UNIVERSIDADE ESTADUAL PAULISTA “JÚLIO DE MESQUITA FILHO” INSTITUTO DE BIOCIÊNCIAS – RIO CLARO unesp PROGRAMA DE PÓS-GRADUAÇÃO EM ECOLOGIA, EVOLUÇÃO E BIODIVERSIDADE REDUCTIO AD ABSURDUM SIMPLIFICATION OF TROPHIC PROCESSES IN TROPICAL FORESTS FERNANDO SILVA LIMA, M.Sc. Dezembro - 2020 Orientador: Prof. Dr. Milton Cezar Ribeiro Co-orientador: Dr. Clinton Neil Jenkins UNIVERSIDADE ESTADUAL PAULISTA “JÚLIO DE MESQUITA FILHO” INSTITUTO DE BIOCIÊNCIAS – RIO CLARO unesp PROGRAMA DE PÓS-GRADUAÇÃO EM ECOLOGIA, EVOLUÇÃO E BIODIVERSIDADE REDUCTIO AD ABSURDUM SIMPLIFICATION OF TROPHIC PROCESSES IN TROPICAL FORESTS FERNANDO SILVA LIMA, M.Sc. Tese apresentada ao Instituto de Biociências do Câmpus de Rio Claro, Universidade Estadual Paulista, como parte dos requisitos para obtenção do título de Doutor em Ecologia, Evolução e Biodiversidade. Dezembro - 2020 Orientador: Prof. Dr. Milton Cezar Ribeiro Co-orientador: Dr. Clinton Neil Jenkins L732r Lima, Fernando Silva Reductio ad absurdum: simplification of trophic processes in tropical forests / Fernando Silva Lima. -- Rio Claro, 2022 96 f. : il., tabs., mapas Tese (doutorado) - Universidade Estadual Paulista (Unesp), Instituto de Biociências, Rio Claro Orientador: Milton Cezar Ribeiro Coorientador: Clinton Neil Jenkins 1. Animais carnívoros. 2. Predação (Biologia). 3. Animais predadores. I. Título. Sistema de geração automática de fichas catalográficas da Unesp. Biblioteca do Instituto de Biociências, Rio Claro. Dados fornecidos pelo autor(a). Essa ficha não pode ser modificada. A minha tia Léa; A meu avô Elon†; A meu pai do mato Cicinho†; e a todos que no fim da jornada podem citar 2 Timóteo 4:7. † in memoriam REFLEXÕES E AGRADECIMENTOS O que é um doutorado? Nos últimos meses de redação deste documento me vi retornando a esta pergunta inúmeras vezes. Seria uma tese? Um conjunto de artigos publicados? Créditos por disciplinas concluídas? Foi nesse momento que parei para pensar no que fiz nesses anos e somente depois de lembrar o por que decidi fazer doutorado é que consegui me aproximar do que imagino ser uma resposta. Depois de me graduar em 2003 me associei a um instituto de pesquisas e – apesar de ter feito uma especialização na Inglaterra em 2006 – somente em 2007 ingressei no mestrado. Senti que passar um tempo fora da universidade, participando de iniciativas práticas focadas em conservação da biodiversidade me trouxeram uma perspectiva um pouco mais abrangente de atuação como pesquisador. Nesse intervalo tive a oportunidade de estudar e participar de muitos cursos e, assim, compensar algumas não poucas lacunas na minha formação durante a graduação. O mestrado, em toda a sua intensidade, me trouxe reflexões importantes sobre o por que da pesquisa. Por que coletamos dados? O que fazer com eles? Por que ir para campo coletar dados é só a divertida ponta do iceberg da ciência (não tão divertido da água para baixo). Minha dissertação contestava alguns dos protocolos colocados em prática na pesquisa com felinos selvagens na época e, apesar de severamente contestada em alguns momentos, serviu de referência para a elaboração de desenhos amostrais em diversas iniciativas no país. Fiquei muito feliz em sentir que não seria apenas mais uma encadernação em capa dura arquivada em alguma biblioteca. Enquanto focava em dar continuidade as minhas iniciativas de pesquisa com jaguatiricas no Pontal do Paranapanema e em colaborar com outros grupos Brasil afora – empolgado com as aplicações práticas de meus estudos – uma importante transição acontecia. Os equipamentos para amostragens de fauna, antes restritos a projetos grandes com muito recurso, se tornaram mais acessíveis viabilizando novas iniciativas e amostragens em regiões pouco conhecidas. As abordagens analíticas, antes compartimentadas em softwares específicos, voltaram a raiz da revolução digital quando era necessário digitar linhas de comando com linguagem de programação até para abrir disquetes com 1.44 mb de memória. O desenvolvimento de pacotes analíticos utilizando linguagens de programação em ambientes de código aberto, associado a capacidades de processamento que fazem meu primeiro computador parecer uma calculadora científica, levaram a ecologia enquanto ciência para uma nova era. O céu se tornou o novo limite. Comecei a sentir que precisava me atualizar. Precisava de um momento de imersão na literatura, nas ferramentas e nas novas e cada vez mais sofisticadas linhas de pesquisa. Era hora de fazer doutorado. No final de 2014 estava procurando uma casa para alugar em Goiânia, onde pretendia me mudar com minha família para iniciar esta nova etapa no PPG em Ciências Ambientais da UFG. Havia sido aprovado em primeiro lugar no processo seletivo com uma bolsa em meu nome. Meses antes havia procurado o Prof. Dr. Milton Ribeiro, que disse que só conversaríamos se o chamasse de Miltinho. Na época de minha primeira visita a Rio Claro, infelizmente Miltinho não tinha mais vagas para orientados. Um tempo depois, enquanto pesquisava por imobiliárias goianas na internet, recebi um e-mail de Miltinho intitulado "interessado no dout ainda?". Fiz a prova sem nenhuma expectativa no dia 21 de Janeiro de 2015, exatos 15 dias depois do nascimento de meu primeiro filho. Passei e decidimos abandonar a idéia de ir para Goiânia. Mesmo tendo prometido a mim mesmo que nunca mais moraria em uma planície depois de 9 anos vivendo em Teodoro Sampaio – extremo oeste do estado de São Paulo - em Maio de 2015 estávamos morando em Rio Claro para avançar com o doutorado. Foram 3 anos difíceis - principalmente para minha esposa - em uma cidade estranha, sem família ou amigos e um bebê. No entanto, entre todos os desafios típicos da rotina acadêmica, que a tanto tempo não faziam parte de minha vida, uma coisa que nunca pude me queixar foi o apoio incondicional de meu orientador. Em momentos de dificuldades pessoais, financeiras, morais, psicológicas, etc. nunca houve "tempo ruim". Com muito carinho e empatia ele estava sempre lá. Mesmo diante de todas minhas limitações enquanto cientista, nunca pude reclamar dessa parceria e amizade. Sempre com um berimbal debaixo do braço, posso dizer que meu orientador de doutorado foi e é uma das pessoas mais importantes minha formação como ser humano, pai e pesquisador. Mesmo com a atual distância física, serei sempre seu aprendiz. Poderia redigir por horas sobre causos, aventuras, desventuras, aprendizados e mandingas que passei com Miltinho em não poucas viagens pelo Brasil e até no exterior. É com mais de uma lágrima que escrevo essas linhas enquanto lido com uma das maiores pandemias da história da humanidade e finalizo minha tese. Toda honra e toda glória a aquele que nunca se corrompeu pela ilusão dos pequenos poderes da hierarquia acadêmica. Obrigado Miltinho! Nesse período em Rio Claro descobri uma paixão: o jiu-jitsu. Na década de 90 eu levava o video cassete da casa do meu avô para a casa de um amigo e lá copiavamos fitas VHS dos primeiros UFCs. Criado por Rorion Gracie em 1993, o objetivo do UFC era provar a superioridade do jiu-jitsu brasileiro sobre as outras artes marciais. Fazia isso por que meu tio praticamente me obrigava e achava muito chato um brasileiro com nome estranho (Royce) ficar mais de uma hora agarrado com um lutador no chão até que o "finalizasse". Um dia passando na Rua 5 vi a academia dos Senseis Leandro Brassoloto e Ivan Andrade e parei lá para perguntar. Estava procurando uma atividade física e achei que podia ser interessante. Nessa época minha esposa estava redigindo sua tese de doutorado e eu ficava a maior parte do tempo cuidando do meu filho para que ela pudesse trabalhar. Descer a Av. 14 para o treino das 19:00 era meu ritual diário, meu momento. Durante uma hora e meia só existia o jiu-jitsu. Todas as angústias, dificuldades e ansiedades eram esquecidas. É muito difícil focar nessas coisas quando tem alguém tentando de estrangular. A camaradagem e bom humor no tatame, o bem estar físico e a autoconfiança que o jiu- jitsu me trouxe é o que me fez passar por este período sem me destruir psicologicamente. Agradeço de coração aos meus senseis e irmãos de tatame por me ajudarem a superar os desafios do doutorado. Oss Quando cheguei no LEEC - Laboratório de Ecologia Espacial e Conservação me senti no mínimo deslocado. Com 38 anos de idade, casado e com um filho me vi cercado de jovens incríveis, no leading edge da ecologia de paisagens e no auge de um grande projeto apoiado pela FAPESP em parceria com a Universidade de Helsinki. Aos poucos fui conhecendo as pessoas e processos. Fiz amigos com os quais criei laços invisíveis para a vida toda, embora distantes fisicamente hoje. Nada forja amizades e relações como por perrengues, desafios e batalhas juntos. São nos momentos de dificuldade e necessidade que caem as máscaras que todos nós vestimos diariamente para viver em sociedade e vemos quem é quem. Não foram poucos os desafios e batalhas e encontrei pessoas com códigos de conduta e ética impecáveis na vida pessoal, profissional e acadêmica, outras nem tanto mas mesmo assim tiveram algo a ensinar. Agradeço ao meu amigo Rafael (Urucum), seu jeitão rústico é só uma carapaça para os desavisados. Embaixo dessa casca grossa está uma das pessoas mais interessantes que tive o prazer de conhecer e conviver nos últimos anos. Agradeço a Renata Muylaert, companheira de não poucas batalhas e desafios. A Milene Eigenheer, a Erison Monteiro, a Natália Stefanini, Paula Montagnana, Cláudia Kanda e Julia Oshima pela amizade, parceria, troca de farpas e discussões sensacionais sobre todo tipo de coisa. Agradeço a minha alma mater o IPÊ - Instituto de Pesquisas Ecológicas. O IPÊ abriu as portas para mim quando era um biólogo recém formado e ao mesmo tempo me abriu as portas para o mundo. Não tenho palavras para descrever a admiração e gratidão por toda a generosidade de Claudio e Suzana Pádua ao longo destes quase18 anos de convivência. Realmente não tenho palavras, estou há um bom tempo na frente do computador, mas não há formas de expressar o que gostaria através da linguagem escrita. Muito, muito obrigado! Agradeço aos meus amigos e mentores Clinton Jenkins e Alexandre Uezu. Uma das coisas que mais sinto falta no dia-a-dia é de tê-los por perto e poder conversar sobre cultura e ciência com essas mentes brilhantes. Agradeço a minha amiga Angela Pellin, por liderar pelo exemplo e me mostrar o estoicismo na prática. A toda equipe do projeto Desenvolvimento de novas tecnologias para avaliação dos serviços ambientais em programas de revegetação IPÊ-CTG, em especial a Williana Marin por todo carinho e atenção na preparação de nossas expedições relâmpagos. Parte desta tese foi viabilizada financeiramente por este projeto e muitos dos resultados dos dados coletados ainda trarão contribuições sobre as estratégias de conexão e padrões de recolonização da fauna em áreas de restauração. A querida Cristina – Tina – Tófoli, minha irmã de coração e toda a equipe do projeto Monitoramento Participativo da Biodiversidade IPÊ-ICMBio por renovar minha fé na conservação. A Fabiana Prado por me mostrar o que é liderança e colaboração na prática. Ao time de elite da 2ª Atualização das Áreas Prioritárias da Mata Atlântica IPÊ-MMA: Clinton Jenkins, Angela Pellin, Alexandre Uezu, Alexandre Martensen, Henrique Shirai e Neluce Soares. A equipe e projeto que tenho o maior orgulho e provilégio de ter participado. Agradeço a todo o staff do IPÊ por essa jornada em busca de um país mais sustentável. Em especial a Edu Ditt, Andrea Peçanha, Marcela Paolino, Patrícia Medici, Pollyana Lemos, Rafael Chiaravalloti, Simone Tenório, Paula Piccin e a meus irmãos de expedições: José Wilson e Cicinho (in memoriam). Sempre tentei explicar meu trabalho para minha família, as vezes escrevendo, as vezes batendo papo. De fato, desde a graduação quando criei o fanzine “Drosophila” há 20 anos atrás, tento falar sobre ecologia e biologia escrevendo. Em 2016 iniciei uma coluna com alguns textos de relativo alcance, mas ainda insipientes. Nessa época, rabisquei em uma prancheta o esboço do que veio a se tornar o DesAbraçando Árvores, projeto lançado em 2018 focado em ecologia e biologia da conservação no formato podcast. De lá para cá posso dizer com tranquilidade que este o projeto mudou minha vida e minha carreira. Agradeço ao amigo e padrinho Fabiano Rodrigues de Melo e Rogério Cunha de Paula – meu irmão nerd – que abraçaram a idéia desde o início. A toda a família FIFA pelo suporte e a Paula Piccin, a querida Laís Duarte, a Fernanda Abra, ao maravilhoso Luiz Antônio Gambá, a Lays Parolin, ao Senhor A e a Hugo Fernandes meu eterno obrigado pela amizade e parceria nesse projeto maluco. Nunca imaginei que gravar tudo aquilo que antes fazia as pessoas me rotularem de chato se tornaria um movimento do bem, divulgando projetos e iniciativas importantes de conservação da biodiversidade e o mais importante: quebrando tabus e acabando com clichês. Agradeço de coração a cada pesquisador e pesquisadora, cada pessoa que passou pelo podcast e generosamente compartilhou sua jornada conosco e com nossos ouvintes. Esse projeto, por mais que desejássemos dar continuidade, não seria viável sem o apoio de um grupo muito especial de pessoas que se juntaram ao movimento e se dispuseram a contribuir com a causa. Obrigado pela confiança, apoio e também pelas críticas. Mas vale sempre a pena lembrar: não nos responsabilizamos por nada! Agradeço a Ryan Holiday por me apresentar o estoicismo, ao imperador Marcus Aurelius por deixar suas meditações para a posteridade e a Jocko Willink (thanks for your service Sir). Agradeço aos autores Bernard Cornwell, Jim Corbett, Yuval Harari, Cal Newport, Jack Donovan, Dakota Meyer (thanks for your service), Nathan Lents, Matthew Walker, John Stryker Meyer (thanks for your service), John Plaster (thanks for your service), Sean Parnell (thanks for your service), Neil DeGrasse Tyson, Steven Novella, Stephen King, Michael Punke, Ken Follett e David Quammen por me ajudarem a mudar minha visão de mundo nesses últimos anos. Alexandre Ottoni (Joven Nerd), a Deive Pasos (Azaghal), e a Atila Iamarino meu muito obrigado pelas centenas de horas de companhia no Nerdcast. A Miriam Perilli, minha cara metade, não há como expressar a gratidão por tudo o que vivemos nesses anos e nesta etapa de nossas vidas. Sua paciência, carinho, parceria e cumplicidade trazem sentido e direção a jornada. Esse ciclo se fecha para nós dois e que venham novos desafios! Obrigado por dividir sonhos, sorrisos e lágrimas. Por dividir a vida, o universo e tudo o mais. Aos pequenos Ian e Lis, por me ensinarem a valorizar o que realmente é importante. Agradeço a minha tia-irmã Leá (tia Cotinha), sem a qual eu não teria feito nem graduação. A minha mãe e a minha querida irmã Cintia. Agradeço também a Dona Miriam Lages, Ana Luiza, Abraão, Maria Regina, Felipe e ao senhor Rômulo Perilli. Obrigado por me receberem de braços abertos na família. Na reta final das análises e redação tive a ajuda de generosos amigos e cientistas incríveis que me estenderam a mão e tentaram contribuir de todas as formas possíveis. Obrigado Marcelo Magioli, Ronaldo Morato, Elildo Carvalho, Alexandre Martensen, Alexandre Uezu e Milene Eigenheer. Vocês são sensacionais! Desculpem não ter sido o melhor dos aprendizes, mas obrigado por tentarem! Enfim, voltando a pergunta inicial, essa tese é apenas um fechamento de um processo de formação de um cientista. Li e estudei compulsivamente, elaborei e ministrei disciplinas, contribui com aulas em disciplinas em diversos estados do Brasil e do exterior, participei de discussões acadêmicas em disciplinas, coletei dados, organizei expedições, trabalhei com equipes incríveis, implodi equipes, abandonei equipes, acertei, errei, montei equipes, fechei parcerias nacionais e internacionais. Escrevi projetos de pesquisa, levantei recursos com agências de fomento, institutos de pesquisa e setor privado. Apresentei e discuti meu trabalho com cientistas, governantes, tomadores de decisão e empresários no Brasil e no exterior. Utilizei minha expertise prévia e novas ferramentas aprendidas durante o doutorado para contribuir com planos de ações de espécies ameaçadas, apresentei propostas de soluções para problemas práticos para grandes corporações internacionais e para o governo brasileiro. Mais tarde passei finais de semanas inteiros editando áudio tentando traduzir a importância disso para minha tia e para o público leigo. Colaborei com dezenas de grupos de pesquisa na redação, revisão e análise de dados em artigos publicados nesse período, outros já submetidos e alguns sendo preparados para submissão nesse exato momento. Passei a entender o doutorado como um processo de crescimento e atualização, de formação de um cientista capaz de pensar em questões teóricas e práticas relevantes para o avanço da ciência e da tecnologia, de fazer parcerias e levantar recursos que viabilizem isso, executar, analisar e reportar. Ser capaz de sintetizar seu conhecimento adquirido e passar adiante. Dificilmente conseguiria resumir esse processo de transformação pessoal e profissional em um documento. Como inúmeros colegas antes de mim, cheguei no final deste processo produzindo uma tese que não correspondeu aos meus anseios no início do processo. Muita coisa ficou para trás por que era ridiculamente inviável desde o início e meu orientador teve a sabedoria de me deixar aprender errando (e para largar de ser teimoso). Outras por falta de organização e outras simplesmente pela dinâmica da vida e mudanças que estão fora do nosso controle. Algumas etapas acabam aqui, algumas vou dar continuidade por que preciso e outras por que quero. Em relação a esta etapa de minha vida posso afirmar que, assim como Paulo, combati o bom combate e terminei minha jornada. O presente trabalho foi realizado com apoio da Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Código de Financiamento 001. So long and thanks for all the fish! Valar Dohaeris Sumário Resumo Geral…………………………………………………………………………………………………………………………..1 General Abstract...........................................................................................................................2 General Introduction .................................................................................................................... 3 References ................................................................................................................................. 5 CHAPTER 01. Reductio ad absurdum: Simplification of trophic processes in tropical forests... 7 Abstract ..................................................................................................................................... 8 Introduction............................................................................................................................... 9 What is an apex predator? .................................................................................................... 9 What is an mesopredator? .................................................................................................. 11 Mesopredator release hypothesis ...................................................................................... 12 Predators in the Atlantic Forest .......................................................................................... 12 Is mesopredator release an underestimated phenomenon in tropical forests? .................... 14 Conclusions.............................................................................................................................. 17 References ............................................................................................................................... 18 CHAPTER 02. Atlantic Camtraps: a dataset of medium and large terrestrial mammal communities in the Atlantic Forest of South America .............................................................. 22 Abstract ................................................................................................................................... 23 Introduction............................................................................................................................. 29 Description .............................................................................................................................. 32 Site description ........................................................................................................................ 35 Data compilation ..................................................................................................................... 35 Research Methods................................................................................................................... 35 References ............................................................................................................................... 46 CHAPTER 03. Home range and movement patterns of jaguars in the Atlantic Forest of South America ....................................................................................................................................... 56 Abstract ................................................................................................................................... 58 Introduction............................................................................................................................. 59 Materials and Methods ........................................................................................................... 60 Study Sites ........................................................................................................................... 60 Telemetry and home range estimates ................................................................................ 61 Results ..................................................................................................................................... 63 Discussion ................................................................................................................................ 66 References ............................................................................................................................... 68 Considerações Finais...............................................................................................................74 APPENDIX I. Produção como discente (2015 – 2020) Colaborações em artigos publicados....................................................................................... 76 Qualis A1 - Biodiversidade .................................................................................................. 76 Qualis B1 - Biodiversidade................................................................................................... 78 Qualis B3 - Biodiversidade................................................................................................... 78 Citações no Google Scholar (2015 – 2020) .............................................................................. 78 Textos de divulgação científica ............................................................................................... 79 Projetos de divulgação científica ............................................................................................. 79 1 RESUMO GERAL A perda e a fragmentação de habitat têm sido descritas mundialmente como as principais ameaças à biodiversidade. Além da redução extrema na densidade e abundância das populações de animais silvestres, esses fenômenos têm implicações nas interações entre as espécies, levando a consequências imprevisíveis. Isso é particularmente sensível quando se trata de interações predador-presa, onde as respostas do predador - ou a ausência dela - às mudanças na paisagem e no habitat podem ter influência direta nas redes alimentares. A importância ecológica dos grandes mamíferos carnívoros (Carnivora) é facilmente reconhecida, pois mesmo poucos indivíduos deste grupo podem exercer um forte controle top down sobre as populações de presas e predadores menores. No entanto, não apenas os grandes predadores, mas as populações de grandes mamíferos em geral estão em declínio em todo o mundo. Esse processo de defaunação tende a favorecer espécies de mamíferos de menor massa corporal, alta taxa reprodutiva, onívoros e generalistas, às vezes descrito como “miniaturização da fauna”. Outro fenômeno relacionado à defaunação é a hipótese da liberação do mesopredador. Usado para descrever as irrupções de predadores menores após a extirpação dos maiores. Na Mata Atlântica, um dos hotspots mundiais de biodiversidade, o predador de ápice (onça-pintada) está regionalmente extinto na maior parte do bioma. Além disso, mais de 50% deste bioma está distribuído em um mosaico de manchas florestais menores que 500 ha. A Mata Atlântica combina as principais variáveis associadas a surtos de liberação de mesopredadores. Nesta tese, reuni as principais características da hipótese de liberação do mesopredador adaptada a um contexto regional: a comunidade de mamíferos carnívoros da Mata Atlântica. Inicialmente, proponho um modelo conceitual baseado em hipóteses gerais e resultados esperados apoiados em pesquisa bibliográfica e conhecimento empírico como referência para orientar futuras análises em larga escala sobre esse fenômeno. Seguindo esta discussão, apresento o conjunto de dados Atlantic-Camtraps, destinado a apoiar os dados necessários para explorar o fenômeno de liberação de mesopredadores na Mata Atlântica. Por fim, trago um estudo de caso sobre o maior predador da Mata Atlântica em um de seus últimos redutos no bioma. Neste capítulo, eu e meus colegas apresentamos os resultados de cinco anos de monitoramento por telemetria e discutimos a ausência de padrões típicos, como sazonalidade e diferenças no tamanho da área de vida entre machos e fêmeas. Palavras-chave: Animais carnívoros, Predação (Biologia), Animais predadores 2 GENERAL ABSTRACT Habitat loss and fragmentation has been described worldwide as the main threats to biodiversity. Additional to extreme reduction on wildlife populations density and abundance, these phenomena have implications on species interactions, leading to unpredicted consequences. This is particularly sensitive when it comes to predator- prey interactions, where predator responses - or the absence of it – to landscape and habitat changes may have direct influence across food webs. The ecological importance of large mammalian carnivores (Carnivora) is easily recognized since even a few individuals can exert strong top-down control on prey populations and smaller predators. Nevertheless, not only large predators, but large mammal populations in general are in decline worldwide. This shift pattern in mammal species pool towards smaller body mass, highly reproductive rate, omnivorous and generalists caused by defaunation has been described as downsizing. One phenomenon related to defaunation is the mesopredator release hypothesis. It was used to describe smaller predators’ irruptions after extirpation of larger ones. In the Atlantic Forest, one of the world’s biodiversity hotspots, the apex predator (jaguars) is regionally extinct in most of the biome. Additionally, more than 50% of this biome is distributed in a mosaic of forest patches smaller than 500 ha. The Atlantic Forest combines the key variables associated with mesopredator outbreaks. In this thesis, I put together the key features of the mesopredator release hypothesis adapted to a regional context: the mammal carnivore community of Atlantic Forest. I propose a conceptual model based on general hypothesis and expected results supported by literature research and empirical knowledge as a reference to guide future large-scale analyses on this phenomenon. Following this discussion, I present the dataset Atlantic-Camtraps, originally intended to support the data needed to explore the mesopredator release phenomenon in the Atlantic Forest. Lastly, I bring a study case on the Atlantic Forest apex predator in one of its last strongholds in the biome. In this chapter me and my colleagues present the results of five years of monitoring through telemetry and discuss the absence of typical patterns such as seasonality and differences in home range size between males and females. Keywords: Predation, Carnivora, Predator-prey interaction 3 GENERAL INTRODUCTION Changes in the abundance and persistence of biodiversity, led by the loss and fragmentation of natural habitats has been described worldwide [1–3]. These changes are generally described and/or predicted as negative, tending to focus on single- species and species diversity models. However, this approach may be missing the effects of habitat loss and fragmentation implications on species interactions, leading to unpredicted and misleading results [4,5]. This is particularly sensitive when it comes to predator-prey interactions, where predator responses - or the absence of it – to landscape and habitat changes may have direct influence across food webs [6]. The ecological importance of large mammalian carnivores (Carnivora) is easily recognized since even a few individuals can exert strong top-down control on prey populations and smaller predators [4,7–9]. Species with these features occupy an elevated position in the trophic ladder, being classified as top predators and their role as ecosystem regulators is now firmly embedded in ecological theory [6,10,11]. Nevertheless, not only large predators, but large mammal populations in general are in decline worldwide and the consequences only recently started to be studied [10]. This shift pattern in mammal species pool towards smaller body mass, highly reproductive rate, omnivorous and generalists caused by defaunation has been described as downsizing, with unknown long-term consequences [12,13]. One phenomenon related with defaunation is the mesopredator release hypothesis. It was used to describe smaller predators’ irruptions after extirpation of larger ones and first appeared in scientific literature in the late 1980's [14]. In the Atlantic Forest, one of the world’s biodiversity hotspots, the apex predator (jaguars) is regionally extinct in most of the biome. Additionally, more than 50% of the biome is distributed in a mosaic of forest patches smaller than 500 ha. The Atlantic Forest combines the key variables associated with mesopredator outbreaks. Nevertheless, to detect it in regions with high redundancy in ecological functions such as tropical rainforests can become a challenge even to insightful and skilled researchers. However, data availability, dissemination and processing dramatically advance in the last decade. The recent adoption of data sharing policies by journals are an important step towards large scale analysis. 4 In the first chapter of this thesis, I put together all the key features of mesopredator release hypothesis adapted to a regional context: the mammal carnivore community of Atlantic Forest. I propose a conceptual model based on general hypothesis and expected results supported by literature research and empirical knowledge as a reference to guide future large-scale analyses on this phenomenon. In the second chapter I present the dataset Atlantic-Camtraps, originally intended to support the data needed to explore the mesopredator release phenomenon in the Atlantic Forest. This data publication was one of the first of a series of datasets combining data mining and raw data from research groups aiming data availability, dissemination, and processing for this biome. In the third chapter I bring a study case on the Atlantic Forest apex predator in one of its last strongholds in the biome. In this chapter me and my colleagues presents the results of five years of monitoring through telemetry and discuss the absence of typical patterns such as seasonality and differences in home range size between males and females. 5 REFERENCES 1. Fahrig L. Rethinking patch size and isolation effects: The habitat amount hypothesis. J Biogeogr. 2013;40: 1649–1663. doi:10.1111/jbi.12130 2. Haddad NM, Brudvig L a., Clobert J, Davies KF, Gonzalez A, Holt RD, et al. Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci Adv. 2015;1: e1500052–e1500052. doi:10.1126/sciadv.1500052 3. Jorge MLSP, Galetti M, Ribeiro MC, Ferraz KMPMB. Mammal defaunation as surrogate of trophic cascades in a biodiversity hotspot. Biol Conserv. 2013;163: 49–57. doi:10.1016/j.biocon.2013.04.018 4. Ryall KL, Fahrig L. Response of predators to loss and fragmentation of prey habitat: A review of theory. Ecology. 2006;87: 1086–1093. 5. Valiente‐Banuet A, Aizen MA, Alcántara JM, Arroyo J, Cocucci A, Galetti M, et al. Beyond species loss: the extinction of ecological interactions in a changing world. Johnson M, editor. Funct Ecol. 2015;29: 299–307. doi:10.1111/1365- 2435.12356 6. Estes J a, Terborgh J, Brashares JS, Power ME, Berger J, Bond WJ, et al. Trophic Downgrading of Planet Earth. Science (80- ). 2011;333: 301–306. doi:10.1126/science.1205106 7. Roemer GW, Gompper ME, Van Valkenburgh B. The Ecological Role of the Mammalian Mesocarnivore. Bioscience. 2009;59: 165–173. doi:10.1525/bio.2009.59.2.9 8. Terborgh J. Ecological Meltdown in Predator-Free Forest Fragments. Science (80- ). 2001;294: 1923–1926. doi:10.1126/science.1064397 9. Soulé ME, Estes JA, Miller B, Honnold DL. Strongly interacting species: Conservation policy, management, and ethics. Bioscience. 2005;55: 168–176. doi:10.1641/0006-3568(2005)055[0168:SISCPM]2.0.CO;2 10. Ripple WJ, Estes J a, Beschta RL, Wilmers CC, Ritchie EG, Hebblewhite M, et al. Status and ecological effects of the world’s largest carnivores. Science (80- ). 2014;343: 1241484. doi:10.1126/science.1241484 6 11. Wallach AD, Izhaki I, Toms JD, Ripple WJ, Shanas U. What is an apex predator? Oikos. 2015;124: 1453–1461. doi:10.1111/oik.01977 12. Cooke RSC, Eigenbrod F, Bates AE. Projected losses of global mammal and bird ecological strategies. Nat Commun. 2019;10: 2279. doi:10.1038/s41467- 019-10284-z 13. Young HS, McCauley DJ, Galetti M, Dirzo R. Patterns, Causes, and Consequences of Anthropocene Defaunation. Annu Rev Ecol Evol Syst. 2016;47: 333–358. doi:10.1146/annurev-ecolsys-112414-054142 14. Soulé M., Bolger D., Alberts A., Wright J, Sorice M, Hill S. Reconstructed of Rapid Extinctions of Dynamics Birds in Urban Habitat Islands. Conserv Biol. 1988;2: 75–92. doi:10.1111/j.1523-1739.1988.tb00337.x CHAPTER 01 REDUCTIO AD ABSURDUM SIMPLIFICATION OF TROPHIC PROCESSES IN TROPICAL FORESTS Onçinha pintada Zebrinha listrada Coelhinho peludo Vão se f****! Porque aqui na face da terra Só bicho escroto É que vai ter Bichos Escrotos, Titãs. 8 ABSTRACT Changes in the abundance and persistence of biodiversity, led by the loss and fragmentation of natural habitats, have been described worldwide. These changes generally focus on single-species and species diversity models. However, this approach may be missing species interactions leading to misleading results. This is particularly sensitive when it comes to predator-prey interactions, where predator responses or lack of them to landscape and habitat changes may have direct influences across food webs. The decline of large predator populations is indeed a global phenomenon. Meanwhile mesopredators are becoming more abundant in fragmented landscapes. This process, described as the Mesopredator Release Hypothesis, can have profound impacts on biodiversity. In the Atlantic Forest the apex predator is regionally extinct in most of the biome. Additionally, 65% of the remaining forest is distributed in mosaic of forests patches smaller than 2000 ha. This presents a high potential for mesopredator release outbreaks and the outcome is anything but predictable. Here I propose a conceptual model describing how this phenomenon may work in Atlantic Forest. 9 INTRODUCTION Changes in the abundance and persistence of biodiversity, led by the loss and fragmentation of natural habitats has been described worldwide [1–3]. These changes are generally described and/or predicted as negative, tending to focus on single- species and species diversity models. However, this approach may be missing the effects of habitat loss and fragmentation implications on species interactions, leading to unpredicted and misleading results [4,5]. This is particularly sensitive when it comes to predator-prey interactions, where predator responses - or the absence of it – to landscape and habitat changes may have direct influence across food webs [6]. The ecological importance of large mammalian carnivores (Carnivora) is easily recognized since even a few individuals can exert strong top-down control on prey populations and smaller predators [4,7–9]. Species with these features occupy an elevated position in the trophic ladder, being classified as top predators and their role as ecosystem regulators is now firmly embedded in ecological theory [6,10,11]. Large predators (higher body mass) naturally occur at low density, demands large areas of natural habitat (larger home range size) and stable prey base (larger average prey size) in order to maintain health populations [12,13] (Figure 01). Nevertheless, not only large predators, but large mammal populations in general are in decline worldwide and the consequences only recently started to be studied [10]. This shift pattern in mammal species pool towards smaller body mass, highly reproductive rate, omnivorous and generalists caused by defaunation has been described as downsizing, with unknown long-term consequences [14,15] (Figure 01). WHAT IS AN APEX PREDATOR? A recent study proposes that predators above a certain weight threshold and functional features are capable to limit their own population densities – i.e. self- regulation – instead of a bottom-up control determined by prey availability [11]. This feature differentiate this particular group from the general top predator definition and are called apex predators [11]. These species usually presents large body size and have a small chance of been predated by other species [11,16]. Indeed, it is not uncommon to these species to have humans as their unique predator. Top-down control promoted by predators is included as one of the primary forces in ecosystems 10 worldwide. However evolutionary forces led apex predators towards slow reproductive rates, sparsely populated territories, higher rates of infanticide and reproductive suppression as proxies for population densities limits [11]. Figure 1 -Major trends of mammal predators’ traits associated with body mass. As body mass decreases, species shifts towards higher reproductive rate, richness, and density; smaller home ranges and average prey sizes; more generalist diet and habitat requirements. 11 Different from apex predators top, meso and small predators are unlikely to self- regulate and are instead adapted to extrinsic regulation pressure, as suggested by a higher reproductive rate, lower investment in each offspring and the potential to attain higher densities [11]. This regulation, commonly reported in trophic cascades theory, is essentially an intraguild interaction among predators and can be direct or indirect [17,18]. Direct lethal encounters as predation for food or elimination of an ecological competitor are widespread among mammals and is high enough to promote large demographic effects on mesopredator populations [19,20]. Fear of direct encounters with top and apex predators promotes change in habitat use, altering foraging behavior and activity patterns. In the last instance it affects population growth, reproduction, survival rates and its impact may even be larger than direct kills [18]. WHAT IS A MESOPREDATOR? A general definition of mesopredator includes mid-ranking mammalian predators based in weight ranges [21]. Nevertheless this approach does not account for ecological patterns and consequences associated with mesopredator release hypothesis [18]. Indeed, this description fits better the definition of mesocarnivores as a functional group, instead of the actual ecological phenomenon which is not restricted to mammals. According to Prugh et al. (2009): "a mesopredator should be defined as any mid-ranking predator in a food web, regardless of its size or taxonomy." It is also important to consider that a mesopredator is a matter of scale. A mesopredator in a system may have the ecological hole of a top predator in another [7,18]. This differentiates the concept of mesopredator from a mesocarnivore in mammal communities. The first more related to the species ecological ranking in a given trophic chain and the latter with its morphological features [18]. Based in these concepts, mesopredator release should be described more broadly, and – paradoxically – more complexly than simple linear smaller predator irruptions after extirpation of larger ones. On the contrary, it is about the expansion in density or distribution, or even the change in behavior of any middle-rank predator as a result from the decline in the density or distribution of an apex predator [17]. 12 MESOPREDATOR RELEASE HYPOTHESIS In the late 19th century, the United States Government started to develop a formal program aimed to control predators under the Department of Agriculture (USDA) [22]. It later culminated with the Animal Damage Control Act in 1931, establishing a systematic eradication campaign on pumas, wolves, coyotes and bears, among others [23,24]. The later herbivore irruptions caused by eradication of these large predators are very well documented [25,26]. At another scale smaller predators’ irruptions after extirpation of larger ones first appeared in scientific literature in the late 1980's and was described as mesopredator release [27]. The term was used to describe a process in which intermediate size predators (i.e. foxes and domestic cats) presented a detectable impact on prey species (birds) in the absence of the local larger predator (coyote) [17,27]. Since then, the Mesopredator Release Hypothesis (MRH) has seen alterations and adjustments on its original description, as well as many misapplications [17]. A common misapplication is to expect a straight cause and effect relation between apex and mesopredators. Negative results reported in the literature often assume that if the apex predator is absent therefore one should expect an immediate and detectable increase in mesopredator abundance. PREDATORS IN THE ATLANTIC FOREST There may be 2 apex predators in Brazil: the jaguar (Panthera onca) and the puma (Puma concolor). If the latter is an apex predator is a matter of dispute, nevertheless pumas, are certainly top predators in neotropical forests. Not different from other large carnivores around the world, jaguar populations are in decline. Despite its classification as Near Threatened globally its status at regional and local level is critic and it is now actually extinct from regions of previous occurrence [28–30]. This is the actual scenario in the Atlantic Rainforest, where jaguars only occupy 18.4% (37,825 km²) of its remaining [29]. The Atlantic Forest along the coast and interior of South America is among the most threatened tropical forest in the world – one of the world’s biodiversity hotspots – and draws a high conservation concern due to its concentration of endemic and small-ranged species [31,32]. Only seven regions in this biome – classified as Jaguar Conservation Units (JCUs) – have records of both males and females [29]. From these, only three JCUs are likely to hold at least 50 individuals (Figure 02) [29]. 13 Despite its critical status in the Atlantic Forest the loss of this specie goes way beyond its regional extinction per se. The loss of jaguar functional hole as the apex predator has profound impacts in the trophic ladder. It is the local representation of a global pattern that predicts a long term shift of mammal species pool towards small, fast-lived, highly fecund, omnivorous, generalists [14]. A study evaluating functional diversity of mammals assemblages in the Atlantic Forest found a positive relationship with forest fragment area [33]. Forest patches smaller than the threshold of 60 ha presents a remarkable loss in functional diversity and an important increase is found in patches larger than 2050 ha [33]. However, 65.5% (107,815 km²) of the remaining forest in the biome are distributed in forest patches equal or smaller than 2050 ha. Therefore, most of the Atlantic Forest mammal assemblages are distribute in forest patches with intermediate (60 – 2050 ha) and low functional diversity (≤ 60 ha). In fact it is estimated that 88% of the remaining Atlantic Forest lacks its apex predator (jaguar), its largest herbivore (tapir), its largest seed predator (white-lipped-peccaries) and its largest arboreal seed disperser (muriqui) [3]. Figure 2 - Jaguar occurrency in the Atlantic Forest. Red boxes indicate the three Jaguar Conservation Units – JCUs that potentially holds 50 individuals. Adapted from Paviolo et. al. (2016) 14 As one of the richest biomes of the planet, the Atlantic Forest holds an equally rich community of mesopredators. Some of these species with wide distribution over the biome (Table I). These species occurrence covers nearly every single forest remnant in the Atlantic Forest in contrast with the apex predator (cf. [34]). Based in traits as weight, average prey size, guild and behavior these species can the generally classified as dominant (mesocarnivores), intermediate and subordinate mesopredators (Table I). IS MESOPREDATOR RELEASE AN UNDERESTIMATED PHENOMENON IN TROPICAL FORESTS? Despite significant research interest and conservation relevance unambiguous demonstration of MRH is no trivial task. The fundamental challenge is to rule out alternative explanations for mesopredator overabundance, such as habitat loss that are usually associated with apex predator loss. A major review on the phenomenon state that the main constraint in ecological studies found in the literature is uncontrolled environmental variation [17]. Indeed the probability of mesopredator outbreaks is expected to be higher in fragmented habitats, such as the Atlantic Forest [18]. Improved resource availability and low top-down regulation - as fragmented landscapes typically present - points mesopredator release as a serious and underestimated phenomenon in imbalanced ecosystems. This should indeed be expected in biomes such as the Atlantic Rainforest where most of the original forest is gone, and more than 50% of the remaining forest is distributed in forest fragments smaller than 500 ha [35]. Associated with the absence of jaguars in most of Atlantic Forest, all other variables put together a perfect environment for mesopredator outbreak in this biome. Here I propose a conceptual model describing how this phenomenon may work in Atlantic Forest, using patches sizes thresholds related with functional diversity loss proposed by Magioli et. al. (2015) (Figure 03). I built this trophic cascade model based on general hypothesis and expected results supported by literature research and empirical knowledge on mammal carnivore communities in Atlantic Forest. 15 Table 1 – Mesopredators with wide occurrence in the Atlantic Forest and potential category of dominance. Some species were not included because their occurrence in the biome is restricted. Average prey size percentage is adapted from Magioli et. al. (2015). Carnivore, terrestrial and social columns are binary (exclusively carnivore or no, exclusively terrestrial or no, social – solitary). AVERAGE PREY SIZE % FAMILY SPECIES IUCN POTENTIAL CATEGORY WEIGHT SMALL MEDIUM LARGE INVERTEBRATES CARNIVORE TERRESTRIAL SOCIAL Canidae Cerdocyon thous LC intermediate 6,1 55,20 2,56 0,17 42,08 n y n Felidae Leopardus guttulus VU subordinate 2,1 94,40 1,40 0,20 4,00 y n n Felidae Leopardus wiedii NT subordinate 3,2 90,90 5,80 0,00 3,30 y n n Felidae Herpailurus yagouaroundi LC intermediate 6,3 94,90 4,20 0,10 0,80 y n n Felidae Leopardus pardalis LC dominant 11,5 85,80 13,70 0,50 0,00 y n n Mustelidae Galictis cuja LC subordinate 1,8 69,60 24,60 0,30 5,50 y y n Mustelidae Eira barbara LC dominant 4,8 73,35 2,09 0,00 24,56 y n n Procyonidae Nasua nasua LC intermediate 4,5 19,11 0,00 0,00 80,89 n n y Procyonidae Procyon cancrivorus LC intermediate 6 35,63 0,52 0,00 63,86 n y n 16 ASSUMPTIONS EXPECTED RESULTS PREDICTIONS a) Landscapes composed by small forest patches (<≈ 60 ha) are dominated by SM. Jaguars are absent; Pumas and DM are rare; IM occurs in specific habitat patches; SM are abundant, including domestic cats and dogs. b) Landscapes composed by medium size forest patchs (≈ 60 to ≈ 2000 ha) increases in species richness, functional diversity with increase in dominance by IM and DM. Jaguar are absent; Pumas and DM occurs and occupy larger patches; IM are more frequent in specific habitat patches; SM are abundant with less influence of domestic cats and dogs. c) Landscapes composed by large size forest patchs (≈ 2000 to ≈ 10000 ha) increases species richness and functional diversity with increase in dominance by DM. Jaguar are rare, mainly dispersing individuals exploring; Pumas and DM are dominant; IM and SM have stable populations. Domestic animals in patches edges and roads. d) Landscapes composed by extra large size forest patchs (< 10000 ha) highest species richness and functional diversity with dominance by AP and DM. Jaguars are present, both sexes present and reproducing in larger areas; Predator community stable; Domestic cats and dogs restricted to areas close to human occupation. Figure 3 - Conceptual model on potential mesopredator release outbreak in Atlantic Forest. Forest patches ranges a - c are based on Magioli et. al. (2015). 17 CONCLUSIONS Apex and top predators require large areas – a result of low densities, need of stable prey populations and large territories – and are more susceptible to habitat loss [36,37]. In addition, this particular group is more likely to be persecuted by humans. As fragmentation and habitat loss intensify, the probability of encounters and killing of domestic animals and livestock also increases [38,39]. Along with these negative effects on apex and top predators, in the opposite direction fragmentation can improve resource availability for mesopredators with the increase of pet food, trash and crop pests (e.g. mices, rats, pigeons) generally associated with regional development [18,40]. The Atlantic Forest presents all the features related with mesopredator outbreaks. Mesopredator release is quite an intuitive ecological phenomenon. Nevertheless, to detect it in regions with high redundancy in ecological functions such as tropical rainforests can become a challenge even to insightful and skilled researchers. However, data availability, dissemination and processing dramatically advance in the last decade. The recent adoption of data sharing policies by journals are an important step towards large scale analysis. For the Atlantic Forest there are a series of open datasets available on different taxa, including the second chapter of this thesis. In this chapter I put together all the key features of mesopredator release hypothesis adapted to a regional context: the mammal carnivore community of Atlantic Forest. I hope this synthesis and general hypothesis may be a useful reference to guide future large-scale analyses on this phenomenon which the outcome and consequences for biodiversity conservation are anything but predictable. 18 REFERENCES 1. Fahrig L. Rethinking patch size and isolation effects: The habitat amount hypothesis. J Biogeogr. 2013;40: 1649–1663. doi:10.1111/jbi.12130 2. Haddad NM, Brudvig L a., Clobert J, Davies KF, Gonzalez A, Holt RD, et al. Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci Adv. 2015;1: e1500052–e1500052. doi:10.1126/sciadv.1500052 3. Jorge MLSP, Galetti M, Ribeiro MC, Ferraz KMPMB. Mammal defaunation as surrogate of trophic cascades in a biodiversity hotspot. Biol Conserv. 2013;163: 49–57. doi:10.1016/j.biocon.2013.04.018 4. Ryall KL, Fahrig L. Response of predators to loss and fragmentation of prey habitat: A review of theory. Ecology. 2006;87: 1086–1093. 5. Valiente‐Banuet A, Aizen MA, Alcántara JM, Arroyo J, Cocucci A, Galetti M, et al. Beyond species loss: the extinction of ecological interactions in a changing world. Johnson M, editor. Funct Ecol. 2015;29: 299–307. doi:10.1111/1365- 2435.12356 6. Estes J a, Terborgh J, Brashares JS, Power ME, Berger J, Bond WJ, et al. Trophic Downgrading of Planet Earth. Science (80- ). 2011;333: 301–306. doi:10.1126/science.1205106 7. Roemer GW, Gompper ME, Van Valkenburgh B. The Ecological Role of the Mammalian Mesocarnivore. Bioscience. 2009;59: 165–173. doi:10.1525/bio.2009.59.2.9 8. Terborgh J. Ecological Meltdown in Predator-Free Forest Fragments. Science (80- ). 2001;294: 1923–1926. doi:10.1126/science.1064397 9. Soulé ME, Estes JA, Miller B, Honnold DL. Strongly interacting species: Conservation policy, management, and ethics. Bioscience. 2005;55: 168–176. doi:10.1641/0006-3568(2005)055[0168:SISCPM]2.0.CO;2 10. Ripple WJ, Estes J a, Beschta RL, Wilmers CC, Ritchie EG, Hebblewhite M, et al. Status and ecological effects of the world’s largest carnivores. Science (80- ). 2014;343: 1241484. doi:10.1126/science.1241484 19 11. Wallach AD, Izhaki I, Toms JD, Ripple WJ, Shanas U. What is an apex predator? Oikos. 2015;124: 1453–1461. doi:10.1111/oik.01977 12. Balme G a., Hunter LTB, Slotow R. Evaluating Methods for Counting Cryptic Carnivores. J Wildl Manage. 2009;73: 433–441. doi:10.2193/2007-368 13. Paviolo A, De Angelo C, Ferraz KMPMB, Morato RG, Martinez Pardo J, Srbek- Araujo AC, et al. A biodiversity hotspot losing its top predator: The challenge of jaguar conservation in the Atlantic Forest of South America. Sci Rep. 2016;6: 37147. doi:10.1038/srep37147 14. Cooke RSC, Eigenbrod F, Bates AE. Projected losses of global mammal and bird ecological strategies. Nat Commun. 2019;10: 2279. doi:10.1038/s41467- 019-10284-z 15. Young HS, McCauley DJ, Galetti M, Dirzo R. Patterns, Causes, and Consequences of Anthropocene Defaunation. Annu Rev Ecol Evol Syst. 2016;47: 333–358. doi:10.1146/annurev-ecolsys-112414-054142 16. Promislow DEL, Harvey PH. Living fast and dying young: A comparative analysis of life-history variation among mammals. J Zool. 1990;220: 417–437. doi:10.1111/j.1469-7998.1990.tb04316.x 17. Brashares JS, Prugh LR, Stoner CJ, Epps CW. Ecological and conservation implications of mesopredator release. Trophic cascades predators, prey, Chang Dyn Nat. 2010; 221–240. 18. Prugh LR, Stoner CJ, Epps CW, Bean WT, Ripple WJ, Laliberte AS, et al. The Rise of the Mesopredator. Bioscience. 2009;59: 779–791. doi:10.1525/bio.2009.59.9.9 19. Palomares F, Caro TM. Interspecific Killing among Mammalian Carnivores. Am Nat. 1999;153: 492–508. doi:10.1086/303189 20. Ritchie EG, Johnson CN. Predator interactions, mesopredator release and biodiversity conservation. Ecol Lett. 2009;12: 982–998. doi:10.1111/j.1461- 0248.2009.01347.x 21. Gebrt SD, Clark WR. Raccoons, coyotes, and reflections on the mesopredator 20 release hypothesis. Wildl Soc Bull. 2003;31: 836–842. doi:10.2307/3784607 22. Bacon T. The Implementation of the Animal Damage Control Act : A Comment on Wildlife Services ’ s Methods of Predatory Animal Control. 2012;32. 23. Hawthorne DW. The history of federal and cooperative animal damage control. Sheep Goat Res J. 2004;19: 13–15. 24. Stolzenburg W. Where the wild things were: life, death and ecological wreckage of vanishing predators. 1st ed. Nature. New York: Bloomsbury; 2008. 25. Berger J, Stacey PB, Bellis L, Johnson MP. A mammalian predator-prey imbalance: Grizzly bear and wolf extinction affect avian neotropical migrants. Ecol Appl. 2001;11: 947–960. doi:10.1890/1051- 0761(2001)011[0947:AMPPIG]2.0.CO;2 26. Ripple WJ, Wirsing AJ, Wilmers CC, Letnic M. Widespread mesopredator effects after wolf extirpation. Biol Conserv. 2013;160: 70–79. doi:10.1016/j.biocon.2012.12.033 27. Soulé M., Bolger D., Alberts A., Wright J, Sorice M, Hill S. Reconstructed of Rapid Extinctions of Dynamics Birds in Urban Habitat Islands. Conserv Biol. 1988;2: 75–92. doi:10.1111/j.1523-1739.1988.tb00337.x 28. Quigley H, Foster RJ, Petracca L, Payan E, Salom R, Harmsen BJ. Panthera onca. IUCN Red List Threat Species. 2017;8235: 8. Available: http://dx.doi.org/10.2305/IUCN.UK.2016-3.RLTS.T20010A22247615.en 29. Paviolo A, De Angelo C, Ferraz KMPMB, Morato RG, Martinez Pardo J, Srbek- Araujo AC, et al. A biodiversity hotspot losing its top predator: The challenge of jaguar conservation in the Atlantic Forest of South America. Sci Rep. 2016;6: 37147. doi:10.1038/srep37147 30. Paviolo A, De Angelo CD, Di Blanco YE, Di Bitetti MS. Jaguar Panthera onca population decline in the Upper Paraná Atlantic Forest of Argentina and Brazil. Oryx. 2008;42: 554. doi:10.1017/S0030605308000641 31. Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Kent J. Biodiversity hotspots for conservation priorities. Nature. 2000;403: 853–858. 21 32. Jenkins CN, Alves MAS, Uezu A, Vale MM. Patterns of Vertebrate Diversity and Protection in Brazil. Stow A, editor. PLoS One. 2015;10: e0145064. doi:10.1371/journal.pone.0145064 33. Magioli M, Ribeiro MC, Ferraz KMPMB, Rodrigues MG. Thresholds in the relationship between functional diversity and patch size for mammals in the Brazilian Atlantic Forest. Anim Conserv. 2015; n/a-n/a. doi:10.1111/acv.12201 34. Nagy‐Reis M, Oshima JE de F, Kanda CZ, Palmeira FBL, Melo FR, Morato RG, et al. NEOTROPICAL CARNIVORES: a data set on carnivore distribution in the Neotropics. Ecology. 2020;101. doi:10.1002/ecy.3128 35. Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota MM. The Brazilian Atlantic Forest: How much is left, and how is the remaining forest distributed? Implications for conservation. Biol Conserv. 2009;142: 1141–1153. doi:10.1016/j.biocon.2009.02.021 36. Crooks KR. Relative sensitivities of mammalian carnivores to habitat fragmentation. Conserv Biol. 2002;16: 488–502. 37. De Angelo C, Paviolo A, Rode D, Cullen L, Sana D, Abreu KC, et al. Participatory networks for large-scale monitoring of large carnivores: pumas and jaguars of the Upper Paraná Atlantic Forest. Oryx. 2011;45: 534–545. doi:10.1017/S0030605310000840 38. Cardillo M, Purvis A, Sechrest W, Gittleman JL, Bielby J, Mace GM. Human population density and extinction risk in the world’s carnivores. PLoS Biol. 2004;2. doi:10.1371/journal.pbio.0020197 39. Cavalcanti SMC, Gese EM. Kill rates and predation patterns of jaguars (Panthera onca) in the southern Pantanal, Brazil. J Mammal. 2010;91: 722–736. doi:10.1644/09-MAMM-A-171.1 40. Crooks K, Soulé M. Mesopredator release and avifaunal extinctions in a fragmented system. Nature. 1999;400: 563–566. doi:10.1038/23028 CHAPTER 02 ATLANTIC CAMTRAPS: a dataset of medium and large terrestrial mammal communities in the Atlantic Forest of South America. O senhor saiba: eu toda a minha vida pensei por mim, forro, sou nascido diferente. Eu sou é eu mesmo. Divirjo de todo o mundo... Eu quase que nada não sei. Mas desconfio de muita coisa. O senhor concedendo, eu digo: para pensar longe, sou cão mestre – o senhor solte em minha frente uma idéia ligeira, e eu rastreio essa por fundo de todos os matos, amém! Riobaldo Tatarana, Grande Sertão: veredas. ATLANTIC-CAMTRAPS: a dataset of medium and large terrestrial mammal communities in the Atlantic Forest of South America FERNANDO LIMA,1,2,36 GABRIELLE BECA,1 RENATA L. MUYLAERT,1 CLINTON N. JENKINS,2 MIRIAM L. L. PERILLI,3 ANA MARIA O. PASCHOAL,4 RODRIGO L. MASSARA,4 ADRIANO P. PAGLIA,4 ADRIANO G. CHIARELLO,5 MAUR�ICIO E. GRAIPEL,6 JORGE J. CHEREM,7 ANDR�E L. REGOLIN,1 LUIZ GUSTAVO R. OLIVEIRA SANTOS,8 CARLOS R. BROCARDO,1,9 AGUST�IN PAVIOLO,10,11 MARIO S. DI BITETTI,10,11,12 LEANDRO M. SCOSS,13 FABIANA L. ROCHA,14 ROBERTO FUSCO-COSTA,15,16 CLARISSA A. ROSA,17 MARINA X. DA SILVA,18 LUDMILA HUFNAGELL,4 PALOMA M. SANTOS,4 GABRIELA T. DUARTE,4 LUIZA N. GUIMAR~AES,4 LARISSA L. BAILEY,19 FL�AVIO HENRIQUE G. RODRIGUES,4 HEITOR M. CUNHA,20 FELIPE M. FANTACINI,21 GRAZIELE O. BATISTA,22 JULIANO A. BOGONI,23 MARCO A. TORTATO,24 MICHELI R. LUIZ,25 NIVALDO PERONI,6 PEDRO V. DE CASTILHO,26 THIAGO B. MACCARINI,27 VILMAR PICINATTO FILHO,28 CARLOS DE ANGELO,10,11 PAULA CRUZ,10,11 VER�ONICA QUIROGA,10,11 MAR�IA E. IEZZI,10,11 DIEGO VARELA,10,11 SANDRA M. C. CAVALCANTI,3 ALEXANDRE C. MARTENSEN,29 ERICAV. MAGGIORINI,30 FAB�IOLA F. KEESEN,31 ANDR�EV. NUNES,24 GISELE M. LESSA,32 PEDRO CORDEIRO-ESTRELA,33 MAYARAG. BELTR~AO,33,34 ANNA CAROLINA F. DE ALBUQUERQUE,33,34 BIANCA INGBERMAN,15 CAMILA R. CASSANO,35 LAURYCULLEN JUNIOR,2 MILTON C. RIBEIRO,1,36 AND MAURO GALETTI 1,36 Abstract. Our understanding of mammal ecology has always been hindered by the difficul- ties of observing species in closed tropical forests. Camera trapping has become a major advance for monitoring terrestrial mammals in biodiversity rich ecosystems. Here we compiled one of the largest datasets of inventories of terrestrial mammal communities for the Neotropi- cal region based on camera trapping studies. The dataset comprises 170 surveys of medium to large terrestrial mammals using camera traps conducted in 144 areas by 74 studies, covering six vegetation types of tropical and subtropical Atlantic Forest of South America (Brazil and Argentina), and present data on species composition and richness. The complete dataset com- prises 53,438 independent records of 83 species of mammals, includes 10 species of marsupials, 15 rodents, 20 carnivores, eight ungulates and six armadillos. Species richness averaged 13 spe- cies (�6.07 SD) per site. Only six species occurred in more than 50% of the sites: the domestic dog Canis familiaris, crab-eating fox Cerdocyon thous, tayra Eira barbara, south American coati Nasua nasua, crab-eating raccoon Procyon cancrivorus and the nine-banded armadillo Dasypus novemcinctus. The information contained in this dataset can be used to understand macroeco- logical patterns of biodiversity, community, and population structure, but also to evaluate the ecological consequences of fragmentation, defaunation, and trophic interactions. Key words: Atlantic Forest; biodiversity hotspot; camera traps; forest fragmentation; invasive species; mammal communities; neotropical mammals. The complete data sets corresponding to abstracts published in the Data Papers section in the journal are published electronically as Supporting Information in the online version of this article at http://onlinelibrary.wiley.com/doi/10.1002/ ecy.1998/suppinfo Manuscript received 5 May 2017; revised 31 July 2017; accepted 16 August 2017. Corresponding Editor: W. K. Michener. 36 E-mail: pardalismitis@gmail.com 2979 Data Papers Ecology, 98(11), 2017, pp. 2979 © 2017 by the Ecological Society of America http://onlinelibrary.wiley.com/doi/10.1002/ecy.1998/suppinfo http://onlinelibrary.wiley.com/doi/10.1002/ecy.1998/suppinfo For Review O nly ATLANTIC-CAMTRAPS: a dataset of medium and large terrestrial mammal communities in the Atlantic Forest of South America Journal: Ecology Manuscript ID ECY17-0483 Wiley - Manuscript type: Data Papers Date Submitted by the Author: 05-May-2017 Complete List of Authors: Lima, Fernando; Universidade Estadual Paulista Julio de Mesquita Filho - Campus de Rio Claro, Spacial Ecology and Conservation Lab; Instituto de Pesquisas Ecologicas, Beca, Gabrielle; Universidade Estadual Paulista Julio de Mesquita Filho - Campus de Rio Claro, Muylaert, Renata; UNESP São Paulo State University Jenkins, Clinton; Instituto de Pesquisas Ecologicas Perilli, Miriam; Instituto Pró-Carnívoros, Paschoal, Ana Maria; Universidade Federal de Minas Gerais Instituto de Ciencias Biologicas, Departamento de Biologia Geral Massara, Rodrigo; Universidade Federal de Minas Gerais Instituto de Ciencias Biologicas, Departamento de Biologia Geral Paglia, Adriano; Universidade Federal de Minas Gerais Instituto de Ciencias Biologicas, Departamento de Biologia Geral Chiarello, Adriano; Universidade de Sao Paulo Campus de Ribeirao Preto, Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras Graipel, Maurício; Universidade Federal de Santa Catarina, Ecology and Zoology Cherem, Jorge; Caipora Cooperativa, Regolin, André; Universidade Estadual Paulista Julio de Mesquita Filho - Campus de Rio Claro, Ecology Oliveira Santos, Luiz Gustavo; Rio de Janeiro Federal University Brocardo, Carlos; Universidade Estadual Paulista Julio de Mesquita Filho, Ecology Paviolo, Agustín; National Research Council (CONICET); Instituto de Biologia Subtropical, Facultad de Ciencias Forestales, Universidad Nacional de Misiones Di Bitetti, Mario; National Research Council (CONICET); Instituto de Biologia Subtropical, Facultad de Ciencias Forestales, Universidad Nacional de Misiones Scoss, Leandro; Bicho do Mato Instituto de Pesquisa, Pesquisa Rocha, Fabiana; Universidade Federal da Paraíba. Campus IV - Litoral Norte, Centro de Ciências Aplicadas e Educação - CCAE Fusco-Costa, Roberto; IPeC-Instituto de Pesquisas Cananéia, ; Universidade Federal do Parana, Zoologia, Pós-graduação Ecologia e Conservação Ecology For Review O nly Rosa, Clarissa; Instituto Alto Montana da Serra Fina, da Silva, Marina; Parque Nacional do Iguaçu, Projeto Carnívoros do Iguaçu; Parque Nacional do Iguaçu Hufnagel, Ludmila; Universidade Federal de Minas Gerais, Biologia Geral Santos, Paloma; Universidade Federal de Minas Gerais Instituto de Ciencias Biologicas, Biologia Geral; Duarte, Gabriela; Universidade Federal de Minas Gerais Instituto de Ciencias Biologicas, Guimarães, Luiza; Universidade Federal de Minas Gerais Instituto de Ciencias Biologicas, Instituto de Ciências Biológicas Bailey, Larissa; Colorado State University, Dept of Fish, Wildlife and Conservation Biology Guimarães Rodrigues, Flavio Henrique; Universidade Federal de Minas Gerais Instituto de Ciencias Biologicas, Biologia Geral Cunha, Heitor; Sete Soluções e Tecnologia Ambiental Ltda, Moreli Fantacini, Felipe; Instituto Ambiental Brüderthal, Batista, Graziele; Universidade Federal de Santa Catarina, Departamento de Ecologia e Zoologia Bogoni, Juliano; Universidade Federal de Santa Catarina, Ecologia e Zoologia Tortato, Marcos; Universidade Federal de Mato Grosso do Sul, Ecology and Conservation Postgraduate Program Luiz, Micheli; Universidade do Extremo Sul Catarinense, Programa de Pos- Graduacão em Gestão de Recursos Naturais; Instituto Felinos do Aguaí, Pesquisa Peroni, Nivaldo; Universidade Federal de Santa Catarina, Department of Ecology and Zoology Volkmer de Castilho, Pedro; Universidade do Estado de Santa Catarina, Maccarini, Thiago; Corpo de Bombeiros Militar de Santa Catarina, Picinatto Filho, Vilmar; Universidade Federal do Parana, De Angelo, Carlos; National Research Council (CONICET); Instituto de Biologia Subtropical, Facultad de Ciencias Forestales, Universidad Nacional de Misiones Cruz, Maria; Instituto de Biología Subtropical, CONICET-Universidad Nacional de Misiones (UNaM), Quiroga, Veronica Andrea; Instituto de Biologia Subtropical (IBS) CONICET/UNaM, Iezzi, Maria; Instituto de Biología Subtropical CONICET and Universidad Nacional de Misiones, Varela, Diego; Instituto de Biología Subtropical (CONICET-Universidad Nacional de Misiones), Cavalcanti, Sandra; Instituto Pró-Carnívoros Martensen, Alexandre; Instituto Nacional de Pesquisas da Amazonia, GCBEv Maggiorini, Erica Vanessa; Prefeitura da Estância Turística de Salto, Secretaria de Meio Ambiente Keesen, Fabíola; Universidade Federal de Ouro Preto, Valle Nunes, André; Universidade Federal de Mato Grosso do Sul, Ecology and Conservation Lessa, Gisele; Universidade Federal de Vicosa, Biologia Animal Cordeiro-Estrela, Pedro; Universidade Federal da Paraiba, Departamento de Sistemática e EcologiaCentro de Ciências Exatas e da Natureza Beltrão, Mayara; Universidade Federal da Paraiba, Ecologia e Evolução Albuquerque, Anna Carolina; Universidade Federal da Paraiba, Departamento de Sistemática e Ecologia Ingberman, Bianca; Instituto de Pesquisas Cananéia, Cassano, Camila; Universidade Estadual de Santa Cruz, Laboratório de Ecologia Aplicada à Conservação Cullen Jr., Laury; Instituto de Pesquisas Ecologicas Ribeiro, Milton; UNESP - São Paulo State University, Ecology Galetti, Mauro; Universidade Estadual Paulista, Ecologia Page 1 of 35 Ecology For Review O nly Substantive Area: Population Ecology < Substantive Area, Data paper < Data < Substantive Area, Community Ecology < Substantive Area Organism: Mammals < Vertebrates < Animals, Marsupials < Mammals < Vertebrates < Animals, Primates < Mammals < Vertebrates < Animals, Carnivores < Mammals < Vertebrates < Animals, Rodents < Mammals < Vertebrates < Animals Habitat: Rain Forest < Tropical Zone < Terrestrial < Habitat, Deciduous Forest < Tropical Zone < Terrestrial < Habitat Geographic Area: Eastern South America (Guyana, Fr. Guiana, Suriname, Brazil) < South America < Geographic Area Additional Keywords: Atlantic Forest, forest fragmentation, camera traps, neotropical mammals, biodiversity hotspot, mammal communities, invasive species Abstract: Our understanding of mammal ecology has always been hindered by the difficulties of observing species in closed tropical forests. Camera trapping has become a major advance for monitoring terrestrial mammals in biodiversity rich ecosystems. Here we compile the largest dataset of inventories of terrestrial mammal communities for the Neotropical region based on camera trapping studies. The dataset comprises 170 surveys of medium to large terrestrial mammals using camera traps conducted in 144 areas by 74 studies, covering six vegetation types of tropical and subtropical Atlantic Forests of South America (Brazil and Argentina), and present data on species composition and richness. The complete dataset comprises 53,438 independent records of 83 species of mammals, includes 10 species of marsupials, 15 rodents, 20 carnivores, 8 ungulates and 6 armadillos. Species richness averaged 13 species (± 6.07 SD) per site. Only six species occurred in more than 50% of the sites: the domestic dog Canis familiaris, crab-eating fox Cerdocyon thous, tayra Eira barbara, south American coati Nasua nasua, crab-eating raccoon Procyon cancrivorus and the nine-banded armadillo Dasypus novemcinctus. The information contained in this dataset can be used to understand macroecological patterns of biodiversity, community, and population structure, but also to evaluate the ecological consequences of fragmentation, defaunation, and trophic interactions. Note: The following files were submitted by the author for peer review, but cannot be converted to PDF. You must view these files (e.g. movies) online. ATLANTIC_CAMTRAPS_1-0_STUDY.csv ATLANTIC_CAMTRAPS_1-0_LOCATION.csv ATLANTIC_CAMTRAPS_1-0_SURVEY.csv ATLANTIC_CAMTRAPS_1-0_RECORDS.csv ATLANTIC_CAMTRAPS_1-0_SPECIES.csv Page 2 of 35Ecology For Review O nly 1 ATLANTIC-CAMTRAPS: a dataset of medium and large terrestrial mammal communities in the Atlantic Forest of South America Fernando Lima1,2*, Gabrielle Beca1, Renata de Lara Muylaert1, Clinton N. Jenkins2, Miriam Lucia Lages Perilli3, Ana Maria de Oliveira Paschoal4, Rodrigo Lima Massara4, Adriano Pereira Paglia4, Adriano Garcia Chiarello5, Maurício Eduardo Graipel6, Jorge José Cherem7, André Luis Regolin1, 5 Luiz Gustavo Rodrigues Oliveira Santos8, Carlos Rodrigo Brocardo1,9, Agustín Paviolo10,11, Mario S. Di Bitetti10,11,12, Leandro Moraes Scoss13, Fabiana Lopes Rocha14, Roberto Fusco-Costa15, 16, Clarissa Alves da Rosa17, Marina Xavier da Silva18, Ludmila Hufnagel4, Paloma Marques Santos4, Gabriela Teixeira Duarte4, Luiza Neves Guimarães4, Larissa Lynn Bailey19, Flávio Henrique Guimarães Rodrigues4, Heitor Morais Cunha20, Felipe Moreli Fantacini21, Graziele Oliveira 10 Batista22, Juliano André Bogoni23, Marco Adriano Tortato24, Micheli Ribeiro Luiz25, Nivaldo Peroni6, Pedro Volkmer de Castilho26, Thiago Bernardes Maccarini27, Vilmar Picinatto Filho28, Carlos De Angelo10,11, Paula Cruz10,11, Verónica Quiroga10,11, María Eugenia Iezzi10,11, Diego Varela10,11, Sandra Maria Cintra Cavalcanti3, Alexandre Camargo Martensen29, Erica Vanessa Maggiorini30, Fabíola Ferreira Keesen31, André Valle Nunes24, Gisele Mendes Lessa32, Pedro 15 Cordeiro-Estrela33, Mayara Guimarães Beltrão33,34, Anna Carolina Figueiredo de Albuquerque33,34, Bianca Ingberman15, Camila Righetto Cassano35, Laury Cullen Junior2, Milton Cezar Ribeiro1,*, Mauro Galetti1,* 1. Universidade Estadual Paulista (UNESP), Instituto de Biociências, Departamento de 20 Ecologia, CP 199, Rio Claro, SP, 13506-900, Brasil 2. IPÊ – Instituto de Pesquisas Ecológicas, CP 47, Nazaré Paulista, SP, 12960-000, Brasil 3. Instituto para Conservação dos Carnívoros Neotropicais (Pró-Carnívoros), Avenida Horácio Neto, 1030, Atibaia, SP, Brasil 4. Universidade Federal de Minas Gerais, Departamento de Biologia Geral, Avenida 25 Antônio Carlos, nº. 6627, Belo Horizonte, MG, 31270-901, Brasil 5. Universidade de São Paulo, Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Avenida Bandeirantes, nº 3900, Ribeirão Preto, SP, 14040- 901, Brasil 6. Universidade Federal de Santa Catarina, Departamento de Ecologia e Zoologia, 30 Florianópolis, SC, 88040-900, Brasil 7. Caipora Cooperativa para a Conservação da Natureza, Florianópolis, SC, 88040-400, Brasil 8. Universidade Federal de Mato Grosso do Sul, Instituto de Biologia, Departamento de Ecologia, Av. Costa e Silva s/ nº, Campo Grande, MS, 79070-900, Brasil 35 9. Instituto Neotropical: Pesquisa e Conservação, Curitiba, PR, Brasil 10. Instituto de Biología Subtropical (IBS), Universidad Nacional de Misiones (CONICET) 11. Asociación Civil Centro de Investigaciones del Bosque Atlántico (CeIBA), Bertoni 85, 3370 Puerto Iguazú, Misiones, Argentina 12. Facultad de Ciencias Forestales, Universidad Nacional de Misiones, Bertoni 124, 3380 40 Eldorado, Argentina 13. Tropical Ecology Assessment and Monitoring Network, Terrestrial Vertebrate, Site Rio Doce, Bicho do Mato Instituto de Pesquisa, Avenida Cônsul Antônio Cadar, 600, Belo Horizonte, MG, 30360-082, Brasil 14. Universidade Federal da Paraíba, Programa de Pós-Graduação em Ecologia e 45 Page 3 of 35 Ecology For Review O nly 2 Monitoramento Ambiental, Campus IV, Rio Tinto, PB, 58297-000, Brasil 15. Instituto de Pesquisas Cananéia (IPeC), Rua Tristão Lobo, nº 199, Cananéia, SP, 11990- 000, Brasil 16. Universidade Federal do Paraná, Programa de Pós-Doutorado em Ecologia e Conservação, CP 19031, Curitiba, PR, 81531-990, Brasil 50 17. Instituto Alto Montana da Serra Fina, BR 354, Km 768, Bairro Engenho de Serra, Itamonte, MG, 37466-000, Brasil 18. Projeto Carnívoros do Iguaçu, Parque Nacional do Iguaçu, Br 469, Km 22.5, Foz do Iguaçu, PR, 85851-970, Brasil 19. Colorado State University, Department of Fish, Wildlife, and Conservation Biology, 1474 55 Campus Delivery, 109 Wagar, Fort Collins, CO 80523, USA 20. Sete Soluções e Tecnologia Ambiental, Rua Pernambuco, nº.1000, Belo Horizonte, MG, 30130-151, Brasil 21. Instituto Ambiental Brüderthal, Brusque, SC, 88353-190, Brasil 22. Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis, SCEN Trecho 60 02, Edifício Sede, Brasília, DF, 70818-900, Brasil 23. Universidade Federal de Santa Catarina, Programa de Pós-Graduação em Ecologia, Florianópolis, SC, 88040-900, Brasil 24. Universidade Federal de Mato Grosso do Sul, Programa de Pós-Graduação em Ecologia e Conservação, Avenida Costa e Silva s/nº, Bairro Universitário, Campo Grande, MS, 65 79070-900, Brasil 25. Instituto Felinos do Aguaí, Siderópolis, SC, 88860-000, Brasil 26. Universidade do Estado de Santa Catarina, Departamento de Engenharia de Pesca, Laguna, SC, 88790-000, Brasil 27. Rua Martim Stahl, 551, apto 803, Bairro Vila Nova, Jaraguá do Sul, SC, 89259-310, Brasil 70 28. Universidade Federal do Paraná, Programa de Pós-Graduação em Engenharia Florestal, Curitiba, PR, 80035-050, Brasil 29. Instituto Nacional de Pesquisas da Amazônia (INPA), Programa de Pós-Graduação em Genética, Conservação e Biologia Evolutiva (GCBEv), Avenida André Araújo, 2936, Aleixo, CP 2223, Manaus, AM, 69060-001, Brasil 75 30. Secretaria de Meio Ambiente, Prefeitura da Estância Turística de Salto, Avenida Nove de Julho, 1053, Salto, SP, 13322-900, Brasil 31. Universidade Federal de Ouro Preto, Programa de Pós-Graduação em Ecologia de Biomas Tropicais, Campus Universitário Morro do Cruzeiro, Ouro Preto, MG, 35400-000, Brasil 80 32. Universidade Federal de Viçosa, Departamento de Biologia Animal, Laboratório de Mastozoologia, CCB2, 3º andar, Av. P.H. Rolfs s/nº, Campus UFV, Viçosa, MG, 36570- 900, Brasil 33. Universidade Federal da Paraíba, Laboratório de Mamíferos, Departamento de Sistemática e Ecologia, CCEN, Jardim Universitário, s/nº, Castelo Branco III, João Pessoa, 85 PB, 58051-900, Brasil 34. Universidade Federal da Paraíba, Programa de Pós-Graduação em Ciências Biológicas (Zoologia) 35. Universidade Estadual de Santa Cruz, Laboratório de Ecologia Aplicada à Conservação, Rodovia Jorge Amado, Km 16, Salobrinho, Ilhéus, BA, 45662-900, Brasil 90 * Correspondence and requests for materials should be addressed to Fernando Lima (email: pardalismitis@gmail.com), Milton Cezar Ribeiro (mcr@rc.unesp.br) or Mauro Galetti (mgaletti@rc.unesp.br). Page 4 of 35Ecology mailto:pardalismitis@gmail.com) mailto:mcr@rc.unesp.br mailto:mgaletti@rc.unesp.br) For Review O nly 3 INTRODUCTION 95 Camera traps have been used in studies of wild animals since the early 20th century (Chapman 1927). From the first attempts by George Shiras III to create self-triggered cameras in the early 1900’s, to modern day camera traps, this tool has become essential in wildlife monitoring (Kucera and Barrett 2011). Its vast potential to monitor mammal communities soon became evident, and wildlife researchers realized that photography would be an invaluable aid to study 100 animals in their natural environment. From then on, the development of camera trap technology, associated with a relative reduction in its costs, allowed an exponential increase in studies applying this method, especially with species difficult to observe and detect otherwise (Ahumada et al. 2013, Pimm et al. 2015). Most terrestrial vertebrates – such as large mammal species – occur at low densities and are 105 very secretive. Consequently, any relevant ecological question at the population or community level requires a huge effort in the field. In addition, with the continuous decline of biodiversity worldwide, many mammal species are becoming increasingly rare in areas with high hunting pressure, habitat loss and habitat fragmentation (Butchart et al. 2010, Ripple et al. 2016). Systematic studies using camera traps over the past decade were aimed mainly at species 110 inventories, activity patterns and estimation of abundance (Tobler et al. 2008a, 2008b). These studies have brought novel information on the distribution and behavior of many species. Long-term wildlife monitoring programs and online databases, such as the Tropical Ecology Assessment and Monitoring Network, are dealing with an unprecedented amount of species records and data from camera traps surveys (Jansen et al. 2014). However, often information is 115 kept trapped and dispersed in dissertations, reports, and all kinds of gray literature. At another level, wildlife surveys conducted by non-governmental agencies and private consultants are rarely easily accessible. Thus, the potential to detect large scale or global patterns by using this large amount of data is still underutilized due to most of the information being fragmented and inaccessible in regional samplings. 120 The Atlantic Forest along the coast and interior of South America is among the most threatened tropical forest in the world – one of the world’s biodiversity hotspots – and draws a high conservation concern due to its concentration of endemic and small-ranged species (Myers et al. 2000, Jenkins et al. 2015). In this hotspot, where only 12% of original forest still remains, the use of camera traps became increasingly accessible and popular in the early 2000’s (Srbek-125 Araujo and Chiarello 2005, Ribeiro et al. 2009). Here we summarize and make available a database on camera trap studies conducted in the Atlantic Forest hotspot. Data were compiled from the existing literature and through direct contact with research groups and professionals. This dataset is a large-scale synthesis of studies that used camera traps to sample medium and large terrestrial mammals in a biodiversity hotspot. It is the first joined effort of field researchers 130 and ecologists to organize a large-scale dataset of this kind, and provides an opportunity for understanding macroecological patterns, improving conservation strategies, and new community ecology research. The uniqueness of this dataset is that we were able to gather a large amount of raw and unpublished data through a network of collaborators and within a representative geographic extension of the Atlantic Forest hotspot. It combines 53,438 135 independent records of 83 mammalian species from 170 surveys conducted in 144 areas by 74 studies. Page 5 of 35 Ecology For Review O nly 4 METADATA CLASS I. DATA SET DESCRIPTORS A. Data set identity: ATLANTIC-CAMTRAPS: a dataset of medium and large terrestrial mammal 140 communities in the Atlantic Forest of South America B. Data set identification code: (1) ATLANTIC_CAMTRAPS_1-0_STUDY.csv (2) ATLANTIC_CAMTRAPS_1-0_LOCATION.csv (3) ATLANTIC_CAMTRAPS_1-0_SURVEY.csv 145 (4) ATLANTIC_CAMTRAPS_1-0_RECORDS.csv (5) ATLANTIC_CAMTRAPS_1-0_SPECIES.csv C. Data set description: Principal Investigator(s): 1. Fernando Lima, Renata de Lara Muylaert, Gabrielle Beca, Carlos Rodrigo Brocardo, Mauro 150 Galetti, Milton Cezar Ribeiro Universidade Estadual Paulista (UNESP), Instituto de Biociências, Departamento de Ecologia, CP 199, Rio Claro, SP, 13506-900, Brasil 2. Fernando Lima, Clinton N. Jenkins, Laury Cullen Jr. 155 IPÊ – Instituto de Pesquisas Ecológicas, CP 47, Nazaré Paulista, SP, 12960-000, Brasil 3. Miriam Lucia Lages Perilli Instituto para Conservação dos Carnívoros Neotropicais (Pró-Carnívoros), Avenida Horácio Neto, 1030, Atibaia, SP, Brasil 160 4. Ana Maria de Oliveira Paschoal, Rodrigo Lima Massara, Adriano Pereira Paglia Universidade Federal de Minas Gerais, Departamento de Biologia Geral, Avenida Antônio Carlos, nº. 6627, Belo Horizonte, MG, 31270-901, Brasil 165 5. Adriano Garcia Chiarello Universidade de São Paulo, Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Avenida Bandeirantes, nº 3900, Ribeirão Preto, SP, 14040-901, Brasil 170 6. Maurício Eduardo Graipel Universidade Federal de Santa Catarina, Departamento de Ecologia e Zoologia, Florianópolis, SC, 88040-900, Brasil 7. Jorge José Cherem 175 Caipora Cooperativa para a Conservação da Natureza, Florianópolis, SC, 88040-400, Brasil Page 6 of 35Ecology For Review O nly 5 8. Luiz Gustavo Rodrigues Oliveira Santos Universidade Federal de Mato Grosso do Sul, Instituto de Biologia, Departamento de Ecologia, Av. Costa e Silva s/ nº, Campo Grande, MS, 79070-900, Brasil 180 9. Carlos Rodrigo Brocardo Instituto Neotropical: Pesquisa e Conservação, Curitiba, PR, Brasil 10. Agustín Paviolo, Mario S. Di Bitetti 185 Instituto de Biología Subtropical (IBS), Universidad Nacional de Misiones (CONICET) 11. Agustín Paviolo, Mario S. Di Bitetti Asociación Civil Centro de Investigaciones del Bosque Atlántico (CeIBA), Bertoni 85, 3370 Puerto Iguazú, Misiones, Argentina 190 12. Mario S. Di Bitetti Facultad de Ciencias Forestales, Universidad Nacional de Misiones, Bertoni 124, 3380 Eldorado, Argentina 195 13. Leandro Moraes Scoss Tropical Ecology Assessment and Monitoring Network, Terrestrial Vertebrate, Site Rio Doce, Bicho do Mato Instituto de Pesquisa, Avenida Cônsul Antônio Cadar, 600, Belo Horizonte, MG, 30360-082, Brasil 200 14. Pedro Cordeiro-Estrela Universidade Federal da Paraíba, Laboratório de Mamíferos, Departamento de Sistemática e Ecologia, CCEN, Cidade Universitária, s/nº, Castelo Branco III, João Pessoa, PB, 58051-900, Brasil 205 15. Roberto Fusco-Costa Instituto de Pesquisas Cananéia (IPeC), Rua Tristão Lobo, nº 199, Cananéia, SP, 11990-000, Brasil 16. Clarissa Alves da Rosa 210 Instituto Alto Montana da Serra Fina, BR 354, Km 768, Bairro Engenho de Serra, Itamonte, MG, 37466-000, Brasil 17. Marina Xavier da Silva Projeto Carnívoros do Iguaçu, Parque Nacional do Iguaçu, Br 469, Km 22.5, Foz do Iguaçu, 215 PR, 85851-970, Brasil Page 7 of 35 Ecology For Review O nly 6 Abstract: Our understanding of mammal ecology has always been hindered by the difficulties of observing species in closed tropical forests. Camera trapping has become a major advance for monitoring 220 terrestrial mammals in biodiversity rich ecosystems. Here we compile the largest dataset of inventories of terrestrial mammal communities for the Neotropical region based on camera trapping studies. The dataset comprises 170 surveys of medium to large terrestrial mammals using camera traps conducted in 144 areas by 74 studies, covering six vegetation types of tropical and subtropical Atlantic Forest of South America (Brazil and Argentina), and present 225 data on species composition and richness. The complete dataset comprises 53,438 independent records of 83 species of mammals, includes 10 species of marsupials, 15 rodents, 20 carnivores, 8 ungulates and 6 armadillos. Species richness averaged 13 species (± 6.07 SD) per site. Only six species occurred in more than 50% of the sites: the domestic dog Canis familiaris, crab-eating fox Cerdocyon thous, tayra Eira barbara, south American coati Nasua nasua, crab-eating raccoon 230 Procyon cancrivorus and the nine-banded armadillo Dasypus novemcinctus. The information contained in this dataset can be used to understand macroecological patterns of biodiversity, community, and population structure, but also to evaluate the ecological consequences of fragmentation, defaunation, and trophic interactions. D. Key words: Atlantic Forest, forest fragmentation, camera traps, neotropical mammals, 235 biodiversity hotspot, mammal communities, invasive species E. Description: The dataset combines 53,438 independent records of 83 species of medium to large terrestrial mammals from 170 surveys using camera traps conducted in 144 areas by 74 studies. We used data exclusively from camera trap surveys as they are ideal to record communities of terrestrial mammals, not selecting a specific group and photographing most 240 species that cross in front of them. For this reason, it is considered the most reliable tool to register the occurrence and ecology of medium to large terrestrial mammals in tropical forests (Tobler et al. 2008a). In addition, it reduces our bias of detecting or missing species when compared with human direct surveys, such as line transect census and track surveys (Silveira et al. 2003). The dataset is restricted to the Atlantic Forest hotspot (Fig. 1). 245 For the general data analysis, we considered only species that are well detected in camera traps and excluded records considered opportunistic (such as bats, primates, and small mammals). However, we kept the full records of all mammalian species in the database. Specifically, we only evaluated 47 species, from 36 genera, 17 families and 8 orders – hereafter, filtered dataset (Fig. 2). The full dataset has 10 orders, 28 families, 58 genera, and 83 species, of which 10% are 250 classified as Vulnerable (VU) by IUCN, 61% are Least Concern (LC), 2% are Critically Endangered (CR), and 5% are invasive. Both species with CR status are primates (the muriqui Brachyteles hypoxanthus, and the buff-headed capuchin Sapajus xanthosternos). From the filtered dataset, seven species are classified as Vulnerable (Brazilian dwarf brocket Mazama nana, white-lipped peccary Tayassu pecari, southern tiger cat Leopardus guttulus, giant armadillo Priodontes 255 maximus, lowland tapir Tapirus terrestris, giant anteater Myrmecophaga tridactyla, bristle- spined rat Chaetomys subspinosus) and five are Near Threatened (maned wolf Chrysocyon brachyurus, bush dog Speothos venaticus, margay Leopardus wiedii, jaguar Panthera onca and the neotropical otter Lontra longicaudis) (Fig. 3). The most frequent species were the nine-banded armadillo Dasypus novemcinctus, the south 260 Page 8 of 35Ecology For Review O nly 7 American coati Nasua nasua, and the crab-eating fox Cerdocyon thous, occurring in 79, 69, and 58% of all sites, respectively (Fig. 3). Species richness averaged 13 species (± 6.07 SD) per site (Fig. 4). Five species occurred in more than 50% of the sites: the domestic dog Canis familiaris, crab-eating fox Cerdocyon thous, tayra Eira barbara, south American coati Nasua nasua, crab- eating raccoon Procyon cancrivorus, and the nine-banded armadillo Dasypus novemcinctus (Fig. 265 3). From the full dataset, in the 144 sites, we had 16 species as singletons (i.e. species recorded in only one site). However, in our filtered dataset we had just two singletons: southern naked- tailed armadillo Cabassous unicinctus and giant armadillo Priodontes maximus (Fig. 3). From all the records, the most frequent species was the Brazilian common opossum Didelphis aurita with 1,283 records in a single site. This species alone is represented 10% of overall survey records 270 (2,637 of 25,535), only considering studies that use a minimum one hour interval among records of the same species to allow comparison (N = 71). Among invasive species, the domestic dog was recorded in 56% of the sites and wild boars (Sus scrofa) in 16%. Survey site altitude varied from sea level to 2,791 m (Parque Nacional do Itatiaia) and 67% were conducted in protected areas, adequately representing the broad altitudinal variation of Atlantic 275 forests. On average the surveys used 12 (±12.76 SD) camera traps. As many studies reported that they moved camera traps during the same survey, the average number of sampling points was 16 (±20.77 SD). Distance between sampling stations varied from 100 to 7,192 m. Sampling effort per time, or trap/days, given by the number of survey days multiplied by the number of sampling points, is one of the main factors determining survey success and the number of 280 recorded species (Srbek-Araujo and Chiarello 2007, Tobler et al. 2008a). This pattern was also detected in our dataset, as species richness showed to be correlated to sampling effort (adjusted R2= 0.51, slope=8.18 ±0.66 SE, df=142, p<0.001, Fig. 5). The average effort among studies was 1,185 trap/days (min 40 – max 9,078). The median effort (450 trap/days) is considered adequate to obtain records from the most common species, while a minimum of 900 trap/days would be 285 needed to detected local species efficiently (Tobler et al. 2008b, Si et al. 2014). Some species can spend several minutes in front of a sampling station and trigger the sensor several times. The same individuals of a given species can also cross at the same sampling station many times in a short period. Also, species that present social behavior such as peccaries and coatis may highly increase the total number of records. To minimize these sources of bias, 290 researchers establish a time interval among consecutive records to determine independence. Most surveys reported one hour minimum interval (42%), while 41 (24%) considered a 24-hour interval as an independent record. Other criteria were: 30 min (7%), 5 min (2%), and 30 seconds (1%). The remaining 24% of studies did not describe any criteria or reported only the total number of records. Only 18% reported having used any kind of baiting to increase detection 295 probability. In Brazil, most surveys were carried out in São Paulo state (27%) followed by Santa Catarina (21%) and Minas Gerais (18%) states. In Argentina, the surveys are concentrated in Misiones province, the southwestern limit of the Atlantic Forest. Several surveys from this region are raw data from a long term participatory network for carnivore monitoring promoted by Argentine 300 researchers (De Angelo et al. 2011). No surveys in the Atlantic Forest of Paraguay were found during our data compilation process. Page 9 of 35 Ecology For Review O nly 8 CLASS II. RESEARCH ORIGIN DESCRIPTORS A. Overall project description 305 Identity: A database integrating information medium to large terrestrial mammals from camera trap studies in the Atlantic Forest hotspot. Period of study: Raw data range from 1999-2017. Objectives: Our main goals in compiling this dataset were: (1) to summarize information on camera trap inventories conducted in the Atlantic Forest hotspot, (2) to make available data 310 restricted to research groups and/or usually available only to Portuguese and Spanish speakers, and (3) to describe the major patterns in the studies and identify gaps of knowledge and information to guide future sampling and conservation efforts. This dataset follows the ATLANTIC biodiversity series, an effort to compile biodiversity information for the Atlantic Forest (e.g. Bovendorp et al. in press., Bello et al. 2017). 315 Abstract: Same as above. Sources of funding: MLLP, SMCC, ACM and EVM studies were funded by Panthera Foundation and Instituto Pró-Carnívoros. CAR studies were funded by the Tropical Forest Conservation Act – TFCA/FUNBIO. RFC and CRB studies were funded by Fundação Grupo Boticário de Proteção à Natureza; AGC, AMOP, RLM and APP were supported by CNPq, CAPES and FAPEMIG. CRB were 320 granted with CNPq Scholarships, also ALR (153423/2016-1); AP, CA, PC and VQ studies were supported by CONICET, WWF, Fundación Vida Silvestre Argentina, The Rufford Foundation and WCS. MX were supported by Belmont Hotel. MB studies were funded by CONICET, Argentina (PIP nº 112 201101 00616); UCAR, Ministerio de Agroindustria, Argentina - PIA 10102/ 2011; Agencia Nacional de Promoción Científica y Tecnológica, Ministerio de Ciencia Tecnología e 325 Innovación Tecnológica, Argentina - PICT 2013 nº 1904. LS, FFK, AVN and GML surveys were funded by Conservation International, TEAM Network, Gordon and Betty Moore Foundation and Instituto Estadual de Florestas-MG. AVN were associated with Museu de Zoologia João Moojen. PCE, FLR, MDGB and ACFA were funded by Rufford Foundation (Project 20950-1), Idea Wild, Rede BioM.A. Inventários (PPBIO Mata Atlântica/CNPq proc.: 457524/2012-0). MCR, MG, GB 330 were funded by São Paulo Research Foundation FAPESP (Proc 2013/50421-2; 2014/01986-0; 2014/23095-0), as was RLM (Proc 2015/17739-4). FL and LC studies were funded by Fundação Grupo Boticário de Proteção à Natureza, The Scott Neotropical Fund of the Lincoln Park Zoological Society, The Species Survival Fund from Wildlife Trust, IdeaWild Grant Program, WWF/US, WWF-EFN Scholarship Program, DICE Small Grant Program, The Liz Claiborne Art 335 Ortenberg Foundation, The Ashoka Foundation, Conservation, Food and Health Foundation, 100% Fund from Fauna and Flora International, The Woodland Park Zoo, The Whitley Awards, The Rolex Awards, Durrell Wildlife Conservation Trust, The Rufford Small Grants Program and Ridgeway Trust. Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) provided support during ACFA MSc., LC, MGB and FL PhD, and FLR PNPD fellowship. LC, FL, and 340 MLLP received financial support from 2012 – 2015 for data management, curation and analysis from Fundo Brasileiro para a Biodiversidade – Tropical Forest Conservation Act agreement (FUNBio/TFCA). AGC, MG and MCR receive a research fellowship from CNPq. MEG studies were funded by Conservação Internacional do Brasil, CNPq and Ministério da Ciência, Tecnologia e Inovação (MCTI). The funders above had no role in the study design, data collection and analysis, 345 decision to publish, or preparation of the manuscript. Page 10 of 35Ecology For Review O nly 9 Site description: Originally, the Atlantic Forest comprised a continuous forest of 150 million ha of evergreen and seasonally-dry forests ranging across a latitudinal gradient of over 3,300 km of the Brazilian Atlantic coast, with extensions in Paraguay and Argentina (Galindo-Leal and Câmara 2003, Tabarelli et al. 2010). The Atlantic Forest is divided into eight biogeographic sub regions, 350 based on endemic species distribution, varying in altitude from sea level to 2,700 m above sea level and annual precipitation up to 4,000 mm/year (Câmara 2003, Silva and Casteleti 2003, Ribeiro et al. 2009). The Atl