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Mastozoología neotropical

On-line version ISSN 1666-0536

Mastozool. neotrop. vol.20 no.2 Mendoza Dec. 2013

 

ARTÍCULO

Bat assemblages from mountain forest areas in the serra negra region, southeastern Brazil

 

Pedro H. Nobre1, Marco A. Manhães2, Omar J. Bastos Neto3, Abraão C. Rezende2, and Alexmar S. Rodrigues2

1 Departamento de Ciências Naturais, Universidade Federal de Juiz de Fora, Rua Visconde de Mauá, 300, CEP 36015- 260, Juiz de Fora, Minas Gerais, Brazil [Correspondence: <Pedro.nobre@ufjf.edu.br>].
2 Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora, Campus Universitário, CEP 36036-900, Juiz de Fora, Minas Gerais, Brazil.
3 Colégio Anibal Khury Neto, Rede Estadual do Paraná. Rua Avelino Mantovani, 430, Curitiba, Paraná, CEP 81590-370, Brazil.

Recibido 9 octubre 2012.
Aceptado 21 mayo 2013.
Editor asociado: D Astúa


ABSTRACT.

The aim of this work was to describe the community composition of bats in mountain forest areas in the Serra Negra region, southeastern Brazil, and to compare species diversity and richness between the southern and northern slopes of mountain chain. During November 2007 to March 2010 a total of 608 captures of 19 bat species belonging to families Phyllostomidae and Vespertilionidae were obtained with mist-nets. Phyllostomidae constituted approximately 97% of the captures, and represented by 15 species, and Vespertilionidae nearly 3% of the captures, represented by 4 species. Sturnira lilium was the most frequently captured species (n = 207), followed by Carollia perspicillata (n = 154), Desmodus rotundus (n = 98) and Artibeus lituratus (n = 50). The number of species found (19) is close to the richness estimated by Chao 1 index (21.7). There was no difference in Simpson diversity indices between the slopes, and rarefaction analysis also showed that there was no difference in species richness. The relative abundance of species was different between northern and southern slopes of Serra Negra, as noted by differences in captures of the most common species. Although the availability of food resources was not directly assessed, some data previously recorded in Serra Negra suggest that the presence of more abundant species may be linked to the availability of food resources.

RESUMEN.

Ensambles de murciélagos de los bosques montanos en la región de Serra Negra, sudeste del Brasil.

El objetivo de este trabajo es describir la composición de la comunidad de murciélagos en las zonas boscosas de montaña en la región de Serra Negra, sudeste de Brasil, y comparar la diversidad y riqueza de especies entre las laderas sur y norte. Durante noviembre 2007 hasta marzo 2010 se obtuvieron con redes de niebla un total de 608 capturas de 19 especies de murciélagos pertenecientes a las familias Phyllostomidae y Vespertilionidae. Phyllostomidae constituyó el 97.4% de las capturas, lo que representa 15 especies; Vespertilionidae conformó el 3% de las capturas, con 4 especies. Sturnira lilium fue la especie más frecuentemente capturada (n = 207), seguida de Carollia perspicillata (n = 154), Desmodus rotundus (n = 98) y Artibeus lituratus (n = 50). El número de especies encontradas (19) está muy cerca de la riqueza estimada por Chao 1 índice (21.7). No hubo diferencia en los índices de diversidad de Simpson entre las pistas, y los análisis de rarificación también mostraron que no había diferencia en la riqueza de especies. La principal diferencia entre las pendientes radica en la composición de la comunidad, como se ha señalado por las diferencias en las capturas de las especies más comunes. A pesar que la disponibilidad de recursos alimenticios no se evaluó directamente, observaciones personales y los datos florísticos registrados previamente en Serra Negra sugieren que la presencia de las especies más abundantes de quirópteros está ligada a la disponibilidad de recursos alimenticios.

Key words: Atlantic Forest; Bat diversity; Bat richness; Mountain forest.

Palabras clave: Bosque de montaña; Diversidad de murciélagos; Mata Atlántica; Riqueza de murciélagos.


INTRODUCTION

Brazil has 701 species of mammals in which 174 (24.8%) are bats (Paglia et al., 2012). Although several surveys have increased the knowledge on the ecology and community structure of the bat fauna in different tropical areas (Stoner, 2005), in Brazil, the increasing accumulation of such information reflects only the disperse knowledge of the bat fauna profiles when each of the different biomes is considered individually (Bernard et al., 2011). In the Atlantic Forest, one of the most fragmented biomes within Brazil, bat assemblages are represented by a large number of very abundant species, which certainly plays important ecological roles, since bats act, for example, as seed dispersers, pollinators or controllers of insect populations (Bawa, 1990; Sazima et al., 1999; Muscarella and Fleming, 2007; Kalka et al., 2008).

The pattern of diversity related to altitudinal variation in tropical areas seems to be somewhat more predictable, showing decrease in species richness at the highest elevations (Patterson et al., 1996; Flores-Saldaña, 2008). Recent studies have indicated that the mid-level elevations comprise the greater species richness for tropical bats (Sánchez-Cordero, 2001) and small non-flying mammals (Brown, 2001). Some studies in the Atlantic rainforest have described communities or studied the effects of fragmentation on the bat fauna (Falcão et al., 2003; Reis et al., 2003; Nobre et al., 2009) at an altitude ranging from 65 to 2070 meters. However, the difficult access to mountainous terrain and the consequent difficulty in sampling make it hard to collect information on bat fauna at high altitude environments.

The Atlantic Forest of the Zona da Mata in Minas Gerais State has experienced strong an-thropogenic pressure, leading to fragmentation and reduction of native habitats (Ribon et al., 2003; Ribon et al., 2004), typical and historical processes in the landscapes of southeastern Brazil. Its mountainous areas, however, still harbour remnants of highland forests, associated with forests in different successional stages. In Minas Gerais State, the Atlantic Forest is reduced to about 4% of its original extent, but this complex mountain chain encompasses around 20% of the remnants of this biome (Costa and Herrmann, 2006). The ability of some volant species, such as bats, to use and move through these natural habitats can reduce the probability of insularization in forest patches (Fariah, 2006).

In this work, our goal was to characterize the structure of bat fauna in terms of richness and diversity in a mountainous area of the Atlantic Forest, where altitudes can be considered intermediate (Oliveira-Filho and Fontes, 2000). When sampling different locations within the limits of the area, we assessed the distribution of species in local forest fragments and compared the richness and diversity of species between the southern and northern slopes of the mountain range.

MATERIAL AND METHODS

The study area, known as Serra Negra (21°58'24"S and 43°53'15"W), is part of the Serra da Mantiqueira mountain range, located in the Zona da Mata, Minas Gerais State. The area encompasses a micro-region of Juiz de Fora city, and includes also the municipalities of Bom Jardim de Minas, Santa Bárbara do Monte Verde, Lima Duarte and Rio Preto (Fig. 1). The Serra Negra region is between 870-1760 m high, and the climate is Cwb (Kop-pen, 1938), humid meso-thermic with an average rainfall of 1946 mm.

The landscape is formed by forests surrounded by rocky outcrops and active or abandoned pastures. We sampled five sites on the southern slope and five sites on the northern slopes of the mountain. On the southern slope, we sampled fragments of semi-deciduous and cloud forests at altitudes ranging from 870 to 1040 m. The northern slope has more forest cover, dominated by patches of native rain forests in advanced successional stage. The sampled sites have altitudes between 900 and 1000 m (Fig. 1). The distances between any two sampling sites of both slopes ranged from a minimum of 1.8 km to a maximum of 10.8 km. At each site, an average of four points was selected to perform captures with mist nets.


Fig. 1. Map of Serra Negra region, Minas Gerais State, southeastern Brazil; modified from Menini Neto (2009). Black dots indicate the sampling sites.

Bat captures were developed in two distinct periods: November 2007 to November 2008, mainly on the southern slope, and December 2008 to March 2010, mainly in the northern slope. The surveys were conducted monthly, for 2-3 nights each, totalizing 31 sampling visits. At each site, the samples were sorted into the following environments: riparian areas, water courses, forest edges, forest gaps and forest interior. At these points, bats were captured with mist nets measuring 6 x 3 m, 9 x 3 m and 12 m x 3 m, with 19 mm mesh, installed at ground level, soon after the sunset, and remained open throughout the next 6 to 8 hours. The number of nets per night ranged from 6-8, according to the sampled environment. The sampling efforts were 32 nights on the southern slope (53 243 m2.h), and 38 nights (56 438 m2.h) on the northern slope. The sampling efforts were calculated according to Straube and Bianconi (2002). The mist nets were monitored every 15 minutes, and the captured bats were kept in individual cotton bags for data collection including biometrics, and identification. After the end of each sampling period, the nets were closed and the bats released close to the place of capture.

Two to four specimens per species were collected as voucher material, fixed in formalin 10% and preserved in alcohol 70° GL, according to Vizotto and Taddei (1973), and deposited in the Chiroptera collection at Universidade Federal de Juiz de Fora (Appendix). The species identification followed Vizotto and Taddei (1973), Barquez et al. (1993); Simmons and Voss (1998); Velazco (2005) and Reis et al. (2007). The nomenclature of the species followed Gardner (2008). The species studied were grouped into trophic categories according to Reis et al. (2007) and Lobova et al. (2009).

Species accumulation (Mao Tau) and estimated richness (Chao 1) curves were generated for the total captures in the whole studied area using the Estimates software, version 8.2 (Colwell, 2009). The species richnesses were compared by rarefaction analysis, while the diversity of communities in four areas was calculated using the inverse of the Simpson index (1-D), and the null hypothesis of no difference in diversity was tested by the bootstrap method by means of 1000 resamplings (Solow, 1993). These two tests were performed with the PAST software, version 2.08b (Hammer, Ø. et al., 2001). Differences in frequencies of captures of more common species on southern and northern slopes were investigated by applying the G-test, aided by the BioEstat 5.0 software (Ayres et al., 2007).

RESULTS

We obtained 608 captures of 19 bat species belonging to 2 families, Phyllostomidae the most abundant and richer, representing 97.4% of the captures and 15 species, and Vespertilionidae reached 2.6% of the captures and was represented by 4 species (Table 1). The species accumulation curves tend toward stabilization. The Chao 1 species richness estimator showed a closer relationship with the observed values at the end of the curve. Thus, the number of identified species (19) is very close to the richness estimated by Chao 1, whose final value (21.7) lies in the confidence interval calculated for the species accumulation curve (Fig. 2).

Table 1. Abundance and capture frequency of bat species in southern (SS) and northern (NS) slopes, Serra Negra, Minas Gerais State, southeastern Brazil. Trophic categories (TC) are: N, nectarivores; F, frugivores; S, sanguivore; C, carnivore; O, omnivore; I: insectivore.


Fig. 2. Accumulation curves of bat species richness observed (Mao Tau) and estimated (Chao 1) in Serra Negra, Minas Gerais State, southeastern Brazil. Dotted lines indicate the 95% confidence interval on the mean.

Sturnira lilium (E. Geoffroy, 1810) was the most common species in the captures (207 captures), followed by Carollia perspicillata (Linnaeus, 1758) (N = 154), Desmodus rotundus (E. Geoffroy, 1810) (N = 98) and Artibeus lituratus (Olfers, 1818) (N = 50). These four species accounted for 83.6% of the captures (Table 1). Captures of S. lilium (G = 8.545, g.l. = 1, p = 0.0035), A. lituratus (G = 13.299, g.l. = 1, p <0.001) and D. rotundus (G = 25.589, df = 1, p <0.001) were associated with the southern slope (Table 1). In contrast, captures of C. perspicillata were associated with the northern slope (G = 29.883, df = 1, p <0.001). Platyrrhinus lineatus (E. Geoffroy, 1810): G = 8.929, df = 1, p = 0.0028) and Platyrrhinus recifinus (E. Geoffroy, 1810): G = 19.2892, df = 1, p <0.0001) had their captures associated with northern slope. Despite the small difference in the number of species per trophic category, frugivores were largely dominant in terms of captures in Serra Negra (Fig. 3). However, the number of captures of frugivores was associated with the northern slope (G = 22.487, df = 1, p <0.0001).


Fig. 3. Proportions among bat trophic categories in Serra Negra, Minas Gerais State, southeastern Brazil. Bars represent percentages of captures and number of species.

There was no difference in the Simpson diversity indices (1-D) between the northern (0.771) and southern (0.733) (p = 0.060) slopes. With 291 captures, the southern slope has only one more species than the northern (16 and 15, respectively), without difference in the number of species recorded in the two areas (Fig. 4).


Fig. 4. Rarefaction analysis for bats on southern and northern slopes (SS and NS, respectively) of Serra Negra, Minas Gerais State, southeastern Brazil. Dotted lines around solid line indicate the 95% confidence interval on the mean. The NS curve between SS confidence interval lines indicates that there is no difference in number of species between slopes.

DISCUSSION

The species accumulation curves indicate that the number of species observed in Serra Negra is very close to the expected number. Following the proposal of Bergallo et al. (2003), after gradually expanding the study area and changing the mist net locations on sampling nights, 608 captures seem to have been enough to sample at least the Phyllostomidae.

Phyllostomidae can have their relative abundance and diversity negatively influenced by human activities (Cosson et al., 1999), and some species are considered good indicator of habitat quality (Alho et al., 2011). Medellín et al. (2000) demonstrated that the presence of Phyllostominae, along with its high diversity, can characterize a region of low environmental disturbance due to the remarkable niche specialization of this group in terms of diet and shelter.

The capture frequencies of the Artibeus and Platyrrhinus are probably linked to the capture method. Captures of A. lituratus occurred mostly in nets installed around fig trees (Ficus - Moraceae). In places where plants did not bear fruit or fruit crop size was low, A. lituratus was captured in nets along contour lines on the top of small elevations at the same level as the canopy of hillside forests nearby. The capture of P. lineatus was also more frequent in the nets installed close to fig trees. However, the capture of frugivores, as A. lituratus and others, were certainly favored by the sampling with understory mist nets, which are less effective for largely insectivorous species, since they can perceive the nets by echolocation (Tuttle, 1974; 1976; Voss and Emmons, 1996).

The dominance of S. lilium can also be observed in other mountainous areas of Minas Gerais State, such as Serra do Ibitipoca (Nobre et al., 2009) and Serra do Caraça (Falcão et al., 2003). According to Mello et al. (2008), S. lilium is one of the most abundant species in tropical areas and an effective disperser of Solanaceae seeds in highlands. Albuquerque et al. (2006), studying and comparing the floristic composition and seed dispersal syndrome of Solanaceae in Mexico and a patch of Atlantic Forest in São Paulo, suggested the possible occurrence of co-adaptation between Solanaceae and bats in Brazil.

In the Serra Negra, Valente et al. (2011) showed an altitudinal increase in the abundance of Solanaceae, becoming the dominant species at 1300 m. Feliciano and Salimena (2011), studying the Solanaceae family in the same region, recorded the occurrence of 19 species of Solanum, and a high consumption of these plants by S. lilium has been documented in several tropical areas (Lobova et al., 2009). In addition, Giannini (1999) reported that, in Argentina, the importance of Solanum in the diet of S. lilium may increase with altitude and lead to a respective increase in species richness of such plants. So, it seems plausible that the dominance of S. lilium in the study area is related to the abundance of species of Solanaceae, especially Solanum.

Another very common bat species in the Serra Negra is C. perspicillata. In an ecologically similar way to S. lilium, the fruits of plants of the genus Piper (Piperaceae) are in general the basis of C. perspicillata's diet, despite the wide spectrum of fruits that can be consumed by this bat species in Neotropical areas (Lobova et al., 2009). The plants of the Piperaceae occur mainly in forest edges and secondary forests (Mikich and Silva 2001), habitats where most of the captures of C. perspicillata in the study area occurred. In floristic studies conducted in the Serra Negra region, the occurrence of 20 species of the Piper was recorded (Universidade Federal de Juiz de Fora 2011), thus possibly influencing the large number of captures of C. perspicillata.

Comparing the Serra Negra slopes, there was alternation of dominance between S. lilium and C. perspicillata, but these two species can be regularly found coexisting in the same area (Marinho-Filho, 1991), and both can either change their diet of fruits or move to other areas temporarily in search of food resources (Mello et al., 2004; Lobova et al., 2009). So, although occurring on both slopes, one would expect the proportions to be similar. Unfortunately, there are no comparative studies on the abundance of fruits or species richness between the two slopes, but a plausible hypotheses is that the availability of resources over the years, in terms of the sequential fruiting species of Solanum and Piper, and the seasonal changes in the diet of each bat species, are sufficient to sustain these species on each slope, so that they spatially avoid competition. Heterogeneous spatial occurrence for these two species was observed by Pedro and Passos (1995). They suggested that the rarity of S. lilium in the Linhares Forest Reserve allows greater consumption of Solanum by C. perspicillata.

Altitudes above 1000 m are considered by Eisenberg and Redford (1999) as a limiting factor to the presence of D. rotundus. However, Graham (1983), studying the distribution of bat species along the altitudinal gradient in the Peruvian Andes, reports the occurrence of D. rotundus up to 2900 m. In the Serra Negra region, it was abundant in areas with altitudes ranging from 100 to 1100 m, often being the only species captured. The highest occurrence of D. rotundus was in the southern slope. This location presents a great deal of farming activ-ity, with large domestic animals, mostly cattle and horses, and a significant number of rock shelters and even small natural underground cavities. At sampling points with preserved forests and little farming activity, such as the northern slope, the frequency of capture was only 7.6%. Thus, the southern slope has attractive resources, which should be the main cause of the distribution pattern of D. rotundus in Serra Negra.

The diversity was rather similar between the slopes as a result of similarity in the number of species and uniformity in the distribution of the captures among species on each slope. Thus, the main difference between the slope lies in the community structure regarding the abundance of some species, as observed by differences in the capture of the six most common of them. Difference in the occurrence of bat species in different habitats are also regularly reported at other Neotropical sites (Bernard et al., 2001; Loayza and Loiselle, 2009).

ACKNOWLEDGMENTS

This work was funded by Fundação de Amparo a Pesquisa do Estado de Minas Gerais (FAPEMIG). The Instituto Brasileiro do Meio Ambiente (IBAMA) provided licenses for scientific activities, numbers 10767-1 and 10767-2. We thank the Instituto Ambiental Vale do Rio Preto (IAVARP) for support during the field work, and land owners for allowing us to work in the RPPN Serra Negra.

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APPENDIX

Specimens deposited at the Universidade Federal de Juiz de Fora/Departamento de Ciências Naturais (UFJF/DCN), coleção de Chiroptera as voucher material.

A. caudifer UFJF/DCN-59, UFJF/DCN -241; C. perspicillata UFJF/DCN -86, UFJF/DCN -92, UFJF/DCN -97, UFJF/DCN -214; D. rotundus UFJF/DCN -52, UFJF/DCN -190, UFJF/DCN -230; C. auritus UFJF/DCN -58, UFJF/DCN -202; M. bennettii UFJF/DCN -187, UFJF/DCN -268; M. minuta UFJF/DCN -186; A. lituratus UFJF/DCN -74, UFJF/DCN -98, UFJF/DCN -200, UFJF/DCN -201; A. fimbriatus UFJF/DCN -57, UFJF/DCN -189, UFJF/DCN -233; P. lineatus UFJF/ DCN -75, UFJF/DCN -76, UFJF/DCN -93; P. recifinus UFJF/DCN -93, UFJF/DCN -212, UFJF/DCN -239; P. bilabiatum UFJF/DCN -53; S. lilium UFJF/DCN -56, UFJF/DCN -188, UFJF/DCN -204, UFJF/DCN -205; V. pusilla UFJF/DCN -54, UFJF/DCN -99, UFJF/DCN -203, UFJF/DCN -232; E. furinalis UFJF/DCN -197, UFJF/DCN -198; M. nigricans UFJF/ DCN -55, UFJF/DCN -95, UFJF/DCN -242, UFJF/DCN -278; M. levis UFJF/DCN -197; M. riparius UFJF/DCN -278; M. ruber UFJF/DCN -280, UFJF/DCN -282.