Medium to large size mammals of southern Serra do Amolar , Mato Grosso do Sul , Brazilian Pantanal

is critical since it is the basis for improving integrated management of the entire biome. Regarding mammal biodiversity, several inventories conducted since the 1980s have identified a total of 174 species in the Brazilian Pantanal (Schaller 1983; Alho et al. 1987; Rodrigues et al. 2002; Trolle 2003; Alho 2008; Alho et al. 2011). In a recent update, Carmignotto et al. (2012) asserted that 79 species of mammals are shared between Cerrado, Caatinga, Amazonian and Atlantic rainforest. Faunal or floral endemism is virtually absent in the Pantanal (Harris et al. 2005; Junk et al. 2006). Although mammal occurrence and distribution in the Pantanal is considered poorly documented (Rodrigues et al. 2002; Trolle 2003; Junk et al. 2006; Desbiez et al. 2010), there is a consensus that this biome serves as a refuge for the largest populations of several threatened and endangered species, such as the marsh deer Blastocerus dichotomus (Illiger, 1815), the giant otter Pteronura brasiliensis (Gmelin, 1788), the giant anteater Myrmecophaga tridactyla (Linnaeus, 1758), the jaguar Panthera onca (Linnaeus, 1758), the giant armadillo Priodontes maximus (Kerr, 1792), and many others as pointed out by Harris et al. (2005) in their appraisal of Pantanal diversity. Considering this point, increased knowledge on the distributions of mammals and their conservation status in the Pantanal can contribute to the improvement of conservation strategies for these species, since the biome is currently facing changes in its landscape (Desbiez et al. 2009a; Desbiez et al. 2010). Thus, the goal of this study is to provide a list of mediumand large-sized mammals found in southern Serra do Amolar, situated in the Pantanal of Brazil, and to assess capture rates based on camera trapping surveys. Introduction The Pantanal is one of the largest continuous wetlands of the world and it covers around 210,000 km2 (Mittermeier et al. 2002) in Brazil, Bolivia and Paraguay. This biome is known for its unique abundance of wildlife (Trolle 2003), which results from seasonal changes in feeding and reproductive niches (Alho 2008; Alho et al. 2011). Despite this fact, the mammalian fauna of the Pantanal is still poorly known (Rodrigues et al. 2002; Desbiez et al. 2010). The threats to the biome are increasing, mainly due to changes in cattle production in the floodplains (particularly through the use of more nutritious pasture) and agriculture on the plateau, both leading to an increase in deforestation and loss of natural habitat (Desbiez et al. 2009a; Desbiez et al. 2009b; Alho and Sabino 2011). Since the early 1970s, ranchers have been clearing land, mainly through the use of fire, and planting pastures of exotic grasses to improve the carrying capacity for livestock (Desbiez et al. 2011). Approximately 17% of the Pantanal has been deforested through the use of fire (Allho 2008) and private ranches, whose main economic activity is beef production, occupy approximately 95% of the Brazilian Pantanal (Harris et al. 2005). Other threats are caused by non-sustainable practices of socio-economic development, such as illegal fishing and hunting, unplanned tourism, and pollution by pesticides, leading to a progressive deterioration of natural habitats (Alho 2008; Alho and Sabino 2011). Within the vulnerability scenario of the Pantanal (Harris et al. 2005; Alho and Sabino 2011), species surveys and inventories provide the essential baseline data for monitoring impacts on wildlife, caused by factors such as habitat conversion and climate change, and for determining conservation priorities (Tobler et al. 2008). In this context, knowledge of the biodiversity of the region Abstract: Serra do Amolar (Amolar Mountain Ridge) is considered a Priority Area for biodiversity conservation in the Pantanal biome according to the Environmental Ministry of Brazil. Despite this fact, it is a little-studied area, lacking basic information such as species inventories. In this study, we provide a list of the mediumto large-sized mammals that inhabit the southern Serra do Amolar. We carried out a survey at Engenheiro Eliezer Batista Private Natural Heritage Reserve and Santa Tereza ranch from March 2009 to May 2013. We used non-invasive methods to generate a list of 33 mammal species from 18 families, including Endangered species such as the giant otter (Pteronura brasiliensis), Vulnerable species such as the lowland tapir (Tapirus terrestris), and Near Threatened species such as the jaguar (Panthera onca), highlighting the importance of this area for mammal conservation in a regional context. 1 University of Aveiro, Biology Department and CESAM – Centro de Estudos do Ambiente e do Mar. 3810-193. Aveiro, Portugal. 2 Instituto Homem Pantaneiro, Environmental Department. Comendador Domingos Sahib Street 300. CEP79300-130. Corumbá, MS, Brasil. 3 University of York, Environment Department. YO10 5DD. Heslington, United Kingdom. * Corresponding author. E-mail: grasi_porfirio@hotmail.com Grasiela Porfirio 1,2*, Pedro Sarmento 1, Nilson Lino Xavier Filho 2, Joana Cruz 3 and Carlos Fonseca 1 Medium to large size mammals of southern Serra do Amolar, Mato Grosso do Sul, Brazilian Pantanal


Introduction
The Pantanal is one of the largest continuous wetlands of the world and it covers around 210,000 km2 (Mittermeier et al. 2002) in Brazil, Bolivia and Paraguay.This biome is known for its unique abundance of wildlife (Trolle 2003), which results from seasonal changes in feeding and reproductive niches (Alho 2008;Alho et al. 2011).Despite this fact, the mammalian fauna of the Pantanal is still poorly known (Rodrigues et al. 2002;Desbiez et al. 2010).The threats to the biome are increasing, mainly due to changes in cattle production in the floodplains (particularly through the use of more nutritious pasture) and agriculture on the plateau, both leading to an increase in deforestation and loss of natural habitat (Desbiez et al. 2009a;Desbiez et al. 2009b;Alho and Sabino 2011).Since the early 1970s, ranchers have been clearing land, mainly through the use of fire, and planting pastures of exotic grasses to improve the carrying capacity for livestock (Desbiez et al. 2011).Approximately 17% of the Pantanal has been deforested through the use of fire (Allho 2008) and private ranches, whose main economic activity is beef production, occupy approximately 95% of the Brazilian Pantanal (Harris et al. 2005).Other threats are caused by non-sustainable practices of socio-economic development, such as illegal fishing and hunting, unplanned tourism, and pollution by pesticides, leading to a progressive deterioration of natural habitats (Alho 2008;Alho and Sabino 2011).
Within the vulnerability scenario of the Pantanal (Harris et al. 2005;Alho and Sabino 2011), species surveys and inventories provide the essential baseline data for monitoring impacts on wildlife, caused by factors such as habitat conversion and climate change, and for determining conservation priorities (Tobler et al. 2008).In this context, knowledge of the biodiversity of the region Abstract: Serra do Amolar (Amolar Mountain Ridge) is considered a Priority Area for biodiversity conservation in the Pantanal biome according to the Environmental Ministry of Brazil.Despite this fact, it is a little-studied area, lacking basic information such as species inventories.In this study, we provide a list of the medium-to large-sized mammals that inhabit the southern Serra do Amolar.We carried out a survey at Engenheiro Eliezer Batista Private Natural Heritage Reserve and Santa Tereza ranch from March 2009 to May 2013.We used non-invasive methods to generate a list of 33 mammal species from 18 families, including Endangered species such as the giant otter (Pteronura brasiliensis), Vulnerable species such as the lowland tapir (Tapirus terrestris), and Near Threatened species such as the jaguar (Panthera onca), highlighting the importance of this area for mammal conservation in a regional context.

Materials and Methods
The study was carried out at Serra do Amolar region on Santa Tereza ranch (18°18′38″ S, 57°30′10″ W) and Engenheiro Eliezer Batista Private Natural Heritage Reserve (18°05′25″ S, 57°28′24″ W).Both properties are situated in the state of Mato Grosso do Sul, approximately 180 km north of Corumbá in the Upper Paraguay Basin, limited to the west by the Bolivian border and to the east by the Pantanal floodplains (Figure 1).Although considered one of the largest floodplains in the world, the Pantanal also has mountainous areas such as the Urucum Massif and Amolar Mountain Ridge (Silva et al. 2000).The highest point is Amolar peak at an altitude of 1000 m.This Precambrian massif establishes an abrupt ecotone with the seasonally flooded plains of the Brazilian Pantanal (Junk et al. 2006), working as a geological control of the water drainage.The climate of the Upper Paraguay Basin (APB) is considered seasonal and as tropical savannah (AW) according to the Köppen classification (Cadavid-Garcia 1984), with a hot and humid climate in the summer, a dry and cold climate during the winter, and an annual average precipitation of 1,300 mm (PCBAP 1997).The predominant vegetation of the Serra do Amolar region is composed of gallery forest and riparian forest along watercourses and the Paraguai River, dry and humid savannahs, seasonal deciduous forest and seasonal semi-deciduous forest, and occasional rocky fields (approximately 1%) (Sá Arruda et al. 2012;Carmignotto et al. 2012).
The first area surveyed was Engenheiro Eliezer Batista Private Natural Heritage Reserve (EEB), covering a total area of 20,268 ha.The EEB protected area was created in 2008 by means of a private initiative to enhance the conservation efforts of the Pantanal Matogrossense National Park.The EEB protected area is shaped by mountains, swamps and seasonally flooded grasslands.The flood-prone area is comprised of water bodies that represent 58% of the EEB PNHR.A Private Natural Heritage Reserve is a category of protected area established by the Brazilian Federal Decree N o .98914 of 1990, and updated by Decree N o .1992 of 1996, where citizens voluntarily engage in the process of effective protection of representative Brazilian ecosystems.
Santa Tereza ranch, the second site surveyed, is in an area contiguous with EEB, and covers 63,000 ha, of which only 3% is used for cattle ranching.No other economic activity is carried out on the ranch.The forest remnants occupy an area surrounding the Baía Vermelha, one of the largest lakes of the Paraguay River basin (Calheiros and Ferreira 1997).
Four traditional communities (Castelo, Paraguai Mirim, Amolar and Barra do São Lourenço), with approximately 400 people, are settled in the neighborhood of the study site, and their main economic activities are associated with fishing and small-scale cattle production.Subsistence hunting is reported by some locals, and is directed at species such as capybaras Hydrochoeris hydrochaeris (Linnaeus, 1766), caimans Caiman yacare (Daudin, 1802), and peccaries Pecari tajacu (Linnaeus, 1758).

Data collection
The  (Silveira et al. 2003;Trolle 2003;Lyra-Jorge et al. 2008).Camera trapping was the main method employed, with the other methods complementing the species list.
Paths, dirt roads, sand banks and watercourse margins were followed during phases I and II in order to record the presence of mammals based on track census and direct observations -this latter particularly for arboreal species at Engenheiro Eliezer Batista Protected Area.Tracks were identified based on Lima-Borges and Tomas (2004).In the other phases, several camera trapping surveys were carried out at Engenheiro Eliezer Batista Protected Area and Santa Tereza ranch (Table 1).The cameras were installed in different habitats, such as gallery forests, savannahs, and deciduous and semi-deciduous forests.All cameras were programmed to operate continuously (24 h/day) and to take pictures at an interval of 30 seconds for the digital models (Bushnell Trophy Cam and Panthera Camera Trap V4), and intervals of five minutes for the analogical equipment (Tigrinus Conventional 6C).The geographic coordinates of camera traps, photographic captures, presence signs, and observations were recorded using a GPS navigator.
Camera trap sampling effort was determined by multiplying the number of camera traps by the number of sampling days (1d=24 hours), as seen in Srbek- Araujo and Chiarello (2005).Food scraps and cat urine were used to attract the animals.Camera trap records were identified according to Lima-Borges and Tomas (2004) and by drawings in Eisenberg and Redford (1999).Nomenclature followed Wilson and Reeder (2005).
To estimate the relative abundance of the terrestrial mammals, we used the Relative Abundance Index (RAI) (Carbone et al. 2001), which is calculated using the number of independent pictures from each species divided by the sampling effort.We used an interval of 24 h between pictures of the same species to guarantee independence between them (Tobler et al. 2008).A species accumulation curve was obtained through randomizations (with 1000 runs) of different sized samples using the software R version 2.15.3.We treated each survey day as a sample, following Tobler et al. (2008).

Results
With a total sampling effort for track census and direct observations equivalent to 378.5 km over 45 field days, and a camera trapping sampling effort of 11,414 cameradays (Table 1), we recorded 33 species from 18 families (Table 2 and Figures 2 and 3).Carnivora was the richest mammalian order in our inventory (Table 2).

Discussion
One of the first inventories in the Pantanal that included a broad multi-taxa sampling effort was conducted by Schaller (1983) on the Acurizal Ranch, which identified 64 species, of which 43 were non-flying mammals.In the Nhecolândia sub-region of the Pantanal, Alho et al. (1987) identified 33 mammal species, excluding bats, while Desbiez et al. (2010)  In this study, we recorded 33 of the 43 non-flying mammal species believed to inhabit the region of our study area according to Schaller (1983).In fact, we recorded similar species to those observed by that author on Acurizal Ranch, which is located 30 km north of our study area in the northern side of Amolar Mountain Ridge.Although we used multiple methods to generate our inventory, we did not register some species observed by Schaller (1983), such as the maned wolf Chrysocyon brachyurus (Illiger, 1815), and some arboreal species such as the prehensile-tailed porcupine Coendou prehensilis (Linnaeus, 1758).Schaller's study was carried out at the end of 1970s and, by that time, these species were already considered extremely rare or difficult to detect (Schaller 1983).
The differences concerning RAIs seem to reflect the behavior and abundance of the terrestrial species.Clearly, the placement of the camera traps near the ground, and the sensitivity of the sensor biased our results in favor of medium-to large-sized ground-dwelling mammals, especially those species that frequently use roads, where camera traps were preferentially installed (Harmsen et al. 2010).That said, we did capture some small mammal species with this method, such as Thrichomys pachyurus (Wagner, 1845) and Philander opossum (Linnaeus, 1758) which has two spots over the eyes, a prehensile tail with less than 20% of the basal portion covered with fur, the rest of which is naked, black in 2/3 basal portion and discolored in 1/3 distal portion as described in Rossi and Bianconi (2011) (Figure 3).Since different species have different probabilities of being detected by camera traps due to distinct behavioral traits, it is important to emphasize that this index is an estimation of species abundance relative to the abundance of all other species identified by the method, and cannot be used as a population size estimator (Walker et al. 2000;Eduardo and Passamani 2009).The dense vegetation and the flooded fields restricted our movements while surveying the area and, due to these difficulties, we consider these results only as a rough estimate.We agree with Sberk-Araujo and Chiarello (2005) that camera traps are a relatively practical and non-intrusive method, especially for surveying nocturnal, rare and cryptic mammals.Although some expected species were not recorded by the camera traps, our species accumulation curve showed an asymptotic tendency, demonstrating that we succeeded in recording the vast majority of the medium-to large-  sized ground-dwelling mammals that are expected for the area, only missing those that might be extinct in the area, that occur in low population densities or those that the methodology was unlikely to capture (Voss and Emmons 1996).
Several threatened species inhabit EEB PHNR and Santa Tereza ranch.Among them, we recorded Endangered species such as the giant otter, which according to Schaller (1983) was considered virtually exterminated in the area due to intensive hunting; Vulnerable species such as the lowland tapir, the marsh deer, and the giant armadillo, with the first camera trapping record for this latter species reported for Serra do Amolar at Engenheiro Eliezer Batista Protected Area in 2012 (Porfirio et al. 2012), and Near Threatened species such as the jaguar.In Brazil, the persecution of jaguars, as well as other wildlife species, is illegal, but there are still cases of jaguars being shot in an attempt to minimize the damage caused by livestock predation (Marchini and Macdonald 2012).Human occupancy around the reserve is primarily by traditional communities that focus on fishing activities, but there are also small-scale cattle-raising systems.Hence, a single cattle depredation event by a native predator is treated as a significant loss that can lead to negative perceptions and attitudes towards these animals.So, in this context, it is quite important to gather all possible data on jaguar presence and abundance in order to apply consistent measures that can minimize these losses.
The white-lipped peccary Tayassu pecari (Link, 1795), which is one of the most important prey of the jaguar (Taber et al. 1997;Weckel et al. 2006) and is a Vulnerable species (IUCN 2013), was recorded only once by camera trap in May 2013, although a medium-sized group of approximately 20 individuals was observed in November 2006 at Santa Tereza ranch (GP, personal observation).The white-lipped peccary is a widespread fruit-eating mammal in Neotropical rainforests (Bodmer 1990), which strongly associates with forested areas (Desbiez et al. 2009b).Although the main threats to the species are related to habitat loss and hunting pressure (Carrillo et al. 2002), we believe that the species may occur in low densities in the study site, as is also the case in the floodplains, because of the unsuitability of the study area habitat.In another study area in the central Pantanal, Desbiez et al. (2009a) found that white-lipped peccary densities were higher in forested landscapes when compared to the floodplain, where the species was rarely sighted.
The southern three-banded armadillo Tolypeutes matacus (Desmarest, 1804), another Near Threatened species found in our inventory, had already been recorded in the Serra do Amolar (Schaller 1983) and in the Pantanal of Nhecolândia (Alho et al. 1987).This species is distributed from southeastern Bolivia and Mato Grosso, Brazil, through the Paraguayan Chaco to the Province of Buenos Aires in Argentina (Wetzell 1985).Considered an opportunistic insectivore (Bolkovic et al. 1995), this species is probably facing a significant decline due to widespread habitat loss through much of its range, and because of exploitation for food (Abba and Superina 2010).
Considering the lack of information for this region, it is also important to highlight the detection of some species categorized as Data Deficient according to the IUCN Red List (2013), for example: the river otter Lontra longicaudis (Olfers, 1818), the agouti Dasyprocta azarae (Lichtenstein, 1823), and the red brocket deer Mazama americana (Erxleben, 1777).These species have been reported in other inventories carried out in the Pantanal (Trolle 2003;Desbiez et al. 2010) and records such as these are essential for mammal conservation at a regional scale, since the presence or absence of a particular species provides the basic information necessary to assess its ecological requirements.
We recorded four of the six primate species reported for the Pantanal according to Rodrigues et al. (2002) and Melo et al. (2009), and these species seem to exhibit a fragmented distribution, except for Alouatta caraya (Humboldt, 1812), which is typically registered over extensive areas.For example, Mico melanura (É.Geoffroy, 1812), occurs only in small isolated and elevated areas such as Urucum Massif (Vivo, 1991), and there is a considerable lack of information of its status in the Pantanal floodplain (Rodrigues et al. 2002).The remaining primate species seem to be associated with specific vegetation types.For example, Azara's night monkey Aotus azarae (Humboldt, 1811), seems to occur in transitional vegetation zones, and on ridges (Rodrigues et al. 2002;Cáceres et al. 2008).Although Aotus azarae is typically nocturnal (Fernandez-Duque and Erkert 2006), it was twice seen during the day in the EEB PNHR.According to Schaller (1983), this species also occasionally calls in the daytime, and Fernandez-Duque and Erkert (2006) found that this species may be more active during the day if unfavorable lightning or temperature conditions prevail during the night.Callicebus pallescens (Thomas, 1907) was identified through direct observation and vocalization.According to Hershkovitz (1990), C. pallescens occurs within the study area, but there is little information about this primate species for the Pantanal overall, and Tomas et al. (2010) has challenged the validity of this species' taxonomic rank.
Deer are represented by four species in the Pantanal: Blastocerus dichotomus, Mazama americana, Mazama gouazoubira and Ozotoceros bezoarticus (Linnaeus, 1758).The first species is associated with marshy and flooded areas, while species from the genus Mazama can be found over the entire floodplain.Ozotoceros bezoarticus, which was not recorded in this study, mainly inhabit field areas (Rodrigues et al. 2002) and, since little of this habitat type is found within the reserve, this could probably explain the absence of the species from our inventory.
The richness of carnivores found in our study site followed a pattern close to that observed in other mammal studies carried out in the Pantanal (Trolle 2003;Desbiez et al. 2010).We registered 50% of the carnivore species that occur in the Pantanal according to Alho et al. (2011).
The presence of such a high number of species suggests that the study area presents sufficient habitat integrity and abundant prey, the most important ecological requirements for carnivores (Pierce et al. 2000).
The importance of the EEB PNHR and Santa Tereza ranch for the conservation of biodiversity is based not only on the presence of endangered and threatened species, but also on the diversity of habitats as a result of the influence of neighboring biomes such as the Chaco, Amazon Forest and Cerrado.Additionally, the EEB PNHR and Santa Tereza ranch are located in a strategic geographical position, i.e. in the corridor formed by the Pantanal Matogrossense National Park and four other Private Natural Heritage Reserves that together comprise the Network for Protection and Conservation of the Serra do Amolar ("Rede de Proteção e Conservação da Serra do Amolar"), a multi-organizational conservation framework for the Serra do Amolar that legally protects 209,000 hectares of Pantanal biome (Bertassoni et al. 2012).Furthermore, our study applies the recommendations of the Environment Ministry of Brazil (MMA 2007) to establish, as a priority, biodiversity inventories for the Serra do Amolar region, since it is classified as an area of extremely high importance for conservation.The results obtained from this study reveal the need to concentrate conservation initiatives in this region, both in public and private areas, since it plays an important role as a refuge for the mammalian fauna in the western floodplains of the Pantanal.

Figure 1 .
Figure 1.Map of the study site located at the Engenheiro Eliezer Batista Private Natural Heritage Reserve, and Santa Tereza ranch, Pantanal of Brazil.

Figure 5 .
Figure 5. Index of Relative Abundance (RAI) obtained by the number of records of each mammal species registered by camera trapping at the Engenheiro Eliezer Batista Private Natural Heritage Reserve and the Santa Tereza Ranch (Amolar Mountain Ridge, Pantanal of Brazil), carried out from August 2011 to May 2013.

Figure 6 .
Figure 6.Species accumulation curve obtained through randomizations (with 1000 runs) considering the camera trapping surveys carried out at the Engenheiro Eliezer Batista Private Natural Heritage Reserve and the Santa Tereza ranch (Amolar Mountain Ridge, Pantanal of Brazil), from August 2011 to May 2013.

Table 1 .
(Alho 2008)et al. 2002)arge-sized mammal species in the same area asAlho et al. (1987)Data from camera trapping campaigns carried out in Engenheiro Eliezer Batista Private Natural Heritage Reserve, and Santa Tereza ranch from August 2011 to May 2013.throughdirectobservations,evidence from tracks or fresh burrows.In the southeastern part of the Pantanal,Trolle (2003)recorded 30 species of medium-to largesized mammals, whileRodrigues et al. (2002)recorded 93 species for the entire floodplain.The PCBAP (Plano de Conservação da Bacia do Alto Paraguai -Conservation Plan for the Upper Paraguay River Basin -Brasil 1997) also provides one of the most complete lists that have been published for the mammals that inhabit the region, listing 75 species, and acts as a reference for the Pantanal region(Rodrigues et al. 2002).Until recently, it was believed that 132 mammal species occurred in the Pantanal(Alho 2008).However, in a recente up date,Alho et al. (2011)cited 174 mammal species inhabiting the Brazilian Pantanal.

Table 2 .
List of species, common name, habitat type, conservation status according toIUCN Red List (2013), and type of record of mammals identified in Engenheiro Eliezer Batista Private Natural Heritage Reserve and Santa Tereza ranch between March 2010 and May 2013.GF= Gallery Forest, RF= Riparian Forest, DS= Dry Savannah, HS= Humid Savannah, SDF= Seasonal Deciduous Forest, SSF= Seasonal Semi-deciduous Forest, RF= Rocky Field, R=River, T= Tracks, CT= Camera trap, DO= Direct Observation, B= Burrow, LC= Least Concern, DD= Data Deficient, V= Vulnerable, NT = Near Threatened, E=Endangered.