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Universidade Federal Do Rio De Janeiro BÁSLAVI MARISBEL CÓNDOR LUJÁN BIODIVERSITY and CONNECTIVITY of CALCAREOUS SPONGES

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Universidade Federal Do Rio De Janeiro BÁSLAVI MARISBEL CÓNDOR LUJÁN BIODIVERSITY and CONNECTIVITY of CALCAREOUS SPONGES Universidade Federal do Rio de Janeiro BÁSLAVI MARISBEL CÓNDOR LUJÁN BIODIVERSITY AND CONNECTIVITY OF CALCAREOUS SPONGES (PORIFERA: CALCAREA) IN THE WESTERN TROPICAL ATLANTIC Rio de Janeiro 2017 ii Biodiversity and Connectivity of calcareous sponges (Porifera: Calcarea) in the Western Tropical Atlantic Báslavi Marisbel Cóndor Luján Tese apresentada ao Programa de Pós-Graduação em Biodiversidade e Biologia Evolutiva, Instituto de Biologia, Universidade Federal do Rio de Janeiro, como parte dos requisitos necessários à obtenção do título de Doutor em Ciências Biológicas. Orientadora: Dra. Michelle Klautau Rio de Janeiro Fevereiro/2017 iii Biodiversity and Connectivity of calcareous sponges (Porifera: Calcarea) in the Western Tropical Atlantic Báslavi Marisbel Cóndor Luján Orientadora: Dra. Michelle Klautau Banca examinadora: Prof. Dra. Carla Zilberberg, IB/UFRJ ______________________________________________ Prof. Dr. Cristiano Valentim da Silva Lazoski, IB/UFRJ _______________________________________________ Prof. Dr. Eduardo Carlos Meduna Hajdu, MN/UFRJ _______________________________________________ Prof. Dr. Guilherme Ramos da Silva Muricy, MN/UFRJ _______________________________________________ Prof. Dr. Marcelo Weksler, MN/UFRJ _______________________________________________ Dr. Fernando Moraes, JBRJ (Suplente) _______________________________________________ Prof. Dr. Paulo Cesar de Paiva, IB/UFRJ (Suplente) _______________________________________________ Rio de Janeiro Fevereiro/2017 iv Trabalho realizado no Laboratório de Biologia de Porifera (LaBiPor) Departamento de Zoologia, Instituto de Biologia Universidade Federal do Rio de Janeiro – UFRJ Orientadora: Profa. Dra. Michelle Klautau Capa: Centro: Rede filogeográfica de Leucetta floridana (modificada). Sentido horário: Leucetta floridana, Leucilla uter, Leucascus luteoatlanticus sp. nov., Ascandra torquata sp. nov., Sycon conulosum sp. nov., Nicola tetela, triactina âncora de Amphoriscus hirstutus sp. nov., triactina atrial de Grantessa tumida sp. nov., esqueleto de Leucandrilla pseudosagittata sp. nov., esqueleto de Ernstia citrea. Créditos: A. Padua, E. Hajdu, F. Azevedo e T. Pérez. v Ficha catalográfica CÓNDOR LUJÁN, Báslavi Marisbel Biodiversity and Connectivity of calcareous sponges (Porifera: Calcarea) in the Western Tropical Atlantic / Báslavi Marisbel Cóndor Luján. Rio de Janeiro: UFRJ, IB, 2017. xiii, 259f. il; 29.7 (cm) Orientador: Michelle Klautau. Tese (Doutorado). UFRJ/IB/Programa de Pós-graduação em Biodiversidade e Biologia Evolutiva, 2017. Referências bibliográficas: 236-256f. 1. Esponjas Calcareas. 2. Mar do Caribe. 3. Costa do Brasil. 4. Conectividade genética. I. Klautau, Michelle. II. Universidade Federal do Rio de Janeiro, Instituto de Biologia, Programa de Pós-graduação em Biodiversidade e Biologia Evolutiva. III. Tese. vi Dedico esta tesis a mis queridos padres quienes, estando lejos, están siempre a mi lado. vii Huk llactapi maypi llapan maskhay runakuna mamaqocha hatun yachaypi, Llapan maskhay runakuna ruanku anchoveta challway, ñoqa huk punchay ruwayramuni qochayuyo sasa llachayta, soqta huata llanqay tukukuy manan llakikamunichu (In Quechua by E. Pezo Zegarra) Translation: In a country where almost all marine science is focused on the fishery of Engraulins ringens (Peruvian anchoveta), I took the risky decision to study sponges. After six carioca years, I do not regret. viii AGRADECIMENTOS Esta tesis es el resultado de un maravilloso viaje a través de las primeras descripciones de las esponjas del Mar del Caribe y del Brasil, colectas en lugares en los que nunca imaginé bucear, interesantes diálogos con especialistas en Porifera y muchas horas dedicadas al microscopio, a la amplificación de secuencias de ADN y a las simulaciones bayesianas. Todo esto sólo fue posible gracias a la colaboración, apoyo e incentivo de muchísimas personas e instituciones. Muchas gracias a todos y en especial a: A minha orientadora Michelle Klautau por ter aceito a minha proposta de doutorado e ter me mostrado o caminho para ser uma boa pesquisadora. Aos membros do projeto MARRIO, em especial ao Eduardo Hajdu e ao Thierry Pérez por terem organisado as maravilhosas expedições que geraram os resultados apresentados nesta tese. Aos membros do LaBiPor, Andrézinho, Bernardo, Bárbara, Gabi, Fernanda, Mattheus, Tayara, Taynara, Pedro e Raissa pela boa disposição para trabalhar em équipe e me auxiliar com os pedidos de último momento pelo whatsapp (rsrs). Às meninas que alguma vez fizeram parte do LabiPor, a Carol e Malena pelo trabalho de bancada e a Natalia e Vivi pela agradável companhia. Aos pesquisadores (alemḿ do LaBiPor) que dedicaram um tempo durante os mergulhos para procurar e coletar Calcarea: A. Bispo, A. Ereskovsky, B. Thacker, C. Leal, C. Ruiz, C. Castello- Branco, C. Diaz, G. Lôbo-Hajdu, H. Fortunato, J. García-Hernández, J. Vacelet, J. Carraro, L. Van Bostal, M. Carvalho, O. Thomas, P. Chevaldonné, S. Chenesseau, S. Zea and S. Salani. Aos pesquisadores espongólogos brasileiros e estrangeiros que conheci ao longo destes anos (Simpósio de Porifera na Bahia, “La Martinique” Sponge Course, Pacotilles Expedition, MARRIO Workshops). Todos eles, certamente, contribuiram na minha formação como pesquisadora. ix Aos profesores do Museu Nacional e do Instituto de Biologia. Um especial “gracias” à Ghennie Rodriguez pela orientação nas ańalises demográficas da Leucetta floridana. Às agencias de fomento CAPES, CNPQ, CNRS, COFECUB, FAPERJ e Grupo Boticário de Proteção à Natureza pelo financiamento das expedicçõs de coleta e os projetos do laboratório. Ao programa PEC-PG e à CAPES pela concessão da bolsa de doutorado. A mi mamá, papá y hermano por el apoyo incondicional y la confianza depositada en mi. A Helmunt quien no sólo ha sabido darme su amor a lo largo de estos años, si no, también me ha ayudado en momentos computacionales muy críticos. Muchas Gracias! Muito obrigada! x ABSTRACT BIODIVERSITY AND CONNECTIVITY OF CALCAREOUS SPONGES (PORIFERA: CALCAREA) IN THE WESTERN TROPICAL ATLANTIC Báslavi Marisbel Cóndor Luján Supervisor: Dr. Michelle Klautau Abstract of the thesis submitted to the Graduate Program Biodiversity and Evolutionary Biology, Institute of Biology, Federal University of Rio de Janeiro – UFRJ, as part of the requirements to obtain the title of Doctor in Biological Sciences. The Western Tropical Atlantic (WTA) is a wide region that comprises the Tropical Northwestern Atlantic (TNA), the North Brazil Shelf (NBS) and the Tropical Southwestern Atlantic (TSA) provinces. Although it harbours a high diversity of marine species, sponges of the class Calcarea have been poorly studied. This lack of knowledge hinders our understanding of the biogeographical affinities of the calcareous sponges in the WTA and the role of the Amazon River as an effective barrier to dispersal of these sponges. In the present study, the diversity of the class Calcarea in the WTA was investigated using morphological and molecular approaches and the population connectivity of a calcareous sponge, Leucetta floridana, was assessed. With this contribution, the number of calcareous sponges from the WTA raised from 67 to 86, including the descriptions of 15 new species and four new records. Among them, 21 species are endemic to the TNA, three to the NBS and 22 to the TSA. The 14 species shared between the TNA and TSA support a Caribbean-Brazilian affinity for calcareous sponges. Genetic analyses evidenced five structured populations in L. floridana: one widespread population maintaining gene flow between the TNA and TSA provinces and four other isolated populations within the Caribbean Sea. The panmitic population suggested that the outflow of the Amazon River in the Atlantic is not an effective barrier to the maintenance of gene flow among trans-Amazonian populations of L. floridana. Keywords: Caribbean Sea, NE Brazilian coast, phylogeography, demography, Amazon River. Rio de Janeiro February, 2017 xi RESUMO BIODIVERSIDADE E CONECTIVIDADE DE ESPONJAS CALCAREAS (PORIFERA, CALCAREA) NO ATLÂNTICO TROPICAL OCIDENTAL Báslavi Marisbel Cóndor Luján Orientadora: Dra. Michelle Klautau Resumo da Tese submetida ao Programa de Pós-Graduação em Biodiversidade e Biologia Evolutiva, Instituto de Biologia, Universidade Federal do Rio de Janeiro – UFRJ, como parte dos requisitos necessários à obtenção do título de Doutor em Ciências Biológicas. O Atlântico Tropical Ocidental (WTA) é uma vasta região que compreende as províncias Atlântico Noroeste Tropical (TNA), Plataforma Norte do Brasil (NBS) e Atlântico Tropical Sudoeste (TSA). Embora abrigue uma grande diversidade de espécies marinhas, as esponjas da classe Calcarea têm sido pouco estudadas. Essa falta de conhecimento dificulta nossa compreensão das afinidades biogeográficas das esponjas Calcarea no WTA e do papel do Rio Amazonas como uma barreira efetiva para a dispersão dessas esponjas. Neste estudo, foi investigada a diversidade da classe Calcarea no WTA por meio de abordagens morfológicas e moleculares e também foi avaliada a conectividade populacional da esponja Calcarea Leucetta floridana. Com a presente contribuição, o número de esponjas da classe Calcarea no WTA aumentou de 67 para 86 espécies, incluindo descrições de 15 espécies novas e 4 novos registros. Entre elas, 21 espécies são endêmicas do TNA, três ocorrem só NBS e 22 são exclusivas do TSA. As 14 espécies compartilhadas entre o TNA e o TSA sugerem uma afinidade Caribe-Brasil para as esponjas calcareas. As análises genéticas evidenciaram cinco populações estruturadas em L. floridana:
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