EXOSKELETON.

The exoskeleton, at any rate in most living forms, is very slightly developed in Amphibia. The only representatives of the epidermal exoskeleton are (1) the minute horny beaks found coating the premaxillae and dentaries in Siren and the tadpoles of most Anura, (2) the nails borne by the first three digits of the pes in Xenopus and by the Japanese Salamander Onychodactylus, (3) the horny covering of the calcar or prehallux of frogs. The Urodela and nearly all the Anura, which form the vast majority of living Amphibia, have naked skins. A few Anura belonging to the genera Ceratophrys and Brachycephalus have bony dermal plates developed in the skin of the back, and these plates become united with some of the underlying vertebrae.

In the Gymnophiona the integument bears small cycloid scales arranged in rings which are equal in number to the vertebrae. These scales contain calcareous concretions. Scales also occur between the successive rings.

In the Labyrinthodontia the dermal exoskeleton is in many genera greatly developed. It is generally limited to the ventral surface and consists principally of a buckler formed of three bony plates, one median and two lateral. These plates protect the anterior part of the thorax, and are closely connected with the adjacent endoskeleton. They probably represent the interclavicle and clavicles. Behind this buckler numerous scutes are generally developed, which often cover the whole ventral surface, and may cover the whole body.

Teeth[59].

In Amphibia teeth are generally present on the maxillae, premaxillae and vomers, and except in Anura on the dentaries; sometimes they occur on the palatines as in many Urodela, most Labyrinthodontia, and the Gymnophiona; less commonly on the pterygoids as in Menobranchus, Siredon, some Labyrinthodontia, and Pelobates cultripes[60], or on the splenials as in Siren and Menobranchus, or parasphenoid as in Pelobates cultripes, Spelerpes belli and Batrachoseps. In some Anura such as Bufo and Pipa the jaws are toothless.

In Gymnophiona, Menobranchus, and Siredon, the teeth are arranged in two concentric curved rows. The teeth of the outer row are borne on the premaxillae and maxillae if present, (the maxillae are absent in Menobranchus), the teeth of the second row on the vomers and pterygoids in Menobranchus and Siredon, and on the vomers and palatines in Gymnophiona. In some Gymnophiona there is a double row of mandibular teeth. The vomerine, palatine and parasphenoid teeth of all forms are numerous and are not arranged in rows.

The teeth of all living Amphibia are simple conical structures ankylosed to the bone, and consisting of dentine, coated or capped with a thin layer of enamel. In the Labyrinthodontia teeth of more than one size are sometimes present. The dentine of the basal part of the larger teeth is in some genera very greatly folded, causing the structure to be highly complicated. These folds, the intervals between which are filled with cement, radiate inwards from the exterior and outwards from the large pulp cavity. The basal part of the teeth of Ceratophrys (Anura) has a similar structure.

ENDOSKELETON.

Vertebral column.

Four regions of the vertebral column can generally be recognised in Amphibia, viz. the cervical, the trunk or thoraco-lumbar, the sacral and the caudal regions. In the limbless Gymnophiona, however, only three regions, the cervical, thoracic, and post-thoracic can be made out. The cervical region is limited to a single vertebra which generally differs from the others in having no transverse processes or indication of ribs. It is generally called the atlas, but it commonly bears a small process arising from the anterior face of the centrum which resembles the odontoid process of higher animals, and renders it probable that the first vertebra of Amphibia corresponds to the axis, not to the atlas. Amphibia generally have a single sacral vertebra.

Three elements go to make up the vertebral column in Amphibia, viz.

1. the notochord,

2. the long vertebral centra,

3. intervertebral cartilage which forms the joints between successive centra.

The relations which these three elements bear to one another are subject to much variation. The successive stages can be well traced in the Urodela.

1. The first stage is found in larval Urodeles in general and in adult Ichthyoidea, and some Salamandrina. In these forms the notochord persists and retains approximately the same diameter throughout the whole length of the vertebral column. Bony biconcave centra are present and constrict it to a certain extent vertebrally, while intervertebrally there is a development of cartilage. The connection between the bony vertebrae is effected mainly by the expanded notochord.

2. In the next stage, as seen in Gyrinophilus porphyriticus, the growth of intervertebral cartilage has caused the almost complete obliteration of the notochord intervertebrally, and its entire disappearance vertebrally, i.e. in the centre of each vertebra. The intervertebral cartilage now forms the main connection between successive vertebrae, and sometimes cases are found whose condition approaches that of definite articulations. Readily recognisable remains of the notochord are still found at each end of the intervertebral constriction.

3. In the third stage differentiation and absorption of the intervertebral cartilage has given rise to definitely articulating opisthocoelous vertebrae. These are found in most adult Salamandrina.

The transverse processes of the earlier trunk vertebrae are divided into two parts, a dorsal part which meets the tubercular process of the rib and is derived from the neural arch, and a ventral part which meets the capitular process of the rib, and is derived from the ventral or haemal arch. In the caudal vertebrae and often also in the posterior trunk vertebrae the two processes are fused.

Siren and Proteus, although they possess minute posterior limbs, have no sacral vertebrae, while Cryptobranchus lateralis has two. The caudal vertebrae, except the first, have haemal arches very similar to the neural arches.

In Labyrinthodontia the centra of the vertebrae are generally well ossified biconcave discs. In some forms however, like Euchirosaurus, the centra are imperfectly ossified, and consist of bony rings traversed by a wide notochordal canal. Each ring is formed of four pieces, a large well-ossified neural arch, a basal piece, and a pair of lateral pieces. Vertebrae of this type are called rachitomous.

In the tail region of other forms each vertebra consists of an anterior centrum bearing the neural arch, and a posterior intercentrum[61] bearing chevron bones. Vertebrae of this type are called embolomerous. Haemal arches similar to the neural arches are often found as in Urodela. The transverse processes are sometimes well developed and are divided into tubercular and capitular portions.

In Gymnophiona the vertebrae are biconcave and are very numerous, they sometimes number about two hundred and thirty. Only quite the last few are ribless and so can be regarded as post-thoracic vertebrae. The first vertebra has nothing of the nature of an odontoid process.

In Anura the number of vertebrae is very greatly reduced, only nine and the urostyle being present. Of these, eight are presacral and one sacral. The urostyle is post-sacral and corresponds to three or more modified vertebrae. The first vertebra is without transverse processes, the remaining presacral vertebrae have the transverse processes fairly large, while the sacral vertebra has them very large, forming in some genera widely expanded plates. The urostyle is a long cylindrical rod which articulates with the sacrum generally by two facets. Ankylosed to its anterior end are the remains of two neural arches.

In Anura remains of the notochord are found in the centre of each vertebra, i.e. vertebrally, while in the Urodela they only occur intervertebrally.

The vertebrae in Anura are, as a rule, procoelous. The eighth vertebra is however generally amphicoelous, while the ninth commonly has one convexity in front, and two behind.

In some forms such as Bombinator, Pipa, Discoglossus and Alytes they are opisthocoelous; in others like Pelobates they are variable.

The Skull[62].

Cranium and mandible.

In the Amphibian skull there are as a rule far fewer bones than in the skull of bony fish. The primordial cartilaginous cranium often persists to a great extent. Only quite a few ossifications take place in it; namely in the occipital region—the exoccipitals, further forwards—the pro-otics, and at the boundary of the orbital and ethmoidal regions—the sphenethmoid. The basi-occipital and basisphenoid are never ossified. As in Mammalia there are two occipital condyles formed by the exoccipitals.

Large vacuities commonly occur in the cartilage of both floor and roof of the primordial cranium. These are roofed over to a greater or less extent by the development of membrane bone. Thus on the roof of the cranium there are paired parietals, frontals, and nasals, and on its floor are paired vomers, and a median unpaired parasphenoid.

In all living forms the parietals meet and there is no interparietal foramen, though this exists in Labyrinthodonts.

The palato-pterygo-quadrate bar is united at each end with the cranium, but elsewhere in most cases forms a wide arch standing away from it. The suspensorium is, as in Dipnoi and Holocephali, autostylic. The palato-pterygo-quadrate bar sometimes remains entirely cartilaginous, sometimes its posterior half is ossified forming the quadrate. In connection with it a number of membrane bones are generally developed, viz. the maxillae, premaxillae, palatines, pterygoids, quadratojugals, and squamosals. The pterygoids are, however, sometimes partially formed by the ossification of cartilage. The cartilage of the lower jaw and its investing membrane bones generally have much the same relations as in bony fishes.

Urodela. The skulls of the various Urodeles show an interesting series of modifications and differ much from one another, but all agree in the absence of the quadratojugals, in the fact that the palatines lie parallel to the axis of the cranium, and in the large size of the parasphenoid.

The lower types Menobranchus, Siren, Proteus, and Amphiuma have longer and narrower skulls than do the higher types.

Menobranchus has a very low type of skull which remains throughout life in much the same condition as that of a young tadpole or larval salamander. The roof and floor of the cranium internal to the membrane bones are formed of fibrous tissue, not of well-developed cartilage. The epi-otic regions of the skull are ossified, forming a pair of large bones which lie external to, and distinct from, the exoccipitals. Proteus and the Labyrinthodonts are the only other Amphibia which have these elements separately ossified. The parietals send a pair of long processes forwards along the sides of the frontals. Nasals and maxillae are absent, as is likewise the case in Proteus. Teeth are borne on the vomers, premaxillae, pterygoids, dentaries and angulo-splenials. The suspensorium is forwardly directed.

The skull of Siren resembles that of Menobranchus in several respects, as in the forward direction of the suspensorium and in the absence of maxillae, but differs in the possession of nasals, in the toothless condition of the premaxillae and dentaries, and in the fusion and dentigerous condition of the vomers and palatines.

Amphiuma has a skull which, though narrow and elongated, differs from those of Menobranchus, Proteus, and Siren, and resembles those of higher types in the following respects:—

(1) the suspensorium projects nearly at right angles to the cranium instead of being directed forwards, (2) the maxillae are well developed, and the premaxillae are completely ankylosed together, (3) there are no palatines.

The skulls of Megalobatrachus, Cryptobranchus and Siredon resemble those of the highest Urodeles the Salamanders in their wide form, in having the pro-otics distinct from the exoccipitals which are ossified continuously with the epi-otics and opisthotics, and in having no palatines, but differ in having the two premaxillae separate, and in the arrangement of the vomerine teeth which in Megalobatrachus and Cryptobranchus are placed along the anterior boundaries of the bones, these meeting in the middle line. In Siredon the vomers are separated by the very large parasphenoid.

The suspensorium in Megalobatrachus and Cryptobranchus projects at right angles to the cranium; in Siredon it projects somewhat downwards and forwards as in the Salamandrina.

Modifications of the vomers, pterygoids and palatines accompany the changes of the larval ichthyoid Siredon into the adult salamandroid Amblystoma, the vomers especially come to resemble to a much greater extent those of the Salamandrina.

The ossification of the skull in the Salamandrina is carried further than in the Ichthyoidea, though the supra-occipital and basi-occipital are not ossified. The skull differs from that in the Ichthyoidea in the size of the part of the vomero-palatines which lies in front of the teeth, in the frequent union of the two premaxillae and in the ossification of all the periotic bones continuously with the exoccipital.

The skull differs from that of Anura in the following respects:—

(1) the bones of the upper jaw do not form a complete arch standing away from the cranium, and the maxillae are not united to the quadrates by quadratojugals, (2) the long axis of the suspensorium passes obliquely downwards and forwards instead of downwards and backwards, (3) there is no sphenethmoid encircling the anterior end of the brain, its place being partly taken by a pair of orbitosphenoids, (4) there is no definite tympanic cavity.

Labyrinthodontia. The skull in Labyrinthodontia is remarkable for its extreme solidity, the large number of bones which are present, and the extent to which the roofing over of the temporal and other fossae has taken place. In many forms the surface of the bones is as in Crocodiles, strongly sculptured (fig. 27, right half) with ridges and grooves which probably lodged sensory organs. The bones forming the roof of the skull are generally very uniform in size, perhaps the most noticeable of them being the paired dermo-supra-occipitals (fig. 27, 19). Paired dermo-supra-occipitals occur also in certain Ganoids. The Labyrinthodont skull also bears resemblance to that of many fish in the development of a pair of long pointed epi-otics (fig. 27, 18), which remain permanently distinct from the surrounding bones. The parietals are small and enclose between them the interparietal foramen (fig. 27, 13). In some forms in which the head is protected with an armour of scutes, these do not roof over the interparietal foramen, and from this fact it has been inferred that the Labyrinthodonts had a functional pineal eye. Both supra- and infra-temporal fossae are partially or completely roofed over by the postorbitals and large supra-temporals (fig. 27, 15).

There is generally a ring of bones in the sclerotic coat of the eye. The pterygoids do not meet in the middle line, being separated by the parasphenoid. The palatines bear teeth, and in some genera (Archegosaurus) form long splints lying along the inner side of the maxillae and more or less surrounding the posterior nares. In others (Nyrania) they lie in the normal position near the middle line, one on each side of the parasphenoid. The vomers bear teeth and sometimes meet in the middle line; they are sometimes confluent with the parasphenoid. On the ventral surface of the cranium there are generally large palatal vacuities.

In the mandible there is often a well-marked postglenoid process, and the articular is generally completely ossified.

Gymnophiona. The skull bears a considerable resemblance to that of Labyrinthodonts, especially in the arrangement of the bones which bound the mouth cavity. The cranium is very hard, and is covered by a complete bony roof formed mainly of the exoccipitals, parietals, frontals, prefrontals, nasals and premaxillae. The nasals and premaxillae are sometimes ossified continuously. There is a median unpaired ethmoid whose dorsal end appears at the surface wedged in between the frontals and parietals. The bone generally regarded as the squamosal[63] is very large, and it and the maxillae generally together surround the orbit, which, in Epicrium, has in it a ring of bones. The palatines form long tooth-bearing bones fused with the inner sides of the maxillae; they nearly surround the posterior nares.

The quadrate bears the knob, and the angular the cup for the articulation of the mandible,—a very primitive feature. The mandible is also noticeable for the enormous backward projection of the angular.

Anura. In Anura the skull is very short and wide owing to the transverse position of the suspensorium. There is often a small ossification representing the quadrate. Sometimes as in Hyla and Alytes there is a fronto-parietal fontanelle.

As compared with the skull in Urodela the chief characteristics of the skull of Anura are:—

1. the presence of a sphenethmoid,

2. the union of the frontals and parietals on each side,

3. the occasional occurrence of small supra- and basi-occipitals,

4. the backward growth of the maxillae and its connection with the suspensorium by means of the quadratojugal,

5. the dagger-like shape of the parasphenoid,

6. the occurrence of a definite tympanic cavity,

7. the frequent occurrence of a predentary or mento-meckelian ossification in the mandible.

The skull of Pipa is abnormal, being greatly flattened and containing little cartilage. The fronto-parietals are fused, and there is no sphenethmoid. The quadrates are well developed and the squamosals and parasphenoid differ much from those of other Anura.

Hyoid and branchial arches.

In larval Amphibia the hyoid and four branchial arches are generally present, and in adult Ichthyoidea they are frequently almost as well represented as in the larva, and are of use in strengthening the swallowing apparatus. They are very well seen in Siredon, and consist of a hyoid attached by ligaments to the suspensorium, followed by four branchial arches of which the first and second are united by a copula (fig. 29, D, 8), while the third and fourth are not. The hyoid is not always the largest and best preserved of the arches, for sometimes as in Spelerpes one of the branchials is far larger than the hyoid. Four branchial arches occur in Siren as in Siredon, but in Proteus there are only three.

In some larval Labyrinthodontia (Branchiosaurus) four branchial arches are known to occur, and their arrangement is almost precisely similar to that in Siredon.

In Gymnophiona the remains of only three branchial arches occur in addition to the hyoid. The four arches are all very similar to one another, each consists of a curved rod of uniform diameter throughout. The hyoid is united with the first branchial arch, but has no attachment to the cranium.

In larval Anura (fig. 29, C) the arrangement of the hyoid and branchial arches is much as in Urodela. In the adult, however, the ventral parts of all the arches unite, forming a compact structure, the basilingual plate (fig. 29, B, 1).

The dorsal parts of the first three branchial arches disappear, but those of the fourth become ossified and form the short, stout thyro-hyals or posterior cornua. The dorsal parts of the hyoid arch in the adult form a pair of long bars, the anterior cornua, which are united to the periotic region of the skull in front of the fenestra ovalis either by short ligaments or by fusion as in Bufo. In Pipa and Xenopus the first and second branchial arches persist as well as the fourth (thyro-hyal), but in Pipa the hyoid is wanting.

Ribs.

Ribs are generally very poorly developed in Amphibia. In Anura they are in most cases absent; when present they generally form minute unossified appendages attached to the transverse processes, but in Discoglossus and Xenopus the anterior vertebrae are provided with distinct ribs. In Urodela and Labyrinthodontia they are generally short structures, each as a rule attached to the vertebra by a bifurcated proximal end. The number of rib-bearing vertebrae varies, but the first and the posterior caudal vertebrae are always ribless. The anterior caudal vertebrae too are generally ribless, but sometimes a few of them bear small ribs. In Spelerpes the last two trunk vertebrae are ribless, and hence may be regarded as lumbar vertebrae.

In Gymnophiona ribs are better developed than in any other Amphibia; they occur on all the vertebrae except the first and last few, and are attached to the transverse processes, sometimes by single, sometimes by double heads.

Sternal ribs are almost unknown in Amphibia, but traces of them occur in Menobranchus.

Sternum.

In Amphibia the sternum is not very well developed; sometimes as in Gymnophiona and Proteus no traces of it occur, and in the Urodela it is never ossified. It is always very intimately related to the pectoral girdle. In the Salamandrina it has the form of a broad thin plate of cartilage, grooved and overlapped by the coracoid.

In most Anura the sternum consists of a number of parts arranged in series. At the anterior end is a flat cartilaginous plate with a bony basal stalk. This plate is called the episternum, and its stalk the omosternum. The continuity of the sternum is now interrupted by a pair of cartilaginous structures, the epicoracoids, which are shoulder-girdle elements, and represent the unossified ventral ends of the coracoids. In some cases cartilaginous epiprecoracoids can also be distinguished. Further back is the long sternum proper, while last comes the xiphisternum, a broad expanded plate of cartilage.

In some Anura such as Pipa and Hyla the number of sternal elements is considerably reduced.

Appendicular Skeleton.

Pectoral girdle.

The most primitive Amphibian shoulder-girdle is found in the Urodela. It consists of a dorsal element, the scapula, a posterior ventral element, the coracoid, and an anterior ventral element, the precoracoid. The clavicle is not developed, and the two coracoids overlap in the middle line. The shoulder-girdle remains largely cartilaginous but the proximal end of the scapula is ossified, and the ossification may extend through part of the coracoid and precoracoid.

In Labyrinthodontia there is an exoskeletal ventral buckler formed of three plates, a median one, which probably represents an interclavicle, and two lateral ones, which are probably clavicles. Traces of endoskeletal structures, probably corresponding to the precoracoid and scapula, are also known in some cases. The Gymnophiona and some of the Labyrinthodontia have lost the pectoral girdle and limbs.

The ossification of the shoulder-girdle has gone on much further in Anura than it has in Urodela. Clavicles are present and the scapula and coracoid of each side are ossified from separate centres. The distal part of the scapula forms a large imperfectly ossified plate, the suprascapula.

The shoulder-girdle of Anura is however subject to considerable variations. In the Toads (Bufonidae) the epicoracoids or unossified ventral ends of the coracoids and precoracoids overlap in the middle line (fig. 30, B, 5). This arrangement is called Arciferous. In the Frogs,—Ranidae, and other forms belonging to the group Firmisternia,—the epicoracoids do not overlap but form a narrow cartilaginous bar separating the ventral ends of the coracoids (fig. 30, A, 5).

Anterior limb.

In many Amphibia and especially in the Urodela the anterior limb has a very simple unmodified arrangement. The humerus is straight and of moderate length, its ends are rounded for articulation on the one hand with the shoulder-girdle, and on the other hand with the radius and ulna. In the Urodela the radius and ulna are distinct. In the Anura they have fused, though the line of junction of the two is not obliterated. Their proximal ends are hollowed for articulation with the convex end of the humerus.

The manus in all recent Amphibia agrees in never having more than four complete digits, but is subject to considerable variation, this statement applying especially to the carpus.

In the larva of Salamandra (fig. 31, A), except that the pollex is absent[64], the manus retains completely the condition which is generally regarded as primitive for the higher Vertebrata. It consists of an anterior row of three elements, the ulnare, intermedium, and radiale, and a posterior row of four, the carpalia 2, 3, 4, and 5. Interposed between the two rows is a centrale. Menobranchus has a similar very simple carpus. In most other Amphibia this simplicity is lost. This loss may be due to:—

(a) fusion of certain structures, e.g. in the adult Salamandra the intermedium and ulnare have fused,

(b) displacement of structures, e.g. in Bufo viridis, the centrale has been pushed up till it comes to articulate with the radius,

(c) the development of supernumerary elements, especially of extra centralia. In Megalobatrachus two or even three centralia sometimes occur.

In the great majority of Amphibia while one digit, probably the first, is absent, the other four digits are well developed. In the forms however with degenerate limbs like Amphiuma, Siren and Proteus the number of digits is still further reduced. In Siren there are three or four, in Proteus three, and in Amphiuma two or three digits in the manus.

In Anura the pollex is represented only by a short metacarpal. There are sometimes traces of a prepollex. The carpus often has two centralia and the intermedium is absent.

In Labyrinthodontia the limbs are generally very simple and resemble those of Urodela. In some forms, however, the manus differs from that of all living Amphibia in possessing five well-developed digits.

Pelvic girdle.

The simplest Amphibian pelvis is that of some of the Labyrinthodontia; thus in Mastodonsaurus it consists dorsally of a short broad ilium placed vertically and attached to the sacrum, and ventrally of a small pubis and of a large ischium meeting its fellow in the middle line. In some Labyrinthodonts the pubes as well as the ischia meet in a ventral symphysis, and in many there are no obturator foramina. In Siren, Gymnophiona and some Labyrinthodontia the pelvic girdle and limbs are absent.

In Urodela the ventral element of the pelvis on each side forms a flat plate which meets its fellow of the opposite side. The anterior part of the plate, representing the pubis, generally remains cartilaginous throughout life; the posterior part representing the ischium is in almost every case well ossified. Attached to the anterior end of the pubes there is an unpaired bifid cartilaginous structure, the epipubis. The ilia are vertically placed.

In most Anura the pelvis is peculiarly modified in correlation with the habits of jumping. The long bone generally called the ilium is placed horizontally and is attached at its extreme anterior end to the sacrum. The ischium is ossified and distinct. Ventrally in front of the ischium there is a tract of unossified cartilage which is often regarded as the pubis. In Xenopus, however, the bone corresponding to the ilium of the Frog is seen to ossify from two centres, one forming the ilium, the other, which lies at the symphysis, being apparently the pubis. This makes it probable that the so-called ilium of the Frog is really to be regarded as an ilio-pubis, and renders the homology of the cartilaginous part uncertain, but it probably corresponds to the acetabular bone of mammals. In Xenopus also there is a minute epipubis similar to that of Urodeles.

Posterior limb.

In Urodela the posterior limb (fig. 31, B) closely resembles the anterior limb, but is even less removed from the primitive condition of the higher vertebrates in the fact that all five digits are commonly present. The tibia and fibula are short bones approximately equal in size. In some cases the number of digits is reduced. Thus in Menobranchus the pes has four digits, in Proteus it has two, and in Amphiuma two or three, while in Siren the posterior limbs have atrophied.

In correlation with their habits of jumping, the posterior limbs in Anura are much lengthened and considerably modified. The tibia and fibula are completely fused. The intermedium is absent, while the tibiale and fibulare are greatly elongated. Tarsalia 4 and 5 are absent. Five digits are always present, and there is a prehallux formed of two or more segments.

In general the posterior limbs in Labyrinthodontia bear the closest resemblance to the anterior limbs; in some cases three centralia are found.

In Ichthyoidea, and in most Labyrinthodontia, the cartilages of the carpus and tarsus remain unossified; in Salamandrina and in Anura they are generally ossified.