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Scyphozoa, Rhizostomeae) 1 Renato Mitsuo Nagata Bases morfo-funcionais da alimentação e o papel trófico de Lychnorhiza lucerna (Scyphozoa, Rhizostomeae) Morphofunctional bases of feeding and the trophic role of Lychnorhiza lucerna (Scyphozoa, Rhizostomeae) Tese apresentada ao Instituto de Biociências da Universidade de São Paulo, para a obtenção de Título de Doutor em Ciências, na Área de Zoologia. Orientador: Dr. André Carrara Morandini São Paulo 2015 2 Nagata, Renato Bases morfo-funcionais da alimentação e o papel trófico de Lychnorhiza lucerna (Scyphozoa, Rhizostomeae) 172 páginas Tese (Doutorado) – Instituto de Biociências da Universidade de São Paulo. Departamento de Zoologia. 1. Medusas 2. Scyphozoa 3. Blooms Universiade de São Paulo. Instituto de Biociências. Departamento de Zoologia Comissão Julgadora: _________________________________ _________________________________ Prof(a). Dr(a). Prof(a). Dr(a).. _________________________________ _________________________________ Prof(a). Dr(a). Prof(a). Dr(a). _____________________________________________ Prof(a). Dr(a). Orientador(a) 3 Epígrafe The poet’s eye, in a fine frenzy rolling, Doth glance from heaven to earth, from earth to heaven; And as imagination bodies forth The forms of things unknown, the poet’s pen Turns them to shapes, and gives to airy nothing A local habitation and a name William Shakespeare, A Midsummer Night’s Dream, Act V, Scene 1 4 Agradecimentos Ao meu orientador Dr. André Carrara Morandini por acreditar na ideia desta tese investindo um grande esforço em sua realização. Ao Dr. John Costello por viabilizar a realização das filmagens das medusas, durante suas visitas ao Brasil e por me receber duas vezes em seu laboratório no Marine Biological Laboratory. Ao Prof. Dr. Marcelo Z. Moreira pela sua colaboração no trabalho com isótopos estáveis e a disponibilização de inúmeras facilidades em seu laboratório. Ao Prof. Dr. Alvaro E. Migotto, pela ajuda com fotos de Lychnorhiza lucerna e por diversos auxílios no CEBIMar. Ao Prof. Dr. Antônio C. Marques pela ajuda na viabilização de duas vindas do Prof. John Costello, fundamentais para a realização desta tese. Ao Prof. Dr. Marcelo R. Carvalho por vários auxílios para a realização da tese À Fundação de Pesquisa do Estado de São Paulo (FAPESP) pela concessão da bolsa e do estágio de doutorado no exterior (BEPE). Às pessoas que compartilharam seu conhecimento, colaboram com ideias e sugestões incorporadas neste trabalho: Dr. Sean Colin, Dr. Lars J. Hansson, Dr. Mark J. Gibbons, Dr. Agustin Schiariti, Dra. Thais N. Cobisier, Dra. Kylie Pitt, Dr. Paulo I.K.L. Prado e ao finado Dr. Hermes Mianzan a quem devo o entusiasmo e inspiração. À Dra. Maria Angélica Haddad e ao Dr. Miodeli Nogueira Jr. por despertar minha paixão por gelatinosos, serei eternamente grato. À Silvia Gonsales pelas excelentes ilustrações e a Carol Silva pela ajuda com mapas. 5 Ao Centro de Biologia Marinha (CEBIMar- USP), principalmente aos técnicos: “Seu Elso”, José Ilton, Edu e ao finado Joseph por sua ajuda em campo. Ao pessoal da administração, sempre muito atenciosos. E a galerinha do Cebimar: Serginho, Sol, Pedro, Pola, Danilo, Mogli, por várias estadias, as vezes inusitadas. Sem esquecer do pessoal do “Projeto Garoupa”, Profa. Dra. Renata G Moreira, Jajá, Bruno, Paulo, Mariana e Jéssica, por ceder tanques para cultivar a Lychnorhiza e também pelos momentos de descontração e pelo surf, além dos churrascos pós-surf. Ao Instituto Oceanográfico (IO-USP) principalmente à Maria F. Farias, Amauri Borges, Clayton Pontes, Clóvis R.X. Junior (Cebola) pela grande ajuda com coletas. Agradeço ao Marine Biological Laboratory (MBL) especialmente à Carol Coughan e Deborah Deering pela ajuda durante as minhas duas estadias nesse instituto. Obrigado à John Furley pela ajuda com bibliografias antigas. Aos companheiros de laboratório Dr. Sérgio Stampar, Julia Beneti, Jonathan Almeida, Leandro Santos, Gisele Tiseo, Henrique Alves, Clarissa Molinari e Priscila Cunha por ajudas em coletas e diversos momentos de descontração durante o trabalho. Agradeço aos colegas do IB Cristiano, Loboda, Sirula, Gordo, Diego, Karla, Bial, Marcão, Isa, Maria, Jimena, Paulo, Bruno, Jajá, Recoder, Raquel, Adri, Chico, Fukuda, Edu pelos bons momentos, alguns copos de cervjas e muitas risadas. Aos rabugentos esses sim, parceiros da casa Zé, Netão, Daniel, Caio e Cora. Aos “Nagatas” Clara e Hiromitsu, minhas irmãs Juliana e Mariana e a minha finada avó Yassuko, por todo seu suporte, valiosos conselhos, sem os quais eu não estaria aqui hoje. E por último porém não menos importante, à Nilvea Ramalho de Oliveia minha companheira em tudo, por seu amor e amizade os quais me fazem prosseguir em todas as circunstâncias. 6 ÍNDICE INTRODUÇÃO GERAL .......................................................................................................... 8 OBJETIVOS ............................................................................................................................ 18 CAPÍTULO 1: IMPLICATIONS OF ANIMAL-FLUID INTERACTIONS TO THE FEEDING BEHAVIOR OF LYCHNORHIZA LUCERNA (SCYPHOZOA, RHIZOSTOMEAE) ........... 28 ABSTRACT ........................................................................................................................ 29 INTRODUCTION ............................................................................................................... 30 MATERIAL AND METHODS .......................................................................................... 35 RESULTS ............................................................................................................................ 40 DISCUSSION ..................................................................................................................... 56 CONCLUSIONS ................................................................................................................. 65 BIBLIOGRAPHY ............................................................................................................... 67 CAPÍTULO 2: DIET, PREY SELECTIVITY AND FEEDING RATES OF THE RHIZOSTOME SCYPHOMEDUSA LYCHNORHIZA LUCERNA IN SOUTHWESTERN ATLANTIC COAST ............................................................................................................... 73 INTRODUCTION ............................................................................................................... 75 MATERIAL AND METHODS .......................................................................................... 79 RESULTS ............................................................................................................................ 87 DISCUSSION ..................................................................................................................... 98 CONCLUSION ................................................................................................................. 106 BIBLIOGRAPHY ............................................................................................................. 108 CAPÍTULO 3: FOOD WEB CHARACTERIZATION BASED ON δ15N AND δ13C REVEALS ISOTOPIC NICHE PARTITIONING BETWEEN FISH AND JELLYFISH IN A RELATIVELY PRISTINE ECOSYSTEM ........................................................................... 114 ABSTRACT ...................................................................................................................... 115 INTRODUCTION ............................................................................................................. 116 MATERIALS AND METHODS ...................................................................................... 119 RESULTS .......................................................................................................................... 125 DISCUSSION ................................................................................................................... 134 BIBLIOGRAPHY ............................................................................................................. 144 DISCUSSÃO GERAL E CONCLUSÕES ............................................................................ 154 RESUMO .............................................................................................................................. 169 ABSTRACT .......................................................................................................................... 171 7 INTRODUÇÃO GERAL Cifomedusas: sua importância para o ecossistema e para o homem O subfilo Medusozoa (Cnidaria) é caracterizado pela presença do estágio de medusa no ciclo de vida e reúne as classes Staurozoa (~50 spp.), Scyphozoa (~200 spp.), Cubozoa (~36 spp.) e Hydrozoa (~ 3500 spp.) (Petersen, 1979; Daly et al., 2007). São caracterizados pela simetria radial e representam geralmente o estágio sexuado e vágil do ciclo de vida. Medusas de Scyphozoa, as águas-vivas, são exclusivamente marinhas e se destacam pelo grande tamanho de algumas espécies (Russell 1970; Mianzan & Cornelius 1999). As cifomedusas, exceto algumas espécies de Coronatae, são conspícuas, medindo geralmente >5 cm e algumas espécies até >2 m de diâmetro (Cornelius, 1997; Arai, 1997; Mianzan & Cornelius, 1999, Kawahara et al., 2006). Uma característica da biologia de algumas cifomedusas são os fenômenos de “blooms”, quando um há um rápido aumento do número de indivíduos que leva a densidades altíssimas (Graham et al., 2001; Boero et al., 2008; Hamner & Dawson, 2009; Miranda et al., 2012). Blooms são uma característica natural da biologia populacional das espécies, estando relacionados
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