Abstract:

The Amazonian rainforest harbors one of the most diverse mammal faunas found anywhere in the world, although this fauna is still poorly known. Inventories are essential for the understanding of the biology and ecology of species, and provide basic data for conservation. Over 15 years of sampling in the Saracá-Taquera National Forest, we recorded 72 species of small (nonvolant), medium, and large mammals belonging to 30 families in 10 orders. These taxa included 29 species endemic to the Amazon biome, and 14 classified as threatened with extinction. Overall, the mammalian species richness recorded in the present study was equal to or greater than that recorded in other Amazonian studies, reflecting high levels of diversity on a biogeographic scale. This reinforces the importance of this national forest for the maintenance of the region's mammalian fauna. Some of the species were recorded in the region for the first time, thus extending their known geographic distribution.

Keywords:
Trombetas; Oriximiná; Amazonia; species richness; environmental monitoring; species list

Resumo:

A floresta amazônica abriga uma das maiores riquezas de mamíferos do mundo. Entretanto, existe pouco conhecimento sobre a fauna local. Estudos de levantamentos podem contribuir para o incremento no conhecimento sobre a biologia e a ecologia das espécies e são a base para a conservação. Ao longo de 15 anos de amostragem, nós registramos 72 espécies de pequenos, médios e grandes mamíferos pertencentes a 10 ordens e 30 famílias, das quais 29 espécies são endêmicas da Amazônia e 14 são também consideradas ameaçadas de extinção. No geral, a riqueza de mamíferos foi igual ou superior ao de outros estudos conduzidos no bioma, indicando uma alta diversidade em escala biogeográfica. Os resultados mostram a importância desses ambientes para a manutenção das espécies. Algumas tiveram seu primeiro registro para a área e outras a ampliação da sua área de distribuição.

Palavras-chave:
Trombetas; Oriximiná; Amazônia; riqueza; monitoramento ambiental; lista de espécies

Introduction

Recent studies (Wilson and Reeder 2005WILSON, D.E. & REEDER, D.M. 2005. Mammals species of the World: a taxonomic and geographic reference, 3rd. ed. Baltimore: The Johns Hopkins University Press, p.2142.; Paglia et al. 2012PAGLIA, A.P., RYLANDS, A.B., HERRMANN, G., AGUIAR, L.M.S., CHIARELLO, A.G., LEITE, Y.L.R., COSTA, L.P. & SICILIANO, S. 2012. Lista Anotada dos Mamíferos do Brasil. 2ª Edição. Conservation International, Arlington, p.762.) have estimated that approximately 700 mammal species occur in Brazil, of which, at least 399 are present in the Amazon biome. This is the most diverse mammalian fauna of any equivalent region in South America. Even so, the number of species found in the Amazon continues to grow, as new species are described, including primarily primates, bats and small rodents (Gualda-Barros et al. 2012GUALDA-BARROS, J., NASCIMENTO, F.O. & AMARAL, M.K. 2012. A new species of Callicebus Thomas, 1903 (Primates, Pitheciidae) from the states of Mato Grosso and Pará, Brazil. Papéis Avulsos de Zoologia 52 (23): 261-279.; Mittermeier et al. 2013MITTERMEIER, R.A. , RYLANDS, A.B. & WILSON, D.E. 2013. Handbook of the Mammals of the World. Vol. 3. Primates. Barcelona, Spain: Lynx Edicions, p.951; Dalponte et al. 2014DALPONTE, J., SILVA, F.E. & SILVA-JR, J.S. 2014. New species of titi monkey, genus Callicebus Thomas, 1903 (Primates, Pitheciidae), from Southern Amazonia, Brazil. Papéis Avulsos de Zoologia 54(32): 457-472.; Oliveira et al. 2016OLIVEIRA, T.G., MAZIM, F.D., VIEIRA, O.Q., BARNETT, A.P.A., SILVA, G.N., SOARES, J.B.G., SANTOS, J.P., SILVA, V.F., ARAÚJO, P.A., TCHAIKA, L. & MIRANDA, C.L. 2016. Nonvolant mammal megadiversity and conservation issues in a threatened central Amazonian hotspot in Brazil. Tropical Conservation Science, 1-16.; Pavan et al., 2017PAVAN, S. E., MENDES-OLIVEIRA, A.C. & VOSS, R.S. 2017. A New Species of Monodelphis (Didelphimorphia: Didelphidae) from the Brazilian Amazon. AMERICAN MUSEUM NOVITATES 3872, 20 pp.; Voss et al. 2018VOSS, R.S., DÍAZ-NIETO, J.F. & JANSA, S.A. 2018. A Revision of Philander (Marsupialia: Didelphidae), Part 1: P. quica, P. canus, and a New Species from Amazonia. American Museum Novitates (3891):1-70.).

Mammals play an great variety of roles in the ecosystems in which they are present (Keuroghlian and Eaton 2009KEUROGHLIAN, A. & EATON, D.P 2009. Removal of palm fruits and ecosystem engineering in palm stands by white-lipped peccaries (Tayassu pecari) and other frugivores in an isolated Atlantic Forest fragment. Biodiversity and Conservation 18: 1733-1750.; Haugassen et al. 2010HAUGAASEN, J.M.T., HAUGAASEN, T., PERES, C.A., GRIBEL, R & WEGGE, P. 2010. Seed dispersal of the Brazil nut tree (Bertholletia excelsa) by scatter-hoarding rodents in a central Amazonian forest. Journal of Tropical Ecology 26(3): 251-262.; Desbiez et al. 2013DESBIEZ, A.L.J. & KLUYBER, D. 2013. The role of giant armadillos (Priodontes maximus) as physical ecosystem engineers. Biotropica 45(5): 537-540.). Marsupials and rodents, in particular, influence the ecological dynamics of Neotropical forests through seed predation and dispersal, as well as the dispersion of mycorrhizal fungi (Brewer and Rejmánek 1999, Mangan and Adler 1999, 2000). Larger-bodied mammals disperse over longer distances and are important in the acquisition and redistribution of nutrients and seeds within the landscape, as well as participating in the control of populations through predation (Asquith et al. 1999ASQUITH, N.M., TERBORGH, J., ARNOLD, A.E. & RIVEROS, C.M. 1999. The fruits the agouti ate: Hymenaea courbaril seed fate when its disperser is absent. Journal of Tropical Ecology 15(2): 229-235.; Fragoso et al. 2006FRAGOSO, J.M.V., SILVIUS, K.M. & CORREA, J.A. 2006. Long-distance seed dispersal by tapirs increases seed survival and aggregates tropical trees. Ecology 84(8): 1998-2016.; Stoner et al. 2007STONER, K.E., RIBA-HERNÁNDEZ, P., VULINEC, K. & LAMBERT, J.E. 2007. The role of mammals in creating and modifying seedshadows in Tropical Forests and some possible consequences of their elimination. Biotropica 39(3): 316-327.). Given this, some mammals are considered to be bioindicator species, given their specific habitat and microhabitat preferences or requirements (Vieira and Monteiro-Filho 2003; Cullen-Jr. et al. 2005CULLEN JR, L., ABREU, K.C. & NAVA, A.F.D. 2005. As onças-pintadas como detetives da paisagem no corredor do Alto Paraná, Brasil. Natureza & Conservação 3(1): 43-58.; Pardini and Umetsu 2006; Morrison et al. 2007MORRISON, J.S., SECHREST, W., DINERSTEIN, E., WILCOVE, D.S. & LAMOUREUX, J.F. 2007. Persistence of large mammal faunas as indicators of global human impacts. Journal of Mammalogy 88(6): 1363-1380.).

Overall, 15.7% of Brazilian mammals are classified as threatened, and at least 10% of these species are found in the Amazon (Costa et al. 2005COSTA, L.P., LEITE, Y.L.R., MENDES, S.L. & DITCHFIELD, A.D. 2005. Mammal conservation in Brazil. Conservation Biology 19(3): 672-679.; Paglia et al. 2012PAGLIA, A.P., RYLANDS, A.B., HERRMANN, G., AGUIAR, L.M.S., CHIARELLO, A.G., LEITE, Y.L.R., COSTA, L.P. & SICILIANO, S. 2012. Lista Anotada dos Mamíferos do Brasil. 2ª Edição. Conservation International, Arlington, p.762.; MMA 2014MMA, 2014. Lista das espécies brasileiras ameaçada de extinção. Portarias nº 444/2014. http://www.icmbio.gov.br/portal/biodiversidade/faunabrasileira/lista-de-especies.html (último acesso em 12/02/2017)
http://www.icmbio.gov.br/portal/biodiver... ). The Amazon is the largest forest formation in Brazil, and one of the most biodiverse ecosystems in the world (Mittermeier et al. 2003MITTERMEIER, R.A., MITTERMIER, C.G., BROOKS, T.M., PILGRIM, J.D., KONSTANT, W.R., FONSECA, G.A.B. & KORMOS, C. 2003. Wilderness and biodiversity conservation. Proceedings of the National Academy of Sciences 100(18): 10309-10313.). However, its unique and complex environments and biota are being increasingly impacted by a range of anthropogenic disturbances, which affect the populations of large numbers of species (Peres and Lake 2003PERES, C.A. & LAKE, I.R. 2003. Extent of nontimber resource extraction in tropical forests: accessibility to game vertebrates by hunters in the Amazon basin. Conservation Biology 17 (2): 521-535.; Benchimol and Venticinque 2014BENCHIMOL, M. & VENTICINQUE, E.M. 2014. Responses of primates to landscape change in Amazonian land-bridge islands-a multi-scale analysis. Biotropica 46(4): 470-478.; Antunes et al. 2016ANTUNES, A.P., FEWTER, R.M., VENTICINQUE, E.M., PERES, C.A., LEVI, T., ROHE, F. & SHEPARD JR. G.H. 2016. Empty forest or empty rivers? A century of commercial hunting in Amazonia. Sciences Advances 2(10): e1600936.).

The mammalian fauna of the Amazon has only been well documented at a few localities, and most inventories are preliminary and incomplete (Voss and Emmons 1996VOSS, R.S. & EMMONS, L.H. 1996. Mammalian diversity in neotropical lowland rainforests: a preliminary assessment. Bulletin of the American Museum of Natural History 230: 1-115.; Peres 2005PERES, C.A. 2005. Why we need megareserves in Amazonia. Conservation Biology 19(3): 728-733.). This deficiency is related primarily to the vast size of the biome, and its many remote and inaccessible areas, which are hard to reach, and extremely difficult to survey, even in a minimally adequate fashion (Silveira et al. 2003SILVEIRA, L., JÁCOMO, A.T.A. & DINIZ-FILHO, J.A.F. 2003. Camera trap, line transect census and track surveys: a comparative evaluation. Biological Conservation 114(3): 351-355.; Peres and Lake 2013). Given this, many areas should be considered to be of high priority for surveys, especially given the importance of occurrence data for other types of ecological study, and in particular conservation planning (Margules and Pressey 2000MARGULES, C. R. & PRESSEY, R.L. 2000. Systematic conservation planning. Nature 405: 243-253.; Peres 2005PERES, C.A. 2005. Why we need megareserves in Amazonia. Conservation Biology 19(3): 728-733.).

Saracá-Taquera National Forest (STNF), located in northwestern Pará, Brazil, was created by federal decree number 98,704 of December 27th, 1989, and has an area of 429,600 ha. Most studies of the mammalian populations of this protected areas have been conducted since early 2000, with the primary aim of monitoring and evaluating the response of local populations to environmental disturbance, in particular, the loss of habitat, and assessing species resilience (Calaça 2014CALAÇA, A.M. 2014. Padrões de distribuição local e de diversidade funcional de mamíferos na Amazônia Central. Tese de doutorado do Programa de Pós-graduação em Ecologia. Universidade Federal do Rio de Janeiro, Rio de Janeiro. 167p.). The management plan of STNF (STCP 2001STCP. 2001. Plano de Manejo da Floresta Nacional de Saracá-Taquera, Estado do Pará - Brasil. STCP - Engenharia de Projetos Ltda, Curitiba, p.708.) listed 58 species of terrestrial, aquatic, and semiaquatic mammals. In subsequent years, however, a number of additional species have been recorded, and the inventory was revised and the list of management plan updated (Gomes et al. 2014GOMES, R., MORATO, S. A. A., CALIXTO, P. O., MENDES, L. R. L. P., MELO, F. R., MIRETZKI, M., FARIA, M. B., CALAÇA, A. M. & OLIVEIRA, A. F. 2014. Guia fotográfico de identificação de mamíferos terrestres e aquáticos da Floresta Nacional de Saracá-Taquera, estado do Pará. Curitiba: STCP Engenharia de Projetos LTDA. Porto Trombetas: MRN - Mineração Rio do Norte SA. 95p.). Given their ecological and morphological differences, mammals can be allocated to three principal groups: "small flying mammals", "small non-volant mammals" and "medium and large mammals", with the latter two groups being the focus of the present study. The main objective of the present study was to update the list of mammalian species known to occur in the Saracá-Taquera National Forest, based on an ecological and conservationist approach, based on three long-term surveys conducted between 2009 and 2015.

Materials and Methods

1. Study area

The study area is located within the Saracá-Taquera National Forest (STNF), which is distributed among the neighboring municipalities of Oriximiná, Faro, and Terra Santa, in northwestern Pará (01°40' S, 56°00' W), a state in northern Brazil. STNF is formed predominantly by dense rainforest, interspersed with areas of alluvial forest, blackwater swamp (igapó), and, to a lesser extent, campinarana scrub (Gomes et al. 2014GOMES, R., MORATO, S. A. A., CALIXTO, P. O., MENDES, L. R. L. P., MELO, F. R., MIRETZKI, M., FARIA, M. B., CALAÇA, A. M. & OLIVEIRA, A. F. 2014. Guia fotográfico de identificação de mamíferos terrestres e aquáticos da Floresta Nacional de Saracá-Taquera, estado do Pará. Curitiba: STCP Engenharia de Projetos LTDA. Porto Trombetas: MRN - Mineração Rio do Norte SA. 95p.). The region's climate is of Köppen's Am type, with rainy summers and dry winters, mean annual precipitation of approximately 2200 mm, and temperatures of 20-35°C (Parrota et al. 1997PARROTA, J.A., KNOELES, O.H. & WUNDERLE JR, J.M. 1997. Development of floristic diversity in 10-year-old restoration forests on a bauxite mined site in Amazonia. Forest Ecology Management 99(1-2): 21-42.). STNF area is rich in bauxite, which is being mined by a consortium of companies known as Mineração Rio do Norte (MRN), which operates on a small number of the plateaus found within the area of the national forest. In the present study, we sampled 12 plateaus, known locally as: Almeidas, Aviso, Aramã, Bacaba, Bela Cruz, Cipó, Greig, Monte Branco, Papagaio, Periquito, Saracá, and Teófilo (Figure 1).

2. Data collection and analysis

To compile the species list, we used primarily data from three surveys, conducted in 2009-2010, 2010-2012, and 2015. During these surveys, different approaches were used to sample small rodents and marsupials, and medium-and large-sized mammals (Silveira et al. 2003SILVEIRA, L., JÁCOMO, A.T.A. & DINIZ-FILHO, J.A.F. 2003. Camera trap, line transect census and track surveys: a comparative evaluation. Biological Conservation 114(3): 351-355.; Ribeiro and Melo 2013RIBEIRO, P.H.P. & MELO, F.R. 2013. Mamíferos de médio e grande porte de uma área agricultável em Terezópolis (GO) com notas sobre métodos de amostragem. Neotropical Biology and Conservation (8): 68 - 78.; Bovendorp et al. 2017BOVENDORP, R.S., MC CLEERY, R.A. & GALETTI, R.A. 2017. Optimising sampling methods for small mammal communities in Neotropical rainforests. Mammal Review (47): 148-158.) and, given this, the results are presented separately. The species richness is presented as the number of species recorded during any given period, independently of indices of biodiversity.

3. Small non-volant small mammals

During the three study periods, from from 2009 to 2015, we trapped small mammals in both rainy and dry seasons, focusing on the tropical rainforest in three topographies, plateau, slope, and valley bottom. Two types of trap were used, metal live traps (Tomahawk and Sherman) and pitfall traps. Captured specimens were identified using Patton et al. (2000PATTON, J.L., DA SILVA, M.N.F. & MALCOLM, J.R. 2000. Mammals of the Rio Juruá and the evolutionary and ecological diversification of Amazonia. Bulletin of the American Museum of Natural History 244:1-306., 2015)PATTON, J.L., PARDIÑAS, U.F.J. & D'ELÍA, G. (eds.). 2015. Mammals of South America, vol. 2. Rodents. University of Chicago Press, Chicago, Illinois. 1336 pp. ISBN 978-0-226-16957-6, price (hard cover)., Bonvicino et al. (2008)BONVICINO, C.R., OLIVEIRA, J.A. & D'ANDREA, P.S. 2008. Guia dos Roedores do Brasil com chaves para gêneros baseadas em caracteres externos. Centro Pan-Americano de Febre Aftosa-OPAS/OMS, Rio de Janeiro, p.120., and Rossi et al. (2010)ROSSI, V.R., BIANCONI, V.G., CARMIGNOTTO, A.P. & MIRADA, C.L. 2010. Mamíferos do Brasil (R.N. Reis, L.A. Peracchi, A.W. Pedro & P.I. Lima, eds). Ordem Didelphimorphia. Edifurb, Londrina, Brasil, p 27-66.. Specimens were allocated to either the order Didelphimorphia (family Didelphidae) or the Rodentia (Cricetidae, Echimydae and Sciuridae). The sampling effort is presented in Table 1.

4. Medium and large mammals

Medium and large mammals, were surveyed by line transect, with individual transects varying in length from 500 m to 4000 m. In all three study periods, surveys were conducted during the day, in the morning (7:00-11:00 h) and afternoon (13:00-17:00 h), and at night, between 19:00 h and 22:00 h. Whenever an animal was visualized or some other evidence was detected, a standard set of data was compiled, including the identification of the species, the type of record, the number of individuals, the time and the location on the transect, and the geographic coordinates. Whenever possible, the animal or vestige were photographed.

To complement these data, we installed two to eight camera traps on each transect, which remained active for six to 20 days, depending on the duration of the fieldwork. During the first period, a trap was installed at each end of the trail on the 500-m transects. During the second period, four traps were installed at 50 m, 100 m, 250 m, and 500 m along the transect, to evaluate the influence of edge effects, while in the third period, the traps were installed at 1000-m intervals along the 4000 m transect. The camera traps were installed on tree trunks, 30 cm above the ground, and were baited with fruit, bacon and/or sardines, to maximize the chances of animals visiting the sites. The sampling effort for each period is shown in Table 1. Species were identified based on Paglia et al. (2012)PAGLIA, A.P., RYLANDS, A.B., HERRMANN, G., AGUIAR, L.M.S., CHIARELLO, A.G., LEITE, Y.L.R., COSTA, L.P. & SICILIANO, S. 2012. Lista Anotada dos Mamíferos do Brasil. 2ª Edição. Conservation International, Arlington, p.762., with the nomenclature updated to include Cingulata and Cetardiodactyla (Montgelard et al. 1997MONTGELARD, C., CATZEFLIS, F.M., & DOUZERY, E. 1997. Phylogenetic relationships of artiodactyls and cetaceans as deduced from the comparison of cytochrome b and 12S rRNA mitochondrial sequences, Molecular Biology and Evolution, 14 (5): 550-559.; Delsuc et al. 2016DELSUC, F., GIBB, G.C., KUCH, M., BILLET, G., HAUTIER, L., SOUTHON, J., ROUILLARD, J.M., FERNICOLA, J.C., VIZCAÍNO, S.F., MACPHEE, R.D.E., POINAR, H.N.P. 2016. The Phylogenetic Affinities Of The Extinct Glyptodonts. Current Biology 26: 155-156.).

To guarantee as complete an inventory as possible, in addition to the field surveys, records of mammals were gleaned from published studies and other records obtained during fieldwork at STNF, including interviews, although the interview data should obviously be treated with caution. These data were not included in the analyses. The trapping and transect data were grouped for the plotting of species accumulation curves using the first-order Jackknife method, run in EstimateS 8.20 (Heltshe and Forrester 1983HELTSHE, J.F. & FORRESTER, N.E. 1983. Estimating species richness using the jackknife procedure. Biometrics, 39 (1): 1-11.; Colwell 2009COLWELL, R.K. 2009. EstimateS 8.2.0. - Statistical Estimation of Species Richness and Shared species from Samples. http://viceroy.eeb.uconn.edu/EstimateS.
http://viceroy.eeb.uconn.edu/EstimateS... ).

Results

Over the 15 years of the study period, we recorded 72 species of small, medium and large mammals in the Saracá-Taquera National Forest (Table 2, Figures 2, 3), of which, five were recorded during interviews with local residents. The composition of the mammalian community was extremely diverse, and included representatives of 30 families and 10 orders. The most diverse orders were the rodents, with 16 species, followed by the carnivores, with 14 species, and the primates and marsupials, with 10 species each (Table 2).

Species accumulation curves for the trapping data, i.e., small non-volant mammals (Figure 4A), and the line transect data, i.e., medium-large mammals (Figure 4B) both reached the asymptote, indicating that the sampling effort employed was sufficient for the registration of the majority of the species that occur in the study area. The accumulation curve for the cameras trap data (Figura 4C) was still following an upward trend, however, indicating that additional species would likely be added, with increased sample effort.

Discussion

Five of the 72 species recorded in the present study were confirmed only by interviews with local residents. While the data are important as complementary records, they must be treated with extreme caution, especially as some of the species cited may not actually occur in the region. In a review of the records of the Pilosa and Cingulata from the Saracá-Taquera National Forest, for example, Oliveira et al. (2006)OLIVEIRA, L.C., MENDEL, S.M., LORETTO, D., SILVA-JR, J.S. & FERNANDES, G.W. 2006. Edentates of the Saracá-Taquera National Forest, Pará, Brazil. Edentata 7: 3-7. found that some of the species cited, such as the Brazilian three-banded armadillo (Tolypeutes tricinctus (Linnaeus, 1758)) are typical of other biomes, such as the semi-arid Caatinga, and are unlikely to be found in the northern Amazon basin. Similarly, while the six-banded armadillo (Euphractus sexcinctus (Linnaeus, 1758)) has been recorded in interviews, and listed in technical reports, it has never been recorded during fieldwork (Oliveira et al. 2006OLIVEIRA, L.C., MENDEL, S.M., LORETTO, D., SILVA-JR, J.S. & FERNANDES, G.W. 2006. Edentates of the Saracá-Taquera National Forest, Pará, Brazil. Edentata 7: 3-7.). Also, the occurrence of two primates, Cebus olivaceus (Schomburgk, 1848) and Aotus trivirgatus (Humboldt, 1812), in the STNF has been confirmed only by interviews and published records (Oliveira et al. 2009OLIVEIRA, L.C., LORETTO, D., VIANA, L.R., SILVA-JR, J.S. & FERNANDES, W. 2009. Primate community of the tropical rain forests of Saracá-Taqüera National Forest, Pará, Brazil. Brazilian Journal of Biology 69(4): 1091-1099.). The wedge-capped capuchin, C. olivaceus, has been recorded from the left margin of the Trombetas River (Oliveira et al. 2009OLIVEIRA, L.C., LORETTO, D., VIANA, L.R., SILVA-JR, J.S. & FERNANDES, W. 2009. Primate community of the tropical rain forests of Saracá-Taqüera National Forest, Pará, Brazil. Brazilian Journal of Biology 69(4): 1091-1099.), although the STNF is located on the right margin. In the Amazon, rivers typically act as geographic barriers to primates (Peres et al. 1996PERES, C.A., PATTON, J.L. & SILVA, M.N.F. 1996. Riverine barriers and gene flow in Amazonian saddle-back tamarins. Folia Primatologica, 67: 113-124.; Boubli et al. 2015BOUBLI, J.P., RIBAS, C., ALFARO, J.W.L.,ALFARO, M.W., SILVA, M.N.F., PINHO, G.M. & FARIAS, I.P. 2015. Spatial and temporal patterns of diversification on the Amazon: A test of the riverine hypothesis for all diurnal primates of Rio Negro and Rio Branco in Brazil. Molecular Phylogenetics and Evolution, 82: 400-412.). In other cases, such as that of the northern tiger cat (Leopardus tigrinus), the species can easily be confused with other small-medium felines, especially by non-expert observers, and Payan & Oliveira (2016)PAYAN, E. & DE OLIVEIRA, T. 2016. Leopardus tigrinus. The IUCN Red List of Threatened Species 2016:e.T54012637A50653881. http://dx.doi.org/10.2305/IUCN.UK.20162.RLTS.T54012637A50653881.en. Downloaded on 22 May 2018.
http://dx.doi.org/10.2305/IUCN.UK.20162.... concluded that this species is rare or absent from large areas of the Amazon basin. In addition to these four species, the tapeti (Sylvilagus brasiliensis (Linnaeus, 1758)), while widely-distributed in South America, has never been recorded in the current study area. While the lack of records of these five species may reflect their local rarity, we believe that continued sampling may eventually confirm their presence in the STNF and, as such, while they are included in the list of species that occur in this national forest, their presence in this protected area cannot yet be confirmed definitively.

Overall, 29 of the species recorded in the present study are considered to be endemic to the Amazon, including the marsupials (Didelphis imperfecta (Mondolfi & Pérez-Hernández, 1984), Gracilinanus emiliae (Thomas, 1909), Marmosops parvidens (Tate, 1931), and Monodelphis arlindoi (Pavan et al., 2012PAVAN, S.E., ROSSI, R.V. & SCHNEIDER, H. 2012. Species diversity in the Monodelphis brevicaudata complex (Didelphimorphia: Didelphidae) inferred from molecular and morphological data, with the description of a new species. Zoological Journal of the Linnean Society, 165: 190-223.), the greater long-nosed armadillo (Dasypus kappleri (Krauss, 1982), two species of sloths (Bradypus tridactylus (Linnaeus, 1758) and Choloepus didactylus Linnaeus, 1758)), all the ten primate species recorded in the present study (see Table 1), the deer Mazama nemorivaga and Odoicoleus virginianus, the Amazonian manatee (Trichechus inunguis (Natterer, 1883)), and the rodents Euryoryzomys macconnelli (Thomas, 1910), Rhipidomys nitela (Thomas, 1901), Zygodontomys brevicauda (Allen, 1897), Myoprocta acouchy (Thomas, 1903), Echimys chrysurus (Zimmermann, 1780), Isothrix pagurus (Wagner, 1845), Mesomys hispidus (Desmarest, 1817), Proechimys cuvieri (Petter, 1978), and Guerlinguetus aestuans (Linnaeus, 1766) (Bonvicino et al. 2008BONVICINO, C.R., OLIVEIRA, J.A. & D'ANDREA, P.S. 2008. Guia dos Roedores do Brasil com chaves para gêneros baseadas em caracteres externos. Centro Pan-Americano de Febre Aftosa-OPAS/OMS, Rio de Janeiro, p.120.; Paglia et al. 2012PAGLIA, A.P., RYLANDS, A.B., HERRMANN, G., AGUIAR, L.M.S., CHIARELLO, A.G., LEITE, Y.L.R., COSTA, L.P. & SICILIANO, S. 2012. Lista Anotada dos Mamíferos do Brasil. 2ª Edição. Conservation International, Arlington, p.762.; Patton et al. 2015PATTON, J.L., PARDIÑAS, U.F.J. & D'ELÍA, G. (eds.). 2015. Mammals of South America, vol. 2. Rodents. University of Chicago Press, Chicago, Illinois. 1336 pp. ISBN 978-0-226-16957-6, price (hard cover).). Monodelphis arlindoi was recently described by Pavan et al. (2012)PAVAN, S.E., ROSSI, R.V. & SCHNEIDER, H. 2012. Species diversity in the Monodelphis brevicaudata complex (Didelphimorphia: Didelphidae) inferred from molecular and morphological data, with the description of a new species. Zoological Journal of the Linnean Society, 165: 190-223., and is endemic to the study region (see Figure 2B). No other species of mammal recorded in the present study is endemic to the Saracá-Taquera National Forest, Martin's bare-face tamarin (Saguinus martinsi (Thomas, 1912)) is protected only by this conservation unit.

Fourteen of the species recorded here are also included in one or more of the lists of species threatened with extinction published by the International Union for Conservation of Nature (IUCN 2017), the Brazilian Ministry of the Environment (MMA 2014MMA, 2014. Lista das espécies brasileiras ameaçada de extinção. Portarias nº 444/2014. http://www.icmbio.gov.br/portal/biodiversidade/faunabrasileira/lista-de-especies.html (último acesso em 12/02/2017)
http://www.icmbio.gov.br/portal/biodiver... ), and Pará state resolution 054/2007 (Table 1). A number of these threatened species are extremely sensitive and have undergone population decline throughout most of their geographic ranges, due primarily to habitat loss and fragmentation, hunting pressure, wildfires, and roadkill (Chiarello et al. 2008CHIARELLO, A.G., AGUIAR, L.M.S., CERQUEIRA, R., MELO, F.R., RODRIGUES, F.H.G. & SILVA, V.M.F. 2008. Mamíferos ameaçados de extinção no Brasil (A.B.B. Machado, C.M. Drummond & A.P. Paglia , eds.). Livro Vermelho da Fauna Brasileira Ameaçada de Extinção. MMA, Fundação Biodiversitas, Minas Gerais, MG, p. 681-874.; Naveda et al. 2008NAVEDA, A., de THOISY, B., RICHARD-HANSEN, C., TORRES, D.A., SALAS, L., WALLANCE, R., CHALUKIAN, S. & de BUSTOS, S. 2008. Tapirus terrestris. The IUCN Red List of Threatened Species 2008: e.T21474A9285933. http://dx.doi.org/10.2305/IUCN.UK.2008.RLTS.T21474A9285933.en. Downloaded on 24 June 2018.
http://dx.doi.org/10.2305/IUCN.UK.2008.R... ; Medici et al. 2012MEDICI, E.P., FLESHER, K., BEISIEGEL, B. M., KEUROGHLIAN, A., DESBIEZ, A.L.J., GATTI, A., MENDES PONTES, A.R., CAMPOS, C.B., TÓFOLI, C.F., MORAES JUNIOR, E.A., AZEVEDO, F.C., PINHO, G.M, CORDEIRO, J.L.P, SANTOS JÚNIOR, T. S., MORAIS, A.A., MANGINI, P.R. , RODRIGUES, L.F., ALMEIDA, L.B. 2012. Avaliação do Risco de Extinção da Anta Brasileira Tapirus terrestris Linnaeus, 1758, no Brasil. Biodiversidade Brasileira 1: 3-11.), although some, such as the tapir, the white-lipped peccary, and the jaguar, may be relatively tolerant of disturbed environments (Naveda et al. 2008NAVEDA, A., de THOISY, B., RICHARD-HANSEN, C., TORRES, D.A., SALAS, L., WALLANCE, R., CHALUKIAN, S. & de BUSTOS, S. 2008. Tapirus terrestris. The IUCN Red List of Threatened Species 2008: e.T21474A9285933. http://dx.doi.org/10.2305/IUCN.UK.2008.RLTS.T21474A9285933.en. Downloaded on 24 June 2018.
http://dx.doi.org/10.2305/IUCN.UK.2008.R... ; Keuroghlian et al. 2013KEUROGHLIAN, A., DESBIEZ, A., REYNA-HURTADO, R., ALTRICHTER, M., BECK, H., TABER, A. & FRAGOSO, J.M.V. 2013. Tayassu pecari. The IUCN Red List of Threatened Species 2013: e.T41778A44051115. http://dx.doi.org/10.2305/IUCN.UK.2013-1.RLTS.T41778A44051115.en.Downloaded on 24 June 2018.
http://dx.doi.org/10.2305/IUCN.UK.2013-1... ; Quigley et al. 2017QUIGLEY, H., FOSTER, R., PETRACCA, L., PAYAN, E., SALOM, R. & HARMSEN, B. 2017. Panthera onca. The IUCN Red List of Threatened Species 2017: e.T15953A50658693.http://dx.doi.org/10.2305/IUCN.UK.20173.RLTS.T15953A50658693.en. Download on 24 June 2018.
http://dx.doi.org/10.2305/IUCN.UK.20173.... ).

The most abundant of the ten marsupial species recorded in the Saracá-Taquera National Forest were Marmosa demerarae (Thomas, 1905) and Marmosops parvidens (Tate, 1931), which were both widely distributed in all the environments sampled. Marmosa demerarae (Thomas, 1905) was captured primarily in Sherman traps and, despite being arboreal, it was commonly captured on the ground and in the pitfall traps, as observed by Voss (2001). By contrast, the rarest marsupials were Philander opossum (Linnaeus, 1758) (N = 1), Gracilinanus emiliae (N = 2) and Didelphis imperfecta (Mondolfi & Pérez-Hernández, 1984) (N = 3). Philander opossum is recorded commonly in the Amazon (Patton et al. 2000PATTON, J.L., DA SILVA, M.N.F. & MALCOLM, J.R. 2000. Mammals of the Rio Juruá and the evolutionary and ecological diversification of Amazonia. Bulletin of the American Museum of Natural History 244:1-306.), although only one individual was trapped in the present study. While this may reflect the local rarity of the species, limitations of the sampling effort cannot be ruled out. Two marsupials, D. imperfecta and Echimys chrysurus (Zimmermann, 1780), were recorded in the region for the first time, extending their known geographical distributions (Faria and Melo 2017FARIA, M.B. & MELO, F.R. 2017. Didelphis imperfecta, Didelphimorphia, Didelphidae (Mondolf & Pérez-Hernández, 1984): a new record in the Brazilian Amazon. Boletim da Sociedade Brasileira de Mastozoologia 79: 44-46.).

A majority of the species of the orders Cingulata and Pilosa were distributed homogeneously among the areas surveyed, with the nine-banded armadillo (Dasypus novemcinctus (Linnaeus, 1758)) and the greater long-nosed armadillo (Dasypus kappleri (Krauss, 1862) being the most frequent. The silky anteater (Cyclopes didactylus (Linnaeus, 1758)) was the rarest member of the Pilosa, which is probably related to the fact that this species is extremely difficult to locate, due to its cryptic, nocturnal and arboreal behavior, and the fact that it rarely descends to the ground (Medri et al. 2011MEDRI, I.M., MOURÃO, G.M. & RODRIGUES, F.H.G. 2011. Ordem Pilosa (N.R. Reis, A.L. Peracchi, W.A. Pedro & I.P. Lima eds.). Mamíferos do Brasil, 2ª Edição, Londrina, Paraná, p. 91-106.). These characteristics, together with the dense vegetation of most of the STNF, may have limited visibility in the extreme, although the species was encountered in riverside habitats (Moura and Sapucuá), where much of the forest is regenerating.

Sloths were also recorded rarely, being found primarily during wildlife rescue operations, prior to planned deforestation for mining. Some sloths have also been rescued from the railroad track that crosses part of the natural forest. This scarcity of records reflects the cryptic coloration and behavior of the sloths, which may be difficult to spot in the high canopy of STNF, despite their relatively large size (for an arboreal mammal).

The diversity of Amazonian primates is among the greatest in the world (Rylands and Mittermeier 2009RYLANDS, A.B. V.G. R.A. MITTERMEIER. 2009. The diversity of the New World primates (Platyrrhini): An annotated taxonomy, (P.A. Garber, A. Estrada, J.C. Bicca-Marques, E.W. Heymann V.G. & K.B. Strier, eds.). South American Primates: comparative perspectives in the study of behavior, ecology and conservation. Springer, New York, USA, p. 23-54.; Mittermeier et al. 2013MITTERMEIER, R.A. , RYLANDS, A.B. & WILSON, D.E. 2013. Handbook of the Mammals of the World. Vol. 3. Primates. Barcelona, Spain: Lynx Edicions, p.951), and more than half the biome's primate genera are found in the Saracá-Taquera National Forest. The bearded saki (Chiropotes sagulatus), bearded capuchin (Sapajus apella), Guianan red howler monkey (Alouatta macconnelli (Elliot, 1910)) and the Guianan spider monkey (Ateles paniscus (Linnaeus, 1758)) were the species encountered most frequently. The ecology of the bearded saki and Martin's bare-face tamarin (Saguinus martinsi (Thomas, 1912)) has been monitored in STNF since 2009, and a number of important findings in the area have already been published (Barnett et al. 2012BARNETT, A.A., BOYLE, S.A., NORCONK, M.N., PALMINTER, S., SANTOS, R.R., L.M. VEIGA, L.M., ALVIM, T.H.G. & BOWLER, M. 2012. Terrestrial activity in Pitheciins (Cacajao, Chiropotes, and Pithecia). American Journal of Primatology 74(12): 1106-1127.; Melo et al. 2013MELO, F.R., MOREIRA, L.S., MOURA, V.S., CARDOSO, T., ALVIM, T.H.G., FILO, A.L., SILVA, L.P. & OLIVEIRA, A.F. 2013. Ecology and behaviour of two groups of Chiropotes sagulatus inhabiting areas under different pressures of mining in the Saracá-Taquera National Forest, Pará, Brazil; pp.94, in: Program of the 36th meeting of the American Society of Primatologists, San Juan, Puerto Rico.; Boyle et al. 2015BOYLE, S.A., THOMPSON, C.L., DELUYCKER, A., ALVAREZ, S.J., ALVIM, T.H.G., AQUINO, R., BEZERRA, B.M., BOUBLI, J.P. et al., 2015. Geographic comparison of plant genera used in frugivory among the Pitheciids Cacajao, Callicebus, Chiropotes, and Pithecia. American Journal of Primatology 78(5): 493-506.; Shaffer et al. 2015SHAFFER, C.A., BARNETT, A.A., GREGORY, T., MELO, F., MOREIRA, L., ALVIM, T.H.G., MOURA, V., FILÓ, A., CARDOSO, T., PORT-CARVALHO, M., SANTOS, R.R. & BOYLE, S.A. 2015. Mixed-species associations in cuxiús (Genus Chiropotes). American Journal of Primatology 78(5): 583-597.).

The order Carnivora had the largest number of endangered species. The bush dog (Speothos venaticus (Lund, 1842)) was the rarest carnivore in the region, being visualized on only a few occasions by other research teams working in STNF. While the bush dog has an ample distribution and is considered to be a habitat generalist, it appears to be naturally rare in most areas in which it is found (Dematteo et al. 2011DEMATTEO, K., MICHALSKI, F. & LEITE-PITMAN, M.R.P. 2011. Speothos venaticus. IUCN Red List of Threatened Species. Accessed at http://iucnredlist.org (último acesso em 30/08/2016)
http://iucnredlist.org... ). The top predators, the jaguar (Panthera onca (Linnaeues, 1758)) and the cougar (Puma concolor (Linnaeus, 1771)), were recorded on most of the plateaus surveyed, including areas of habitat recuperation. The other carnivore species had a more irregular distribution within the study area.

Aquatic mammals of the orders Cetardiodactyla and Sirenia were recorded mainly during transit to the sampling points at Moura and Sapucuá, during the 2009-2010 survey. In 2011, in addition, the Amazonian manatee was monitored more directly at these sites, in particular Sapucuá Lake. At the same time, conflicts were observed between members of the local riverside communities and the dolphins, due to their attempts to retrieve fish caught in fishing nets, a behavior also observed in other regions (Loch et al. 2009LOCH, C., MARMONTEL, M. & SIMÕES-LOPES, P.C. 2009. Conflicts with fisheries and intentional killing of freshwater dolphins (Cetacea: Odontoceti) in the Western Brazilian Amazon. Biodiversity and Conservation 18(14): 3979-3988.).

Ungulates (orders Perissodactyla and Cetartiodactyla) were common in the study area, and were abundant in areas of habitat recuperation. The Amazonian brown brocket deer (Mazama nemorivaga (Cuvier, 1817)) was recorded recently in the region, with its presence being confirmed by experts, indicating the need for a taxonomic review of this and a number of other species (mainly rodents) recorded in STNF. Other ungulates, such as the peccaries (Pecari tajacu (Linnaeus, 1758) and Tayassu pecari (Link, 1795)), were recorded on a number of different plateaus and, together with the tapir (Tapirus terrestris (Linnaeus, 1758)), may play a unique, and vitally important functional role in the local ecosystem (Calaça 2014CALAÇA, A.M. 2014. Padrões de distribuição local e de diversidade funcional de mamíferos na Amazônia Central. Tese de doutorado do Programa de Pós-graduação em Ecologia. Universidade Federal do Rio de Janeiro, Rio de Janeiro. 167p.).

The order Rodentia was represented by some of the most abundant species found in the study area, such as the red-rumped agouti (Dasyprocta leporina (Linnaeus, 1758)) and the red acouchi (Myoprocta acouchy (Erxleben, 1777)). Both these species were common, and were recorded frequently within the study area, especially as, when they detect the presence of researchers, these animals emit a characteristic alarm vocalization before fleeing (Eisenberg and Thorington 1973EISENBERG, J.F. & THORINGTON, W. 1973. A preliminary analysis of a Neotropical mammal fauna. Biotropica 5(3): 150-161.; De Thoisy et al. 2008DE THOISY, B., BROSSE, S. & DUBOIS, M.A. 2008. Assessment of large-vertebrate species richness and relative abundance in Neotropical Forest using line-transect censuses: what is the minimal effort required? Biodiversity and Conservation 17(11): 2627-2644.). The most common small rodents were Cuvier's spiny rat, Proechimys cuvieri (Petter, 1978) and the large-headed rice rat (Hylaeamys megacephalus (Fischer, 1814)), which were both common and widespread (Patton, et al. 2015PATTON, J.L., PARDIÑAS, U.F.J. & D'ELÍA, G. (eds.). 2015. Mammals of South America, vol. 2. Rodents. University of Chicago Press, Chicago, Illinois. 1336 pp. ISBN 978-0-226-16957-6, price (hard cover).). Other rodents were distributed more irregularly within the study area.

The order Lagomorpha, represented by a single species in Brazil, the tapeti (Sylvilagus brasiliensis (Linnaeus, 1758)), was only recorded in the study region through interviews, and most local residents, in particular the younger individuals, are unfamiliar with the species. Although the tapeti is common and widely distributed (Diersing 1981DIERSING, V.E. 1981. Systematic status of Sylvilagus brasiliensis and S. insonus from North America. Journal of Mammalogy 62(3): 539-556.), it is possible that it may be very rare in the study area, or has become locally extinct.

The mammalian fauna of the Saracá-Taquera National Forest is rich and diverse, with at least as many species as most other, similar areas that have been surveyed in the Amazon biome (George et al. 1988GEORGE, T.K., MARQUES, S.A., VIVO, M., BRANCH, L.C., GOMES, N. & RODRIGUES, R. 1988. Levantamento de mamíferos do Parna Tapajós. Brasil Florestal 63: 33-41.; Calouro 1999CALOURO, A.M. 1999. Riqueza de mamíferos de médio e grande porte do Parque Nacional da Serra do Divisor (Acre, Brasil). Revista Brasileira de Zoologia 16 (2): 195-213.; Marques-Aguiar et al. 2003MARQUES-AGUIAR, S.A., MELO, C.C.S., AGUIAR, G.F.S. & QUEIROZ, J.A.L. 2003. Levantamento preliminar da mastofauna da região da Anajás-Muaná, Ilha de Marajós, Pará, Brasil. Revista Brasileira de Zoologia 19(3): 841-854.; Pontes et al. 2008PONTES, A.R.M., T. SANAIOTTI & W.E. MAGNUSSON. 2008. Mamíferos de Médio e grande porte, (M.L. Oliveira, F.B. Baccaro, R. Braga-Neto & W.E. Magnusson, eds.). Reserva Ducke - a bidiversidade amazônica através de uma grade. Attema Designe Editorial, Manaus, MA, p. 51-61.; Bergallo et al. 2012BERGALLO, H.G., CARVALHO, A.S. & MARTINS-HATANO, F. 2012. Médios e grandes mamíferos;, (F.D. Martins, A.F. Castilho, J. Campos, F.M. Hatano & S.G. Rolim, eds.). Fauna da Floresta Nacional de Carajás: estudos sobre vertebrados terrestres. São Paulo, p. 180-195.; Santos and Mendes-Oliveira 2012Santos, F.S. V.G. A.C. Mendes-Oliveira. 2012. Diversidade de mamíferos de médio e grande porte da região do rio Urucu, Amazonas, Brasil. Biota Neotropica 12(3): 282-291 http://www.biotaneotropica.org.br/v12n3/en/abstract?inventory+bn02712032012 (último acesso em 27/08/2012)
http://www.biotaneotropica.org.br/v12n3/... ). While some other regions in the Amazon may have higher species richness, reinforcing their priority for conservation (Oliveira et al., 2016OLIVEIRA, T.G., MAZIM, F.D., VIEIRA, O.Q., BARNETT, A.P.A., SILVA, G.N., SOARES, J.B.G., SANTOS, J.P., SILVA, V.F., ARAÚJO, P.A., TCHAIKA, L. & MIRANDA, C.L. 2016. Nonvolant mammal megadiversity and conservation issues in a threatened central Amazonian hotspot in Brazil. Tropical Conservation Science, 1-16.), the relatively high species richness recorded in the present study emphasizes the importance of this environment for the maintenance of local and regional diversity. The ecological diversity found in the present study, in terms of habitat use and feeding adaptations, is vitally important for complementary coexistence at the community level. This diversity is essential for balanced community structure and efficient ecosystem functioning (Walker 1992Walker, B.H. 1992. Biodiversity and ecological redundancy. Conservation Biology 6(1): 18-23.).

Acknowledgements

We thank the ICMBio for the authorization for the execution of the study at Saracá-Taquera National Forest. The Mineração Rio Norte (MRN) S.A., STCP Project Engineering LTDA and EcoSystema for the financial and structural support which were essential to the development of the work, as well as to all the people who collaborated with data collection in the field, in particular D. Ferraz, A. Valle, H. Moura and Da Mata, P.

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