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Mastozoología Neotropical ISSN: 0327-9383 [email protected] Sociedad Argentina para el Estudio de los Mamíferos Argentina

Suarez-Castro, Andrés F.; Ramírez-Chaves, Héctor E.; Rodríguez-Posada, Miguel E.; García, Javier NEW RECORDS OF LEUCOPTERA AND FIRST RECORD OF PEROPTERYX PALLIDOPTERA (CHIROPTERA-) FROM COLOMBIA Mastozoología Neotropical, vol. 19, núm. 1, enero-junio, 2012, pp. 165-171 Sociedad Argentina para el Estudio de los Mamíferos Tucumán, Argentina

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NEW RECORDS OF Peropteryx leucoptera AND FIRST RECORD OF Peropteryx pallidoptera (CHIROPTERA- EMBALLONURIDAE) FROM COLOMBIA

Andrés F. Suarez-Castro1,3, Héctor E. Ramírez-Chaves2, Miguel E. Rodríguez-Posada1,3, and Javier García4

1 Laboratorio de Mamíferos, Facultad de Ciencias, Instituto de Ciencias Naturales, Universidad Nacional de Colombia, Carrera 45 #26-85, Sede Bogotá D.C., Colombia [Correspondence: Andrés Suarez-Castro ]. 2 Erasmus Mundus Master Programme in Evolutionary Biology: Ludwig Maximilians University of Munich, Germany and University of Groningen, The Netherlands. 3 Grupo de Investigación en Conservación y Manejo de Vida Silvestre, Universidad Nacional de Colombia. 4 Fundación Herencia Natural, Carrera 69f #64h-85, Bogotá, Colombia.

ABSTRACT: We present new records of Peropteryx leucoptera from two localities in the Colombian Llanos. For this species these records constitute both the northern- most record and the first time it has been found in a different ecosystem such asthe savannas of the Orinoco. In addition we report the first record of P. pallidoptera from the eastern Andean slopes in the Amazonian foothills of Colombia, which constitutes the northern-most known record for this species.

RESUMEN: Nuevo registros de Peropteryx leucoptera y primer registro de Peropteryx pallidoptera (Chiroptera-Emballonuridae) para Colombia. Presentamos nuevos registros de Peropteryx leucoptera de dos localidades de los Llanos Orientales de Colombia. Para esta especie, estos reportes constituyen los registros más al norte y la primera vez que es encontrada en un ecosistema diferente como lo son las sabanas del Orinoco. Adicionalmente presentamos el primer registro de P. pallidoptera en la vertiente oriental de los Andes, piedemonte amazónico de Colombia, que constituye el registro más al norte que se conoce de esta especie.

Key words. Amazonas. . Colombian Llanos. Distribution extension. Orinoco.

Palabras clave. Amazonia. Extensión de distribución. Llanos de Colombia. Murciélagos. Orinoquia.

The doglike bats of the genus Peropteryx with a basiesphenoideal pit not divided by Peters, 1867, are restricted to the Neotropics a longitudinal septum and spicule-like ante- and currently five species are recognized (Lim rior upper premolar (Sanborn, 1937; Jones et al., 2010; McDonough et al., 2011). The and Hood, 1993; Hood and Gardner, 2008). bats of this genus are differentiated from other Hitherto, three species of Peropteryx have representatives of Neotropical Emballonuridae been registered in Colombia (Alberico et al., by the absence of dorsal lines or hair tufts in 2000; Simmons, 2005; Hood and Gardner, the skin; wing-sac present and located near 2008): Peropteryx kappleri Peters, 1867; the anterior border of the propatagium; wing P. leucoptera Peters, 1867; and P. macrotis attached to the leg on the ankle; the skull (Wagner, 1843).

Recibido 17 mayo 2011. Aceptado 27 octubre 2011. Editor asociado: UFJ Pardiñas 166 Mastozoología Neotropical, 19(1):165-171, Mendoza, 2012 AF Suarez-Castro et al. http://www.sarem.org.ar

P. leucoptera inhabits the greater Amazon The specimen of Lemke et al. (1982) is basin of Ecuador, French Guiana, Guyana, housed in the Instituto de Recursos Biológicos Surinam, Venezuela, Colombia, Peru and east- Alexander von Humboldt (IAvH). Our new ern Brazil (Jones and Hood, 1993; Hood and records have voucher specimens deposited in Gardner, 2008; Lim et al., 2010; McDonough the Instituto de Ciencias Naturales (ICN) of et al., 2011). In Colombia, P. leucoptera is the Universidad Nacional de Colombia (Ap- known from one specimen captured in undis- pendix). External measurements (mm) were turbed lowland tropical forest of Campamento taken from the specimens in the field, including Chamusa, Serranía de la Macarena, Department total length (TL), length of tail (TV), length of Meta, where it was roosting alone in a of hind foot (HF), length of ear (EAR), length tangle of roots under an overhanging stream of tragus (TR), and length of forearm (FA). bank of the Río Duda (Lemke et al., 1982). Cranial measurements were recorded with The species is easily distinguished from other digital calipers to the nearest 0.1 mm including Neotropical Emballonuridae by the presence of greatest length of skull (GLS), condylo-incisive white wings; ears connected by a low band of length (CIL), breadth across zygomatic arches skin across the forehead and a skull large and (ZB), breadth across mastoids (MB), breadth robust for the genus with the basisphenoideal of braincase (BBC), breadth across postorbital pit between two large, deep pterygoid pits constriction (POC), length of maxillary tooth separated by a mesopterygoid extension (Hood row (CM3), and breadth across upper molars and Gardner, 2008; Lim et al., 2010). (M3M3). Measurements were taken accord- Recently, Lim et al. (2010) described P. ing to Lim et al. (2010) and McDonough et pallidoptera from the lowlands of the western al. (2011). Amazonia of Ecuador and Peru. This species We confirm that the Lemke et al. (1982) was confused previously with P. leucoptera specimen belongs to P. leucoptera. Although (McDonough et al., 2011). Although the wings the skull is broken and we could not confirm of this species are pale and mostly similar to cranial measurements, and the skin has lost the white wings of P. leucoptera, the ears are its original color, we can distinguish that the not joined above the head. Additionally, P. dactylopatagioum are white, in addition to an pallidoptera is similar to P. macrotis in body evident interauricular band. This combination size and cranial morphology and the lateral of morphological characters is diagnostic for pteygoid pits are not as large and deep as they P. leucoptera and any other species described are in P. leucoptera. In P. macrotis, the ptery- as Peropteryx present these characters (San- goid pits are separated by a basisphenoideal born, 1937; Jones and Hood, 1993; Hood and pit, while in P. pallidoptera are separated by Gardner, 2008; Lim et al., 2010; McDonough a mesopterygoid extension (Lim et al., 2010; et al., 2011). McDonough et al., 2011). Given that specimens Two P. leucoptera were collected by Ramírez- of P. pallidoptera were previously misidentified Chaves (HERC) and Rodríguez-Posada (field as P. leucoptera (McDonough et al., 2011), we numbers HERC 768, HERC 769) in a reexamined the specimen reported by Lemke inventory in the Pacific Rubiales Inc. Kifa et al. (1982) as P. leucoptera to verify its cor- Este oil concession block (Fig. 1, Appendix) rect taxonomic assignation. Furthermore we in October 2009. Bats were caught with mist report the first records of P. leucoptera from nets 6 m in length, with a mesh diameter of 36 the savannas of the Colombian Llanos; these mm, set at a height of 3 m above the ground specimens constitute the first records of the inside the forest. Specimens were preserved species in an ecosystem distinct to the lowland in 96% ethanol and the skull of HERC 768 tropical rainforest from the Amazonas basin. was extracted for taxonomic identification. In addition, we report the first record for Co- The vegetation in this area is dominated by lombia of P. pallidoptera from the Amazonian savannas adjacent to riparian forest, and palm foothills of the Andes. swamps (Fig. 2a, b). The forest where these NEW RECORDS OF Peropteryx FROM COLOMBIA 167

Fig. 1. Distribution of records of Peropteryx leucoptera and P. pallidoptera from Colombia. 1. P. leucoptera (FSC 107 and 193); 2. P. leucoptera (HERC 768-769); 3. P. leucoptera (IAvH 2241 Lemke et al. 1982); 4. P. pallidoptera (JGV 015 and 021). Black region represents the Eastern foothills of the cordillera Oriental. Regions adapted from Ferrer-Pérez et al. (2010).

(Schreber, 1774), Desmodus rotundus (É. Geof- froy St.-Hilaire, 1810), Phyllostomus elongatus (É. Geoffroy St.-Hilaire, 1810), Chrotopterus auritus (Peters, 1856), Mimon crenulatum (É. Geoffroy St.-Hilaire, 1803), Micronycteris megalotis (Gray, 1842), Trachops cirrhosus (Spix, 1823), Glossophaga soricina (Pallas, 1766), Carollia brevicauda (Schinz, 1821), Rhinophylla pumilio Peters, 1865 and Artibeus planirostris (Spix, 1823). Two additional P. leucoptera were collected by Suarez-Castro (FSC, field numbers FSC 107, FSC 193) in the Alange Energy Corp bats were captured has a canopy height of about Cubiro oil concession block, in the municipal- eight meters, and constitutes a small isolated ity of San Luis de Palenque, Department of fragment crossed by a stream (where the net Casanare (Fig. 1, Appendix) in September was placed) surrounded by grasslands. Other 2009 and January 2010. P. leucoptera was one species collected at Kifa Este and deposited in of 31 species of bats captured in that survey the ICN collection were leptura (Suárez-Castro and Sánchez-Palomino, 2011). Vegetation consists of savan- nas and disturbed gallery for- est surrounded by agricultural and pasture areas. Most of the land is used extensively for livestock; crops are scarce and limited to subsistence farming; and much of the native vegetation has disap- peared (Castellanos-Castro et al., 2011). Bats were captured with mist nets of 9 x 2.5 m set

Fig. 2. Locality record of specimens of Peropteryx leucoptera in the Orinoco region, Colombia: a) gen- eral landscape; b) forest fragment at the Pacific Rubiales Inc.’s Kifa Este oil concession block, Puerto Gaitán, Meta; c) and d) vegetation physionomy of forest fragment at the Cubiro’s Alange oil concession block, San Luis de Palenque, Casanare. 168 Mastozoología Neotropical, 19(1):165-171, Mendoza, 2012 AF Suarez-Castro et al. http://www.sarem.org.ar at 3 m above the ground in a riparian forest of Montañita, adjacent to “El Oso” stream with no vertical stratification, and a canopy (Fig. 1, Appendix) on 24 January 2007. The height of 10 m (Fig. 2c, d). Specimens were captures were made in a small cave (0.5 x preserved as skin and skull preparations. 0.3 x 1m) with entomological nets. The cave All specimens of P. leucoptera here reported is adjacent to a multi-stratified forest with a match all diagnostic characteristics for the canopy height of 25 m, in a typical Caquetá species, including white wings; ears connected foothill landscape, which constitutes a transi- by a band (Fig. 3a), and the skull with large tional zone between the eastern slopes of the pterygoid pits separated by a mesopterygoid Cordillera Oriental and the Amazonian basin. extension (Sanborn, 1937; Jones and Hood, Voucher specimens of P. pallidoptera con- 1993; Hood and Gardner, 2008; Lim et al., form in all respects to previous descriptions of 2010; McDonough et al., 2011) (Fig. 3b). the species (Lim et al., 2010; McDonough et The external and cranial measurements of our al., 2011), including the small pterygoid pits voucher specimens of P. leucoptera fall within separated by a mesopterygoid extension (Fig. the range of size variation documented for other 4), wings with paler tips and ears not connected localities (Lim et al., 2010; McDonough et al. by a lower band of skin. Our specimens are 2011) (Table 1). smaller than the average in most measurements Finally, two P. pallidoptera were captured of specimens from Ecuador and Peru (Table 2). by Garcia (JGV, field numbers JGV 015, JGV The records here presented show the distri- 021) in Department of Caquetá, municipality bution of P. leucoptera into a different kind

Table 1 Skin and skull measurements (mm) of specimens of Peropteryx leucoptera reported in this study in comparison to the mean and range (parentheses) for specimens of Peropteryx leucoptera reported in previous studies. Measurements from the holotype of Peropteryx leucoptera cyclops housed in the British Museum of Natural History (BMNH) were obtained from Lim et al. (2010) and McDonough et al. 2011. Abbreviations of measurements as explained in the text.

P. leucoptera HERC HERC FSC FSC IAvH McDonough et al. 2011 cyclops 768 769 107 193 2241 BMNH 24.3.1.6 Sex F M M M F F = 9 M = 14 M TL 73 60 64 60 82 62.8 (54-66) 63.5 (56-69) 65 TV 17 14 11 12 - 13.5 (12-17) 12.6 (5-16) 15 HF 7 9 7 8 9 8.7 (7-10) 8.8 (7-10) - EAR 18 18 13 17 17 16.6 (15-18.5) 16.8 (13-20) 17 FA 44.3 42 39.9 43.3 42.5 43.9 (42-46.4) 43.5 (41-46) 44.8 GLS 16.1 - 15.1 16 - - 15.3 (14.9-15.6) 16.2 CIL 14.7 - 13.8 14.5 - - 14.0 (13.9-14.1) 14.5 ZB 10.1 - - 9.5 - - 9.5 (9.3-9.6) - MB 8.0 - 7.9 7.7 - - 7.8 (7.6-8.0) 9.2 BBC 7.4 - 6.8 6.9 - - 7.2 (7.0-7.3) 7.8 POC 3.4 - 3.6 3.3 - - 3.3 (3.1-3.3) 3.2 CM3 6.6 - 6.3 6.4 - - 6.1 (6.1-6.2) 6.5 M3M3 7.5 - 6.9 6.9 - - 6.9 (6.7-7.0) 7.6 NEW RECORDS OF Peropteryx FROM COLOMBIA 169

Fig. 3. Photograph of a fe- male Peropteryx leucoptera (HERC 768) showing: a) band across the forehead connecting the ears; b) wings apparently white; c) dorsal, ventral and lateral views of the skull, showing large pterygoid pits (Pp) separated by a mesop- terygoid extension (Me). Scale = 10 mm.

of ecosystem such as the savannas of the Orinoco. Previously the species was known only from Neotropical rainforest of the Amazonian and Orinoco basins. In con- trast the vegetation in the sites of our records are dominated by extensive savannas mainly com- posed by herbaceous vegetation, principally grasslands; and the arboreal vegetation is represented by riparian forest along streams and rivers without water shortage in the dry season. For these reasons our report, some 450 km beyond the known range, appears to be the northern-most record of this species. It therefore represents an important ecological extension of the habitat of the species and large increase of area and ecosystem potentially used by the P. leucoptera. We report the first record of P. pallidoptera for the country, also a northern-most known record for this species (280 km from the next closest record). The ecological conditions of the vegetation in the site of our record are similar to those previously reported for the species (Lim et al., 2010; McDonough et al., 2011). As Lim et al. (2010) stated, it seems probable that these species are widely dis- tributed and will soon turn up at other sites where appropriate survey methods are used to inventory diversity. Species of Peropteryx have been collected in a variety of habitats, Fig. 4. Lateral (bottom), dorsal (center) and ventral (top) including cavities along stream banks; dark views of the skull of Peropteryx pallidoptera (JGV 021); note the small pterygoid pits (Pp) separated by a mesop- spaces under large fallen trees; within hol- terygoid extension (Me). Scale = 10 mm. low trees; and in mistnets placed in forest 170 Mastozoología Neotropical, 19(1):165-171, Mendoza, 2012 AF Suarez-Castro et al. http://www.sarem.org.ar

Table 2 Skin and skull measurements (mm) of specimens of Peropteryx pallidoptera reported in this study in comparison to the mean and range (parentheses) for specimens of Peropteryx pallidoptera reported by Lim et al. (2010) and McDonough et al. (2011) from Ecuador and Peru. Abbrevia- tions of measurements as explained in the text.

JGV 021 JGV 015 Lim et al., 2010 McDonough et al., 2011 Sex F M F = 14 M = 2 F TL 52 54 63.0 (58-67) 59.5 (57-62) 55.0 TV 12 12 12.7 (11-14) 13 (11-15) 12.0 HF 10 8 9.3 (8-10) 9 7 EAR 14 13 15.4 (15-17) 15 14.5 FA 37 40 42.1 (41-43) 39.5 (39-40) 42.0 GLS 13.7 13.6 13.9 (13.6-14.1) 14.1 - CIL 12.4 12 12.6 (12.2-12.8) 12.5 - ZB 7.9 - 8.3 (8.0-8.7) 8.15 (8.1-8.2) - MB 6.9 7.1 7.2 (6.9-7.4) 7.25 (7.2-7.3) - BBC 6.2 6.3 6.5 (6.3-6.7) 6.45 (6.4-6.5) - POC 2.4 2.2 2.7 (2.6-2.9) 2.8 (2.6-2.9) - CM3 5.4 5.4 5.3 (5.0-5.5) 5.2 (5.0-5.3) - M3M3 6 5.9 6.0 (5.7-6.4) 5.9 (5.8-5.9) -

(Sanborn, 1937; Lemke et al., 1982; Brosset field trip. We thank Susan Cousineau (MEME Programme) and Charles-Dominique, 1991; Simmons and for revision of the English text. We also thank the curators of the ICN and IAvH mammal collections. Julio Betancur Voss, 1998). It is important to emphasize facilitated the use of the stereoscope for taking photos of that all our specimens were captured in areas skulls. Finally, we thank to Miguel Pinto, Carlos Delgado- that are under strong anthropogenic pressure, V., Hugo Mantilla Meluk and Burton K. Lim for their specifically large development projects that comments on the manuscript. could cause a strong impact on ecosystems and biodiversity loss (Rourke and Connolly, LITERATURE CITED 2003; Hooper et al., 2005). It is essential to ALBERICO M, A CADENA, J HERNÁNDEZ- develop more inventories, which constitute the CAMACHO and Y MUÑOZ-SABA. 2000. Mamíferos first step in assessing management and conser- (Synapsida: Theria) de Colombia. Biota Colombiana vation plans. The information here presented 1(1):43-75 BROSSET A and P CHARLES-DOMINIQUE. 1990. The is important for establishing morphological bats from French Guiana: a taxonomic, faunistic and and morphometric patterns among species of ecological approach. Mammalia 54:509-559. white and pale winged Peropteryx across their CASTELLANOS-CASTRO C, L PINZÓN PÉREZ, A continental-wide distribution. CARDONA CARDOZO, C MORA FERNÁNDEZ, and O VARGAS RÍOS. 2011. Estado de conservación de la vegetación del Bajo Río Pauto, Casanare Aknowledgments. FSC records were obtained during the (Colombia). Pp. 155-190, in: Mamíferos, Reptiles project: “Inventario de los mamíferos y reptiles silvestres y ecosistemas del Bloque Cubiro (Casanare): del área de explotación petrolera Cubiro de la empresa Educación Ambiental para la Conservación (T León Monctez S. A. en los municipios de Trinidad y San Luis Sicard, P Sánchez Palomino and O Vargas, eds.). de Palenque (Casanare, Colombia)”. FSC thanks David Universidad Nacional de Colombia Instituto de Andrés Marín Cardona and Pedro Sánchez-Palomino for Estudios Ambientales - Departamento de Biología their assistance in his study. HERA thanks Raul Pedroza FERRER PÉREZ A, M BELTRÁN, AP DÍAZ-PULIDO, F and Jonh Jairo Mueses for the collaboration in the Kifa´s TRUJILLO, H MANTILLA-MELUK, O HERRERA, NEW RECORDS OF Peropteryx FROM COLOMBIA 171

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APPENDIX Specimens examined: Peropteryx leucoptera: COLOMBIA, Meta, Puerto Gaitán, Campo Rubiales, bloque Kifa Este (03º50`N; 71º57`W, 350 m), October of 2009; HERC 768 adult female (fluid, skull removed); HERC 769 juvenile male (fluid, skull removed); Casanare, San Luis de Palenque, vereda La Venturosa, finca El Jordán (5º12’16,2’’ N; 71º 20’22.9’’W, 350 m), September of 2009, FSC 107 male (skin and skull) ; January of 2010, FSC 193 male (skin and skull). IAvH 2241: Meta, Río Duda, Campamento Chamusa (2º42’ N, 74º10’W, 250 m), female (skin and skull). Peropteryx pallidoptera: COLOMBIA, Caquetá, Montañita, vereda Las Juntas, hacienda Las Delicias, quebrada El Oso, cueva La Virgen (01º30’9.6”N; 75º22’5.9”W, 274 m), January 24 of 2007, JGV 021 female and JGV 015 male (skin and skull).