Bat-species richness in the Pantanal floodplain and its surrounding uplands

We studied the bat fauna of the Pantanal floodplain and its surrounding plateaus in Mato Grosso do Sul, Brazil, based on the scientific collection at Universidade Anhanguera – Uniderp and on the Projeto Morcegos do Pantanal data bank at UFMS, comprising 9,037 captures of 56 species recorded from 1994 to 2007. The Pantanal surveys were carried out in the Nhecolândia, Aquidauana, Miranda, and Paraguai sub-regions; the uplands surveys took place in the Maracaju, Bodoquena, and Urucum formations. Bat specimens were mist-netted over 376 nights in 35 sites, predominantly near fruiting trees, bat shelters, and forest patches. In the floodplain 46 species were recorded (n = 6,292 individuals), and 44 species were found in the uplands (n = 2,745 individuals). Six families were recorded: Phyllostomidae (30 species), Molossidae (12 species), Verpertilionidae (nine species) Noctilionidae (two species), Emballorunidae (two species) and Mormoopidae (one species). The bat fauna was predominantly composed of insectivore (32) and frugivore (15) species. The frugivorous Artibeus planirostris (n = 3,101 individuals) was the commonest species in floodplain and uplands. Other common species were Myotis nigricans (n = 762), Molossus molossus (n = 692), Noctilio albiventris (n = 681), Platyrrhinus lineatus (n = 633), Sturnira lilium (n = 461), Carollia perspicillata (n = 451), Glossophaga soricina (n = 436), Artibeus lituratus (n = 320), and Desmodus rotundus (n = 281). In the floodplain there were three insectivores among the most common species, contrasting with the uplands dominated by the frugivores. The diversity for the 35 sites assembled (H’ = 2.5) is comparable to that recorded for tropical forests. The bat fauna presented here represents 34% of the Brazilian bat species, and 62% of species reported for the Upper Paraguay River Basin. Additionally, five species are reported for the first time in Mato Grosso do Sul.

Cerrado plateaus, as well as to discuss the present status of natural habitat conservation and their bat-associated species.

Pantanal flood plain and surrounding uplands
The maze of fluctuating water levels, nutrients, and biota in the Pantanal forms a dynamic ecosystem (Alho, 2008).The degree of inundation creates a range of major habitats.Flooding occupies about 80% of the whole Pantanal.In contrast, during the dry season, most of the flooded areas stay dry, when the water returns to the river beds or evaporates.Major habitats include patches (~ 0.5-5 ha) of semi-deciduous forests (capões) surrounded by grasslands, belts of cerradão or semi-deciduous forests surrounding lagoons (cordilheiras), riparian semi-deciduous forests, and mono-specific forests of woody species such as Tabebuia aurea (paratudal) and Vochysia divergens (cambarazal) (Silva et al., 2000;Araújo and Sazima, 2003).The upper ground (where there are capões and cordilheiras) is at most only a couple of metres above average water level.Rivers and depressions locally known as corixos are lined by riparian forests.In these forest habitats, different species of Ficus and other trees serve as food supply and shelter for frugivores (Teixeira et al., 2009).The uplands surrounding the Pantanal are covered by senso strictu cerrado, cerradão and semi-deciduous forests, which are severely threatened by agriculture and cattle ranching (Alho, 2008;Scariot et al., 2005).Bats were sampled in 35 sites in the Pantanal floodplain and its bordering plateaus, as described below.

Introduction
Bats are often the most species-rich mammalian taxonomic group in the tropics (Patterson et al., 2001) and represent nearly one-third of Brazilian land fauna (Marinho-Filho and Sazima, 1998).Different studies have shown latitudinal gradients contributing to the understanding of geographic distribution of bat diversity, by analysis of species richness patterns on a large scale, across wide spatial areas or with regional focus (Rohde, 1992;Willig, 2000;Stevens and Willig, 2002).Another approach is to examine changes in species richness along environmental gradients, when an assemblage of interacting bat species utilizes the same resource, for example seasonal productivity, which is carried out on smaller spatial scales (Alho, 2008;Drobner et al., 1998;Wilsey and Potvin, 2000).Some environmental factors limit the occurrence and abundance of some species, including habitat heterogeneity, seasonality and conservation status (Alho, 2005;Keddy et al., 2009).
Large and environmentally heterogeneous wetlands like the Pantanal (147,574 km² -latitude 15° 30'-22° 30' S and longitude 54° 45'-58° 30' W), exhibiting annual changes in evenness along environmental gradients, play an important role in biological diversity, because of the heterogeneity of natural habitats, offering opportunities for feeding and reproductive niches (Alho, 2008;Keddy et al., 2009).Differences in bat species abundance may respond to local environmental annual changes or to degree of habitat degradation.Because the Pantanal and its surrounding habitats harbour a large number of bat species, some common (high abundance) and some relatively rare, intensive survey efforts are needed to estimate confidently the species abundance distributions.
Artibeus planirostris (n = 3,101 individuals) was by far the most dominant bat species throughout the entire focal region (Figure 4), showing one order of magnitude more captures than the next nine highly common species -Myotis nigricans (n = 762), Molossus molossus (n = 692), Noctilio albiventris (n = 681), Platyrrhinus lineatus (n = 633), Sturnira lilium (n = 461), Carollia perspicillata (n = 451), Glossophaga soricina (n = 436), Artibeus lituratus (n = 320), and Desmodus rotundus (n = 281).Such strong dominance of A. planirostris has been also reported in other local surveys in the Pantanal floodplain and in its neighbouring upland regions (Camargo, 2003;Camargo et al., 2009;Cunha et al., 2009;Teixeira et al., 2009).Although the dominance by A. planirostris occurred in both regions, in the Pantanal floodplain there were three insectivorous non-phyllostomid species (Myotis nigricans, Noctilio albiventris, and Molossus molossus) among the most common bats, contrasting with the upland plateaus where the commonest species were all frugivorous phyllostomids (Figure 4).The frugivorous C. perspicillata was the second most abundant species in the uplands, but it was not one of the top ten species in the floodplain (Figure 4).Thus, the relative abundance of insectivorous bats appears to be higher in the floodplain than in the uplands, probably for the same reasons which explain the exceptionally high richness of insectivores as discussed above.Calculated values for the Shannon index of diversity were similar between the Pantanal floodplain (H' = 2.3) and its neighbouring uplands (H' = 2.5).Assembling all the 35 sampling sites, diversity was found to be H' = 2.5.These values are higher than those (H' = 1.5 to 1.8) found in short-term surveys in the Bodoquena region (Camargo et al., 2009;Cunha et al., 2009), and closer to values (H' = 1.8 to 2.3) found for different areas in the Atlantic forest in southeastern Brazil (Pedro and Taddei, 1997;Esbérard, 2003).
In pockets of cerrado habitats the most abundant species are Artibeus planirostris (n = 431), Noctilio albiventris (n = 381) and Molossus molossus (n = 362).In fragments of semi-deciduous and deciduous forest on plateaus on the outskirts of the Pantanal the common species are: Myotis nigricans (n = 489), Noctilio albiventris (n = 168) different procedures, predominantly straightforward mistnet surveys, and on the Projeto Morcegos do Pantanal databank at UFMS, Campo Grande, MS, with 4,798 bat entries through mist-net captures between 1998 and 2007.Surveys covered different hydrological seasons of the Pantanal and its surroundings in different habitats, near fruiting trees, bat shelters, or forest canopies.Total capture effort was about 290,000 h.m 2 (time in which nets were kept open multiplied by the area of the nets), distributed throughout 376 nights, with four to 12 nets of variable sizes open per night.Biometrical data were obtained and voucher specimens were prepared for identification, which followed the criteria established by Vizotto and Taddei (1973), Taddei (1983), Anderson (1997), Lopez-González et al. (2001), Gregorin and Taddei (2002), Vicente et al. (2005), and Reis et al. (2006Reis et al. ( , 2007)).

Bat fauna in south Pantanal and surrounding uplands
In all 35 sites 9,037 individuals belonging to 56 species, 36 genera and six families were recorded (Table 1).This number of species represents 34% of the whole richness of bats in Brazil, including the Amazon, annotated by Reis et al. (2006Reis et al. ( , 2007)); it reaches 62% of the total richness reported for the entire Upper Paraguay River Basin (n = 90 bat species), including the northern area in Mato Grosso, Brazil, and the Bolivian and Paraguayan areas (Tomas et al., 2009).In the floodplain sites, 6,292 individuals of 46 species were captured, a number which reaches 64% of the bat species already registered in the whole Pantanal floodplain (Tomas et al., 2009;Alho et al., 2003); in the upland sites surrounding the Pantanal 2,745 individuals of 44 species were recorded, representing 65% of the bat species already reported to occur along the entire Pantanal borders (Tomas et al., 2009).The large number of captures and the cumulative curve of species captured (Figure 2), throughout a relatively long period of time dedicated to survey (1994)(1995)(1996)(1997)(1998)(1999)(2000)(2001)(2002)(2003)(2004)(2005)(2006)(2007), indicate that overall species richness was well sampled and that this is a reliable representation of bat diversity in the focal region.In addition, five species found here -Diphylla ecaudata, Mimon bennettii, Trachops cirrhosus, Uroderma magnirostrum, and Molossus pretiosus -were still not reported for Mato Grosso do Sul (Cáceres et al., 2008), increasing to 66 the number of bat species registered in this state.
The richest and most abundant families in our 35 study sites were Phyllostomidae (30 species and 6,228 individuals) and Molossidae (12 species and 1,071 individuals) (Table 1), corresponding to 34% and 46% of the Brazilian species in these two families respectively (Gregorin and Taddei, 2002;Reis et al., 2006Reis et al., , 2007)).Richness of molossid bats (all insectivorous) in the floodplain (n = 11) was almost twice that in the upland plateaus (n = 6), largely contributing to the high number of insectivorous species exclusively found in the floodplain rather than in plateaus (Figure 3).that the most caught family was Phyllostomidae, represented by Glossophaga soricina and Artibeus lituratus; and some rare species such as Lophostoma brasiliense, Lonchophylla mordax and Lionycteris spurrelli (Bordignon, 2006).
To analyse possible grouping of species or assemblages in the three major habitats, we performed a non-metric multi-dimensional scaling analysis taking the frequencies of species distribution, and that the grouping composed of Myotis albescens, Molossops temminckii, Sturnira lilium, Phyllostomus hastatus, Desmodus rotundus, Glossophaga soricina, Carollia perspicillata, Platyrrhinus lineatus, Molossus molossus, Artibeus planirostris and Noctilio albiventris occurs in the three major habitats: cerrado, semi-deciduous forest and disturbed habitats (with 82% of similarity).is sensitive to disturbance.Some authors (Bergallo et al., 2000) consider this species as threatened by extinction, but it is not listed in the "Livro Vermelho da Fauna Brasileira Ameaçada de Extinção [The Red Book of Brazilian Fauna under Threat of Extinction]", published by the Ministry for the Environment (Ministério do Meio Ambiente) in 2008.No species found in our survey for the Pantanal is officially listed as threatened.Chrotopterus auritus is a large carnivore/insectivore, preying on small mammals, birds and insects, which is very sensitive to environmental disturbance, requiring good forest habitats and shelter in caves.Artibeus lituratus was recorded at only 1.5% in our study, but it is a good coloniser of disturbed habitat, besides living in low densities.The survey conducted in the region of Aporé-Sucuriú, northern Mato Grosso do Sul, revealed in abundance, whereas the abundance of frugivorous stenodermatines and nectarivorous glossophagines decreases (C.Santos, unpublished data).
Our data show a high number of Phyllostomidae, which may represent a good indicator for low levels of habitat disturbance (Pedro at al., 1995;Pedro, 1998;Medellín et al., 2000).This family is well diversified in number of species and in feeding habits.The high number of frugivore species in the family implies that the habitats support a high number of fruit-bearing trees (see Pott and Pott, 1994).In addition, the high primary production favours an increased of arthropods, which supports the guild of insectivore bats.The abundance of frugivore species reflects the importance of this guild for the Pantanal bat assemblages.In addition, bats play an important role in regulating the Pantanal ecosystem as seed dispersers, pollinators and regulators of insect populations (Gonçalves et al., 2007;Munin, 2008;Teixeira et al., 2009).Given that some bat species or bat assemblages require pristine habitat conditions while others are opportunistic, taking advantage of some disturbance, the group should be more studied as an indicator of levels of change in the natural environment.Drastic human alteration in natural habitats may result in simplifying bat diversity and assemblage, since those species which require more specific items in feeding strategy tend to disappear, while those with a wide spectrum of feeding habits, such as insectivore-omnivore and frugivore-omnivore, are generally less affected by environmental changes.
Effects of forest fragmentation on frugivore and nectarivore species have been pointed out in French Guiana (Cossons, 1999).The role of frugivorous bats has been emphasised in tropical forest succession (Muscarella and Flemming, 2007).Overall, Phyllostomid bats have been identified as indicators of habitat disruption in the Neotropics (Fenton et al., 1992).Work conducted in forest habitats of Paraguay has shown that abundance was highest for Artibeus lituratus in deforested landscapes and for Chrotopterus auritus in forested habitats; in contrast, Artibeus fimbriatus, Carollia perspicillata, Glossophaga soricina, Platyrrhinus lineatus, Pygoderma bilabiatum, and Sturnira lilium attained highest abundance in moderately fragmented forest landscapes.Forest cover, patch size, and patch density frequently were associated with abundance of species (Gorresen and Willig, 2004).
Therefore, our data indicate that bat species richness and assemblages in the Pantanal and its surrounding habitats are still well preserved, and it is hoped that these findings may be useful for constructive lines of biodiversity conservation and management in this important wetland ecosystem.

Bat species as bio-indicator
The Pantanal is undoubtedly an important domain and therefore deserves comprehensive ecosystem studies.Our present information on bat species richness and assemblages, considering such abundant sampling data, contributes to making a more general interpretation of species magnitude for conservation purposes.Bat species, for example, can serve as indicators for habitat quality.Natural habitats of the Pantanal have been disrupted by non-sustainable practices of socio-economic development, mainly by conversion of natural vegetation to pastures for cattle ranching and agriculture (Alho, 2008).Farms have been established in the floodplain and in its surrounding uplands, where much of the natural vegetation has been converted to soybean plantations or to other human activities.Studies concluded that 17% of the Pantanal has been deforested through the use of fire (mainly cerrado patches or "capões de cerrado"), with an annual rate of deforestation of 2.3%; and 63% of the natural vegetation cover of the surrounding plateaus in the Planalto (savanna woodland and semi-deciduous forests) has been destroyed (Harris et al., 2005).Deforestation between1976 and 2008 in the Pantanal floodplain increased 26.5 times (12.14%), compared to 40.97% of deforestation within the Upper Paraguay basin (Silva et al., 2010).
In pastures continuously used for cattle ranching, the dominance of A. planirostris in the bat assemblages is higher than in areas used intermittently by cattle (C.Santos, unpublished data), indicating that cattle ranching may cause a reduction in bat diversity.In addition, fire events seem to promote changes in bat species composition.Artibeus planirostris has been found to be the most abundant bat in both burned and unburned sites in the floodplain; however, after fire, the insectivorous phyllostomine bats increase were provided by Earthwatch Institute, Fundação O Boticário de Proteção à Natureza, Conservation International, Wildlife Conservation Society, and Fundação Neotrópica do Brasil.Some data of this paper are part of the Master's dissertation of Larissa F. Oliveira-Pissini, working under the academic and scientific advice of Professor Cleber Alho at Uniderp.We thank Dr. Silvio Favero -Coordinator of the environmental Master's program of Uniderp -for his support.We would like to emphasise the enormous value of the bat scientific collection constructed by Dr. Valdir Antonio Taddei, and in his honourin memoriam -we dedicate this work.Celina Alho and Susan Casement reviewed the manuscript.

Figure 1 .
Figure 1.Sampling sites in the Pantanal floodplain (triangles) and in the neighbouring Cerrado upland plateaus (black circles), and cities (grey circles) in Mato Grosso do Sul, Brazil.

Figure 2 .
Figure 2. Rarefaction curves for bats sampled in 19 sites in the Pantanal floodplain (a), and in 16 sites in the surrounding upland plateaus (b), in Mato Grosso do Sul, Brazil.The upper curve refers to all these 35 sites assembled (c).

Figure 3 .
Figure 3. Richness of bats according to feeding niche, based on 9,037 individuals examined belonging to 56 species, in the Pantanal floodplain and in its neighbouring upland plateaus, Mato Grosso do Sul, Brazil.Light grey bars indicate species exclusive to the floodplain, grey bars species only found in plateau, and dark grey bars those occurring in both floodplain and plateau.

Figure 4 .
Figure 4. Rank abundance distribution of 56 species of bats in a) the Pantanal floodplain and b) its surrounding upland plateaus in Mato Grosso do Sul, Brazil.Asterisks indicate species which were recorded in both the floodplain and uplands.

Figure 5 .
Figure5.Distribution of the bat species in three major habitats in Mato Grosso do Sul, Brazil.SAV: savanna or Cerrado; AA: disturbed areas near ranches and other human occupation; and ATE: the ecotone zone between the floodplain and the upland "planalto", covered by semi-deciduous forest.

Table 1 .
Number of surveyed individuals from 1995 to 2007 and feeding niche of 56 bat species in the Pantanal floodplain and its surrounding upland plateaus, Mato Grosso do Sul, Brazil.
habitats: Cerrado, disturbed habitats and semi-deciduous forest of plateaus.On the other hand, 24 rare species were detected, such as Chiroderma doriae, Chrotopterus auritus, and Artibeus lituratus (Table1).Chiroderma doriae is a species which requires habitat integrity and so and Molossus molossus (n = 155).In disturbed areas, near the houses of cattle ranchers, the common species are: Carollia perspicillata (n = 129), Molossus molossus (n = 125) and Artibeus planirostris (n = 97).Figure5shows the distribution of the species within three major kinds of