Darwin M. Morales-Martínez 1, M. Alejandra Camacho 2 and Santiago F. Burneo 2. Artículo

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1 Mastozoología Neotropical, 25:391398, Mendoza, 2018 Versión online ISSN Copyright SAREM, Artículo DISTRIBUTION AND MORPHOMETRIC VARIATION OF Micronycteris schmidtorum (SANBORN, 1935) (CHIROPTERA: PHYLLOSTOMIDAE) IN NORTH SOUTH AMERICA WITH THE FIRST RECORD FROM ECUADOR Darwin M. MoralesMartínez 1, M. Alejandra Camacho 2 and Santiago F. Burneo 2 1 Grupo de Conservación y Manejo de Vida Silvestre and Instituto de Ciencias Naturales, Universidad Nacional de Colombia, Bogotá, Colombia. [Correspondence: Darwin M. MoralesMartínez <dmmoralesm@unal.edu.co>] 2 Sección Mastozoología, Museo de Zoología, Escuela de Ciencias Biológicas, Facultad de Ciencias Exactas y Naturales, Pontificia Universidad Católica del Ecuador, Quito, Ecuador. ABSTRACT. We present a revision of distribution of Micronycteris schmidtorum in Northern South America reporting fourteen new localities of the species for Colombia and Ecuador on both sides of the Andes. We present the first records of the species for Ecuador, the first record for the biogeographic region of El Chocó, and fill the gap in Amazonian localities between Peru, Venezuela and Colombia. Finally, we determine morphometric variation of the species: Colombian specimens are larger than other Central and South American specimens and specimens of French Guiana are the smallest. We found size differentiation between cis and transandean populations in Colombia and Ecuador, apparently mediated by the Andes Cordillera. RESUMEN. Distribución y variación morfométrica de Micronycteris schmidtorum (Sanborn, 1935) (Chiroptera: Phyllostomidae) en el norte de Sudamérica con el primer registro en el Ecuador. En este trabajo presentamos una revisión de la distribución de Micronycteris schmidtorum en el norte de Sudamérica al reportar catorce nuevas localidades de la especie en Colombia y Ecuador en ambos lados de la cordillera de los Andes. Mostramos los primeros registros de la especie para Ecuador, el primer registro para la región biogeográfica del El Chocó y llenamos el vacío de distribución de las localidades amazónicas entre Perú, Venezuela y Colombia. Finalmente, determinamos la variación morfométrica de la especie: los especímenes colombianos son más grandes que otros especímenes de Centro y Sudamérica, mientras que los ejemplares de Guayana Francesa son los más pequeños. Encontramos la diferenciación de tamaño entre las poblaciones cis y transandinas en Colombia y Ecuador aparentemente mediadas por la cordillera de los Andes. Key words: Andes mountains, geographic distribution, Micronycteris, Neotropical bats, Phyllostomidae. Palabras clave: cordillera de los Andes, distribución geográfica, Micronycteris, murciélagos neotropicales, Phyllostomidae. Recibido 26 diciembre Aceptado 3 junio Editor asociado: R. Stevens

2 392 Mastozoología Neotropical, 25:391398, Mendoza, D. M. MoralesMartínez et al. INTRODUCTION Micronycteris schmidtorum is a poorly known, mediumsized bat known from Southern Mexico to Southwestern Brazil (Williams & Genoways 2008), it occupies a wide range of habitats including evergreen and deciduous forests, thorn forests, swamps, pastures, and orchards (Williams & Genoways 2008; Tavares & Taddei 2003; Sampaio 2016). In South America M. schmidtorum has been reported from Colombia, Venezuela, French Guiana, Brazil, Peru, and Bolivia (Ascorra et al. 1991; Simmons 1996; Simmons & Voss 1998; Porter et al. 2007; Williams & Genoways 2008; Da Rocha et al. 2017). The species is recognized by the following set of characters: a grayishwhite venter, a moderately notched band between ears, calcar longer than foot, zygomatic breadth greater than mastoid breadth, and second premolar (p3) smaller than first (p2) and third (p4) premolars (Sanborn 1949; Ascorra et al. 1991; Simmons 1996; Williams & Genoways 2008). Although confusion of Micronycteris schmidtorum with M. megalotis and M. minuta due to overlapping measurements is common, the morphological differentiation of species of Micronycteris has been well referenced in the literature (Sanborn 1949; Ascorra et al. 1991; Simmons 1996; Simmons & Voss 1998; Simmons et al. 2002; Williams & Genoways 2008; Feijó et al. 2015). Six species have been reported for the neighboring countries of Ecuador and Colombia. Three of them: M. hirsuta (W. Peters, 1869), M. megalotis (Gray, 1842), and M. minuta (P. Gervais, 1856) happen to occur in both countries whereas M. giovanniae Baker and Fonseca, 2006 is endemic to Northwestern Ecuador, and M. microtis Miller, 1898 and M. schmidtorum (Sanborn, 1935) have been reported to Colombia (Solari et al. 2013) with no records in Ecuador to date (Tirira 2017). In Colombia, M. schmidtorum is only known from two localities: Maipures Río Orinoco, Vichada department (Simmons 1996) and Puerto Nare, Antioquia department (Cuartas & Muñoz 1999). Ascorra and colleagues (1991) reported geographical size variation in M. schmidtorum with specimens from Peru and Brazil being smaller than individuals from northern Central and South America. However, morphological variation of the species is not clearly defined for two reasons: 1) evidence of specimens from Mexico analyzed by EscobedoCabrera and colleagues (2006) are inconsistent with Ascorra s hypothesis; and 2) specimens from Sitio Luanda, Ceará, Brazil, and from Jenaro Herrera, Loreto, Peru, reported by Ascorra and colleagues (1991) were later correctly identified by Simmons (1996) and Simmons & Voss (1998) as M. sanborni and M. brosseti, respectively (Williams & Genoways 2008). Herein, we review the geographical distribution of Micronycteris schmidtorum in South America, including new locality records from Colombia and the first records of this species for Ecuador. Also, we propose some insights on morphometric variation of this species throughout its distribution. MATERIALS AND METHODS To evaluate distribution and geographical variation of M. schmidtorum we gathered locality records and measurements from the literature and reviewed Micronycteris specimens conserved in two Colombian collections: Colección de Mamíferos Alberto Cadena García from Instituto de Ciencias Naturales de la Universidad Nacional de Colombia (ICN), and Colección Teriológica Universidad de Antioquia (CTUA); and two collections from Ecuador: Mammal collection of the Museo de Zoología at Pontificia Universidad Católica del Ecuador (QCAZM) and Museo de Historia Natural Gustavo Orcés V. at Escuela Politécnica Nacional (EPN; Appendix 1). We obtained 7 external and 8 craniodental measurements: total length (TL); tail length (TaL); hindfoot length (HF); ear length (Ear); forearm length (FA); tibia length (TiL); greatest length of the skull (GLS); condylobasal length (CBL); condyloincisive length (CIL); postorbital breadth (PB); braincase breadth (BB); mastoid breadth (MB); zygomatic breadth (ZB); maxillary toothrow length (MTRL); and breadth across molars (BAM). External measurements were taken for specimen s tag. Cranial measurements were taken according to Simmons & Voss (1998). We compared the mean and standard deviation of external and craniodental measurements of different populations from Central and South America to evaluate geographical variation in size

3 Micronycteris schmidtorum IN NORTH SOUTH AMERICA 393 throughout the distribution of this species. A total of 16 Micronycteris schmidtorum individuals were analyzed, 11 from Colombia and 5 from Ecuador. RESULTS We report the first records of M. schmidtorum from Ecuador, represented by five museum vouchers deposited at QCAZM and EPN (Fig. 1). One adult male specimen belongs to the eastern region of Ecuador from Yasuni Research Station, Yasuni National Park, cantón Aguarico, Orellana Province (QCAZ 4556), corresponding to the Evergreen Forest of Napo Curaray lowlands according to the Ecuadorian ecosystems classification (Ministerio del Ambiente del Ecuador 2013). Another adult male from the Eastern region of Ecuador from Domono Lundiji, Cantón Morona, Morona Santiago province (EPN 11150), corresponding to an intervened area near the Evergreen Piedmont Evergreen Forest of the Southern Eastern Andes Cordillera (Ministerio del Ambiente del Ecuador 2013).These records fill the existing gap in Amazonia of 1300 km between the nearest record to the east reported from Territorio Federal Amazonas, Rio Mavaca, 108 km SSE Esmeralda, Venezuela (2USNM ; Ascorra et al. 1991) and 1200 km for the nearest record to the south from Madre de Dios, Manu, Pakitza, Peru (MUSM 6803; Simmons 1996). Also, we report two records from Western Ecuador, one adult female from Quingue, cantón Muise, Esmeraldas Province (QCAZ 6096), corresponding to the Evergreen Forest of the Equatorial Chocó lowlands according to the Ecuadorian ecosystems classification (Ministerio del Ambiente del Ecuador 2013), and one adult male from Hacienda El Cortijo, cantón Santo Domingo, Santo Domingo de los Tsáchilas Province (QCAZ 6057), corresponding to an agriculture intervened zone according to the Ecuadorian ecosystems classification (Ministerio del Ambiente del Ecuador 2013). Both northwestern specimens correspond to the first records of this species for the biogeographic Chocó region. Finally, we found one specimen from the Tarangaro Community, cantón Arajuno, Pastaza Province (QCAZ 14801), corresponding to the Evergreen Forest of TigrePastaza lowlands, but near an agriculture intervention zone according to the Ecuadorian ecosystems classification (Ministerio del Ambiente del Ecuador 2013); this specimen was reported by Tinoco & Camacho (2015) as M. megalotis and presumably correspond to M. schmidtorum based in size of lower premolars, although identification is difficult due to the fragmented skull. Vouchers QCAZ 4556 and QCAZ 6096 are preserved as dried skins and skulls, QCAZ corresponds to a partial skeleton and QCAZ 6057 is preserved as a fluid specimen with skull removed. For Colombia we report ten new localities for M. schmidtorum in two biogeographical provinces according HernándezCamacho et al. (1992). Pericaribbean Arid Belt: Barrancas, La Guajira department (ICN 14750, 14752; CTUA 1255) and PNN Tayrona, Santa Marta, Magdalena department (ICNCCG 010); and Orinoco Llanos: Río Casanare, Tame, Arauca department (ICNRCFR 427); San Luis de Palenque, Casanare (ICNMRP 889); Reserva Natural La Palmita, Caño Guajivo, Trinidad, Casanare department (ICND3M 290; ICN RCFR 253); Támara, Casanare department (ICNGEP 815) San Carlos de Guaroa, Meta department (ICN 21576); San Martín, Meta department (ICNFSC 451) and Villavicencio, Meta department (ICNEMG 095; Fig. 1). All the specimens with exception of QCAZ 6057 show the diagnostic characters of M. schmidtorum including a white or grayishwhite venter, a moderate notched band between ears, calcar longer than foot, and second premolar (p3) smaller than first (p2) and third (p4) premolars (Sanborn 1949; Ascorra et al. 1991; Simmons 1996; Williams & Genoways 2008; Fig. 2). QCAZ 6057 was identified based on size of lower premolars, and measurements ranges. Almost 60% of M. schmidtorum specimens referenced here are misidentifications of M. megalotis (QCAZ 4556; QCAZ 14801; EPN11150; ICNRCFR 427; ICND3M 290; ICNRCFR 253; ICNGEP 815; ICN 21576) or M. minuta (QCAZ 6096; QCAZ 6057). The evident contrast between dorsal and ventral fur

4 394 Mastozoología Neotropical, 25:391398, Mendoza, D. M. MoralesMartínez et al. Fig. 1. Geographic distribution of Micronycteris schmidtorum. Solid circles: Localities from the literature including Ascorra et al. (1991), Simmons (1996) EscobedoCabrera et al. (2006) Williams and Genoways (2008) and Da Rocha et al. (2017). Solid triangles: First records of Micronycteris schmidtorum from Ecuador. Solid squares: New records of Micronycteris schmidtorum from Colombia. coloration in the species is not distinctive in some specimens and could be the cause of the misidentifications with M. megalotis. Therefore, a comparison of lower premolars size is necessary to make a correct identification. Morphometric variation of M. schmidtorum shows that specimens from Colombia are slightly larger than specimens from Central and South America. In Colombia and Ecuador, western specimens are larger than eastern ones suggesting that the Andean Cordillera could be a geographic barrier that promotes differentiation of isolated populations; although that variation should be confirmed with additional sampling from those populations. West of the Andes in Panama are the smallest individuals, and for populations east of the Andes specimens from French Guiana show the smallest sizes, being the smallest of all known from the geographic distribution of this species (Table 1). This pattern is different to the one found by Ascorra et al. (1991). DISCUSSION AND CONCLUSIONS Distributional records show that M. schmidtorum occupies a wide range of habitats and natural regions including the Amazon basin and the Chocó, although rarity of the species could be related to small populations or low detectability using standard methods; Simmons & Voss (1998) reported two males in 3126 captures (>1% relative abundance), and in three localities reported here abundance did not reach 1% of the assemblage: Trinidad Casanare (0.002%; 2 of 818 individuals), Támara,

5 Micronycteris schmidtorum IN NORTH SOUTH AMERICA 395 bat species associated with a cistrans Andean diversification (Artibeus, Dermanura; Larsen et al. 2007; Hoofer et al. 2008; Solari et al. 2009) and morphometric variation (Phyllostomus; RodríguezPosada & SanchezPalomino 2009), which is possibly associated with morphometric differences between cis and transandean size differences in M. schmidtorum. 2) Size differences are part of cryptic diversity of the species not assessed to date. According to Siles et al. (2013) M. schmidtorum has 3% genetic divergences among Peruvian and Panamanian specimens and could be related to the morphological variation found herein. It is necessary to verify Andean influence and cryptic diversity with further sampling, and to include a revision of discrete characters and molecular analyses of different populations to resolve taxonomic entities. ACKNOWLEDGEMENTS We give special thanks to Hugo López Arevalo (ICN), Sergio Solari (CTUA) and Luis Albuja (EPN) for permitting us to study specimens under their care. Rubén D. Jarrín took photographs of the specimen QCAZ 6096 included in the paper. DMM thanks to División de Investigación de la sede Bogotá (DIB), Universidad Nacional de Colombia for providing funding to review the collection of CTUA and QCAZ. Fig. 2. Dorsal, ventral and lateral view of skull and lateral view of mandible of M. schmidtorum (QCAZ 6096) from W Ecuador. A) Relation of length of zygomatic breadth compared to mastoid breadth. B) Size of second premolar (p3) that is smaller than first (p2) and third (p4) premolars. Scale bar 3 mm. Casanare (0.003%; 1 of 398 individuals); and Tame, Arauca (0.002%; 1 of 574 individuals; unpublished data). Described morphometric variation does not support the hypothesis of Ascorra and colleagues (1991). Size differences within the geographic distribution of M. schmidtorum could be related to two hypotheses: 1) Andes represents a considerable barrier that causes cisand transandean size differences. These mountains are considered the principal biogeographic barrier in north South America for lowland LITERATURE CITED Ascorra, C. F., D. E. Wilson, & A. L. Gardner Geographic distribution of Micronycteris schmidtorum Sanborn (Chiroptera: Phyllostomidae). Proceedings of the Biological Society of Washington 104: Cuartas, C., & J. Muñoz Nemátodos en la cavidad abdominal y el tracto digestivo de algunos murciélagos colombianos. Caldasia 21:1025. Da Rocha, P. A. et al New records of Micronycteris schmidtorum Sanborn, 1935 (Phyllostomidae, Chiroptera) for Northeastern Brazil. Mastozoología Neotropical 24: EscobedoCabrera, E., L. LeónPaniagua, & J. Arroyo Cabrales Geographic distribution and some taxonomic comments of Micronycteris schmidtorum Sanborn (Chiroptera: Phyllostomidae) in Mexico. Caribbean Journal of Science 42: Feijó, A., P. A. Da Rocha, & S. F. Ferrari How do we identify Micronycteris (Schizonycetris) sanborni Simmons, 1996 (Chiroptera, Phyllostomidae) reliably and where we can find this species in Brazil? Papéis Avulsos de Zoologia 55: HernándezCamacho, J. I., A. H. Guerra, R. O. Quijano, & T. Walschburger Unidades biogeográficas de Colombia. La diversidad biológica

6 396 Mastozoología Neotropical, 25:391398, Mendoza, D. M. MoralesMartínez et al. de Iberoamérica (G. Halffter, ed.). Acta Zoológica Mexicana, México D.F. Hoofer, S. R., S. Solari, P. A. Larsen, R. D. Bradley, & R. J. Baker Phylogenetics of the fruiteating bats (Phyllostomidae: Artibeina) Inferred from Mitochondrial DNA Sequences. Occasional Papers Museum of Texas Tech University 277:115. Larsen, P. A. et al Phylogenetics and phylogeography of the Artibeus jamaicensis complex based on Cytochromeb DNA sequences. Journal of Mammalogy 88: Ministerio del Ambiente del Ecuador Sistema de Clasificación de los Ecosistemas del Ecuador Continental. Subsecretaría de Patrimonio Natural, Quito. Porter, C. A., S. R. Hoofer, C. A. Cline, F. G. Hoffmann, & R. J. Baker Molecular phylogenetics of the phyllostomid bat genus Micronycteris with descriptions of two new subgenera. Journal of Mammalogy 88: RodríguezPosada, M. E., & P. SánchezPalomino Taxonomía del género Phyllostomus (Chiroptera: Phyllostomidae) en Colombia. Mastozoología Neotropical 16: Sampaio, E., Lim, B., & S. Peters Micronycteris schmidtorum. The IUCN Red List of Threatened Species 2016: e.t13383a Sanborn, C. C Bats of the genus Micronycteris and its subgenera. Fieldiana Zoology 31: Siles, L. et al A new species of Micronycteris (Chiroptera: Phyllostomidae) from Bolivia. Journal of Mammalogy 94: Simmons, N. B A new species of Micronycteris (Chiroptera: Phyllostomidae) from Northeastern Brazil, with Comments on Phylogenetic Relationships. American Museum Novitates 3158:134. Simmons, N. B., & R. S. Voss The mammals of Paracou, French Guiana: A neotropical lowland rainforest fauna Part 1. Bats. Bulletin of the American Museum of Natural History 237:1219. Simmons, N. B., R. S. Voss, & D. Fleck A new Amazonian species of Micronycteris (Chiroptera: Phyllostomidae) with notes on the roosting behavior of sympatric congeners. American Museum Novitates 3358:114. Solari S. et al Operational criteria for genetically defined species: analysis of the diversification of the small fruiteating bats Dermanura (Phyllostomidae: Stenodermatinae). Acta Chiropterologica 11: Solari, S., Y. MuñozSaba, J. V. RodríguezMahecha, T. R. Defler, H. E. RamírezChaves, & F. Trujillo Riqueza, endemismo y conservación de los mamíferos de Colombia. Mastozoología Neotropical 20: Tavares, V. C., & V. A. Taddei Range extension of Micronycteris schmidtorum Sanborn, 1935 (Chiroptera: Phyllostomidae) to the Brazilian Atlantic forest, with comments on taxonomy. Mammalia 67: Tinoco, N., & M. A. Camacho Records of bats predated by Leopardus pardalis (Carnivora: Felidae) in eastern Ecuador. Revista Biodiversidad Neotropical. 5: Tirira, D. G Guía de campo de los mamíferos del Ecuador. 2nd edition. Editorial Murciélago Blanco, Quito. Williams, S. L., & H. H. Genoways Subfamily Phyllostominae Gray, Mammals of South America. Volume 1: Marsupials, Xenarthrans, Shrews, and Bats. (A. L. Gardner, ed.). University of Chicago Press, Chicago and London. APPENDIX 1 Specimens examined: COLOMBIA. Arauca, Tame (ICNRCFR 427); Casanare: San Luis de Palenque (ICNMRP 889 ); Támara (ICNGEP 815); Trinidad, Reserva Natural La Palmita, Caño Guajivo, (ICND3M 290 ; ICNRCFR 253 ); La Guajira: Barrancas (ICN 14750, ; CTUA 1255 ); Magdalena: Santa Marta, Parque Nacional Natural Tayrona, Bahía Concha (ICN CCG 010 ); Meta: San Carlos de Guaroa (ICN ); San Martín (ICNFSC 451); Villavicencio (ICNEMG 095 ). ECUADOR. Esmeraldas: Muisne, Quinque, Cerca al poblado de Quinque (QCAZ 6096 ); Morona Santiago: Cantón Morona, Parroquia San Isidro, Domono Lundiji (EPN ); Orellana: Parque Yasuní (QCAZ 4556 ); Pichincha: Santo Domingo (QCAZ 6057 ); Pastaza: Alrededores de Villano, Comunidad Tarangaro (QCAZ 14801)

7 Table 1 Means and standard deviations of measurements of Micronycteris schmidtorum over its range of distribution. 1 Data from EscobedoCabrera et al. (2006); 2 Data from Ascorra et al. (1991); 3 Data from Tavares & Taddei (2003) and Da Rocha et al. (2017); 4 Data from Simmons and Voss (1998). Numbers in parenthesis show the sample size. TL TaL HF Ear FA TiL GLS 20.1 ± 0.26 CBL ± 0.49 CIL PB 4.10 ± 0.09 BB MB 8.49 ± 0.17 Mexico 1 Guatemala 2 Costa Rica 2 Panama 2 NW. Colombia E. Colombia W. Ecuador E. Ecuador Venezuela 2 Brazil 3 French Guiana ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 0.13 Micronycteris schmidtorum IN NORTH SOUTH AMERICA 397

8 ZB 9.06 ± 0.05 MTL 7.19 ± 0.16 Mexico 1 Guatemala 2 Costa Rica 2 Panama 2 NW. Colombia E. Colombia W. Ecuador E. Ecuador Venezuela 2 Brazil 3 French Guiana ± ± ± ± ± ± 0.19 BAM 6.74 ± ± ± ± ± ± ± ± ± ± ± ± 4.47 (30) 7.27 ± ± 0.17 (Table 1 cont.) 7.15 ± ± Mastozoología Neotropical, 25:391398, Mendoza, D. M. MoralesMartínez et al.