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Papéis Avulsos de Zoologia

Print version ISSN 0031-1049

Pap. Avulsos Zool. (São Paulo) vol.51 no.2 São Paulo  2011

http://dx.doi.org/10.1590/S0031-10492011000200001 

Distribution, vocalization and taxonomic status of hypsiboas roraima and h. angelicus (Amphibia: Anura: Hylidae)

 

 

César L. Barrio-AmorósI, *; Josefa Celsa SeñarisII; Ross D. MaccullochIII; Amy LathropIII; Juan M. GuayasaminIV; William E. DuellmanV

IFundación AndígenA, Apartado Postal 210, 5101 A, Mérida, Venezuela
IIMuseo de Historia Natural La Salle, Apartado 1930, Caracas 1010 A, Venezuela
IIICentre for Biodiversity and Conservation Biology, Royal Ontario Museum, Toronto, Ontario, Canada
IVMuseo de Zoología, Escuela de Ciencias Biológicas, Pontificia Universidad Católica del Ecuador, Quito, Ecuador
VDivision of Herpetology, Biodiversity Institute, The University of Kansas, Lawrence, Kansas, USA

 

 


ABSTRACT

The distribution of the poorly known hylid frog Hypsiboas roraima Duellman & Hoogmoed, on the Guiana Shield is redefined, including new records from Venezuela. The advertisement call of this species is analyzed and Hypsiboas angelicus Myers & Donnelly is associated as a junior synonym of H. roraima.

Keywords: Hypsiboas roraima; H. angelicus; Hylidae; Guiana Shield; Guyana; Venezuela.


RESUMEN

Redefinimos la distribución del hílido guayanés Hypsiboas roraima Duellman & Hoogmoed. Analizamos su canto y consideramos Hypsiboas angelicus Myers & Donnelly como un sinónimo menor de H. roraima.

Palabras-clave: Hypsiboas roraima; H. angelicus; Hylidae; Escudo Guayanés; Guyana; Venezuela.


 

 

INTRODUCTION

Hypsiboas roraima (Fig. 1) was described from three females collected at elevations of 1430-1480 m on the northern slopes of Mount Roraima in Guyana. Originally, the species was described as Hyla roraima and assigned to the Hyla geographica group (Duellman & Hoogmoed, 1992). Hypsiboas roraima superficially resembles H. fasciatus but the latter exhibits bold markings on the posterior surfaces of the thighs (absent in H. roraima). A comprehensive comparison of H. roraima with other sympatric hylids can be found in Duellman & Hoogmoed (1992). Faivovich et al. (2005) presented a phylogenetic analysis of the family Hylidae, placed this species in the genus Hypsiboas, and more particularly within the Hypsiboas benitezi Group (with no close relationship with H. fasciatus which is currently in the Hypsiboas albopunctatus Group after Faivovich et al., 2005), supported mainly by molecular data and by the presence of flat mental gland.

MacCulloch & Lathrop (2005) extended the distribution of Hypsiboas roraima to Mount Ayanganna, Guyana, at 870-1550 m and offered a more complete description of the species based on 18 females and 11 males. Up to this point, the species was reported only in Guyana, but its presence in Venezuela was expected (Barrio-Amorós, 1998, 2004) inasmuch as the type locality is on the northern slopes of Mount Roraima, a tepui that includes the triple border point of Venezuela, Guyana, and Brazil. Simultaneously, Barrio-Amorós & Duellman (2009) and Señaris et al. (2009) reported Hypsiboas roraima from Venezuela, although without mentioning any voucher specimen.

Recently, Myers & Donnelly (2008) described Hypsiboas angelicus from a single specimen collected on the summit of Auyán-tepui in Bolivar state, Venezuela. They mentioned its remarkably similarity to Hypsiboas roraima, distinguished only by the pattern of pigmentation on the palpebral membrane.

Herein, we redefine the distribution of Hypsiboas roraima, describe its advertisement call, and associated Hypsiboas angelicus Myers & Donnelly as a junior synonym of H. roraima Duellman & Hoogmoed.

 

MATERIAL AND METHODS

We examined all available specimens of Hypsiboas roraima and the single specimen of H. angelicus. Thirteen measurements on each specimen were made using digital callipers to 0.1 mm: SVL: snout-vent length; SL: shank length from outer edge of flexed knee to heel; FL: foot length from proximal edge of outer metatarsal tubercle to tip of toe IV; HeL: head length from tip of snout to the posterior border of skull; HW: head width between angle of jaws; ED: horizontal eye diameter; IOD: inter-orbital distance between proximal edges of eyelids; UEW: upper eyelid width; TD: horizontal tympanum diameter; F3D: width of Finger III; T4D: width of Toe IV; 1FiL: length of Finger I from inner edge of thenar tubercle to tip of finger; 2FiL: length of Finger II from inner edge of thenar tubercle to the tip of finger. Life and/or preserved color patterns were analysed. Vocalizations were recorded by JCS using a Sony WM D6C with a Sennheiser directional microphone model Me-80. The recording was digitized at a sampling rate of 22050 Hz and size of 16 bits and analyzed using Canary 1.2 software (Charif et al., 1995) on a Macintosh computer. Institutional acronyms follow Frost (2009) with the exception of UGDB - University of Guyana Department of Biology (now UG-CSBD).

 

RESULTS AND DISCUSSION

Venezuelan specimens of Hypsiboas roraima

After the report of Hypsiboas roraima from Sierra de Lema, Venezuela (Barrio-Amorós & Duellman, 2009), there are further observations, which expand its distribution and provide data on its natural history. During a survey of the herpetofauna of the Río Cucurital Basin in the western part of Canaima National Park in Venezuela, JCS collected two specimens of Hypsiboas roraima on the slopes of Auyán-tepui at 950-1000 m (Señaris et al., 2009). These specimens (MHNLS 16085, 16086) were calling inside arboreal bromeliads in a shrubby area adjacent to Quebrada Rutapá, a tributary of the Cucurital river (05°43'17.7"N, 62°34'21.1"W, 950 m) on 9 November 2002.

A specimen (MHNLS 11380) collected by S. Gorzula on 28 February 1988 at Sur Sima Aonda (06°00'N, 62°35'W, 1600 m) on the summit of Auyán-tepui was reported as "Hylid species b" by Gorzula & Señaris (1999). Another specimen (MHNLS 11101) was collected by S. Gorzula on 26 November 1982 at "Caminata Uno" Guayaraca (05°42'N, 62°31'W, 950 m) on the southern slope of Auyán-tepui. This specimen was misidentified as "Scinax species a" by Gorzula & Señaris (1999), who mentioned its close similarity to other specimens collected by J. Ayarzagüena from La Escalera region in Sierra de Lema. Two specimens (MHNLS 10103 and KU 181072, Fig. 1C) are from higher elevations in the Sierra de Lema, Salto El Danto (1150 m), and km 112 on the El Dorado-Santa Elena de Uairén road (860 m), respectively. CLBA found an adult female (MHNLS 19656) at La Laja, Sierra de Lema (05°57'N, 61°30'W, 490 m) (Fig. 1B, D), and a subadult female (MHNLS 19657) at El Peñón, on the southern slope of Auyán-tepui, 1700 m (Fig. 1A).

Distribution and Habitat

In addition to the Venezuelan localities mentioned above, Hypsiboas roraima is known from Mounts Roraima, Ayanganna, and Wokomung in Guyana (Fig. 2). Although it has not been reported from Brazil, its presence in northern Roraima State is expected. The elevation range of the species is from 490 m at La Laja (Sierra de Lema) to 1700 m at Auyán-tepui summit. Only a few hylids have been reported from above 1500 m (Señaris & Ayarzagüena, 2002; MacCulloch et al., 2007) in the eastern Pantepui highlands (with the exception of H. roraima at Auyán-tepui and H. jimenezi at Auyán-tepui and Chimantá Gorzula, 1992; Señaris et al., 2009, and several species of Tepuihyla and Myersohyla McDiarmid & Donnelly 2005). Hypsiboas roraima is nocturnal. Some specimens were collected on branches or leaves in forest. Two males (MHNLS 16085-16086) were detected at night by their calls and both were calling in arboreal bromeliads between 2.5 and 4 m above the ground. The only water available in the area was inside leaves of bromeliads. A male (MHNLS 11101) was found on an epiphytic bromeliad on a tree, similar to the observations for MHNLS 10103 in the Sierra de Lema (J. Ayarzagüena, field notes May 1986). Based on a comment by D.B. Means, Faivovich et al. (2006) mentioned that males of Hypsiboas roraima call from bromeliads close to small streams.

 

 

Vocalization

Advertisement calls of Hypsiboas roraima from Quebrada Rutapá, headwater of Río Cucurital, Canaima National Park, Bolívar State, Venezuela (MHNLS 16085), were recorded on 8 November 2002, between 07:45 and 08:30 PM, at 22°C. The call consists of one modulated note (Fig. 3) repeated continuously, with a rate of 3-5 calls per second (180-300 calls/minute). The notes duration vary from 14.1 to 23.7 msec (x = 19.05 ± 2.9, n = 52) and the notes intervals from 200.7 to 417.4 msec (x = 285,5 ± 52,01, n = 51). The fundamental frequency ranges from 1600 to 1700 Hz and the dominant frequency from 2540 Hz to 2661 Hz (x = 2616 ± 33, n = 22). Other harmonics appear at 5050-5170 Hz, 7278-7903 Hz, 10150-10160 Hz and 12092-12854 Hz (Fig. 3A, B).

 


 

Compared with the recorded vocalization of Hypsiboas roraima, the advertisement call of H. angelicus (Myers & Donnelly, 2008) also is a long train of short "beeps" for one minute at 16.4°C (taken at 1600 m). The rate was 2.6 notes per minute and the dominant frequency rises from 1800 to 2400 Hz. The variation between the call of both species could be attributed to the differences in air temperature, as in the case of Hyloscirtus labialis (Lüddecke & Sánchez, 2002).

Morphology and Color Pattern

Measurements of all examined specimens are in Table 1. All measurements fall within the ranges reported by Duellman & Hoogmoed (1992) and MacCulloch & Lathrop (2005).

Although MacCulloch & Lathrop (2005) reported no webbing on the hand in H. roraima, basal webbing is present in all specimens, as illustrated in Duellman & Hoogmoed (1992).

Myers & Donnelly (2008:29-30) discuss the presence of elongate tubercles on either side of a vertical channel below the vent in the holotype of H. angelicus. They expressed uncertainty if these tubercles might be diagnostic of H. angelicus or they are resulting from the fusion of round cloacal tubercles. Similar elongate tubercles were found in two specimens of H. roraima from Mount Wokomung, ROM 43423 and 43432, and one male from the base of Auyán-tepui, MHNLS 16085 (Fig. 4A), and less developed in a female from the high slopes of Auyán-tepui, MHNLS 19657 (Fig. 4B). We conclude that the pattern of cloacal tubercles is variable in H. roraima.

Color pattern of nearly all specimens is similar to that reported in Duellman & Hoogmoed (1992) and MacCulloch & Lathrop (2005). Interestingly, none of the Venezuelan specimens exhibits the dorsal pattern of large dark brown patches on a reddish-brown background. Five of seven Venezuelan specimens have a middorsal line (broken in MHNLS 10103). One specimen (MHNLS 10103) has a striking dorsal pattern resembling that of Myersiohyla kanaima (Goin & Woodley). However, other characters, notably iris color (gray with contrasting pupil in preservative in H. roraima vs uniformly black in M. kanaima), conclusively demonstrate that this specimen is H. roraima. Color patterns of Venezuelan specimens are shown in Fig. 1; photos of specimens from Guyana are in MacCulloch & Lathrop (2005).

Pigmentation pattern on the palpebral membrane in Hypsiboas roraima shows considerable individual variation. The holotype of H. angelicus, as referred by Myers & Donnelly (2008), lacks pale (or white) reticulation on the palpebral membrane (Fig. 5A). Most specimens have extensive reticulation (Fig. 5C) and in some it is reduced (Fig. 5B). A few specimens have small unconnected dark brown spots with or without reticulation (Fig. 5D). Color of the pigment also is variable. In most individuals it is white (Fig. 5C), whereas in some specimens it is pale brown (Fig. 5B) or white and brown together (Fig. 5D).

Taxonomic status of Hypsiboas angelicus Myers & Donnelly

Altogether the authors have had the opportunity of examining all known voucher specimens of Hypsiboas roraima (see Appendix) and the holotype of H. angelicus. Myers & Donnelly (2008) described H. angelicus from the summit of Auyán-tepui (1600 m). Although recognizing its close similarity to H. roraima, they defended the particularity of H. angelicus by its lack of pale reticulation on the palpebral membrane (vs. pale reticulation in H. roraima). Myers & Donnelly (2008) stated that because variability in the amount of palpebral membrane reticulation in H. roraima had never been demonstrated, it would serve as a valid character to distinguish H. angelicus from H. roraima.

In a larger series of H. roraima from Guyana (Roraima, Ayanganna, and Wokomung) and Venezuela (Sierra de Lema and Auyán-tepui, including specimens from the summit [type locality of H. angelicus]) we found that the pale (usually bright white, occasionally pale brown) reticulation on the palpebral membrane can be well defined (28 of 46 specimens examined for this character, e.g. MHNLS 16085), poorly defined, represented by small white or brown spots instead of lines (15 of 46, e.g. MHNLS 10103, 16086), or represented by small brown spots (MHNLS 19656 and EBRG 2733, holotype of H. angelicus). Three specimens of 43 (EBRG 2733 - holotype of H. angelicus; MHNLS 11380 and 11101) have no reticulation. The condition of the palpebral membrane in the holotype of H. angelicus, although rare, is within the range of variability exhibited by H. roraima. There are no other characters supporting the validity of the taxon H. angelicus (Table 1; Myers & Donnelly, 2008). Therefore, we consider Hypsiboas angelicus Myers & Donnelly, 2008 as a junior synonym of H. roraima Duellman & Hoogmoed, 1992.

 

ACKNOWLEDGMENTS

CLBA thanks C. Brewer Carías for his support at all times, and for his invitation to the Lema expedition in 2006-2007. CLBA collected under permit 2231 issued by the Venezuelan Ministerio del Ambiente. The Río Cucurital Basin and Auyán-tepui slopes project was made possible by grant Nº 98003384 of the Fondo Nacional de Ciencia, Tecnología e Innovación (FONACIT), the Ministerio del Ambiente y de los Recursos Naturales (MARN), Instituto Nacional de Parques (INPARQUES), and the indigenous communities of Kamaimö and Guayaraca, which provided the permits for fieldwork and collections to JCS (Providencia Administrativa Nº PA-INP-026-2002). Fundación La Salle de Ciencias Naturales (FLSCN) and the tourist camps Parakaupa and Ucaima in the Canaima Lagoon also supported the expeditions to Auyán-tepui slopes. JCS thanks C. Lasso, C. Molina, G. Rivas, and D. Lew for their help in the field. RDM and AL thank B. Hubley, C. Cox, and S. Khan for field assistance. Specimens from Ayanganna and Wokomung were collected and exported under permits 121004 BR 019 and 191104 SP 016 issued by the Guyana Environmental Protection Agency. Specimens were euthanized according to animal use protocols approved by the ROM Animal Care Committee. RDM and AL were funded by grants from the Royal Ontario Museum Governors, the ROM Department of Natural History, and a Smithsonian BDG Fellowship. This is contribution 342 of the Centre for Biodiversity and Conservation Biology, ROM, and number 161 in the Smithsonian's Biological Diversity of the Guiana Shield Program publication series. Duellman's field work in the Sierra de Lema was funded by the National Science Foundation, USA.

 

REFERENCES

BARRIO-AMORÓS, C.L. & DUELLMAN, W.E. 2009. Herpetofauna de la Sierra de Lema, Estado Bolívar, Venezuela. Boletín RAP de Evaluación Ecológica, 55:137-155.         [ Links ]

BARRIO-AMORÓS, C.L. 1998. Sistemática y Biogeografía de los anfibios (Amphibia) de Venezuela. Acta Biologica Venezuelica, 18:1-93.         [ Links ]

BARRIO-AMORÓS, C.L. 2004. Amphibians of Venezuela, Systematic list, Distribution and References, an Update. Revista Ecología Latino Americana, 9:1-48.         [ Links ]

CHARIF, R.A.; MITCHELL, S. & CLARK, C.W. 1995. Canary 1.2 User's Manual. Cornell Laboratory of Ornithology, Ithaca, New York, 229p.         [ Links ]

DUELLMAN, W.E. & HOOGMOED, M.S. 1992. Some hylid frogs from the Guiana Highlands, Northeastern South America: New species, distributional records and generic reallocation. Occasional Papers Museum Natural History University of Kansas, 147:1-21.         [ Links ]

FAIVOVICH, J.; HADDAD, C.F.B.; GARCIA, P.C.A.; FROST, D.R.; CAMPBELL, J.A. & WHEELER, W.C. 2005. Systematic review of the frog family Hylidae, with special reference to Hylinae: phylogenetic analysys and taxonomic revision. Bulletin of the American Museum of Natural History, 294:1-240.         [ Links ]

FAIVOVICH, J.; MORAVEC, J.; CISNEROS-HEREDIA, D.F. & KÖHLER, J. 2006. A new species of the Hypsiboas benitezi Group from the Western Amazon (Amphibia: Anura: Hylidae). Herpetologica, 62:96-108.         [ Links ]

FROST, D.R. 2009. Amphibian Species of the World: an Online Reference. Version 5.3. American Museum of Natural History, New York, USA. Available at: <http://research.amnh.org/herpetology/amphibia> Access in: 12.Feb. 2009.         [ Links ]

GORZULA, S. & SEÑARIS, J.C. 1999. Contribution to the herpetofauna of the Venezuelan Guayana. I. A data base. Scientia Guaianae, 8: 267.         [ Links ]

GORZULA, S. 1992. La herpetofauna del macizo del Chimantá. In: Huber, O. (Ed), El Macizo del Chimantá, Escudo de Guayana. Venezuela. Un ensayo ecológico tepuyano. Todtmann Editores, Caracas, p. 267-280.         [ Links ]

LÜDDECKE, H. & SÁNCHEZ, O.R. 2002. Are tropical highland frog calls cold-adapted? The case of the Andean frog Hyla labialis. Biotropica, 34:281-288.         [ Links ]

MACCULLOCH, R.D. & LATHROP, A. 2005. Hylid frogs from Mount Ayanganna, Guyana: new species, redescriptions, and distributional records. Phyllomedusa, 4(1):17-37.         [ Links ]

MACCULLOCH, R.D.; LATHROP, A.; REYNOLDS, R.P.; SEÑARIS, J.C. & SCHNEIDER, G.E. 2007. Herpetofauna of Mount Roraima, Guiana Shield region, northeastern South America. Herpetological Review, 38:24-30.         [ Links ]

MCDIARMID, R.W. & DONNELLY, M.A. 2005. The Herpetofauna of the Guayana Highlands: Amphibians and Reptiles of the Lost World. In: Donnely, M.A.; Crother, B.I.; Guyer, C.; Wake, M.H. & White, M.E. (Eds.), Ecology and Evolution in the Tropics: A Herpetological Perspective. University of Chicago Press, Chicago, p. 461-560.         [ Links ]

MYERS, C.W & DONNELLY, M.A. 2008. The summit herpetofauna of Auyantepui, Venezuela: Report from the Robert G. Goelet American Museum-TERRAMAR Expedition. Bulletin of the American Museum of Natural History, 308:1-147.         [ Links ]

SEÑARIS, J.C. & AYARZAGÜENA, J. 2002. A new species of Hyla (Anura; Hylidae) from the highlands of Venezuelan Guayana. Journal of Herpetology, 36:634-640.         [ Links ]

SEÑARIS, J.C.; RIVAS, G. & MOLINA, C. 2009. Anfibios y reptiles del Parque Nacional Canaima: In: Señaris, J.C.; Lew, D. & Lasso, C. (Eds.), Biodiversidad del Parque Nacional Canaima: Bases Científicas para la Conservación de la Guayana Venezolana. Fundación La Salle de Ciencias Naturales and The Nature Conservancy, Caracas, p. 70-92.         [ Links ]

 

 

Recebido em: 12.01.2010
Aceito em: 14.12.2010
Publicado em: 31.03.2011

 

 

* Corresponding author: cesarlba@yahoo.com, atelopus@andigena.org

 

 

APPENDIX

Specimens examined

Hypsiboas roraima: Venezuela, Estado Bolívar: EBRG 2733 (holotype of H. angelicus), male from summit of Auyán-tepui, 05°58'N, 62°33'W, 1600 m. MHNLS 16085-16086, from Rutapa creek, Cucurital river, SE slopes of Auyán-tepui, 05°43'17.7"N, 62°34'21.1"W, 950 m. MHNLS 11101, from Guayaraca, southern slope of Auyán-tepui, 05°42'N, 62°31'W, 950 m. MHNLS 11380, from the Auyán-tepui summit, south of Sima Aonda, 06°00'N, 62°35'W, 1600 m. MHNLS 19657, female from El Peñón, southern slopes of Auyán-tepui, 05°03'N, 62°28'W, 1700 m. MHNLS 10103, from Salto El Danto, La Escalera, 05°57'44"N, 61°23'45"W, 1160 m. MHNLS 19656, an adult female from la Laja, Sierra de Lema, 05°57'N, 61°30'W, 490 m. KU 181072, immature female, from La Escalera, km 112 El Dorado-Santa Elena de Uairén road, 06°00'02"N, 61°23'30"W, 860 m. Guyana; Rupununi District: BMNH 1979.560 (holotype), an adult male, KU 182470, UGDB 14 (paratypes), from north slope of Mount Roraima, 05°38'N, 60°44'W, 1480 m. ROM 39596-39627, from Mount Ayanganna, 05°24'N, 59°57'W, 870-1550 m. ROM 43423-43436, from Mount Wokomung, 05°06'N, 59°50'W.

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