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Introduction
The Atlantic Forest, one of the most threatened biomes on the planet, contains 298 species of mammals, 90 of which are endemic (Paglia et al. 2012) and 14% threatened under extinction (Chiarello et al. 2008). With approximately 60% of the Brazilian population living in these areas (Pinto et al. 2006), the Atlantic Forest remains under pressure due to urbanization, increasing road network, construction of pipelines, uncontrolled growth of ecotourism (SMA 1999, MMA 2002), hunting and extraction of plant resources (Galetti & Chivers 1995, Dean 1996, Galetti & Fernandez 1998, Cullen et al. 2000). As a consequence, currently less than 11% (16,377,472 ha) of its original vegetation remains, and of these, only 13.8% are legally protected (Ribeiro et al. 2009).
Although threatened and with an urgent need for scientific surveys, biodiversity in few localities of this biome have been investigated, and most often, few groups were targeted for study. In the case of mammals, this scenario is further complicated. Rare are the times in which the group is inventoried as a whole (e.g. Voss & Emmons, 1996), studies with partial sampling being more common. These “partial” studies lacks some methods and/or last just a short time. Mammal surveys tend to adopt the following division, based on animals' habits and different sampling protocols: small terrestrial mammals (e.g. Barros-Battesti et al. 2000, Pardini & Umetsu 2006, Pinto et al. 2009), Bats (e.g. Bianconi et al. 2004, Faria et al. 2006, Luz et al. 2011) and medium and large bodied mammals (e.g. Negrão & Valladares-Pádua 2006, Abreu & Köhler 2009). Exceptions being studies, such as Geise et al. (2004), Cunha & Rajão (2007) and Passamani et al. (2005) that included all non-flying mammals, or even Paglia et al. (2005) and Modesto et al. (2008) that additionally included bats.
The largest set of Atlantic Forest remnants is located in the Serra do Mar, mainly in the state of São Paulo and represents approximately 7% of what remains of the biome (Ribeiro et al. 2009). The Serra do Mar State Park (“Parque Estadual da Serra do Mar” - PESM ) protects an area of 315,000 ha in this region, situated in a highly populated area of São Paulo (ca. 14 million) (Instituto Florestal 2006). Due to its size, the park is managed through eight regional administrative centers that are in different situations with regard to regularization, environmental pressures, conservation status and fiscalization (Instituto Florestal 2006).
Located in the northern portion of PESM the Núcleo Santa Virginia (NSV) is recognized for its high biological diversity, being an active site for important faunal and floristic studies in the state of São Paulo (e.g., Galetti et al. 2009, Rocha-Mendes 2010, Martins 2011, Silva & Tozzi 2013). Among terrestrial vertebrates, some groups that have been locally assessed include birds (Goerck 1999), serpents (Hartmann et al. 2009) and fish (Gomiero & Braga 2006). For mammals, the species list available comes from the Management Plan of the park (Instituto Florestal 2006) and Wang (2002), who described the diets of three spotted cats and listed their preys. With the aim of expanding the knowledge of mammals in this important conservation area, the PESM, and in particular the NSV, this paper presents the results obtained through a combination of field sampling methods applied during the period of 2002-2009 to survey non-flying mammals.
Material and methods
Study area
Núcleo Santa Virginia (NSV - 23°17’ to 23°24’S and 45°03’ to 40°11’W) is an administrative division of the Serra do Mar State Park. NSV covers approximately 17,000 ha, and is located within the municipalities of Cunha, Natividade da Serra, São Luis do Paraitinga and Ubatuba in the State of São Paulo (Figure 1). NSV is situated on a narrow strip of the Atlantic plateau between the coast and the Paraiba valley, forming the Atlantic Plateau Unit (“Unidade Planalto Atlântico”) - of the Upper Paraíba Basin (“Bacia Superior do Paraíba”). The local climate is "coastal humid characteristic of tropical coasts exposed to the Atlantic" with an annual average rainfall of 2,200 mm and seasonal rainfall differences, with the austral autumn and winter periods considered driest. The average temperature ranges from 18 °C to 22 °C (Instituto Florestal 2006).
Figure 1 Location of Núcleo Santa Virgínia, Serra do Mar State Park - east São Paulo State, in the context of Brazil, showing remnants of Atlantic Forest (source: SOS Mata Atlântica 2010). In detail the study sites: Vargem Grande base = circle, Itamambuca base = triangle.
Vegetation cover consists of 60 % dense rainforests and pristine/little changed montane forests, with the remainder a mixture of disturbed areas and plantations of Pinus spp. and Eucalyptus saligna (Tabarelli et al. 1994, Instituto Florestal 2006), the relief is very steep with embedded valleys and straight strands, and the average altitude is 860 meters to 1500 meters (Instituto Florestal 2006). Hunting pressure within NSV ranges from almost nonexistent to moderate (Marques 2004) and it is considered a priority area for PESM biodiversity conservation, due to the floral and faunal importance of the region, with species restricted to the plateau and highly diverse primary vegetation (Instituto Florestal 2006). Most of the mammal sampling effort was concentrated around two research bases: Itamambuca (headquarters - 45°5’16”W/23°19’29”S) - located in the northern portion, bordering Núcleo Cunha and Vargem Grande (headquarters - 45°14’39”W/23°26’16”S) - located in the central portion, bordering Núcleo Picinguaba (Figure 1).
Data collection
Mammal species were recorded through a combination of standardized methods, namely: diurnal and nocturnal line transect census, camera trapping, track-stations, live-traps (Sherman traps of three different sizes [23 x 7.5 x 8.5 cm, 30 x 7.5 x 9.5 cm , and 37.5 x 10 x 12 cm], and Tomahawk traps [45 x 16 x 16 cm]), pitfalls, as well as occasional records and information from third parties.
Sampling of small non-flying mammals - here marsupials and cricetidae and echimyids rodents - was performed with equal effort in both research bases in bimonthly sessions of five capture nights, from September 2008 to September 2009. One hundred and eighty live traps were distributed equally in six sample plots of 0.6 ha (60 x 100 m), three at each base. Each plot consisted of 24 sample locations (20 m equidistant), which randomly received a Sherman trap, and six also received a Tomahawk, totaling 30 traps per plot, always located on the ground. Additionally, twelve lines of pitfall traps were installed, six in each base. Each line consisted of four 60 L plastic buckets separated by 10 m and joined by a plastic screen (approximately 50 cm tall), the lines were paired, equally spaced 30 meters. At the same base, both live trap plots and pitfall line pairs were separated by at least 100 m from the closest plot or line pair.
The live traps, as well as pitfalls were baited with a mix of mashed banana, peanut butter, bacon and ground cornmeal. The marsupials and rodents caught were identified and marked with numbered tags (Ear tags, National Band and Tag Co., Newport, Kentucky, USA) and then released (following guidelines of the American Society of Mammalogists - ASM, Sikes et al. 2011). Due to the difficulty of identifying species using only external characters, some specimens were retained for morphological, cytogenetic and molecular analysis (with specialists’ help), and comparison with reference collections (IBAMA license No. 14428-2). These specimens were submitted as references to the Museu de Zoologia da Universidade de São Paulo (MZUSP), Museu Nacional (MN) and Museu da Universidade Federal do Espírito Santo (UFES). Specimens that had not been deposited yet in these scientific collections are denoted by the initials of the collector: Carolina Lima Neves (CLN) (more information Di-Nizo et al. 2014).
The sampling success of terrestrial small mammals was assessed using species accumulation curves and rarefaction curve (Jackknife 1), both related to the sampling effort in number of traps per night - EstimateS Version 8.2.0 (Copyright R. K. Colwell: http://viceroy.eeb.uconn.edu/estimates) program (Colwell 2009).
The records of other terrestrial mammals took place during two sampling periods, from 2002 to 2005 and then from 2007 to 2009. The methods used were line transects, camera traps and track-stations, along pre-existing trails within NSV (trails: Rio Grande, Rio do Veado, Pau de Bala, Santa Virgínia-Cunha), predominantly close to the research bases of Itamambuca and Vargem Grande, in native vegetation area. Transects were walked (average speed of 1 km/h) throughout the day and timings varied with climatic conditions. The camera traps were placed along the trails and in the forest, where they remained active for seven to 30 consecutive days. Track-stations were used for only three months (August-November 2004) and consisted of sand plots (50 x 50 cm x 3 cm deep), spaced every 100 m along four trails, totaling 59 stations. Each of the track-station trails was evaluated for six to eight times during the sample period.
The sampling effort employed at the end of the study using systematic methods can be seen in Table 1, in addition, other records were collected on an occasional basis over the course of field activities as well as through informal conversations with NSV staff and locals. To compile the species list for the area, basic information from the Parks management plan was also considered (Instituto Florestal 2006). The conservation status of the species in state and national levels followed the information available at: Fauna Ameaçada de Extinção no Estado de São Paulo: Vertebrados (2009), MMA & Fundação Biodiversitas (2008) and Machado et al. (2005).
Results
A total of 58 species of non-flying mammals were recorded at NSV, of which 50 were captured or observed using standardized techniques (present study), six from reports regarding current or historical presence in the area (Chironectes minimus, Callicebus nigrifrons, Brachyteles arachnoides, Panthera onca, Chrysocyon brachyurus and Speothos venaticus), and two during the implementation of the Management Plan (Monodelphis americana and Akodon cursor) (Table 2). With 20 species Rodentia was the best represented order, followed by Carnivora (n=9) and Didelphimorphia (n=9) (Table 2). Canis lupus familiaris was the only exotic species recorded in the NSV, however was not included in the final listing.
Table 2 Mammal species recorded in Núcleo Santa Virginia, Serra do Mar State Park, São Paulo. Taxonomic classification based on Wilson & Reeder (2005).
Type of record = VLT - Visual during line transects, Ct - camera traps, Ts - track-station, Lt - live trap (Sherman or Tomahawk), Pf - pitfall, Ro - occasional record, In - Interviews, B - bibliographic data (Wang 2002, Instituto Florestal 2006).
Conservation Status (species classification category IUCN 2001)/Level of Threat following Decreto N° 53.494, (2 October 2008), Fauna Ameaçada de Extinção no Estado de São Paulo: Vertebrados (2009), MMA & Fundação Biodiversitas (2008) and Machado et al. (2005): NT (Near threatened); LC (Least concern); DD (Data deficient); VU (Vulnerable); EN (endangered); CR (Critically endangered).
Among the methods used, interviews and the occasional records provided the greatest number of species, with 29 (50% of the total) and 26 (45%) species, respectively. Approximately 41% of the species were uniquely identified by a single sampling method and approximately 29% were recorded using two different methods. Track-stations and line transects did not produce unique records of any mammal, while the data collected using live-traps, pitfalls and interviews resulted in three, seven and six unique records, respectively (Table 2).
Mean cumulative species curve, made on the basis of 20 taxa of small mammals captured, considering the effort of both the live and pitfall traps, showed a tendency towards stabilization, whereas the cumulative curve of species caught showed that only two additional taxa were included in the sample after the first half of the sampling effort (3,870 trap.nights) (Figure 2). This richness of small mammals corresponds to 87% of that predicted using the Jackknife 1 estimator (23 species).
Figure 2 Mean species accumulation curve (red line) and cumulative curve of species captured (in black) of small non-volant mammals in relation to sampling effort.
Regarding the conservation status, 14 of the 58 species (i.e., 24% of the total) are under threat at the state level. Being classified as "Critically Endangered" (CE): Panthera onca, "Endangered" (EN): Leopardus wiedii, Brachyteles arachnoides, and Tayassu pecari and "Vulnerable" (VU): another 10 species (Table 2). Eleven other species are classified as "Near Threatened" (NT) (i.e. there is an indication that they are close to being classified into one of these categories in the near future), while five qualify as "Data Deficient" (DD). According to the national list of threatened species, eight species are classified as VU and one is listed as EN (Brachyteles arachnoides), while four are classified as NT and four as DD (Table 2).
Discussion
Considering the species of non-flying mammals occurring in Brazil (Paglia et al. 2012), São Paulo (Vivo et al. 2011) and, potentially occurring in the study region (cf. NaturaServe 2014), NSV has 12% of the recorded species for the country, 45% of those occurring in the state, and between 55-68% of species expected for the region (Table 3).
Table 3 Representation of mammals occurring in Núcleo Santa Virginia in relation to Brazil (Paglia et al. 2012), São Paulo State (Vivo et al. 2011) and NatureServe (2014) projections.
| Order | Brazil | São Paulo | Projection of NatureServe | Núcleo Santa Virginia |
| Didelphimorphia | 55 | 24 | 19-22 | 9(a) |
| Cingulata | 11 | 5 | 5-6 | 3 |
| Pilosa | 8 | 3 | 3 | 2 |
| Primates | 118 | 10 | 5-8 | 5(b) |
| Lagomorpha | 1 | 1 | 1 | 1 |
| Carnivora | 26 | 17 | 12-15 | 14(c) |
| Perissodactyla | 1 | 1 | 1 | 1 |
| Artiodactyla | 10 | 8 | 6 | 3 |
| Rodentia | 234 | 58 | 33-42 | 20 |
| TOTAL | 464 | 127 | 85-104 | 58 |
(a) One species with unconfirmed record;
(b) Two species with unconfirmed records;
(c) Three species with unconfirmed records.
In comparing the results of this study with other studies carried out in the Atlantic Forest of southeastern Brazil, NSV has one of the highest species richness of non-flying mammals (Table 2 and 3). In the Parque Estadual do Desengano (RJ - 22,400 ha) a total of 41 taxa were recorded, 17 of them based solely on the reports of others (Modesto et al. 2008). Cunha & Rajão (2007) recorded 26 species in the Terra Indígena Sapukai (RJ - 2,100 ha), including three exotics (Canis lupus familiaris, Felis catus and Mus musculus), and Passamani et al. (2005) recorded 48 species around the Estação Ecológica Santa Lucia (ES - 440 ha). For the state of São Paulo, De Vivo and Gregorin (2001) reported 58 species for Parque Estadual de Intervales (SP - 48,000 ha) and, more recently, Brocardo et al. (2012) reported 53 species for the Parque Estadual Carlos Botelho (SP - 37,644 ha) - Paranapiacaba forest continuum. Particularly for the PESM, Pinheiro & Geise (2008) recorded 13 species of small mammals (five marsupials and eight rodents) in núcleo Pinciguaba, located in the lowland forests of the protected area, compared to 24 species (9 marsupials and 15 rodents) considered in the present study.
Six new species records have been added to the list of non-flying mammals (n = 69) available in the PESM Management Plan - which considers the entire length of the unit (Instituto Florestal 2006). They are, the marsupial Monodelphis sp. and rodents Akodon montensis and Kannabateomys amblyonyx; the armadillo Cabassous tatouay and the canids Chrysocyon brachyurus and Speothos venaticus. Although the last two records came from third-party reports, for the maned wolf the source of information is reliable (J.P. Villani, area manager, reports the capture of an individual within the limits of NSV), and for the bush dog, there is corroborating data available (Emmons & Feer 1997, Eisenberg & Redford 1999, Cheida et al. 2011) including the study region (lato sensu) within its range. Exclusive records of small mammals from Wang (2002) were not used, because it is not a specific work with the group, which has so many identification intrinsic problems.
For other taxa that were only recorded through interviews, evidences of their current or historical presence in the area are strong and persuasive. Callicebus nigrifrons, for example, occurs in dense mountain rain forest in PESM (Cunha/Indaiá), a vegetation formation also present in the NSV (Instituto Florestal 2006). Brachyteles arachnoides was recorded in the vicinity, specifically in Cunha (Marques 2004), which is part of the same continuous forest. And, Panthera onca was recently confirmed by genetic analysis of scats carried out by the Departamento de Genética e Evolução - Universidade Federal de São Carlos (P.M. Galetti Jr. pers. com). Finally, Chironectes minimus, the only small species to be recorded only through the reports of others, in addition to being easily identified by their conspicuous traits, is also a specialist animal for a particular type of habitat (streams, usually isolated) (Bianconi & Rossi 2011), which is frequent in the area.
Both species of small mammals (Monodelphis americana and Akodon cursor) recorded exclusively during the elaboration of the Management Plan (Instituto Florestal 2006) deserve caution. Besides having cryptic characteristics, these taxa were not identified with cytogenetic or molecular analyzes during the technical work (A.P. Carmignotto pers. com.). All specimens of the genus Akodon and Monodelphis (with three stripes) collected during this study were genetically identified as A. montensis and Monodelphis iheringi respectively (R.D. Cardoso pers. com.). Thus, more detailed examination of the specimens collected on the Management Plan would be prudent to elucidate whether these species occur in sympatry in NSV.
As noted in the Management Plan, a single deer species represented the order Artiodactyla: Mazama americana. This result may be related to the low population density of co-generas - especially M. gouazoubira, which is considered to be the most abundant and widely distributed Brazilian deer species (Duarte 1996) - or even the absence of individuals in the region. For the other orders of non-flying mammals, the richness observed in NSV was very close to the expected (Instituto Florestal 2006, NatureServe 2014).
The use of several complementary sampling methods was essential to provide a complete as possible list of mammals occurring in the NSV. For small mammals, the observed richness was satisfactory, accounting for 87% of the estimated species (Jackknife 1), of which 90% were registered in the first half of the sampling effort (Figure 2). However, based on the collectors curve and the state and regional lists (Vivo et al. 2011, NatureServe 2014), new taxa should be incorporated, especially through the effort increment and sampling in other environments, such as different successional stages and altitudes.
Based on the elevated mammal richness, including many endangered species (Table 2) and with the presence of species from various trophic levels (e.g., herbivores, frugivores, carnivores, prey and predators), the uniqueness and significance of NSV for the maintenance and conservation of regional biodiversity becomes explicit. Also noteworthy is its relevance as a location for diverse ecological studies as well as studies that continue to inventory the local mammals, with an expansion of sampling methods and inclusion of the order Chiroptera.
