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, 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 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, 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 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]).