Vertebrate Embryology - A Text-book for Students and Practitioners (1893) 3

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Marshall AM. Vertebrate Embryology: A Text-book for Students and Practitioners. (1893) Elder Smith & Co., London.

   Vertebrate Embryology 1893: 1 Introduction | 2 Amphioxus | 3 Frog | 4 Chick | 5 The Rabbit | 6 Human Embryo | Illustrations
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Contents

Chapter III. The Development of the Frog

Frogs belong to the class Amphibia, of which toads, newts. and salamanders are other well-known members, while less familiar examples are afforded by the axolotl of Mexico, the Proteus of the caves of Carniola and Dalmatia, the cryptobranch of Japan, which attains a length of three feet or more, and the curious snake-like Coecilia of tropical countries.

As a group, Amphibia are characterised more especially by the double nature of their breathing organs. When adult, they all have lungs ; but in the early stages of almost all genera, and throughout life in a large number, true gills are present, corresponding in structure and in mode of use to those of fish.

In the frog itself these gills are only present during the early, or tadpole, period of existence ; in the later stages they are replaced functionally by lungs, and in the adult they have disappeared completely. The frog is thus, in the course of its own life history, transformed from a water-breathing to an airbreathing animal ; and, in accordance with the principle of Recapitulation explained in the introductory chapter, this transformation is to be interpreted as indicating that frogs are descended from fish-like ancestors, each frog in its own development repeating the ancestral history.

The frog thus holds a position midway between Fish and the higher Vertebrates ; and as frog's eggs can readily be obtained in large numbers, and the embryos and tadpoles develop well in captivity, the frog becomes a very convenient and instructive 'form for practical laboratory study.

--General Account of the Development of the Frog==

Frogs' eggs are laid in water, usually during March or the early part of April.

During the act of oviposition, which may last several days, the male frog clasps the female firmly, embracing her with his arms ; and as the eggs are passed out from the cloaca of the female into the water, they are fertilised by spermatozoa discharged over them by the male.

The eggs, which are very numerous, are small spherical bodies about 1'75 mm. in diameter; they are invested by thin coatings of an albuminous substance, which swell up very greatly in the water, and stick together to form the bulky masses we call frog's spawn. Such spawn consists of a transparent gelatinous mass, formed by the swollen albuminous matter, in which the eggs are embedded ; these latter appear as small spherical bodies, each presenting a black half and a white half.

If a number of hen's eggs were broken into a basin, care being taken not to rupture the yolks, a mass would be produced similar to frog's spawn ; the yellow yolks corresponding to the frog's eggs, and the whites or albuminous investments of the yolks to the gelatinous matrix of the spawn.

The frog's eggs, laid in this way, and fertilised by spermatozoa shed over them by the male, begin to develop at once. The rate of development depends very largely on the temperature, and varies within very wide limits, warmth hastening development, and cold retarding it. Freezing of the water in which the eggs are kept merely retards development, and does not injure the eggs, provided the eggs themselves are not actually frozen. The times mentioned in this chapter may be taken as representing the average rate of development in this country.

Each egg is at first spherical, and remains so during the early stages of development ; at the close of segmentation it becomes slightly ovoid, and then rapidly increases in length. A transverse constriction appears, separating the head from the trunk, and the tail buds out as a small process from the hinder end of the embryo. The embryo soon becomes fish-like in appearance, the tail growing veiy rapidly ; two pairs of branching tufts, the external gills, followed shortly by a third pair, grow out from the sides of the neck, and in about a fortnight from the time of laying of the eggs the young tadpoles, now about 7 mm. in length, wriggle their way out of the gelatinous mass of the spawn, and swim freely in the water (Fig. 44, 3, 4).


At the time of hatching, the cloacal opening is already present ; but the tadpole has no mouth, and is dependent for nutrition, as it has been during all the earlier stages, on the granules of food-yolk contained in the egg itself. A horse-shoe shaped sucker is present on the under surface of the head, by which the tadpole attaches itself, at first to the gelatinous mass of the spawn, and later on to weeds or other objects in the water.

A few days after hatching, the mouth appears, bordered by a pair of horny jaws, and fringed with fleshy lips studded with horny papillas. The alimentary canal, which has hitherto been short and wide, rapidly increases in length, becoming tubular and convoluted ; the liver and pancreas are formed ; and the tadpole feeds eagerly on confervas and other plants, especially 011 decomposing vegetable matter.

About the time of appearance of the mouth, i.e. shortly after hatching, a series of four slit-like openings, the gill-clefts, appear on each side of the neck, leading from the phaiynx to the exterior. The margins of the slits become folded, and form the internal gills ; the external gills at the same time decreasing in size and becoming shrivelled in appearance.

While the internal gills are developing, a fold of skin, the operculum, appears on each side of the head, in front of the gills. The two opercular folds, Avhich soon become continuous with each other across the ventral surface of the head, grow backwards over the gills so as to inclose them in gill-chambers. Towards the end of the fourth week, the hinder edges of the opercular folds fuse with the body wall along the right side and across the ventral surface of the head. On the left side a spout-like opening remains, which communicates with the gillchambers of both sides ; through this opening the water, taken in at the mouth for respiration, and passed out through the gillslits, makes its escape to the exterior (cf. Fig. 83).

During this time the tadpole has been feeding freely, and has greatly increased in size. The body (Fig. 44, 8) is broad and round ; the tail is much larger than before, and forms a powerful swimming organ ; while the sucker on the under surface of the head, though still present, is small, and divided into two separate halves ; and is but little used.

Very shortly afterwards, rudiments of the hind limbs can be seen as a pair of small papillae at the root of the tail, one on each side of the cloacal opening (Fig. 71); the limbs increase steadily in size ; about the seventh week they become divided into joints, and a week or so later the toes appear. The fore limbs arise about the same time as the hind limbs, but are covered by the opercular folds, and hence do not become visible until a later stage (Figs. 84 and 85, LA).

Towards the end of the second month the lungs come into use, and the tadpoles, which now have the form shown in Fig. 44, 9 and 10, frequently come to the surface of the water to breathe. The gills begin to degenerate, but for some time respiration is carried on both by the gills and the lungs.



FIG. 44. Various stages in the development of the Frog. (From Brehm's ' Thierleben.')

1, eggs just laid. 2, eggs shortly after laying. 3, tadpole shortly before hatching. 4, tadpoles just' hatched. 5 and 6, tadpoles with external gills. 7' and 8, tadpoles with fully formed opercular folds. 9 and 10, tadpoles with we l-developed hind legs, shortly before the metamorphosis. 11, tadpole during the metamorphosis. 12, young frog witli tail only partially absorbed.


A fortnight or three weeks later a distinct metamorphosis occurs, whereby the tadpole becomes transformed, from the fishlike condition in which it has hitherto been, to the purely airbreathing state characteristic of the adult. The tadpole ceases to feed ; a casting, or ecdysis, of the outer layer of the skin takes place; the horny jaws are thrown off; the large frilled lips shrink up ; the mouth loses its rounded suctorial form and becomes much wider; the tongue, previously small, increases considerably in size. The eyes, which as yet have been small, become larger and more prominent. The fore-limbs appear, the left one being pushed through the spout-like aperture of the gill-chamber, and the right one forcing its way through the opercular fold, in which it leaves a ragged hole. The abdomen shrinks ; the stomach and liver enlarge, but the intestine becomes considerably shorter than befoi'e, and of smaller diameter ; the animal, previously a vegetable feeder, now becomes carnivorous. The gill-clefts close up ; the gills themselves are gradually absorbed ; and important modifications, accompanying the change in the mode of breathing, occur in the blood-vessels of the pharynx. The kidneys undergo considerable changes ; the bladder is formed ; and sexual differentiation is definitely established. The tail, which is still of great length (Fig. 44, n), now begins to shorten, and is soon completely absorbed ; the hind legs lengthen considerably, and the animal leaves the water as a frog.

By preventing tadpoles from breathing air directly, as by placing a wire net an inch or so below the surface of the water in which they are living, the occurrence of the metamorphosis can be indefinitely deferred. Under these conditions tadpoles increase greatly in size, but do not become transformed into frogs.

In the remainder of this chapter the several stages in the development of the tadpole, and the formation of the various organs and systems, will be described in detail.

The Frog's Egg

1. Formation of the Egg.

The early stages in the formation of the eggs cannot be seen in the adult frog, but must be studied in tadpoles.

In tadpoles of about 10 mm. length, shortly after the opening of the mouth, a pair of longitudinal ridge-like thickenings of the peritoneum appear along the dorsal surface of the body cavity, close to the root of the mesentery. These genital ridges are found in all tadpoles alike, no difference of sex being established until a considerably later period.

Each genital ridge is at first due merely to a modification in shape of the peritoneal epithelial cells, which, elsewhere flattened, become here cubical or slightly columnar. The ridges soon become more prominent, especially at their anterior ends, their growth being due, partly to increase of the epithelial cells by repeated division, the epithelial layer becoming several cells thick ; and partly to ingrowth of an axial core of connective tissue, from the basal membrane of the peritoneum, along which blood-vessels gain access to the ridge. The anterior third of each genital ridge undergoes degenerative changes at an early period (Figs. 85, 86), and ultimately becomes the fat body of the adult ; the posterior two-thirds develop into the reproductive organ, OR.

At an early stage, certain of the epithelial cells of the genital ridge become conspicuous by their larger size and more spherical shape ; these are the primitive ova or gonoblasts. Eound each primitive ovum the neighbouring cells become arranged so as to form a capsule or follicle ; the follicles forming distinct projections on the surface of the genital ridge. New primitive ova are formed from the surface epithelium, and also by division of those already present ; they, also, soon become inclosed in follicles formed by the neighbouring cells.

Sexual differentiation appears at the time of the metamorphosis. In the female, the changes consist essentially in a great increase in the size of the genital ridges, which now become the ovaries, and in the number of the contained follicles ; and in the formation of the permanent ova or eggs. The permanent ova are formed from the primitive ova, but different accounts have been given of the details of the process, and it is possible that they are not the same in all cases. As a rule, each primitive ovum divides rapidly to form a nest of cells, one of which becomes a permanent ovum, while the rest form part of the follicle which surrounds it, and serves for its protection and nutrition. In other cases it is stated that a primitive ovum may become directly converted into a permanent ovum.

The permanent ovum, in whatever manner it is formed, differs from the primitive ovum : (i) in its much greater size ; (ii) in possessing a very large vesicular nucleus, or germinal vesicle ; and (iii) in containing a number of yolk-granules, imbedded in the protoplasm of its cell-body.

The egg nucleus, or germinal vesicle, is a spherical capsule, with a diameter of from one-third to half that of the ovum itself.


It consists of a thick elastic nuclear membrane, apparently perforated by fine radial pores, and inclosing a watery nuclear fluid ; the latter is traversed by a finely granular protoplasmic network, enlarged at the nodes to form nucleoli, or germinal spots, of which one is usually larger than the others.


The yolk granules are small, sharply defined, spherical or ovoidal, yellowish particles of food-substance, which are elaborated by the follicle cells and passed on from them into the ovum. They are confined to the protoplasm of the cell-body, not penetrating into the nucleus. They increase rapidly in number as the egg approaches maturity, and it is to them that the size of the egg as well as its opacity are chiefly due.

When the egg has attained a diameter of about 0'5 mm. an exceedingly thin structureless investment, the vitelline membrane, is formed immediately around it, and within the follicle. The mode of origin of the vitelline membrane is not clearly made out, but it seems to be formed from the egg itself rather than from the follicular epithelium.

A little later, and as the egg is approaching its full size, a layer of black pigment appears on its surface ; this is at first irregularly distributed over the whole surface, but, as the egg ripens, the pigment becomes restricted to one half or hemisphere, and the distinction between the white and black poles of the egg is thus established. The pigment is contained, and apparently formed, within the egg itself ; but it is not clear how it is formed, or what purpose it fulfils. The facts, that the pigment is confined to the pole of the egg which develops most rapidly, and that warmth greatly increases the rate of development, suggest that the pigment may facilitate development by promoting the absorption of heat.

2. Maturation of the Egg

Our knowledge of the phenomena accompanying the maturation of the frog's egg is based almost entirelv on the researches of O. Schultze, and is still in many respects imperfect. An account of these changes has already been given in the introductory chapter, but will be repeated here in order that the developmental history of the frog may be given as fully as practicable.

The process of ripening or maturation commences in an egg while it is still in the ovary, shortly before it reaches its full size, and the successive stages are shown in Fig. 45.

The whole nucleus shrinks considerably, becoming reduced to less than half its former diameter. This shrinking is accompanied by exudation of part of the nuclear fluid, through the nuclear membrane, into the protoplasm of the cell-body (Fig. 45, A, UH), where it forms a fluid layer surrounding the nucleus: at the same time the nuclear membrane becomes wrinkled, its surface, which was previously smooth, becoming raised into little wart-like projections, so as to present an appearance something like a blackberry (Fig. 45, A) Within the nucleus a number of the larger chromatiii granules, or nucleoli, remain close to the nuclear membrane, often lying within the wart-like protuberances ; a number of others, chiefly smaller ones, collect towards the centre, where they surround a clear region in which lie a number of exceedingly minute chromatin granules. These latter are at first scattered irregularly, but soon run together to form moniliform threads of extreme slenderness, which interlace and unite to form a minute nuclear skein (Fig. 45, A).

About the time of discharge of the egg from the ovary further changes occur, which are apparently stimulated by the act of copulation. The nuclear membrane disappears completely ; and its contents, the nuclear fluid and nucleoli, become distributed through the yolk. The only part of the egg nucleus which persists is the minute nuclear skein : this moves towards the surface of the egg, and takes up a position at the upper or black pole of the egg, immediately below its surface (Fig. 45, B) ; here it lies in a lenticular patch, which is rather more fluid and more transparent than the rest of the yolk, and is separated from this by an ill-defined capsule of pigment, prolonged towards the centre of the egg in the manner shown in the figure.

The nuclear skein (Fig. 45, B, UG), now assumes a spindle form, and lies at first with its long axis tangential to the surface of the egg. Shortly afterwards the spindle turns so that its axis becomes radially situated, one of its poles being at the surface of the egg, and the other directed towards the interior ; it then divides transversely into two parts, of which one (Fig. 45, C, UG), remains within the egg, while the other (Fig. 45, C, PB), is extruded as the first polar body. Shortly before the formation of the polar body the black pole of the egg becomes slightly flattened, leaving a space between the egg and the vitelline membrane (Fig. 45, C) ; this space is occupied at once by a perivitelline fluid, exuded from the egg, and in this fluid the polar body may be seen as a minute ovoidal white body, usually lying in a small depression on the surface of the egg (Fig. 45, C, PB).



FIG. 45. Successive stages in the maturation of the egg of the Frog. The eggs are represented as bisected vertically, x 25. (After O. Schultze.)

A, stage in which the nucleus has commenced to shrink, and the nuclear skein is formed in its centre. B> stage in which the nuclear skein has moved to the surface of the egg, just prior to the formation of the first polar body. C> stage in which the first polar body has been formed, by division of the nuclear skein, and extruded. D. stage in which the second polar body has been extruded, and the remaining part of the nuclear skein, or female pronucleus, has retreated from the surface of the egg, and is about to unite with the male pronucleus or head of the spermatozoon.

PB, first polar body. PB', second polar body. TJF, female pronucleus. UG, egg nucleus, or germinal vesicle. TJH, peri-vitelline fluid exuded from germinal vesicle. TJM, male pronucleus. Z, vitelline membrane.


The formation of the second polar body in the frog has not been seen, but there can be little doubt that it is due, as in other animals, to a farther division of the part of the nuclear spindle which remains within the egg, after extrusion of the first polar body. According to Schultze, the extrusion of the second polar body from the egg does not take place until about half an hour after fertilisation of the egg ; i.e. after the entrance of the spermatozoon, but before the completion of the act of fertilisation.

The two polar bodies are of about equal size ; they lie freely on the yolk, in the peri-vitelline fluid, and shift about with this latter if the eggs are rotated.

3. Laying of the Eggs

The eggs when ripe are discharged from the ovary, and fall into the body cavity ; along this they pass forwards, directed partly by contraction of the muscular body walls, partly by the action of the cilia of the peritoneum, to the mouths of the oviducts, which are situated at the extreme anterior end of the body cavity, opposite the roots of the lungs. Within the first or thick-walled part of the oviduct the eggs acquire gelatinous investments secreted by glands in its walls : the terminal part of each oviduct is a thin-walled pouch, capable of great distension, within which the eggs accumulate in large numbersFinally, at the time of copulation, the eggs are passed out through the cloacal opening into water, in which the albuminous investments of the eggs speedily swell up to form the gelatinous mass of the frog's spawn.


4. Fertilisation of the Egg

The spermatozoa, after being shed over the spawn by the male frog, swim actively by means of their long tails, work their way into the gelatinous mass of the spawn, bore through the vitelline membranes, and so penetrate into the eggs themselves, which they enter at, or close to, their upper or black poles.

A single spermatozoon is sufficient to fertilise an egg, and it is doubtful whether more than one is ever concerned in the process. About an hour after the spermatozoon has entered, a pigmented process may be seen projecting into the egg from the point of entry (Fig. 45, D), and in the centre of the process a clear spot. This spot (Fig. 45, D, UM), is the nucleus ofthe spermatozoon, or male pronucleus ; it penetrates further into the egg, carrying the pigment with it, and soon meets the female pronucleus, or part of the nuclear skein which remains within the egg after extrusion of the two polar bodies.

The two pronuclei come into close contact with each other, and, after having increased considerably in size, fuse together to form the segmentation nucleus. This fusion, which occurs about two and a half hours after the spermatozoon first entered the egg, completes the act of fertilisation.

Almost immediately after the spermatozoon enters the egg a considerable extrusion of peri-vitelline fluid takes place, between the egg and the vitelline membrane (Figs. 45, C and D). This separates the egg from the vitelline membrane, and greatly facilitates the rotation of the egg within the membrane ; from this time, in whatever position the spawn be placed, the black poles of the eggs will always, from their less specific gravity, be uppermost, and the white poles, which are of higher specific gravity owing to the greater abundance of yolk-granules in them, will be undermost. The extrusion of the peri-vitelline fluid, and the consequent separation of the egg from the vitelline membrane, may possibly serve further to prevent or hinder the entrance of a second spermatozoon.


The Early Stages of Development of the Frog's Egg

1. Segmentation of the Egg

Segmentation of the frog's egg is, like that of Amphioxus, a process of cell-division ; but although the processes in the two animals are essentially similar, there are important differences in detail, due to the much larger amount of food-yolk present in the egg of the frog, and its unequal distribution.

Food-yolk consists of small granules of highly nutritious matter, imbedded in the substance of the egg ; but although it forms a store of readily assimilated'nutriment, at the expense of which the development of the embryo can be effected, it must be remembered that until it has been so assimilated the yolk granules will be foreign bodies, and, like any other foreign bodies, will be a hindrance rather than an aid to development. The direct influence of food-yolk is to mechanically impede the activity of the protoplasm in which it is imbedded, acting in exactly the same way as so many grains of sand or other foreign matter would do, and actually checking the processes of development.

The frog's egg is a telolecithal egg ; i.e. one in which the foodyolk is not uniformly distributed throughout the yolk, being more abundant in the lower or white hemisphere than in the upper or black one. The passage from one pole to the other is a gradual, not an abrupt one ; there is no line of demarcation between the two ; still, the black pole is much less encumbered with food-yolk than the white or lower pole, and it is to this fact that the relatively rapid development of the black pole is due. Very shortly after the completion of the act of fertilisation and the formation of the segmentation nucleus, this latter loses its spherical form and becomes spindle-shaped, the yolk granules at the same time showing a tendency to arrange themselves along lines radiating outwards from the ends of the spindle.



FIGS. 46, 47, and 48. Segmentation of the Frog's Egg. x 20.

Fig. 46. The egg just before the completion of the first cleft, by which it is divided into two equal blastomeres : the egg is represented in vertical section.

Fig. 47. A surface view of an egg at the completion of the third cleft : the egg is now divided into eight blastomeres, an upper tier of four small ones, and a lower tier of four much larger ones.

Fig. 48. A vertical section of an egg at the same stage as Fig. 47. In the middle, between the inner ends of the blastomeres, is the commencing segmentation cavity. If.


The nucleus now divides into two halves, which move away from each other ; the yolk granules tend to aggregate themselves around the two nuclei, and a thin vertical plate of finely granular protoplasm, almost free from yolk granules, is left, dividing the egg into two halves. This plate, which soon becomes pigmented, splits vertically into two, the split appearing near the centre of the egg, and at first not reaching to its surface.

At the upper or black pole of the egg a depression now appears, at first as a small pit, and then elongating to form a groove, which rapidly extends all round the egg. The groove deepens, and, meeting with the split already present in the interior of the egg (Fig. 46), divides the whole egg into two completely separate and equal parts, the plane of division corresponding with the vertical pigmented plane mentioned above.

This first plane of division is stated to correspond to the median sagittal plane of the future embryo and adult ; i.e. the two cells into which the egg is divided by the first segmentation plane are said to correspond respectively to the right and left halves of the body of the frog.

Each of the two nuclei soon becomes spindle-shaped, and then divides into two ; and a second cleft is then formed in a similar manner to the first. This second cleft is also a vertical one, but in a plane at right angles to the first one ; on its completion the egg is divided into four similar and equal cells, or blastomeres.

The third cleft is horizontal, but not equatorial, lying (Fig. 47) much nearer the upper than the lower pole. It divides each of the four cells or blastomeres into two, an upper smaller and a lower larger one.

From this stage segmentation proceeds rapidly, but according to no definite rule, the several cells dividing independently of one another. Throughout the process the upper cells divide more rapidly, and are consequently always of smaller size than the lower cells, the latter being hampered by the large number of yolk-granules they contain : in all cases division of the cells is preceded by division of their nuclei, as in the earlier stages.


At the stage represented by Figs, 47 and 48, when eight cells are present, i.e. on the completion of the third cleft, a small cavity appears in the centre of the egg, between the inner ends of the cells (Fig. 48). This is the segmentation cavity or blastocoel. From its first appearance it is situated nearer the upper than the lower pole of the egg. It is filled with fluid, and during the later phases of segmentation it increases considerably in size (Figs. 49, 50).

At the close of segmentation the egg has the structure shown in section in Fig. 50. It is a hollow ball, the same size as the original ovum, with a small, excentrically-placed cavity, and with walls of very unequal thickness. The cells of the upper half are small, approximately uniform in size, and arranged more or less definitely in two layers, outer and inner ; while the cells of the lower half are larger, and much more irregular in shape, size, and arrangement : furthermore, the superficial cells of the upper half are deeply pigmented at their outer ends, while those of the lower half are nearly colourless.



FIG. 49. The blastula stage in the development of the Frog's Egg, bisected vertically, x 20. FIG. 50. The Frog's Egg at the close of segmentation, bisected vertically. x20.

B, segmentation cavity or blastocoel.


The distinction between upper and lower cells is, however, not an absolute one, the cells at the equator being intermediate in all respects between those of the upper and lower poles.

The stage represented in Fig. 49 is the one which corresponds most closely with the blastula stage of Amphioxus (Fig. 14, vm). There are, however, important differences between the two. In the blastula stage of the frog there are fewer component cells ; the cells differ more markedly from one another in shape and size ; and the segmentation cavity is much smaller relatively to the entire ovum, and is excentric instead of central in position. From the description given above it will be seen that all these differences may be attributed to the greater amount of food-yolk present in the frog's egg.

2. The Epiblast

Of the two kinds of cells of which the egg consists at the close of segmentation (Fig. 50), the smaller pigmented cells of the upper half are the epiblast cells, while the larger unpigmented cells of the lower half, in which the yolk-granules are mainly contained, may be spoken of as the lower layer cells or yolk-cells.


FIG. 51. Median sagittal section of a Frog Embryo, showing the spreading of the epiblast and the commencing formation of the mesenteron. x 25.

B, blastocoel or segmentation cavity. BP, lip of blastopore. EE, outer or epidermic layer of epiblast. EN", inner or nervous layer of epiblast. Y, lower layer or yolk cells.

The distinction between the two is not an absolute one, the cells at the equator of the egg being intermediate in all respects between the epiblast and the yolk-cells. As seen from the surface, the limit is indicated by the boundary line between the black and the white areas of the egg, and at the close of segmentation these two areas are approximately equal in extent. In the succeeding stages the black area increases rapidly at the expense of the white area (Figs. 51, 52, 54), and in a few hours the pigmented epiblast cells have covered the whole of the egg with the exception of a small circular patch at the lower pole (Figs. 52, Y, and 54 YP), where alone the white yolk-cells come to the surface.

This extension of the epiblast occurs all round its margin, and is effected by the addition of cells cut out from the superficial layer of yolk-cells. This superficial layer first becomes pigmented, and then divides into, (i) a surface stratum of small epiblast cells, which from the first are similar to the original epiblast cells, and are added on round their margin ; and (ii) a deeper mass of larger and non-pigmented yolk-cells.

During this extension of the epiblast, the process of cell division has been continuing rapidly in all parts of the embryo. The epiblast now consists of two very definite layers of cells : an outer or epidermic layer (Fig. 51, EE), formed by a single stratum of short columnar cells, which are deeply pigmented, and packed close together side by side ; and an inner or nervous layer (Fig. 51, EN), consisting of smaller, more spherical cells, less strongly pigmented than those of the epidermic layer, and arranged two or three deep. The cells that are added on round the margin of the epiblast, during its spreading, are similar in shape and size to the epiblast cells derived from the upper pole of the egg, and, like these, soon become arranged in epidermic and nervous layers.

3. The Mesenteron

The alimentary cavity, or mesenteron, is formed as a narrow slit, opening to the surface at the lower pole of the egg and extending a certain distance into its interior (Fig. 51, BP). The slit rapidly deepens, spreading concentrically with the surface of the egg, and lying near to what will subsequently become the dorsal surface of the embryo ; it is at first exceedingly shallow, its two walls being almost in contact (Figs. 52, 53, T) ; but very shortly, by depression of the lower wall or floor (Figs. 54, 55, 56. T), the cavity becomes of t considerable size, and forms the alimentary tract of the embryo.

This slit-like mesenteron was formerly described as arising by a process of invagination, the epiblast cells being said to grow into the interior of the egg to form the wall of the mesenteron cavity. Later investigations have shown that this description is incorrect, and that the cavity is formed, not by invagination from the surface, but by splitting apart of the yolk-cells as described above, this splitting being preceded by the formation of pigment in the adjacent surfaces of the cells between which the split is to appear.

The mesenteric slit appears first as a slightly crescentic groove on the surface of the egg (Fig. 51, BP), at the margin of the spreading epiblast, and about midway between the equator and the lower pole of the egg. It is very conspicuous, because the pigmented epiblast cells stop sharply at its upper or convex border, so that the boundary between the epiblast and yolk cells is here an abrupt one, while round the rest of the circumference, as shown on the right-hand side of Fig. 51, the transition is more gradual.


FIG. 52. Sagittal section of a Frog Embryo during the formation of the mesenteron. x 25.

B, blastocoel or segmentation cavitv. BP, upper or dorsal lip of blastopore. BP', lower or ventral lip of blastopore. EE, outer or epidermic layer of epiblast. EN, inner or nervous layer of epib'.ast. H, hypoblast. T, mesenteron. Y, yolk-plug.


The groove rapidly extends at its extremities, becoming semicircular, then horse-shoe shaped, and finally, by meeting of its limbs, a complete circle. This circular groove separates the epiblast, which now ends sharply against it round its entire margin, from a circular patch of yolk-cells (Fig. 52, Y, and Fig. 58, A), which still remains at the surface of the egg. The circular aperture in the epiblast, defined by this groove, is spoken of as the blastopore, or anus of Rusconi ; and the mass of yolkcells which fills up the aperture, as the yolk-plug.

The blastopore lies at first at the lower pole of the egg. Reference to Figs. 54, 55, and 58 will show that this lower pole becomes subsequently the hinder or tail end of the embryo, so that the lips of the blastopore, BP and BP', may be spoken of as dorsal and ventral respectively.

From the figures, and from the above description, it will be seen that the groove which limits the blastopore appears first at its dorsal margin, BP, and spreads round the sides to the ventral margin, BP'. The slit extends at first radially inwards, towards the centre of the egg (Figs. 51, BP, and 52, BP') ; but ajong the dorsal surface the slit, after a short radial course (Fig. 52, BP), turns sharply at right angles (Fig. 52, T), and spreads forwards concentrically with the surface of the embryo.



FIG. 53. Horizontal section across a Frog Embryo of the same age as that shown in Fig. 52, the section being taken along a line joining the reference letters T and B in Fig. 52. x 25.

B, blastoccel or segmentation cavity. EE, outer or epidermic layer of epiblast. EN, inner or nervous layer of epiblast. TT, liypoblast. M, mesoblast. T, mesenteroii. Y, yolk-cells.


The whole embryo, which up to this stage has been spherical, now begins to elongate, becoming ellipsoidal, with the blastopore marking the posterior pole (Figs. 54, 55). By an alteration in the position of the cells of its floor, the mesenteric slit (Fig. 52, T) becomes widened out into a large cavity (Fig. 54, T) ; the roof or dorsal wall of which is formed by a well-defined layer of small cells, arranged three or four deep, and lying in close contact with the epiblast, while the floor and sides consist of yolk-cells (Fig. 54, Y).


FIG. 54. Sagittal section of a Frog Embryo just before the disappearance of the segmentation cavity, x 25.

B, blastocoel or segmentation cavity. BP, upper or dorsallip of the blasto pore. BP'. lower or ventral lip of the blastopore. CH, notochord. EE, outer or epidermic layer of epiblast. EJyT, inner or nervous layer of epiblast. TT, hypoblast forming dorsal wall of meseuteron. M, mesoblast. T, mesenterou. Y, yolk-cells. YP, yolk-plug.


During this change the segmentation cavity, B, gradually becomes reduced in size, and ultimately disappears altogether. It can always be distinguished from the mesenteron by the fact that it lies between the epiblast and the yolk-cells, and that its wall is therefore formed on one side by epiblast cells only (Figs. 52 and 53, B) ; while the mesenteron, T, always has walls formed by both epiblast and lower layer cells.

Figs. 52, 54, and 55 show that the segmentation cavity becomes reduced and obliterated, partly by the growth forwards of the cells which form the roof of the mesenteron ; and partly by a shifting in the position of the yolk-cells forming the floor of the mesenteron, which accompanies the elongation of the embryo and the enlargement of the mesenteric cavity. The mesenteron and the segmentation cavity may, as shown in Figs. 52 and 54, communicate with each other for a time during these changes.


FIG. 55. Sagittal section of a Frog Embryo after the disappearance of the segmentation cavity and completion of the mesenteron. x 25.

BP, blastopore. CH, notochord. E, epiblast : the cell outlines and the distinction between the epidermic and nervous layers are not shown. TT, hypoblast. TVT, mesoblast. T, meseuteron. Y, yolk-cells.

4. Formation of the Hypoblast, the Notochord, and the Mesoblast

During the formation of the mesenteron, the cells forming its walls (Figs. 54 and 56) become arranged in two concentric layers : an inner layer, the hypoblast, which forms the true wall of the mesenteron ; and an outer layer, the mesoblast (Fig. 56, M), which lies between the hypoblast and the epiblast.

The splitting off of the mesoblast commences in the dorsolateral walls of the mesenteron, and spreads towards the median plane, both dorsally and ventrally. Before this splitting reaches the mid-dorsal plane, a pair of longitudinal clefts appear along the dorsal surface, by which a median longitudinal rod of cells (Fig. 56, CH) is cut off from the two laterally placed mesoblast sheets, M. This rod, CH, remains attached to the hypoblast for a short time after the mesoblast sheets are completely separated ; but very shortly afterwards the rod in its turn splits off from the hypoblast, and becomes the notochord.

The mesoblast (Fig. 56, M) thus arises in the frog as two lateral sheets of cells, split off from the outer surface of the hypoblast and yolk-cells. The two sheets very early become continuous with each other in the mid-ventral plane, but are separated dorsally by the notochord, which is formed, independently, from the hypoblast in the mid-dorsal region.

At intervals along their length, the mesoblast sheets remain for a time attached to the hypoblast along the dorsal surface of the mesenteron, not far from the median plane ; and, at these places, slight pouch-like diverticula from the mesenteron (Fig. 56, HM) may be seen extending into the mesoblast^ sheets. It has been suggested by Hertuig that these diverticula are possibly indications of a mode of origin of the mesoblast as hollow diverticula from the mesenteron, such as occurs in Amphioxus (</. Figs. 24 and 28, CE).



FIG. 56. A transverse section through the middle of the length of a Frog Embryo at about the stage represented in Fig. 55. x 25.

CH, notochonl. E, epiblast. HM, pouch-like diverticulum of the hypoblast into the mesoblast. M, mesoblast. NG, neural groove. NP, neural plate. T, mesenterou. Y, yolk-cells.


5. The Blastopore and the Primitive Streak

The blastopore, or anus of Rusconi, has been defined above as the circular aperture in the epiblast which is filled up by the yolk-plug (Figs. 52 and 58, A) ; the lip of the blastopore and the yolk-plug being separated from each other by the narrow circular groove which leads into the mesenteron. In the immediately succeeding stages the blastopore becomes greatly reduced in size, though still retaining its circular outline (cf. Figs. 52, 54, 55). This reduction is effected, not by contraction of the whole circumference of the blastopore, but by a folding together, or concrescence, of its lips in the median plane, beginning at the lower or ventral margin and proceeding upwards towards the dorsal margin, the line of fusion being marked by a faint vertical groove on the surface of the embryo (cf. Fig. 58, A and B).

At the lip of the blastopore, round its entire circumference, the three germinal layers, epiblast, mesoblast, and hypoblast, are indistinguishably fused together (Figs. 54, 55) ; the separation between the layers first appearing a little distance beyond the margin of the blastopore. As the lips of the blastopore meet and unite from below upwards, in the manner described above, a vertical band is produced by their union, at the hinder end of the embryo, in which the three germinal layers are fused. This band is spoken of as the primitive streak ; and the faint median groove, already described (Fig. 58, B, C), which runs along it, and marks the line of union of the right and left lips of the blastopore, is named the primitive groove.

The primitive streak and primitive groove are comparatively inconspicuous features in the frog embryo, but are much more prominent in the chick and the rabbit. They are probably to be regarded as secondary rather than as essential characters, and as associated with the great distension which the egg has undergone in consequence of the number of yolk-granules imbedded in its substance.

The further development of the primitive streak, and the ultimate fate of the blastopore, will be described in a later part of this chapter.

The reduction in size of the blastopore, caused by the concrescence of its lips, gives rise to a corresponding diminution of the yolk-plug (cf. Figs. 52, 54, YP) ; and at the close of the period now being described this withdraws completely from the surface of the embryo (Fig. 55).


6. Comparison of the Early Stages in the Development of the Frog with those of Amphioxus

The frog's egg is more than 5,000 times the bulk of that of Amphioxus : this large size is due mainly to the much greater amount of food-yolk present in the frog's egg, and it is chiefly owing to this food-yolk that the development of the two forms is so different. In the earliest stages the differences are less marked than in the succeeding ones. The first two segmentation clefts divide the frog's egg in the same way as they do that of Amphioxus ; the third cleft is in both cases a horizontal one, but while in Amphioxus it is nearly equatorial, in the frog it lies much nearer the upper pole. The stage shown for the frog in Fig. 49 corresponds fairly closely, in essential respects, with the blastula stage of Amphioxus ; but from this point the development of the two forms becomes widely diffei^ent.

There is no stage in the frog which exactly corresponds to the gastrula stage in Amphioxus ; for at the stage shown in Fig. 52, which most nearly approaches to this, both epiblast and hypoblast are already three or more cells thick, instead of being, as in Amphioxus, single layers of cells. Moreover, the primitive digestive cavity of the frog (Fig. 52, T)is formed, not by invagination, as in Amphioxus, but by a process of splitting, or separation, among the yolk-cells occupying the interior of the embryo. The history of development in some allied animals, notably in the newt, suggests that the process of splitting is a secondary modification, which has arisen in consequence of the hindrance offered by the large mass of yolk-cells to the occurrence of invagination.

The early establishment of the two-layered condition of the epiblast is another point in which the frog presents a modified and specialised condition : in the corresponding stages of the newt the epiblast consists, as in Amphioxus, of a single layer of cells.

Development of the Nervous System

It will be convenient from this point to deal with the several systems one by one, following each up to its condition in the adult. The order in which the systems are taken is chiefly a matter of convenience, but for several reasons the nervous system is the most suitable to commence with. It is formed from the epiblast, which is the earliest of the germinal layers to be definitely established ; it appears at a very early stage ; and it plays a prominent part, especially in the younger embryos, in determining the shape and proportions of the body.

1. General History of the Central Nervous System

The epiblast of the frog, as already described, consists, almost from the first, of two layers, the distinction between which is established before the close of the period of segmentation. Of these, the upper or epidermic layer is a single stratum of closely fitted, short columnar or cubical cells ; while the lower or nervous layer (Figs. 51, 52) consists of spherical or ovoid cells, more loosely arranged, and two or three deep : it is from this lower layer that the nervous system is developed.

The first trace of the nervous system appears at a stage immediately succeeding that shown in Fig. 55, when the embryo is ellipsoidal in shape, and the blastopore has become much reduced, and less conspicuous owing to the yolk-plug having withdrawn from the surface.

The dorsal surface of the embryo now flattens slightly, and along the flattened area the deeper or nervous layer of the epiblast thickens to form the neural plate, a triangular area extending aJong the back of the embryo, wider in front but narrowing posteriorly towards the blastopore. Slightly raised ridges, the neural folds (Fig. 57, NF), soon appear, bordering the neural plate laterally ; and a shallow neural groove (Figs. 56, 57, NG) is formed along its dorsal surface in the median line, extending forwards from the blastopore.


Fig. 57. A Frog Embryo at the time of appearance of the neural folds : seen from the dorsal surface, x 20.

N"P, neural fold : the reference line points to the junction of the anterior and the left lateral folds. NG, neural groove. YP, yolk plug, greatly reduced in size, but still visible through the blastopore.


Anteriorly, the two neural folds are connected by a transverse fold (Fig. 57). which runs across the anterior end of the neural plate, and slightly raises it above the level of the surrounding parts ; while at their hinder ends the two neural folds are continuous with the lateral lips of the blastopore.

The neural folds rapidly increase in height and thickness : the groove between them deepens; and the folds, becoming more and more prominent (Figs, 58, 50j, approach each other, and finally meet in the median plane and fuse together, converting the neural groove into a tube.

The neural folds first meet about the junction of the head and neck of the embryo ; and from this point the fusion extends rapidly backwards, and more slowly forwards. The point at which fusion last occurs is a little distance behind the anterior end of the neural tube, at the spot where the pineal body is formed later, the part of the tube in front of this point being roofed in by growth backwards of the anterior or transverse neural fold seen in Fig. 57.



FIG. 58. Stages in the early development of the Frog Embryo, seen obliquely from the hinder end. (From a series of wax models by Dr. F. Ziegler, of Freiburg i_15.j

A, stage in which the blastopore is nearly circular, and is occupied by the white yolk- plug. B. stage in which the lateral lips of the blastopore have met and fused to form the primitive streak ; the short vertical line, corresponding to the position of the blastopore in A, is the primitive groove ; the depression at the upper end of the primitive groove is the greatly reduced blastopore, and the depression at the lower eud'of the primitive groove is the commencing proctodajal or anal invagination. Above the bl pore is seen the commencing neural groove, bordered by the neural folds. C, later stage, in which the neural groove has deepened, while the neural folds are more prominent and are growing inwards to meet each other. D, stage in which the neural folds have met and the tail is commencing to form. Both blastopore and proctodseum are still pre>om. B, later stage, in which the neural tube is completed and the tail has increased in size. The blastopore has finally closed, and the black spot below the tail is the proctodaeum.


The neural groove extends back as far as the blastopore (Figs. 57 and 58, B), and the neural folds, as noticed above, become continuous at their hinder ends with the lips of the blastopore. For a short time, after completion of the neural tube, the blastopore still remains open, communicating, as seen in Fig. 60, both with the mesenteron and with the cavity of the neural tube. Very shortly, however, the fusion, by which the neural tube is closed, extends further back, so as to involve the lips of the blastopore, and the external opening of the blastopore becomes finally closed (Fig. 58, E, and Fig. 61). The communication between the neural tube and the mesenteron still persists, however, as a narrow tubular passage, the neurenteric canal (Fig. 61), passing round the hinder end of the notochord.


FIG. 59. Transverse section through a Frog Embryo, at a stage corresponding to Fig. 58, C, and showing the neural folds shortly before they meet each other to complete the neural tube.

C, coelom or body cavity. CH, notochord. EE, outer or epidermic layer of epiblast. EN", inner or nervous layer of epiblast. M, niesoblast. ME, outer or somatopleuric layer of niesoblast. MH, inner or splanchnopleuric layer of mesoblast. M"C. neural groove. ND, dorsal root of a spinal nerve. M"S, spinal cord. T, rnesenterou. W, liver diverticulum. Y, yolk.

The neurenteric canal persists only for a very short time. In the immediately succeeding stages the tail begins to lengthen rapidly, carrying the hinder end of the neural tube far away from the mesenteron, and the channel of communication between the two becomes speedily obliterated. At the time of hatching (Fig. 69, p. 146), the hinder end of the neural tube curves slightly downwards, round the end of the notochord, but ends blindly a long distance from the meseuteron. A string of cells, connecting the two structures, is at this stage the sole indication of the former communication between them.

The neural tube, formed in the way described above, by fusion of the neural folds, soon separates along its entire length from the external epiblast, and by thickening of its walls and various histological changes becomes converted into the central nervous system ; the anterior part forming the brain, and the posterior part the spinal cord. The lumen or cavity of the neural tube persists throughout life as the central canal of the spinal cord and the ventricles of the brain (cf. Figs. 60, 61, 64, and 65).



FIG. 60. Sagittal section of a Frog Embryo shortly before closure of the blastopore, and of the same age as the embryo shown in Fig. 58, D. x BO.

B, blastopore. BF, fore-brain. BH, hind-brain. BM, mid-brain, H, hypoblast. L, liver. M, inesoblast. MN, mesenteron. N, notochord. N"C, neurenteric canal. P, ingrowth of epiblast to form the pituitary body. PD, proctodaeum. H., rectal diverticulum of meseuteron. S, central canal of spinal cord. Y, yolk cells.


The further changes undergone by the spinal cord are comparatively slight, and will not be described in detail. Almost from the first (Fig. 70, p. 147), the spinal cord is oval in transverse section, the central canal being a vertical slit. The layer of cells lining the central canal, derived (cf. Fig. 59) from the outer or epidermic layer of the epiblast, remains throughout life as a layer of columnar ciliated epithelial cells ; while the outer wall of the neural tube, formed from the deeper or nervous layer of the epiblast, gives rise directly to the nervous elements, i.e. to the nerve cells and nerve fibres, of the adult spinal cord. The histological changes by which the nervous elements are formed will be described in the chapters dealing with the chick and the rabbit, in which animals they have been investigated more completely than in the frog.

The spinal cord extends to the extremity of the tail, which in the later stages of tadpole life is of great length (Fig. 44, 9,10,11). During the absorption of the tail, at the time of the metamorphosis, fully two-thirds of the length of the spinal cord are lost.

2. The Development of the Brain

The brain is merely the specialised anterior part of the neural tube, and is directly continuous posteriorly with the spinal cord.



FIG. 01. Sagittal section of a Frog Embryo, shortly after closure of the blastopore and formation of the anus, and of the same age as the embryo shown in Fig. 58, E. x 25.

BF. fore-brain. BH, hind-brain. BM, mid-brain. CH, notochord. M, mesoblast. NC, cavity of neural tube. NT, neurenteric canal. PN", pineal body. PT, ingrowth of epiblast which gives rise to the pituitary body. TI, intestinal region of raesenteron. TP, pharyngeal region of mesenteron. TJ, proctodseal or cloacal apertiire. "W, liver, Y, yolk-cell*.


While the spinal cord is straight, or nearly so, the brain is from its first appearance bent rather sharply, and nearly at right angles, about the middle of its length ; the axis of the posterior part being horizontal and continuous with that of the spinal cord, and the axis of the anterior part vertical. The whole central nervous system may be compared to a retort (Fig. 60), the bulb of the retort being formed by the anterior and vertical part of the brain, BF, and the neck by the posterior horizontal part of the brain, together with the spinal cord.

This bending of the brain is spoken of as cranial flexure. It takes place, as shown in Fig. 60, round the anterior end of the notochord, and is due, in the first instance, to the spherical shape of the surface of the egg on which the neural plate is formed. A similar ventral flexure of the hinder end of the neural tube is present at first, but becomes early obliterated by the outgrowth of the tail (cf. Fig. 58, B, C, D, E). The ventral flexure of the brain, round the anterior end of the notochord, persists throughout life.

Very shortly after the closure of the brain-tube is completed, a slight transverse constriction appears, at the bend between the horizontal and vertical portions of the brain, and a little later a second constriction is formed rather further forwards. By these constrictions the brain (Figs. 60 and 61) becomes divided into three portions, named fore-brain, mid-brain, and hind-brain respectively.

The fore-brain (Figs. 60 and 61, BF) is the terminal vertical portion, corresponding to the bulb of the retort ; the midbrain. BM, which is the smallest of the three divisions, forms the angle of the bend, opposite the anterior end of the notochord ; and the hind-brain, BH, is the horizontal portion, continuous posteriorly with the spinal cord. This division of the embryonic brain into three regions, anterior, middle, and posterior, is a convenient one, as it obtains throughout the higher groups of Vertebrates, from fishes to mammals, each of the divisions giving rise to important and characteristic parts of the adult brain.

The walls of the brain-tube are at first of approximately uniform thickness in all parts, excepting the roof of the hindbrain, which from the first is thin. By unequal thickening of various parts, especially of .the sides, and by outgrowths, either median or paired, with accompanying histological changes, the adult brain is gradually built up.

In these changes the most important share is taken by the fore-brain. The fore-brain itself becomes the part known in the adult as the thalainencephalon, its cavity persisting as the third ventricle ; from it the pineal body and the iafundibulum are developed as median diverticula, dorsal and ventral respectively ; while the optic vesicles and cerebral hemispheres arise as paired lateral and anterior outgrowths.

The mid-brain undergoes comparatively little change ; from its roof the optic lobes of the adult are formed.

The hind-brain becomes the medulla oblongata of the adult : from the roof of its anterior part the cerebellum is formed.

Before considering the development of the several parts of the brain in detail it will be well to notice the general proportions and relations of the brain during the successive stages of its formation. These will be readily understood from comparison of Figs. 60, 61, 64, 65, and 89.


Fig. 62. The brain of the adult Frog : dorsal surface. FIG. 63. The brain of the adult Frog: ventral surface. x4. x4.


C, cerebellum. CH, cerebral hemisphere. CP, choroid plexus of third ventricle. F, fourth ventricle. IN, infuudibulum. M, medulla oblongata. O, olfactory lobe. OC, optic chiasina. OL, optic lobe. P, stalk of pineal body. PB, pituitary body. T, thalarnencephalon. I, olfactory nerve. II, optic nerve. Ill, third or motor oculi nerve. IV, fourth nerve. V, fifth or trigeminal nerve. VI, sixth nerve. VII and VIII, combined root of facial and auditory nerves. IX and X, combined root of glossopharyngeal and pneumogastric nerves.


At the time of the first formation of the brain-tube, before the hatching of the tadpole (Figs. 60, 61), cranial flexure is very strongly marked, and the fore-brain, BF, projects far in front of all other organs of the body. Later on (Figs. 64, 65), both these relations are changed ; the brain appears to become straightened out, and it also recedes some distance from the anterior end of the head.

The straightening of the brain, or rectification of the cranial flexure as it is sometimes termed, is apparent rather than real, and is brought about principally by the formation of the cerebral hemispheres (Figs. G4, 65, EC), which grow forwards from the fore-brain, and speedily attain so large a size relatively to the other parts of the brain as to alter the direction of the axis of the brain as a whole, and to completely obscure the original flexure, which really persists throughout life. The receding of the brain from the anterior end of the head is due to the more rapid growth of the surrounding parts, and more especially of the face and lips, which causes the brain to take a much less prominent share in determining the shape of the head.



FIG. 64. Sagittal section of the head end of a Tadpole just before the opening of the mouth.

A, dorsal aorta. BC, vesicle of the hemispheres. BH, lurid-brain. BM. mid-brain. CH, notochord. DS, septum separating stomatodseum and pharynx. IN", infundibulum. PN , pineal body. PT, pituitary body. US, sinus venosus. "B.T, truncus arteriosu<. RV, ventricle. TH, thyroid body. TI, intestine. TP, pharynx. TO, plug of epithelial cells blocking up the oesophagus. ~W, liver. "WG, gall-bladder.





In describing the development of the brain in detail it will be convenient to take the several parts in order, from behind forwards, commencing with the medulla oblongata.


The medulla oblongata undergoes less change than an}* other part of the brain. In the early stages, up to about the time of formation of the mouth, it is the widest part of the brain, but afterwards it is exceeded by both the optic lobes and the cerebral hemispheres. It is continuous posteriorly, without any line of demarcation, with the spinal cord ; while anteriorly it is separated from the mid-brain by a well-marked constriction, deepest dorsally and at the sides.

From the first, the roof of the medulla oblongata is thin ; in the later stages the sides and floor thicken very considerably, while the roof (Figs. 65 and 84) widens out and becomes reduced to an extremely thin membrane, consisting of a single layer of pigmented and ciliated epithelial cells, without nervous elements of any kind.

This thin roof is at first smooth and level ; but about the time of formation of the mouth opening, i.e. in tadpoles of about 9 mm. length, the roof becomes thrown into folds (Fig. 65, x'), which become deeper and more pronounced as the tadpole increases in size. Lying on this thin roof, and in very close contact with it, is a rich network of blood-vessels, the choroid plexus, which extends between the folds of the roof, and so appears to hang down into the cavity of the medulla, though always in reality separated from this by the thin epithelial roof.

The cavity of the medulla oblongata, or fourth ventricle, is of considerable size : it is wide in front, and tapers gradually towards its hinder end, where it passes into the central canal of the spinal cord.

The cerebellum is an inconspicuous structure throughout the early stages of tadpole life. Up to the time of the opening of the mouth it can hardly be said to exist (Fig. 64) ; but shortly after this event it appears as a thickening of the roof of the fourth ventricle, in the form of a transverse band, immediately behind the constriction separating the medulla oblongata from the mid-brain. In the later stages of development it increases gradually in size (Fig. 89, BL), but even in the adult frog it is very small as compared with its condition in most other Vertebrates.

The mid-brain does not undergo very great changes. Its floor remains thin in the actual median plane ; but immediately to the right and left of this the sides become thickened by the formation of the crura cerebri, two longitudinal bundles of nerve fibres which connect the mid-brain with the fore-brain. The roof of the mid-brain is thin in the early stages ; but shortly after the opening of the mouth the two halves of the roof thicken considerably, and, bulging upwards, form a pair of rounded swellings, the optic lobes (Fig. 62, OL), separated by a median groove. The optic lobes continue to increase in size, and about the time of the metamorphosis become, as in the adult frog, the widest portion of the brain. The cavity of the mid-brain persists as a fairly wide passage, the Sylvian aqueduct.

The thalamencephalon is the original fore-brain of the embryo ; and in connection with it important changes occur. Its cavity, the third ventricle, is at first large ; but, owing to thickening of its walls to form the optic thalami, the cavity becomes early reduced to a vertical cleft, very narrow from side to side.

The roof of the thalamencephalon is very thin, consisting, like that of the medulla oblongata, of a single layer of epithelial cells, devoid of nervous elements. About the middle of its length, and at the place where the final closure of the neural tube was effected, the pineal body is formed. This appears in embryos of about 3 mm. length (Fig. 61, PN) as a median hollow diverticulum, which at the time of hatching of the tadpole (Fig. 64, PN), forms a small round knob on the top of the brain, immediately beneath the surface epiblast. This grows forwards, and becomes dilated distally. At the time of opening of the mouth it forms a small rounded vesicle, connected with the brain by a tubular stalk ; it is of a glistening white appearance, owing to the presence of small snow-white particles imbedded in its substance, and stands in this respect in marked contrast to the rest of the brain, which is pigrnented rather strongly. In tadpoles of 12 mrn. length the pineal body itself is solid (Fig. 65, PN), but its stalk is still tubular. Shortly after this, on the formation of the skull, the pineal body becomes cut off from its stalk, and lies outside the skull, just beneath the skin of the top of the head. It persists throughout the tadpole stages, but disappears at the time of the metamorphosis. The stalk of the pineal body persists throughout the life of the frog, retaining its tubular character, and its communication with the third ventricle.

About the time the roof of the fourth ventricle is becoming folded, and the choroid plexus established in connection with it, a similar change is going on in relation with the third ventricle. Immediately in front of the pineal body, the thin roof of the thalamencephalon becomes thrown into folds which hang down into the ventricle (Fig. 65, x). A dense plexus of blood-vessels lies on the roof and grows in between its folds, giving rise to a choroid plexus similar to that of the fourth ventricle, but more restricted in its extent. The vascular plexus on the surface of the thalamencephalon forms also a dorsally projecting process, the supra-plexus, with which the distal end of the stalk of the pineal body is in very close relation (Fig. 89, PN).

The infundibulum (Figs. G4, 65, IN) is a depression of the floor of the thalamencephalon, with which the pituitary body comes into close relation at an early stage. The infundibulum is already recognisable at the time of closure of the neural tube : its hinder wall is in close relation with the anterior end of the notochord, and it is in fact the infundibular depression (Fig. 61) which causes the brain to appear to be bent round the end of the notochord, one of the most striking features of cranial flexure. The infundibulum is separated from the mid-brain (Figs. 61, 65) by a deep transverse groove, running across the ventral surface of the brain, and very conspicuous when the brain is seen from below. On the appearance of the optic vesicles, a second transverse groove (Fig. 64) is formed, further forwards, between the optic vesicles and the infundibulum. The infundibulum retains the same character and relations throughout all the later stages of development : it appears as a wide thin-walled sac, forming a conspicuous projection on the under surface of the brain, and having the pituitary body in close relation with it posteriori}* (Fig. 89, IN).

The pituitary body, although not really a part of the brain, may conveniently be described here. It arises (Figs. 60, P, and 61, PT) as a plug-like ingrowth of the deeper or nervous layer of the epiblast, immediately below the anterior end of the brain. It appears very early, and may be recognised as a slight thickening of the epiblast even before the neural tube is closed ; and at the time of completion of the tube (Fig. 60) it projects inwards as a small, solid, tongue-like process beneath the brain, between this and the dorsal wall of the pharynx.

The projection continues its growth inwards, and expands at its end into a somewhat flattened mass of cells, which lies immediately beneath the infundibulum, close to the anterior end of the notochord, and which becomes the pituitary body itself (Fig. 64, PT); the rest of the process forms a slender stalk, which connects the pituitaiy body with the surface epiblast. About the time of opening of the mouth, the pituitary body becomes hollow and separates from the stalk, which atrophies and soon disappears completely. The pituitary body (Fig. 65, PT), which is now all that remains of the original ingrowth, acquires close relations with the hinder end of the infundibulum, which it retains throughout life (Fig. 63, PB). It becomes partially divided into anterior and posterior portions, of which the latter forms a complicated mass of convoluted tubes.

The optic vesicles. From the sides of the fore-brain, about the time that closure of the neural tube is effected, a pair of hollow lateral outgrowths, the optic vesicles, arise. Each optic vesicle soon becomes constricted at its base, so as to form a bulb, opening by a tubular stalk into the fore-brain. From the bulbs, the eyes are developed in a manner that will be described later on ; while the optic stalks form paths along which the fibres of the optic nerves pass from the eyes to the brain.

About the time of opening of the mouth (Fig. 64), a transverse groove runs across the floor of the fore-brain, in front of the infundibulum, IN, and between this and the vesicle of the hemispheres, BC. This groove is bounded in front and behind by transverse ridges, and is produced outwards at its two ends into the tubular optic stalks. At a slightly later stage, about the time of appearance of the hind limbs (Fig. 65), the stalks become solid along their whole length ; the further changes in connection with them will be described in the section dealing with the development of the eye.

The cerebral hemispheres. The hemispheres, although the largest part of the adult brain (Figs. 62, 63), are the last to appear. About the time of hatching of the tadpole, the anterior end of the fore-brain begins to grow forwards as a median thinwalled vesicle of the hemispheres ; this steadily increases in size, but, up to the time of the formation of the mouth, remains undivided. At this stage (Fig. 64, BC), it is approximately spherical, and about equal in size to the mid-brain : its roof and anterior wall are both extremely thin, but its side walls are much thickened, so that the central cavity is compressed laterally.

The vesicle continues to increase in size, but remains single and undivided up to a stage slightly later than that shown in Fig. 65, when a division between the two hemispheres appears. This is effected by the roof and anterior wall becoming folded vertically along the median plane ; the fold, which is continuous posteriorly with the choroid plexus of the third ventricle, projects into the cavity of the vesicle, and partially divides this into right and left halves, which become the lateral ventricles of the hemispheres.

By further growth forwards of the hemispheres, with thickening of their walls, the proportions of the adult brain are gradually acquitted ; the brain at the time of the metamorphosis being practically identical with that of the fully formed frog. The anterior or distal extremities of the hemispheres become the olfactory lobes ; these are at first separate from each other, but ultimately become fused together along their inner surfaces.

3. The Development of the Peripheral Nervous System

It will be convenient to give first a general description of the early stages of development of the peripheral nervous system of the frog, and then to deal separately with the cranial and the spinal nerves in regard to the later phases of their formation. There are still many points on which our knowledge of the development of the nervous system in the frog is imperfect and unsatisfactory.

The early stages of development of the nerves. The dorsal roots of the spinal nerves, and the majority of the cranial nerves, arise in closely similar manner, and at a very early period. The first commencements are seen in embryos which are still almost spherical, and in which the neural plate and neural ridges are just commencing to form, but have not yet begun to fold in to inclose the neural tube (Fig. 57).

The neural plate is formed, as described above, by thickening of the deeper or nervous layer of the epiblast along the dorsal surface of the embryo. Along the sides of the neural plate, where it passes into the unmodified epiblast of the body wall, and on its inner or deeper surface, opposite to the commencing neural ridges, a pair of longitudinal bands of epiblast appear. These are at first merely the lateral edges of the neural plate, but they soon become separated by lines of demarcation from the neural plate, and rather later from the epiblast along their outer sides. In transverse sections they appear as a pair of small triangular wedges, at the sides of the neural plate, continuous with the epiblast above, but separated by divisional planes, often indistinctly marked, from the neural plate on the inner side and the general epiblast on the outer side (cf. Fig. 59, ND).

These bands of epiblast cells, cut out from the inner or nervous layer of the epiblast, are at first continuous structures, extending the whole length of the embryo. They are spoken of as the neural ridges, and from them the dorsal roots of the spinal nerves, and the majoi'ity of the cranial nerves, are derived.

As the neural folds grow upwards to inclose the neural tube, the neural ridges get carried up with them ; and at a time when the lips of the tube are about to unite, the neural ridges form a pair of longitudinal bands (Fig. 59, ND), projecting outwards on either side from the angle between the external epiblast, EE, and the wall of the neural tube, NS.

On the closure of the neural tube, the neural ridges separate completely from the external epiblast, and the ridges of the two sides become continuous with each other across the median plane, forming a plate of cells, the neural crest, attached, to the dorsal surface of the brain and spinal cord (Fig. 70, ND).

As the several divisions of the brain are formed, the originally continuous neural ridge of each side becomes discontinuous, growing outwards so as to become more prominent at certain parts of its length, and disappearing in the intervening regions ; it thus becomes broken up into a series of outgrowths, which are the rudiments of the nerves.

The neural crest, formed by the fusion of the two neural ridges, and therefore also the nerves into which the crest becomes cut up, are at first connected with the dorsal surface of the neural tube. The permanent attachments of the nerves to the sides of the neural tube are acquired at a later stage, by the growth of processes from the cells of the nerves into the substance of the brain, or spinal cord.

Up to this point the development of the cranial and the spinal nerves is practically the same ; the cranial nerves appear at an earlier stage in the formation of the neural tube than do the spinal nerves, and are from the first of much larger size than these latter, but the history of the early stages is essentially the same in the two cases.

The spinal nerves. After reaching the neural crest stage, the development of the spinal nerves proceeds for a time very slowly. The nerve rudiments, after a rather long pause, grow slowly down between the myotomes and the sides of the spinal cord. The permanent attachment to the side of the cord is acquired in the manner described above, by growth of nerve fibres from the nerve rudiment, or ganglion, into the cord. The ganglion itself enlarges, and the nerve fibres continue their course beyond it to form the trunk of the dorsal or sensory root of the spinal nerve.

The ventral or motor root arises quite independently : the details of its development have not been determined so accurrately in the frog as in other animals, but each ventral root appears to arise as a number of outgrowths from the lower part of the side of the spinal cord, which from the first occupy their permanent positions in regard to the cord, and which very early become connected distally with the muscles of the body.

The dorsal and ventral roots of each nerve lie close alongside each other, and become bound together by a common connective-tissue sheath to form the trunk of the spinal nerve, from which branches soon arise supplying the various parts to which the nerve is distributed in the adult (cf. Figs. 87 and 88).

The cranial nerves. The development of the cranial nerves of the frog has not been very thoroughly studied ; and there are several points on which our knowledge is still in an unsatisfactory condition. The nerves which are undoubtedly derived from the neural ridges are the trigeminal, the facial and auditory, and the sensory branches of the glosso-pharyngeal and pneumogastric ; i.e. the fifth, seventh, eighth, ninth, and tenth cranial nerves according to the ordinary nomenclature. The olfactory nerve is perhaps to be added to these. The optic nerve develops in a very special manner ; and the mode of development of the third, fourth, and sixth nerves in the frog has not yet been determined with accuracy.

The trigeminal, facial, glosso-pharyngeal, and pneumogastric nerves, although arising from the neural ridges in the same way as the dorsal roots of the spinal nerves, yet differ from these, and agree amongst themselves, in certain important features, of which the following are the principal :

i. The nerves in question, in place of growing downwards, like the spinal nerves, alongside the central nervous system, grow outwards, close to the surface of the embryo, between the epiblast and the mesoblast.

ii. Each of these four nerves acquires a new connection with the surface epiblast some considerable distance beyond the root of origin from the brain, and at about the horizontal level of the notochord ; at this place, and at any rate in part from the surface epiblast itself, the ganglion of the nerve is formed.

iii. The nerves have special relations to the gill-slits, each nerve dividing into two main branches, which embrace between them one of the gill-slits.

iv. A special system of cutaneous nerves is developed from the surface epiblast in connection with these four nerves, forming the lateral line system of nerves.

In dealing with the several cranial nerves individually it will be convenient to consider them in order from behind forwards.

X. The pneumogastric, vagus, or tenth cranial nerve. This grows rapidly in the early stages, and soon attains an enormous size. In embryos of about 3 mm. length (cf. Figs. 58, C, and 59), when the neural folds have not quite met in the hinder part of the head, and the neural groove is, therefore, still open, the pneumogastric nerves are already present as a pair of winglike expansions of the neural ridges. The root of attachment of the nerve, in the re-entering angle at the top of the brain, between the epiblast and the brain wall, is slender ; but the rest of the nerve is of great thickness. It extends more than half way down the side of the pharynx, lying between the mesoblast and the surface epiblast, very close to the latter but distinct from it along its entire length (cf. Fig. 79, x). The nerves of the two sides are in some cases unequally developed at this stage.


In embryos of about 4 mm. length (cf. Fig. 61), the nerves themselves have undergone but little further change. At the level of the notochord the external epiblast presents, on each side, a very distinct and localised thickening of its inner or nervous layer. This thickening projects inwards, and lies very close to the pneumogastric nerve, a little below the middle of its length, but as yet the two structures are independent. The thickening is well marked, and extends horizontally backwards a little distance beyond the nerve.

At the time of hatching, i.e. in tadpoles of about 7 mm. length (cf. Figs. 69, 72, and 73), the epiblastic thickening and the nerve have fused, and together form the ganglion of the pneumogastric : the horizontal extension backwards of the thickening, which forms the lateral line nerve, has grown enormously, reaching now almost to the hinder end of the body of the tadpole. The mode in which this lateral line nerve grows has not been determined with certainty in the frog ; at its first appearance it is clearly a ridge-like thickening of the inner surface of the epiblast, but it is difficult to decide whether the extension backwards, which is effected with great rapidity, is due to a splitting off from the epiblast, or to growth backwards of a solid rod of cells from the ganglion of the pneumogastric. Such evidence as is forthcoming rather favours the latter view. In transverse sections at this stage (Fig. 82, NL), the lateral line nerve has the appearance of a solid rod of cells, lying in a groove along the inner surface of the epiblast, at the level of the lower part of the spinal cord. The lateral line nerve is of large size throughout the whole period of tadpole life ; it is present during the metamorphosis, but disappears completely at its close. During the later tadpole stages it separates from the skin, and becomes more deeply placed among the muscles of the body wall. Besides the main lateral line nerve described above, other similar cutaneous branches are formed in connection with the pneumogastric ganglion ; a more slender nerve is developed nearer the mid-dorsal line ; and a stout nerve runs at first ventralwards from the ganglion, and then backwards along the sides of the ventral surface of the abdominal region.

Concerning the further development of the pneumogastric nerve itself there are some points of interest. The root of attachment to the brain, which is acquired in the same manner as that of the dorsal root of a spinal nerve, is from the first of considerable length horizontally. About the time of opening of the mouth the root divides into two ; an anterior one, which runs nearly straight outwards from the brain ; and a posterior one, which runs very obliquely forwards, to join the anterior root just before it reaches the ganglion. The ganglion lies immediately behind the ear; beyond it the nerve divides into a set of branches which supply the three hinder branchial clefts, and a set of visceral branches, which run to the heart and alimentary canal. All these branches are well established by the time the mouth of the tadpole is formed.

IX. The glosso-pharyngeal, or ninth cranial nerve, is formed from the part of the neural ridge immediately in front of that from which the pneumogastric nerve is developed, the roots of the two nerves being at first continuous with each other. The nerve is very similar to the pneumogastric, but of smaller size : in the tipper part of its course it lies immediately in front of the pneumogastric ; it then runs forwards and outwards, round the hinder border of the auditory vesicle, to the upper edge of the first branchial cleft, where it expands to form the ganglion. The ganglion, like that of the pneumogastric, is formed in part from an independently arising thickening of the external epiblast, which fuses with the nerve rudiment about the time of hatching of the tadpole. The ganglion of the glosso-pharyngeal nerve is separated from that of the pneumogastric by the anterior cardinal vein. Beyond the ganglion the glosso-pharyngeal runs downwards, as a slender nerve, along the anterior edge of the first branchial arch, giving a small praebranchial branch to the hyoid arch. All the main branches are present at the time of opening of the mouth of the tadpole.

VIII. The auditory, or eighth nerve, arises from the neural crest, in common with the seventh nerve, opposite the middle of the auditory vesicle ; the two nerves being absolutely continuous with each other up to the time of formation of the mouth. The auditory portion of the combined nerve forms a large ganglionic swelling, which is continuous with the inner wall of the auditory vesicle from its very earliest appearance. In the later stages, as the various parts of the ear become differentiated, the auditory nerve- divides into separate branches supplying its several parts. (Cf. Fig. 75, vui.)


VII. The facial, or seventh nerve, as noticed above, is, in its early stages, continuous with the auditory nerve. Beyond the auditory vesicle the facial nerve runs downwards and forwards, close to the surface epiblast. Shortly before the time of hatching of the tadpole, the nerve becomes connected with an ingrowth of the epiblast at the level of the upper border of the notochord r and at this place the ganglion is formed. Beyond the ganglion the nerve divides into three principal branches : (i) a small cutaneous branch which appears to develop in connection with the epiblastic ingrowth, and to belong to the lateral line series of nerves ; (ii) a stout post-branchial branch, which runs downwards and forwards along the hyoid arch, close to its surface ; and (iii) a small palatine nerve, which runs forwards in the roof of the pharynx, not far from the median plane.

VI. The development of the sixth, or abducent nerve, ha& not been determined in the frog. From its general relations, and from what is known concerning its mode of formation in other animals, it is probably comparable to a ventral root of a spinal nerve.

V. The trigeminal, or fifth cranial nerve, is the largest of the whole series ; it lies immediately in front of the facial nerve, with which it is in close relation from the first.

The trigeminal nerve, like the pneumogastric, early attain? a large size, and in 4 mm. tadpoles (cf. Figs. 58, E, and 61) extends half way down the side of the pharynx. At or shortly before this stage, a thickening of the external epiblast occurs at the level of the upper border of the notochord, immediately behind the eye, and in front of the auditory vesicle ; this meets and fuses with the nerve, the two together forming the ganglion. The thickening of the epiblast extends forwards a short distance in front of the ganglion, and gives rise to a cutaneous nerve, similar to the lateral line nerve formed in connection with the pneumogastric nerve. Shortly after hatching of the tadpole, the ganglion of the trigeminal nerve recedes somewhat from the surface, and becomes more deeply placed, though still remaining connected with the surface by the cutaneous branch.

Before the hatching of the tadpole, the trigeminal nerve divides distally into ophthalmic and mandibular branches, of which the former runs horizontally forwards, and the latter downwards and forwards, the eye lying in the fork between the two.

At the time of opening of the mouth, in tadpoles of about "9 mm. length, the condition of the trigeminal nerve is as follows : The nerve arises on each side, by a single root, from the side of the medulla oblongata ; and, running downwards and forwards, expands to form the Gasserian ganglion, which lies midway between the eye and ear, and immediately in front of the ganglion of the facial nerve. From the ganglion three branches arise : (i) a small but well-marked cutaneous brancli runs directly outwards, behind the eye, to the skin, along which it continues forwards for a short distance, (ii) A large ophthalmic branch runs horizontally forwards between the eye and the brain, parallel to the outer margin of the brain, and dorsal to the optic nerve and to the nose ; in front of the nose it turns slightly downwards, and ends in branches supplying the skin of the snout: the hindmost or proximal part of the ophthalmic nerve is very thick and ganglionic, the distal part is thin, (iii) A very thick mandibular branch, which is also ganglionic at its proximal end, runs downwards and forwards below the eye, close to the ganglion of the facial nerve, but separated from this by the anterior cardinal vein ; it runs through the jaw muscles, and ends in the floor of the mouth. From the mandibular branch a slender maxillary brancli runs forwards, beneath the eye, and along the upper jaw to the anterior end of the head, where it ends in the skin of the upper lip.

IV. The mode of development of the fourth cranial nerve ot the frog has not been determined.

III. The third cranial nerve is also very imperfectly known. Its early development has not yet been ascertained. At the time of opening of the mouth, in tadpoles of about 9 mm. length, it is present as a slender nerve, arising from the lower part of the side of the mid-brain, not far from the median plane, and having already the course and relations of the nerve in the adult.

II. The optic, or second cranial nerve, will be best dealt with in the description of the development of the eye. The nervefibres arise in connection with the retina, and grow inwards along the optic stalk to the brain.

I. The olfactory, or first cranial nerve. The early stages in the development of the olfactory nerve in the frog have not been seen ; there are reasons for suspecting that it is developed in part from the epithelium of the olfactory pit itself, and perhaps also in part from the anterior end of the neural ridge. The nerve develops early, and is recognisable before the hatching of the tadpole as a short thick trunk, connecting the side of the brain with the thickened epithelium of the olfactory pit.

The nerve remains short, up to the time of opening of the mouth, or rather up to the time when the cerebral hemispheres begin to grow forwards. This anterior growth of the cerebral hemispheres is accompanied, as already noticed, by still more rapid growth of the anterior part of the head, in consequence of which the olfactory pits are carried forwards from their original position at the sides of the brain, and become situated in front of it. This causes lengthening of the olfactory nerves, and a change in their direction ; in place of running outwards from the brain, they now run almost directly forwards : the roots of the nerves, however, still arise from the ventral surface of the brain, some distance from its anterior end, as in the adult.

The sympathetic nervous system. The sympathetic system develops as a series of outgrowths from certain of the cranial, and from all the spinal nerves. These develop ganglionic swellings, which, in the body region (Figs. 84 and 87, NY), lie beneath the notochord, and alongside the dorsal aorta. At an early stage, shortly after the formation of the mouth, the several ganglia of each side become connected together by a longitudinal nervecord, but whether this cord arises independently of the ganglia, or, as is more probable, by the formation of outgrowths from the ganglia, has not been definitely determined.


Development of the Sense Organs

The organs of special sensation, like the nervous system itself, are developed from the deeper or nervous layer of the epiblast, and are continuous with their respective nerves from a very early stage in their formation. The derivation of the sense organs from the epiblast is explained by the fact that they are concerned in the appreciation of the presence and nature of external objects, and are therefore necessarily formed on the surface of the body. They are in all cases to be regarded as specially modified parts of the epidermis.


1. The Nose

The olfactory organs appear at a very early period of development, about the time of closure of the brain, as a pair of thickenings of the nervous layer of the epiblast at the anterior end of the head, lying at the sides of the fore-brain, and in front of, and slightly dorsal to, the position in which the mouth will afterwards appear.




FIG. 66. Diagrammatic horizontal section of a 12 mm. Tadpole, at the time of appearance of the hind limbs. The plane of section of the right side of the head is taken at a more dorsal level than that of the left side, x 30.

A, aorta. AC, carotid artery. ACE, pharyngeal artery. ACI, anterior cerebral artery. AP, pulmonary artery. AT cutaneous artery. EF-1, EF.2, EF.3, EF.4, efferent branchial vessels of tirst, second, third, and fourth branchial arches. GM, gloruerulus. HC-1, first branchial cleft. KA, right segmental duct. KA', hinder end of left segmental duct. KP, head kidney. KS, nephrostome. LC, laryngeal chamber. LG, lung. OC, optic cup. OF, olfactory pit. OL, lens. PA, pancreas. PD, pancreatic duct. TD, duodenum. TI, intestine.



The two layers of epiblast soon lose their distinctness in these patches ; and a pitting in of the surface, involving both layers, appears in each of the patches. The pits so formed become the nasal sacs ; the mouths of the pits forming the nostrils or anterior nares, and the epiblastic lining of the pits becoming converted into the olfactory epithelium. The condition of these pits at the time of hatching of the tadpole is shown from the surface in Fig. 72, OC, and in horizontal section in Fig. 74, OF.

The olfactory pits rapidly deepen (Fig. 66, OF), rather by the upgrowth of folds of skin round their margins than by depression of the floors of the pits themselves ; the result of this process being the formation' of a pair of deep pits, of which the inner walls are derived from the original patches of olfactory epithelium.

A short time after hatching of the tadpole, a solid rod of epithelial cells is formed by proliferation of the cells of the floor of each olfactory pit. These rods of cells grow downwards and inwards towards the roof of the pharynx, meeting and fusing with this immediately behind the septum between the pharynx and the stomatoda3um (Fig. 64). Shortly after the mouth opening is established, by perforation of this septum, these rods of cells become tubular ; and in tadpoles of 12 mm. length, in which the hind limbs are just appearing, the tubes open into the roof of the mouth as the posterior nares (Fig. 76, zi).

By further folding of the walls, and by the formation of caecal outgrowths from each sac, the complicated olfactory labyrinth of the adult is developed. A special diverticulum of the ventral wall of each sac gives rise to the organ of Jacobson.

2. The Eye

The eye differs from the other sense organs inasmuch as an accessory part, the lens, is alone formed from the surface epiblast ; while the sensitive part of the eye, or retina, arises as an outgrowth from the brain, and thus is only indirectly derived from the epidermis.

The optic vesicles have already (p. 125) been described as a pair of hollow outgrowths, which arise from the fore-brain about the time that closure of the neural tube is effected ; they project outwards at right angles to the axis of the head, their outer walls being in close contact with the epidermis of the sides of the head. Each of the vesicles becomes constricted at its base, so as to form a spherical optic bulb, connected with the fore-brain by a hollow tubular stalk. The outer wall of the bulb, which is in contact with the external epidermis, soon becomes flattened, and then thickens so greatly as almost to obliterate the cavity of the vesicle (Fig. 67, oc).

The lens. About this time a thickening of the inner, or nervous, layer of the surface epiblast takes place opposite to the centre of each optic vesicle ; this thickening increases rapidly, and at the time of hatching of the tadpole forms a solid spherical body projecting inwards from the surface ; this soon becomes hollow, by breaking down of the cells in its centre, and then separates from the surface epiblast. It may now be spoken of as the lens vesicle (Fig. 66, OL) ; in the later stages, after the formation of the mouth opening, the lens vesicle becomes solid once more (Fig. 67, OL), mainly through lengthening of the cells of its inner wall ; and by further increase in size it becomes the lens of the adult eye.


FIG. 67. Transverse section through the head of a Tadpole of 6 mm. length, about the time of hatching : the section passing through the fore-brain and the developing eyes, x 45.

AC, carotid artery. BF, fore-brain. DS, stomatoclaeal imagination. WL, cutaneous or lateral line branch of the trigeminal nerve. OC, inner wall of optic cup. OD, outer wall of optic cup. OL, lens. OS, optic stalk. PT, pituitary body. TP, pharynx. V J, jugular vein.


The optic cup. Partly in consequence of the ingrowth of the lens vesicle, but 'mainly through active growth of the walls of the optic vesicle itself, this latter becomes pitted on its outer surface, and so converted into a cup (Figs. 66, 67). This optic cup, as it is termed, has double walls : the inner wall (Figs. 66 and 67, oc) is very thick, and consists of cells arranged three or four deep ; the outer wall (Fig. 67, on) is thin, and consists of a single layer of flattened cells, in which pigment is early developed. (Of. Fig. 76, oc.)

In the later stages of tadpole life the optic cup slowly enlarges ; it remains in contact with the lens at its edge or lip, but elsewhere is separated from this by a space, which becomes the posterior chamber of the eye, and in which the vitreous body is formed.

The inner, or thicker, wall of the optic cup gives rise to the retina ; the molecular and nuclear layers, and the layers of nerve cells and nerve fibres, being formed by modification of the cells of the wall itself; while the rods and cones of the bacillary layer arise as outgrowths from its outer surface, which grow towards, and become imbedded in, processes developed from the pigmented cells of the outer wall (Fig. 67, OD) of the optic cup.

If the mode of development of the brain be called to mind, it will be seen that the layer of epithelial cells which lines the cavity, or ventricle, of the fore-brain (Fig. 67, BF) is morphologically equivalent to the outer or epidermic layer of the surface epiblast, and was originally directly continuous with this, before closure of the neural groove was effected. As the optic vesicle is an outgrowth from the fore-brain, the cells lining its cavity, i.e. the cells lining the space between the inner, oc, and outer, OD, walls of the optic cup, will be of the same nature as those lining the cavity of the fore-brain itself.

The optic nerve. The fibres of the optic nerve are developed on the inner surface of the inner layer of the optic cup, i.e. the surface next to the vitreous body, and grow inwards along the optic stalk to the brain. It follows from what has been said in the previous paragraph that this inner surface of the optic cup is morphologically equivalent to the deeper or nervous layer of the epidermis, from which we have seen that all the other nerves are developed, directly or indirectly.

Up to the time of hatching there is no trace of the optic nerve-fibres ; but shortly after this period (Fig. 66) certain of the epithelial cells at the inner surface of the optic cup become pyriform in shape, forming what are termed neuroblasts. From the narrower ends of the neuroblasts, nerve-fibres grow out which spread over the ventral edge of the optic cup, and grow back as a bundle of nerve-fibres along the ventral and posterior wall of the optic stalk, and towards the brain. The optic stalk itself apparently takes no direct part in the formation of the nerve-fibi-es ; its cavity becomes obliterated shortly after the mouth opening is established, except at the end next the brain, where the cavity persists, as the optic recess, throughout life. The rest of the stalk gradually becomes broken up, as the distance between the brain and the eye increases with growth of the tadpole.

The optic fibres reach the under surface of the brain shortly after the mouth opens, and cross over almost at once to the opposite side of the brain to form the optic chiasma.

The outer coats of the eye, choroid, sclerotic, and cornea, are formed from the mesoblast surrounding the optic cup.

The eye develops very slowly, and during the greater part of the tadpole stage of existence is in an imperfect condition ; at the time of the metamorphosis it moves nearer to the surface, and becomes a functionally more perfect organ.

3. The Ear

General account. The ears are developed as a pair of pitlike imaginations of the deeper or nervous layer of the epiblast, at the sides of the hind-brain. The invaginations do not involve the epidermic or outer layer of the epiblast, which is continued across the mouths of the pits. The auditory pits, therefore, do not, in the frog, open at any time to the exterior.

The mouths of the pits very early narrow and close, and the auditory vesicles so formed separate completely from the epiblast, and lie imbedded in the mesoblast at the sides of the head. By folding of its walls, and by the ingrowth of septa, the vesicle, from being a simple, almost spherical sac, becomes divided up into the complicated auditory vestibule of the adult.

The auditory nerve becomes connected with the inner wall of the vesicle at a very early stage, indeed almost from its first appearance ; the relations of the nerve to the wall of the vesicle being essentially similar to those between the other cranial nerves and the special patches of epiblast with which they become fused.

Certain of the accessory organs of hearing, especially the Eustachian tube and the tympanic cavity, may conveniently be described here, although they are essentially independent of the auditory apparatus, and only become secondarily connected with this.

The early development of the ear. About the time of closure of the neural groove, the auditory epithelium can be recognised as a pair of thickened circular patches of the deeper layer of epiblast, one at each side of the hind-brain, with which patches the auditory nerves are already continuous.

Soon after closure of the neural tube, in embryos of about 3 mm. length (Fig. 60), each of these patches becomes depressed, forming a shallow pit, semicircular in transverse section, and covered at its mouth by the outer layer of epiblast, which is continued over it without interruption. The pit deepens, and the mouth gradually closes by ingrowth of its lips. Shortly before the hatching of the tadpole the closure is completed, and the auditory vesicle separates from the surface epiblast.

At the time of its separation the vesicle is a closed sac, somewhat pyriform in shape ; its lower or ventral portion being spherical, and lying opposite the notochord, and its dorsal wall being prolonged upwards into a short blind diverticulum lying at the side of the hind-brain. The wall of the vesicle consists of a single layer of cubical or columnar cells ; those of the inner wall, with which the auditory nerve is continuous, being rather more elongated and more deeply pigmented than the rest.

The internal ear or labyrinth. After closure of its mouth the vesicle increases considerably in size, and becomes further separated from the surface by ingrowth of mesoblast between its outer wall and the external epiblast. Up to the time of the formation of the mouth it undergoes no further change of importance, remaining as a spherical sac with a blind dorsal diverticulum.

Shortly after the opening of the mouth, i.e. in tadpoles of from 10 to 12 mm. in length, the various parts of the internal ear become gradually differentiated, the chief process by which the changes are brought about being the formation of septa, by folding of the wall of the vesicle, which project inwards into the cavity and partially subdivide it. Mesoblast soon grows in between the two layers of each fold, the septa thereby acquiring increased thickness.

The first septum which appears divides the vesicle into its two main cavities, saccnlus and utriculus. It arises in tadpoles of about 11 mm. length as a fold of the outer wall of the vesicle, which projects somewhat obliquely across the cavity, dividing it into an upper and inner division, the utriculus ; and a lower and outer portion, the sacculus. The septum is at first confined to the hinder part of the vesicle, but soon extends all round it ; and, growing inwards, separates the two divisions almost completely from each other, a very small aperture of communication alone persisting between them.

From the utriculus, the semicircular canals are formed. Each canal is really a portion of the utriculus, which becomes partially shut off from the main cavity by the formation of a septum along the middle portion of its length ; remaining, however, in communication with the cavity at each end. Each septum is formed by two separate folds, which grow towards each other from opposite sides of the vesicle, meet along their edges, and fuse to complete the septum (Fig. 75, p. 162). The septum soon thickens, through the ingrowth of mesoblast between its layers ; it also elongates, and so causes lengthening of the canal, which gradually acquires the adult shape and relations.

Of the three semicircular canals, the anterior vertical and the horizontal are formed simultaneously, and first appear in tadpoles of about 11 mm. length. The posterior vertical canal arises in the same way, but at a slightly later stage, in tadpoles of about 15 mm. length.

The ampullae of the semicircular canals are formed later than the canals themselves, not as dilatations of the canals, but by constriction of parts of the utriculus, at the places where the canals open into it.

The second division of the vesicle, or sacculus, grows downwards, and soon acquires the pouch-like character it has in the adult. From its upper and hinder portions three small bulgings or pouch-like outgrowths appear, which together form the cochlea. Of these, the lagena cochleae is the largest and the earliest to appear, arising in tadpoles of about 15 mm. length; the pars neglecta appears shortly afterwards, and the pars basilaris last of all.


The inner wall of the auditory vesicle, facing the brain, is from the first composed of cells which are more columnar in shape than those of the rest of the vesicle (Fig. 75, EV) ; and it is with these elongated cells that the auditory nerve is connected. As the vesicle grows, and as the septa form, by which it is divided up into its various portions, the patch of epithelium with which the nerve is continuous also divides, giving rise to all the sensory patches present in the adult ear. Of these there are eight : one in each of the three ampulke of the semicircular canals, three in the cochlea, one in the wall of the sacculus, and one in that of the utriculus.

The dorsally directed diverticulum, to which the pyriform shape of the vesicle in its early stages is due, persists in the adult, and undergoes a rather remarkable development.

On the formation of the septum, dividing the vesicle into sacculus and utriculus, the divdrticulum remains in connection with the inner side of the sacculus. It elongates considerably, growing upwards close alongside the brain as the recessus vestibuli (Fig. 75, ER). In tadpoles of about 20 mm. length, the distal blind end of the recessus vestibuli dilates to form a thin-walled vesicle, lying on the roof of the fourth ventricle ; while the rest of its length forms a narrow tubular duct with rather thick walls, which connects the dilated end with the sacculus.

At the time of the metamorphosis the distal thin-walled dilatation, or saccus endolymphaticus, has increased greatly; it lies within the skull, between this and the brain, as a large sac with thin but very vascular walls, covering the roof of the hind-brain for a considerable length, and extending downwards along the sides of the brain and beneath its floor as well. The sacs of the two sides meet, both above and below the brain, and apparently open inuo each other; in their cavities abundant calcareous concretions are found.

The stalk, or ductus endolymphaticus, persists as a narrow tube, which passes through a hole in the skull wall, and connects the saccus endolymphaticus with the sacculus of the internal ear. These relations of the saccus and ductus endolymphaticus are retained in the adult frog.

In the mesoblast surrounding the internal ear the perilymph spaces are formed ; and beyond these the cartilaginous and osseous walls of the auditory capsule are laid down. (Cf. Figs. 75 and 68.)

The accessory auditory apparatus. It will be convenient to consider here the development of the Eustachian tube, and the tympanic cavity and membrane, which, though only secondary parts of the organ of hearing, are exceedingly characteristic of terrestrial Vertebrates, as contrasted with the truly aquatic Vertebrates, or Fishes.

The Eustachian tube and tympanic cavity. The details of development of these parts are not thoroughly determined.

The Eustachian tube appears first in tadpoles of about 25 mm. length, as a solid rod of epithelial cells, running forwards from the anterior and dorsal edge of the first branchial cleft,

At the time of the metamorphosis, when the fore legs are protruded, the Eustachian tube is a rod of cells with a very illdefined lumen, starting from the dorsal and anterior part of the pharynx, and extending straight forwards beneath the eye ; it is slightly dilated at its distal end, which lies opposite the anterior border of the eye.

During the metamorphosis, the Eustachian tube separates from the pharynx, and divides into a variable number of short lengths ; these gradually shift backwards to the position occupied by the Eustachian tube in the adult frog ; by the time the tail of the tadpole is completely absorbed, the several lengths unite together, and with a diverticulum from the pharynx, to form the definite Eustachian tube of the adult, which now runs almost directly outwards beneath the ear. The tympanic cavity is merely the dilated outer end of this tube, lying just beneath the surface ; and the layer of skin closing its outer end is the tympanic membrane. (Cf. Fig. 68, E, D.)

From this account it appears that the tympanic cavity does not at any period open on the surface of the head ; and it is doubtful whether the Eustachian tube in the frog has any definite relation to a gill-cleft. It is very probable that in this, as in many other features of its embryological history, the frog shows a modified rather than a primitive type of development.

The tympanic cartilage. In tadpoles of about 40 mm. length, shortly before the fore legs emerge, the tympanic cartilage appears as a dense mass of cells, surrounding the anterior end of the Eustachian tube at a time when this lies below the eye. During the metamorphosis, this ring of cells preserves its relation with the outer end of the Eustachian tube, or tympanic cavity, and gradually shifts back with this latter to its adult position. A bar of cartilage appears in its ventral portion, which gradually extends at its ends until it forms the complete annular tympanic cartilage.



FIG. 68. A transverse section across the posterior part of the head of an adult Frog, showing the position and relations of the auditory organs, Eustachian tube, and hyoid apparatus. On the right side the section passes through the tympanic cavity and the columella ; on the left side through the anterior cornu of the hyoid. The cartilage is dotted, and the bones, except the columella, represented black.

A, parasphenoid. AS, angulosplenial. B, buccal cavity. C, columella. D. tympanic membrane. E, Eustachian tube. F, anterior cornu of the hyoid. FP, frontoparietal. Q-, glottis. H, arytenoirl cartilage. I, posterior cornu of the hyoid. K, auditory nerve. L, vestibule of the ear. M, anterior vertical semicircular canal. N, horizontal semicircular canal. O. pro-otic. P. pterygoid. Q, quadrate cartilage. R, quadrate jugal. S, squamosal. T, tympanic cartilage. V, vocal cord. X, mid-brain.


The development of the auditory ossicle, or columella (Fig. 68, c), will be described in the section dealing with the development of the skull (p. 209).

4. The Cutaneous Sense Organs

During the tadpole stage, while the animal is leading an aquatic life, special sense organs in the form of small epidermal papillae are present, arranged in rows along the body, round the eyes, and on other parts of the head. They are supplied by the lateral line series of branches of the trigeminal and pneumogastric nerves, which have already been described (pp. 130, 132) ; they are lost completely at, or shortly after, the time of the metamorphosis.

The mouth of the tadpole is also provided with special papillae, probably gustatory in function, which are lost at the time of the transformation to the frog.


Development of the Alimentary Canal

1. General Account

The alimentary canal of the frog, like that of other Vertebrates, is developed in three lengths : (i) the mesenteron (Fig. 69, T), which is formed, as already described, by a process of splitting amongst the yolk-cells, and which corresponds to the mesenteron or gastrula cavity of Amphioxus : the mesenteron of the frog gives rise to almost the whole length of the alimentary canal, from the pharynx to the rectum ; and from it are developed the gill-clefts, the thyroid, the thymus, the lungs, the liver, the pancreas, and the bladder, (ii) The stomatodaeum (Fig. 69, DS) is a pitting in at the anterior end of the body, from which the mouth opening and buccal cavity are formed, and in connection with which the lips and teeth are developed, (iii) The proctodseum (Fig. 60, PD) is a pocket-like depression at the hinder end of the body, which gives rise to the anal or cloacal opening.

The mesenteron. The mode of development of the mesenteron, up to the stage shown in Fig. 55, has already been described. At its first appearance, and throughout the early stages, the mesenteron has walls of very unequal thickness ; the roof or dorsal wall (Fig. 56) being thin ; and the floor or ventral wall being of great thickness, owing to the large size of the yolkcells which form it.

After separation of the mesoblast cells as a distinct layer, and the definite formation of the notochord, this difference becomes still more marked, the roof of the mesenteron (Fig. 56, T) consisting of a single layer of hypoblast cells, while the floor is formed by the thick mass of yolk-cells ; at the sides the transition from the thin roof to the thick floor is a somewhat abrupt one.

As the central nervous system is formed, and the shape of the embryo becomes more clearly established, the mesenteron acquires more definite characters (cf. Figs. 55, T; 60, MN). By enlargement of its anterior end a wide pharyngeal cavity (Fig. Gl, TP) is formed, of which the floor and sides, as well as the roof, are formed of a single layer of hypoblast cells. The hinder or intestinal region of the mesenteron (Fig. 61, TI), has much the same relations as before, its roof being thin, but its floor and sides (Fig. 70) of great thickness. The mass of yolkcells, forming the floor of the intestinal region, becomes more compactly arranged and more definitely resti'icted ; in front it is sharply marked off from the pharyngeal region by a backwardly directed diverticulum (Fig. 60, L), which forms the first commencement of the liver ; while at the hinder end of the body, by withdrawal of the yolk-plug from the surface of the embryo (cf. Figs. 55 and 60), the posterior limit of the yolk-mass becomes clearly denned, and the short rectal diverticulum (Fig. 60, R) opened out.

At the time of hatching of the tadpole (Figs. 69 and 74), this distinction between a wide, thin-walled pharyngeal region and a narrow, thick-walled intestinal portion is very well marked, the passage from one region to the other (Fig. 74) being an abrupt one. Up to this time the alimentary canal has been perfectly straight, but shortly after hatching, and especially after the formation of the mouth, the intestinal region elongates very rapidly ; the food-yolk is speedily absorbed, and the intestine becomes a long tube, coiled in a characteristic spiral manner, and of approximately uniform diameter along its whole length (Fig. 65). Owing to this rapid elongation, and the convolutions into which it necessarily becomes thrown, the intestine, which at first is closely attached to the dorsal wall of the body cavity, immediately beneath the notochord, shifts ventralwards, remaining, however, suspended from the mid-dorsal wall of the body cavity by the mesentery.



FIG. 70. Transverse section across the middle of the length of a Frog embryo 3| mm. in length. {Cf. Figs. 58, D, and 60 for other views of embryos of the same age.) x 52.

CH, notochord. C J, subnotochordal rod. CM, myocoel. CS, splanchnoeoel. E' epiblast. KB, archinephric duct. M, mesoblast. MS, mesoblastic somite. ND, ilni-sal root of spinal nerve. ITS, spinal cord. SO, somatopleuric layer of mesoblast. SP, splanchnopleuric layer of mesoblast. T, intestinal region of mesenteron. Y, yolkcells.


At the time of the metamorphosis the alimentary canal shortens rapidly and very considerably ; and the distinction in diameter between the stomach, small intestine, and large intestine becomes much more pronounced. During these changes the entire alimentary canal is in a condition of active inflammation, and no food is taken, nutrition being effected by the gradual absorption of the tadpole's tail.

///I The stomatodaeum. At the time of hatching (Fig. 09, DS),

the stomatodaBum is a well marked though shadow pit on the under surface of the head ; its floor is in close re^tion with the anterior wall of the pharynx, the epiblast of the stomatodasal pit and the hypoblast of the pharyngeal wall being in contact with each other, without any intervening rnesoblast. From the dorsal border of the stomatodaeum, the pituitary body (Fig. 69, PT) projects inwards between the brain and the pharynx.

The stomatodagal pit rapidly deepens, not by depression of its floor, but by uprising of its walls (Fig. 64), the margins of which give rise to the lips. The septum between the stomatodaBum and the pharynx gradually becomes thinner, and in tadpoles of from 9 to 10 mm. length is perforated ; the mouth opening is thus established, and the pharynx placed in direct communication with the exterior.

In the later stages the limits of the original stomatodaeal invagination can be fairly accurately determined. In the section of a 12 mm. tadpole given in Fig. 65 the boundary is indicated by a difference in the mode of shading employed ; the epiblastic lining of the stomatodasurn is represented by a thick black line, while the hypoblastic wall of the pharynx is shown by a double, cross-hatched line. The posterior nares mark the boundary between the two regions exactly ; they open (cf. Fig. 76, zi) into the pharynx immediately behind the septum, so that a line drawn across the roof of the mouth, through the anterior borders of the narial openings, divides the stomatodaeal from the pharyngeal portion.

After the mouth opening is established, the lips of the stomatodaeum grow forwards rapidly, and in connection with them the powerful horny jaws of the tadpole, by which it crops its food, are speedily developed (Fig. 65, j).

The proctodaeum. The mesenteron, from its first appearance, and throughout the early stages of development, communicates with the exterior through the blastopore (Fig. 60, B). It also communicates, through the neurenteric canal, TS T C, with the central canal of the spinal cord and brain ; this communication persists for some time after the blastopore has closed (Fig. 61)," but is lost when the tail begins to lengthen (Fig. 69).

The proctodaeal invagination appears as a pit-like depression at the ventral end of the primitive streak (Figs. 58, B, c, D, and 60, PD). In embryos of about 4 mm. length (Fig. 61), this invagination reaches and opens into the rectal portion of the mesenteron, i.e. the portion which lies posterior to the mass of yolk-cells.

The closure of the blastopore usually occurs before the anal perforation is completed ; but it may happen that the two openings into the mesenteron are present for a time simultaneously.

In the frog this proctodeeal invagination is a new opening into the mesenteron, and is not a persistent part of the original communication of the mesenteron with the exterior, through the blastopore. If it be borne in mind, however, that the proctodasal invagination appears in the primitive streak, and as an actual deepening of the ventral end of the primitive groove (Fig. 58, B) ; and further, that the primitive streak is formed by concrescence of the lips of the blastopore, then the formation of the proctodaeal invagination may be viewed, not as an entirely independent depression of the surface, but as a re-opening of the ventral portion of the blastopore. This view is strongly supported by the development of other Amphibians, in some of which the blastopore actually persists as the anus.

It will be noticed that the proctodaeal, or anal, opening is established some time before the embryo hatches, while the stomatodaeal or mouth opening is not formed until a considerably later period. This early appearance of the proctodeeal opening is perhaps to be associated with the early formation of the kidneys, which are already present, and have ducts opening into the hinder end of the mesenteron (Figs. 69, KA, and 74, KP, KA), shortly before the time of hatching of the tadpole.

The development of the several regions of the alimentary canal, and the structures arising in connection with them, will now be described in more detail, with the exception of the gillclefts and gills, which form the subject of the next section of tliis chapter.

2. The Lips

The mouth of the tadpole is very small compared with that of the frog (cf. Figs. 85 and 86, p. 193). It is surrounded by prominent frill-like lips, which form a short conical proboscis (Figs. 83 and 85, LI, LJ). The inner surfaces of the lips bear rows of minute teeth, and at the bottom of the funnel, separating the proboscis, or labial cavity, from the buccal cavity, is the beak, formed by the two powerful horny jaws (Fig. 65, j).

There are two lips, upper and lower, which are continuous with each other at the angles of the mouth, so as to completely surround the opening. The upper lip (Figs. 65 and 83, Li) is a crescentic fold of integument bounding the labial cavity in front ; it is smaller and less mobile than the lower lip, and bears along its free edge a row of minute horny teeth. The lower lip (Figs. 65 and 83, Lj) is both longer and deeper than the upper ; it is also softer and much more mobile. It is separated behind by a well-marked transverse groove from the under surface of the head, and is produced at its free edge into a series of small fleshy papillae. These papillae, which are probably tactile in function, are more numerous at the angles of the mouth, where they are arranged in groups.

The inner surfaces of the lips, between their free edges and the beak, bear transverse ridges or folds, which support along their crests comb-like rows of minute black horny teeth. Of these rows, the upper lip, in addition to the row round the margin already mentioned, has three incomplete rows, interrupted in the middle by a considerable interval. The lower lip bears four similar but complete rows of teeth.

Each of these teeth is formed by modification of a single epithelial cell. In shape it is a hollow cone, produced at its apex into a spoon-shaped process, notched at its free edge. These horny epithelial teeth are easily rubbed off during use, and are speedily replaced by other similar ones formed beneath them. Each tooth is in fact the top member of a column of specially modified epithelial cells, imbedded in the general epithelium of the lip. In each column the deepest cells are ordinary epithelial cells, scarcely distinguishable from those in which they are imbedded : the succeeding cells of the column, nearer the surface, become first flattened, then cup-shaped, and finally conical, the apex of the cone fitting into the cavity of the cell next above it.

The deeper cells of the column are soft, and have distinct nuclei ; nearer the surface the cells have their outer layers converted into horny matter, while their shape gradually approaches that of the fully formed teeth. The nucleus becomes less distinct, and finally disappears, as the cornificatioii extends deeper and deeper into the substance of the cell.

Each tooth is thus formed by cornification of a single epithelial cell, which commences its career in the deeper lay er of the epidermis, at the base of the column, and gradually approaches the surface through loss of the teeth above it, acquiring, as it does so, the characters of the fully formed tooth. On reaching the surface it comes into functional use for a time, and then in its turn becomes rubbed off and lost.

3. The Beak

The beak consists of the two jaws, upper and lower, and is in shape not unlike that of a bird or turtle (Figs. 65 and 71). Each jaw is a strong, curved band of cornified epithelium, supported at its base by the labial cartilages (Fig. 90, LU, LL), and ending at its free surface in a sharp biting edge. The upper or maxillary jaw (Fig. 65) is longer and less sharply curved ; the lower or mandibular jaw, which bites behind the upper jaw, is shorter, stronger, and almost horse-shoe shaped in outline.

The minute structure of the two jaws is the same, each consisting of modified epithelial cells. The cutting edge of the jaw is formed by a row of horny teeth, very similar to those of the labial rows, but placed so closely side by side as to form a continuous blade. Each of these teeth is, as in the case of the labial teeth, the uppermost of a column of cells, the more deeply placed members of which are indifferent epithelial cells, but which as they approach the surface become first flattened, then cupped, and finally hollow cones fitting into one another. As in the labial teeth, the hardness is due to cornificatiou of the cells, invading first the outer surface and ultimately the entire cell. As the biting edge of the jaw gets worn away by use, it is constantly renewed by the more deeply placed cells.

The rest of the jaw consists of a dense mass of flattened and cornified epithelial cells, which become firmly fused together, and which, like the cells of the cutting edge, are renewed from the indifferent epithelial cells of the deeper layers. Into this deeper layer vascular papillas of the dennis project, increasing the extent of the nutritive surface of the jaw.

At the metamorphosis the horny jaws are cast off, and lost.

4. The Pharynx

The characteristic feature of the pharynx, both in the tadpole and in the adult frog, is its great width from side to side (cf. Figs. 74 and 68) ; and this is acquired, as already described, at a very early developmental stage. In horizontal section the pharynx of the tadpole is somewhat lozenge-shaped (Fig. 74), narrowing rather gradually in front to open into the buccal cavity, and much more abruptly behind, where it passes back into the oesophagus.

The roof of the pharynx may be divided into two regions : an anterior part, clothed by a flattened pavement epithelium, and bearing taste bulbs and sensory papillae ; and a posterior part, covered by a ciliated epithelium, and containing numerous multicellular glands.

The gills, which are the most important structures in connection with the sides of the pharynx, will be described in the next section (pp. 157 to 163).

The tongue is formed on the floor of the pharynx, but does not appear until shortly before the metamorphosis ; it then grows rapidly and soon attains its adult shape and proportions (Fig. 89, TN).

5. The Thyroid Body

About the time of hatching of the tadpole, or a little earlier, a short median longitudinal groove appears along the floor of the pharynx (Fig. G9, TH). The groove is shallow anteriorly, but deepens at its hinder end, where it leads into a small, conical, pitlike depression of the hypoblast forming the pharyngeal floor, just in front of the pericardial cavity (Fig. 69, CP.)

At a later stage, shortly before the opening of the mouth, the median groove is still present. The pit at its hinder end has deepened slightly, and the hypoblast cells, forming the floor of the pit, have grown back as a solid rod of cells (Fig. 64, TH), closely connected at its hinder end with the anterior wall of the pericardium ; this solid rod of cells becomes the thyroid body.

Soon after the mouth opens, the thyroid body separates completely from the floor of the pharynx, remaining as a solid rounded mass of pigmented cells, in close contact with the anterior wall of the pericardium. A little later, in tadpoles of about 12 mm. length (Fig. 65, TH), the thyroid body becomes divided into right and left halves by the growth downwards of a median keel from the basihyal cartilage (Fig. 65, HB). The two halves remain connected by a narrow bridge of cells below the cartilage for a short time, but soon separate and become the paired thyroid bodies of the adult frog.

After their separation the thyroid bodies increase considerably in size ; they are at first solid, but the component cells soon become arranged iru strings, which become hollowed out along their axes, and so form a series of rounded or oval vesicles, which communicate freely with one another, and are filled with fluid.

The thyroid bodies are very vascular ; they lie in the floor of the mouth, a short way in front of the glottis, immediately to the inner sides of the lingual arteries, which supply them, and along the course of the lingual veins.

6. The Oesophagus

The oesophagus is formed from the most anterior part of the narrow or intestinal region of the mesenteron, and leads directly from the pharynx. It is at first tubular, but in tadpoles of about 8 mm. length, shortly before the opening of the mouth, the cavity of the oesophagus becomes completely blocked up, by proliferation of the cells forming its walls (Fig. 64, TO). This solid portion of the oesophagus lies immediately behind the pharynx, and has a length of about O15 mm. The solid condition lasts for a little time after the opening of the mouth ; and then, in tadpoles of about 10^ mm. length, the lumen is gradually re-established, though it is for a time exceedingly narrow.

This blocking up of the oesophagus, which prevents any food getting into the digestive part of the alimentary canal until some little time after the mouth opening is established, is a curious developmental feature ; it occurs also in the chick and in many other Vertebrates, but its meaning has not yet been explained satisfactorily.

7. The Lungs

The lungs arise as a pair of pouch-like diverticula of the side walls of the oesophagus, shortly before the hatching of the tadpole ; they are at first exceedingly small, and have strongly pigmented walls. After hatching, the lungs increase slowly in size, growing backwards along the sides of the oesophagus ; in 9 mm. tadpoles, at the time when the oesophagus is solid, the lungs are present as a pair of lateral outgrowths immediately behind the oesophageal plug (Fig. 64, TO), but sometimes arising from the solid part itself. After the re-opening of the oesophagus, the part of the ventral wall from which the lung sacs arise becomes depressed to form the laryngeal chamber : the mouth of the depressed portion narrows to form the glottis, and the lungs themselves rapidly increase in size.

In 12 mm. tadpoles, in which the hind limbs are just appearing (Figs. 65 and 75), the glottis is a narrow slit-like opening, guarded in front by a well-developed epiglottis, and leading into a large laryngeal chamber (Fig. 65, LC), from which the two lungs arise; these latter are thin-walled vascular sacs (Fig. 76, LG), which now reach to the hinder end of the body cavity, lying along the sides of the alimentary canal.

From their mode of development as outgrowths of the oesophagus, it follows that the lungs are lined by an epithelium which is of hypoblastic origin ; the connective tissue and vascular elements of the lung wall are, like those of other parts of the body, mesoblastic.

8. The Liver

About the time of first appearance of the nervous system, the yolk-mass becomes marked off in front by a deep, backwardly projecting depression (Fig. 60, L), from the thin-walled anterior region of the mesenteron. This depression becomes still more marked in the later stages (Fig. 69, w) ; and from its anterior wall the liver is developed.



FIG. 71. Horizontal section of the head and body of a 12 mm. Tadpole; drawn from the dorsal surface, x 27.

AF.l, 2, 3, 4, afferent branchial vessels of first, second, third, and fourth branchial arches. BR.3, cartilaginous bar of third branchial arch. EF.l, efferent branchial vessel of first branchial arch. HB, basihyal cartilage. HY, cartilaginous bar of hyoid arch. J, jaw. KA, posterior end of archinephric duct, opening into cloaca. WD, bile duct. 'WGr, gall bladder. Z, commencing hind limb.


This anterior wall becomes early invested by mesoblast on its outer surface, and in this mesoblast numerous blood-vessels of large size are developed. The wall now becomes thrown into folds (Fig. 64, w) ; the blood-vessels following in between the folds. By a continuation of this process, accompanied by the formation of outgrowths from the hypoblast cells, and ingrowth of the blood-vessels, the liver rapidly increases in size and acquires the structure shown in Fig. 71, w; consisting of a trabecular framework of solid rods of hypoblast cells, the meshes of the framework being occupied by the hepatic blood-vessels. As the liver attains definite shape and increased size, it separates more distinctly from the intestine, remaining, however, connected with this by the bile-duct, which is formed by lengthening out of the original diverticulum from the mesenteron. The gallbladder is a lateral outgrowth from the bile-duct ; it develops at an early period (Fig. 64, WG), and is of large size during the whole of tadpole life (Fig. 71, WG).

9. The Pancreas

The pancreas develops as a pair of hollow outgrowths from the mesenteron, behind the liver. In the later stages (Fig. 71. PA), the ducts shift so as to open into the bile-duct instead of, as at first, directly into the intestine.

The secreting cells of the pancreas, like those of the liver, are of hypoblastic origin.

10. The Bladder

The bladder is absent during the greater part of the tadpole period; but shortly before the metamorphosis it arises as a median ventral outgrowth from the hinder end of the mesenteron, which soon becomes bifid distally (Fig. 89, TB).

11. The Post-anal Gut.

Post-anal gut is the name given to an extension of the hinder end of the mesenteron into the base of the tail, which appears as this latter is developed.

The mode of formation of the neurenteric canal as a tubular communication between the hinder end of the neural canal and the mesenteron has already been described (cf. Fig. 61, NT). As the tail lengthens, the notochord and spinal cord grow backwards with it, and the neurenteric canal becomes drawn out into the post-anal gut. This is an evanescent structure, disappearing completely at a very early stage : at the time of hatching of the tadpole (Fig. 69), the only trace of the post-anal gut is a solid cord of cells, running in a slightly irregular course beneath the notochord, from the hinder end of the sprnal cord to the mesenteron.


Development of the Gill-Clefts and the Gills

The gills and gill- clefts, which form the main respiratory apparatus of the tadpole, are developed in connection with the side walls of the pharynx. The gill-clefts are a series of slit-like perforations in these walls, leading from the pharynx to the exterior ; while the gills themselves are vascular tufts developed on the gill-arches, i.e. on the parts of the pharyngeal wall between the successive gill-clefts.


FIG. 72. Side view of a Tadpole at the time of hatching, x 16. FIG. 73. Ventral view of the same Tadpole.

BR.l, external gill of first branchial arch. BR.2, external gill of second branchial arch. DS, stomatodaeal pit. MT, mesoblastic somites seen through the skin. OC, olfactory pit. Q, sucker. TJ, proctodseal or cloacal aperture.


1. The Gill-clefts

The gill-clefts are formed as vertical, pouch-like foldings of the side walls of the pharynx (Fig. 74, HM. HC), which grow outwards towards the exterior. They appear first at a very early stage, while the blastopore is still open (Fig. 60), and even before the closure of the neural canal is completed ; they develop rapidly, reaching the external epiblast, and fusing with it, at an early stage.


FIG. 74. Horizontal section of a Tadpole at the time of hatching, x 40.

AF, afferent branchial vessel of first branchial arcli. BF. fore-brain. BB..1, first branchial arch. BK-2, second branchial arch. BR.3, third branchial arch. C, body cavity or coelnm. EF, efferent branchial vessel of first branchial arch. HM, hyornandibular gill-pouch. HY, hyoid arch. IN, infundibulum. KA, archinephric duct of right side. KA', archinephric duct of left side, seen in section. KP, head kidney or pronephros. KS, third nephrostome of right pronephros. KS', third nephrostome of left pronephros, seen in section. OF, olfactory pit. OS, optic stalk. TP, pharyngeal region of meseuteron. TI, intestinal region of inesenttron. Y, yolk-cells.


In tadpoles of 3 mm. length there are three pairs of gillpouches present, which appear almost simultaneously ; and by the time of hatching of the tadpole two additional pairs are formed behind these, making five pairs in all.

The condition at this stage is well shown in the horizontal section given in Fig. 74. The gill-pouches form vertical partitions, radiating outwards from the pharynx to the surface epiblast. Each pouch is formed of a double fold of hypoblast, the two layers of which are in close contact with each other. The outer ends of all five pairs of gill-pouches reach the epiblast, and fuse with its inner or nervous layer.

Of the five pouches of each side, the most anterior one is the hyomandibular pouch or cleft (Fig. 74, ELM), and the succeeding ones are named first, second, third, and fourth branchial pouches respectively : the hindmost or fourth branchial pouch (Fig. 74, HC.4) is smaller than the others, and is often imperfectly developed at this stage..

The parts of the wall of the pharynx between the successive gill-pouches are spoken of as the visceral or gill arches. The arch between the hyomandibular and the first branchial pouches is named the hyoid arch (Fig. 74, HY) ; and then in succession come the first branchial arch, ER.I : second branchial arch, BR.2, and third branchial arch, BR.S. Behind the fourth branchial pouch, HC.4, is an imperfectly defined fourth branchial arch.

The pharynx is widest opposite the first branchial arches ; and between the pair of fourth branchial arches it passes back into the narrow oesophagus.

About the time of formation of the mouth, the two hypoblastic lamellse, of which each gill-pouch consists, separate from each other, so as to form a narrow vertical slit, or chink, leading from the pharynx to the exterior. These slits are the gillclefts.

The first clefts to open in this way are the second and third branchial clefts, i.e. the ones immediately behind the first and second branchial arches respectively. At a slightly later stage the first branchial cleft, between the hyoid and first branchial arches, also opens in a similar way ; and later still the fourth, or hindmost branchial cleft opens.

The hyomandibular pouch, although it is in its early stages exactly like the hinder branchial clefts, and is fused in similar manner with the external epiblast, yet does not open to the exterior. Shortly before the mouth opening is established, the hyomandibular gill-pouch separates from the external epiblast and recedes somewhat from the surface. The two hypoblastic lamella? separate from each other, so as to form a saccular diverticulum from the pharynx, and this gradually opens out into the cavity of the pharynx, and in tadpoles of about 20 mm. length ceases to be recognisable as a distinct pouch.

The Eustachian tube and tympanic cavity are formed near to the hyomandibular pouch, but independently of it, and in a manner which has already been described in the section dealing with the development of the ear (p. 143).

2. The Gills

There are two sets of gills in the tadpole, external and internal respectively ; the former being branching processes projecting outwards from the first three branchial arches on each side, while the internal gills are formed later as vascular tufts on the sides of all four branchial arches. The two sets of gills differ in some important respects, and it is generally considered that they are independent series of structures.

The external gills appear shortly before the time of hatching, as two pairs of small, backwardly directed processes from the first and second branchial arches. They are at first somewhat conical in shape, with rounded or very slightly notched borders : the gill of the first arch overlaps that of the second arch, and is placed rather more ventrally than this latter.

By the time of hatching (Figs. 72 and 73, BR.I, BR.2), the external gills have increased in size. The first one is notched at its free posterior border into three blunt lobes ; and the second into two or three similar ones.

In the succeeding stages the external gills grow rapidly, and the lobes into which they are divided become larger and more numerous. A third external gill appears on the third branchial arch of each side (Figs. 73, 74) : it is very small, and is overlapped and almost concealed by the two anterior gills.

The external gills attain their maximum development about the time of opening of the mouth. At this stage (Figs. 44, 5, and 77), they form much-branched plumose tufts, exceeding in length the transverse diameter of the head. Each of the two anterior gills consists of from five to seven main lobes, decreasing in size from above downwards ; and each main lobe gives off minor lobes along its posterior border. The third or posterior gill (Fig. 77) is much smaller than the other two, and only slightly subdivided.

The external gills are usually carried projecting outwards and backwards from the head, at an angle of about 45 with the -axis of the body. Each gill has, however, muscles of its own, by means of which the entire gill or its individual lobes can be moved freely and independently.

The course of the circulation in the external gills can be well studied in the living animal. Each main lobe, and each of its minor lobes, contains two blood-vessels, afferent and efferent, which lie alongside each other and are directly continuous at the tip of the lobe ; the afferent vessel being posterior, and in part ventral to the efferent vessel (Fig. 77, AF and EF).

Before the mouth opens, the opercular folds arise, as a pair of folds of skin from the posterior edges of the hyoid arches, which soon become continuous with each other across the ventral surface of the head. Shortly after the formation of the mouth, the opercular fold begins to grow back rapidly, covering over the gills like a hood. The posterior border of the fold fuses with the body wall along the right side, and across the ventral surface : on the left side of the body it remains free, and is prolonged backwards as a short tubular spout (Fig. 71, OP), through which the opercular cavity opens to' the exterior. After completion of the opercular fold the external gills rapidly shrink up, those of the left side persisting longer than those of the right side, and often protruding for a time through the opercular spout.

External gills occur in the adult or in the larval stages of most, though not of all Amphibians. Their morphological value has been much discussed, and it is commonly held that they are to be regarded as secondarily acquired or larval organs, essentially different in their nature to the internal gills.

The internal gills. In tadpoles of from 9 to ] mm. length the mouth opening is formed, by perforation of the oral septum {p. 148, and Fig. 64, DS) ; and about the same time the gill-clefts open to the exterior. Almost directly after the opening out of the gill-clefts, the internal gills begin to form, as a series of small papilke along their margins, ventral to the external gills : the tadpole now begins to breathe in the typical fish-like manner, taking in water at its mouth, and passing it through the gill-clefts, and so over the internal gills, into the opercular cavity, from which it escapes by the opercular spout.


FIG. 75. Transverse section through the head of a 12 mm. Tadpole ; the section passing through the auditory organs, the pharynx and internal gills, the glottis and laryngeal chamber, and the heart, x 40.

A, aorta. AF, afferent blood-vessel of second branchial arch. BH. hind-brain. BR.l, .2, .3, .4, first, second, third, and fourth branchial arches. CH, notochord. CP, pericardia! cavity. EA, anterior vertical semicircular canal. EF, efferent bloodvessel of second branchial arch. EH, horizontal semicircular canal. ER. recessus vestihuli. EV. vestibule of ear. Q-I, internal gills. HC.2, second branchial cleft. LC, liirynjreal chamber. LT, glottis. LY. lymphatic space. OP, opercular cavitv. RA, auricle of heart. RV, ventricle. TP. "pharynx. V.4, fourth ventricle. X'. Hmroid plexus of fourth ventricle. VIII, auditory nerve.

The internal gills rapidly increase in size, and branch so as to form plumose tufts arranged in a double row along the ventral half of each of the first three branchial arches, and a single row along the fourth arch (cf. Figs. 75 and 83). From their first appearance the internal gills are very vascular, receiving branches from the afferent and efferent branchial vessels, which are connected by capillaries in the gill-tufts themselves.

The relations remain much the same up to the time of the metamorphosis, the gills forming a series of vascular tufts arranged in double rows along the ventral surfaces of the gill arches (Fig. 75, Gi), and hanging down into the opercular cavity, which they in great part fill. The dorsal or pharyngeal borders of the gill ai'ches develop a complicated system of tooth-like processes, which form a filtering or straining apparatus, preventing the passage of food from the pharynx through the gillclefts. This is still further obviated by a pair of velar plates, anterior and posterior, on each side of the floor of the pharynx, which cover over the gill-arches, and separate them from the pharyngeal cavity ; a rather narrow slit is left between the edges of the two plates of each pair, for the passage of water from the mouth to the gill-clefts, for the purpose of respiration.

The disappearance of the gills. Towards the end of the tadpole period of existence, large numbers of lymph follicles form on the inner surface of the opercular membrane ; and at the same time a great proliferation of epithelial cells takes place from the epithelium of the opercular membrane, and from the gills themselves. On the gills the cells become cubical, and then by rapid division form layers several cells thick. In this way, by thickening of its walls, the opercular cavity becomes greatly reduced in size, and ultimately completely blocked up. The gillclefts become closed, by fusion of their walls with one another ; and the gills themselves, with the branchial cartilages, and the entire gill apparatus, degenerate and are rapidly absorbed.

Portions of the ventral ends of the gills persist, even in the adult, as a pair of soft, lymphoid bodies, reddish in colour, which lie at the sides of the larynx, just behind the thyroid bodies, and a little further apart than these. They are sometimes spoken of as tonsils.

Remnants of the dorsal ends of the gills also persist for a time as a pair of compact lymphoid masses, lying immediately beneath the skin, and just behind the ears ; they usually disappear in the course of the second year.

3. The Thymus

The thymus arises in tadpoles of about 8 mm. length, shortly after hatching, as a pair of epithelial buds from the wall of the pharynx, opposite the dorsal ends of the first branchial clefts. Soon after the opening of the mouth, these buds separate from the epithelium as a pair of solid rounded bodies, formed of deeply-staining epithelial cells, which lie imbedded in the roof of the mouth, below the anterior ends of the auditory vesicles, and between the ganglia of the facial and glosso-pharyngeal nerves.

In each thymus a distinction early appears between an outer cortical layer of small deeply pigmented cells, and a central medullary portion consisting of large pale granular cells. At a later stage the distinction becomes less evident, owing to the cortical cells extending inwards through all parts of the thymus.

The thymus lies behind the quadrate cartilage, and is carried backwards by the rotation of this cartilage which accompanies the widening of the mouth at the time of the metamorphosis. The thymus is larger in the tadpole than in the frog, and undergoes degenerative changes after the metamorphosis. In the frog it lies behind the ear and the tympanic membrane, and slightly ventral to these.

Buds similar to those from which the thymus is formed are developed opposite the dorsal ends of the hyomandibular clefts, simultaneously with the thymus buds ; and at a slightly later stage opposite the second and third branchial clefts as well. These all disappear before the metamorphosis and take no part in the formation of the adult thymus.

4. The Post-branchial Bodies

A pair of small diverticula of the floor of the pharynx arise, in tadpoles of about 8 mm. length, behind the last gill-clefts, and at the sides of the glottis. These soon separate from the epithelium as a pair of small vesicular bodies, lined by cylindrical epithelium. ; they disappear shortly after the metamorphosis. It is possible that they represent, in a modified form, a fifth pair of branchial clefts.


Development of the Heart and Bloodvessels

1. Preliminary Account

The blood-vessels arise in the inesoblast. In most parts of the body of the tadpole they appear first as irregular spaces or lacunae, formed by separation of the mesoblast cells from one another. These lacunar spaces are at first independent, but soon extend so as to meet and open into one another as irregular channels. The cells surrounding these channels assume more definite arrangement and character, and in this way the channels become converted into blood-vessels. The blood corpuscles are either cells which are inclosed from the first within the lacunar spaces, or more usually are cells budded off at a later stage from the walls of the vessels into their cavities.

Each blood corpuscle is a single cell. In the early stages of development all the blood corpuscles of the frog embryo are alike, consisting of spherical cells in which are imbedded numerous yolkgranules. These yolk-granules are gradually used up for the nutrition of the embryo, and shortly after the hatching of the tadpole the corpuscles begin to acquire the shape and characters of the red blood corpuscles in the adult frog.

The chief point of interest in the development of the bloodvessels of the frog is afforded by the changes which occur during the transition from the gill-breathing to the lung-breathing condition.

While the tadpole is breathing by means of gills its circulation is in all essential respects that of a fish. The venous blood, returned from the body at large, enters the posterior end of the heart, or sinus venosus : from this it passes into the second or auricular chamber, thence to the ventricle, and from that to the truncus arteriosus (Fig. 64). The blood passes through the several cavities in succession, there being as yet no division between the right and left sides of the heart.

The truncus arteriosus divides distally into right and left branches, from each of which four afferent branchial vessels (Fig. 76, AF) arise. The four vessels of each side run outwards along the hinder borders of the four branchial arches, giving off' along their whole length numerous branches to the gill-tufts on these arches. From the gills the blood, now aerated, passes into the efferent branchial vessels (Fig. 76, EF). These lie alongside the afferent branchial vessels, and just in front of them, but do not communicate with them except through the capillaryloops of the gills.


The four efferent branchial vessels of each side unite in the dorsal wall of the pharynx to form the aorta : the two aortas are continued forwards to the head as the carotid arteries, while posteriorly they unite to form the single dorsal aorta, from which branches arise supplying all parts of the body.

The lungs arise at a very early stage, but are for a long time extremely small and of little functional importance. Each lung receives blood from a branch of the fourth efferent branchial vessel (Fig. 76, AP), and returns it directly to the auricle by a pulmonary vein, VP. As the tadpole increases in size, and the lungs become of greater importance, a septum appears, dividing the auricle into systemic or venous, and pulmonary or arterial cavities. Simultaneously with this, valves are formed in the truncus arteriosus, by which the venous and arterial streams of blood are kept apart to a certain extent.

At the time of the metamorphosis the gill circulation is cut off, by the establishment of direct communications between the afferent and efferent branchial vessels, and the pulmonary circulation becomes of much greater importance than before.

2. The Heart

The heart lies at first (Fig. 69, p. 146) on the under surface of the head, below the floor of the pharynx, above and slightly behind the sucker, and immediately in front of the commencing liver.

In this region the mesoblast, as in the body generally (Fig. 70, so, SP), is split into somatic and splanchnic layers, separated by a distinct space. This space becomes the pericardial cavity ; the outer or somatic layer of mesoblast forming the wall of the pericardial cavity ; and the inner or splanchnic layer giving rise to the muscular wall of the heart.

The endothelial lining of the heart is derived from a number of scattered cells, which appear below the floor of the pharynx, and which are formed partly, if not entirely, by direct proliferation of the hypoblast cells of the pharyngeal wall and of the liver (c/. Fig. 69). These cells are at first irregularly arranged, but soon become disposed so as to form a tubular lining to the heart, which is for a time closed in front, while its posterior wall is formed by the anterior surface of the liver diverticulum (Figs. 64 and 69).

The heart remains attached at its hinder end to the liver, and in front to the floor of the pharynx ; but along the rest of its length it becomes free, and increasing rapidly in length becomes twisted on itself in a letter S shape. At the same time, constrictions appear, partially dividing the cavity into chambers, the first loop of the S forming the auricular, the second the ventricular portion of the heart ; while the posterior jtnd anterior limbs become the sinus venosus and truncus arteriosus respectively (Fig. 64).

At the time of opening of the mouth the heart is still more markedly twisted on itself, and the successive chambers more sharply separated from one another; and a little later a septum grows down from the dorsal wall of the auricle, dividing its cavity into a small left auricle and a much larger right auricle.

The condition of the heart in tadpoles of 12 mm. length is shown from the right side in Fig. 76, p. 166 ; in sagittal section in Fig. 65, p. 121 ; and in horizontal section in Fig. 71, p. 155. The sinus venosus, or proximal division of the heart, is a wide transverse vessel (Fig. 71, RS), which runs across the hinder and dorsal part of the pericardial cavity, and receives the blood returning from the body generally.

The sinus venosus opens in front by a large round median aperture into the right auricle (Figs. 65 and 71, RA). From the auricle the blood passes through a narrow auriculo-ventricular aperture (Fig. 65) into the ventricle, which receives also the blood from the smaller left auricle. The cavity of the ventricle is much subdivided by muscular trabecula?. which, growing inwards from its walls (Fig. 65 and 75, RV). branch and unite to form a kind of spongework, in the meshes of which lie the blood corpuscles.

From the ventricle a small aperture leads into the truncus arteriosus. This latter is divided into proximal and distal parts, by a pair of valve-like folds, just before the point where it bifurcates into right and left branches ; of these, the proximal part, which becomes the pylangium of the adult, is partially subdivided by a longitudinal fold, which runs along its interior in a somewhat spiral course. It is difficult to imagine that these valves can play any part in directing the blood into one pair of afferent branchial vessels rather than another ; but it is significant that they should appear just at the time when the auricular septum is being completed and the lungs are coming into use.

At the time of the metamorphosis the condition of the heart is practically that of the adult. The proximal and distal parts of the trillions arteriosus, or pylaiigium and synangium, are now separated by three pocket valves in place of the two simple valves originally present ; the spiral valve of the pylangium is more strongly developed than before ; and the synangium is divided internally into anterior and posterior portions, the former communicating with the first and second pairs of aortic arches, and the latter with the third and fourth pairs.

The mode in which the thickening of the wall of the ventricle is effected, by the formation of a muscular reticulum within the cavity, and not by a simple increase in thickness of the wall itself, is of interest, inasmuch as it explains why the ventricle of the frog's heart has no nutrient blood-vessels. The blood within the ventricle occupies the meshes of the muscular reticulum and so comes in close contact with all parts of the ventricular walls. a condition which renders special nutrient vessels unnecessary.

The pericardial cavity, in its early stages, communicates freely with the general body cavity, of which it is merely the anterior portion. Owing to the great bulk of the mass of yolk cells, the body cavity in the abdominal region of the embryo is at first merely a narrow chink (Fig. 70, cs) ; while the pericardial cavity is already a space of considerable size.

Later on, and especially as the large veins opening into the sinus venosus increase in size, the opening between the pericardial cavity and the general body cavity becomes much reduced ; but up to the time of the metamorphosis there is free communication between the two cavities, through a pair of apertures at the dorsal and posterior border of the pericardial cavity, close to the sides of the laryngeal chamber.

3. The Branchial Blood-vessels

The blood-vessels of the pharynx have close relations with the visceral arches, into which the side walls of the pharynx are divided by the gill-clefts.

The first vessels to appear in the body, with the exception of the heart and the great veins opening into it, are the dorsal aorta?. These arise on each side as a series of isolated lacunar spaces along the roof of the pharynx, which by opening into one another form a pair of longitudinal vessels ; these soon extend backwards along the body, but remain for some time distinct from each other.



FIG. 77. Diagrammatic figure of the head and anterior part of the body of a 7 mm. Tadpole, shortly after batching ; showing the branchial bloodvessels from the ventral surface. The heart has been removed, x 35.

FIG. 78. Diagrammatic figure of the same embryo from the right side. The heart is represented in situ, but the external gills of the first and second branchial arches have been cut off short at their bases, x 35.

A, dorsal aorta. AB, basilar artery. AC, carotid artery. AF.l, AP.2, AF.3, afferent branchial vessels of first, second, ami third branchial arches. AP, pulmonary artery. AR, anterior cerebral artery. AT, anterior palatine artery. CA. anterior commissural vessel. CP, posterior commissural vessel. EF.l, EF.2, EF.3, EF.4, efferent branchial vessels of first, second, third, and fourth branchial arches. EH, efferent vessel of hyoid arch. EM, efferent vessel of mandibular arch. GE, external frills. G-M, glomerulus. KA, segmental duet. KP, head kidney or pronephros. KS.l, XS.3. first and third nephrostomes of head kidney. LV.4, efferent lacunar vessel of fourth branchial arch. BA, auricle. RV, ventricle. R.T, truneus arteriosus. VD, Cuvierian vein. VH, hepatic veins. VK, vein of sucker. VM, mandibular vein. VY, hyoidean vein.


In the four branchial arches, blood-vessels are formed on a definite plan. In the first and second branchial arches these vessels appear immediately after the dorsal aortas, and are well established at the time of hatching ; in the third and fourth branchial arches they arise in a similar manner, but at a somewhat later stage. In the hyoid and mandibular arches, vessels comparable to those of the branchial arches appear at an early stage : these, however, never quite conform to the type seen in the branchial arches, and early undergo degenerative changes.


FIG. 7!). A diagrammatic transverse section through the head of a 7 mm. Tadpole, seen from behind ; the section is taken just behind the auditory vesicles, and passes through the first branchial arch on each side. On the right side both the afferent and efferent vessels of this arch are shown ; on the left side the greater part of the afferent vessel has been removed in order to expose the efferent vessel more thoroughly, x 50.

A, aorta. AF.l, afferent vessel of first branchial arch. BH, medulla oblongata. CH, notochonl. CP. pericarilial cavity. EF.l, efferent vessel of first branchial arch. Gr, capillary loop of gill, connecting the afferent anil efferent vessels together. Q,, sucker. RT, truncus arteriosus. TP, pharynx. V, inferior jugular vein. VJ, anterior cardinal vein. V.4, fourth ventricle. XL, pm.'iniioira.stric nerve.



a. The vessels of the first branchial arch may conveniently be taken as typical of the series. The vessels proper to the arch are derived from four factors : (i) an efferent lacunar vessel, which appears in the mesoblast opposite the base of the external gill, and may be recognised in tadpoles some little time before hatching ; (ii) an efferent diverticulum from the dorsal aorta ; (iii) an afferent diverticulum from the truncus arteriosus ; (iv) an afferent lacunar vessel, which lies opposite the base of the external gill, immediately behind the efferent lacnnar vessel.

These four vessels appear in the order given above ; they are at first quite independent of one another ; and, for some time after their first appearance, the lacunar vessels, afferent and efferent, have no connection with any other vessels.

The efferent lacunar vessel grows rapidly ; it extends dorsally until it meets with, and opens into, the efferent diverticulum from the aorta ; and it extends ventrally towards, but not to meet, the truncus arteriosus. It is widest in the middle part of its course, opposite the external gill ; and here it becomes connected with the afferent lacunar vessel by capillary loops in the substance of the gill. This is the condition reached at the time of hatching.

Shortly after this, the afferent lacunar vessel and the diverticulum from the truncus arteriosus grow towards each other and unite. The circulation in the gill is now definitely established (Figs. 77 and 78) ; the blood passes from the heart to the truncus arteriosus, RT. and from this along the afferent diverticulum and the afferent lacunar vessel, which now form one continuous afferent branchial vessel, AF, to the gill loops, in which it becotnes aerated ; from the gill loops it passes along the efferent lacunar vessel and efferent diverticulum, which form a continuous efferent branchial vessel, EF.i, to the dorsal aorta.

As the external gill increases in size, and becomes fimbriated or lobed at its margin, the original capillary loops become lengthened out, and additional ones are developed; but the afferent and efferent vessels remain connected by capillaries alone, and it is only by passing through the gill capillaries that blood can get from the heart to the aorta.

At a later period of tadpole life, shortly after the mouth opening is established, the internal gills are developed on the gill arch as a double row of branching tufts, ventral to the external gill. Capillary loops soon appear in these tufts, forming a series of capillary connections between the afferent and efferent branchial vessels, . similar to those in the external gill, but situated more ventrally. At the same time the external gill diminishes considerably in size.

The next change of importance is the establishment of a direct connection between the afferent and efferent branchial vessels. The two vessels (Figs. 77 and 79, AF.I and EF.l) lie alongside each other in the arch, the afferent being the posterior of the two. In tadpoles of about 12 mm. length, in which the sucker is disappearing, and the hind limbs are present as a pair of small rounded papillae at the base of the tail, a direct communication is established between the ventral ends of the afferent and efferent vessels, close to the truncus arteriosus, (Fig. 80). The precise mode in which the communication is established will be described in the section dealing with the development of the carotid gland (p. 181). As the communication is ventral to the gills, both external and internal, any blood which passes across it will get from the heart direct to the aorta, without passing through any part of the gill circulation, i.e. without being aerated ; and the efficiency of the gill respiration will consequently be impaired in direct proportion to the amount of blood which takes this short cut in preference to the circuitous route through the gill capillaries.



FIG. 80. Diagrammatic figure of the head of a ]2 mm. Tadpole from the right side, showing the heart and branchial blood-vessels. The capillary loops of the gills are omitted, x 33.

A, aorta. AB, basilar artery. AF-1, AF.2, AF.4, afferent branchial vessels of first, second, anil fourth branchial arches. AL, lingual artery. AP, pulmonary artery. AR, anterior cerebral artery. AS, posterior palatine artery. AT, anterior palatinp artery. ATT, cutaneous artery. AY, pharyngeal artery. CA, anterior cornmissnral vessel, seen in section. CGr, bulb-like ililatatioii on the lingual artery. OP, posterior commissural vessel, seen in section. EF.l, EF.2, EF-3, EF.4, efferent branchial vessels of first, second, third, and fourth branchial arches. QM, glorneralus. RA, right auricle. RB, left auricle. RT, truncus arteriosus. RV, ventricle. VD, Cuvierian vein. VH, hepatic vein. VI, posterior vena cava. VP, pulmonary vein.


The subsequent changes in the vessels of the first branchial arch may conveniently be considered after the vessels of the other arches have been described.

b. The vessels of the second branchial arch (Figs. 77, 78, and 80, AF.2, EF.2) develop in exactly the same way as those of the first branchial arch, and almost simultaneously with these.

c. The vessels of the third branchial arch (Figs. 77, 78, and 80, AF.3, EF.S) are formed rather later. They are of smaller size than those of the first and second branchial arches, but in other respects are similar to these. The external gill, and the vessels supplying it, are considerably smaller than those of the two arches in front.

d. The vessels of the fourth branchial arch (Figs. 77, 78, and 80, AF.4, EF.-i) arise still later, but in essentially the same manner, except that no external gill is formed 011 this ai'ch. The vessels are well established before the mouth opening appears. From the dorsal end of the efferent vessel of this arch the pulmonary artery, AP, arises as a diverticulum which gi'ows backwards along the outer side of the lung (cf. Fig. 7G, p. 166).

It should be noticed that the pulmonary artery arises, and acquires its relations with the lung, before the afferent branchial vessel of the arch has joined the diverticulum from the truncus arteriosus ; indeed, before this latter has commenced to develop (cf. Fig. 78). Consequently, the only blood that can at this stage reach the lung is blood from the dorsal aorta, and not blood from the heart ; in other words, the lu-ng in the early stages of its development receives arterial and not venous blood.

The afferent vessels of the fourth branchial arch develop verv late : and the afferent diverticulum from the truncus arteriosus (Fig. 80, AF.4), really a branch from that of the third arch, does not commence to form until after the mouth of the tadpole is established.

e. The vessels of the hyoid arch. In the hyoid arch, at an early stage of development, vessels are present which agree closely in relations and in arrangement with those of the branchial arches; but which, after developing up to a certain point, undergo degenerative changes, and in the later stages of tadpole existence lose all trace of their original disposition.

In tadpoles of 5 mm. length, not long before hatching, the hyoid vessels consist of: (i) an elongated efferent lacunar vessel, lying parallel to, and in front of, the efferent vessel of the first branchial arch; and (ii) a very small diverticulum from the dorsal aorta, which lies opposite the upper end of the lacunar vessel, but does not quite meet this.

In newly hatched tadpoles two further changes have occurred : (i) a small blind diverticulum arises from the truncus arteriosus, just in front of the diverticulum for the first branchial arch ; and (ii) the efferent lacunar vessel has become obliterated about the middle of its length, and so divided into two separate portions, dorsal and ventral. Of these, the dorsal one has no communication with any other vessel, although it lies very close to the diverticulum from the aorta ; while the ventral portion, which may be spoken of as the hyoidean vein, opens below into an irregular longitudinal venous sinus lying just above the sucker.

In tadpoles shortly after hatching (Fig. 78), the diverticulum from the truncus arteriosus has disappeared, as has also the dorsal portion of the efferent sinus ; so that the only vessels remaining are the small diverticulum, EH, from the aorta, and the ventral portion of the efferent sinus, or hyoidean vein. VY, which opens below into the veins of the sucker, VK. By the time the mouth opening is established, the diverticulum from the aorta has also vanished, and the hyoidean vein is the only persistent part of the series of hyoidean vessels.

It thus appears that in the hyoid arch vessels are developed which are essentially similar to those of a branchial arch ; the chief difference being that no afferent lacunar vessel is formed in the hyoid arch, a difference which may clearly be correlated with the absence of gills, both external and internal, from the arch. The arrangement and mode of development of the vessels which are actually present in the hycid arch, agree so closely with those seen in the vessels of the branchial arches as to strongly suggest that frogs must be descended from ancestors in which gills were present on the hyoid arch as well as on the branchial arches.

f. The vessels of the mandibular arch. These appear later than the vessels of the hyoid arch, and depart even more markedly from the typical branchial arrangement.

Up to the time of hatching there are no vessels at all in the mandibular arch. Shortly after hatching there appears in the lower or ventral part of the arch a lacunar vessel, which lies parallel to and in front of the similar vessel in the hyoid arch, and, like this, opens into the venous sinuses above the sucker ; it may be spoken of as the mandibular vein. There is also present a very small diverticulum from the dorsal aorta.

A little later (Fig. 78), both these factors have grown considerably. The mandibular vein, VM, has extended dorsal wards, and the aortic diverticulum, EM, ventrahvards ; and the two vessels are now continuous with each other. Shortly after the mouth opens, the two again separate ; the mandibular vein gradually shrinks up, as the sucker degenerates, and the aortic diverticulum grows forwards as the pharyngeal artery of the adult (Fig. 80, AY).

From the above account it appears that the vessels of the mandibular arch, though still referable to the type of the branchial vessels, are even more modified than those of the hyoid arch ; the afferent lacunar vessel and the diverticulum from the truncus arteriosus are completely absent, and at no time have the vessels any connection with the heart.

g. The changes in the branchial vessels at the metamorphosis. For some time before the metamorphosis the tadpole breathes by lungs as well as by gills, though the main part of the respiratory work is performed by the latter.

The condition of the blood-vessels during this period of double respiration is as follows. The mandibular and hyoid vessels may be omitted, as, although these are formed on the type of the branchial vessels, they have no connection with the heart, and no gills are developed in relation with them.

Gills are present on all four branchial arches, and the arrangement of the vessels is practically the same in all. In each arch (Fig. 80) there are two main vessels, afferent and efferent, which lie side by side close to each other. Of these, the afferent vessel is a branch of the truncus arteriosus, and lies in the posterior part of the arch ; while the efferent vessel lies immediately in front of the afferent, and opens at its <lorsal end into the aorta. The afferent vessel is confined to the ventral half of the arch ; while the efferent extends along its whole length, its ventral termination lying in the floor of the mouth, close to the origin of the afferent vessel from the truncus arteriosus.

The afferent and efferent vessels of each arch are connected together in two ways : (i) by the capillary loops of the gills, of which the most dorsally placed belong to the external gill, and the ventral series to the internal gills ; (ii) by each afferent vessel opening directly into the corresponding efferent vessel, the communication (Fig. 80) being ventral to the gills, and of very small size. This direct connection between the afferent and efferent vessels is present in all four branchial arches, though its position and relations are not easy to determine. The blood entering an afferent vessel from the heart has thus two courses open to it : it may either continue along the afferent vessel, and pass through the gill capillaries to the efferent vessel, and so reach the aorta ; or it may pass across at once, through the aperture of communication, to the efferent vessel, and reach the aorta without having passed through the gills.

At the commencement of the metamorphosis these direct communications enlarge, so that an increasing quantity of blood passes from the heart to the aorta without going through the gills. The gills thus receive less and less blood, and gradually diminish in size and in efficiency. Increased work is thereby thrown on the lungs ; and an increasing supply of blood is sent to the lungs and skin by enlargement of the pulmonary and cutaneous arteries, which are branches of the efferent vessel of the fourth branchial arch (Fig. 80), close to its dorsal end.

By further enlargement of the direct communications between the afferent and efferent vessels, the definite aortic arches are formed, leading directly from the heart to the aorta ; each aortic arch (cf. Figs. 80 and 81) consisting of the basal or proximal end of the afferent branchial vessel, and the whole length of the efferent vessel ; while very nearly the whole length of the afferent vessel, and all the gill capillaries, disappear completely.

Very slight changes will now convert the branchial system of the tadpole to the aortic system of the adult frog. Of the four aortic arches, the first, in the first branchial arch, becomes the carotid arch of the frog (Fig. 81, i). The portion of the dorsal aorta between the points of opening of the first and second aortic arches remains an open tubular vessel for some time, and may even retain its lumen in the adult. More usually, however, the cavity becomes obliterated, and the walls of the vessel persist merely as a pigmented band, connecting the dorsal ends of the carotid and systemic arches with each other. After the obliteration of this part of the aorta, the blood in the carotid arch is distributed exclusively to the head.



FIG. 81. Diagrammatic figure of the arterial system of an adult male

Frog, from the right side, x 1.

a, stomach, b, nostril, c, small intestine, ca, carotid artery, cf, carotid eland . cm , coehaco-mesenteric artery, en, cutaneous artery. <l. large 'intestine, da, dorsal lorta. /, lemur, fl, spleen. //, hepatic artery. , right lung, la, lingual arterv. m, Wtt. o, kidney, oa, occipito-vertebral artery, pa, pulmonary artery, r, pelvic: girdle, s, sternum, sa, subclavian arterv. sc, sciatic arterv. t, tongue, ta, trnncus arteriosus. ua, urinogenital arteries, v, ventricle. 1, carotid arch. 2, svstemic arch. 3, puluio-cutaneous arch.


The second aortic arch, in the second branchial arch of the tadpole, becomes the systemic arch of the frog (Fig. 81,2).

The third aortic arch, in the third branchial arch of the tadpole, disappears altogether. In young frogs of the first year it loses its connection with the aorta, and then gradually shortens up, the distal part becoming a solid cellular cord, and the proximal or cardiac part retaining for a time its lumen. Before the end of the first year this vessel has entirely disappeared.


The fourth aortic arch, in the fourth branchial arch of the tadpole, becomes the pulmo-cutaneous arch of the frog. It retains its communication with the aorta for some time after the dorsal part of the third arch has atrophied ; but before the end of the first year, the part of the fourth arch above the origin of the cutaneous artery loses its cavity and becomes solid, so that the pulmo-cutaneous arch no longer opens into the aorta.

The condition of the aortic arches is now that of the adult frog (Fig. 81).

Before leaving the branchial circulation, it should be noticed that in other species of frogs the development of the bloodvessels differs in some important respects from that described above for the common English frog, Rana temporaria. In Rana esculenta, according to Maurer, the efferent lacunar vessel of each arch becomes connected at its ventral end with the truncus arteriosus, and at its dorsal end with the aorta, before the afferent branchial vessel is formed ; so that in this species of frog there is a stage, prior to the formation of the gills, in which there is a direct passage from the heart to the aorta. As the gills appear, the afferent gill-vessel arises as an outgrowth from the ventral end of the efferent vessel, with which it becomes connected, more dorsally, through the gill-capillaries. During the time that the tadpole is breathing by gills, the direct connection between the ventral ends of the afferent vessel and the efferent vessel is lost, but it is re-established at the time of the metamorphosis, after which time the further changes are the same as in Rana temporaria. A similar mode of development has been observed as an exceptional occurrence in Rana temporaria itself, and there are reasons for thinking that this plan of development, in which there is, from the first, direct connection between the heart and the aorta, through the aortic arches, and in which the whole gill circulation is secondarily derived from this condition, is more primitive than the mode of development usually seen in Rana temporaria. This more primitive type of larval vessels is comparable to the condition obtaining throughout life in the branchial blood-vessels of Amphioxus.

4. The Dorsal Aorta and its Branches

There are at first two aortse, one on either side of the body. These appear, as described above, as a number of isolated lacunar spaces in the roof of the pharynx, which run together to form a pair of continuous vessels. These are widest apart opposite the first branchial arches (Fig. 77, A) ; further back, behind the pharyngeal region, they lie close alongside each other, and soon fuse to form the definite dorsal aorta.

a. The arteries of the head are derived from the anterior ends of the dorsal aortas.

The carotid arteries (Fig. 78, AC), which are the direct continuations forwards of the dorsal aortae, become early connected by two transverse vessels, the anterior and posterior commissural vessels (Fig. 77, CA, CP), which, with the carotid arteries themselves, form an arterial circle surrounding the infundibulum. In front of the anterior commissural vessel the carotid arteries are continued forwards as the anterior cerebral arteries (Figs. 78 and 80, AR).

The basilar arteries (Figs. 78 and 80, AB), appear shortly before the mouth opens, as a pair of vessels which arise from the outer ends of the posterior commissural vessel, and run backwards along the ventral surface of the brain and spinal cord, not far from the median plane.

The anterior palatine arteries (Figs. 78 and 80, AT) arise as branches from the carotid arteries, just before these enter the skull, and run forwards in the mucous membrane of the roof of the mouth as far as the nose ; they appear very shortly after the tadpole hatches.

The pharyngeal artery (Fig. 80, AY) is formed, as already described, from the dorsal part of the efferent vessel of the mandibular arch (Fig. 78, EM). From it the posterior palatine artery {Fig. 80, AS) arises as a small, anteriorly directed branch, which runs forwards and outwards in the roof of the pharynx.

The lingual artery (Fig. 80, AL) is of considerable interest. It appears shortly before the mouth opens, and in tadpoles of about 9 mm. length is present on each side of the head as a very short vessel, lying in the floor of the mouth immediately in front of the truncus arteriosus. In the middle of its course it presents a swollen bulb-like dilatation, from which arise : (i) an anterior branch, the lingual artery proper, which runs forwards a short distance, giving oif a small thyroid artery to the thyroid body ; and (ii) a posterior branch, which runs a short distance outwards and backwards towards the ventral end of the efferent branchial vessel of the first branchial arch, EF.I, but does not quite meet this. At this stage, therefore, the lingual artery is a closed vessel, having no communication with any other blood-vessel.

Slightly later, in tadpoles of about 12 mm. length, the posterior end of the lingual artery and the ventral end of the first efferent branchial vessel become directly continuous with each other (Fig. 80). The bulb-like swelling is still present, and it is immediately dorsal to this that the direct connection between the afferent and efferent branchial vessels is effected, as described above. The anterior end of the lingual artery has by this time grown forwards considerably (Fig. 80), extending to the lower jaw and lower lip.

The lingual artery thus arises in the floor of the mouth independently of any other vessel, but soon acquires connection with the ventral end of the first efferent branchial vessel, of which in the later stages it appears to be a direct continuation.

b. The carotid gland of the frog is formed by elaboration of* the direct passage between the afferent and efferent vessels of the first branchial arch. At 12 mm., as just noticed, the lingual artery and the first efferent branchial vessel are continuous ; the lingual artery has at its base (Fig. 80) a small bulb-like swelling, CG, and immediately dorsal to this swelling the afferent and efferent branchial vessels are in direct communication with each other. This direct passage is at present a single, and a narrow one : it traverses a small plate of epithelial cells, which is budded off from the epithelium of the first branchial cleft, and wedged in between the afferent and efferent vessels.

In the later stages of development this passage becomes plexiform, there being now three or four openings into the afferent vessel, and about the same number into the efferent vessel, one or more of the latter leading directly into the bulblike swelling at the base of the lingual artery.

This plexiform communication forms the carotid gland ; the history of its formation shows that it is not to be regarded as a persistent or modified part of a gill, as was formerly held to be the case, but that it is a specially acquired structure, formed by elaboration of the direct passage between the afferent and efferent branchial vessels, a passage which is present in a simpler form in the hinder arches as well.

Solid epithelial plates, of a similar character to that in which the carotid gland is formed, are developed, at a slightly later stage, between the ventral ends of the afferent and efferent vessels of the second and third branchial arches, and perhaps in the fourth arch as well ; and it is by perforation of these plates that the direct communications between the afferent and efferent vessels are established. After the metamorphosis the epithelial plates persist, and even increase in size, forming solid epithelial bodies, lying in the floor of the mouth, in the angles between the carotid and systemic, and systemic and pulmocutaneous arches respectively. They acquire connective tissue capsules, and have been spoken of as accessory thyroid bodies.

c. The hinder part of the dorsal aorta. The union of the two aortas to form the definite dorsal aorta occurs almost immediately behind the pharyngeal region (Fig. 77).

At, or close to, their point of union each aorta has, at the time of hatching, a small bulging of its ventral wall. Later on, these bulgings increase in size and become sacculated, forming a pair of prominent, pigmented, thick-walled swellings, the glomeruli of the head kidneys (Figs. 77 and 78, GM), which hang down into the dorsal part of the body cavity, lying opposite the head kidneys, KP, along almost their entire length.

In their further development, the glomeruli keep pace with the head kidneys; they remain large up to about 23 mm., i.e. so long as the head kidneys remain functional (cf. Figs. 83, 84, and 85) ; but in the later stages, when the head kidneys begin to degenerate, the glomeruli also become smaller. They are still present, though of very small size, up to the end of the first year, but disappear completely in the second year. Certain further points in connection with the glomeruli will be noted in the section dealing with the kidneys.

d. The pulmonary arteries arise, as described above, shortly after the time of hatching (Figs. 77, 78, AP), as diverticula from the dorsal ends of the efferent vessels of the fourth branchial arches. As the connection of the afferent vessel of this arch with the truncus arteriosus is not acquired until some time after the mouth opening is established, there is a considerable period during which the supply of blood to the lungs is derived from the aorta and not from the heart, i.e. is arterial and not venous ; a condition which suggests that the lungs had originally some function other than respiration to fulfil.

The cutaneous artery (Fig. 80, AU) is a branch of the fourth efferent vessel, which arises very close to the pulmonary artery, but independently of this, and at a rather later stage.

5. The Veins

The veins, in the earlier stages of their development, are chiefly characterised by their large size, and irregular lacunar character.

a. The vitelline veins are the first veins to be formed in the body. They appear as irregular lacuna? in the mesoblast of the splanchnopleure, along the sides of the yolk-mass and of the liver diverticulum, and unite in front to form the sinus venosus or most posterior part of the heart ; they carry to the heart the food matter absorbed from the yolk-mass.

About, or shortly after, the time of hatching, the liver diverticulum becomes more definitely bounded, and the vitelline and hepatic veins become distinct from one another ; later still, by folding of the wall of the hepatic diverticulum, the hepatic veins are carried deeply into the substance of the liver (Figs. 64 and 76), as already described in the section dealing with the development of the liver (p. 154).

b. The sinus venosus (Fig. 71, RS) is at first formed merely by the union of the vitelline veins, but very early becomes a definite transverse vessel, running across the body in close contact with the anterior wall of the liver, and opening into the auricular portion of the heart by a large anterior aperture.

c. The anterior cardinal veins are paired, and return blood from all parts of the head, except the floor of the mouth. Each is formed by the union, behind the ear, of two principal veins : the jugular vein, which returns blood from the brain and dorsal part of the head ; and the facial vein, which runs more superficially along the side of the head, ventral to the eye and ear.

d. The posterior cardinal veins (Fig. 84, vc) are also paired, and are in special relation with the head kidneys, which they completely surround. They are of enormous size during the early stages of tadpole life, when the head kidneys are functionally active, forming vascular networks which occupy the spaces between the tubules of the head kidneys. Each posterior cardinal vein receives somatic veins from the hinder part of the body wall, and unites, in front, with the anterior cardinal vein, at the level of the hinder border of the pericardial cavity, to form the Cuvierian vein (Fig. 71). The two Cuvierian veins, right and left, run almost vertically downwards to open into the outer ends of the sinus venosus (Fig. 71). The Cuvierian veins persist as the anterior venae cava3 of the frog.

e. The inferior jugular veins collect the blood from the floor of the mouth, including the large sinuses above the sucker into which the mandibular and hyoidean veins open (Fig. 78) : they then run back in the side walls of the pericardial cavity, a ad open into the right and left Cuvierian veins respectively, just before these reach the sinus venosus.

f. The posterior vena cava is a large median vein (Fig. 70. vi), which develops shortly after the mouth opening is established ; it is continuous posteriorly with the hinder portions of the two posterior cardinal veins, which unite together ; and, further forwards, it runs in a deep groove along the left side of the liver (Fig. 71. VH), joins with the hepatic veins, and then opens into the sinus venosus. The blood from the hinder part of the body can now return to the heart either along the posterior cardinal and Cuvierian veins, or else by the posterior vena cava. In the later stages of tadpole life more and more of the blood follows the latter course, and the anterior ends of the posterior cardinal veins gradually diminish in size, and during the metamorphosis disappear completely.

g. The renal portal veins are formed by longitudinal anastomotic communications between the transverse, or vertebral, veins of the hinder part of the body ; they are joined posteriorly by the iliac veins, and with these form the afferent renal system of veins.

h. The anterior abdominal vein is at first paired, and is in connection , not with the liver, but the heart. The pair of vessels appear first in the ventral body wall, extending backwards a short distance from the sinus venosus ; they soon extend further backwards, and acquire communications with the veins of the hind legs and of the bladder. At a later stage, the two anterior abdominal veins unite at their hinder ends, in front of the bladder, while further forwards the vein of the right side disappears, the left one alone persisting. Later still, the anterior abdominal vein loses its direct communication with the sinus venosus, and acquires a secondary one with the hepatic portal veins, or afferent veins of the liver.

i. The pulmonary veins (Fig. 70. VP) develop early, but not quite so soon as the pulmonary arteries. They appear, about the time of establishment of the mouth opening, as a series of irregular lacunar spaces along the inner or median walls of the lungs, and at first do not reach the heart. Very shortly afterwards, they are completed along their whole length, about the time of formation of the inter-auricular septum in the heart.

6. The Lymphatic System

The most striking point about the lymphatic system in the tadpole stages is the great development of the subcutaneous lymph spaces. In tadpoles of about 20 mm. length, and upwards, these form sacs of literally enormous size, filled with a coagulable fluid, and almost completely surrounding the sides and ventral surface of the body and head (cf. Figs. 71, 75, and 88, LY) ; in the living tadpole they give rise to the appearance of a semi-transparent border surrounding the head and trunk.

The early development of the lymphatics appears to take place in the same manner as that of the blood-vessels ; the lymphatics appearing first as intercellular lacunar spaces, to which proper walls are formed later by the surrounding tissues.

The lymph-cells appear rather late, after the internal gills are well established ; according to Maurer, they are derived from the hypoblast cells of the wall of the mesenteroii, and wander thence into the connective tissue.

The spleen arises as a spherical bud on the mesenteric artery ; it consists of cells similar to those of the lymphatic tissues, and, like these, is said to be derived originally from the hypoblast cells of the mesenteron.


Development of the Urinary and Reproductive Organs

1. Preliminary Account

The excretory organs of the tadpole are the head kidneys, a pair of globular bodies (Fig. 83, KP), imbedded in the dorsal body- wall, immediately behind the pericardial cavity. Each head kidney, or pronephros, consists of a convoluted and complex mass of tubules, with glandular walls, opening into the body cavity by three ciliated mouths or nephrostomes ; the tubules are surrounded by, or rather imbedded in, the large posterior cardinal veins, and it is from the blood in these veins that the excretory matters are separated. The excretions are carried away from the head kidneys by a pair of tubes, the segment al ducts, KA, which run along the dorsal wall of the body to its hinder end, where they open into the cloaca, or hinder part of the alimentary canal.

The head kidneys and their ducts are well developed in the tadpole at the time of hatching ; they subsequently increase considerably in size, and are the sole excretory organs of the tadpole during the earlier stages of its existence. About the time the hind legs appear, the adult kidneys, or Wolffian bodies, begin to form in the hinder part of the body, as a series of tubes which grow towards, and open into, the segmental ducts (Fig. 83, KM) ; these ducts carrying away the excretory matters separated by both the larval and adult kidneys. The Wolffian bodies rapidly increase in size and in complexity, especially at their posterior ends, and by the time of the metamorphosis (Figs. 85 and 8G) have attained considerable dimensions. The head kidneys at the same time undergo degenerative changes, and gradually disappear, while the Wolffian bodies, growing still larger, become the kidneys of the frog.

The genital ducts are formed in close relation with the segmental ducts, or actually from these ducts ; and the Wolffian bodies become so closely related to the reproductive organs in both sexes, that it is desirable to describe the development of the two systems, urinary and reproductive, together.

2. The Head Kidney and Segmental Duct

The segmental duct (Fig. 70, KB) first appears, in embryos of between 3^ and 4 mm. length, as a longitudinal ridge of the somatopleuric mesoblast, immediately below the ventral borders of the myotomes, MS. This ridge lies immediately beneath the epiblast, but is, in the frog, distinct from this at all stages of its development. It is difficult to determine whether or not it is solid at its first appearance, but it very soon becomes grooved along its inner surface (Fig. 70) ; the groove communicating with the body cavity, and the entire ridge having, in transverse section, the appearance of a fold of the mesoblast, with a well-defined ventral or outer lip, and a less distinct dorsal boundary.

In the hinder part of the body the lips of the groove meet, so as to form a tube, lying between the rnesoblast and the epiblast ; and this tube is the segmental duct. At the anterior end, the lips remain separate for a time, so that the duct opens in. front into the body cavity by a longitudinal slit-like mouth.


FIG. 82. Transverse section through the body of a Tadpole at the time of hatching ; the section passing through the second pair of nephrostomes, and the third pair of myotomes. x 50.

T, intestinal region of inesenteron. ~VC, posterior cardinal vein. VH, hepatic vein,



By meeting of the lips at two places this slit becomes divided into three openings or nephrostomes, lying one behind another, and immediately below the ventral edges of the second, third, and fourth myotomes respectively (cf. Figs. 74 and 82).

The anterior end of the duct, and especially the parb between the second and third nephrostomes, now increases rapidly in length, becoming twisted on itself; and at the same time the nephrostomes become drawn out into short tubes. At its hinder end the duct grows backwards, and, shortly before the hatching of the tadpole, acquires an opening into the cloaca.

The condition at the time of hatching is shown in Figs. 74 and 82. The head kidney, KP, is a slightly convoluted tube, opening into the body cavity by the three nephrostoraes, KS ; of which the anterior one is at a level slightly ventral to that of the other two. Opposite the nephrostomes, and projecting into the dilated dorsal portion of the body cavity, is the glomerulua (Fig. 82, GM), a sacculated diverticulum of the aorta, the development of which has been described above. Behind the nephrostomes, the segmental duct is continued backwards in an almost straight course to the hinder end of the body, where it opens into the cloaca (Fig. 74, KA).

After the tadpole has hatched, the head kidney increases considerably in size (Figs. 76, 83, and 84). The tubules of which it consists become more markedly convoluted ; and further complication is caused by the formation of lateral diverticula, of which there are three principal ones, directed outwards, and themselves branched. The three nephrostomial openings persist ; their walls are formed of pigmented cells, bearing long flagella, directed inwards. The head kidney reaches its full development in tadpoles of about 12 mm. length (Figs. 83 and 84), when it is almost spherical in shape, and formed of an intricately coiled mass of tubes, imbedded in the greatly dilated anterior cardinal sinus, vc.

In tadpoles of about 20 mm. length, the head kidneys commence to degenerate. The first step in the process consists in irregular dilatation of the tubules, more especially of the blind lateral diverticula. This dilatation may be so great that a single tubule may nearly equal in diameter the entire head kidney of the earlier stages ; but as the dilatation of some tubules is accompanied by compression of others, the size of the head kidney as a whole remains practically unaltered.

This irregular dilatation is accompanied by, and perhaps due to, partial or complete obstruction of the segmental duct behind the head kidney. The epithelium of the kidney tubules soon shows degenerative changes, the cells becoming flattened out in an irregular manner, their outlines indistinct, the cell contents cloudy, and the inner surfaces of the cells ragged. From this time degeneration proceeds steadily, and the whole organ diminishes in size. In 10 mm. tadpoles (Fig. 85) the head kidneys are less than half their former size, and the tubules are completely collapsed. By the time of the metamorphosis, the head kidneys have almost disappeared (Figs. 86 and 88), a few pigmented and slightly twisted tubules alone remaining.



FIG. 83. Diagrammatic figure of a 12 mm. Tadpole, dissected from the ventral surface, to show the heart and branchial vessels, and the head kidneys and commencing Wolffian bodies. The alimentary canal, from the oesophagus to the rectum, has been removed, x 22.

A, aorta. AP.l, AF.3, afferent branchial vessels of first and third branchial arches. AL, lingual artery. CQ-, dilatation at the base of the lingual artery. EA, communication between the afferent and efferent vessels of the first branchial arch, by further elaboration of which the carotid gland will be formed. EF.l, EF.3, efferent branchial vessels of first and third branchial arches. QM, glonierulus. KA, segmental duct. KM, Wolffian tubules. KP, head kidney. KS.l, first nephrostouie. KS.3, third nephrostome. LI, upper lip. L J", lower lip. LP, commencing hind limb. O A, spout-like aperture of opercular cavity. OP, opercular cavity. R.S, sinus venosus. B.T, trillions arteriosus. RV, ventricle. TC, cloaca. TO, oesophagus. TR, aperture of rectul spout.


All three nephrostomes disappear : the anterior one is the first to close, and the middle one soon follows ; the third or most posterior one persists for a short time longer, and then in its turn closes, loses its connection with the peritoneum, and disappears. Shortly before the closure of the third nephrostome, the head kidney separates completely from the segmental duct, which then ends blindly in front.

The glomerulus of the head kidney (Figs. 83, 84, GM) arises, as described above (p. 182), as a sacculated outgrowth from the ventral and outer wall of the aorta, bulging outwards into the body cavity opposite the nephrostomes. At the time of hatching of the tadpole (Fig. 82) the dorsal portion of the body cavity is practically the only part present : for although the splitting of the mesoblast extends down the sides of the body to the ventral surface, yet the two layers, somatic and splanchnic, are in contact with each other, owing to the distension of the body by the mass of food-yolk, except at the upper or dorsal angle. The glomerulus, therefore, appears at this stage to lie in a special cavity, which later on opens into the general body cavity, as the yolk becomes absorbed and the abdominal viscera acquire more definite form.



FIG. 84. Transverse section across a 12 mm. Tadpole ; the section passing through the middle of the length of the head kidney, x 44.

A, aorta. AP, pulmonary artery. BH, medulla oblongata. CH, notochonl. GI, portion of a gill. GM, glomerulns. KP, tubule of head kidney. KS, second nephrostome. LA, commencing fore limb. LG, root of lungs. NY, sympathetic ganglion. OP, opereular cavity. TI, intestine. TO, oesophagus. V.4, fourth ventricle. VC, posterior cardinal vein. VH, posterior vena cava. VP, pulmonary vein. "W, liver. X, ganglion of spinal nerve. X', thin roof of fourth ventricle.


At a later stage still, the part of the body cavity in which the glomerulus lies becomes partially boxed in, by fusion of the outer wall of the lung with the peritoneal covering of the head kidney (cf. Fig. 84). This inclosure is only an incomplete one, as the part of the ccelom lodging the glomerulus still opens into the general body cavity, both in front of the root of the lung and behind this.

The position of the glomerulus, opposite the nephrostomes of the head kidney, and the fact that its development, both progressive and retrogressive, keeps pace with that of the head kidney, point to the existence of some close physiological connection between the two organs, though it is not easy to imagine of what precise nature this connection can be.

The glomerulus, with the part of the body cavity in which it lies, may be compared to one of the Malpighian bodies of the adult kidney ; the glomerulus itself corresponding to the capillary knot of vessels ; the localised part of the coelom in which it lies corresponding to the capsule of the Malpighian body ; and the nephrostomial tube leading from the coelom answering to the neck of the Malpighian body.


3. The Wolffian Body

The development of the Wolffian body, or kidney, commences in tadpoles of about 10 to 12 mm. length, by the formation of the Wolffian tubules (Fig. 83, KM). These appear as a series of small, paired masses of mesoblast cells, lying along the inner sides of the segmental ducts, between these and the aorta. The Wolffian tubules develop from behind forwards ; the hindmost, and at first the largest pair, being a short distance in front of the cloaca, and the most anterior pair being about three segments behind the head kidneys. They are at first segmentally arranged, one pair corresponding to each pair of muscle segments or myotomes ; but this definite arrangement is early lost in the hinder resrion.


The Wolffian tubules are. at first, solid masses of spherical cells; these arise in the mesoblast of the body wall, and are for a time independent of both the peritoneum and the segmental ducts. The cellular masses soon become elongated into solid rods ; by separation of the component cells along their axes, the rods become tubes; and these tubes, growing outwards and towards the dorsal surface, meet with the segmental ducts and open into these.

At the opposite end of each tubule, a Malpighian body is formed, the end of the tubule being dilated into a bulb-like enlargement, which becomes doubled up, to form the Malpighian. capsule, by the ingrowth of a knot of blood-vessels derived from a branch of the dorsal aorta (c/. Fig. 87, A).

From the neck, or part of the tubule immediately beyond the Malpighian body, a short solid rod of epithelial cells arises, which grows towards the peritoneum and fuses with this. By separation of the cells the rod becomes tubular, and opens at its outer or peritoneal end into the body cavity. The peritoneal opening is a nephrostome (Fig. 87, KS), and the tube into which it leads may be called the nephrostomial tubule.

Although the walls of the nephrostomial tubules are at first continuous with the necks of the Malpighian bodies, it is very doubtful whether the nephrostomial tubules ever open into the Wolffian tubules ; and, shortly after their first appearance, in tadpoles of 18 to 20 mm. length, the nephrostomial tubules break away completely from the Wolffian tubules, and acquire openings at their inner ends into the renal veins, on the ventral surface of the kidney. This curious arrangement persists throughout life. ' On the ventral surface of the kidney of an adult frog there are as many as two hundred or more of these nephrostomes present, as funnel-like depressions or mouths : these lead into short tubes, lined by flagellated epithelial cells, and running obliquely inwards into the substance of the kidney, where they end by opening into the renal veins.

The anterior three or four pairs of Wolffian tubules never complete their development, but early undergo fatty degeneration. The hinder tubules are at first segmentally arranged, but, owing to the formation of new tubules, soon become much more numerous than the segments in which they lie. They increase greatly in length, become markedly convoluted, and soon become massed together, with the blood-vessels in relation with them, to form the definite Wolffian bodies or kidneys (Figs. 85, 8G, and 87, KM).

4. The Wolffian Ducts or Ureters

The segmented duct is at first the duct for the head kidney alone (Fig. 74, KA) ; in the later stages (Figs. 83 and 85), it serves for both the head kidney and the Wolffian body.


FIG. 85. A 40 mm. Tadpole, dissected from the ventral surface to show the heart, the branchial vessels, and the urinary and reproductive organs. The tail, and the alimentary canal, from the oesophagus to the rectum, have been removed, x 4.

FIG. 86. A Tailed Frog, during the metamorphosis, dissected from the ventral surface to show the urinary and reproductive organs. The alimentary canal has been removed, x 3J.

A, aorta. AF.l, AF.4, afferent vessels of first and fourth branchial arches. AL, lingual artery. CGK carotid gland. EF.l. EF.4, efferent vessels of first and fourth branchial arches. F, fat body. GM. glonierulus. KA, segmental duct. K"IVr. Wolffiaii body. KP, head kidney. KU, \Volffian duct or ureter. LA, fore limb. LI, upper lip. LJ, lower lip. LP, hind limb. O, mouth. OR, genital ridge. RT. truncus arteriosus. RV, ventricle. TO. cloaca. TO, oesophagus. TR, aperture of rectal spout.


During the metamorphosis, and shortly before the complete disappearance of the tail, the head kidney separates from the segmented duct. For a short time, a portion of the segment al duct still persists in front of the Wolffian body ; but this soon loses its lumen, undergoes degenerative changes, and disappears : the remaining, or posterior part of the segmental duct, which is now connected with the Wolffian body alone, is from this time spoken of as the Wolffian duct or ureter.



FIG. 87. Transverse section through the hinder part of the body of a Tailed Frog during the metamorphosis (cf. Fig. 86). On the right side a spinal nerve is shown, on the left side the vertebral column, x 1 7.

A, aorta. CH. notochord. F, fat body. 1C, centrum of vertebra. IE, neural arcli of vertebra. KA, Wolffian duct. KS^ nephrostome. KT, Wolffian body. LG, lung. LS, stomach. LY, subcutaneous lymph space. ML, myotome. M"C, spinal cord. ND, dorsal root of spinal nerve. NM", spinal nerve, main trunk. NV, ventral root of spinal nerve. M"Y, sympathetic nerve ganglion. OV, ovary. PA, pancreas. SN, spleen. TI, intestine. VA, anterior abdominal vein. VI, posterior vena cava. VO, hepatic portal vein. VE,, renal portal vein. 'W", liver. ~WD, bile duct. "WG. gall bladder.


The vesicula seminalis is a glandular body developed in connection with the hinder end of the Wolffiaii duct, close to the cloaca. It attains a large size in the male frog, but is absent or rudimentary in the female.


FIG. 88. Transverse section through the anterior part of the body of a Tailed Frog during the metamorphosis (cf. Fig. 86). The section passes through the second spinal nerve on the right side, and on the left side immediately in front of this nerve, x 14.

A, aorta. AP, pulmonary artery. CH. notoclionl. CO, coracoid portion of shoulder girdle. FN, neural arcli of vertebra. FT, transverse process of third vertebra. GrC, glenoid cavity of shoulder girdle. GM, glonierulus. HIT, head of humerus. KS, tliird or posterior nephrostome of head kidney. LGr, lung. LY, subcutaneous lymph space. N"C, spinal canal. WD, dorsal root of second spinal nerve. N"!N", dorsal and ventral branches of second spinal nerve. NS, spinal cord. NV, ventral root of second spinal nerve. NY, sympathetic nerve ganglion. RS, sums venosus. SC, scapular portion of shoulder girdle. SS, supra-scapular portion of shoulder girdle. TO, oesophagus. VI*, pulmonary vein.

5. The Müllerian Ducts

The Müllerian ducts form the oviducts of the female frog ; they are present in the male as well, but are of very small size, and apparently of no functional importance. The early stages in the development of the Müllerian ducts are difficult to investigate, and have not yet been determined with absolute certainty ; but there is no doubt that the greater part of the length, and perhaps the whole, of the duct arises independently of the Wolffian duct ; and apparently from a modified strip of peritoneal epithelium which runs parallel to the Wolffian duct, along its outer side.


Towards the close of the metamorphosis, and during the absorption of the tail, a patch of modified peritoneal epithelium appears on the ventral surface of the now rapidly disappearing head kidney, below and to the outer side of the nephrostomes, of which, as a rule, only one persists at this stage (Fig. 88, KS). This patch of epithelium differs from the general peritoneal epithelium in its cells being columnar instead of squamous in shape. A longitudinal groove forms on the surface of this patch of columnar epithelium, to the outer side of the nephrostome ; and, by fusion of its lips, the groove becomes a tube, opening in front into the body cavity, and ending blindly behind. This tube is the first formed part of the Miillerian duct ; it lies very close to the anterior end of the segmental duct, but it is not clear that there is any connection between the two ; it is quite independent of the nephrostome, which closes up and disappears very shortly after this stage.

The Müllerian duct extends forwards, as an open groove, some distance in front of the point at which the duct is first formed ; and, by closure of the lips of the groove from behind forwards, the mouth of the duct is carried forwards, outwards, and downwards, round the anterior end of the body cavity, to its adult position at the root of the lung.

The growth backwards of the Mtillerian duct is effected by a longitudinal band of cells, which appears a little to the outer side of the Wolfnan duct, but quite independent of this, and apparently derived directly from the peritoneal epithelium. This band, which is continuous with the hinder end of the Mtillerian duct, ultimately becomes tubular, and acquires posteriorly an independent opening into the cloaca.

In the male frog the Müllerian duct stops at this stage. In the female it undergoes further changes by which it becomes converted into the oviduct. It increases in length, becoming sinuous, and ultimately convoluted along the greater part of its length ; its walls thicken greatly, and the epithelium lining them gives rise to the gelatinous secretion which is poured out over the eggs as they pass down the duct, and which, on reaching the water, swells up to form the mass of the frog's spawn. The hinder end of the oviduct remains thin-walled, but dilates very greatly, forming a capacious sac in which the eggs accumulate before being laid.

6. The Reproductive Organs

The development of the reproductive organs has already been described (p. 94), but a few further details may be given here, more especially with regard to the relation between the reproductive organs and the Wolffian bodies, and the development of the fat bodies, or corpora adiposa.

The reproductive organs appear in tadpoles of about 10 mm. length, as a pair of ridge-like folds of the peritoneum, lying along the inner borders of the Wolffian bodies, close to the root of the mesentery (Fig. 85, OR, and 87, ov). These genital folds soon become more conspicuous, and undergo changes which have already been described in detail, by which the germinal cells or gonoblasts are formed.

As the Malpighian bodies develop on the tubules of the Wolffian body, those lying nearest to the genital ridge give off hollow tubular diverticula, which, arising from the capsules of the Malpighian bodies, grow towards the median plarie, and into the substance of the genital ridge (</". Fig. 87), where they form the so-called tubuliferous tissue.

So far, the processes of development are the same in both sexes, but from this point differences occur. In the ovary of the female the tubules of the tubuliferous tissue expand very greatly, and give rise to the large axial cavities of the ovary, of which there are usually about fifteen in the adult.

In the male, the outgrowths from the Malpighian capsules acquire still more intimate relations with the reproductive organs than in the female, and become the vasa efferentia of the adult, which convey the spermatozoa from the testis to the kidney. The Malpighian bodies with which the vasa efferentia are connected are at first perfectly normal ; but later on they undergo retrogressive changes, and by the end of the first year their glomeruli have disappeared, and the Malpighian bodies themselves merely, remain as slight ampulliform enlargements of the tubules, which have now completely lost their kidney structure and function. The .tubules of these Malpighian bodies do not join those of the other parts of the kidney, but open at once into the terminal or collecting tubules of the Wolffiaii body, so that there is practically a sharp separation of the kidney into two portions, excretory and reproductive respectively.

7. The Fat Bodies

The fat bodies, which are conspicuous and characteristic structures in the adult frog, are formed by fatty degeneration of the anterior ends of the genital ridges. In tadpoles of about 40 mm. length (Fig. 85) each genital ridge becomes divided by a slight constriction into two parts of about equal length. Of these, the posterior part, OH, forms the smooth genital ridge ; while the anterior part, F, is irregularly notched along its ventral surface, and is already commencing to undergo fatty degeneration. In the later stages (Fig. 86, F) the fat bodies increase greatly in size, and are produced at their margins into the characteristic finger-like lobes of the adult.

Histologically, the changes by which the fat body is formed are due to the accumulation of fat within cells, which are at first indistinguishable from those of the hinder, or reproductive, part of the genital ridge.


Development of the Skeleton and the Teeth

1. The Vertebral Column

The earliest skeletal structure, and for a time the only one, is the notochord, the development of which, from the mid-dorsal wall of the meseuteron, has already been described (p. 109).

The notochord (Fig. 61, CH) is a cylindrical rod, extending from the blastopore to the pituitary body ; and growing backwards along the tail as this is formed (Fig. 69, CH). It consists of vacuolated cells, filled with fluid : the cells are all alike, and their nuclei, which at first are conspicuous, disappear in the later stages. Around the notochord a delicate structureless elastic sheath is formed at an early period ; this is really double, consisting of a thicker inner, and an outer thinner layer ; both layers are homogeneous, and cuticular in nature.

About the time of appearance of the hind limbs as buds, a delicate skeletal tube, at first soft, but soon becoming cartilaginous, is formed from the mesoblast surrounding the notochord (Fig. 84, CH). This grows upwards at the sides of the spinal cord as a pair of longitudinal ridges, with which a series of cartilaginous arches, which appeared at the sides of the spinal cord at a slightly earlier stage, soon become continuous (Figs. 87, 88).

By the appearance of transverse lines of demarcation, this axial skeleton becomes cut up into a series of nine vertebrae, followed by a posterior unsegmented portion, which later on gives rise to the urostyle. The vertebras are cut off in order, from before backwards, and the division at first involves the cartilaginous tube alone, the notochord remaining as a continuous structure until the complete absorption of the tail, at the end of the metamorphosis (Fig. 89).

Shortly before the metamorphosis, thin rings of bone, slightly constricted in their middles so as to be hour-glass shaped in section, are developed in the membrane investing the cartilaginous sheath of the notochord ; these from their first appearance correspond with the nine vertebrae, to the bony centra of which they give rise. Like the cartilaginous vertebrae, they develop in order from before backwards.

In the intervertebral regions, between the successive bony rings, annular thickenings of the cartilaginous sheath occur, which grow inwards so as to constrict, and ultimately obliterate the notochord. Each of these intervertebral rings, after the metamorphosis, becomes divided into anterior and posterior portions, which fuse with the bony centra of the adjacent vertebras, and ossify to form their articular ends.

From the circumference, and from the articular ends of each vertebra, ossification gradually spreads inwards ; but a small portion of the notochord persists in the middle of each centrum for a long time, or even throughout life.

The vertebras do not lie opposite the muscle segments or myotomes, but alternate with these ; so that each vertebra is acted on by two myotomes on each side, one pulling it forwards, and the other backwards.

The transverse processes arise independently of the corresponding vertebras, bat very early fuse with these. They extend along the connective-tissue septa between the successive myotomes, and very probably correspond to the ribs of other Vertebrates.

The urostyle is the hindmost part of the axial skeleton, which does not become segmented into vertebrae. The cartilage of the urostyle forms a continuous tube in front, surrounding the notochord : posteriorly, it extends back as a flattened epichordal plate above the notochord, and a thick median hypochordal rod below it. During the shortening of the tail, on the completion of the metamorphosis, the epichordal and hypochordal cartilages extend and meet, so as to completely surround the notochord. Later still, the cartilage becomes in great part replaced by bone ; but the hinder end persists as a terminal plug of cartilage throughout life.

The anterior end of the notochord, imbedded in the base of the skull, is gradually encroached upon by the cartilage and bone around it ; and ultimately, in half-grown frogs, is completely absorbed.

2. The Skull

a. The skull of the tadpole. The skull of the tadpole consists almost entirely of cartilage ; none of the bones of the skull, with the exception of the parasphenoid, appearing until a short time before the metamorphosis.

In the cartilaginous skull of the tadpole two main elements may be distinguished :

(i) The cranium, with the olfactory and auditory capsules, which may conveniently be taken together.

(ii) The visceral skeleton, which consists of a series of cartilaginous bars developed in the visceral arches, and encircling the pharynx.

Speaking generally, the skull as a whole develops from before backwards ; the first formed parts being at the anterior end, in connection with the jaws ; and the hinder end of the skull being very imperfect in the early stages of tadpole life.

True cartilage does not appear until the tadpole is about 10 to 11 mm. in length; i.e. when the opercular covering of the gills is almost completed, and the hind limbs are visible as minute buds at the base of the tail. Long before true cartilage is present, however, the skeletal elements can be readily distinguished, as tracts of condensed and modified mesoblast.

The first stage in the histological differentiation, by which cartilage is formed, consists in a number of mesoblast cells becoming more closely compacted together ; these cells have large nuclei and very scanty protoplasm, and are further distinguished from the surrounding mesoblast cells by having only a slight tendency to develop processes, and by being almost completely devoid of yolk-granules.


FIG. 90. The skull of a 12 mm. Tadpole, seen from the right side. The notochord, the brain, and the entire head are represented in outline, in order to show the relations of the skull to them, x 30.

FIG. 91. The same skull from the dorsal surface. The lower jaw, and the hyoidean and branchial bars are omitted, x 30.

FIG. 92. -The same skull from the ventral surface, x 30.

BB, basi-branehial. BH, roof of hiinl-brain. BM, roof of mid-brain. BR.l. BR.2, BR.3. BR.4, first, second, third, and fourth branchial bars. BS, cerebnil hemisphere. CH, notochord. EC, auditory capsule. HB, basihyal. HO, urohynl. HQ,, articulation of ceratohyal with quadrate. HR, ceratohyal. JL, lower jaw. JTJ, upper jaw. LI, upper lip. LJ, lower lip. LL, lower labial cartilage. LTJ, upper labial cartilage. MC, Jleckel's cartilage. PW, pineal bodv. Q, quadrate. QO, orbital processof quadrate. QP, palato-pterygoid process. Q,R, connection of quadrate witli trabecula. RC, pai-achonlal cartilage. RL, trabccula cranii. SA, meuibranous patch in the outer wall of the auditory capsule, in which the stapes is developed at a slightly later stage. X. clioroid plexus of third ventricle.


In the next stage the cells become still more closely compacted, so that the nuclei of adjacent cells lie very close to one another, while the protoplasm of the several cells becomes fused into a continuous plasma or matrix. Very slight further changes convert this into true cartilage.

(i) The cranium or brain case. This, in its fully formed condition (Fig. 93), is an unsegmented cartilaginous tube, incomplete dorsally, and inclosing the brain. It is developed in the following manner.

Shortly after hatching of the tadpole, a pair of longitudinal rods of condensed mesoblast, the trabeculae cranii, appear, one on either side of the anterior end of the brain. These are at first entirely in front of the notochord (cf. Fig. 64) : their posterior ends lie alongside the fore-brain ; while anteriorly they are flattened dorso-ventrally, and fused to form a horizontal plate lying between the two nasal sacs ; the extreme anterior ends of the trabeculre separate again, and bend downwards into the upper lip, which they support.

As the tadpole grows, the trabeculas rapidly extend backwards along the sides of the infundibulum, and soon reach the anterior end of the notochord : thev continue backwards alongside the notochord, and in close contact with this, as a pair of horizontal rods, the parachordals, which with the notochord form the floor of the brain case.

In tadpoles of 12 mm. length (Figs. 90, 91, and 92) the trabeculae have become cartilaginous ; their extreme anterior ends chondrify independently as a pair of thin curved plates, the upper labial cartilages, LU, which support the upper lip. Behind the labial cartilages the two trabeculae remain separate for a short distance, but soon fuse to form a median horizontal plate of cartilage, lying between the two nasal sacs, and supporting the extreme anterior end of the brain ; behind this they are continued backwards a? two parallel bars of cartilage, lying at the sides of, and slightly ventral to the brain; behind the infundibulum, and just in front of the anterior end of the notochord (Fig. 91), the two trabeculas are again connected by a narrow transverse bridge of cartilage, beyond which they continue backwards, as two narrow parachordal bands, RC, along the sides of the notochord, to the hinder end of the skull.

In the later tadpole stages the trabeculse extend horizontally inwards to form the floor of the skull, while their outer edges grow upwards, forming low ridges along the sides of the brain in the ethmoidal region, in front of the eye, and in the occipital region behind the ear. Opposite the eyes, the side walls of the cranium are formed by a pair of cartilaginous plates, which appear independently, in the membrane at the sides of the brain, and soon extend ventralwards to meet, and fuse with, the trabeculae.

The side walls and roof of the hinder part of the cranium are mainly formed by the auditory capsules. At an early period the mesoblast surrounding each auditory vehicle forms a definite capsule around it : in this a thin shell of cartilage is formed, first in the outer wall, but soon spreading round to the floor, where it becomes continuous with the outer edge of the parachordal cartilage (Figs. 70, 90, 91, EC). This cartilaginous auditory capsule spreads more slowly over the dorsal surface of the auditory vesicle, and then extends downwards, between the brain and the ear, to form the side wall of this part of the skull. Later still, in tadpoles of about 20 mm. length, the cartilage of the dorsal borders of the auditory capsules spreads inwards across the top of the brain case, and so completes its roof in this region.

The hindmost end, or occipital region of the skull, is formed by upgrowth of the edges of the parachordal cartilages. This occurs very slowly, and quite independently of the auditory capsules ; it is not completed until shortly before the metamorphosis.

In the outer wall of each auditory capsule, a large oval or circular patch remains unchondrified : this is the fenestra ovalis (Fig. 90, SA). In the middle of this membranous patch the stapes appears, in tadpoles of about 16 mm. length, as a cartilaginous nodule (c/. Fig. 93, SA), the further development of which will be considered later.

At the anterior end of the cranium, the nasal or olfactory organs become roofed in by cartilage, which arises as a vertical crest from the upper surface of the median internasal plate formed by the trabeculas, and spreads out right and left as a pair of thin horizontal plates, covering over the olfactory organs, and forming the cartilaginous olfactory capsules (Fig. 93, OF).

It thus appears that the trabeculas, with their posterior continuations, the parachordals, give rise to the floor of the cranium along its whole length ; they also, by upgrowth of their edges, form the sides and the roof of the extreme anterior and posterior ends of the skull. In the orbital region the side walls of the skull arise independently, but grow down to, and fuse with, the trabeculre ; while the roof remains membranous. Finally, in the auditory region, both the sides and roof are formed as extensions of the auditory capsules.

(ii) The visceral skeleton. This consists of a series of cartilaginous hoops or bars (Figs. 90, 92), developed in the mandibular, the hyoidean, and the four branchial arches, which tend to encircle the pharynx. Each hoop consists of right and left halves, which are independent at their dorsal ends, but fused or closely connected ventrally. Like the cranium itself, the visceral skeleton develops from before backwards.

The mandibular bar is one of the very earliest parts of the skull to be developed ; it may be recognised at the time of hatching of the tadpole as a curved band of condensed mesoblast, lying transversely across the floor of the mouth, close to its anterior end. The outer ends of the bar are enlarged, and produced upwards into vertical processes, which lie at the sides of the mouth cavity, and are continuous above with the trabeculas cranii at a level between the nose and eye ; a connection which afterwards gives rise to the palato-pterygoid bars.

After hatching, the mandibular bar grows rapidly, and undergoes important changes. It becomes divided on each side into three parts : (i) a small anterior segment, which later on becomes the lower labial cartilage, and which is continuous across the median plane with its fellow of the opposite side ; (ii) a small middle segment, which becomes later the basis of the lower jaw, or Meckel's cartilage ; and (iii) a hindmost or quadrate segment, which is much the largest of the three, and which is connected with the trabecula by the palato-pterygoid bar mentioned above, while from its outer side a dorsal ly directed, leaf-like, orbital process projects upwards.

On the appearance of cartilage, in tadpoles of about 12 mm. length, the condition of the mandibular bar is as shown in Figs. 90, 91, and 92. The hinder part of the bar forms the quadrate cartilage, Q, a stout horizontal subocular bar, which lies parallel to the trabecula, but some distance from this, and along the under and outer surface of the eyeball . The hinder end of the quadrate turns sharply inwards, QR, and is connected with the trabecula just in front of the ear capsule, EC. From the outer edge of the quadrate the prominent, vertical, orbital process, QO, projects upwards ; and the anterior end of the quadrate, like its posterior end. turns sharply inwards, to form the palato-pterygoid bar, QP, which is fused with the trabecula, between the nose and the eye. The quadrate may thus be described as a horizontal bar of cartilage, lying to the outer side of the trabecula, and connected with this by two struts, one in front of the eye and one behind it.

The second segment of the mandibular bar, or Meckel's cartilage, MC, is a short, stout bar of cartilage, which runs inwards and forwards across the floor of the mouth. The third segment, or lower labial cartilage, LL, is a much smaller bar at the inner end of Meckel's cartilage, which meets, or is actually fu*ed with, its fellow of the other side in the median plane.

The chief further changes that occur in the mandibular bar during the later periods of tadpole life (cf. Fig. 93) : are (i) a progressive diminution in size of the orbital process, QO ; and (ii) the development of an additional connection between the hinder end of the quadrate and the auditory capsule, by means of an otic process (Fig. 03. QE).

At the time of the metamorphosis, very considerable and important changes take place, which will be described later on.

The hyoid bar appears directly after the mandibular bar, and immediately behind this. At first the right and left bars are separate ventrally, but they soon become connected by a median plate. The hyoid bar thickens rapidly, and at 12 mm. (Figs. 90, 92) forms a broad, somewhat S-shaped plate of cartilage, the ceratohyal, HR, which lies across the floor of the mouth. The outer end of the ceratol^al is enlarged, and turned upwards, and articulates with the ventral surface of the quadrate about the middle of its length (Fig. 90, HQ). The inner ends of the two ceratohyals are connected, across the floor of the mouth, by a median basihyal cartilage. HB, the posterior end of which grows back as a keel-like urohyal process (cf. Fig. 05, HB), which separates the two halves of the thyroid body from each other.

The branchial bars are a series of four pail's of cartilaginous rods, developed in the four brancliial arches of each side. They appear in order, from before backwards, as slender curved bands of cartilage (Fig. 92, BR.I to BR.-I). The dorsal end?; of the four bars of each side very early become connected together. The ventral ends are at first independent, but the ends of the first branchial bars early unite to form a broad median basibranchial plate (Fig. 92, BB), with which the ventral ends of the hinder branchial bars soon join.

The chief chai'acteristic of the skull of the tadpole is the early development, and large size, of the cartilages of the extreme anterior end, in connection with the jaws. The early formation and great size of the anterior ends of the trabeculas, the large labial cartilages, the early attachment of the mandibular arch to the anterior end of the trabecula by the palato-pterygoid bar, the enormous and singularly shaped orbital process of the quadrate, and the massive character of the hyoid arch in the floor of the mouth, are all connected with the need for a firm supporting skeleton for the horny jaws, and an extensive surface of origin for the muscles by which these jaws are worked. All these are characters which concern the tadpole, and not the frog ; and they are all lost, or greatly modified, in the adult animal.

b. The skull of the frog. About the time of the metamorphosis, the skull undergoes important changes, by which the adult condition and proportions are attained.

A complete cartilaginous floor is formed to the skull, between the two trabecula?. The hinder end of the skull acquires definite shape : the parachordals increase greatly in size, growing inwards so as to encroach upon, and ultimately to obliterate the notochord ; they fuse with the auditory capsules and grow up behind these to complete the occipital ring. The side walls and roof of the skull are formed in the manner already described (p. 204). The nasal capsules are formed by expansion of the anterior ends of the trabecula3 ; the upper labial cartilages persisting as the pro-rhinal cartilages, which bound the anterior nostrils in front. A thin cartilaginous shell is formed in the sclerotic coat of each eye, but remains throughout life free from the skull proper.

In the mandibular arch great modifications occur, associated with the change from the small ventral mouth of the tadpole to the wide, slit-like, and terminal mouth of the frog. The anterior end of the quadrate rotates downwards and backwards, causing great lengthening of the palato-pterygoid bar (Figs. 90 and 93, Qr), which becomes drawn out to form the framework of tinupper jaw. At the same time, Meckel's cartilage, MC, forming the basis of the lower jaw, becomes also greatly lengthened, while the lower labial cartilages disappear. At the time of the metamorphosis, the quadrate still slopes downwards and forwards (Fig. 93) ; but the rotation continues until the quadrate becomes vertical, and finally, before the end of the first year, acquires the inclination downwards and backwards so characteristic of the adult (Fig. 94). The orbital process of the quadrate early becomes inconspicuous (Fig. 93, QO), and finally disappears.



FIG. !)3. Skull of a Tailed Frog towards the close of the metamorphosis, from the right side. The head and eye are represented in outline, x 13.

BB. basibranchial. BR.2, BR.4. second ami fourth branchial bars. CL, columella. EC, auditory capsule. HR. ccratohyal. MC, ileckel's cartilage. OC, outline of eye. OF, olfacto'ry capsule. OL, outline of lens. ON, foramen for optic nerve, 'Q. quadrate. Q,E. connection of quadrate with auditory capsule. Q,O, orbital process of quadrate. Q.P. palato-pterygold process. SA, stapes.


The hyoid bar, which is massive in the tadpole, becomes very slender in the frog. It gradually elongates, extending dorsalwards until it meets, and fuses with, the ventral surface of the auditory capsule (Fig. 94, r,).

The branchial bars become more and more slender as the gills begin to shrink, and ultimately disappear almost completely. The basihyal and basiforanchial cartilages give rise to the body of the hyoid (Fig. 94, H) : from the ventral ends of the fourth branchial bars, the backwardly directed thyrohyals (Fig. 94, T) are formed ; while the rest of the fourth branchial bar, and the whole of the first three bars disappear.

The fenestra ovalis has been described above as a large aperture, left in the outer and ventral wall of the auditory capsule (Fig. 90, SA). This aperture is closed by membrane, and in this membrane, shortly before the metamorphosis, the stapes is formed as a disc-like plug of cartilage (Fig. 93, SA).

The columella appears, in tadpoles of about 40 mm. length (cf. Fig 93, CL), as a minute bar of cartilage immediately in front of the stapes, and with its outer end directed forwards. At the time of the metamorphosis the columella grows rapidly,



FIG-, i'4. The skull of an adult Frog, from the right bide, x 2.

A, parasphenoiil. AS, angulosplenial. B, anterior cornu of hyoid. C, coluiueHa ~D, deutary. E. exoccipital. F, nostril. FP, fronto-parietal. BE, body of hyoiil. L aperture for exit of optic nerve. M, maxilla. MM, mento-meekelian. M'. upertui c for exit of fifth ami seventh nerves. M", nasal. O, pro-otic. P, pterygoM. PM, prcmaxilla. Q,, quadratojugal. B, a]>erture for exit of ninth and tenth nerves. S. squamosal. SE, sphen-ethmoiil. T, posterior cornu of hyoid, or thyrohyal.

and becomes rotated outwards, so that its outer end conies into close relation with the tympanic membrane, while its inner end fuses with the stapes. At first, the columella lies in the dorsal wall of the tympanic cavity, but this latter gradually extends upwards around it, until the columella acquires its adult relations, and appears to cross the tympanic cavity (cf. Fig. 68, C, p. 144). In its actual development, the columella of the frog shows no sign of any connection with either the hyoid or mandibular bars, but comparison with other vertebrates renders it very possible that the frog is in this, as in so many other respects, in a modified rather than a primitive condition.

The bones of the skull are of two kinds : (i) cartilage bonec, which are formed in direct connection with the primary or cartilaginous skeleton ; and (ii) membrane bones, which arise independently of the cartilaginous skeleton, although they may in their later stages become firmly grafted on to this.

The membrane bones of the skull appear in a connectivetissue layer, very rich in cells, which is found immediately outside the cartilaginous cranium. In this connective tissue, trabeculas and spicules of calcified substance appear, and soon interlace to form a network ; surrounding the spicules are osteoblasts or bone cells, by which the further growth of the framework is effected, a consistent bony lamella with imbedded bone cells being ultimately formed.

The first bone to be developed is the parasphenoid, which appears, in tadpoles of about 20 mm. length, in the connective tissue underlying the floor of the skull. The exoccipitals, and the frontals and parietals, which are at first separate from one another, soon follow. The premaxilla, maxilla, dentary, and angulare are formed at the commencement of the metamorphosis; and towards its close the vomer, palatine, pterygoid, and other bones appear.

By the time the metamorphosis is completed, and the tail absorbed, all the bones of the skull are present except the sphen-ethmoid, which appears rather late, in the course of the first summer, as a narrow transverse splinter of bone, crossing the roof of the skull near its anterior end.

3. The Teeth

In the frog the teeth are confined to the preniaxilla?, maxillae, and vomers, the lower jaw being edentulous.

The upper jaw bears a single row of small conical teeth arranged along its inner border, each tooth being attached to the bone at its base and along its outer surface, and only a very small part of the tooth projecting freely.


FIG. 95. The skull of an adult Frog, from the ventral surface. x 11

x i 2 .

a, parasphenoid. c, columella. e, exoccipital. f.p, fronto-parietal. m, maxilla. , vomer. o, pro-otic. p, pterygoid. pa, palatine, pm, premaxilla. (/, quadrato-jugal. #?, csphen-ethmoid.


Each tooth is a hollow cone ; the central or pulp-cavity containing the blood-vessels and nerves. The basal part of the cone consists of bone, the apical part of dentine, capped at the tip by a very thin layer of enamel. The teeth are readily lost, and are replaced by new ones developed below them.

The teeth do not begin to form until the time of the metamorphosis. Round the border of the jaw, a solid ridge-like ingrowth of the deeper layer of the epidermis takes place into the underlying connective tissue ; and opposite the edge of this ridge a series of small processes, the dentinal papillae, are formed in the dermis. These papillae, which are very rich in cells, grow into the epidermal ridge, which thus forms a cap over each of them. The inner lining of each cap, immediately covering the papilla, consists of a single layer of short columnar cells, the enamel cells ; while the rest of the cap, which is three or four cells thick, consists of indifferent cells, the outermost layer of which forms a more or less definite capsule.

Of the hard tissues of the tooth, the thin cap of enamel is formed by calcification of the ends of the enamel cells next to the papilla. The dentine is formed by calcification of the surface layer of the papilla itself, the cells of the papilla sending processes into the dentinal substance while it is forming.

The young tooth now separates from the epithelial ridge, and moves towards the surface ; it lengthens, by formation of bony matter at its base, but does not acquire its definite attachment to the bones of the jaw until some time after the completion of the metamorphosis, usually during the autumn of the first year. The dermal papilla persists as the pulp of the tooth.

The replacing teeth are developed in precisely similar fashion , and from the original epidermal ridge. They lie at first to the inner side of the first row of teeth, but during their development shift their positions so as to lie directly above these. By further growth downwards, accompanied by absorption of the bony bases of the teeth in use, the new teeth move towards the surface; they often lie for a time partly within the pulp cavities of their predecessors, and, as these latter fall out, speedily grow into their places.

The vomerine teeth are straighter than those of the margin of the jaw, but are otherwise similar to these, both in structui .and in mode of development.

4. The Appendicular Skeleton

The limbs arise about the time of completion of the opercular fold, and shortly after the opening of the mouth, i.e. in tadpoles of about 11 or 12 mm. length.

The hind limbs (Fig. 83, LP) appear as a pair of small rounded buds from the ventral surface of the hinder part of the body wall, at the base of the rectal spout.

The fore limbs (Fig. 84, LA) are similar buds, whicli arise about the same time, from the sides of the body wall at its anterior end, opposite the head kidneys. They lie in the dorsal angle between the body wall and the opercular fold, and, being covered by this latter, are not visible from the surface.

The limbs grow from the somatopleure alone ; each is a solid mass of compact mesoblast, covered by a cap of epidermal cells, which differ in their cubical or columnar shape from the flattened cells of the general surface of the. body.

The limbs at first grow slowly. They gradually elongate, become segmented, and then divided distally into fingers and toes (Fig. 85, LA, LP). Up to the time of the metamorphosis the hind limbs are small, while the fore limbs remain concealed within the opercular cavity. During the metamorphosis (Fig. 86), both pairs of limbs grow rapidly, more especially the hind limbs.

The skeleton of the limbs, and of the liinb-girdles by which the limbs are attached to the body, does not assume definite form until a short time before the metamorphosis.

a. The pectoral girdle develops as two half-rings of cartilage, one on each side of the body, which they encircle at the level of the second or third vertebra. The dorsal ends of the half-rings (Fig. 88, ss) lie superficially to the transverse processes of the vertebrae, FT, and are connected with these by muscles and ligaments ; the ventral ends, CO. meet each other in the median plane.

Each half- ring has on its outer surface, rather below the middle of its length, a cup-shaped depression, the glenoid cavity. GC, with which the head of the humerus, HU, articulates. The part of the ring above the glenoid cavity is the scapular portion, the part below it the coracoid portion.

The scapular portion is divided, shortly before the metamorphosis, into a dorsal blade-like part, the suprascapula, ss, which remains in great part cartilaginous throughout life ; and a ventral, more slender, and shaft-like part, the scapula, sc, round which a ring of bone soon forms.

The coracoid portion is, from the first, split into two diverging processes ; an anterior or pre-coracoid portion, and a posterior or coracoid proper. The ventral ends of the coracoid and pre-coracoid of each side grow towards each other and meet, forming a longitudinal band of cartilage, the epi-coracoid ; the two epi-coracoids lie in close contact with each other in the median plane, but do not fuse. Along the anterior border of the pre-coracoid cartilage, a bony rod, the pre-coracoid bone or clavicle, is formed ; and around the coracoid cartilage a tubular sheath of bone, the coracoid bone, is developed. There is thus at first no trace of a sternum, either as a median or paired structure.

During and after the metamorphosis further changes occur. The bones increase in size, especially the scapula and coracoid. The two epi-coracoid cartilages, in place of merely meeting in the median plane, overlap each other to a certain extent, the left epi-coracoid lying dorsal to the right one. From the anterior ends of the epi-coracoid cartilages a pair of small processes grow forwards ; these soon fuse to form the omosternum, which rapidly increases in size. Behind the epi-coracoids, and in close contact with them, a pair of cartilaginous bands appear, which fuse together to form a flat median plate of cartilage ; this gives rise in front to the sternum, round which a ring of bone soon forms, and behind to the xiphi-sternum, which remains permanently cartilaginous.

b. The pelvic girdle also consists at first of two half-rings of cartilage, encircling the hinder part of the trunk. The ventral ends of the half-rings, which are flattened and expanded, are in contact in the median plane, and very early fuse firmly together to form the pelvic symphysis. The dorsal ends are more slender : at first they lie free in the muscles of the body wall ; later on they become connected with the transverse processes of the ninth or sacral vertebra.

Each half-ring has on its outer surface, close to its ventral end, a depression, the cotyloid or acetabular cavity, for articulation with the head of the femur. The part above the acetabulum, which corresponds with the scapular portion of the pectoral girdle, ossifies as the ilium : in the part below the acetabulum, the anterior or pubic portion remains cartilaginous, while the posterior portion ossifies as the ischium.

The pelvic girdle is, in its early stages, and until shortly before the metamorphosis, about the same length as the pectoral girdle ; and, like this, lies at right angles to the vertebral column. As the hind limbs lengthen, during and after the metamorphosis, the ventral or acetabular end of the girdle moves backwards, so that the ilium, which lengthens considerably at the same time, now lies, as in the adult, almost parallel to the backbone ; and the hip joint is shifted to the extreme hinder end of the body.



FIG. 96. The skeleton of the Frog, seen from the dorsal surface, supra-scapula and scapula have been removed.

The left

a, astragalus, c, calcaneum. d, supra-scapula. <?, exoccipital. /, femur, fp, frontoparietal. g, metacarpals. h, hurnerus. i, ilium. To, metatarsals. 1, carpus. j, maxilhi. n, nasal, o, pro-otic, p, pterygoid. pm, premaxilla. g, quadrato-jugal. r, radio-ulna. s, squamosal. se, spheu-etlinioid. sv, sacral vertebra, t, tibio-fibula. . urostylf.



c. The limbs. The skeletal framework of each limb develops from the proximal towards the distal end ; the humerus and the femur being the first bones to be differentiated. The radius and ulna, and the tibia and fibula, are at first independent of each other, but the cartilages of each pair soon fuse. Of the digits, the two preaxial, radial or tibial, of each limb are established first : the others budding out in succession. There is some doubt as to which of the normal five digits is absent in the hand of the adult frog ; and the embryological evidence, though not conclusive, is rather in favour of the view that it is the fifth, and not, as is commonly held, the first digit or pollex that is wanting.

Bibliography

List of the more important Publications dealing with the Development of Frogs.

Alcock, T. : ' On the Development of the Common Frog.' Memoirs of the

Manchester Literary and Philosophical Society, series iii., vol. viii. 1883. Assheton, R. : ' The Development of the Optic Nerve of Vertebrates.' Quarterly

Journal of Microscopical Science, vol. xxxiv. 1892. Balfour, F. M. : 'A Treatise on Comparative Embryology,' vol. ii. 1881. Bambeke, C. van: ' Recherches sur le Developpement du Pelobate brun.' 1867. ' Nouvelles Recherches sur 1'Embryologie des Batraciens.' Archives

de Biologic, i. 1880. Barfurth, D. : ' Versuche fiber die Verwandlung der Froschlarven.' Archiv

fur mikroskopische Anatomie, xxix. 1887.

' Die Riickbildung des Froschlarvenschwanzes und die sogenannten

Sarkoplasten.' Archiv fur mikroskopische Anatomie, xxix. 1887. Bedot, M. : ' Recherches sur le D6veloppement des Nerfs Spinaux chez les

Tritons.' Archives des Sciences Phys. et Nat., xi. 1884. Boas, J. E. V. : ' Ueber den Conus arteriosus und die Arterienbogen der Amphi

bien.' Morphologisches Jahrbuch, vii. 1881.

' Beitrage zur Angiologie der Amphibien.' Morphologisches Jahrbuch, viii. 1882. Bourne, A. G. : On Certain Abnormalities in the Common Frog.' Quarterly

Journal of Microscopical Science, xxiv. 1884. Cope, E. D. : ' On the Relations of the Ilyoid and Otic Elements of the Skeleton

in the Batrachia.' Journal of Morphology, ii. 1888. Duges, A. : ' Recherches sur 1'Osteologie eb la Myologie des Batraciens a leurs

differents Ages.' Memoires de 1'Academie des Sciences. Paris. 1835. Duval, M. : 'Sur le Developpement del'AppareilGenito-urinairede la Grenouille. 1

Revue des Sciences Naturelles. 1882.


Ecker, A. : ' Icones Physiological' Leipzig. 1851-lSV.i.

'The Anatomy of the Frog.' English translation by G. Haslam.

Oxford. 1889. Erlanger, R. von : ' Ueber den Blastoporus der anuren Amphibien, sein

Schicksal und seine Beziehungen zum bleibenden After.' Zoolo gische Jahrbiicher : Abtheilung fiir Anatomie und Ontogenie der Thiere,

iv. 1890. Field, H. F. : ' The Development of the Pronephros and Segmental Duct in

Amphibia.' Bulletin of the Museum of Comparative Anatomy at Harvard College, xxi. ]S9J.

Fiirbringer, M. : ' Zur Entwickelung der Amphibienniere.' Heidelberg. 1877. Gatehouse, J. W. : ' The Development and Life History of the Tadpole.'

Journal of Microscopical and Natural Science, i. ii. 1888 and 1889. Goette, A. : ' Die Entwickelungsgeschichte der Unke.' Leipzig. 187~>. Goppert, E. : ' Die Entwicklung und das spiitere Verhalten des Pankreas der

Amphibien.' Morphologisches Jahrbuch, xvii. 1891. Heron-Royer and C. van Bambeke : ' Le Vestibule de la Douche chez les

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1889. Hertwig, O. : ' Ueber das Zahnsystem der Amphibien und seine Bedeutung

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thierischen Eies.' Morphologisches Jahrbuch, iii. 1877.

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Hinckley, Mary H. : ' Notes on the Development of Rana sylvatica.' Proceedings of the Boston Society of Natural History. 1882. Hochstetter, F. : ' Beitriige zur vergleichenden Anatomie und Entwickelungsgeschichte des Venensystems der Amphibien und Fische.' Morphologisches Jahrbuch, xiii. 1887. Hoffmann, C. K. : ' Zur Entwicklung?geschichte der Urogenitalorgane bei den

Anamnia.' Zeitschrift fiir wissenschaftliche Zoologie, xliv. 1886. Bronn's Klassen und Ordnungen des Thierreichs : Amphibia. 1 873 1878. Houssay, F. : ' Etudes d'Embryologie sur les Vertebres.' Archives de Zoologie

Experimentale, 1890; and Bulletin Scientifique de la France et de la

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of the Zoological Society. 1888. Huxley, T. H. : Article ' Amphibia.' Encyclopaedia Britannica, 9th edition.

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' The Development of the Blood-vessels in the Frog.' Studies from

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Selenka, E. : ' Der embryonale Excretionsapparat der kiemenlosen Hylodes Martinicensis.' Sitzungsberichte der koniglichen Akademie der - \Vissenschaften zu Berlin. 1882. Shore, T. : ' Notes on the Origin of the Liver.' Journal of Anatomy and

Physiology, xxv. 1891. Sidebotham, H. : 'Note on the Fate of the Blastopore in Rana temporaria.

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   Vertebrate Embryology 1893: 1 Introduction | 2 Amphioxus | 3 Frog | 4 Chick | 5 The Rabbit | 6 Human Embryo | Illustrations

Marshall AM. Vertebrate Embryology: A Text-book for Students and Practitioners. (1893) Elder Smith & Co., London.

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