Short Note. Keywords: Amazon; Brazilian fauna; Cerrado; stenodermatinae.
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1 Mammalia 2015; aop Short Note Patrício A. da Rocha*, Marcus V. Brandão, Guilherme S.T. Garbino, Irineu N. Cunha and Caroline C. Aires First record of Salvin s big-eyed bat Chiroderma salvini Dobson, 1878 for Brazil DOI /mammalia Received May 8, 2015; accepted July 24, 2015 Abstract: The present work reports the first record of Salvin s big-eyed bat, Chiroderma salvini, for Brazil. One specimen was captured with mist nets set in the canopy, about 20 m high, in the Porto Velho municipality, Rondônia. Additionally, an old specimen from Aricá, Mato Grosso, deposited in the zoological collection of the Museu de Zoologia da Universidade de São Paulo and identified as C. villosum, was here determined to be C. salvini. In the past two decades, approximately two new bat species are added to the Brazilian fauna per year. The expansion of sampling in border areas of the country, as in the case reported here, certainly increases the likelihood of finding new records. Keywords: Amazon; Brazilian fauna; Cerrado; stenodermatinae. The genus Chiroderma comprises six species: C. villosum Peters, 1860; C. doriae Thomas, 1891; C. improvisum Baker and Genoways, 1976; C. trinitatum Goodwin, 1958; C. vizottoi Taddei and Lim, 2010; and C. salvini Dobson, 1878 *Corresponding author: Patrício A. da Rocha, Graduate Program in Zoology, Department of Systematics and Ecology, Federal University of Paraiba, Cidade Universitária, João Pessoa, , Paraíba, Brazil, parocha2@yahoo.com.br Marcus V. Brandão: Graduate Program in Biological Diversity and Conservation, Department of Biology, Federal University of São Carlos, Itinga, Sorocaba, , São Paulo, Brazil Guilherme S.T. Garbino: Ecological Research Institute (IPÊ), Nazaré Paulista, , São Paulo, Brazil Irineu N. Cunha: Braz Cubas University, Mogilar, Mogi das Cruzes, , São Paulo, Brazil Caroline C. Aires: Mogi das Cruzes University, Vila Partenio, Mogi das Cruzes, , São Paulo, Brazil (Simmons 2005, Taddei and Lim 2010). Chiroderma salvini occurs in western and southern Mexico, on the Pacific and Caribbean coasts of Central America, northern and western Colombia, northern Venezuela, in Ecuador on both sides of the Andes, and there is a disjunct population east of the Andes in southern Peru and northern/central Bolivia (Gardner 2007). The present work reports the first record of Salvin s big-eyed bat, Chiroderma salvini, for Brazil. One female (MZUSP 35408) was captured with mist nets set in the canopy, about 20 m high, on July 7, 2014 (Figure 1; see Greenlaw and Swinebroad 1967). The locality lies close to the left margin of the middle Rio Madeira at the Mutum Paraná district, municipality of Porto Velho (Figure 2), Brazilian state of Rondônia ( S, W, approximately 100 m a.s.l.). The predominant vegetation type in the area is dense alluvial ombrophilous forest ( Ivanauskas et al. 2008). The specimen was handled in accordance with Sikes et al. (2011), fixed in 10% formaldehyde and preserved in 70% ethanol, with subsequent extraction of the skull. After recording the basic external and cranial measurements (Table 1), the specimen was deposited in the zoological collection of the Museu de Zoologia da Universidade de São Paulo (MZUSP). For morphometric comparisons, we measured the Chiroderma specimens deposited in MZUSP, Universidade Estadual Paulista, São José do Rio Preto, Brazil (DZSJRP) and Museo de La Salle, Bogotá, Colombia (MLS) (Table 1). Following Vizotto and Taddei (1973), the following cranial and external measurements were taken using a digital caliper: forearm length (FA), ear, length of the first phalanx of the third digit (1P3D), length of the second phalanx of the third digit (2P3D), greatest length of the skull (GLS), condylobasal length (CBL), length of maxillary toothrow (LMT), length of mandible (ML), breadth across upper canines (C-C) and post-orbital constriction (POB). Chiroderma salvini can be distinguished from its congeners by having a forearm larger than 43 mm (versus < 42 mm in C. trinitatum) but shorter than 47.5 mm (versus longer than 49.5 mm in C. doriae and C.
2 2 P.A. da Rocha et al.: First record of Chiroderma salvini for Brazil Figure 1: (A) Chiroderma salvini from Porto Velho, Rondônia (MZUSP 35408), (B) dorsal view of the same specimen note the median dorsal stripe; (C) mist nets set in the canopy. improvisum); conspicuous facial stripes, dorsal stripe present and usually conspicuous (versus faint or absent in C. villosum); thick upper inner incisors (Figure 3B), obliquely placed and in contact at tips (versus in contact along most of its length in C. trinitatum, C. doriae and C. vizottoi or with a distinct large gap in C. villosum) (Thomas 1891, Baker and Genoways 1976, Gardner 2007, Taddei and Lim 2010, Garbino et al. 2012). Morphologically, the species most similar to Chiroderma salvini is C. villosum, which occurs in sympatry in the Rondônia locality reported here. However, a distinction between those species can be made even as the live animal was handled in the field. We examined 22 specimens of C. villosum from several localities ( Appendix 1) and none of them presents distinctive facial and dorsal stripes as C. salvini, and all present a distinct gap between the upper inner incisors, which are parallel. One specimen (MZUSP 6494) from Aricá, Mato Grosso, has a very similar skull to the recently captured C. salvini specimen (Figure 3), including the upper inner incisors, which are almost identical in position. Although the fur was too faded to see any stripes (it is an old specimen, from 1920), on the basis of dental morphology and external and cranial m easurements, we concluded that it also refers to C. salvini. After comparing the external characteristics of the captured specimen (Figure 1), we found some discrepancies from Dobson s original description, who stated that the type specimen of Chiroderma salvini had a head with four very broad and very white streaks (Dobson 1878:
3 P.A. da Rocha et al.: First record of Chiroderma salvini for Brazil 3 Figure 2: Known records of Chiroderma salvini in South America (modified from Gardner [2007]). Stars represent the new records for Brazil. BRAZIL: (1) Porto Velho, Rondônia (this study) and (2) Aricá, Mato Grosso (this study); BOLIVIA: (3) Rıo Pitasama, Santa Cruz; (4) Serranıa Bella Vista, La Paz and (5) Independencia, Pando; PERU: (6) Rıo La Torre, Madre de Dios; (7) Consuelo; (8) Cashiriari and (9) Ridge Camp, Cusco; ECUADOR: (10) and (11) Pacaritambo, Guayas and (12) Limoncocha, Sucumbios; COLOMBIA: (13) Popayan, Cauca; (14) Rio Zabaletas, Valle del Cauca; (15) La Tebaida, Antioquia; VENEZUELA:(16) Barinas; (17) San Agustın, Monagas; (18) Pico Avila, Distrito Federal; (19) La Copa, Carabobo. 533). This feature is observed in specimens from Central America (Reid 1997), whereas in a specimen from Bolivia (AMNH ) analyzed by us through photos and on the one captured by us, the facial stripes are not so wide and contrasting. Bernard et al. (2011) suggest the likely occurrence of Chiroderma salvini for the Brazilian Amazon, given the proximity of the records from Bolivia. The record presented here is about 350 km east from the nearest locality in Independencia, Department of Pando in Bolivia (Figure 2), thereby corroborating their hypothesis. Despite this relative proximity, the fact that this species had been captured only once and only after a sampling effort of h.m 2 (sensu Straube and Bianconi 2002) may denote their rarity in the area. We must note, however, that canopy-level mist nets were used only in two field campaigns (1620 h.m 2 ), which might have increased the chance of sampling the species in these campaigns. In a study comparing canopyand ground-level mist nets, Kalko and Handley (2001) captured 92% of the C. trinitatum and 100% of the C. villosum in canopy nets. Similarly, in French Guiana, C. villosum was one of the few phyllostomids sampled with nets set more than 20 m high (Simmons and Voss 1998). Among the three species of the genus Chiroderma that occur in the Amazonia, C. salvini is the one that has the most restricted distribution in this biome. Given that it is a poorly studied species, the factors that limit its distribution along the Amazon basin are still unknown. However, it is noteworthy that C. salvini generally only occurs in sympatry with C. trinitatum and C. villosum in peripheral regions of the distribution of the latter two species. Finally, it is worth mentioning that although we do not have detailed data of the record from Aricá, this locality is found within the Cerrado domain, an ecosystem where only C. villosum and C. doriae have been recorded so far (see Gardner 2007, Carmignotto et al. 2012). Nogueira et al. (2014) recently listed 178 species of bats with confirmed record in Brazil. The present record adds another species to this list. According to a survey made by these authors, approximately two new bat species to the Brazilian fauna are reported per year in the past two decades. The expansion of sampling in border areas of the country, as was the case reported here, certainly increases the likelihood of finding new records.
4 4 P.A. da Rocha et al.: First record of Chiroderma salvini for Brazil Table 1: External and cranial measurements (in mm) of four species of Chiroderma. Measurements Chiroderma salvini C. villosum C. doriae C. trinitatum New records MZUSP ( ) MZUSP 6494 ( ) Holotype a b ( ) c (5 ) (12 ) (11 ) (5 ) (7 ) (1 ) (3 ) FA (11) (11) (5) (7) (3) ( ) ( ) ( ) ( ) ( ) ( ) ( ) Ear (4) (7) (4) (6) (1) ( ) ( ) ( ) ( ) ( ) 1P3D (4) (9) (4) (6) (3) ( ) ( ) ( ) ( ) ( ) 2P3D (4) (9) 29.1 (4) (6) (3) ( ) ( ) ( ) ( ) ( ) GLS (7) (2) 28.5 (4) (n = 5) (3) ( ) ( ) ( ) ( ) ( ) ( ) ( ) CBL , (7) 22.2 (1) (4) (5) (3) ( ) ( ) ( ) ( ) ( ) ( ) LMT (7) 8.75 (2) (4) (5) (3) ( ) ( ) ( ) ( ) ( ) ( ) ( ) ML (7) 16.5 (2) 20.1 (4) (5) (3) ( ) ( ) ( ) ( ) ( ) ( ) C C (7) 5.6 (1) 5.99 (4) 6.02 (5) (3) ( ) ( ) ( ) ( ) ( ) POB (7) 5.83 (2) 6.54 (4) 6.41 (5) (3) ( ) ( ) ( ) ( ) ( ) ( ) ( ) Mean (n) and range values are presented when more than one specimen is available for each sex. See text for acronyms. a Values taken from Carter and Dolan (1978); b A male and a specimen with undetermined sex were lumped, both from Colombia; c Values taken from Taddei and Lim (2010).
5 P.A. da Rocha et al.: First record of Chiroderma salvini for Brazil 5 Chiroderma salvini BRAZIL: Mato Grosso: Aricá (MZUSP 6494); Rondônia: Porto Velho, Mutum Paraná (MZUSP 35408). COLOMBIA: Caquetá: Florencia (MLS 2037); Norte de Santander: Bochalema (MLS 2220). Chiroderma trinitatum BRAZIL: Pará: LT Jurupari, rio Xingu (MZUSP 35033); Rondônia: Monte Negro (MZUSP 35026). VENEZUELA: Amazonas: Belén (MZUSP 27166, 27167). Chiroderma villosum Figure 3: (A) Dorsal, ventral and lateral views of the skull and lateral view of the mandible (Scale bar = 10 mm); (B) Frontal view of the upper and lower incisors (Scale bar = 5 mm) of Chiroderma salvini (MZUSP 35408) from Porto Velho, Rondônia. Acknowledgments: We are grateful to Arcadis Logos S/A, Dr. Mario de Vivo and Juliana Gualda de Barros from MZUSP, Dr. Eliana Morielle-Versute from DZSJRP and Hno. José Edilson Espítia and Diego Perico Manrique from MLS. We also thank CNPq for research grants to PAR (501701/ and /2015-7), Drs. Valeria da C. Tavares and Bruce D. Patterson for generously providing pictures of C. salvini museum specimens. Appendix 1: Specimens examined Chiroderma doriae BRAZIL: Rio Grande do Norte: Baia Formosa, Usina Pedrosa (MZUSP 35027); Mato Grosso do Sul: Brasilândia, Fazenda Barma (MZUSP 28591, 28688); São Paulo: Cajuru, Fazenda Santa Carlota (MZUSP 35028); Cananéia, P.E. Ilha do Cardoso (MZUSP 28037); Iguape (MZUSP 21082); Ilhabela, P.E. de Ilhabela (MZUSP 35029); Iporanga, Caverna Morro Preto (MZUSP 34012); Pindorama, Estação Experimental (DZSJRP 16506); Sete Barras, Barra do Ribeirão Onça Parda (MZUSP 10632); Ubatuba, P.E. Ilha Anchieta (MZUSP 29456, 31852). BRAZIL: Acre: Cruzeiro do Sul (DZSJRP 13029, 13030, 13031, 13032, 13033); Amazonas: Chaparito (MZUSP 27168); Humaitá, km 27 of BR319 highway (DZSJRP 14121); Pará: Cachoeira do Espelho, rio Xingu (MZUSP 22677); Lago Jacaré, rio Trombetas (MZUSP 13335); Lago Leonardo, rio Trombetas (MZUSP 13197, 13209); Ourilândia do Norte, Centro Kaiapó de Estudos Ecológicos (MZUSP 29150); Uruá, rio Tapajós (MZUSP 12627, 12628, 12629); Rondônia: Ariquemes, Pedra Branca (MZUSP 22827); Cachoeira de Nazaré, rio Machado (MZUSP 20200); Minas Gerais: Frutal (DZSJRP 14480); São Paulo: Neves Paulista (DZSJRP 14305, 14319); EspÍrito Santo: Aracruz, Aracruz Celulose (MZUSP 35032); Linhares, Fazenda Santa Terezinha (MZUSP 35030, 35031) References Baker, R.J. and H.H. Genoways A new species of Chiroderma from Guadeloupe, West Indies (Chiroptera: Phyllostomidae). Occas. Pap. Mus. Texas Tech Univ. 39: 1 9. Bernard, E., V.C. Tavares and E. Sampaio Updated compilation of bat species (Chiroptera) for the Brazilian Amazonia. Biota Neotrop. 11: Carter, D.C. and P.G. Dolan Catalogue of type specimens of neotropical bats in selected European museums. Spec. Publ. Mus. Texas Tech Univ. 15: Carmignotto, A.P., M. de Vivo and A. Langguth Mammals of the Cerrado and Caatinga: distribution patterns of the tropical open biomes of Central South America. In: (B.D. Patterson and L.P. Costa, eds.) Bones, clones, and biomes: the history and geography of recent Neotropical mammals. University of Chicago Press, Chicago, IL. pp Dobson, G.E Catalogue of the Chiroptera in the collection of the British Museum. British Museum (Natural History), London, UK. pp. 567.
6 6 P.A. da Rocha et al.: First record of Chiroderma salvini for Brazil Garbino, G.S.T., C.C. Aquino and C.C. Aires First record for the state of Rondônia and revised distribution map of Chiroderma trinitatum Goodwin, 1958 (Mammalia: Chiroptera: Phyllostomidae) in Brazil. Check List 8: Gardner, A.L Genus Chiroderma W. Peters, In: (A.L. Gardner, ed.). Mammals of South America. Vol. 1, Marsupials, xenarthrans, shrews and bats. Chicago: The University of Chicago Press, Chicago, IL. pp Greenlaw, J.S. and J. Swinebroad A method for constructing and erecting aerial-nets in a forest. Bird Banding 38: Ivanauskas, N.M., R. Monteiro and R.R. Rodrigues Classificação fitogeográfica das florestas do Alto Rio Xingu. Acta Amazon. 38: Kalko, E.K.V. and C.O. Handley Neotropical bats in the canopy: diversity, community structure, and implications for conservation. Plant Ecol. 153: Nogueira, M.R., I.P. Lima, R. Moratelli, V.C. Tavares, R. Gregorin and A.L. Peracchi Checklist of Brazilian bats, with comments on original records. Check List 10: Peters, W Eine neue Gattung von Flederthieren, Chiroderma villosum, aus Brasilien. Monatsber. König. Preuss. Akad. Wiss, Berlin, BE. 1861: Reid, F.A A field guide to the mammals of Central America and southeast Mexico. Oxford University Press, New York, NY. pp Sikes, R.S., W.L. Gannon, and the Animal Care and Use Committee of the American Society of Mammalogists Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J. Mammal. 92: Simmons, N.B Order Chiroptera. In: (D.E. Wilson and D.M. Reeder, eds.) Mammal species of the world: a taxonomic and geographic reference. The Johns Hopkins University Press, Baltimore, MD. pp Simmons, N.B. and R.S. Voss The mammals of Paracou, French Guiana: a neotropical lowland rainforest fauna. Part 1. Bats. Bull. Am. Mus. Nat. Hist. 237: Straube, F.C. and G.V. Bianconi Sobre a grandeza e a unidade utilizada para estimar esforço de captura com utilização de redes de neblina. Chiroptera Neotrop. 8: Taddei, V.A. and B.K. Lim A new species of Chiroderma (Chiroptera, Phyllostomidae) from Northeastern Brazil. Braz. J. Biol. 2: Thomas, O Note on Chiroderma villosum, Peters, with the description of a new species of the genus. Ann. Mus. Civ. Stor. Nat. Genova. 10: Vizotto, L.D. and V.A. Taddei Chave para determinação de quirópteros brasileiros. Bolm. Ciên. Fac. Filos. Ciên. Letras, 1:1 72.
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