; hypocentrum of, 418; in- 
tervertebral ligaments of, 421; 
ossification of, 421-424; pleuro- 
centrum of, 418; stage of chondri- 
fication of, 418; suspensory liga- 
ments of, 421; 

Vertebral column, 411; condition on 
fourth day, 414; condition on fifth 
day, 415, 417; condition on sev- 
enth and eighth days, 418, 420; 
membranous stage of, 414 


sinus 


Vertebral segmentation, origin of, 
412 ff 

Visceral arches, 175; clefts, 174, 
307; furrows, 174; pouches, 174; 


472 


pouches, early development of, 175— 

178; pouches, fate of, 307, 308 
Vitelline membrane, 10, 30, 31 
Vitreous humor, 275 


White matter of spinal cord, origin 
of, 239, 241 

Wing, origin of skeleton of, 434, 456 

Wolffian body (see mesonephros) ; 
atrophy, 380, 9382, 401; sexual 
and non-sexual portions, 396; at 
ninety-six hours, 379; on the 
sixth day, 382; on the eighth day, 
382, 383; on the eleventh day, 385 


INDEX 


Wolffian duct, 191, 193, 194, 391, 401 


Yolk, 17, 19; formation of, 29 

Yolk-sae, 148, 225-231; entoderm 
of, 50; blood-vessels of, 227-230; 
septa of, 225-227; ultimate fate 
of, 230) 231 

Yolk-spheres, 19, 20 

Yolk-stalk, 182, 225 


Zona radiata, 10, 30, 31 
Zone of junction, 52, 57 
Zones of the blastoderm, 127-129 


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