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Fabrizio Marcondes Machado UNIVERSIDADE ESTADUAL DE CAMPINAS INSTITUTO DE BIOLOGIA FABRIZIO MARCONDES MACHADO DESVENDANDO A DIVERSIDADE DOS ANOMALODESMATA (MOLLUSCA: BIVALVIA): UMA ABORDAGEM MORFOLÓGICA E FILOGENÉTICA UNRAVELLING THE DIVERSITY OF ANOMALODESMATA (MOLLUSCA: BIVALVIA): A MORPHOLOGICAL AND PHYLOGENETIC APPROACH Campinas 2018 FABRIZIO MARCONDES MACHADO DESVENDANDO A DIVERSIDADE DOS ANOMALODESMATA (MOLLUSCA: BIVALVIA): UMA ABORDAGEM MORFOLÓGICA E FILOGENÉTICA UNRAVELLING THE DIVERSITY OF ANOMALODESMATA (MOLLUSCA: BIVALVIA): A MORPHOLOGICAL AND PHYLOGENETIC APPROACH Tese apresentada ao Instituto de Biologia da Universidade Estadual de Campinas como parte dos requisitos exigidos para a obtenção do título de Doutor em Biologia Animal na área de Biodiversidade Animal. Thesis presented to the Institute of Biology of the University of Campinas in partial fulfillment of the requirements for the degree of PhD in Animal Biology in the area of Animal Biodiversity. ESTE ARQUIVO DIGITAL CORRESPONDE À VERSÃO FINAL DA TESE DEFENDIDA PELO ALUNO FABRIZIO MARCONDES MACHADO E ORIENTADO PELO PROF. DR. FLÁVIO DIAS PASSOS. Orientador: Prof. Dr. Flávio Dias Passos Campinas 2018 Agência(s) de fomento e nº(s) de processo(s): CAPES ORCID: https://orcid.org/0000-0002-5085-865X Ficha catalográfica Universidade Estadual de Campinas Biblioteca do Instituto de Biologia Mara Janaina de Oliveira - CRB 8/6972 Machado, Fabrizio Marcondes, 1984- M18d Desvendando a diversidade dos Anomalodesmata (Mollusca: Bivalvia) : uma abordagem morfológica e filogenética / Fabrizio Marcondes Machado. – Campinas, SP : [s.n.], 2018. Orientador: Flávio Dias Passos. Tese (doutorado) – Universidade Estadual de Campinas, Instituto de Biologia. 1. Bivalve. 2. Microtomografia por raio-X. 3. Filogenia. 4. Anatomia. 5. Molusco. I. Passos, Flávio Dias, 1971-. II. Universidade Estadual de Campinas. Instituto de Biologia. III. Título. Informações para Biblioteca Digital Título em outro idioma: Unravelling the diversity of Anomalodesmata (Mollusca: Bivalvia) : a morphological and phylogenetic approach Palavras-chave em inglês: Bivalves X-ray microtomography Phylogeny Anatomy Mollusks Área de concentração: Biodiversidade Animal Titulação: Doutor em Biologia Animal Banca examinadora: Flávio Dias Passos [Orientador] Antonia Cecília Zacagnini Amaral Eliane Pintor Arruda Cléo Dilnei de Castro Oliveira André Rinaldo Senna Garraffoni Data de defesa: 16-01-2018 Programa de Pós-Graduação: Biologia Animal Campinas, 16 de janeiro de 2018. COMISSÃO EXAMINADORA Prof. Dr. Flávio Dias Passos (orientador) Profa. Dra. Antonia Cecília Zacagnini Amaral Profa. Dra. Eliane Pintor de Arruda Prof. Dr. Cléo Dilnei de Castro Oliveira Prof. Dr. André Rinaldo Senna Garraffoni Os membros da Comissão Examinadora acima assinaram a Ata de Defesa, que se encontra no processo de vida acadêmica do aluno. DEDICATÓRIA “Everybody is a genius. But if you judge a fish by its ability to climb a tree, it will live its whole life believing that it is stupid". (Albert Einstein) “-Lembre-se meu filho, somos dois contra o mundo” (Minha mãe) AGRADECIMENTOS Ao orientador e amigo, Prof. Dr. Flávio Dias Passos, pela confiança e ensinamentos ao longo de todos esses anos e por ter sido um exemplo de humildade, inteligência e paciência. Ao amigo e colaborador, Prof. Dr. Brian Morton por ser fonte constante de conhecimento e exemplo de vivacidade e amor a profissão. À CAPES, pela concessão das bolsas de doutorado e doutorado sanduíche durante o decorrer dessa pesquisa. Ao Projeto temático BIOTA/FAPESP-Araçá, pelo apoio logístico e pelo financiamento durante minhas coletas. À Profa. Dra. Cecília Amaral (DBA-UNICAMP) por diversas vezes ter me ‘adotado’ como um de seus alunos e também por ter me incluído no Projeto BIOTA/FAPESP-Araçá. Ao CEBIMar-USP, pelo apoio logístico. Em especial ao Prof. Dr. Álvaro Esteves Migotto e Prof. Dr. Maicon Di Domenico pela ajuda durante as filmagens da espécie Cardiomya cleryana. Ao LNNano – Brazilian Nanotechnology National Laboratory, pelo uso do microtomógrafo. Em especial as funcionárias Rubia e Bruna pela ajuda durante o manuseio do equipamento e pelas dicas sobre reconstruções tridimensionais. À PETROBRAS SA/ CENPES pelo Projeto HABITATS e pela concessão de alguns espécimes estudados nessa Tese. Ao Instituto de Biologia e ao Departamento de Biologia Animal, pela utilização da infraestrutura. Aos membros do grupo de Malacologia da Unicamp, Dra. Gisele Introíni, Dra. Lenita Tallarico, MSs. Ariane Campos e Dra. Shirley Maria Recco Pimentel pela frutífera colaboração durante todos esses anos. Em especial as amigas e sempre incentivadoras do meu trabalho, Dra. Gisele Introíni e Dra. Lenita Tallarico, obrigado por tudo. A todos os amigos da Ecologia e Biologia Animal pelas risadas, em especial aos amigos, Msc. Pedro Ribeiro Piffer, Msc. Nathalia Padovani, Msc. Rachel Furioso, Msc. Renata Allito, Msc. Talita Foroni, Msc. Hélio Checon, Dr. Guilherme Corte e Dra. Ana Cristina (Tina) por terem muitas vezes transformado momentos tristes em alegres. À Dra. Michela Borges, curadora do Museu de Zoologia da Unicamp, pelo profissionalismo, amizade e também pela ajuda com o tombamento e envio de materiais de pesquisa ao exterior. À Profa. Fosca Pedini Leite e a todos os seus alunos pelo companheirismo em especial as amigas Msc. Ana Paula, Msc. Karine e Dra. Silvana. Aos professores e amigos Dr. Paulo Oliveira (Paulinho) e Dr. André Freitas (Baku), por toda a sabedoria transmitida durante nossas conversas. Ao Prof. Dr. André Garrafoni pela excelente disciplina sobre sistemática filogenética e pela ajuda na codificação de alguns caracteres que compõem o segundo capítulo dessa Tese. Ao Prof. Dr. Paulo Sumida, Instituto Oceanográfico da USP, e também aos seus alunos Bruno e Maurício pelos ensinamentos sobre biologia molecular. As biólogas Adriane Sporgis e Stella Ferraz, pelo auxílio e extrema habilidade no manuseio do Microscópio Eletrônico de Varredura. A todos os companheiros de laboratório: MSc. Paulo Correa (Aplacophora), Msc. Pedro Longo (Gastropoda), MSc. Marcel Sabino, MSc. Amanda Fantinatti (Little) e aos alunos de iniciação científica, Ana Clara e Allan. Agradeço imensamente ao Prof. Dr. José Paulo L. Guadanucci por ter compartilhado comigo um pouco do seu vasto conhecimento sobre sistemática filogenética. Ao Prof. Dr. Gonzalo Giribet pela excelente orientação durante o Doutorado Sanduíche na Universidade de Harvard. A todos os amigos do Giribet Lab - Harvard University, Tauana Cunha, Ligia Benavides, Caitlin Baker, Kate Sheridan, Vanessa González, Shoyu Saito, Julia Cosgrove e ao Prof. Dr. Robert M. Woollacott (Bob), o meu muito obrigado. Ao curador do Museum of Comparative Zoology – Harvard University, Dr. Adam Baldinger (captain) ao incrível funcionário Murat Recevik, e a todos os membros da equipe, muito obrigado pela ajuda. À Profa. Dra. Elena Krylova, do P.P Shirshov Institute of Oceanology of Russian Academy of Sciences, por ter gentilmente traduzido alguns de seus trabalhos para o Inglês. Ao Dr. José H. Leal, curador do Bailey - Matthews National Shell Museum- USA por ter fornecido algumas imagens da espécie Dillema frumarkenorum. À Dra. Andréia Salvador e ao fotógrafo K. Webb, ambos do Natural History Museum- UK, por fornecerem algumas fotos da espécie Clistoconcha insignis. Ao Dr. Guido Pastorino, do Museu Argentino de Ciencias Naturales, por fornecer um raro exemplar da espécie Allograma formosa. Aos Drs. H. Takuma and Dr H. Saito do Museu Nacional do Japão pelas fotos das espécies Halicardia nipponensis and Bentholyonsia teramachii. Aos amigos e roommates que fizeram minha estada em Boston ser inesquecível, MSc. Sidney Alcantara, Toninho (Trator), Mari, Talita, MSc. Luciana Tavares, Eduardo Café, Salomon Bandeira, Marcelo Oliveira e Dona Silvia (chaveirinho). A toda minha família pelo carinho, confiança e apoio incondicional. Em especial as tias Eliana, Madalena e Nirde por estarem sempre ao meu lado. Aos queridos sobrinhos Alexandra, Manoel, Tiago, Fernanda, Felipe, Stephanie e aos irmãos Xandinho, Sérgio e Marjorie, obrigado pelo carinho. Aos meus sogros Dona Nina e Seu Antônio e a querida amiga Cristina pelo carinho e orações durante esse doutorado. Aos queridos primos Walter Gratti e Gabriel Lago Ao irmão e primo Marcelo Cardillo pela amizade eterna. À minha linda Luana, obrigado por fazer parte da minha vida. À minha querida mãezinha, Elizete, pelo amor incondicional e por ser um exemplo de integridade, coragem, fé e honestidade. RESUMO Considerado um grupo monofilético, os Anomalodesmata Dall, 1889 possuem atualmente mais de 800 espécies, abrigando alguns dos bivalves marinhos mais raros, bizarros e especializados. Essa raridade aliada a uma carência de informações anatômicas detalhadas sobre suas espécies sempre foram obstáculos para a compreensão de suas relações internas, consequentemente, resultando também em uma baixa representatividade de táxons em reconstruções filogenéticas. Com o intuito de preencher algumas das principais lacunas no conhecimento dos Anomalodesmata, a presente Tese propôs três objetivos específicos, buscando, através de diferentes ferramentas, ampliar, atualizar e apresentar novas idéias ao conhecimento evolutivo, morfológico e taxonômico desse importante grupo de bivalves. O primeiro objetivo se deu por meio de coletas realizadas na Baía do Araçá, litoral Norte do Estado de São Paulo, onde foi possível observar e descrever em detalhes a morfologia funcional e o comportamento de Cardiomya cleryana, trazendo novos insights sobre os bivalves carnívoros como um todo. O segundo objetivo
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