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Mastozoología neotropical

versión impresa ISSN 0327-9383versión On-line ISSN 1666-0536

Mastozool. neotrop. vol.23 no.1 Mendoza jun. 2016

 

ARTÍCULO

Distribution of the spix's disk-winged bat, Thyroptera tricolor SPIX, 1823 (Chiroptera: Thyropteridae) in Colombia, with first records for the middle Magdalena Valley

 

Nicolás Reyes-Amaya1, Julián Lozáno-Flórez2, David Flores1, and Sergio Solari3

1 Unidad Ejecutora Lillo (CONICET - Fundación Miguel Lillo), Miguel Lillo 251, San Miguel de Tucumán, Argentina [Correspondencia: <nicolas.reyes2@gmail.com>].
2 Universidad Industrial de Santander, Calle 9 con Carrera 27, Ciudad Universitaria, Bucaramanga, Colombia.
3 Instituto de Biología, Universidad de Antioquia, Calle 67 No. 53-108, Medellín, Colombia.

Recibido 22 septiembre 2015.
Aceptado 13 febrero 2016.
Editor asociado: E Lessa.


ABSTRACT.

Thyroptera tricolor is a rarely collected bat species that inhabits lowland forests in Central and South America. We review the distribution of T. tricolor in Colombia, using previous and new records deposited in scientific collections of the world, providing a distribution map and a gazetteer with comments on available geographical information. We also provide first records for the Middle Magdalena Valley, with external and cranial measurements. These new records reduce the distributional gap between northern and southern records of the country. Additionally, by comparing dental measurements of our recent specimens with fossil records of thyropterids from the Magdalena Valley (La Venta deposits), we contribute to understanding the evolution and distribution of this group, reinforcing the hypothesis of evolutionary stasis.

RESUMEN.

Distribución del murciélago de ventosas de Spix, Thyroptera tricolor Spix, 1823 (Chiroptera: Thyropteridae) en Colombia, con nuevos registros para el valle del Magdalena Medio.

Thyroptera tricolor es un murciélago rara vez colectado, que habita bosques de tierras bajas en Centro y Suramérica. Revisamos la distribución de T. tricolor en Colombia, utilizando registros previos y nuevos depositados en colecciones científicas del mundo, incluyendo un mapa de distribución y un directorio geográfico con comentarios sobre la información geográfica disponible. Proveemos los primeros registros para el valle del Magdalena Medio, con medidas externas y craneales. Los nuevos registros reducen la brecha de distribución entre el norte y el sur del país. Adicionalmente, mediante la comparación de mediciones dentales entre nuestros registros recientes y fósiles de thyroptéridos del valle del Magdalena (depósitos de La Venta), contribuimos a la comprensión de la evolución y distribución de este grupo, reforzando la hipótesis de estasis evolutiva.

Key words: New records; Lowland forest bat.

Palabras clave: Murciélago de bosques de tierras bajas; Nuevos registros.


INTRODUCTION

The disk-winged bats family (Chiroptera: Thy­ropteridae) comprise five species: Thyroptera tricolor, T. discifera, T. lavali, T. devivoi and T. wynneae, the last two recently recognized (Gregorin et al., 2006; Velazco et al., 2014). These bats are characterized by the presence of circular adhesive disks on the sole of the foot and base of the thumb (Simmons, 1998), which they use to roost inside furled leaves of Heliconia (Heliconiaceae), Musa (Musaceae), Calathea (Marantaceae), Phenakospermum (Strelitziaceae) and dead leaves of Musa, Cecropia (Cecropiaceae) or palm fronds (Are­caceae) (Velazco et al., 2014).

Thyropterids inhabit lowland forests (Findley and Wilson, 1974) from southern Mexico to southeastern Brazil, being T. tricolor (Fig. 1) the most widely distributed species (Wilson, 2008); discontinuously in Central America from southern Mexico to Panama (not registered in El Salvador), and continuously in South America through Colombia, Venezuela, the Guianas, Trinidad, Ecuador, Peru, Bolivia and Brazil. Studies of this species have focused on ecology (Findley and Wilson, 1974; Vonhof and Fenton, 2004), ethology (Chaverri and Gillam, 2015), development (Wimsatt and Enders, 1980), functional morphology (Riskin and Fenton, 2001; Dechmann et al., 2006) and genetics (Vonhof et al., 2001; Buchalski et al., 2014). Even be­ing considered the most commonly collected and studied thyropterid (Velazco et al., 2014), it presents a low capture incidence with conven­tional techniques for chiropterans (Castaño-Salazar et al., 2004), as occurs with the remaining species of the group. This would be the principal cause of lacking information on distribution, natural history, and phylogenetic relationships of the group (Solari et al., 2004). In this report, we review previous and new collection records of T. tricolor for Colombia, a country with low scientific records for many mammal species (Gardner, 2008; Patton et al., 2015), includ­ing comments on geographical information available at present. We also report the first records for the Middle Magdalena Valley (Santander and Antioquia) with external and cranial measurements, plus dental measurement comparisons with unique fossils recorded for the group, coming from the same valley (La Venta deposits, Czaplewski et al., 2003).


Fig. 1. Adult female and juvenile male of Thyroptera tricolor from Barrancabermeja, Santander, part of the new records for the Middle Magdalena Valley (A). Detail of the wing circular disk of the adult female (B).

MATERIALS AND METHODS

All known records of T. tricolor for Colombia were obtained by comprehensive revision of the literature published on the species, data bases of the Global Biodiversity Information Facility (GBIF), Mammal Networked Information System (MaNIS), Sistema de Información sobre Biodiversidad de Colombia (SIB) (data sets including records from the American Museum of Natural History, AMNH; Field Museum of Natural History, FMNH; United States National Museum, USNM; Instituto Alexander von Humboldt, IAvH) and the information directly provided by most scientific collections of mammals in Colombia: Colección Mastozoológica del Chocó (CMCH), Colección de Mamíferos Alberto Cadena García at the Instituto de Ciencias Naturales (ICN), Museo de Historia Natural-Universidad Industrial de Santander (MHN-UIS), Museo Javeriano de Historia Natural Lorenzo Uribe (MPUJ-MAMM), Universidad del Valle-Vertebrados Mamíferos (UV), Colección de Mastozoología Universidad del Quindío (CMUQ), Museo de Ciencias Universidad El Bosque (MCUB), Colección Teriológica Univer­sidad de Antioquia (CTUA) and Museo de Historia Natural Universidad de La Salle (MLS), as well as specimens analyzed from new collects in inclusion process by scientific collections (ICN and CTUA). We offer a gazetteer and a map with all known records of T. tricolor for Colombia (Appendix 1 [Supplementary Material]; Fig. 2), excluding re­cords without voucher evidence, and records with no geographical coordinates and locality registered. Each locality available was checked in order to identify any ambiguous information, mistakes, and lack of information. When geographical coordinates or part of the locality was not available, they were inferred from other gazetteers (Lemke et al., 1982; Botero et al., 2005; Gardner, 2008; Ramírez-Chaves, 2011; Saavedra-Rodríguez and Rojas-Díaz, 2011; Velazco et al., 2014) or from the locality information avail­able using point-radius method (Wieczorek and Hijmans, 2004; Escobar et al., 2014) through the software QGIS 2.8.2 (accessed on 05/09/2015; QGIS Project, 2015), generating geographical coordinates with limited accuracy, measured by an uncertainty range in meters.


Fig. 2. Distribution map of Thyroptera tricolor for Co­lombia based on collection records, showing localities previously reported with geo­graphic coordinates associated (empty circles), localities previ­ously reported with coordinates inferred in this study from locality information registered (filled circles) and new re­cords (first for Antioquia and Santander, also including first for the Middle Magdalena Val­ley; filled triangles). Numbers indicate the locality registered in the gazetteer provided, and numbers in parentheses indicate the amount of records associated with those localities (see Appendix 1 [Supplementary Material]).

New records of T. tricolor reported for Colombia were deposited at ICN and CTUA collections, provid­ing geographical information, kind of preparation, collector name, collection date (Appendix 1 [Supplementary Material]), ecological data (Table 1), as well as external and cranial measurements (Table 2). For measurements and identification of specimens we followed Velazco et al., (2014). Dental measure­ment comparisons with fossil records of thyropterids from the Magdalena Valley (La Venta deposits; Czaplewski, 1996, 1997; Czaplewski et al., 2003) deposited at Instituto Nacional de Investigaciones Geológico-Mineras, Bogotá, Colombia (IGM) were obtained using ImageJ software (Schneider et al., 2012) (Table 3).

Table 1 Ecological information associated with Thyroptera tricolor new collection records from Colombia.

Table 2 External and cranial measurements (mm) and weights (g) of Thyroptera tricolor new records from Colombia (Total length, TL; Ear, E; Forearm, FA; Tail, T; Hindfoot, H, Weight, W; Greatest length of skull, GLS; Condyloincisive length, CIL; Braincase breadth, BB; Rostral length, ROL; Zygomatic breadth, ZB; Postor­bital breadth, PB; Maxillary toothrow length, MTRL; Width at M3, M3-M3; Length of mandible, LMA; Mandibular toothrow length, MANDL). Juveniles were excluded. Measurements taken from Velazco et al (2014) indicates: mean, observed range (in parentheses), and sample size. * indicates values that fall out of the ones reported by Velazco et al. (2014) for the species.

Table 3 Dental measurement (mm) comparisons of Thyroptera tricolor new records from the m Middle Magdalena Valley with fossil records of thyropterids from La Venta deposits (Magdalena Valley). Juveniles were excluded. When fossil measurements have more than one value in each measure, they correspond to different teeth vouchers (see Czaplewski, 1996; 1997; Czaplewski et al., 2003). Acronyms: Colección Teriológica Universidad de Antioquia (CTUA) and Colección de Mamíferos Alberto Cadena García at the Instituto de Ciencias Naturales (ICN).

RESULTS

We compiled 89 records (80 previous and 9 new), distributed along 37 localities of the 5 natural regions of Colombia, in lowland and subandean forests with altitudes since sea level to aproximately 1800 meters (Table 1; Appendix 1 [Supplementary Material]). Just two records were found from our literature revision: MHNUC 381 (Museo de Historia Natural Universidad de Caldas) from Caldas Department (Castaño-Salazar et al., 2004) and MPUJ-MAMM 1216 from Quindío De­partment (Pérez-Torres and Cortés-Delgado, 2009). However, the last record was corrected as T. lavali by S. Solari, and has been excluded from this report. The collections of this species in Colombia started in 1910 decade (with two collects), reached its peak in the 1970 decade (with 34 collects), and since 2003 until 2015 increased in just 13 specimens (Appendix 1 [Supplementary Material]). Twenty one records presented some ambiguous informa­tion that was corroborated, 55 were lacking information that was supplemented (10 cases corresponding to geographical coordinates inferred from locality, 40 geographical coor­dinates inferred from literature, 5 localities inferred from geographical coordinates), and 18 presented some wrong information that was corrected (Appendix 1 [Supplementary Material]).

Six out of the nine new records provided for Colombia were first ones for Santander, and the remaining three for Antioquia. Eight of them were first records for the Middle Magdalena Valley (Fig. 2; Table 1). Records from Santander were captured by hand from its roosting place; a juvenile male from Landazuri municipality was captured in February 2015 inside a furled leaf of Heliconia (Heliconiaceae), within a patch of gallery forest highly inter­vened beside a paddock. Few minutes later, in the same place, an adult female flew inten­tionally to roost over the carry bag in which the juvenile was stored, being also captured (Table 1). All individuals from Barrancaber­meja municipality (three adults, one juvenile) were captured by hand in July 2015 next to a highly traveled road, in an agro-ecosystem within a patch of secondary forest highly in­tervened, inside furled leaves of Heliconia and Calathea (Marantaceae) (Fig. 1; Table 1). The individuals from Antioquia were captured in 1993, 1996 and 2008, but only now, with our work, they were catalogued into a scientific collection (CTUA) (Table 1). We lack precise field data (locality and date) for specimens from 1993 and 1996, but we have information for the specimen collected in 2008. This adult female was netted within a secondary growth tropical forest, near to the Alicante River in Maceo municipality, on May (Table 1).

External and cranial measurements of our recent T. tricolor records for Colombia showed slight differences regarding measurements reported by Velazco et al. (2014) for the species (Table 2). Dental measurement comparisons with fossils showed that recent records of T. tricolor specimens have smaller teeth dimensions by about 3.75% to 40.72% (m2 talonid width and M2 transverse width, respectively) regarding T. cf. lavali fossils (Czaplewski, 1996; Czaplewski et al., 2003); nevertheless, they have larger anteroposterior length of the m1 and m2 by about 4.17% to 9.60% (Table 3). On the other hand, similar comparisons of our T. tricolor specimens regarding T. cf. tricolor fossils (Czaplewski, 1997) showed that dental dimensions of current specimens closely match or slightly exceed those of fossil ones (Table 3).

DISCUSSION

According to Galindo-González (2004), T. tricolor is sensitive to habitat disturbance, principally because of its highly specialized diet and habitat requirements. However, this author also recognized that the species inhabits secondary forests and agro-ecosystems. The latter agrees with our findings and those of Findley and Wilson (1974) and Boada et al. (2010). While recognizing the likely sensitivity of this species to specialized roosting places availability (Vonhof and Fenton, 2004), in our study, this was observed in plant populations of Heliconia and Calathea located in disturbed and fragmented patches of agro-ecosystems, and gallery forests with recurrent human activities, supporting the fact that this species is tolerant to highly disturbed habitats. Com­piled records for Colombia show the presence of the species in subandean forests, between 1000 and 1818 meters (Table 1; Appendix 1 [Supplementary Material]), contrasting with the typical lowland distribution (Findley and Wilson, 1974). Previous data on reproductive activity of T. tricolor shows pregnant females in Costa Rica during August (Costa Rica; Findley and Wilson, 1974), while in Peru (Ascorra et al., 1996) and Bolivia (Anderson and Webster, 1983) pregnant females were observed from September to November (those from Bolivia coupled with adult females nursing neonates); however, in Nicaragua females were inactive in November (Medina-Fitoria et al., 2015), and a reproductive male was observed in April (Medina-Fitoria, com pers.). This information, along with ours, suggests that this species may reproduce throughout the year; we found two adult females with juveniles in February and July (Table 1), but more evidence is needed to understand its reproductive cycles. Specific echolocation calls are recognized for T. tricolor, allowing group and strong individual recognition (Chaverri and Gillam, 2015). This behavior could be in agreement with the one registered for the adult female collected in Landazuri municipality (Santander; Table 1), which flew to roost over a carry bag containing a juvenile captured few minutes earlier.

New records of T. tricolor for Colombia extend the known distribution of this species in the country, previously restricted to the northernmost and the southern portions, providing continuity and filling the northern portion of the Andean region at the Middle Magdalena Valley (Santander and Antioquia; Fig. 2). Minor differences found between measures of the new records for Colombia (from the Middle Magdalena Valley) and those reported by Velazco et al. (2014) for the species (Table 2) could be interesting. The whole Magdalena Valley is recognized as a complex biogeographic area, where at least six areas of endemism of mammals overlap its boundaries (Noguera-Urbano and Escalante, 2015). Also, the Middle Magdalena Valley is proposed as part of the Nechí-San Lucas refuge, a hu­mid biological refuge during the Pleistocene. Uprising of the Andean cordilleras, initiated during the Cretaceous and completed during the Pliocene and latter Pleistocene, formed three cordilleras and their inter-andean valleys in Colombia, allowing emergence of new environments relatively isolated from others and generating a direct impact on evolution of fauna and flora (Hernández-Camacho et al., 1992). New records of T. tricolor from the Middle Magdalena Valley provide valuable material for the understanding of the evolution and distribution of disk-winged bats, through comparisons with fossil records of thyropterids from La Venta (Magdalena Valley), a deposit from the Miocene, just before the Andean cordilleras were completely formed (approxi­mately 12.5 million years ago, Czaplewski, 1996; Czaplewski, 1997; Czaplewski et al., 2003; Table 3). These fossils are unique for the family, but their taxonomic affinities are not clearly resolved (Velazco et al., 2014). Dental com­parison between new T. tricolor specimens with T. cf. tricolor fossils was consistent with those reported by Czaplewski et al., (2003), showing no significant differences between T. cf. tricolor fossils and current T. tricolor specimens (not reaching 0.5 mm difference in any instance; Table 3). This finding reinforces the possible presence of evolutionary stasis (at least in dental dimensions). Additionally, comparisons of new T. tricolor specimens with T. cf. lavali fossils was consistent with that reported by Czaplewski (1996; 1997), showing fossils dental dimensions considerably bigger than current T. tricolor specimens. Nevertheless, our report also shows that the anteroposterior dimensions of m1 and m2 teeth are bigger in current T. tricolor specimens than in T. cf. lavali fossils (Table 3). In general, the dental dimension with bigger variation between current T. tricolor specimens and thyropterid fossils (T. cf. tricolor and T. cf. lavali) is the M2 transverse width.

The review of previous and new records of T. tricolor for Colombia reveals a low amount of specimens in scientific collections (89 records). This not necessarily means the species is un­common (Vonhof and Fenton, 2004), but shows that it is poorly captured with conventional techniques for chiropterans, maybe due to its life history (Castaño-Salazar et al., 2004). Most records of this species in Colombia come from the Pacific coasts region (56.18%), followed by the Caribbean coast and the Andean regions (20.22% each), being concentrated in scientific collections out of Colombia (61.80%), princi­pally collected between 1942 and 1975 (65.43%; excluding eight records without collection date; Appendix 1 [Supplementary Material]). This summary urges for an increasing collection of specimens in subsampled regions, to be deposited at local scientific collections, facilitating its physical revision by local researchers. Comprehensive revision of localities registered, correcting and complimenting them, and providing geographical coordinates, constitute a goal of this report, supplying a more accurate idea of previous and current known distribu­tion of T. tricolor in Colombia (Fig. 2). Recent taxonomic arrangements in genus Thyroptera, associated with increased collections in some countries (Velazco et al., 2014), reveal the importance of scientific collections for species whose taxonomy and distribution are poorly known.

ACKNOWLEDGEMENTS

We thank H. López-Arévalo and C. Cárdenas-González (ICN), A.M. Jiménez (CMCH), M.P. Ramírez-Pinilla (MHN-UIS), J. Pérez-Torres (MPUJ-MAMM), H. Mantilla-Meluk (CMUQ), F. Dueñas and A. Alviz (MCUB), and D. Zurc (MLS), for providing access to information from the collections they are in charge of. We thank V. Rojas-Díaz for his help obtaining information from the UV collection, A. Jerez at the Laboratorio de Equipos Ópticos Compartidos (LEOC) in the Departamento de Biología-Universidad Nacional de Colombia, for taking the pictures of the teeth of the specimens from Santander, M.C. Calderón-Capote, for helping the inclusion process of specimens from Santander at ICN collection and checking their sex, N. Rey and M. Torres, for their advice in point radius methodology, and the anonymous reviewers, for their valuable comments. We also thank Corporación para el Desarrollo Tecnológico Sostenible (CINDETS) and Biotica Consultores LTDA, for placing specimens collected in Landazuri (Santander) into a scientific collection (ICN), facilitating its inclusion in this work.

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SUPPLEMENTARY MATERIAL ONLINE

Appendix 1.

Compiled records of Thyroptera tricolor for Colombia. The documented geographi­cal coordinates or altitude marked with asterisk (*) correspond to values previously inferred by scientific collection possessing voucher specimen associated to such information, but not to a real value recorded by the collector.

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