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Medium- and large-sized mammals in a steppic savanna area of the Brazilian Pampa: survey and conservation issues of a poorly known fauna/Mamiferos de medio e grande porte em uma area de savana estepica do Pampa Brasileiro: levantamento e questoes de conservacao sobre uma fauna pouco conhecida.

1. Introduction

Biomes are regions that can be distinguished by their geography, climate, and associated flora and fauna (Campbell, 1996). In southern South America, there is a biome known as the Pampa, which is a fitophysiognomic formation characterized by grasslands with sparse shrub and tree formations (Berreta, 2001). The Pampa occupies an area of approximately 700,000 [km.sup.2] in Argentina, Brazil and Uruguay (Bilenca and Minarro, 2004). In southern Brazil, the Pampa biome is located between latitudes 28[degrees] 00' S and 34[degrees] 00' S and longitudes 49[degrees] 30' W and 58[degrees] 00' W (IBGE, 2004), and covers approximately 176,000 [km.sup.2], corresponding to 2.1% of the area of the country (Collares, 2006). The Brazilian Pampa is home to a total of 83 native mammal species with potential occurrence, 12 of which are endemic to this biome, and 35 of which are mammals of medium and large size (Paglia et al., 2012). The Brazilian Pampa is the third largest biome in Brazil in terms of the percentage of endangered mammal species, approximately 13% (Costa et al., 2005), and over time, it has been profoundly modified by human activities, often leaving only small remnants of native fields (Porto, 2002). Recently, the Pampa has seen the expansion of soybean cultivation and the conversion of grasslands areas into extensive areas of silviculture (mainly Pinus spp. and Eucalyptus spp.), for the purpose of producing cellulose and wood (Verdum, 2006; Binkowski, 2009). Approximately 51% of the original grassland vegetation has been devastated as a result of human economic activities (Hasenack, 2006).

Although the northern portion of the Pampa biome, which is located in southern Brazil in the state of Rio Grande do Sul, potentially has a large number of endangered species of medium- and large-sized mammals (Fontana et al., 2003), basic information on the occurrence of this fauna is lacking, and few species surveys have been conducted in the southern portion of this state. The studies of medium- and large-sized mammals in the state of Rio Grande do Sul that have been conducted to date have involved mainly the forested areas of the northern (Wallauer and Albuquerque, 1986; Marques and Ramos, 2001; Santos et al., 2004; Kasper et al., 2007a; Marques, 2013) and central parts of the state (Kasper et al., 2007b; Santos et al., 2008). Most of these areas are characterized as forest formation areas (Atlantic forest and Araucaria moist forest). In the southern portion of the state, which is characterized by an open fitophysiognomic formation (Vieira, 1983), the few survey studies of this fauna have been conducted in the region of the coastal plain (Gianuca, 1997, 1998; Oliveira et al., 2013). Therefore, there is still a large gap in the information available on the occurrence of medium- and large-sized mammals in the Brazilian Pampa. Thus, surveys and biological inventories in previously unexplored areas will contribute to further research and to the elaboration of strategies and new measures for the conservation of medium- and large-sized mammals in the Brazil's wildlife.

The purpose of this study was to contribute to the conservation of medium- and large-sized mammals in the Brazilian Pampa by identifying the species present in the studied steppic area, aiming to contribute to the knowledge of the mammalian fauna of this biome, updating information on species with conservation issues in an area under anthropic influence.

2. Material and Methods

2.1. Study area

This study was conducted in two gallery forest fragments located in a micro-basin of the Ibicui River in southern Brazil, between the coordinates 29[degrees] 43' 27" S, 54[degrees] 50' 15" W and 29[degrees] 47' 29" S, 54[degrees] 45' 58" W (Espinosa, 2011). The total area of the micro-basin is approximately 3116.33 hectares, and the total study area (the sum of the two forest fragments) was 164 hectares (Figure 1). Fragment A, with an area of 116 hectares, and fragment B, with an area of 48 hectares, are both set in a matrix of native grassland used for agricultural and cattle-raising activities. The studied area is located in a steppic savanna physiographic region, based on the distribution of trees (UFSM, 2007).

According to the classification system of the Brazilian National Institute of Geography and Statistics (IBGE, 2004), the Brazilian Pampa consists of a vegetated coastal belt and a savanna environment that dominates the entire western part of the biome (Leite and Klein, 1990). Dense forest formations are not common in the Pampa biome; grasslands dominate the landscape. The main forest formations are found at the northern limit of the biome, in the transition area to Atlantic rain forest. In other regions, plant formations with trees exist mainly as gallery forests, shrub forests and islands of trees within the grassland (Overbeck et al., 2006).

2.2. Methods

The sampling of medium- and large-sized mammals was conducted over a period of 16 months, from May 2009 to October 2010, except during the months of February and March 2010, when the sampling was interrupted due to heavy rain that made the use of the survey equipment impossible. We used a camera trapping method exclusively. Camera trapping has been proven as a highly efficient method at recording Neotropical mammals (Trolle and Emmons, 2004; Sanderson and Trolle, 2005; Kasper et al., 2007a; Srbek-Araujo and Chiarello, 2008; Carvalho et al., 2013).

A total of 112 points, 51 in fragment A and 61 in fragment B, were sampled. Each month, a total of 10 camera traps (each one representing a sampling point) were used for 15 uninterrupted days. The minimum distance between the sampling points was 150 meters. After each 15-day sampling period, the traps were reviewed and relocated. The traps were placed along trails in water bodies or in places that exhibited traces of the presence of medium- and large-sized mammals (feces, fur or footprints). The sampling was carried out within these areas of woody vegetation because these sites are used as refuges for medium- and large-sized species.

The relative frequencies of the species in the region were calculated as i/N, where i = the number of species records I and N = the total number of species records (Crooks, 2002). We treated each record as an independent sample. The relative frequencies were expressed as percentages.

[FIGURE 1 OMITTED]

3. Results

We obtained a total of 341 photographic records of 17 medium- and large-sized mammal species belonging to seven orders and 11 families: Artiodactyla (Cervidae), Carnivora (Canidae, Procyonidae, Mephitidae and Felidae), Cingulata (Dasypodidae), Didelphimorphia (Didelphidae), Lagomorpha (Leporidae), Pilosa (Myrmecophagidae) and Rodentia (Caviidae and Cuniculidae) (Paglia et al., 2012). In addition, we directly observed the species Alouatta caraya (Humboldt, 1812) (Primates, Atelidae), adding the total 18 medium- and large-sized mammal species registered for the area, belonging to eight orders and 12 families. The order Carnivora was the most representative, with four families and eight species registered, followed by the order Cingulata, with one family and three species, and the order Rodentia, with two families and two species (Table 1).

The species Mazama gouazoubira (G. Fischer [von Waldheim], 1814) presented the highest occurrence frequency in the study area, with 21.11% of the total records. The second most frequently occurring species was Cerdocyon thous (Linnaeus, 1766) (19.35%), followed by Dasypus novemcinctus Linnaeus, 1758 (13.78%), Lycalopex gymnocercus (G. Fischer, 1814) (11.14%), Leopardus wiedii (Schinz, 1821) (7.92%), Conepatus chinga (Molina, 1782) (6.16%), Euphractus sexcinctus (Linnaeus, 1758) (4.69%), Dasypus hybridus (Desmarest, 1804) (4.40%), Cuniculuspaca (Linnaeus 1766) (2.64%), Procyon cancrivorus (G.[Baron] Cuvier, 1798) (2.35%), Tamandua tetradactyla (Linnaeus, 1758) (1.76%), Puma yagouaroundi (E. Geoffroy Saint-Hilaire, 1803) (1.47%), Hydrochaerus hydrochaeris (Linnaeus, 1766) (0.88%), Leopardus geoffroyi (d'Orbigny & Gervais, 1844) (0.88%), Leopardus colocolo (Molina, 1782) (0.59%), Lepus europaeus Pallas, 1778 (0.59%) and Didelphis albiventris Lund, 1840 (0.29%) (Figure 2).

4. Discussion

We registered a total of 18 species of mammals of medium and large size, and among them, eight (45%) are threatened with extinction in the state of Rio Grande do Sul (Fontana et al., 2003), two are listed as "endangered", and six are listed as "vulnerable". In this context, the importance of the studied area and of the natural fragments present in this region to the conservation of these mammals in this biome is clear.

We found four species to be exceptionally common in the area: M. gouazoubira, C. thous, D. novemcictus and L. gymnocercus. Another four species were apparently relatively common: L. wiedii, C. chinga, E. sexcinctus and D. hybridus. On the other hand, a number of species seem to occur at relatively low frequencies: C. paca, P. cancrivorus, T. tetradactyla, P yagouaroundi, H. hydrochaeris, L. geoffroyi, L. colocolo, L. europaeus and D. albiventris.

[FIGURE 2 OMITTED]

The most commonly observed species in the study area (M. gouazoubira, C. thous, D. novemcintus and L. gymnocercus) exhibited the highest occurrence frequencies, most likely because the camera traps might have recorded the same individuals, although we treated each "capture" as an independent sample. In addition, it is known that many mammals, such as species of the genera Mazama (Erxleben, 1777) have the habit of preferring to move on pre-existing trails (Tomas and Miranda, 2003), and as these trails were the focus of our sample, such mammals could have been overanalyzed.

The relatively common species, such as C. chinga, inhabit mainly open areas and were found even in densely urbanized areas, indicating the high degree of adaptation of these species to modified environments (Oliveira et al., 2013). The species E. sexcinctus and D. hybridus were also found in disturbed and open areas (Eisenberg and Redford, 1999), and this environment seems to be favorable for these species. The most common feline species in the area was the margay L. weidii. The margay is more forest-dependent, reaching its greatest abundance in lowland rainforests (Oliveira et al., 2008). According to Kasper et al. (2007a), most felines have the habit of moving over trails and moving long distances. They tend to be commonly recorded in camera traps, although their density is always considerably lower than the densities of others species referred here as being relatively common in the area. The presence of the margay reflects the importance of natural fragments of the Pampa landscape, because they shelter more forest-dependent species such as this.

Among the species listed, those that were present at low frequencies were noted. The occurrence of carnivores, such as P. yagouaroundi and L. geoffroyi, whose populations have declined in the state due to the loss of natural habitats (Indrusiak and Eizirik, 2003), demonstrates the regional importance of the study area. In addition, the low occurrence frequency of T. tetradactyla may reflect the low carrying capacity of the area for the species. Despite its use of the arboreal stratum, the species is commonly photographed on the ground in other locations and ecosystems (Oliveira et al., 2007). The low percentage of recordings of L. colocolo compared to the other species suggests that they are not common in the study area. It should also be noted that L. colocolo is considered a rare species: it is found over a wide geographic range, is a habitat specialist, and occurs at low population densities. The pampas regions of Argentina and Uruguay, like our study area, have been heavily settled and grazed, which is suspected to have had a negative impact on pampas cat populations (Garman, 1997; IUCN, 2013).

The species C. paca, P. cancrivorus, H. hydrochaeris and L. europaeus were also observed at low frequencies. Cuniculuspaca is locally listed as an endangered species (Fontana et al., 2003). Some surveys report disturbing signs of decline of the species population due to extensive hunting and habitat loss (Queirolo et al., 2008; Huanca-Hurachi et al., 2011). The species P. cancrivorus is naturally rare in some areas of its range and does not seem as adaptable to human activity, although it is considered stable throughout South America (Glatston, 1994). The rodent H. hydrochaeris occurs only in habitats close to water, including areas along rivers and streams (Eisenberg and Redford, 1999), and is generally more often found in anthropized places (Dias and Mikich, 2006; Negrao and Valladares-Padua, 2006; Kasper et al., 2007a; Pires and Cademartori, 2012). This rodent is very common in the region, but few individuals were recorded in our survey, because there is a dam located adjacent to our study area, where the individuals are concentrated. The only exotic species found in the region was L. europaeus, which is considered an invasive species that occupies open areas and pastures and is considered an agricultural pest in several countries in South America (Jaksic et al., 2002; Reis et al., 2011; Oliveira et al., 2013). The low frequency of occurrence of the species is due to our sample being focused on forested areas, while this species prefers to inhabit fields.

The richness and composition of medium- and large-sized mammals found in this area of the Pampa, with a predominance of generalist species and less frequent recordings of rare and specialist species, suggest that the area is in a medium state of conservation. Despite the human influence, we can affirm that natural forest remnants present within the Pampa may play an important role in the conservation of medium- and large-sized mammals, most likely because these natural forest fragments can provide food resources and shelter for such species. However, these two remnants by themselves may not be able to maintain the mammalian fauna in the region, which requires evaluations on the scale of the full landscape.

Considering that the entire region of the Pampa biome in southern Brazil has been little studied, new species will undoubtedly be recorded. Our results contribute to the knowledge of faunal diversity in the Pampa biome and its associated habitats, warn about threats and provide support for conservation measures. We have proven that many important mammal species survive in the area. However, there is a great need for concern: many species in the region are considered to be rare, and the fragmentation and substitution of natural fields is no doubt the major factor contributing to the rarity of these species, although hunting may also have played a role for certain species. Although a longer-term investigation is needed, these preliminary observations are highly valuable, given that the Pampa biome in Brazil, and in particular the human-influenced areas making up the majority of the region, is so little known.

http://dx.doi.org/10.1590/1519-6984.12714

Acknowledgements

We thank Capes and the CNPq/Brazilian Ministry of Science and Technology. We are grateful to Helinton Welter Keller for support of all of the fieldwork and to Tatiane Campos Trigo for suggestions and for reviewing this manuscript. We also thank the colleagues of the Museu Regional do Alto Uruguai e das Missoes (MuRAU) for their support at various stages of this research. We acknowledge the support of Universidade Regional Integrada do Alto Uruguai e das Missoes--Campus de Erechim.

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C. C. Espinosaa, D. Galiano (a) *, B. B. Kubiak (a) and J. R. Marinho (b)

(a) Programa de Pos-graduacao em Biologia Animal, Universidade Federal do Rio Grande do Sul - UFRGS, Av. Bento Goncalves, 9500, CEP 91501-970, Porto Alegre, RS, Brazil

(b) Programa de Pos-graduacao em Ecologia, Universidade Regional Integrada do Alto Uruguai e das Missoes - URI, Campus de Erechim, Av. Sete de Setembro, 1621, CEP 99700-000, Erechim, RS, Brazil

* e-mail: galiano3@hotmail.com

Received: July 14, 2014--Accepted: November 5, 2014--Distributed: February 29, 2016 (With 2 figures)
Table 1. Medium- and large-sized mammal species registered in a
steppic savanna physiographic region of the Brazilian Pampa,
located in a micro-basin of the Ibicui River in southern Brazil.
The conservation status of each species is given according to
Fontana et al (2003): Vulnerable (VU), Endangered (EN) and not
threatened (-).

Family/Species                  Common name             Conservation
                                                           status

Didelphidae
Didelphis                   White-eared Opossum              --
  albiventris

Dasypodidae
Dasypus                    Nine-banded Armadillo             --
  novemcinctus
Dasypus hybridus       Southern Long-Nosed Armadillo         --
Euphractus                  Six-Banded Armadillo             --
  sexcinctus

Myrmecophagidae
Tamandua                     Southern Tamandua               VU
  tetradactyla

Atelidae
Alouatta caraya         Black-and-gold Howler Monkey         VU

Canidae
Cerdocyon thous               Crab-eating Fox                --
Lycalopex                        Pampas Fox                  --
  gymnocercus

Felidae
Leopardus colocolo               Pampas Cat                  EN
Leopardus geoffroyi            Geoffroy's Cat                VU
Leopardus wiedii                   Margay                    VU
Puma yagouaroundi                Jaguarundi                  VU

Mephitidae
Conepatus chinga          Molina's Hog-nosed Skunk           --

Procyonidae
Procyon cancrivorus         Crab-eating Raccoon              --

Cervidae
Mazama gouazoubira              Gray Brocket                 VU

Cuniculidae
Cuniculus paca                  Spotted Paca                 EN

Caviidae
Hydrochaerus                      Capybara                   --
  hydrochaeris

Leporidae
Lepus europaeus                European Hare                 --
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Article Details
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Title Annotation:Original Article
Author:Espinosa, C.C.; Galiano, D.; Kubiak, B.B.; Marinho, J.R.
Publication:Brazilian Journal of Biology
Article Type:Survey
Date:Feb 1, 2016
Words:4362
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