Neotropical Hylid Frogs, Genus Smilisca

The tadpoles of S. baudini, cyanosticta, phaeota, and puma are pelagic inhabitants of shallow ponds. Early stages of S. baudini in which external gills are present have been observed to hang vertically with the gills spread out at the surface of the water, a behavior noted by Zweifel (1964:206) in tadpoles of Phrynohyas venulosa, which also develop in warm, standing water having a relatively low oxygen-tension. When disturbed the pelagic tadpoles usually dive and seek shelter amidst vegetation or in mud on the bottom. This behavior was observed in S. baudini, cyanosticta, and phaeota by day and at night. No tadpoles of S. puma were observed by day; those seen at night were near the surface of small water-filled depressions in a grassy marsh; they responded to light by taking refuge in the dense grass. Perhaps tadpoles of this species are negatively phototactic and remain hidden by day.

The stream-inhabiting tadpoles of S. sila and sordida live in clear pools in rocky streams, where they were observed to cling by their mouths to rocks in the stream and to seek shelter amidst pebbles or beneath rocks and leaves on the bottom. These tadpoles are not found in shallow riffles.

We have not found tadpoles of two species of Smilisca in the same body of water and therefore cannot offer observations on ecological relationships in sympatric situations.

Two phyletic lines evolved from this prototype. The first of these was the stock that gave rise to the baudini group. The evolutionary changes that took place in this line included increase in size, development of a lateral curvature of the maxillary, and an increased amount of cranial ossification, especially in the dermal roofing bones. This phyletic line retained the larval characters and breeding call of the prototype. The second phyletic line gave rise to the sordida group and diverged from the prototype in the development of an angular maxillary and a breeding call consisting of a primary note followed by secondary notes. The frogs in this phyletic line retained the moderate size of the prototype and did not develop additional dermal bone. Our concept of the phylogenetic relationships is shown graphically in Figure 17.

Within the baudini group one stock retained separate nasals and did not develop a bony squamosal-maxillary arch, but broad lateral processes developed on the frontoparietals. The tadpoles remained unchanged from the primitive type. This stock evolved into S. phaeota. In the other stock the nasals became fully ossified and a bony squamosal-maxillary arch developed. One branch of this second stock retained tadpoles having only one row of labial papillae and did not develop lateral processes on the frontoparietals; this branch evolved into S. cyanosticta. The other branch diverged and gave rise to S. baudini by developing relatively shorter hind legs, large lateral processes on the frontoparietals, and tadpoles having two rows of labial papillae.

Within the sordida group the cranial features remained unchanged in one line, which gave rise to S. sila, whereas in a second line the nasals were reduced, and their long axes shifted with the result that they are not parallel to the maxillaries; the amount of ossification of the ethmoid was reduced, and the tadpoles developed two rows of labial papillae. In this second line one branch retained the pond-breeding habits and gave rise to S. puma, whereas a second branch became adapted to stream-breeding and gave rise to S. sordida.

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.

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 Panamá). 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 México. 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 Panamá 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 México 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 Panamá through eastern Panamá 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.