Notes on the geographic range and distribution of two free-tailed bat species (Chiroptera, Molossidae) in Costa Rica

Nyctinomops laticaudatus (É. Geoffroy St.-Hilaire, 1805) and Eumops nanus (Miller, 1900) are 2 species with distributions that are expected for Costa Rica. However, voucher specimens that confirm the presence of these species in the country are absent or missing in museum collections. Here we document voucher specimens and present data that confirm the presence of N. laticaudatus and E. nanus in Costa Rica.


Introduction
The Molossidae are a family of medium-sized to large bats with about 16 genera and more than 100 species distributed worldwide (Simmons 2005, Eger 2008). The members of the family are characterized by the presence of long tails that project beyond the tail membrane or uropatagium (Emmons andFeer 1997, Reid 2009). Their common name, free-tailed bats, originates from this characteristic.
Despite growing information on the geographic distribution of free-tailed bat species in the Neotropics (e.g. Gregorin and Taddei 2000, Pineda et al. 2008, Baker et al. 2009, Bianconi et al. 2009, Feijó et al. 2010, Gregorin et al. 2011, Rodríguez-Herrera et al. 2014, Medina-Fitoria et al. 2015, González-Terrazas et al. 2016, there are still many distributional gaps, creating the illusion that some of the species are rare, patchily distributed, or absent in some areas (Reid 2009). This rarity seems to be a direct consequence of the difficulty in capturing these bats with traditional methods, such as placing mist nets at ground level (Reid 2009), and more complex inventory techniques, such as acoustic recordings that are not always available to all tropical bat researchers. Moreover, many free-tailed bats possess complex and varied search call designs (Jung et al. 2014) that complicate their identification.
Despite that approximately 5 genera and 14 species of free-tailed bats have been reported for the country (Rodríguez-Herrera et al. 2014), Costa Rica still has several information gaps regarding the presence of some of them, mainly by the absence of direct evidence (i.e. voucher specimens). This is the case of some free-tailed bats of the genera Nyctinomops Miller, 1902 andEumops Miller, 1906.
Nyctinomops includes 4 native species of America (Simmons 2005), the Peale's Free-tailed Bat, N. aurispinosus (Peale, 1848); the Pocketed Free-tailed Bat, N. femorosaccus (Merriam, 1889); the Broad-eared Bat, N. laticaudatus (É. Geoffroy St.-Hilaire, 1805), and the Big Free-tailed Bat, N. macrotis (Gray, 1840). With exception of N. femorosaccus, which has a restricted distribution in areas of Mexico and the United States (Kumirai andJones 1990, Simmons 2005), the rest of species have been detected in northern and southern parts of the New World, suggesting that there are likely to occur in Central American countries such as Costa Rica. In particular, 1 of these 3 species, N. laticaudatus, has never been captured in Costa Rica despite indirect evidence that links the acoustic information collected by LaVal and , with its presence in Costa Rica in the Central Pacific Coast and Central Valley.
The presence of E. nanus in the Costa Rica is a controversial issue (Pineda et al. 2008). Eumops nanus was allegedly reported in the Pacific and Atlantic lowlands of the country by Rodríguez and Chinchilla (1996) on the basis of 3 voucher specimens deposited in the Museo de Zoología, Universidad de Costa Rica (UCR175, UCR515, and UCR785). Nevertheless, despite the intense search efforts made at the museum, the specimens were not found, which leads us to think that they have been lost (Pineda et al. 2008, this study).
Both, N. laticaudatus and E. nanus, has been repeatedly included and excluded from the literature of the country using several arguments (Janzen and Wilson 1983, Rodríguez and Chinchilla 1996, Timm and LaVal 1998, Rodríguez-Herrera and Wilson 1999, LaVal and Rodríguez-Herrera 2002; thus, in order to resolve this situation, we present voucher specimens and confirm the presence of N. laticaudatus and E. nanus in Costa Rica.

Methods
The specimens reported here came from 2 different localities of Costa Rica. The first was at Santa Ana canton, in the southwestern of the San José province, a specimen of Nyctinomops laticaudatus was found dead, at a medium level of decomposition, on the ground by two of us (AGQ and LLH). The site of collection is characterized by the presence of several forest patches surrounded by open areas dedicated to cattle, crops and human settlements, and shows an annual biotemperature and precipitation regimens of between 12-18 °C and 4,000-8,000 mm respectively (Holdridge 1967). The second locality was at Río Enmedio, Santa Cruz canton, in the northwestern Pacific lowlands of the Guanacaste province, where 4 individuals of Eumops nanus were captured by BRH and DVC at 2 independent times with mist nets set above the river (0.5 m depth). The capture site of the animals belongs to a governmental protected forested area and shows an annual biotemperature and precipitation regimens of between 24-30 °C and 2,000-4,000 mm respectively (Holdridge 1967).
Voucher specimens were collected with permissions from MINAET-SINAC (Resolución No.

SINAC-SE-CUSBSE-PI-R-131-2016 and Resolución
No. ACT-OR-DR-147-14). In the case of E. nanus, bats were sacrificed following the standards of the American Society of Mammalogy (Sikes et al. 2016). All specimens collected were fixed in 10% formalin and then preserved in 70% ethanol. The skull from 1 specimen per species was extracted and cleaned after fixation. Using a digital caliper, the following morphometric and cranial measurements were recorded following Freeman (1981)

Identification. Nyctinomops laticaudatus differs from
all other species of the genus potentially distributed in Costa Rica (i.e. N. aurispinosus and N. macrotis) in being overall smaller in several external and cranial measurements (Table 1). In the field, the length of the forearm is one of the most useful characters to identify species of Nyctinomops (Jones and Arroyo-Cabrales 1990, Milner et al. 1990, Timm and LaVal 1998, Avila-Flores et al. 2002, Díaz et al. 2011, as N. aurispinosus and N.  In comparison with other similar species in terms of size and external morphology (for example T. brasiliensis) some distinguishing characters such as the ears joined at base, extended beyond the tip of the snout when laid forward, and the upper incisors parallel to each other, confirms the identity of our specimens as N. laticaudatus and not Tadarida brasiliensis (Fig. 1B, 1C). Figure 2 New record. Costa Rica: Guanacaste province: Santa Cruz: Río Enmedio at Parque Nacional Diriá (10.1738° N, 085.5961° W; 1778 m a.s.l., Fig. 2A

Identification.
When comparing E. nanus with other bonneted bat species from Costa Rica (except E. hansae which overlaps in some characteristics), this species can be recognized by its smaller size in several external and cranial measurements (Table 1). Live animals can be distinguish from other species of Eumops by smaller measurements of body length, forearm length and body mass (Eger 1977, Timm and LaVal 1998, LaVal and Rodríguez-Herrera 2002, Reid 2009).
Despite that when specimens of E. nanus and E. hansae from Costa Rica are directly compared the first is usually smaller, a combination of several external and cranial characters are needed to confidently separate and identify the live as well as the museum specimens. For example, the fur is long (5 mm), pale, and whitish at the base in E. nanus, while E. hansae have a relatively short fur (2-3 mm) and hairs are dark at the base (Eger 1977, Reid 2009 (Fig. 2B). The presence of few short hairs along the edge of the calcar in E. nanus and their absence in E. hansae also separate these species (Reid 2009). Cranial and tooth morphology are also useful to compare these species. In E. nanus the skull is nearly flat when viewed laterally (Fig. 2C), while the skull of E. hansae is more bulbous (Pineda et al. 2008). Moreover, the tips of the upper incisors of E. nanus are distally convergent and somewhat procumbent (Fig. 2C), contrary to the widely separated tips and slightly recurved inward upper incisors of E. hansae (Pineda et al. 2008).

Discussion
Our findings confirm the assumptions of several authors regarding the presence of these 2 free-tailed bat species in Costa Rica (Koopman 1993, Rodríguez and Chinchilla 1996, Timm and LaVal 1998, LaVal and Rodríguez-Herrera 2002, Pineda et al. 2008. Our observations corroborate that, in Costa Rica, N. laticaudatus can be found at middle elevations in the Central valley and in disturbed habitats that are not necessarily protected. Based on this observation, we concur with LaVal and  who predicted that the N. laticaudatus is expected to inhabit in several types of habitats with a wide range of altitudinal variation (between 0-1,800 m a.s.l.). Moreover, this record helps to close the distribution gap of N. laticaudatus in Central America. Our new record is about 489 km from the closest known locality in Nicaragua and by 231 km from the closest known locality in Panama (Fig. 1A).
The absence of Rodríguez and Chinchilla's (1996) voucher specimens of E. nanus and the lack of other evidence such as photographs of diagnostic characteristics of the species preclude us from accepting their report of this species in Costa Rica. There is the possibility of a misidentification by Rodríguez and Chinchilla (1996) because the E. nanus bat is easily confused with E. hansae as well as with other free-tailed bats such as N. laticaudatus or the Brazilian Free-tailed Bat, Tadarida brasiliensis (I. Geoffroy, 1824) (Pineda et al. 2008, Reid 2009). Based on this, our findings constitute the first confirmed record of E. nanus for the country, filling a distribution gap of E. nanus in Central America. Our record is approximately 379 km from the closest known locality in Nicaragua, and by 380 km from the closest known locality in Panama ( Fig. 2A).
Finally, based on the mammal list published by Rodríguez-Herrera et al. (2014) and other recent publications related to this topic (Ramírez-Fernández et al. 2015, Villalobos-Chaves et al. 2016, Woodman and Timm 2016, our results increase the total number of living mammals of Costa Rica to 253 species and to 115 the total number of bats species. These discoveries also show that despite that the order Chiroptera is considered a well-studied mammal group in the country, the most basic aspects of species biology such as geographic distribution and natural history are still unknown for many species of small mammals, mainly bats and rodents. This highlights the need for more field work and research to improve our knowledge of the ecology of these poorly known mammal species.