THE DISTRIBUTION OF BATS OF GENUS LASIURUS (VESPERTILIONIDAE) IN COLOMBIA, WITH NOTES ON TAXONOMY, MORPHOLOGY AND ECOLOGY

In order to clarify the distribution of bats of the genus Lasiurus in Colombia, we performed a morphological study of 49 specimens from four Colombian collections. Our review confirms the presence of three species in Colombia (L. blossevillii, L. cinereus, and L. ega) with distribution in all natural regions that include six of the nine biogeographic provinces. These species can be easily differentiated based on external and cranial characters. Lasiurus cinereus is the largest species (forearm length > 52 mm) and L. blossevillii is the smallest (forearm < 42 mm); L. ega has a distinctive skull shape with a developed sagittal crest. While previous literature make claims that L. egregius and L. castaneus occur in Colombia, our analysis found no support for this and even contradicts the evidence cited for their presence in the country. We demonstrate that one specimen attributed to L. egregius in literature corresponds to a misidentified L. blossevillii. Furthermore, we found that there are not any specimens of L. castaneus from the Department of Cundinamarca despite several reports in the literature. The status of subspecies in Colombia remains controversial and more specimens are needed to determine whether there are clear distinctions between forms in any geographical region. Most of the specimens examined were males and in some cases, were collected opportunistically from dead individuals found in cities in the Andean region.


INTRODUCTION
The genus Lasiurus comprises between 15-17 species of aerial insectivores distributed along North and South America (Simmons 2005, Gardner & Handley 2008).In Colombia, the number of species present is controversial.Historically, between three (Aellen 1970, Solari et al. 2013) and five species (Cuervo Díaz et al. 1986, Alberico et al. 2000) have been reported.The first account of Lasiurus in Colombia provided by Aellen (1970) included the species L. borealis (Müller, 1766), L. cinereus (Palisot de Beavois, 1796), and L. ega (Gervais, 1856).Two additional taxa have historically been included in the Colombian fauna: L. castaneus and L. egregius.Cuervo-Díaz et al. (1986) introduced records of L. casteneus [sic.](= L. castaneus Handley 1960) in the warm mountain areas of the Department of Cundinamarca, and Rodríguez-Mahecha et al. (1995) included L. castaneus in Colombia as a whole.Neither publication, however, provided voucher specimens or specific localities.Cuervo-Díaz et al. (1986) also listed L. egregius (Peters, 1870) as potentially present in Colombia based on records from adjacent countries.Alberico et al. (2000) followed the suggestions of Cuervo-Díaz et al. (1986) and claimed that specimens of L. castaneus are housed in the collections of Instituto de Ciencias Naturales (ICN) in Bogotá. Later, Muñoz (2001) indicated that the presence of L. castaneus and L. egregius is only probable in Colombia.Bejarano-Bonilla et al. (2007) listed L. egregius for the Andean region (Department of Tolima) based on the capture of one individual housed in the Zoological collections of Universidad de Tolima (CZUT).This individual is the first reported specimen of L. egregius in Colombia.The records of Cuervo-Díaz et al. (1986) and Bejarano-Bonilla et al. (2007), were not properly discussed in recent accounts of the genus (Gardner & Handley 2008, Solari et al. 2013).However, the distribution of L. egregius has been recently updated (López-Baucells et al. 2014) and two literature records from Colombia (Alberico et al. 2000 andBejarano-Bonilla et al. 2007) were included in that update.
In order to clarify the distribution of genus Lasiurus and to address the debate on the presence of L. castaneus and L. egregius in Colombia, we reviewed specimens from 4 natural history collections.We provide an updated distribution of the species within the genus, a comparison of their morphological and morphometric traits, and some ecological notes based on vouchered literature records and specimens reviewed.
We reviewed all available specimens housed at the ICN, searching for vouchers of L. castaneus as well as the specimen CZUT-M 0213 identified as L. egregius by Bejarano-Bonilla et al. (2007) to assess the accuracy of their identifications.We compared each specimen with the characters provided by Handley (1960), Shump & Shump (1982) and Gardner & Handley (2008).Additionally, we describe the morphological characters and their degree of variation in each of the species distributed in Colombia to facilitate future identification under field and laboratory conditions.
We created distribution maps for each species using specimen localities in addition to those available in the literature (Handley 1960, Gardner & Handley 2008), and housed in the collections of the American Museum of Natural History (AMNH), New York; Field Museum of Natural History (FMNH), Chicago; Muséum d'histoire naturelle de la Ville de Genève (MHNG), Geneve; and Royal Ontario Museum (ROM), Ontario.Furthermore, we analyzed the presence or absence of each species among the different geographic regions and provinces of Colombia (Table 1) proposed by Hernández Camacho et al. (1992).Finally, ecological observations were obtained from information associated with reviewed specimens.

RESULTS
Based on the reviewed specimens, we identified three distinct species distributed in Colombia: L. blossevillii, L. cinereus, and L. ega (Table 1).These species are easily differentiated by external measurements and cranial characters (Table 2, Table 3, Fig. 1).We found no evidence for the presence of L. castaneus and L. egregius in Colombia.No specimens matched the diagnostic characters of L. castaneus in the collections reviewed.Furthermore, our review of the only reported L. egregius specimen from Colombia (CZUT-M 0213; Fig. 2) reveals that it belongs to L. blossevillii, based on the following cranial, external, and morphometric characters: a developed lacrimal ridge, rusty red pelage coloration, and small size (FA 39 mm).In contrast, L. egregius lacks a lacrimal ridge, has a bright red pelage, and a larger size (FA > 46 mm) (Shump & Shump 1982, Bianconi & Pedro 2007; Table 2, Fig. 1).The probable cause for CZUT-M 0213 misidentification is the presence of only one upper premolar in the specimen, a condition generally seen in L. egregius versus the two upper premolars found in L. blossevillii.We consider this condition a dental abnormality of the individual since all other measurements of CZUT-M 0213 most resemble those of other L. blossevillii specimens from Colombia (Table 2).
Lasiurus blossevillii was the most abundant in number of specimens in the visited collections with a total of 28 from the Amazonia, Peri-Caribbean arid belt, Guyana and North Andean provinces (Table 1; Fig. 3a).It can be identified based on the following characters: medium size (FA < 42 mm), with red-colored pelage varying from rusty red to brownish red, and dorsal pelage extending to the knees over the uropatagium.It has a small and short skull (GLS < 13.1 mm), with a developed lacrimal ridge (Fig. 1).The dental formula can be variable (I1/3 C1/1 P1-2/2 M3/3) and generally presents two upper premolars.No morphological differences associated to any geographical distribution were observed, and all specimens reviewed (n = 28) belong to the same subspecies, that we attributed to L. b. frantzii following Handley (1960) and Gardner & Handley (2008).
Lasiurus cinereus is known only from nine records in Colombian collections, all of these limited to Sierra Nevada de Santa Marta Province, the eastern slopes of Western Cordillera and western slopes of Eastern Cordillera of the North Andean Province (Table 1, Fig. 3b).It is the largest species of the genus in the country (FA 52.4-54.0mm; Table 2) with frosty pelage mixed with dark brown, grey and white tips.The skull is comparatively large for the genus with a relatively short rostrum (Fig. 1), a poorly developed lacrimal ridge, and the dental formula I1/3 C1/1 P2/2 M3/3.All the specimens reviewed are similar in size and external morphology and belong to a single subspecies that we attributed to L. c. pallescens following Gardner & Handley (2008) suggestions.
Table 1.Composition of species, based on presence or absence of records (Appendix), from seven of the nine geographic provinces of the country proposed by Hernández Camacho et al. (1992); no records from the insular territories of the country are known.AM, Amazonia; CA, Peri-Caribbean arid belt; CH-MG, Chocó-Magdalena; GU, Guyana; SN, Sierra Nevada de Santa Marta, NA, North Andean, OR, Orinoco.Elevation range (E) in meters.*Elevational upper limit obtained from Solari et al. (2013) which is 900 m approx.higher than any locality of the specimens.Lasiurus ega is a medium sized bat (FA ~ 45 mm) with records in Colombian collections from the Amazon, Caribbean and Pacific regions, and six geographical provinces (Table 1, Fig. 3b, Appendix).It exhibits a high variation in pelage color, from gold to dusk white coloration, even within the same biogeographic region of Colombia.Therefore, they could not be clearly assigned to any of the three subspecies with suggested presence in Colombia neither with morphological characters nor in distribution.This species has the most distinctive cranial morphology of the three species in Colombia.It has a small but elongated and flattened skull with a pronounced sagittal crest and a poorly developed lacrimal ridge (Fig. 1).The dental formula is I1/3 C1/1 P1/2 M3/3.

Most of the Lasiurus specimens from
Colombian collections were males (100% of L. cinereus, 75% of L. ega, and 75% of L. blossevillii; Table 2).For L. cinereus, the available reproductive information of six specimens show that males with inguinal testes were found from October to February.For L. ega five male specimens with reproductive activity are found from February to July.For L. blossevillii three male specimens were reproductively active from  We found a similar result for L. blossevillii in Colombia, for which the distribution was based on two marginal localities: one in the western slopes of the Eastern Cordillera (Cundinamarca, Sasaima), and a second in the upper Cauca River basin in the eastern   2008), to date there is no evidence of its presence in the country.
Confusion in the identification of Lasiurus in Colombia might be caused by inconsistencies in the characters used by different researchers.
In reference to dental characters, Shump & Shump (1982) mentioned that L. egregius has two upper premolars, but the species generally has only one (Bianconi & Pedro 2007, Gardner & Handley 2008).Furthermore, wing characters are also controversial.Handley (1996), andGardner &Handley (2008) mentioned that L. egregius has black wing membranes, with no conspicuously reddish coloration along the metacarpals and phalanges (paler than adjacent wing membranes in dried specimens).In contrast, Bianconi & Pedro (2007), and López-Baucells et al. (2014) reported that L. egregius has wings with a paler region along metacarpals and phalanges than the adjacent wing membranes.We are not able to say which combination of characters is the correct, considering that the species is not being registered to date in Colombia

Ecological notes
The species of the Lasiurus genus are not commonly caught in mist nests (Bianconi & Pedro 2007), and most records of L. blossevillii and L. cinereus are occasional and generally come from cities in which they are found dead.Although museum data are always biased due variable collection techniques (Cryan 2003), the remarkably uneven ratio of male vs. female specimens found in Colombian collections, might be caused by sex differences in migratory patterns and/or physiological constraints.For L. cinereus, the absence of female specimens from mountainous regions during summer has been suggested as possibly associated to physiological inability to raise young in these areas due to the climatic conditions and low density of resources (Cryan 2003).Alternatively, altitudinal sexual segregation likely represents partial altitudinal migrants because sexes must occur sympatrically to mate (McGuire & Boyle 2013).Both, the physiological inability and the migration events could also being affecting the populations in Colombia and might explain the absence of females from high Andean ecosystems of the country.
Using alternate methods is recommended for capturing information on these bat species (such as recording echolocation calls) and the collection of additional specimens to increase the number of the samples in the country for future comparisons.Genetic analysis would be useful to determine the validity of the subspecies classifications currently in use and some ecological aspects, such as migratory movements, and reproductive periods of the species found in Colombia.

Figure 2 .
Figure 2. Dorsal (above), ventral (middle) views of the cranium, and lateral (below) views of the skull, and dorsal view of the mandible of specimen CZUT-M 0213 reported as "Lasiurus egregius" by Bejarano-Bonilla et al. (2007) and re-identified as Lasiurus blossevillii.Note the presence of a developed lacrimal ridge (a) that is a character to differentiate Lasiurus blossevillii from Lasiurus egregius.Scale bar: 10 mm.

Table 2 .
External and skull measurements (mm) and body mass (g) of CZUT-M 0213 specimen reported byBejarano-Bonilla et al. (2007)and specimens for Lasiurus blossevillii (deposited in the ICN and IAvH collections); Lasiurus cinereus (ICN); and Lasiurus ega (ICN and IAvH).Data show average, number of specimens in parenthesis and range.See text for definitions of characters listed.

Table 3 .
External and cranial characters for Lasiurus from Colombia.See text for definitions of characters listed.
November to May.Furthermore, six female L. blossevillii nursing specimens were found from June to March.Finally, several records of L. blossevillii and L. cinereus are based on dead individuals found in large cities such asBogotá, Villavicencio, and Cali.

Table 1 ;
(Thomas 1901, Gardner & Handley 2008m the L. b. frantzii specimens found in other regions of Colombia.However, to date there are not available specimens from lower part of the Amazonia Province of Colombia to raise further conclusions.For L. ega, the distribution includes the lowlands of Colombia as reported by Gardner &Handley (2008)andGonzalez et al. (2008).Although only four localities from Colombia have been listed in the most recent update of the distribution of L. ega in America(Leal & Gomes-Silva 2015), we found 12 confirmed localities from six of the nine geographic provinces or the country (Appendix).Subspecies identification, however, is controversial.The external characters provided byThomas (1901)to differentiate among subspecies reportedly distributed in Colombia(Thomas 1901, Gardner & Handley 2008) are ambiguous, Figure 3. Localities of Lasiurus from Colombia.A. Lasiurus blossevillii, B. Lasiurus cinereus (white circles) and Lasiurus ega (black circles).Localities and sources are explained in