Part 19

baudini \ cyanosticta \ / + phaeota sordida \ / / + puma / \ \/ sila \ /____/ \ / \ / \ / | | Prototype

Certain aspects of this proposed phylogeny warrant further comment. Features such as the deposition of additional bone that roofs the skull or that forms lateral projections from the frontoparietals, like those in S. baudini and phaeota, are minor alterations of dermal elements and not basic modifications of the architecture of the skull. Consequently, we hypothesize the independent development of these dermal changes in S. baudini and phaeota. Similar kinds of dermal modifications have evolved independently in many diverse groups of frogs.

Likewise, we propose the parallel development of stream-adapted tadpoles in S. sordida and sila; in both cases the tadpoles adapted to changing environmental conditions (see following section on evolutionary history). Tadpoles of S. sordida already had two rows of labial papillae before entering the streams; subsequently the tadpoles developed complete rows of papillae, ventral mouths and long tails having low fins. Possibly the tadpoles of S. sila had two rows of labial papillae prior to their adapting to stream conditions; in the process of adapting they developed ventral mouths and long tails having low fins. Similar modifications in tadpoles have occurred in many diverse groups of Middle American hylids, such as Plectrohyla, Ptychohyla, the Hyla uranochroa group, and the Hyla taeniopus group.

Our lack of concern about coloration is due to the fact that, with the exception of the blue spots on the flanks and posterior surfaces of the thighs in some species, the coloration of Smilisca, consisting of a pattern of irregular dark marks on a paler dorsum and dark transverse bars on the limbs, is not much different from that of many other Neotropical hylids. Blue is a structural color, rare among Amphibia, which is achieved by the absence of lipophores above the guanophores. Thus, the incident light rays at the blue end of the spectrum are reflected by the guanophores without interference by an overlying yellow lipophore screen. According to Noble (1931), lipophores are capable of amoeboid movement that permits shifts in their positions, between or beneath the guanophores. We do not know whether this behavior of lipophores is widespread and is effected in response to environmental changes, or whether it is a genetically controlled attribute that is restricted in appearance. If the latter is the case we must assume that the prototype of Smilisca possessed such an attribute which was lost in S. baudini, phaeota, and puma. The development of blue spots is not constant in S. sordida and S. sila; in S. cyanosticta the spots range in color from blue to pale green.

The coloration of the tadpoles is not distinctive, except for the presence of dorsal blotches on the tails of S. sila and sordida. However, the similarity in pattern cannot be interpreted as indicating close relationships because nearly identical patterns are present in Hyla legleri and some species of Prostherapis. This disruptive coloration seems to be directly associated with the pebble-bottom, stream-inhabiting tadpoles.

In the baudini group, S. phaeota and cyanosticta are allopatric, whereas S. baudini occurs sympatrically with both of those species. The call of S. baudini differs notably from the calls of S. phaeota and cyanosticta, which are more nearly alike. Although in the phylogenetic scheme proposed here S. sila is considered to be more distantly related to S. puma than is S. sordida, the calls of S. sila and puma more closely resemble one another than either resembles that of S. sordida. Smilisca sila and puma are allopatric, whereas S. sordida is broadly sympatric with both of those species. We assume that in their respective phyletic lines the differentiation of both S. baudini and sordida was the result of genetic changes in geographically isolated populations. Subsequently, each species dispersed into areas inhabited by other members of their respective groups. Selection for differences in the breeding calls helped to reinforce other differences in the populations and thereby aided in maintaining specificity.

Evolutionary History

With respect to temporal and spatial aspects of evolution in Smilisca, we have tried to correlate the phylogenetic evidence on Smilisca with the geologic data on Middle America presented by Lloyd (1963), Vinson and Brineman (1963), Guzman and Cserna (1963), Maldonado-Koerdell (1964), and Whitmore and Stewart (1965). Likewise, we have borne in mind the evidence for, and ideas about, the evolution of the Middle American herpetofauna given by Dunn (1931b), Schmidt (1943), Stuart (1950, 1964) Duellman (1958, MS), and Savage (MS).

According to Stuart's (1950) historical arrangement of the herpetofauna, Smilisca is a member of the Autochthonous Middle American Faunal Element, and according to Savage's (MS) arrangement the genus belongs to the Middle American Element, a fauna which was derived from a generalized tropical American unit that was isolated in tropical North America by the inundation of the Isthmian Link in early Tertiary, that developed in situ in tropical North America, and that was restricted to Middle America by climatic change in the late Cenozoic.

Savage (MS) relied on the paleogeographic maps of Lloyd (1963) to hypothesize the extent and centers of differentiation of the Middle American Faunal Element. According to Lloyd's concept, Middle America in the Miocene consisted of a broad peninsula extending southeastward to about central Nicaragua, separated from the Panamanian Spur of continental South America by shallow seas. A large island, the Talamanca Range, and remnants of the Guanarivas Ridge formed an archipelago in the shallow sea. The recent discovery of remains of mammals having definite North American affinities in the Miocene of the Canal Zone (Whitmore and Stewart, 1965) provides substantial evidence that at least a peninsula was continuous southeastward from Nuclear Central America to the area of the present Canal Zone in early mid-Miocene time. South America was isolated from Central America by the Bolivar Trough until late mid-Pliocene.

Thus, in the mid-Tertiary the broad peninsula of Nuclear Central America, which consisted of low and moderately uplifted regions having a tropical mesic climate, provided the site for the evolution of Smilisca. It is not possible to determine when the genus evolved, but to explain the differentiation of the species it is unnecessary to have the ancestral Smilisca present prior to the Miocene.

We view the Miocene Smilisca as the prototype described in the preceding section, and suppose that it lived in the mesic tropical environment of the eastern part of the Central American Peninsula (in what is now Costa Rica and western Panama). Two stocks differentiated, probably in middle Miocene times; one of these, the ancestral stock of the baudini group, was widespread on the Caribbean lowlands from the Nicaraguan Depression to the Bolivar Trough, and the other, the ancestral stock of the sordida group, was restricted to the Pacific lowlands of the same region. In late Miocene time the ancestral stock of the baudini group dispersed northwestward around the deep embayment in the Nicaraguan depression into upper Central America (in what is now Honduras and Guatemala) and thence into southern Mexico. Apparently differentiation took place on each side of the Nicaraguan Depression; the frogs to the south of the depression evolved into S. phaeota, whereas those to the north of the depression represented the stock from which S. baudini and cyanosticta arose. Prior to the uplift of the mountains in the late Miocene and the Pliocene the baudini-cyanosticta stock probably was widespread in northwestern Central America. The elevation of the mountains resulted in notable climatic changes, principally the development of sub-humid environments on the Pacific lowlands. The frogs living on the Pacific lowlands became adapted to sub-humid conditions and developed into S. baudini. The stock on the Caribbean lowlands remained in mesic environments and evolved into S. cyanosticta.

Possibly in the middle Miocene before the Talamanca Range in Costa Rica and western Panama was greatly uplifted, the ancestral stock of the sordida group invaded the Caribbean lowlands of what is now Costa Rica. The subsequent elevation of the Talamanca Range in the Pliocene effectively isolated the ancestral stock of S. sila on the Pacific lowlands from the puma-sordida stock on the Caribbean lowlands. The former was subjected to the sub-humid conditions which developed on the Pacific lowlands when the Talamanca Range was uplifted. It adapted to the sub-humid environment by living along streams and evolving stream-adapted tadpoles. On the Caribbean side of the Talamanca Range the puma-sordida stock inhabited mesic environments. The stock that evolved into S. puma remained in the lowlands as a pond-breeding frog, whereas those frogs living on the slopes of the newly elevated mountains became adapted for their montane existence by developing stream-adapted tadpoles and thus differentiated into S. sordida.

Probably the six species of Smilisca were in existence by the end of the Pliocene; at that time a continuous land connection existed from Central America to South America. The climatic fluctuations in the Pleistocene, and the post-Wisconsin development of present climatic and vegetational patterns in Middle America, brought about the present patterns of distribution of the species. From its place of origin on the Caribbean lowlands of lower Central America, S. phaeota dispersed northward into Nicaragua and southward along the Pacific slopes of northwestern South America. Perhaps in the late Pleistocene or in post-Wisconsin time when mesic conditions were more widespread than now, S. phaeota moved onto the Pacific lowlands of Costa Rica. Its route could have been through the Arenal Depression. Subsequent aridity restricted its range on the Pacific lowlands to the Golfo Dulce region. Climatic fluctuation in northern Central America restricted the distribution of S. cyanosticta to mesic habitats on the slopes of the Mexican and Guatemalan highlands and to certain humid areas on the lowlands. Smilisca baudini was well adapted to sub-humid conditions, and the species dispersed northward to the Rio Grande Embayment and to the edge of the Sonoran Desert and southward into Costa Rica. In southern Mexico and Central America the species invaded mesic habitats. Consequently, in some areas it is sympatric with S. cyanosticta and phaeota.

Smilisca puma dispersed northward onto the Caribbean lowlands of southern Nicaragua. Its southward movements probably were limited by the ridges of the Talamanca Range that extend to the Caribbean coast in the area of Punta Cahuita in Costa Rica. Smilisca sila dispersed along the Pacific lowlands and slopes of the mountains from eastern Costa Rica and western Panama through eastern Panama to northern Colombia. Climatic fluctuation in the Pleistocene evidently provided sufficient altitudinal shifts in environments in the Talamanca Range to permit S. sordida to move onto the Pacific slopes. From its upland distribution the species followed streams down to both the Caribbean and Pacific lowlands, where it is sympatric with S. puma on the Caribbean lowlands and S. sila on the Pacific lowlands.

The evolution of the species-groups of Smilisca was effected through isolation by physical barriers in the Cenozoic; the differentiation of the species was initiated by further isolation of populations by changes in physiography and climate. Present patterns of distribution resulted from Pleistocene and post-Wisconsin climatic changes. Today, sympatric species have different breeding habits and breeding calls which reinforce the differences in morphology.

SUMMARY AND CONCLUSIONS

The genus Smilisca is composed of six species of tree frogs; each species is defined on the basis of adult morphology, larval characters, and breeding behavior. Keys are provided to aid in the identification of adults and of tadpoles.

Analysis of the characters and examination of type specimens indicates that several currently-recognized taxa are synonymous, as follows:

1. Hyla beltrani Taylor, 1942 = Smilisca baudini. 2. Hyla gabbi Cope, 1876 = Smilisca sordida. 3. Hyla manisorum Taylor, 1954 = Smilisca baudini. 4. Hyla nigripes Cope, 1876 = Smilisca sordida. 5. Hyla wellmanorum Taylor, 1952 = Smilisca puma.

Smilisca phaeota cyanosticta Smith, 1953 is elevated to specific rank, and one new species, Smilisca sila, is named and described.

The skeletal system of developmental stages and the adult of Smilisca baudini is described, and the skull is compared with that of other members of the genus.

The tadpoles are described, compared, and illustrated; the larval development of Smilisca phaeota is described.

Breeding behavior and breeding calls are described and compared. Some species of Smilisca have breeding choruses. Two species, S. sila and sordida, breed in streams, whereas the others breed in ponds.

The genus is considered to be part of the Middle American Faunal Element; the species are thought to have differentiated in response to ecological diversity and historical opportunities provided by Cenozoic changes in physiography and climate.

LITERATURE CITED

BAIRD, S. F.

1854. Descriptions of new genera and species of North American frogs. Proc. Acad. Nat. Sci. Philadelphia, 7:59-62. April 27.