Chapter III: Part I: Amphibia (2)

The HYOID APPARATUS of the Anura is complicated. It is originally composed of the hyoidean and four branchial arches, with one median, copular piece. The branchial arches form in the early life of the tadpole the elaborate framework of the filtering apparatus mentioned on p. 44. During metamorphosis the whole filter disappears, owing to resorption of the greater part of the branchial arches; only their median portions remain, and fuse with the enlarged copular piece and the hyoidean arches into a broad shield-shaped cartilage (_corpus linguae_), whence several lateral processes sprout out, the posterior pair of which are generally called thyrohyals or thyroid horns. The true hyoid horns give up their larval lean-to articulation with the quadrate, become greatly elongated, and gain a new attachment on the otic region of the cranium. The transformation of the whole apparatus has been studied minutely by Ridewood, in _Pelodytes punctatus_.[13]

SKIN

The epidermis of the young larvae of Amphibia is furnished with cilia, which later on are suppressed by the development of a thin hyaline layer or cuticula, but clusters of such cilia remain, at least during the larval life and during the periodical aquatic life of the adult, in the epidermal sense-organs. In the frog, currents are set up by the ciliary action at an earlier stage, and are maintained to a later stage than in the newt. In the latter the tail loses its ciliation, whereas in the frog it remains active almost up to the time of the metamorphosis. In tadpoles of 3-10 mm. nearly the whole surface is ciliated (Assheton).[14] The cilia work from head to tail, causing the little animal, when perfectly quiet, to move forwards slowly in the water. Beneath the cuticula, in the Perennibranchiata and the larvae of the other Urodela, lies a somewhat thicker layer of vertically striated cells, the so-called pseudo-cuticula, which disappears with the transformation of the upper layers of the Malpighian cells into the stratum corneum. The latter is very thin, consists of one or two layers of flattened cells, and is shed periodically by all {32}Amphibia in one piece. In the Urodela it generally breaks loose around the mouth, and the animal slips out of the delicate, transparent, colourless "shirt," which during this process of ecdysis or moulting becomes inverted. In the Anura it mostly breaks along the middle line of the back, the creature struggles out of it, pokes it into its mouth, and swallows it. Urodela also eat this skin. As a rule the first ecdysis takes place towards the end of the metamorphosis, preparatory to terrestrial life. So long as the animal grows rapidly, the skin has to be shed frequently, since this corneous layer is practically dead and unyielding. Adult terrestrial Urodela do not seem to moult often, mostly only when they take to the water in the breeding season. Anura, on the other hand, moult often on land, at least every few months. The surface of the new skin is then quite moist and slimy, but it soon dries and hardens.

The Malpighian stratum consists of several layers, thickest in the Perennibranchiata; in them it contains mucous cells throughout life, in others such slime-cells are restricted to larval life. Later, regular slime-glands are developed, which open on the surface. They are very numerous, and more evenly distributed, over most parts of the body, than the specific or poison-glands, which are restricted to certain parts, often forming large clusters, especially on the sides of the body. They reach their greatest development in the "parotoid glands" of the Anura. Both kinds of glands are furnished with smooth muscle-fibres, which are said to arise from the basal membrane underlying and forming part of the Malpighian layer; these muscle-cells extend later downwards into the corium. For the action of the poison, see p. 37.

The stratum corneum is mostly thin, but on many parts of the body, especially in Anura, the epidermal cells proliferate and form hard spikes or other rugosities, generally stained dark brown. With these may be grouped the nuptial excrescences so frequent in the Anura, especially on the rudiment of the thumb, and on the under surface of the joints of the fingers and toes. In many Anura, less frequently in the Urodela, the tips of the fingers and toes are encased in thicker horny sheaths, producing claws or nails. They are best developed among newts in _Onychodactylus_, among the Anura in _Xenopus_ and _Hymenochirus_. The horny covering of the metatarsal tubercles reaches its greatest size in {33}the digging spur or spade of _Pelobates_. In most of these cases the cutis is elevated into more or less wart-like papillae, covered, of course, by the proliferated and cornified epidermis. In the female of _Rana temporaria_ nearly the whole surface of the body becomes covered with rosy papillae during the breeding season. Similar nuptial excrescences are common, and are most noteworthy in the male of the Indian _Rana liebigi_.

The epidermis also contains sense-organs. They attain their highest development in the larvae; later on they undergo a retrogressive change. Each of these sense-organs is a little cup-shaped papilla, visible to the naked eye. It is composed of elongated cells which form a mantle around some central cells, each of which ends in a stiff cilium perforating a thin, hyaline membrane which lines the bottom of the cup, and is perhaps the representation of the cuticula. These ciliated cells are connected with sensory fibres, the nerve entering at the bottom of the whole organ. The cilia are in direct contact with the water, but the outer rim of the whole apparatus is protected by a short tube of hyaline cuticula-like secretion. These sense-organs are, in the larvae, scattered over the head, especially near the mouth and around the eyes, whence they extend backwards on to the tail, mostly in three pairs of longitudinal rows, one near the vertebral column, the others lateral. They are supplied by the lateral branch of the vagus nerve. They disappear during the metamorphosis, at least in the Anura, with the exception of _Xenopus_, in which they form conspicuous white objects. The white colour is caused by the tubes becoming choked with the débris of cells or coagulating mucous matter, so that it is doubtful if these organs, which moreover have sunk deeper into the skin, are still functional. In the terrestrial Urodela these organs undergo a periodical process of retrogression and rejuvenescence. During the life on land they shrink and withdraw from the surface, and their nerves likewise diminish, but in the breeding season, when the newts take again to aquatic life, they revive, are rebuilt and become prominent on the surface. They are an inheritance from the fishes, in which such lateral line organs are universally present.

The cutis of most Amphibia is very rich in lymph-spaces, which, especially in the Anura, assume enormous proportions, since the so-called subcutaneous connective tissue forms {34}comparatively few vertical septa by which the upper and denser layers, the corium proper, are connected with the underlying muscles. The spaces are filled with lymph, and into some of them the abnormally expanded vocal sacs extend, notably in _Paludicola_, _Leptodactylus_, and other Cystignathidae, and in _Rhinoderma_.

The cutis frequently forms papillae and prominent folds, sometimes regular longitudinal keels on the sides of the back; but dermal, more or less calcified or ossified scales are restricted to the Stegocephali and to the Apoda, _q.v._, pp. 79, 87. We conclude that the Urodela and Anura have entirely lost these organs. Dermal ossifications, besides those which now form an integral part of the skeleton, like many of the cranial membrane-bones, are rare, and are restricted to the Anura. They are least infrequent on the head, where the skin is more or less involved in the ossification of the underlying membrane-bones, for instance in _Triprion_, _Calyptocephalus_, _Hemiphractus_ and _Pelobates_. The thick ossifications in the skin of the back of several species of _Ceratophrys_ are very exceptional. In _Brachycephalus ephippium_ these dermal bones enter into connection with the vertebrae; small plates fuse with the dorsal processes of the first to third vertebrae, while one large and thick plate fuses with the rest of the dorsal vertebrae. Simple calcareous deposits in the cutis are less uncommon, for instance, in old specimens of _Bufo vulgaris_. We are scarcely justified in looking upon these various calcifications and even ossifications as reminiscences of Stegocephalous conditions.

The skin contains PIGMENT. This is either diffuse or granular. Diffuse pigment, mostly dark brown or yellow, occurs frequently in the epidermis, even in the stratum corneum. The granular pigment is stored up in cells, the chromatophores, which send out amœboid processes, and are restricted to the cutis, mostly to its upper stratum, where they make their first appearance. Contraction of the chromatophores withdraws the pigment from the surface, expansion distributes it more or less equally. The usual colours of the pigment are black, brown, yellow, and red. Green and blue are merely subjective colours, due to interference. A peculiar kind of colouring matter is the white pigment, which probably consists of guanine, and is likewise deposited within cells; cf. the description of the white spots in the skin of _Hyla coerulea_.

{35}Most Amphibia are capable of changing colour, the Urodela, however, far less than the Anura, some of which exhibit an extraordinary range and adaptability in their changes.

The mechanism by which the change of colour is produced in frogs has been recently studied by Biedermann.[15] If we examine the green skin of the common Tree-frog, _Hyla arborea_, under a low power and direct light, we see a mosaic of green, polygonal areas, separated by dark lines and interrupted by the openings of the skin-glands. Seen from below the skin appears black. Under a stronger power the black layer is seen to be composed of anastomosing and ramified black pigment-cells. Where the light shines through, the skin appears yellow. The epidermis itself is quite colourless. The mosaic layer is composed of polygonal interference-cells, each of which consists of a basal half which is granular and colourless, while the upper half is made up of yellow drops. Sometimes the tree-frog appears blackish, and if then the black pigment-cells are induced to contract, for instance, by warming the frog, it appears silver-grey; in this case the pigment in the yellow drops is no longer diffuse, but is concentrated into a round lump lodged between the interstices of the granular portions; the black pigment-cells are likewise balled together. These black chromatophores send out numerous fine branches, which occasionally stretch between and round the polygonal cells. When each of these is quite surrounded and covered by the black processes, the frog appears black. On the other hand, when the black pigment-cells withdraw their processes, shrink up, and, so to speak, retire, then the light which passes through the yellow drops is, by interference, broken into green.

Stoppage of the circulation of the blood in the skin causes the black chromatophores to contract. Carbon dioxide paralyses them and causes them to dilate. This is direct influence without the action of nerves. But stimulation of the central nerve-centres makes the skin turn pale. Low temperature causes expansion, high temperature contraction, of the chromatophores. Hence hibernating frogs are much darker than they are in the summer. Frogs kept in dry moss, or such as have escaped into the room and dry up, turn pale, regardless of light or darkness, probably owing to a central, reflex, nerve-stimulus.

Tree-frogs turn green as the result of the contact with leaves. {36}Dark frogs will turn green when put into an absolutely dark vessel in which there are leaves. This is reflex action, and blinded specimens do the same. The principal centres of the nerves which control the chromatophores, lie in the corpora bigemina and in the optic thalami of the brain. When these centres are destroyed, the frog no longer changes colour when put upon leaves, but if a nerve, for instance the sciatic, be stimulated, the corresponding portion of the body, in this case the leg, turns green. Rough surfaces cause a sensation which makes the frog turn dark. _Rana_ seems to depend chiefly upon temperature and the amount of moisture in the air, so far as its changes of colour are concerned. Biedermann concludes that the "chromatic function of frogs in general depends chiefly upon the sensory impressions received by the skin, while that of fishes depends upon the eye."

All this sounds very well, but the observations and experiments are such as are usual in physiological laboratories, and the frogs, when observed in their native haunts, or even when kept under proper conditions, do not always behave as the physiologist thinks they should. There is no doubt that in many cases the changes of colour are not voluntary, but reflex actions. It is quite conceivable that the sensation of sitting on a rough surface starts a whole train of processes: roughness means bark, bark is brown, change into brown; but one and the same tree-frog does not always assume the colour of the bark when it rests, or even sleeps upon, such a piece. He will, if it suits him, remain grass-green upon a yellow stone, or on a white window-frame. I purposely describe such conditions, changes, coincidences, and discrepancies in various species, notably in _Hyla arborea_, _H. coerulea_, _Rana temporaria_, _Bufo viridis_, to show that in many cases the creature knows what it is about, and that the eye plays a very important part in the decision of what colour is to be produced. The sensory impression received through the skin of the belly is the same, no matter if the board be painted white, black, or green, and how does it then come to pass that the frog adjusts its colour to a nicety to the general hue or tone of its surroundings?

Boulenger[16] has given us a summary of the action of the POISON of Amphibia:

{37}It is well known to all who have handled freshly-caught newts, and certain toads, especially _Bombinator_, that their secretion acts as a sternutatory, and causes irritation of the nose and eyes, the effects produced on us by _Bombinator_ being comparable to the early stages of a cold in the head. Many collectors of Batrachians have learned, to their discomfiture, how the introduction of examples of certain species into the bag containing the sport of their excursion may cause the death of the other prisoners; for although the poison has no effect on the skin of individuals of the same species, different species, however closely allied, may poison each other by mere contact. But when inoculated the poison acts even on the same individual.

Miss Ormerod, to personally test the effect, pressed part of the back and tail of a live Crested Newt between the teeth. "The first effect was a bitter astringent feeling in the mouth, with irritation of the upper part of the throat, numbing of the teeth more immediately holding the animal, and in about a minute from the first touch of the newt a strong flow of saliva. This was accompanied by much foam and violent spasmodic action, approaching convulsions, but entirely confined to the mouth itself. The experiment was immediately followed by headache lasting for some hours, general discomfort of the system, and half an hour after by slight shivering fits."

Numerous experiments have shown that the poison of toads, salamanders, and newts is capable, when injected, of killing mammals, birds, reptiles, and even fishes, provided, of course, that the dose be proportionate to the size of the animal. Small birds and lizards succumb as a rule in a few minutes; guinea-pigs, rabbits, and dogs in less than an hour.

This poison of Amphibia is not septic, but acts upon the heart and the central nervous system. That of the common toad has been compared, in its effects, to that of _Digitalis_ and _Erythrophlaeum_. Some authorities hold that the poison is an acid, others regard it as an alkaloid.

Phisalix[17] has come to the conclusion that toads and salamanders are possessed of two kinds of glands, different both anatomically and physiologically. These are, first the mucous glands, spread over the greater part of the body, with an alkaloid secretion, which acts as a narcotic; secondly, specific glands, as {38}the parotoids and larger dorsal glands, the secretion of which is acid, and acts as a convulsive.

The Indians of Colombia are said to employ the secretion of _Dendrobates tinctorius_ for poisoning their arrows. The poison is obtained by exposing the frog to a fire, and after being scraped off the back is sufficient for poisoning fifty arrows. It acts on the central nervous system, and is used especially for shooting monkeys. Concerning the use of this poison for "dyeing" parrots, see p. 272.

The milky secretion of toads protects them against many enemies, although not always against the grass-snake. A dog which has once been induced to bite a toad, suffers so severely that it will not easily repeat the experiment. The handling of tree-frogs also irritates both nose and eyes. The hind limbs of the Water-frog, _Rana esculenta_, have a very bitter, acrid taste. In short, most, if not all, Amphibia are more or less poisonous, and it is significant that many of the most poisonous, e.g. _Salamandra maculosa_, _Bombinator_, _Dendrobates_, exhibit that very conspicuous combination of yellow or orange upon a dark ground, which is so widespread a sign of poison. Other instances of such warning colours, protective in a defensive sense, are the Wasps and _Heloderma_, the only poisonous lizard.

NERVES

SPINAL NERVES.–Each spinal nerve issues originally immediately behind the neural arch of the vertebral segment to which it belongs. This intra-vertebral position is ultimately modified into a more inter-vertebral one, owing to the predominant share of the neural arches, basidorsalia, in the composition of the whole vertebra. Consequently the nerves issue behind their corresponding vertebra.

The first spinal nerve, or N. suboccipitalis, is exceptional in several respects. It develops a dorsal and a ventral root like a typical spinal nerve, but the dorsal root soon degenerates in all Amphibia, while in the Phaneroglossal Anura the whole nerve disappears. The first spinal nerve reduced to its ventral half persists therefore only in the Apoda, Urodela, and the Aglossal Anura. It issues originally between the occiput and the atlas, but in the adult it is partly imbedded in the anterior portion of the atlas. Its own vertebra is lost, having probably been added to the cranium.

{39}In the Urodela the first spinal nerve either remains separate, or it joins the second spinal, forming with it and with a branch from the third nerve the cervical plexus, which supplies the muscles of the cervical region. The third, fourth, and fifth nerves, and sometimes also the sixth, form the brachial plexus.

In the Aglossal Anura N. spinalis I. mostly sends a fine thread to the second spinal nerve, the rest supplies chiefly the M. levator scapulae, in _Pipa_ the abdominal muscles also. In all the other Anura this N. spinalis I. is lost; occasional vestiges have been reported in _Bufo vulgaris_ and _Rana catesbiana_, and remnants of it may possibly be found in Pelobatidae and Discoglossidae. The first actually persisting nerve of the Phaneroglossa is consequently N. spinalis II.

The brachial plexus is composed as follows:–_Pipa_, N. spinalis II. and III.; _Xenopus_ and Phaneroglossa, N. spinalis III. and IV., with a small branch from the second; the next following three nerves, numbers V., VI., and VII., behave like ordinary trunk nerves.

The pelvic plexus of the Phaneroglossa is formed in _Rana_ by the VIII. + IX. + X. + XIth nerves, the tenth issuing between the sacral vertebra and the coccyx. In _Bufo_ and _Hyla_ the plexus is composed of five nerves, the seventh spinal sending a branch to it. Occasionally the twelfth nerve contributes a small branch to the posterior portion of the plexus. This and the eleventh nerve leave the coccyx by separate holes, thereby indicating its composition. The rest of the spinal cord gives off no more recognisable nerves, owing to its reduction during the later stages of metamorphosis; its terminal filament passes out of the posterior end of the coccygeal canal.

Concerning the CRANIAL NERVES it is necessary to draw attention to one point only. The last nerve which leaves the cranium of the Amphibia is the vagus or tenth cranial nerve. There is consequently no eleventh, and no twelfth or hypoglossal, pair of cranial nerves. Their homologues would be the first and second spinal nerves, but the whole tongue of the Amphibia, with its muscles, is supplied by the glossopharyngeal, or ninth cranial pair, and is morphologically not homologous with the tongue of the Amniota.

{40}RESPIRATORY ORGANS

A very important and characteristic feature of the Amphibia is the development of two sets of respiratory organs: Gills and Lungs. It is as well to give definitions of these organs. _Lungs_ are hollow evaginations from the ventral wall of the pharynx, and their thin, vascularised walls enable the blood to exchange, by osmosis, carbon dioxide for oxygen from the air which enters the lungs by the mouth or the nostrils, and the windpipe. The latter is unpaired, the lungs themselves are paired. _Gills_ are highly vascularised, more or less ramified excrescences, covered by a thin epithelium of ecto- or endo-dermal origin, which permits of the exchange of carbon dioxide for oxygen from the air which is suspended in the surrounding water. It is obvious that this definition applies to all sorts of well-vascularised organs whose thin surface comes into contact with the water. Various recesses of the pharyngeal cavity, the dorsal and ventral folds of the tail-fin, nay, even any part of the skin of the body can, and does occasionally, assume additional respiratory functions. The proper definition of gills, in Vertebrates, requires, therefore, the restriction that they must be developed upon and carried by visceral arches.

The general statement that the Amphibia breathe by lungs, and, at least during some stage of their life, also by gills, requires various restrictions. As a rule the majority of Amphibia first develop gills, later on also lungs, whereupon, during the metamorphosis, the gills are gradually suppressed, so that the perfect animal breathes by lungs only (see p. 61). But a number of Urodela retain their gills throughout life, although the lungs are also functional. These are the Perennibranchiata, not a natural group, but a heterogenous assembly, Proteidae and Sirenidae. Some species of _Amblystoma_ remain individually Perennibranchiate (cf. Axolotl, p. 112). On the other hand, in some Anura the gills are almost or entirely suppressed, or restricted to the embryonic period only. Lastly, a considerable number of Salamandridae have lost their lungs; they breathe by gills until their metamorphosis, but have in the adult state to resort to respiration by the skin (cf. p. 46).

The general plan of the development of the branchial respiratory apparatus is as follows:–The six visceral arches, {41}namely, the mandibular, the hyoidean, and the four branchial arches, correspond, long before they are cartilaginous, with four main arterial arches of the truncus arteriosus. The first, the arteria hyo-mandibularis, belongs to the hyoidean and mandibular segments, the second to the first branchial, the third to the second branchial, while the fourth soon splits in two for the third and fourth or last branchial arch. On the dorsal side these branchial arterial arches combine to form the radix of the dorsal aorta. These arches, especially the three branchials, appear in newts, less clearly in frogs, as transverse ridges on the sides of the future neck. Between the arches the pharynx gradually bulges out in the shape of five lateral gill-pouches; the first between the mandibular and the hyoidean arch, the second between the hyoidean and the first branchial arch, etc. These pouches soon break through to the outside and become gill-clefts, except the first pouch in Urodela. _Before_ the breaking through of the clefts there appears upon the outside of the middle of the rim of each arch a little knob, which soon ramifies and forms an external gill. The knob owes its origin to the development of a blood-vessel which buds from the arterial arch, ramifies and breaks up into capillaries, and returns a little further dorsalwards into the arch. A secondary loop to the outside of the primary arterial arch is thus formed; and whilst this outer loop sprouts out further, driving before it the likewise proliferating skin, and thus producing the gill, the middle portion of the primary arch remains in the Urodela as a short cut, but in the Anura it partly obliterates, and henceforth acts as the internal _efferent_ vessel of the gill. When, during metamorphosis, the gills disappear, their intrinsic _afferent_ and _efferent_ vessels vanish likewise, and the short cut completes the circuit. In order to do this they have, in the Anura, to form new connections with the trunks of the afferent vessels.

The arterial arches themselves are modified as follows:–The first pair become the carotids, the second form the right and left aortic arches, while the third and fourth unite and are transformed into the pulmonary arteries and "ductus Botalli," the last arterial arch having previously sent a branch into the developing lungs. In the Anura the third arch obliterates.

The gills and clefts present various modifications. The Urodela possess three pairs of gills, one each upon the dorsal {42}half of the three branchial arches, just near the upper corners of the clefts; and the skin of the body is continued upon the stem of each gill, pigmented like the rest of the surface of the body. Such a gill is more or less like a blade, standing vertically, and is composed of a stem of connective tissue, thick at the base, and, as a rule, carrying two series of fine lamellae, which, however, do not form two opposite series, but hang downwards, being, so to speak, folded down, so that the upper surface of the stem is bare, and carries the lamellae on its under side. In the Axolotl some of these lamellae are further subdivided. In _Necturus_ they are enormously increased in numbers, but are rather short, and they stand no longer in two rows, but are crowded into one. Those of _Proteus_ form two rows of dendritic filaments; those of _Siren_ are likewise much ramified.

The larvae of the Urodela have four clefts. In the adult _Siren_ these are reduced to three, the first, namely, that between the hyoid and the first branchial arch, being closed up. In _Necturus_, _Proteus_, and _Typhlomolge_ the clefts are further reduced to two, owing to the closing up of the first and last, only those between the first, second, and third arches remaining. _Amphiuma_, and usually _Cryptobranchus alleghaniensis_, possess only one pair of clefts, while in _C. japonicus_ and in the Salamandridae all the clefts are abolished.

The gills of the Urodela are always uncovered, although a short operculum is formed from the posterior margin of the hyoidean arch; the halves of this fold meet below the throat, and persist in various terrestrial and aquatic species as the "gular fold." It reaches its greatest size just before metamorphosis, but scarcely ever produces a proper outer gill-chamber, and it does not cover the gills owing to their rather pronounced dorsal position. It is perhaps best developed in _Typhlomolge_, and even there its dorsal portion is continued upon the first of the three broad vertical and short-fringed blades which form the gills.

A description of the gills of the Apoda will be found in the systematic part.

In the Anura the gills are complicated, owing to the development of the so-called internal gills. First appear, exactly in the same way as in the Urodela, the external gills, one upon each of the first three branchial arches. In the larva of _Rana esculenta_, 5 mm. in length, a little protuberance appears upon the first, {43}and then upon the second arch. In the 6 mm. larva the first gill shows four knobs, the second two, the third one knob. They are always delicate and thin, although sometimes pigmented, long, and much-ramified structures. The first pair is always the largest; well developed and persisting a long time in _Rana temporaria_; smaller in _R. esculenta_ and _Bufo vulgaris_; very short, scarcely forked, in _B. viridis_ and _Hyla arborea_. They are relatively largest in _Alytes_, while still in the egg. Numerous descriptions of these gills will be found in the systematic part.

Great changes take place about the time when the fourth or last branchial arch and the pulmonary arteries are developed. This occurs in _R. esculenta_ when the larva is about 9 mm. long. The sprouting of the gills extends gradually downwards along the arches upon their ventral halves, and these new gill-filaments or loops transform themselves into numerous dendritic bundles, resting in several thickset rows upon the hinder margin of the first to the third arch, one row only on the fourth arch, which carries no external gill. These "internal gills" look like red bolsters or thick and short-tasselled bunches. Whilst they are developing the dorsal, older gills become arrested in their growth and disappear, and at the same time a right and left opercular fold grows out from the head and covers these new gills, shutting them up in an outer branchial chamber, just like that of Teleostei and other Tectobranch fishes. This is the reason why these new gills have been called internal, and the mistaken notion has sprung up that they are comparable with the true internal gills of fishes. In reality Amphibia have only external gills. They are always covered by ectoderm, are restricted to the outside of the branchial arches, and are developed before the formation of the clefts. These gills are in many cases directly continuous with the more dorsally and more superficially placed earlier external gills; but although nearly every one who has studied their development has observed this agreement, the old error still prevails. They are morphologically as little internal as the true internal gills of Elasmobranch embryos are external gills, because these have become so elongated that they protrude out of the gill-clefts.

The fact that the Amphibia possess only external gills throws important light upon their phylogeny. Not only do the Apoda, Urodela, and Anura agree much more with each other than {44}would be the case if the Anura possessed both internal and external gills, but the Amphibia reveal themselves also in this point as connected with the Crossopterygii and the Dipnoi, some of which fishes also possess external gills. It is of course quite possible that the Amphibia have developed these organs independently, but we understand now that the latter are accessory, and not the primitive respiratory organs; they are developed in adaptation to embryonic conditions and to prolonged larval, occasionally perennibranchiate, aquatic life (cf. the chapter on Neoteny, p. 63).

There is no valid reason for supposing that the Stegocephali had true internal gills. We know their branchial skeleton, and we can discern even gill-rakers on the arches. Such gill-rakers occur also, although but feebly developed, in Urodela. The whole branchial framework of the Urodela and Apoda undergoes simple reductions during metamorphosis (see p. 86), but in the Anura these arches are in early tadpole life transformed into a most complicated basket-work which acts as a straining apparatus or filter, to prevent any particle of food or other foreign matter from finding its way into the delicate gills, the current of water passing from the mouth through the filter, past the gills and out of the clefts. During metamorphosis this whole elaborate apparatus is again transformed, almost beyond recognition, into the hyoidean apparatus for the support of the generally very movable and much-specialised tongue. The fact that the hyoid apparatus of the Aglossa, especially that of _Xenopus_, is constructed upon the same lines, is a strong indication that these creatures have arrived at their tongueless condition through the loss of this organ, and this is intelligible in correlation with their absolutely aquatic life.

The opercular folds assume great dimensions in all tadpoles. They cover the whole gill-region, thereby producing on either side an outer gill-chamber. The posterior margins of the folds gradually become continuous with the rest of the surface of the body. Each gill-chamber opens at first by one lateral canal, usually called the spiracle. This condition prevails in the tadpoles of the Aglossa. In the Discoglossidae the two canals gradually converge and combine into one median opening on the middle of the belly. In all the other Anura the right opening becomes closed, or rather its canal passes over to and joins that of the {45}left side, both opening by one short tube laterally on the left side, at a variable distance between the eye and the vent. Hence the elegant terms of Amphi-, Medio-, and Laevo-gyrinidae (γυρῖνος being the Greek for tadpole).

The external gills lead to a further consideration. _Protopterus_ possesses a vestigial external gill on the shoulder-girdle. _Lepidosiren_ has them on the gill-arches, resembling piscine internal gills, and _Polypterus_ has a large biserially fringed external gill (in some cases not disappearing until the fish is adult), which starts from the mandibular arch, at the level of the spiracle or first visceral cleft, and overlaps the operculum externally. The axis of this peculiar organ is possibly based upon the homologues of the spiracular cartilages, which themselves are the branchiostegal rays of the dorsal half of the quadrato-mandibular arch. The branchiostegal rays of the hyoidean arch, at least their material, have given rise to the elaborate opercular apparatus; and, in conformity herewith, the hyomandibular itself is not known to carry a gill. Quite possibly the large external gill of _Polypterus_ is not serially homologous with other external gills–it may not be a true gill at all, it has perhaps quite a different function–but it seems to throw light upon a mysterious pair of organs which are common in larval and young Urodela, in the larval Aglossa and in the Apoda. These are the "balancers."

In _Triton taeniatus_, before hatching, there appears a little protuberance behind and below the eye; it rests upon the angle of the mandibular arch, and is separated from the first transverse, externally visible ridge of the first branchial arch by the beginnings of the hyoidean arch. A few days later the arteria hyomandibularis sends a vessel into this knob, forms a vascular coil, and leaves it as a vein which, instead of returning into the arterial arch, passes into the veins of the body. Its epithelium is not covered with flat, but with cubical cells; and sensory cells have not been found in it. These organs attain some size, and are shaped like rods, with thickened ends; they are movable, and are used by the larvae as "balancers," keeping the head from sinking into the slime at the bottom. But they may have other functions besides, and it is not unlikely that they develop into sensory organs like feelers. They occur in many Salamandridae, and are not reduced until, or even after, the metamorphosis, and during this time they shift their place with relation to the eye and the mouth.

{46}The same kind of organs occur in _Amblystoma_.[18] They appear, previous to the breaking open of the gill-clefts, as protrusions of epiblast, long before any of the external gills on the branchial arches. When the clefts have broken open, the quadrate sends out laterally a tiny crescent-shaped process a little above the jaw-joint, and this process extends to the base of the balancer, but not into it, and a bundle of muscle-cells grows into the balancer. It is easy to recognise the same organ in the extremely long thread-like structures of the larva of _Xenopus_. In the Apoda they are likewise present, but are retained permanently as highly specialised, probably tentacular organs (cf. p. 86, Apoda).

One of the most unexpected features is the SUPPRESSION OF THE LUNGS in various kinds of Salamandridae. The lungs are either reduced to useless vestiges or they are quite absent. This occurs in aquatic and terrestrial, American and European forms, and it is noteworthy that the reduction of the lungs does not apply to all the species of the various genera, nor is it restricted to one sub-family.

The following list is due to the researches of H. H. Wilder,[19] L. Camerano,[20] E. Lönnberg,[21] and G. S. Hopkins[22]:–All the Desmognathinae and Plethodontinae; Amblystomatinae, _Amblystoma opacum_; Salamandrinae, _Salamandrina perspicillata_. In _Triton_ and other Salamandrinae the length of the lungs varies; in some they extend more, in others less, than half way down the distance between head and pelvis. Hopkins remarks: "Two questions are naturally suggested by this apparently aberrant condition of the respiratory organs. First, what structures or organs have taken on the function of the lungs and branchiae; and secondly, is there any modification in the form or structure of the heart which in any way may be correlated with the above-mentioned peculiarities of the lungless forms?" Wilder concluded that respiration was probably carried on by the skin, and perhaps, to some extent, by the mucosa of the intestine. Camerano thinks that, at least in the European forms, respiration is effected by the bucco-pharyngeal cavity, and that the skin affords no efficient aid. The left auricle in the lungless forms is much {47}smaller in comparison than the right, and there is no pulmonary vein. The auricular septum has a large aperture, the communication between the auricles being larger than even in _Necturus_ (which breathes essentially by gills). The sinus venosus, instead of opening into the right auricle only, opens more freely into the left than into the right, and the latter communicates more directly with the ventricle than the left, instead of about equally. In short, the heart of these creatures appears almost bilocular, instead of being trilocular, at least functionally.

The lungs of the Urodela are always simple, extremely thin-walled bags. They are highly developed in the Anura, the walls being modified into numerous air-cells, whereby the respiratory surface is considerably increased. The lungs are filled with air by the pumping motion of the throat while the mouth is closed, the nostrils being provided with muscular valves. A muscular apparatus assists the filling of the lungs in the Anura.[23]

Most, if not all, Anura and some Urodela have a VOICE produced by the larynx, which, especially in the Anura, is provided with a complicated cartilaginous and muscular apparatus and with vocal cords. The voice of the Urodela is at the best a feeble squeak. The females of the Anura are either mute or they produce a mere grunt, but that of many males is very loud, and, moreover, in many species it is intensified by _vocal sacs_ which act as resonators. These sacs are diverticula of the lining of the mouth-cavity, and bulge out the outer skin and the muscles, chiefly the mylo-hyoid, of the throat. The nostrils and the mouth are firmly closed during the croaking. "The sacs are called internal when they are covered by the unmodified gular integument, however much this may be distended; external when their membrane projects through slits at {48}the sides of the throat, as in _Rana esculenta_ (Fig. 52, p. 269), or when the skin is thinned and converted into a bladder-like pouch, as in _Hyla arborea_."[24] These sacs exhibit many modifications. They may be unpaired and median, and open by two slits into the mouth, on either side below the tongue; in _Bufo_ one of the slits or openings, either the right or the left, is obliterated. They may be paired and symmetrical, and open one on each side of the head, below and near the posterior angle of the jaws. These modifications differ in closely allied species. They reach their greatest complication in _Rhinoderma_ and in some of the Cystignathidae by extending far back beneath the skin into the wide lymphatic spaces. In _Rhinoderma_ they are put to the unique use of nurseries for the young (see p. 228). _Leptodactylus typhonius_ has a very distinct pair of outer vocal sacs and a well-marked unpaired sac which extends into the belly and communicates with each outer sac. Several species of _Paludicola_, e.g. _P. fuscomaculata_ and _P. signifera_, have a similar arrangement, in addition to an unpaired gular sac which can be inflated independently of the rest (see Fig. 45, p. 220).

URINO-GENITAL ORGANS

The kidneys and the male generative glands are still intimately connected with each other. The general plan is as follows:–

The kidneys consist of a large number of glomeruli, produced by the coiled segmental tubes, each of which is composed of a nephrostome or funnel opening into the body-cavity, a Malpighian body and an efferent canal. The latter combine to form the segmental duct which opens into the cloaca. The testes, composed of a large number of sperm-producing glands, are drained by transverse canals which combine into a longitudinal canal, and this again sends off numerous efferent canals which open into the efferent canals of the kidney, so that the segmental duct (Leydig's duct of many authors) conveys both sperma and urine.

{49}

{50}In the female the network of transverse and longitudinal canals, which originally connect the generative glands with the kidney's efferent canals, is deduced in so far as the connection is interrupted and the vestiges of the transverse canals are no longer functional. The eggs fall into the body-cavity and are caught up by the ostium or inner abdominal opening of a special duct, the oviduct (Müllerian duct of many authors). Vestiges, more or less complete, of these oviducts persist in the males of most Amphibia.

This general scheme presents some modifications in the various groups of Amphibia.

The Apoda retain the most primitive conditions. The kidneys are still long and narrow, and the glomeruli are, at least in the anterior part of the organ, still strictly segmental, agreeing in number and position, each with a vertebral segment; later, the number of the glomeruli is greatly increased, and the former agreement becomes quite disturbed. The generative glands still retain their segmental arrangement, but they are restricted to a much shorter region than the kidneys. In the male Apoda a considerable portion of the cloaca can be everted by special muscles, and acts as an intromittent organ. Both sexes possess a ventral urinary bladder.

In the Urodela both kidneys and testes are much concentrated, the testes especially have lost all outward appearance of segmentation, and their efferent canals, connecting them with the longitudinal collecting canal, are much reduced in numbers. The greater portion of the kidneys, at least their anterior half, has all the appearance of a degenerating organ and is on the way to losing its urinary function, although it still possesses Malpighian bodies and complete ducts; the main function of the latter is now the conveyance of the sperma. In the Perennibranchiata, and in some others, e.g. _Spelerpes variegatus_, the longitudinal collecting canal, between testis and kidney, is sometimes suppressed, a very simple, but pseudo-primitive arrangement. A urinary bladder is present. The cloaca is not eversible.

In most Anura, e.g. _Rana_ and _Bufo_ (Fig. 7; 4, 5), the same scheme is adhered to. The efferent canals of the testis form a network, with a longitudinal canal, and open into the efferent canals of the kidney, in the substance of which they are more or less deeply imbedded. The ducts which lead out of the kidney to compose Leydig's duct, are frequently dilated, or the latter duct is much elongated, convoluted or varicated, and this whole portion is enclosed in a sheath of connective tissue, giving an {51}appearance as if the single duct itself were dilated in the greater part of its length; hence the occasional name of vesicula seminalis. Such means of storing the sperma enable the latter to be ejected suddenly in great quantities.

In _Bombinator_ (6) some of the most anterior seminal canals do not perforate the kidney, but run over it superficially and open directly into a branch of Leydig's duct. This branch, no doubt equivalent to a number of segmental canals which have lost their uriniferous function, is curved round the upper end of the permanent kidney, while its forward continuation, ending blindly, is the remnant of its former headward extension. This arrangement of _Bombinator_ is carried further in _Discoglossus_ (7). The testis conveys its sperma through a wide duct directly into Leydig's canal, without interfering with the kidney, and all the testicular efferent network is lost. The anterior end of Leydig's duct still extends headwards; its middle portion acts solely as a vas deferens, while the lower portion still behaves like a typical segmental duct, conveying both sperma and urine. Lastly, in _Alytes_ (8) the functional division of the old segmental duct has been carried to an extreme. The kidney is drained by one canal only, now a true ureter, and this is of course produced by a consolidation of the multiple exclusively uriniferous canals of the lower half of the kidney. The whole of the segmental duct is now in the service of the testis, and near its junction with the ureter it forms a large diverticulum or true vesicula seminalis.

Remnants of oviducts, or Müllerian ducts, are common in the male Anura; they are best developed in _Bufo_, much reduced, and individually absent, in _Rana_. In _Bombinator_ each duct is restricted to its upper or abdominal portion, and is attached to the vestigial headward extension of Leydig's duct. Lastly in _Discoglossus_ and in _Alytes_ all traces of oviducts seem to have vanished, at least in the adult males.

It is interesting to note that in the arrangement of the urino-genital ducts the Discoglossidae are the most advanced of all Amphibia, instead of showing the most primitive conditions. This is rather unexpected, but is paralleled by the epichordal type of the vertebral column.

The oviducts of the Apoda and Urodela remain more or less straight; in the viviparous species they form uterus-like dilatations. In the Anura they become greatly elongated during the {52}breeding season and form many convolutions. As a rule each oviduct opens separately into the cloaca, but in _Hyla_ they have one unpaired opening, while in _Bufo_ and _Alytes_ the lower parts of both oviducts are themselves confluent.

All Amphibia possess FAT-BODIES. They consist of richly vascularised lymphatic tissue, the meshes of which are filled with lymph-cells, globules of fat and oil. In the Apoda these bodies lie laterally to the generative glands, and along the posterior half of the kidneys. In the Urodela they accompany the anterior half of the kidney. In the Anura they are lobate, and are placed upon the anterior end of the testes or ovaries. Their exact function is still doubtful, but it is intimately connected with that of the generative glands. The old notion, that they are simply stores of fat for the nourishment of the animal during hibernation, is quite untenable. The fat-bodies do not decrease during this period, on the contrary they attain their fullest size in the spring at the time of the rapidly awaking activity of the reproductive organs, and they enable considerable quantities of sperma and of eggs to be produced and ripened without detriment to, or utter exhaustion of, the animals, which often spawn before they have had time or opportunity to feed. After the spawning season the fat-bodies have dwindled down to inconspicuous dimensions.

Lastly, there is in some Anura, hitherto observed in _Bufo_ only, a mysterious organ, intercalated between the fat-body and the testis or ovary. This is "Bidder's organ" and it seems to be a rudimentary ovary, or rather that upper, anterior portion of the whole organ which undergoes retrogressive metamorphosis. It disappears in old female toads, but in the males it sometimes assumes a size equal to, or surpassing that of the testes. The males are in this respect hermaphrodite, and cases are known in which parts of the generative glands have developed testes and egg-bearing ovaries.

The SPERMATOZOA of the Apoda and Urodela have an undulating membrane along the tail, while the head-end is either pointed or truncated. Those of _Spelerpes fuscus_ and of _Ichthyophis glutinosa_ measure about 0.7 mm. in total length, those of the other Urodela being much smaller. A peculiarity of the Urodela is that their spermatozoa are massed together in or upon spermatophores, an arrangement which undoubtedly facilitates the internal {53}fecundation of the female without actual copulation. The female takes up such a deposited spermatophore with the cloacal lips, squeezes the sperma out of the capsule which remains behind, and either conveys the former into a special receptaculum seminis, _e.g._ in _Salamandra atra_ and in _Triton_, or the spermatozoa wriggle their way, thanks to the undulating tail, directly up the oviducts to the ova.

The spermatophores are composed of a colourless, soft, gelatinous mass, which is probably produced by the cloacal gland. The shell of jelly is in fact a cast of the cloacal cavity, reproducing all its ridges, furrows and folds, while a toad-stool-shaped papilla of the cloaca makes the inside lumen of the cast, _e.g._ in _Triton_. Those of _Salamandra maculosa_ are much simpler, consisting, in conformity with the absence of a cloacal papilla, merely of a cone with a globular mass of sperma on the top. Those of _Amblystoma_ are similar.

The spermatozoa of the Anura show considerable differences in the various genera, of which, however, only the European forms have been properly examined. The "head" is wound like a corkscrew in _Discoglossus_, _Pelobates_, and _Pelodytes_; spindle-shaped, more or less curved, in _Rana temporaria_ and _R. agilis_, _Hyla_, _Bufo_ and _Bombinator_, in the latter with an irregular membrane on one side; cylindrical in _Rana esculenta_ and _R. arvalis_. The tail is mostly long and filiform, but in _Bufo vulgaris_ and _Discoglossus_ it is provided with an undulating membrane. Their size is generally very small, only about 0.1 mm., excepting those of _Discoglossus_ which reach the astonishing length of 3 mm. These differences in shape, especially that of the head, explain why species of the same genus, e.g. _Rana temporaria_ and _R. arvalis_, cannot fertilise each other.

]

The EGGS differ much in size, colour, and numbers. They are holoblastic, with unequal cleavage, but those species which possess an unusual amount of food-yolk, for instance _Rhacophorus schlegeli_ and the Apoda, approach the meroblastic type of segmentation. As a rule, the greater the amount of yolk, the smaller is the number of eggs produced. But the number which is laid {54}during one season is not only difficult to calculate, but it varies individually, old females laying more than young specimens. Moreover, some kinds, _e.g._ the Discoglossidae, spawn several times in one year. _Alytes_, _Rhinoderma_, _Hylodes_, _Rhacophorus_, _Pipa_, in fact those kinds which are remarkable for special nursing habits, lay only a few dozen eggs at a time. _Hyla arborea_ produces up to 1000, _Rana temporaria_ about 3000, _Bufo vulgaris_ averages 5000, _Bufo viridis_ and _Rana esculenta_ up to 10,000 and more. T. H. Morgan[26] has observed a _Bufo lentiginosus_ which laid 28,000 eggs within ten hours! The number of eggs produced by the Apoda and Urodela is comparatively moderate, in the average a few dozen, _Amblystoma_ alone laying about 1000.

The eggs possess a gelatinous mantle of variable thickness and consistency. In _Amphiuma_ they are strung together like the beads of a rosary, and the envelope hardens into a kind of shell. Many Newts and some Anura fasten their eggs singly on to plants and other objects in the water, with or without threads of stiffening mucus. In many Anura, _e.g._ Bufonidae, they pass out as closely-set strings of beads, one string out of each oviduct; in others, _e.g._ Ranidae, they are disconnected, and form large, lumpy masses, especially when the gelatinous mantle swells up in the water. The use of this mantle seems to be chiefly the protection of the growing embryo, which in many species, when hatched out of the egg proper, drops into and remains for some time in the softened jelly. Possibly the latter affords some nutriment to the early larva.

Concerning the mode of FECUNDATION it is to be remarked that copulation proper takes place only in the Apoda. For the Urodela Boulenger[27] has given the following summary. In no case does actual copulation take place. The male deposits the spermatophores which it is the office of the female to secure:–

I. No amplexus, but a lengthy courtship in the water; the male is more
brilliantly coloured than the female, and ornamented with dorsal and
caudal crests, or other appendages: _Triton_, cf. also systematic part.

II. Amplexus takes place; there are no marked sexual differences in
colour and no ornamental dermal appendages.

A. Amplexus of short duration, partly on land, but deposition of the
sperma in the water. No accessory sexual characters: Terrestrial
Salamanders, namely _Salamandra_, _Chioglossa_, _Salamandrina_.
_Spelerpes_ breeds in damp caves without water.

{55}B. Amplexus of lengthy duration and in the water.

_a._ The male, distinguished by a greater development of the
fore-limbs, which are armed with temporary excrescences, clasps the
female in the axillary region with the fore-limbs: _Triton waltli_.

_b._ The male, distinguished by a greater development of the
hind-limbs and a prehensile tail, clasps the female in the lumbar and
caudal regions: The _Euproctus_-group of newts: _Triton asper_, _T.
rusconii_, and _T. montanus_.

The act of fecundation of most of the other kinds of Urodela, notably _Cryptobranchus_, _Amphiuma_, _Proteus_, has not yet been observed.