Book - Vertebrate Zoology (1928) 12

From Embryology

Vertebrate Zoology G. R. De Beer (1928)

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Chapter XII Development of Rana (the Frog)=


The egg contains a large quantity of yolk, which is aggregated at the vegetative pole. This pole is light in colour when seen from outside, whereas the opposite animal pole, and indeed the whole animal hemisphere, is darkly pigmented. The nucleus is near the animal pole, which is determined in the ovary, probably by the relation of the developing egg to the little arteries and veins.

The egg is surrounded by three membranes. The inner vitelline membrane is secreted by the egg itself. Outside this is a tough membrane formed by the follicle-cells which surround the egg in the ovary. Outside this again is a coating layer of jelly which is secreted by the glands of the wall of the oviduct, as the egg passes down the latter on its way to the exterior.

At the time of spawning, the males climb on to the backs of the females, and as the latter extrude the eggs from their cloacal apertures, the former shed the sperm over them. Fertilisation thus takes place in the water outside the bodies of the animals. One polar body has been extruded before the egg is laid, the second polar body is pushed out after penetra- tion of the sperm, and the egg- and sperm-pronuclei then fuse.

The jelly swells out on contact with the water, and after fertilisation the vitelline membrane becomes lifted off from the surface of the egg. The egg is then able to rotate, and comes to rest with the axis vertical, i.e. the vegetative pole with the heavy yolk is turned downwards.

The point of entrance of the sperm determines the median plane of symmetry of the future embryo, and, soon after fertili- sation, this is indicated by the formation of the grey crescent (due to the retreat of pigment into the egg) at the point dia- metrically opposite to that at which the sperm entered. The egg can now be orientated with regard to the axes of the future embryo. The animal pole will become the head, and the vegetative pole the tail ; the grey crescent marks the future dorsal side, and the opposite side (where the sperm entered) will be ventral.

Fig. 73. Egg of Rana temporaria (common frog) before and after fertilisa- tion, showing the formation of the grey crescent. (From Jenkinson.) A and B seen from the side ; C and D seen from below ; A and C before and B and D after fertilisation. The animal hemisphere is pig- mented, the vegetative hemisphere is light in colour.


Cleavage in the frog's egg is total, but the size of the various blastomeres is very unequal, owing to the large quantity of yolk. The cells at the vegetative pole are much larger (and fewer in number) than those at the animal pole. The blastoccel is small, and situated nearer to the animal than to the vegetative pole. The bias tula is now a hollow ball, but the hollow is small and its walls are several layers thick.


The cells of the animal hemisphere (which are darkly pigmented) are relatively free from yolk, and there- fore divide faster than the larger light-coloured yolk-laden cells of the vegetative hemisphere. One result of this is that the animal-pole cells begin to grow down over the lighter- coloured cells. This process starts by the formation of a lip of overgrowth in the centre of the grey crescent, forming the dorsal lip of the blastopore. Underneath this lip is a groove formed by the cells tucking in. The lips of the blastopore extend right and left from the site of its first appearance. At the same time the edge of overgrowth moves down towards the vegetative pole, and more and more of the lighter-coloured cells become covered over by the overgrowing darker ones.


Fig. 74. — Formation and closure of the blastopore during gastrulation in Rana, seen from below. (From Jenkinson.) In A the dorsal lip of the blastopore has just appeared ; in B the lateral lips have extended, and they almost meet in C ; in D the ventral lip of the blastopore (which is now a complete circle) has been formed ; and the diameter of the blastopore decreases in E and F.


Fig. 75. — The process of gastrulation in Rana as shown by sagittal sections.

In A the dorsal lip of the blastopore bias just appeared, and it is accen- tuated in B ; in C a definite ingrowth is visible resulting in the formation of the archenteron : in D the ventral lip of the blastopore has appeared, and the yolk-containing cells of the vegetative hemisphere project through the now circular blastopore as the yolk-plug ; in E the archenteron has extended greatly at the expense of the blastocoel, which in F is almost obliterated. During gastrulation the yolk-cells are heaped up on the ventral side of the archenteron, as a result of which the egg rotates until its original axis is more or less horizontal.

a, archenteron ; ap t animal pole ; b, blastoccel ; br, brain ; dl, dorsal lip of blastopore ; in, mesoderm ; ?i, notochord ; nee, neurenteric canal ; np, neuropore ; sc, spinal cord : vl, ventral lip of blastopore ; yc, yolk-cells; yp, yolk-plug.


Fig. 76. — Transverse sections through the closed blastopore of Rana (A) and the primitive streak of Gallus (B).

The groove between the fused lips of the blastopore of Rana is the rem- nant of the blastopore, and corresponds to the primitive groove (ps) of Gallus. ec, ectoderm ; e?i, endoderm ; m, mesoderm ; all of which are continuous with one another at the rim of the blastopore or primitive streak.

Eventually the two horns of the lip of the blastopore meet on the ventral side, and the blastopore is then a closed ring, formed by overgrowing dark cells, and beneath which the tucking-in takes place. This tucking-in is most active on the dorsal side. The groove sinks deeper and deeper into the embryo, as the ingrowing cells push farther and farther fonvards beneath the superficial layer. The groove represents the cavity of the archenteron, largely rilled up by the yolk-cells of the vegetative pole, which are visible inside the rim of the blastopore. The cavity of the blastoccel becomes reduced and obliterated as the cavity of the archenteron increases and gastrulation proceeds ; and the yolk-laden cells of the vegetative pole come to lie on the ventral side of the archenteron.

As the blastopore approaches the vegetative pole its diameter decreases, until when it reaches it, it is a small spherical hole with yolk-cells showing through as the so-called yolk-plug.

The processes of gastrulation therefore entail overgrowth or epiboly, and invagination ; but the invagination cannot take place simply as in Amphioxus owing to the large quantity of yolk present, and it is more in the nature of an ingrowth. At all events, the result of gastrulation is the conversion of the single-layered hollow ball (blastula) into a double-layered sac (gastrula) ; the outer layer (ectoderm) is formed of the cells of the animal hemisphere and those which have grown over, the inner layer (future endoderm and mesoderm) is formed of the cells which have grown in, and of the yolk-laden cells of the vegetative hemisphere. The latter form most of the ventral and the former most of the dorsal wall of the archenteron. The heaping up of the heavy yolk-cells at the ventral side causes the gastrula to rotate within its membranes, so that the former egg-axis lies more or less horizontal instead of vertical ; the ventral side now points downwards and the dorsal side upwards.

Mesoderm and Notochord

The wall of the archenteron contains the cells which are destined to give rise to the noto- chord and to the mesoderm. A strip of cells running along the middle line of the roof of the archenteron is the rudiment of the notochord, and the mesoderm arises as a splitting off (or delamination) of a layer of cells from the remainder of the wall of the archenteron. This layer of mesoderm now separates the ectoderm from the endoderm in most parts of the embryo. Soon, a split arises in the mesoderm layer itself, dividing it into an inner splanchnic layer and an outer parietal or somatic layer. This split is of course the coelomic cavity.

The notochord splits off as a solid rod from the surface of the roof of the archenteron, which still forms a complete covering to the archenteric cavity. This delamination of the mesoderm and notochord from the wall of the archenteron begins in the anterior region of the embryo ; farther back they are not distinct, and merge into the rim of the blastopore. The rim of the blastopore may indeed be defined as the region where the ectoderm, mesoderm, endoderm and notochord are all in contact with a zone of actively growing cells, which contributes new tissue to each layer.

The new mesoderm formed from the blastopore-rim is peristomial, that split off from the wall of the archenteron farther forward, is called gastral mesoderm. Apart from their method of formation, there is no difference between these two kinds of mesodermal tissue.

This activity of the lip or rim of the blastopore is a continua- tion of the process of epiboly, and its result is to produce an elongation of the embryo. Eventually the blastopore becomes oval and slit-like by the apposition to one another of its lateral lips, and its former aperture is represented only by a short groove on the outer surface between these lips. This fact is of importance in connexion with the interpretation of develop- ment in higher forms. The activity of the cells of the blastopore-rim continues after the blastopore is closed, and leads to the outgrowth of the tail.

Fig. 77. — Transverse section through an embryo of Rana showing the separation of the mesoderm (m) from the endodermal wall (en) of the gut (g). ec, ectoderm ; y, yolk-cells. Dorsally the ectoderm is thickening to form the neural folds (nf).

Fig. 78. Transverse section through an embryo of Rana slightly older than the previous, showing the origin of the notochord (n) from the middle line of the roof of the gut. The neural folds (nf) have risen up and enclose a groove between them.

Fig. 79. Transverse section through an embryo of Rana slightly older than the previous, showing the complete separation of the notochord («) from the endodermal wall (en) of the gut (g).

The coelom (c) has arisen as a split in the mesoderm (m), which forms a somite (ms) on each side of the notochord. The neural folds («/) have closed over the groove converting it into the nerve-tube (nc)> on each side of which are the neural crests (ncr). ec, ectoderm ; y, yolk cells.

Fig. 80. — Sagittal section through an embryo of Rana.a, anus ; b, brain ; g, gut ; h, hypophysis ; ht, heart ; /, liver notochord ; sc> nerve- (spinal) cord ; y, yolk-cells.


The ectoderm along the middle line of the dorsal side thickens forming the neural plate. A pair of longitudinal ridges arise on each side of it, known as the neural folds, and they enclose a groove between them. This groove is wider in front, where the brain will be, than behind, in the region of the future spinal cord. Posteriorly the neural folds embrace the blastopore. As the folds rise up they arch over the groove, which becomes converted into the nerve-tube. The nerve-tube communicates with the cavity of the gut posteriorly through the neurenteric canal and blastopore, which is still open at this stage.

The lateral part of the thickening which gave rise to the neural plate does not get folded into the nerve-tube when the neural folds meet. It lies just to the side of the point of fusion of the neural folds, and forms the neural crest. The cells of the neural crest are destined to give rise to the afferent sensory nerve-cells, whose cell-bodies form the ganglia on the dorsal roots of the nerves, and to the sheaths of the nerves.


The mesoderm on each side of the nerve- tube and notochord becomes thickened and divided into blocks, which are the somites from which the myotomes develop ; they are metamerically segmented. This segmentation begins anteriorly and proceeds backwards ; but it does not affect the more ventrally-situated mesoderm. Whereas the dorsal portion of the ccelomic cavity (on a level with the myotomes) is interrupted by transverse septa separating the mesodermal somites from the somites in front and behind, and consists of a number of myoccels equal to the number of somites, the ventral portion of the ccelomic cavity is continuous and un- interrupted by septa.

The segmented region of the mesoderm is called the verte- bral plate, the unsegmented portion is the lateral plate. Between each somite and the lateral plate immediately below it is a small region of segmented mesoderm known as the inter- mediate cell-mass, or nephrotome. From these structures the tubules of the kidneys will arise, and they are therefore also segmental. Eventually, the vertebral plate separates completely from the lateral plate, and the myotomes grow down in the body- wall lateral to the splanchnoccel to give rise to the muscles of the ventral surface, of the limbs, and the hypoglossal muscula- ture beneath the mouth.

Muscles formed from myotomes are always innervated by ventral nerve-roots, and as the myotomes are segmental, the ventral nerve-roots which grow freely out from the nerve-tube are segmental also. Further, the neural crest becomes sub- divided into pieces corresponding to the myotomes, these are the rudiments of the dorsal-root ganglia. The cells in these ganglia develop one process which grows into the nerve- tube, and another which pushes out to its destination in the body. These dorsal nerve-roots are therefore segmental also.

Median to the myotomes, cells are proliferated by the somites to form clouds of mesenchyme surrounding the nerve- tube and notochord. These cells are the sclerotomes (likewise segmental) from which later on the vertebrae are developed.

Another instance of segmentation will be seen in connexion with blood-vessels, which run transversely in the septa between adjacent segments. Although in the adult animal much of this segmentation is obscured and modified, it is important to note that in development, metameric segmentation is as well marked as in Amphioxus, except for the splanchnocoel.

Fig. 81. — Transverse section through a young tadpole larva of Rana showing the origin of the kidneys.

Fig. 82. — Transverse section through a tadpole larva of Rana older than the previous, showing the formation of the kidneys and the lungs. The section'passes through the transverse septum across which the duc- tus Cuvieri lead from the cardinal veins to the heart, c, ccelom dorsal to the transverse septum ; cv, cardinal vein ; dC, ductus Cuvieri ; g, gut ; gl, glottis ; icm, intermediate cell-mass or nephrotome ; /, lung ; Ida, lateral dorsal aorta ; Ir, liver ; m, mesoderm ; my, myotome ; n, notochord ; nc, nerve-cord ; tier, neural crest ; nl, nephrocoel ; pt, pronephric tubules ; sp, splanchnoccel ; y, yolk-cells.

As in invertebrates, segmentation begins with the mesoderm and extends to the other tissues.

The Gut

The gut is a cavity with an accumulation of yolk- cells in the hinder part of its floor. This posterior region will become the intestine, and in front of it will develop the pharynx, oesophagus, and stomach. After the blastopore has closed, the anus breaks through near the same spot, as a result of the sinking in of an ectodermal pit (the proctodeum) till it meets the endoderm, and perforation ensuing. In a similar way, the mouth perforates in front, at the bottom of an ectodermal pit (the stomodaeum).

Behind the mouth, in the region of what will be the pharynx, five pouches grow out on each side from the endoderm to the ectoderm. These are the rudiments of the visceral clefts. The first pair corresponds to the spiracles of the dogfish, but here they do not become perforated to the exterior. Their cavities persist as the Eustachian tubes. The remaining four pairs of pouches become the gill-slits, through which the pharynx communicates with the exterior.

Alternating with the visceral clefts are the visceral arches. The 1 st or mandibular arch separates the mouth from the Eustachian tube (or hyomandibular cleft) ; the 2nd (or hyoid arch) is between the latter and the 1st gill-slit. The 6th visceral arch is behind the 4th gill-slit.

From the upper part of the 3rd, 4th, and 5th visceral arches, tufts grow out on each side which will become the external gills ; blood-vessels enter them, and they serve as the first respiratory organs. The dorsal part of the 1st gill-pouch on each side proliferates to form a body which is the rudiment of the thymus gland.

In the floor of the pharynx between the 2nd gill-slits, a downgrowth is formed, which ultimately loses its connexion with the pharynx and forms the thyroid gland. Close to the point of origin of the thyroid gland is an elevation which will eventually give rise to the tongue. A little farther back, also in the middle line of the floor of the pharynx, the rudiment of the larynx appears as a groove. This deepens into a tube remaining in connexion with the pharynx through the glottis.

From the posterior end of the larynx, the lungs develop as sacs stretching back parallel to the oesophagus on each side.


Fig. 83. — Horizontal section through the head of a tadpole of Rana, showing the formation of the visceral clefts (gill-slits).

b 1, b 3, b 4, b 5, b 6, blood-vessels running in the first, third, fourth, fifth, and sixth visceral arches (the vessels in the third and fourth arches will become the carotid and systemic arches respectively) ; eg, external gills ; 1, infundibulum (floor of the forebrain) ; ic, internal carotid artery ; n, nasal sac ; oe, oesophagus ; pd, pronephric duct ; pt, pronephric funnel ; sp, splanchnoccel ; vc, 1 to 5, first to fifth visceral cleft (the first will give rise to the Eustachian tube) ; V, VII, IX, branches of the trigeminal, facial, and glossopharyngeal nerve, running in the first, second, and third visceral arches respectively.

The liver arises as a ventral outgrowth of the floor of the gut, just in front of the mass of yolk-cells, and extending back beneath them. Part of the cavity of this diverticulum becomes the gall-bladder, and the open connexion with the rest of the gut persists as the bile-duct. Close to this point, the pancreas arises as a number (three) of outgrowths, which remain con- nected with the gut by the pancreatic duct.

The cavity of the intestine is still small owing to the presence of the yolk-cells. After hatching, this yolk becomes absorbed and the intestine elongates very much, becoming coiled like a watchspring. Behind the intestine is the region of the gut which will become the rectum and cloaca. A downgrowth from the latter gives rise to the urinary bladder.

During this time, the right and left splanchnoccelic cavities have applied their outer for somatic) layer to the body- wall, and their inner (or splanchnic) layer to the endoderm of the gut and all its derivatives. Ventrally, most of the membranes forming the separation between the right and left splanchno- ccelic cavities break down ; but dorsally these walls persist forming the dorsal mesentery. This mesentery is composed of two closely apposed layers of ccelomic epithelium spreading round the gut and suspending it. It may be noticed, therefore, that the gut is not strictly in the ccelomic cavity at all ; it merely hangs in a fold of ccelomic epithelium which bulges into the ccelomic cavity. From the cells of this splanchnic layer are developed the smooth muscles of the stomach, intestine, and bladder.


Beneath the floor of the gut, and between it and the underlying splanchnic layer of ccelomic epithelium, there are some scattered mesoderm-cells which become arranged in the form of a tube, or subintestinal vessel. In the region of the pharynx, this tube forms the endothelial lining of the heart. The ccelomic epithelium (splanchnic layer) surrounds this tube and suspends it as it were in a little mesentery of its own from the floor of the pharynx (the dorsal mesocardium). The musculature of the wall of the heart is derived from this layer of ccelomic epithelium, and that part of the splanchnocoel in which the heart finds itself is now called the pericardium. Later on, the various parts of the heart are differentiated. Posteriorly, the heart is continuous with two tubes, the vitelline veins, which run from the yolk-cells and the rudiment of the liver.

The dorsal aorta arises as a pair of longitudinal vessels, close beneath the notochord. The two remain separate anteriorly, as the lateral dorsal aortas and their prolongations into the head, the internal carotids. Behind, they join and fuse together along the whole of the rest of the body, forming the single dorsal aorta.

Fig. 84. Transverse sections through embryos of Rana, showing the origin of the heart. Only the ventral portion of the body is shown. A, early stage ; the cells which will give rise to the endothelial lining of the heart (e) are still scattered ; they lie between the endodermal floor of the gut (ef) and the mesoderm (m) ; the mesoderm contains right and left ccelomic cavities (p) still separated by a septum ; ec, ectoderm. B, later stage, the endothelial cells are begin- ning to arrange themselves, and the ccelomic epithelium underlying them becomes thickened and depressed. C, the endothelial lining of the heart is now a closed tube, and the ccelomic epithelium has folded round it forming its muscular wall (mzv) ; it remains connected with the ordinary ccelomic epithelium above by the dorsal mesocardium (dtti) ; beneath the heart, the septum between the right and left ccelomic cavities has disappeared so that the ccelom is continuous and is now known as the pericardium (p, pc).

Beneath the pharynx, the heart communicates forwards with the ventral aorta. In each of the 3rd to 6th visceral arches, between the gill-slits, a vessel appears which com- municates below with the ventral aorta and above with the lateral dorsal aorta of its own side. In this way the series of pairs of aortic arches arise, alternating with the gill-slits. When the capillaries of the gills arise, they connect with the aortic arches which become interrupted. There are now afferent branchial arteries carrying blood from the ventral aorta to the gills, and efferent branchial arteries connecting the gills with the lateral dorsal aorta. Rudiments of aortic arches appear in the mandibular and hyoid arches.

The dorsal aorta sends arteries to the gut, which they reach by passing down between the two layers which form the dorsal mesentery.

The arteries become surrounded by coats of smooth muscle. Of the veins, the posterior cardinals arise near and parallel to the dorsal aorta. Their anterior prolongations are the anterior cardinal veins which run one on each side of the brain, and which, later on, contribute to the formation of the internal jugulars. At this period, the pericardial cavity is open posteriorly and communicates with the general perivisceral splanchnoccel. In the region of the heart, the splanchnic and somatic layers of the ccelomic epithelium approach one another and fuse, forming the lateral mesocardia which connect the gut- wall with the body- wall. This connexion of course interrupts the coelomic cavity, and soon the pericardial cavity is completely shut off from the perivisceral cavity behind it. The partition formed by the lateral mesocardia is the transverse septum, and it is important in that it enables the cardinal veins, which are in the body-wall, to communicate via the ductus Cuvieri (or superior venae cava?) with the heart, which is of course situated in the gut- wall.

A third connexion between the heart and the veins of the body-wall is established by the formation of the inferior vena cava, which runs down in the mesentery from the hinder region of the body.

As the liver develops, the vitelline veins (which are really that part of the subintestinal vessel which is behind the heart) undergo some modification. The hinder portion connects the intestine behind with the liver in front, forming the hepatic portal vein. The anterior portion connects the liver with the heart, and gives rise to the hepatic veins. The formation of the renal portal veins will be described in connexion with the kidneys.

The blood itself, or rather its red corpuscles, arise from structures known as blood-islands. These are formed from the layer of mesoderm which was split off from the floor of the original archenteric wall just beneath the mass of yolk-cells, behind the rudiment of the liver ; they are regions of rapid cell- proliferation. From here, the corpuscles enter the blood- vessels (which were previously empty) through the vitelline veins.

The Kidneys

The kidneys are formed from the meso- dermal tissue situated at the junction between the myoccels and the splanchnoccel and which is known as the nephrotome or intermediate cell-mass. On each side a thickening appears in the region of the 2nd to 4th segments of the trunk of the embryo. This thickening extends back on each side as a rod of cells, between the outer layer of the splanchnocoel and the skin, to the cloaca. The thickening hollows out and a cavity appears which connects with the splanchnoccel by three openings surrounded with cilia. These are the ccelomic funnels. The rod of cells also becomes hollow and opens into the cloaca behind and connects with the cavity in front into which the ccelomic funnels open. There is now therefore a direct communication on each side between the ccelom and the cloaca. The three ccelomostomes and the little tubes or tubules into which they lead, together form the pronephros, which is the first and most anterior portion of the kidney to develop. The tube connecting it with the cloaca is the pronephric duct.

The tubules elongate and coil about, and as the posterior cardinal veins develop just in this region, the tubules are as it were bathed in the venous spaces. At the same time, capillaries grow out from the dorsal aorta forming the glomus, which projects laterally towards the openings of the ccelo- mostomes from the mesentery, on each side.

The pronephros is the functional kidney of the embryo and early larva. Later on, however, it degenerates, and its function is taken over by another set of coelomic funnels and tubules, which together form the mesonephros.

The mesonephros is developed from the of half a dozen segments, some little distance behind the pro- nephros. Cavities hollow out in the nephro tomes, and these connect with the splanchnoccel by coelomic ciliated funnels, and by coiled tubules with the pronephric duct. The latter loses connexion with the degenerating pronephros, and, after being tapped so to speak by the mesonephric tubules, it is known as the mesonephric or Wolffian duct.

The tubules multiply by branching, and form little chambers or Bowman's capsules which lose their connexion with the coelomic funnels. Arterioles from the dorsal aorta and venules from the posterior cardinal veins form little bunches of capillaries which project into the capsules forming glomeruli. Capsule and glomerulus together form a Malpighian corpuscle. That portion of the posterior cardinal veins which lies behind the mesonephros becomes the renal portal vein, which brings blood from the posterior regions of the body to the kidneys. The mesonephros is the functional kidney of the adult. It extracts excretory matter from the blood stream and passes it down the Wolffian duct to the cloaca, which develops a ventral outpushing, the urinary bladder.

Reproductive Organs

The gonads arise as ridges which project into the splanchnoccel on each side of the dorsal mesentery. The germ-cells which they contain are derived partly from the coelomic epithelium in situ, and partly from cells which have migrated up in the mesentery from the yolk- mass. For a long time the sexes are indistinguishable. Strings of germ- cells grow in, away from the surface of the gonads, forming the genital strands. In embryos which are going to be males, these hollow out forming the seminiferous tubules which become connected with the cavities of the tubules of the mesonephros. In this way the vasa efferentia are formed, and they may be regarded as persistent coelomic funnels, placing the testis in communication with the exterior (via the cloaca). The sperms therefore make their way through the tubules of the mesonephros, down the Wolffian duct or vas deferens as it can also be called, to the exterior.

The Mullerian ducts develop as grooves in the roof of the splanchnocoel at the side of the gonads. The sides of the groove grow over, and convert it into a tube which opens into the coelomic cavity in front (near the place where the pronephric funnels were), and grows back to open into the cloaca behind. In males the Mullerian ducts disappear.

The kidneys and gonoducts are mesodermal all the way, and are really ccelomoducts, whose primitive function is probably to connect the coelomic cavity with the exterior and so allow the germ-cells to escape. They take on the function of excretion as a result of the proximity of the tubules to the blood-vessels.

On the other hand, the nephridia have excretion as their primitive function ; they do not occur in Chordate animals other than Amphioxus.

Paired Sense-organs and Brain. — The eyes make their appearance as outpushings from the sides of the brain, forming the optic vesicles. Each of these vesicles grows towards the overlying ectoderm, and becomes an optic cup, with the concave side turned outwards. The lens is formed from the ectoderm overlying the optic cup, as a little vesicle which soon becomes nipped off, and sinks into place at the mouth of the cup. While the cup is really part of the brain, the lens is part of the epidermis, but both are ectodermal. The outer lining of the cup forms the pigment or tapetum layer, the inner lining of the cup differentiates to form the sensitive retina, and it is inverted since the nerve-fibres run between the sensitive cells and the seen object (see p. 24). Outside the tapetum, mesodermal tissue gives rise to the choroid and sclerotic (including the transparent cornea) layers, just as round the brain it forms the pia mater (vascular) and dura mater (protective). The eye-muscles arise from mesodermal tissue which represents the three first somites of the head.

The ears arise as a pair of ingrowths from the ectoderm behind the eyes, forming the auditory vesicles. Their connexion with the ectoderm becomes severed and the remains of the connecting stalk is the ductus endolymphaticus. Each vesicle now forms a closed sac at the side of the hinder part of the brain, and above the tympanic cavity, which develops as an expansion of the hyomandibular visceral pouch (Eustachian tube). From the dorsal portion of each vesicle three shelf- like projections are formed. The centre of each shelf becomes perforated, converting the shelf into a half- ring. In this way the semicircular canals are formed. The cavity of the auditory sac contains endolymph. Between the wall of the sac and the capsule of connective tissue which surrounds it, is the perilymph. The capsule eventually becomes cartilaginous, and later on, bony ; but certain apertures are left. One of these is the fenestra rotunda, and another is the fenestra ovalis on to which the base of the columella auris fits. The outer end of the columella auris is applied to the thin lateral wall of the tympanic cavity which forms the tympanic membrane.

It may be mentioned here that, remarkable as it may seem, the ears are responsible for the formation of the so-called calci- gerous glands, or glands of Schwammerdamm. These glands are conspicuous objects in the trunk of the frog, lying on each side of the vertebrae, close to the points of exit of the spinal nerves. Diverticula from the auditory vesicles grow into the brain-case, and back down the canal formed by the vertebrae and which contains the spinal cord. From here, the diverticula of the auditory vesicle emerge through the foramina for the spinal nerves and give rise to the glands of Schwammerdamm (function unknown).

Fig. 85. Transverse sections through the head of embryos of Rana showing the development of the eyes.

A, early stage, in which the optic vesicles (ov) have been pushed out on each side from the forebrain (fb). B, the outer walls of the optic vesicles have been pushed in, converting them into optic cups (oc) ; the lens (/) arises opposite the mouth of the optic cup from the ectoderm (ec). C, late stage ; the cavity of the optic vesicle has been almost obliterated, the lateral layer of the optic cup is the retina (r) and the median layer is the pigment layer (pi), the stalk attaching the optic cup to the forebrain is the optic nerve (on), the lens has become detached from the ectoderm.

Fig. 86. Transverse section through an embryo of Rana showing the formation of the ears.

an, auditory nerve ; av, auditory vesicle ; bv, blood-vessels running in the visceral arches ; eg, external gills ; g, gut ; h, heart ; hb, hindbrain ; n, notochord ; p, pericardium ; ta, truncus arteriosus ; vs, ventral sucker.

The olfactory organs arise as a pair of thickenings of the ectoderm, which sink in to form pits just above the mouth. The cells lining these pits will give rise to the olfactory epithe- lium. Behind, the pits reach the roof of the mouth and break through forming the internal nostrils.

The various regions of the brain are roughly marked out even before the neural folds have closed over. The definitive form of the brain is soon reached by means of foldings and thickenings of its walls in certain places.

A median ectodermal inpushing arises from the epidermis of the front of the head, just above the mouth. This is the hypophysis which grows back beneath the floor of the fore- brain until it meets and fuses with the infundibular downgrowth from the brain. Hypophysis and infundibulum together form the pituitary body.

Placodes and Lateral-line Organs

The dorsal nerves and ganglia in the region of the trunk consist of nerve- cells which have been derived entirely from the neural crests. In the region of the head, the dorsal nerve-ganglia are derived not only from the neural crest, but also from thickenings of the ectoderm at the sides of the head called placodes. Placodes are proliferations of the deeper layers of the epidermis which contribute cells to the underlying ganglia. The profundus, trigeminal, facial, glossopharyngeal and vagus ganglia all derive cells from the epidermis in this way, and the auditory nerve is formed from the placode which invaginates with the auditory sac. Indeed, the thickenings of the epidermis which later become pushed in to form the olfactory sacs, the lens, and the auditory sacs, may themselves be regarded as placodes.

There are two kinds of placodes : an upper row of dorso- lateral placodes which give rise to the lateral-line sense- organs and to the nerve-cells whose fibres innervate them ; a lower row of epibranchial placodes situated at the dorsal ends of the visceral slits, and which give rise to the nerve- cells whose fibres innervate the sense-organs of taste.

Sympathetic System and Adrenals. — The dorsal nerve- root, formed by fibres which have grown out from cells in the dorsal-root ganglion, and the ventral nerve-root which has grown out from the spinal cord, join to form a mixed nerve. Certain cells migrate out from the spinal cord, and, leaving the mixed nerve, make for the side of the dorsal aorta where they form the sympathetic ganglia. These ganglia remain con- nected with the mixed nerve by the rami communicantes. The sympathetic ganglia are, like the mixed spinal nerves, seg- mentary arranged. They soon become connected by fibres running to the (sympathetic) ganglia in front and behind them forming the sympathetic trunks. From the sympathetic ganglia, " postganglionic " fibres are distributed to the smooth muscles of the gut, oviducts, and blood-vessels. Other cells migrate out from the sympathetic ganglia, and give rise to the medulla of the adrenal bodies. The cortex of these bodies is derived from the ccelomic epithelium in the region between the mesonephric kidneys.

It may be mentioned that cells migrate out from the hind- brain along the vagus and eventually come to lie on the surface of the heart and gut, forming part of the parasympathetic system.


The vertebral column arises in the form of paired cartilages beside the notochord, derived from the sclerotomes. Each vertebra arises opposite the septum separating two segments ; the vertebrae are therefore inter- segmental in position.

In the skull, paired trabecular arise as struts underlying the forebrain, and, behind them, paired parachordals flank the notochord. The ptery go- quadrate or skeleton of the upper jaw arises early, and fuses on to the remainder of the skull by its ascending process. The auditory sac becomes surrounded by a cartilaginous capsule which gets attached to the para- chordals on each side. Similarly, nasal capsules surround the olfactory sacs and become attached to the front of the trabecular. The floor of the skull is established in this way, and the sides and roof develop later.

In each of the visceral arches separating the gill-slits, cartilaginous struts develop. In the mandibular arch, these are the pterygo-quadrate, and Meckel's cartilage which forms the lower jaw. The dorsal portion of the skeleton of the 2nd or hyoid arch forms the columella auris. The cartilages of the remainder of the arches eventually form a plate beneath the floor of the mouth and pharynx, and which by raising and lowering this floor assists in the process of respiration. The skeleton of the limbs and girdles does not appear until a late stage of development.

This cartilaginous skeleton is later on partly replaced by cartilage-bones, and in addition, membrane-bones are developed.

Teeth arise late. In their formation, an ingrowth of ecto- derm takes place inside the margin of the mouth, forming the enamel-organs of the teeth. These secrete a cap of enamel beneath which the mesodermal cells produce the body of the tooth which is composed of dentine. Eventually the tooth is pushed up through the surface of the mouth and its base is attached to the bone of the jaw.


By the time that differentiation and the forma- tion of organs have proceeded as far as has just been described, the embryo emerges from its membranes and hatches into a free-swimming larva which is familiarly known as the tadpole. Its ectoderm is ciliated, and just beneath the mouth it has a V-shaped sucker by means of which it can attach itself to objects. Its tail elongates and develops dorsal and ventral extensions or fins, which make it a very efficient organ for swimming. Its food consists of vegetable matter, its stock of yolk being by now used up. Food is seized by the edges of the mouth or lips which are assisted by horny epidermal teeth, which have of course nothing to do with the true teeth.

From the sides of the head, folds grow back which cover over the gill-slits. The external gills disappear, and so-called internal gills develop in the walls of the gill-slits and subserve the function of respiration. The folds just mentioned form the operculum, which leaves only a small hole on the left side through which the water which passes through the gill-slits may escape.

The organisation of the larva is just like that of a fish, and there is little indication of the frog into which it will develop. The changes which take place in the conversion of the tadpole into the frog are known as metamorphosis.


The chief differences between the organisation of the tadpole and that of the frog concerns the limbs, lungs and pulmonary respiration, intestine, tongue, and tail.

The limbs arise as buds in tadpoles about half an inch long, and muscles grow into them from the myotomes. The buds of the forelimbs are, however, concealed beneath the operculum, and are therefore invisible. Those of the hind- limbs are situated at the base of the tail, on each side of the cloaca. In time, the fore limbs grow out through the operculum, making use of the opening on the left side and making a new one on the right. Soon the limbs become visibly jointed and the toes appear.

Meanwhile, the lungs are developing, and to each of them there runs a blood-vessel which is formed as a branch from the efferent artery of the last or 6th arch. This vessel is the rudiment of the pulmonary artery. From time to time, the tadpole takes in a gulp of air at the surface of the water and fills its lungs. A certain amount of oxygenation of the blood now begins to take place in the lungs, and the gill-circulation becomes reduced by the establishment of direct connexions between the afferent and efferent branchial arteries. The gills therefore become " short-circuited," and left out of the circulation gradually as more and more of the blood goes to the lungs to be oxygenated, and returns to the heart by the pulmonary veins. The now continuous vessel in the 3rd visceral arch becomes the carotid, that in the 4th becomes the systemic arch, that in the 5th disappears, and the 6th as already seen becomes the pulmonary. The lateral dorsal aorta between the dorsal ends of the carotid and systemic arches (the ductus caroticus) disappears, as also does the connexion between the pulmonary artery and the lateral dorsal aorta (ductus arteriosus, or Botalli). After this change, the organism is perfectly adapted to breathe in air after the manner of land-animals.

The gills disappear ; the gill-slits close up ; the animal ceases feeding, and the horny teeth drop off. The mouth becomes wider and its angle moves farther back. The tongue develops, and the eyes become more prominent and bulge out from the top of the head. The lateral-line organs disappear and the skin is shed. Glands appear which will keep it moist on land. Internally, great changes take place in the intestine, which loses its watchspring-like coils, and becomes relatively much shorter. This is an adaptation to the carnivorous habits of the frog, for less surface is required for the digestion of a meal of animal food. Lastly, the tail becomes reduced and finally completely absorbed, its debris being ingested by wandering white blood-corpuscles, or phagocytes.

This astonishing and comparatively rapid change is brought about by the secretion of the thyroid gland, which has been increasing until it reaches a size sufficient to " pull the trigger " of metamorphosis. During the process of change the weight of the body actually decreases, but after coming out on land and recommencing to feed, the size of the young frog increases.


Jenkinson, J. W. Vertebrate Embryology. Oxford, at the Clarendon Press, 1913.

Kellicott, W. E. Chordate Development. Henry Holt, New York, 1913.

Morgan, T. H. The Development of the Frog's Egg. Macmillan, New York, 1897.

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Pages where the terms "Historic" (textbooks, papers, people, recommendations) appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms, interpretations and recommendations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)
Vertebrate Zoology 1928: PART I 1. The Vertebrate Type as contrasted with the Invertebrate | 2. Amphioxus, a primitive Chordate | 3. Petromyzon, a Chordate with a skull, heart, and kidney | 4. Scyllium, a Chordate with jaws, stomach, and fins | 5. Gadus, a Chordate with bone | 6. Ceratodus, a Chordate with a lung | 7. Triton, a Chordate with 5-toed limbs | 8. Lacerta, a Chordate living entirely on land | 9. Columba, a Chordate with wings | 10. Lepus, a warm-blooded, viviparous Chordate PART II 11. The development of Amphioxus | 12. The development of Rana (the Frog) | 13. The development of Gallus (the Chick) | 14. The development of Lepus (the Rabbit) PART III 15. The Blastopore | 16. The Embryonic Membranes | 17. The Skin and its derivatives | 18. The Teeth | 19. The Coelom and Mesoderm | 20. The Skull | 21. The Vertebral Column, Ribs, and Sternum | 22. Fins and Limbs | 23. The Tail | 24. The Vascular System | 25. The Respiratory system | 26. The Alimentary system | 27. The Excretory and Reproductive systems | 28. The Head and Neck | 29. The functional divisions of the Nervous system | 30. The Brain and comparative Behaviour | 31. The Autonomic Nervous system | 32. The Sense-organs | 33. The Ductless glands | 34. Regulatory mechanisms | 35. Blood-relationships among the Chordates PART IV 36. The bearing of Physical and Climatic factors on Chordates | 37. The origin of Chordates, and their radiation as aquatic animals | 38. The evolution of the Amphibia : the first land-Chordates | 39. The evolution of the Reptiles | 40. The evolution of the Birds | 41. The evolution of the Mammalia | 42. The evolution of the Primates and Man | 43. Conclusions | Figures | Historic Embryology

Cite this page: Hill, M.A. (2024, June 18) Embryology Book - Vertebrate Zoology (1928) 12. Retrieved from

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