Emballonurid bats from Colombia: Annotated checklist, distribution, and biogeography

Murciélagos embalonúridos de Colombia: Lista anotada, distribución y biogeografía 

Hugo Mantilla-Meluk^1*, Héctor E. Ramírez-Chaves², Alex M. Jiménez-Ortega³ y Miguel E. Rodríguez-Posada⁴

¹ Programa de Biología, Universidad del Quindío, Carrera 15, Calle 12 Norte Armenia, Quindío, Colombia, Sur América. E-mail: hugo.mantillameluk@gmail.com. *Corresponding author.

³ Universidad Tecnológica del Chocó, Diego Luis Córdoba, Quibdó, Chocó, Colombia. E-mail: alexmauriciojimenez@gmail.com (AMJ-O).

⁴ Pontificia Universidad Javeriana, Bogotá D. C., Colombia. E-mail: migrodriguezp@gmail.com.

Sometido: 20 de enero de 2014.
Revisado: 21 de marzo de 2014.
Aceptado: 20 de abril de 2014.

Abstract

Introduction: Genetic data hypothetically place the origin of the most recent common ancestor of the subfamily Emballonurinae in Africa, suggesting a dispersal event from Africa to South America during the Oligocene (30 Ma), and a subsequent allopatric radiation in the New World. Emballonurid genera exist in Central America where, to date, only one event of diversification has been documented for Balantiopteryx before the completion of the Isthmus of Panama land connection in the Pliocene.

Results: We report 16 confirmed emballonurid bat species for Colombia and three species potentially present in the country, for a total of 19 species representing the eight recognized Neotropical emballonurid genera. At 16 known species, Colombia has the second greatest number of Neotropical emballonurid bats after Brazil (17 spp.).

Discussion and conclusion: The checklist presented herein is accompanied by 11 taxonomic and distributional comments explaining recent changes in taxonomy, species distribution rearrangements, as well as clarifications and a refinement of the previous records for Colombia. In addition, Geographic Information System (GIS) models of potential distribution were created for all confirmed species in Colombia, and species richness patterns were analyzed. Finally, in a Parsimony Analysis of Endemism was performed for Colombian emballonurids we found that diversity within this group of bats in geographically subdivided in Colombia into four main regions including: The Biogeographic Chocó; the Magdalena Valley; The Orinoquia; and the Guianan-Amazon region.

Key words: Chiropterans, Parsimony Analysis of Endemism, sheath-tailed bats, sac-wing bats, distribution maps.

Resumen

Se reportan 16 especies confirmadas de murciélagos embalonúridos para Colombia y tres especies potencialmente presentes en el país, que representan un total de 19 especies, que incluyen a los ocho géneros de embalonúridos neotropicales reconocidos. Estas 16 especies, posicionan a Colombia como el segundo país en número de especies de embalonúridos del Neotrópico después de Brasil (17 spp.). La lista está acompañada de 11 comentarios que explican cambios recientes en la taxonomía y arreglos en la distribución para el grupo; así como aclaraciones sobre los registros de embalonúridos analizados. Adicionalmente, se crearon modelos de distribución potencial de especies, basados en Sistemas de Información Geográfica (SIG), para las especies confirmadas en Colombia y se analizaron los patrones de riqueza derivados de su superposición. Finalmente, se condujo un Análisis de Parsimonia de Endemismo para los embalonúridos de Colombia, con algunos comentarios sobre la biogeografía del grupo.

Palabras clave: Análisis de Parsimonia de Endemismo, mapas de distribución, murciélagos de cola, murciélagos de alas con bolsillos, quirópteros.

Introduction

There are two supraspecific taxonomic proposals to organize the diversity contained within Neotropical sheath bats: Simmons (2005) placed Neotropical emballonurids in a single subfamily (Emballonurinae), and commented that McKenna and Bell (1997) subdivided the subfamily Emballonurinae into two tribes: Diclidurini, including all Neotropical forms; and Emballonurini containing the genera: Mosia, Emballonura, and Coleura. In contrast, Hood and Gardner (2008), assert that Neotropical emballonurids are represented by two subfamilies: Diclidurinae (Gray 1866), including the genera Diclidurus and Cyttarops; and Emballonurinae (Gervais 1856), including the genera: Balantiopteryx, Cormura, Peropteryx, and Saccopteryx. The most recent systematic assessments (Lim et al. 2004, Lim 2007, Lim et al. 2008) regard all Neotropical emballonurids as part of the tribe Diclidurini. Genetic data hypothetically place the origin of the most recent common ancestor of the subfamily Emballonurinae in Africa, suggesting a dispersal event from Africa to South America during the Oligocene (30 Ma), and a subsequent allopatric radiation in the New World resulting in the tribe Diclidurini (Lim et al. 2004).

Diclidurinin bats have dispersed throughout the continental Neotropics, not reaching the Caribbean except for Peropteryx trinitatis, present as far north as Grenada. Emballonurid genera exist in Central America where, to date, only one event of diversification has been documented for Balantiopteryx before the completion of the Isthmus of Panama land connection in the Pliocene. This scenario was independently corroborated by a molecular analysis of the mitochondrial ND3-4 gene region (Lim et al. 2004).

Fossil records have been reported from the Miocene Colombian deposits of La Venta (12.5 - 12.3 Mya). Colombian fossil records include a small form of Diclidurus, and a specimen of an undetermined genus, which might represent a new taxon, sharing some characters of its upper canine with both Old World and New World emballonurids (Czaplewski 1997, Czaplewski et al. 2003). Although some Neotropical emballonurid species have wide distributions and are locally abundant, there are distributional gaps to examine in order to obtain a better understanding about their ecological requirements.

Herein, museum voucher specimens were used as primary source to generate a checklist of emballonurid bats from Colombia. In addition, selected museum voucher specimens were analyzed to verify their identifications. To facilitate the comparison of our checklist to that of Alberico et al. (2000) and Solari et al. (2013; the most comprehensive checklists of Colombian mammals available to date), we follow their format. Differences between Alberico et al. (2000), Solari et al. (2013) and the current checklist are highlighted by symbols in the table containing the list, and they are explained in more detail in the text.

The checklist is accompanied by references as well as models of potential distribution for each Colombian emballonurid species. These distribution maps were used to investigate the affinities, in species composition, among Colombian ecoregions as outlined by Hernández-Camacho et al. (1992), and to determine emballonurid richness distribution in Colombia and the relationship between environmental variables and patterns of species richness in this group of bats in the country.

Materials and Methods

Museum specimens. In order to create the checklist, we reviewed Colombian emballonurid bat records in museum collections in Colombia and the United States, as well as records reported in the scientific literature (Appendix I).

Distribution models. Models of potential distribution were created for each emballonurid bat species present in Colombia using 1,165 museum georeferenced records. Records by institution are presented in Appendix II. The georeferencing process was based upon information obtained from electronic gazetteers available at www.fallingrain.com and the National Geospatial Intelligence available at: http://geonames.nga.mil/ggmaviewer/MainFrameSet.asp. Georeferenced Colombian emballonurid sampling localities were converted into point polygon layer in ArcGIS 9.3. Each layer representing species distributional points was placed over a polygon layer of Neotropical ecoregions obtained from the website of the World Wildlife Fund (http//:www.wwf.org). Ecoregions intercepting species distributional records were selected using the Select by location option of ArcGIS 9.3 and exported as vector files. The exported files representing selected ecoregions were set as masks in the Spatial Analyst extension of ArcGIS 9.3.

Patterns of species richness. A model of emballonurid species richness in Colombia was produced by combining all raster files representing individual species distribution models in the Spatial Analyst extension of ArcGIS 9.3.

Correlation between richness and environmental variables. A raster layer representing the Colombian territory was created with a cell size of 0.05 dpi and later each cell was converted into points by applying the Conversion tool in the Spatial Analyst extension of ArcGIS 9.3; as a result of this procedure we obtained a point layer of 397 points.

This point grid was used to extract values from the species richness model, using the Extract values to point tool in the Spatial Analyst extension of ArcGIS 9.3. The same procedure was applied to raster layers representing elevation, evapotranspiration, mean annual temperature, minimum temperature of the coldest month of the year, maximum temperature of the warmest month of the year, mean annual precipitation, and vegetation (climate data from www.diva-gis.org/climate.htm). Databases associated with the point layers extracted from each environmental variable, as well as the database associated with the richness point layer, were combined into a single database and exported to the statistical package PAST (version 1.90), available at folk.uio.no/ohammer/past, and a Spearman correlation was performed among richness and environmental variables.

Parsimony Analysis of Endemism (PAE) for Colombian emballonurid bats. To identify biogeographic affinities among Colombian natural regions for emballonurid bats, a Parsimony Analysis of Endemism (PAE) was performed for the 16 recognized species for the country, based upon the arbitrary subdivision of the Colombian territory into a grid of 114 quadrants. A hypothetical ancestral area, with total absence of species, was added to the data matrices in order to group by presence rather than by absence of taxa. The program Winclada (Nixon 2002) was used to build the matrix as a subsequent interface for parsimony analysis using NONA (Goloboff 1993). The PAE was performed in TNT (Goloboff et al. 2008).

Results and Discussion

List summary. We report 16 confirmed emballonurid species for Colombia (Table 1) and three species potentially present in the country: Centronycteris maximiliani potentially present in the Amazon and Orinoquia, based upon records from Venezuela); Diclidurus isabella, potentially present in the Amazon and Orinoquia, based upon records from Brazil and Venezuela; and Peropteryx trinitatis, potentially present in the Orinoquia, based upon records from Venezuela; for a total of 19 species representing eight genera.

At 16 known species, including the endemic Saccopteryx antioquensis, Colombia has the second greatest number of Neotropical bat species of emballonurid bats, after Brazil (17 spp.) surpassing other countries of larger geographic area and greater overall mammalian diversity such as Mexico, Peru, and Venezuela (Table 2).

Taxonomic and distribution comments. Eleven taxonomic and distributional comments are included, designated by • in Table 1:

•2) Balantiopteryx infusca: the species was incorrectly included as potentially present in the department of Caquetá, based on "nearby localities" by Marín-Vásquez and Aguilar-González (2005:216). However, their conclusion was based on seven specimens deposited at the Instituto de Ciencias Naturales, Universidad Nacional de Colombia (ICN) (ICN 7737-39 and ICN 9312-15) collected in Río Engaño, and El Chanco respectively, both localities in the department of Valle del Cauca, on the western versant of the Colombian Andes. We restricted the distribution of B. infusca to the western versant of the Colombian Andes along the piedmonts of the Biogeographic Chocó and considered Alberico et al. (2000) inclusion of the species within the Andean region in that sense. To date, there is no indication of a trans-Andean flow for this taxon (Lim et al. 2004). McCarty et al. (2000) provides information on the ecology of collecting localities of B. infusca and listed the rainforest of northern Ecuador as the typical ecotype for the species.

•3) Centronycteris centralis: The presence of the species in the department of Antioquia is supported by a specimen collected at La Tirana, 25 km S, and 22 km W of Zaragoza (7° 21' N, - 75° 03' W) by N. Peterson and deposited at the University of Washington Zoological Museum (UWZM) (♂UWZM-NEP 291170). Although Cuartas-Calle and Muñoz-Arango (2003) reported C. centralis as present in the department of Antioquia, their assumption was based on records from localities adjacent to the department. The specimen of Centronycteris centralis deposited at the Field Museum of Natural History FMNH (no catalogue number provided by authors) in Cuartas-Calle and Muñoz-Arango (2003), corresponds to specimen FMNH 98230 collected by F. Medem on February first 1963 (collectors number 125), at Alto Uré, department of Córdoba (7° 46' N, - 75° 31' W, 141 m). Alto Uré is adjacent to the northern border of the department of Antioquia. An additional female record of C. centralis from the Colombian Andes (Norcasia, department of Caldas, (5° 39' N, - 74° 50' W, 420 m), deposited at the collections of the Museo de Historia Natural de la Universidad de Caldas (MHNUCa 0441), was reported by Castaño and Corrales (2007). Norcasia is adjacent to the southeastern border of the department of Antioquia. A specimen of C. centralis from Anchicayá 8 km W of Danubio (03° 37' N, - 76° 53' W), department of Valle del Cauca is deposited at the Mammal Collection of the University of Kansas (9KU 135138). Centronycteris centralis was proposed as potentially present in the Colombian Amazon region by Alberico et al. (2000), and Marín-Vásquez and Aguilar-González (2005). However, we find no specimens representing this taxon from the northern portion of the Amazon Basin.

•4) Centronycteris maximiliani: Cuervo-Díaz et al. (1986) mentioned one specimen of the species from the Colombian isolated mountainous system of the Sierra de la Macarena, extending the distribution of this taxon into the Colombian Orinoquia.

However, we found no museum specimens from this or any other locality in Colombia.

Centronycteris centralis was considered as a subspecies of C. maximiliani and it may be that this is the origin of some misidentifications and misinterpretations on species geographic boundaries between these two taxa. That was the case with a specimen of C. maximiliani (American Museum of Natural History, AMNH 74820) reported by Lemke et al. (1982) and included by Alberico et al. (2000) as reference material for this taxon in Colombia. Identification of specimen AMNH 74820 was corrected by Simmons and Handley (1998) as C. centralis. Solari et al. (2013) included C. maximilliani as present in the country based upon Simmons and Handley (1998). We regard C. maximiliani as probably present in the northern portion of the Colombian Amazon and the southern Orinoquia. Our assumption is based on a single record of C. maximiliani from the Venezuela department of Amazonas in the Guianan-Amazon Biogeographic province adjacent to the department of Vichada in Colombia, reported by Linares (1998) and deposited at the AMNH (♂AMNH 74820). Cuervo-Díaz et al. (1986:474) reported an additional record from "Province of Nechi, department of Antioquia." However, no museum record was associated with this locality, and probably this record refers to C. centralis.

•5) Cormura brevirostris: In the checklist of bats from the department of Caquetá, Marín-Vásquez and Aguilar-González (2005: 216) referred to specimen ICN 14597 of Cormura brevirostris as "recorded based on a misidentification" . We examined specimen ICN 14597 and confirmed its identification as C. brevirostris. Specimen ICN 14597 was previously misidentified as Peropteryx macrotis. Cormura brevirostris has also been recorded from the southern portion of the Colombian Amazon. We included in our list a record of C. brevirostris from Leticia, department of Amazonas, represented by a male specimen collected by Robert J. Baker on July 1 1969 (Texas Tech University Museum TTU 8825). This record was not included in Alberico et al. (2000).

•6) Cyttarops alecto: Alberico et al. (2000) reported this species from the department of Vichada apparently deposited at the Instituto Alexander von Humboldt (IAvH). However, we found no records of C. alecto from the department of Vichada at the IAvH. Cyttarops alecto is present in the southern portion of the Colombian Amazon with a record from Leticia, department of Amazonas reported by Ochoa et al. (1994), also included in Hood and Gardner (2008), corresponding to specimen IAvH 358, collected by H. Chiriví, R. W. Cooper, A. Diaz D. on March 10, 1972.

•7) Diclidurus albus: In Alberico et al. (2000) the distribution of D. albus in the Andean (and) region and the presence of D. albus in the department of Valle del Cauca (vc) were accompanied by question marks (and? vc?). We confirm the presence of D. albus in the department of Valle del Cauca (Andean Region). The record reported by Alberico et al. (2000) and also by Cuervo-Díaz et al. (1986) corresponds to a female specimen from Cali, department of Valle del Cauca collected by M. Arango on January 1^st 1949 and preserved in fluid with extracted skull (AMNH 149167); a photograph of the skull of AMNH 149167 was used by Goodwin and Greenhall (1961: plate 9) as example of the morphology of the species. To clarify the origin of Colombian D. albus records in this work, they are presented (from west to east) as follows: a specimen from Catival Upper Río San Jorge, department of Córdoba (120 m) at the Colombian Caribbean Region, collected by P. Hershkovitz (collector number 3585) on July 20, 1949 deposited at the FMNH (FMNH 69366). The above mentioned record was not included in Hershkovitz (1949); three specimens from the department of Norte de Santander collected by Brother Nicéforo María in Convención, and Cúcuta respectively (Nicéforo María 1955) deposited at the museum of Instituto de La Salle (ISL, in the publication); museum vouchers of these two specimens disappeared as a consequence of the fire which destroyed the collections of the Museo de La Salle in Bogotá during the rebellion of 9 of April of 1948; a third specimen of D. albus (virgo) from Catatumbo region, department of Santander (skull lost in the preparation) collected by Adriano Gasparoni on October 9^th 1954 close to an oil drill, was also referenced in the publication of Brother Nicéforo María (1955) as deposited at the Instituto Biffi in the city of Barranquilla, Colombia; a record from the municipio of Toledo, department of Norte de Santander collected by Germán Jurado Orozco and Guillermo Cote B. in October 2004, deposited at the IAvH; a record from the Colombia Orinoquia without precise location (Los Llanos) collected by E. Guzman in1963, deposited at the Royal Ontario Museum (ROM 75741), and a record from Villavicencio, Meta deposited at the Instituto de Ciencias Naturales (ICN 6601), preserved in fluid and collected at Villavicencio "Las Mercedes" Hacienda La Reserva, 450 m.

Although not supported by voucher specimens, we include in this revision the capture of male individual of Diclidurus, reported for the department of Vichada in an anonymous note published in the Boletín Científico, Centro de Museos, Universidad de Caldas (2012). The individual, putatively assigned to D. albus, was captured at the private reserve Bojonawi, Puerto Carreño, Vichada; 54 m, in January 7, 2012 by P. Giraldo B. The record was documented by a photograph, taken by P. Giraldo B.; no measurements are included, and authors mentioned J. H. Castaño as a contact person.

The author mistakenly cited Marinkelle and Cadena (1972) and Tamsitt and Valdivieso (1964) in reference to Colombian records from Leticia, department of Amazonas and Turbo, department of Antioquia respectively. The same error is repeated in Cuartas-Calle and Muñoz-Arango (2003) who incorrectly attributed a record of D. albus from the Urabá region, department of Antioquia, to Marinkelle and Cadena (1972). We reviewed Marinkelle and Cadena (1972), as well as Tamsitt and Valdivieso (1964) and found no reference on D. albus in these two publications. In a personal communication with Dr. Alberto Cadena, he stated that he had never added specimens of D. albus to any Colombian collection. We were unable to locate the D. albus specimens from Turbo, Antioquia supposedly deposited in the mammal collections of the Universidad de Antioquia.

•8) Diclidurus ingens: Mantilla-Meluk et al. (2009a) extended the distribution of D. ingens into the Biogeographic Chocó based on a record from Cértegui, department of Chocó deposited at the Colección Mastozoológica del Chocó (CMCH 001649). This record constituted the only record from this taxon from the western versant of the Andes.

Although the morphology observed in specimen CMCH 001649 was closer to D. ingens, Mantilla-Meluk et al. (2009a) highlighted some morphological differences present in their D. ingens Chocoan specimens with respect to Colombian known specimens from the eastern versant of the Andes, raising the possibility of cryptic diversity within this taxon.

•9) Diclidurus scutatus: This species was considered potentially present in Colombia based on Venzuelan records reported by Linares (1998) from localities adjacent to the Colombo-Venezuelan border. Marinkelle and Cadena (1972) followed Cuervo-Díaz et al. (1986) and listed D. scutatus as potentially present in Colombia. Escobedo and Velazco (2012), confirmed the presence of D. scutatus in the country based upon two specimens from the Lower Rio Apaporis, Yai-Gojes, deposited at the FMNH (FMNH 88234-88235).

•10) Saccopteryx antioquensis. Saccopteryx antioquensis Muñoz and Cuartas 2001, was described based on material collected at La Soledad, Municipio de Sonsón,department of Antioquia (5° 36' N, - 75° 56' W 2,171 m). Saccopteryx antioquensis can be distinguished from other species of the genus in Colombia (S. bilineata, S. canescens, and S. leptura) by the absence of dorsal stripes, as well as the connection of the wing to the metatarsal and not to the ankle. Allen (1900) made reference to coat color variation among S. bilineata including differences in the distinctiveness of the dorsal stripes. The author refers to this variation as follows: "The white markings on the back (of S. bilineata) vary much in distinctness in different specimens, being sometimes almost clear white and strongly defined, in other specimens brownish white, and sometimes obsolete". Allen also mentioned that an almost uniform color is common among juvenile S. bilineata.

Muñoz and Cuartas (2001) considered S. antioquensis closely related in morphology to the alloptaric S. gymnura. Saccopteryx antioquensis can be differentiated from S. gymnura by its larger size (forearm 36.2-38.0) (Muñoz and Cuartas 2001). Although Lim et al. (2007) were unable to include S. antioquensis in their phylogenetic analyses, due to the unavailability of tissues of the only two known specimens representing this taxon they proposed a split of the common ancestor of S. gymnura from S. canescens around 6 Mya. This evidence, in conjunction with differences in ecological requirements of S. antioquensis with respect to other species in the genus leads us to hypothesize an evolutionary scenario for the divergence of S. antioquesis associated with the Andean uplifting. Saccopteryx gymnura with type locality in Santarem, Pará, Brazil, is known only from the northeastern Guiana and is not present in Colombia.

•11) Saccopteryx bilineata: This species is widespread, and is distributed in Neotropical lowlands from Mexico (Ceballos and Oliva 2005) to southeastern Brazil (Simmons 2005). Elevational ranges proposed for S. bilineata across its distribution are all below 800 m, including 98 S. bilineata localities in Venezuela which are within a 0 - 630 m elevational range reported by Linares (1998). Among Colombian records recovered from the literature, there is a specimen of S. bilineata from Bogotá, Colombia (2,600 m), reported by Dobson (1878) in his revision of material deposited at the British Museum. It is likely that the Colombian S. bilineata reported by Dobson (1878) are from an unknown locality in the lowlands surrounding Bogotá in the department of Cundinamarca. Known records of S. bilineata from de department of Cundinamarca include a female specimen reported by Tamsitt and Valdivieso (1963) collected at Girardot (4° 18' 11 N, - 74° 48' 3W, 223 m) (not included in Alberico et al. 2000), on October 28 1961 by James R. Tamsitt (JRT-1418), preserved in alcohol and deposited at the American Museum of Natural History (AMNH 207767). There is a second specimen (AMNH 207928) from the same locality collected by James R. Tamsitt on October 15 1961, without collector' s number. Allen (1900) mentioned two well-marked color phases black and brown among S. bilineata from the Colombia Caribbean, with a few intermediate specimens between the two phases.

General emballonurid distributional patterns. The Colombian territory is ecosystemically diverse due to a combination of complex geologic, ecological, and biogeographic processes that result in a variety of niche opportunities for bats (Mantilla-Meluk et al. 2009b). The geographic diversity of the Colombian territory can be divided into five natural regions: Amazon, Andean, Caribbean, Orinoquia, and Pacific (Chocó), each one characterized by unique arrangements of ecological variables (Hernández-Camacho et al. 1992). Our analysis revealed that richness distribution among emballonurids decreased with elevation, with the Andes as a major barrier separating allopatric emballonurid populations from the eastern and western versants of the system (Fig. 1). The greatest number of emballonurid species is associated with the lowlands of the upper Amazon (10 spp.), followed by the eastern piedmonts of the Eastern Cordillera; the northern portion of the Colombian Orinoquia; and the Biogeographic Chocó (each with more than seven species; Fig. 1). A large number of species were shared among regions (Table 3, Appendix II, IV) with only five species documented from only one region: C. alecto (Amazon), D. scutatus (Amazon), S. antioquensis (Andean), P. leucoptera (Orinoquia), and B. infusca (Pacific). The Amazon and the Orinoquia are more similar and shared the largest number of species (8 spp.); while the Biogeographic Chocó and the Orinoquia are the most dissimilar regions sharing only five species.

Our multiple correlations between emballonurid richness and environmental variables showed that emballonurid richness in Colombia had a significant, positive correlation with evapotranspiration, and a significant, negative correlation with elevation (Table 4). Higher numbers of species were found in areas with average precipitation greater than 2,000 mm, average temperature greater than 25 °C, and elevations lower than 500 m. These conditions are widely distributed across the Colombian geography, in all natural regions of the country.

Parsimony analysis of endemism. The PAE showed three subunits of higher biogeographic affinity for Colombian emballonurids: 1) Guianan Amazon region (green quadrants, Fig. 2); the Orinoquia (yellow quadrants); and 3) Biogeographic Chocó (dark blue quadrants). The Andean, as well as the Caribbean region, encloses a more variable composition of emballonurid species. Although most of the quadrants representing the Inter-Andean Valley of the Magdalena River in its lower portion (northern part of the country) appear in the PAE output as an independent clade, quadrant 19 was associated in composition with the Biogeographic Chocó. A biogeographic affinity between the Magdalena Valley, the western Caribbean and the Biogeographic Chocó was proposed by Hernández-Camacho et al. (1992).

Globally, these results are in accordance with a vicariant pattern associated with the uplifting of the Andean System, separating Colombian Cis-Andean emballonurid fauna (Amazon and Orinoquia) from its counterpart at the western portion of the country (Biogeographic Chocó). This pattern has been documented for different groups of fauna including bats (Mantilla-Meluk et al. 2009b). In the eastern portion of the country, the piedmonts of the Andes and Altillanura of the Colombian Orinoquia enclose a large number of emballonurid species, decreasing through the southern Orinoquia. In contrast to the more constant conditions of the eastern Andean piedmonts, the southern Orinoquia is characterized by dramatic fluctuations of ecological variables (Marchant et al. 2006) potentially affecting emballonurid diversity. However, it is important to consider, that the Orinoquia is one of the less understood regions of the country and the observed pattern potentially is an artifact of low sampling efforts in this portion of the country.

Final biogeographic considerations. The Guianan region, which includes the highest diversity of emballonurids, has been proposed as the center of radiation of diclidurine bats in the Neotropics (Lim et al. 2007). Two aspects are mentioned by Lim et al. (2007) as important for this radiation: 1) the uplifting of the Andes, and 2) climatic changes in the Early Miocene between 19.4 and 18.0 mya. Geologic reconstructions of ecogeographic conditions around Early Miocene suggest a different landscape in northern South America than that prevailing today. During the Miocene the presence of extensive savannas was more common and forested areas in the Amazon region were more reduced than today. During the Early Miocene the Andean system was not completely raised and an interconnection between the eastern and western versants of the proto Andes was possible along extensive areas. The Cuenca basin in Ecuador (Wesseling and Salo 2006) represents the lowest point of the Andean continental divide, and could act as a potential bridge between the two versants of the system (Fig. 3). The Trans-Andean communication between lowlands across the Cuenca Bridge was terminated around 3 Mya with the last uplifting of the Andes. On the eastern side of northern South America there was the internal lake of the Pebas system that prevailed between 23 to 8 Mya. It is likely that the Pebas formation worked as a weak barrier for lowland species between the Guianan shield and the western portion of South America. The inundated lowlands of the system may have limited the east-west communication in northern South America to the Guianan-Macarenan Bridge along the projections of the Guianan Shield into the eastern portion of the Colombian region.

Acknowledgements

This work would not be possible without the generous help of curators and personnel in charge of the scientific collections visited. We specially thank: D. Wilson, K. Helgen, A. Gardner, and L. Gordon for their assistance at the mammal collections of the USNM of the Smithsonian Institution; B. D. Patterson, L. Heaney, W. Stanley, P. Velazco, and R. Baniasek for their help at the mammal collections of the FMNH; Y. Muñoz-Saba, H. López, and C. Cárdenas for their assistance at the ICN; P. Rivas at the MHNUC, Oscar Murillo at the UV; D. Perico for his collaboration at the collections of the IAvH; A. Asprilla, L. Palacios, and O. Rios for their support at the CMCH of the UTCH.

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Editor asociado: Robert Owen

Diseño gráfico editorial: Gerardo Hernández