OCUPAÇÃO DE PREDADORES TOPO DE CADEIA E DE SUAS PRESAS EM UMA PAISAGEM HETEROGÊNEA NO CERRADO

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1 UNIVERSIDADE FEDERAL DE UBERLÂNDIA PROGRAMA DE PÓS-GRADUAÇÃO EM ECOLOGIA E CONSERVAÇÃO DE RECURSOS NATURAIS OCUPAÇÃO DE PREDADORES TOPO DE CADEIA E DE SUAS PRESAS EM UMA PAISAGEM HETEROGÊNEA NO CERRADO LUCAS ISSA 2017 Uberlândia, MG

2 OCUPAÇÃO DE PREDADORES TOPO DE CADEIA E DE SUAS PRESAS EM UMA PAISAGEM HETEROGÊNEA NO CERRADO Dissertação apresentada à Universidade Federal de Uberlândia, como parte das exigências para obtenção do título de Mestre em Ecologia e Conservação de Recursos Naturais. Orientadora: Prof.ª Dra. Natália Mundim Tôrres Uberlândia Fevereiro de 2017 Lucas Issa

3 Dedicado ao meu primo, Danilo (in memoriam). Espero que você ainda esteja vendo a vida através dos meus olhos. Dedico também a todos os animais do IOP!

4 AGRADECIMENTOS Dissertações e teses, apesar de levarem o nome de apenas uma pessoa na capa, são na verdade o fruto de um imenso trabalho em equipe. Trabalho que envolve conhecer não apenas um objeto de estudo, mas conhecer um ao outro e aprender a ser forte junto, e não sozinho. Não poderia começar essa seção sem agradecer aos meus amigos de campo, com quem tanto aprendi e cresci como biólogo e como pessoa. Ananda, Gi, Thomas (Curau) e Maysa, vocês são parte deste fundamental desse trabalho, e eu não teria chegado aqui sem vocês. Vocês são as melhores companhias que eu poderia ter no meio do mato. Muito obrigado! Agradeço imensamente a todo o apoio oferecido pelo Instituto Onça-Pintada e pelas pessoas do Leandro e da Anah. Obrigado por compartilharem tanto do conhecimento e da experiência de vocês! Obrigado também ao Tiago, que me proporcionou tantas risadas! Agradeço à Natália, por ter aceitado me orientar nessa difícil jornada e por suas considerações ao meu trabalho. Agradeço aos membros da banca, Prof. Paulo De Marco, Prof.ª Kátia Facure e Prof.ª Natália Leiner, por terem aceitado participar da minha banca e pelas contribuições que farão ao meu trabalho. Agradeço à Poliana, por tudo o que me ensinou e pela paciência enorme com as minhas dúvidas e desesperos. Ao Paulinho e ao André, do MetaLand, por suas boas ideias ao meu trabalho e por estarem sempre dispostos a ajudar, obrigado! Meu reconhecimento também ao Programa de Pós-Graduação da Universidade Federal (em especial aos professores, por todo o aprendizado), e à CAPES pelo apoio financeiro. Agradeço ao Rafa (Ceará), por suas incríveis contribuições e revisões no meu texto. Muito obrigado por sua ajuda enorme!

5 Ao pessoal da pós: Meu muito obrigado à Claire, por seu carinho e ajuda sinceros; ao Pitilin, pela boa convivência e amizade nesses dois anos no ap 102 (ainda sem nome oficial), valeu, cara!; à Karen Neves (que dispensa comentários); às migas Bia (apoio logístico toda hora) e Liégy (suas loucas!!); aos melhores vizinhos, Lino e Adilson; à Teté, sempre querida; ao Carioca, Vitão, Ingrid, Gudryan, Drielly, Vinícius, Kaká, Luana, Regiane, Marcela, Helen, Jonas, Uiara, Dimas, Tito, e tooodos os outros por todos os bons momentos. Aos meus companheiros de laboratório: Mardiany, Marcela, Lucas xará, Letícia e Aline, que tanto ajudaram nas tarefas esgotantes. Aproveito e agradeço também a todos os estagiários e estudantes que passaram pelo IOP: Shannon, Saul, Danilo, Ennio, André, Ana Rita... são tantos! Desejo um futuro brilhante a todos vocês. Agradeço com muito amor aos meus pais, Mírian e Marco Antônio, por todo o amor de vocês, por apostarem e acreditarem em mim e por me apoiarem tanto, sempre. Cada sonho realizado é por vocês! E aos meus irmãos, Maria Clara e Matheus, meus companheiros de vida de quem eu sinto tanto orgulho! Aos amigos/irmãos de longa data: Cyrce, Max, Fernando, Paulista, Marco Túlio, e também todo o pessoal da antiga Rep. Integração (e agregados). Vocês são parte de mim. Ao Leonel, por expandir meus horizontes. Tenho certeza de que você estará sempre aí! E por último e sim, mais importante, talvez ao Bené, que foi quem me mostrou o mundo lá fora tantas vezes que já nem sei mais... Foi ruim? Foi ótimo!!!!!

6 ÍNDICE Resumo...ii Abstract...iii Introdução Geral...1 Referências Bibliográficas...4 Manuscript Folder...5 Introduction...10 Methods...13 Study Area and Land Use Classification...13 Camera Trapping...15 Species Selection...16 Occupancy Modeling...17 Results...18 Discussion...19 Conclusions...24 References...25 Supplementary Material...41 Tables...41 Figures...46

7 ii RESUMO Issa, L Ocupação de predadores topo de cadeia e de suas presas em uma paisagem heterogênea no Cerrado. Dissertação de Mestrado em Ecologia e Conservação de Recursos Naturais. UFU. Uberlândia-MG. 55p. As espécies respondem de diferentes formas às variações no ambiente. Algumas são generalistas e podem ocorrer em diferentes tipos de vegetação, enquanto especialistas possuem distribuição limitada. O Cerrado brasileiro apresenta uma alta diversidade de ambientes que permitem a ampla distribuição espacial da fauna de médio e grande porte. A conversão da vegetação natural em agropecuária, no entanto, reduziu consideravelmente a disponibilidade de ambientes naturais para as espécies nativas. Algumas espécies generalistas são capazes de utilizar os recursos oferecidos por paisagens agrícolas e persistir nesses locais. Conflitos entre fauna silvestre e agroprodutores são comuns devido aos prejuízos econômicos ocasionados pela presença de grandes herbívoros em lavouras. Predadores topo de cadeia são elementos fundamentais na manutenção da biodiversidade nessas paisagens, pois controlam as populações de herbívoros e mantém a estrutura dos ecossistemas. Contudo, grandes carnívoros estão mais vulneráveis à extinção. Consequentemente, compreender como esses animais se distribuem em paisagens agrícolas é fundamental para o estabelecimento de estratégias para a conservação da biodiversidade. Os objetivos deste trabalho foram entender como os diferentes tipos de vegetação nativa e a agricultura influenciam na presença local de predadores topo de cadeia (onça-pintada e onça-parda) e de suas presas (tamanduá-bandeira, cateto, queixada, veado-campeiro, anta e ema) em uma paisagem heterogênea no Cerrado. O estudo foi feito no Parque Nacional das Emas, uma das principais áreas protegidas do bioma, e na região do seu entorno. Foram utilizados dados de presença e ausência das espécies obtidos a partir de armadilhamento fotográfico realizado na região entre julho e dezembro de Os efeitos dos diferentes tipos de vegetação sobre esses dados foram testados utilizando modelos de ocupação, levando em consideração as diferenças de detectabilidade entre os locais amostrados. Não foram observados efeitos dos diferentes tipos de vegetação sobre a presença dos predadores. Veados-campeiros e emas estiveram restritos a áreas de campo nativo e de agricultura. Antas e queixadas apresentaram distribuição generalista, enquanto catetos estão associados a áreas de agricultura anual, possivelmente como resultado de exclusão competitiva por queixadas. A diversidade de ambientes na região do Parque Nacional das Emas aumenta a diversidade de microhabitats disponíveis, e permite que várias espécies se estabeleçam na paisagem. Especialistas de áreas campestres estão limitados a área do Parque, e a conectividade com as lavouras do entorno é importante para evitar o isolamento de suas populações. Generalistas se beneficiam da heterogeneidade ambiental e são mortos em retaliação aos danos causados às lavouras. A fraca relação de onçaspintadas e pardas com os tipos de vegetação podem ser explicados pela ampla disponibilidade de presas na paisagem heterogênea. Assim, a diversidade de ambientes pode ser benéfica para a persistência de predadores topo de cadeia em áreas nãoprotegidas. Por fim, tamanduás-bandeira também apresentaram fraca associação aos tipos de vegetação, e sua ocorrência na região pode estar sendo restrita por outros fatores, como a incidência de queimadas no Parque, os atropelamentos em rodovias do entorno, e a presença de predadores. Palavras-chave: espécies generalistas; predadores topo de cadeia; paisagens agrícolas; heterogeneidade ambiental; modelo de ocupação

8 iii ABSTRACT Issa, L Apex predators and prey occupancy in a heterogeneous landscape in Cerrado. MSc Thesis. UFU. Uberlândia-MG. 55p. Species can respond to environment variation in several ways. Generalist species can occur in different vegetation types, while specialists present limited distribution patterns. The Cerrado Biome presents a wide set of environments, allowing for broad distribution of its medium and large-sized fauna. However, the conversion of natural vegetation into cropland and pastures has considerably reduced natural environments availability for native species. Some generalist species are capable of utilizing cropland resources and persist in such places. Conflicts between wildlife and farmers rise in these landscapes due to the economical injure caused by large herbivores. Apex predators are keystone species in keeping biodiversity in non-protected areas, as they control herbivores populations and maintain ecosystems structure. Despite of this, large carnivore species are more vulnerable to extinction. Consequently, to comprehend how these animals are distributed in agricultural landscapes is fundamental to the establishment of effective conservation strategies. In this study we aimed to observe how different native vegetation types and crops affect the local presence of apex predators (jaguar and cougar) and their prey (giant anteater, collared peccary, white-lipped peccary, pampas deer, tapir and rhea) in a heterogeneous landscape in Cerrado. The study took place in Emas National Park, one of Cerrado s largest and most important protected areas, and its surrounding region. We used presence/absence data obtained from a camera trap sampling that occurred from July to December The effect of the different vegetation types on this dataset through occupancy modeling, a method that takes detectability differences between sampling sites into account. We did not detect a relation between predator species presence and vegetation types. Pampas deer and rhea were restricted to open fields and cropland areas. Tapirs and white-lipped peccaries presented generalist distribution, while collaredpeccaries were associated to annual croplands, possibly as a result of competition displacement by white-lipped peccaries. The different environments in Emas National Park region enhances microhabitats availability and allows a rich community to be established within the landscape. Grassland specialists are restricted to the Park area, and the permeable croplands in the surrounding region are important to avoid their population isolation. Generalists benefit from environmental heterogeneity and are killed in retaliation for the cropland damage. The weak relation between jaguars and cougars to the vegetation types may be therefore explained by the landscape-wide prey availability. Thus, environmental diversity may be beneficial for apex predators persistence in nonprotected areas. Lastly, giant anteaters also presented weak relationship to the vegetation types, and their occurrence in the region may be constrained by other factors, such as the constant wildfires in Emas National Park, the intense road traffic in the surrounding region, and the predators presence. Keywords: generalist species; apex predators; agricultural landscapes; environmental heterogeneity; occupancy modeling

9 1 INTRODUÇÃO GERAL Dois diferentes conceitos básicos podem ser compreendidos a partir da teoria de nicho ecológico. O primeiro, chamado nicho fundamental, se refere às condições ambientais que permitem que uma espécie sobreviva em um determinado local, enquanto o outro, o nicho realizado, prediz o espectro de condições nas quais essa espécie pode de fato estar presente considerando todas as restrições à sua ocorrência, incluindo a disponibilidade de recursos e suas interações ecológicas (Hutchinson, 1957). Baseado nesses conceitos, as espécies podem ser compreendidas a partir do quanto toleram as alterações na disponibilidade de recursos e nas condições ambientais ao longo do espaço (Levins, 1968; Colwell e Futuyma, 1971). Assim, as espécies podem responder diferentemente à heterogeneidade nas paisagens, onde generalistas se beneficiam de ambientes altamente diversos, enquanto especialistas concentram sua distribuição em ambientes homogêneos (Futuyma e Moreno, 1988; Kassen, 2002). Alguns Biomas apresentam alta diversidade ambiental em sua extensão e são bons sistemas para compreender a distribuição espacial de especialistas e generalistas. O Cerrado, um Bioma savânico neotropical, é constituído por uma variedade de tipos de vegetação (i.e., fitofisionomias), incluindo campos de gramíneas, savanas arbustivas e matas densas (Oliveira-Filho e Ratter, 2002; Ribeiro e Walter, 2008). Esses diferentes ambientes permitem que uma ampla gama de recursos esteja disponível na paisagem, resultando em complexos mosaicos capazes de abrigar maior biodiversidade (Johnson et al., 1999; Oliveira-Filho e Ratter, 2002). Como previsto em ecossistemas heterogêneos, a fauna de médio e grande porte do Cerrado é composta em sua maioria por espécies generalistas, capazes de ocupar as diferentes fitofisionomias do Bioma, embora

10 2 especialistas também ocorram em ambientes específicos (da Fonseca and Robinson, 1999; Marinho-Filho et al., 2002). O Cerrado, contudo, é um dos Biomas mais ameaçados do Brasil devido à sua importância agropecuária, e estima-se que 38,9% de sua área natural já tenha sido perdida para atividades antrópicas (Cavalcanti e Joly, 2002; Klink e Moreira, 2002; Sano et al., 2010). Como resultado dessa intensa fragmentação, manchas de vegetação nativa se isolam e a disponibilidade de recursos nas paisagens é alterada, modificando assim os padrões de distribuição das espécies (Franklink e Lindenmayer, 2009; Barreto et al., 2012). Espera-se que espécies generalistas se beneficiem desses processos devido às suas capacidades de utilizar os recursos oferecidos pela matriz (Reyna-Hurtado e Tanner, 2007; Lyra-Jorge et al., 2010). No entanto, alterações na distribuição dos recursos e das espécies nas paisagens podem ser prejudiciais aos ecossistemas, e consequências associadas a esses processos incluem a extinção local de espécies e a perda de serviços e processos ecológicos (McKinney e Lockwood, 1999; Valiente-Banuet et al., 2014; Galetti et al., 2015). Conflitos entre fauna selvagem e produtores rurais também podem surgir neste contexto, onde herbívoros e carnívoros são mortos em retaliação aos danos causados às lavouras e rebanhos (Jácomo, 2004; Silveira et al., 2008; Marchini e Crawshaw, 2015). Compreender como as espécies animais respondem aos processos e dinâmicas dos agrossistemas é fundamental para evitar esse cenário de perda de espécies e de conflito entre conservação e produção agropecuária. Adicionalmente, é necessário entender o papel de predadores topo de cadeia nesses sistemas devido à importância do grupo no controle das populações de presas e, consequentemente, na estrutura das paisagens (Ripple et al., 2001; Terborgh et al., 2001; Estes et al., 2011). Predadores topo de cadeia são também mais vulneráveis à extinção por atividades humanas (Morato et al., 2013; Ripple et al., 2014). Desta forma, é necessário considerar a importância de agrossistemas

11 3 em propriedades privadas para a persistência desses animais em áreas não-protegidas. Matrizes agrícolas permeáveis à fauna permitem a conectividade entre áreas protegidas e amortecem as mesmas de efeitos de borda, mantendo alta biodiversidade local e regional (Ricketts, 2001; Hansen and DeFries, 2007; Perfecto and Vandemeer, 2010; Boron et al., 2016). Logo, a implementação de matrizes capazes de oferecer recursos e refúgio à vida silvestre e que permitam o fluxo de espécies entre manchas de vegetação nativa é uma ação de manejo fundamental para a conservação da biodiversidade (Perfecto and Vandemeer, 2010). Modelos de ocupação são ferramentas úteis para compreender como a presença de predadores e presas se relaciona a diferentes variáveis ambientais, incluindo aos diferentes tipos de vegetação e matrizes (MacKenzie et al., 2002). Estes modelos pressupõem que existem diferenças nas probabilidades de detecção das espécies entre os locais amostrados, e fornecem, então, estimativas mais precisas dos valores de ocupação das espécies (MacKenzie et al., 2002). Adicionalmente, tais modelos utilizam valores de detecção/ não-detecção das espécies e não necessitam da individualização dos animais registrados, garantindo menores custos e maior flexibilidade dos métodos usados na obtenção dos dados (MacKenzie et al., 2002; MackKenzie e Nichols, 2004; O Connell e Bailey, 2011). Portanto, modelos de ocupação são frequentemente a única opção viável para estudos de distribuição de espécies raras, como onças-pintadas. No presente estudo, foram utilizados modelos de ocupação com o objetivo de entender como os diferentes tipos de vegetação nativa e agricultura em uma área protegida no Cerrado e na região do seu entorno afetam a presença local de predadores topo de cadeia e de suas presas.

12 4 REFERÊNCIAS BIBLIOGRÁFICAS Barreto, L., Van Eupen, M., Kok, K., Jongman, R.H., Ribeiro, M.C., Veldkamp, A.,... & Oliveira, T.G. (2012). The impact of soybean expansion on mammal and bird, in the Balsas region, north Brasilian Cerrado. Journal for Nature Conservation, 20(6), Boron, V., Tzanopoulos, J., Gallo, J., Barragan, J., Jaimes-Rodriguez, L., Schaller, G., & Payán, E. (2016). Jaguar densities across human-dominated landscapes in Colombia: the contribution of unprotected areas to long term conservation. PloS one, 11(5), e Cavalcanti, R. B., & Joly, C. A. (2002). Biodiversity and conservation priorities in the Cerrado region. The Cerrados of Brazil. Ecology and Natural History of a Neotropical Savanna, Colwell, R. K., & Futuyma, D. J. (1971). On the measurement of niche breadth and overlap. Ecology, 52(4), da Fonseca, G. A., & Robinson, J. G. (1990). Forest size and structure: competitive and predatory effects on small mammal communities. Biological conservation, 53(4), Estes, J. A., Terborgh, J., Brashares, J. S., Power, M. E., Berger, J., Bond, W. J.,... & Marquis, R. J. (2011). Trophic downgrading of planet Earth. science, 333(6040), Franklin, J. F., & Lindenmayer, D. B. (2009). Importance of matrix habitats in maintaining biological diversity. Proceedings of the National Academy of Sciences, 106(2),

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17 9 APEX PREDATOR AND PREY OCCUPANCY IN A HETEROGENEOUS LANDSCAPE IN CERRADO Authors: Lucas Issa, Giselle Bastos Alves, Ananda Barban, Thomas Giozza, Poliana Mendes, Rafael Rios Moura, Natália Mundim Tôrres, Anah Tereza de Almeida Jácomo and Leandro Silveira Texto formatado segundo as normas da revista Landscape Ecology.

18 10 INTRODUCTION Ecological niche theory is a central topic in ecology. Hutchinson (1957) has stablished the concept of fundamental niche as the range of environmental conditions that allows a species to survive in a given area, while the realized niche is the range of environmental conditions in which it actually survives considering all the constraints to its occurrence. This theory is the basis for understanding how species respond to the ecological variations along their range, including the differences in how much they tolerate environmental and resource availability alterations over space (Levins, 1968; Colwell and Futuyma, 1971). Based on their niche breadth species are therefore classified as specialists if they depend on specific conditions or resources, and as generalists if they tolerate wide environmental variation (Colwell and Futuyma, 1971; Futuyma and Moreno, 1988). Niche breadth may provide predictions about the consequences of habitat heterogeneity on species distribution (Gehring and Swihart, 2003; Slatyer et al., 2013). Specialists are expected to benefit from homogenous environments, whereas generalists should benefit from high environmental heterogeneity (Futuyma and Moreno, 1988; Kassen, 2002). Thus, the distribution of generalists and specialists in a landscape may depend on how diverse it is. A landscape, in fact, is defined as a heterogeneous mosaic with a wide range of different habitats, and each of them has a unique structure with a different set of accessible resources (Metzger, 2001). Some Biomes may actually present a wide range of environmental variation and microhabitats along their landscapes, such as the Brazilian Savanna (hereafter the Cerrado) (Oliveira-Filho and Ratter, 2002; Ribeiro and Walter, 2008). The Cerrado is constituted by a great diversity of vegetation types, which greatly contrast in their structure, conditions and resource availability. These

19 11 habitats can vary from forestry, to savanic and grassland structure (e.g. grassland fields, scrublands, gallery forests and palm tree savanna wetlands) and also differ in several other aspects, like elevation, terrain roughness and watercourse dependency and proximity (Ribeiro and Walter, 2008). Therefore, Cerrado s complex landscapes with great niche availability house high species diversity (Johnson et al., 1999; Oliveira-Filho and Ratter, 2002). This mosaic provides a good framework to evaluate the effects of highly diverse landscapes on the distribution of specialist and generalist species. The medium and large-sized fauna of Cerrado (i.e. over one kilogram, according to Chiarello, 2000) is composed of a rich species community with distinct resource use strategies. Most of these species are habitat generalists, but specialists are also present to a lesser degree, especially in forests (da Fonseca and Robinson, 1999; Marinho-Filho et al., 2002; Comparatore and Yagueddú, 2016). As an example, Alves et al. (2014) investigated the mammalian fauna within a Cerrado fragment and found that most species presented generalist habitat use, occupying both forests and savannas, while a minority of species were limited to either habitat type. Therefore, the medium and large-sized fauna can be distributed in Cerrado landscapes according to the different habitats availability and settings. Nonetheless, Cerrado landscapes have been highly fragmented since Brazilian government started investing in agricultural production in the late 1960s (Cavalcanti and Joly, 2002; Klink and Moreira, 2002). The farming sector plays a pivotal role in the country s economy and, consequently, 38.9% of the Biome s range has already been lost to human activities (Sano et al., 2010). The land conversion is responsible for altering spatial resource availability through the reduction of natural vegetation and increase of patches isolation, change in the physical and chemical properties of the soil and the presence of exotic species (Franklin and Lindenmayer, 2009; Bennett and Saunders,

20 ; Lira et al., 2012). Such habitat alteration may differently affect species distribution and have negative effects on specialist species (Thuiller et al., 2005; Devictor et al., 2008; Barreto et al., 2012; Slatyer et al., 2013). Otherwise, some generalist species may thrive in human-altered environments due to their capacity of using the matrix resources and persisting in highly altered habitats, like collared peccaries (Dotta and Verdade, 2007; Reyna-Hurtado and Tanner, 2007; Lyra-Jorge et al., 2010). In addition, some generalists may also benefit from anthropic disturbance due to reduction of competition and predation in those areas (da Fonseca and Robinson, 1999). This ecological release may result in biotic homogenization and the loss of biodiversity and ecological interactions, services and processes (McKinney and Lockwood, 1999; Marvier et al., 2004; Valiente- Banuet et al., 2014; Bello et al., 2015; Galetti et al., 2015). Moreover, conflicts between wildlife and farmers may arise in lands where croplands are intensively consumed by herbivores (Jácomo, 2004; Nyhus and Tilson, 2004; Marchini and Crawshaw, 2015). Apex predators, which may be the source of conflict to livestock farming, may play the opposite role in agricultural lands, where they control herbivores populations (Newsome, 1990; Jácomo, 2004; Lindsey et al., 2005; Skonhoft, 2006; Silveira et al., 2008; Wallach et al., 2010). Predators are keystone species, and their local extinction may have top-down effects on food web (Ripple et al., 2001; Terborgh et al., 2001; Estes et al., 2011). Therefore, their conservation is a relevant approach for keeping Neotropical ecosystems function and dynamics (Jorge et al., 2013; Ripple et al., 2014). Despite their importance, apex predators are also more vulnerable to extinction by human activities, especially habitat loss for anthropization (Azevedo et al., 2013; Morato et al., 2013; Ripple et al., 2014). The jaguar (Panthera onca), for example, is classified as Vulnerable in the Brazil Red Book of Threatened Species of Fauna (MMA, 2016), and as Near Threatened according to IUCN Red List (Caso et al., 2008; IUCN, 2010). It is then

21 13 necessary to consider agroecosystems in private lands as critical habitats for both prey and predators, because high-quality matrixes allow connectivity and dispersal among core protected areas and buffer them from edge effects (Ricketts, 2001; DeFries et al., 2005; Hansen and DeFries, 2007; Perfecto and Vandemeer, 2010; Ripple et al., 2014; Boron et al., 2016). Habitable and permeable agroecosystems present an opportunity to allow human resource use and economic development, while species conservation is still promoted (Tscharntke et al., 2005; Perfecto and Vandermeer, 2010; Shackelford et al., 2015). The spatial distribution of prey and their predators may provide important information for the development of effective conservation strategies and for choosing priority conservation areas. They may also estimate the relevance of buffer zones on the species habitat use. Here, we investigated how different vegetation types in a Cerrado protected area and its surroundings affect the local presence of apex predator species and their prey. We used a hierarchical occupancy modeling to test the hypothesis that predators occurrence is related to dense vegetation, that generalist prey species occupy cropland areas and that specialist prey species are limited to natural vegetation types. METHODS Study Area and Land Use Classification The study area comprises Emas National Park (ENP) and its northern surrounding region (18º19 S; 52º45 W), in southwestern Goiás state (Figure 1). The region is under the influence of three different drainage basins and contains the headwaters of Araguaia and Taquari rivers, which respectively connects ENP to the Amazon and Pantanal Biomes. This hydrological network plays an important role for Cerrado species

22 14 conservation, as it works as an ecological corridor between these biomes (Silveira et al., 2014). The region is characterized by Tropical Savanna Climate (Aw/As) under Köppen climate classification (Köopen, 1884; Álvares et al., 2013). There are two dominant seasons throughout the year: a hot wet season from October to March, and a dry cold one, from April to September (Álvares et al., 2013). ENP is one of the Brazilian Cerrado s largest Conservation Units, covering an area of approximately 132,000 hectares. It is mainly composed of open grassland plains, maintaining one of the biggest continuous grasslands in the biome, while patches of scrublands and riparian forests compose the remaining extent of the Park (IBAMA, 2004). ENP northern surrounding region is a heterogeneous fragmented landscape, with a highly productive agricultural land where historical corn, soybean, cotton and, more recently, sugar cane crops are grown large-scale. The remnant vegetation is mostly riparian forest, with few patches of scrubland and grassland (Silveira, 2004). The vegetation types present in the landscape were classified in Quantum GIS software v (Quantum GIS Development Team, 2009). The habitat type map (Figure 1) was generated using two Landsat 8 satellite images (from June 06, 2013 and June 18, 2013) obtained from Brazilian Ministry of Environment. The mapping was made under the Quantum GIS complement Semi-Automatic Classification Plugin from Congedo (2016). We manually checked the habitat types by visual inspection on a scale of 1:15,000, and then identified and classified four main habitat types relevant for the studied species ecology: (1) open Cerrado vegetation, including grassland fields and campo sujo vegetation; (2) closed vegetation, including all dense structure natural formations, such as dense scrubland and forests; (3) perennial agriculture, for sugarcane crops; and (4) annual agriculture, comprising corn, soybean and cotton crops. Species with high mobility, such as the ones in this study, tend to respond to environmental

23 15 variations at coarser scales (Lyra-Jorge et al., 2010). For this reason, we created 2km radii buffers around the camera trapping points to account for the proportion of each habitat type in the sampling sites. Camera Trapping To model species occupancy, I used detection/ non-detection data from a camera trap dataset provided by Jaguar Conservation Fund (JCF), a Brazilian NGO that has been studying jaguars ecology and conservation in this region for over two decades (Silveira, 2004). JCF had deployed 34 camera trap stations in ENP and 7 stations in the Park s surroundings between July and December 2013, on a range-wide 3 x 3 km grid designed for jaguar population density studies (Silver, 2004; Sollmann et al., 2011). The cameras arrangement across the landscape is depicted in Figure 1. All the cameras used were Bushnell, NatureView Essential HD model, in the sole video or picture format or the hybrid video and picture format. All the cameras were located along roads and game trails, with the cameras strapped on trees or stakes at approximately 50 cm above ground. They were all programmed to work 24h/day during the sampling period and were checked every month for Memory Card and battery replacement. Some of the cameras installed were arranged in pairs in order to allow jaguar individuals identification. This difference in the detectability between camera stations should not affect the results as occupancy modelling already accounts for imperfect detections (MacKenzie et al., 2002). Five periods of 20 sampling days were selected as the survey periods for occupancy analysis. The camera sites and their respective functioning periods and number of cameras per site are listed in Table 1.

24 16 Species Selection The two largest felid species within the Americas are also Cerrado s top predators: the jaguar (Panthera onca) and the cougar (Puma concolor). Both species are able to survive in a wide range of habitats, although jaguars are known to depend mostly on dense-vegetation habitats close to watercourses and to avoid human-dominated landscapes (Azevedo and Murray, 2007; Zeller, 2007; Colchero et al., 2011; Sollmann et al., 2012; Arroyo-Arce et al., 2014). Cougars, however, are largely habitat generalists, being able to occupy drier areas and agricultural patches and to tolerate human presence (Culver, 2010; Sollmann et al., 2012; Zarco-González et al., 2012; Magioli et al., 2014). Both species act as opportunistic predators, preying upon the locally available medium and large-sized species in general (Logan & Sweanor, 2001; Astete et al., 2008; Cavalcanti and Gese, 2010). Thus, we selected for analysis the entire prey community registered in the study area, excluding only those species whose registration from camera trapping method was limited (e.g. arboreal and semi-arboreal species) and those species occurring in less than 20% or more than 80% of the sampling units, as required by occupancy modelling premises (Mackenzie et al., 2006). The six prey species present in the area selected for the analyses are the giant anteater (Myrmecophaga tridactyla), the collared peccary (Pecari tajacu), the white-lipped peccary (Tayassu pecari), the pampas deer (Ozotoceros bezoarticus), the lowland tapir (Tapirus terrestris) and the greater rhea (Rhea americana). The selection of species was made based on previous studies of jaguars and cougars feeding ecology in ENP region (Silveira, 2004; Sollmann et al.; 2013). The national and global conservation status of these species are listed in Table 2. The pampas deer and the greater rhea are open areas specialists (Codenotti and Alvarez, 2000; Silveira et al., 2008; Duarte et al., 2012). Giant anteaters are insectivorous mammals and similarly forage in open habitats, although they are also known for

25 17 occupying gallery forests to a lesser extent, usually for shelter, cooling or to search for water (Emmons et al., 2004; Medri and Mourão, 2005). Both peccary species and the lowland tapir are considered habitat generalists and can also use agricultural resources to some degree (Peres, 1996; Reyna-Hurtado and Tanner, 2007; Zeller et al., 2011; Cordeiro et al., 2016). Occupancy Modeling Occupancy models main function is to determine the probability of a certain location being occupied by a certain species under imperfect detectability conditions in order to avoid false absences (i.e. when a species occurs in the site but goes undetected) (MacKenzie et al., 2002; MacKenzie et al., 2003). It depends on detection/ non-detection data only, which can be obtained from methods with greater flexibility, less costly and/or with less sampling effort than abundance surveys (MacKenzie and Nichols, 2004; O Connell and Bailey, 2011). Hence, occupancy modeling is frequently the only viable option for rare species, and has been globally used to provide species distribution estimations (e.g. for apex predators Hines et al., 2010; Khorozyan et al., 2010; Thorn et al., 2011; Zeller et al., 2011; Alexander et al., 2015). This method applies maximum likelihood statistics on species detection histories obtained from repeated surveys across several sites to estimate the species naïve occupancy, occupancy (Ψ) and detectability (p) parameters. The naïve occupancy indicates the proportion of surveyed sites effectively occupied by species, occupancy is the probability that a site is occupied, and the detectability is the probability of detecting the species on a certain survey, given the species is present at the site. This information can also be related to landscape variables and provide valuable information about endangered animal species habitat use and

26 18 therefore effective management actions regarding their conservation (Burton et al., 2012; Farris et al., 2014; Santos et al., 2016). In order to perform the model in the study area, a set of 16 candidate models was built using the variables that were thought to influence species occurrence (i.e., closed and open vegetation, annual crops, and perennial crops). These models included one null hypothesis model with constant occupancy and detection, and the remaining 15 models included occupancy as a function of the covariates either individually or combined (Table 3). The models were fit in the PRESENCE software version 11.8 (Hines, 2006) to perform occupancy modeling statistics. The software supplied Akaike s Information Criterion (AIC) values and the differences in AIC (ΔAIC) among the models was used to evaluate which models provide the biggest empirical support for species occupancy. Models with ΔAIC < 2 have substantial empirical support, while those between 4 and 7 have less support and those with values > 10 have no support (Burnham and Anderson, 2004). RESULTS The camera trap sampling resulted in approximately recording hours of 44 native species of medium and large-sized vertebrates (two reptiles, seven birds, and 35 mammals) in Emas National Park and in its northern surroundings (Figure 2). Twelve of these species are listed to some degree of global threat (IUCN, 2010), and 11 of them are listed in Brazil Red List of Fauna (MMA, 2016). Six domestic species were registered in the region, including a horse, cats and dogs inside the Park. Table 2 contains a detailed list of the registered species, their respective conservation status and whether they were registered inside or outside ENP.

27 19 The naïve occupancy values varied between the focal species (Table 4). The lowland tapir and the pampas deer had the highest naïve occupancy values (77% both). The greater rhea and white lipped peccaries also occupied a great area (72 and 70%, respectively), while cougars, jaguars and anteaters were rarely registered (57, 42 and 37%, respectively). Collared peccaries had the lowest naïve occupancy values of all focal species (20%) and is therefore the rarest of the focal species. Table 4 lists the three best fitted models for each species and their respective AIC, ΔAIC and naïve occupancy values. There was no general model explaining the focal species presence. Rather, distinct species responded uniquely to the different vegetation types. Jaguars, cougars, giant anteaters and tapirs presences weren t mainly affected by any of the vegetation types. However, cougars positively responded to perennial crops in the second concurrent model. Likewise, tapirs also presented positive responses to native vegetation in general and to annual croplands. White-lipped peccaries presented generalist behavior and were positively related to all vegetation types, while collared peccaries were negatively affected by native vegetation and were more common in annual croplands. Pampas deer were present in open vegetation and annual cropland areas, and were constrained by closed vegetation and sugarcane crops. Rheas, like white-lipped peccaries, were associated to all vegetation types, although closed vegetation had negative effects in concurrent models. DISCUSSION The medium and large-sized fauna of Cerrado have distinct strategies to explore resources in natural vegetation types (da Fonseca and Robinson, 1999; Marinho-Filho et al., 2002). However, the high fragmentation of Cerrado vegetation since the 1960s

28 20 (Cavalcanti and Joly, 2002; Klink and Moreira, 2002), has negatively affected fauna distribution (Thuiller et al., 2005; Devictor et al., 2008; Barreto et al., 2012; Slatyer et al., 2013). Otherwise, some species have benefited from high resource availability in agricultural areas (Dotta and Verdade, 2007; Reyna-Hurtado and Tanner, 2007; Lyra- Jorge et al., 2010). In this study, we evaluated how different vegetation types of a Cerrado protected area and its surroundings influence medium and large-sized fauna distribution. We observed distinct species responses to the habitat types instead of a general pattern for the community. Distinct responses of species were expected, because Cerrado s medium and large-sized fauna is composed of both ecological generalists and specialists (Marinho-Filho et al., 2002; Comparatore and Yagueddú, 2016). Conserving different vegetation types within the landscape may increase the diversity of microhabitats available and, consequently, maintain high community richness, benefitting especially the generalists, but also specialists (Kassen, 2002). As expected, the grassland specialists (pampas deer and rhea) were positively associated to the open vegetation type. The populations of both species inside the park are, in fact, among the greatest populations within their distribution range (Redford, 1985; Rodrigues & Monteiro-Filho, 2000) because the park holds one of Cerrado s largest continuous grassland areas (IBAMA, 2004). Nevertheless, this vegetation is highly limited to the park area, while its surroundings are mainly composed of forests, thus limiting grassland specialists occurrence. Connectivity to other protected areas is consequently necessary to avoid the isolation and genetic bottleneck of these populations (Carlson, 2000; Öckinger et al., 2010; Furlan et al., 2012). Hence, the positive responses of pampas deer and rheas to croplands (especially annual croplands) may allow these species to persist in the region as crops may play the connectivity role in farmlands (Ricketts, 2001; Perfecto and Vandemeer, 2010; Ripple et al., 2014; Boron et al., 2016).

29 21 Oppositely, white-lipped peccaries presented generalist distribution, as described in literature (Reyna-Hurtado and Tanner, 2007), occupying both native vegetation and croplands, especially perennial crops. Herbivore species may use sugarcane crops as food and shelter, due to sugarcane plantations dense structure (Dotta & Verdade, 2007; Silveira, pers. comm.). On the other hand, collared peccaries, which are weaker competitors to white-lipped peccaries, were mostly related to annual croplands. Collaredpeccaries were, in fact, the rarest of all focal species, as they occurred in only 20% of the surveyed sites. Collared-peccaries tend to be abundant species wherever they occur, and their distribution pattern in ENP region could be limited by competition for restricted resources, especially in natural vegetation patches (DeBach, 1966; Reyna-Hurtado and Tanner, 2007). Tapirs, in turn, were the commonest species along with the pampas deer, and occupancy models suggested weak relations between tapirs presence and habitat types, and other factors could be shaping its spatial distribution. However, alternative models with substantial support to explain tapirs occurrence included both open and closed natural vegetation types and annual croplands, which is an expected distribution pattern for a generalist species like the lowland tapir (Cordeiro et al., 2016). Based on this, we can infer that the high habitat diversity in ENP region may cause tapirs populations to thrive. Lowland tapirs are Vulnerable species in both national and global scales (Naveda et al., 2008; MMA, 2016), and our results may indicate the importance of ENP region for the species conservation in the regional scale. In megadiverse countries with farming-based economies, like Brazil, it is essential to comprehend how species respond to the matrix in order to provide information for appropriate landscape management and selection of priority areas for conservation. Thus, maintaining suitable and permeable matrixes can allow species to persist in humanaltered areas and to disperse through natural remnants (Daily et al., 2003; Prugh et al.,

30 ; Franklin and Lindenmayer, 2009; Shackelford et al., 2015). Well-managed matrixes may also contribute to community conservation. However, careful interpretation to this issue is needed. Crops and agroecosystems may provide additional resources for some species, but natural vegetation areas, like the ones required by Brazilian Forest Code, have essential resources for their survival and development (Daily et al., 2003; Casatti, 2010; Develey and Pongiluppi, 2010; Imperatriz-Fonseca and Nunes-Silva, 2010; Boron et al., 2016). Moreover, large continuous croplands may house herbivores, although this interaction causes conflicts between farmers and wildlife (Hill, 2000; Nyhus and Tilson, 2004; Marchini and Crawshaw, 2015). In Emas National Park region, whitelipped peccaries are known to farmers as great crop consumers and are often killed in retaliation (Jácomo, 2004). This mammal species is listed as Vulnerable to extinction in both national and global scales (Keuroghlian et al., 2013; MMA, 2016). Therefore, protecting natural vegetation fragments should reduce the impact of the white-lipped peccaries on cropland production and avoid its local extinction. Thus, protected areas benefit farmers and species conservation. Natural fragments and green areas in ENP surroundings are also important to connect populations of the Cerrado to those of other biomes, because the Park is located in a watershed connecting the Amazon and Pantanal Biomes (Silveira et al., 2014). These corridors are especially important for jaguars, as both Biomes house the two largest jaguar populations along the species distribution (Sanderson et al., 2002; Silveira et al., 2014). In fact, the conservation of highly mobile species, such as jaguars and cougars, also depends on unprotected areas, because Conservation Units often can t protect large populations of these species (Sollmann et al., 2008; Petracca et al., 2014; Boron et al., 2016). Thus, properly managed agricultural lands may play a major role in predator species conservation if predator-related habitat types are available.

31 23 This study, however, failed to show apex predators relation to the different habitat types in the study area. As the null hypothesis model was the best model for both jaguars and cougars, it is likely that their presence could be related to other variables rather than vegetation type. Apex predator distribution depend on prey species presence, and prey species were differently distributed across the mosaic (Fuller and Sievert, 2001; Bled et al., 2015). This distribution pattern could drive both predators to widely occur in the landscape, using habitats according to their prey availability instead of their structure. Jaguars and cougars are opportunistic hunters, so prey presence in different habitats might help predators populations to persist in the unprotected lands (Logan & Sweanor, 2001; Novack et al., 2005; Weckel et al., 2006; Cavalcanti and Gese, 2010; Foster et al., 2010; Gómez-Ortiz et al., 2015). In fact, although cougars had weak relationship to habitat types, perennial crops were shown to influence its presence. Several studies in São Paulo state found that cougar populations are able to persist in sugarcane croplands (Lyra-Jorge et al., 2008; Miotto et al., 2011), possibly due to the prey availability in these areas (Dotta & Verdade, 2007; Culver, 2010). As aforementioned, keeping well-managed permeable matrixes should benefit the species and could also help reduce herbivores-farmers conflicts through natural control of herbivores populations. Consequently, apex predators have a pivotal role in ecosystems becoming priority species for biodiversity conservation purposes, and their local extinction could have negative results for both community structure and agriculture production (Zavaleta et al., 2001; Estes et al., 2011). Further studies including prey as predictor of predators presence should help elucidate this issue and allow for proper landscape management in the region. Other prey types are also available in the area, including insectivores and smaller carnivores. Silveira (2004) and Sollmann et al. (2013) identified giant anteaters as one of jaguars main prey species in ENP region, accounting for more than 75% of biomass to

32 24 its diet. In this study, giant anteater s distribution was also not directly affected by vegetation structure. Although it is known to forage in open habitats, it usually depends on scrublands and forests for shelter and is also related to water habitats (Emmons et al., 2004; Medri and Mourão, 2005). Thus, it is expected that anteaters would benefit from ENP s suitable forage areas. However, they are highly affected by the park s constant wildfires (Silveira et al., 1999), and intense road traffic in the Park surroundings also affects the species local persistence (Diniz and Brito, 2013). These threats, along with high predation pressure could be constraining giant anteaters occurrence. The species is Vulnerable to extinction in both national and global scales (Miranda et al., 2014; MMA, 2016), and further information about the species distribution and population status in ENP region is important to promote its local conservation. CONCLUSIONS The present study focus on Cerrado s medium and large-sized fauna s responses to the habitat types within a Protected Area and its surroundings. We found that different vegetation types influence species distribution. Therefore, high habitat diversity in a landscape may be a good approach for large animals conservation, especially because Cerrado medium and large-sized fauna varies in habitat use strategies. Additionally, green areas around protected areas may also be useful for conservation strategies if matrixes are habitable and permeable to species. Moreover, the rich animal community in Emas National Park s region and the Park s strategical location play an important regional role for species and ecosystems conservation.

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49 41 SUPPLEMENTARY MATERIAL TABLES Table 1. Camera-trap sites and their respective sampling time periods and number of cameras per site (1 or 2). Missing values (-) account for periods that cameras did not work, and therefore sampling did not occur. CAM Jul Jul. 31 Aug Aug. 30 Sept. 7 - Sept. 26 Oct Oct. 29 Nov Nov. 29 CAMAR CAMBL CAMDM CAMDM CAMMF CAMRJ CAMV CAM BJ CAM CK CAM DC CAM FE CAM GF CAM J CAM JG CAM KA CAM MN CAM MN CAM MN CAM OM CAM OM CAM OM CAM OM CAM P2V CAM PO CAM PO CAM PO CAM RQ CAM TU CAM TU CAM TU CAM UO CAM VU CAM VY

50 42 CAM VY CAM VY CAM WP CAM XW CAM YW CAM YZ CAM YZ CAM ZX Table 2. Candidate set of 16 occupancy models for predator and prey species for survey data from Emas National Park and its northern surrounding region, Brazil. Models were estimated with occupancy (Ψ) as a function of open vegetation; closed vegetation; annual croplands; and perennial croplands. Detectability (p) varied as a function of each survey period and number of cameras per trapping site. Candidate Models Ψ(.),p(.) Ψ(openhabitats),p(survey+cam) Ψ(closedhabitats),p(survey+cam) Ψ(annualcrops),p(survey+cam) Ψ(perennialcrops),p(survey+cam) Ψ(openhabitats+closedhabitats),p(survey+cam) Ψ(openhabitats+annualcrops),p(survey+cam) Ψ(openhabitats+perennialcrops),p(survey+cam) Ψ(closedhabitats+annualcrops),p(survey+cam) Ψ(closedhabitats+perennialcrops),p(survey+cam) Ψ(annualcrops+perennialcrops),p(survey+cam) Ψ(openhabitats+closedhabitats+annualcrops),p(survey+cam) Ψ(openhabitats+closedhabitats+perennialcrops),p(survey+cam) Ψ(openhabitats+annualcrops+perennialcrops),p(survey+cam) Ψ(closedhabitats+annualcrops+perennialcrops),p(survey+cam) Ψ(openhabitats+closedhabitats+annualcrops+perennialcrops),p(survey+cam)

51 43 Table 3. List of medium and large-sized vertebrate species registered in Emas National Park (ENP) and its northern surrounding region between July and December Asterisk sign (*) indicates species analyzed in this study. Brazil Red List Status and IUCN Status indicate species national and global conservation status, respectively. (LC = Least Concern; NT = Near Threatened; VU = Vulnerable; DD = Data Deficient). Species Name Common Name Inside Outside Brazil Red IUCN ENP ENP List Status Status REPTILES Salvator duseni yellow tegu lizard x x - - Salvator merianae black-and-white tegu lizard x x - LC BIRDS Cariama cristata red-legged seriema x x - LC *Rhea americana greater rhea x x - NT Crypturellus parvirostris small-billed tinamou x x - LC Rhynchotus rufescens red-winged tinamou x x - LC Crax fasciolata bare-faced curassow x x - VU Penelope superciliaris rusty-margined guan x x - LC Aramides cajanea grey-necked wood rail x - LC MAMMALS Chironectes minimus water opossum x - LC Didelphis albiventris white-eared opossum x x - LC Cabassous unicinctus naked-tailed armadillo x x - LC Dasypus novemcinctus nine-banded armadillo x x - LC Euphractus sexcinctus hairy armadillo x x - LC Priodontes maximus giant armadillo x x VU VU *Myrmecophaga tridactyla giant anteater x x VU VU Tamandua tetradactyla lesser anteater x x - LC Alouatta caraya black howler monkey x - LC Sapajus libidinosus bearded capuchin monkey x - LC Coendou prehensilis brazilian porcupine x - LC Cuniculus paca spotted paca x - LC Dasyprocta azarae Azara's agouti x x - DD

52 44 Hydrochoerus hydrochaeris capybara x x - LC *Pecari tajacu collared peccary x x - LC *Tayassu pecari white-lipped peccary x x VU VU Blastocerus dichotomus marsh deer x x VU VU *Ozotoceros bezoarticus pampas deer x x VU NT Mazama americana red brocket deer x x - LC Mazama gouazoubira gray brocket deer x x - LC *Tapirus terrestris lowland tapir x x VU VU Eira barbara tayra x x - LC Galictis cuja lesser grison x x - LC Lontra longicaudis neotropical otter x - NT Conepatus semistriatus striped hog-nosed skunk x x - LC Nasua nasua ring-tailed coati x x - LC Procyon cancrivorus crab-eating raccoon x x - LC Cerdocyon thous crab-eating fox x x - LC Lycalopex vetulus hoary fox x VU LC Chrysocyon brachyurus maned wolf x x VU NT Leopardus colocolo pampas cat x x VU NT Leopardus pardalis ocelot x x - LC *Puma concolor cougar x x VU LC Puma yagouaroundi jaguarundi x - LC *Panthera onca jaguar x x VU NT DOMESTIC Gallus gallus domesticus domestic chicken x Sus scrofa domesticus feral pig x Bos indicus domestic cattle x Equus ferus caballus domestic horse x Canis lupus familiaris domestic dog x x Felis catus domestic cat x

53 45 Table 4. The three best fitted models for each studied species and their respective AIC, ΔAIC and naïve occupancy values. Values in red indicate models with less strength of inference. Models were estimated with occupancy (Ψ) as a function of open vegetation; closed vegetation; annual croplands; and perennial croplands. Detectability (p) varied as a function of each survey period and number of cameras per trapping site. Species Name Common Name P. onca jaguar Model AIC ΔAIC naïve Ψ psi(.),p(.) 108,28 0,00 psi(open),p(survey+cam) 115,56 7,28 psi(perennial),p(survey+cam) 115,88 7,60 0,4250 Pu. Concolor cougar psi(.),p(.) 133,54 0,00 psi(perennial),p(survey+cam) 134,66 1,12 psi(annual),p(survey+cam) 136,57 3,03 0,5750 M. tridactyla giant anteater psi(.),p(.) 112,41 0,00 psi(annual),p(survey+cam) 115,99 3,58 psi(closed+annual),p(survey+cam) 117,27 4,86 0,3750 Pe. Tajacu collared peccary psi(open+annual),p(survey+cam) 69,19 0,00 psi(open+closed),p(survey+cam) 69,55 0,36 psi(open+closed+annual+perennial),p(survey+cam) 70,50 1,31 0,2000 T. pecari white-lipped peccary psi(open+closed+annual+perennial),p(survey+cam) 140,83 0,00 psi(annual),p(survey+cam) 151,50 10,67 psi(open),p(survey+cam) 151,68 10,85 0,7000 Ta. Terrestris lowland tapir psi(.),p(.) 154,50 0,00 psi(open+closed),p(survey+cam) 155,70 1,20 psi(annual),p(survey+cam) 156,26 1,76 0,7750 O. bezoarticus pampas deer psi(open+annual+perennial),p(survey+cam) 128,13 0,00 psi(closed+annual+perennial),p(survey+cam) 128,13 0,00 psi(open+closed+anual),p(survey+cam) 128,30 0,17 0,7750 R. americana greater rhea psi(open+closed+annual+perennial),p(survey+cam) 139,31 0,00 psi(closed),p(survey+cam) 140,97 1,66 psi(open+closed),p(survey+cam) 141,23 1,92 0,7250

54 46 FIGURES Figure 1. Emas National Park location in Goiás state and Brazil, and the vegetation types and camera-trapping sites in Emas National Park and its surrounding region.

55 47 Figure 2. Focal species considered in this study. A: jaguar (Panthera onca); B: cougar (Puma concolor); C: giant anteater (Myrmecophaga tridactyla); D: lowland tapir (Tapirus terrestris); E: white-lipped peccary (Tayassu pecari); F: collared-peccary (Pecari tajacu); G: pampas deer (Ozotoceros bezoarticus); H: greater rhea (Rhea americana). All pictures were taken by Jaguar Conservation Fund s automatic camera traps in Emas National Park region, southwestern Goiás state, Brazil, between July and December, 2013.