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MUSEUM OF NATURAL HISTORY The University of Kansas Lawrence, Kansas --------------------------------------------------------------- NUMBER 1 APRIL 29, 1971 ---------------------------------------------------------------

A SYNOPSIS OF NEOTROPICAL HYLID FROGS, GENUS _OSTEOCEPHALUS_

By

LINDA TRUEB[1] AND WILLIAM E. DUELLMAN[2]

[1] Research Associate, Division of Herpetology, Museum of Natural History, University of Kansas.

[2] Curator, Division of Herpetology, Museum of Natural History, University of Kansas.

When we initiated a study of the herpetofauna at Santa Cecilia in Amazonian Ecuador in 1966, we were immediately confronted with many kinds of animals that we could not identify with the existing literature. Comparisons of our specimens with those preserved in other museums resolved some of the problems, but many identifications could be made only after study of type specimens; even then some determinations remained questionable. We now find that in order to prepare a meaningful account of the herpetofauna of Santa Cecilia, we must complete several taxonomic studies, the limits of which extend far beyond eastern Ecuador. Because of our interests in hylids we have begun our studies on these frogs.

One of us (Trueb, 1970a) studied the cranial osteology of casque-headed hylid frogs and redefined the genus Osteocephalus but did not determine the number of species in the genus. Our work in Amazonian Ecuador resulted in the discovery of the sympatric occurrence of three species at each of two localities; one of these species was found with a fourth species at another locality. Study of museum specimens confirmed the recognition of these four species in the Amazon Basin and lower Amazonian slopes of the Andes. A fifth species from Bolivia and Perú also is included in the genus. Examination of museum specimens has provided data on the geographic variation in, and distribution of, the five species. However, our conclusions pertaining to some populations need substantiation, because we have been hampered by inadequate material from areas beyond Ecuador. More than half of the 905 specimens of _Osteocephalus_ are from Ecuador, a relatively small part of the total range of the genus.

In this paper we are presenting a taxonomic review of the genus _Osteocephalus_; of necessity our study has been at the alpha level. We have utilized all of the usual external characters, as well as osteological features in our definitions of the species. Tadpoles and mating calls are available for only one species, _O. verrucigerus_ (Trueb and Duellman, 1970); these and other important systematic characters, such as karyotypes, are not available for the group at this time. Our tendency has been to take a conservative view of species; thus it is doubtful that any subsequent worker will recognize fewer species in the genus. Our observations on these frogs in Amazonian Ecuador are presented in a final section of this paper.

ACKNOWLEDGMENTS

For the loan of specimens or for the provision of working space in their respective institutions, we are indebted to James E. Böhlke, Werner C. A. Bokermann, F. W. Braestrup, Nelly Carrillo de Espinoza, Osvaldo R. da Cunha, Josef Eiselt, M. J. Fouquette, Jr., Alice G. C. Grandison, Jean Guibé, Birgitta Hansson, Walter Hellmich, M. J. Hoogmoed, Robert F. Inger, Konrad Klemmer, Jean Lescure, Alan E. Leviton, Clarence J. McCoy, Robert H. Mount, Charles W. Myers, Umberto Parenti, Günther Peters, James A. Peters, William F. Pyburn, Juan A. Rivero, Dorothy M. Smith, Paulo E. Vanzolini, Greta Vestergren, David B. Wake, Charles F. Walker, Ernest E. Williams, and Richard G. Zweifel.

Study of specimens in European museums was made possible by a grant (No. 5063) from the Penrose Fund of the American Philosophical Society. Field work in Ecuador was partially supported by grants from the Watkins Fund of the Museum of Natural History, University of Kansas. At our base camp at Santa Cecilia, Ecuador, we enjoyed the hospitality of Ing. Ildefonso Muñoz B. Transportation in Ecuador was generously provided by the Texaco Petroleum Company. During the course of our field work Stephen R. Edwards and Thomas H. Fritts contributed directly to our study of _Osteocephalus_. Michael J. Tyler of the South Australian Museum provided information on the vocal sac structure. We extend our sincere thanks to all of these persons for their contributions to our endeavors.

MATERIALS AND METHODS

We have examined 893 preserved frogs, including the type specimens of all included nominal taxa, 8 skeletons, 1 lot of eggs, and 3 lots of tadpoles that we refer to the genus _Osteocephalus_; in addition skulls were removed from five preserved specimens, and radiographs were made of 12 other preserved specimens. We have been fortunate in seeing living individuals of all species, except _O. pearsoni_, but we have colored photographs of a living specimen of that species. Figures 1 and 2 were drawn from projected colored transparencies of living frogs. Terminology follows that of Duellman (1970b). On the distribution maps solid symbols indicate localities from which we have examined specimens; open symbols represent additional locality records based on the literature. Throughout the text specimens are listed by their catalogue numbers preceded by the appropriate museum abbreviation, as follows:

AMNH American Museum of Natural History ANSP Academy of Natural Sciences of Philadelphia ASU Arizona State University AUM Auburn University Museum BMNH British Museum (Natural History) CAS California Academy of Sciences CAS-SU Stanford University Collection (In California Academy of Sciences) CM Carnegie Museum FMNH Field Museum of Natural History KU University of Kansas Museum of Natural History MCZ Museum of Comparative Zoology, Harvard University MIZS Museo ed Istituto di Zoologi Sistematico, Università di Torino MJP Museo Javier Prado, Lima MNHN Muséum National d'Histoire Naturelle, Paris MPEG Museu Paraense Emiliano Goeldi, Belém MVZ Museum of Vertebrate Zoology, University of California, Berkeley MZUSP Museu de Zoología, Universidade da São Paulo NHMG Naturhistoriska Museet Göteborg NHMW Naturhistorisches Museum, Wien NHRM Naturhistoriska Riksmuseet, Stockholm RMNH Rijksmuseum van Natuurlijke Histoire, Leiden SMF Senckenbergische Museum, Frankfurt UIMNH University of Illinois, Museum of Natural History UMMZ University of Michigan Museum of Zoology UP Université de Paris UPR-M University of Puerto Rico, Mayagüez UTA University of Texas, Arlington USNM United States National Museum UZM Universitets Zoologiske Museum, Copenhagen WCAB Werner C. A. Bokermann, São Paulo, Brasil ZMB Zoologisches Museum Berlin ZSM Zoologisches Sammlung München

HISTORICAL RESUMÉ

Because of the taxonomic confusion that has surrounded the generic name _Osteocephalus_ and two of the species (and their synonyms), we present a brief resumé of the taxonomic history of the group.

Among the amphibians sent to the Muséum National d'Histoire Naturelle in Paris by a Monsieur Leprieur in French Guiana was a single female specimen of a moderately large hylid having a well-ossified skull and smooth dorsal skin. This specimen escaped from the covetous eyes of Johann Tschudi, who prematurely named several species on the basis of specimens in Paris, and survived without an epithet until Duméril and Bibron (1841) proposed for it the name _Hyla leprieurii_. The description of the species is fairly detailed, but the specimen was not illustrated. This is the earliest trivial name now associated with _Osteocephalus_.

Fitzinger (1843) in his generic synopsis of amphibians and reptiles proposed the generic name _Osteocephalus_ but did not associate a specific name with the genus. Consequently, _Osteocephalus_ Fitzinger, 1843, is a _nomen nudum_. Franz Steindachner followed Leopoldo Fitzinger at the Naturhistorisches Museum in Vienna, where he had access to Fitzinger's notes and, of course, the important collections housed in that museum. Steindachner (1862) named two species of _Osteocephalus_ on the basis of Brasilian specimens collected by Johann Natterer. Both species were named in the same publication; _O. taurinus_ appeared on page 77, and _O. favolineatus_, on p. 80. This is the earliest association of the generic name _Osteocephalus_ with a specific name and a description, both of which satisfy the Code of Zoological Nomenclature for generic availability. Therefore, Steindachner is the authority for the generic name _Osteocephalus_, which has _O. taurinus_ as the type species by original designation. It is not possible to determine whether or not Steindachner's usage of _Osteocephalus_ was the same as that intended by Fitzinger 19 years earlier.

Steindachner (1862) gave reasonably good descriptions of his two new species and provided excellent illustrations of the two specimens, both large females. Apparently impressed by the similarities between _Trachycephalus nigromaculatus_ Tschudi, 1838, and _Osteocephalus taurinus_, Steindachner (1867) used the combination _Trachycephalus (Osteocephalus) taurinus_. This ambiguous usage for the 1860's precludes our determining if Steindachner was in effect synonymizing _Osteocephalus_ with _Trachycephalus_ or whether he was placing _Osteocephalus_ in a subgeneric status. Steindachner (1867) did not mention _O. flavolineatus_; perhaps by that time he had concluded that _flavolineatus_ was only a color morph of _taurinus_.

Cope (1867) placed _Hyla leprieurii_ in the genus _Hypsiboas_ Wagler, 1830. Cope (1874) named _Osteocephalus planiceps_ from Nauta, Perú. The single specimen was among the collections made by the Orton Expedition to the upper Amazon Basin and was deposited in the Academy of Natural Sciences in Philadelphia.

Boulenger (1882) placed both _Osteocephalus_ and _Trachycephalus_ the synonymy of _Hyla_; he recognized _Hyla taurina_ (with _O. flavolineatus_ as a synonym), _H. leprieurii_, and _H. planiceps_. In the same publication Boulenger named _Hyla buckleyi_ on the basis of 10 specimens in the British Museum from Ecuador; in the description he stated that _buckleyi_ was like _leprieurii_ and _taurinus_ in having paired lateral vocal sacs. Boulenger held a lasting influence on taxonomic herpetology, and his generic synonymy of _Osteocephalus_ was unchallenged until only a decade ago.

Goin (1961) presented a generic synopsis of the genera of hylid frogs, in which he recognized _Osteocephalus_ and stated: "There are perhaps eight or ten species of this genus in South America. Certainly _taurinus_, _britti_, _leprieuri_, _buckleyi_ and _pearsoni_ belong here. _O. planiceps_ is surely a synonym of _leprieuri_ and I believe that _garbei_ is as well. The status of such forms as _macrotis_, _riopastazae_, and _depressa_ has not yet been settled." Goin defined _Osteocephalus_ as follows: "Males with paired vocal pouches, one at each angle of the jaw; derm of head not co-ossified with skull but roof of skull exostosed." Trueb (1970a) elaborated on Goin's definition and assuredly included only _O. taurinus_ and _O. leprieurii_ in the genus.

Goin's inclusion of _buckleyi_, _britti_, and _pearsoni_ in _Osteocephalus_ was the first association of any of these names with that genus. Duellman (1970a) demonstrated that _Garbeana garbei_ Miranda-Ribeiro, 1926, was a member of the _Hyla rubra_ group. _Hyla macrotis_ Andersson, 1945, is a _Phrynohyas_. Trueb and Duellman (1970) determined that _Hyla verrucigera_ Werner, 1901, is the earliest name for an _Osteocephalus_ displaying striking sexual dimorphism in coloration and texture of the dorsal skin; _Hyla riopastazae_ Andersson, 1945 (female holotype), and _Hyla orcesi_ Funkhouser, 1956 (male holotype), were placed in the synonymy of _Osteocephalus verrucigerus_.

_Hyla pearsoni_ Gaige, 1929, is a small species of _Osteocephalus_. Our findings substantiate Goin's suggestions relative to two other taxa. _Hyla leprieurii britti_ Melin, 1941, from the Rio Uaupés, Brasil, and _Hyla depressa_ Andersson, 1945, from the Río Pastaza watershed, Ecuador, are members of the genus _Osteocephalus_, but both are synonyms of earlier names--_leprieurii_ and _taurinus_, respectively. Another name proposed by Melin (1941), _Hyla (Trachycephalus) vilarsi_ from Taracuá, Brasil, also is placed in the synonymy of _O. taurinus_.

Cochran and Goin (1970) were unaware of the identities of _Hyla verrucigera_ and _riopastazae_; they used the later name _Osteocephalus orcesi_ for Colombian frogs that are correctly referred to _O. verrucigerus_. Although Goin (1961) placed _Hyla buckleyi_ and _H. pearsoni_ in _Osteocephalus_, Cochran and Goin (1970) recognized a "_buckleyi_ group" in _Hyla_ that included these two species plus a new species, _Hyla cabrerai_ from Amazonian Colombia and Brasil (total of three specimens). Also, these authors named _Hyla carri_ from a single Colombian specimen. Study of the types of _Hyla cabrerai_, _H. carri_, and _H. festae_ Peracca, 1904, from Ecuador, reveal that all of these names are synonyms of _Osteocephalus buckleyi_.

Much of the taxonomic confusion and multiplicity of trivial names is due to the great amount of color variation in _taurinus_ and to the sexual dimorphism in the texture of the dorsal skin in all of the species. The details of variation in these and other characters and our justifications for the synonymies are given in the accounts of the species. All of the trivial names that apply to species herein recognized as members of the genus _Osteocephalus_ are listed in table 1.

=Osteocephalus= Steindachner, 1862

_Osteocephalus_ Steindachner, 1862:77 [Type species.--_Osteocephalus taurinus_ Steindachner, 1862, by original designation]. Not _Osteocephalus_ Fitzinger, 1843:50 (_nomen nudum_).

_Diagnostic Definition._--1) Skull broader than long; 2) dermal roofing bones of skull well ossified, exostosed, and/or co-ossified in some species; 3) prenasal and internasal bones absent; 4) parasphenoid alae posterolaterally oriented; 5) dentigerous processes of prevomers angular (/--\); 6) vocal sacs paired, posterior, and when inflated protruding posteroventral or posterolateral to angles of jaws; 7) submentalis muscle moderate in size and araphic; 8) intermandibularis muscle undifferentiated and bearing an elongate median aponeurosis; 9) parotoid glands absent or poorly developed, skin not producing viscous secretion characteristic of _Phrynohyas_; 10) skin on dorsum tuberculate in males, smooth in females; 11) tympanum large, 60 percent or more of diameter of eye; 12) fingers about one-third, toes more than three-fourths webbed; 13) discs large, round; 14) nuptial excrescences present in breeding males; 15) inner metatarsal tubercle not modified for digging; 16) outer metatarsal tubercle absent; 17) tarsal fold weak or absent; 18) pupil horizontal; 19) palpebrum clear; 20) known tadpoles having two upper and five lower rows of teeth.

TABLE 1.--Alphabetical Synonymy of the Species of _Osteocephalus_.

Trivial Name, Original Generic Name, Author, Date Current Name ---------------------------------------------------------------------- _britti (Hyla leprieurii)_ Melin, 1941 _O. leprieurii_ _buckleyi (Hyla)_ Boulenger, 1882 _O. buckleyi_ _cabrerai (Hyla)_ Cochran and Goin, 1970 _O. buckleyi_ _carri (Hyla)_ Cochran and Goin, 1970 _O. buckleyi_ _depressa (Hyla)_ Andersson, 1945 _O. taurinus_ _festae (Hyla)_ Peracca, 1904 _O. buckleyi_ _flavolineatus (Osteocephalus)_ Steindachner, 1862 _O. taurinus_ _leprieurii (Hyla)_ Duméril and Bibron, 1841 _O. leprieurii_ _orcesi (Hyla)_ Funkhouser, 1956 _O. verrucigerus_ _pearsoni (Hyla)_ Gaige, 1929 _O. pearsoni_ _planiceps (Osteocephalus)_ Cope, 1874 _O. taurinus_ _riopastazae (Hyla)_ Andersson, 1945 _O. verrucigerus_ _taurinus (Osteocephalus)_ Steindachner, 1862 _O. taurinus_ _verrucigera (Hyla)_ Werner, 1901 _O. verrucigerus_ _vilarsi (Hyla)_ Melin, 1941 _O. taurinus_

_Content._--As defined here, the genus contains five known species: _O. buckleyi_ (Boulenger), _O. leprieurii_ (Duméril and Bibron), _O. pearsoni_ (Gaige), _O. taurinus_ Steindachner, and _O. verrucigerus_ (Werner).

_Distribution._--The Guianas and Amazon Basin; also in the upper Orinoco and Magdalena drainages. Most localities are at elevations below 500 m, but the genus ascends the Amazonian slopes of the Andes to elevations of about 1800 m.

ANALYSIS OF CHARACTERS

_Size and Proportions._--Frogs of the genus _Osteocephalus_ are moderate to large hylids. The largest species is _taurinus_, attaining a snout-vent length of 103.1 mm; the smallest is _pearsoni_, which attains a length of 54.7 mm. Considerable intraspecific geographic variation occurs in adult size, especially in _taurinus_. Females of all species attain a noticeably larger size than males, but no significant differences are apparent in proportions (Table 2).

TABLE 2.--Comparison of Size and Proportions in the Species of _Osteocephalus_. (Means are given in parentheses below observed ranges)

======================================================================================================== Species N Snout-vent Tibia Length/ Foot Length/ Head Length/ Head Width/ Tympanum/ Length S-V L S-V L S-V L S-V L Eye -------------------------------------------------------------------------------------------------------- _O. buckleyi_ [M] 30 37.9-48.1 0.478-0.580 0.375-0.444 0.319-0.357 0.329-0.368 0.608-0.820 (43.3) (0.520) (0.408) (0.343) (0.351) (0.711) [F] 31 48.6-75.1 0.476-0.599 0.363-0.469 0.310-0.358 0.318-0.367 0.574-0.905 (61.7) (0.553) (0.428) (0.333) (0.348) (0.734)

_O. leprieurii_ [M] 21 41.2-48.4 0.514-0.571 0.383-0.430 0.308-0.357 0.326-0.368 0.652-0.884 (44.7) (0.538) (0.408) (0.335) (0.348) (0.777) [F] 21 46.6-61.5 0.516-0.592 0.382-0.453 0.314-0.343 0.328-0.363 0.698-0.909 (57.1) (0.539) (0.404) (0.329) (0.349) (0.785)

_O. pearsoni_ [M] 2 45.3-46.2 0.481-0.504 0.404-0.437 0.322-0.335 0.327-0.342 0.660-0.673 (45.8) (0.493) (0.421) (0.329) (0.335) (0.666) [F] 1 54.7 0.521 0.405 0.318 0.346 0.862

_O. taurinus_ [M] 59 40.3-84.6 0.512-0.576 0.387-0.445 0.296-0.345 0.301-0.355 0.638-0.896 (66.3) (0.541) (0.416) (0.318) (0.324) (0.752) [F] 45 45.1-103.1 0.520-0.577 0.391-0.448 0.306-0.334 0.308-0.347 0.640-0.817 (75.8) (0.542) (0.420) (0.321) (0.327) (0.758)

_O. verrucigerus_ [M] 11 50.4-54.3 0.494-0.552 0.409-0.442 0.322-0.346 0.328-0.344 0.623-0.804 (53.0) (0.519) (0.427) (0.333) (0.337) (0.730) [F] 3 63.1-65.8 0.532-0.561 0.435-0.463 0.345-0.347 0.348-0.379 0.692-0.808 (64.5) (0.545) (0.448) (0.346) (0.358) (0.731) --------------------------------------------------------------------------------------------------------

_Coloration._--All _Osteocephalus_ are predominantly brown frogs usually with some darker dorsal markings (Figs. 1 and 2). _Osteocephalus verrucigerus_ has a nearly uniform dark brown dorsum and no distinct transverse bars on the limbs, whereas all of the other species have distinct bars on the limbs. The dorsal markings on the body consist of irregular blotches in _buckleyi_, _pearsoni_, and _taurinus_ but are narrow transverse marks in _leprieurii_. A narrow middorsal cream or yellow stripe is present in some individuals of _buckleyi_ and _taurinus_ but absent in all individuals of the other species. The flanks are uniform pale tan in _leprieurii_ and uniform reddish brown in _verrucigerus_; in the other species the flanks are cream to brown with dark brown or black spots (also dark diagonal marks in some _buckleyi_). A creamy white anal stripe is present in some specimens of _leprieurii_ but absent in all individuals of other species.

The postocular region, encompassing the tympanum, is dark brown in most specimens. In adults of _pearsoni_ and _taurinus_ the upper lips are dark brown. A pale cream or tan suborbital spot is present in _pearsoni_ and in some _taurinus_; in some specimens of _taurinus_ the suborbital spot is expanded posteriorly forming a labial stripe on the posterior part of the lip. The labial markings of _verrucigerus_ are similar to the latter pattern, except that in females a distinct, light labial stripe extends the length of the lip. _Osteocephalus leprieurii_ has a distinct, broad, pale labial stripe. The lips are barred cream and dark brown in _buckleyi_.

The venter is uniform creamy white or pale tan in _leprieurii_, uniform white in some _buckleyi_ (most males), and uniform tan in some _taurinus_. The other species and some individuals of _taurinus_ and _buckleyi_ (most females) have dark ventral markings. These markings are most distinctive in _verrucigerus_, in which the venter is white with bold black mottling and spots (Fig. 3c). Those individuals of _taurinus_ having ventral markings usually have indistinct, diffuse brown spots on the throat and chest (Fig. 3b). _Osteocephalus pearsoni_ is characterized by a fine brown reticulation on the venter and on the anterior and posterior surfaces of the thighs in adults (Fig. 3a). Individuals of _buckleyi_ that have ventral markings vary between the patterns illustrated for _pearsoni_ and _taurinus_ (Figs. 3b and c).

Ontogenetic change in coloration is slight or non-existent in _buckleyi_, _pearsoni_, and _taurinus_, except that juveniles lack ventral markings. A dark blotch on the back and distinct transverse bars on the limbs are evident in juveniles of _verrucigerus_; these markings are obscured in the adults. Juveniles of _leprieurii_ are olive-brown with yellow dorsolateral stripes; the transverse dark marks, characteristic of the adults, appear before the stripes are lost.