ARTÍCULO

Assemblage of chiropterans in a remnant of semideciduous seasonal forest in southern Brazil and latitudinal patterns of species diversity in the Atlantic Forest

 

Daniel Paulo de S. Pires¹, Rosane V. Marques², Tiago C. Cabral³, Camila S. de Lima⁴, and Cristina V. Cademartori³

¹ Conselho Regional de Biologia 03, Setor de Fiscalização, Coronel Corte Real, 662, Petrópolis, 90630-080 Porto Alegre, RS, Brasil [correspondence: <pires.daniel@yahoo.com.br>].
² Unidade de Assessoramento Ambiental, Divisão de Assessoramento Técnico, Procuradoria Geral de Justiça do Estado do Rio Grande do Sul, Rua General Andrade Neves, 106 10° andar, 90210-210 Porto Alegre, RS, Brasil.
³ Laboratório de Conservação e Manejo da Biodiversidade, Pós-Graduação e Pesquisa, Unilasalle, Av. Victor Barreto, 2288, 92010-000 Canoas, RS, Brasil.
⁴ PPG em Biologia Animal, Depto. de Zoologia, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Av. Bento Gonçalves, 9500, Prédio 43435, Agronomia, 91540-000 Porto Alegre, RS, Brasil.

Recibido 4 marzo 2014.
Aceptado 20 agosto 2014.

Editor asociado: P Velazco

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ABSTRACT.

Observed and expected richness, capture success, diversity, dominance, evenness and the effect of latitude on the above variables at the regional level were evaluated with regard to the chiropteran fauna of a semideciduous seasonal forest remnant in the state of Rio Grande do Sul, southern Brazil. Sampling occurred between July 2008 and June 2010 using mist nets erected at ground level. So that chiropteran fauna could be described and compared to other studies in the Atlantic Rainforest throughout the 10°-30°S using multivariate regression. One hundred and sixteen specimens were captured, comprising 9 species and 3 families: Phyllostomidae, Vespertilionidae and Molossidae. Capture success was 0.0008 ind/m²h, with a diversity index (H') of 1.623; dominance (BP) of 0.4783; evenness (J') of 0.7385, and expected richness of 11 species. Sturnira lilium had the highest capture rate. There was a significant relationship between latitude and capture success and richness (CS: R²=0.64, p=0.0005; S: R² = 0.28, p=0.0473). Distribution and abundance of bats at the regional scale was related to latitude as well as the differentiation of assemblages in the Atlantic Rainforest.

RESUMO.

Assembleia de quirópteros de um remanescente de Floresta Estacional Semidecidual do sul do Brasil e gradientes latitudinais na diversidade de espécies.

A riqueza observada e esperada, o sucesso de captura, a diversidade, a dominância e a equitabilidade (evenness), bem como a influência da latitude sobre estas variáveis em escala regional, foram avaliados, considerando-se a quiropterofauna de um remanescente de Floresta Estacional Semidecidual no estado do Rio Grande do Sul, Brasil. As amostragens transcorreram de julho de 2008 a junho de 2010 por meio de oito redes de neblina instaladas ao nível do solo. Assim, foi possível descrever a quiropterofauna e compará-la, usando-se regressão multivariada, com outros estudos realizados na Mata Atlântica ao longo de um gradiente de 10° a 30°S. Capturaram-se 116 indivíduos pertencentes a nove espécies e três famílias, Phyllostomidae, Vespertilionidae e Molossidae. O sucesso de captura foi 0.0008 ind/ m²h. O índice de diversidade (H') foi 1.623, dominância (BP), 0.4783, evenness (J'), 0.7385, e a riqueza esperada compreendeu 11 espécies. Sturnira lilium registrou o maior número de capturas. Encontrou-se relação significativa entre latitude e sucesso de captura e riqueza (SC: R²=0.64, p=0.0005; S: R² = 0.28, p=0.0473). A distribuição e a abundância de morcegos, em escala regional, estão relacionadas com a latitude, assim como a diferenciação das assembleias na Mata Atlântica.

Key words: Abundance; Atlantic Forest; Bats; Species richness.

Palavras-chave: Abundância; Mata Atlântica; Morcegos; Riqueza de espécies.

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INTRODUCTION

Knowledge of richness and diversity of species is a primary source of information for ecological and zoogeographic studies (Townsend et al., 2006). Further, the study of organisms has been shown to be a useful tool for the evaluation of environmental change, whilst information on diversity provides good indicators of environmental disturbances which, in turn, are important in conservation biology (Primack and Rodrigues, 2001).

Bats contribute significantly to the maintenance of forests since they have an important role in the dispersal of seeds, pollination and predation of insects (Helversen and Winter, 2003; Jones and Rydell, 2003; Patterson et al., 2003; Fabián et al., 2008). In fact, the chiropteran fauna has been shown to be very suitable for the evaluation of environmental modifications and as an indicator of its state of conservation (Medellin et al., 2000; Mikich and Bianconi, 2005).

Diversity and richness of bat species depend on numerous factors, such as the habitat's conservation degree and complexity, availability of food resources, water or shelter, elevation, latitude, stratification and seasonality (Kunz and Kurta, 1988; Pedro and Taddei, 1997; Reis et al., 2003; Esberard and Bergallo, 2005; Dias et al., 2008; Kalko et al., 2008; Pacheco et al., 2010). Examination of latitudinal gradients on assemblages of chiropterans demonstrated that species richness and diversity significantly increased toward lower latitudes, while dominance and evenness did not show the same trend (Patterson et al., 2003).

Although richness of species is actually affected by latitude gradients (Lyons and Willig, 1999), studies on bats do not include assemblages at or below 30°S (Stevens et al., 2006). The effect of scale and its consequences is a relevant issue in contemporary ecology while it becomes more and more evident that results obtained for a particular space or temporal scale are not necessarily reproduced at bigger or smaller scales (Lyons and Willig, 1999). Since assemblages in southern Brazil do not feature in publications on the theme, an evaluation that includes the region and comprises scientific observations at latitudes between 10°S and 30°S will help to understand whether global patterns also apply at a regional scale. Empirical research comprising latitudinal gradients and diversity contributes towards the understanding of a universal pattern and contexts in which exceptions occur (Willig et al., 2003).

Various studies on bats in the forests of Brazil's southern region have been published (e.g., Sipinski and Reis, 1995; Sekiama et al., 2001; Bianconi et al., 2004; Arnone and Passos, 2007; Carvalho et al., 2009). However, few have involved sampling longer than one annual cycle (e.g., Marques and Fabián, 1994; Fabián and Marques, 1996; Marques and Fabián, 2010; Ortêncio-Filho et al., 2010; Marques and Fabián, 2011). The state of Rio Grande do Sul, in particular, still lacks ecological studies on bats, mainly with regard to their diversity and species richness (Weber et al., 2011; Pires and Fabián, 2013). Most studies are important contributions on reproduction, behavior and distribution of species (Marques and Fabián, 1994; Fabián and Marques, 1996; Rui and Fabián, 1997; Fabián et al., 1999; Marques and Pacheco, 1999; Rui et al., 1999; Pacheco et al., 2007; Weber et al., 2007; Bernardi et al., 2009) or available ecological information from surveys that cover all groups of mammals (Kasper et al., 2007a; Kasper et al., 2007b; Penter et al., 2008; Marques et al., 2011). Due to lack of studies on bat species richness and diversity in the semideciduous seasonal forest in Rio Grande do Sul, the current study aims are 1) to determine the composition of chiropteran species and dominance relationships in a semideciduous seasonal forest in Rio Grande do Sul; 2) to evaluate richness and diversity of species of the chiropteran fauna and to compare them with surveys carried out in other forest areas; 3) to investigate whether latitude influences capture success, richness, diversity, dominance and evenness of species of bats in the Atlantic Forest in Brazil.

MATERIAL AND METHODS

The study area comprises the Morro do Coco, a remnant of semideciduous seasonal forest located in the municipality of Viamão, Rio Grande do Sul (30°16'15"S, 51°02'54"W), on the margins of Lago Guaiba (Fig. 1). It is a region comprising private estates without any status of legally protected area. The region's forest vegetation, although secondary, has been restored and well preserved (Backes, 2000). Region climate is Cfa type, according to Koppen's classification (C = Temperate climate or warm temperate; f = humid climate without a marked dry season and well distributed rainfall around the year; a = hot summer). There are 4 well-defined seasons throughout the year (Hasenack and Ferraro, 2006; Livi, 2006), with mean annual temperature at 19.5°C, mean temperature of the warmest month above 22°C, minimum at 3°C in the winter and maximum at 41°C in the summer. Mean annual rainfall is approximately 1300 mm throughout the year, featuring a photoperiod varying between about 10 h on June 21 to 14 h on December 21.

Fig. 1. Localization of Morro do Coco, municipality of Viamão, state of Rio Grande do Sul, Brazil. Right upper corner: the state of Rio Grande do Sul in Brazil; left upper corner: the circle indicates the study area in Rio Grande do Sul.

The current study was carried out during two years, from July 2008 to June 2010, with monthly expeditions of 3 consecutive nights. Seventy-two samplings were performed using eight 12 x 3 m mist nets, placed at a height of 0.5-3.5 m from the ground. Each net remained open for 7 h per night, between 19:00 h and 02:00 h, at the edge of or inside the forest, in clearings, close to fruiting trees and close to houses, to capture insectivorous species that potentially take shelter on roofs. Captured specimens were placed in cotton sacks and later identified with help of an identification key and specific literature (Gardner, 2008; Reis et al., 2007; Barquez and Díaz, 2009). Voucher specimens were collected, fluid-preserved with the skull removed and deposited in the collection of the Museu de Ciências Naturais La Salle (authorization from SISBIO, #12094-2 of 2008).

Sampling effort was calculated by multiplying total area of nets by exposure time and number of repetitions, following Straube and Bianconi (2002). Sampling effort totaled 145 152 m².h (72 m².h close to houses). Capture success (CS) was calculated as the ratio between number of captures and sampling effort, also calculated by other studies undertaken in Atlantic Forest of different Brazilian states (Faria, 2006; Althoff, 2007; Faria and Baumgarten, 2007; Carvalho et al., 2009; Luz et al., 2009; Nobre et al., 2009; Oprea et al., 2009; Ortêncio-Filho and Reis, 2009; Britto et al., 2010; Rocha et al., 2010; Perachi et al., 2011; Weber et al., 2011; Pires and Fabián, 2013); the same occurred with species richness (S), Shannon-Wiener diversity index (H'), Berger Parker dominance index (BP) and evenness (J'), as estimated by Pielou's ratio (Pielou 1969). Consequently, comparisons may be made. These parameters were obtained exclusively on the basis of total number of specimens captured per species (absolute frequency) without taking into consideration habitat distinctions in species composition and abundance, for example, to obtain the broadest possible estimate for each locality. For comparative purposes, the only previous studies utilized were those that met the following two criteria: 1) they were conducted in the Atlantic Forest and 2) mist nets were employed.

Sampling sufficiency was evaluated by species accumulation curve (C.I. 95%). A second order Jackknife estimation of species richness determined expected number of species for the study area since it provided a reliable assessment of species richness regardless of sample size (Zahl, 1977).

Each species recorded was included in an ensemble, according to data of its diet obtained from field observations and in line with the classification proposed by Patterson et al. (2003).

Multivariate regression analysis tested influence of latitude on biodiversity on a regional scale, where the predictor variable (X axis) was latitude and the response variables (Y axis) were capture success (CS), richness (S), diversity (H'), dominance (BP) and evenness (J'), according to Patterson et al. (2003). Influence of latitude on each separate variable was also tested by linear regression analysis. Response is multivariate regression, or rather, y = (y₁,...,y_p), and variables y₁,...,y_p are measured within the same sampling unit and, as in the univariate case, associated to p sets of non-randomized predictor variables. When parameters of p regressions are estimated as a whole by multivariate regression, a gain in the efficiency of estimators is obtained. However, this analysis also verifies p of each regression separately.

Multivariate regression, linear regression, capture success (CS), richness (S), diversity (H'), dominance (BP) and evenness (J') were calculated with Past 4.01 (Hammer et al., 2001) and species richness was estimated with EstimateS 8.1 (Colwell, 2001).

RESULTS

A total of 116 specimens were captured including 9 species and 3 families (Table 1). Capture success corresponded to 0.0008 bats/ m²h. When compared to other sites in Atlantic Forest, capture success obtained at Morro do Coco was always lower (Table 2).

Table 1. Species of bats captured with mist nets at the Morro do Coco, municipality of Viamão, state of Rio Grande do Sul, Brazil, from July 2008 to June 2010. N = Number of captures; E = Ensemble (F, frugivorous; H, hematophagous; I, insectivorous; N, nectarivorous).

Table 2. Rates of capture success, richness, diversity, dominance, and evenness of chiropteran species in different locations of the Brazilian forest formations of the Atlantic Forest. L = latitude (°S); CS = capture success; S = richness; H' = Shannon-Wiener diversity; BP = Berger Parker dominance; J' = evenness.

The most represented family was Phyllostomidae, with 5 recorded species and 83% of captures. Molossidae and Vespertilionidae, although represented by 2 species each, differed in number of captures. Sturnira lilium was the dominant species (Table 1, Fig. 2).

Fig. 2. Percentages of captures of bats at the Morro do Coco, municipality of Viamão, Rio Grande do Sul, Brazil, between July 2008 and June 2010.

By statistical extrapolation of probability of occurrence for each species, the second order Jackknife estimator of species richness demonstrated that the curve did not reach an asymptote but showed a slight trend towards stabilization (C.I. 95% ± 0.54), estimating about 11 species for the study area (Fig. 3). Likewise, since the species accumulation curve does not show a complete asymptote, an increase in sample size implies an increase in the number of species (C.I. 95% ± 0.49). In fact, there was a gradual increase in the number of species with an increase in the number of captures, such that, with about 86% of the night's samples, 100% of the species found in this study were already recorded. Diversity, calculated by the diversity index (H'), was 1.623, dominance (BP) 0.4783, and evenness (J') 0.7385.

Fig. 3. Species accumulation curves of chiropterans captured from July 2008 to June 2010 at the Morro do Coco, municipality of Viamão, Rio Grande do Sul, Brazil.

The comparison of diversity gradients with regard to latitude (Fig. 4) demonstrated that latitude was significantly related to the gradients as a whole (F = 8.94, R² = 0.289, p = 0.003). At higher latitudes, capture success and richness were significantly lower (SC: R²= 0.64, p= 0.0005; S: R² = 0.28, p= 0.0473) and there was an increase in capture success and richness as latitude decreased. In other words, there was an inverse relation between capture success and richness and latitude. Diversity, dominance and evenness, however, were not significantly influenced by latitude (H': R² = 0.27, p= 0.0520; BP: R² =0.11, p = 0.23126; J': R² = 0.14, p= 0.17).

Fig. 4. Relationship of latitude with (a) capture success; (b) richness; (c) diversity; (d) dominance; and (e) evenness in studies in the Atlantic Rainforest at latitudes 10°-30º S.

DISCUSSION

The richness observed at the Morro do Coco included 22.5% of the species recorded in Rio Grande do Sul and about 48% of the species expected for the hydrographic basin of Lago Guaiba (Pacheco et al., 2007; Passos et al., 2010). However, the collector's curve suggested that it was not possible to record all species expected for the study area (Fig. 3). In particular, the families of insectivores (Vespertilionidae and Molossidae), which according to Bernard (2001) are more difficult to sample when mist nets are employed, could show higher numbers of recorded species with the utilization of other sampling techniques. Nevertheless, the use of mist nets was one of the criteria to compare data from studies in the Atlantic Forest.

Similar studies on semideciduous seasonal forests in southern Brazil reported a higher number of species than that at the Morro do Coco. Ortêncio-Filho and Reis (2009) found 17 species; Bianconi et al. (2004) demonstrated the presence of 16 species; Ortêncio-Filho et al. (2005) recorded 12 species; Gallo et al. (2008) and Britto et al. (2010) reported 10 species each. Although the sampling effort at the Morro do Coco was not low and the size of the forest remnant reached approximately 140 ha, observed richness failed to attain the minimum number of species registered for the smallest areas already analyzed in the same vegetation formation. However, Weber et al. (2011), in a survey carried out in a deciduous seasonal forest, also recorded 9 species, with differences only in species composition and number of captures. Pires and Fabián (2013) reported the same species number and composition to those of the current study in their research in a seasonal semideciduous forest close to the Morro do Coco (approximately 10 km). In comparison to similar environments of other Brazilian regions, lower species richness in Rio Grande do Sul was expected since the state has the lowest number of bat species in southern Brazil, especially phyllostomids (Passos et al., 2010).

The predominance of phyllostomids appears to be consistent across Neotropical studies. In fact, it is the family with the greatest richness and abundance reported in studies carried out in southern Brazil (Bianconi et al., 2004; Carvalho et al., 2009; Weber et al., 2011). The fact that most phyllostomids captured were frugivorous may be due to the sampling method, with nets set between 0.5 m and 3 m above the ground, that is, the height of most fruit trees (Fabián et al., 2008). The abundance and richness of species of the families Vespertilionidae and Molossidae, observed at the Morro do Coco, did not differ much from other studies in the southern region of Brazil, where it seemed that the variety of the number of species depended on the type of area and method employed in the study (Reis et al., 2000; Sekiama et al., 2001; Esberard, 2003; Weber et al., 2011).

Despite the high sampling effort, capture success was very low when compared to that registered in other studies. From a biogeographic perspective, the study area is located in the mid-latitude subtropical region and in the southern boundary of phyllostomid species. Phyllostomidae is a tropical and subtropical family with limited thermo-regulating requirements and physiological restrictions (Willig and Bloch, 2006). Thus, the possibility that capture success was low might not be discarded due to the small population size of the species of this family in the region. In fact, it is common that populations are small at their distributional limits (Begon et al., 2007). An inverse relation between capture success and latitude, such as that found on a regional scale, supports this idea.

The latitudinal gradient of species richness and diversity of bats in the tropical region is a known pattern, while dominance and evenness do not show a correlation with latitude (Patterson et al., 2003). The evaluation of studies carried out in the Atlantic Forest, between 15° and 30° of latitude south, confirmed, on a regional scale, the pattern expected for species richness, but not for diversity, which varied regardless of latitude, even though results were only marginally significant. Dominance and evenness, on a regional scale, also varied regardless of latitude. Empirical evidence shows that diversity measures vary neither together nor identically across latitudes and comparisons of biodiversity, weighed by species abundance, may be impaired if not based on identical bases (Willig et al., 2003). According to Patterson et al. (2003), temperature, rainfall and insolation are the latitudinal factors that influence variations in assemblages of tropical bats and their capture success. Richness determinants for New World bat species are defined as a set of energy availability, environmental and seasonal heterogeneity, followed by energy and seasonality and, lastly, heterogeneity with one of the variables mentioned above (Tello and Stevens, 2010). The species richness of bats in the Atlantic Forest primarily varies as a result of temperature variations (Stevens, 2013). The scarcity of food supplies and low temperatures can cause torpor during the winter, which limits the number of species able to withstand this stress factor. Tropical ecosystems receive more sunshine and show seasonality according to the rainy or dry periods; in a special way, forests have higher heterogeneity in habitats and resources. Less species richness is thus expected in subtropical environments even though one should not discard the fact that species evolution and distribution have been affected by climate and history throughout millions of years (Stevens, 2011).

In spite of lower capture success, richness and diversity of species at the Morro do Coco were equivalent or higher to those in other areas of the Atlantic Rainforest (Table 2). Bat assemblage at the Morro do Coco generally revealed higher dominance and evenness rates (Table 2). Regression analysis between latitude and richness showed that an inverse relationship exists among these components, with an absence of association between latitude and diversity, or rather, different from that expected. Neither evenness nor dominance exhibits any systematic variation linked with latitude. At lower latitudes the rates of increase in the number of rare species outstrip those of common species, with a greater impact on richness than on evenness, which varies less as a result (Stevens and Willig, 2002). The arbitrariness and limitations of the composition of diversity indexes by richness and evenness, to which different weights are given, have been pointed out by Melo (2008). In the case of diversity, the index obtained in this study was higher than that found by Bianconi et al. (2004) in fragments of a semideciduous seasonal forest in the state of Paraná, equal to 1.38, and by Weber et al. (2011) in a fragment of a deciduous seasonal forest in Rio Grande do Sul, equal to 1.55.

The current study showed that S. lilium was the species with the highest number of records which overwhelmed the next species by 100%. Results are not surprising, since the species is common in places with a greater degree of anthropogenic influence where the more generalist species tend to increase considerably their density (Bianconi et al., 2004; Reis et al., 2006). Although the results of this investigation differ from those carried out in more preserved areas (Rex et al., 2008; Dias et al., 2008), evenness demonstrates that the species are distributed in a reasonably even way within the community.

Inventories of bats in Brazil usually show some dominant species coexisting with rarer ones (Esberard, 2003; Bianconi et al., 2004; Dias et al., 2008). The locally common S. lilium was the species with the highest number of captures. This fact coincides with other investigations in the state of Rio Grande do Sul (Weber et al., 2011, Pires and Fabián, 2013) and indicates that it is also one of the commonest species in inventories in the state. Artibeus lituratus and A. fimbriatus also had higher capture frequency when compared to that of other species. The 3 taxa together comprised 72% of records known for their high frequency in inventories in the southern region of Brazil (Bianconi et al., 2004; Weber et al., 2011). The presence of these species may be strictly related to their feeding preferences for Piperaceae, Solanaceae and Moraceae, respectively (Fabián et al., 2008) plant species with known occurrence at the Morro do Coco (Backes, 1999).

All taxa of Vespertilionidae at the Morro do Coco were considered rare in the sample, as in other studies conducted in southern Brazil, in which vespertilionids are few in number, sometimes constituting the second most represented family in forest surveys that utilize mist nets (Dias et al., 2008; Carvalho et al., 2009; Britto et al., 2010; Weber et al., 2011).

The 15 specimens of Molossus molossus captured as well as the only specimen of M. rufus were trapped with nets set in front of the exit of a tile-roofed house, a strategy that increased the probability of sampling the Molossidae (Esberard, 2003). Despite the low sampling effort employed for the capture of molossid bats, M. molossus was the third species with the highest number of specimens. The facts demonstrated the importance of these animals in the assemblage of chiropterans in the region. The species is considered unusual in urban and periurban environments in Rio Grande do Sul (Pacheco et al., 2010), especially when compared to Tadarida brasiliensis which was not recorded at the Morro do Coco.

There was no capture of piscivorous bats, but at least one specimen was sighted flying over a small flooded area between the field and forest fragment in the study area. Moreover, there is a record of an occurrence of Noctilio leporinus in the region (Marques and Pacheco, 1999). Besides the low number of captures compared to the high sampling effort, all the ensembles occupied by chiropterans in the region were represented in this study. The presence of frugivorous, nectarivorous, hematophagous, low-flying insectivorous (vespertilionids), high-flying insectivorous (molossids) and piscivorous bats accounted for the 6 different types of ensembles and demonstrated that, despite low species richness and capture success, the trophic diversity resembled that of tropical environments. Comparisons between bat assemblages in different environments (the wet tropical forests of Central America and the Amazon and more open formations such as the Caatinga and the Cerrado) indicated up to 7 guilds (Stevens and Willig, 2000), although featuring higher species richness than that at the Morro do Coco. In spite of low species richness, 6 trophic groups were reported in the area under analysis.

The current study surveyed a representative portion of the fauna of bats for the region. Since inventories represent the starting point for ecological studies of communities, many aspects of the chiropteran fauna still need to be investigated. Densities, temporal population fluctuations, roosts, and reproductive and activity patterns may be elucidated in the future with the application of suitable methods, for a better understanding of the partitioning of resources and coexistence of species in the subtropics.

As demonstrated in the current analysis, latitude is related to the distribution and abundance of bats on a regional scale too and thus contributes towards the differentiation of assemblages, albeit within the same biome of Atlantic Rainforest. The proportionally inverse relationship between latitude, richness and capture success may explain the low number of bat captures often reported for Rio Grande do Sul.

ACKNOWLEDGMENTS

The authors would like to thank the team that helped them with field work. Thanks are also due to the Lasalle Brothers for allowing the authors to conduct the study on their estate. They are also grateful to the Laboratório de Geoprocessamento do Unilasalle, especially Diego Medeiros, for the preparation of the map of the area. Thanks are also due to CNPq for its financial support.

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