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Comparative Morphology and Evolution of Frogs of the Neotropical Genera Atelopus, Dendrophryniscus, Melanophryniscus, and Oreophrynella

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Comparative Morphology and Evolution of Frogs of the Neotropical Genera Atelopus, Dendrophryniscus, Melanophryniscus, and Oreophrynella COMPARATIVE MORPHOLOGY AND EVOLUTION OF FROGS OF THE NEOTROPICAL GENERA ATELOPUS, DENDROPHRYNISCUS, MELANOPHRYNISCUS, AND OREOPHRYNELLA By ROY W. McDIARMID BULLETIN OF THE LOS ANGELES COUNTY MUSEUM OF NATURAL HISTORY SCIENCE: NUMBER 12 DECEMBER I, 1971 COMPARATIVE MORPHOLOGY AND EVOLUTION- Or FROGS OF THE NEOTROPICAL GENERA ATELOPUS, DENDROPHRYNISCUS, MELANOPHRYNISCUS, AND OREOPHRYNELLA By RoY W. McDIARMID' ABSTRACT: Atelopodid frogs are one of the most interesting and diverse groups of Neotropical Anura. The systematic status and evolutionary history of the genera in this family have been poorly understood. The purpose of this study is to analyze available knowledge of the morphology and biology of these frogs in order to clarify their evolutionary relationships and history. The group includes approximately 50 species in four genera: Atelopus, Dendroph­ ryniscus, Melanophryniscus, and Oreophrynella. Data indicate that Brachy­ cephalus, a genus originally included in the family, is not closely related to the four genera. Its relationships will be discussed elsewhere. Representative specimens of all genera and most species were examined. Information concerning myology, osteology, and reproductive morphology was gathered. All available literature was reviewed and pertinent information was assimilated into this report. A detailed description of thigh and jaw musculature and osteology of the species is presented. The skulls, pectoral girdles, and hyoid appara(i are described and illustrated. Components of the auditory apparatus, certain aspects of their external morphology, reproductive biology, and ecology are described. Each genus is defined according to 43 characters. Their geographical distributions are stated briefly and their included and referred species arc listed. Atelopus minutus Melin and Atelopus proboscideus Boulenger are placed in the genus Dendrophryniscus. A telopus rubriventris Vellard is placed in the genus Melanophryniscus. The four genera are discussed and their character states compared. Melanophryniscus has the greatest number of primitive states and the least number of advanced states and is probably most similar to the ancestral stock. Ate/opus also has many primitive states but possesses the greatest number of advanced states. A telorJUs and Melanophryniscus were derived from the same lineage, but A telopus has undergone a significant radiation at the species level and has several advancements not found in the other genera. Dendrophrynis­ cus was derived from the M elanophryniscus line and exhibits parallel evolu­ tion in some character states with Atelopus. Oreophrynella has more advanced character states than either Melanophryniscus or Dendrophryniscus and only one less than A telopus. However, Oreophrynella has the highest number of unique states and the lowest number of primitive states. Oreophrynella ap­ parently was derived from the apcestral stock at a different time from the Melanophryniscus-Ate/opus-Dendrophryniscus line and has subsequently be­ come greatly specialized. Major evolutionary trends and morphological character shifts apparently are associated with changes in means of locomotion; other-s are the result of differential metamorphosis. Biological modifications associated with the loss of the middle ear apparatus and the development of aposematic coloration are important. The familial status of the Atelopodidae is discussed and re­ jected. The genera Ate/opus, Dendrophryniscus, Melanophryniscus, and Oreo­ phrynella are placed in the family Bufonidae which is redefined. The ancestral stock from which the four genera were derived probably was present in South America before the beginning of the Cenozoic. The an­ cestral Melanophryniscus-Dendrophryniscus-Atelopus stock probably occur­ red in a savanna or deciduous forest habitat in southeastern Brazil. Melano­ phryniscus has retained many of the generalized ancestral characteristics and currently is found in the same general type of habitat. Dendrophryniscus was derived from the Melanophryniscus stock and has adapted to the wet tropical forest of eastern Brazil and the Amazon Basin. A telopus has adapted to a stream-side habitat and moved into montane areas which became available with the uplift of the Andes in Late Cretaceous and Early Tertiary. This new habitat has been successfully exploited by Ate/opus and has been a major fac­ tor contributing to their specific radiation. Oreophrynel/a is a very specialized frog that was derived from an old bufonid stock and subsequently restricted to Mount Roraima, an ancient part of the Guiana Shield. 'Research Associate, Section of Herpetology, Los Angeles County Museum of Natural History; and Department of Biology, University of South Florida, Tampa. I 2 BULLETIN OF LOS ANGELES COUNTY MUSEUM OF NATURAL HluTORY No.l2 INTRODUCTION dant and may be the dominant vertebrate in the The South American continent, with its complex area; at other times, this same species may be nearly physiography and vast areas of tropical, subtropi­ impossible to find. cal, and temperate forest, is a center of diversity for The reproductive biology and life history of only anuran amphibians. There are more than 750 four of the more than 40 species of the genus species assigned to ten families and approximately Ate/opus, which has the greatest spectrum of adap­ 105 genera recorded from the continent. One of the tive types, are known. Limited information is avail­ most interesting of the South American groups is able on the life histories of two species of M elano­ the nominal family Atelopodidae which includes phryniscus and two species of Dendrophryniscus, about 50 species of frogs that are restricted to Cen­ but nothing is known concerning the reproductive tral and South America. Most anuran systematists biology of Oreophrynella. consider these frogs to be species of Ate/opus, Den­ The generic relationships and systematic status drophryniscus, Melanophryniscus, Oreophrynella, of these frogs are poorly understood. Since the first and Brachycephalus. At the outset of this study I species were described in the mid-1800's, they have assumed that these five genera formed a natural been variously placed in approximately one-half of group (Atelopodidae). As the study progressed it the currently recognized anuran families, and three became more and more apparent that the mono­ of the four genera have been placed in their own typic genus Brachycephalus is not closely related families. In one of the classic works on salientian to the other four genera. Therefore, only A telopus, phylogeny, Noble (1922) placed the genera, to­ Dendrophryniscus, Melanophryniscus, and Oreo­ gether with several genera that now comprise the phrynella are considered here. The status of Bra­ family Dendrobatidae, the firmisternal members of chycephalus is discussed elsewhere (McDiarmid, the Leptodactylidae, and the Rhinodermatidae, in MS). a single family. Most workers, including Noble, Within this group there is considerable biological agree that the atelopodids are related to the Bufoni­ and morphological diversity. Species of Ate/opus, dae, but no one has demonstrated the nature of Dendrophryniscus and Oreophrynella are primarily this relationship. tropical forms. One species of A telupus is found at It was apparent that this group of frogs pro­ sea level in the warm, wet rain forests of the Choc6 vided an ideal opportunity for a study of major in Colombia; another species is adapted to the cold, patterns of anuran evolution. This opportunity, unforestcd paramos at over 4000 meters elevation coupled with my interest in ecology and zoogeogra­ in the Andes. Species of M elanophryniscus are phy of tropical organisms, was the stimulus for this primarily subtropical and south temperate in dis­ study. The project is designed to answer the follow­ tribution, although one form is known from a ing questions: I) What types of variation, morpho­ locality in the Amazon Basin. While species of logical or otherwise, are characteristic of each Ate/opus, Dendrophryniscus, and Me/anophrynis­ genus? 2) What characteristics are most useful in cus are wide ranging forms, the two species of defining the genera from the phylogenetic view­ Oreophrynel/a are restricted to a single mountain point'' 3) What types of relationship exist among massif. Most species are terrestrial as adults, but the generic categories? 4) What are the evolutionary some may be semifossorial, and one species of implications of the morphological changes within Dendrophryniscu., is arboreal and deposits its eggs and among the genera? 5) How do the characteris­ in bromeliads. Adults range from 14 mm in males tic features of the genera considered as a unit, com­ of a small species of Dendrophryniscus to nearly pare with other groups of closely related genera? 60 mm in females of a large species of Ate/opus. 6) What can be said concerning the patterns of Individuals of most species are thin and elongate historical development of the genera? with long, spindly legs; some, however, are short This study describes in detail the osteology of and robust. Many species are brightly colored and each genus (based on examination of about 70% have variable markings of red, green, yellow, of the included species) and certain aspects of their orange, or black; others may be gray, dull brown, myology and reproductive morphology. All known or black. Some forms have smooth skin while features of behavior, ecology, and natural history others have rugose and warty skin. Some species are considered. The genera are redefined,
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