The Works of Francis Balfour 3-7

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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 eggs of most Amphibia 2 are laid in water. They are smallish nearly spherical bodies, and in the majority of known Anura (all the European species), and in many Urodela (Amblystoma, Axolotl, though not in the common Newt) part of the surface is dark or black, owing to the presence of a superficial layer of pigment, while the remainder is unpigmented. The pigmented part is at the upper pole of the egg, and contains the germinal vesicle till the time of its atrophy ; and the yolkgranules in it are smaller than those in the unpigmented part. The ovum is closely surrounded by a vitelline membrane 3 , and receives, in its passage down the oviduct, a gelatinous investment of varying structure.

In the Anura the eggs are fertilized as they leave the oviduct. In some of the Urodela the mode of fertilization is still imperfectly understood. In Salamanders and probably Newts it is internal 4 ;

1 The following classification of the Amphibia is employed in the present chapter: fAGLOSSA.


( Trachystomata. PERENNIBRANCHIATA \ Proteidce

ii. Urodela.



( Amblystomidae . MYCTODERA <,, , , .,


III. Gymnophiona.

2 I am under great obligations to Mr Parker for having kindly supplied me, in answer to my questions, with a large amount of valuable information on the development of the Amphibia.

3 Within the vitelline membrane there appears to be present, in the Anura at any rate, a very delicate membrane closely applied to the yolk.

4 Allen Thomson informs me that he has watched the process of fertilization in the Newt, and that the male deposits the semen in the water close to the female. From the water it seems to enter the female generative aperture. Von Siebold has shewn that there is present in female Newts and Salamanders a spermatic bursa. In this bursa the spermatozoa long (three months) retain their vitality in some Salamanders. Various peculiarities in the gestation are to be explained by this fact.


but in Amblystoma punctatum (Clark, No. 98), the male deposits the semen in the water. The eggs are laid by the Anura in masses or strings. By Newts they are deposited singly in the angle of a bent blade of grass or leaf of a water-plant, and by Amblystoma punctatum in masses containing from four eggs to two hundred. Salamandra atra and Salamandra maculosa are viviparous. The period of gestation for the latter species lasts a whole year.

A good many exceptions to the above general statements have been recorded 1 .

In Notodelphis ovipara the eggs are transported (by the male?) into a peculiar dorsal pouch of the skin of the female, which has an anterior opening, but is continued backwards into a pair of diverticula. The eggs are very large, and in this pouch, which they enormously distend, they undergo their development. A more or less similar pouch is found in Nototrema marsupiatum.

In the Surinam toad (Pipa dorsigera) the eggs are placed by the male on the back of the female. A peculiar pocket of skin becomes developed round each egg, the open end of which is covered by a gelatinous operculum. The larvae are hatched, and actually undergo their metamorphosis, in these pockets. The female during this period lives in water. Pipa Americana (if specifically distinct from P. dorsigera) presents nearly the same peculiarities. The female of a tree frog of Ceylon (Polypedates reticulatus) carries the eggs attached to the abdomen.

Rhinoderma Darwinii 2 behaves like some of the Siluroid fishes, in that the male carries the eggs during their development in an enormously developed laryngeal pouch.

Some Anura do not lay their eggs in water. Chiromantis Guineensis attaches them to the leaves of trees ; and Cystignathus mystacius lays them in holes near ponds, which may become filled with water after heavy rains.

The eggs of Hylodes Martinicensis are laid under dead leaves in moist situations.

Formation of the layers.

Anura. The formation of the germinal layers has so far only been studied in some Anura and in the Newt. The following description applies to the Anura, and I have called

1 For a summary of these and the literature of the subject vide "Amphibia," by C. K. Hoffmann, in Bronn's Classen ^^nd Ordnungen d. Thier-reichs.

2 Vide Spengel, " Die Fortpflanzung des Rhinoderma Darwinii." Zeit. f. wiss. Zool., Bd. XXIX., 1877. This paper contains a translation of a note by Jiminez de la Espada on the development of the species.



attention, at the end of the section, to the points in which the Newt is peculiar.

The segmentation of the Frog's ovum has already been described (Vol. II. pp. 95-7), but I may remind the reader that the segmentation (fig. 69) results in the formation of a vesicle, the cavity of which is situated excentrically; the roof of the cavity being much thinner than the floor. The cavity is the segmentation cavity. The roof is formed of two or three layers of smallish pigmented cells, and the floor of large cells, which form the


The numbers above the figures refer to the number of segments at the stage figured.

greater part of the ovum. These large cells, which are part of the primitive hypoblast, will be spoken of in the sequel as yolkcells : they are equivalent to the food-yolk of the majority of vertebrate ova.

The cells forming the roof of the cavity pass without any sharp boundary into the yolk-cells, there being at the junction of the two a number of cells of an intermediate character. The cells both of the roof and the floor continue to increase in number, and those of the roof become divided into two distinct strata (fig. 70, ep}.

The upper of these is formed of a single row of somewhat cubical cells, and the lower of several rows of more rounded cells. Both of these strata eventually become the epiblast, of which they form the epidermic and nervous layers. The roof of the segmentation cavity appears therefore to be entirely constituted of epiblast.

The next changes which take place lead (i) to the formation


I2 3

of the mesenteron 1 , and (2) to the enclosure of the yolk-cells by the epiblast.

The mesenteron is formed as in Petromyzon and Lepidosteus by an unsymmetrical form of invagination. The invagination first commences by an inflection of the epiblast-cells for a small arc on the equatorial line which marks the junction between the epiblastic cells and the yolk-cells (fig. 70, x].

The inflected cells become continuous with the adjoining cells ; and the region where the inflection is formed constitutes a kind of lip, below which a slit-like cavity is soon established. This lip is equivalent to the embryonic rim of the Elasmobranch blastoderm, and the cavity beneath it is the rudiment of the mesenteron.

The mesenteron now rapidly extends by the invagination of the cells on its dorsal side. These cells grow inwards towards the segmentation cavity as a layer of cells several rows deep. At its inner end, this layer is continuous with the yolk-cells ; and is divided into two strata (fig. 71 A), viz. (i) a stratum of several rows of cells adjoining the epiblast, which becomes the mesoblast (m), and (2) a stratum of a single row of more columnar cells lining the cavity of the mesenteron, which forms the hypoblast (Jiy). The growth inwards of the dorsal wall of the mesenteron is no doubt in part a true invagination, but it seems probable that it is also due in a large measure to an actual differentiation of yolk-cells along the line of growth. The mesenteron is at first a simple slit between the yolk and the hypoblast (fig. 71 A), but as the involution of the hypoblast and

1 Since the body cavity is not developed as diverticula from the cavity of invagination, the latter cavity may conveniently be called the mesenteron and not the archenteron.


S S- segmentation cavity ; //. large yolkcontaining cells ; ep. small cells at formative pole (epiblast) ; x. point of inflection of epiblast ; y. small cells close to junction of the epiblast and yolk.

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mesoblast extends further inwards, this slit enlarges, especially at its inner end, into a considerable cavity ; the blind end of which is separated by a narrow layer of yolk-cells from the segmentation cavity (fig. 71 B).

In the course of the involution, the segmentation cavity becomes gradually pushed to one side and finally obliterated. Before obliteration, it appears in some forms (Pelobates fuscus) to become completely enclosed in the yolk-cells.

While the invagination to form the mesenteron takes place as above described, the enclosure of the yolk has been rapidly proceeding. It is effected by the epiblast growing over the yolk at all points of its circumference. The nature of the growth is however very different at the embryonic rim and elsewhere. At the embryonic rim it takes place by the simple growth of the rim, so that the point x in figs. 70 and 71 is carried further and A B


ep. epiblast; m, dorsal mesoblast; m'. ventral mesoblast; hy. hypoblast; yk. yolk ; jr. point of junction of the epiblast and hypoblast at the dorsal side of the blastopore ; al. mesenteron ; sg. segmentation cavity.

further over the surface of the yolk. Elsewhere the epiblast at first extends over the yolk as in a typical epibolic gastrula, without being inflected to form a definite lip. While a considerable patch of yolk is still left uncovered, the whole of the edge of the epiblast becomes however inflected, as at the embryonic rim (fig. 71 A); and a circular blastopore is established, round the


whole edge of which the epiblast and intermediate cells are continuous.

' From the ventral lip of the blastopore the mesoblast (fig. 71,

  1. '), derived from the small intermediate cells, grows inwards till

it comes to the segmentation cavity ; the growth being not so much due to an actual invagination of cells at the lip of the blastopore, as to a differentiation of yolk-cells in situ. Shortly after the stage represented in fig. 71 B, the plug of yolk, which fills up the opening of the blastopore, disappears, and the mesenteron communicates freely with the exterior by a small circular blastopore (fig. 73). The position of the blastopore is the same as in other types, viz. at the hinder end of the embryo.

By this stage the three layers of the embryo are definitely established. The epiblast, consisting from the first of two strata, arises from the small cells forming the roof of the segmentationcavity. It becomes continuous at the lip of the blastopore with cells intermediate in size between the cells of which it is formed and the yolk-cells. These latter, increasing in number by additions from the yolk-cells, give rise to the mesoblast and to part of the hypoblast ; while to the latter layer the yolk-cells, as mentioned above, must also be considered as appertaining. Their history will be dealt with in treating of the general fate of the hypoblast.

Urodela. The early stages of the development of the Newt have been adequately investigated by Scott and Osborn (No. 114). The segmentation and formation of the layers is in the main the same as in the Frog. The ovum is without black pigment. There is a typical unsymmetrical invagination, but the dorsal lip of the blastopore is somewhat thickened. The most striking feature in which the Newt differs from the Frog is the fact that the epiblast is at first constituted of a single layer of cells (fig. 75, ep\ The roof of the segmentation cavity is constituted, during the later stages of segmentation, of several rows of cells (Bambeke, No. 95), but subsequently it would appear to be formed of a single row of cells only (Scott and Osborn, No. 114).

General history of the layers.

Epiblast : Anura. At the completion of the invagination the epiblast forms a continuous layer enclosing the whole ovum, and constituted throughout of two strata. The formation of the medullary canal commences by the nervous layer along the axial dorsal line becoming thickened, and giving rise to a some



what pyriform medullary plate, the sides of which form the projecting medullary folds (fig. 77 A). The medullary plate is thickened at the two sides, and is grooved in the median line by a delicate furrow (fig. 72, r). The dilated extremity of the medullary plate, situated at the end of the embryo opposite the blastopore, is the cerebral part of the plate, and the remainder



/. medullary groove; r. axial furrow in the medullary groove; h. nervous layer of epidermis ; as. outer portion of vertebral plate ; is. inner portion of vertebral plate ; s. lateral plate of mesoblast ; g. notochord ; e. hypoblast.

the spinal. The medullary folds bend upwards, and finally meet above, enclosing a central cerebro-spinal canal (fig. 74). The point at which they first meet is nearly at the junction of the brain and spinal cord, and from this point their junction extends backwards and forwards; but the whole process is so rapid that the closure of the medullary canal for its whole length is effected nearly simultaneously. In front the medullary canal ends blindly, but behind it opens freely into the still persisting blastopore, with the lips of which the medullary folds become, as in other types, continuous. Fig. 73 represents a longitudinal section through an embryo, shortly after the closure of the medullary canal (nc) ; the opening of which into the blastopore (x) is clearly seen.

On the closure of the medullary canal, its walls become separated from the external epiblast, which extends above it as a continuous layer. In the formation of the central nervous system both strata of the epiblast have a share, though the main mass is derived from the nervous layer. After the central


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nervous tube has become separated from the external skin, the two layers forming it fuse together ; but there can be but little doubt that at a later period the epidermic layer separates itself again as the central epithelium of the nervous system.

Both the nervous and epidermic strata have a share in forming the general epiblast ; and though eventually they partially fuse together yet the horny layer of the adult epidermis, where such can be distinguished, is probably derived from the epidermic layer of the embryo, and the mucous layer of the epidermis from the embryonic nervous layer.

In the formation of the organs of sense the nervous layer shews itself throughout as the active layer. The


SECTION OF THE EMBRYO OF A FROG. (Modified from Gotte.)

nc. neural canal ; x. point of junction of epiblast and hypoblast at the dorsal lip of the blastopore ; al. alimentary tract ; yk. yolkcells ; m. mesoblast. For the sake of simplicity the epiblast is represented as if composed of a single row of cells.

lens of the eye and the auditory sack are derived exclusively from it, the latter having no external opening. The nervous layer also plays the more important part in the formation of the olfactory sack.

The outer layer of epiblast-cells becomes ciliated after the close of the segmentation, but the cilia gradually disappear on the formation of the internal gills. The cilia cause a slow rotatory movement of the embryo within the egg, and probably assist in the respiration after it is hatched. They are especially developed on the external gills.

Urodela. In the Newt (Scott and Osborn, No. 114) the medullary plate becomes established, while the epiblast is still formed of a single row of cells ; and it is not till after the closure of the neural groove that any distinction is observable between the epithelium of the central canal, and the remaining cells of the cerebro-spinal cord (fig. 75).

Before the closure of the medullary folds the lateral epiblast becomes divided into the two strata present from the first in the Frog ; and in the subsequent development the inner layer behaves as the active layer, precisely as in the Anura.



The mesoblast and notochord : Anura. After the disappearance of the segmentation cavity, the mesoblast is described by most observers, including Gotte, as forming a continuous sheet round the ovum, underneath the epiblast. The first important differentiations in it take place, as in the case of the epiblast, in the axial dorsal line. Along this line a central cord of the mesoblast becomes separated from the two lateral sheets to form the notochord. Calberla states, however, that when the mesoblast is distinctly separated from the hypoblast it does not form a continuous sheet, but two sheets one on each side, between which is placed a ridge of cells continuous with the hypoblastic sheet. This ridge subsequently becomes separated from the hypoblast as the notochord. Against this view Gotte has recently strongly protested, and given a series of careful representations of his sections which certainly support his original account. r

My own observations are in favour of Calberla's statement, and so far as I can determine from my sections the mesoblast never appears as a perfectly continuous sheet, but is always deficient in the dorsal median line. My observations are unfortunately not founded on a sufficient series of sections to settle the point definitely.

After the formation of the notochord (fig. 72), the mesoblast may be regarded as consisting of two lateral plates, continuous ventrally, but separated in the median dorsal line. By the division of the dorsal parts of these plates into segments, which commences in the region of the neck and thence extends backwards, the mesoblast of the trunk becomes divided into


as"', medulla oblongata ; is*, splanchnopleure ; as*, somatopleure in the vertebral part of the mesoblastic plate ; s. lateral plate of mesoblast ; f. throat ; e. passage of epithelial cells into yolk-cells ; d. yolk-cells ; r. dorsal groove along the line of junction of the medullary folds.



a vertebral portion, cleft into separate somites, and a lateral unsegmented portion (fig. 74).

The history of these two parts and of the mesoblast is generally the same as in Elasmobranchs.

The mesoblast in the head becomes, according to Gotte, divided into four segments, equivalent to the trunk somites. Owing to a confusion into which Gotte has fallen from not recognizing the epiblastic origin of the cranial nerves, his statements on this head must, I think, be accepted with considerable reserve ; but some part of his segments appears to correspond with the head-cavities of Elasmobranchii.

Urodela. Scott and Osborn (No. 114) have shewn that in the Newt the mesoblast (fig. 75) is formed of two lateral plates, split off from the hypoblast, and that^the ventral growth of these plates is largely effected by the conversion of yolk-cells into mesoblast-cells. They have further shewn that the notochord is formed of an axial portion of the hypoblast, as in the types already considered (fig. 75). The body cavity is continued into the region of the head ; and the mesoblast lining the cephalic section of the body cavity is divided into the same number of head cavities as in Elasmobranchii, viz. one in front of the mouth, and one in the mandibular and one in each of the following arches.

The hypoblast. There are no important points of difference in the relations of the hypoblast between the Anura and Urodela. The mesenteron, at the stage represented in fig. 73, forms a wide cavity lined dorsally by a layer of invaginated hypoblast, and ventrally by the yolk-cells. The hypoblast is continuous laterally and in front with the yolk-cells (figs. 72, 74 and 75). At an earlier stage, when the mesenteron has a less definite form, such a continuity between the true hypoblast and the yolk-cells does not exist at the sides of the cavity.

The definite closing in of the mesenteron by the true hypoblast-cells commences in front and behind, and takes place last B. in. 9



In.hy. invaginated hypoblast, the dorsal part of which will form the notochord ; ep. epiblast of neural plate; sp. splanchnopleure ; al. alimentary tract ; yk. and Y.hy. yolk-cells.



of all in the middle (fig. 76). In front this process takes place with the greatest rapidity. The cells of the yolk-floor become continuously differentiated into hypoblast-cells, and very soon the whole of the front end becomes completely lined by true hypoblastic cells, while the yolk-cells become confined to the floor of the middle part.

The front portion of the mesenteron gives rise to the oesophagus, stomach and duodenum. Close to its hinder boundary there appears a ventral outgrowth, which is the commencement of the hepatic diverticulum (fig. 76, /). The yolk is thus post-hepatic, as in Vertebrates generally.

The stomodaeum is formed comparatively late by an epiblastic invagination (fig. 76, m).

It should be noticed that the conversion of the yolk-cells into hypoblast-cells to form the ventral wall of the anterior region of the alimentary tract is a closely similar occurrence to the formation of cells in the yolk-floor of the anterior part of the alimentary tract in Elasmobranchii. This conversion is apparently denied by Gotte, but since I find cells in all stages of transition between yolk-cells and hypoblast-cells I cannot doubt the fact of its occurrence.

At first, the mesenteron freely communicates with the exterior by the opening of the blastopore. The lips of the blastopore gradually approximate, and form a narrow passage on the dorsal side of which the neural tube opens, as has already been described (fig- 73)- The external opening of this passage finally becomes obliterated, and the passage itself is left as a narrow diverticulum leading from the hind end of the mesenteron into the neural canal (fig. 76). It forms the post-anal gut, and gradually narrows and finally atrophies. At its front border, on the ventral side, there may be seen a slight ventrally directed



m. mouth ; an. anus ; /. liver ; ne. neurenteric canal ; me. medullary canal ; ch. notochord ; pn. pineal gland.


diverticulum of the alimentary tract, which first becomes visible at a somewhat earlier stage (fig. 73). This diverticulum becomes longer and meets an invagination of the skin (fig. 76, an), which arises in Rana temporaria at a somewhat earlier period than represented by Gotte in Bombinator. This epiblastic invagination is the proctodaeum, and an anal perforation eventually appears at its upper extremity.

The differentiation of the hinder end of the prseanal gut proceeds in the same fashion as that of the front end, though somewhat later. It gives rise to the cloacal and intestinal part of the alimentary tract. From the ventral wall of the cloacal section, there grows out the bifid allantoic bladder, which is probably homologous with the allantois of the higher Vertebrata. After the differentiation of the ventral wall of the fore and hind ends of the alimentary tract has proceeded for a certain distance, the yolk only forms a floor for a restricted median region of the alimentary cavity, which corresponds to the umbilical canal of the Amniota. The true hypoblastic epithelium then grows over the outer side of the yolk, which thus constitutes a true, though small, and internal yolk-sack. The yolk-cells enclosed in this sack become gradually absorbed, and the walls of the sack form part of the intestine.

General growth of the Embryo.

Anura. The pyriform medullary plate, already described, is the first external indication of the embryo. This plate appears about the stage represented in longitudinal section in fig. 71 B. The feature most conspicuous in it at first is the axial groove. It soon becomes more prominent (fig. 77 A), and ends behind at the blastopore (bl\ the lips of which are continuous with the two medullary folds. As the sides of this plate bend upwards to form the closed medullary canal, the embryo elongates itself and assumes a somewhat oval form. At the same time the cranial flexure becomes apparent (fig. 73), and the blastopore shortly afterwards becomes shut off from the exterior. The embryo now continues to grow in length (fig. 77 B), and the mesoblast becomes segmented. The somites are first formed in the neck, and are added successively behind in





the unsegmented posterior region of the embryo. The hind end of the embryo grows out

into a rounded prominence, __ A ^ oc

which rapidly elongates, and becomes a well-marked tail entirely formed by the elongation of the post-anal section of the body. The whole body has a very decided dorsal flexure, the ventral surface being convex. Fig. 78 represents an embryo of Bombinator in side view, with the tail commencing to project. The longitudinal section (fig. 76) is taken through an embryo of about the same age. In the cephalic region important changes have taken place. The cranial flexure has become more marked, but


A. Young stage represented enclosed in the egg-membrane. The medullary plate is distinctly formed, but no part of the medullary canal is closed, bl. blastopore.

B. Older embryo after the closure of the medullary canal, oc, optic vesicle. Behind the optic vesicle are seen two visceral arches.


(After Gotte.)

a, mid-brain, a', eye; b. hind-brain; d. mandibular arch; if. Gasserian ganglion; e. hyoid arch ; e'. first branchial arch ; f, seventh nerve ; f, glossopharyngeal and vagus nerve; g. auditory vesicle; i. boundary between liver and yolk-sack ; k. suctorial disc; /. pericardial prominence; m, prominence formed by the pronephros.

is not so conspicuous a feature in the Amphibia as in most other types, owing to the small size of the cerebral rudiment. The mid-brain is shewn at fig. 78 a forming the termination of the



long axis of the body, and the optic vesicles (a'} are seen at its sides.

The rudiments of the mandibular (d), hyoid (e), and first branchial (e) arches project as folds at the side of the head, but the visceral clefts are not yet open. Rudiments of the proctodaeum and stomodaeum have appeared, but neither of them as yet communicates with the mesenteron. Below the hyoid arch is seen a peculiar disc (/) which is an embryonic suctorial organ, formed of a plate of thickened epiblast. There is a pair of these discs, one on each side, but only one a,

of them is shewn in the figure. At a later period they meet each other in the middle line, though they separate again before their final atrophy. They are found in the majority of the Anura, but are absent according to Parker in the Aglossa(PipaandDactylethra(fig.83)). They are probably remnants of the same primitive organs as the suctorial disc of Lepidosteus.

The embryo continues to grow in length, while the tail becomes more and more prominent, and becomes bent round to the side owing to the confinement of the larva within the egg-membrane. At the front of the head the olfactory pits become distinct. The stomodaeum deepens, though still remaining blind, and three fresh branchial arches become formed ; the last two being very imperfectly differentiated, and not visible from the exterior. There are thus six arches in all, viz. the mandibular, the hyoid and four branchial arches. Between the mandibular and the hyoid, and between each of the following arches, pouches of the mesenteron push their way towards the external skin. Of these pouches there are five, there



a. fold of epiblast continuous with the dorsal fin ; is*. neural cord ; m. lateral muscle ; as*, outer layer of muscle-plate; s. lateral plate of mesoblast ; b. mesentery ; tt. fold of the peritoneal epithelium which forms the segmental duct ; f. alimentary tract ; f. ventral diverticulum which becomes the liver; e. junction of yolkcells and hypoblast-cells ; d. yolk -cells.


being no pouch behind the last branchial arch. The first of these will form the hyomandibular cleft, the second the hyobranchial, and the third, fourth and fifth the three branchial clefts.

Although the pouches of the throat meet the external skin, an external opening is not formed in them till after the larva is hatched. Before this takes place there grow, in the majority of forms, from the outer side of the first and second branchial arches small processes, each forming the rudiment of an external gill ; a similar rudiment is formed, either before or after hatching, on the third arch; but the fourth arch is without it (figs. 80 and 82).

These external gills, which differ fundamentally from the external gills of Elasmobranchii in being covered by epiblast, soon elongate and form branched ciliated processes floating freely in the medium around the embryo (fig. 80).

Before hatching the excretory system begins to develop. The segmental duct is formed as a fold of the somatic wall at the dorsal side of the body cavity (fig. 79, u). Its anterior end alone remains open to the body cavity, and gives rise to a pronephros with two or three peritoneal openings, opposite to which a glomerulus is formed.

The mesonephros (permanent .kidney of Amphibia) is formed as a series of segmental tubes much later than the pronephros, during late larval life. Its anterior end is situated some distance behind the pronephros, and during its formation the pronephros atrophies.

The period of hatching varies in different larvae, but in most cases, at the time of its occurrence, the mouth has not yet become perforated. The larva, familiarly known as a tadpole, is at first enclosed in the detritus of the gelatinous egg envelopes. The tail, by the development of a dorsal and ventral fin, very soon becomes a powerful swimming organ. Growth, during the period before the larva begins to feed, is no doubt carried on at the expense of the yolk, which is at this time enclosed within the mesenteron.

The mouth and anal perforations are not long in making their appearance, and the tadpole is then able to feed. The gill slits also become perforated, but the hyomandibular diverticulum in most species never actually opens to the exterior, and in all cases becomes very soon closed.



There can be but little doubt that the hyomandibular diverticulum gives rise, as in the Amniota, to the Eustachian tube and tympanic cavity, except when these are absent (i.e. Bombinatoridye). Gotte holds however that these parts are derived from the hyobranchial cleft, but his statements on this head, which would involve us in great morphological difficulties, stand in direct contradiction to the careful researches of Parker.

Shortly after hatching, there grows out from the hyoid arch on each side an opercular fold of skin, which gradually covers over the posterior branchial arches and the external gills (fig. 80 d}. It fuses with the skin at the upper part of the gill arches, and also with that of the pericardial wall below them ; but is free in the middle, and so assists in forming a cavity, known as the branchial cavity, in which the gills are placed. Each branchial cavity at first opens by a separate widish pore behind


FIG. 80. TADPOLES WITH EXTERNAL BRANCHIAE. (From Huxley; after Ecker.)

A. Lateral view of a young tadpole.

B. Ventral view of a somewhat older tadpole.

kb. external branchiae; m. mouth; n. nasal sack; a. eye; o. auditory vesicle; z. horny jaws ; s. ventral sucker; d. opercular fold.

C. More advanced larva, in which the opercular fold has nearly covered the branchiae.

s. ventral sucker ; ks. external branchiae ; y. rudiment of hind limb.

(fig. 80), and in Dactylethra both branchial apertures are preserved (Huxley). In the larva of Bombinator, and it would seem also that of Alytes and Pelodytes, the original widish openings of the two branchial chambers meet together in the ventral line, and



form a single branchial opening or spiracle. In most other forms, i. e. Rana, Bufo, Pelobates, etc., the two branchial chambers become united by a transverse canal, and the opening of the right sack then vanishes, while that of the left remains as the single unsymmetrical spiracle. In breathing the water is taken in at the mouth, passes through the branchial clefts into the branchial cavities, and is thence carried out by the spiracle.

Immediately after the formation of the branchial cavities, the original external gills atrophy, but in their place fresh gills, usually called internal gills, appear on the outer side of the middle region of the four branchial arches.

There is a single row of these on the first and fourth branchial arches, and two rows on the second and third. In addition to these gills, which are vascular processes of the mesoblast, covered, according to Gotte, with an epiblastic (?) epithelium, branchial processes appear on the hypoblastic walls of the three branchial clefts. The lastnamed branchial processes would appear to be homologous with the gills of Lampreys. In Dactylethra no other gills but these are formed (Parker).

The mouth, even

before the tadpole begins to feed, acquires a transversely oval form (fig. 81), and becomes armed with provisional structures in the form of a horny beak and teeth, which are in use during larval life.



(After Gotte.)

Behind the mouth are placed the two suckers, and behind these are seen the gills projecting through the spiracles.

The beak is formed of a pair of horny plates moulded on the upper and lower pairs of labial cartilages. The upper valve of the beak is the larger of the two, and covers the lower. The beak is surrounded by a projecting lip formed of a circular fold of skin, the free edge of which is covered by papillse. Between the papilla; and the beak rows of horny teeth are placed on the inner surface of the lip. There are usually two rows of these on the upper side, the inner one not continuous across the middle line, and three or four rows on the lower side, the inner one or two divided into two lateral parts.


As the tadpole attains its full development, the suctorial organs behind the mouth gradually atrophy. The alimentary canal, which is (fig. 81) at first short, rapidly elongates, and fills up with its numerous coils the large body cavity. In the meantime, the lungs develop as outgrowths from the oesophagus.

Various features in the anatomy of the Tadpole point to its being a repetition of a primitive vertebrate type. The nearest living representative of this type appears to be the Lamprey.

The resemblance between the mouths of the Tadpole and Lamprey is very striking, and many of the peculiarities of the larval skull of the Anura, especially the position of the Meckelian cartilages and the subocular arch, perhaps find their parallel in the skull of the Lamprey 1 . The internal hypoblastic gill-sacks of the Frog, with their branchial processes, are probably equivalent to the gill-sacks of the Lamprey 2 ; and it is not impossible that the common posterior openings of the gill-pouches in Myxine are equivalent to the originally paired openings of the branchial sack of the Tadpole.

The resemblances between the Lamprey and the Tadpole appear to me to be sufficiently striking not to be merely the results of more or less similar habits ; but at the same time there are no grounds for supposing that the Lamprey itself is closely related to an ancestral form of the Amphibia. In dealing with the Ganoids and other types arguments have been adduced to shew that there was a primitive vertebrate stock provided with a perioral suctorial disc ; and of this stock the Cyclostomata are the degraded, but at the same time the nearest living representatives. The resemblances between the Tadpole and the Lamprey are probably due to both of them being descended from this stock. The Ganoids, as we have seen, also shew traces of a similar descent ; and the resemblance between the larva of Dactylethra (fig. 83), the Old Red Sandstone Ganoids 3 and Chimasra, probably indicates that an extension of our knowledge will bring to light further affinities between the primitive Ganoid and Holocephalous stocks and the Amphibia.

Metamorphosis. The change undergone by the Tadpole in its passage into the Frog is so considerable as to deserve the name of a metamorphosis. This metamorphosis essentially consists in the reduction and atrophy of a series of provisional embryonic organs, and the appearance of adult organs in their

1 Vide Huxley, " Craniofacial apparatus of Petromyzon." Journ. of Anat. and Phys. Vol. X. 1876. Huxley's views about the Meckelian arch, etc., are plausible, but it seems probable from Scott's observations that true branchial bars are not developed in the Lamprey. How far this fact necessarily disproves Huxley's views is still doubtful.

" Conf. Huxley and Gotte. a Cf. Parker (No. 107).



place. The stages of this metamorphosis are shewn in fig. 82, 5, 0, 7, 8.

The two pairs of limbs appear nearly simultaneously as small buds ; the hinder pair at the junction of the tail and body (fig. 82, 5), and the anterior pair concealed under the opercular membrane. The lungs acquire a greater and greater importance, and both branchial and pulmonary respirations go on together for some time.

FIG. 82. TADPOLES AND YOUNG OF THE COMMON FROG. (From Mivart. ) i. Recently-hatched Tadpoles twice the natural size. 2. Tadpole with external

gills. 20. Same enlarged. 3 and 4. Later stages after the enclosure of the gills

by the operailar membrane. 5. Stage with well-developed hind-limbs visible.

6. Stage after the ecdysis, with both pairs of limbs visible. 7. Stage after partial

atrophy of the tail. 8. Young Frog.

When the adult organs are sufficiently developed an ecdysis takes place, in which the gills are completely lost, the provisional horny beak is thrown off", and the mouth loses its suctorial form.


The eyes, hitherto concealed under the skin, become exposed on the surface, and the front limbs appear (fig. 82, 6). With these external changes important internal modifications of the mouth, the vascular system, and the visceral arches take place. A gradual atrophy of the tail, commencing at the apex, next sets in, and results in the complete absorption of this organ.

The long alimentary canal becomes shortened, and the, Jn the main, herbivorous Tadpole gradually becomes converted into the carnivorous Frog (fig. 82, 6, 7, 8).

The above description of the metamorphosis of the Frog applies fairly to the majority of the Anura, but it is necessary to notice a few of the more instructive divergences from the general type.

In the first place, several forms are known, which are hatched in the condition of the adult. The exact amount of metamorphosis which these forms pass through in the egg is still a matter of some doubt. Hylodes Martinicensis is one of these forms. The larva no doubt acquires within the egg a long tail ; but while Bavay 1 states that it is provided with external gills, which however are not covered by an operculum, Peters 2 was unable to see any traces of such structures.

In Pipa Americana, and apparently in Pipa dorsigera also if a distinct species, the larva leaves the cells on the back of the mother in a condition closely resembling the adult. The embryos of both species develop a long tail in the egg, which is absorbed before hatching, and according to Wyman 3 P. Americana is also temporarily provided with gills, which atrophy early.

The larva of Rhinoderma Darwinii is stated by Jiminez de la Espada to be without external gills, and it appears to be hatched while still in the laryngeal pouch of the male. In Nototrema marsupiatum the larvae are also stated to be without external gills.

Amongst the forms with remarkable developments Pseudis paradoxa deserves especial mention, in that the tadpole of this form attains an immensely greater bulk than the adult ; a peculiarity which may be simply a question of nutrition, or may perhaps be explained by supposing that the larva resembles a real ancestral form, which was much larger than the existing Frog.

Another form of perhaps still greater morphological interest is the larva of Dactylethra. The chief peculiarities of this larva (fig. 83) have been summarized by Parker (No. 107, p. 626), from whom I quote the following passage :

a. "The mouth is not inferior in position, suctorial and small, but is very wide like that of the ' Siluroids and Lophius ;' has an underhung lower

1 AnnaL de Sciences Nat., 5th Series, Vol. xvn., 1873.

2 Berlin. Monatsbericht, 1876, p. 703, and Nature, April 5, 1877.

3 Proceed, of Boston Nat. Hist. Society, Vol. v., 1854.


jaw, an immensely long tentacle from each upper lip, and possesses no trace of the primordial horny jaws of the ordinary kind.

b, "In conformity with these characters the head is extremely flat or depressed, instead of being high and thick.

FIG. 83. LARVA OF DACTYLETHRA. (After Parker.)

c. " There are no claspers beneath the chin.

d. " The branchial orifice is not confined to the left side, but exists on the right side also.

e. " The tail, like the skull, is remarkably chimaeroid ; it terminates in a long thin pointed lash, and the whole caudal region is narrow and elongated as compared with that of our ordinary Batrachian larvaa.

f. " The fore-limbs are not hidden beneath the opercular fold." Although most Anurous embryos are not provided with a sufficient

amount of yolk to give rise to a yolk-sack as an external appendage of the embryo, yet in some forms a yolk-sack, nearly as large as that of Teleostei, is developed. One of these forms, Alytes obstetricans, belongs to a wellknown European genus allied to Pelobates. The embryos of Pipa dorsigera (Parker) are also provided with a very large yolk-sack, round which they are coiled like a Teleostean embryo. A large yolk-sack is also developed in the embryo of Pseudophryne australis.

The actual complexity of the organization of different tadpoles, and their relative size, as compared with the adult, vary considerably. The tadpoles of Toads are the smallest, Pseudophryne australis excelling in this respect ; those of Pseudis are the largest known.

The external gills reach in certain forms, which are hatched in late larval stages, a very great development. It seems however that this development is due to these gills being especially required in the stages before hatching. Thus in Alytes, in which the larva leaves the egg in a stage after the loss of the external gills, these structures reach in the egg a very great development. In Notodelphis ovipara, in which the eggs are carried in a dorsal pouch of the mother, the embryos are provided with long vesicular gills attached to the neck by delicate threads. The fact (if confirmed) that some of the forms which are not hatched till post-larval stages are without external gills, probably indicates that there may be various contrivances for embryonic respiration 1 ; and that the external gills only attain a great development in

1 In confirmation of this view it may be mentioned that in Pipa Americana the tail appears to function as a respiratory organ in the later stages of development (Peters).


those instances in which respiration is mainly carried on by their means. The external gills of Elasmobranchii are probably, as stated in a previous chapter, examples of secondarily developed structures, which have been produced by the same causes as the enlarged gills of Alytes, Notodelphis, etc.

Urodela. Up to the present time complete observations on the development of the Urodela are confined to the Myctodera 1 .

The early stages are in the main similar to those of the Anura. The body of the embryo is, as pointed out by Scott and Osborn, ventrally instead of dorsally flexed. The metamorphosis is much less complete than in the Anura. The larva of Triton may be taken as typical. At hatching, it is provided with a powerful swimming tail bearing a well-developed fin : there are three pairs of gills placed on the three anterior of the true branchial arches.

Between the hyoid and first branchial arch, and between the other branchial arches, slits are developed, there being four slits in all. At the period just before hatching, only three of these have made their appearance. The hyomandibular cleft is not perforated. Stalked suckers, of the same nature as the suckers of the Anura, are formed on the ventral surface behind the mouth. A small opercular fold, developed from the lower part of the hyoid arch, covers over the bases of the gills. The suctorial mouth and the provisional horny beak of the Anura have no counterpart in these larvae. The skin is ciliated, and the cilia cause a rotation in the egg. Even before hatching, a small rudiment of the anterior pair of limbs is formed, but the hindlimbs are not developed till a later stage, and the limbs do not attain to any size till the larva is well advanced. In the course of the subsequent metamorphosis lungs become developed, and a pulmonary respiration takes the place of the branchial one. The branchial slits at the same time close and the branchiae atrophy.

The other types of Myctodera, so far investigated, agree fairly with the Newt.

The larva of Amblystoma punctatum (fig. 84) is provided with two very

1 The recent observations on this subject are those of Scott and Osborn (No. 114) on Triton, of Bambeke (No. 95) on various species of Triton and the Axolotl, and of Clark (No. 98) on Amblystoma punctatum.




long processes (j), like the suctorial processes in Triton, placed on the throat in front of the external gills. They are used to support the larva when it sinks to the bottom, and have been called by Clarke (No. 98) balancers. On the development of the limbs, these processes drop off. The external gills atrophy about one hundred days after hatching.

It might have been anticipated that the Axolotl, being a larval form of Amblystoma, would agree in development with Amblystoma punctatum. The conspicuous suctorial processes of the latter form are however represented by the merest rudiments in the Axolotl.

The young of Salamandra maculata leave the uterus with external gills, but those of the Alpine Salamander (Salamandra atra) are born in the fully developed condition without gills. In the uterus they pass through a metamorphosis, and are provided (in accordance with the principle already laid down) with very long gill-filaments 1 .

Salamandra atra has only two embryos, but there are originally

a larger number of eggs (Von Sie,,,,,.,.,,. f ., .

bold), of which all but two fail to

develop, whi,e their remains are

used as pabulum by the two which

survive. Both species of Sala mander have a sufficient quantity of food-yolk to give rise to a


Spelerpes only develops three post-hyoid arches, between which slits are formed as in ordinary types. Menobranchus and Proteus agree with Spelerpes in the number of post-hyoid arches.

One of the most remarkable recent discoveries with reference to the metamorphosis of the Urodela was made by Dumeril 2 . He found that some of the larvae of the Axolotl, bred in the Jardin des Plantes, left the water, and in the course of about a fortnight underwent a similar metamorphosis to that of the Newt, and became converted into a form agreeing in every

1 Allen Thomson informs me that the crested Newt, Triton cristatus, is in rare instances viviparous.

- Comptes RenJits, 1870. 11.782.




particular with the American genus Amblystoma. During this metamorphosis a pulmonary respiration takes the place of a branchial one, the gills are lost, and the gill slits close. The tail loses its fin and becomes rounded, the colour changes, and alterations take place in the gums, teeth, and lower jaw.

Madame von Chauvin 1 was able, by gradually accustoming Axolotl larvae to breathe, artificially to cause them to undergo the above metamorphosis.

It seems very possible, as suggested by Weismann 2 , that the existing Axolotls are really descendants of Amblystoma forms, which have reverted to a lower stage. In favour of this possibility a very interesting discovery of Filippi's 3 may be cited. He found in a pond in a marsh near Andermat some examples of Triton alpestris, which, though they had become sexually mature, still retained the external gills and the other larval characters. Similar sexually mature larval forms of Triton taeniatus have been described by Jullien. These discoveries would seem to indicate that it might be possible artificially to cause the Newt to revert to a perennibranchiate condition.

Gymnophiona. The development of the Gymnophiona is almost unknown, but it is certain that some larval forms are provided with a single gill-cleft, while others have external gills.

A gill-cleft has been noticed in Epicrium glutinosum (Miiller), and in Ccecilia oxyura. In Ccecilia compressicauda, Peters (No. 108) was unable to find any trace of a gill-cleft, but he observed in the larvae within the uterus two elongated vesicular gills.


(93) Ch. van Bambeke. " Recherches sur le developpement du Pelobate brun." Memoires couronnes, etc. de F Acad. roy. de Belgique, 1868.

(94) Ch. van Bambeke. "Recherches sur 1'embryologie des Batraciens." Bulletin de I'Acad. roy. de Belgique, 1875.

(95) Ch. van Bambeke. " Nouvelles recherches sur 1'embryologie des Batraciens." Archives de Biologie, Vol. I. 1880.

(96) K. E. von Baer. " Die Metamorphose des Eies der Batrachier." Muller's Archiv, 1834.

(97) B. Benecke. " Ueber die Entwicklung des Erdsalamanders. " Zoologischer Anzeiger, 1880.

1 Zeit.f. wiss. ZooI.,"Bd.. xxvn. 1876.

2 Zeit.f. wiss. Zool., Bd. xxv. sup. 1875.

3 Archivio per la Zoologia, /' Anatomia e la Fisiologia, Vol. I. Genoa, 1861. Conf. also Von Siebold, " Ueber die geschlechtliche Entwicklung d. Urodelen-Larven." Zeit.f. wiss. Zool., Bd. xxvm., 1877.


(98) S. F. Clarke. "Development of Amblystoma punctatum," Part I., External. Studies from the Biological Laboratory- of the Johns Hopkins University, No. II. 1880.

(99) H. Cramer. "Bemerkungen lib. d. Zellenleben in d. Entwick. d. Froscheies." Mullcr's Archiv, 1848.

(100) A. Ecker. Icones Physiolog. 1851 1859.

(101) A. Gotte. Die Entwicklungsgeschichte der Unke. Leipzig, 1875.

(102) C. K. Hoffmann. "Amphibia." Klassen u. Ordnungen d. T/iierreicks, 18731879.

(103) T. II. Huxley. Article "Amphibia" in the Encyclopedia Britannica.

(104) A. Moquin-Tandon. "Developpement des Batraciens anures." Annales des Sciences Naturelles, III. 1875.

(105) G. Newport. " On the impregnation of the Ovum in Amphibia " (three memoirs). Phil. Trans. 1851, 1853, and 1854.

(106) W. K. Parker. " On the structure and development of the Skull of the common Frog." Phil. Trans., CLXI. 1871.

(107) W. K. Parker. "On the structure and development of the Skull of the Batrachia." Phil. Trans., Vol. CXLVI., Part a. 1876.

(108) W. C. H. Peters. " Ueber die Entwicklung der Coecilien und besonders von Coecilia compressicauda." Berlin Monatsbericht, p. 40, 1874.

(109) W. C. H. Peters. "Ueber die Entwicklung der Coecilien." Berl. Monatsbericht , p. 483, 1875.

(110) J. L. Prevost and J. B. Dumas. " Deuxieme Mem. s. 1. generation. Developpement de 1'ceuf d. Batraciens." Ann. Sci. Nat. II. 1824.

(111) R. Remak. Untersuchungen iiber die Entwicklung der Wirbelthiere, 18501858.

(112) M. Rusconi. Developpement de la grenouille commune depttis le moment de sa naissance jusqu 'd son (tat parfait, 1826.

(113) M. Rusconi. Histoire naturelle, developpement et metamorphose de la Salamandre terrestre, 1854.

(114) W. B. Scott and H. F. Osborn. "On the early development of the common Newt." Quart. J. of Micr. Science, Vol. xxix. 1879.

(115) S. Strieker. "Entwicklungsgeschichte von Bufo cinereus." Sitzb. der kaiserl. Acad. zu Wien, 1860.

(116) S. Strieker. "Untersuchungen liber die ersten Anlagen in BatrachierEiern." Zeitschrift f. wiss. Zoologie, Bd. xi. 1861.