Adaptive Radiation of Salamanders in Middle American Cloud Forests

Tailed amphibians, or salamanders, occur in the tropics only in the New World, where they are concentrated primarily in Middle America and northwestern South America. All are members of the family Plethodontidae, the lungless salamanders. As recently as 1926 only 30 species of tropical salamanders were known, and all were placed in a single genus. Today 11 genera are recognized. All occur in Middle America, and over 140 species have been described. Many local tropical regions are very rich in numbers of species, and as many as 21 species may be present along a single altitudinal gradient. Community organization of species of salamanders in the tropics differs from that in temperate regions in that species of tropical salamanders tend to be segregated into discrete elevational zones, with any given species restricted to a narrow elevational band. Within elevational zones, species are segregated by major habitat type, then by microhabitat, body size, and finally trophic and behavioral features. Cloud forests at middle elevations, from about 750 m to 2,500 m, are especially rich in salamanders, in both diversity and density. In Nuclear Central America nearly 50% of arboreal bromeliads in a local sample (N = 903) contained salamanders. Some species are found almost exclusively in bromeliads, and over 30 salamanders have been encountered in a single bromeliad. Farther south, in Costa Rica, cloud forests harbor salamanders in bromeliads as well as in arboreal and terrestrial moss mats. Extreme microhabitat specialization enriches the Costa Rican fauna to the maximum number of species present locally anywhere in the tropics. In the relatively lower latitudes (e.g., Costa Rica and Panama) the proportion of species occurring at lower elevations increases compared with Mexican and Guatemalan transects. Bromeliads and moss mats in the mid-elevational wet and rain forests are ideal microhabitats for these insectivorous, direct developing amphibians. Bromeliads offer abundant food resources, egg deposition sites, protection from predation, and microenvironments buffered against temperature extremes and low humidity. Salamanders are top carnivores in the bromeliad microhabitat. The extensive adaptive radiation of plethodontid salamanders in Middle America has featured both convergent and parallel evolution. The mid-elevational cloud forests, with their rich epiphytic assemblages and highly dissected topography, have been of great significance in speciation, morphological and behavioral diversification, geographical ecology, and historical biogeography of tropical plethodontid salamanders. The cloud forests of Middle America are home to a unique group of vertebrates-lungless, climbing salamanders that belong to the family Plethodontidae. By "cloud forest" I refer rather loosely to those forest assemblages which form in the presence of fog. Clouds condense at varying elevational levels in Middle America, depending on many local and regional factors such as temperature of the water of the nearest ocean, topography, rainfall patterns, and wind direction (Grubb & Whitmore, 1966; Myers, 1969). In general, cloud forests form between elevations of about 800 and 2,700 m. Both upper and lower boundaries shift with climatic changes, with the lowest occurring along humid slopes in the low latitudes and the highest being found in the northern tropics along the Pacific slopes. Cloud forests offer ideal conditions for tropical salamanders, all of which are nonaquatic, direct developing species. Although they do not breed in water, these organisms nevertheless require moist conditions for activity, and the cloud forest I Research reported in this paper has been a collaborative effort involving many individuals, especially James F. Lynch and Theodore J. Papenfuss, both of whom have given helpful criticisms of the manuscript. Marvalee H. Wake carefully reviewed the manuscript and David Darda and Nancy Staub also provided useful comments. My research has been supported by the National Science Foundation and the Museum of Vertebrate Zoology. I gratefully acknowledge the cooperation of governmental agencies in Mexico, Guatemala, and Costa Rica in obtaining permission to conduct research in their countries, and Douglas Robinson and Pedro Leon for their help and cooperation in Costa Rica. I dedicate this paper to the memory of L. C. Stuart, who generously offered his unparalleled knowledge of the Guatemalan herpetofauna to me, and whose published work remains as an inspiration to future students of Guatemalan and other tropical environments. 2 Museum of Vertebrate Zoology and Department of Zoology, University of California, Berkeley, California 94720, U.S.A. Paper received 7 July 1985. ANN. MISSOURI BOT. GARD. 74: 242-264. 1987. This content downloaded from 157.55. 39.17 on Wed, 31 Aug 2016 04:38:07 UTC All use subject to http://about.jstor. org/terms 1987] WAKE-ADAPTIVE RADIATION OF SALAMANDERS 243 environments are effectively buffered from desiccating conditions as well as from extremes of temperature. In addition, these forests typically support abundant epiphytes that are used extensively by salamanders. There are more than 140 species of plethodontid salamanders in the New World tropics; about 80% occur in Middle America (Wake & Lynch, 1976; Frost, 1985). What makes them unusual is their great diversity in the New World tropics and their total absence from the Old World tropics. Middle America has been the setting for an extensive, unique adaptive radiation that has remained very localized. The success of these species can be measured against that of salamanders generally. Worldwide, there are about 350 species of salamanders divided among nine families (Frost, 1985). Eight families are restricted to North Temperate regions. Over 200 of the species are members of the family Plethodontidae, the only group of salamanders to radiate in tropical regions. All tropical species of salamanders are members of the supergenus Bolitoglossa (Wake, 1966), which contains 11 genera and about 40% of the species of salamanders in the world. The supergenus is exclusively New World in distribution and does not occur north of Mexico. The plethodontids have a curious distribution, with two primary areas of evolutionary diversification: North America with concentration in the Appalachian region, and Middle America (Fig. 1). In eastern North America are found three major groups of plethodontids, two of which have life histories involving an aquatic larval stage. The Middle American region contains members of a fourth major group, the tribe Bolitoglossini, members of which have a uniphasic life history featuring direct development without a larval stage (Wake, 1966). The other two supergenera in the Bolitoglossini occur in California and Oregon (and possibly in Alaska and Mexico), and on Sardinia, the Italian mainland, and a tiny portion of southeastern France. I have argued elsewhere that the absence of an aquatic larval stage facilitated occupancy of the relatively densely crowded, predator-rich tropics (Wake, 1966; Hanken et al., 1980). A unique feeding mechanism and an associated behavioral repertoire (Lombard & Wake, 1977, 1986; Roth & Wake, 1985a, 1985b), which could evolve its particular characteristics only in a group lacking aquatic larvae, may have aided in the successful radiation of the tropical species. Those animals 5,6