The Works of Francis Balfour 3-3

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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
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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:

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Pages where the terms "Historic" (textbooks, papers, people, recommendations) 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, interpretations and recommendations 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)


THE impregnation of the ovum is effected in the oviduct. In most forms the whole of the subsequent development, till the time when the embryo is capable of leading a free existence, takes place in the uterus ; but in other cases the egg becomes enveloped, during its passage down the oviduct, first in a layer of fluid albumen, and finally in a dense horny layer, which usually takes the form of a quadrilateral capsule with characters varying according to the species. After the formation of this capsule the egg is laid, and the whole of the development, with the exception of the very first stages, takes place externally.

In many of the viviparous forms (Mustelus, Galeus, Carcharias, Sphyrna) the egg is enclosed, during the early stages of development at any rate, in a very delicate shell homologous with that of the oviparous forms ; there is usually also a scanty albuminous layer. Both of these are stated by Gerbe (No. 42) to be absent in Squalus spinax.

The following are examples of viviparous genera : Hexanchus, Notidanus, Acanthias, Scymnus, Galeus, Squalus, Mustelus, Carcharias, Sphyrna, Squatina, Torpedo ; and the following of oviparous genera : Scyllium, Pristiurus, Cestracion, Raja 1 .

The ovum at the time of impregnation has the form of a large spherical mass, similar to the yolk of a bird's egg, but without a vitelline membrane 2 . The greater part of it is formed of peculiar oval spherules of food-yolk, held together by a protoplasmic network. The protoplasm is especially concentrated in a small lens-shaped area, known as the germinal disc, which is not separated by a sharp line from the remainder of

1 For further details, vide Miiller (No. 48). - Vide Vol. II., p. 62.


the ovum. Yolk spherules are present in this disc as elsewhere, but are much smaller and of a different character. The segmentation has the normal meroblastic character (fig. 15) and is confined to the germinal disc. Before it commences the germinal disc exhibits amoeboid movements. During the segmentation nuclei make their appearance spontaneously (?) in the yolk adjoining the germinal- disc (fig. 15, nx'}, and around them portions of the yolk with its protoplasmic network become segmented off. Cells are thus formed which are added to those resulting from the segmentation proper. Even after the segmentation numerous nuclei are present in the granular matter below the blastoderm (fig. 16 A, n')\ and around these cells

FIG. 15.


. nucleus ; nx. nucleus modified prior to division ; nx'. modified nucleus in the yolk ; f. furrow appearing in the yolk adjacent to the germinal disc.

are being continually formed, which enter the blastoderm, and are more especially destined to give rise to the hypoblast. The special destination of many of these cells is spoken of in detail below.

At the close of segmentation the blastoderm forms a somewhat lens-shaped disc, thicker at one end than at the other ; the thicker end being the embryonic end. It is divided into two strata an upper one, the epiblast formed of a single row of columnar cells ; and a lower one, the primitive hypoblast, consisting of the remaining cells of the blastoderm, and forming a mass several strata deep. These cells will be spoken of as the


lower layer cells, to distinguish them from the true hypoblast which is one of their products.

A cavity very soon appears in the lower layer cells, near the non-embryonic end of the blastoderm, but the cells afterwards


FlG. 16. TWO LONGITUDINAL SECTIONS OF THE BLASTODERM OF A PfUSTIURUS EMBRYO DURING STAGES PRIOR TO THE FORMATION OF THE MEDULLARY GROOVE. ep. epiblast ; //. lower layer cells or primitive hypoblast ; m. mesoblast ; hy. hypoblast ; sc. segmentation cavity ; es. embryo swelling ; '. nuclei of yolk ; er. embryonic rim. c. lower layer cells at the non-embryonic end of the blastoderm.

disappear from the floor of this cavity, which then lies between the yolk and the lower layer cells (fig. 16 A, sc}. This cavity is the segmentation cavity equivalent to that present in Amphioxus, Amphibia, etc. The chief peculiarity about it is the relatively late period at which it makes its appearance, and the fact that its roof is formed both by the epiblast and by the


EMBRYO OF THE SAME AGE AS FIG. 28 B. ep. epiblast ; er. embryonic rim ; m. mesoblast ; al. mesenteron.

lower layer cells. Owing to the large size of the segmentation cavity the blastoderm forms a thin layer above the cavity and a thickened ridge round its edge.

The epiblast in the next stage is inflected for a small arc at the embryonic end of the blastoderm, where it becomes continuous with the lower layer cells ; at the same time some of the lower layer cells of the embryonic end of the blastoderm assume



a columnar form, and constitute the true hypoblast. The portion of the blastoderm, where epiblast and hypoblast are continuous, forms a projecting structure which will be called the embryonic rim (fig. 16 B, er).

This rim is a very important structure, since it represents the dorsal portion of the lip of the blastopore of Amphioxus. The space between it and the yolk represents the commencing mesenteron, of which the hypoblast on the under side of the lip is the dorsal wall. The ventral wall of the mesenteron is at first formed solely of yolk held together by a protoplasmic network with numerous nuclei. The cavity under the lip becomes rapidly larger (fig. 17, al}, owing to the continuous conversion of lower layer cells into columnar hypoblast along an axial line passing from the middle of the embryonic rim towards the centre of the blastoderm. The continuous differentiation of the hypoblast towards the centre of the blastoderm corresponds with the invagination in Amphioxus. During the formation of the embryonic rim the blastoderm grows considerably larger, but, with the exception of the formation of the embryonic rim, retains its primitive constitution.

The segmentation cavity undergoes however important changes. There is formed below it a floor of lower layer cells, derived partly from an ingrowth from the two sides, but mainly from the formation of cells around the nuclei of the yolk (fig. 1 6). Shortly after the floor of cells has appeared, the whole segmentation cavity becomes obliterated (fig. 17).

The disappearance of the segmentation cavity corresponds in point of time with the formation of the hypoblast by the pseudo-invagination above described ; and is probably due to this pseudo-invagination, in the same way that the disappearance of the segmentation cavity in Amphioxus is due to the true invagination of the hypoblast.

When the embryonic rim first appears there are no external indications of the embryo as distinguished from the blastoderm, but when it has attained to some importance the position of the embryo becomes marked out by the appearance of a shield-like area extending inwards from the edge of the embryonic rim, and formed of two folds with a groove between them (fig. 28 B, mg), which is deepest at the edge of the blastoderm, and



shallows out as it extends inwards. This groove is the medullary groove ; and its termination at the edge of the blastoderm is placed at the hind end of the embryo.

At about the time of its appearance the mesoblast becomes first definitely established.

At the edge of the embryonic rim the epiblast and lower layer cells are continuous. Immediately underneath the medullary groove, as is best seen in transverse section (fig. 18), the whole of the lower layer cells become converted into hypoblast, and along this line the columnar hypoblast is in contact with the epiblast above. At the sides however this is not the case ; but at the junction of the epiblast and lower layer cells the latter remain undifferentiated. A short way from the edge the lower layer cells become divided into two distinct layers, a lower one continuous with the hypoblast in the middle line, and an upper one between this and the epiblast (fig. 18 B). The upper layer is the commencement of the mesoblast (m). The mesoblast thus arises as two independent lateral


plates, one on each side 01 AN EMBRYO OF THE SAME AGE AS FIG. 17.

A. Anterior section.

B. Posterior section.

mg. medullary groove ; ep. epiblast ; hy. hypoblast ; cells formed round the nuclei of the yolk which have entered the hypoblast ; 111. mesoblast.

The sections shew the origin of the mesoblast.

the medullary groove, which are continuous behind with the undifferentiated lower layer cells at the edge of the embryonic rim. The mesoblast plates are at first very short, and do not extend to the front end of the embryo. They soon however grow forwards as two lateral ridges, attached to the hypoblast, one on each side of the medullary groove (fig. 18 A, ;#). These ridges become separate from the hypoblast, and form two plates, thinner in front than behind ; but still continuous at the edge of the blastoderm with the undifferentiated cells of the lip of the blastopore, and laterally with the lower layer



cells of the non-embryonic part of the blastoderm. It results from the above mode of development of the mesoblast, that it may be described as arising in the form of a pair of solid outgrowths of the wall of the alimentary tract ; which differ from the mesoblastic outgrowths of the wall of the archenteron in Amphioxus in not containing a prolongation of the alimentary cavity.

A general idea of the structure of the blastoderm at this stage may be gathered from the diagram representing a longi



Epiblast without shading. Mesoblast black with clear outlines to the cells. Lower layer cells and hypoblast with simple shading.

ep. epiblast ; m. mesoblast ; al. alimentary cavity ; sg. segmentation cavity ; nc. neural canal ; ch. notochord ; x. point where epiblast and hypoblast become continuous at the posterior end of the embryo ; . nuclei of yolk.

A. Section of young blastoderm, with segmentation cavity enclosed in the lower layer cells.

B. Older blastoderm with embryo in which hypoblast and mesoblast are distinctly formed, and in which the alimentary slit has appeared. The segmentation cavity is still represented as being present, though by this stage it has in reality disappeared.

C. Older blastoderm with embryo in which the neural canal has become formed, and is continuous posteriorly with the alimentary canal. The notochord, though shaded like mesoblast, belongs properly to the hypoblast.

4 6


tudinal section through the embryo (fig. 19 B). In this figure the epiblast is represented in white and is seen to be continuous at the lip of the blastopore (x) with the shaded hypoblast. Between the epiblast and hypoblast is seen one of the lateral plates of mesoblast, represented by black cells with clear outlines. The non-embryonic lower layer cells of the blastoderm are represented in the same manner as the mesoblast of the body. The alimentary cavity is shewn at al, and below it is seen the yolk with nuclei (;/). The segmentation cavity is represented as still persisting, though by this stage it would have disappeared.



A. Section through the cephalic plate.

B. Section through the posterior part of the cephalic plate.

C. Section through the trunk.

ch. notochord ; mg. medullary groove ; al. alimentary tract ; lp. lateral plate of mesoblast ; //. body cavity.

As to the growth of the blastoderm it may be noted that it has greatly extended itself over the yolk. Its edge in the meantime forms a marked ridge, which is due not so much to a thickening as to an arching of the epiblast. This ridge is continuous with the embryonic rim, which gradually concentrates itself into two prominences, one on each side of the tail of the embryo, mainly formed of masses of undifferentiated lower layer cells. These prominences will be called the caudal swellings.


By this stage the three layers of the body, the epiblast, mesoblast, and hypoblast, have become definitely established. The further history of these layers may now be briefly traced.

Epiblast. While the greater part of the epiblast becomes converted into the external epidermis, from which involutions give rise to the olfactory and auditory pits, the lens of the eye, the mouth cavity, and anus, the part of it lining the medullary groove becomes converted into the central nervous system and optic cup. The medullary groove is at first continued to the front end of the medullary plate ; but the anterior part of this plate soon enlarges, and the whole plate assumes a spatula form (fig. 28 C, h, and fig. 20 A and B). The enlarged part becomes converted into the brain, and may be called the cephalic plate.

The posterior part of the canal deepens much more rapidly than the rest (fig. 20 C), and the medullary folds unite dorsally and convert the posterior end of the medullary groove into a closed canal, while the groove is still widely open elsewhere. The medullary canal does not end blindly behind, but simply forms a tube not closed at either extremity. The importance of this fact will appear later.

Shortly after the medullary folds have met behind the whole canal becomes closed in. This occurs in the usual way by the junction and coalescence of the medullary folds. In the course of the closing of the medullary groove the edges of the cephalic plate, which have at first a ventral curvature, become bent up in the normal manner, and enclose the dilated cephalic portion of the medullary canal. The closing of the medullary canal takes place earlier in the head and neck than in the back.

An anterior pore at the front end of the canal, like that in Amphioxus and the Ascidians, is not found. The further differentiation of the central nervous system is described in a special chapter: it may however here be stated that the walls of the medullary canal give rise not only to the central nervous system but to the peripheral also.

Mesoblast. The mesoblast was left as two lateral plates continuous behind with the undifferentiated cells of the caudal swellings.

The cells composing them become arranged in two layers (fig. 20 C, lp\ a splanchnic layer adjoining the hypoblast, and a

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somatic layer adjoining the epiblast. Between these two layers there is soon developed in the region of the head a well-marked cavity (fig. 20 A, //) which is subsequently continued into the region of the trunk, and forms the primitive body cavity, equivalent to the cavity originating as an outgrowth of the archenteron in Amphioxus. The body cavities of the two sides are at first quite independent.

Coincidentally with the appearance of differentiation into somatic and splanchnic layers the mesoblast plates become in the region of the trunk partially split by a series of transverse lines of division into mesoblastic somites. Only the dorsal parts of the plates become split in this way, their ventral parts remaining quite intact. As a result of this each plate becomes divided into a dorsal portion adjoining the medullary canal, which is divided into somites, and may be called the vertebral plate, and a ventral portion not so divided, which may be called the lateral plate. These two parts are at this stage quite continuous with each other ; and the body cavity originally extends uninterruptedly to the summit of the vertebral plates (fig. 21).

The next change results in the complete separation of the vertebral portion of the plate from the lateral



nc. neural canal ; pr. posterior root of spinal nerve ; x. subnotochordal rod ; ao. aorta ; sc. somatic mesoblast ; sp. splanchnic mesoblast ; mp. muscle-plate ; mp' . portion of muscle -plate converted into muscle ; Vv. portion of the vertebral plate which will give rise to the vertebral bodies ; al. alimentary tract.


The section is taken at the level of the notochord, and shews the separation of the cells to form the vertebral bodies from the muscle-plates.

ch. notochord ; ep. epiblast ; Vr. rudiment of vertebral body ; mp. muscle-plate ; mp' . portion of muscle-plate already differentiated into longitudinal muscles.


portion ; thereby the upper segmented part of the body cavity becomes isolated, and separated from the lower and unsegmented part. As a consequence of this change the vertebral plate comes to consist of a series of rectangular bodies, the mesoblastic somites, each composed of two layers, a somatic and a splanchnic, between which is the cavity originally continuous with the body cavity (fig. 23, mp}. The splanchnic layer of the plates buds off cells to form the rudiments of the vertebral bodies which are at first segmented in the same planes as the mesoblastic somites (fig. 22, Vr\ The plates themselves remain as the muscle-plates (mp}, and give rise to the whole of the voluntary muscular system of the body. Between the vertebral and lateral plates there is left a connecting isthmus, with a narrow prolongation of the body cavity (fig. 23 B, st], which gives rise (as described in a special chapter) to the segmental tubes and to other parts of the excretory system.

In the meantime the lateral plates of the two sides unite ventrally throughout the intestinal and cardiac regions of the body, and the two primitively isolated cavities contained in them coalesce. In the tail however the plates do not unite ventrally till somewhat later, and their contained cavities remain distinct till eventually obliterated.

At first the pericardial cavity is quite continuous with the body cavity ; but it eventually becomes separated from the body cavity by the attachment of the liver to the abdominal wall, and by a horizontal septum in which run the two ductus Cuvieri (fig. 23 A, sv}. Two perforations in this septum (fig. 23 A) leave the cavities in permanent communication.

The parts derived from the two layers of the mesoblast (not including special organs or the vascular system) are as follows :

From the somatic layer are formed

(1) A considerable part of the voluntary muscular

system of the body.

(2) The dermis.

(3) A large part of the inter-muscular connective tissue.

(4) Part of the peritoneal epithelium. From the splanchnic layer are formed

(i) A great part of the voluntary muscular system.

B. III. 4


(2) Part of the inter-muscular connective tissue.

(3) The axial skeleton and surrounding connective


(4) The muscular and connective-tissue wall of the

alimentary tract.

(5) Part of the peritoneal epithelium.

In the region of the head the mesoblast does not at first become divided into somites ; but on the formation of the gill A. B.





Figure A shews the separation of the body cavity from the pericardial cavity by a horizontal septum in which runs the ductus Cuvieri ; on the left side is seen the narrow passage which remains connecting the two cavities. Fig. B through a posterior part of the trunk shews the origin of the segmental tubes and of the primitive ova.

sp.c. spinal canal ; W. white matter of spinal cord ; pr. commissure connecting the posterior nerve-roots ; ch. notochord ; x. sub-notochordal rod ; ao. aorta ; sv. sinus venosus ; cav. cardinal vein ; ht. heart ; //. body cavity ; pc. pericardial cavity ; <xs. solid oesophagus ; /. liver ; mp. muscle-plate ; mp'. inner layer of muscle-plate ; Vr. rudiment of vertebral body ; st. segmental tube ; sd. segmental duct ; sp.v. spiral valve ; v. subintestinal vein.

clefts a division takes place, which is apparently equivalent to the segmentation of the mesoblast in the trunk. This division causes the body cavity of the head to be divided up into a series


of separate segments, one of which is shewn in fig. 24, pp. The walls of the segments eventually give rise to the main muscles of the branchial clefts, and probably also to the muscles of the mandibular arch, of the eye, and of other parts. The cephalic sections of the body cavity will be spoken of as head cavities.

In addition to the parts already mentioned the mesoblast gives rise to the whole of the vascular system, and to the generative system. The heart is formed from

part of the splanchnic meso- FlQ ^ HORIZONTAL SECTION THROUGH blast, and the generative THE LAST VISCERAL ARCH BUT ONE OF AN


system from a portion of the

mesoblast of the dorsal nart e ?' e P iblast 5 vc - P ouch of hypoblast sai pare which win form the walls of a visceral cleft .

of the body cavity. pp- segment of body-cavity in visceral arch ;

mt- i- TT aa. aortic arch.

The hypoblast. Very

shortly after the formation of the mesoblastic plates as lateral differentiations of the lower layer cells, an axial differentiation of the hypoblast appears, which gives rise to the notochord verymuch in the same way as in Amphioxus.

At first the hypoblast along the axial line forms a single layer in contact with the epiblast. Along this line a rod-like thickening of the hypoblast very soon appears (fig. 25, B and C, Ch'} at the head end of the embryo, and gradually extends backwards. This is the rudiment of the notochord ; it remains attached for some time to the hypoblast, and becomes separated from it first at the head end of the embryo (fig. 25 A, ch} : the separation is then carried backwards.

A series of sections taken through an embryo shortly after the first differentiation of the notochord presents the following characters.

In the hindermost sections the hypoblast retains a perfectly normal structure and uniform thickness throughout. In the next few sections (fig. 25 C, Ch'} a slight thickening is to be observed in it, immediately below the medullary groove. The layer, which elsewhere is composed of a single row of cells, here becomes two cells deep, but no sign of a division into two layers is exhibited.

In the next few sections the thickening of the hypoblast becomes much more pronounced ; we have, in fact, a ridge projecting from the hypoblast towards the epiblast (fig. 25 B, Ch'}. This ridge is pressed firmly against



A &

the epiblast, and causes in it a slight indentation. The hypoblast in the region of the ridge is formed of two layers of cells, the ridge being entirely due to the uppermost of the two.

In sections in front of this a cylindrical rod, which can at once be recognized as the notochord, and is continuous with the ridge just described, begins to be split off from the hypoblast (fig. 25 A, Ch). It is difficult to say at what point the separation of this rod from the hypoblast is completed, since all intermediate gradations between complete separation and complete attachment are to be seen.

Shortly after the separation takes place, a fairly


The sections shew the development of the notochord.

Ch. notochord ; Ch' . developing notochord ; mg. medullary groove ; Ip. lateral plate of mesoblast ; ep. epiblast ; Ay. hypoblast.

thick bridge is found connecting the two lateral halves of the hypoblast, but this bridge is anteriorly excessively delicate and thin, and in some cases is barely visible except with high powers. In some sections I have observed possible indications of the process like that described by Calberla for Petronyzon, by which the lateral parts of the hypoblast grow in underneath the axial part, and so isolate it bodily as the notochord.

It is not absolutely clear whether the notochord is to be regarded as an axial differentiation of the hypoblast, or as an axial differentiation of the lower layer cells.

The facts of development both in Amphioxus and Elasmobranchii tend towards the former view ; but the nearly simultaneous differentiation of the notochord and the mesoblastic plates lends some support to the supposition that the notochord may be merely a median plate of mesoblast developed slightly later than the two lateral plates.

The alimentary canal or mesenteron was left as a space between the hypoblast and the yolk, ending blindly in front, but





Ch. notochord ; hy. hypoblast ; al, alimentary tract ; na. cells passing in from the yolk to form the ventral wall of the alimentary tract.

opening behind by a widish aperture, the blastopore or anus of Rusconi (vide fig. 19 B).

The conversion of this irregular cavity into a closed canal commences first of all at the anterior extremity. In this conversion two distinct processes are concerned. One of these is a process of folding off of the embryo from the blastoderm. The other is a simple growth of cells independent of any fold. To the first of these processes the depth and narrowness of the alimentary cavity is due ; the second is concerned in forming its ventral wall. The process of the folding off of the embryo from the blastoderm resembles exactly the similar process in the embryo bird. The fold is a perfectly continuous one round the front end of the embryo, but may be conveniently spoken of as composed of a head-fold and two lateral folds.

Of far greater interest than the nature of these folds is the formation of the ventral wall of the alimentary canal. This originates in a growth of cells from the two sides to the middle line (fig. 26). The cells for it are not however mainly derived from pre-existing hypoblast cells, but are formed de novo around the nuclei of the yolk which have already been spoken of (fig. 26, no). The ventral wall of the mesenteron is in fact, to a large extent at any rate, formed as a differentiation of the primitive yolk floor.

The folding off and closing of the alimentary canal in the anterior part of the body proceeds rapidly, and not only is a considerable tract of the alimentary canal formed, but a great part of the head is completely folded off from the yolk before the medullary groove is closed.


The section shews the communication which exists between the neural and alimentary canals.

nc. neural canal ; al. alimentary tract ; Ch. notochord ; Ts. tail swelling.



The posterior part of the alimentary canal retains for a longer time its primitive condition. Finally however it also becomes closed in, by the lips of the blastopore at the hind end of the embryo meeting and uniting. The peculiarity of the closing in of the posterior part of the alimentary canal consists in the fact that a similar continuity to that in Amphioxus obtains between the neural and alimentary canals. This is due to the medullary folds being continuous at the end of the tail with the lips of the blastopore, which close in the hind end of the alimentary canal ; so that, when the medullary folds unite to form a canal, this canal becomes continuous with the alimentary canal, which is closed in at the same time. In other words, the medullary folds assist in enveloping the blastopore which does not therefore become absolutely closed, but opens into the floor of the neural canal. It will afterwards be shewn that it is only the posterior part of the blastopore that becomes closed during the above process, and that the anterior and ventral part long remains open. The general arrangement of the parts, at the time when the hind end of the mesenteron is first closed, is shewn in fig. 27. The same points may be seen in the diagrammatic longitudinal section fig. 19 C.

The middle portion of the alimentary tract is the last to be closed in since it remains till late in embryonic life as the umbilical or vitelline canal, connecting the yolk-sack with the alimentary cavity. The umbilical canal falls into the alimentary tract immediately behind the entrance of the hepatic duct.

At a fairly early stage of development a rod is constricted off from the dorsal wall of the alimentary canal (figs. 27* and 23 x], which is known as the subnotochordal rod. It is placed immediately below the notochord, and disappears during embryonic life.


df. dorsal fin ; s/>.c. spinal cord ; pp. body cavity ; sf. splanchnic layer of mesoblast ; so. somatic layer of mesoblast ; mp. commencing differentiation of muscles; ch. notochord; x. sub-notochordal rod arising as an outgrowth of the dorsal wall of the alimentary tract ; al. alimentary tract.


General features of tlie Elasnwbranch embryo at successive stages.

Shortly after the three germinal layers become definitely established, the rudiment of the embryo, as visible from the surface, consists of an oblong plate, which extends inwards from the periphery of the blastoderm, and is bounded on its inner side by a head-fold and two lateral folds (fig. 28 B). This plate is the medullary plate ; along its axial line is a shallow groove the medullary groove (ing). The rudiment of the embryo rapidly increases in length, and takes a spatula-like form (fig. 28 C). The front part of it, turned away from the edge of the blastoderm, soon becomes dilated into a broad plate, the cephalic plate (//) while the tail end at the edge of the blastoderm is also enlarged, being formed of a pair of swellings the tail swellings (ts) derived from the lateral parts of the original embryonic rim. By this stage a certain number of mesoblastic somites have become formed but are not shewn in my figure. They are the foremost somites of the trunk, and those behind them continue to be added, like the segments in Chaetopods. between the last formed somite and the end of the body. The increase in length of the body mainly takes place by growth in the region between the last mesoblastic somite and the end of the tail. The anterior part of the body is now completely folded off from the blastoderm, and the medullary groove of the earlier stage has become converted into a closed canal.

By the next stage (fig. 28 D) the embryo has become so much folded off from the yolk both in front and behind that the separate parts of it begin to be easily recognizable.

The embryo is attached to the yolk by a distinct stalk or cord, which in the succeeding stages gradually narrows and elongates, and is known as the umbilical cord (so. s.). The medullary canal has now become completely closed. The anterior region constitutes the brain ; and in this part slight constrictions, not perceptible in views of the embryo as a transparent object, mark off three vesicles. These vesicles are known as the fore, mid, and hind brain. From the fore-brain there is an outgrowth on each side, the first rudiment of the optic vesicles {op). The tail swellings are still conspicuous.


The tissues of the body have now become fairly transparent, and there may be seen at the sides of the body seventeen mesoblastic somites. The notochord, which was formed long



A. A blastoderm before the formation of the medullary plate, sc. segmentation cavity ; cs. embryonic swelling.

B. A somewhat older blastoderm in which the medullary groove has been established, mg. medullary groove.

C. An embryo from the dorsal surface, as an opaque object, after the medullary groove has become posteriorly converted into a tube. mg. medullary groove : the reference line points very nearly to the junction between the open medullary groove with the medullary tube ; h. cephalic plate ; ts. tail swelling.

D. Side view of a somewhat older embryo as a transparent object, ch. notochord ; op. optic vesicle ; I.v.c. ist visceral cleft; al. alimentary tract ; so.s. stalk connecting the yolk-sack with the embryo.

E. Side view of an older embryo as a transparent object, mp. muscle-plates ; au.v. auditory vesicle ; vc. visceral cleft ; lit. heart ; in. mouth invagination ; an. anal diverticulum ; al.v. posterior vesicle of post-anal gut.

F. G. II. Older embryos as opaque objects.



before the stage represented in figure 28 D, is now also distinctly visible. It extends from almost the extreme posterior to the anterior end of the embryo, and lies between the ventral wall of the spinal canal and the dorsal wall of the intestine. Round its posterior end the neural and alimentary tracts become continuous with each other. Anteriorly the termination of the notochord cannot be seen, it can only be traced into a mass of mesoblast at the base of the brain, which there separates the epiblast from the hypoblast. The alimentary canal (al) is completely closed anteriorly and posteriorly, though still widely open to the yolk-sack in the middle part of its course. In the region of the head it exhibits on each side a slight bulging outwards, the rudiment of the first visceral cleft. This is represented in the figure by two lines (l. v.c.}.

The embryo represented in fig. 28 E is far larger than the one just described, but it has not been convenient to represent this increase of size in the figure. Accompanying this increase in size, the folding off from the yolk has considerably progressed, and the stalk which unites the embryo with the yolk is proportionately narrower and longer than before.

The brain is now very distinctly divided into the three lobes, the rudiments of which appeared during the last stage. From the foremost of these the optic vesicles now present themselves as well-marked lateral outgrowths, towards which there has appeared an involution from the external skin (op) to form the lens.

A fresh organ of sense, the auditory sack, now for the first time becomes visible as a shallow pit in the external skin on each side of the hind-brain (au.v). The epiblast which is involuted to form this pit becomes much thickened, and thereby the opacity, indicated in the figure, is produced.

The mesoblastic somites have greatly increased in number by the formation of fresh somites in the tail. Thirty-eight of them were present in the embryo figured. The mesoblast at the base of the brain is more bulky, and there is still a mass of unsegmented mesoblast which forms the tail swellings. The first rudiment of the heart (Jit) becomes visible during this stage as a cavity between the mesoblast of the splanchnopleure and the hypoblast.


The fore and hind guts are now longer than they were. An invagination from the exterior to form the mouth has appeared (m) on the ventral side of the head close to the base of the thalamencephalon. The upper end of this eventually becomes constricted off as the pituitary body, and an indication of the future position of the anus is afforded by a slight diverticulum of the hind gut towards the exterior, some little distance from the posterior end of the embryo (an}. The portion of the alimentary canal behind this point, though at this stage large, and even dilated into a vesicle at its posterior end (al.v), becomes eventually completely atrophied. It is known as the post-anal gut. In the region of the throat the rudiment of a second visceral cleft has appeared behind the first ; neither of them is as yet open to the exterior.

In a somewhat older embryo the first spontaneous movements take place, and consist in somewhat rapid excursions of the embryo from side to side, produced by a serpentine motion of the body.

A ventral flexure of the prae-oral part of the head, known as the cranial flexure, which commenced in earlier stages (fig. 28 D and E), has now become very evident, and the mid-brain 1 begins to project in the same manner as in the embryo fowl on the

1 The part of the brain which I have here called mid-brain, and which unquestionably corresponds to the part called mid-brain in the embryos of higher vertebrates, becomes in the adult what Miklucho-Maclay and Gegenbaur called the vesicle of the third ventricle or thalamencephalon.

cl. ul


A is the posterior section.

nc. neural canal ; al. post-anal gut ; alv. caudal vesicle of post-anal gut ; x. sub-notochord rod ; inp. muscle-plate; th. notochord; cloaca; ao. aorta ; v.cati. caudal vein.


third day, and will soon form the anterior termination of the long axis of the embryo. The fore-brain has increased in size and distinctness, and the anterior part of it may now be looked on as the unpaired rudiment of the cerebral hemispheres.

Further changes have taken place in the organs of sense, especially in the eye, in which the involution for the lens has made considerable progress. The number of the muscle-plates has again increased, but there is still a region of unsegmented mesoblast in the tail. The thickened portions of mesoblast, which caused the tail swellings, are still to be seen, and would seem to act as the reserve from which is drawn the matter for the rapid growth of the tail, which occurs soon after this. The mass of the mesoblast at the base of the brain has again increased. No fresh features of interest are to be seen in the notochord. The heart is very much more conspicuous than before, and its commencing flexure is very apparent. It now beats actively. The post-anal gut is much longer than during the last stage ; and the point where the anus will appear is very easily detected by a bulging out of the gut towards the external skin. The alimentary vesicle at the end of the post-anal gut, first observable during the last stage, is now a more conspicuous organ. There are three visceral clefts, none of which are as yet open to the exterior.

Figure 28 F represents a considerably older embryo viewed as an opaque object, and fig. 29 A is a view of the head as a transparent object. The stalk connecting it with the yolk is now, comparatively speaking, quite narrow, and is of sufficient length to permit the embryo to execute considerable movements.

The tail has grown immensely, but is still dilated terminally. The terminal dilatation is mainly due to the alimentary vesicle (fig. 28* alv), but the post-anal section of the alimentary tract in front of this is now a solid cord of cells. Both the alimentary vesicle and this cord very soon disappear. Their relations are shewn in section in fig. 28*.

The two pairs of limbs have appeared as differentiations of a continuous but not very conspicuous epiblastic thickening, which is probably the rudiment of a lateral fin. The anterior pair is situated just at the front end of the umbilical stalk ; and the



posterior pair, which is the later developed and less conspicuous of the two, is situated some little distance behind the stalk.

The cranial flexure has greatly increased, and the angle between the long axis of the front part of the head

and of the body is less (

_, mb Jv^gi^.

than a right angle. The \^f* B^. iv.v

conspicuous mid-brain (29 A, mb) forms the anterior termination of the long axis of the body. The thin roof of the fourth ventricle (lib] may be noticed in the figure behind the mid-brain. The auditory sack (au.V) is nearly closed, and its opening is not shewn in the figure. In the eye (op) the lens is completely formed. The olfactory pit (ol) is seen a little in front of the eye.

Owing to the opacity of the embryo, the muscle-plates are only indistinctly indicated in fig. 28 F, other features of the mesoblast are to be seen.

The mouth is now a deep pit, the hind borders of which are almost completely formed by a thickening in front of the first branchial or visceral cleft, which may be called the first branchial arch or mandibular arch.

Four branchial clefts are now visible, all of which are open to the exterior, but in the embryo, viewed as a transparent


A. Frist iurus embryo of the same stage as fig. 28 F.

B. Somewhat older Scyllium embryo.

///. third nerve ; V. fifth nerve ; VII. seventh nerve ; au.n. auditory nerve ; gl. glossopharyngeal nerve ; Vg. vagus nerve ; ft. fore-brain ; pn. pineal gland ; nib. mid-brain ; hb. hind-brain ; iv.v. fourth ventricle ; cb. cerebellum ; ol. olfactory pit ; op. eye ; au. V. auditory vesicle ; m. mesoblast at base of brain ; ch. notochord ; ht. heart ; Vc. visceral clefts ; eg. external gills ; //. sections of body cavity in the head.



object, two more, not open to the exterior, are visible behind the last of these.

Between each of these and behind the last one there is a thickening of the mesoblast which gives rise to a branchial arch. The arch between the first and second cleft is known as the hyoid arch.

Fig. 29 B is a representation of the head of a slightly older embryo in which papillae may be seen in the front wall of the second, third, and fourth branchial clefts : these papillae are the commencements of filiform processes which grow out from the gill-clefts and form external gills. The peculiar ventral curvature of the anterior end of the notochord (cJi) both in this and in the preceding figure deserves notice.

A peculiar feature in the anatomy makes its appearance at this period, viz. the replacement of the original hollow oesophagus by a solid cord of cells (fig. 23 A, ces) in which a lumen does not reappear till very much later. I have found that in some Teleostei (the Salmon) long after they are hatched a similar solidity in the oesophagus is present. It appears not impossible that this feature in the oesophagus may be connected with the fact that in the ancestors of the present types the oesophagus was perforated by gill slits ; and that in the process of embryonic abbreviation the stage with the perforated oesophagus became replaced by a stage with a cord of indifferent cells (the oesophagus being in the embryo quite functionless) out of which the non-perforated oesophagus was directly formed. In the higher types the process of development appears to have become quite direct.

By this stage all the parts of the embryo have become established, and in the succeeding stages the features characteristic of the genus and species are gradually acquired.

Two embryos of Scyllium are represented in fig. 28 G and H, the head and anterior part of the trunk being represented in fig. G, and the whole embryo at a much later stage in fig. H.

In both of these, and especially in the second, an apparent diminution of the cranial flexure is very marked. This diminution is due to the increase in the size of the cerebral hemispheres, which grow upwards and forwards, and press the original forebrain against the mid-brain behind.

In fig. G the rudiments of the nasal sacks are clearly visible as small open pits.


The first cleft is no longer similar to the rest, but by the closure of the lower part has commenced to be metamorphosed into the spiracle.

Accompanying the change in position of the first cleft, the mandibular arch has begun to bend round so as to enclose the front as well as the sides of the mouth. By this change in the mandibular arch the mouth becomes narrowed in an anteroposterior direction.

In fig. H are seen the long filiform external gills which now project out from all the visceral clefts, including the spiracle. They are attached to the front wall of the spiracle, to both walls of the next four clefts, and to the front wall of the last cleft. They have very possibly become specially developed to facilitate respiration within the egg ; and they disappear before the close of larval life.

When the young of Scyllium and other Sharks are hatched they have all the external characters of the adult. In Raja and Torpedo the early stages, up to the acquirement of a shark-like form, are similar to those in the Selachoidei, but during the later embryonic stages the body gradually flattens out, and assumes the adult form, which is thus clearly shewn to be a secondary acquirement.

An embryonic gill cleft behind the last present in the adult is found (Wyman, No. 54) in the embryo of Raja batis.

The unpaired fins are developed in Elasmobranchs as a fold of skin on the dorsal side, which is continued round the end of the tail along the ventral side to the anus. Local developments of this give rise to the dorsal and anal fins. The caudal fin is at first symmetrical, but a special lower lobe grows out and gives to it a heterocercal character.

Enclosure of the yolk-sack and its relation to the embryo.

The blastoderm at the stage represented in fig. 28 A and B forms a small and nearly circular patch on the surface of the yolk, composed of epiblast and lower layer cells. While the body of the embryo is gradually being moulded this patch grows till it envelopes the yolk ; the growth is not uniform, but


is less rapid in the immediate neighbourhood of the embryonic part of the blastoderm than elsewhere. As a consequence of this, that part of the edge, to which the embryo is attached, forms a bay in the otherwise regular outline of the edge of the blastoderm, and by the time that about twothirds of the yolk is enclosed this bay is very conspicuous. It is shewn in fig. 30 A, where bl points to the blastoderm, and yk to the part of the yolk not yet covered by the blastoderm. The embryo at this time is only connected with the yolksack by a narrow umbilical cord ; but, as shewn in the figure, is still attached to the edge of the


Shortly subsequent to this the bay in the blastoderm, at the head of which the embryo is attached, becomes obliterated by its two sides coming together and coalescing. The embryo then ceases to be attached at the edge of the blastoderm. But a linear streak


The shaded part (bl) is the blastoderm; the white part the uncovered yolk.

A. Young stage with the embryo still attached at the edge of the blastoderm.

B. Older stage with the yolk not quite enclosed by the blastoderm.

C. Stage after the complete enclosure of the yolk.

yk. yolk ; bl. blastoderm ; v. venous trunks of yolk-sack; a. arterial trunks of yolk-sack; y. point of closure of the yolk blastopore ; x. portion of the blastoderm outside the arterial sinus terminalis.

formed by the coalesced

edges of the blastoderm is left connecting the embryo with the


edge of the blastoderm. This streak is probably analogous to (though not genetically related with) the primitive streak in the Amniota.

This stage is represented in fig. 30 B. In this figure there is only a small patch of yolk (yk] not yet enclosed, which is situated at some little distance behind the embryo. Throughout all this period the edge of the blastoderm has remained thickened : a feature which persists till the complete investment of the yolk, which takes place shortly after the stage last described. In this thickened edge a circular vein arises which brings back the blood from the yolk-sack to the embryo. The opening in the blastoderm, exposing the portion of the yolk not yet covered, may be conveniently called the yolk blastopore. It is interesting to notice that, owing to the large size of the yolk in Elasmobranchs, the posterior part of the primitive blastopore becomes encircled by the medullary folds and tailswellings, and is so closed long before the anterior and more ventral part, which is represented by the uncovered portion of the yolk. It is also worth remarking that, owing to the embryo becoming removed from the edge of the blastoderm, the final closure of the yolk blastopore takes place at some little distance from the embryo.

The blastoderm enclosing the yolk is formed of an external layer of epiblast, a layer of mesoblast below in which the bloodvessels are developed, and within this a layer of hypoblast, which is especially well marked and ciliated (Leydig, No. 46) in the umbilical stalk, where it lines the canal leading from the yolk-sack to the intestine. In the region of the yolk-sack proper the blastoderm is so thin that it is not easy to be quite sure that a layer of hypoblast is throughout distinct. Both the hypoblast and mesoblast of the yolk-sack are formed by a differentiation of the primitive lower layer cells.

Nutriment from the yolk-sack is brought to the embryo partly through the umbilical canal and so into the intestine, and partly by means of blood-vessels in the mesoblast of the sack. The blood-vessels arise before the blastoderm has completely covered the yolk.

Fig. 30 A represents the earliest stage of the circulation of the yolk-sack. At this stage there is visible a single arterial


trunk (a) passing forwards from the embryo and dividing into two branches. No venous trunk could be detected with the simple microscope, but probably venous channels were present in the thickened edge of the blastoderm.

In fig. 30 B the circulation is greatly advanced. The blastoderm has now nearly completely enveloped the yolk, and there remains only a small circular space (yk] not enclosed by it. The arterial trunk is present as before, and divides in front of the embryo into two branches which turn backwards and form a nearly complete ring round the embryo. In general appearance this ring resembles the sinus terminalis of the area vasculosa of the Bird, but in reality bears quite a different relation to the circulation. It gives off branches on its inner side only.

A venous system of returning vessels is now fully developed, and its relations are very remarkable. There is a main venous ring in the thickened edge of the blastoderm, which is connected with the embryo by a single stem running along the seam where the edges of the blastoderm have coalesced. Since the venous trunks are only developed behind the embryo, it is only the posterior part of the arterial ring that gives off branches.

The succeeding stage (fig. 30 C) is also one of considerable interest. The arterial ring has greatly extended, and now embraces nearly half the yolk, and sends off trunks on its inner side along its whole circumference. More important changes have taken place in the venous system. The blastoderm has now completely enveloped the yolk, and the venous ring is therefore reduced to a point. The small veins which originally started from it may be observed diverging in a brush-like fashion from the termination of the unpaired trunk, which originally connected the venous ring with the heart.

At a still later stage the arterial ring embraces the whole yolk, and, as a result of this, vanishes in its turn, as did the venous ring before it. There is then present a single arterial and a single venous trunk. The arterial trunk is a branch of the dorsal aorta, and the venous trunk originally falls into the heart together with the subintestinal or splanchnic vein. On the formation of the liver the proximal end of the subintestinal vein becomes the portal vein, and it is joined just as it enters B. in. 5


the liver by the venous trunk from the yolk-sack. The venous trunk leaves the body on the right side, and the arterial on the left.

The yolk-sack persists during the whole of embryonic life, and in the majority of Elasmobranch embryos there arises within the body walls an outgrowth from the umbilical canal into which a large ampunt of the yolk passes. This outgrowth forms an internal yolk-sack. In Mustelus vulgaris the internal yolk-sack is very small, and in Mustelus laevis it is absent. The latter species, which is one of those in which development takes place within the uterus, presents a remarkable peculiarity in that the vascular surface of the yolk-sack becomes raised into a number of folds, which fit into corresponding depressions in the vascular walls of the uterus. The yolk-sack becomes in this way firmly attached to the walls of the uterus, and the two together constitute a kind of placenta. A similar placenta is found in Carcharias.

After the embryo is hatched or born, as the case may be, the yolk-sack becomes rapidly absorbed.


(40) F. M. B a 1 f o u r. "A preliminary account of the development of the Elasmobranch Fishes." Quart. J. of Micr. Science, Vol. xrv. 1876.

(41) F. M. Balfour. "A Monograph on the development of Elasmobranch Fishes." London, 1878. Reprinted from the Journal of Anat. and Physiol. for 1876, 1877, and 1878.

(42) Z. Gerbe. " Recherches sur la segmentation de la cicatrule et la formation tits produits adventifs de Fceuf des Plagiostomes et particular em ent des Rates." Vide also Journal de FAnatomie et de la Physiologie, 1872.

(43) W. His. " Ueb. d. Bildung v. Haifischenembryonen." Zeit.ftir Anat. u. Entwick., Vol. n. 1877.

(44) A. Kowalevsky. "Development of Acanthias vulgaris and Mustelus Isevis." (Russian.) Transactions of the Kieiv Society of Naturalists, Vol. I. 1870.

(45) R. Leuckart. " Ueber die allmahlige Bildung d. Korpergestalt bei d. Kochen." Zeit. f. wiss. Zoo!., Bd. II., p. 258.

(46) Fr. Leydig. Rochen u. Haie. Leipzig, 1852.

(47) A. W. Malm. " Bidrag till kannedom om utvecklingen af Rajae." Kongl. vctenskaps akademiens forhandlingar. Stockholm, 1876.

(48) Joh. M tiller. Clatter Haie des Aristoteles und iiber die Verschicdcnheitcn unlcr den Haifischen und Rochen in der Entwicklung des Eies. Berlin, 1 840.

(49) S. L. Schenk. " Die Eier von Raja quadrimaculata innerhalb tier Eileiter." Sitz. der k. Akad. IVien, Vol. LXXIII. 1873.


(50) Alex. Schultz. " Zur Entwicklungsgeschichte des Selachiereies. " Archiv fiir micro. Anat., Vol. XI. 1875.

(51) Alex. Schultz. " Beitrag zur Entwicklungsgeschichte d. Knorpelfische." Archiv fiir micro. Anat., Vol. xm. 1877.

(52) C. Semper. "Die Stammesverwandschaft d. Wirbelthiere u. Wirbellosen." Arbeit, a. d. zool.-zoot. Instit. Wurzburg, Vol. II. 1875.

(53) C. Semper. " Das Urogenitalsystem d. Plagiostomen, etc." Arbeit, a. d. zool.-zoot. Instit. Wurzburg, Vol. II. 1875.

(54) Wyman. " Observations on the Development of Raja batis." Memoirs of the American Academy of Arts and Sciences, Vol. IX. 1864.