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Universidade Estadual De Campinas Instituto De Biologia Mariane Ueda Vaz Ronque Ecology, Behavior and Microbiology of Fungus-Far

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Universidade Estadual De Campinas Instituto De Biologia Mariane Ueda Vaz Ronque Ecology, Behavior and Microbiology of Fungus-Far UNIVERSIDADE ESTADUAL DE CAMPINAS INSTITUTO DE BIOLOGIA MARIANE UEDA VAZ RONQUE ECOLOGY, BEHAVIOR AND MICROBIOLOGY OF FUNGUS-FARMING ANTS (FORMICIDAE, MYRMICINAE, ATTINI, ATTINA) IN ATLANTIC RAINFOREST ECOLOGIA, COMPORTAMENTO E MICROBIOLOGIA DE FORMIGAS CULTIVADORAS DE FUNGO (FORMICIDAE, MYRMICINAE, ATTINI, ATTINA) NA MATA ATLÂNTICA CAMPINAS 2018 MARIANE UEDA VAZ RONQUE ECOLOGY, BEHAVIOR AND MICROBIOLOGY OF FUNGUS- FARMING ANTS (FORMICIDAE, MYRMICINAE, ATTINI, ATTINA) IN ATLANTIC RAINFOREST ECOLOGIA, COMPORTAMENTO E MICROBIOLOGIA DE FORMIGAS CULTIVADORAS DE FUNGO (FORMICIDAE, MYRMICINAE, ATTINI, ATTINA) NA MATA ATLÂNTICA Thesis presented to the Institute of Biology of the University of Campinas in partial fulfillment of the requirements for the degree of Doctor in Ecology. Tese apresentada ao Instituto de Biologia da Universidade Estadual de Campinas como parte dos requisitos exigidos para a obtenção do título de Doutora em Ecologia. ESTE ARQUIVO DIGITAL CORRESPONDE À VERSÃO FINAL DA TESE DEFENDIDA PELA ALUNA MARIANE UEDA VAZ RONQUE E ORIENTADA PELO PROF. DR. PAULO SÉRGIO MOREIRA CARVALHO DE OLIVEIRA. Orientador: PAULO SÉRGIO MOREIRA CARVALHO DE OLIVEIRA Co-orientadores: MAURÍCIO BACCI JÚNIOR MARIANA LÚCIO LYRA CAMPINAS 2018 Campinas, 27 de julho de 2017. COMISSÃO EXAMINADORA Prof. Dr. Paulo Sérgio Moreira Carvalho de Oliveira Prof. Dr. Alexander Vicente Christianini Prof. Dr. Fernando Barbosa Noll Prof. Dra. Maria Santina de Castro Morini Prof. Dr. Rodrigo dos Santos Machado Feitosa Os membros da Comissão Examinadora acima assinaram a Ata de Defesa que se encontra no processo de vida acadêmica da aluna. Com todo meu amor e gratidão dedico essa tese de doutorado aos meus pais Enio e Denise. E ao meu companheiro de vida Gustavo. Ofereço em especial essa tese aos meus avós: Alice, Dayzo, Edson & Rosa (que deixa muitas saudades). AGRADECIMENTOS Ao meu Deus, que guia meus passos e me dá força para seguir meus objetivos. Aos meus pais Enio e Denise agradeço por todo amor e dedicação de uma vida inteira. Agradeço o constante apoio e ajuda nessa minha caminhada, que me fizeram chegar até aqui. Ao meu companheiro de vida, Gustavo, agradeço pelo amor, carinho, amizade e paciência nos meus momentos difíceis. Agradeço a colaboração e imensurável apoio nessa tese: por toda ajuda em campo, por pensar junto comigo em como fazer esse trabalho melhor, pelas inúmeras discussões científicas e por toda ajuda com a estatística. Que a nossa parceria (pessoal e profissional) siga por toda nossa vida! E que venham as novas etapas e desafios... Agradeço toda a minha família, por sempre estarem torcendo pelo meu sucesso. Em especial agradeço aos meus avós (Alice, Dayzo, Edson e Rosa) e meu tio Dani, por todo amor, carinho e orações. Aos meus sogros Maria e Antônio, por toda ajuda. Agradeço meu orientador Paulo S. Oliveira por toda a dedicação e amizade ao longo desses anos. Agradeço ao Paulo por sempre estar disponível, por partilhar seu conhecimento científico que me ajudou na realização desse projeto, pela confiança depositada no meu trabalho, por todos os ensinamentos que me ajudaram na minha formação profissional e pessoal. Agradeço meus co-orientadores Maurício Bacci Jr. e Mariana Lyra por fazerem possível uma grande parte desse projeto. Agradeço ao Maurício por toda a disponibilidade, discussões científicas e acreditar no potencial do projeto. Agradeço à Mariana por aceitar a me ajudar, por todos os ensinamentos sobre genética, por toda a paciência e disponibilidade, pelas inúmeras discussões científicas, por acreditar e se entusiasmar com o meu projeto e pela amizade construída ao longo desse tempo de convivência. Agradeço o Prof. Dr. Rodrigo Feitosa pela colaboração nesse trabalho e a Ana Ješovnik pela identificação das formigas Sericomyrmex. Agradeço todos os membros da pré-banca e banca (Prof. Dr. Alexander Christianini, Prof. Dr. Fernando Noll, Prof. Dra. Maria Santina Morini e Prof. Dr. Rodrigo Feitosa) pelas valiosas considerações e sugestões nesse trabalho, que contribuíram muito para a versão final dessa tese e também para os artigos. Agradeço também a Dra. Paula Omena pelas sugestões que irão contribuir muito para os artigos. Sou grata aos meus amigos do Laboratório de Ecologia e Comportamento de Formigas que estiveram junto comigo durante esse doutorado: Nádia, Hélio, Aninha, Mary, Felipe, André, Javier, Sebastian, Verônica, Luísa, Luis. Agradeço principalmente as conversas descontraídas, os inúmeros cafés para relaxar e também as discussões científicas. Em especial agradeço: à Nádia pela amizade sincera ao longo desses anos e que vou levar por toda minha vida! À Aninha por sempre estar disponível em me ajudar, por cuidar com tanta dedicação das minhas colônias e pela oportunidade de colaborar no seu projeto de mestrado, me ajudando a crescer profissionalmente e pessoalmente. Ao André pela ajuda no campo e com tudo que precisei no laboratório. Agradeço aos amigos Paula Omena e Tiago Bernabé pela boa amizade e os momentos de descontração nos cafés. A amiga Fernanda Vasconcellos pela companhia nos 3 anos em que moramos juntas. E também as amigas-irmãs que a vida me trouxe: Isis, Gabi, Carol, Dani e Carla, que mesmo longe estão sempre torcendo pelo meu sucesso. Em especial ofereço essa tese a minha amiga-irmã Isis: que adorava ouvir as histórias das formigas, que me mandava fotos de insetos “diferentes” da fazenda e que torceu e esperou tanto por esse momento da minha defesa... Esteja onde estiver, receba essa minha pequena homenagem! Agradeço à Universidade Estadual de Campinas (UNICAMP) pelo ensino de qualidade e gratuito. Aos professores e funcionários do Programa de Pós-graduação em Ecologia e Departamento de Biologia Animal. Agradeço a CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) pela concessão da bolsa de doutorado. Ao Instituto Florestal de São Paulo e Parque Estadual Serra do Mar (Núcleo Picinguaba) pela autorização para conduzir este trabalho. Agradeço a Eliane Rodrigues por permitir parte deste trabalho na Pousada Betânia. MUITO OBRIGADA A TODOS! RESUMO Formigas cultivadoras de fungo (Formicidae, Myrmicinae, Attini, Attina) representam um exemplo de mutualismo: as formigas cultivam no interior de seus ninhos um fungo simbionte para obtenção de recursos nutricionais para a colônia e, em troca fornecem ao fungo nutrição, dispersão e proteção contra parasitas e competidores. Adicionalmente, essas formigas apresentam interações com microrganismos que podem afetar o mutualismo formiga-fungo. Através de uma abordagem multidisciplinar, esse trabalho teve como objetivo principal estudar a história natural, comportamento e a comunidade bacteriana associada a cinco espécies de formigas cultivadoras de fungo da Mata Atlântica: Mycocepurus smithii, Mycetarotes parallelus, Mycetophylax morschi, Sericomyrmex parvulus e Sericomyrmex saussurei. Essas formigas apresentam ninhos no solo, com poucas câmaras e não muito profundas. Em geral, o ritmo diário de atividade dessas espécies é diurno. As operárias coletam principalmente fezes de artrópodes e material vegetal para cultivar o fungo simbionte. Em campo, foi registrado pela primeira vez para as formigas atíneas o comportamento de cleptobiose, no qual Mycetarotes parallelus rouba itens (fezes de artrópodes) para a fungicultura diretamente das mandíbulas de operárias de Mycetophylax morschi, quando estas retornam ao ninho. Esse comportamento pode ser considerado uma forma de competição por interferência, com custos para Mycetophylax morschi e benefícios para Mycetarotes parallelus. No capítulo de comunidade de bactérias associadas às atíneas estudadas observamos que a composição das comunidades bacterianas foi diferente entre as espécies, indicando provavelmente um efeito do hospedeiro nessas comunidades. Houve também diferenças na composição das comunidades bacterianas entre ninhos de uma mesma espécie, mostrando que a comunidade bacteriana associada pode ser ninho-específico. Esses resultados evidenciam uma variação intra e interespecífica nas comunidades bacterianas dessas espécies. Finalmente, observações com colônias cativas revelaram que comportamentos relacionados ao “cuidado do fungo”, “autolimpeza”, “locomoção” e “inatividade” foram os mais praticados por essas formigas no interior do ninho. Além disso, as categorias comportamentais relacionadas ao “cuidado do fungo”, “interação entre operárias”, “cuidado com a prole” e “interações com operárias mortas” influenciaram na composição da comunidade bacteriana das atíneas estudadas. Esse resultado indica que a comunidade bacteriana associada às formigas cultivadoras de fungo pode ser mediada por comportamentos desempenhados no interior da colônia. Esse trabalho reúne informações sobre vários aspectos biológicos (história natural, ecologia, comportamento e interação com microrganismos) das formigas atíneas. Numa perspectiva mais ampla, esse trabalho contribui para um melhor entendimento da relação simbiótica multitrófica que essas formigas participam, fornecendo também importantes informações de campo sobre o papel ecológico destas formigas em Mata Atlântica. ABSTRACT Fungus-farming ants (Formicidae, Myrmicinae, Attini, Attina) represent an example of mutualism: the ants cultivate inside their nests a symbiont fungus to obtain nutritional resources for the colony and in return the ants provide the fungus with nourishment, dispersal, and protection against parasites and competitors. Additionally, these ants have interaction with microorganisms, which may affect the ant-fungus mutualism. Using a multidisciplinary
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