Bats ( Mammalia , Chiroptera ) in a remnant of Atlantic Forest , Rio de Janeiro , southeastern Brazil Morcegos ( Mammalia , Chiroptera ) em remanescente de Floresta Atlântica

Biodiversity inventories are essential to generate information leading to the proposal of conservation plans, especially for threatened areas. Despite being one of the best sampled regions for bats in Brazil, some areas of Rio de Janeiro still represent knowledge gaps. Between May 2011 and June 2012, we performed 36 nightly samplings to conduct an inventory of bat species in Reserva Ecológica de Guapiaçu, in Cachoeiras de Macacu, in the state of Rio de Janeiro, southeastern Brazil. We used 10 mist-nets per night opened from sunset to sunrise. A total of 1,290 individuals belonging to 31 bat species were caught. They were distributed in three families, Phyllostomidae (24 species), Vespertilionidae (four species) and Molossidae (three species). We recorded two other species of two families, Noctilionidae and Thyropteridae, by direct observations. The species richness of bats in Reserva Ecológica de Guapiaçu is one of the largest ever recorded in the Atlantic Forest.


Introduction
Since the sixteenth century many economic cycles (e.g., pau-brasil, gold, sugarcane and coffee), followed by processes of industrialization and unplanned urban expansion, led to a drastic reduction of the Atlantic Forest, leaving only about 8% of the original vegetation (Ribeiro et al., 2009).The remaining fragments of the Atlantic Forest are usually small and isolated from large forests.Such fragments consist of secondary forests ranging from early stage to late secondary succession of vegetation (Viana et al., 1997;Metzger et al., 2008).This situation put under threat a large proportion of its species, leading this biome to be one of the most important biodiversity hotspots in the world (Myers et al., 2000;Tabarelli et al., 2005) though still suffering constant anthropogenic pressures (Souza et al., 2013).In heterogeneous and highly diverse forests, such as the Brazilian Atlantic Forest, which still holds a large number of unknown species (Lewinsohn and Prado, 2005), biodiversity inventories are essential to generate information leading to the proposal of conservation plans (Esbérard, 2003).Despite the large amount of biological data collected over the past decades in this biome, some areas still have large gaps in knowledge, which hinders the development of measures for their conservation (Metzger et al., 2008;Bernard et al., 2011).Therefore, the first step to promote conservation strategies and better understand the ecological dynamics of native biota in different habitats is the inventory of species.According to Paresque et al. (2004), the Atlantic Forest comprises an important ecosystem for Neotropical mammals.In Brazil, this group achieves a high richness (almost 700 species) and a high rate of endemism (about 30% of species) (Paglia et al., 2012).Chiroptera is the second richest order in species within Mammalia (after Rodentia) and has more than 170 species recorded in Brazil, with 113 of them found in the area of Atlantic Forest (Paglia et al., 2012).Rio de Janeiro is the most well sampled state for bats in Brazil (Bergallo et al., 2003;Bernard et al., 2011).Currently 78 bat species are known to this state, representing 69% of bat richness in the Atlantic Forest (Paglia et al., 2012).However, the metropolitan east of the State of Rio de Janeiro has few studies on bats, being considered a region of knowledge gap.Here we present the results of an inventory of bat species of Reserva Ecológica de Guapiaçu, southeastern Brazil.

Study area
The Reserva Ecológica de Guapiaçu -REGUA (22°25'53"S; 42°45'20"W) is located in the city of Cachoeiras de Macacu, state of Rio de Janeiro, southeastern Brazil (Figure 1).REGUA is a private reserve of natural heritage and comprises 5,500 ha formed by a mosaic of forest remnants at different levels of conservation, from secondary forests in early successional to mature forest in the highest parts (Rocha et al., 2007), and disturbed areas (including plantations and pastures).The vegetation represents the typical forest formations of low and medium altitudes in the coastal region of Brazil (Morellato and Haddad, 2000;Oliveira-Filho and Fontes, 2000;Veloso et al., 1991).The average annual temperature in this region is approximately 23°C with an average of annual rainfall of about 2,600 mm (Kurtz and Araújo, 2000;Bernardo et al., 2011).The region has a warm and rainy period between November and April, and a colder and drier period between May and October (Almeida-Gomes, 2011).REGUA is within an extensive set of strategic forest remnants for the conservation of biodiversity and natural resources, to protect part of the watersheds that flow into Guanabara Bay (Conservação Internacional et al., 2000;Rocha et al., 2003).

Sampling
From May 2011 to June 2012, we performed 36 nightly captures in REGUA with 10 mist nets (9 m x 3 m) in open trails, vegetation gaps, dense vegetation, and on streams (Kunz and Kurta, 1988).The sampling of bats was carried out in three areas with different levels of conservation and different vegetation types, including disturbed areas, secondary vegetation in early stages of ecological succession, late successional vegetation and mature secondary forest area with little anthropic disturbance.The mist nets were open from sunset to sunrise, totaling 116,640 m² of sampling effort (Straube and Bianconi, 2002), equal for all three sampling areas.The captured bats were identified in the field with the aid of the descriptions provided by Simmons and Voss (1998), Barquez et al. (1999), Dias et al. (2002), Reis et al. (2007), Dias and Peracchi (2008) and Peracchi et al. (2010).The first two specimens of each species caught, as well as the individuals which generated doubts about the identification, were collected and incorporated as a material-reference in the collection of mammals from the National Museum of Rio de Janeiro (Appendix 1), as license by SISBIO/ICMBio (3893-1/28717).All ethic guidelines in manipulating animals were followed using recommendations by Sikes and Gannon (2011).At the end of the handling, we marked the captured individuals with numbered metal rings on the forearm to record recaptures.Later, we released these individuals on the same capture site.The classifications of species into trophic guilds followed Kalko et al. (1996).

Results
We captured 1,290 bats of three families: Phyllostomidae (24 species), Vespertilionidae (four species) and Molossidae (three species).In addition, two other species of two fami-lies, Noctilionidae and Thyropteridae, were recorded through direct observation (without capture), totaling 33 species of bats recorded in the Reserva Ecológica de Guapiaçu (Table 1).We recaptured 146 individuals of 11 species: Carollia perspicillata (Linnaeus, 1758) ( 94 We recorded nine trophic guilds for the species in the study area.Fruit bats were dominant both in species richness and in abundance, representing about 81% of the captures.

Discussion
Species richness of bats found in the Reserva Ecológica de Guapiaçu is among the largest recorded for the State of Rio de Janeiro (e.g.Bergallo et al., 2003;Esbérard, 2003;Esbérard et al., 2006;Menezes Jr., 2008;Bolzan et al. 2010;Esbérard et al., 2010;Lourenço et al., 2010;Luz et al., 2011).A preliminary survey of Costa et al. (2010) recorded 14 species and estimated (using the Chao 1 richness estimator) a maximum richness of 22 species of bats in the study area.Although we recorded a higher number of species, our capture effort was considerably higher and we sampled different habitats within the reserve.The high abundance of phytophagous bats recorded in the present study is related to difficulties in capturing insectivorous bats with mist nets, as these species have a more sensitive echolocation and can easily detect networks (Bergallo et al., 2003).The use of different methods, such as search for roosts, could record more species, especially of the families Molossidae and Emballonuridae, with low or no representativeness in the present study.We observed that the success of capturing different species is linked to the location of the nets, taking into consideration aspects of the landscape and information gathered from the literature.As an example, we captured individuals of Lonchophylla peracchi near banana trees (Musa paradisiaca, Musaceae) (see Novaes et al., 2010).Besides, bats of this species were observed visiting flowers of banana trees in Reserva Particular do Patrimônio Natural El Nagual, Magé, Rio de Janeiro (A.C.Siqueira and E. Ribeiro, unpublished data).We suggest focusing the effort on banana plantations to sample this species, especially near flowering individuals.Cattle ranching and poultry breeding near the capture sites facilitated the capture of the three vampire bat species.We captured Vampyrodes caraccioli both in mature secondary forest with low anthropic disturbance (400 m elevation) and in a forest edge area (150 m elevation).Velazco et al. (2010) noted that this species is rare at low altitude and with few records to the southeast of Brazil.We captured two individuals near a fruiting Ficus sp.Despite being one of the most well sampled states for bats, some regions of Rio de Janeiro still remain as gaps in knowledge.The high species   Kalko et al. (1996).
Bats (Mammalia, Chiroptera) in a remnant of Atlantic Forest, Rio de Janeiro, southeastern Brazil richness presented here is more indicative of the urgency to conduct inventories in yet unsampled areas.These efforts will enable us to enhance conservation strategies as well as to create actions that mitigate the impact of human activity on native biota.

Figure 1 .
Figure 1.Location of Reserva Ecológica de Guapiaçu, Cachoeiras de Macacu, in the context of remnants of the Atlantic Forest in the state of Rio de Janeiro (gray), in the southeastern of Brazil.

Table 1 .
Species of bats recorded in an Atlantic Forest remnant, Reserva Ecológica de Guapiaçu, southeastern Brazil, with numbers of individuals sampled (N), percentage yield (%), and classification into trophic guilds based on