Book - Outlines of Chordate Development 3
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Kellicott WE. Outlines of Chordate Development (1913) Henry Holt and Co., New York.
- Outlines of Chordate Development: 1. Amphioxus | 2. Early Frog | 3. Later Frog Organogeny | 4. Early Chick - Embryonic Membranes and Appendages | 5. Later Chick - Organogeny | 6. Early Mammal - Embryonic Membranes and Appendages | Figures
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- 1 Chapter 3 The Later Development Of The Frog - Organogeny
- 1.1 Introduction
- 1.2 The Nervous System
- 1.3 The Special Sense Organs
- 1.4 The Alimentary Tract And Its Appendages
- 1.5 The Mesodermal Somites
- 1.6 The Vascular System
- 1.7 The Urinogenital System
- 1.8 The Skeleton And Teeth
- 1.9 References to Literature
Chapter 3 The Later Development Of The Frog - Organogeny
IN this chapter we shall trace the chief events in the development of the frog tadpole, from the stage described at the close of the preceding chapter, i.e., just after elongation is inaugurated by the enlargement of the head and the outgrowth of the tail. The more important changes in external form and in habit have been described in the introduction to the preceding chapter, and we may turn at once to the description of the internal processes of development.
The developmental history of no single species of frog is known with even fair completeness, and we should note that this chapter presents a composite account of the development of the genus Rana. No attempt has been made, save in occasional instances, to distinguish the species serving as the basis for different sections; these vary somewhat in details, but since details are largely omitted, little confusion is likely to follow such treatment. The species of Rana chiefly serving as the material for this account are the American species, sylvatica, palustris, and virescens, and the European temporaria, esculenta, fusca, and muta.
While the early history of the frog embryo is fairly well known, there are still many gaps in our knowledge of the later development of the tadpole, gaps which sometimes seem of remarkable proportions in view of the extent to which the frog is used as an object of embryological study.
No accurate and convenient description of the age of the frog larva has been determined, since the rate of development varies so markedly with temperature changes before the opening of the mouth, and afterward with the abundance of food. At the time of hatching, which is usually between one and two weeks after fertilization, the larvae of most species are approximately 6-7 mm. in total length. Another frequent reference point is the time of the opening of the mouth, which usually occurs in tadpoles of 9-10 mm., only a few days after hatching. The limbs appear as small buds in tadpoles of 11-12 mm.; the fore-limbs are of course concealed underneath the operculum, but they develop at about the same time and rate as the hindlimbs.
The Nervous System
The Central Nervous System
In the preceding chapter we described the formation of the neural tube and noted the differentiation between the narrow spinal cord and the dilated brain region. Posteriorly the cord is bent downward toward the blastopore, and the cavity of the cord is continuous with the archenteron by way of the neurenteric canal. Anteriorly the brain is strongly flexed around the tip of the notochord. The neuropore, which is located anteriorly from the tip of the chorda, has just closed and remains connected with the surface ectoderm by a broad cone of pigmented cells (Fig. 37, A).
The development of the brain from the stage described is comparatively simple. In its early history it differs from most other forms in two important respects; no neuromeres or brain segments are indicated, and the division of the primitive brain into its primary fore-, mid-, and hind-brain regions is incompletely indicated and appears relatively late. The chief morphological characteristics of the brain result largely from two groups of processes, (a) thickenings and thinnings, (6) outgrowths and ingrowths of the wall. In describing these processes it is convenient to distinguish the roof, floor, and sides of the brain tube.
One of the chief features of the brain is its well-marked ventral flexure, the large anterior part of the brain lying below the level of the notochord (Figs. 37, 40); this flexure remains a permanent characteristic of the brain, although as we shall see, it soon becomes masked by the unequal growth of the neighboring regions. Just opposite the tip of the chorda the floor of the brain becomes slightly thickened as the tuberculum posterius, and in the roof, obliquely upward and forward from this., appears a rather extensive dorsal thickening (Fig. 41). With the aid of these landmarks we may map out the location of the future brain regions. A plane passing from the tuberculum posterius in front of the dorsal thickening, marks approximately the limit between the primary fore-brain or prosencephalon, and the mid-brain or mesencephalon; while a plane passing from the tuberculum posterius behind the dorsal thickening, marks the limit between mesencephalon and the primary hind-brain or rhombencephalon. The beginning of the rhombencephalon is also indicated by a considerable transverse extension of the brain tube; posteriorly the rhombencephalon passes insensibly into the spinal cord.
We may now proceed to describe the more important events in the development of each of these primary divisions of the brain. We should note in advance that the prosencephalon forms the olfactory lobes and cerebral hemispheres (tekncephalori) and the between-brain (diencephalon) : the mesencephalon forms the region of the optic lobes and chiasma: the rhombencephalon forms the cerebellum (metencephalon) and the medulla oblongata or spinal bulb (myelencephalon) .
The Prosencephalon. The cells of the ectodermal cone opposite the neuropore (Fig. 40) , soon scatter, as the tissues of the head push out in advance of the brain, and no trace is left of the original location of this structure, save a slight bay or olfactory recess, which soon disappears. Below this level the anterior wall of the fore-brain remains somewhat thickened for a time, as the lamina terminalis. This extends to the ventral side of the brain where the optic stalks extend out from the fore-brain. These are hollow and their cavities are continuous with the cavity of the prosencephalon. The regions of the anterior and posterior borders of their attachment early become considerably thickened as the torus transversus and the rudiments of the optic chiasma and thalami, respectively (Figs. 41, 42); the former becomes the seat of the anterior, and certain other, commissures of the brain. The narrow depression between these two thickenings is the recessus options, i.e., the passage to the cavities of the optic stalks. The posterior side of the prosencephalon extends backward beneath the tip of the notochord forming a well-marked outgrowth, the infundibulum.
Fig. 40. Median sagittal section through the brain of an embryo R. fusca, of 2.3 mm. From Von Kupffer (Hertwig's Handbuch, etc.). cd, Notochord; d, superficial layer of ectoderm ("deckschicht") ; en, endodermal lining of pharynx; g, inner or nervous layer of ectoderm; hy, hypophysis; J, infundibulum; kg, conical proliferation of ectoderm cells at the point of closure of the neural folds.
Somewhat later the entire dorsal wall of the prosencephalon becomes thinner, and toward its posterior limit an evagination appears which is the beginning of the epiphysis or pineal body (Fig. 42). In front of this the roof ultimately becomes nonnervous and forms a series of highly vascular folds projecting down into the cavity of the brain; this is the choroid plexus of the third ventricle. Later there develop, between this choroid plexus and the epiphysis, the habenular ganglia and commissure, and much later there develops, in front of this, a dorsal outgrowth of the wall, the paraphysis. That part of the prosencephalon extending from the choroid plexus and epiphysis on the dorsal side, to the inf undibulum on the ventral side, is known as the diencephalon or between-brain, while the remaining anterior portion is the telencephalon or secondary fore-brain.
Fig. 41. Median sagittal section through the brain of an embryo R. fusca, of 2.3 mm. length, but in a more advanced stage than that of Fig. 40. From Von Kupffer (Hertwig's Handbuch, etc.). cd, Notochord; cw, rudiment of optic chiasma; dw, dorsal thickening; e, rudiment of epiphysis; en, endodermal lining of pharynx; hy, hypophysis; /, inf undibulum; It, lamina terminalis; M, mesencephalon; P, prose ncephalon; R, rhombencephalon; sk, rudiment of olfactory placode; tp, tuberculum posterius; tr, torus transversus.
Considerably later (about 7 mm. or time of hatching) the rudiments of the cerebral hemispheres appear, growing outward and forward from the sides of the telencephalon (Fig. 42, A). These ultimately become very large and extend far in front of the median region. They have thick inner and outer walls, and contain extensions of the cavity of the telencephalon known as the lateral or first and second ventricles, while the remaining median cavity of the telencephalon and diencephalon is known as the third ventricle. The ventricles of the cerebral hemispheres are laterally compressed, and open out of the third ventricle by a pair of openings known as the foramina of Monro. The thickenings of these anterior extensions of the telencephalon and of the regions of the optic thalami and anterior commissure produce an apparent straightening of the original ventral flexure of the brain; this does not really disappear, however, and the infundibulum continues to extend below and in front of the tip of the notochord.
The hypophysis, while originally not a part of the brain, becomes intimately related with it. This forms very early as a strand of cells extending inward from the inner layer of the surface ectoderm (Figs. 37, 40), below the telencephalon and just above the future mouth region (oral plate) . These cells multiply and form a definite mass lying between the endoderm and the infundibulum, just at the tip of the chorda. This rudiment later cuts off from the ectoderm, and after fusing with the dorsal wall of the pharynx, comes into intimate relation with the lower surface of the infundibulum, forming the essential part of the pituitary body.
The mesencephalon undergoes only slight modification during the larval period. While its roof and floor remain thin, its ventro-lateral walls thicken as the crura cerebri, connecting with the prosencephalic wall: its dorso-lateral walls form the large rounded optic lobes. In front of these the anterior limit of the mid-brain is marked later by the posterior commissure. The cavity of the mesencephalon is called the aqueduct of Sylvius; it becomes narrow and connects the third ventricle with the cavity of the rhombencephalon.
The rhombencephalon is an elongated part of the brain lying wholly above the notochord. The usual division of this part of the brain into an anterior metencephalon and a posterior myelencephalon, is scarcely indicated in the frog. The wide cavity of the rhombencephalon is known as the fourth ventricle; it is continuous anteriorly with the aqueduct of Sylvius and posteriorly with the cavity of the spinal cord. The metencephalon is the region of the cerebellum; this is very small in the frog, and appears late in larval life, as a dorsal and dorso-lateral thickening. Ventrally the walls of the two regions are uniformly continuous.
Fig. 42. Median sagittal sections through the brain of the frog. From Von Kupffer (Hertwig's Handbuch, etc.). A. Of a larva of R. fusca of 7 mm. in which the mouth was open. B. R. esculenta at the end of metamorphosis. c, Cerebellum; ca, anterior commissure; erf, notochord; ch, habenular commissure; cp, posterior commissure; cpa, anterior pallial commissure; cq, posterior corpus quadrigeminum; ct, tubercular commissure; cw, optic chiasma; d, diencephalon; dt, tract of IV cranial nerve; e, epiphysis; hm, cerebral hemisphere; hy, hypophysis; J, infundibulum; M, mesencephalon; Ml, myelencephalon; Mt, metencephalon; p, antero-dorsal extension of diencephalon; pch, choroid plexus of third ventricle; R, rhombencephalon; rm, recessus mammillaris; ro, optic recess; se, roof of diencephalon; t, telencephalon; tp, tuberculum posterius; tr, torus transversus (telencephali) ; vc, valvula cerebelli; vi, ventriculus impar (telencephali) (third ventricle).
The broad roof of the myelencephalon is wholly non-nervous and forms the folded choroid plexus of the fourth ventricle (Fig. 42, B). The floor and ventro-lateral walls of the rhombencephalon become greatly thickened, forming chiefly the nervous pathways extending between the cord and brain and the nuclei of origin of most of the cranial nerves. Posteriorly the myelencephalon narrows gradually and passes insensibly into the spinal cord.
Fig. 43. Transverse sections through the spinal cord of R. fusca. From Von Kupffer (Hertwig's Handbuch, etc.). A. Through the anal region of a larva of 7 mm. B. Through the anterior body region of a larva during metamorphosis, a, Spinal artery; c, central canal; d, dorsal column (white substance); dw, dorsal root of spinal nerve; dz, atrophied dorsal cells; g, gray substance; vz, ventral cells; w, dorso-lateral column (white substance).
The spinal cord is at first flexed posteriorly toward the blastopore (Fig. 37), but when the tail begins to grow out this flexure disappears. The cavity of the cord is the central canal; it is lined with a layer of non-nervous cells known as ependymal cells, while the true nerve cells composing the greater part of its wall are termed the germinal cells (Fig. 43). Part of the germinal cells become the supporting or glia cells, while the remainder become the functional nerve cells or neuroblasts. The closure of the neural folds is complete and no dorsal fissure is left in the cord.
The thickening of the walls of the cord begins dorsally and dorso-laterally, so that the central canal is given a ventral location, its floor formed only by a layer of ependymal cells. Later the ventral wall thickens slightly and the ventro-lateral walls extend below its level forming a shallow groove, the ventral fissure. The central canal becomes compressed laterally, and is later completely surrounded by neuroblasts (gray matter), the outgrowths of which form a superficial layer known as the white matter of the cord (Fig. 43).
The Peripheral Nervous System
We should recall in a few words the morphological arrangement of the spinal and cranial nerves. The spinal nerves, of which there are but ten pairs in the adult, although in the tadpole upward of forty pairs, arise from the cord by a dorsal or afferent root, on which is located the spinal ganglion, and a ventral or efferent root. These roots join to form the trunk of the spinal nerve which is then divided into dorsal and ventral rami and a ramus communicans which passes to the sympathetic system (Fig. 46). Of the cranial nerves, connected with the brain, there are commonly described ten pairs, considerably varied in morphological, as well as in functional, characteristics. Those regarded as the most typical are primarily related with the gill clefts and are therefore known as the branchiomeric nerves; these are the V, VII, IX, and X. Each of these arises by a single, though in some cases compound, root of mixed character, i.e., afferent and efferent, passes into a large ganglion, beyond which it gives off a horizontal branch, and then divides into two branches which pass anteriorly and posteriorly to the gill cleft with which the nerve is associated. The III, IV, and VI cranial nerves are simple, purely efferent, supplying the muscles of the eye- ball. The development of the nerves commonly described as I and II will be considered in connection with the development of the olfactory and optic sense organs.
Embryologically the rudiments of the cranial nerves are composite structures, three elements entering into their formation. These are, (a) cell masses derived from the neural crests, (&) cells from ectodermal patches on the surface of the head, (c) cell processes extending out from neuroblasts in the ventrolateral walls of the spinal cord. In the spinal nerves the elements from the surface ectoderm are lacking.
A. THE CRANIAL NERVES
The rudiments of certain of the cranial nerves appear very early, and we may therefore describe them first although they are more complicated than the later appearing spinal nerves. While the central nervous system is still in the form of a flat plate we have already seen that its margin is considerably thickened, on account of the proliferation of the cells of the inner or nervous layer there. These thickened margins are visible on the surface of the embryo as the medullary ridges. Transverse sections of this stage (Fig. 44) show that these thickened masses of inner ectoderm become delaminated, both from the outer stratum of ectoderm and from the medial portion of the medullary plate which then goes to form the neural tube proper. These lateral cell masses are the beginnings of the neural crests. In the head region these masses become very large, and as the neural plate begins to close each becomes transversely divided into three masses. Posteriorly to the brain region the neural crests are much smaller, but are typically formed. As the neural tube closes these cell masses are left in situ along the sides of the brain and cord (Corning, Brachet).
The three divisions of the head portion of each crest soon become quite distinct. The anterior section, which begins in the mid-brain region, is to be recognized as the rudiment of the trigeminal ganglion (V nerve), the middle section as the rudiment of the acustico-facialis ganglion (VIII and VII nerves), and the posterior as the rudiment of the ganglion of the glossopharyngeal (IX) and vagus (X) nerves. The delamination of these rudiments from the medullary plate is not quite complete, and when the neural tube is fully formed, each may be seen to be' connected with the dorsal surface of the myelencephalon by a slender chain of cells (Fig. 45).
Fig. 44. Sections through young frog embryos (R. fused), illustrating the development of the crest ganglia and placodes. After Brachet. A. Transverse section through the neural plate of an embryo before elongation begins. B. Sagittal section, to one side of the mid-line, through an embryo of the same age as A. (This is also the stage of Fig. 32, G.) C. Sagittal section, to one side of the mid-line, through an embryo just beginning to elongate. D. Transverse section through, an embryo slightly older than that of A and B. E. Frontal section through an embryo with three or four pairs of mesodermal somites. F, G, H. Three transverse sections through an embryo just beginning to elongate (same age as C), showing the trigeminal, acustico-facial and glossopharyngealvagus crest ganglia, a/, Acustico-facialis ganglion; c, notochord; en, endoderm; g, gut cavity; gl, glossopharyngeal ganglion; gv, glossopharyngeal-vagus ganglion; I, liver diverticulum ; m, mesoderm; mp, primitive medullary plate; mpd, definitive medullary plate; nc, neural crest; s, mesodermal somites; tg, trigeminal ganglion; va, vagus (pneumogastric) ganglion.
Opposite each of these crest ganglia the cells of the inner or nervous layer of the ectoderm very early (stage with 3-4 somites) proliferate and form a patch, in places three or four cells deep (Fig. 45). These thickened patches are known as placodes: they are undoubtedly to be interpreted as vestigial sense organs. In each placode two separate elements are distinguishable, a superficial sensory element, which usually disappears (the exceptions will be noted below), and a deeper ganglionic portion which is usually retained to a varying extent. The ganglionic portion of the placode typically fuses with the cells of the associated crest ganglion, and together they form the rudiment of the chief sensory or afferent components of the cranial nerve. From this point onward we may describe separately the history of the chief cranial nerves. (Reference is unavoidably made to the visceral arches and clefts whose development must be described later, in connection with the history of the pharynx).
The Trigeminal Nerve (V). This is the chief nerve of the mouth and mandibular arch. The trigeminal portion of the neural crest is very large, extending from the eye to the hyomandibular cleft (Fig. 44, C, E, F). The crest ganglion grows downward and comes ventrally into contact with the mesoderm of the mandibular arch. These ectodermal and mesodermal cell groups then fuse, cells of the apposed surfaces intermingling, and finally a cell mass is formed in which the two elements are indistinguishable; this becomes the mesenchyme of the mandibular arch (Fig. 45, A, B).
The dorsal and superficial cells of the crest ganglion retain their nervous character and come into relation with the large placode of this region. The superficial or sensory portion of this placode disappears, but its deeper or ganglionic portion enlarges and divides into two parts. An anterior part separates from the surface ectoderm as the ophthalmic ganglion of the ophthalmic branch of the V nerve, whose fibers grow out anteriorly, through the dorsal head region, and also medially connecting with the medulla. The posterior part of the placode ganglion then fuses with the crest ganglion and together they form the trigeminal ganglion proper (Gasserian ganglion). From the neuroblasts of this ganglion, cell processes extend centripetally, entering the dorsal side of the medulla and forming the sensory root of the V nerve, while centrifugal processes rapidly grow out to the surface of the head (cutaneous branch of the V nerve), and also in front of and behind the mouth (mandibular and maxillary branches). These branches, as indeed those of most of the other branchiomeric nerves as well, are established before the time of the opening of the mouth. The cells which formed the original attachment of the crest ganglion with the medulla, appear to form the medullary sheath cells of the root of this nerve, while the sheaths of the peripheral branches are apparently derived from other migratory cells of the crest ganglion itself.
Fig. 45. Portions of sections through the head of the frog (R. fused), illustrating the formation of the placodes and the history of the crest ganglia. After Brachet. A. Transverse section through the trigeminal ganglion of an embryo of 3 mm. B. Transverse section through the acustico-facialis ganglion of an embryo with three or four pairs of mesodermal somites. C. Transverse section through the facial ganglion and auditory placode of an embryo of 2.8 mm. ei, inner or nervous layer of ectoderm; en, endoderm; eo, outer layer of ectoderm; m, mesoderm; mpd, definitive medullary plate; n, nerve cord; pa, auditory placode; pf, facial placode; ptg, trigeminal placode; r, spinal prolongation of ganglion; tg, trigeminal ganglion.
The Facial and Auditory Nerves (VII and VIII). It is convenient to describe these together, since both are derived from the acustico-facialis crest ganglion and its associated placode. The VII nerve is the nerve of the hyo-mandibular cleft, while the VIII nerve is not one of the branchiomeric series, but is purely sensory (auditory) .
The early history of these nerves is similar to that of- V; the major part of the crest ganglion contributes to the mesenchyme of the hyoid arch. The nervous part of the crest ganglion is somewhat more extensive than that of the V nerve, i.e., a greater part of the original ganglion remains of nervous function. The first important distinctive character here, consists in the fact that the sensory or superficial part of the placode does not disappear, but, continuing to enlarge, gradually sinks below the surface of the head, invaginates, and forms the rudiment of the ear, the auditory sac (Fig. 45, (7). The deeper placode ganglion cells in connection with this sensory epithelium remain in close contact with the sac forming the rudiment of the VIII nerve. From the neuroblasts of this rudiment processes grow into the medulla forming the root of the VIII nerve.
The remainder of the placode ganglion joins with the nervous portion of the crest ganglion, forming the ganglion of the VII nerve, from which centripetal processes grow out connecting the ganglion with the medulla, while centrifugal processes extend into the hyoid arch and neighboring regions (hyomandibular and palatine nerves).
The Glossopharyngeal and Vagus (Pneumogastric) Nerves (IX and X). These are the nerves of the remaining visceral clefts, the first to fourth branchial clefts (third to sixth visceral arches). The IX nerve is limited to the region of the first branchial cleft, while the X nerve is distributed around the remaining gill clefts, and is to be regarded as a compound nerve, equivalent to several branchiomeric nerves. The crest ganglion of these nerves forms the large posterior section of the crest in the head region (Fig. 44, E, H}. Essentially it resembles that of V; it rapidly grows very large, extends farther ventrally and posteriorly, and contributes to the formation of mesenchyme to a considerably less extent than the ganglion of the V nerve. The placode of the IX nerve develops typically; its superficial sensory portion disappears, while its ganglionic portion comes only slightly into relation with the crest ganglion. Posterior to this, the large placode of the X nerve appears simultaneously and has a similar early history, save that it fuses more extensively with the nervous portion of the crest ganglion. When the fibers grow out from the IX and X ganglia they pass together into the medulla as a single root. The IX ganglion is only incompletely separated from that of X by the passage of the anterior cardinal vein (see below). From the IX portion of the ganglion, which is thus almost wholly placodal in origin, fibers grow peripherally into the- usual relation with the first branchial cleft, while from the mixed ganglion of the X nerve, branches grow out with typical relations to all the remaining clefts.
From the vagus ganglion certain other important processes grow out posteriorly. From the placode a considerable tongue of cells grows posteriorly, forming the rudiment of the sense organs of the lateral line (see below), and accompanying this, fibers grow out from the ganglion as the rudiment of the lateral line nerves (Fig. 53), this branch is present throughout the tadpole stage but disappears at metamorphosis. The vagus ganglion also sends out processes which grow posteriorly, to the thoracic and abdominal viscera; these form the visceral branch of the X nerve.
The branchiomeric cranial nerves include, beside the afferent or sensory components, whose development has just been outlined, efferent or motor fibers in varying numbers. These do not arise by a morphologically separate root, but neuroblasts in the wall of the medulla send out processes (axons), which leave the cord in association with the afferent roots described above. They are distributed with the branches which pass posterior to the gill clefts.
The development of the III, IV, and VI cranial nerves is incompletely known. They form, comparatively late, as outgrowths of neuroblasts located in the ventral parts of the medulla. These processes extend through the mesenchyme of the head into the orbit and innervate the muscles attached to the eye-ball. The III nerve is the first to appear (Held) at a time when 8-9 somites are present (5-6 mm.).
B. THE SPINAL NERVES
The spinal nerves differ from the cranial nerves in two important respects: (a) they are related primarily with the mesodermal somites instead of the visceral clefts, and (6) there are no placodal elements connected with them.
The neural crests continue from the head region as much smaller strands of cells; these become broken into segments which are the rudiments of the spinal ganglia. From the neuroblasts of each ganglion, cell processes grow out, some centripetally into the cord, forming the dorsal root of the spinal nerve, others centrif ugally, forming the peripheral afferent fibers which are distributed chiefly to the skin and other sensory surfaces (Fig. 46) . The ventral root of the spinal nerve is formed by outgrowths (axons) from neuroblasts in the ventral side of the cord.
They first appear in the anterior part of the body in the larva of about 4 mm. As they grow outward they meet the dorsal root, just beyond the ganglion, and pass thence in part to the mesodermal myotomes, and in part are distributed with the sympathetic system. The two most anterior myotomes are without spinal nerves; these are occipital in position and later disappear.
C. THE SYMPATHETIC SYSTEM
The development of the sympathetic system is very imperfectly known in the frog. The first definite indication of it appears in the embryo of about 6 mm., as slight collections of cells on the spinal nerves about the level of the dorsal aorta. From what is known here and to be inferred from the conditions in other lower vertebrates, it may be said that these cell groups are composed of elements from the spinal ganglia and certain of the posterior cranial ganglia. These ,
Fig. 46. Transverse section
r through 8.6 mm. larva of R.
Cells, Coming from the ganglia, mi- esculenta, illustrating the rela grate ventro-medially and form a ^J^S^SfSt
pair of longitudinal Sympathetic COrds Dorsal aorta; c, spinal cord; d, dorsal (sensory, afferent) root
along the Sides of the dorsal aorta O f spinal nerve; m, myotome;
(Fig. 46). From the Cells Of these n ' notochord; r, ramus com mumcans; sc, sympathetic cord; COrds processes appear to grOW back sg, spinal ganglion; sn, spinal
to the spinal ganglia forming the %?* $%?*' rami communicantes, and also* peripherally to the visceral organs and surfaces. Along the paths thus marked out fibers grow out from other spinal ganglion cells, and quite likely other cells migrate from the cord forming additional sympathetic elements. From the sympathetic cords, cells also migrate peripherally, forming the peripheral sympathetic ganglia in connection with the great blood vessels and the thoracic and abdominal viscera. The ganglion of the III cranial nerve is also sympathetic in character, but its origin is uncertain in the frog, as is also the origin of the sympathetic fibers of the head region in general.
The Special Sense Organs
In the preceding chapter we described the earliest traces of the eyes. These consist of a pair of patches in the superficial ectoderm of the medullary plate, before this has begun to fold together. The cells of these patches are distinguished by their comparatively large size and by the presence of pigment in their outer ends (Fig. 47). When the medullary plate folds into a tube these patches are carried inward and are left toward the antero-ventral border of the fore-brain (telencephalon). Their pigment then gradually disappears, but it is clear that their originally free ends now border the cavity of the brain. Before the brain folds have entirely closed together, the regions surrounding and including these patches have already evaginated and formed the pair of optic stalks and vesicles extending quite to the surface of the head. The cavities of these structures are continuous with the brain cavity (third ventricle), so that the relation of the optic cells to the optic vesicle is the same as to the original cavity of the brain, and the free surfaces of these cells are now turned away from the surface of the head ; the true optic cells form the most distal part of the optic vesicle.
Fig. 47. Transverse section through the anterior part of the medullary plate of an embryo of R. palustris, in which the medullary ridges are just forming. From Froriep (Hertwig's Handbuch, etc.), after Eycleshymer. au, Optic grooves; en, endoderm; ep, ectoderm (epidermis); med, medullary plate; ms, mesoderm.
The sensory, or recipient, and the nervous elements of the eye (retina and optic nerve fibers), originally on the surface of the head, are the essential parts of the eye; they now form the optic vesicles, and are to be distinguished from the various accessory parts (the choroid and sclerotic coats, the aqueous and vitreous humors, and the cornea), which are derived chiefly from the mesoderm (mesenchyme) of the region, and from the ectoderm outside of the optic vesicle (lens and cornea, in part).
Fig. 48. Frontal section through the fore-brain and optic vesicle of an embryo of R. fusca, in which the tail is just growing out. From Von Kupffer (Hertwig's Handbuch, etc.). a, Optic vesicle; as, opening of optic stalk out of fore-brain; J, posterior wall of infundibulum; I, rudiment of lens (placode) ; P, wall of prosencephalon; r, rudiment of olfactory organ.
Upon reaching the surface of the head the optic vesicle is converted into the optic cup. The peripheral part of the vesicle becomes flat and then folds into the proximal part, forming a roughly hemispherical, two-layered cup, obliterating the original cavity of the optic vesicle and establishing a new cavity (Figs. 49, 50). The extent of the optic cup is increased immediately by the outgrowth of its free margin, which gradually draws partially together, leaving a small opening toward the surface of the head; this is the rudiment of the pupil. In the optic cup then we distinguish an inner and an outer layer, and a central cavity; these are respectively, the rudiments of the true retinal layer, the pigment layer, and the posterior chamber of the eye.
During the growth and invagination of the optic cup the optic stalk remains attached to its ventral side, so that the retinal
layer of the cup is continuous with the lower side of the optic stalk (Fig. 49). The infolding of the retinal layer is not a simple invagination, but, owing to this ventral attachment of the optic stalk, the infold is continued as a groove from the middle of the vesicle to the ventral border of the cup where it joins the stalk. This groove remains narrowly open for a time and is known as the choroid fissure, the pupil appearing as a dilatation of its upper end in the middle of the cup (Figs. 49, 128). That part of the cup opposite the pupil is referred to as the fundus region.
While the vesicle is invaginating the rudiment of the lens is formed as a thickening of the ectoderm opposite the pupillary region (Figs. 48, 50). This thickening involves only the deeper or nervous layer of the ectoderm and is, in all essential respects, similar to the ganglionic portion of the ectodermal placodes described in connection with the cranial nerves. This lens placode is immediately anterior to the placode of the V cranial nerve. By the time of hatching this forms a prominent rounded thickening, which is cut off from the ectoderm as a solid spheroidal cell mass (Fig. 50). After hollowing out internally it again becomes solid through the elongation of the cells of its inner side : the outer side remains as a thin epithelial layer over the distal surface of the solid lens. When the pupil begins to narrow the lens moves into the opening and finally remains included just within it, in the cavity of the optic cup. (In other vertebrates, except the Teleosts, the lens forms as a hollow vesicle resulting from an invagination of the surface ectoderm.)
stalk of the frog. /, Choroid fissure; I, lens; pc, posterior chamber of eye; pi, outer or pigmented layer of optic cup; rl, inner or retinal layer of optic cup; s, optic stalk; v, original cavity of optic vesicle.
Fig. 50. The development of the eye in the Urodele, Siredon pisciformis. After Rabl. A. Of embryo with about twenty-five pairs of somites, showing the thickening of the lens rudiment. B. Invagination of the lens and formation of the optic cup. C. Lens separating from the superficial ectoderm in an embryo of about thirty-five pairs of somites. D. Thickening of the inner wall of the lens. E. Shortly before hatching; differentiation of the rods and cones in the retinal layer, a, Anterior chamber of eye; c, cavity of primary optic vesicle; co, cornea; e, ectoderm of head; /, choroid fissure; i, inner or retinal layer of optic cup; tr, rudiment of iris; k, optic stalk; I, lens; o, outer or pigmented layer of optic cup; p, posterior chamber of eye.
After hatching the cells of the optic cup layers begin to differentiate into the histological elements characteristic of the adult eye. The outer layer becomes very thin and pigmented, while in the thick inner layer the characteristic cell layers of the retina appear (Fig. 50, D, E). The cells in contact with the pigment layer gradually differentiate as the rods and cones; this process begins in the fundus region and spreads thence to the more peripheral regions of the retina. Other cells of the retina are neuroblasts and send out nerve processes; those from the cells bordering the cavity of the optic cup (posterior chamber) grow down, by way of the margins of the choroid fissure, to the optic stalk. Entering the ventral and posterior sides of this, they pass thence to the ventral wall of the forebrain, forming there the optic chiasma and optic thalami. The cavity of the optic stalk is finally obliterated by the collection of these fibers; in the brain the optic recess marks the region of its original opening (Figs. 41, 42, 43). The component cells of the stalk become largely non-nervous, forming the supporting neuroglia cells. The optic stalks are commonly known as the II pah- of cranial nerves, but it is evident from their development that they are tracts of the brain, without any similarities to the true cranial nerves.
The eye develops very slowly during the larval period after hatching, but at the time of metamorphosis it is rapidly perfected. The details in the later development are not very well known. The rudiment of the vitreous body, occupying the posterior chamber of the eye, is of mixed origin, although purely ectodermal. It arises from outgrowths of cells from the inner surface of the lens placode and also from the retinal layer of the cup. These elements intermingle and form the stroma of the vitreous humor or body. In its essential composition it thus resembles a typical cranial nerve ganglion which is derived from placode cells and neural crest; of course, in this region, the neural crest is not typically present, but the retinal cells have somewhat similar relations to the neural tube proper. A day or two before hatching the choroid fissure of the optic cup begins to close, first in the fundus region. Blood vessels have already entered the posterior chamber and the margins of the fissure embrace these. The region last to fuse, at the margin of the cup, becomes enlarged as the ventral choroid knot, and from this the iris develops, gradually extending dorsally around the outer side of the pupil. The cornea and outer coats of the eye-ball, as well as muscles are formed from the mesenchyme around the optic cup.
Like the eye this organ is a complex, derived from diverse sources; the essential parts, composing the membranous labyrinth, are derived from the ectoderm of the surface of the head, while the accessory parts, tubo-tympanic cavity and columella, are of endodermal and mesodermal origin. We shall describe first the formation of the membranous labyrinth or internal ear.
We have already mentioned the first formation of the auditory organ as the auditory placode, which appears just as the neural folds close together (Fig. 45, C). As the embryo begins to elongate each of these placodes becomes depressed below the surface of the head and invaginates, forming the ovoid auditory sac or otocyst, about 0.2 mm. in diameter (Fig. 51, A). For a time this remains connected with the surface of the head by a narrow tube of cells, but just before hatching it becomes completely closed and separates entirely from the surface ectoderm, sinking in toward the lateral surface of the myelencephalon (Fig. 51, B). The superficial layer of the ectoderm does not share in the formation of the auditory sac but remains continued across the surface of the head outside the invaginating auditory epithelium. The wall of the auditory sac is only one cell in thickness, except in its medio-ventral region where the ganglionic portion of the placode is located. A small fingerlike outgrowth of the sac extends a short distance dorsally, from its medio-dorsal region: this is the rudiment of the endolymphatic duct. From this condition the auditory sac changes very little until after the opening of the mouth (10-12 mm.) when it continues its development.
Fig. 51. The development of the auditory organ in the frog and toad. A, B, F, after Krause; C, D, E, after Villy. A. Section through the auditory vesicle of an embryo just beginning to elongate. B. Section through the auditory vesicle that has very nearly separated from the' superficial ectoderm. C. Transverse section, somewhat oblique, through the auditory organs of a 12 mm. R. temporaria. D. Slightly more advanced stage than C. E. Section through the auditory organs of a 25 mm. R. temporaria. F. Membranous labyrinth of the toad (Bufo vulgaris). a, Auditory sac; aa, anterior ampulla; ac, anterior vertical semicircular canal; 6, pars basilaris; d, dorsal outgrowth of primitive auditory vesicle (rudiment of endolymphatic duct); e, endolymphatic duct; g, ganglion of auditory (VIII) nerve; he, horizontal semicircular canal; I, lagena or cochlea; pa, posterior ampulla; pc, posterior vertical semicircular canal: s, saccule; ss, sinus superior; u, utricle; VIII, auditory nerve.
The next differentiations of the auditory sac result from the formation of various ridges and septa extending into its cavity (Fig. 51, C, D, E). The first of these appears obliquely along the outer and posterior walls of the sac, and finally divides the otocyst into two regions, an inner and upper part, known as the utricle, and a lower and outer part, the saccule; these two divisions remain connected by a small perforation in the septum. The endolymphatic duct is connected with a dorsal extension of the saccule, while from the utricle the three semicircular canals grow out. These canals are formed first by the growth of couples of ridges into the cavity of the utricle, approximately in the relative positions of the future canals; the couples meet and fuse save at their ends, so that the cavities enclosed by them open directly into the utricle. Each rudiment then begins to enlarge and pushes above the surface of the utricle, first as a ridge, which becomes plate-like and then tunneled between the canal and the wall of the utricle. The posterior canal is formed somewhat later than the anterior and the horizontal canals. The ampullae are added to the canals by additional constrictions of the wall of the utricle.
Shortly after the appearance of the semicircular canals, the saccuie commences to differentiate. First there appears a postero-ventral outpocketing, the rudiment of the lagena or cochlea, which forms a simple sac of considerable size. Then posteriorly to this appears a second ventral extension, the basilar chamber (pars basilaris).
Upon the division of the auditory sac into utricle and saccule, the endolymphatic duct remained in connection with the latter. The duct slowly elongates dorsally, along the surface of the hind-brain, on the dorsal side of which its tip forms an expansion known as the endolymphatic sac. These sacs enlarge very considerably, fuse together, and finally, after metamorphosis, form a vascular structure, covering a large portion of the roof and sides of the myelencephalon : they remain throughout life, connecting with the saccule by the narrow endolymphatic ducts which pass through openings in the walls of the auditory capsules (Fig. 51, F).
The epithelial lining of the membranous labyrinth becomes truly sensory only in certain patches with which fibers of the VIII cranial nerve are related. These patches are located in the cochlea (3), utricle (1), saccule (1), and the ampulla (3). The peril ymph and the cartilaginous and bony labyrinths are laid down around the membranous labyrinth by the surrounding mesenchyme.
The parts of the middle ear develop relatively late and are not well differentiated until after metamorphosis. As in other vertebrates the tubo-tympanic cavity is a derivative of the pharynx, more precisely of the region of the first gill pouch (the spiracular pouch, between the hyoid and mandibular arches; see below). In the frog this gill pouch is vestigial: it is never perforated, indeed does not contain a cavity, and is represented only by a fold of the endodermal wall of the pharynx which does not quite reach to the surface ectoderm. From the dorsal end of this vestige a rod of cells grows out and terminates as a solid knob, beneath the eye (Fig. 57). During metamorphosis spaces appear in this rod and in the terminal knob, and it moves back into the region of the ear, losing its connection with the pharynx. After metamorphosis it acquires a secondary connection with the pharynx, and its distal portion enlarges very considerably, occupying the space between the ear and the integument of the side of the head: the integument here later becomes the tympanic membrane, the expanded cavity is the tympanic cavity, and the narrow connection with the pharynx is the Eustachian tube.
In the adult the auditory capsule and the tympanic membrane are connected by a rod, the columella, extending across the tympanic cavity. This is the last part of the auditory apparatus to be formed. Its inner end is formed as a cartilage (the operculum) appearing in the tissue plugging the large foramen ovate in the outer side of the cartilaginous auditory capsule. From this region another cartilage, the plectrum, differentiates, toward the close of metamorphosis, along the dorsal wall of the tympanic cavity, finally extending to the tympanic membrane where it connects with a ring-like cartilage developed from the palato-quadrate cartilage (see below) . The elements of the columella are thus not genetically related with the visceral skeleton (palato-quadrate cartilage). While the opercular part of the columella is becoming chondrified, the tympanic cavity extends dorsally and finally surrounds it completely, leaving it in its definitive position crossing the tympanic cavity.
The Olfactory Organ
The olfactory organs appear very early, before the brain closes, as a pair of ectodermal thickenings either side of the head, above and anterior to the future mouth region. Only the deeper nervous layer of the ectoderm is involved in the thickening, and the superficial layer disappears here, leaving only its pigment scattered among the remaining cells. These thickenings are immediately anterior to the lens placodes and may be termed the olfactory placodes (Fig. 52, A): these appear to have no relation to the median anterior ectodermal thickening which is present at this time. These placodes soon fold inward forming simple olfactory pits, the rudiments of the true olfactory cavities, their walls becoming the olfactory epithelium (Fig. 52, B). A few cells detach from the inner surface of the olfactory placode and mingle with cells derived from the surface of the telencephalon : these appear to be equivalent to the crest ganglion, and from them are formed, apparently, the sheath cells of the true olfactory nerve fibers, which are outgrowths of the sensory cells of the olfactory placode.
Fig. 52. The development of the olfactory organ in R. fusca. After Hinsberg. A, B, C. Sections through the olfactory groove and organ of 5 mm., 6 mm., and 11 mm. larvae, respectively. D. Lateral view of a model of the olfactory organ of a 31 mm. larva. The dotted line marks the limit between the sensory and non-sensory portions of the epithelial lining of the olfactory cavities, c, Notochord; ch, internal nares (choanas); d, dorsal lumen; dc, dorsal sac; en, external nares; g, olfactory groove; i, cut edge of integument; in, internal nares (choanae) ; Z, elongation toward the mouth; la, lateral appendix; m, mouth cavity; n, inner or nervous layer of ectoderm; ns, part of chamber lined with non-sensory epithelium; p, olfactory placode; r, ridge marking the limit between middle and ventral chambers; s, superficial layer of ectoderm; se, part of chamber lined with sensory epithelium; st, stomodaeum; t, telencephalon; v, thickened bands of superficial ectoderm cells (possibly the vestige of a primitive sense organ) ; vc, ventral sac; vg, ventral nasal gland attached to Jacobson's organ; x, elevation around external nares; y, canal leading to olfactory cavity; z, fold around internal narial opening.
About the time of hatching (6 mm.) a thick strand of cells extends from each olfactory pit to the roof of the pharynx just within the limit of the stomodseum (Fig. 52, B). Later (9-12 mm.) each strand acquires a lumen which opens into the olfactory sac, and also into the pharynx as the internal nares or choance (Fig. 52, (7).
The extent of the olfactory cavity is increased by a cavity formed in a dorsal cell proliferation of the olfactory epithelium. This region soon forms a separate dorso-lateral lobe which disappears entirely during metamorphosis.
The surface of the head pushes out above the olfactory sac so that the duct leading to it is considerably elongated, and meanwhile, on account of the enlargement of the fore-brain and the formation of the cartilage of the skull in this region, the openings of the olfactory tubes or external nares are carried to the dorsal side of the head, so that the entire olfactory organ extends along a straight perpendicular axis (Fig. 52, D).
During metamorphosis the olfactory organ becomes considerably complicated by the appearance of various foldings and out-pocketings of its walls, and by a sharp flexure of its axis. We may mention only the more important of these outgrowths. The first is an extension from the ventral side of the olfactory chamber; here a solid mass of cells proliferates, acquires a cavity, and, enlarging rapidly, turns transversely toward the medial side. This is the rudiment of Jacobson's organ; a large glandular mass develops upon its medial end. Other outgrowths are formed from parts of the olfactory sac that are non-nervous, i.e., lined with indifferent cells. One of these appears opposite Jacobson's organ and soon becomes a large sac whose cavity is added to the olfactory chamber. Another appears anteriorly at the base of the olfactory duct; this receives the ducts of the lachrymal glands. Later a dorsal sac grows out from the medial and posterior walls of the tube. During late metamorphosis the axis of the olfactory organ is sharply bent on account of the posterior shifting of the internal nares. In addition to the glands of Jacobson's organ, other glands appear as outgrowths of the olfactory chamber and in the posterior wall of the internal nares.
The Sense Organs of the Lateral Line
As mentioned above, the sense organs of the lateral line are derived from the placode of the X cranial nerve, and are innervated by the ramus lateralis of this nerve. When the embryo has elongated to about 4 mm. a small dorso-lateral section of the vagus ganglion separates from the remainder (Fig. 53, A, B) remaining closely in relation with the ectodermal placode (Harrison). The placode now begins to elongate posteriorly; the deeper cells multiply rapidly and form a long narrow tongue which pushes along through the epidermis just outside the basement membrane (Fig. 53, (7). Finally, just before hatching, it reaches to the tip of the tail. Differentiation of this cord progresses posteriorly commencing in the older anterior part. The cells become grouped at intervals, each group representing the rudiment of a sense organ of the lateral line. In each rudiment a few central cells become sensory and are surrounded by a layer of enveloping cells (Fig. 53, D). These groups push up through the epidermal layer to the surface of the body, and the sensory cells develop hair-processes.
As the placodal rudiment grows posteriorly it is accompanied by outgrowths (axons) from neuroblasts of the dorso-lateral portion of the vagus crest ganglion. These processes lie within the basement membrane of the epidermis, but when the definite sense organs develop the nerve fibers pass up among the sensory cells. The cells forming the medullary sheaths of these fibers appear to wander along the fibers from the vagus ganglion.
Similar series of integumentary sense organs are formed in definite rows on the head, and dorsally from the lateral line; these are innervated by branches of the VII, IX, and X nerves. The VIII nerve and the auditory organ also belong in this group of sense organs. At metamorphosis they all disappear save the auditory organ and nerve.
Fig. 53. The development of the lateral line organs in R. syhatica. After Harrison. A. Part of a frontal section through the level of the notochord of a 3.3 mm. embryo. B. Part of a transverse section through the vagus region of a 4mm. embryo. C. Part of a frontal section through a 4 mm. embryo of R. virescens. D. Section through the lateral line organ of a 15.5 mm. larva of R. syhatica. a, Auditory vesicle (in A, its rudiment); 6, basement membrane of epidermis; ch, notochord; g, gut; gV, trigeminal ganglion, of V cranial nerve; gVIII, acoustic ganglion of VIII cranial nerve; gX, vagus ganglion; gXl, ganglion of the lateral nerve (branch of the vagus) ; i, intersegmental thickenings of the epidermis (ectoderm) ; I, rudiment of lateral line nerve; Ip, lateral plate of mesoderm; my, myotomes; n, inner or nervous layer of epidermis (ectoderm); nc, nerve cord; p, pigment in epidermis; s, superficial layer of epidermis (ectoderm) ; si, inner sheath cells of lateral line organ; sn, sensory cells of lateral line organ; so, outer sheath cells of lateral line organ.
The Alimentary Tract And Its Appendages
In the preceding chapter we described the formation of the enteron or gut cavity and its development up to the time the embryo is just beginning to elongate (Fig. 37). We have described, therefore, the formation of the fore-, mid-, and hindgut and have seen that up to this time the chief differentiations are connected with the fore-gut. After the mesoderm and the notochord have been split off from the endoderm, the wall of the enteron is but one cell layer in thickness, excepting the floor of the mid-gut which is occupied by the large yolkmass. The hind- and mid-gut cavities are narrow, while the fore-gut expands widely in front of the yolk-mass, and in connection with it we have described the first indications of the mouth region, of two or three visceral pouches, and of the liver.
We may proceed now to outline the further development of each section of the alimentary tract. Before taking up the history of the fore-gut we must notice the development of certain structures associated with the mouth.
The stomodceum has already been mentioned as a shallow median depression of the head, just below the olfactory and fore-brain region. At hatching this is still rather shallow, but its floor has come into contact with the wall of the enteron, establishing a fusion known as the oral plate (Figs. 57, 58, A), for this is the region where the mouth forms a few days after hatching (9-10 mm.). In the older larvaB the inner boundary of the stomodffial region is marked by the internal nares or choanse, which lie just within the boundary between ec todermal and endodermal territory. The formation of the oral sucker, just below the stomodaeal invagination (Fig. 57), was described in the previous chapter.
The margins of the stomodaeum are at first formed chiefly by the mandibular ridges, but soon the integument above these becomes drawn out in the form of lips. The mouth itself remains small in the tadpole, but the lips, of which there are an upper and a lower, soon project considerably in front of the mouth, enlarging the stomodseal cavity; the lower lip is the larger and is freely movable (Fig. 58, B). The lips form the important feeding organs of the tadpole, and as such they become furnished with various horny structures, described as teeth and jaws (Fig. 58, B), but not at all to be compared with the true teeth and jaws which develop later. These horny structures are purely larval organs and are entirely lost at the time of metamorphosis. The " teeth" develop from strands or piles of cells of the deeper layer of the epidermis. Each cell, as it nears the surface, undergoing cornification, becomes conical in form, and pushes through the skin, soon to be replaced by the next cell (" tooth") underlying it. The upper lip bears three medially interrupted rows of these " teeth," the lower lip four complete rows. Toward the base of each lip, near the mouth, a closely set row of teeth, together with intermediate horny cells, form a continuous ridge; these ridges, of which that of the lower lip is the larger, form the "jaws" or beak of the tadpole. During metamorphosis the horny teeth and jaws are lost, the lips are retracted, and as the mouth rapidly enlarges the true teeth and definitive jaws are formed.
The Derivatives of the Fore-gut
The organs derived from the fore-gut region that we shall describe, are the pharynx, oesophagus, stomach, liver and pancreas; in connection with the pharynx we shall describe the development of the visceral pouches and arches, the internal and external gills, the thymus, the ultimo branchial bodies, epithelioid bodies, the thyroid body, tongue, and the lungs.
In front of the yolk-mass the fore-gut is widely expanded transversely as the pharyngeal cavity (Fig. 37) ; antero-ventrally its wall is fused with the ectoderm as the oral plate, while postero-ventrally the liver region is indicated as a small cavity extending backward beneath the yolk. Dorsal to the yolk the fore-gut is narrowed as the rudiment of the oesophagus. Along the sides of the pharynx a series of vertically elongated ridges, or solid outfoldings, appear and extend to the surface ectoderm with which they fuse (Figs. 54, 57). These are the visceral pouches. They appear very early and the formation of the first two or three pairs was mentioned in the preceding chapter. Altogether six pairs are formed, decreasing in size and importance posteriorly. As these pouches extend out to the ectoderm they divide the mesodermal tissue lying between ectoderm and endoderm, into a series of vertical rods known as the visceral arches. The most anterior visceral pouch is the hyomandibular; in front of it, between this and the mouth, lies the mesodermal mandibular arch. The remaining pouches are the first to fifth branchial pouches. Between the hyomandibular and first branchial pouches is the hyoid arch, while between successive branchial pouches are the branchial arches. Like the pouches these diminish in size posteriorly until the last is quite small and incompletely marked. Some additional facts will be mentioned later in connection with the ultimobranchial
Fig. 54. Diagram of a frontal regarding the last branchial pouch section of a frog larva at the time of hatching. After Marshall (modi-
lum; in, intestine; n, nephrostome; bodies. o, base of optic stalk; ol, olfactory .pit (placode); p, pharynx; t, pro- About the time the mouth IS
nephric tubules; II, hyoid arch; nr , pr , Ar l Qr Qnmj arm^ar within *>ar>Vi
ni-vi, first to fourth branchial opened^ spaces appear within each
arches; 1, hyomandibular pouch; branchial pOUch; these Cavities 2-6, first to fifth branchial pouches.
become continuous with the pharyngeal cavity, and soon perforate the area of ectodermal and endodermal fusion, forming the branchial clefts or gill clefts. The second and third clefts are perforated earliest, and soon after, the first and fourth. The hyomandibular pouch is never perforated; shortly before the opening of the second and third clefts it loses its connection with the ectoderm and gradually disappears. The formation, from the dorsal wall of the hyomandibular pouch, of the rudiment of the tubotympanic cavity of the ear, has already been described (Fig. 57).
The chief structures associated internally with the visceral arches are the aortic arches and the visceral skeleton, the development of which will be described in later sections. From the external surface of certain visceral arches are developed the gills, both external and internal. Reference has previously been made to the external gills: these appear just before hatching, as small outgrowths from the outer surfaces of the dorsal ends of the first and second branchial (second and third visceral) arches (Fig. 22, G.) Later a small external gill appears on the third branchial arch. The two anterior pairs grow very rapidly and about the time the mouth opens -they form large branched or lobed processes, extending out from the sides of the pharynx (Figs. 64, 65). They become extremely vascular and are the earliest respiratory organs of the tadpole. The posterior pair remains small and comparatively simple.
After a few days the external gills become covered by the operculum, and then they are gradually absorbed and finally disappear completely. The operculum makes its first appearance before the perforation of the mouth, as a pair of outgrowths from the posterior borders of the hyomandibular arches. These folds grow backward rapidly, and just as the external gills reach their maximum development, the operculum extends to and outside of them, enclosing them in an opercular cavity. This cavity finally becomes entirely enclosed on the right side by the fusion of the posterior border of the right opercular fold with the surface of the body; this fusion extends across the ventral side also, and thus puts the right cavity in connection with the left (Fig. 58, B). The left fold remains partly free and the margins of the opening are drawn out forming a short opercular tube or "spiracle."
The internal gills appear just after the gill clefts are perforated, about the time the mouth opens, as a series of small elevations on the postero-external faces of the branchial arches (Figs. 64, 65). Like the external gills, these are covered with a thin layer of ectoderm cells which move in, covering their original endodermal coat. These rudiments soon become doubled on the first three branchial arches, but remain in a single row on the fourth branchial arch. They enlarge rapidly and form long branched processes or gill filaments, along the whole border of the arch below the external gills. The filaments become very vascular and project freely into the opercular cavity, where they are bathed in the respiratory current entering the mouth and passing out through the gill clefts and opercular tube.
The inner borders of the branchial arches become serrated by the formation of a series of papilla, forming a kind of filtering organ (Fig. 64, D, E). The continued widening of the dorsal part of the pharynx throws the branchial portion into a ventral position, and then this whole region becomes partly separated from the dorsal region by the anterior and posterior folds of the pharyngeal floor; these are the velar plates (Fig. 64, D, E).
As the period of metamorphosis approaches, the opercular cavity and the gill clefts become occluded by the rapid proliferation of the cells lining these spaces, and of the gills themselves. The most of this solid mass of cells becomes completely resorbed. Various structures of the young frog are derived from vestiges of the gill clefts.
The thymus body appears just before hatching, as a solid internal proliferation from the epithelium of the upper side of the first branchial pouch (second visceral, or hyobranchial pouch) (Fig. 56). A similar smaller proliferation from the hyomandibular pouch has only a transitory existence. The thymus rudiment enlarges slowly, separating from the wall of the pouch at about 12 mm. After metamorphosis the thymus bodies are seen toward the outer surface of the head, just back of the auditory capsule and jaw articulation.
From the dorsal ends of the other branchial clefts somewhat similar bodies are formed; these become lymphoid and appear to have no correspondence with the thymus rudiments. From the ventral ends of the anterior gill pouches additional epithelial proliferations are formed about the time the internal gills appear. Those derived from the first branchial pouch form the carotid glands, while the others form the so-called epithelioid bodies. These remain present throughout life, lying just below the aortic arches (Fig. 56).
Fig. 55. Diagram of the branchial pouch derivatives in the frog. After Maurer, with Greil's modification, eg, Carotid gland; e\, 62, ea, epithelioid bodies; ih, thyroid body; tmi, tmz, thymus bodies; ub, ultimobranchial body; I-VI, first to sixth visceral pouches. (/, hyomandibular; II-VI, first to fifth branchial pouches.)
Fig. 56. Diagrams of the derivatives of the visceral pouches and arches in the frog. After Maurer, with Greil's modification. A. Lateral view, frog larva. B. Lateral view, after metamorphosis. C. Transverse section through gill of frog larva. D. Transverse section through gill region, just after metamorphosis; the gills have not quite disappeared, a, Afferent branchial arteries; c, carotid gland; d, dorsal gill remainder; e, epithelioid bodies; g, internal gills; m, middle gill remainder; o, operculum; s, supr^apericardial or postbranchial body; t, thyroid body; th, thymus bodies; v, ventral gill remainder; I-VI, visceral arches; /, mandibular arch; II, hyoid arch; 1 1 I-VI, first to fourth branchial arches; 1-6, visceral pouches; 1, hyomandibular pouch; 2, hyobranchial pouch; 3-6, first to fourth branchial pouches.
A body described as the pseudothyroid body appears in the postero- ventral branchial region; this seems to have no relation with the remains of the disappearing gill clefts. In addition to the dorsal remains of the gill clefts, mentioned above, middle and ventral traces may be seen for some time after metamorphosis.
Fig. 57. Semi-diagrammatic optical section of the head of a 7.5 mm. larva of R. temporaria, illustrating the relations of the visceral pouches and chondrocranium. After Spemann. The wall of the pharynx toward the observer has been removed, so that the visceral arches are shown in section, a, Auditory organ; ac, anterior ascending process of the palato-quadrate cartilage; e, eye; E, rudiment of Eustachian tube; ep, epiphysis; h, hypophysis; hy, hyoid cartilage; ra, oral membrane; md, mandibular cartilage; n, notochord; o, olfactory organ; os, oral sucker (in section); p, pharyngeal cavity; pq, palato-quadrate cartilage; s, stomodseum; t, trabecular cartilage; tc, trabecular cornu; th, rudiment of thyroid body; ty, rudiment of thymus; 1-4, first to fourth visceral pouches.
A pair of ultimobranchial bodies, known also as post-branchial or suprapericardial bodies, are found in the frog, lying posterior to the fifth visceral pouch. These are formed as solid proliferations from the pharyngeal wall just back of the fifth visceral pouch (fourth branchial pouch). They clearly represent the vestiges of a sixth pair of visceral pouches, although they never extend out as far as the surface ectoderm. They soon separate from the pharyngeal wall and acquire internal cavities, remaining in the floor of the pharynx, in a suprapericardial position (Figs. 54, 55, 56).
The remaining structures of the pharyngeal region have no genetic relationship with branchial structures. The thyroid body appears just before hatching, as a median evagination, narrow and elongated, from the floor of the pharynx (Fig. 57). This slowly pinches off from the pharyngeal epithelium, forming a solid rod of cells, and a few days after the opening of the mouth it divides into a pair of bodies, which then enlarge rapidly and become very vascular.
The lungs appear just before hatching as a pair of solid proliferations from the ventral wall of the posterior part of the fore-gut, between the yolk-mass and the heart. These rudiments slowly extend posteriorly along the sides of the fore-gut, and early acquire cavities proximally. Some time after the opening of the mouth, the wall of the fore-gut between and around the openings of these diverticula, becomes depressed as a transverse groove, the laryngeal chamber (Fig. 58, B), which is then partly constricted off from the alimentary tract; the opening that remains is the glottis. The lungs now rapidly elongate, pushing out into the body cavity and becoming very vascular (Fig. 72); the mesodermal constituents surrounding the endodermal lining of the lungs, are derived from the splanchnic mesoderm.
The tongue appears very late, just before metamorphosis. It is first indicated as an elevation in the floor of the anterior part of the pharynx, just back of the region from which the thyroid body was derived. In front of this elevation, between it and the lower jaw, the floor of the pharynx is depressed and glandular. During metamorphosis the rapid anterior extension of the tongue carries this glandular area upward so that it lies on the free anterior tip of the tongue.
The liver appears very early, even before the embryo begins to elongate, as a postero-ventral extension of the cavity of the fore-gut, beneath the yolk-mass (Fig. 37). This rudiment enlarges very slowly at first, the solidity of the yolk preventing its penetration. The liver lies just posterior to the heart and separated from it only by a mass of scattered mesoderm cells, which come to be added to the anterior wall of the liver diverticulum, forming its mesodermal components. Some of the yolk cells adjoining the liver appear to be added to it, forming true hepatic cells. After hatching, the wall of the anterior part of the diverticulum becomes folded, and later forms the chief part of the definitive liver (Fig. 58, A). The posteroventral extension of the diverticulum is the rudiment of the gall-bladder, which becomes somewhat separated from the anterior hepatic portion; the original opening of the diverticulum out of the fore-gut remains as the bile-duct (Figs. 58, 59).
Fig. 58. Diagrams of median sagittal sections of the anterior ends of frog larvae. After Marshall. A. Of a larva just before the opening of the mouth. B. Of a 12 mm. larva (at the appearance of the hind-limb buds), a, Auricle; ao, dorsal aorta; 6, gall bladder; bh, basihyal cartilage; ch, cavity of cerebral hemisphere (lateral ventricle); e, epithelial plug closing the oesophagus; ep, epiphysis; g, glottis; h, hypophysis; H, hind-brain; hr, cerebral hemisphere; ht, horny "teeth"; hv, hepatic vein; i, intestine; if, infundibulum; /, lower jaw; Z, liver; ly, laryngeal chamber; ra, mouth; M, mid-brain; mb, oral membrane (oral septum); n, notochord; o, median portion of opercular cavity; oe, oesophagus; p, pharynx; pb, pineal body; pc, pericardial cavity; pd, pronephric (mesonephric) duct; pt, pituitary body; pv, pulmonary vein; pill, choroid plexus of third ventricle; pIV, choroid plexus of fourth ventricle; r, rostral cartilage; ro, optic recess; s, stomodseum; sv, sinus venosus; ,' thyroid body; ta, truncus arteriosus; tp, tuberculum posterius; v, ventricle; w, inferior (posterior) vena cava.
In later stages the liver
Fig. 59. Models of the digestive tract of frog embryos. After Hammar (Maurer.) A. Lateral view of the tract of a 7 mm. larva. The anterior portion has been opened by a median sagittal section. B. Dorsal view of the tract of an 8.5 mm. larva, d, Ductus choledochus; g, gall bladder; h, liver; Z, enlarges Very Considerably lung; m, mid-gut; p, pancreas; pd, dorsal and Shifts its position pOS- rudiment of Pancreas; r, rectum.
teriorly; the gall-bladder also becomes very large in the tadpole.
The pancreas develops in the region where the liver diverticulum originally opens out of the fore-gut (Fig. 59). It arises from three rudiments. A dorsal rudiment appears as a solid outgrowth of the dorsal wall of the fore-gut, from which it soon separates entirely. Right and left ventral rudiments grow out from the fore-gut, just in the posterior margin of the opening of the bile-duct. These ventral rudiments, retaining a common connection with the gut, then enlarge and, passing around the sides of the bile-duct, fuse together in front of it.
Later the dorsal rudiment unites with the fused ventral parts, and the entire pancreas is then connected by the pancreatic duct with the ventral wall of the gut. The opening of the pancreatic duct marks the boundary between the fore- and mid-gut regions during these early stages; later the opening of the duct shifts just within the margin of the bile-duct.
The chief steps in the differentiation of the oesophagus, stomach, and intestines occur just after hatching. The region between the lung rudiments and the openings of the hepatic and pancreatic ducts, elongates as the region from which the oesophagus and stomach are formed (Fig. 59). Shortly after hatching (8 mm.) the anterior end of the oesophagus becomes completely occluded by a proliferation of its wall just anterior to the laryngeal opening (Fig. 58, A). The oesophagus remains closed until shortly after the opening of the mouth (10-11 mm.) when it reacquires cummunication with the pharynx. The stomach appears as a dilation of the posterior portion of the fore-gut. Its axis is at first longitudinal, but soon it becomes bent so as to lie transversely. Throughout the larval period the stomach remains comparatively small and not clearly marked off from oesophagus and intestine.
The Derivatives of the Mid-gut
Up to the time of hatching the mid-gut remains as a narrow opening, dorsal to the yolk-mass which forms the floor of this, the intestinal region; its roof and sides are but one cell thick (Fig. 37). After hatching, the yolk is rapidly absorbed and the intestine begins to elongate. The process of yolk absorption is most rapid during the first week after hatching; in part the yolk cells degenerate, and in part they become modified into the glandular epithelium of the intestinal wall. Some of the cells of the endodermal lining of the intestine seem to wander outside the wall of the gut, into the mesentery (see below) and contribute to the formation of lymphatic tissue.
As a result of the elongation of the intestine it becomes thrown into a transverse or duodenal loop, extending across the body cavity from the posterior end of the stomach (Fig. 59). The elongation of the intestine continues rapidly, and soon it becomes thrown into a double spiral which occupies the entire ventral part of the body cavity. At its maximum length it is about nine times the length of the body. The oesophagus and stomach also elongate somewhat during this period, so that the pancreas and liver are pushed back into the body cavity. The relations of the mesentery are described below. During the period of metamorphosis the entire digestive tract shortens to about one-third its maximum larval length; this shortening affects chiefly the intestine and stomach.
One structure developing in connection with the enteron has not been mentioned as yet; this is the hypochordal rod. This has no direct relation with the notochord. It appears in tadpoles of about eight somites (3-4 mm.) as a median ridge along the outer surface of the endodermal wall of the midgut (Fig. 70, C). Later this ridge extends both anteriorly and posteriorly, as the part first formed separates from the enteric wall; it becomes entirely free at about 4.6 mm. Finally it extends the entire length of the gut posterior to the dorsal pancreas; through the tail it lies above the postanal gut. It is a narrow rod, only two or three cells in diameter, lying between the dorsal aorta and the notochord. Shortly after the opening of the mouth (13 mm.) it breaks into short pieces and its cells either disappear or scatter; in the older larva no traces remain.
The Derivatives of the Hind-gut
This is the smallest section of the enteron. We have described, in the preceding chapter the formation of the neurenteric canal and proctodaBum, and the terminal dilation of the enteron which becomes the rectal region (Fig. 37). Just after the tail has begun to elongate (4 mm.) the fusion between the rectal and proctodaBal walls becomes perforated by the anal opening, so that the gut opens directly to the outside. The proctocteal region becomes the cloaca of the tadpole and frog, and receives not only the opening of the rectum, but the openings of the excretory and reproductive ducts as well. The urinary bladder is formed just before metamorphosis as a ventral outgrowth from the cloaca.
As the tail grows out, the nerve cord and notochord extend into it, while the true enteron remains limited to the body region, and the neurenteric canal consequently is drawn out posteriorly. It soon cuts, off from the nerve cord, but for a time its antero- ventral limb remains open into the rectum and is known as the postanal gut. This gradually closes, and by the time of hatching it is represented only by a strand of cells extending posteriorly from the rectum, nearly to the tip of the tail; finally it disappears entirely. Throughout the larval stage the rectum remains short and only slightly dilated; during metamorphosis it enlarges and elongates, forming a considerable terminal portion of the alimentary canal.
The Mesodermal Somites
All of the remaining systems are primarily associated with the mesoderm. In the preceding chapter we described the early history of the mesoderm and in a few words we may recall its arrangement at the time the larva is about to commence its elongation.
In the body region the mesoderm is already differentiated into the thickened proximal portion along the chorda, known as the segmental or vertebral plate, and the thinner peripheral lateral plate, which passes around the sides of the yolk-mass to the ventral surface. Dorso-laterally the lateral plate is split into two sheets, the outer or somatic layer, and the inner or splanchnic layer, separated by a narrow splanchnoccel or rudimentary body cavity (Fig. 70, A). Through most of the body region the vertebral and lateral plates are continuous and the cavity of the lateral plate is continued into the vertebral plate as the myoccel At this stage, however, in the anterior body region, the vertebral plate is already transversely divided into three or four pairs of somites, which have separated, distally, from the lateral plate.
In the region of the head and pharynx the mesoderm is in the form of scattered groups of cells, mesenchymal in character, filling the irregular spaces among the organs of these regions, brain, sense organs, ganglia, gillpouches, etc. Some of the details of the later history of this mesoderm have already been mentioned in connection with the visceral pouches, and others will be considered with the history of the vascular and skeletal systems. We may mention here, however, the essential facts regarding the development of the somites and lateral plate.
The formation and differentiation of the somites and lateral plate occur progressively in the posterior direction, so that in a young larva all of the process may
- be read in a Series Of
The Cavity Of the SO . ,. mite, the myOCOel, lies
toward its surface; the outer wall, only one cell thick, forms the cutis plate or dermatome, lying just beneath the surface ectoderm (Fig. 60). The inner wall of the somite is much thickened as the myotome or muscle plate; through the continued thickening of the myotome the myocoel is early obliterated. The myotomal cells or muscle cells, elongate antero-posteriorly through the entire segment; the formation of muscle fibrillse in these cells begins very early (5 mm.) on the side toward the chorda (Fig. 53).
Fig. 60. Transverse section through the sixth mesodermal somite of a 5 mm. larva of R. temporaria, illustrating the arrangement of the meso derm. From Maurer (Hertwig's Handbuch, etc.). c, Cutis plate; Ch, notochord; D, gut wall; m, myotome (muscle plate) ; we, nerve cord; p, lateral plate ;, ventral process of my o torae and cutis plate '
From the ventro-medial portion of the myotome, cells proliferate and move downward below the chorda, and upward between the chorda and the myotome, forming the rudiment of the sclerotome. The somite now separates entirely from the lateral plate, and soon the sclerotome separates from the somite, and extends dorsally around the nerve cord, forming a considerable mesenchymal mass surrounding this and the notochord. This is the region where the cartilaginous vertebral column forms later.
Just after the separation of the sclerotome (5 mm.) the myotome and dermatome send down a ventro-lateral outgrowth, which soon separates from the myotome and forms later the ventral musculature (Fig. 60); from the myotomes of the limb regions these outgrowths extend into the rudiments of the limbs, later giving rise to their voluntary musculature.
The cutis plate breaks into groups of branched mesenchyme cells, some of which become applied to the inner surface of the ectoderm and form the dermal layer of the dorsal half of the embryo, while others pass in between the mytomes, forming the connective-tissue septa or myocommata. In the trunk region of the frog, thirteen pairs of somites are formed altogether, but the two anterior pairs disappear about the time the limbs appear, leaving eleven in the adult. The region of these two transitory somites later becomes incorporated into the head, as the occipital region. The accompanying table, based upon the observations of Elliot, summarizes the history of the somites and spinal nerves of the body region of the embryo. In the tadpole there is, of course, a large, and varying, number of somites in the tail region; Harrison has counted about forty-five pairs in a 5.5 mm. larva of Rana virescens. All posterior to the thirteenth (eleventh of the adult series) disappear during metamorphosis.
Table Of Somites, Vertebra, And Related Nerves Of The Tadpole (Elliot)
Cartilaginous elements in sclerotome
Occipital region of skull
Absent (Disappears at formation of limbs)
Boot of vagus nerve
Absent (Disappears at formation of vertebrae)
No nerve. Ganglion only
Ganglion and nerve Absent in adult
1 spinal nerve ("hypoglossal")
2 1 f brachial plexus
5 ! to body wall
8 [ sciatic plexus
Part of urostyle
10 to pelvic region
Before the separation of the somites and lateral plate, the latter shows traces of segmentation in the region adjoining the somites, from which later the pronephros is formed (see below). This region may therefore be termed nephrotome or intermediate cell mass. These traces disappear, very quickly, and the lateral plate itself is never segmented. The cavity of the lateral plate, the general body cavity, gradually extends ventrally, and finally divides the entire lateral plate into somatic and splanchnic layers. Except in the extreme anterior and posterior ends of the trunk, the cavities of the two sides meet and fuse across the mid- ventral line, establishing a continuous body cavity and completely separating the somatopleure , or body wall, consisting of the somatic mesoderm and integument, from the splanchnopleure, or gut wall, consisting of splanchnic mesoderm and enteric wall.
In the pharyngeal region, the layers of mesoderm remain fused together medially, below the gut; consequently the splanchnocoel is paired in this region, where the heart develops later. The median fusion is a vestige of a ventral mesentery. Along the dorsal side of the enteron, the splanchnic layers of mesoderm push in between the chorda and the enteron, and form the dorsal mesentery by which the gut remains connected with the dorsal wall of the body cavity, and through which later the vessels, nerves, etc., pass to and from the gut. When the yolk is absorbed and the narrowed gut passes to the ventral side of the body cavity, the mesentery forms a thin double fold of membrane. Then as the intestine elongates the mesentery is thrown into folds corresponding with those of the gut.
Through the absence of a ventral mesentery, save in the heart region, the body cavity is continuous from side to side beneath the gut; dorsally the mesentery interrupts such a communication. Later on, the body cavity becomes incompletely divided transversely into anterior and posterior parts, but this and the formation of the pericardial portion of the body cavity, are more conveniently described in connection with the vascular system.
The Vascular System
The first parts of the vascular system to appear are the heart and the large veins connected with its posterior .end. We have already said that the cardiac region lies beneath the hinder part of the pharynx, immediately anterior to the liver and posterior to the thyroid body. In this region the somatic and splanchnic layers of the lateral plate are separated by a wide cavity which is the beginning of the pericardial cavity (Fig. 61). This is at first directly continuous posteriorly with the general body cavity, though we shall see that later it becomes completely closed off. Dorsally there is no definite coelomic space in this, the pharyngeal region. The pericardial wall and the muscular wall of the heart are derived from the lateral plate mesoderm, while the inner lining of the heart, the endothelium, is derived from scattered mesoderm cells lying between the splanchnic mesoderm and the enteron, cells that have been formed from the endoderm in the same way that much of the lateral plate mesoderm has been, i.e., through a splitting off of cell groups from the surface of the enteric wall (Fig. 61). These scattered mesoderm cells are often regarded as belonging primarily with the ventral ends of the hyoid visceral arches. They become distinct by the time two mesodermal somites are formed.
Fig. 61. Sections showing the formation of the heart in the frog. A-D. Series of transverse sections through corresponding regions of a series of embryos of R. temporaria. After Brachet. E. F. Sections through the same region in older embryos of R. sylvatica. A. 2.6 mm. embryo. Mesoderm approaching the mid-line; endothelium appearing. B. Older embryo of same length as A. C. 3 mm. embryo showing enlargement of pericardial cavity and the beginning of the folding of the somatic mesoderm. D. 3.2 mm. embryo. Endothelial cells becoming arranged in the form of a tube. E. Embryo of about 3 mm. F. Embryo of 5-6 mm. Heart tube established; dorsal mesocardium still present, dm, Dorsal mesocardium; e, cardiac endothelial cells; en, endoderm; g, wall of gut (pharynx); p, pericardia! cavity; so, somatic layer of mesoderm; sp, splanchnic layer of mesoderm.
Fig. 61 shows how the layers of the lateral plate extend beneath the pharynx, remaining fused in the mid-line as the ventral mesocardium. The inner or splanchnic wall of the pericardial cavity now folds together dorsally, enclosing the endothelial cells, which have become arranged in the form of a short tube. Finally the splanchnic folds meet and fuse dorsally, forming a tube outside of the endothelial tube and connected with the dorsal wall of the pericardial cavity; this tube forms the muscular wall of the heart and the connection is the dorsal mesocardium.
Fig. 62. Diagrams of frontal projections of the hearts of early frog embryosAfter Weber. A. Heart of an embryo of 2.7 mm. showing the median bulbus arteriosus and the separate auricular and ventricular cavities. B, Heart of a 3.2 mm. embryo showing the fusion of the auricular and ventricular cavities. The broken line marks the incomplete separation between the endothelial auricular and ventricular regions. C. Heart of a 3.5 mm. embryo. At this stage the ventricle is strongly looped ventrally. a, Auricle; ba, bulbus arteriosus; ra, roots of aortic arches; s, incomplete septum between endothelial tubes of auricle and ventricle; v, ventricle; vl, root of left vitelline vein; vr, root of right vitelline vein.
The endothelial tube, which is to be regarded as the primary rudiment of the heart, really consists of a pair of short tubes (Weber); these very early fuse together anteriorly forming a median region, the future bulbus aortce (Fig. 62). From the antero-lateral margins of the bulbus, two short strands of cells extend forward in the floor of the pharynx as the rudiments of the bifurcated truncus arteriosus or ventral aortce. Posteriorly the two endothelial tubes are only incompletely fused and are asymmetrically developed. That of the right side forms a dilated flexed tube which is the rudiment of the ventricle and the right vitelline vein, while that of the left side is more elongated and is dilated posteriorly as the rudiment of the auricle, continuing posteriorly as the left vitelline vein (Fig. 62). Both vitelline veins pass directly into the liver and yolk-mass. These two cardiac tubes gradually fuse more extensively and their cavities become somewhat confluent, so that the ventricular region is in a small degree formed of the left tube also; the more posterior auricle similarly receives a small addition from the end of the right tube with which the right vitelline vein is continuous.
The heart rudiment begins to elongate at once and is thrown, by horizontal folds, into an S-form, whereupon the dorsal mesocardium disappears, leaving the heart tube attached to the pericardial wall only at its ends. The posterior limb of the heart lies toward the left side and abuts against the liver; this forms the region of the sinus venosus and auricles. The anterior section, and the right or middle section which is the region of the ventricle, soon swing downward, becoming relatively ventral in position, while the auricle then extends through nearly the entire dorsal part of the pericardial cavity (Fig. 66).
These limbs of the heart tube are very early separated from one another by constrictions. Shortly after the opening of the mouth the auricle becomes divided into right and left auricles by the downgrowth of the interauricular septum from its dorsal wall. The sinus venosus remains connected with the right auricle. The left auricle receives the pulmonary veins, but these are only slightly represented during the tadpole stage. The wall of the ventricle becomes much thickened by the ingrowth of a muscular network from its inner surface. A few davs after the mouth opens, the bulbus aortae becomes divided into the anterior and posterior parts characteristic of the adult frog, and in the former, now known as the truncus arteriosus, a longitudinal fold appears separating its cavity into right and left channels.
The Origin of the Blood and Vessels
Details regarding the exact method of origin of the blood vessels of the frog are scanty. For the most part they seem to arise (4-4.5 mm.) as irregular and often isolated lacunar spaces in the mesenchyme and splanchnic mesoderm. The cells bordering these spaces gradually form a definite boundary and the sinuses thus formed are linked into continuous vessels. In some cases the smaller vessels seem to be preformed as short solid strands of cells, which become rearranged to form the walls of hollow tubes.
Fig. 63. Sections showing the formation of the blood islands in the frog. After Brachet. A. Part of a transverse section through the middle of the yolk region of a 2.8 mm. embryo of R. temporaries. B. Same of a 3.2 mm. embryo. en, Endothelium; i, blood island; m, mesoderm.
At first these vessels, like the heart itself, are devoid of cellular (corpuscular) elements. Some have described the origin of blood corpuscles directly from the walls of the vessels, but it seems doubtful whether such a process is at all common. For the most part the blood corpuscles are formed from a large group of blood islands, groups of cells occupying the ventral side of the yolk-mass, between the liver diverticulum and the ventral margin of the original blastoporal region (Fig. 63).
The ventro-lateral surfaces of the endodermal yolk-mass, as we have seen, give off the mesoderm by delamination, but in this ventral region the superficial cells of the yolk-mass split off irregularly in groups. These cell groups are the blood islands (Brachet). While some of these cells are converted into the walls of the veins of the yolk, they are mostly transformed into red blood corpuscles, which thus enter the circulation by way of these veins. The corpuscles enter the circulation in Iarva3 of about 5 mm., and for some time their origin from the yolk region is indicated by their abundant yolk content; not until after hatching do they assume the histological characteristics of the definitive corpuscles.
The Arterial System
The earliest arteries to appear (about 4 mm.) are .the paired lateral dorsal aorta, dorsal to the pharyngeal region. At first a series of separate spaces or lacunae in the mesenchyme of the head, these soon connect forming definite vessels extending forward into the cranial region. Posterior to the pharynx these vessels unite forming the median dorsal aorta, which then extends to the posterior extremity of the embryo.
The blood vessels of the visceral arches develop very early. Those of all the branchial arches are essentially similar, while the arteries of the hyoid and mandibular arches are considerably modified from the branchial type and are largely vestigial in character. There is some variation here among different species of Rana; we shall outline the history of these vessels in R. esculenta, as described by Maurer. Here, in each branchial arch a lacunar vascular space appears (about 4.5 mm.) which early connects ventrally with the truncus arteriosus, and dorsally with the lateral dorsal aorta, forming thus, before the gills appear, a continuous aortic arch in each branchial arch (Fig. 64, A). There are, therefore, in the branchial arches, four pairs of aortic arches; these are really the third to sixth pairs of aortic arches, the first and second being formed in the mandibular and hyoid visceral arches.
Fig. 64. Sections through the branchial region of tadpoles of R. esculenta, showing the development of the gills and the history of the aortic arches. After Maurer. A.^ 4 mm. larva showing the continuous first branchial aortic arch. B. 5 mm. larva showing the anastomosis between the afferent and efferent portions of the aortic arch. C. 6 mm. larva with vascular loops in the external gills. D. 13 mm. larva. On the left the opercular cavity is closed and the external gill is beginning to atrophy, while on the right this cavity is still open and the external gill well developed and projecting through the opercular opening. E. 17 mm. larva. Vessels of the second branchial arch. External gill represented only by a minute pigmented vestige, cti, First branchial aortic arch; ab, afferent branchial artery; ao, root of lateral dorsal aorta; au, auditory organ; c, conus arteriosus; e, epithelioid body; eb, efferent branchial artery; eg, external gill; i, internal (anterior) carotid artery; ig, internal gills; n, nerve cord; o, operculum; p, pharynx; pc, pericardial cavity; r, gill rakers; s, oral sucker; v, velar plate; x, anastomosis between afferent and efferent branchial arteries.
When the external gills appear an additional vessel develops dorso-laterally to the aortic arch, along the base of the gill, forming its supply. This vessel opens out of the ventral end of the aortic arch and joins it again toward its upper end (Fig. 64, B); the lower end of the aortic arch may then be termed the afferent branchial artery, its dorsal end the efferent branchial artery. The small vessels of the external gills form loops connecting the dorsal and ventral parts of this second vessel. Then as the external gills disappear and the internal gills develop on the branchial arches, the direct ventral connection between the original aortic arch and the second vessel, becomes interrupted by the disappearance of a part of the aortic arch, and the vascular networks of the internal gills connect the two vessels. In this way the original aortic arch becomes almost entirely the efferent branchial artery, while the second vessel serves as the afferent branchial artery (Figs. 64, 65).
Fig. 65. Diagrams of the aortic arch of the adult frog and tadpole. After Maurer. A. The continuous aortic arch of the adult; showing the parts corresponding with the larval vessels. B. First external gill and associated vessels in young tadpole. C. Internal gill and associated vessels in the tadpole after the disappearance of the external gills, ab, Afferent branchial artery; e, epithelioid body; eb, efferent branchial artery; eg, external gill; ig, internal gill; o, operculum; 'x, direct anastomosis between afferent and efferent branchial arteries.
When the internal gills disappear, during metamorphosis, the lower end of the efferent branchial artery (original aortic arch) reacquires a direct connection with the afferent branchial artery and the blood again passes directly from the truncus to the dorsal aorta (Fig. 65, A). This connection enlarges as the gill capillaries diminish, and finally these direct paths remain as the only vessels of the branchial arches.
Fig. 66. Diagrams of the branchial blood vessels in frog larvae. After Marshall. A. Of a 7 mm. larva (shortly after hatching). The vessels supplying the external gills are removed, only their roots being indicated. B. Of a 12 mm. tadpole. The vascular loops in the gills are omitted, a, Auricle; ac, anterior (internal) carotid artery; am, anterior commissural artery; ao, dorsal aorta; ap t anterior palatine artery; 6, basilar artery; c, anterior cerebral artery; eg, carotid gland; cv, posterior (inferior) vena cava; dC, ductus Cuvieri; g, pronephric glomerulus; h, hepatic veins; hy, hyoidean vein; I, lingual artery; m, mandibular vein; p, pulmonary artery; ph, pharyngeal artery; pm, origin of posterior oommissural artery; pp, posterior palatine artery; pv, pulmonary vein; s, vein of oral sucker; t, truncus arteriosus; u, cutaneous artery; v, ventricle; 1-4, first to fourth afferent branchial arteries; /, II, efferent arteries of the mandibular and hyoid arches; III-VI, first to fourth efferent branchial arteries; VII, lacunar vessel of the fourth branchial arch.
In the fourth branchial arch, which lacks external gills, the history is essentially modified only to the extent of the omission of the vessels related to these structures. The vessels of this arch appear considerably later than in the anterior arches.
The development of the vessels of the mandibular and hyoid arches seems to be quite variable among the different species of Rana. The most consistent account is that of Marshall and Bles, of R. temporaria. Here, in tadpoles of about 5 mm. a lacunar vessel representing the aortic arch (the second of the whole series) appears in the hyoid arch, and a small outgrowth of the lateral dorsal aorta extends toward it, but never actually joins it, disappearing about the time the mouth opens (Fig. 66, A). At hatching a small outgrowth of the truncus arteriosus may be seen extending into the lower end of the hyoid arch; this has a very brief duration. At the same time the vestige of the aortic arch has .divided into dorsal and ventral portions; of these, the former soon disappears while the latter, now known as the hyoidean vein, connects with a large vascular sinus in the region of the oral sucker.
The vessels of the mandibular arch appear shortly before hatching; these are, a lacunar vessel in the lower part of the arch, representing the original aortic arch, and a small outgrowth of the lateral dorsal aorta into the dorsal part. Soon these unite and also join the hyoidean vein. After the mouth opens, the outgrowth from the lateral dorsal aorta separates from the other vessels and grows forward as the pharyngeal artery, while the hyoidean vein disappears with the oral sucker (Fig. 66, B).
The continuations of the lateral dorsal aortse into the head form the roots of the anterior or internal carotid arteries, whose numerous branches supply the organs of the whole dorsal part of the head; the internal carotids become connected by two transverse commissural arteries passing anterior and posterior to the infundibulum (Fig. 66). The ventral part of the head is supplied by the lingual or external carotid arteries; these vessels appear, some time before the opening of the mouth, as a pair of sinuses in the floor of the buccal cavity and pharynx. About the time the mouth opens, they extend backward and connect with the ventral ends of the efferent branchial arteries of the first branchial arch, in the region where the carotid gland (see above) develops later.
About the time of hatching, outgrowths of the dorsal aorta, just back of the pharyngeal region, extend laterally into the region of the pronephros or head kidney (see below). These later become very large and form the vascular glomi of this kidney (Figs. 66, 72); traces of these remain, long after the pronephros itself has disappeared.
During metamorphosis, as the gills disappear, the branchial blood vessels are considerably modified. We have seen that a continuous aortic arch is reestablished in each of the , ao four branchial arches by the fusion
Fig. 67. Diagram of the of the afferent and efferent arteries.
aortic arches and their chief rrn n , v i_ i ' i/xi_'i
branches in an adult frog. The ^^ branchial aortic arch (third Ventral view, ao, Dorsal aorta; o f the whole series) remains as the
c, carotid artery; eg, carotid .
gland; cu, cutaneous artery; /, root of the anterior carotid artery, and is known as the subciavian artery; t, truncus (Fig. 67). The lateral dorsal aorta
arteriosus; v, vertebral artery.
between the first and second (third and fourth) aortic arches, becomes reduced to a solid strand of connective tissue, and the second (fourth) pair of aortic arches consequently become the roots of the dorsal aorta, and are known as the systemic arches. The third (fifth) aortic arch, after becoming a solid strand of tissue, disappears entirely. The fourth (sixth) arch remains as the root of the pulmonary and cutaneous arteries of the adult, and is known as the pulmocutaneous arch.
The pulmonary arteries appear just after hatching as small outgrowths from the upper ends of the efferent branchial arteries of the fourth branchial arch. (Figs. 66, 67). They extend backward to the lung rudiments, which they reach before the vessels of this arch have acquired a connection with the truncus arteriosus. Later the cutaneous arteries leave the pulmonary, and extend dorsally, spreading over the skin of the back and sides. Some time after metamorphosis that part of the aortic arch between the origin of these vessels and the lateral dorsal aorta, known as the ductus Botalli, slowly atrophies and becomes a solid strand.
Longitudinal septa appear in the truncus arteriosus, dividing it into three channels. One of these leads to the carotid arches, and in the heart receives blood from the left side, i.e., fully aerated blood which has been received through the left auricle from the lungs and skin. Another channel leads from the right side of the heart and carries the venous blood to the pulmo-cutaneous arches. The remaining channel connects with the systemic arches; in the heart its closer connection is with the left side.
The Venous System
The large veins of the yolk-mass are in reality the first parts of the vascular system differentiated. These are the paired, but asymmetrical, omphalomesenteric veins (known also as the vitello-intestinal or the vitelline veins) arising on the ventral surface of the yolk, in the region of the blood islands described above, and passing along the lateral surfaces of the yolk and liver diverticulum, to enter the sinus venosus. This posterior chamber of the heart appears to be formed chiefly by the fusion of these large veins, although it receives later a pair of large veins, the ductus Cuvieri or Cuvierian sinuses, coming from the body wall opposite the sinus venosus. As the liver develops, both of the vitello-intestinal veins break up into capillary nets within its substance, and the parts of the two veins between the liver and the heart fuse into a single hepatic vein. Posteriorly from the liver the right vein seems to disappear as a definite channel, while the left partly remains as the root of the definitive hepatic portal vein, ultimately receiving branches from the digestive tract and its appendages.
The ductfts Cuvieri pass from the sinus venosus obliquely upward in a nearly vertical plane, to the body wall where they divide, passing thence anteriorly and posteriorly. The anterior branches are the anterior cardinal veins. These continue forward as the superior jugular veins, receiving blood from the brain and dorsal parts of the head, and from the region of the eye and ear (facial branch). The inferior jugular veins, coming from the region of the mouth, sucker, and ventral surface of the head, open into the roots of the ductus Cuvieri, just before these open into the sinus venosus.
The posterior branches of the ductus Cuvieri are the posterior cardinal veins. These are primarily the veins of the body wall and the excretory systems. They pass posteriorly through the pronephric region, and thence along the medial side of the pronephric ducts (see below) (Figs. 68, 72, 76) receiving blood from the veins of the body wall (segmental veins). A median caudal vein, passing forward through the entire length of the tail, just ventral to the dorsal aorta or caudal artery, upon reaching the body cavity divides above the cloacal region, and its branches connect directly with the extremities of the posterior cardinal veins, so that these receive blood from the tail also. In the region of the head kidney or pronephros (see below) each of these veins forms a large sinusoidal system among the tubules of this excretory organ. Shortly after the opening of the mouth, as the definitive kidney or mesonephros (see below) commences to develop, the arrangement of the posterior cardinal veins is profoundly modified. The hinder parts of the two veins begin to fuse together at about 15 mm., and ultimately form a median vessel, which may be termed the median cardinal vein (Fig. 68). Anteriorly this vessel effects a new and direct connection with the sinus venosus.
This connection is brought about by the development of the posterior or inferior vena cava or postcaval vein. This important vessel is first indicated by the marking out of a definite pathway in the vessels of the dorsal side of the liver, vessels which are branches of the left vitello-intestinal vein (Shore). This vessel then leaves the surface of the liver and passes through the suspensory fold of the liver (mesohepaticum) to the right posterior cardinal vein, with which it connects, just in front of the beginning of the median cardinal vein (i.e., immediately posterior to the pronephric region). This new channel enlarges rapidly and ultimately becomes the largest blood vessel of the body. Through the liver it passes directly to the sinus venosus, and the hepatic vein comes to open directly into it instead of into the sinus venosus.
Fig. 68. The development of the posterior part of the venpus system in the frog. After Shore. A. Portion of a transverse section through the posterior mesonephric region of an 18 mm. tadpole. B. Diagram of the veins of a 25-30 mm. tadpole. C. Diagram of the veins of the adult frog, a, Dorsal aorta; c, vena cava; e, nuclei of the endothelial lining of the mesopheric sinus, continuous with the vascular endothelium; /, femoral vein; i, iliac vein; lc, lateral mesonephric channel of the posterior cardinal vein; m, mesentery; ran, mesonephros; n, mesonephric tubules; p, posterior cardinal veins (in C showing their original location); pv, pelvic vein; rp, renal-portal vein; rr, revehent renal veins; sc, sciatic vein; st, nephrostome; u, caudal vein; vcm, median mesonephric channel of the posterior cardinal vein; W, Wolffian duct; x, connection between caudal vein and the lateral mesonephric channels; 1-1, part of the renal-portal vein formed from the lateral channel of the posterior cardinal; 2-2, part of the renalportal vein formed from the median channel of the posterior cardinal vein.
As the pronephroi degenerate the pronephric sections of the posterior cardinal veins diminish also, and by the time of metamorphosis they have entirely disappeared. The ductus Cuvieri consqeuently remain as the proximal parts of the anterior cardinal veins only, and are sometimes known as the anterior; or superior vence cavce or precaval veins. As the result of these changes, all of the blood from the posterior parts of the body wall, and from the tail, passes directly to the heart through the median cardinal and postcaval veins (Fig. 68). '
The development of the mesonephroi, which begins as the pronephroi diminish, entirely alters the relations of the median cardinal vein. On each side the tubular components of the mesonephros, whose development will be described below, push into this vein, dividing it roughly into three parallel channels, one median and two lateral (Fig 68). The caudal vein remains for a time, opening directly into the posterior end of the median channel, while iliac veins, coming from the hindlegs, open into the lateral channels. The caudal vein disappears later, of course, while the iliac veins remain as the chief vessels leading to the mesonephric region.
The arrangement of the vessels in the adult may now be understood easily. The iliac veins and lateral channels of the median cardinal vein, with which they are continuous, become the afferent or advehent mesonephric veins or the renal portal veins (Fig. 68, C). The small veins from the posterior body wall (posterior vertebral veins) open into the renal portal veins. The vascular spaces of the mesonephros remain connected, by a series of short pathways the revehent mesonephric or renal veins, with the median channel of the median cardinal vein, which therefore remains alone as the posterior continuation of the postcaval vein.
Summarizing we may say that the inferior vena cava or postcaval vein is composed of four different elements. An hepatic section derived from the left vitelline vein, is followed by a short section which represents a new structure; next comes a very short region derived from the original right posterior cardinal vein, and finally, the entire posterior section is formed from the median channel, derived from the fused right and left posterior cardinal veins. The renal portal veins consist of two sections: a posterior part is derived from the iliac vein, and an anterior part is formed from the lateral channel of the median cardinal vein, which represents the hinder part of the original posterior cardinal veins.
A pair of lateral veins develops late, in the ventral abdominal wall, for a time opening directly into the sinus venosus. Posteriorly these connect with the iliac veins, and then continue, fusing together medially. The anterior portions of these vessels then lose thair connection with the sinus venosus and the anterior part of the right vessel disappears entirely, the left vein forming a new connection with the hepatic portal vein, when it is known as the anterior abdominal vein.
The rudiments of the pulmonary veins are indicated very early (about 6 mm.) as proliferations of the endot helium on the dorsal side of the sinus venosus (Federow). These cells later form a definite tube opening proximally into the left side of the auricle, and distally leaving the wall of the sinus venosus and passing dorsally to the rudiments of the lungs. At the base of the lung it bifurcates, each branch passing along the medio-ventral side of each lung rudiment. Later, when the lungs become functional the pulmonary veins discharge into the left auricle.
The Lymphatic System and Spleen
The first indications of this system appear shortly before hatching. In the larva of 6.5 mm. (Knower) a single pair of anterior lymph hearts is present, as small sac-like outgrowths of a pair (usually the fourth) of intersegmental veins (i.e., veins running between the fourth and fifth myotomes, and opening into the posterior cardinal veins at the posterior limit of the pronephros). These hearts lie between the peritoneum and the integument, below the level of the myotomes. The endothelial wall of the lymph hearts is continuous with that of the veins. Outside the endothelium is a syncytial layer or network of striated muscle fibers, which commence rhythmic contraction about the time the mouth opens.
Shortly after hatching (7.5-8 mm.) two lymphatic vessels may be seen passing anteriorly and posteriorly from each heart, along the lateral nerve, in the connective tissue beneath the integument. The anterior vessel extends forward into the head region, while the posterior vessel extends along the sides of the trunk for a considerable distance. The openings of these vessels into the lymph hearts, and of the hearts into the veins, are guarded by long valves. These vessels are formed as blind tubular outgrowths from the endothelium of the lymph heart; they grow rapidly and give off a rich network of fine lymphatic capillaries and vessels which spread generally among the other tissues and especially just beneath the skin.
Fig. 69. Dorsal, lateral and ventral views of the lymphatics in a 26 mm. tadpole of R. temporaries. From Hoyer. For description see text.
In the older tadpole of about 26 mm. (Hoyer) the lymphatic system is quite extensively developed. At this time the anterior vessel runs forward and downward, connecting with a large lymph sinus around the mouth and heart and branchial region (Fig. 69), while the posterior trunk passes to the base of the tail, where it divides into dorsal and ventral branches. The dorsal and ventral branches of each side then unite forming two large vessels which extend through the tail, lying above and below the myotomes (Fig. 69).
The large subcutaneous lymph sacs, so characteristic of both the tadpole and the adult frog, are formed very early from the network growing out from these vessels. The small lymphatics in the subcutaneous connective tissue branch abundantly and anastomose freely, forming a rich network; their walls then disappear and the wide lymph sacs are left, still connected with the lymph hearts by way of the lateral trunks described.
The thoracic ducts also appear to arise from the anterior lymph hearts, as a pair of outgrowths which extend posteriorly, between the dorsal aorta and the posterior cardinal veins. When the hind-legs appear, from one to three pairs of posterior lymph hearts develop in connection with the intersegmental veins of the region, in much the same way that the anterior hearts developed. They open for a time into the posterior cardinal veins, and later, therefore, into the renal-portal veins, whether by the intersegmental veins or by the ischiadic branch is not clear.
The spleen is first indicated in larvae of about 10 mm. by a collection of mesenchymal lymphoid cells in the mesentery, around the mesenteric artery, just dorsal and posterior to the stomach (Radford). These cells multiply and in a 15 mm. larva form a definite projection from the mesentery, covered therefore, by a coelomic or peritoneal epithelium. During this period of enlargement, the spleen appears to receive some cells which wander out from the intestinal epithelium. Later this organ becomes very vascular and in the 25-27 mm. larva it forms a definite ovoid body, in the position where it is found in the adult.
The Formation of the Septum Transversum
We have seen that the pericardial cavity is formed as a median ventral section of the ccelom. This remains completely closed anteriorly and laterally, but posteriorly it is at first directly, though incompletely, open into the general body cavity or peritoneal cavity. During the early stages the liver forms the hinder wall of the pericardial cavity, medially, but it still remains open postero-laterally, either side of the liver, and medio-ventrally, below it. When the ductus Cuvieri are formed, passing from body wall to sinus venosus, they traverse this region of the coelom and aid in establishing the hinder wall of the pericardial cavity. Incomplete peritoneal folds from the body wall accompany the ductus Cuvieri from the body wall to the heart; these are known as the lateral mesocardia. Dorsally the lateral mesocardia remain incomplete for a long time, but ventrally they gradually extend to the body wall entirely across the coelom and form a complete ventral partition, between pericardial and peritoneal cavities. The transverse peritoneal fold thus formed is the pericardio-peritoneal septum, or septum transversum. Its median ventral portion appears to be formed by the peritoneum originally covering the anterior face of the liver; this separates from the liver and becomes added to the septum transversum. On the right side it becomes continuous with the posteriorly directed suspensory fold of the liver (mesohepaticum). Not until after metamorphosis is the septum transversum fully united dorsally with the dorsal mesentery, and the separation of the pericardial and peritoneal cavities entirely completed.
The Urinogenital System
The excretory and reproductive systems develop independently and at widely different times, but in their definitive state they form a complex, in which structures orignally excretory, have assumed morphological and functional relations with the reproductive system, while other parts function, at different times, both as excretory and reproductive organs.
The Excretory System
A functional excretory system is already established, before the rudiments of the reproductive system have more than made their appearance. This is the embryonic or larval pronephric system or larval kidney, known also as the head kidney. This kidney is limited to early larval life and is replaced during the tadpole stage by an excretory organ which remains the definitive kidney of the adult; this is the mesonephros, which, it should be noted, retains as its efferent duct, the duct of the original pronephros . We have then to describe the development of the pronephros and the pronephric duct, the development of the mesonephros, and the disappearance of the pronephros. We shall see how, during the later stages, the arrangement of these parts is complicated by the relation between the excretory and the reproductive systems. Since these organs are symmetrically paired we may describe only the organs of one side.
A. THE PRONEPHROS AND THE PRONEPHRIC DUCT
In a preceding section we described the position and relations of that part of the mesodermal somite known as the intermediate cell mass or nephrotome, and said that this formed a rudiment of the pronephric system. The first indication of the pronephros is seen before the nephrotomal region has separated from either the myotome or the lateral plate, as a solid thickening of the somatic mesoderm anteriorly (Fig. 70, B). This thickening, which begins before the cavity (ccelom) of the lateral plate and nephrotome appears, gradually extends posteriorly along the nephrotomal level, and finally reaches to the region opposite the cloaca, although this is not until the anterior part of the rudiment has become quite markedly differentiated. Anteriorly, in the region of somites 2-4, the pronephros itself is formed, while the posterior remainder forms the pronephric or segmental duct. As the thickening of the anterior pronephric region becomes marked, the rudiment here begins to extend ventro-laterally, like an epaulet, over the outer surface of the dorsal margin of the lateral plate (Fig. 70, C). Spaces appear in this cell mass, about the same time that the ccelom appears in the lateral plate; in the lateral or distal part of the thickening a continuous space is formed, from which there extend medially or proximally, toward the lateral plate, three small irregular canals which open into the upper margin of the coelom of the lateral plate opposite the middle of each of the three pronephric somites (Field). From the posterior end of this peripheral space or common trunk, the cavity leads directly into the cavity of the pronephric duct, which is continuous posteriorly with this portion of the pronephric rudiment.
Fig. 70. Sections through frog embryos (R. sylvatica) illustrating the formation of the pronephros. After Field. A. Through the anterior body region of an embryo at the commencement of its elongation. B. Through the anterior end of the pronephric rudiment of an embryo in which the neural folds are just closed together. C. Through the second nephrostome of an embryo of about 3.5 mm. c, Ccelom; ca, rudiment of pronephric capusle; cc, communicating canal; ec, ectoderm; en, endoderm; g, gut cavity; mp, medullary plate; my, myotome; my 2, second myotome; n, notochord; nc, rudiment of neural crest; si, 82, first and second pronephric nephrostomes; sc, spinal cord; sn, subnotochordal rod (hypochorda) ; so, somatic layer of mesoderm (in A the reference line points to the rudiment of the pronephros) ; sp, splanchnic layer of mesoderm; t, pronephric tubule; v, vertebral plate of mesoderm.
There are now established the primary elements of the pronephros. The three short canals with their cellular walls are the rudiments of the three pronephric tubules, and their openings into the coelom are the nephrostomes. The tubules and also the proximal part of the pronephric duct, now elongate rapidly, and as a consequence become thrown into complicated loops and folds (Figs. 71, 72) forming a conspicuous mass whose position is marked externally by a slight elevation. The pronephric duct gradually acquires a lumen throughout its extent; at about 4.5 mm. the duct effects a connection with the wall of the cloaca, and its cavity then opens into the cloacal chamber (Fig. 54).
FlG . n ._ To tal views of the pronephros
The nephrostomes become of the frog (R. sylvatica). After Field. A.
... ... , . , Right pronephros of an embryo of about 3.5
lined With large Cilia Which mm. The crosses mark the location of the nrnrhipp f\ onrrpnt out of nephrostomes. B. Right pronephros of a
- larva of about 6 mm. First tubule dotted;
the COelom, passing by Way second white; third obliquely ruled; pro,. , , i j nephric (segmental) duct shaded with lines.
of the pronephric duct to the cloaca.
Meanwhile the pronephros acquires a rich vascular supply, both arterial and venous. It will be remembered that the posterior cardinal veins are passing along the pronephric ducts, and in the region of the pronephros itself these veins become greatly enlarged. As the pronephric tubules elongate, they push up into the posterior cardinal sinus, which is ultimately nearly filled by them. Each tubule carries around it a reflected layer of the thin vascular wall and so is completely bathed in the venous stream (Fig. 72).
Fig. 72. Sections through frog larvae illustrating the later development of the pronephros. A. Through the first nephrostome of a larva of R. syhatica of about 8 mm., with prominent external gills. After Field. B. Through the region of the second nephrostome of a 12 mm. larva of R. temporaria. After Furbringer. c, Coelom; cv, sinuses of posterior cardinal vein; eg, external glomerulus; g, gut cavity; gX, ganglion nodosum (part of the ganglion of the vagus nerve) ; I, lung; TO, mesenchyme; myz, second myotome; p, peritoneum; si, sz, first and second pronephric nephrostomes; tr, common trunk; X, root of vagus nerve.
At the same time an arterial supply is derived from the dorsal aorta. This is the pronephric glomus already mentioned.
The first indication of this is a horizontal fold of the splanchnic or medial wall of the dorsal coelom just opposite the second nephrostome. This fold appears at about 4.5 mm. and its development is in general parallel with that of the pronephros. It soon extends the entire length of the pronephric region and becomes considerably elevated, projecting freely into the coelom opposite the nephrostomes (Fig. 72). In it vascular spaces soon appear, some of which form the long convoluted vessels of the glomus proper, while others go to form a vessel, connecting with a branch of the dorsal aorta, which is apparently one of the segmental arteries passing ventrally from the aorta. Later this section of the body cavity is cut off, as the pronephric chamber, by the lateral projection of the lung (Fig. 72, B) which carries a fold of peritoneum across to the peritoneum covering the pronephros, with which it fuses. for a short distance. This pronephric chamber remains open into the body cavity both anteriorly and posteriorly to the lung region.
A definite pronephric capsule is formed early from two sources. The ventro-lateral walls of the myotomes, which we have seen give rise elsewhere to mesenchyme, here, in the pronephric region, evaginate over the dorsal and lateral surfaces of the pronephros, and meet folds coming up from the somatic layer of the lateral plate (about 6 mm.). These folds form a definite connective tissue layer enclosing the pronephros and the pronephric sinus of the posterior cardinal vein.
The pronephros reaches its full development in the larva of about 12 mm., when it consists of a large mass composed of the coiled proximal end of the pronephric duct and the three tubules, each of which has acquired blind tubular outgrowths, the whole mass interpenetrated by the vascular sinus of the posterior cardinal vein. In the larva of about 20 mm. the pronephros commences to degenerate. At this time the pronephric duct becomes closed just back of the pronephros; the tubules become variously dilated and constricted, breaking into irregular sections and gradually disappearing (Fig. 73, C). The nephrostomes approach one another and finally meet, opening into a common cavity known as the common nephrostome, which is then closed, and the nephrostomes thus cut off from the body cavity (Fig. 73, C). The glomus shrinks, and by the time of metamorphosis only a few scattered traces of the pronephros remain, although the glomus remains indicated for some months after metamorphosis. The pronephric ducts do not take part in this process of degeneration, posterior to the pronephric region; they remain, closed anteriorly. The disappearance of the pronephros is correlated with the development of the second excretory system, the mesonephros, to the formation of which we shall now turn.
B. THE MESONEPHROS OR WOLFFIAN BODY
This begins to develop in tadpoles of 8-10 mm. Its rudiment is formed by the nephrotomes of the seventh to twelfth somites, and it is consequently both somatic and splanchnic in origin. The nephrotomes of these segments fuse into a continuous longitudinal strip of irregularly arranged cells, lying between the pronephric duct and the dorsal aorta, along the posterior cardinal vein. In this mass, cell groupings appear, forming definite swellings of the cord. These are the rudiments of the mesonephric vesicles; they are not strictly metameric, but are somewhat more numerous than the mesodermal segments.
All of these rudiments have essentially the same history (Hall). First each becomes divided into a large ventral chamber and a small dorsal one; the larger chamber is a primary mesonephric unit, the smaller a secondary mesonephric unit (Fig. 73, B). The secondary units divide similarly, though much later, into secondary units proper and tertiary mesonephric units. All three series of units develop similarly though successively, and we shall therefore describe only the history of the primary series.
From the vesicular primary unit two outgrowths are formed (Fig. 74). One, known as the inner tubule, extends dorsolaterally to the pronephric duct and opens into it. The other, the outer tubule, grows ventro-medially to the peritoneum with which it fuses and opens into the body cavity. The connections of the inner tubules with the pronephric duct convert this into the mesonephric or Wolffian duct, which remains as the ureter of the mesonephros or definitive kidney. The inner tubules elongate and become coiled, forming the tubular portion of the later kidney.
Fig. 73. Sections through the developing mesonephros and the common nephrostome of R. sylvatica. After Hall. A. Section through the eighth somite of an 8.5 mm. larva. B. Section through the mesonephric rudiment of a 25 mm. larva. C. Section through the common nephrostome of a 25 mm. larva, o, Dorsal aorta; c, coelom; en, common nephrostome; g, germ cell; i, inner tubule; m, mesonephric rudiment; my, myotome; o, outer tubule; p, remains of pronephros; pc, posterior cardinal vein; s, shelf cutting off the common nephrostome from the remainder of the ccelom; so, somatic mesoderm; sp, splanchnic mesoderm; W. Wolffian duct; /, primary mesonephric tubule; //, secondary mesonephric tubule.
Subsequently the outer tubules have a rather unusual history in the frog. From the proximal portion an outgrowth appears, which forms the capsule (Bowman's capsule) around the glo merulus associated with each tubule, the two forming the Malpighian body. Each glomerulus is connected with a small twig derived from the dorsal aorta, and structurally resembles essentially a miniature glomus like that of the pronephros.
Fig. 74. Series of diagrams illustrating the development of the primary mesonephric tubules in R. sylvatica. After Hall. The Wolffian duct is drawn in outline simply. The mesonephric vesicles are shaded; the somatic part of the tubule is shaded by continuous lines, the splanchnic part by dotted lines. A. Wolffian duct and simple mesonephric vesicle. B. Mesonephric vesicle dividing into the large primary mesonephric unit and the small dorsal chamber. The latter elongates antero-posteriorly and represents the rudiment of the secondary and later mesonephric units. C. Formation of the rudiment of the inner tubule. D. Inner tubule extending upward and toward the mesonephric duct; formation of rudiment of outer tubule. E. Outer tubule fused with peritoneum and rudiment of nephrostome thus established. Bowman's capsule forming. Commencement of differentiation of secondary mesonephric tubules. F. Separation of nephrostomal rudiment from remainder of tubule. G. Connection cf nephrostome with branch of posterior cardinal vein. Separation of secondary tubule, and beginning of tertiary tubule indicated, c, Bowman's capsule; i, inner tubule; n, nephrostome; o, outer tubule; p, peritoneum; v, branch of posterior cardinal vein; /, primary mesonephric tubule; //, secondary mesonephric tubule; ///, tertiary mesonephric tubule.
This pare of the outer tubule now separates from the remainder, retaining the connection with the inner tubule, while the distal part retains its connection with the body cavity; this connection now becomes ciliated and forms a typical nephrostome. This nephrostomal region is short and effects a new connection at its inner end, with the sinus of the posterior cardinal vein. It will be remembered that, as the tubules of the mesonephros enlarge (15 mm.) this body seems to extend freely into the posterior cardinal vein, which has a sinusoidal character here and interpenetrates the substance of the mesonephros, its walls being closely reflected around the surfaces of the tubules.
During the later development of the mesonephros, the secondary and tertiary units acquire, similarly, connections with the mesonephric duct, Malpighian bodies, and nephrostomal connections with the body cavity and cardinal vein. Additional outer tubules and nephrostomes are formed later, but it is not clear whether they form as independent evaginations of the peritoneum or by splitting off from those previously formed; perhaps both processes occur. The number finally formed is very large (about two hundred according to Marshall and Bles.)
Upon the development of the reproductive organs certain of the mesonephric tubules become modified and take on new functions; these processes will be described below.
Just before metamorphosis the urinary bladder appears as a median ventral evagination of the wall of the cloaca, nearly opposite the openings of the mesonephric ducts or ureters. The rudiment forms just at the border between the ectoderm and endoderm lining the cloaca. It is at first a long narrow sac, directed anteriorly; later its diameter increases and as it enlarges it becomes bifid at its extremity.
The Reproductive System
In order to make the devlopment of this system easier to understand we may first repeat, very briefly, the arrangement and composition of the adult system as described in the preceding chapter (Figs. 24, 25). In the male each of the paired testes, suspended from the dorsal body wall by a double fold of peritoneum, the mesorchium, is connected by a series of small tubules, the vasa efferentia, with the upper end of the Wolffian duct or mesonephric duct. The vasa efferentia are modified mesonephric tubules, and the mesonephric duct therefore functions here both as excretory (ureter) and reproductive (vas deferens) duct, i.e., as a urinogenital duct. The homolog of the oviduct or Mullerian duct of the female, is represented in the male by a vestigial cord.
In the female the ovaries are similarly suspended by mesovaria. They are not directly connected with the reproductive ducts or oviducts, and consequently, in this sex the Wolffian or mesonephric duct remains purely excretory in function (ureter). The oviduct is a long convoluted tube which develops from the peritoneal epithelium, quite independently of the excretory ducts.
A. THE GONODUCTS
It will be convenient to describe the formation of the gonoducts first. The vas deferens of the male is the original mesonephric duct or ureter, and nothing need be added to the account of its development given above, save to point out that in connection with each duct a glandular seminal vesicle develops, just in front of the opening of the duct into the cloaca. In the female the mesonephric duct remains unmodified, and the seminal vesicles are barely represented.
The Mullerian ducts for a long time develop similarly in both sexes, although they become fully developed and functional, as the oviducts, only in the female. The Mullerian duct appears during the early stages of the degeneration of the pronephros, just beneath the common nephrostome, the formation of which has been mentioned. Here a peritoneal proliferation forms an elongated thickening along the dorso-lateral wall of the body cavity. From the dorsal border of this thickening a thin shelf of cells forms and projects downward (Fig. 75), parallel with the peritoneal thickening. The free lower margin of this shelf or flap then fuses with the peritoneal wall forming a short compressed tube open at both ends. This tube then extends anteriorly and posteriorly: anteriorly it reaches to the anterior end of the body cavity and then turns ventrally, stopping near the base of the lung, where its open end forms, the rudiment of the ostium or infundibulum of the oviduct. Posteriorly the formation of the shelf and its closure continue parallel with and just to the outer side of the mesonephric duct, and entirely
Fig. 75. Sections through the developing Miillerian duct of a 34 mm. tadpole of R. sylvatica. After Hall. A. Section passing through the beginning of the Miillerian evagination. B< Section posterior to A. Duct established but still connected with peritoneum. C. Section still farther posterior, showing the separation of the duct from the peritoneum. M . Mtillerian duct; p, peritoneum ; t, third pronephric tubule
- independent of it, until it reaches the cloaca, with which it connects some time after metamorphosis.
In the male the development of the Miillerian duct ceases at this stage, but in the female it continues to thicken and to elongate, so that it becomes entirely free from the body wall, though remaining suspended from it by a double fold of peritoneum; finally it acquires the characteristics described in the beginning of the preceding chapter.
B. THE GONADS
The primitive germ cells are distiriguislia'ble quite early (about 6 mm.) as a definite thotigh slight ridge along the median dorsal side of the endodermal wall of the intestine. The cells composing this ridge resemble closely the other cells of this part of the enteric wall, and are to be distinguished chiefly by their behavior (Fig. 76, A). The mesentery is formed shortly after this stage, and when the mesodermal folds push in toward the mid-line, above the gut, this ridge of primitive germ cells seems to separate from the gut and to move dorsally, so that when thfe mesentery is formed they are found in its base, near the body wall (Fig. 76, B, C). Here they form a definite median strand of cells between the posterior cardinal veins (8-9 mm.) (Allen).
Fig. 76. Sections showing the origin of the sex-cells (germ cells) in R. sylvatica. After Allen. A, B, Sections of a 7.5 mm. larva showing (^4.) sex-cell ridge of endoderm and (B) its separation as the sex-cell cord. C, Part of a section of an 8.3 mm. larva showing the beginning of the migration of the sex-cells. a, Dorsal aorta; ch, notochord; cv, posterior cardinal vein; e, endoderm cells; g, gut cavity; I, lateral plate of mesoderm; m, mesentery; my, myotome; n, nerve cord; sc, sex-cell cord; sch, subchordal rod (hypochorda) ; sr, sex-cell ridge; W, Wolffian duct.
This germinal strand now divides longitudinally and the halves move more laterally, projecting slightly into the body cavity as the genital ridges, near the attachment of the mesentery and just beneath the cardinal veins. The genital ridges now become more conspicuous through the proliferation of the primitive germ cells and the peritoneal cells covering them, to which are added mesenchyme cells from the body wall. In this cell mass the mesenchyme elements are concerned in the formation of the stroma of the ridge. The peritoneum continues to form a thin superficial covering and later forms the suspensory folds (mesorchia, mesovaria) of the gonads, as the ridges may be called when they project freely into the body cavity. As the primitive germ cells begin to multiply, they form the nests of cells described in the preceding chapter, the further development of which need not be repeated here.
Before metamorphosis begins the anterior third or half of each genital pole of R. temporaria. After Bouin. /, Follicle cells; g,
ridge commences to degenerate and primitive germ ceU;m,mesenbecomes converted into the fat body terv ;. "nests" formed by
multiplication of the primitive (see above). The posterior portion germ cells; s, genital strand has previously acquired secondary (
connections with the mesonephric duct in the following manner. From the stalks of a few (7-8, Nussbaum) of the Malpighian bodies of the posterior part of the mesonephros, there grow out solid strands of cells known as the sexual cords. These become tubular and gradually extend downward into the substance of the gonad, either forming or connecting with spaces within this organ (Fig. 77). From this point onward their history is different in the two sexes. In the male, the sexual cords, after metamorphosis, establish intimate connections with the cavities of the testis and form the efferent ducts (vasa efferentia) by which the spermatozoa are conducted from the gonad to the gonoduct (vas deferens). In the female, while the intragonadial portions of the sexual cords may give rise to cavities there, the parts connecting the gonad and the mesonephros undergo degeneration and remain vestigial in the adult, forming what is known as Bidder's organ.
The sexes are morphologically indistinguishable during the early stages of development , and in R. temporaria it is not until the -tadpole reaches a length of about 30 mm. (Bouin) that the sex can be distinguished. About this time the ovary acquires a central lumen; the sex cords appear larger in the male, and trie form of the nests of germ cells can be distinguished, in that in the testis groups of similar cells are formed while in the ovary the cells become arranged as a follicle surrounding a large central primitive ovum,
The Adrenal Bodies
The adrenal bodies of the adult frog consist of a thin layer of irregularly distributed tissue on the ventral surface of the pelvic portion of the mesonephros and intimately connected with it. Histological examination shows that the tissue consists of a coarse network of cell strands with occasional groups of darkly staining " phaBOchrome " tissue. The spaces within this meshwork are occupied by sinusoids of the efferent renal (median posterior cardinal) vein. These two kinds of tissue areknown respectively as the cortical and the medullary tissues, not because they have such a relation here, but because the corresponding elements of the adrenals in higher forms have such a disposition.
The cortical substance of the adrenal appears first, in the larva of about 12 mm. in the form of small cell groups along either side of the wall o the median posterior cardinal vein (Fig. 78, A). They lie below the level of the mesonephroi, and beneath the peritoneal epithelium from which they appear to have arisen. Just after metamorphosis these cell groups separate from the peritoneum, and begin to send out branching and anastomosing processes which soon form a network, like that of the cortical substance of the adult.
The medullary or phaeochrome substance is derived originally from ganglia of the sympathetic nervous system. After the central network is established there appear within the sympathetic ganglia of the mesonephric region groups of cells, the precise origin of which is not clear, having the properties of these phseochrome cells. Some of these cell groups remain in the sympathetic ganglia, while others appear to migrate into the rudiment of the adrenal body, where they become scattered through the cortical tissue (Fig. 78, B). The method by which they extend into the adrenal is not clearly known in the frog.
Fig. 78. Parts of sections through young R. temporaria, showing the origin of the adrenal bodies. After Srdinko. A. Through 30 mm. tadpole. B. Through 11 mm. frog after metamorphosis, a, Dorsal aorta; ac, cortical cells of adrenal body; am, medullary cells of adrenal body; ct, connective tissue; g, gonad; gs, sympathetic ganglion; m, mesentery; n, mesonephros; ro, revehent renal vein; v, vena cava; x, point where ganglion cells enter mesonephros and adrenal body.
The Skeleton And Teeth
In describing the development of the skeletal system we shall limit our account to the establishment of the essential structures of the tadpole, merely indicating the trend of later development. The later history of the skeleton falls largely without our province.
The Vertebral Column
The formation of the notochord has been described previously, but its differentiation deserves a further word. The chorda cells early become flattened antero-posteriorly, and about the time the embryo begins to elongate, vacuoles appear within the protoplasm of the cells and also between adjacent cells. The chorda becomes surrounded by three sheaths. The primary or elastic sheath is formed on the surface of the chorda by the action of the superficial chorda cells. The secondary or fibrous sheath is formed within the primary sheath by the chorda epithelium, which is composed of a layer of cells M within the primary sheath. Concolumn in the body region siderably later a skeletogenous sheath is
of a larva of Xenopus capensis. After Schauinsiand. c, laid down outside the primary sheath;
Notochord; d, dorsal ver- fa^ j g f orme d by the Sclerotomal Out tebral cartilaginous arch; i,
inner chorda sheath of scle- growths of the SOmiteS, whose formation was described above (Fig. 79). The skeletogenous layer is continued dorsally around the nerve cord, and it also extends a short distance laterally from the chorda, between successive myotomes.
The vertebral column is formed within this skeletogenous layer. First there appears (about 15 mm.) a metameric series of cartilages, along the dorso-lateral surfaces of the chorda in the base of the neural arch. A metameric series of cartilages appears also in the skeletogenous layer along the median ventral surface of the chorda (Fig. 79). The cartilages of the dorsal series become united on each side, so that a pair of continuous strips extends along the entire chorda, while the ventral elements similarly fuse forming a median ventral strip.
drial connective tissue; v, ventral (hypochordal) vertebral cartilage.
Separate vertebra now become marked out by the appearance, in these continuous cartilages, of metameric rings of fibrous tissue; these are the beginnings of the intervertebral ligaments. They appear opposite the middle of each mesodermal segment, consequently the segments of the vertebral column (vertebrae) alternate with the muscle segments. Cartilage now begins to form across the notochord, between successive vertebrae, so that the notochord becomes completely segmented, remaining only intravertebrally. In each of these transverse partitions appears a curved split, concave anteriorly. The intervertebral cartilages then fuse with the adjoining vertebrae and thus determine the procoelous character of the vertebral centra.
The ventral cartilages now grow up around the sides of the chorda, meeting and fusing with the dorsal series. From the former there extend outward short cartilaginous processes which become the transverse processes of the vertebra. Laterally from these, bits of cartilage are formed later which represent ribs. These fuse with the tips of the transverse processes so that no separate ribs are subsequently distinguishable. In the meantime outgrowths from the dorsal elements have extended inward beneath the nerve cord, as well as laterally and dorsally to it (neural arch).
Bony tissue appears first, before the beginning of metamorphosis, in the region between the dorsal and ventral series of cartilages. It soon invades the entire cartilaginous structure, forming a complete shell around the intravertebral notochordal remains, and dorsally around the nerve cord. In addition to the articulation of the procoelous vertebral centra, intervertebral articulations develop on short processies of the neural arches.
The foregoing description applies only to the nine vertebrae of the body. In the greater part of the tal cartilage is not formed. But in the region of the future urostyle three longitudinal strips of cartilage are formed as in the trunk, but these fuse completely enclosing the chorda in a cylinder of cartilage which is never segmented into vertebrae.
The fully formed skull is a complex organ formed by the association, and more or less extensive fusion, of several diverse elements; these are (a) the cranium, (6) the sense capsules, (c) the visceral arches (in part), (d) the notochord (in part), (e) vertebral elements, (/) membrane or derm bones. Before proceeding to describe the formation and association of these elements in the frog, we should note that here no embryologically distinct vertebral elements are included in the skull; their inclusion in the above list is based upon phyletic and comparative grounds, and upon the behavior of the anterior somites.
A. THE CRANIUM AND SENSE CAPSULES
In tadpoles of about 7 mm. the first rudiments of the cranium are formed as a pair of curved strands of dense tissue, soon becoming cartilaginous, along the ventro-lateral surfaces of the fore-brain. These are the rudiments of the trabeculce or trabecular cartilages (Fig. 80, A). They rapidly extend forward and fuse across the mid-line between the olfactory organs, forming there the rudiment of the internasal plate; each rod then continues forward as the trabecular cornu, which expands slightly, partly enclosing the olfactory organ and forming the olfactory capsule. In front of the olfactory capsule the trabecula3 unite with the rudiments of a pair of labial or suprarostral cartilages, lying in the extended upper lip. Posteriorly the trabeculse extend beneath the mid-brain, embracing between their ends the anterior extremity of the notochord, which it will be recalled extends forward to the mid-brain region. Soon similar tissue thickenings extend posteriorly each side of the notochord in the hind- brain region; these are the indications of the parachordce or parachordal cartilages. The rudiments of the parachordals now fuse with the posterior ends of the trabeculaB, enclosing the tip of the chorda and forming a continuous plate beneath the hind- brain, known as the parachordal plate (Fig. 80, A).
In the tadpole at this stage (shortly after hatching) there are present also rudiments of parts of the visceral arches; the general development of these will be described below, but it is necessary to mention here one of these elements, the palato-quadrate, since from the beginning it takes part in the formation of the cranium. The paired palato-quadrate rudiments are formed as short, flattened, crescentic rods, lateral to the trabeculaB. They soon connect with the trabeculaB by anterior ascending processes a short distance back of the olfactory region, and by posterior ascending processes opposite the extremity of the chorda. The rudiments of the cranium thus marked out are now converted into a continuous cartilaginous structure having the appearance illustrated in Fig. 80, A . The large basi-cranial fontanelle in front of the chorda is the seat of the inf undibulum and pituitary body.
Fig. 80. Dorsal views of the chondrocranium of the frog larva. A. Chondrocranium of a 7.5 mm. larva of R. temporaries. After Gaupp, from Stohr-Ziegler model. B. Chondrocranium of a 14 mm. larva of R. fusca. After Gaupp, from Ziegler model, a, Auditory capsule; bp, basal plate; c, notochord; ct, trabecular cornu; /, basicranial fontanelle; in, internasal plate; ir, infrarostral cartilage; j, jugular foramen (for IX and X cranial nerves); m, muscular process; M, Meckel's cartilage; mo, mesotic cartilage; o, occipital process; pa, anterior ascending process of palato-quadrate cartilage; pi, parachordal plate; pp, posterior ascending process of palato-quadrate cartilage; pq, palato-quadrate cartilage; sr, suprarostral cartilage; t, trabecular cartilage.
Immediately subsequent events concern chiefly the posterior part of the cranium. The auditory organ becomes partially enclosed by a connective tissue capsule which is early chondrified, forming a cap open toward the mid-line (Fig. 80, B). A cartilage (mesotic cartilage) then extends posteriorly and laterally from the parachordal plate and becomes united with the auditory capsule- by anterior and posterior ventral connections, leaving between them a wide space. Posteriorly to this mesotic cartilage the floor of the cranium is continued as the occipital cartilage. This also fuses with the floor of the auditory capsule leaving, however, a small space which represents the jugular foramen transmitting the IX and X cranial nerves. The floor of the posterior part of the cranium, composed of the occipital and mesotic cartilages and the parachordal plate, is known as the basal plate.
Fig. 81. Chondrocranium of 29 mm. larva of R. fusca. After Gaupp, from Ziegler. To the left, the ventral surface; to the right, the dorsal surface, o, Auditory capsule; bp, basal plate; c, notochord; ct, trabecular cornu; /, basicranial fontanelle; fa, foramen for carotid artery; fm, foramen magnum; fo, foramen for olfactory nerve; ir, infrarostral cartilage; j, jugular foramen for IX and X cranial nerves; I, perilymphatic foramina; ra, muscular process; M, Meckel's cartilage; o, otic process of palato-quadrate; pf, palatine foramen; pq, palato-quadrate cartilage; sr, suprarostral cartilage; t, trabecular cartilage; v, secondary fenestra vestibuli.
By the time the tadpole has reached a length of about 14 mm. the chondrocranium has acquired the form shown in Fig. 80, B. A still later stage is illustrated in Fig. 81. Comparison of these two figures brings out most of the facts of later development. We need therefore mention specifically only a few details. No traces of the notochord finally remain; it is partly replaced by, and partly converted into cartilage of the basal plate. The occipital region slowly extends vertically forming the hinder wall of the cranial cavity, and fuses extensively with the auditory capsule. Finally the occipital cartilage extends dorsally around the nerve cord, enclosing the foramen magnum. In the frog the occipital cartilage shows no definite indications of its vertebral origin.
The auditory capsule becomes more complete externally, remaining open into the cranial cavity by a large foramen. From the inner surface of the capsule cartilage grows in, surrounding the elements of the membranous labyrinth previously described. On the outer side of the capsule an opening is formed, the secondary fenestra vestibuli, which becomes plugged by the movable operculum. In connection with the ear we described above the development of the plectrum or columella y and its connection later with the annular cartilage in the superficial tympanic membrane. We should repeat that the columella is not related with the elements of the visceral skeleton in the frog.
In the orbital region the trabeculaB gradually grow across the basicranial fontanelle, closing it and forming the floor of this part of the cranial cavity. They also extend vertically forming the lateral walls of the cranial cavity, separating it from the orbits; these walls are perforated only for the passage of nerves and blood vessels. Anteriorly, cartilages from the trabeculaB also extend dorsally across the mid-line forming a narrow dorsal bridge. The large supracranial fontanelle between this bridge and the supraoccipital region is not closed by cartilage.
Fig. 82. A. Anterior portion of chondrocranium of R. fusca during metamorphosis. Lateral view. After Gaupp, from Ziegler. B. Skull of 2 cm. R, fusca, after metamorphosis. Dorsal view. Membrane bones removed from left side. After Gaupp, from Ziegler. a, Auditory capsule; am, anterior maxillary process; an, annulus tympanicus; art, articular process of palato-quadrate cartilage; eo, exoccipital bone; /, fronto-parietal bone; fpo, prootic foramen; mx, maxillary bone; n, nasal bone; o, olfactory cartilages; on, orbito-nasal foramen; pa, anterior ascending process of palato-quadrate; pg, pterygoid bone; pi, plectrum; pm, posterior maxillary process; pp, posterior ascending process of palato-quadrate; pq, palato-quadrate cartilage; pt, pterygoid process of palatoquadrate; px, prem axillary bone; qj, quadrato-jugal bone; II, foramen for optic nerve; ///, foramen for III cranial nerve; IV, foramen for IV cranial nerve.
The ethmoid region remains comparatively simple throughout the tadpole stage; its extreme complication comes later. During the larval period the internasal septum extends dorsally, forming the anterior wall of the cranial cavity, perforated by the olfactory nerves. The trabecular cornua remain separate from the olfactory capsules and connect anteriorly with the suprarostral or labial cartilages. During metamorphosis the labial cartilages and the anterior ends of the cornua disappear in front of the olfactory capsules (Fig. 82).
The formation of the bony elements of the skull occurs relatively late in the frog. As a matter of fact, the derm or membrane bones appear before those which are formed in the cartilage cranium, but they will be described later. There are, in the frog's skull the following elements formed as cartilage bones in the original cranium.
(a) The exoccipitals (lateral occipitals) which form from the posterior parts of the occipital cartilage and auditory capsule; the occipital condyles and the median dorsal and ventral parts of the occipital region remain cartilaginous.
(6) The prootics, which form from the anterior parts of the auditory capsules and the parts of the basal plate and orbital region adjacent to the auditory capsules.
(c) The columellce, whose development has been described in another place.
(d) The ethmoids which form as vertical elements in the anterior part of the inner wall of the orbit; later the two ethmoids unite above and below, forming a band-like element around the cranium. This is often known as the sphenelhmoid or orbito-sphenoid.
In the palato-quadrate cartilage, bone appears only in the region of the articulation with the lower jaw (see below). This region does not form a distinct element of the skull, however, but unites with a membrane bone, the two together forming the quadrato-jugal.
With the exception of the ethmoids, these elements are all present by the end of metamorphosis: the ethmoids form some weeks later.
B. THE VISCERAL ARCHES
The elements of the visceral skeleton are formed in the pharyngeal visceral arches, which are established by the fusion of the serial gill pouches with the ectoderm. We have described the formation of the mandibular, hyoid and four branchial visceral arches. In each of these save the last branchial, skeletal elements appear. The mandibular and hyoid skeletal arches appear about the time the full number of visceral pouches is established, as condensations in the mesenchyme of the visceral arch regions, soon becoming cartilaginous. The mandibular arch appears first as a short rod, lying transversely to the axis of the embryo, in the floor and sides of the mouth cavity (Fig. 57). It is very early divided into two parts, the separation between them marking the jaw articulation. The dorsal section, or upper jaw rudiment, known as the palatoquadrate, has already been described; the ventral section, or lower jaw rudiment, becomes subdivided into Meckel's cartilage, or lower jaw proper, and the infrarostral cartilage. The last two elements remain ventral to the olfactory region as small relatively undifferentiated elements during early development, but the palato-quadrate rapidly enlarges and grows backward, becoming roughly parallel with the trabeculaB and fusing with them at two points as described above. Later (about 21 mm.) the posterior or quadrate portion of this cartilage forms a connection with the auditory capsule. During metamorphosis, as the mouth enlarges and extends far posteriorly, the arrangement of the jaw elements is very considerably modified. The upper end of Meckel's cartilage, which has been in the olfactory region, rapidly extends posteriorly and reaches to the quadrate cartilage, below and in front of the auditory capsule. The quadrate, meanwhile, elongates ventro-laterally. That part of the palato-quadrate lying in the orbital region, softens and largely disappears, and the anterior connection with the trabecula is drawn back in its place and remains as the seat of the future pterygoid and palatine regions. The jaw articulation is thus carried rapidly from the anterior to the posterior region of the cranium, and through the elongation of the quadrate, also some distance laterally from the cranial wall (Fig. 82).
The infrarostral cartilages, which very early fuse across the mid-line forming the apex of the lower jaw, also elongate at this time, and now fuse with the Meckelian cartilages as the mento-Meckelian cartilages. Later on each becomes bony and fuses with the dentary, the chief membrane bone of the lower jaw (see below). A small median element between the infrarostrals fuses with them.
Fig. 83. Hyoid and branchial arches of a 29 mm. larva of R. fusca. Ventral view. After Gaupp, from Ziegler. 66, Basibranchial (first), or copula; bh, basihyal; ch, ceratohyal; ho, hypobranchial plate; 1-4, first to fourth ceratobranchials.
The annulus tympanicus surrounding the tympanic membrane of the frog, forms as an outgrowth of the quadrate cartilage; it becomes separate and gradually extends to the surface of the head, forming first a crescentic, then a circular cartilage, and later bone, long after the completion of metamorphosis (Fig. 82, B).
The development of the hyoid and branchial arches may conveniently be described together. These all appear first as paired rods of dense tissue, lying in the corresponding visceral arches. The hyoid arch forms about the same time as the mandibular, the first branchial just after hatching, the second branchial at 9-10 mm., and the third and fourth branchials shortly after.
On each side, the hyoid cartilage or ceratohyal, extends dorsally, connecting with the palato-quadrate just behind the jaw articulation; ventrally it unites with its fellow (Fig. 83). The first branchials also unite ventrally. The other branchial cartilages do not reach the mid- ventral line, but the lower end of each unites with that anterior to it; later they similarly connect dorsally. In the ventral region of the pharynx a median element, the copula (basibranchial) appears, between the hyoid and the first branchial, connecting with the ventral ends of both these arches. The basihyoid cartilage is represented only by a small median copula in front of the hyoid cartilage. The lower ends of the first branchials become flattened and expanded as the hypobranchial plate, with which the ventral ends of the other three branchials then fuse. Only the lateral or middle sections of the branchial cartilages, between the visceral pouches, then remain separate from one another as the first to fourth ceratobranchials.
Fig. 84. A. Hyobranchial apparatus of R. fusca, toward the end of metamorphosis. The left side is shown in a more advanced stage than the right, in that less cartilage is present. The original cartilage is indicated by fine stipples. The coarse stipples indicate the cartilage added during the early part of metamorphosis* After Gaupp, from Ziegler. B. Hyobranchial apparatus of a 2 cm. R. fusca, after metamorphosis. After Gaupp, from Ziegler. a, Alar process; ac, anterior process of hyoid cornu; 6, body of hyobranchial cartilage; bb, basibranchial (first)< or copula; ch, ceratohyal (hyoid cornu in B)\ ho, hypobranchial plate; I, postero-lateral process of hyobranchial cartilage; m> manubrium; 2, remains of second ceratobranchial (postero-medial process of hyobranchial cartilage).
The arrangement of these arches is profoundly modified during metamorphosis, when the gill slits close and the jaw articulation moves backward. The hyoid bar, or ceratohyal, loses its connection with the palato-quadrate, and becomes considerably reduced in diameter. The copula becomes reduced and a pair of new cartilages develops each side of it, connecting with the hypobranchial plate and hyoid elements; these are the manubrial cartilages (Fig. 84, A).
The hyobranchial apparatus of the fully metamorphosed frog consists of a broad median plate of cartilage formed of the fused manubria, copula, and hyobranchial plate (Fig. 84, B). The ceratohyals remain as slender processes of this, known as the hyoid cornua. Other processes of the median cartilage develop anew, and only the posterior processes formed from the second branchials, represent primary elements of the branchial series; the other elements disappear entirely.
C. THE DERMAL ELEMENTS
The derm bones of the skull begin to appear in the dermal layer of the integument covering the head and lining the mouth before any other bony elements of the skeleton are indicated.
The first derm bone to appear is the median parasphenoid, in the roof of the mouth of the tadpole of about 20 mm. (shortly after the hind-legs appear). This bone finally becomes daggershaped and covers the large basicranial fontanelle of the chondrocranium. The paired f rentals and parietals appear somewhat later, roofing the cranium and covering the supracranial fontanelle; these elements later unite forming the paired frontoparietals (Fig. 82, B). A pair of nasals roof the olfactory capsules, while within the capsules appear the septo-nasals (intranasals) .
During metamorphosis the dermal elements of the mandibular arch and the other bones of the mouth appear. Premaxillce and maxillce form the margin of the upper jaw, connecting later with the teeth (see below), while in the lower jaw MeckeFs cartilage becomes surrounded by the dentary and angular; the dentary then connects with the infrarostrals of Meckel's cartilage. Paired vomers beneath the olfactory capsules, and palatines across the anterior margins of the orbits develop next. The pterygoids develop along the inner faces of the palatoquadrate cartilages, and the squamosals along their outer surfaces, finally extending back over the auditory capsules. The quadrato-jugal represents a dermal element developed in connection with the posterior angle of the palato-quadrate cartilage, and fused with the cartilage quadrate bone of the palatoquadrate itself. With the exception of this element the derm bones remain easily separable from the cartilage bones and the remains of the chondrocranium, even in the skull of the fully grown frog.
Teeth are present in the adult on the premaxillse, maxillae, and vomers. During the larval period the teeth are functionally replaced by the horny "jaws" and "teeth," so that the true teeth develop relatively late. They form independently of the bones with which they are later associated. During metamorphosis a series of dermal papillae forms around the margin of the upper jaw and covering the vomers. These are the tooth germs; they project into an associated thickening of the epidermis. The Malpighian cells of the epidermis covering each tooth germ become the enamel organ and secrete a layer of enamel over the surface of the hollow cone of the dentine which is formed by the surface of the dermal papilla. The cellular core of the papilla remains as the pulp cavity of the tooth. The teeth are elongated by the formation of bony tissue at their bases, and they gradually push through the epidermis. This basal mass of bony tissue serves also to attach the teeth to the inner sides of the jaw, and to the surface of the posterior part of the vomer; their attachment does not occur until some time after metamorphosis.
The teeth are continually wearing away and dropping out of the jaw; they are replaced by new teeth which develop similarly deeper in the dermis. There are therefore always present in the jaws, teeth in various stages of development.
The Appendicular Skeleton
The elements of the pectoral and pelvic arches and limbs do not appear until just before metamorphosis. We shall make only the briefest reference to these structures.
The pectoral arch appears as a pair of crescentic cartilages around the lateral and ventral parts of the body, opposite the anterior end of the vertebral column. Just below its middle each rod forms an articulation (gknoid cavity) with the head of the humerus. Above this are formed the bony scapula and the cartilaginous terminal suprascapula. Below the glenoid cavity the arch is divided into the posterior coracoid and the anterior procoracoid elements. The coracoid becomes bony, while in connection with the procoracoid a dermal element, the clavicle, develops later. The lower ends of the coracoids and procoracoids become united on each side by a cartilaginous epicoracoid. Later the two epicoracoids fuse together in the mid-line.
Posterior to the epicoracoids a median cartilage develops which is the rudiment of the sternum. Later this fuses with the epicoraccids, and its proximal section becomes bony while posteriorly it forms the cartilaginous xiphisternum. Anterior to the epicoracoids a similar omosternum is formed.
The pelvic arch also appears first as a pair of cartilaginous rods, but these are early in contact medio-ventrally, and soon fuse together. These articulate with the femora, and the parts dorsal to the articulations (acetabuld) form the ilia, which connect with the transverse processes of the last or ninth vertebra (sacral vertebra). The postero- ventral region of each arch becomes the bony ischium, while the antero-ventral part remains cartilaginous as the pubis.
While the pelvic arch is, like the pectoral, originally at right angles to the vertebral column, after metamorphosis it rotates so as to lie nearly parallel with the vertebral column and at the same time the ilia elongate enormously, throwing the attachment of the hind limbs far backward.
The details regarding the development of the elements of the limb skeleton are outside our province. For information the student may be referred to the papers of Zwick (1898), Tschernoff (1907), and Schmalhausen (1907, 1908), and to the literature there cited.
References to Literature
CHAPTERS II and III
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Outlines of Chordate Development: 1. Amphioxus | 2. Early Frog | 3. Later Frog Organogeny | 4. Early Chick - Embryonic Membranes and Appendages | 5. Later Chick - Organogeny | 6. Early Mammal - Embryonic Membranes and Appendages | Figures
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