Rapid surveys as a key tool for the inventory of the bat fauna of Brazil : New records for the coastal restinga

This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International (CC BY 4.0), which permits reproduction, adaptation, and distribution provided the original author and source are credited. 1 Universidade Federal da Paraíba. Programa de Pós-Graduação em Ciências Biológicas (Zoologia). Cidade Universitária, 58051-900, João Pessoa PB, Brazil. 2 Universidade Federal de Sergipe. Núcleo de Educação em Ciências Agrárias e da Terra. Rodovia Engenheiro Jorge Neto, km 3, 49680-000, Nossa Senhora da Glória, SE, Brazil. 3 Universidade Federal do Sergipe. Programa de Pós-Graduação em Ecologia e Conservação. Av. Marechal Rondon, s/n, 49100-000, São Cristóvão, SE, Brazil. Rapid surveys as a key tool for the inventory of the bat fauna of Brazil: New records for the coastal restinga


Introduction
The Brazilian Atlantic Forest, known for its diversity and species endemism (Myers et al., 2000), originally occupied the entire eastern coast of Brazil.In the present day, however, this biome has less than 15% of its original area (Ribeiro et al., 2009).The Atlantic Forest is a coastal formation, influenced profoundly by marine and fluvial forces, resulting in the establishment of distinct plant communities, such as mangroves and coastal restinga.The restinga is associated with sandy coastal plains and dune fields (CONAMA, 1996).The composition of its plant communities vary according to the limitations imposed by the type of soil, ranging from strictly herbaceous or shrubby vegetation to forest (CONAMA, 1996).
The restinga vegetation can be considered a subset of the adjacent ecosystems, with few endemic species (Rizzini, 1997), resulting in considerable variation in the floristic structure and composition along the latitudinal and morphoclimatic gradients in which this ecosystem occurs (Gonzatti, 2015).This variation presumably has a direct influence on the set of conditions and resources available for the local animal communities, including mammals.
Similarly, only a subset of the bat species typically found in the Atlantic Forest are also encountered in neighboring areas of restinga (Nogueira et al., 2010).In this case, while 115 bat species have been recorded in the Atlantic Forest (Paglia et al., 2012;Nogueira et al., 2014), only 38 species (26 genera from five families) are confirmed to date for the restinga (see Fogaça and Reis, 2008;Nogueira et al., 2010;Luz et al., 2011).However, all bat inventories in restinga habitats were carried on the southern Atlantic Forest.
The lack of knowledge about bat diversity extends to all Brazilian biomes throughout the country and makes it difficult to decide on priority areas for bat conservation efforts (Bernard et al., 2010).In this sense, rapid inventories of bat diversity may contribute to the fulfillment of the gaps and provide high quality information in a short time (Martins et al., 2006;Lourenço et al., 2010).
Given this background, the present study is the first to assess the bat fauna of a coastal restinga habitat in the northern Atlantic Forest, in northeastern Brazil.We present new records of bat species for this ecosystem, and discuss the observed variation in the richness and composition of bat species along the Brazilian coast.

Study site
We conducted the present study in the Caju Private Natural Heritage Reserve (RPPN Caju; 11°6'10.12"S, 37°11'4.59"W; 763.37 ha), a protected area in the municipality of Itaporanga D'Ajuda, Sergipe, northeastern Brazil (Figure 1).The reserve, created in 2011, is part of the experimental campus of the local unit of the Brazilian Agri- Rapid surveys as a key tool for the inventory of the bat fauna of Brazil: New records for the coastal restinga cultural Research Company (EMBRAPA).The RPPN Caju comprises a variety of habitats associated with the Atlantic Forest biome, such as coastal restingas, mangroves, and salt flats, a typical profile of the coastal lowlands of Sergipe, and much of the northeastern Brazil (Silva et al., 2000).
The local soil is sandy and has a natural low fertility (Silva et al., 2000;Araujo Filho et al., 1999).The relief is predominantly flat or slightly undulating, while the mangroves are tidal (EMBRAPA, 2013).The climate is tropical megathermal with dry season in the summer, As in Köppen's classification (Alvares et al., 2013).The rainy season occurs typically between May and August.

Sampling
We conducted the bat survey on 10 consecutive days between October 21 st and 31 st , 2014 using mist net trapping (n = 10; 12 m x 2.5 m).We opened the mist nets at ground level from 5 p.m.h to midnight and checked them every 20 minutes.On each day, we also searched different points of the RPPN actively.When choosing the sampling points, we prioritized areas near flowering or fruiting plants, and water sources.We also searched for potential shelters, both to set up the mist nets at night or for active searches during the day.
We placed the captured bats in cotton bags and released most individuals after identification (based on Gardner, 2007), noting gender, age category, reproductive phase, forearm length and body mass.Before release, each individual was marked with a numbered metal band.Voucher specimens of each species were fixed with 10% formalin solution and preserved in wet medium (70% alcohol), before being deposited in the Mammal Collection of the Federal University of Sergipe (Appendix 1).

Data analysis
We calculated the sampling effort by multiplying the total area of the mist-nets by the number of hours they were kept open (Straube and Bianconi, 2002).Species were considered dominant if their relative abundance was higher than 1/S, where S = species richness (Uramoto et al., 2005).We calculated the Jackknife1 species richness and plotted the cumulative species curves (observed and estimated) based on 1000 iterations (see Colwell and Coddington, 1994) in EstimateS 8.0 (Colwell, 2005).Finally, we classified the recorded species according to their trophic guild, based on Kalko et al. (1996), as insectivorous, frugivorous, nectarivorous, piscivorous or hematophagous.

Results
Total effort of mist-netting was 16.200 h.m 2 , with an additional 30 hours of active search.We captured 191 bats (no recaptures) of 16 species (Figure 2), 14 genera and 5 families (Table 1).Active searches were unsuccessful.The richness estimated by Jackknife 1 was 21.33, with a significant difference (t = -16.68,df = 16, p = 0.0001) between the observed and expected richness, which reinforces the need to increase the sample effort (Figure 3).

Discussion
The bat species richness recorded in the present study (16 spp.) is one of the highest recorded for restinga habitats to date.The species richness recorded in previous restinga inventories ranges from two species -in the Maricá Environmental Protection Area (Cerqueira et al., 1990) and in the municipality of Quissamã (Pessôa et al., 2010), both in the state of Rio de Janeiro -to 16 species at Praia das Neves in Presidente Kennedy, Espírito Santo (Luz et al., 2009).Mean species richness in all restinga inventories done in Brazil (n = 18) is 9.05 (SD ± 4.83) species, although sampling effort varies considerably among fieldworks, ranging from 350 h.m² (Pessôa et al., 2010) to 127,500 h.m² (Rosa, 2004).In the present study, we placed mist-nets purposely in the largest possible number of habitats, in order to maximize the sampling of different microenvironments, and a larger number of habitat-dependent species.The efficiency of this strategy was reflected in the high species richness recorded, even though most species were represented by only one or a few (5 or less) specimens.
The present study confirms the predominance of phyllostomids in inventories with mist nets in the Neotropi-Patrício A. da Rocha, Juan Ruiz-Esparza, Raone Beltrão-Mendes, Saulo M. Silvestre, Viviane Sodré Moura, Natasha Moraes de Albuquerque, Rodrigo Farias de Carvalho Terra, Luana Marina de Castro Mendonça, Stephen Francis Ferrari Volume 12 number 2  may -august 2017 cal region, as well as those previously conducted in the restinga (Nogueira et al., 2010).The Phyllostomidae is the most diverse family of Neotropical bats (Gardner, 2007) and capture is favored by placing mist nets at ground level, while emballonurids, molossids and vespertilionids have a more sophisticated echolocation system, which permits better detection of the nets (Fenton et al., 1992;Simmons and Voss, 1998).
Despite the bias associated with the use of mist nets, the presence of emballonurids, represented by Peropteryx macrotis (Wagner 1843) and Saccopteryx leptura, appears to be unusual in the restinga.Peropteryx macrotis had been recorded previously at only one location, the Rio da Onça State Park in Paraná (Fogaça and Reis, 2008), while this is the first record of S. leptura in this type of environment.
Seven of the 16 species listed here (41.1%) appear to be common in restinga habitats.Artibeus lituratus has been recorded in 83.3% of previous inventories (n = 18), followed by Glossophaga soricina (Pallas 1766) (72.2%),Myotis nigricans (Schinz 1821) (72.2%), A. obscurus (Schinz 1821) (55.6%) and P. lineatus, S. lilium and C. perspicillata (50.0%).Remarkably, we did not capture A. fimbriatus Gray 1838 in the RPPN Caju, despite the fact that this species has records for half of all previous inventories.In contrast, A. planirostris -the most abundant species in the present study -has records only for two other restinga locations, the Superagui National Park (n = 2) and the Rio da Onça State Park (n = 1), both in the state of Paraná (Fogaça and Reis, 2008).This contrast is related to the distribution of these species within the Atlantic Forest.While A. fimbriatus is common in the southern Atlantic Forest and rare in northeastern Brazil, A. planirostris has the opposite distributional pattern (Gardner, 2007).
Frugivorous species dominated (species richness and abundance) in the present study area, probably at least partly because of the sampling method (mist-netting) as mentioned above, which is typical of the Atlantic Forest (e.g.: Carvalho et al., 2009;Gomes et al., 2016;Luz et al., 2009).Noctilio leporinus is the only piscivorous species known to occur in the restinga and, despite being expected to occur in fluvial and marine environments, it has been recorded previously at only five locations (Oprea et al., 2009;Luz et al., 2009;Luz et al., 2011).
All previous bat inventories in coastal restinga habitats have focused on sites in southern Brazil.The present study, at RPPN Caju, is the first for the Northeast.With the new records presented here, the total number of bat species known to occur in the restinga has increased to 41, and the number of genera to 28 genera (including Saccopteryx and Molossops).The records of Molossops temminckii and Eptesicus brasiliensis also increase the number of bat species known to occur in the state of Sergipe to 50 (Mikalauskas, 2005;Mikalauskas et al., 2006Mikalauskas et al., , 2011Mikalauskas et al., , 2014;;Ástua and Guerra, 2008;Feijó and Nunes, 2010;Rocha et al., 2010Rocha et al., , 2011Rocha et al., , 2014aRocha et al., , 2014bRocha et al., , 2013Rocha et al., , 2015, in press;, in press;Donato et al., 2012;Brito and Bocchiglieri, 2012;Bocchiglieri et al., 2016;Souza et al., 2016;Bomfim et al., 2017).
Molossops temminckii is uncommon in inventories, and is known from little more than twenty localities in  Rapid surveys as a key tool for the inventory of the bat fauna of Brazil: New records for the coastal restinga Brazil, mostly in the Caatinga and Cerrado domains (Eger 2008;Nunes et al., 2013).This record is nevertheless unexpected, as it is only the second in the northern extreme of the Atlantic Forest, approximately 500 km south of the first record in the Reserva Biológica Guaribas, Paraíba.Nunes et al. (2013) captured 16 individuals at this site, all in the canopy, indicating that this species is under-sampled in mist nets set at ground level.
No species of Eptesicus has been recorded previously in Sergipe.As in the case of M. temminckii, even considering the methodological bias, there are few records of Eptesicus brasiliensis from the Atlantic Forest of northeastern Brazil.The current record fills a gap of approximately 900 km between southern Bahia (Faria et al., 2006) and the state of Paraíba (Feijó and Langguth, 2011).
These records indicate that rapid surveys can be an important inventory tool, especially in Brazil, where less than 10% of the country was minimally surveyed, and there are no records of bats at all from almost 60% of its territory (Bernard et al., 2010).We also found that the "wandering" placement of mist nets, which were set at a different point each night, is a relatively effective approach to increase the number of bat species recorded, especially in rapid surveys.This approach was based on the assumption that capture rates tend to decline over time because the bats learn the locations of the nets, and are thus able to avoid capture (Larsen et al., 2007;Marques et al., 2013).The daily relocation of the nets may not only minimize this avoidance effect (Marques et al., 2013), but also guarantee the sampling of new microhabitats, including roosts, bodies of water, and feeding patches, which may lead to an increase in capture rates.
In addition to complement the management plan of the RPPN Caju, which currently includes no data on the local bat diversity, the present study has advanced our understanding of the patterns of occurrence of bat species in restinga habitats, which are closely linked to the bat diversity of the surrounding region.

Figure 1 .
Figure 1.Location of the Caju Private Natural Heritage Reserve, in the municipality of Itaporanga D'Ajuda, Sergipe, northeastern Brazil.

Figure 4 .
Figure 4. Relative abundances of the bat species recorded in the Caju Private Natural Heritage Reserve, in Itaporanga D'Ajuda, Sergipe, northeastern Brazil.