OCCASIONAL PAPERSof theMUSEUM OF NATURAL HISTORYThe University of KansasLawrence, KansasNUMBER 1APRIL 29, 1971A SYNOPSIS OF NEOTROPICAL HYLID FROGS,GENUSOSTEOCEPHALUSByLinda 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 geographicvariation 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 ofOsteocephalusare from Ecuador, a relatively small part of the total range of the genus.In this paper we are presenting a taxonomic review of the genusOsteocephalus; 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.ACKNOWLEDGMENTSFor 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 ofOsteocephalus. Michael J. Tyler of the South Australian Museum provided information on the vocal sac structure. We extend oursincere thanks to all of these persons for their contributions to our endeavors.MATERIALS AND METHODSWe 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 genusOsteocephalus; 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, exceptO. pearsoni, but we have colored photographs of a living specimen of that species. Figures1and2were 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:AMNHAmerican Museum of Natural HistoryANSPAcademy of Natural Sciences of PhiladelphiaASUArizona State UniversityAUMAuburn University MuseumBMNHBritish Museum (Natural History)CASCalifornia Academy of SciencesCAS-SUStanford University Collection (In California Academy of Sciences)CMCarnegie MuseumFMNHField Museum of Natural HistoryKUUniversity of Kansas Museum of Natural HistoryMCZMuseum of Comparative Zoology, Harvard UniversityMIZSMuseo ed Istituto di Zoologi Sistematico, Università di TorinoMJPMuseo Javier Prado, LimaMNHNMuséum National d'Histoire Naturelle, ParisMPEGMuseu Paraense Emiliano Goeldi, BelémMVZMuseum of Vertebrate Zoology, University of California, BerkeleyMZUSPMuseu de Zoología, Universidade da São PauloNHMGNaturhistoriska Museet GöteborgNHMWNaturhistorisches Museum, WienNHRMNaturhistoriska Riksmuseet, StockholmRMNHRijksmuseum van Natuurlijke Histoire, LeidenSMFSenckenbergische Museum, FrankfurtUIMNHUniversity of Illinois, Museum of Natural HistoryUMMZUniversity of Michigan Museum of ZoologyUPUniversité de ParisUPR-MUniversity of Puerto Rico, MayagüezUTAUniversity of Texas, ArlingtonUSNMUnited States National MuseumUZMUniversitets Zoologiske Museum, CopenhagenWCABWerner C. A. Bokermann, São Paulo, BrasilZMBZoologisches Museum BerlinZSMZoologisches Sammlung MünchenHISTORICAL RESUMÉBecause of the taxonomic confusion that has surrounded the generic nameOsteocephalusand 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 nameHyla leprieurii. The description of the species is fairly detailed, but the specimen was not illustrated. This is the earliest trivial name now associated withOsteocephalus.Fitzinger (1843) in his generic synopsis of amphibians and reptiles proposed the generic nameOsteocephalusbut did not associate a specific name with the genus. Consequently,OsteocephalusFitzinger, 1843, is anomen 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 ofOsteocephaluson the basis of Brasilian specimens collected by Johann Natterer. Both species were named in the same publication;O. taurinusappeared on page 77, andO. favolineatus, on p. 80. This is the earliest association of the generic nameOsteocephaluswith 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 nameOsteocephalus, which hasO. taurinusas the type species by original designation. It is not possible to determine whether or not Steindachner's usage ofOsteocephaluswas 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 betweenTrachycephalus nigromaculatusTschudi, 1838, andOsteocephalus taurinus, Steindachner (1867) used the combinationTrachycephalus (Osteocephalus) taurinus. This ambiguous usage for the 1860's precludes our determining if Steindachner was in effect synonymizingOsteocephaluswithTrachycephalusor whether he was placingOsteocephalusin a subgeneric status. Steindachner (1867) did not mentionO. flavolineatus; perhaps by that time he had concluded thatflavolineatuswas only a color morph oftaurinus.Cope (1867) placedHyla leprieuriiin the genusHypsiboasWagler, 1830. Cope (1874) namedOsteocephalus planicepsfrom 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 bothOsteocephalusandTrachycephalusinthe synonymy ofHyla; he recognizedHyla taurina(withO. flavolineatusas a synonym),H. leprieurii, andH. planiceps. In the same publication Boulenger namedHyla buckleyion the basis of 10 specimens in the British Museum from Ecuador; in the description he stated thatbuckleyiwas likeleprieuriiandtaurinusin having paired lateral vocal sacs. Boulenger held a lasting influence on taxonomic herpetology, and his generic synonymy ofOsteocephaluswas unchallenged until only a decade ago.Goin (1961) presented a generic synopsis of the genera of hylid frogs, in which he recognizedOsteocephalusand stated: "There are perhaps eight or ten species of this genus in South America. Certainlytaurinus,britti,leprieuri,buckleyiandpearsonibelong here.O. planicepsis surely a synonym ofleprieuriand I believe thatgarbeiis as well. The status of such forms asmacrotis,riopastazae, anddepressahas not yet been settled." Goin definedOsteocephalusas 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 onlyO. taurinusandO. leprieuriiin the genus.Goin's inclusion ofbuckleyi,britti, andpearsoniinOsteocephaluswas the first association of any of these names with that genus. Duellman (1970a) demonstrated thatGarbeana garbeiMiranda-Ribeiro, 1926, was a member of theHyla rubragroup.Hyla macrotisAndersson, 1945, is aPhrynohyas. Trueb and Duellman (1970) determined thatHyla verrucigeraWerner, 1901, is the earliest name for anOsteocephalusdisplaying striking sexual dimorphism in coloration and texture of the dorsal skin;Hyla riopastazaeAndersson, 1945 (female holotype), andHyla orcesiFunkhouser, 1956 (male holotype), were placed in the synonymy ofOsteocephalus verrucigerus.Hyla pearsoniGaige, 1929, is a small species ofOsteocephalus. Our findings substantiate Goin's suggestions relative to two other taxa.Hyla leprieurii brittiMelin, 1941, from the Rio Uaupés, Brasil, andHyla depressaAndersson, 1945, from the Río Pastaza watershed, Ecuador, are members of the genusOsteocephalus, but both are synonyms of earlier names—leprieuriiandtaurinus, respectively. Another name proposed by Melin (1941),Hyla (Trachycephalus) vilarsifrom Taracuá, Brasil, also is placed in the synonymy ofO. taurinus.Cochran and Goin (1970) were unaware of the identities ofHyla verrucigeraandriopastazae; they used the later nameOsteocephalus orcesifor Colombian frogs that are correctly referred toO. verrucigerus. Although Goin (1961) placedHyla buckleyiandH. pearsoniinOsteocephalus, Cochran and Goin (1970) recognized a "buckleyigroup" inHylathat included these two species plus a new species,Hyla cabreraifrom Amazonian Colombia and Brasil (total of three specimens). Also, these authors namedHyla carrifrom a single Colombian specimen. Study of the types ofHyla cabrerai,H. carri, andH. festaePeracca, 1904, from Ecuador, reveal that all of these names are synonyms ofOsteocephalus buckleyi.Much of the taxonomic confusion and multiplicity of trivial names is due to the great amount of color variation intaurinusand 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 genusOsteocephalusare listed intable 1.OsteocephalusSteindachner, 1862OsteocephalusSteindachner, 1862:77 [Type species.—Osteocephalus taurinusSteindachner, 1862, by original designation]. NotOsteocephalusFitzinger, 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 elongatemedian aponeurosis; 9) parotoid glands absent or poorly developed, skin not producing viscous secretion characteristic ofPhrynohyas; 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 ofOsteocephalus.Trivial Name, Original Generic Name, Author, DateCurrent Namebritti (Hyla leprieurii)Melin, 1941O. leprieuriibuckleyi (Hyla)Boulenger, 1882O. buckleyicabrerai (Hyla)Cochran and Goin, 1970O. buckleyicarri (Hyla)Cochran and Goin, 1970O. buckleyidepressa (Hyla)Andersson, 1945O. taurinusfestae (Hyla)Peracca, 1904O. buckleyiflavolineatus (Osteocephalus)Steindachner, 1862O. taurinusleprieurii (Hyla)Duméril and Bibron, 1841O. leprieuriiorcesi (Hyla)Funkhouser, 1956O. verrucigeruspearsoni (Hyla)Gaige, 1929O. pearsoniplaniceps (Osteocephalus)Cope, 1874O. taurinusriopastazae (Hyla)Andersson, 1945O. verrucigerustaurinus (Osteocephalus)Steindachner, 1862O. taurinusverrucigera (Hyla)Werner, 1901O. verrucigerusvilarsi (Hyla)Melin, 1941O. taurinusContent.—As defined here, the genus contains five known species:O. buckleyi(Boulenger),O. leprieurii(Duméril and Bibron),O. pearsoni(Gaige),O. taurinusSteindachner, andO. 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 CharactersSize and Proportions.—Frogs of the genusOsteocephalusare moderate to large hylids. The largest species istaurinus, attaining a snout-vent length of 103.1 mm; the smallest ispearsoni, which attains a length of 54.7 mm. Considerable intraspecific geographic variation occurs in adult size, especially intaurinus. 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 ofOsteocephalus.(Means are given in parentheses below observed ranges)SpeciesNSnout-ventLengthTibia Length/S-V LFoot Length/S-V LHead Length/S-V LHead Width/S-V LTympanum/EyeO. buckleyi♂3037.9-48.10.478-0.5800.375-0.4440.319-0.3570.329-0.3680.608-0.820(43.3)(0.520)(0.408)(0.343)(0.351)(0.711)♀3148.6-75.10.476-0.5990.363-0.4690.310-0.3580.318-0.3670.574-0.905(61.7)(0.553)(0.428)(0.333)(0.348)(0.734)O. leprieurii♂2141.2-48.40.514-0.5710.383-0.4300.308-0.3570.326-0.3680.652-0.884(44.7)(0.538)(0.408)(0.335)(0.348)(0.777)♀2146.6-61.50.516-0.5920.382-0.4530.314-0.3430.328-0.3630.698-0.909(57.1)(0.539)(0.404)(0.329)(0.349)(0.785)O. pearsoni♂245.3-46.20.481-0.5040.404-0.4370.322-0.3350.327-0.3420.660-0.673(45.8)(0.493)(0.421)(0.329)(0.335)(0.666)♀154.70.5210.4050.3180.3460.862O. taurinus♂5940.3-84.60.512-0.5760.387-0.4450.296-0.3450.301-0.3550.638-0.896(66.3)(0.541)(0.416)(0.318)(0.324)(0.752)♀4545.1-103.10.520-0.5770.391-0.4480.306-0.3340.308-0.3470.640-0.817(75.8)(0.542)(0.420)(0.321)(0.327)(0.758)O. verrucigerus♂1150.4-54.30.494-0.5520.409-0.4420.322-0.3460.328-0.3440.623-0.804(53.0)(0.519)(0.427)(0.333)(0.337)(0.730)♀363.1-65.80.532-0.5610.435-0.4630.345-0.3470.348-0.3790.692-0.808(64.5)(0.545)(0.448)(0.346)(0.358)(0.731)Coloration.—AllOsteocephalusare predominantly brown frogs usually with some darker dorsal markings (Figs. 1 and 2).Osteocephalus verrucigerushas 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 inbuckleyi,pearsoni, andtaurinusbut are narrow transverse marks inleprieurii. A narrow middorsal cream or yellow stripe is present in some individuals ofbuckleyiandtaurinusbut absent in all individuals of the other species. The flanks are uniform pale tan inleprieuriiand uniform reddish brown inverrucigerus; in the other species the flanks are cream to brown with dark brown or black spots (also dark diagonal marks in somebuckleyi). A creamy white anal stripe is present in some specimens ofleprieuriibut absent in all individuals of other species.The postocular region, encompassing the tympanum, is dark brown in most specimens. In adults ofpearsoniandtaurinusthe upper lips are dark brown. A pale cream or tan suborbital spot is present inpearsoniand in sometaurinus; in some specimens oftaurinusthe suborbital spot is expanded posteriorly forming a labial stripe on the posterior part of the lip. The labial markings ofverrucigerusare similar to the latter pattern, except that in females a distinct, light labial stripe extends the length of the lip.Osteocephalus leprieuriihas a distinct, broad, pale labial stripe. The lips are barred cream and dark brown inbuckleyi.The venter is uniform creamy white or pale tan inleprieurii, uniform white in somebuckleyi(most males), and uniform tan in sometaurinus. The other species and some individuals oftaurinusandbuckleyi(most females) have dark ventral markings. These markings are most distinctive inverrucigerus, in which the venter is white with bold black mottling and spots (Fig. 3c). Those individuals oftaurinushaving ventral markings usually have indistinct, diffuse brown spots on the throat and chest (Fig. 3b).Osteocephalus pearsoniis characterized by a fine brown reticulation on the venter and on the anterior and posterior surfaces of the thighs in adults (Fig. 3a). Individuals ofbuckleyithat have ventral markings vary between the patterns illustrated forpearsoniandtaurinus(Figs. 3b and c).Ontogenetic change in coloration is slight or non-existent inbuckleyi,pearsoni, andtaurinus, except that juveniles lack ventral markings. A dark blotch on the back and distinct transverse bars on the limbs are evident in juveniles ofverrucigerus; these markings are obscured in the adults. Juveniles ofleprieuriiare olive-brown with yellow dorsolateral stripes; the transverse dark marks, characteristic of the adults, appear before the stripes are lost.Fig. 1.Species ofOsteocephalus:Top.O. pearsoni, KU 136312, ♂;Middle.O. buckleyi, KU 123172, ♂;Bottom.O. verrucigerus, KU 123177, ♂. ×1.5.Fig. 2.Species ofOsteocephalus:Top.O. leprieurii, KU 126611, ♀;Bottom.O. taurinus, KU 126648, ♂. ×10.Fig. 3.Diagrammatic views of ventral color patterns inOsteocephalus:a.O. pearsoni, UMMZ 57533, ♂;b.O. taurinus, USNM 166037, ♂;c.O. verrucigerus, KU 123185, ♀.Skin.—The dorsal skin of all males ofOsteocephalusis tuberculate to varying degrees, whereas the dorsal skin of females is smooth, or nearly so (Fig. 4).Osteocephalus verrucigerusdiffers from other members of the genus by the presence of numerous, large tubercles bearing keratinized tips. The tubercles ofleprieuriiare numerous and spinous but much smaller than those ofverrucigerus; those oftaurinusare spinous but less numerous than inleprieurii.Osteocephalus buckleyihas a mixture of large and small, non-spinous tubercles, andpearsonihas only a few, small, scattered, non-spinous tubercles. Fleshy tubercles occur on the eyelids and supratympanic fold in females ofbuckleyi; a few small tubercles are present on the back of females ofpearsoni, whereas the dorsal skin in females of the other species is smooth. The skin on the flanks of both sexes ofbuckleyiis weakly areolate; in the other species the flanks are smooth. The skin on the top of the head intaurinusis rugose as a consequence of co-ossification. In all species the anal opening is directed posteriorly at the upper level of the thighs.Hands and Feet.—The feet ofOsteocephalusare fully webbed ornearly so. Webbing between fingers one and two is basal in all species. Webbing between fingers two, three, and four is most extensive intaurinus, in which the three fingers are about one-half webbed (Fig. 5).Osteocephalus buckleyi,pearsoni, andverrucigerushave reduced webbing between fingers two and three, andleprieuriihas reduced webbing between fingers two, three, and four. All members of the genus have well-developed subconical subarticular tubercles on the fingers and toes; there is a tendency for the distal tubercle on the fourth finger to be weakly bifid. Palmar and plantar supernumerary tubercles are well developed intaurinus, moderately developed inbuckleyi,leprieurii, andpearsoni, and barely evident inverrucigerus. All of the species have a noticeable fold on the wrist and enlarged prepollices, bearing horny nuptial excrescences in breeding males. The prepollex is least enlarged inbuckleyi. Outer metatarsal tubercles are absent. The inner metatarsal tubercle is moderately well developed and ovoid inleprieuriiandpearsoni; it is elliptical and flat in the other species. Tarsal folds are absent in all species exceptverrucigerus, in which the folds are barely evident.Fig. 4.Segments of dorsal skin of males ofOsteocephalusshowing size and arrangement of tubercles:a.O. verrucigerus, KU 123183; b.O. taurinus, USNM 166033; c.O. leprieurii, KU 126616; d.O. buckleyi, USNM 165999.Each square = 1 sq. cm.Cranium.—As a genus, the cranial structure is remarkably uniform and quite generalized when viewed in the context of the family Hylidae. The skulls are broad and relatively flat, each being only slightly more broad than long and about one-third as high as long. In dorsal aspect the snouts are broadly rounded; the snout ofbuckleyiis somewhat less rounded and appears to be slightly longer than the snouts of other species. This subtle difference relates to the relative narrowness of the premaxillaries inbuckleyi.Fig. 5.Palmar views of hands of males ofOsteocephalus:a.O. buckleyi, KU 109506; b.O. leprieurii, KU 126627; c.O. pearsoni, MCZ 15565; d.O. taurinus, KU 126653; e.O. verrucigerus, KU 123177. ×4.Fig. 6.Skulls of two species ofOsteocephalus:a and b.O. leprieurii, KU 125961; c and d.O. pearsoni, UMMZ 67465. ×3.The genus is characterized by well-developed dermal roofing bones and an unusually large exposure of the sphenethmoid dorsally (Fig. 6). The conformation of the sphenethmoid exposed dorsally is determined by the marginal positions of the adjacent, overlapping elements—the nasals and frontoparietals. Medially the nasals overlap the lateral margins of the sphenethmoid. Anteromedially, the nasals converge inleprieuriiandtaurinus, are narrowly separated inbuckleyiandpearsoni, or are more widely separated inverrucigerus. In all species the nasals terminate at the anterodorsal corner of the orbit. The frontoparietals ofbuckleyi,leprieurii, andtaurinushave an anterolateral extension, which marginally overlaps the dorsolateral edge of the sphenethmoid and articulates with the posterodorsal corner of the nasal inbuckleyiandtaurinus; the bones are narrowly separated inleprieurii. The frontoparietals ofpearsoniandverrucigerushave more extensive median ossification and less extensive anterolateral ossification. Thus, in those species the posteromedian portion of the sphenethmoid is obscured, and thelateral margins are partly exposed. The frontoparietal fontanelle is completely covered in all species, exceptbuckleyiandleprieurii, in which an irregular, median separation of the frontoparietals exposes a small portion of the fontanelle. The posterolateral margins of the frontoparietals lie medial to the epiotic eminences.Dermal ornamentation, involving the nasals, frontoparietals, and sphenethmoid, occurs intaurinusand, to a limited extent, inpearsoni. In the latter species marginal portions of the frontoparietals, the dorsal surfaces of the nasals, and the posteromedial part of the exposed sphenethmoid are slightly exostosed, resulting in an open, reticulate pattern of dermal sculpturing of exceedingly low relief (Fig. 6c).Osteocephalus taurinusis characterized by casquing, co-ossification, and a rather intricate pattern of dermal sculpturing, which was described in detail and illustrated by Trueb (1970a).The squamosals of all species are moderately large structures having otic plates that overlie the lateral portion of the cristae paroticae. The posterior rami are short; the zygomatic rami of all species, excepttaurinus, extend slightly more than one-half of the distance to the maxillary. Intaurinusthe zygomatic ramus extends nearly to, or articulates with, the maxillary.The maxillary arches are complete and relatively robust. The alary processes of the premaxillaries are vertically oriented inleprieurii,pearsoni, andtaurinusand very slightly inclined posteriorly inbuckleyiandverrucigerus. The maxillaries are uniformly characterized by the absence of postorbital processes and by the presence of preorbital processes that articulate with the maxillary processes of the nasals. The partes facialae of the maxillaries are moderately developed in all species, excepttaurinus, in which the pars fascialis tends to articulate with the lateral margin of the nasal in well-ossified individuals. The partes palatinae are poorly developed in all species, exceptbuckleyi, in which the pars palatina of the premaxillary is moderately robust.The pterygoids are uniformly tri-radiate structures. The anterior rami terminate at about the mid-level of the orbit, and the medial rami articulate firmly with the anterolateral corner of the otic capsule. The palatines are well-developed elements bearing ventral ridges; the ridges are somewhat irregular inbuckleyi,taurinus, andverrucigerusbut smooth inleprieuriiandpearsoni. The parasphenoids are large elements characterized by acuminate cultriform processes and posterolaterally inclined alary processes. The basal areas of the cultriform processes bear small odontoid protuberances inbuckleyi,taurinus, andverrucigerus, whereas they are smooth inleprieuriiandpearsoni. The prevomers are remarkably uniform, moderately well-developed structures. In each species the anterior ramus lies adjacent to the premaxillary, and the lateral wings form the anterior, medial, and posteromedial margins of the internal nares. The dentigerous processes are characteristically large and angular and bear numerous teeth. The sphenethmoid and otoccipitals are well ossified; a dermal sphenethmoid is present only intaurinus.Fig. 7.Dorsal views of vertebral columns of two species ofOsteocephalus:a.O. leprieurii, KU 125962, ♀; b.O. buckleyi, USNM 165997, ♀. ×2.Vertebral Column.—The cervical cotyles are uniformly widely displaced. The neural arches are low and non-imbricate. The transverse processes of the third presacral vertebrae are approximately equal in width to the sacral diapophyses in all species, exceptbuckleyi, in which the processes of the third presacral are slightly narrower than the diapophyses.Osteocephalus buckleyiis further distinguished by the presence of narrow transverse processes on presacrals five through eight (Fig. 7b); males have narrower processes than do females. The processes are moderately wide but subequal in width inpearsoni,taurinus, andverrucigerus, whereas they are nearly equivalent in width to one another and to the sacral diapophyses inleprieurii(Fig. 7a). Thesacraldiapophyses of all species are moderately dilated and posterolaterally inclined. The coccyx bears a distinct dorsal ridge and has a bicondylar articulation with the sacrum.Pectoral Girdle.—The pectoral girdles are fully arciferal and bear small, cartilaginous omosterna and moderately large cartilaginous sterna. The coracoids are robust, and the clavicles are strongly arched. Procoracoid cartilage seems to be absent. Thescapulae are large, longer than the clavicles, and bicapitate proximally. The suprascapulae are moderately large and well ossified inleprieuriiandtaurinus. The suprascapula ofverrucigerusis poorly ossified, and that ofbuckleyiis not ossified.Pelvic Girdle.—The ilia ofbuckleyi,taurinus, andverrucigeruslack any indication of a crest on the shaft, whereasleprieuriihas a low crest. The dorsal acetabular expansion of the ilia is moderately low intaurinusandverrucigerus, but distinctly lower inbuckleyiandleprieurii. The ilia of all species bear low dorsal protuberances. The ischia ofleprieurii,taurinus, andverrucigerusare moderately expanded; that ofbuckleyiis somewhat less expanded dorsally. The pubis ofleprieurii,taurinus, andverrucigerusare calcified, whereas that ofbuckleyiremains cartilaginous.Throat Musculature and Vocal Sac Structure.—Tyler (1971) described the throat myology ofOsteocephalus. The genus is characterized by a moderate-sized araphic submentalis muscle and an undifferentiated intermandibularis having an elongate median aponeurosis. The intermandibularis and submentalis are completely independent inbuckleyi, whereas in the other species there is a small attachment between these muscles.According to Tyler (pers. com.),Osteocephalushas three distinctive types of vocal sac structure which result from differences in the development of the interhyoideus muscle and the overlying skin. Inleprieuriiandverrucigerusthe supramandibular portions of the interhyoideus form a simple tubular, posterolateral extension; there is no modification of the associated skin.Osteocephalus buckleyiandpearsonihave more extensive development of the supramandibular portions of the interhyoideus; furthermore, the associated skin forms a broad, loose fold extending from the ventromedial surface of the throat dorsolaterally to the base of the supratympanic fold. Likebuckleyiandpearsoni, the supramandibular portion of the interhyoideus is much expanded intaurinus. The vocal sac structure oftaurinusdiffers from that of other members of the genus in that the skin oftaurinusforms an everted pouch, which dangles loosely beneath the supratympanic fold.Key to the Species ofOsteocephalus1.Inner edge of third finger webbed to mid-length of antepenultimate phalange; dorsum brown with dark brown spots or median blotch; skull in adults casqued and co-ossified with prominent supraorbital flangesO. taurinusInner edge of third finger webbed to base of antepenultimate phalange; dorsum plain or marked with dark blotches or transverse bars; skull in adults smooth or slightly exostosed, lacking supraorbital flanges22.Skin on flanks areolate; dorsum in males bearing a mixture of large and small non-spinous tubercles; lips distinctly barredO. buckleyiSkin on flanks smooth; dorsum in males bearing tubercles of uniform size; lips not barred33.Dorsal pattern consisting of narrow transverse dark bars; dorsum in males bearing numerous small spinous tuberclesO. leprieuriiDorsal pattern not consisting of transverse bars; dorsal tubercles large or few in number44.Dorsum uniformly dark brown; venter heavily mottled with black, especially in females; dorsum in males bearing large, keratinized tuberclesO. verrucigerusDorsum tan with irregular dark brown blotches; venter cream with fine brown reticulations; dorsum in males bearing few, small non-spinous tuberclesO. pearsoni
OCCASIONAL PAPERS
of the
MUSEUM OF NATURAL HISTORYThe University of KansasLawrence, Kansas
A SYNOPSIS OF NEOTROPICAL HYLID FROGS,GENUSOSTEOCEPHALUS
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.
[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 geographicvariation 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 ofOsteocephalusare from Ecuador, a relatively small part of the total range of the genus.
In this paper we are presenting a taxonomic review of the genusOsteocephalus; 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 ofOsteocephalus. Michael J. Tyler of the South Australian Museum provided information on the vocal sac structure. We extend oursincere 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 genusOsteocephalus; 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, exceptO. pearsoni, but we have colored photographs of a living specimen of that species. Figures1and2were 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:
AMNHAmerican Museum of Natural HistoryANSPAcademy of Natural Sciences of PhiladelphiaASUArizona State UniversityAUMAuburn University MuseumBMNHBritish Museum (Natural History)CASCalifornia Academy of SciencesCAS-SUStanford University Collection (In California Academy of Sciences)CMCarnegie MuseumFMNHField Museum of Natural HistoryKUUniversity of Kansas Museum of Natural HistoryMCZMuseum of Comparative Zoology, Harvard UniversityMIZSMuseo ed Istituto di Zoologi Sistematico, Università di TorinoMJPMuseo Javier Prado, LimaMNHNMuséum National d'Histoire Naturelle, ParisMPEGMuseu Paraense Emiliano Goeldi, BelémMVZMuseum of Vertebrate Zoology, University of California, BerkeleyMZUSPMuseu de Zoología, Universidade da São PauloNHMGNaturhistoriska Museet GöteborgNHMWNaturhistorisches Museum, WienNHRMNaturhistoriska Riksmuseet, StockholmRMNHRijksmuseum van Natuurlijke Histoire, LeidenSMFSenckenbergische Museum, FrankfurtUIMNHUniversity of Illinois, Museum of Natural HistoryUMMZUniversity of Michigan Museum of ZoologyUPUniversité de ParisUPR-MUniversity of Puerto Rico, MayagüezUTAUniversity of Texas, ArlingtonUSNMUnited States National MuseumUZMUniversitets Zoologiske Museum, CopenhagenWCABWerner C. A. Bokermann, São Paulo, BrasilZMBZoologisches Museum BerlinZSMZoologisches Sammlung München
HISTORICAL RESUMÉ
Because of the taxonomic confusion that has surrounded the generic nameOsteocephalusand 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 nameHyla leprieurii. The description of the species is fairly detailed, but the specimen was not illustrated. This is the earliest trivial name now associated withOsteocephalus.
Fitzinger (1843) in his generic synopsis of amphibians and reptiles proposed the generic nameOsteocephalusbut did not associate a specific name with the genus. Consequently,OsteocephalusFitzinger, 1843, is anomen 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 ofOsteocephaluson the basis of Brasilian specimens collected by Johann Natterer. Both species were named in the same publication;O. taurinusappeared on page 77, andO. favolineatus, on p. 80. This is the earliest association of the generic nameOsteocephaluswith 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 nameOsteocephalus, which hasO. taurinusas the type species by original designation. It is not possible to determine whether or not Steindachner's usage ofOsteocephaluswas 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 betweenTrachycephalus nigromaculatusTschudi, 1838, andOsteocephalus taurinus, Steindachner (1867) used the combinationTrachycephalus (Osteocephalus) taurinus. This ambiguous usage for the 1860's precludes our determining if Steindachner was in effect synonymizingOsteocephaluswithTrachycephalusor whether he was placingOsteocephalusin a subgeneric status. Steindachner (1867) did not mentionO. flavolineatus; perhaps by that time he had concluded thatflavolineatuswas only a color morph oftaurinus.
Cope (1867) placedHyla leprieuriiin the genusHypsiboasWagler, 1830. Cope (1874) namedOsteocephalus planicepsfrom 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 bothOsteocephalusandTrachycephalusinthe synonymy ofHyla; he recognizedHyla taurina(withO. flavolineatusas a synonym),H. leprieurii, andH. planiceps. In the same publication Boulenger namedHyla buckleyion the basis of 10 specimens in the British Museum from Ecuador; in the description he stated thatbuckleyiwas likeleprieuriiandtaurinusin having paired lateral vocal sacs. Boulenger held a lasting influence on taxonomic herpetology, and his generic synonymy ofOsteocephaluswas unchallenged until only a decade ago.
Goin (1961) presented a generic synopsis of the genera of hylid frogs, in which he recognizedOsteocephalusand stated: "There are perhaps eight or ten species of this genus in South America. Certainlytaurinus,britti,leprieuri,buckleyiandpearsonibelong here.O. planicepsis surely a synonym ofleprieuriand I believe thatgarbeiis as well. The status of such forms asmacrotis,riopastazae, anddepressahas not yet been settled." Goin definedOsteocephalusas 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 onlyO. taurinusandO. leprieuriiin the genus.
Goin's inclusion ofbuckleyi,britti, andpearsoniinOsteocephaluswas the first association of any of these names with that genus. Duellman (1970a) demonstrated thatGarbeana garbeiMiranda-Ribeiro, 1926, was a member of theHyla rubragroup.Hyla macrotisAndersson, 1945, is aPhrynohyas. Trueb and Duellman (1970) determined thatHyla verrucigeraWerner, 1901, is the earliest name for anOsteocephalusdisplaying striking sexual dimorphism in coloration and texture of the dorsal skin;Hyla riopastazaeAndersson, 1945 (female holotype), andHyla orcesiFunkhouser, 1956 (male holotype), were placed in the synonymy ofOsteocephalus verrucigerus.
Hyla pearsoniGaige, 1929, is a small species ofOsteocephalus. Our findings substantiate Goin's suggestions relative to two other taxa.Hyla leprieurii brittiMelin, 1941, from the Rio Uaupés, Brasil, andHyla depressaAndersson, 1945, from the Río Pastaza watershed, Ecuador, are members of the genusOsteocephalus, but both are synonyms of earlier names—leprieuriiandtaurinus, respectively. Another name proposed by Melin (1941),Hyla (Trachycephalus) vilarsifrom Taracuá, Brasil, also is placed in the synonymy ofO. taurinus.
Cochran and Goin (1970) were unaware of the identities ofHyla verrucigeraandriopastazae; they used the later nameOsteocephalus orcesifor Colombian frogs that are correctly referred toO. verrucigerus. Although Goin (1961) placedHyla buckleyiandH. pearsoniinOsteocephalus, Cochran and Goin (1970) recognized a "buckleyigroup" inHylathat included these two species plus a new species,Hyla cabreraifrom Amazonian Colombia and Brasil (total of three specimens). Also, these authors namedHyla carrifrom a single Colombian specimen. Study of the types ofHyla cabrerai,H. carri, andH. festaePeracca, 1904, from Ecuador, reveal that all of these names are synonyms ofOsteocephalus buckleyi.
Much of the taxonomic confusion and multiplicity of trivial names is due to the great amount of color variation intaurinusand 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 genusOsteocephalusare listed intable 1.
OsteocephalusSteindachner, 1862
OsteocephalusSteindachner, 1862:77 [Type species.—Osteocephalus taurinusSteindachner, 1862, by original designation]. NotOsteocephalusFitzinger, 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 elongatemedian aponeurosis; 9) parotoid glands absent or poorly developed, skin not producing viscous secretion characteristic ofPhrynohyas; 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 ofOsteocephalus.
Content.—As defined here, the genus contains five known species:O. buckleyi(Boulenger),O. leprieurii(Duméril and Bibron),O. pearsoni(Gaige),O. taurinusSteindachner, andO. 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 genusOsteocephalusare moderate to large hylids. The largest species istaurinus, attaining a snout-vent length of 103.1 mm; the smallest ispearsoni, which attains a length of 54.7 mm. Considerable intraspecific geographic variation occurs in adult size, especially intaurinus. 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 ofOsteocephalus.(Means are given in parentheses below observed ranges)
Coloration.—AllOsteocephalusare predominantly brown frogs usually with some darker dorsal markings (Figs. 1 and 2).Osteocephalus verrucigerushas 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 inbuckleyi,pearsoni, andtaurinusbut are narrow transverse marks inleprieurii. A narrow middorsal cream or yellow stripe is present in some individuals ofbuckleyiandtaurinusbut absent in all individuals of the other species. The flanks are uniform pale tan inleprieuriiand uniform reddish brown inverrucigerus; in the other species the flanks are cream to brown with dark brown or black spots (also dark diagonal marks in somebuckleyi). A creamy white anal stripe is present in some specimens ofleprieuriibut absent in all individuals of other species.
The postocular region, encompassing the tympanum, is dark brown in most specimens. In adults ofpearsoniandtaurinusthe upper lips are dark brown. A pale cream or tan suborbital spot is present inpearsoniand in sometaurinus; in some specimens oftaurinusthe suborbital spot is expanded posteriorly forming a labial stripe on the posterior part of the lip. The labial markings ofverrucigerusare similar to the latter pattern, except that in females a distinct, light labial stripe extends the length of the lip.Osteocephalus leprieuriihas a distinct, broad, pale labial stripe. The lips are barred cream and dark brown inbuckleyi.
The venter is uniform creamy white or pale tan inleprieurii, uniform white in somebuckleyi(most males), and uniform tan in sometaurinus. The other species and some individuals oftaurinusandbuckleyi(most females) have dark ventral markings. These markings are most distinctive inverrucigerus, in which the venter is white with bold black mottling and spots (Fig. 3c). Those individuals oftaurinushaving ventral markings usually have indistinct, diffuse brown spots on the throat and chest (Fig. 3b).Osteocephalus pearsoniis characterized by a fine brown reticulation on the venter and on the anterior and posterior surfaces of the thighs in adults (Fig. 3a). Individuals ofbuckleyithat have ventral markings vary between the patterns illustrated forpearsoniandtaurinus(Figs. 3b and c).
Ontogenetic change in coloration is slight or non-existent inbuckleyi,pearsoni, andtaurinus, except that juveniles lack ventral markings. A dark blotch on the back and distinct transverse bars on the limbs are evident in juveniles ofverrucigerus; these markings are obscured in the adults. Juveniles ofleprieuriiare olive-brown with yellow dorsolateral stripes; the transverse dark marks, characteristic of the adults, appear before the stripes are lost.
Fig. 1.Species ofOsteocephalus:Top.O. pearsoni, KU 136312, ♂;Middle.O. buckleyi, KU 123172, ♂;Bottom.O. verrucigerus, KU 123177, ♂. ×1.5.
Fig. 1.Species ofOsteocephalus:Top.O. pearsoni, KU 136312, ♂;Middle.O. buckleyi, KU 123172, ♂;Bottom.O. verrucigerus, KU 123177, ♂. ×1.5.
Fig. 2.Species ofOsteocephalus:Top.O. leprieurii, KU 126611, ♀;Bottom.O. taurinus, KU 126648, ♂. ×10.
Fig. 2.Species ofOsteocephalus:Top.O. leprieurii, KU 126611, ♀;Bottom.O. taurinus, KU 126648, ♂. ×10.
Fig. 3.Diagrammatic views of ventral color patterns inOsteocephalus:a.O. pearsoni, UMMZ 57533, ♂;b.O. taurinus, USNM 166037, ♂;c.O. verrucigerus, KU 123185, ♀.
Fig. 3.Diagrammatic views of ventral color patterns inOsteocephalus:a.O. pearsoni, UMMZ 57533, ♂;b.O. taurinus, USNM 166037, ♂;c.O. verrucigerus, KU 123185, ♀.
Skin.—The dorsal skin of all males ofOsteocephalusis tuberculate to varying degrees, whereas the dorsal skin of females is smooth, or nearly so (Fig. 4).Osteocephalus verrucigerusdiffers from other members of the genus by the presence of numerous, large tubercles bearing keratinized tips. The tubercles ofleprieuriiare numerous and spinous but much smaller than those ofverrucigerus; those oftaurinusare spinous but less numerous than inleprieurii.Osteocephalus buckleyihas a mixture of large and small, non-spinous tubercles, andpearsonihas only a few, small, scattered, non-spinous tubercles. Fleshy tubercles occur on the eyelids and supratympanic fold in females ofbuckleyi; a few small tubercles are present on the back of females ofpearsoni, whereas the dorsal skin in females of the other species is smooth. The skin on the flanks of both sexes ofbuckleyiis weakly areolate; in the other species the flanks are smooth. The skin on the top of the head intaurinusis rugose as a consequence of co-ossification. In all species the anal opening is directed posteriorly at the upper level of the thighs.
Hands and Feet.—The feet ofOsteocephalusare fully webbed ornearly so. Webbing between fingers one and two is basal in all species. Webbing between fingers two, three, and four is most extensive intaurinus, in which the three fingers are about one-half webbed (Fig. 5).Osteocephalus buckleyi,pearsoni, andverrucigerushave reduced webbing between fingers two and three, andleprieuriihas reduced webbing between fingers two, three, and four. All members of the genus have well-developed subconical subarticular tubercles on the fingers and toes; there is a tendency for the distal tubercle on the fourth finger to be weakly bifid. Palmar and plantar supernumerary tubercles are well developed intaurinus, moderately developed inbuckleyi,leprieurii, andpearsoni, and barely evident inverrucigerus. All of the species have a noticeable fold on the wrist and enlarged prepollices, bearing horny nuptial excrescences in breeding males. The prepollex is least enlarged inbuckleyi. Outer metatarsal tubercles are absent. The inner metatarsal tubercle is moderately well developed and ovoid inleprieuriiandpearsoni; it is elliptical and flat in the other species. Tarsal folds are absent in all species exceptverrucigerus, in which the folds are barely evident.
Fig. 4.Segments of dorsal skin of males ofOsteocephalusshowing size and arrangement of tubercles:a.O. verrucigerus, KU 123183; b.O. taurinus, USNM 166033; c.O. leprieurii, KU 126616; d.O. buckleyi, USNM 165999.Each square = 1 sq. cm.
Fig. 4.Segments of dorsal skin of males ofOsteocephalusshowing size and arrangement of tubercles:a.O. verrucigerus, KU 123183; b.O. taurinus, USNM 166033; c.O. leprieurii, KU 126616; d.O. buckleyi, USNM 165999.Each square = 1 sq. cm.
Cranium.—As a genus, the cranial structure is remarkably uniform and quite generalized when viewed in the context of the family Hylidae. The skulls are broad and relatively flat, each being only slightly more broad than long and about one-third as high as long. In dorsal aspect the snouts are broadly rounded; the snout ofbuckleyiis somewhat less rounded and appears to be slightly longer than the snouts of other species. This subtle difference relates to the relative narrowness of the premaxillaries inbuckleyi.
Fig. 5.Palmar views of hands of males ofOsteocephalus:a.O. buckleyi, KU 109506; b.O. leprieurii, KU 126627; c.O. pearsoni, MCZ 15565; d.O. taurinus, KU 126653; e.O. verrucigerus, KU 123177. ×4.
Fig. 5.Palmar views of hands of males ofOsteocephalus:a.O. buckleyi, KU 109506; b.O. leprieurii, KU 126627; c.O. pearsoni, MCZ 15565; d.O. taurinus, KU 126653; e.O. verrucigerus, KU 123177. ×4.
Fig. 6.Skulls of two species ofOsteocephalus:a and b.O. leprieurii, KU 125961; c and d.O. pearsoni, UMMZ 67465. ×3.
Fig. 6.Skulls of two species ofOsteocephalus:a and b.O. leprieurii, KU 125961; c and d.O. pearsoni, UMMZ 67465. ×3.
The genus is characterized by well-developed dermal roofing bones and an unusually large exposure of the sphenethmoid dorsally (Fig. 6). The conformation of the sphenethmoid exposed dorsally is determined by the marginal positions of the adjacent, overlapping elements—the nasals and frontoparietals. Medially the nasals overlap the lateral margins of the sphenethmoid. Anteromedially, the nasals converge inleprieuriiandtaurinus, are narrowly separated inbuckleyiandpearsoni, or are more widely separated inverrucigerus. In all species the nasals terminate at the anterodorsal corner of the orbit. The frontoparietals ofbuckleyi,leprieurii, andtaurinushave an anterolateral extension, which marginally overlaps the dorsolateral edge of the sphenethmoid and articulates with the posterodorsal corner of the nasal inbuckleyiandtaurinus; the bones are narrowly separated inleprieurii. The frontoparietals ofpearsoniandverrucigerushave more extensive median ossification and less extensive anterolateral ossification. Thus, in those species the posteromedian portion of the sphenethmoid is obscured, and thelateral margins are partly exposed. The frontoparietal fontanelle is completely covered in all species, exceptbuckleyiandleprieurii, in which an irregular, median separation of the frontoparietals exposes a small portion of the fontanelle. The posterolateral margins of the frontoparietals lie medial to the epiotic eminences.
Dermal ornamentation, involving the nasals, frontoparietals, and sphenethmoid, occurs intaurinusand, to a limited extent, inpearsoni. In the latter species marginal portions of the frontoparietals, the dorsal surfaces of the nasals, and the posteromedial part of the exposed sphenethmoid are slightly exostosed, resulting in an open, reticulate pattern of dermal sculpturing of exceedingly low relief (Fig. 6c).Osteocephalus taurinusis characterized by casquing, co-ossification, and a rather intricate pattern of dermal sculpturing, which was described in detail and illustrated by Trueb (1970a).
The squamosals of all species are moderately large structures having otic plates that overlie the lateral portion of the cristae paroticae. The posterior rami are short; the zygomatic rami of all species, excepttaurinus, extend slightly more than one-half of the distance to the maxillary. Intaurinusthe zygomatic ramus extends nearly to, or articulates with, the maxillary.
The maxillary arches are complete and relatively robust. The alary processes of the premaxillaries are vertically oriented inleprieurii,pearsoni, andtaurinusand very slightly inclined posteriorly inbuckleyiandverrucigerus. The maxillaries are uniformly characterized by the absence of postorbital processes and by the presence of preorbital processes that articulate with the maxillary processes of the nasals. The partes facialae of the maxillaries are moderately developed in all species, excepttaurinus, in which the pars fascialis tends to articulate with the lateral margin of the nasal in well-ossified individuals. The partes palatinae are poorly developed in all species, exceptbuckleyi, in which the pars palatina of the premaxillary is moderately robust.
The pterygoids are uniformly tri-radiate structures. The anterior rami terminate at about the mid-level of the orbit, and the medial rami articulate firmly with the anterolateral corner of the otic capsule. The palatines are well-developed elements bearing ventral ridges; the ridges are somewhat irregular inbuckleyi,taurinus, andverrucigerusbut smooth inleprieuriiandpearsoni. The parasphenoids are large elements characterized by acuminate cultriform processes and posterolaterally inclined alary processes. The basal areas of the cultriform processes bear small odontoid protuberances inbuckleyi,taurinus, andverrucigerus, whereas they are smooth inleprieuriiandpearsoni. The prevomers are remarkably uniform, moderately well-developed structures. In each species the anterior ramus lies adjacent to the premaxillary, and the lateral wings form the anterior, medial, and posteromedial margins of the internal nares. The dentigerous processes are characteristically large and angular and bear numerous teeth. The sphenethmoid and otoccipitals are well ossified; a dermal sphenethmoid is present only intaurinus.
Fig. 7.Dorsal views of vertebral columns of two species ofOsteocephalus:a.O. leprieurii, KU 125962, ♀; b.O. buckleyi, USNM 165997, ♀. ×2.
Fig. 7.Dorsal views of vertebral columns of two species ofOsteocephalus:a.O. leprieurii, KU 125962, ♀; b.O. buckleyi, USNM 165997, ♀. ×2.
Vertebral Column.—The cervical cotyles are uniformly widely displaced. The neural arches are low and non-imbricate. The transverse processes of the third presacral vertebrae are approximately equal in width to the sacral diapophyses in all species, exceptbuckleyi, in which the processes of the third presacral are slightly narrower than the diapophyses.Osteocephalus buckleyiis further distinguished by the presence of narrow transverse processes on presacrals five through eight (Fig. 7b); males have narrower processes than do females. The processes are moderately wide but subequal in width inpearsoni,taurinus, andverrucigerus, whereas they are nearly equivalent in width to one another and to the sacral diapophyses inleprieurii(Fig. 7a). Thesacraldiapophyses of all species are moderately dilated and posterolaterally inclined. The coccyx bears a distinct dorsal ridge and has a bicondylar articulation with the sacrum.
Pectoral Girdle.—The pectoral girdles are fully arciferal and bear small, cartilaginous omosterna and moderately large cartilaginous sterna. The coracoids are robust, and the clavicles are strongly arched. Procoracoid cartilage seems to be absent. Thescapulae are large, longer than the clavicles, and bicapitate proximally. The suprascapulae are moderately large and well ossified inleprieuriiandtaurinus. The suprascapula ofverrucigerusis poorly ossified, and that ofbuckleyiis not ossified.
Pelvic Girdle.—The ilia ofbuckleyi,taurinus, andverrucigeruslack any indication of a crest on the shaft, whereasleprieuriihas a low crest. The dorsal acetabular expansion of the ilia is moderately low intaurinusandverrucigerus, but distinctly lower inbuckleyiandleprieurii. The ilia of all species bear low dorsal protuberances. The ischia ofleprieurii,taurinus, andverrucigerusare moderately expanded; that ofbuckleyiis somewhat less expanded dorsally. The pubis ofleprieurii,taurinus, andverrucigerusare calcified, whereas that ofbuckleyiremains cartilaginous.
Throat Musculature and Vocal Sac Structure.—Tyler (1971) described the throat myology ofOsteocephalus. The genus is characterized by a moderate-sized araphic submentalis muscle and an undifferentiated intermandibularis having an elongate median aponeurosis. The intermandibularis and submentalis are completely independent inbuckleyi, whereas in the other species there is a small attachment between these muscles.
According to Tyler (pers. com.),Osteocephalushas three distinctive types of vocal sac structure which result from differences in the development of the interhyoideus muscle and the overlying skin. Inleprieuriiandverrucigerusthe supramandibular portions of the interhyoideus form a simple tubular, posterolateral extension; there is no modification of the associated skin.Osteocephalus buckleyiandpearsonihave more extensive development of the supramandibular portions of the interhyoideus; furthermore, the associated skin forms a broad, loose fold extending from the ventromedial surface of the throat dorsolaterally to the base of the supratympanic fold. Likebuckleyiandpearsoni, the supramandibular portion of the interhyoideus is much expanded intaurinus. The vocal sac structure oftaurinusdiffers from that of other members of the genus in that the skin oftaurinusforms an everted pouch, which dangles loosely beneath the supratympanic fold.
Key to the Species ofOsteocephalus