First report of the Broad-toothed Tailless Bat, Anoura latidens Handley, 1984 (Chiroptera, Phyllostomidae), in Bolivia

Anoura latidens Handley, 1984 is a nectarivorous bat with a wide elevational and latitudinal distribution, from Venezuela and Guyana to southeastern Peru. We reviewed mammal collections of the genus Anoura Gray, 1838 and identified two individuals previously attributed to A. caudifer (É. Geoffroy Saint-Hilaire, 1818) as A. latidens based on their premolar morphology and morphological measurements. In this note we report the first record of A. latidens in the Yungas forests of Bolivia, which extends its geographic range by 1,006 km southeast of its previous southernmost record in Peru.


Introduction
The Broad-toothed Tailless Bat, Anoura latidens Handley, 1984, is a large-bodied species of Anoura Gray, 1838 characterized by broad molars and premolars in comparison to the other species of the genus (Handley 1984). Anoura latidens was described from Pico Ávila, Caracas, Venezuela at 2,150 m a.s.l. and is reported from at least 14 localities in the country (Handley 1984). Most of these localities correspond to montane ecosystems, being more abundant in localities between 1,000 and 1,500 m a.s.l. in moist evergreen forests (Handley 1984;Linares 1998). Anoura latidens occupies a variety of ecosystems throughout South America and has an altitudinal range from 50 to 2,600 m a.s.l.
Outside of Venezuela; A. latidens is reported in Colombia, Guyana and Peru (Handley 1984;Solari et al. 1999Solari et al. , 2013Alberico et al. 2000;Lim and Engstrom 2001;Mora-Beltrán and López-Arévalo 2018), although the records are scarce, widespread and with few specimens. In Colombia, this species is distributed from at least seven localities in the three cordilleras, most in the central and western cordilleras and, even though present in protected areas (Mora-Beltrán and López-Arévalo 2018), some localities are highly transformed landscapes (Calderón-Acevedo 2019). In Guyana, it is represented by a single specimen from the protected Iwokrama Forest, Cuyuni-Mazaruni, Kuwaima Falls, in the Pakaraima Highlands biogeographical region; this is the easternmost point of distribution of this species (Lim and Engstrom 2001). The current southernmost records correspond to two localities in the Yungas forests of southeastern Peru: one specimen from the department of Junín, Tarma, 2 km northwest of San Ramón (884 m a.s.l.) (revised by Handley 1984) and four specimens from the department of Pasco, Oxapampa, San Alberto (2,600 m a.s.l.) (revised by Solari et al. 1999). Currently, the southern distribution of A. latidens is limited to the eastern Andes, however, in the latest assessment from the International Union for Conservation of Nature (IUCN) Red List (Mantilla-Meluk and Molinari 2015) and the recent update of the distribution of Neotropical Noctilionoidea (Rojas et al. 2018), it was assumed that the western Peruvian Andes are part of the distribution of A. latidens, although there are no records to date. Only three species of Anoura, A. caudifer (É. Geoffroy Saint-Hilaire, 1818), A. cultrata Handley, 1960, andA. geoffroyi Gray, 1838 are reported from Bolivia. Here, we present the first records of A. latidens for Bolivia, extending its distribution southeast of Peru.

Methods
In a revision of the genus Anoura we visited the mammal collections of the American Museum of Natural History (AMNH) and the National Museum of Natural History, Smithsonian Institution (USNM). We measured the following characters to the nearest 0.01 mm: forearm, length of the tibia, greatest length of skull, zygomatic width, postorbital breadth, brain case breadth, height of brain case, maxillary tooth-row length, post palatal length, breath across third upper molars, breath across upper canines, mandibular length, and mandibular toothrow length. A total of 56 specimens were identified and measured. Taxonomic identification followed Handley (1984) and Griffiths and Gardner (2008).

Results
After a taxonomic revision of Anoura specimens we found two records of Anoura latidens for Bolivia, which were previously identified as A. caudifer (Anderson, 1997). These constitute the first records of this species in the country (Fig. 1).    Pacheco, Sánchez-Vendizú &Solari, 2018, andA. luismanueli Molinari, 1994  Although A. latidens is similar to the other two species of large-bodied Anoura (A. geoffroyi and A. cultrata) in terms of forearm and skull size, it has a unique dentition not present in any other species of Anoura. Specifically, it has a second upper premolar (P3) that lacks a developed anterobasal cusp (a trait found in A. geoffroyi) and a last upper premolar (P4) with a triangular shape caused by the medial-internal cusp being enclosed by the base of the P4, also lacking the distinct bladelike first lower premolar of A. cultrata.

Anoura latidens
Both specimens from Bolivia can be diagnosed as A. latidens and meet all the dental diagnostic criteria defined by Handley (1984), including a reduced anterobasal cusp on the second upper premolar (P3) and a triangular tooth base enclosing the anteriomedial cusp of the last upper premolar (Fig. 2). These specimens have measurements falling within the known range of variation in the other examined specimens of A. latidens (Table 1). These specimens also have short rostrums and incomplete zygomatic arches. We found that the fur of our Bolivian specimens of A. latidens is greyer in contrast to the pale-brown or sepia of Venezuelan specimens described by Handley (1984) (Fig. 3). This could be due to intraspecific variation, since the external characters of A. latidens have not been evaluated thoroughly aside from the initial description and the scattered records from Colombia, Guyana, and Peru.

Discussion
This represents the first report of Anoura latidens in Bolivia. Previous work shows that this species is also distributed from the east of South America in Guyana, through the Venezuelan Guayana, and Andean regions, across the eastern and western Andes from Colombia, and in the eastern Peruvian Andes (Handley 1984;Solari et al. 1999Solari et al. , 2013Alberico et al. 2000;Lim and Engstrom 2001; Mora-Beltrán and López-Arévalo 2018; Calderón-Acevedo 2019). It has not been reported in Ecuador. In Guyana, A. latidens is reported from the central Iwokrama forest (Lim and Engstrom 2001), a lowland Neotropical rain forest and one of the protected areas in South America with the highest recorded bat diversity. Records from Venezuela show the plasticity that this species exhibits in habitat selection; it is reported from 14 localities, occupying a wide variety of ecosystems, from lowland forest to the high Andean slopes of the Cordillera de Mérida, with most records in middle elevations from 1,000 to 1,500 m a.s.l. (Handley 1976(Handley , 1984Ochoa et al. 1993;Linares 1998;Lew et al. 2009). Records from Colombia suggest a primarily Andean distribution in mid-elevation premontane forests (Alberico et al. 2000;Solari et al. 2013; Mora-Beltrán and López-Arévalo 2018; Calderón-Acevedo 2019). In Peru, A. latidens is reported only from two localities in the eastern Andes, at an elevation of 884 m a.s.l. (Handley 1984) and 2,600 m a.s.l (Solari et al. 1999), which is the highest recorded elevation for the species (Handley 1984;Solari et al. 1999).
The IUCN assessment of A. latidens is currently Least Concern, given that the species is reported in national parks through its range, has presumably stable populations, and, although areas of its distribution are under threat, there are presumably no major threats to its habitat (Mantilla-Meluk and Molinari 2015).
The paucity of individuals in collections indicates that A. latidens is a rare species (Arita 1993) with a scattered distribution and small populations. It was not previously reported for Bolivia (Anderson et al. 1982;Anderson 1985Anderson , 1993Anderson , 1997Salazar-Bravo et al. 2003;Aguirre et al. 2010Aguirre et al. , 2019, and the new Bolivian records extend the geographic range of this species by 1,006 km southeast of its previously known southernmost record in Tarma, Junín, Peru (Handley 1984;Solari et al. 1999).
The new records come from Yungas forests, which is one of the most diverse ecosystems in Bolivia. The Yungas include over 48% of the bat diversity in the country where 59 species have been recorded (Vargas and Patterson 2007). These forests are identified as important areas for bat conservation (Vargas et al. 2010). With this addition, the genus Anoura in Bolivia is represented by four species, A. caudifer, A. cultrata, A. geoffroyi, and A. latidens (Salazar-Bravo et al. 2003;Calderón-Acevedo and Muchhala 2018;Aguirre et al. 2019). The new records, along with the previous records from Peru and Colombia, suggest that A. latidens is more widespread in South America than previously thought, although apparently always in low abundances in its southern distribution.