Part 3

Comparing the girdle of a salamander with that of a frog, the closest similarity can be seen between Ascaphus and a salamander in which the scapula and coracoid ossify separately. Both have the median "sternum" in contact with the coracoid plates. The major difference, of course, is the lack of clavicle and cleithrum in the salamander.

CARPUS AND TARSUS

In Ascaphus (Ritland, 1955a; cleared and stained specimens of nearly grown males) distal carpals 1, 2, 3 and 4 are present and separate, increasing in size in the order given (Fig. 9). A prepollex rests against centrale 1; centralia 2 and 3 are fused; the radiale fuses with centrale 4, and the intermedium fuses with the ulnare; radius and ulna are fused with each other as in other frogs. The digits (and metacarpals) are considered by Ritland to be 1-4, in addition to the prepollex, rather than 2-5.

In the Jurassic Notobatrachus Stipanicic and Reig (1956) have shown the carpus with surprising clarity (Fig. 9). If their nomenclature of the parts be revised, we obtain a fairly close resemblance to Ascaphus, except that centralia 2 and 3 are not fused, distal carpals 1 and 2 do not show (which would easily be understood if they were of the size of those in Ascaphus, or not ossified), and the intermedium remains separate from the ulnare.

In Salamandra (Francis, 1934; Nauck, 1938) distal carpals 1 and 2 are fused in both larva and adult, and 3 and 4 are separate; the radiale, intermedium and ulnare are separate in the larva but the latter two fuse in the adult; centrale 1 (labelled prepollical cartilage by Francis) and centrale 2 are separate. Francis considers the digits (and metacarpals) to be 1-4. Apparently the arrangement here indicated for the larva is characteristic of other larval salamanders, except where further reduced, and reduction below the number given for the adult is common in other terrestrial forms. The radius and ulna are, of course, separate.

The ossification of carpals is more likely to be complete in adult frogs than in salamanders, but some ossification of all parts named is found in several of the latter. A common ancestor of frogs and salamanders could be expected to have the following elements present and ossified in the adult: distal carpals 1-4 separate; 3 centralia; radiale, intermedium and ulnare separate. Comparison with fossils older than Notobatrachus is fruitless on these points, unless we go back to forms too distant to have any special value, such as Eryops. This is because of inadequate preservation and because the elements are not fully ossified in many immature specimens.

For the purpose of this review there is no special value in a comparison of the tarsi of frogs and salamanders, since the leaping adaptation of the former leaves very little common pattern between them. Even in Protobatrachus, where the legs were not yet conspicuously lengthened, the tibiale and fibulare ("astragalus" and "calcaneum" respectively) were already considerably elongated. The carpus and tarsus of Amphibamus are as yet undecipherable.

THE LARVA

Considering the postembryonic developmental stages of modern Amphibia, there can be no doubt that a gill-bearing, four-legged larva of a salamander, in which lateral line pores and a gular fold are present, represents much more closely the type of larva found in labyrinthodonts than does the limbless, plant-nibbling tadpole of the Anura. Salamander-like larvae of labyrinthodonts are well known, especially those formerly supposed to comprise the order Branchiosauria. Many, perhaps the majority of, labyrinthodonts show some features associated with aquatic life even when full-grown, as do the lepospondyls. These features may include impressions of sensory canals on the dermal bones of the skull, persistence of visceral arches, reduction in size of appendages, and failure of tarsal and carpal elements to ossify. In fact, it appears that very few of the Paleozoic Amphibia were successful in establishing themselves as terrestrial animals even as adults.

Nevertheless, in the ancestry of Anura, and that of at least the Hynobiid, Ambystomid, Salamandrid and Plethodontid salamanders, there must certainly have been a terrestrial adult, transforming from an aquatic larva. The leaping mechanism of Anura, shown in so many features of their anatomy, is perhaps to be explained as a device for sudden escape from land into the water, but it was not yet perfected in the Triassic Protobatrachus or the Jurassic Notobatrachus.

The middle ear, its sound-transmitting mechanism, and the tympanum, well developed in most Anura, are readily derived from those of early labyrinthodonts, and are presumably effective for hearing airborne sounds whether on land or while floating in the water. Reduction of these organs in Urodela may be correlated with their customary restriction to subsurface habitats and inability to maintain a floating position while in water.

Some light may be shed on the significance of the tadpole of Anura by considering the early stages of the ribbed frogs, Liopelmidae. Leiopelma and Ascaphus are so closely similar in the adult that there is no doubt that they belong in one family, primitive in some respects (including articulated ribs; pyriformis and caudalipuboischiotibialis muscles) but not in others (absence of tympanum and middle ear). In both genera the eggs are large, 5 mm. in Leiopelma, 4.5 mm. in Ascaphus, and unpigmented; but at this point the resemblance ends.

Stephenson (1955) showed that embryos of L. hochstetteri develop equally well on land (in damp places) or in the water, and that embryos prematurely released from egg capsules develop successfully in the water. The larvae possess both pairs of legs (Fig. 10) and a broad gular fold similar to that of larval salamanders. In L. hochstetteri the fold grows back over the forelegs temporarily, but remains free from the body and presently the legs reappear, whereas in L. archeyi the forelegs are not covered at any time. No branchial chamber or spiracle is formed. Of course direct development, without a tadpole, occurs in several other groups of Anura, but in each case terrestrial adaptations are obvious. This is not true of Leiopelma, which Stephenson regards as more nearly comparable with Urodela in its development than with other Anura, and he sees in it a "primary and amphibious" mode instead of a terrestrial specialization.

The Ascaphus tadpole bears no outward resemblance to the larva of Leiopelma, but is a normal tadpole in form, although sluggish in activity. Its greatly expanded labial folds bear numerous rows of horny epidermal "teeth," which, with the lips, serve to anchor the tadpole to stones in the swift water of mountain brooks. Noble (1927) noticed that particles of food were taken in through the external nares, and that a current of water passed through these openings and out by way of the median spiracle. It appears that any action by the teeth and jaws in scraping algae from the rocks (which were bare in the stream where I have collected Ascaphus) would be quite incidental, and that the lips and teeth must be primarily a clinging mechanism. Certain other mountain brook tadpoles (for example, Borborocoetes) show similar devices, but these are developed independently, as specializations from the usual sort of tadpole.

May it not be that closure of the gill-chamber by the opercular (=gular) fold, retardation of limb development, expansion of the lips, growth of parallel rows of horny teeth, and other correlated features that make a tadpole, were brought about as an adaptation of the primitive Anuran larva to a swift-stream habitat, and that this "basic patent" then later served to admit the tadpoles of descendant types to an alga-scraping habit in quiet water as well? The tadpole, as a unique larval type among vertebrates, bears the hallmarks of an abrupt adaptive shift, such as might have occurred within the limits of a single family, and it seems difficult to imagine the enclosed branchial chamber, the tooth-rows, and lips of a familiar tadpole as having evolved without some kind of suctorial function along the way.

SUMMARY

The Anura probably originated among temnospondylous labyrinthodonts, through a line represented approximately by Eugyrinus, Amphibamus, and the Triassic frog Protobatrachus, as shown by Watson, Piveteau and others. The known Paleozoic lepospondyls do not show clear indications of a relationship with Urodela, but Lysorophus may well be on the ancestral stem of the Apoda.

Between Urodela and Anura there are numerous resemblances which seem to indicate direct relationship through a common stock: (1) a similar reduction of dermal bones of the skull and expansion of palatal vacuities; (2) movable basipterygoid articulation in primitive members of both orders; (3) an operculum formed in the otic capsule, with opercularis muscle; (4) many details of cranial development, cranial muscles, and thigh muscles, especially between Ascaphus and the Urodela, as shown by Pusey and Noble; (5) essentially similar manner of vertebral development, quite consistent with derivation of both orders from Temnospondyli; (6) presence in the larva of Leiopelma of a salamander-like gular fold, four limbs, and no suggestion of modification from a tadpole (Stephenson).

LITERATURE CITED

Broom, R.

1918. Observations on the genus Lysorophus Cope. Ann. Mag. Nat. Hist., (9)2:232-239.

Bystrow, A. P.

1938. Dvinosaurus als neotenische Form der Stegocephalen. Acta Zool., 19:209-295.

Case, E. C.

1935. Description of a collection of associated skeletons of Trimerorhachis. Contrib. Mus. Pal. Univ. Michigan, 4:227-274.

Cope, E. D.

1889. The Batrachia of North America. Bull. U. S. Nat. Mus., 34:1-525.

de Beer, G. R.