Large and medium-sized mammals of Carajás National Forest, Pará state, Brazil

The Carajas National Forest is located in the Amazonian region, Para State, Brazil and is part of a mosaic of conservation units comprising over one million hectares. This region has been explored for its mineral reserves, but knowledge of the distribution of animals and plants is lacking. The objective of this paper is to provide a list of the medium and large-sized mammals recorded from the Carajas NF. We used four methods to record mammals: linear transects, camera traps, records of road-killed animals, and opportunistic observations. We recorded 45 species distributed in nine taxonomic orders, eight of them currently on the Brazilian list of threatened species and seven in the IUCN red list. The area has high mammalian diversity and holds 56% of the threatened species known for the State, confirming that the study area is correctly categorized as Extremely High Priority for the conservation of Brazilian biodiversity.


Introduction
Conservation units are effective barriers against the disturbance of occupation and destruction of natural habitats, which is an ever increasing alarming threat in Brazil (Silva 2005). In the Amazon region, conservation strategies have focused more on areas used by humans (reserves of sustainable use) than in uninhabited areas (complete protection) (Soares-Filho et al. 2006). The Carajás National Forest (Carajás NF - Figure 1) is part of a mosaic of conservation units covering more than one million hectares. The Conservation and Sustained Use of the Brazilian Biological Diversity Project (PROBIO) selected the entire mosaic as an area of high priority for the conservation of Brazilian biodiversity (MMA, 2003). Both, sustainable use and complete protection areas are found within this mosaic.
Some regions of Brazil, especially in the Amazon, present large gaps in scientific information. The southern part of Pará, including the Carajás NF is considered to be scientifically very poorly known (Paglia et al. 2008), despite being regarded as an area of high priority for conservation. The objective of this paper is to provide a list of the medium and large-sized mammals documented in the Carajás NF.
Abstract: The Carajás National Forest is located in the Amazonian region, Pará State, Brazil and is part of a mosaic of conservation units comprising over one million hectares. This region has been explored for its mineral reserves, but knowledge of the distribution of animals and plants is lacking. The objective of this paper is to provide a list of the medium and large-sized mammals recorded from the Carajás NF. We used four methods to record mammals: linear transects, camera traps, records of road-killed animals, and opportunistic observations. We recorded 45 species distributed in nine taxonomic orders, eight of them currently on the Brazilian list of threatened species and seven in the IUCN red list. The area has high mammalian diversity and holds 56% of the threatened species known for the State, confirming that the study area is correctly categorized as Extremely High Priority for the conservation of Brazilian biodiversity. old-growth forest and two with metaphilic savannah (located in N2 and N4). One old-growth-forest area and N4 savannah are located in areas adjacent to an iron ore mine. The mined areas are approximately 7.2 km from areas not mined.
The study was carried out from October 2008 to July 2010. Recording effort consisted of 66 days of linear transects and 241 days of camera trapping.

Linear Transects
Three of the four areas had five linear transects, each approximately 1200-meters long, parallel and distant 300 meters from each other. The fourth area, of metaphilic savannah, had only four transects because of its slightly smaller size. Each transect was sequentially marked and geo-referenced every 20 m, so that all records would have a precise geographic coordinate.
Four sampling periods were carried out in each area, resulting in approximately 24 km of linear transects. The transects were walked in alternating diurnal (6:00-10:00) and crepuscular sampling periods (14:00-18:00). Approximately 4 km were walked during each sampling period (average speed of 1km/h) each day, and we attempted to maintain an equal sampling effort among transects. During transect surveys, recordings were made of visual sightings and other signs (vocalizations, footprints, burrows and skeletal remains). Mammal species recorded by signs were identified following Borges and Tomás (2004) and Mamede and Alho (2008).

Camera traps
Twenty-five camera-trap sites were distributed in five transects in each of the study areas. The camera traps were set along the transects, with a minimum of 300 m between traps, giving an equal sampling effort for each of the four study areas.
A total of 50 camera traps (Tigrinus®, model 6.0) with Sony 10.1 mega-pixel digital cameras were used simultaneously in two study areas. In most cases, the mode program "prog1f" was used in forested habitats, and mode program "prog2f" was used in metaphilic savannah habitats, which are the programs recommendations for closed and open areas, respectively.

Road kills
The road kill data was collected from December 2008 to April 2010. The data was initially collected for another project and was used in this survey to complement the list of medium and large mammal species. Animals were collected from a vehicle that traversed a total of 286 km every day along the Raymundo Mascarenhas Highway, the main road accessing the interior region of the Carajás NF. Surveys were conducted twice a day (morning and evening) continuously, including weekdays and holidays.

Opportunistic observations
During field work, opportunistic observations from camera-trapping and direct observation (with photos whenever possible) were made in the Carajás NF. Each sampling point for these opportunistic records was georeferenced. Two river surveys were also carried out: one along the Parauapebas River and one on the Itacaiúnas River. The Itacaiúnas River (Figure 3), which forms the border with the Tapirapé-Aquiri National Forest, was sampled continuously along 99.77 km (including the return trip), with short breaks for resting and eating. The Parauapebas River, which separates the Carajás NF from the urban and rural regions of the municipality of Parauapebas, was traversed for 50 km using the same method.
Aiming to complement the methodology of "opportunistic observations" we aggregated information collected by ICMBio (Federal Agency responsible for managing the protect areas) for the presence of mammalian species. Between 2008 and 2010, during the reserve management activities such as monitoring, environment education and licensing inspection, any evidence of mammals of medium and large size was recorded.
Species names followed Wilson and Reeder (2005). Identification of species was based on illustrations and photographs available in the specialized literature (e.g. Eisenberg and Redford 1999; Reis et al. 2006;Bonvicino et al. 2008), always taking into consideration the regional distribution of specious taxa. Whenever doubts were raised, species identity was confirmed, through photos, by specialists. The rarefaction curve of mammals species (transects and camera-traps) was created in the software EstimateS 8.0.0 (Colwell 2006) with 1000 randomizations and the firstorder jackknife (Jackknife 1) estimator.

Results and Discussion
A total of 432 km of transects were walked and 3,572 camera-traps*day were set in the four study areas. In both methods, the rarefaction curve tended to stabilize and plotted values for Jackknife 1 estimator were higher than the species richness observed (Figure 4).
Adding the records obtained by opportunistic observations, road kills, transect and camera-traps a total of 45 species of medium and large-sized mammals were registered (Figures 5-8). The use of four distinct methodologies was extremely important in producing our results and in verifying the presence of the different taxa of mammals.
The recorded species belong to nine orders: 15 species of Carnivora, six of Primates, five of Cingulata, seven of Rodentia, four of Artiodactyla, five of Pilosa, one of Lagomorpha, one of Perissodactyla one of Didelphimorphia (Table 1). For the last six orders cited, we registered all of the species of large and medium-sized mammals of probable occurrence in the southeastern region of Pará, listed in Reis et al. (2006). For Primates, all of the locally distributed species with diurnal habits were registered in this study (only Aotus sp. was not recorded, but it is a nocturnal species).
This study complements two surveys made previously in the area. Using only capture and direct observations, Toledo et al. (1999) recorded nine species (all included in this survey), which corresponds to 20% of the present list. The Management Plan for the Carajás NF (2003) presented a list containing 21 species of medium and large-sized mammals, of which only one species, Mazama rufina, is not on our list. This deer, nevertheless, is not supposed to occur in Brazil. It is restricted to the Andes of Colombia, Ecuador and Peru (Eisenberg and Redford, 1999;Lizcano and Alvarez, 2008). Most probably, it was a misidentification.
Our list presents 19 new records for the Carajás National Forest (Table 1). In Pará, 15 species of mammals are listed as Species Threatened with Extinction, of which nine are terrestrial/arboreal. Of those, six occur in the Carajás NF, or 56% of the threatened species (SECTAM 2006). These are: Panthera onca, Puma concolor, Pteronura brasiliensis, Priodontes maximus, Myrmecophaga tridactyla and Chiropotes utahickae. Eight species on the Brazilian list of threatened species (Machado et al. 2008) occur in the area of study. These include the same species listed above (except P. concolor), plus Speothos venaticus, Leopardus  The diversity of mammals of medium and large size found in the Carajás NF is quite high when compared to other protected areas in the Amazon. In Gurupi Biological Reserve, located in eastern Amazon, Maranhão State, Lopes and Ferrari (2000) recorded 18 species of mammals of medium and large size. In Humaitá National Forest, in Acre State, 27 species of large and medium-sized mammals were recorded using two sampling methods at different times: transects in the years 1999 and 2000 and camera trapping during 2009and 2010(Botelho et al. 2012. Another study conducted between 2008 and 2009 in the forest area of Base Operating Pedro de Moura located in Urucu River Basin, Amazonas State, covering an area of about 514,000 ha found a total of 41 mammalian species of medium and large size (Santos and Mendes-Oliveira 2012). Iwanaga (2004) sampled 42 species to the Jau National Park, whereas Haugaasen and Peres (2007) recorded 27 species in Lake Uauaçú, in the Purus River. Patton et al. (2000) studied several areas along the river Juruá, and recorded 18 species in the lower portion of the river, 21 species in the central portion (both located in the state of Amazonas), and 28 species in the headwaters of the river, in the state of Acre. Among all the published inventories of large and medium-sized mammals of the Brazilian Amazon, the present study was the one with the highest number of species. It is worth noting that our results are probably related to the fact that four complementary methodologies were used (transect census, camera-trapping, road-killing inventory and opportunistic records) and not necessarily that Carajás NF has a greater medium-large mammal