Part 2

Abbreviations Used in Figures

b'd.c.--basidorsal cartilage (neural arch) b'oc.--basioccipital ce.{1-4}--centrale{1-4} ch.--ceratohyal clav.--clavicle clei.--cleithrum cor.--coracoid d.c.{1-4}--distal carpal{1-4} diap.--diapophysis exoc.--exoccipital ep.--episternum hyost.--hyostapes i.--intermedium Mk.--Meckel's cartilage n.--notochord om.--omosternum op.--operculum opis.--opisthotic par.--parietal par. proc.--paroccipital process peri. cent.--perichordal centrum p'p.--postparietal prep.--prepollex pro.--prootic p'sp.--parasphenoid pt.--pterygoid p.t.f.--post-temporal fossa postzyg.--postzygapophysis qj.--quadratojugal qu.--quadrate ra.--radiale r.hy.--hyomandibular ramus of VII rib-b.--rib-bearer r.md.--mandibular ramus of VII sc.--scapula sc'cor.--scapulocoracoid s'd.--supradorsal cartilage s'd.(postzyg.)--supradorsal (postzygapophysis) soc.--supraoccipital sp.c.--spinal cord sq.--squamosal s'sc.--suprascapula s't.--supratemporal sta.--stapes ster.--sternum tab.--tabular uln.--ulnare v.a.--vertebral artery xiph.--xiphisternum I,IV--digits I and IV V, VII, X, XII--foramina for cranial nerves of these numbers (in Fig. 4, VII is the facial nerve) ]

In temnospondylous Amphibia the tympanum generally occupied an otic notch, at a high level on the skull, bordered dorsomedially by the tabular and ventrolaterally by the squamosal. In this position the tympanum could receive airborne sounds whether the animal were entirely on land or lying nearly submerged with only the upper part of its head exposed. Among those Anura in which the ear is not reduced the same is true, except that the tabular is lost. In Temnospondyli (Fig. 3) the posterior wall of the otic capsule was usually formed by the opisthotic, which extended up and outward as a buttress from the exoccipital to the tabular, and sometimes showed a paroccipital process for the insertion, presumably, of a slip or tendon of the anterior axial musculature. The stapes, in addition to its foot in the fenestra ovalis and its tympanic or extrastapedial process to the tympanum, bore a dorsal process (or ligament) to the tabular, an "internal" process (or ligament) to the quadrate or an adjacent part of the squamosal, and a ligament to the ceratohyal. Some of these attachments might be reduced or absent in special cases, but they seem to have been the ones originally present both phylogenetically and embryonically in Amphibia.

Among typical frogs (Fig. 4) the base, or otostapes, is present and bony, the extrastapedial process (extracolumella, or hyostapes) is usually cartilaginous, the dorsal process (processus paroticus) is of cartilage or ligament, but the other two attachments are absent in the adult. The exoccipital extends laterally, occupying the posterior face of the otic capsule. Between it and the otostapes is a small disc, usually ossified, the operculum, which normally fits loosely in a portion of the fenestral membrane, and is developed from the otic capsule. The opercularis muscle extends from this disc to the suprascapula, in many but by no means all families of Anura.

Among Urodela (Fig. 4) the middle ear cavity and tympanum are lacking, and the stapes (columella) consists of no more than its footplate and the stylus, which is attached to the border of the squamosal, thus corresponding to the "internal" process. In families in which individuals metamorphose and become terrestrial (Hynobiidae, Ambystomidae, Salamandridae, Plethodontidae), an operculum and opercularis muscle appear in the adult, just as in frogs, except that in Plethodontidae, the most progressive family, the operculum fuses with the footplate of the stapes. Among neotenous or perennibranchiate urodeles there is no separate operculum or opercularis. The evidence given by Reed (1915) for fusion of the operculum with the columella in Necturus appears inconclusive, in spite of the great care with which his observations were made. On the other hand, Necturus and Proteus alone among living salamanders have a distinct opisthotic on the posterior wall of the otic capsule (Fig. 3), as do the Cretaceous Hylaeobatrachus and the Eocene Palaeoproteus. Probably these Proteidae should be regarded as primitive in this respect, although many other features may be attributed to neoteny.

There is a contrast between Anura and most Urodela in the relative positions of the stapes and facial nerve, as shown in DeBeer's (1937) diagrams. In the latter (Ambystoma) the nerve is beneath, and in the former (Rana) above, the stapes. Judging by figures of Neoceratodus, Hypogeophis, and several types of reptiles and mammals, the Urodela are exceptional. Necturus, however, has the nerve passing above its stapes, and this may be primitive in the same sense as the persistent opisthotic. There can be, of course, no question of the nerve having worked its way through or over the obstructing stapes in order to come below it in salamanders; rather, the peripheral growth of neuron fibers in the embryo must simply pursue a slightly different course among the partially differentiated mesenchyme in the two contrasting patterns.

Although DeBeer (1937) shows in his figure of Hypogeophis (one of the Apoda) an operculum, this is apparently a mistake. The stapes has a large footplate, and its stylus articulates with the quadrate, but no true operculum or opercularis has been described in the Apoda. The facial nerve passes above the stapes. It does not seem necessary to regard the conditions in this order as related directly to those of either salamanders or frogs, but a reduction of the stapes comparable to that in salamanders has occurred.

The presence in both frogs and terrestrial salamanders of a special mechanism involving the opercularis muscle and an operculum cut out in identical fashion from the wall of the otic capsule behind the stapes seems to require some other explanation than that of a chance convergence or parallelism. Although the stapes and otic region are readily visible in a number of labyrinthodonts and lepospondyls, no indication of an operculum seems to be reported among them. But in the Triassic Protobatrachus (Fig. 1), which is unmistakably a frog in its skull, pelvis and some other features, Piveteau (1937) has shown, immediately behind the foot of the stapes, a small bony tubercle, which he and Watson (1940) designated opisthotic. Very clearly it served for insertion of a muscle, and it is equally clear that the bone is a reduced opisthotic, carrying the paroccipital process already mentioned as characteristic of it in some temnospondyls. Since the remainder of the posterior wall of the otic capsule consists of cartilage, meeting the exoccipital, it may be that the opisthotic becomes the operculum in frogs. Protobatrachus was too far specialized in the Anuran direction, although it still had a tail, and the forelegs and hind legs were nearly the same size, to be considered a possible ancestor of the Urodeles. But at one stage in the general reduction of the skull in the ancestry of both groups, a condition similar to that in Protobatrachus may have characterized the otic region, long before the Triassic.

In the argument thus far we have considered terrestrial, adult amphibians, since it is only in these that either the normal middle ear and tympanum, or the opercular apparatus, is present. But among the urodeles several neotenic types occur (this term applies also to the perennibranchs). For most of these there is nothing about the otic region that would be inconsistent with derivation, by neoteny, from known families in which adults are terrestrial; for example, Cryptobranchus could have had a Hynobiid-like ancestor. But this, as mentioned above, does not hold for the Proteidae, which possess an opisthotic of relatively large size, distinctly separate from the exoccipital and prootic. Either this bone is a neomorph, which seems improbable, or there has not been in the ancestry of this particular family an episode of reduction comparable to that seen in the terrestrial families, where there is an operculum instead of a normal opisthotic. Therefore the Proteidae probably are not derived from the general stem of other salamanders, but diverged sufficiently long ago that the bones of the otic region were reduced on a different pattern. They need not be removed from the order, but, in this respect, recognized as more primitive than any other existing Urodela or Anura. A recent paper by Hecht (1957) discusses many features of Necturus and Proteus, and shows that they are remote from each other; his evidence does not seem to prove, however, that they were of independent origin or that they need be placed in separate families.

VERTEBRAE AND RIBS

Development of the vertebrae and ribs of Recent Amphibia has been studied by Gamble (1922), Naef (1929), Mookerjee (1930 a, b), Gray (1930) and Emelianov (1936), among others. MacBride (1932) and Remane (1938) provide good summaries. In this section reference will be made to the embryonic vertebral cartilages by the names used for them in these studies, although the concept of "arcualia" is currently considered of little value in comparative anatomy.

The centrum in Anura (Fig. 5) is formed in the perichordal sheath (Rana, Bufo) or only in the dorsal portion thereof (Bombinator, Xenopus). The neural arch develops from the basidorsal cartilages that rest upon, and at first are entirely distinct from, the perichordal sheath. Ribs, present as separate cartilages associated with the 2nd, 3rd and 4th vertebrae in the larvae of Xenopus and Bombinator, fuse with lateral processes (diapophyses) of the neural arches at metamorphosis, but in Leiopelma and Ascaphus the ribs remain freely articulated in the adult. Basiventral arcualia have been supposed to be represented by the hypochord, a median rod of cartilage beneath the shrinking notochord in the postsacral region, which at metamorphosis ossifies to produce the bulk of the urostyle. Fig. 5, lower right, a transverse section taken immediately posterior to the sacral ribs in a transforming specimen of Ascaphus, shows that the "hypochord" is a mass of cartilage formed in the perichordal sheath itself, and very obviously is derived from the ventral part of postsacral perichordal centra; there are, then, no basiventral arcualia, and the discrete hypochord shown in MacBride's diagram (Fig. 5, upper right) of a frog vertebra does not actually occur below the centrum, but only below the notochord in the postsacral region.

In Urodela (Fig. 6) the pattern of vertebral and rib development is more complex, and there has been much controversy over its interpretation. Neural arches and perichordal centra form in the same manner as in frogs, but with the addition in certain cases (Triton) of a median supradorsal cartilage, which gives rise to the zygapophyses of each neural arch. Difficulty comes, however, in understanding the relationship of the ribs to the vertebrae. Each rib, usually two-headed, articulates with a "transverse process" that in its early development seems to be separate from both the vertebra and the rib, and is therefore known, noncommittally, as "rib-bearer." This lies laterally from the centrum, neural arch, and vertebral artery; upon fusing with the vertebra it therefore encloses the artery in a foramen separate from the one between the capitulum and tuberculum of the rib (the usual location of the vertebral artery). At least four different interpretations of these structures have been suggested:

(1) Naef (1929) considered the rib-bearer a derivative of the basiventral, which, by spreading laterally and dorsally to meet the neural arch, enclosed the vertebral artery. He then supposed that by reduction of the rib-bearer in other tetrapods (frogs and amniotes) the vertebrarterial foramen and costal foramen were brought together in a single foramen transversarium. The implication is that the Urodele condition is primitive, but it cannot now be supposed that Urodela are ancestral to any other group, and the rib-bearer is most probably a specialization limited to salamanders. This does not, of course, invalidate the first part of his interpretation.

(2) Remane (1938), noting that rib insertions of early Amphibia are essentially as in Amniota, argued that the rib-bearer is not from the basiventral but is a neomorph which originates directly from the neural arch and grows ventrally. This he inferred mainly from Gamble's (1922) observation on Necturus, but his assumption that Necturus is more primitive than other salamanders (such as the Salamandridae), where the pattern differs from this, is not necessarily correct. Rather, the perennibranchs are distinguished mainly by their neotenous features, and their development is likely to show simplifications which are not necessarily primitive. The suggestion of a "neomorph" ought not to be made except as a last resort, for it is simply an acknowledgment that the author does not recognize homology with any structure already known; sometimes further information will make such recognition possible.

(3) Gray (1930), using Molge taeniatus, concluded that the normal capitulum of the rib was lost, but that the tuberculum bifurcated to make the two heads seen in Urodela, thus accounting for the failure of the costal foramen to coincide with that of the vertebral artery. This answer, too, seems to entail an unprovable assumption which should not be made without explicit evidence.

(4) Finally, Emelianov (1936) regarded the rib-bearer as a rudimentary ventral rib, on account of its relationship to the vertebral artery, and considered the actual rib to be a neomorph in the dorsal position characteristic of tetrapod ribs in general. This argument would fit the ontogenetic picture satisfactorily, provided that (a) there were some evidence of ventral, rather than dorsal, ribs in early Amphibia, and (b) we accept the invention of another neomorph in modern Amphibia as an unavoidable necessity. Emelianov's conclusion (p. 258) should be quoted here (translation): "The ribs of Urodela are shown to be upper ribs, yet we find besides these in Urodela rudimentary lower ribs fused with the vertebral column. The ribs of Apoda are lower ribs. In Anura ribs fail to develop fully, but as rare exceptions rudiments of upper ribs appear."

Of these various interpretations, that of Naef seems to involve the minimum of novelty, namely, that the rib-bearer is the basiventral, expanded and external to the vertebral artery. It is not necessary to take this modification as the ancestral condition in tetrapods, of course. The basiventral (=intercentrum) would merely have expanded sufficiently to provide a diapophysis for the tuberculum as well as the (primitive) facet for the capitulum. No neomorph appears under this hypothesis, which has the distinct advantage of simplicity.

Figures of early stages in vertebral development by the authors mentioned show that the basidorsals chondrify first, as neural arches, while a separate mass of mesenchyme lies externally and ventrally from these. This mesenchyme may chondrify either in one piece (on each side) or in two; in Molge the part adjacent to the centrum is ossified in the 20-mm. larva, and subsequently unites with the more dorsal and lateral cartilaginous part, while the rib, appearing farther out, grows inward to meet this composite "rib-bearer." In Necturus the mesenchyme below the neural arch differentiates into a cartilage below the vertebral artery (position proper to a basiventral), a bridge between this and the neural arch, and a rib, the latter two chondrifying later than the "basiventral" proper. In the "axolotl" (presumably Ambystoma tigrinum) the rib-bearer grows downward from its first center of chondrification at the side of the neural arch (Emelianov, 1936).

Thus it appears that the simplest hypothesis to account for the rib-bearer is that (a) it is the basiventral, (b) it is recognizable just before chondrification as a mass of mesenchyme in contact with both the notochordal sheath and the basidorsal cartilage, (c) it may chondrify or ossify first in its ventral portion or in its dorsal portion, the two then joining before it fuses with the rest of the vertebra, (d) the enclosure of the vertebral artery is a consequence of the extension of the basiventral beyond the position occupied by it in primitive Amphibia, and (e) there is no indication that this took place in other orders than the Urodela.

It seems that the vertebrae in Urodela have at least the following components: perichordal centra, separate basidorsal cartilages, and basiventrals, which are somewhat specialized in their manner of development. The vertebrae of Anura develop in the fashion just described except that basiventrals are lacking. It would seem no more difficult to accept the derivation of salamander vertebrae from the temnospondylous type than it is in the case of frogs, if other evidence points to such an ancestry.

Fig. 7, lower right, is Watson's (1940) illustration of the anterior trunk vertebrae of Amphibamus (Miobatrachus), in which the intercentrum is shown as a single median piece. Fig. 7, lower left, shows two of the more posterior trunk vertebrae seen as impressions in a cast of the type of "Miobatrachus romeri;" evidently the inter-centra were paired at about the level of the 16th vertebra, and relatively large. Gregory's (1950) figure of the type specimen of "Mazonerpeton" (also equivalent to Amphibamus) shows the anterior trunk vertebrae in relation to the ribs essentially as they appear to me in the cast of Miobatrachus, and rather differently from Watson's figure of the latter. Gregory is probably right in considering the specimens to represent various degrees of immaturity. So far as present information goes, then, the vertebrae of salamanders and frogs show no clear evidence of derivation from those of any particular group among the early Amphibia, but their features are not inconsistent with a simplification of the pattern of Temnospondyli.

PECTORAL GIRDLE

Hecht and Ruibal (Copeia, 1928:242) make a strong point of the nature of the pectoral girdle in Notobatrachus, as described recently by Stipanicic and Reig (1955, 1956) from the Jurassic of Patagonia, and quite rightly recommend that the significance of the arciferal and firmisternal types of girdle be restudied. That of Notobatrachus is said to be firmisternal; in view of the arciferal condition in the supposedly primitive Leiopelma, Ascaphus, Bombinator, etc., this comes as a surprise. Is the firmisternal girdle, as seen in Rana, Bufo, and others, actually the ancestral type, and has the arciferal been derived from something like this?

In the figures given by Stipanicic and Reig the ossified parts of the girdle are figured in detail (Fig. 8) and Reig's discussion of it is thorough. The decision to call it firmisternal was taken with some hesitancy, for no median elements are indicated, and the position and shape of those seen is closely similar to the ossified parts in Ascaphus and Leiopelma; there is no bony sternum or omosternum. It is safe to suppose that some cartilage lay in the midline between the clavicles and coracoids, but there is no evidence as to its extent, rigidity, or degree of overlapping if any. Apparently, then, there is not sufficient reason to infer that this Jurassic frog had a pectoral girdle comparable with the modern firmisternal type.

Piveteau (1955:261) remarks that the only living Anuran that can be compared usefully with Protobatrachus (Triassic) with regard to its pectoral girdle is Ascaphus. Again, the extent of cartilage in Protobatrachus (Fig. 8) can only be inferred, and there are no median elements. The agreement with Ascaphus includes the presence, in both, of a separate coracoid ossification situated posterior to the ossified "scapulocoracoid" (actually scapula). This ossification is evidently that shown in Notobatrachus as "coracoid." Direct comparison of the three genera with one another suggests that if we use the term arciferal for any, we should use it for all.

In the remote predecessor of Anura, Amphibamus of the Pennsylvanian, the pectoral girdle was less substantial than in many of its contemporaries, but it contained the primitive median interclavicle in addition to the clavicle, cleithrum, and scapulocoracoid. (The figure of Watson, 1940, and that by Gregory, 1950, are of individuals of different ages, the latter being older.) It is clear that the paired elements of such a girdle were held rigid by their attachment to the interclavicle, via the clavicles. Subsequent elimination of the interclavicle in the Anuran line of descent, and decrease of ossification, left a girdle like that of Protobatrachus, Notobatrachus, Ascaphus and Leiopelma. But in several advanced families a more rigid median "sternum," of one or two bony pieces plus cartilage, is developed secondarily, possibly (as Cope, 1889: 247, suggested) in correlation with axillary amplexus.

Among Urodela no dermal bones occur in the pectoral girdle. There is usually a scapulocoracoid ossified as a single piece, from which a thin cartilaginous suprascapula extends dorsally and a broad cartilaginous coracoid plate extends medially, overlapping the one from the opposite side; a precoracoid lobe of this reaches forward on either side, and a median, posterior "sternum" of cartilage may make contact with the edges of the two coracoids. In Siren and Amphiuma two centers of ossification are found for each scapulocoracoid, and in Triton and Salamandra three. Probably the more dorsal and lateral of these represents the primitive scapula and the other one (or two) the primitive coracoid.