The Works of Francis Balfour 3-8

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Foster M. and Sedgwick A. The Works of Francis Balfour Vol. III. A Treatise on Comparative Embryology 2 (1885) MacMillan and Co., London.

Cephalochorda | Urochorda | Elasmobranchii | Teleostei | Cyclostomata | Ganoidei | Amphibia | Aves | Reptilia | Mammalia | Comparison of the Formation of Germinal Layers and Early Stages in Vertebrate Development | Ancestral form of the Chordata | General Conclusions | Epidermis and Derivatives | The Nervous System | Organs of Vision | Auditory, Olfactory, and Lateral Line Sense Organs | Notochord, Vertebral Column, Ribs, and Sternum | The Skull | Pectoral and Pelvic Girdles and Limb Skeleton | Body Cavity, Vascular System and Glands | The Muscular System | Excretory Organs | Generative Organs and Genital Ducts | The Alimentary Canal and Appendages in Chordata
Online Editor 
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This historic 1885 book edited by Foster and Sedgwick is the third of Francis Balfour's collected works published in four editions. Francis (Frank) Maitland Balfour, known as F. M. Balfour, (November 10, 1851 - July 19, 1882) was a British biologist who co-authored embryology textbooks.



Foster M. and Sedgwick A. The Works of Francis Balfour Vol. I. Separate Memoirs (1885) MacMillan and Co., London.

Foster M. and Sedgwick A. The Works of Francis Balfour Vol. II. A Treatise on Comparative Embryology 1. (1885) MacMillan and Co., London.

Foster M. and Sedgwick A. The Works of Francis Balfour Vol. III. A Treatise on Comparative Embryology 2 (1885) MacMillan and Co., London.

Foster M. and Sedgwick A. The Works of Francis Balfour Vol. IV. Plates (1885) MacMillan and Co., London.
Modern Notes:

Historic Disclaimer - information about historic embryology pages 
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Pages where the terms "Historic Textbook" and "Historic Embryology" appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms and interpretations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)


Draft Version - Notice removed when completed.

Vol. III. A Treatise on Comparative Embryology 2 (1885)

CHAPTER VIII. AVES

INTRODUCTION.

THE variations in the character of the embryonic development of the Amniota are far less important than in the case of the Ichthyopsida. There are, it is true, some very special features in the early developmental history of the Mammalia, but apart from these there is such a striking uniformity in the embryos of all the groups that it would, in many cases, be difficult to assign a young embryo to its proper class.

Amongst the Sauropsida the Aves have for obvious reasons received a far fuller share of attention than any other group; and an account of their embryology forms a suitable introduction to this part of our subject. For the convenience of the student many parts of their developmental history will be dealt with at greater length than in the case of the previous groups.

The development of the Aves.

Comparatively few types of Birds have been studied embryologically. The common Fowl has received a disproportionately large share of attention ; although within quite recent times the



FIG. 85. YOLK ELEMENTS FROM THE EGG OF THE FOWL. A. Yellow yolk. B. White yolk.

Duck, the Goose, the Pigeon, the Starling, and a Parrot (Melopsittacus undulatus) have also been studied. The result of these

B. III. 10


146 GERMINAL DISC.


investigations has been to shew that the variations in the early development of different Birds are comparatively unimportant. In the sequel the common Fowl will be employed as type, attention being called when necessary to the development of the other forms.

The ovum of the Fowl, at the time when it is clasped by the expanded extremity of the oviduct, is a large yellow body enclosed in a vitelline membrane. It is mainly formed of spherules of food-yolk. Of these there are two varieties ; one known as yellow yolk, and the other as white. The white yolk spherules form a small mass at the centre of the ovum, which is continued to the surface by a narrow stalk, and there expands into a somewhat funnel-shaped disc, the edges of which are continued over the surface of the ovum as a delicate layer. The major part of the ovum is formed of yellow yolk. The yellow yolk consists of large delicate spheres, filled with small granules (fig. 85 A) ; while the white yolk is formed of vesicles of a smaller size than the yellow yolk spheres, in which are a variable number of highly refractive bodies (fig. 85 B).

In addition to the yolk there is present in the ovum a small protoplasmic region, containing the remains of the germinal vesicle, which forms the germinal disc (fig. 86). It overlies the



w.y.


FIG. 86. SECTION THROUGH THE GERMINAL DISC OF THE RIPE OVARIAN OVUM

OF A FOWL WHILE YET ENCLOSED IN ITS CAPSULE.

a. Connective-tissue capsule of the ovum ; b. epithelium of the capsule, at the surface of which nearest the ovum lies the vitelline membrane; c. granular material of the germinal disc, which becomes converted into the blastoderm. (This is not very well represented in the woodcut. In sections which have been hardened in chromic acid it consists of fine granules.) w.y. white yolk, which passes insensibly into the fine granular material of the disc ; x. germinal vesicle enclosed in a distinct membrane, but shrivelled up; y. space originally completely filled up by the germinal vesicle, before the latter was shrivelled up.

funnel-shaped disc of white yolk, into which it is continued without any marked line of demarcation. It contains numerous


AVES.


147


minute spherules of the same nature as the smallest white yolk spherules.

Impregnation takes place at the upper extremity of the oviduct.

In its passage outwards the ovum gradually receives its accessory coverings in the form of albumen, shell-membrane, and shell (fig. 87).


y-y


c-fi.Z



FIG. 87. DIAGRAMMATIC SECTION OF AN UNINCUBATED FOWL'S EGG.

(Modified from Allen Thomson.)

bl. blastoderm; w.y. white yolk. This consists of a central flask-shaped mass and a number of layers concentrically arranged around it. y.y. yellow yolk ; v.t. vitelline membrane ; x. layer of more fluid albumen immediately surrounding the yolk ; w. albumen consisting of alternate denser and more fluid layers; ch.l. chalaza; a.ch. air-chamber at the broad end of the egg. This chamber is merely a space left between the two layers of the shell-membrane, i.s.m. internal layer of shell-membrane; s.m. external layer of shell-membrane ; s. shell.

The segmentation commences in the lower part of the oviduct, shortly before the shell has begun to be formed. It is meroblastic, being confined to the germinal disc, through the full depth of which however the earlier furrows do not extend. It is mainly remarkable for being constantly somewhat unsymmetrical (Kolliker) a feature which is not represented in fig. 88, copied from Coste. Owing to the absence of symmetry the cells at one side of the germinal disc are larger than those at the other, but the relations between the disc and the axis of the

10 2


148


SEGMENTATION.


embryo are not known. During the later stages the segmentation is irregular, and not confined to the surface ; and towards its




ABC

FIG. 88. SURFACE VIEWS OF THE EARLY STAGES OF THE SEGMENTATION

IN A FOWL'S EGG. (After Coste.)

a. edge of germinal disc; b. vertical furrow; c. small central segment; d. larger peripheral segment.

close the germinal disc becomes somewhat lenticular in shape ; and is formed of segments, which are smallest in the centre and increase in size towards the periphery (figs. 89 and 90). The superficial segments in the centre of the germinal disc are moreover smaller than those below, and more or less separated as a distinct layer (fig. 90). As development proceeds the segmentation reaches its

limits in the centre,

, , , . , , , FIG. 89. SURFACE VIEW OF THE GERMINAL DISC

tne OF FOWL'S EGG DURING A LATE STAGE OF THE SEGperiphery; and thus MENTATION.

c. small central segmentation spheres; b. larger segments outside these ; a. large, imperfectly circumscribed, marginal segments; e. margin of germinal



disc.


eventually the masses at the periphery become of the same size as those at the centre. At the time when the ovum is laid (fig. 91) the uppermost layer of segments has given rise to a distinct membrane, the epiblast, formed of a single row of colum


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149


nar cells (ep). The lower or hypoblast segments are larger, in some cases very much larger, than those of the epiblast, and are



FIG. 90. SECTION OF THE GERMINAL DISC OF A FOWL DURING THE LATER STAGES OF SEGMENTATION.

The section, which represents rather more than half the breadth of the blastoderm (the middle line being shewn at c), shews that the upper and central parts of the disc segment faster than those below and towards the periphery. At the periphery the segments are still very large. One of the larger segments is shewn at a. In the majority of segments a nucleus can be seen; and it seems probable that the nucleus is present in them all. Most of the segments are filled with highly refracting spherules, but these are more numerous in some cells (especially the larger cells near the yolk) than in others. In the central part of the blastoderm the upper cells have commenced to form a distinct layer. No segmentation cavity is present.

a. large peripheral cell ; b, larger cells of the lower parts of the blastoderm ; c. middle line of blastoderm; e. edge of the blastoderm adjoining the white yolk; w. white yolk.

so granular that their nuclei can only with difficulty be seen. They form a somewhat irregular mass, several layers deep, and thicker at the periphery than at the centre : they rest on a bed of white yolk, from which they are in parts separated by a more or less developed cavity, which is probably filled with fluid yolk matter about to be absorbed. In the bed of white yolk nuclei are present, which are of the same character, and have the same general fate, as those in Elasmobranchii. They are generally more numerous in the neighbourhood of the thickened periphery of the blastoderm than elsewhere. Peculiar large spherical bodies are to be found amongst the lower layer cells, which superficially resemble the larger cells around them, and have been called formative cells \vide Foster and Balfour (No. 126)]. Their real nature is still very doubtful, and though some are no doubt true cells, others are perhaps only nutritive masses of yolk. In a surface view the blastoderm, as the segmented germinal disc may


ISO


FORMATION OF THE LAYERS.


now be called, appears as a circular disc ; the central part of which is distinguished from the peripheral by its greater transparency, and forms what is known in the later stages as the area pellucida. The narrow darker ring of blastoderm, outside the area pellucida, is the commencing area opaca.

FIG. 91. SECTION OF A BLASTODERM OF A FOWL'S EGG AT > ^

THE COMMENCEMENT OF INCUBATION.

The thin epiblast ep composed of columnar cells rests on the incomplete lower layer /, composed of larger and more granular hypoblast cells. The lower layer is thicker in some places than in others, and is especially thick at the periphery. The line below the under layer marks the upper surface of the white yolk. The larger so-called formative cells are seen at b, lying on the white yolk. The figure does not take in quite the whole breadth of the blastoderm ; but the reader must understand that both to the right hand and to the left ep is continued farther than /, so that at the extreme edge it rests directly on the white yolk.

As a result of incubation the blastoderm undergoes a series of changes, which end in the definite formation of three germinal layers, and in the establishment of the chief systems of organs of the embryo. The more important of these changes are accomplished in the case of the common Fowl during the first day and the early part of the second day of incubation.

There is hardly any question in development which has been the subject of so much controversy as the mode of formation of the germinal layers in the common Fowl. The differences in the views of authors have been caused to a large extent by the difficulties of the investigation, but perhaps still more by the fact that many of the observations were made at a time when the methods of making sections were very inferior to those of the present day. The subject itself is by no means of an importance commensurate with the attention it has received. The characters which belong to the formation of the layers in the Sauropsida are second- ^^ -, arily derived from those in the Ichthyopsida, and are of but little importance for the general questions which concern the nature and origin of the germinal layers. In the account in the sequel I have avoided as much as possible discussion of controverted points. My statements are founded in the main on my own observations, more especially on a recent investigation carried on in conjunction with my pupil, Mr Deighton. It is to Kolliker (No. 135), and to Gasser (No. 127) that the most important of the more recent advances in our knowledge are due. Kolliker,


AVES.


in his great work on Embryology, definitely established the essential connection between the primitive streak and the formation of the mesoblast ; but while confirming his statement on this head, I am obliged to differ from him with reference to some other points.

Gasser's work, especially that part of it which relates to the passages leading from the neural to the alimentary canal, which he was the first to discover, is very valuable.

The blastoderm gradually grows in size, and extends itself over the yolk ; the growth over the yolk being very largely effected by an increase in the size of the area opaca, which during this process becomes more distinctly marked off from the area pellucida. The area pellucida gradually assumes an oval form, and at the same time becomes divided into a posterior opaque region and an anterior transparent region. The posterior opacity is named by some authors the embryonic shield.



FIG, 92. TRANSVERSE SECTION THROUGH THE BLASTODERM OF A CHICK

BEFORE THE APPEARANCE OF THE PRIMITIVE STREAK.

The epiblast is represented somewhat diagrammatically. The hyphens shew the points of junction of the two halves of the section.

During these changes the epiblast (fig. 92) becomes two layers deep over the greater part of the area pellucida, though still only one cell deep in the area opaca. The irregular hypoblast spheres of the unincubated blastoderm flatten themselves out, and unite into a definite hypoblastic membrane (fig. 92). Between this membrane and the epiblast there remain a number of scattered cells (fig. 92) which cannot however be said to form a definite layer altogether distinct from the hypoblast They are almost entirely confined to the posterior part of the area pellucida, and give rise to the opacity of that part.

At the edge of the area pellucida the hypoblast becomes continuous with a thickened rim of material, underlying the epiblast, and derived from the original thickened edge of the blastoderm and the subjacent yolk. It is mainly formed of yolk granules,


152


FORMATION OF THE LAYERS.


with a varying number of cells and nuclei imbedded in it. It is known as the germinal wall, and is spoken of more in detail on pp. 160 and 161.

The changes which next take place result in the complete differentiation of the embryonic layers, a process which is



FIG. 93. DIAGRAMS ILLUSTRATING THE POSITION OF THE BLASTOPORE, AND THE RELATION OF THE EMBRYO TO THE YOLK IN VARIOUS MEROBLASTIC VERTEBRATE OVA.

A. Type of Frog. B. Elasmobranch type. C. Amniotic Vertebrate. mg. medullary plate ; ne. neurenteric canal ; bl. portion of blastopore adjoining the neurenteric canal. In B this part of the blastopore is formed by the edges of the blastoderm meeting and forming a linear streak behind the embryo ; and in C it forms the structure known as the primitive streak, yk. part of yolk not yet enclosed by the blastoderm.

intimately connected with the formation of the structure known as the primitive streak. The meaning of the latter structure, and its relation to the embryo, can only be understood by comparison with the development of the forms already considered. The most striking peculiarity in the first formation of the embryo Bird, as also in that of the embryos of all Amniota, consists in the fact that they do not occupy a position at the edge


AVES.


153


of the blastoderm, but are placed near its centre. Behind the embryo there is however a peculiar structure the primitive streak above mentioned which is a linear body placed in the posterior region of the blastoderm. This body, the nature of which will be more fully explained in the chapter on the comparative development of Vertebrates, is really a rudimentary part of the blastopore, of the same nature as the linear streak behind the embryo in Elasmobranchii formed by the concrescence of the edges of the blastoderm (vide p. 64) ; although there is no ontogenetic process in the Amniota, like the concrescence in Elasmobranchii. The relations of the blastopore in Elasmobranchii and Aves is shewn in figs. B and C of the diagram (fig. 93).

In describing in detail the succeeding changes we may at first confine our attention to the area pellucida. As this gradually assumes an oval form the posterior opacity becomes replaced by a very dark median streak, which extends forwards some distance from the posterior border of the area (fig. 94). This is the first rudiment of the primitive streak.



FIG. 94. AREA PELLUCIDA OF A VERY YOUNG BLASTODERM OF A CHICK, SHEWING THE PRIMITIVE STREAK AT ITS FIRST APPEARANCE.

pr.s. primitive streak ; ap. area pellucida ; a.op. area opaca.


In the



FIG. 95. TRANSVERSE SECTION THROUGH A BLASTODERM OF ABOUT THE AGE REPRESENTED IN FIG. 94, SHEWING THE FIRST DIFFERENTIATION OF THE PRIMITIVE

STREAK.

The section passes through about the middle of the primitive streak, pvs. primitive streak; ep. epiblast; hy. hypoblast; yk. yolk of the germinal wall.

region in front of it the blastoderm is still formed of two layers


154


THE PRIMITIVE STREAK.


only, but in the region of the streak itself the structure of the blastoderm is greatly altered. The most important features in it are represented in fig. 95. This figure shews that the median portion of the blastoderm has become very much thickened (thus producing the opacity of the primitive streak), and that this thickening is caused by a proliferation of rounded cells from the epiblast. In the very young primitive streak, of which fig. 95 is a section, the rounded cells are still continuous throughout with the epiblast, but they form nevertheless the rudiment of the greater part of a sheet of mesoblast, which will soon arise in this region.

In addition to the cells clearly derived from the epiblast, there are certain other cells (vide fig. 95), closely adjoining the hypoblast, which appear to me to be the derivatives of the cells interposed between the epiblast and hypoblast, which gave rise to the posterior opacity in the blastoderm during the previous stage. In my opinion these cells also have a share in forming the future mesoblast

The number and distribution of these cells is subject to not inconsiderable variations. In a fair number of cases they are entirely congregated along the line of the primitive streak, leaving the sides of the blastoderm quite free. They then form a layer, which can only with difficulty be distinguished from the cells derived from the epiblast by slight peculiarities of staining, and by the presence of a considerable proportion of large granular cells. It is, I believe, by the study of such blastoderms that Kolliker has been led to deny to the intermediate cells of the previous stage any share in the formation of the mesoblast. In other instances, of which fig. 95 is a fairly typical example, they are more widely scattered. To follow with absolute certainty the history of these cells, and to prove that they join the mesoblast is not, I believe, possible by means of sections, and I must leave the reader to judge how far the evidence given in the sequel is sufficient to justify my opinions on this subject.



FIG. 96. SURFACE VIEW OK THE AREA PELLUCIDA OF A CHICK'S BLASTODERM SHORTLY AFTER THE FORMATION OF THE PRIMITIVE

GROOVE.

fr. primitive streak with primitive groove ; of. amniotic fold.

The darker shading round the primitive streak shews the extension of the mesoblast.


AVES. 155

In the course of further growth the area pellucida soon becomes pyriform, the narrower extremity being the posterior. The primitive streak (fig. 96) elongates considerably, so as to occupy about two-thirds of the length of the area pellucida ; but its hinder end in many instances does not extend to the posterior border of the area pellucida. The median line of the primitive streak becomes marked by a shallow groove, known as the primitive groove.

During these changes in external appearance there grow from the sides of the primitive streak two lateral wings of mesoblast cells, which gradually extend till they reach the sides of the area pellucida (fig. 97). The mesoblast still remains



FIG. 97. TRANSVERSE SECTION THROUGH THE FRONT END OF THE PRIMITIVE

STREAK OF A BLASTODERM OF THE SAME AGE AS FIG. 96. pv. primitive groove; m. mesoblast; ep. epiblast; hy. hypoblast; yh. yolk of germinal wall.

attached to the epiblast along the line of the primitive streak. During this extension many sections through the primitive streak give an impression of the mesoblast being involuted at the lips of a fold, and so support the view above propounded, that the primitive streak is the rudiment of the coalesced lips of the blastopore. The hypoblast below the primitive streak is always quite independent of the mesoblast above, though much more closely attached to it in the median line than at the sides. The part of the mesoblast, which I believe to be derived from the primitive hypoblast, can generally be distinctly traced. In many cases, especially at the front end of the primitive streak, it forms, as in fig. 97, a distinct layer of stellate cells, quite unlike the


1 5 6


FORMATION OF MESOBLAST.


rounded cells of the mesoblastic involution of the primitive streak.

In the region in front of the primitive streak, where the first trace of the embryo will shortly appear, the layers at first undergo no important changes, except that the hypoblast becomes somewhat thicker. Soon, however, as shewn in longitudinal section in fig. 98, the hypoblast along the axial line becomes continuous behind with the front end of the primitive streak. Thus at this



FIG. 98. LONGITUDINAL SECTION THROUGH THE AXIAL LINE OF THE PRIMITIVE STREAK, AND THE PART OF THE BLASTODERM IN FRONT OF IT, OF AN EMBRYO CHICK SOMEWHAT YOUNGER THAN FIG. 99.

pr.s. primitive streak ; ep. epiblast ; hy. hypoblast of region in front of primitive streak ; . nuclei ; yk. yolk of germinal wall.

point, which is the future hind end of the embryo, the mesoblast, the epiblast, and the hypoblast all unite together ; just as they do in all the types of Ichthyopsida.

Shortly afterwards, at a slightly later stage than that represented in fig. 96, an important change takes place in the constitution of the hypoblast in front of the primitive streak. The rounded cells, of which it is at first composed (fig. 98), break up into (i) a layer formed of a single row of more or less flattened elements below the hypoblast and (2) into a layer formed of several rows of stellate elements, between the hypoblast and the epiblast the mesoblast (fig. 99). A separation between these two layers is at first hardly apparent, and before it has become at all well marked, especially in the median line, an axial opaque line makes its appearance in surface views, continued forwards



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157


from the front end of the primitive streak, but stopping short at a semicircular fold the future head-fold near the front end of the area pellucida. In section (fig. 100) this opaque line is seen to be due to a special concentration of cells in the form of a cord.



FIG. 99. TRANSVERSE SECTION THROUGH THE EMBRYONIC REGION OF THE BLASTODERM OF A CHICK SHORTLY PRIOR TO THE FORMATION OF THE MEDULLARY GROOVE AND NOTOCHORD.

m. median line of the section; ep. epiblast; //. lower layer cells (primitive hypoblast) not yet completely differentiated into mesoblast and hypoblast ; n. nuclei of germinal wall.

This cord is the commencement of the notochord (ch\ In some instances the commencing notochord remains attached to the hypoblast, while the mesoblast is laterally quite distinct (vide fig. 100), and is therefore formed in the same manner as in most Ichthyopsida ; while in other instances, and always apparently in the Goose (Gasser, No. 127), the notochord appears to become differentiated in the already separated layer of mesoblast. In all cases the notochord and the hypoblast below it unite with the front end of the primitive streak; with which also the two lateral plates of mesoblast become continuous.

From what has just been said it is clear that in the region of the embryo the mesoblast originates as two lateral plates split off from the hypoblast, and that the notochord originates as a median plate, simultaneously with the mesoblast, with which it may sometimes be at first continuous.

Kolliker holds that the mesoblast of the region of the embryo is derived from a forward growth from the primitive streak. There is no theoretical objection to this view, and I think it would be impossible to shew for certain by sections whether or not there is a growth such as he describes ; but such sections as that represented in fig. 99 (and I have series of similar sections from several embryos) appear to me to be conclusive in favour of the view that the mesoblast of the region of the embryo is to a large extent derived


158


FORMATION OF MESOBLAST.


from a differentiation of the primitive hypoblast. I am however inclined to believe that some of the mesoblast cells of the embryonic region have the derivation which Kolliker ascribes to all of them.



'e/l.


FIG. 100. TRANSVERSE SECTION THROUGH THE EMBRYONIC REGION OF THE BLASTODERM OF A CHICK AT THE TIME OF THE FORMATION OF THE NOTOCHORD, BUT BEFORE THE APPEARANCE OF THE MEDULLARY GROOVE.

ep. epiblast; hy. hypoblast; ch. notochord; me. mesoblast; n. nuclei of the germinal wall yk.

As regards the mesoblast of the primitive streak, in a purely objective description like that given above, the greater part of it may fairly be described as being derived from the epiblast. But if it is granted that the primitive streak corresponds with the blastopore, it is obvious to the comparative embryologist that the mesoblast derived from it really originates from the lips of the blastopore, as in so many other cases ; and that to describe it, without explanation, as arising from the epiblast, would give an erroneous impression of the real nature of the process.

The differentiation of the embryo may be said to commence with the formation of the notochord and the lateral plates of mesoblast. Very shortly after the formation of these structures



FIG. iot. TRANSVERSE SECTION OF A BLASTODERM INCUBATED FOR 18 HOURS.

The section passes through the medullary groove me., at some distance behind its front end.

A. epiblast. B. mesoblast. C. hypoblast.

m.c. medullary groove; m.f. medullary fold; ch. notochord.

the axial part of the epiblast, above the notochord and in front of the primitive streak, which is somewhat thicker than


AVES.


159


the lateral parts, becomes differentiated into a distinct medullary plate, the sides of which form two folds the medullary folds enclosing between them a medullary groove (fig. 101).

In front the two medullary folds meet, while posteriorly they thin out and envelop between them the front end of the primitive streak. On the formation of the medullary folds the embryo assumes a form not unlike that of the embryos of many Ichthyopsida at a corresponding stage. The appearance of the embryo, and its relation to the surrounding parts is somewhat diagrammatically represented in fig. 102. The primitive streak now ends with an anterior swelling (not represented in the figure), and is usually somewhat unsymmetrical. In most cases its axis is more nearly continuous with the left, or sometimes the right, medullary fold than with the medullary groove. In sections its front end appears as a ridge on one side or on the middle of the floor of the widened end of the medullary groove.

The mesoblast and hypo


FIG. 102. SURFACE VIEW OF THE PELLUCID AREA OF A BLASTODERM OF l8

HOURS.

None of the opaque area is shewn, the pear-shaped outline indicating the limits of the pellucid area.

At the hinder part of the area is seen the primitive groove pr., with its nearly parallel walls, fading away behind, but curving round and meeting in front so as to form a distinct anterior termination to the groove, about halfway up the pellucid area.

Above the primitive groove is seen the medullary groove m.c., with the medullary folds A. These, diverging behind, slope away on either side of the primitive groove, while in front they curve round and meet each other close upon a curved line which represents the headfold.

The second curved line in front of and concentric with the first is the commencing fold of the amnion.


blast, within the area pellucida, do not give rise to the whole of these two layers in the surrounding area opaca ; but the whole of the hypoblast of the area opaca, and a large portion of the mesoblast, and possibly even some of the epiblast, take their origin from the peculiar material already spoken of, which forms the germinal wall, and is continuous with


160 GERMINAL WALL.


the hypoblast at the edge of the area opaca (vide figs. 91, 94, 97, 98, 99, 100).

The exact nature of this material has been the subject of many controversies. Into these controversies it is not my purpose to enter, but subjoined are the results of my own examination. The germinal wall first consists, as already mentioned, of the lower cells of the thickened edge of the blastoderm, and of the subjacent yolk material with nuclei. During the period before the formation of the primitive streak the epiblast extends itself over the yolk, partly, it appears, at the expense of the cells of the germinal wall, and possibly even of cells formed around the nuclei in this part. This mode of growth of the epiblast is very similar to that in the epibolic gastrulas of many Invertebrata, of the Lamprey, etc. ; but how far this process is continued in the subsequent extension of the epiblast I am unable to say. The cells of the germinal wall, which are at first well separated from the yolk below, become gradually absorbed in the growth of the hypoblast, and the remaining cells and yolk then become mingled together, and constitute a compound structure, continuous at its inner border with the hypoblast. This structure is the germinal wall usually so described. It is mainly formed of yolk granules with numerous nuclei, and a somewhat variable number of largish cells imbedded amongst them. The nuclei typically form a special layer immediately below the epiblast, some of which are probably enclosed by a definite cell-body. A special mass of nuclei (vide figs. 98 and 100, ) is usually present at the junction of the hypoblast with the germinal wall.

The germinal wall at this stage corresponds in many respects with the granular material, forming a ring below the edge of the blastoderm in Teleostei.

It retains the characters above enumerated till near the close of the first day of incubation, i.e. till several mesoblastic somites have become established. It then becomes more distinctly separated from the subjacent yolk, and its component parts change very considerably in character. The whole wall becomes much less granular. It is then mainly formed of large vesicles, which often assume a palisade-like arrangement, and contain granular balls, spherules of white yolk, and in an early stage a good deal of granular matter (vide fig. 115). These bodies have some resemblance to cells, and have been regarded as such by Kolliker (No. 135) and Virchow (No. 150) : they contain however nothing which can be considered as a nucleus. Between them however nuclei 1 may easily be seen in specimens hardened in picric acid, and stained with hasmatoxylin (these nuclei are not shewn in fig. 115). These nuclei are about the same size as those of the hypoblast cells, and are surrounded by a thin layer of granular protoplasm,

1 The presence of numerous nuclei in the germinal wall was, I believe, first clearly proved by His (No. 132). I cannot however accept the greater number of his interpretations.


AVES. l6l

which is continuous with a meshwork of granular protoplasm enveloping the above described vesicles. The germinal wall is still continuous with the hypoblast at its edge ; and close to the junction of the two the hypoblast at first forms a layer of moderately columnar cells, one or two deep and directly continuous with the germinal wall, and at a later period usually consists of a mass of rounder cells lying above the somewhat abrupt inner edge of the germinal wall.

The germinal wall certainly gives rise to the hypoblast cells, which mainly grow at its expense. They arise at the edge of the area pellucida, and when first formed are markedly columnar, and enclose in their protoplasm one of the smaller vesicles of the germinal wall.

In the later stages (fourth day and onwards) the whole germinal wall is stated to break up into columnar hypoblast cells, each of them mainly formed of one of the vesicles just spoken of. After the commencing formation of the embryo the mesoblast becomes established at the inner edge of the area opaca, between the germinal wall and the epiblast ; and gives rise to the tissue which eventually forms the area vasculosa. It seems probable that the mesoblast in this situation is mainly derived from cells formed around the nuclei of the germinal wall, which are usually specially aggregated close below the epiblast. Disse (No. 122) has especially brought evidence in favour of this view, and my own observations also support it.

The mesoblastic somites begin to be formed in the lateral plates of the mesoblast before the closure of the medullary folds. The first somite arises close to the foremost extremity of the primitive streak, but the next is stated to arise in front of this, so that the first formed somite corresponds to the second permanent vertebra 1 . The region of the embryo in front of the second formed somite at first the largest part of the embryo is the cephalic region. The somites following the second are formed in the regular manner, from before backwards, out of the unsegmented posterior part of the embryo, which rapidly grows in length to supply the necessary material (fig. 103). As the somites retain during the early stages of development an approximately constant breadth, their number is a fair test of the length of the trunk. With the growth of the embryo the primitive streak is continually carried back, the lengthening of the embryo always taking place between the front end of the primitive streak and the last somite ; and during this

1 Further investigations in confirmation of this widely accepted statement are very desirable.

B. III. I *


1 62


FIRST FORMATION OF THE EMBRYO.



FIG. 103. DORSAL VIEW OF THE HARDENED BLASTO


process the primitive streak undergoes important changes both in itself and in its relation to the embryo. Its anterior thicker part, which is enveloped in the diverging medullary folds, soon becomes distinguished in structure from the part behind this, and placed symmetrically in relation to the axis of the embryo (fig. 103, a.pr\ and at the same time the medullary folds, which at first simply diverge on each side of the primitive streak, bend in again and meet behind so as completely to enclose the front part of the primitive streak. The region of the embryo bird, where

the medullary folds diverge, is known DERM OF A CHICK WITH FIVE as the sinus rhomboidalis, though it MESOBLASTIC SOMITES. THE

.,,.,, MEDULLARY FOLDS HAVE MET

has no connection with the similarly FOR PART OF THEIR EXTENT, named structure in the adult. By the BUT HAVE NOT UNITED. time that ten somites are formed the a -P r - anterior part of the

..... primitive streak ; p-pr. pos Sinus rhomboidalis IS completely CS- terior part of the primitive

tablished, and the medullary groove streak has become converted into a tube till close up to the front end of the sinus. In the following stages the closure of the medullary canal extends to the sinus rhomboidalis, and the folding off of the hind end of the embryo from the yolk commences. Coincidently with the last-named changes the sides of the front part of the primitive streak become thickened, and give rise to conspicuous caudal swellings ; in which the layers of the embryo are indistinguishably fused. The apparently hinder part of the primitive streak becomes, as more particularly explained in the sequel, folded downwards .and forwards on the ventral side.


This is a convenient place to notice remarkable appearances which present themselves close to the junction of the neural plate and the primitive streak. These are temporary passages leading from the hinder end of the neural tube into the alimentary canal. They vary somewhat in different species of birds, and it appears that in the same species there may be several openings of the kind, which appear one after the other and then


AVES. 163

close again. They were first discovered by Gasser (No. 127). In all cases 1 they lead round the posterior end of the notochord, or through the point where the notochord falls into the primitive streak.

If the primitive streak is, as I believe, formed of the lips of the blastopore, there can be but little doubt that these structures are disappearing, and functionless rudiments of the opening of the blastopore, and they thus lend support to my view as to the nature of the primitive streak. That, in part, they correspond with the neurenteric canal of the Ichthyopsida is clear from the detailed statements below. Till their relations have been more fully worked out it is not possible to give a more definite explanation of them.

According to Braun (No. 120) three independent communications are to be distinguished in Birds. These are best developed in the Duck. The first of these is a small funnel-shaped diverticulum leading from the neural groove through the hypoblast. It is visible when eight mesoblastic somites are present, and soon disappears. The second, which is the only one I have myself investigated, is present in the embryo duck with twenty-six mesoblastic somites, and is represented in the series of sections (fig. 104). The passage leads obliquely backwards and ventralwards from the hind end of the neural tube into the notochord, where the latter joins the primitive streak (B). A narrow diverticulum from this passage is continued forwards for a short distance along the axis of the notochord (A, ch}. After traversing the notochord, the passage is continued into a hypoblastic diverticulum, which opens ventrally into the future lumen of the alimentary tract (C). Shortly behind the point where the neurenteric passage communicates with the neural tube the latter structure opens dorsally, and a groove on the surface of the primitive streak is continued backwards from it for a short distance (C). The first part of this passage to appear is the hypoblastic diverticulum above mentioned.

This passage does not long remain open, but after its closure, when the tail-end of the embryo has become folded off from the yolk, a third passage is established, and leads round the end of the notochord from the closed medullary canal into the post-anal gut. It is shewn diagrammatically in fig. 1 06, ne, and, as may be gathered from that figure, has the same relations as the neurenteric canal of the Ichthyopsida.

In the goose a passage has been described by Gasser, which appears when about fourteen or fifteen somites are present, and lasts till twentythree are formed. Behind its opening the medullary canal is continued back as a small diverticulum, which follows the course of the primitive groove and is apparently formed by the conversion of this groove into a canal. It is at first open to the exterior, but soon becomes closed, and then atrophies.

In the chick there is a perforation on the floor of the neural canal,

1 This does not appear to be the case with the anterior opening in Melopsittacus undulatus, though its relations are not clear from Braun's description (No. 120).

II 2


164


NEURENTERIC CANAL.


which is not so marked as those in the goose or duck, and never results in a complete continuity between the neural and alimentary tracts ; but simply leads from the floor of the neural canal into the tissues of the tail-swelling, and thence into a cavity in the posterior part of the noto


FlG. 104. FOUR TRANSVERSE SECTIONS THROUGH THE NEURENTERIC PASSAGE AND ADJOINING PARTS IN A DUCK EMBRYO WITH TWENTY-SIX MESOBLASTIC SOMITES.

A. Section in front of the neurenteric canal shewing a lumen in the notochord.

B. Section through the passage from the medullary canal into the notochord.

C. Section shewing the hypoblastic opening of the neurenteric canal, and the groove on the surface of the primitive streak, which opens in front into the medullary canal.

D. Primitive streak immediately behind the opening of the neurenteric passage. me. medullary canal; ep. epiblast; hy. hypoblast; ch. notochord; pr. primitive

streak.

chord. The hinder diverticulum of the neural canal along the line of the primitive groove is, moreover, very considerable in the chick, and is not so soon obliterated as in the goose. The incomplete passage in the chick arises when about twelve somites are present. It is regarded by Braun as equivalent to the first formed passage in the duck, but I very much doubt whether there is a very exact equivalence between the openings in different types, and think it. more probable that they are variable remnants of a primitive neurenteric canal, which in the ancestors of those forms persisted through the whole period of the early development. The third passage is formed in the chick (Kupffer) during the third day of incubation. In



AVES. 165

Melopsittacus undulatus the two first communications are stated by Braun (No. 120) to be present at the same time, the one in front of the other.

It is probable, from the above description, that the front portion of the primitive streak in the bird corresponds with that part of the lips of the blastopore in Elasmobranchii which becomes converted into the tail-swelling and the lining of the neurentic canal ; while the original groove of the front part of the primitive streak appears to be converted into the posterior diverticulum of the neural canal. The hinder part of the primitive streak of the bird corresponds, in a very general way, with the part of the blastopore in Elasmobranchii, which shuts off the embryo from the edge of the blastoderm (vide p. 64), though there is of course no genetic relation between the two structures. When the anterior part of the streak is becoming converted into the tail-swelling, the groove of the posterior part gradually shallows and finally disappears. The hinder part itself atrophies from behind forwards, and in the course of the folding off of the embryo from the yolk the part of the blastoderm where it was placed becomes folded in, so as to form part of the ventral wall of the embryo. The apparent hinder part of the primitive streak is therefore in reality the ventral and anterior part 1 .

It has generally been maintained that the primitive streak and groove become wholly converted into the dorsal portion of the trunk of the embryo, i. e. into the posterior part of the medullary plate and subjacent structures. This view appears to me untenable in itself, and quite incompatible with the interpretation of the primitive streak given above. To shew how improbable it is, apart from any theoretical considerations, I have compiled two tables of the relative lengths of the primitive streak and the body of the embryo, measured by the number of sections made through them, in a series of examples from the data in Gasser's important memoir (No. 127). In these tables each horizontal line relates to a single embryo. The first column shews the number of somites, and the second the number of sections

1 This nomenclature may seem a little paradoxical. But on reflection it will appear that so long as the embryo is simply extended on the yolk-sphere, the point where the ventral surface begins has to be decided on purely morphological grounds. That point may fairly be considered to be close to the junction of the medullary plate and primitive streak. To use a mathematical expression the sign will change when we pass from the dorsal to the ventral surface, so that in strict nomenclature we ought in continuing round the egg in the same direction to speak of passing backwards along the medullary, but forwards along the primitive streak. Thus the apparent hind end of the primitive streak is really the front end, and vice versa. I have avoided using this nomenclature to simplify my description, but it is of the utmost importance that the morphological fact should be grasped. If any reader fails to understand my point, a reference to fig. 52 B will, I trust, make everything quite clear. The heart of Acipenser (At) is there seen apparently in front of the head. It is of course really ventral, and its apparent position is due to the extension of the embryo on a sphere. The apparent front end of the heart is really the hind end, and vice versd.


1 66


HISTORY OF THE GERMINAL LAYERS.


through the primitive streak. Where the primitive streak becomes divided into two parts the sections through the two parts are given separately : the left column (A) referring to the anterior part of the streak ; the right column (P) to the posterior part. The third column gives the number of sections through the embryo. The first table is for fowl embryos, the second for goose embryos.


No. of Somites.


No. of sections through the Primitive Streak.


No. of sections through the Embryo.



29


7


o


45


10


o


39


23


2


3


30


4


3


3



A P



5 or 6


10+17 = 27



8


12 + 20 = 32


48


12


13+10 = 23



14


9+12 = 21



18


10+ 7 = 17


70



8+ 4=12




8+ 3 = 11



No. of Somites.


No. of sections through the Primitive Streak.


No. of sections through the Embryo.


o


10


4


o 28


5


o 44


12


36


32


4


24


4 2



A P



9


10+ 10 = 20


61


H


8+10 = 18


68


17


8+ 5 = i3



22


9+ 6=15



26


6+ 5 = 11



An inspection of these two tables shews that an actual diminution in the length of the primitive streak takes place just about the time when the first somites are being formed, but there is no ground for thinking that the primitive streak becomes then converted into the medullary plate. Subsequently the primitive streak does not for a considerable time become markedly shorter, and certainly its curtailment is not really sufficient to account for the increased length of the embryo an increase in length, which (with the exception of the head) takes place entirely by additions at the hind end. At the stage with fourteen somites the primitive streak is still pretty long. In the later stages, as is clearly demonstrated by the tables, the diminution in the length of the primitive streak mainly concerns the posterior part and not that adjoining the embryo.

General history of tJie germinal layers.

The epiblast. The epiblast of the body of the embryo, though several rows of cells deep, does not become divided into two strata till late in embryonic life ; so that the organs of sense formed from the epiblast, which are the same as in the types already described, are not specially formed from an inner nervous stratum. The medullary canal is closed in the same


AVES.


167


manner as in Elasmobranchii, the Frog, etc., by the simple conversion of an open groove into a closed canal. The closure commences first of all in the region of the mid-brain, and extends rapidly backwards and more slowly forwards. It is completed in the Fowl by about the time that twelve mesoblastic somites are formed.

The mesoblast. The general changes of this layer do not exhibit any features of special interest the division into lateral and vertebral plates, etc., being nearly the same as in the lower forms.

The hypoblast. The closure of the alimentary canal is entirely effected by a process of tucking in or folding off of the embryo from the yolk-sack. The general nature of the process is seen in the diagrams figs. 105 and 121. The folds by which it is effected are usually distinguished as the head-, the tail- and the lateral folds. The head-fold (fig. 105) is the first to appear ;

JVC.



FIG.


105.


DIAGRAMMATIC LONGITUDINAL SECTION THROUGH THE AXIS OF AN EMBRYO BIRD.

The section is supposed to be made at a time when the head-fold has commenced but the tail-fold has not yet appeared.

f.So. head-fold of the somatopleure. F.Sp. head-fold of the splanchnopleure.

pp. pleuroperitoneal cavity; Am. commencing (head-) fold of the amnion; D. alimentary tract; N.C. neural canal; Ch. notochord; A. epiblast ; B. mesoblast; C. hypoblast.

and in combination with the lateral folds gives rise to the anterior part of the mesenteron (D) (including the oesophagus, stomach and duodenum), which by its mode of formation clearly ends blindly in front. The tail-fold, in combination with the two lateral folds, gives rise to the hinder part of the alimentary tract, including the cloaca, which is a true part of the mesenteron. At the junction between the two folds there is present


1 68


HISTORY OF THE GERMINAL LAYERS.


a circular opening leading into the yolk-sack, which becomes gradually narrowed as development proceeds. The opening is completely closed long before the embryo is hatched. Certain peculiarities in reference to the structure of the tail-fold are caused by the formation of the allantois, and are described with the embryonic appendages. The stomodaeum and proctodaeum are formed by epiblastic invaginations. The communication between the stomodaeum and the mesenteron is effected comparatively early (on the 4th day in the chick), while that between the proctodaeum and mesenteron does not take place till very late (i$th day in the chick). The proctodaeum gives rise to the bursa Fabricii, as well as to the anus. Although the



FIG. 106. DIAGRAMMATIC LONGITUDINAL SECTION THROUGH THE POSTERIOR END OF AN EMBRYO BIRD AT THE TIME OF THE FORMATION OF THE ALLANTOIS. ep. epiblast ; Sp.c. spinal canal ; ch. notochord ; n.e . neurenteric canal ; hy. hypoblast; p-a.g. post-anal gut; pr. remains of primitive streak folded in on the ventral side; al. allantois; me. mesoblast; an. point where anus will be formed ', p.c. perivisceral cavity ; am. amnion ; so. somatopleure ; sp. splanchnopleure.

opening of the anus is so late in being formed, the proctodaeum itself is very early apparent. Soon after the hinder part of the primitive streak becomes tucked in on the ventral side of the embryo, an invagination may be noticed where the tail of the embryo is folded off. This gradually becomes deeper, and finally comes into contact with the hypoblast at the front (primitively the apparent hind) border of the posterior section of the primitive streak. An early stage in the invagination is shewn in the diagram (fig. 106, an}. It deserves to be noted that the anus lies some way in front of the blind end of



AVES. 169

the mesenteron, so that there is in fact a well-developed postanal section of the gut (fig. 106, p.a.g), which corresponds with that in the Ichthyopsida. For a short period, as mentioned above (p. 163), a neurenteric canal is present connecting the post-anal gut with the medullary tube in the duck, fowl, and other birds. On the ventral wall of the post-anal gut there are at first two prominences. The posterior of these is formed of part of the tail-swelling, and is therefore derived from the apparent anterior part of the primitive streak. The anterior is formed from what was originally the apparent posterior part of the primitive streak. The post-anal gut becomes gradually less and less prominent, and finally atrophies.

General development of the Embryo.

It will be convenient to take the Fowl as a type for the general development of the Sauropsida.

The embryo occupies a fairly constant position with reference to the egg-shell. Its long axis is placed at right angles to that of the egg, and the broad end of the egg is on the left side of the embryo. The general history of the embryo has already been traced up to the formation of the first formed mesoblastic somites (fig. 107). This stage is usually reached at about the close of the first day. After this stage the embryo rapidly grows in length, and becomes, especially in front and to the sides, more and more definitely folded off from the yolksack.

The general appearance of the embryo between the 3Oth and 4Oth hours of incubation is shewn in fig. 108 from the upper surface, and in fig. 109 from the lower. The outlines of the embryo are far bolder than during the earlier stages. Fig. 109 shews the nature of the folding, by which the embryo is constricted off from the yolk-sack. The folds are complicated by the fact that the mesoblast has already become split into two layers a splanchnic layer adjoining the hypoblast and a somatic layer adjoining the epiblast and that the body cavity between these two layers has already become pretty wide in the lateral parts of the body of the embryo and the area pellucida. The fold by which the embryo is constricted off from the yolk


I/O


GENERAL DEVELOPMENT OF THE EMBRYO.



sack is -in consequence a double one, formed of two limbs or laminae, an inner limb constituted by the splanchnopleure, and an outer limb by the somatopleure. The relation of these two limbs is shewn in the diagrammatic longitudinal section (fig. 105), and in the surface view (fig. 109) the splanchnic limb being shewn at sf and the somatic at so. Between the two limbs, and closely adjoining the splanchnopleure, is seen the heart (hf). At the stage figured the head is well marked off from the trunk, but the first separation between the two regions was effected at an earlier period, on the appearance of the foremost somite (fig. 107). Very shortly after the cephalic region is established, and before the closure of the medullary folds, the anterior part of the neural canal becomes enlarged to form the first cerebral vesicle, from which two lateral diverticula rudiments of the optic lobes are almost at once given off (fig. 108, op.v). By the stage figured the cephalic part of the neural canal has become distinctly differentiated into a fore(/.), a mid- (m.b] and a hind-brain (k.b} ; and the hind-brain is often subdivided into successive lobes. In the region of the hind-brain two shallow epiblastic invaginations form the rudiments of the auditory pits (au. p}.

A section through the posterior part of the head of an embryo of 30 hours is represented in fig. no. The enlarged part of the neural tube, forming the hind-brain, is shewn at (hb). It is still connected with the epidermis, and at its dorsal border an outgrowth on each side forming the root of the vagus nerve is present (vg). The notochord (ch) is seen below the brain, and below this again the crescentic foregut (al). The commencing heart (hi), formed at this stage of two distinct tubes, is attached to the ventral side of the foregut.

On the dorsal side of the foregut immediately below the notochord is


FIG. 107. DORSAL VIEW OF THE HARDENED BLASTODERM OF A CHICK WITH FIVE MESOBLASTIC SOMITES. THE MEDULLARY FOLDS HAVE MET

FOR PART OF THEIR EXTENT, BUT HAVE NOT UNITED.

a.pr. anterior part of the primitive streak ; f-pf. posterior part of the primitive streak.


AVES.


171


ojt.v:


seen a small body (x) formed as a thickening of the hypoblast. This may possibly be a rudiment of the subnotochordal rod of the Ichthyopsida.

In the trunk (fig. 108) the chief point to be noticed is the complete closure of the neural canal, though in the posterior part, where the open sinus rhomboidalis was situated at an earlier stage, there may still be seen a dilatation of the canal (fig. 1 08, s.r}, on each side of which are the tail-swellings ; while the mesoblastic somites stop short somewhat in front of it. Underneath the neural canal may be seen the notochord (fig. 109, cJi) extending into the head, as far as the base of the midbrain. At the sides of the trunk are seen the mesoblastic somites (/. v), the outer edges of which mark the boundary between the vertebral and lateral plates. A fainter line can be seen marking off the part of the lateral plates which will become

FIG. 108. EMBRYO OF THE CHICK BETWEEN 30 AND 36 HOURS VIEWED FROM ABOVE

AS AN OPAQUE OBJECT. (Chromic acid preparation.)

f.b. front-brain; m.b. midbrain; h.b. hind-brain; op.v. optic vesicle ; ati.p. auditory pit; o.f. vitelline vein; p.v. mesoblastic somite; m.f. line of junction of the medullary folds above the medullary canal ; s.r. sinus rhomboidalis ; t. tail-fold ; p.r. remains of primitive groove (not satisfactorily represented) ; a.p. area pellucida.

The line to the side between p.v. and m.f. represents the true length of the embryo.

The fiddle-shaped outline indicates the margin of the pellucid area. The head, which reaches as far back as o.f., is distinctly marked off; but neither the somatopleuric nor splanchnopleuric folds are shewn in the figure ; the latter diverge at the level of o.f., the former considerably nearer the front, somewhere between the lines m.b. and h.b. The optic vesicles op.v. are seen bulging out beneath the superficial cpiblast. The heart lying underneath the opaque body cannot be seen. The tail-fold t. is just indicated; no distinct lateral folds are as yet visible in the region midway between head and tail. At m.f. the line of junction between the medullary folds is still visible, being lost forwards over the cerebral vesicles, while behind may be seen the remains of the sinus rhomboidalis, s.r.



P- r


172


DEVELOPMENT DURING THE SECOND DAY.


FIG. 109. AN EMBRYO CHICK OF ABOUT THIRTY-SIX HOURS VIEWED FROM BELOW AS A TRANSPARENT OBJECT.

FB. the fore-brain or first cerebral vesicle, projecting from the sides of which are seen the optic vesicles op. A definite head is now constituted, the backward limit of the somatopleure fold being indicated by the faint line S. O. Around the head are seen the two limbs of the amniotic head-fold: one, the true amnion <z, closely enveloping the head, the other, the false amnion a', at some distance from it. The head is seen to project beyond the anterior limit of the pellucid area..

The splanchnopleure fold extends as far back as sp. Along its diverging limbs are seen the conspicuous venous roots of the vitelline veins, uniting to form the heart h, already established by the coalescence of two lateral halves which, continuing forward as the bulbus arteriosus b.a, is lost in the substance of the head just in front of the somatopleure fold.

HB. hind-brain; MB. mid-brain; p.v. and v.pl. mesoblastic somites ; ch. front end of notochord; me. posterior part of notochord; . parietal mesoblast; //. outline of area pellucida; pv. primitive streak.



hi,



FIG. 110. TRANSVERSE SECTION THROUGH THE POSTERIOR PART OF THE HEAD

OF AN EMBRYO CHICK OF THIRTY HOURS.

lib. hind-brain; vg. vagus nerve; ep. epiblast; ch. notochord; x. thickening of hypoblast (possibly a rudiment of the subnotochordal rod); al. throat; hi. heart; pp. body cavity ; so. somatic mesoblast ; s/. splanchnic mesoblast ; hy. hypoblast.


AVES.


173


part of the body-wall, from that which pertains to the yolksack.

During the latter half of the second day, and during the third day, great progress is made in the folding off of the


FlG. III. CHICK OF THE THIRD DAY (54 HOURS) VIEWED FROM UNDERNEATH AS A TRANSPARENT


IIB


OBJECT.

a', the outer amniotic fold or false amnion. This is very conspicuous around the head, but may also be seen at the tail.

a, the true amnion, very closely enveloping the head, and here seen only between the projections of the several cerebral vesicles. It may also be traced at the tail, t.

In the embryo of which this is a drawing the head-fold of the amnion reached a little farther backward than the reference u, but its limit cannot be distinctly seen through the body of the embryo.

C.H. cerebral hemisphere; F.B. vesicle of the third ventricle ; M.S. mid-brain; H.B. hind-brain; Op. eye; Ot. auditory vesicle.

OfV. vitelline veins forming the venous roots of the heart. The trunk on the right hand (left trunk when the embryo is viewed in its natural position from above) receives a large branch, shewn by dotted lines, coming from the anterior portion of the sinus terminalis. Ht. the heart, now completely twisted on itself. Ao. the bulbus arteriosus, the three aortic arches being dimly seen stretching from it across the throat, and uniting into the aorta, still more dimly seen as a curved dark line running along the body. The other curved dark line by its side, ending near the reference y, is the notochord ch.

About opposite the line of reference x the aorta divides into two trunks, which running in the line of the somewhat opaque somites on either side, are not clearly seen. Their branches however, Of. a, the vitelline arteries, are conspicuous and are seen to curve round the commencing side- folds.

Pv. mesoblastic somites.

x is placed at the "point of divergence " of the splanchnopleure folds. The blind foregut begins here and extends about up to near y, the more transparent space marked by that letter is however mainly due to the presence there of investing mass at the base of the brain, x marks the hind limit of the splanchnopleure folds. The limit of the more transparent somatopleure folds cannot be seen.

It will be of course understood that all the body of the embryo above the level of the reference x, is seen through the portion of the yolk-sack (vascular and pellucid area), which has been removed with the embryo from the egg, as well as through the double amniotic fold.

The view being from beiow, whatever is described in the natural position as being to the right appears here to the left, and vice versft.



174 DEVELOPMENT DURING THE THIRD DAY.

embryo. Both the head- and tail-ends of the embryo become quite distinct, and the side-folds make such considerable progress that the embryo is only connected with the yolk by a broad stalk. This stalk is double, and consists of an inner splanchnic stalk, continuous with the walls of the alimentary canal, and an outer somatic stalk, continuous with the body-walls of the embryo. The somatic stalk is very much wider than the splanchnic. (Compare fig. 121 E and F, which may be taken as diagrammatic longitudinal and transverse sections of the embryo on the third day.) A change also takes place in the position of the embryo. Up to the third day it is placed symmetrically, on the yolk, with its ventral face downwards. During this day it turns so as partially to lie on its left side. This rotation affects first the head (fig. in), but in the course of the fourth day gradually extends to the rest of the body (fig. 1 1 8). Coincidently with this change in position the whole embryo undergoes a ventral and somewhat spiral flexure.

During the latter part of the second day and during the third day important changes take place in the head. One of these is the cranial flexure. This, which must not be confounded with the curvature of the body just referred to, commences by the bending downwards of the front part of the head round a point which may be considered as the extreme end either of the notochord or of the alimentary canal.

The cranial flexure progresses rapidly, the front-brain being more and more folded down till, at the end of the third day, it is no longer the first vesicle or fore-brain ; but the second cerebral vesicle or mid-brain, which occupies the extreme front of the long axis of the embryo. In fact a straight line through the long axis of the embryo would now pass through the mid-brain instead of, as at the beginning of the second day, through the fore-brain, so completely has the front end of the neural canal been folded over the end of the notochord. The commencement of this cranial flexure gives the body of an embryo of the third day somewhat the appearance of a chemist's retort, the head of the embryo corresponding to the bulb. On the fourth day the flexure is still greater than on the third, but on the fifth and succeeding days it becomes less obvious.

The anterior part of the fore-brain has now become greatly



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dilated, and may be distinguished from the posterior part as the unpaired rudiment of the cerebral hemispheres. It soon bulges out laterally into two lobes, which do not however become separated by a median partition till a much later period.

Owing to the development of the cerebral rudiment the posterior part of the fore-brain no longer occupies the front position (fig. HI, and 112 FB], and ceases to be the conspicuous object that it was. Inasmuch as its walls will hereafter be developed into the parts surrounding the so called third ventricle of the brain, it is known as the vesicle of the third ventricle, or the thalamencephalon.

On the summit of the thalamencephalon there may now be seen a small conical projection, the rudiment of the pineal gland, while the centre of the floor is produced into a funnel-shaped process, the infundibulum, which, stretching towards the extreme end of the alimentary canal, joins the pituitary body.

Beyond an increase in size, which it shares with nearly all parts of the embryo, and the change of position which has already been referred to, the mid-brain undergoes no great alterations during the third day. Its sides will ultimately become developed into the corpora bigemina or optic lobes, its floor will form the crura cerebri, and its cavity will be reduced to the narrow canal known as the iter a tertio ad quartum ventriculum and two diverticula leading from this into the optic lobes.

In the hind-brain, or third cerebral vesicle, the roof of the part which lies nearest to the mid-brain, becomes during the third day marked off from the rest by a slight constriction. This distinction, which becomes much more evident later on by


FIG. 112. SIDE VIEW OF THE HEAD OF AN EMBRYO CHICK OF THE THIRD DAY AS AN OPAQUE OBJECT. (Chromic acid preparation.)

CH. Cerebral hemispheres ; F.B. Vesicle of third ventricle ; M.B. Mid-brain; Cb. Cerebellum; H.B. Medulla oblongata ; N. Nasal pit ; ot. auditory vesicle in the stage of a pit with the opening not yet closed up ; op. Optic vesicle, with /. lens and ch.f. choroidal fissure. The choroidal fissure, though formed entirely underneath the superficial epiblast, is distinctly visible from the outside.

i F. The first visceral fold ; above it is seen a slight indication of the superior maxillary process.

2, 3, 4 F. Second, third and fourth visceral folds, with the visceral clefts between them.


176 DEVELOPMENT DURING THE THIRD DAY.

a thickening of the walls and roof of the front portion, separates the hind-brain into the cerebellum and the medulla oblongata (fig. 1 1 2 Cb and HB\ While the walls of the cerebellar portion of the hind-brain become very much thickened as well at the roof as at the sides, the roof of the posterior portion or medulla oblongata thins out into a mere membrane, forming a delicate covering to the cavity of the vesicle (fig. 114 IV\ which here becoming broad and shallow with greatly thickened floor and sides, is known as the fourth ventricle, subsequently overhung by the largely-developed posterior portion of the cerebellum.



FIG. 113. HEAD OF AN EMBRYO CHICK OF THE FOURTH DAY VIEWED AS AN OPAQUE OBJECT : FROM THE FRONT IN A, AND FROM THE SIDE IN B. (Chromic acid preparation.)

CH. cerebral hemispheres ; FB. vesicle of the third ventricle ; Op. eyeball ; nf. naso-frontal process; M. cavity of mouth; SM. superior maxillary process of F. i, the first visceral fold (inferior maxillary process) ; F. 2, F. 3, second and third visceral folds ; N. nasal pit ; ot. otic vesicle.

In order to gain the view here given the neck was cut across between the third and fourth visceral folds. In the section e thus made, are seen the alimentary canal a!, the neural canal n.c., the notochord cA, the dorsal aorta AO, and the vertebral veins V.

The third day, therefore, marks the distinct differentiation of the brain into five distinct parts : the cerebral hemispheres, the central masses round the third ventricle, the corpora bigemina, the cerebellum and the medulla oblongata ; the original cavity of the neural canal at the same time passing from its temporary division of three single cavities into the permanent arrangement of a series of connected ventricles, viz. the lateral ventricles, the


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third ventricle, the iter (with a prolongation into the optic lobe on each side), and the fourth ventricle.

By the third day the lens of the eye has become formed by an invagination of the epiblast, and other changes in the eye have taken place. The external opening of the auditory pit is closed before the completion of the third day (fig. 114, RL) ; and the rudiments of the external parts of the organ of smell have become formed as small pits on the under surface of the fore-brain (fig. 112, N). Like the lens and the labyrinth of the ear, they are formed as invaginations of the external epiblast ; unlike them they are never closed up.

During the second and third days there are formed the visceral or branchial clefts, homologous with those of the


cv



cc


FIG. 114. SECTION THROUGH THE HIND-BRAIN OF A CHICK AT. THE END OF THE THIRD DAY OF INCUBATION.

IV. Fourth ventricle. The section shews the very thin roof and thicker sides of the ventricle. Ch. Notochord; CV. Anterior cardinal vein; CC. Involuted auditory vesicle ; CC points to the end which will form the cochlear canal ; RL . Recessus labyrinth! (remains of passage connecting the vesicle with the exterior); hy. Hypoblast lining the alimentary canal; AO., AOA. Aorta, and aortic arch.

Ichthyopsida, though never developing branchial processes from their walls.

They are however real clefts or slits passing right through the walls of the throat, and are placed in series on either side B. in. 12


178 VISCERAL ARCHES.


across the axis of the alimentary canal, lying not quite at right angles to that axis nor parallel to each other, but converging somewhat to the middle of the throat in front (fig. 112 and

fig. US) Four in number on either side, the anterior is the first to be formed, the other three following in succession. They originate as pouches of the hypoblast, which meet the epiblast. At the junction of the epiblast and hypoblast an absorption of the tissue is effected, placing the pouches in communication with the exterior.

No sooner has a cleft been formed than its anterior border (i.e. the border nearer the head) becomes raised into a thick lip or fold, the visceral or branchial fold. Each cleft has its own fold on its anterior border, and in addition the posterior border of the fourth or last visceral cleft is raised into a similar fold. There are thus five visceral folds to four visceral clefts (figs. 1 1 2 and 1 1 3). The last two folds however, and especially the last, are not nearly so thick and prominent as the other three, the second being the broadest and most conspicuous of all. The first fold meets, or nearly meets, its fellow in the middle line in front, but the second falls short of reaching the middle line, and the third, fourth and fifth do so in an increasing degree. Thus in front views of the neck a 'triangular space with its apex directed towards the head is observed between the ends of the several folds (fig. 113 A).

Into this space the pleuroperitoneal cavity extends, the somatopleure separating from the splanchnopleure along the ends of the folds ; and it is here that the aorta plunges into the mesoblast of the body.

The history of these most important visceral folds and clefts will be dealt with in detail hereafter ; meanwhile I may say that in the Chick and higher Vertebrates the first three pairs of folds are those which call for most notice.

The first fold on either side, increasing rapidly in size and prominence, does not, like the others, remain single, but sends off in the course of the third day a branch or bud-like process from its upper edge (fig. 113). This branch, starting from near the outer end of the fold, runs forwards and upwards in front of the stomodaeum, tending to meet the corresponding branch


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from the fold on the other side, ,at a point in the middle line nearer the front of the head than the junction of the main folds (fig. 1 1 3, sm}. The two branches do not quite meet, being separated by a median process, which at the same time grows down from the extreme front of the head, and against which they abut (fig. 120, /). Between the main folds, which are directed somewhat downwards and their branches which slant upwards the somewhat lozenge-shaped stomodseum is placed,


M.c.


So.


So.



FIG. 115. TRANSVERSE SECTION THROUGH THE DORSAL REGION OF AN EMBRYO

CHICK OF 45 HOURS.

M.c . medullary canal ; P.v. mesoblastic somite ; W.d. Wolffian duct ; So. Somatopleure ; S.p. Splanchnopleure ; /./. pleuroperitoneal cavity ; ao. aorta ; v. bloodvessels; iv. germinal wall; ch. notochord; op. junction between area opaca and area pellucida.

which, as the folds become more and more prominent, grows deeper and deeper (fig. 120 A). The main folds form the mandibular arch, and their branches the maxillary processes, and the descending process which helps to complete the anterior margin of the stomodseum or oral cavity is called, from the parts which will be formed out of it, t\\Qfronto-nasal process.

In two succeeding pairs of visceral folds, which correspond with the hyoid and first branchial arches of the Ichthyopsida, are developed the parts of the hyoid bone, which will be best

12 2


ISO SECTIONS DURING THE SECOND AND THIRD DAY.


considered in connection with the development of the skull. The last two disappear in the Chick without giving rise to any permanent structures. The external opening of the first visceral i.e. hyomandibular cleft becomes closed 1 , but the inner part of the cleft, opening into the mouth, gives rise to the Eustachian tube and the tympanic cavity, the latter being formed as a special diverticulum.

Part of the membranous mandibular and hyoid arches form a wall round the dorsal part of the original opening of this cleft, and so give rise to the meatus auditorius externus. At the bottom of this is placed the tympanic membrane, which is probably derived from the tissue which grows over the dorsal part of the opening of the first cleft. It is formed of an external epiblast epithelium, a middle layer of mesoblast, and an internal hypoblastic epithelium.



FIG. 1 16. TRANSVERSE SECTION THROUGH THE TRUNK OF A DUCK EMBRYO

WITH ABOUT TWENTY-FOUR MESOBLASTIC SOMITES.

am. amnion ; so. somatopleure ; sp. splanchnopleure ; wd. Wolffian duct ; st. segmental tube; ca.v. cardinal vein; ms. muscle-plate; sp.g. spinal ganglion; sp.c. spinal cord ; c h. notochord ; ao. aorta ; hy. hypoblast.

1 Vide Moldenhauer, " Die Entwicklung des mittleren und des ausseren Ohres." Morphologisches Jahrbuch, Vol. III. 1877.


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The general nature of the changes, which take place in the trunk between the commencement of the second half of the second day and the end of the third day, is illustrated by the sections figs. 115, 116, 117.


tup



so


117.


SECTION THROUGH THE DORSAL REGION OF AN EMBRYO CHICK AT

THE END OF THE THIRD DAY.

Am. amnion ; m.p. muscle-plate. C. V. cardinal vein. Ao. dorsal aorta. The section passes through the point where the dorsal aorta is just commencing to divide into two branches. Ch. notochord ; W.d. Wolffian duct ; W.b. commencing differentiation of the mesoblast cells to form the Wolffian body ; ep. epiblast ; So. somatopleure ; Sp. splanchnopleure; hy. hypoblast. The section passes through the point where the digestive canal communicates with the yolk-sack, and is consequently still open below.

In the earliest of these sections there is not a trace of a folding off of the embryo from the yolk, and the body walls are quite horizontal. In the second section (fig. 116), from an embryo of about two days, the body walls are already partially inclined, and the splanchnopleure is very distinctly folded inwards. There is a considerable space between the notochord and the hypoblast, which forms the rudiment of the mesentery.


1 82 SECTIONS DURING THE SECOND AND THIRD DAY.

In the third section (fig. 117) the body walls have become nearly vertical, the folding of the splanchnopleure is nearly completed, and it is only for a small region that the alimentary tract is open, by the vitelline duct, to the yolk-sack.

These three sections further illustrate (i) the gradual diffe


ffJ3



FIG. 118. EMBRYO CHICK AT THE END OF THE FOURTH DAY SEEN AS A TRANSPARENT OBJECT.

The amnion has been completely removed, the cut end of the somatic stalk is shewn at S.S. with the allantois (Al) protruding from it.

C.H. cerebral hemisphere; F.B. vesicle of the third ventricle with the pineal gland (Pn) projecting from its summit; M.B. mid-brain; Cb. cerebellum. IV. V. fourth ventricle; Z. lens; ch.s. choroid slit. Owing to the growth of the optic cup the two layers of which it is composed cannot any longer be seen from the surface, but the retinal surface of the layer alone is visible. Cen. V. auditory vesicle; s.rn. superior maxillary process; i f, if, etc. first, second, third and fourth visceral arches; V. fifth nerve sending one branch to the eye, the ophthalmic branch, and another to the first visceral arch ; VII. seventh nerve passing to the second visceral arch ; G.Ph. glossopharyngeal nerve passing towards the third visceral arch ; Pg. pneumogastric nerve passing towards the fourth visceral arch; iv. investing mass. No attempt has been made in the figure to indicate the position of the dorsal wall of the throat, which cannot be easily made out in the living embryo; ch. notochord. The front end of this cannot be seen in the living embryo. It does not end however as shewn in the figure, but takes a sudden bend downwards and then terminates in a point. Ht. heart seen through the walls of the chest; M.P. muscle-plates. W. wing; //. /.. hind limb. Beneath the hind limb is seen the curved tail.



AVKS.


183


rentiation of the mesoblastic somites (fig. 115, P.v] into (a) the muscle-plates (figs. 116, ms and 117, m.p), and (b} the tissue to form the vertebral bodies and adjacent connective tissue ; (2) the formation of a mass of tissue between the lateral plates and the mesoblastic somites (fig. 115), known as the intermediate cell mass, on the dorsal side of which the Wolffian duct is formed, while the intermediate cell mass itself breaks up into the segmental tubes (fig. 116, st) and connective tissue of the Wolffian body.


W.R



FIG. 119. SECTION THROUGH THE LUMBAR REGION OF AN EMBRYO CHICK AT THE END OF THE FOURTH DAY.

n.c. neural canal; p.r. posterior root of spinal nerve with ganglion; a.r. anterior root of spinal nerve; A.G.C. anterior grey column of spinal cord; A.W.C. anterior white column of spinal cord just commencing to be formed, and not very distinctly marked in the figure; m.p. muscle-plate; ch. notochord; W.R. Wolffian ridge; A 0. dorsal aorta ; V.c.a. posterior cardinal vein ; W.d. Wolffian duct; W.b. Wolffian body, consisting of tubules and Malpighian bodies ; g.e. germinal epithelium ; d. alimentary canal ; M. commencing mesentery; SO. somatopleure ; SP. splanchnopleure ; V. blood-vessels ; pp. pleuroperitoneal cavity.


1 84


DEVELOPMENT DURING THE FOURTH DAY.


Various other features in the development of the vascular system, general mesoblast, etc., are also represented in these sections. It may more especially be noted that there are at first two widely separated dorsal aortae, which gradually approach (figs. 115 and 116); and meeting first of all in front finally coalesce (figs. 1 17 and 119) for their whole length.

The general appearance of the embryo of the fourth day may be gathered from fig. 118.



FIG. 120. HEAD OF A CHICK FROM BELOW ON THE SIXTH AND SEVENTH DAYS OF INCUBATION. (From Huxley.)

/". cerebral vesicles; a. eye, in which the remains of the choroid slit can still be seen in A ; g . nasal pits ; k. fronto-nasal process ; /. superior maxillary process ; i. inferior maxillary process or first visceral arch; ?.. second visceral arch; x. first visceral cleft.

In A the cavity of the mouth is seen enclosed by the fronto-nasal process, the superior maxillary processes and the first pair of visceral arches. At the back of it is seen the opening leading into the throat. The nasal grooves leading from the nasal pits to the mouth are already closed over and converted into canals.

In B the external opening of the mouth has become much constricted, but it is still enclosed by the fronto-nasal process and superior maxillary processes above, and by the inferior maxillary processes (first pair of visceral arches) below.

The superior maxillary processes have united with the fronto-nasal process, along nearly the whole length of the latter.

The changes which have taken place consist for the most part in the further development of the parts already present, and do not need to be specified in detail. The most important event of the day is perhaps the formation of the limbs. They appear as outgrowths from a slightly marked lateral ridge (fig. 1 19, WR], which runs on the level of the lower end of the muscle-plates for



AVES. 185

nearly the whole length of the trunk. This ridge is known as the Wolffian ridge. The first trace of the limbs can be seen towards the end of the third day ; and their appearance at the end of the fourth day is shewn in fig. 1 18, W and HL.

A section through the trunk of the embryo on the fourth day is represented in fig. 119. The section passes through the region of the trunk behind the vitelline duct. The mesentery (M) is very much deeper and thinner than on the previous day. The notochord has become invested by a condensed mesoblastic tissue, which will give rise to the vertebral column. The two dorsal aortae have now completely coalesced into the single dorsal aorta, and the Wolffian body has reached a far more complete development.

In the course of the fifth day the face begins to assume a less embryonic character, and by the sixth and succeeding days presents distinctive avian characters.

The general changes which take place between the sixth day and the time of hatching do not require to be specified in detail.

Fcetal Membranes.

The Reptilia, Aves and Mammalia are distinguished from the Ichthyopsida by the possession of certain provisional fcetal membranes, known as the amnion and allantois.

As the mode of development of these membranes may be most conveniently studied in the Chick, I have selected this type for their detailed description.

The Amnion. The amnion is a peculiar sack which envelopes and protects the embryo.

At the end of the first day of incubation, when the cleavage of the mesoblast has somewhat advanced, there appears, a little way in front of the semilunar head-fold, a second fold (fig. 102, also fig. 121 C, d/ and fig. 122, Am], running more or less parallel or rather concentric with the first and not unlike it in general appearance, though differing widely from it in nature. This second fold gives rise to the amnion, and is limited entirely to the somatopleure. Rising up as a semilunar fold with its concavity directed towards the embryo (fig. 121 C, of], as it increases in height it


1 86


HKTAI, MEMBRANES.


is gradually drawn backwards over the developing head of the embryo. The fold thus covering the head is in due time accompanied by similar folds of somatopleure, starting at some


A /



-/- pj*


FIG. 121.

Fig. 121 A to N forms a series of purely diagrammatic representations introduced to facilitate the comprehension of the manner in which the body of the embryo is formed, and of the various relations of the yolk-sack, amnion, and allantois.

In all vt is the vitelline membrane, placed, for convenience sake, at some distance from its contents, and represented as persisting in the later stages; in reality it is in direct contact with the blastoderm or yolk, and early ceases to have a separate existence. In all e indicates the embryo proper; pp the general pleuroperitoneal space with its extension between the membranes; of the folds of the amnion; a the amnion proper ; ae or ac the cavity holding the liquor amnii ; al the allantois ; a the alimentary canal ; y or ys the yolk or yolk-sack.

A, which may be considered as a vertical section taken longitudinally along the axis of the embryo, represents the relations of the parts of the egg at the time of the first appearance of the head-fold, seen on the right-hand side of the embryo e. The blastoderm is spreading both behind (to the left hand in the figure), and in front (to right hand) of the head-fold, its limits being indicated by the shading and thickening for a certain distance of the margin of the yolk y. As yet there is no fold on the left side of e corresponding to the head-fold on the right.

B is a vertical transverse section of the same period drawn for convenience sake on a larger scale (it should have been made flatter and less curved). It shews that the blastoderm (vertically shaded) is extending laterally as well as fore and aft, in fact in all directions ; but there are no lateral folds, and therefore no lateral limits to the body of the embryo as distinguished from the blastoderm.




AVES.


I8 7


Incidentally it shews the formation of the medullary groove by the rising up of the lamina; dorsales. Beneath the section of the groove is seen the rudiment of the notochord. On either side a line indicates the cleavage of the mesoblast just commencing.

In C, which represents a vertical longitudinal section of later date, both head-fold (on the right) and tail-fold (on the left) have advanced considerably. The alimentary canal is therefore closed in, both in front and behind, but is in the middle still widely open to the yolk y below. Though the axial parts of the embryo have become thickened by growth, the body-walls are still thin ; in them however is seen the cleavage of the mesoblast, and the divergence of the somatopleure and splanchnopleure. The splanchnopleure both at the head and at the tail is folded in to a greater extent than the somatopleure, and forms the still wide splanchnic stalk. At the end of the stalk, which is as yet short, it bends outwards again and spreads over the surface of the yolk. The somatopleure, folded in less than the splanchnopleure to form the wider somatic stalk, sooner bends round and runs outwards again. At a little distance from both the head and the tail it is raised up into a fold, af, of, that in front of the head being the highest. These are the amniotic folds. Descending from either fold,



1-1



I 88 FCETAL iMEMBRANES.

it speedily joins the splanchnopleure again, and the two, once more united into an uncleft membrane, extend some way downwards over the yolk, the limit or outer margin of the opaque area not being shewn. All the space between the somatopleure and the splanchnopleure is shaded with dots, pp. Close to the body this space may be called the pleuroperitoneal cavity ; but outside the body it runs up into either amniotic fold, and also extends some little way over the yolk.

D represents the tail end at about the same stage on a more enlarged scale, in order to illustrate the position of the allantois al (which was for the sake of simplicity omitted in C), shewn as a bud from the splanchnopleure, stretching downwards into the pleuroperitoneal cavity //. The clotted area representing as before the whole space between the splanchnopleure and the somatopleure, it is evident that a way is open for the allantois to extend from its present position into the space between the two limbs of the amniotic fold of.

E, also a longitudinal section, represents a stage still farther advanced. Both splanchnic and somatic stalks are much narrowed, especially the former, the cavity of the alimentary canal being now connected with the cavity of the yolk by a mere canal. The folds of the amnion are spreading over the top of the embryo and nearly meet. Each fold consists of two walls or limbs, the space between which (dotted) is as before merely a part of the space between the somatopleure and splanchnopleure. Between these arched amniotic folds and the body of the embryo is a space not as yet entirely closed in.

F represents on a different scale a transverse section of E taken through the middle of the splanchnic stalk. The dark ring in the body of the embryo shews the position of the neural canal, below which is a black spot, marking the notochord. On either side of the notochord the divergence of somatopleure and splanchnopleure is obvious. The splanchnopleure, more or less thickened, is somewhat bent in towards the middle line, but the two sides do not unite, the alimentary canal being as yet open below at this spot ; after converging somewhat they diverge again and run outwards over the yolk. The somatopleure, folded in to some extent to form the body-walls, soon bends outwards again, and is almost immediately raised up into the lateral folds of the amnion of. The continuity of the pleuroperitoneal cavity, within the body, with the interior of the amniotic fold, outside the body, is evident; both cavities are dotted.

G, which corresponds to D at a later stage, is introduced to shew the manner in which the allantois, now a considerable hollow body ; whose cavity is continuous with that of the alimentary canal, becomes directed towards the amniotic fold.

In H a longitudinal, and I a transverse section of later date, great changes have taken place. The several folds of the amnion have met and coalesced above the body of the embryo. The inner limbs of the several folds have united into a single membrane (a), which encloses a space (ae or ac] round the embryo. This membrane a is the amnion proper, and the cavity within it, i.e. between it and the embryo, is the cavity of the amnion containing the liquor amnii. The allantois is omitted for the sake of simplicity.

It will be seen that the amnion a now forms in every direction the termination of the somatopleure; the peripheral portions of the somatopleure, the united outer or descending limbs of the folds af'm C, D, F, G having been cut adrift, and now forming an independent continuous membrane, the serous membrane, immediately underneath the vitelline membrane.

In I the splanchnopleure is seen converging to complete the closure of the alimentary canal a' even at the stalk (elsewhere the canal has of course long been closed



AVES.


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in), and then spreading outwards as before over the yolk. The point at which it unites with the somatopleure, marking the extreme limit of the cleavage of the mesoblast, is now much nearer the lower pole of the diminished yolk.

As a result of these several changes, a great increase in the dotted space has taken place. It is now possible to pass from the actual peritoneal cavity within the body, on the one hand round a great portion of the circumference of the yolk, and on the other hand above the amnion a, in the space between it and the serous envelope.

Into this space the allantois is seen spreading in K at al.

In L the splanchnopleure has completely invested the yolk-sack, but at the lower pole of the yolk is still continuous with that peripheral remnant of the somatopleure now called the serous membrane. In other words, cleavage of the mesoblast has been carried all round the yolk (ys) except at the very lower pole.



In M the cleavage has been carried through the pole itself; the peripheral portion of the splanchnopleure forms a complete investment of the yolk quite unconnected with the peripheral portion of the somatopleure, which now exists as a continuous membrane lining the interior of the shell. The yolk-sack (ys) is therefore quite loose in the pleuroperitoneal cavity, being connected only with the alimentary canal (a 1 ) by a solid pedicle.

Lastly, in N the yolk-sack (ys) is shewn being withdrawn into the cavity of the body of the embryo. The allantois is as before, for the sake of simplicity, omitted ; its pedicle would of course lie by the side of ys in the somatic stalk marked by the usual dotted shading.

It may be repeated that the above are diagrams, the various spaces being shewn distended, whereas in many of them in the actual egg the walls have collapsed, and are in near juxtaposition.

little distance behind the tail, and at some little distance from the side (fig. 121 C, D, E, F, and 116, am}. In this way the


FCETAL MEMBRANES.


embryo becomes surrounded by a series of folds of thin somatopleure, which form a continuous wall all round it. All are drawn gradually over the body of the embryo, and at last meet and completely coalesce (fig. 121, H, I, and 117, Am), all traces of their junction being removed. Beneath these united folds there is therefore a cavity, within which the embryo lies (fig. 121 H, ae). This cavity is the cavity of the amnion.

Each fold is necessarily formed of two limbs, both limbs consisting of epiblast and a very thin layer of mesoblast ; but in one limb the epiblast looks towards the embryo, while in the other it looks away from it. The space between the two limbs of the fold, as can easily be seen in fig. 121, is really part of the space between the somatopleure and splanchnopleure ; it is therefore continuous with the general space, part of which afterwards becomes the pleuroperitoneal cavity of the body, shaded with dots in the figure and marked (//) ; so that it is possible to pass from the cavity between the two limbs of the amniotic folds into the cavity which surrounds the alimentary canal. When the several folds meet and coalesce together above the embryo, they unite in such a way that all their inner limbs unite to form a continuous inner membrane or sack, and all


JVC.


f.So



FIG. 112. DIAGRAMMATIC LONGITUDINAL SECTION THROUGH THE AXIS OF AN

EMBRYO.

The section is supposed to be made at a time when the head-fold has commenced but the tail-fold has not yet appeared.

F.So. fold of the somatopleure. F.Sp. fold of the splanchnopleure; D. fore-gut.

//. pleuroperitoneal cavity between somatopleure and splanchnopleure ; Am. commencing (head) fold of the amnion. For remaining reference letters vide p. 167.

their outer limbs a similarly continuous outer membrane or sack. The inner membrane thus built up forms a completely closed sack round the body of the embryo, and is called the amniotic




AVES. Ipl

sack, or amnion proper (fig. 121, H, I, &c., a), and the fluid which it afterwards contains is called the amniotic fluid, or liquor amnii. The space between the inner and outer sack is, from the mode of its formation, simply a part of the general cavity found everywhere between somatopleure and splanchnopleure. The outer sack over the embryo lies close under the vitelline membrane, and the cavity between it and the true amnion is gradually extended over the whole yolk-sack.'

The actual manner in which the amniotic folds meet is somewhat peculiar (His and Kolliker). The head-fold of the amnion is the earliest formed, and completely covers over the head before the end of the second day. The side and tail folds are later in developing. The side-folds finally meet in the dorsal line, and their coalescence proceeds backwards from the head-fold in a linear direction, till there is only a small opening left over the tail. This also becomes closed early on the third day.

The allantois 1 is essentially a diverticulum of the alimentary tract into which it opens immediately in front of the anus. Its walls are formed of splanchnic mesoblast with blood-vessels, within which is a lining of hypoblast. It becomes a conspicuous object on the third day of incubation, but its first development takes place at an earlier period, and is intimately connected with the formation of the posterior section of the gut.

At the time of the folding in of the hinder end of the mesenteron the splitting of the mesoblast into somatopleure and splanchnopleure has extended up to the border of the hinder division of the primitive streak. As has been already mentioned, the ventral wall of the postanal section of the alimentary tract is formed by the primitive streak. Immediately in front of this is the involution which forms the proctodaeum ; while the wall of the hindgut in front of the anus owes its origin to a folding in of the splanchnopleure.

The allantois first appears as a protuberance of the splanchnopleure just in front of the anus. This protuberance arises, however, before the splanchnopleure has begun to be tucked in so as

1 For details on the development of the allantois the reader is referred to the works of Kolliker (No. 135), Gasser (No. 127), and for a peculiar view on the subject Kupffer (No. 136). In addition to these works he may refer to Dobrynin " Ueber die erste Anlage der Allantois." Sitz. der k. Akad. Wien, Bd. 64, 1871. E. Gasser, Beitrdge zur Entwicklungsgeschichte d. Allantois, etc.


192


ALLANTOIS.


to form the ventral wall of the hindgut ; and it then forms a diverticulum (fig. 123 A, All} the open end of which is directed forward, while its blind end points somewhat upwards and towards the peritoneal space behind the embryo.

As the hindgut becomes folded in the allantois shifts its position, and forms (figs. 123 B and 124) a rather wide vesicle

A.


S.O



FlG. 123. TWO LONGITUDINAL SECTIONS OF THE TAIL-END OF AN EMBRYO

CHICK TO SHEW THE ORIGIN OF THE ALLANTOIS. A AT THE BEGINNING OF

THE THIRD DAY ; B AT THE MIDDLE OF THE THIRD DAY. (After Dobrynin.)

/. the tail; m. the mesoblast of the body, about to form the mesoblastic somites; x'. the roof of x" . the neural canal ; Dd. the hind end of the hindgut ; So. somatopleure; Spl. splanchnopleure ; u. the mesoblast of the splanchnopleure carrying the vessels of the yolk-sack ; pp. pleuroperitoneal cavity ; Df. the epithelium lining the pleuroperitoneal cavity; All. the commencing allantois; r.'. projection formed by anterior and posterior divisions of the primitive streak; y. hypoblast which will form the ventral wall of the hindgut ; v. anal imagination ; G. cloaca.

lying immediately below the hind end of the digestive canal, with which it communicates freely by a still considerable opening; its blind end projects into the pleuroperitoneal cavity below.

Still later the allantois grows forward, and becomes a large spherical vesicle,still however remaining connected with the cloaca by a narrow canal which forms its neck or stalk (fig. 1 2 1 G, al}. From the first the allantois lies in the pleuroperitoneal cavity. In this cavity it grows forwards till it reaches the front limit of the hindgut, where the splanchnopleure turns back to enclose the yolk-sack. It does not during the third day project beyond this point ; but on the fourth day begins to pass out beyond the body of the chick, along the as yet wide space between the


AVES. 193

splanchnic and somatic stalks of the embryo, on its way to the space between the external and internal folds of the amnion, which it will be remembered is directly continuous with the pleuroperitoneal cavity (fig. 121 K). In this space it eventually spreads out over the whole body of the chick. On the first half of the fourth day the vesicle is still very small, and its growth is not very rapid. Its mesoblast wall still remains very thick. In



FIG. 124. DIAGRAMMATIC LONGITUDINAL SECTION THROUGH THE POSTERIOR END OF AN EMBRYO BlRD AT THE TIME OF THE FORMATION OF THE ALLANTOIS.

ep. epiblast; Sp.c. spinal canal; ch. notochord; n.e. neurenteric canal ; hy. hypoblast ; p.a.g. post-anal gut ; pr. remains of primitive streak folded in on the ventral side; al. allantois; me. mesoblast; an. point where anus will be formed ', p.c. perivisceral cavity ; am. amnion; so. somatopleure; sp. splanchnopleure.

the latter half of the day its growth becomes very rapid, and it forms a very conspicuous object in a chick of that date (fig. 118, A I}. At the same time its blood-vessels become important. It receives its supply of blood from two branches of the iliac arteries known as the allantoic arteries 1 , and the blood is brought back from it by two allantoic veins which run along in the body walls (fig. 119) and after uniting into a single trunk fall into the vitelline vein close behind the liver.

Before dealing with the later history of the fcetal membranes, it will be convenient to complete the history of the yolk-sack.

Yolk-Sack. The origin of the area opaca has already been described. It rapidly extends over the yolk underneath the vitelline membrane ; and is composed of epiblast and of the

1 I propose to call these arteries and the corresponding veins the allantoic arteries and veins, instead of using the confusing term ' umbilical.'

B. III. 13


194


YOLK-SACK.


hypoblast of the germinal wall continuous with that of the area pellucida, which on the fourth day takes the form of a more or less complete layer of columnar cells 1 . Between the epiblast and hypoblast there is a layer of mesoblast, which does not extend as far as the two other layers. The yolk is completely surrounded by the seventh day.

Towards the end of the first day blood-vessels begin to be


CaV.



L.O/.A


L.of


FIG. 125. DIAGRAM OF THE CIRCULATION OF THE YOLK-SACK AT THE END OF

THE THIRD DAY OF INCUBATION.

H. heart; A A. the second, third and fourth aortic arches; the first has become obliterated in its median portion, but is continued at its proximal end as the external carotid, and at its distal end as the internal carotid; AO. dorsal aorta; L.Of.A. left vitelline artery; R.Of.A. right vitelline artery; 5 1 . T. sinus terminalis; L.Of. left vitelline vein; R.Of. right vitelline vein; S.V. sinus venosus; D. C. ductus Cuvieri ; S.Ca.V. superior cardinal vein; V.Ca. inferior cardinal vein. The veins are marked in outline and the arteries are black. The whole blastoderm has been removed from the egg and is supposed to be viewed from below. Hence the left is seen on the light, and vice vcrsA.

1 Further investigations are required as to the character of this layer.



AVES. 195

developed in the inner part of the mesoblast of the area opaca. Their development is completed on the second day ; and the region through which they extend is known as the area vasculosa. The area vasculosa also grows round the yolk, and completely encloses it not long after the area opaca. The part of the blastoderm which thus encloses the yolk forms the yolksack. The splitting of the mesoblast gradually extends to the mesoblast of the yolk-sack, and eventually the somatopleure of the sack, which is continuous, it will be remembered, with the outer limb of the amnion, separates completely from the splanchnopleure ; and between the two the allantois inserts itself. These features are represented in fig. 121 E, K, and L.

The circulation of the yolk-sack is most important during the third day of incubation. The arrangement of the vessels during that day is shewn in fig. 125.

The blood leaving the body of the embryo by the vitelline arteries (fig. 125, R.Of.A, L.Of.A], which are branches of the dorsal aortae, is carried to the small vessels and capillaries of the vascular area, a small portion only being appropriated by the pellucid area.

From the vascular area part of the blood returns directly to the sinus venosus by the main lateral trunks of the vitelline veins (R.Of., L.Of), and so to the heart. During the second day these venous trunks join the body of the embryo considerably in front of, that is nearer, the head than the corresponding arterial ones. Towards the end of the third day, owing to the continued lengthening of the heart, the veins and arteries run not only parallel to each other, but almost in the same line, the points at which they respectively join and leave the body being nearly at the same distance from the head.

The rest of the blood brought by the vitelline arteries finds its way into the lateral portions of a venous trunk bounding the vascular area, which is known as the sinus terminalis, 5. T., and there divides on each side into two streams. Of these, the two which, one on either side, flow backward, meet at a point about opposite to the tail of the embryo, and are conveyed along a distinct vein which, running straight forward parallel to the axis of the embryo, empties itself into the left vitelline vein. The

132


196 FCETAL MEMBRANES.


two forward streams reaching a gap in the front part of the sinus terminalis fall into either one, or in some cases two veins, which run straight backwards parallel to the axis of the embryo, and so reach the roots of the heart. When one such vein only is present it joins the left vitelline trunk ; where there are two they join the left and right vitelline trunks respectively. The left vein is always considerably larger than the right ; and the latter when present rapidly gets smaller and speedily disappears. After the third day, although the vascular area goes on increasing in size until it finally all but encompasses the yolk, the prominence of the sinus terminalis becomes less and less.

The foetal membranes and the yolk-sack may conveniently be treated of together in the description of their later changes and final fate.

On the sixth and seventh days they exhibit changes of great importance.

The amnion, at its complete closure on the fourth day, very closely invested the body of the chick : the true cavity of the amnion was then therefore very small. On the fifth day fluid begins to collect in the cavity, and raises the membrane of the amnion to some distance from the embryo. The cavity becomes still larger by the sixth day, and on the seventh day is of very considerable dimensions, the fluid increasing with it. On the sixth day Von Baer observed movements of the embryo, chiefly of the limbs ; he attributes them to the stimulation of the cold air on opening the egg. By the seventh day very obvious movements begin to appear in the amnion itself; slow vermicular contractions creeping rhythmically over it. The amnion in fact begins to pulsate slowly and rhythmically, and by its pulsation the embryo is rocked to and fro in the egg. This pulsation is probably due to the contraction of involuntary muscular fibres, which seem to be present in the attenuated portion of the mesoblast, forming part of the amniotic fold. Similar movements are also seen in the allantois at a considerably later period.

The growth of the allantois has been very rapid, and it forms a flattened bag, covering the right side of the embryo, and rapidly spreading out in all directions between the primitive folds of the



AVES. 197

amnion, that is, between the amnion proper and the false amnion or serous envelope. It is filled with fluid, so that in spite of its flattened form its opposite walls are distinctly separated from each other.

The vascular area has become still further extended than on the fifth day, but with a corresponding loss in the definite character of its blood-vessels. The sinus terminalis has indeed by the end of the seventh day lost all its previous distinctness ; and the vessels which brought back the blood from it to the heart are no longer to be seen.

Both the vitelline arteries and veins now pass to and from the body of the chick as single trunks, assuming more and more the appearance of being merely branches of the mesenteric vessels.

The yolk is still more fluid than on the previous day, and its bulk has (according to von Baer) increased. This can only be due to its absorbing the white of the egg, which indeed is diminishing rapidly.

During the eighth, ninth, and tenth days, the amnion does not undergo any very important changes. Its cavity is still filled with fluid, and on the eighth day its pulsations are at their height, henceforward diminishing in intensity.

The splitting of the mesoblast has now extended to the outer limit of the vascular area, i.e. over about three-quarters of the yolk-sack. The somatopleure at this point is continuous (as can be easily seen by reference to fig. 121) with the original outer fold of the amnion. It thus comes about that the further splitting of the mesoblast merely enlarges the cavity in which the allantois lies. The growth of this organ keeps pace with that of the cavity in which it is placed. Spread out over the .greater part of the yolk-sack as a flattened bag filled with fluid, it now serves as the chief organ of respiration. It is indeed very vascular and a marked difference may be observed between the colour of the blood in the outgoing and the returning vessels.

The yolk now begins to diminish rapidly in bulk. The yolksack becomes flaccid, and on the eleventh day is thrown into a series of internal folds, abundantly supplied by large venous trunks. By this means the surface of absorption is largely increased, and the yolk is more and more rapidly taken up by the


198 FCETAL MEMBRANES.

blood-vessels, and in a partially assimilated condition transferred to the body of the embryo 1 .

By the eleventh day the abdominal parietes, though still much looser and less firm than the walls of the chest, may be said to be definitely established ; and the loops of intestine, which have hitherto been hanging down into the somatic stalk, are henceforward confined within the cavity of the abdomen. The body of the embryo is therefore completed ; but it still remains connected with its various appendages by a narrow somatic umbilicus, in which run the stalk of the allantois and the solid cord suspending the yolk-sack.

The cleavage of the mesoblast is still progressing, and the yolk is completely invested by a splanchnopleural sack.

The allantois meanwhile spreads out rapidly, and lies over the embryo close under the shell, being separated from the shell membrane by nothing more than the attenuated serous envelope, formed out of the outer primitive fold of the amnion and the remains of the vitelline membrane. With this membrane the allantois partially coalesces, and in opening an egg at the later stages of incubation, unless care be taken, the allantois is in danger of being torn in the removal of the shell-membrane. As the allantois increases in size and importance, the allantoic vessels are correspondingly developed.

On about the sixteenth day, the white having entirely disappeared, the cleavage of the mesoblast is carried right over the pole of the yolk opposite the embryo, and is thus completed (fig. 121). The yolk-sack now, like the allantois which closely wraps it all round, lies loose in a space bounded outside the body by the serous membrane, and continuous with the pleuroperitoneal cavity of the body of the embryo. Deposits of urates now become abundant in the allantoic fluid.

The loose and flaccid walls of the abdomen enclose a space which the empty intestines are far from filling, and on the nineteenth day the yolk-sack, diminished greatly in bulk but still of some considerable size, is withdrawn through the somatic stalk into the abdominal cavity, which it largely distends. Outside the embryo there now remains nothing but the highly vascular

1 For details on this subject vide A. Courty, "Structure des Appendices Vitellins chez le Poulet." An. Set. Nat. Ser. III. Vol. IX. 1848.



AVES. 199

allantois and the bloodless serous membrane and amnion. The amnion, whose fluid during the later days of incubation rapidly diminishes, is continuous at the umbilicus with the body-walls of the embryo. The serous membrane (or outer primitive amniotic fold) is, by the completion of the cleavage of the mesoblast and the withdrawal of the yolk-sack, entirely separated from the embryo. The cavity of the allantois, by means of its stalk passing through the umbilicus, is of course continuous with the cloaca.

When the chick is about to be hatched it thrusts its beak through the egg-membranes and begins to breathe the air contained in the air chamber. Thereupon the pulmonary circulation becomes functionally active, and at the same time blood ceases to flow through the allantoic arteries. The allantois shrivels up, the umbilicus becomes completely closed, and the chick, piercing the shell at the broad end of the egg with repeated blows of its beak, casts off the dried remains of allantois, amnion and serous membrane, and steps out into the world.

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(117) K. E. vonBaer. " Ueb. Enhvicklungsgeschichte d. Thiere." Konigsberg, 18281837.

(118) F. M. Balfour. "The development and growth of the layers of the Blastoderm," and "On the disappearance of the Primitive Groove in the Embryo Chick." Quart. J. of Micros. Science, Vol. XIII. 1873.

(119) M. Braun. " Die Entwicklung d. Wellenpapagei's." Part I. Arbeit, d. zool.-zoot. Instit. Wiirzburg. Vol. v. 1879.

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(121) J. Disse. " Die Entwicklung des mittleren Keimblattes im Hiihnerei." Archivfiir mikr. Anat., Vol. xv. 1878.

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(123) Fr. Durante. "Sulla struttura della macula germinativa delle uova di Gallina." Ricerche nel Laboratorio di Anatomia della R. Universita di Roma.

(124) E. Dursy. Der Primitivstreif des Hilhnchens. 1867.

(125) M. Duval. "Etude sur la ligne primitive de 1'embryon de Poulet." Annales des Sciences Natureiles, Vol. vil. 1879.

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(134) E. Klein. "Das mittlere Keimblatt in seiner Bezieh. z. Entwick. d. ers. Blutgefasse und Blutkorp. im Hiihnerembryo." Sitzungsber. Wien. Akad., Vol. LXIII. 1871.

(135) A. Kb Hiker. Entwicklungsgeschichte d. Menschen u. d. hoheren Thiere. Leipzig, 1879.

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(137) C. Kupffer and B. Benecke. " Photogramme z. Ontogenie d. Vogel." Nov. Act. d. k. Leop.-Carol.-Deutschen Akad. d. Natiirforscher, Vol. XLI. 1879.

(138) J. Oellacher. "Untersuchungen iiber die Furchung u. Blatterbildung im Hiihnerei. " Strieker's Studien. 1870.

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(145) S. L. Schenk. "Beitrage z. Lehre v. d. Organanlage im motorischen Keimblatt." Sitz. Wien. Akad., Vol. LVII. 1860.

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(148) S. Strieker. " Mittheil. iib. d. selbststandigen Bewegungen embryonaler Zellen." Sitz. Wien. Akad., Vol. XLIX. 1864.

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(150) H. Virchow. Ueber d. Epithel d. Dottersackes im Hiihnerei. Inaug. Diss. Berlin, 1875.

(151) W. Waldeyer. "Ueber die Keimblatter und den Primitivstreifen bei der Entwicklung des Huhnerembryo." Zeitschrift fiir rationelle Medicin. 1869.

(152) C.F.Wolff. Theoria generationis. Hake, 1759.

(153) C. F. Wolff. Ueb. d. Bildung d. Darmcanals im bebriiteten Hiinchen. Halle, 1812.