Introduction

Material and methods

Study areas

The study was conducted in the municipalities of Varre-Sai, Sumidouro, and Cantagalo (Fig. 1). The three areas are highly fragmented due to the historical process of land use for agriculture and cattle ranching, and they represent gaps in the knowledge of occurrence of mammals, in general, and bats, in particular, for the state of Rio de Janeiro (Bergallo et al. 2009).

a

b

c

d

Figure 1.

Location and landscape of the studied areas in the Atlantic Forest of Rio de Janeiro, Southeastern Brazil.

a: Remnants of Atlantic Forest in the state of Rio de Janeiro (dark green), and location of the three surveyed areas in the municipalities of Varre-Sai (1), Cantagalo (2) and Sumidouro (3).  
b: Sampled area in Varre-Sai.  
c: Sampled area in Cantagalo.  
d: Sampled area in Sumidouro.  

Varre-Sai is in the extreme north of the state of Rio de Janeiro, bordering the state of Espírito Santo. The locality sampled is situated at the Serra da Sapucaia (20°55'50''S, 41°53'54''W; altitude ca. 800 m), an extension of the Serra do Caparaó, in the Mantiqueira range. Sampling was carried out in fragments of seasonal semideciduous forest surrounded by matrix of pastures, agricultural fields and coffee plantations.

Sumidouro is in the mountains of the central region of Rio de Janeiro, at the continental border of the Serra do Mar. Fieldwork was carried out in a small fragment of dense ombrophilous forest on top of an inselberg-type rock formation named Pedra de Santa Rita (22°07'38"S, 42°41'00"W; altitude ca. 900–1000 m), an area with several natural caves.

Cantagalo is also in the mountains of the central region of the state of Rio de Janeiro, in the north of the continental border of Serra do Mar. Samplings were carried out in the Novo Tempo cave and surrounding areas (21°48'53"S, 42°11'57"W; altitude ca. 400 m), in a region of dense ombrophilous forest. The Novo Tempo cave is one of the largest caves in the state of Rio de Janeiro, and is located in a region formed by a mosaic of secondary forest fragments of various sizes, agricultural fields and open areas (pastures).

Data resources

Results and Discussion

We captured a total of 148 bats of 17 species for the three localities together (Sumidouro = 82 individuals of 11 species; Cantagalo = 25 individuals of seven species; Varre-Sai = 41 individuals of nine species). Carollia perspicillata was the most frequent species in the three areas, representing more than 50% of all bats recorded at Varre-Sai and more than 35% of the records from the other two areas (Table 1). Carollia perspicillata seems to be the dominant species in most Atlantic Forest localities in Rio de Janeiro (see Esbérard et al. 2006, Dias et al. 2008, Luz et al. 2011, Delciellos et al. 2012), and one of the most common in the Neotropics.

Table 1.

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Absolute and relative abundances (%) of bat species, and parameters of the bat community (species richness, dominance, equitability, and diversity) for the three localities studied here.

Taxa	Trophic guild	Captures
		Sumidouro	Cantagalo	Varre-Sai
Emballonuridae
Peropteryx macrotis	Insectivore	0	5	0
Phyllostomidae
Desmodontinae
Desmodus rotundus	Sanguivore	10	5	0
Diphylla ecaudata	Sanguivore	1	2	1
Glossophaginae
Anoura caudifer	Nectarivore	21	1	2
Glossophaga soricina	Nectarivore	0	1	0
Carolliinae
Carollia perspicillata	Frugivore	30	10	22
Phyllostominae
Chrotopterus auritus	Carnivore	3	0	0
Macrophyllum macrophyllum	Insectivore	1	0	0
Stenodermatinae
Artibeus fimbriatus	Frugivore	0	0	2
Artibeus lituratus	Frugivore	5	0	1
Artibeus obscurus	Frugivore	3	0	0
Chiroderma doriae	Frugivore	3	0	0
Platyrrhinus lineatus	Frugivore	0	0	1
Platyrrhinus recifinus	Frugivore	3	0	0
Sturnira lilium	Frugivore	0	0	10
Vampyressa pusilla	Frugivore	2	0	1
Vespertilionidae
Myotis nigricans	Insectivore	0	1	1
Total		82	25	41
Species richness		11	7	9
Capture efficiency (m².h)		0.010	0.005	0.006
Dominance (D')		0.224	0.251	0.355
Equitability (J')		0.761	0.821	0.648
Shannon-Wiener index (H')		1.826	1.599	1.426

Individuals of frugivorous bats accounted for most of the captures in the three areas, and in the four habitats sampled as well. The dominance of frugivorous species typical of forest edge, such as C. perspicillata, is common in secondary forest fragments and agricultural areas (Heithaus and Fleming 1978, Faria 2006, Rocha et al. 2010, Novaes et al. 2014), since these species are benefited by the presence of pioneer vegetation and by high fruit production (Herrera et al. 1994, Murcia 1995, Guariguata and Sáenz 2002, Asbjornsen et al. 2004). The use of mist-nets may biased the low sampling of insectivorous bats, becuase it is more efficient for sampling representatives of phytophagous species (such as stenodermatines and carolliines) than animalivorous species, which can detect mist-nets easily (Portfors et al. 2000, Gorresen et al. 2008).

The three areas sampled had similar values for species diversity, equitability and dominance (Table 1). However, there were significant differences between these indices when compared by habitat. The forest interior showed higher species richness and species diversity (H’=2.27) than the other habitats, but there were no dominance (D’=0.12) (Table 2), indicating that the forest interior is subject to less environmental stress than the other habitats. The forest interior also had a high evenness of species composition (J’=0.91), and a greater number of exclusive species (five) when compared with the other habitats.

Table 2.

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Bat species richness by habitat, considering the three areas combined.

Species	Habitats
	Forest	Edge	Riparian	Open areas
Peropteryx macrotis	0	0	0	5
Anoura caudifer	7	2	1	14
Artibeus fimbriatus	2	0	0	0
Artibeus lituratus	5	1	0	0
Artibeus obscurus	3	0	0	0
Carollia perspicillata	7	13	19	23
Chiroderma doriae	3	0	0	0
Chrotopterus auritus	3	0	0	0
Desmodus rotundus	10	0	0	5
Diphylla ecaudata	1	1	0	2
Glossophaga soricina	0	0	0	1
Macrophyllum macrophyllum	0	0	1	0
Platyrrhinus lineatus	0	0	1	0
Platyrrhinus recifinus	3	0	0	0
Sturnira lilium	1	8	1	0
Vampyressa pusilla	2	1	0	0
Myotis nigricans	0	0	1	1
Total of captures	47	26	24	51
Species richness	12	6	6	7
Capture efficiency (m².h)	0.012	0.006	0.006	0.013
Dominance (D')	0.121	0.355	0.635	0.300
Equitability (J')	0.913	0.715	0.472	0.745
Shannon-Wiener index (H')	2.270	1.282	0.847	1.451

The higher species richness within the forested areas was expected, since these environments have more heterogeneous habitats, allowing coexistence of more species from different trophic guilds than other habitats, including those species with more specialized feeding habits (Kalko et al. 1996). Nevertheless, five species were recorded neither in the interior nor at the edge of forests, among them: Peropteryx macrotis and Glossophaga soricina were collected only in open areas; Macrophyllum macrophyllum and Platyrrhinus lineatus were collected only near or over water bodies in riparian forest; and Myotis nigricans was collected both in open areas and riparian forest. These observations reinforce the importance of sampling different habitats during short-term species surveys.

The three regions sampled showed low richness and diversity of species compared to other studies carried out in mountainous areas and other close localities (e.g., Esbérard 2007, Moratelli and Peracchi 2007, Dias et al. 2008, Esbérard et al. 2010). This may be due to the low sampling effort employed in the present study, when compared with the aforementioned studies, or even due to the characteristics of the landscape, since most of the previous studies conducted in mountainous regions of Rio de Janeiro were concentrated in areas of continuous forest, which support higher species richness (Medellín et al. 2000). Therefore, it is possible that the high degree of human-induced disturbance and habitat fragmentation in these areas have resulted in the loss of more sensitive species.

Even considering the low species richness, the areas sampled in the present study yielded some interesting records. An individual of Macrophyllum macrophyllum, a species considered rare in the state of Rio de Janeiro, was captured in a mist-net placed over water bodies, in Sumidouro. According to Weinbeer et al. (2005), this species has a strong association with habitats with collections of water, since it forages close to the water, catching aerial insects or “fishing” semi-aquatic insects from the water surface (Meyer et al. 2005).

We known very little about bats inhabiting caves in Southeastern Brazil. Captures with mist-netsset up inside the Novo Tempo cave revealed colonies of Peropteryx macrotis, Desmodus rotundus, Diphylla ecaudata, Carollia perspicillata and Artibeus obscurus.

Considering the three areas combined, the list of species obtained here is still very preliminary, with the species accumulation curve did not reaching an asymptote (Fig. 2). However, the results of this study indicate that sampling different habitats within a given locality increase the efficiency of bat inventories, in particular, during short surveys.

Figure 2.  

Species rarefaction curve for the three bat assemblages in Rio de Janeiro, southeastern Brazil (see Suppl. material 1).

Discussion

Acknowledgements

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