Rediscovery of Vampyressa thyone (Chiroptera, Phyllostomidae) in Honduras: updated distribution and notes on its conservation

In Central America, Vampyressa is represented by two species, Vampyressa elisabethae and V. thyone. The latter is the only representative of the genus in Honduras and the most recent record was in 2007. Six surveys were carried out in the Departments of Cortés, Atlántida and Gracias a Dios. Only seven individuals of V. thyone were recorded between March 2016 and September 2017. The low abundance of V. thyone supports the fact that it is an uncommon species in the country; however, these records update the distribution in northern Honduras. We recommend systematic bat assessments on the three protected areas in which we recorded V. thyone for a better comprehension of the local populations on this species in the country.


Bat sampling and ethical guidelines
To capture bats, we used two mist-nets (9 × 2.5 m and 14 × 2.5 m; with a mesh of 35 mm) that remained opened from 16:30 h until 02:30 h and checked every 20 minutes. We selected their position and location based on Kunz and Kurta (1988), using the vegetation, topography and bodies of water as reference. In the field, we determined the sex of the bats following Kunz et al. (1996) and the biological age following Brunet-Rossinni and Wilkinson (2009). We took measurements using a caliper with a spire Mitutoyo (505-675) to the closest 0.01 mm, in accordance with Srinivasulu et al. (2010) as follows: forearm length (FA), tibia length (Tib), ear length (E), ear width (EW), thumb length (Th), noseleaf length (LN), tragus length (Tr), calcaneus length (Ca), body height (BH), hind foot length (HF), wingspan (WS), metacarpal of third finger (3mt), first phalange of third finger (1ph), second phalange of third finger (2ph) and third phalange of third finger (3ph). Body mass (BM) was measured with a scale of 10 (Table 2). We followed Timm et al. (1999), Medellín et al. (2008) and Mora (2016) for the taxonomic identification of the bats and Porter and Baker (2004) and Tavares et al. (2014) for the systematics of Vampyressa. Finally, we calculated the sampling effort following Straube and Bianconi (2002).

Results
Two families (Phyllostomidae and Mormoopidae), 15 species and 96 individuals were recorded in a sampling effort of 16,854 m 2. h. Phyllostomidae was represented by 95.83% of the individuals, 14 species and three subfamilies: three species of Glossophaginae (4.17% of individuals), three species of Carollinae (23.96%) and eight species of Stenodermatinae (67.70%). Pteronotus mesoamericanus (4.17%) was the only species that we captured of Mormoopidae in all the surveys (Table 3). Seven individuals of V. thyone were captured, four males (three adults and one juvenile) and three females (two adults and one juvenile). None of the individuals was reproductively active. V. thyone individuals were captured between 18:00-21:05 h and only one individual was recorded at 00:00 h. The specimens of V. thyone caught at PANACAM represent the first records of this species in this protected area. All individuals were released except for one adult male captured in Pico Dama (Gracias a Dios Department). This specimen was euthanised according to the guidelines for the use of mammals in wildlife research (Sikes et al. 2016). It was deposited in the Zoological Collection of the Museum Biodiversidad y Ciencia of the Universidad Nacional Autónoma de Honduras (UNAH) in the Sula Valley with catalogue number UVS-V-02071 (Fig. 2).  Valdez and LaVal (1971)  V. thyone is similar to Mesophylla macconnelli and Vampyriscus nymphaea; however, our specimens identified as V. thyone had no dorsal line, which is present in V. nymphaea. All V. thyone specimens presented a hairy interfemoral membrane which is hairless in V. nymphaea and M. macconnelli (Medina-Fitoria 2014;  Tavares et al. 2014). Finally, the forearm length of the seven specimens was smaller in comparison to V. nymphaea, which is larger (FA = 35-39 mm) (Medina-Fitoria 2014; Tavares et al. 2014). Despite the overlap between the forearm of V. thyone and M. macconnelli (FA = 29-33 mm), the latter has not been recorded in Honduras (Turcios-Casco et al. 2020a).
Considering the historical occurrence of V. thyone in Honduras, 14 of these records, dating from 1964 to 1991, are available in the GBIF (2020) database. The specimens of these records are deposited in the mammal collections of the Museum of Texas Tech University (TTU), the Museum of South-western Biology (MSB) and the Texas A&M University Biodiversity Research and Teaching Collections (TCWC). These are distributed as follows: Olancho Department: three specimens collected in Dulce Nombre de Culmí (Garner 2016a, b, c) and three specimens from Catacamas (Prestridge 2019c, d, e); Atlántida Department: one specimen from Tela (Prestridge 2019a) and four specimens from Lancetilla (Valdez and LaVal 1971;Lee and Bradley 1992;Garner 2016d;Prestridge 2019f); Copán Department: one specimen from Copán Ruinas (Prestridge 2019b); Gracias a Dios Department: two specimens from Río Plátano (Cook 2020a, b). Furthermore, the most recent records for the country were reported by Estrada-Villegas et al. (2007) in Cusuco National Park, Cortés Department (Table 1).

Discussion
For Honduras, many records and distributions of bat species are separated by decades, which dulls the conservation and education actions, and for V. thyone, this is no exception. Our study, despite the few records of V. thyone, provides important updates in the distribution of the species in Honduras. From the seven specimens captured, only one female and one male were juveniles and none of the adults was in any reproductive condition. In general, Lewis and Wilson (1987) mentioned pregnant females in January, February, March, April, June, July, August and November; and lactating females in March, April, May, June and July, suggesting a binomial polyestrous pattern. However, for Honduras, there is only a record of Valdez and LaVal (1971) of a female captured in August in 1969 with an embryo of 18 mm.
According to our records, V. thyone was frequently active during the first hours after sunset and these results agree with the activity patterns reported by other authors. For example, Davis and Dixon (1976) captured 78.84% of individuals of V. thyone between 18:30 h-21:00 h in Peru and Bonaccorso (1979) stated that the activity of this species is higher during the first two hours after sunset in Panama. Furthermore, Bonaccorso (1979) obtained more captures of V. thyone (referred as V. pusilla) at subcanopy levels compared to ground levels. In this study, all mist-nets were set at ground levels and near or over streams, which may partially explain why V. thyone remained as one of the species with less capture frequency.
According to the IUCN (International Union for the Conservation of Nature), V. thyone is categorised as Least Concern (LC) (Tavares et al. 2015). However, populations of this species may be locally threatened throughout its distribution in Honduras. V. thyone highly depends on mature and well-preserved forests, forages in evergreen forests and has a relatively low abundance in Mexico and Central America being considered an uncommon species (Handley 1966;Jones et al. 1971;Lewis and Wilson 1987;Medina-Fitoria 2014;Zamora Mejías and Rodríguez Herrera 2017;Mora et al. 2018;Hernández-Canchola et al. 2019). In addition to Valdez and LaVal (1971), the sites in Lancetilla may no longer be undisturbed, because we found plantations of rambutans (Nephelium lappaceum) near the studied areas. On the other hand, the areas where V. thyone was captured in Gracias a Dios Department included preserved forests. While Tavares et al. (2015) and Davis and Dixon (1976) mentioned that V. thyone may be locally common within its distribution range in South America, the capture frequency in our study was of 0.0004 individuals per m 2. h. The low abundance obtained supports the fact that V. thyone is an uncommon species in Honduras.
The records provided in this study were reported in protected areas within the Caribbean slope of Honduras. The rarity of V. thyone, combined with the constant and degenerative changes of the Honduran forests, could turn V. thyone into a vulnerable species. According to ICF (2017), the wood extracted from forests in Honduras was estimated to be 122,061,763.3 board feet per year. In addition, forest coverage is significantly affected yearly by bushfires; since 2007 to 2014, a total of 81,506.3 ha of forest have been lost. One of the most affected Departments was Gracias a Dios (CONADEH 2015), which harbours the most important extension of tropical moist forest (including a part of the RPBR) in the country. This negative pressure turns into a gradual and constant perturbation to the different types of habitats throughout the RPBR.
It is important to mention that the sampling sites in Gracias a Dios took place near the limits of RPBR, the most important region for wildlife conservation in Honduras. Nonetheless, the RPBR is facing illegal cattle ranching, which is the main reason for forest loss in the reserve (Turcios-Casco et al. 2020b); therefore we recommend including V. thyone in the present RPBR management plan because it currently is mainly focusing on felines, primates and birds as fauna with priority for conservation. However, the RPBR is the only protected area in Honduras that includes a bat species (Ectophylla alba) in its conservation plan. We also recommend the inclusion of a systematic bat assessment in PANACAM and LBG, because it may provide a better comprehension of the local populations of V. thyone in Honduras. Finally, it is important to determine which species are used as tents by V. thyone in the study areas, not only to understand more about its ecology, but to know which plant species are also needed for conservation.