Morphology and geographical distribution of the poorly known snake Umbrivaga pygmaea (Serpentes: Dipsadidae) in Brazil

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Phyllomedusa 10(2):177 182, 2011 2011 Departamento de Ciências Biológicas - ESALQ - USP ISSN 1519-1397 Short Communication Morphology and geographical distribution of the poorly known snake Umbrivaga pygmaea (Serpentes: Dipsadidae) in Brazil Ricardo Alexandre Kawashita-Ribeiro 1, Vinícius Tadeu de Carvalho 2, Ana Caroline de Lima 3, Robson Waldemar Ávila 4, and Rafael de Fraga 2 1 Coleção Zoológica de Vertebrados, Instituto de Biociências, Universidade Federal de Mato Grosso. Av. Fernando Corrêa da Costa, s/n, 78060-900, Cuiabá, MT, Brazil. E mail: serpentesbr@gmail.com. 2 Instituto Nacional de Pesquisas da Amazônia, Departamento de Biologia Aquática e Limnologia, Coleção de Anfíbios e Répteis. Av. André Araújo, 2936, 69011-970, Manaus, AM, Brazil. E mails: colubridae@hotmail.com; r.defraga@gmail.com. 3 Programa de Pós-graduação em Zoologia, Universidade Federal do Rio de Janeiro, Museu Nacional. Quinta da Boa Vista s/n, 20940-040, Rio de Janeiro, RJ, Brazil. E mail: analima02@gmail.com. 4 Universidade Regional do Cariri, Centro de Ciências Biológicas e da Saúde, Departamento de Ciências Biológicas, Campus do Pimenta. Rua Cel. Antonio Luiz, 1161, 63105-100, Crato, CE, Brazil. E mail: robsonavila@gmail.com. Keywords: Amazonia, hemipenis, snakes. Palavras-chave: Amazônia, hemipênis, serpentes. The South American snake genus Umbrivaga Roze, 1964, is found in Colombia, Peru, Ecuador, French Guiana, Venezuela, and Brazil (Peters and Orejas-Miranda 1970, Markezich and Dixon 1979, Miyata 1982, Dixon and Soini 1986, Vanzolini 1986, Martins and Oliveira 1998, Fernandes et al. 1999, Vigle 2008, Vidal et al. 2010). Although the validity of this genus remains uncertain (Vidal et al. 2010), three species currently are recognized: U. pygmaea (Cope, 1868), U. mertensi Roze, 1964, and U. pyburni Markezich and Dixon, 1979 (Vidal et al. Received 9 May 2011. Accepted 1 September 2011. Distributed December 2011. 2010). Umbrivaga pygmaea was described by Cope (1868) from an undetermined locality either Napo or the vicinity of Marañon in Peru. It is the most widely distributed species in the genus, with records in Colombia, Ecuador, French Guiana, Peru, and Brazil (Peters and Orejas-Miranda 1970, Markezich and Dixon 1979, Miyata 1982, Dixon and Soini 1986, Vanzolini 1986, Martins and Oliveira 1998, Fernandes et al. 1999, Vigle 2008, Vidal et al. 2010). Despite its broad distribution, specimens are relatively rare in collections and thus, it is poorly known. In Brazil, U. pygmaea was recorded in the municipalities of Manaus and Tefé, state of Amazonas (Martins and Oliveira 1998, Fernandes et al. 1999), and in the municipality of Almerim, state of Pará (Ávila-Pires 177

Kawashita-Ribeiro et al. et al. 2010). Herein, we describe the hemipenis, along with variation in morphological characters and color pattern, and present new distributional data for U. pygmaea in Amazonas, Brazil, based upon new specimens collected in areas of dense forest. We examined seven specimens of Umbrivaga pygmaea housed in two Brazilian collections the Herpetological Collection of the Instituto Nacional de Pesquisas da Amazônia (INPA-H) and the Museu Nacional (MNRJ). All were from the state of Amazonas, as follow: Reserva Extrativista do baixo Juruá: (INPA-H 17160 62); Iranduba: Gasoduto Coari-Manaus (INPA-H 18260); Manicoré: Rodovia BR-319, Km 350 (INPA-H 22984) and Rodovia BR-319, Km 300 (INPA-H 26290); and Urucará: (MNRJ 17979). Ventral scales were counted following the method of Zaher et al. (2008). The right hemipenis was prepared from a previously fixed specimen (MNRJ 17979) following the technique of Pesantes (1994) and Manzani and Abe (1988). We used the hemipenial morphological terminology of Zaher (1999). Sex was determined by the presence or absence of an hemipenis detected through a ventral incision at the base of the tail. The hemipenes are slightly bilobed, bearing several spines and apical discs in the distal region of the lobes, which are neither capitate nor calyculate. Inverted, the organ extended to the level of the eighth subcaudal scale. The sulcus spermaticus is deep and divides on the basal region of the organ; the sulcus branches in a centrifugal direction and terminates on the distal part of the apical disc. Apical disks are located laterally in the distal region of the lobes. On the sulcate side, the basal portion of the hemipenis bears several spines. The enlarged intrasulcar spines decrease in size toward the distal regions of lobes. The asulcate side has small spines on the lobes and the basal region of the organ. Enlarged spines are concentrated on the lateral region of medial portion of the organ; they decrease in size toward the lobes and the center of hemipenial body (Figure 1). A B Figure 1. The right hemipenis of Umbrivaga pygmaea (MNRJ 17979) collected in the municipality of Urucará, state of Amazonas, Brazil. (A) asulcate side, (B) sulcate side. Meristic data for the seven specimens (Table 1) are similar to those available in the literature with a few exceptions; values presented by Markezich and Dixon (1979) are noted parenthetically. Subcaudal scales vary from 27 33 (29 38). One specimen (INPA-H 18260) is distinguished by having three supralabials (3 5) in contact with the orbit on the right side of head and an extra posterior temporal scale (1 + 3) on both sides of the head (Table 1). The dorsal color pattern of preserved specimens is coffee-brown; the flanks are lighter. The dorsal scales on the anterior part of the body have white edges; this part of the dorsum bears transverse dark bands that are most evident in defensive hood-displays (Figure 2). A longitudinal dark stripe extends along the side of the snake from the midlength of the body to the tip of tail. The dorsal surface of the head is reddish brown and the supralabials are whitish cream (Figure 3). The color pattern of specimens agrees with Cope s original description (Cope 1868) and subsequent literature (Dixon and Soini 1986, Martins and Oliveira 1998), with exception of the brighter orange ventral coloration in life of the specimen that was collected (Figure 2); the orange changed to cream when the individual was preserved. 178

Morphology and geographical distribution of the poorly known snake Umbrivaga pygmaea Table 1. Morphometric and meristic data for Umbrivaga pygmaea. Abbreviations: SVL (snout vent length, mm); TL (tail length, mm); M (male); F (female); D (dorsal row on neck/midbody/precloacal); V (ventrals); SC (subcaudals); Cl (cloacal); d (divided); SL (supralabial scales); SLO (supralabial scales in contact with orbit); IL (infralabial scales); ILA (number of infralabials scales in contact with anterior chinshields); ILP (number of infralabial scales in contact with posterior chinshields); POc (preocular); PoOc (postocular); T (temporals). Specimen Sex SVL TL D V SC Cl SL SLO IL ILA ILP POc PoO T INPA-H 17160 M 160 27 17/17/15 127 29 d 6/6 3+4/3+4 8/8 1 4/1 4 4, 5/4, 5 1/1 1/1 1+2/1+2 INPA-H 17161 M 159 32 17/17/15 123 31 d 6/6 3+4/3+4 8/8 1 4/1 4 4, 5/4, 5 1/1 1/1 1+3/1+2 INPA-H 17162 M 154 26 17/17/15 124 27 d 6/6 3+4/3+4 8/8 1 4/1 4 4, 5/4, 5 1/1 1/1 1+2/1+2 INPA-H 18260 F 79 13 17/17/15 124 27 d 7/6 3+4+5/3+4 8/8 1 4/1 4 4, 5/4, 5 1/1 1/1 1+3/1+3 INPA-H 22984 M 166 30 17/17/15 129 30 d 6/6 3+4/3+4 8/8 1 4/1 4 4, 5/4, 5 1/1 2/2 1+2/1+2 INPA-H 26290 M 113 19 17/17/15 136 31 d 6/6 3+4/3+4 8/8 1 4/1 4 4, 5/4, 5 1/1 2/2 1+2/1+2 MNRJ 17979 M 125 23 17/17/15 124 33 d 6/6 3+4/3+4 8/8 1 4/1 4 4, 5/4, 5 1/1 1/1 1+2/1+2 Markezich and Dixon 1979 M 17/17/15 122 133 29 38 d 6/7 2+3/3+4 8/9 1 4/1 4 4, 5/4, 5 1/1 1/1 1+2/1+2 Markezich and Dixon 1979 F 17/17/15 122 129 33 38 d 6/7 2+3/3+4 8/9 1 4/1 4 4, 5/4, 5 1/1 1/1 1+2/1+2 179

Kawashita-Ribeiro et al. A B Figure 2. Live specimen of Umbrivaga pygmaea (MNRJ 17979, male, SVL 125 mm) from the municipality of Urucará, Amazonas, Brazil. (A) Dorsal and ventral patterns; (B) defensive hood-display. The present study extends the known geographical distribution of Umbrivaga pygmaea about 230 km southward (straight line) and represents the southernmost record of this species (Figure 4). Although the species has a relatively wide geographic distribution, there are many gaps its range. This probably reflects a sampling bias of this relatively small, secretive snake. In addition, specimens were collected near large rivers, suggesting that the presumed habitat preferences reported by Dixon and Soini (1986) and Martins and Oliveira (1998) may be an artifact of easily accessible collecting sites near large rivers in Amazonia. Figure 3. Head detail of preserved specimen of Umbrivaga pygmaea (MNRJ 17979) from the municipality of Urucará, Amazonas, Brazil. From top to bottom: dorsal, ventral and lateral color pattern. 180 Acknowledgments. We thank Biodinâmica Engenharia Consultiva for logistical support and permission to use the data collected. Ronaldo Fernandes (MNRJ) and Richard Vogt (INPA) allowed us to examine specimens in their care. Ronaldo Fernandes and Paulos Passos (MNRJ) provided helpful comments on the manuscript. The collecting permit (number 124/2009) was issued by IBAMA (Instituto Brasileiro do Meio Ambiente e dos Recursos Renováveis). Phyllomedusa - 10(2), December 2011

Morphology and geographical distribution of the poorly known snake Umbrivaga pygmaea Figure 4. Geographic distribution of Umbrivaga pygmaea in the Amazon region (AM) of Brazil. Star: type-locality; circle: bibliographic records; triangle: new record in this study. (1) Marañon, Peru; (2) Napo, Peru; (3) Juruá, AM; (4) Juruá, AM; (5) Tefé, AM; (6) Manicoré, AM; (7) Manicoré, AM; (8) Iranduba, AM; (9) Manaus, AM; (10) Urucará, AM; (11) Almerim, Pará. References Ávila-Pires, T. C. S., M. S. Hoogmoed, and W. A. Rocha. 2010. Notes on the vertebrates of nothern Pará, Brazil: a forgotten part of Guiana region, I. Herpetofauna. Boletim do Museu Paraense Emilio Goeldi 5: 13 112. Cope, E. D. 1868. An examination of the Reptilia and Batrachia obtained by the Orton Expedition to Equador and the Upper Amazon, with notes on other species. Proceedings of the Academy of Natural Sciences, Philadelphia 20: 103. Dixon, J. R. and P. Soini. 1986. The reptiles of the upper Amazon basin, Iquitos region, Peru. II. Crocodilians, turtles and snakes. Contributions in Biology and Geology, Milwaukee Public Museum 12: 1 91. Fernandes, D. S., F. L. Franco, and V. J. Germano. 1999. Umbrivaga pygmaea. Herpetological Review 30: 175. Manzani, P. R. and A. S. Abe. 1988. Sobre dois novos métodos de preparo do hemipênis de serpentes. Memórias do Instituto Butantan 50: 15 20. Markezich, A. L. and J. A. Dixon. 1979. A new South America species of snake and comments on the genus Umbrivaga. Copeia 1979: 698 701. Martins, M. and M. E. Oliveira. 1998. Natural history of snakes in forests of Manaus region, Central Amazonia, Brazil. Herpetological Natural History 6: 78 150. Miyata, K. 1982. A checklist of the amphibians and reptiles of Ecuador with a bibliography of Ecuadorian herpetology. Smithsonian Herpetology Information Service 54: 1 70. Pesantes, O. S. 1994. A method for preparing the hemipenis of preserved snakes. Journal of Herpetology 28: 93 95. Peters, J. A. and B. Orejas-Miranda. 1970 Catalogue of the Neotropical Squamata. Part I. Snakes. Washington, D. C. and London. Smithsonian Institute Press. 347 pp. Roze, J. A. 1964. The snakes of the Leimadophis-Urotheca- Liophis complex from the Parque Nacional Henri Pitier 181

Kawashita-Ribeiro et al. (Rancho Grande), Venezuela, with a description of a new genus and species (Reptilia, Colubridae). Senckenbergiana Biologica 45: 533 542. Vanzolini, P. E. 1986. Addenda and corrigenda. Part I: Snakes. Pp. 1 26 in J. A. Peters and B. Orejas-Miranda (eds.), Catalogue of the Neotropical Squamata. Part I. Snakes. Washington D. C. and London. Smithsonian Institute Press. Vidal, N., M. Dewynter, and D. J. Gower. 2010. Dissecting the major American snake radiation: A molecular phylogeny of the Dipsadidae Bonaparte (Serpentes, Caenophidia). Comptes Rendus Biologies 333: 48 55. Vigle, G. O. 2008. The amphibians and reptiles of the Estación Biológica Jatun Sacha in the lowland rainforest of Amazonian Ecuador: a 20-year record. Breviora 514: 1 30. Zaher, H. 1999. Hemipenial morphology of the South American Xenodontine snakes, with a proposal for a monophyletic Xenodontinae and a reappraisal of Colubroid hemipenis. Bulletin of the American Museum of Natural History 240: 1 240. Zaher, H., M. E. Oliveira, and F. L. Franco. 2008. A new, brightly species of Pseudoboa Schneider, 1801 from the Amazon Basin (Serpentes, Xenodontinae). Zootaxa 1674: 27 37. 182