DISSERTAÇÃO DE MESTRADO

Transcrição

1 UNIVERSIDADE ESTADUAL PAULISTA JÚLIO MESQUITA FILHO INSTITUTO DE BIOCIÊNCIAS PÓS-GRADUAÇÃO EM CIÊNCIAS BIOLÓGICAS ÁREA DE CONCENTRAÇÃO: ZOOLOGIA DISSERTAÇÃO DE MESTRADO BIOLOGIA E ECOLOGIA DE ERMITÕES (CRUSTACEA, ANOMURA) DO SUBLITORAL NÃO CONSOLIDADO DO SUDESTE BRASILEIRO Israel Fernandes Frameschi de Lima Orientador: Prof o. Dr. Adilson Fransozo Co-orientador: Prof o. Dr. Fúlvio Aurélio de Morais Freire Botucatu SP 2014

2 BIOLOGIA E ECOLOGIA DE ERMITÕES (CRUSTACEA, ANOMURA) DO SUBLITORAL NÃO CONSOLIDADO DO SUDESTE BRASILEIRO Israel Fernandes Frameschi de Lima Orientador: Prof o. Dr. Adilson Fransozo Co-orientador: Prof o. Dr. Fúlvio Aurélio de Morais Freire Dissertação apresentada ao curso de pósgraduação em Ciências Biológicas: Zoologia, do Instituto de Biociências, Universidade Estadual Paulista (UNESP), Campus de Botucatu, como parte dos requisitos para a obtenção do título de Mestre em Ciências Biológicas Área de Concentração: Zoologia. Botucatu - SP 2014

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4 Dedico esta dissertação À minha Mãe, Issuileni Maria Frameschi, pelo amor, esforço e dedicação para criar eu e meu irmão; ao meu irmão Raony Cézar Frameschi de Lima que tanto me ensinou, e ainda ensina todos os dias. Vocês são o que tenho de melhor, minha segurança. À minha esposa Luciana S. Andrade, que desde quando era minha professora acreditou na minha capacidade, confiou, incentivou, mostrou os caminhos para ser um bom professor e me tornar uma pessoa melhor a cada dia. Ao meu orientador Adilson Fransozo, que confiou em mim desde quando cheguei a Botucatu. E o melhor: deixou-me carregar água salgada, e tudo que nela continha, dentro da camionete!

5 Agradecimentos À Deus, que me deu forças, saúde e proteção, me confortando nos momentos difíceis. Ao Prof. Dr. Adilson Fransozo pela amizade, confiança, e por ter aberto as portas do seu laboratório e se dispor em ser meu orientador. Por ter me dado a oportunidade de conhecer e ter contato com animais fantásticos como os ermitões e me ensinado sobre eles. Por ter tido paciência ao longo de todo período de convivência. Ao Prof. Dr. Fúlvio Aurélio de Morais Freire pelo exemplo de profissional e por me auxiliar nessa etapa final do mestrado. À Profa. Dra. Maria Lucia Negreiros Fransozo pelo exemplo de profissionalismo e por todo conhecimento transmitido desde que cheguei ao laboratório. À CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) e ao CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) pela bolsa concedida durante todo meu mestrado. Ao Núcleo de Estudos em Biologia, Ecologia e Cultivo de Crustáceos (NEBECC), por toda infraestrutura de laboratórios e materiais utilizados, à Fundação de Amparo à Pesquisa do Estado de São Paulo FAPESP, processos 97/ ; 97/ e 97/ , os quais tornaram viável a realização deste trabalho; e pelos veículos utilizados (#94/ e #98/ ). Á Prof a. Lissandra Corrêa Fernandes-Goés por todo apoio, profissionalismo e dicas quanto aos estudos dos ermitões. A todos integrantes do NEBECC e funcionários envolvidos, que de alguma forma contribuiram para a execução do projeto. Aos amigos que estão ou passaram pelo NEBECC desde a minha chegada. Aos meus co-autores: Prof. Dr. Antônio L. Castilho, Prof a. Dr a. Vivian Fransozo, Prof. Dr. Gustavo Monteiro Teixeira, Prof a. Dr a. Lissandra Corrêa Fernandes-Goés,

6 Prof a. Dr a. Luciana S. Andrade, Dr a. Michele Furlan, e MSc. Carlos Eduardo R. D. Alencar, pelas valorosas contribuições durante a produção dos manuscritos. Ao Prof. Dr. Marcio R. Pie e Prof a. Dr a. Janet W. Reid, pelos valorosos auxílios com as traduções português-inglês, e emendas da língua nativa. À minha mãe, que sempre se esforçou para me manter em Botucatu até que eu pudesse me sustentar. Por me receber de braços abertos e com belo sorriso no rosto todas as vezes que eu fui visita-la. Ao meu irmão Raony, que me apoiou quando decidi mudar de Maringá para continuar os estudos. Por ter segurado as pontas com a mãe e com a vó quando estive ausente. À minha avó Mafalda Cemato Flamesque, que sempre ajudou na minha educação e me incentivou a estudar. Por sempre me esperar com café quente. Ao Rayan e à Laís de Andrade Andrade, por alegrarem meus dias mais difíceis, estimulando meu crescimento pessoal. Aos meus sogros e amigos José C. Andrade e Ivanir J. S. Andrade, pelos valorosos conselhos e por confiarem em mim para cuidar do pedacinho da família de vocês. À minha eterna professora e esposa Luciana. Obrigado pelas inúmeras discussões que se estendiam desde o momento que acordávamos (e eu odiava), até o momento que íamos dormir (e ela odiava!). Por ter paciência nos meus momentos de máxima irritação e permanecer ao meu lado, me dando carinho e dizendo que me ama todos os dias.

7 Índice CONSIDERAÇÕES INICIAIS Referências bibliográficas CAPÍTULO I: Ecological distribution of the red brocade hermit crab Dardanus insignis (Anomura: Paguroidea) in shallow waters of three bays in a tropicalsubtropical transition zone on the Brazilian coast Abstract Introduction Material and Methods Results Discussion References CAPÍTULO II: Life-history traits of the red brocade hermit crab Dardanus insignis on the subtropical Brazilian coast Abstract Introduction Material and Methods Results Discussion References CAPÍTULO III: Traços da história de vida do ermitão endêmico do Atlântico Sul Loxopagurus loxochelis (Anomura: Paguroidea) em águas rasas da zona de transição tropical-subtropical na costa brasileira Resumo... 61

8 Introdução Material e Métodos Resultados Discussão Referências CAPÍTULO IV: Shell occupation by the hermit crab Dardanus insignis (Decapoda, Diogenidae) in a subtropical region of Brazil Abstract Introduction Material and Methods Results Discussion References CAPÍTULO V: Shell occupation by the South Atlantic endemic hermit crab Loxopagurus loxochelis (Moreira, 1901) (Anomura: Diogenidae) Frameschi I.F., Andrade L.S., Alencar C.E.R.D., Fransozo V., Teixeira G.M., Fernandes-Goés L.C., Nauplius CONSIDERAÇÕES FINAIS

9 Considerações iniciais

10 Considerações iniciais Frameschi IF 2014 A ordem Decapoda é uma das mais ricas entre os Crustacea, reunindo mais de espécies conhecidas, das quais mais de fazem parte da fauna atual e cerca de espécies com apenas registro fóssil (De Grave et al. 2009). Os crustáceos decápodos se encontram divididos em duas grandes subordens, os Dendrobranquiata, representados pelos camarões Peneoidea e Sergestoidea, e a subordem Pleocyemata, que reúne os animais das infraordens Achelata, Anomura, Astacidea, Axiidea, Brachyura, Caridea, Gebiidea, Glypheidea, Polychelida e Stenopodidea (De Grave et al. 2009). A infraordem Anomura MacLeay, 1838, compreende sete superfamílias: Kiwaoidea, Lomisoidea, Galatheoidea, Aegloidea, Lithodoidea, Hippoidea e Paguroidea. Esta última compreende os ermitões, os quais estão organizados em seis famílias: Coenobitidae Dana, 1851; Diogenidae Ortmann, 1892; Paguridae Latreille, 1802; Parapaguridae Smith, 1882; Pylochelidae Bate, 1888 e Pylojacquesidae McLaughlin & Lemaitre, 2001 (McLaughlin et al. 2007; Mclaughlin et al. 2010). Os representantes da superfamília Paguroidea são distinguidos dos demais Anomura pela presença do abdome nu, não segmentado e usualmente curvado, tipicamente protegido por uma concha de Gastropoda vazia e espiralada para a direita, uma vez que a maioria das conchas são dextrógiras (Hazlett 1981; Lancaster 1988). Cerca de 1100 espécies de ermitões são encontradas no mundo todo, distribuídos em 120 gêneros (McLaughlin et al. 2010). No litoral brasileiro há registro de aproximadamente 50 espécies descritas (Nucci & Melo 2003). Destas, 26 são encontradas do litoral paulista, explorando regiões intertidais e sublitorâneas, de substratos consolidados e não consolidados (Nucci & Melo 2007). Os ermitões da família Diogenidae são os mais representativos, com 18 espécies (Melo, 1999). A presente dissertação aborda diversos aspectos da história de vida de duas espécies Diogenidae: Dardanus insignis (Saussure, 1858) e Loxopagurus loxochelis (Moreira, 1901). O ermitão D. insignis ocorre em quase toda a costa oeste do Atlântico, desde a Carolina do Norte (EUA) até a Argentina. No Brasil, é encontrado do Rio de Janeiro ao Rio Grande do Sul, limitando-se a gradientes de profundidade entre 1,5 e 500 metros (Melo 1999). Esta é a espécie mais abundante do sublitoral não-consolidado do sudeste brasileiro (Fransozo et al 2011, 2012; 2

11 Considerações iniciais Frameschi IF 2014 Furlan et al. 2013), sendo este um dos motivos pelo qual é classificado como uma das mais relevantes na estruturação da megafauna bentônica da região (Pires 1992; De Léo & Pires- Vanin 2006). Com distribuição mais restrita, L. loxochelis pertence a um gênero monotípico endêmico do Atlântico Sul (Nucci & Melo 2007), ocorrendo do estado da Bahia ao Rio Grande do Sul (Brasil), Uruguai e Argentina (Melo 1999). Em seus limites de ocorrência, L. loxochelis é a segunda espécie mais representativa em profundidades de até 30 metros (Fransozo et al. 2008). A grande abundância das espécies supracitadas em relação às demais coexistentes no sudeste brasileiro (Fransozo et al. 1998, 2008; Mantelatto & Garcia 2002) é intrigante. Numerosos estudos foram realizados nos últimos anos com a finalidade de investigar os padrões populacionais que regem a expressiva abundância de D. insignis (Hebling & Mansur 1995; Miranda et al. 2006; Branco et al. 2002; Fernandez-Goés et al. 2005) e de L. loxochelis (Martinelli & Mantelatto 1999; Mantelatto & Martinelli 2001; Martinelli et al. 2002; Bertini et al. 2004; Mantelatto et al. 2004; Biagi et al. 2006; Ayres-Peres & Mantelatto 2008; Carranza et al. 2008; Torati & Mantelatto 2008; Ayres-Peres et al. 2012; Frameschi et al. 2013). Tais estudos auxiliam de forma direta ou indireta na identificação de padrões que são modificados por estratégias que visam obtenção do fitness populacional em regiões que são constantemente alteradas. Uma dessas alterações do ambiente pode ser decorrente da pesca camaroeira, a qual promove alterações no sedimento que perturbam a comunidade bentônica, afetando principalmente os crustáceos, elasmobrânquios e cefalópodes (Wassenberg & Hill 1989). Além das modificações causadas pelo aumento da pesca de arrasto no sudeste do brasileiro (Costa et al. 2000), deve-se ressaltar que as zonas costeiras dessa região são ambientes dinâmicos, sujeitos às influências continentais, atmosféricas e oceânicas, sendo classificada por Boschi (2000) como uma área de transição hidrológica e faunística, a qual abriga uma mistura de faunas provenientes de regiões tropicais, 3

12 Considerações iniciais Frameschi IF 2014 subtropicais e subantárticas (Sumida & Pires-Vanin 1997). Essa instabilidade também age sobre a comunidade bentônica determinando padrões de densidade e distribuição, além de direcionar relações tróficas entre as espécies (Santos & Pires-Vanin 2004). Nesse sentido, essa dissertação pretende contribuir com informações sobre a biologia e ecologia das duas espécies de ermitões mais abundantes do sublitoral do sudeste brasileiro, D. insignis e L. loxochelis, numa abordagem comparativa e multivariada das relações entre as espécies, ambiente e recursos. Assim, o resultado final desse estudo foi dividido em cinco capítulos. O primeiro e segundo capítulos, Ecological distribution of the red brocade hermit crab Dardanus insignis (Anomura: Paguroidea) in shallow waters of three bays in a tropical-subtropical transition zone on the Brazilian coast e Life-history traits of the red brocade hermit crab Dardanus insignis on the subtropical Brazilian coast, foram encaminhados para apreciação das revistas Marine Biodiversity e Marine Biology Research, respectivamente; e referem-se aos padrões de distribuição, período reprodutivo, recrutamento juvenil, maturidade sexual, crescimento e longevidade de D. insignis. O terceiro, Traços da história de vida do ermitão endêmico do Atlântico Sul Loxopagurus loxochelis (Anomura: Paguroidea) em águas rasas da zona de transição tropical/subtropical na costa brasileira, avalia as características da história de vida de L. loxochelis com foco em sua distribuição espaço-temporal, estrutura populacional, maturidade sexual, período reprodutivo, proporção sexual, crescimento, longevidade e relações com variáveis ambientais. Os dois últimos capítulos investigam sobre o padrão de utilização de conchas pelos ermitões estudados nessa dissertação. O quarto capítulo, Shell occupation by the hermit crab Dardanus insignis (Decapoda, Diogenidae) in a subtropical region of Brazil está em processo de revisão no Brazilian Journal of Biology; enquanto que o quinto e último capítulo, Shell ocupation by the South 4

13 Considerações iniciais Frameschi IF 2014 Atlantic endemic hermit crab Loxopagurus loxochelis (Moreira, 1901) (Anomura: Diogenidae), foi recentemente publicado na revista Nauplius. Referências bibliográficas Ayres-Peres, L. & Mantelatto, F.L Análise comparativa da estrutura populacional do ermitão endêmico do Atlântico Ocidental Loxopagurus loxochelis (Decapoda, Anomura) em duas regiões do Estado de São Paulo, Brasil. Iheringia, 98(1): Ayres-Peres, L.; Quadros, A.F. & Mantelatto, F.L Comparative analysis of shell occupation by two southern populations of the hermit crab Loxopagurus loxochelis (Decapoda, Diogenidae). Brazilian Journal of Oceanography, 60(3): Bertini, G.; Fransozo, A. & Braga, A.A Ecological distribution and reproductive period of the hermit crab Loxopagurus loxochelis (Anomura, Diogenidae) on the northern coast of São Paulo State, Brazil. Journal of Natural History, 38(18): Biagi, R.; Meireles, A.L.; Scelzo, M.A. & Mantelatto, F.L Comparative study of shell choice by the southern endemic hermit crab Loxopagurus loxochelis from Brazil and Argertina. Revista Chilena de Historia Natural, 79(4): Boschi, E.E Species of Decapod Crustaceans and their distribution in the American marine zoogeographic provinces. Revista de Investigación y Desarrollo Pesquero, 13: Branco, J. O.; Turra, A. & Souto, F.X Population biology and growth of the hermit crab Dardanus insignis at Afirmacao do Itapocoroy, southern Brazil. Journal of the Marine Biological Association of the United Kingdom, 82: Carranza, A.; Segura, A.; Lopez, J. & Rubio, L Shell use patterns of the hermit crab Loxopagurus loxochelis (Decapoda: Diogenidae) in Cerro Verde - La Coronilla (Rocha, Uruguay). Comunicaciones de la Sociedad Malacológica del Uruguay, 9(91): Costa, R.C.; Fransozo, A.; Mantelatto, F.L.M. & Castro, R.H Occurrence of shrimp species (Crustacea: Decapoda: Natantia: Penaeidea and Caridea) in Ubatuba Bay, Ubatuba, SP, Brazil. Proceedings-Biological Society of Washington, 113(3): De Grave, S.; Pentcheff, N.D.; Ahyong, S.T.; Chan, T.Y.; Crandall, K.A.; Dworschak, P.C.; Felder, D.L.; Feldmann, R.M.; Fransen, C.H.J.M.; Goulding, L.Y.D.; Lemaitre, 5

14 Considerações iniciais Frameschi IF 2014 R.; Low, M.E.Y.; Martin, J.W.; Ng, P.K.L.; Schweitzer, C.E.; Tan, S.H.; Tshudy, D. & Wetzer, R A classification of living and fossil genera of decapod crustaceans. Raffles Bulletin of Zoology, 21: De Léo, F.C. & Pires-Vanin, A.M.S Benthic megafauna communities under the influence of the South Atlantic Central Water intrusion onto the Brazilian SE shelf: A comparison between an upwelling and a non-upwelling ecosystem. Journal of Marine Systems, 60(3): Fernandes-Goés, L.C.; Fransozo, A. & Goés, J.M Population dynamics of Dardanus insignis (Saussure, 1858) (Crustacea, Anomura, Diogenidae) in the Ubatuba region, São Paulo, Brazil. Nauplius, 13(2): Frameschi, I.F.; Andrade, L.S.; Alencar, C.E.R.D.; Fransozo, V.; Teixeira, G.M. & Fernandes-Goés, L.C Shell occupation by the South Atlantic endemic hermit crab Loxopagurus loxochelis (Moreira, 1901) (Anomura: Diogenidae). Nauplius, 21(2): Fransozo, A.; Bertini, G.; Braga, A.A. & Negreiros-Fransozo, M.L Ecological aspects of hermit crabs (Crustacea, Anomura, Paguroidea) off the northern coast of São Paulo State, Brazil. Aquatic Ecology, 42: Fransozo, A.; Fernandes-Góes, L.C.; Fransozo, V. Góes, J.M. & Cobo, V.J.; Teixeira, G.M. & Gregati, R.A Marine anomurans (Decapoda) from the nonconsolidated sublittoral bottom at the Southeastern of Brazil. Crustaceana, 84(4): Fransozo, A.; Furlan, M.; Fransozo, V.; Bertini, G.; Costa, R.C. & Fernandes-Góes, L.C Diversity of decapod crustaceans at the interface of unconsolidated seabed areas and rocky shores in tropical/subtropical Brazil. African Journal of Marine Science, 34(3): Fransozo, A.; Mantelatto, F.L.M.; Bertini, G.; Fernandes-Góes, L.C. & Martinelli, J.M Distribution and assemblages of anomuran crustaceans in Ubatuba Bay, North coast of São Paulo State, Brazil. Acta Biologica Venezuelica, 18(4): Furlan, M.; Castilho, A.L.; Fernandes-Góes L.C.; Fransozo, V.; Bertini, G. & Costa, R.C Effect of environmental factors on the abundance of decapod crustaceans from soft bottoms off southeastern Brazil. Anais da Academia Brasileira de Ciências, 85(4): Hazlett, B.A The behavioral ecology of hermit crabs. Annual Review of Ecology and Systematics, 12,

15 Considerações iniciais Frameschi IF 2014 Hebling, N.J. & Mansur, C.B Desenvolvimento larval de Dardanus insignis (Saussure) (Crustacea, Decapoda, Diogenidae), em laboratório. Revista Brasileira de Zoologia, 12(3): Lancaster, I Pagurus bernhardus (L.) an introduction to the natural history of hermit crabs. Field Studies, 7(1): Mantelatto, F.L. & Garcia, R.B Hermit crab fauna from the infralittoral zone of Anchieta Island (Ubatuba, Brazil). In: Modern Approaches to the study of Crustacea. Springer. pp Mantelatto, F.L. & Martinelli, J.M Relative growth and sexual dimorphism of the South Atlantic hermit crab Loxopagurus loxochelis (Anomura, Diogenidae) from Ubatuba, Brazil. Journal of Natural History, 35(3): Mantelatto, F.L.; Martinelli, J.M. & Fransozo, A Temporal-spatial distribution of the hermit crab Loxopagurus loxochelis (Decapoda, Anomura, Diogenidae) from Ubatuba Bay, São Paulo State, Brazil. Revista de Biologia Tropical, 51(4): Martinelli, J.M. & Mantelatto, F.L Shell utilization by the hermit crab Loxopagurus loxochelis (Diogenidae) in Ubatuba Bay, Brazil. In: Schram, F.R. & Vanpel Klein, J.C. (eds.) Crustaceans and the Biodiversity Crisis, 1: Martinelli, J.M.; Mantelatto, F.L. & Fransozo, A Population structure and breeding season of the South Atlantic hermit crab, Loxopagurus loxochelis (Anomura, Diogenidae) from the Ubatuba region, Brazil. Crustaceana, 75(6): McLaughlin, P.A.; Boyko, C.B.; Crandall, K.A.; Komai, T.; Lemaitre, R.; Osawa, M. & Rahayu, D.L Annotated checklist of anomuran decapod crustaceans of the world (exclusive of the Kiwaoidea and families Chirostylidae and Galatheidae of the Galatheoidea) preamble and scope. The Raffles Bulletin of Zoology, 23: 1-4. McLaughlin, P.A.; Lemaitre, R. & Sorhannus, U Hermit crab phylogeny: a reappraisal and its fall-out. Journal of Crustacean Biology, 27(1): Melo, G.A.S Manual de identificação dos Crustacea Decapoda do litoral Brasileiro: Anomura, Thalassinidea, Palinuridea e Astacidea. São Paulo, Editora Plêiade, 551p. Miranda, I.; Meireles, A.L.; Biagi, R. & Mantelatto, F.L Is the abundance of the red brocade hermit crab Dardanus insignis (Decapoda: Anomura: Diogenidae) in the infralittoral region of southern Brazil determined by reproductive potential. Crustacean Research, 6:

16 Considerações iniciais Frameschi IF 2014 Nucci, P.R. & Melo, G.A.S A new species of Pagurus (Decapoda, Anomura, Paguridae) from Brazil. Journal of the Marine Biological Association of the United Kingdom, 83: Nucci, P.R. & Melo, G.A.S Hermit crabs from Brazil. Family Paguridae (Crustacea: Decapoda: Paguroidea): Genus Pagurus. Zootaxa, 1406: Pires, A.M.S Structure and dynamics of benthic megafauna on the continental shelf offshore of Ubatuba, southeastern Brazil. Marine Ecology Progress Series, 86(1): Santos, M.F.L.D. & Pires-Vanin, A.M.S Structure and dynamics of the macrobenthic communities of Ubatuba Bay, southeastern Brazilian coast. Brazilian Journal of Oceanography, 52(1): Sumida, P.Y.G. & Pires-Vanin, A.M.S Benthic associations of the shelfbreak and upper slope off Ubatuba-SP, south-eastern Brazil. Estuarine, Coastal and Shelf Science, 44(6): Torati, L.S. & Mantelatto, F.L Uncommon mechanism of egg incubation in the endemic Southern hermit crab Loxopagurus loxochelis: how is this phenomenon related to egg production? Acta Zoologica, 89(1): Wassenberg, T.J. & Hill, B.J The effect of trawling and subsequent handling on the survival rates of the by-catch of prawn trawlers in Moreton Bay, Australia. Fisheries Research, 7(1):

17 Capítulo I Ecological distribution of the red brocade hermit crab Dardanus insignis (Anomura: Paguroidea) in shallow waters of three bays in a tropicalsubtropical transition zone on the Brazilian coast

18 Shallow water distribution of D. insignis Frameschi IF 2014 Abstract: Dardanus insignis is the most abundant hermit crab on sublittoral of soft bottoms along the southeastern coast of Brazil. It is among the Decapoda species that structure the macrobenthic community, from shallow regions to deeper areas up to 100 m. This study evaluated the distribution of D. insignis in a tropical-subtropical transition zone. In three bays (Ubatumirim, Ubatuba and Mar Virado), sampling was conducted monthly for two years, on four transects parallel to the coastline (at depths of 5, 10, 15, and 20 m), as well as one transect sheltered from wave action, and another in a more exposed area. Environmental variables were monitored in each sampling. The study sites differed in water temperature, salinity, organic-matter content and substrate composition. The size fractions of coarse, medium and fine sand were correlated mainly with Ubatumirim and Ubatuba bays, on transects 15 and 20 m deep. The distribution of demographic groups showed a positive relationship with these variables, with large numbers of individuals found in Ubatuba and on the deepest transects. These results suggest that living farther from the coast might provide protection for D. insignis against the oscillation of environmental variables, especially those that are affected by rainfall regimes, such as the sediment. Keywords: Distribution, Spatial variation, Environmental factors, Diogenidae 10

19 Shallow water distribution of D. insignis Frameschi IF 2014 Introduction Studies on the distribution of marine organisms are essential to obtain information about coastal regions affected by human activity and contamination. Detailed studies of species with important roles in the dynamics of small areas may contribute to understanding the factors controlling their distributions (Mantelatto et al. 2004). Shallow benthic habitats are structurally complex environments, where a large number of biological and environmental factors (such as inter -and intraspecific relationships or physical changes, respectively) determine habitat quality and generate different stress levels that determine population and community structure and dynamics (Pallas et al. 2006). In shallow marine coastal areas, the marine soft-bottom fauna is frequently composed of a large number of species with different patterns of distribution and temporal dynamics (Van Hoey et al. 2004). Coastal zones of southeastern Brazil are variable environments, directly subject to continental, atmospheric and oceanic influences. The instability of the coastal zone affects the benthic community, determining the patterns of distribution and density and the trophic relationships among the species (Santos and Pires-Vanin 2004). As described by Boschi (2000), the southern and southeastern coast of Brazil is an area of hydrological and faunal transition, and consequently contains species of various origins in addition to the local endemics. This region harbors a mixture of faunas originating from tropical, subtropical and subantarctic regions (Sumida and Pires-Vanin 1997). Located along the northern coastline of the state of São Paulo, the Ubatuba region is an important area for crustacean research (Mantelatto and Fransozo 2000). The spatial and temporal distribution of a species results from aspects of the 11

20 Shallow water distribution of D. insignis Frameschi IF 2014 animal s biology such as the feeding mode, behavior and local characteristics (Negreiros-Fransozo et al. 1997; Sant' Anna et al. 2006). Hermit crabs are an important part of intertidal benthic communities over much of the continental shelf (Fransozo and Mantelatto 1998). The red brocade hermit crab Dardanus insignis (Saussure 1858) occurs in almost all the western Atlantic, from North Carolina (USA) to Argentina. In Brazil, it is distributed from Rio de Janeiro to Rio Grande do Sul, over a wide depth gradient from 1.5 to 500 m (Melo 1999). It is the most abundant hermit crab of soft bottoms off southeastern Brazil (Fransozo et al. 2011, 2012; Furlan et al. 2013). D. insignis is classified as one of the species that structure the benthic megafauna, from shallow regions to depths greater than 100 m (Pires 1992; De Léo and Pires-Vanin 2004). The abundance of this species in relation to the number of coexisting species of hermit crabs in this area (Fransozo et al. 1998, 2008; Mantelatto and Garcia 2002) is puzzling. Several recent studies have described some features of D. insignis, including the post-embryonic development (Hebling and Mansur 1995), fecundity (Miranda et al. 2006), and population dynamics (Branco et al. 2002; Fernandez-Goés et al. 2005). However, the scarcity of studies on its distribution, as well as the spatio-temporal relationships to environmental variables, leaves a gap to be filled, which may reveal patterns that help us unravel the reasons for its great abundance along the southeastern Brazilian coast. This study investigated the distribution pattern of D. insignis in shallow water, in a transition zone between the tropical and subtropical regions. The study included (a) the environmental characterization of six transects in three bays, (b) the spatial-temporal variation in the abundance of D. insignis, and (c) the relationship among environmental variables and the distribution of demographic groups. Materials and methods Study area 12

21 Shallow water distribution of D. insignis Frameschi IF 2014 In this tropical/subtropical portion of the Brazilian coast, the Serra do Mar coastal range nears the Atlantic Ocean, enclosing a narrow coastal plain. The northern coast of São Paulo State is markedly sinuous, forming many embayments that have some typical features of semi-confined environments. The study area comprised the shallow waters of three bays (Ubatumirim, Ubatuba and Mar Virado) on this coast. Ubatumirim Bay faces southwest, with several small islands close to its mouth; Ubatuba Bay faces east and has a seaward constriction formed by rocky projections; and the seaward end of Mar Virado Bay faces southeast (Mahiques 1995). Field collections Hermit crabs were collected monthly during 1998 (first year) and 1999 (second year), in Ubatumirim, Ubatuba and Mar Virado bays. Six transects were established in each bay: at depths of 5, 10, 15, and 20 m (parallel to the beach line), as well as one transect in an area sheltered (She) from wave action, and another in a more exposed area (Exp) (Fig.1). Figure 1. Map showing the location of three bays (Ubatumirim, Ubatuba, Mar Virado) and the sampling depths. A shrimp-fishing boat equipped with double-rig nets (mesh size 20 mm and 15 mm in the cod end) was used for trawling. In each trawl, the nets were deployed for 2 km over a period of 30 min, covering an area of approximately 18,000 m 2. Environmental variables 13

22 Shallow water distribution of D. insignis Frameschi IF 2014 Monthly measurements for each transect, the bottom- and surface-water temperatures and bottom salinity were recorded using a mercury thermometer attached to a Nansen bottle and an optical refractometer. An ecobathymeter coupled with a GPS was used to record depths at the sampling sites. Sediment samples were collected in each season with a Van Veen grab, sampling a bottom area of 0.06 m 2 to measure the organic-matter content (%) and grain size of the sediment. The sediment was dried at 70 C for 72 h in an oven. The sediment organic matter content (%) was obtained through ash-weighing: 3 aliquots of 10 g each per station were placed in porcelain crucibles and incinerated for 3 h at 500 C. The samples were then re-weighed to calculate the organic-matter content. The sediment remaining after analysis of the organic matter was re-dried and passed through a series of sieves with graduated mesh sizes, following the Wentworth (1922) scale. All the procedures for sediment analysis followed Håkanson and Jansson (1983) and Tucker (1988). Laboratory procedures After each trawl, all collected material was inspected, frozen, and transported to the laboratory, where the samples were kept until the analysis. Hermit crabs were identified according to Melo (1999). All individuals of D. insignis were counted, manually removed from their shells, sexed based on the position of the gonopores (on the coxa of the third pair of pereiopods in females and fifth pereiopods in males), and had their cephalothoracic shield length (CSL) measured with a caliper (0.10 mm). Juveniles were classified based on size, shape and color of gonads observed under a stereomicroscope (gonad thin and translucent, undifferentiated for males and females) (Lancaster 1988). Statistical analyses Principal Components Analysis (PCA) was used to extract the underlying annual patterns of environmental variables for each transect, using a correlation matrix based 14

23 Shallow water distribution of D. insignis Frameschi IF 2014 on the mean values of the data. To determine which principal components would be utilized, we used the hypothesis of randomness obtained from the Broken-Stick model (see Peres-Neto et al. 2005). Environmental variables with load components 0.5 were retained in the description of the main components (Mccune and Grace 2002; Maliao et al. 2008). Abundance data were evaluated for normality by the Shapiro-Wilk normality test (Shapiro and Wilk 1965). When not normal, the data were log-transformed (log x+1) and an analysis of variance (One-way ANOVA) was performed in order to assess the differences in abundance among seasons (temporal analysis) and mong transects (spatial analysis). The length (CSL) of specimens in each demographic group of each bay was compared by ANOVA (One-way). The Tukey multiple comparison test, at the 5% probability level, was applied to identify differences among the sample means (Zar 1999). The differences in sex ratio were tested for significant divergence from the expected 1:1 ratio, by a binomial test (Wilson and Hardy 2002). Data for the abundance of each demographic group in each bay and transect were organized in a two-factor contingency table to conduct a Correspondence Analysis (CA). During the CA the associations of both types of variables (demographic group and spatial distribution) were summarized by the frequency of each table cell, and then positioned in a geometric dimensional space, since the positions of each line and column were consistent with the associations of the table. Statistical significance of the eigenvalues and proportion was assessed using the chi-squared test with simulated p- value (based on 2000 randomizations) (Nenadic and Greenacre 2007). The Redundancy Analysis (RDA) was used to detect possible relationships between fluctuations in the abundance of demographic groups and the environmental variables measured. The RDA produces final scores of coordination that summarize the linear relationship between the explanatory and response variables (Jongman et al. 15

24 Shallow water distribution of D. insignis Frameschi IF ). Randomization tests (Monte Carlo test, 999 permutations), which provided p- values, were performed to check the validity of the PCA axes, and to check the linear relationship between response and explanatory matrices, and association between the first and second sets of sample unit ordination scores in RDA analyses (ter Braak 1986). P-values from these randomization tests indicate the confidence level of the predictions (Peck 2010). The multivariate analyses were run in PC-ORD (version 6, Mccune and Mefford 2011). Results Environmental variables The three bays have different geomorphological characteristics, and show temporal and spatial variations in environmental factors. The Monte Carlo permutation test indicated that the variation captured by regressions and PCA axes was significant, leading us to reject the null hypothesis of no relationship between the variables (Table 1). Table 1. Result of principal components analysis (PCA). Coefficients were obtained from the Pearson correlation. Bold numbers indicate the closest relationships Environmental variables Component PC 1 PC 2 Percent variance explained Monte Carlo test (P-value) Bottom Temperature (BT) Surface Temperature (ST) Bottom Salinity (BS) % Organic Matter (OM) Mean grain size (Phi) Biodetritus fragments (BDF) Very coarse sand (VCS) Coarse sand (CS) Medium sand (MS) Fine sand (FS) Very fine sand (VFS) Silt and clay (S+C)

25 Shallow water distribution of D. insignis Frameschi IF 2014 The first two PCA axes explained 69.83% of the total variability of the data, which were retained for interpretation. Silt + clay, phi, organic matter content and bottom temperature were positively correlated with the first axis, PC1 (Table 1). Bottom salinity, biodetritus fragments, and very coarse, coarse, medium and fine sand were negatively correlated with PC1. Very fine sand was the only factor that showed a high positive correlation with the second axis, PC2. The PCA ordination (Fig. 2) on the first axis established a depth gradient. In this gradient, the deeper transects were more distant from the center due to the larger fluctuations in salinity and sediment composition, ranging from very coarse sand to fine sand, over the two years of study (Fig. 2). Figure 2. Principal Components Analysis among environmental variables of each bay. (Ubm) Ubatumirim, (Uba) Ubatuba, (Mv) Mar Virado. (I) indicates first year; (II) indicates second year; Refer to Table 1 for codes of each environmental variable Spatio-Temporal variation In 432 hauls made during 24 months, 3169 hermit crabs were caught, 2232 in the first year and 846 in the second year. In both periods, the abundance of D. insignis was higher in Ubatuba Bay (1 st year = 1319, 2 nd year = 357), compared with Ubatumirim 17

26 Shallow water distribution of D. insignis Frameschi IF 2014 Bay (1 st year = 557, 2 nd year = 283) and Mar Virado Bay (1 st year = 447, 2 nd year = 206). The abundance of hermit crabs was significantly different between the bays (F = 14.42, p < 0.01) and study periods (F = 3.84, p < 0.01). The highest abundance of D. insignis during the first period occurred in winter (F = 1.123, p < 0.01). Temporal variation in the abundance of males and females followed the same pattern as the total abundance in each bay (Fig. 3). Figure 3. Mean abundance (point) and standard deviation (line) of Dardanus insignis caught per trawl in each bay by season of the year. Values in each figure indicate results of ANOVA test. Values with at least one letter in common after each point in the graph did not differ statistically (ANOVA; a posteriori Tukey test; P < 0.05) 18

27 Shallow water distribution of D. insignis Frameschi IF 2014 Table 2. Number of hermit crabs Dardanus insignis caught and sex ratio in each bay and season, on the northern coast of São Paulo State, Brazil. Numbers in bold indicate the significance of the sex ratio (P < 0.05) and * means= presence of ovigerous females First year Ubatumirim Ubatuba Mar Virado Males Females M:F Males Females M:F Males Females M:F Summer 72 68* * Autumn Winter 79 76* * Spring 42 29* * Second year Summer Autumn Winter * Spring 45 34* * * 0.94 The sex ratio over time was skewed toward males in all three bays. Higher proportions of females were observed during the spring and summer (Table 2). Hermit crabs were more abundant on the deeper transects, at 20 m and 15 m (p < 0.05; Fig. 4), with the exception of the protected transects (She) and exposed (Exp) in Ubatuba Bay. The highest abundance found on transect Exp UBA is clearly related to spatial segregation in the young (Fig. 4). Males and females occupied most transects in similar proportions, with rare exceptions (Table 3). The largest adult males were captured in UBA (Fig. 5). No difference was observed in the sizes of females and young between the bays. Females were significantly smaller than males in all the bays (Fig. 5). The first two axes accounted for 53.1% of the RDA variation in demographic groups of D. insignis (Fig. 6). 19

28 Shallow water distribution of D. insignis Frameschi IF 2014 Table 3. Number of each demographic group of Dardanus insignis (M = males; F = females; OF = ovigerous females) and sex ratio (M:F) in each bay and on each transect, on the northern coast of São Paulo State, Brazil. Values with at least one letter in common on the line do not differ statistically (P < 0.05; a posteriori Tukey test). n = total of individuals; * = (P < 0.05) First year Transects Ubatumirim Ubatuba Mar Virado n M F OF M:F n M F OF M:F n M F OF M:F 20 m 261 a 141 a 113 a 7 1: b 211 b 174 b 9 1: a 235 a 188 a - 1:0.8* 15 m 203 a 114 b 85 b 4 1: c 8 b 7 bc - 1:0.8 7 b 4 b 3 b - 1: m 42 bc 15 cd 26 b 1 1:1.8 3 c 2 b 1 bc - 1:0.5 3 b 2 b 1 b - 1:0.5 5 m c 12 b 10 bc 2 1: Exp 31 bc 24 cd 7 b - 1:0.3* 876 a 537 a 258 a 81 1:0.6* 3 b 3 b She 20 bc 12 cd 5 b 3 1:0.7 7 c 3 b 4 bc - 1: b 8 b 3 b - 1:0.4 Second year 20 m 108 b 60 c 37 b 11 1: c 58 b 42 bc 2 1: b 100 b 86 b 2 1: m 142 ab 90 c 49 b 3 1:0.6* 18 c 13 b 5 bc - 1: b 8 b 6 b - 1: m 9 bc 7 cd 2 b 1:0.3 2 c 1 b 1 bc - 1:1 1 b 1 b m 1 bc 1 cd c 8 b 5 bc Exp 8 c 7 cd 1 b - 1:0.1* 4 c - 4 bc She 15 bc 11 cd 3 b 1 1: b 141 b 45 bc 30 1:0.5* 3 b 1 b 2 b - 1:2 20

29 Shallow water distribution of D. insignis Frameschi IF 2014 Figure 4. Distribution of the relative abundance of Dardanus insignis on transects in three bays, indicating the differential distribution of demographic groups. (a) Abundance of juveniles; (b) Abundance of adult males; (c) Abundance of adult females; (d) Abundance of ovigerous females. The values in each figure indicate the correspondence analysis (CA) results, and the statistical significance of the proportions Figure 5. Mean, standard deviation, and minimum (Min) and maximum (Max) size of cephalothorax shield length for demographic groups of Dardanus insignis in each bay. Values with at least one letter in common on the line did not differ statistically (ANOVA; a posteriori Tukey test; P < 0.05) 21

30 Shallow water distribution of D. insignis Frameschi IF 2014 Relationship between abundance and environmental variables The RDA permutation test revealed that the observed eigenvalue for the first axis (RDA1) was significant, allowing us to reject the null hypothesis of no structure between the matrices, indicating that the patterns of association were identified (Table 4). This permutation also showed that the variation observed between the fitted scores and the scores on the space of the response variable was significant, which allows us to infer that the environmental variables explain part of the observed variation in the distribution of demographic groups (Table 4). Table 4. Summary results of Redundancy Analysis (RDA) for each demographic group of Dardanus insignis in a tropical-subtropical transition zone on the coast of Brazil. Values are correlations among the respective variables with ordination axes. Values in bold indicate the highest correlations Axes RDA1 RDA2 Eigenvalue (total inertia = 0.792) Cumulative % variation explained Species-predictor correlation Juvenile Males (JM) Juvenile Females (JF) Adult Males (AM) Adult Females (AF) Ovigerous Females (OF) Bottom Temperature (BT) Bottom Salinity (BS) % Organic Matter (OM) Mean grain size (Phi) Biodetritus fragments (BDF) Very coarse sand (VCS) Coarse sand (CS) Medium sand (MS) Fine sand (FS) Very fine sand (VFS) Silt and clay (S+C) P (Monte-Carlo permutation test) 22

31 Shallow water distribution of D. insignis Frameschi IF 2014 Correlations between environmental variables and the ordination axes showed that the coarse, medium and fine sand particle size fractions showed a positive correlation with the distribution of demographic groups. On the other hand, the mean grain size (Phi) and silt + clay adversely affected the distribution of the species (Fig. 6). According to the correlation values (Table 4), the latter variables were most important in explaining the variability in the distribution of demographic groups of D. insignis. Juveniles of both sexes were positively associated with the particle size fractions that affected axis 1 (see Table 4). Adult males and females showed no environmental specific relationship similar to the juveniles, but did show a negative relationship with the mean grain size. The distribution of ovigerous females was negatively affected by the bottom temperature. Figure 6. Biplot of the redundancy analysis (RDA) of variations in environmental variables (indicated by solid arrows) of demographic groups of Dardanus insignis (indicated by broken arrows). Refer to Table 4 for codes of each demographic group and environmental variables 23

32 Shallow water distribution of D. insignis Frameschi IF 2014 Discussion The three bays differed with respect to environmental variables. The southeastern coast of Brazil is affected by three water masses (Coastal Water - CW, Tropical Water - TW, and South Atlantic Central Water - SACW) with different distribution patterns in summer and winter (Castro Filho et al. 1987). These patterns are responsible for seasonal changes in temperature, salinity and nutrient concentration (Costa et al. 2000). According to Mahiques et al. (1998), the direction of the opening of each bay, and the presence of physical barriers make the physical characteristics act at different intensities throughout the time and space. The sediment characteristics differed among the bays, reflecting changes in the predominance of the finer sediment fractions (very fine sand, silt and clay) from south to north. These changes result from more homogeneous hydrodynamics, because of the presence of physical barriers represented by the islands of São Sebastião and Mar Virado, reflecting the formation of an area of deposition of fine sediments, especially silt, in Mar Virado Bay, in relation to Ubatumirim (Pires-Vanin et al. 1993). The results also reveal alterations in the texture of the sediment of transects according to depth, during the two study periods. According to Mahiques et al. (1998), the sediment of the inner parts of the bays is mainly composed of silt + clay, with higher organic-matter contents, due to the local hydrodynamics that allows the deposition of fine sediments in these locations. Beginning at 15 and 20 m, the influence of the open sea is stronger, with no physical obstacle and little influence from the coast and land. This leads to more homogeneous sediment, with a predominance of coarse sediments and lower organic-matter content (Soares-Gomes and Pires-Vanin 2003). According to Pires (1992), the diversity, occurrence and abundance of benthic macro-organisms are strongly related to the complexity of micro-environments. This 24

33 Shallow water distribution of D. insignis Frameschi IF 2014 relationship is determined by the composition of the substrate, which can be used for shelter, feeding site and a nutritional resource (Abele 1974). The significant numbers of D. insignis on transect Exp of UBA (first period) can be explained by the high rates of deposition of sediment and organic matter originating from the continent. According to precipitation records, rainfall was especially intense between winter 1997 and winter 1998 (CIIAGRO, 2013), causing a drastic change in the composition of the sediment from the nearest coastal regions. According to Posey et al. (1996), large amounts of rainfall altered the characteristics of the sediment, determining the presence / absence of benthic organisms, especially those which show a preference for firmer substrate. The results obtained here allowed us to establish a relationship between the abundance of the hermit crab D. insignis and the medium and coarse sand fractions. This sediment characteristic seems to limit the distribution of this species to the transects farther than 15 m from shore. The sediment also seems to account for the differential occupation of young compared to adults. According to Hazlett (1981), the different stages of ontogenetic development in hermit crabs directly affect the differential occupation of space, especially when individuals are young or when they are ovigerous (Pardo et al. 2007). Fransozo et al. (2008, 2012) suggested that species characteristic of unconsolidated substrate in the subtropical region of Brazil have higher diversity and richness during the summer, but species of decapods reach their highest abundance during the colder months of the year (autumn and winter). This pattern is consistent with the results obtained here for D. insignis, as well as those of Fernandes-Goés et al. (2005) and with the record of Branco et al. (2002) for the same species, respectively for the bays of Ubatuba and Armação do Itapocoroy in southern Brazil. This higher abundance in the colder months may be due to seasonal reproduction, which according 25

34 Shallow water distribution of D. insignis Frameschi IF 2014 to Miranda et al. (2006) occurs in the warmer months of the year (spring and summer). This breeding period coincides with the months of higher primary productivity, since the entrance of SACW in these seasons promotes nutrient enrichment in the region, increasing the available food for planktonic larvae (De Léo and Pires-Vanin 2006). The population of D. insignis studied here showed temporal and spatial oscillations in the sex ratio, always in favor of males. Similar higher abundances of males compared to females were also reported by Branco et al. (2002) for a population of D. insignis on the southern coast of Brazil, as well as for other hermit crabs including Loxopagurus loxochelis (Moreira, 1901) and Petrochirus diogenes (Linnaeus, 1758) studied by Bertini and Fransozo (1999) and Bertini et al. (2004), respectively. According to Gherardi (1991), an unequal sex ratio can be explained by several factors, including differential migration by demographic groups, ontogenetic development, growth, and mortality between the sexes. Hazlett (1981) stated that in hermit crabs, these factors are determined by an essential feature: gastropod shells. Also according to this author, sexual dimorphism favors a higher abundance of males, because they reach larger sizes. This statement can also be extended to D. insignis. Young (immatures) of this species do not show differences in growth, but as adults, males and females use energy in different ways, since upon reaching sexual maturity, females allocate energy to egg production (Abrams 1988), while males continue directing energy to somatic growth. Asakura (1995) and Hess and Bauer (2002) suggested that the reason is that larger males are more likely to win in intraspecific fights for obtaining females for copulation, as well as more appropriate gastropod shells. Environmental temperature and salinity factors had little influence on the distribution of D. insignis, since the species was most abundant on transects with wider variations of temperature and salinity. Possibly the local variations are well within the 26

35 Shallow water distribution of D. insignis Frameschi IF 2014 tolerance limit of this species. The composition of the sediment appeared to be the most important environmental characteristic affecting the distribution of D. insignis. Thus, for species that have an exclusively benthic habit, such as hermit crabs, the type of substrate seems to be essential for their occurrence, which explains the high correlation of all demographic groups of D. insignis with the mean grain size (Phi) and the granulometric fractions. The nature of the substrate may influence not only the abundance and frequency of individuals, but also the ease of burying, especially during the molting process (Rebach 1974). The type of substrate also seems to coincide with habitats that harbor a wider diversity of gastropods (Dias et al. 2011), resulting in greater availability of shells. The abundance and richness of shells is a limiting factor for the distribution and abundance of populations of hermit crabs (Childress 1972, Bertini and Fransozo 2000, Meireles et al. 2003). Because of these factors, these species rarely choose a substrate other than predominantly sand. D. insignis was found in greater abundance on transects farther from the coastline, places that are less affected by the continual environmental oscillations in coastal regions and which therefore offer greater protection and stability for hermit crabs. The decrease in numbers of crabs in the second study period can be explained by the process of migrating to deeper regions, since the sediment in the bays changed more during periods of heavy rainfall, making the sampling areas less favorable for the species. The great abundance of D. insignis in southeastern Brazil is related to a large number of variables, including (1) the highest fertility rate of all species coexisting in the study region (Miranda et al. 2006), (2) robustness in shell occupation, using a wide diversity of gastropod species (Fransozo et al. 2008), and (3) good availability of shells, an indispensable resource for rapid growth of hermit crabs (Lancaster 1990). This study allowed us to add these variables: (4) the sediment found in the region is conducive to 27

36 Shallow water distribution of D. insignis Frameschi IF 2014 the establishment of this species, and (5) males are larger and more abundant than females, favoring intra- and interspecific competition for shells (Yoshino and Goshima 2002). Additionally, due to high mortality, larval survival and settlement are critical stages in the hermit-crab life cycle; and D. insignis has the largest number of larval developmental stages among diogenids (Hebling and Mansur 1995). These have a higher survival rate compared to other species of hermit crabs from the nonconsolidated sublittoral bottom of tropical-subtropical zone on the coast of Brazil. References Abele LG (1974).Species diversity of decapod crustaceans in marine habitats. Ecology 55: Abrams PA (1988) Sexual difference in resource use in hermit crabs: consequences and causes. In: Chelazzi G, Vannini M (Eds). Behavioral Adaptations to Intertidal Life. Plenum Publishers, New York, pp Asakura A (1995). Sexual differences in life history and resource utilization by the hermit crab. Ecology 76(7): Bertini G, Fransozo A (1999) Spatial and seasonal distribution of Petrochirus diogenes (Anomura, Diogenidae) in the Ubatuba Bay, São Paulo, Brazil. Iheringia 86: Bertini G, Fransozo A (2000) Patterns of shell utilization in Petrochirus diogenes (Decapoda, Anomura, Diogenidae) in the Ubatuba Region, São Paulo, Brazil. J Crustac Biol 20(3): Bertini G, Fransozo A (2004) Bathymetric distribution of brachyuran crab (Crustacea, Decapoda) communities on coastal soft bottoms off southeastern Brazil. Mar Ecol Prog Ser 279: Bertini G, Fransozo A, Braga AA (2004) Ecological distribution and reproductive period of the hermit crab Loxopagurus loxochelis (Anomura, Diogenidae) on the northern coast of São Paulo State, Brazil. J Nat Hist 38(18): Boschi EE (2000) Species of decapod crustaceans and their distribution in the American marine zoogeographic provinces. Rev Invest Desarro Pesq 13:7 136 Branco JO, Turra A, Souto FX (2002) Population biology and growth of the hermit crab Dardanus insignis at Armação do Itapocoroy, southern Brazil. J Mar Biol Ass UK 82: Castro-Filho BM, Miranda LB, Myao SY (1987) Condições hidrográficas na plataforma continental ao largo de Ubatuba: Variações sazonais e em média escala. Bolm Inst Oceanogr 35(2):

37 Shallow water distribution of D. insignis Frameschi IF 2014 Childress JR (1972) Behavioral ecology and fitness theory in a tropical hermit crab. Ecology 3(5): CIIAGRO - Centro Integrado de Informações Agrometeorológicas. Available at: < Acceesed on: 19 Mar Costa RC, Fransozo A, Mantelatto FLM, Castro RH (2000) Occurrence of shrimp species (Crustacea: Decapoda: Natantia: Penaeidea and Caridea) in Ubatuba Bay, Ubatuba, SP, Brazil. Proc Biol Soc Wash 113(3): De Léo FC, Pires-Vanin AMS (2006) Benthic megafauna communities under the influence of the South Atlantic Central Water intrusion onto the Brazilian SE shelf: A comparison between a upwelling and a non-upwelling ecosystem. J Mar Syst 60: Dias TLP, Leo Neto LA, Alves RRN (2011) Molluscs in the marine curio and souvenir trade in NE, Brazil: species composition and implications for their conservation and management. Biodivers Conserv 20: Fernandes-Goés, LC, Fransozo A, Goés JM (2005) Population dynamics of Dardanus insignis (Saussure, 1858) (Crustacea, Anomura, Diogenidae) in the Ubatuba region, São Paulo, Brazil. Nauplius 13(2): Fisher RA (1930) The Genetical Theory of Natural Selection. Clarendon Press, Oxford Fransozo A, Bertini G, Braga AA, Negreiros-Fransozo ML (2008) Ecological aspects of hermit crabs (Crustacea, Anomura, Paguroidea) off the northern coast of São Paulo State, Brazil. Aquat Ecol 42: Fransozo A, Fernandes-Góes LC, Fransozo V, Góes JM, Cobo VJ, Teixeira GM, Gregati RA (2011) Marine anomurans (Decapoda) from the non-consolidated sublittoral bottom at the Southeastern of Brazil. Crustaceana 84(4): Fransozo A, Furlan M, Fransozo V, Bertini G, Costa RC, Fernandes-Góes LC (2012) Diversity of decapod crustaceans at the interface of unconsolidated seabed areas and rocky shores in tropical/subtropical Brazil. Afr J Mar Sci 34(3): Fransozo A, Mantelatto FL (1998) Population structure and reproductive period of the tropical hermit crab Calcinus tibicen (Decapoda: Diogenidae) in the region of Ubatuba, São Paulo, Brazil. J Crustac Biol 18(4): Fransozo A, Mantelatto FLM, Bertini G, Fernandes-Góes LC, Martinelli JM (1998) Distribution and assemblages of anomuran crustaceans in Ubatuba Bay, North coast of São Paulo State, Brazil. Acta Biol Venez 18:17 25 Furlan M, Castilho AL, Fernandes-Góes LC, Fransozo V, Bertini G, Costa RC (2013) Effect of environmental factors on the abundance of decapod crustaceans from soft bottoms off southeastern Brazil. An Acad Bras Cienc 85:83 92 Gherardi F (1991) Relative growth, population structure and shell utilization of the hermit crab Clibanarius erythropus in the Mediterranean. Oebalia 17: Håkanson L, Jansson M (1983) Principles of Lake Sedimentology. Springer-Verlag, Berlin Hazlett BA (1981) The behavioral ecology of hermit crabs. Annu Rev Ecol Syst 12(1):

38 Shallow water distribution of D. insignis Frameschi IF 2014 Hebling NJ, Mansur CB (1995) Desenvolvimento larval de Dardanus insignis (Saussure) (Crustacea, Decapoda, Diogenidae), em laboratório. Rev Bras Zool 12(3): Hess GS, Bauer RT (2002) Spermatophore transfer in the hermit crab Clibanarius vittatus (Crustacea, Anomura, Diogenidae). J Morphol 253: Peres-Neto PR, Jackson DA, Somers KM (2005) How many principal components? Stopping rules for determining the number of non-trivial axes revisited. Comput Stat Data An 49(4): Jongman R, ter Braak CJF, Van Tongeren O (1995) Data Analysis in Community and Landscape Ecology. Cambridge University Press, Cambridge Lancaster I, (1988) Pagurus bernhardus (L.) an introduction to the natural history of hermit crabs. Field Studies 7(1): Lancaster I, (1990) Reproduction and life history strategy of the hermit crab Pagurus bernhardus. J Mar Biol Ass UK 70: Legendre P, Legendre L (1998) Numerical Ecology. Elsevier, New York Mahiques MM, Tessler MG, Furtado VV (1998) Characterization of energy gradient in enclosed bays of Ubatuba region, South-eastern Brazil. Est Coast Shelf Sci 47: Mahiques MM (1995) Dinâmica sedimentar atual nas enseadas da região de Ubatuba, Estado de São Paulo. Bolm Inst Oceanogr 43(2): Mantelatto FLM, Fransozo A (1999) Characterization of the physical and chemical parameters of Ubatuba Bay, northern coast of São Paulo State, Brazil. Rev Bras Biol 59:23 31 Mantelatto FLM, Fransozo A (2000) Brachyuran community in Ubatuba Bay, Northern Coast of São Paulo State, Brazil. J Shellfish Res 19(2): Mantelatto FL, Garcia RB (2002) Hermit crab fauna from the infralittoral area of Anchieta Island (Ubatuba, Brazil). In: Briones EE, Alvarez F (eds), Modern Approaches to the Study of Crustacea. Kluwer Academic/Plenum Publishers, New York, pp Mantelatto, FLM, Martinelli JM, Fransozo A (2004) Temporal-spatial distribution of the hermit crab Loxopagurus loxochelis (Decapoda, Diogenidae) from Ubatuba Bay, São Paulo, Brazil. Rev Biol Trop 52(1):47 55 Mccune B, Grace JB (2002) Analysis of ecological communities. MJM Software Design, Gleneden Beach Mccune B, Mefford MJ (2011) PC-ORD. Multivariate analysis of ecological data. Version 6.0. MjM Software Design, Gleneden Beach Meireles, AL, Biagi R, Mantelatto FL (2003) Gastropod shell availability as a potential resource for the hermit crab infralittoral fauna of Anchieta Island (SP), Brazil. Nauplius 11(2): Melo GAS (1999) Manual de Identificação dos Crustacea Decapoda do Litoral Brasileiro: Anomura, Thalassinidea, Palinuridea, Astacidea. Editora Plêiade, São Paulo Maliao RJ, Turingan RG, Lin J (2008) Phase-shift in coral reef communities in the Florida Keys National Marine Sanctuary (FKNMS), USA. Mar Biol 154:

39 Shallow water distribution of D. insignis Frameschi IF 2014 Miranda I, Meireles AL, Biagi R, Mantelatto FLM (2006) Is the abundance of the red brocade hermit crab Dardanus insignis (Decapoda: Anomura: Diogenidae) in the infralittoral region of southern Brazil determined by reproductive potential? Crustac Res 6:45 55 Negreiros-Fransozo ML, Fransozo A, Mantelatto FLM, Pinheiro MAA, Santos S (1997) Anomuran species (Crustacea, Decapoda) and their ecological distribution at Fortaleza Bay sublittoral, Ubatuba, São Paulo, Brazil. Iheringia 83: Nenadic O, Greenacre M (2007) Correspondence analysis in R, with two- and three dimensional graphics: The ca package. J Stat Softw 20(3):1 13 Pallas A, García-Calvo B, Corgos A, Bernárdez C, Freire J (2006) Distribution and habitat use patterns of benthic decapod crustaceans in shallow waters: a comparative approach. Mar Ecol Prog Ser 324: Pardo ML, Piraud F, Mantelatto FL, Ojeda PF (2007) Ontogenetic pattern of resource use by the tiny hermit crab Pagurus villosus (Paguridae) from the temperate Chilean coast. J Exp Mar Biol Ecol 353:68 79 Peck JE (2010) Multivariate analysis for community ecologists: step-by-step using PC- ORD. MjM Software Design, Gleneden Beach Pires AMS (1992) Structure and dynamics of benthic megafauna on the continental shelf offshore of Ubatuba, Southeastern Brazil. Mar Ecol Prog Ser 86:63 76 Pires-Vanin AMS, Rossi-Wongtschowski CLB, Aidar E, Mesquita HSL, Soares LSH, Katsuragawa M, Matsuura I (1993) Estrutura e função do ecossistema de plataforma continental do Atlântico Sul brasileiro: síntese dos resultados. Publ Esp Inst Oceanogr 10: Posey M, Lindberg W, Alphin T, Vose F (1996) Influence of storm disturbance on an offshore benthic community. B Mar Sci 59: Rebach S (1974) Burying behavior in relation to substrate and temperature in the hermit crab, Pagurus longicarpus. Ecology 55: Sant Anna BS, Zangrande CM, Reigada, ALD, Severino-Rodrigues E (2006) Spatial distribution and shell utilization in three sympatric hermit crabs at non-consolidated sublittoral of estuarine-bay complex in São Vicente, São Paulo, Brazil. Rev Biol Mar Oceanogr 41(2): Santos MFL, Pires-Vanin AMS (2004) Structure and dynamics of the macrobenthic communities of Ubatuba Bay, Southeastern Brazilian coast. Braz J Oceanogr 52(1):59 73 Shapiro SS, Wilk MB (1965) An analysis of variance for normality (complete samples). Biometrika 52: Soares-Gomes A, Pires-Vanin AMS (2003) Padrões de abundância, riqueza e diversidade de moluscos bivalves na plataforma continental ao largo de Ubatuba, São Paulo, Brasil: uma comparação metodológica. Rev Bras Zool 20: Sumida PY, Pires-Vanin AMS (1997) Benthic associations of the shelfbreak and upper slope off Ubatuba-SP, South-eastern Brazil. Estuar Coast Shelf Sci 44(6): Ter Braak CJF, (1986) Canonical correspondence analysis: a new eigen-vector technique for multivariate direct gradient analysis. Ecology 67:

40 Shallow water distribution of D. insignis Frameschi IF 2014 Tucker M (1988) Techniques in Sedimentology. Blackwell Scientific Publications, Boston Van Hoey GV, Degraer S, Vincx M (2004) Macrobenthic community structure of softbottom sediments at the Belgian continental shelf. Estuar Coast Shelf Sci 59: Wentworth WC (1922) Grade and class terms for clastic sediments. J Geol 30: Wilson K, Hardy ICW (2002) Statistical analysis of sex ratios: an introduction. In: Hardy ICW (ed), Sex Ratios: Concepts and Research Methods. Cambridge, University Press Cambridge, pp Yoshino K, Goshima S (2002) Sexual dominance in hermit crab shell fights: asymmetries in owner-intruder status, crab size and resource value between sexes. J Ethol 20:63 69 Zar JH (1999) Biostatistical Analysis. Prentice-Hall, New Jersey 32

41 Capítulo II Life-history traits of the red brocade hermit crab Dardanus insignis on the subtropical Brazilian coast

42 Life-history traits of D. insignis Frameschi IF 2014 Abstract: We evaluated the population characteristics of Dardanus insignis in this study focusing the reproductive period, juvenile recruitment, sexual maturity, growth and longevity. Samples were collected monthly over two years (1998 and 1999), by trawling, in a subtropical region of Brazil. The hermit crabs were counted by demographic group, weighed (W) and measured for shield length (CSL), and their gonadal stage was identified under a stereomicroscope. A total of 3169 hermit crabs were captured (1838 males and 1331 females). The ovigerous females were found from September to March; juvenile recruitment occurred throughout the year, peaking in the summer. Males reached sexual maturity at larger sizes (CSL50 = 4.4 mm) than females (CSL50 = 4.1 mm). Longevity was estimated at 4.75 years for males and 4.08 years for females. Seasonal reproductive strategy as well as to fundamental events for the establishment and maintenance of hermit crabs, such as sexual maturity at similar sizes for males and females, continuous recruitment and differential growth Key words: growth, gonadal stage, reproduction, sexual dimorphism, Paguroidea, South Atlantic coast. 34

43 Life-history traits of D. insignis Frameschi IF 2014 Introduction The subtropical region of the Brazilian coast has a wealth of hermit crabs, with 26 species recorded (Nucci & Melo 2007). Of the nine species that coexist on subtidal unconsolidated bottoms, the hermit crab Dardanus insignis (Saussure 1858) is the most abundant (Fransozo et al. 2008; 2011; 2012). Investigations of the life history of this species are important for conservation, because the population has been continually impacted by shrimp fishing (Keunecke et al. 2007; Batista et al. 2009; Fransozo et al. 2012) and commercial exploitation in the aquarium trade (Calado et al. 2003; Gasparini et al. 2005; Matos-Caraballo & Mercado-Porrata 2007). Identification of longevity, age and size at sexual maturity, reproductive period, and juvenile recruitment are essential for understanding the timing of the life history strategy of a species, which governs other aspects of population biology. The model developed by von Bertalanffy (1938) is the most commonly accepted to estimate age, growth in size and weight of crustaceans (Pauly et al. 1984; D Incao & Fonseca 2000; Pinheiro et al. 2005; Leite Jr. & Petrere Jr. 2006; Diele & Koch 2010). This model was used to assess the growth of Diogenes pugilator Roux, 1829 and Pagurus brevidactylus Stimpson, 1859 by Manjón-Cabeza and García-Raso (1998) and Mantelatto et al. (2005), respectively. These studies found differences in growth between the sexes. The differential growth between the sexes leads to different requirements for shell occupation, suggesting that this component modulates the pace at which development occurs in hermit crabs (Hazlett 1981; Wada et al. 1997). According Bertness (1981a), this resource regulated trade-off between growth and reproduction of the hermit crabs plasticity in important life-history traits. This author postulated the main limitations shells of gastropods can bring to hermits: (1) the frequency of reproduction, which increases with reduced shell supply; (2) the minimum size of reproduction, which 35

44 Life-history traits of D. insignis Frameschi IF 2014 decreases with decreasing shell availability; (3) investment into growth at the cost of decreased allocation to immediate reproduction, which decreases with decreasing shell adequacy, and (4) reproductive effort (as measured by clutch size), which increases with decreasing shell quality Hartnoll & Gould (1988) and Lancaster (1988) stated that the age and size at which gonadal maturation occurs are important factors to determine the reproductive capacity, since an estimated sexual maturity is associated with the development of the gonads (López-Greco & Rodriguez 1999). The period of juvenile recruitment may be controlled by these factors, but can also be influenced by physical and chemical attributes of the water masses, since the life cycle of D. insignis includes a planktonic stage, wich consists of eight stages of zoea, characterized as the most numerous among Diogenidae known (Hebling & Mansur 1995) Reproductive patterns are assumed adaptations that will maximize fitness of a species over evolutionary time (Yoshino et al. 2002). According with Litulo (2004), hermit crabs may display continuous (with or without peaks) or seasonal reproductive patterns regardless of the family and geographical region. The temporal segregation in appearance of ovigerous females and larvae among sympatric species has been well documented. This phenomenon is considered to be effective in reducing intra and interspecific competition (Reese 1968; Wada et al. 2000). For the purpose of combining knowledge of the reproductive biology and growth of a hermit crab, this study determined the period of reproduction and recruitment, estimating sexual maturity and assessing the growth and longevity of D. insignis in southeastern Brazil. 36

45 Life-history traits of D. insignis Frameschi IF 2014 Materials and methods Hermit crabs were collected monthly from January 1998 to December 1999 in Ubatumirim, Ubatuba and Mar Virado bays in the Ubatuba region, northern coast of the State of São Paulo, Brazil. A shrimp-fishing boat equipped with double-rig nets (mesh size 20 mm and 15 mm in the cod end) was used for trawling. In each trawl, the nets were deployed for 2 km over a period of 30 min, covering an area of approximately 18,000 m 2. After each trawl, all collected material was inspected, frozen, and transported to the laboratory, where hermit crabs were identified according to Melo (1999). Individuals of D. insignis were counted, manually removed from their shells, sexed based on the position of the gonopores (on the coxa of either the third or the fifth pair of pereiopods in females and males, respectively), weighed on a precision balance (0.01 g) and had their cephalothoracic shield length (CSL) measured with a caliper (0.10 mm). To determine the gonadal development stages for both sexes, the soft abdomen was dissected and the gonads observed under a stereomicroscope. Based on the size, shape and color, four stages of gonadal development were used for both males and females (Tab. 1). The mean CSL in each size class was plotted on a graph, which was fitted by the least-squares method (Vazzoler 1996; Bertini et al. 2010) to a sigmoid curve given by 1 the logarithmic equation: Y r CSL CSL50 1 e where CSL50 = cephalothoracic shield length at which 50% individuals attained sexual maturity and r = the slope of the curve. 37

46 Life-history traits of D. insignis Frameschi IF 2014 Table 1. Developmental stages for male and female gonads of Dardanus insignis (modified from Lancaster, 1988) Stage Male Female Immature Rudimentary Developing Developed Gonad thin and translucent, undifferentiated, no obvious coloration Gonad initial stages with two small white ducts Initial filament winding of white/pale coloration Strong winding of the testis with dominant visible organ of white/pale coloration and white vas deferens Gonad not developed, the ovaries appear as two slender whitish filaments Maturation beginning, the ovaries conspicuous are small and reddish Ovaries are dark red. Is visibly internal organ dominant The reproductive period was determined from the percentage of mature females (developed gonads + ovigerous females) in relation to the total number of adult females. The occurrence of juveniles (individuals of both sexes characterized with immature gonads) determined the recruitment in the population (Garcia & Mantelatto 2001; Martinelli et al. 2002). To compare the CSL between the sexes in different stages of gonadal development, the Mann-Whitney test (Zar 1996) was used since the data did not satisfy the assumptions of normality. The growth of the individuals of the population was estimated for males and females separately through monthly monitoring of the modal displacement (adjustment method using non-linear model). Growth parameters, k and t0 were fitted to our dataset using the von Bertalanffy (1938) growth curve: CSLt = CSL (1-exp -k(t-t0) ), where CSLt is the mean CSL estimated at age t, k is a growth constant defining how rapidly CSL is reached, and t0 is the theoretical age at which the crabs would have zero CSL. For modal analysis, the data were grouped into size classes of 1.8 mm (CSL). The modal peak was detected using the software PeakFit v.4 (SPSS Inc., Chicago). Frequency data were smoothed to remove noise using an automated procedure in PeakFit, where and optimum smoothing level, based on least square polynomial fitting, 38

47 Life-history traits of D. insignis Frameschi IF 2014 is determined automatically, as described in detail by Lee et al. (2007). A statistical summary of each monthly adjustment was analyzed, consisting of the coefficient of determination (R 2 ), the degrees of freedom (DF) and the calculated critical value of F (Fonseca & D Incao, 2003). Adjustments were accepted only when the observed value of F was higher than the calculated critical F and the coefficient of determination was greater than 0.9. Where this did not occur, the automatically detected modal peaks were carefully analyzed for partial overlap with other peaks in the same modal distribution. By mechanical elimination, the adjusted results were compared with the initial (complete) dataset, verifying the acceptance of modal peaks through the calculation of critical F. Then through a dispersion graph of the modal peaks vs. age (time), the growth rate of the cohorts was determined. The values for the growth constant (k) and the theoretical age (t0) were tested in various nuances by trial and error to find the possible cohorts in the population. Growth parameters found for each cohort were calculated through the tool "Solver" in Microsoft Excel software for routine non-linear fit GRG2 (Generalized Reduced Gradient), which minimizes the sums of residues between the lengths observed in the field and those calculated by the model of von Bertalanffy (1938), varying the equation parameters (k and t0). Only cohorts were accepted that showed resembling growth, including longevity, growth constant (k) and asymptotic length (CSL ). Finally, the similar growth cohorts were used for calculating a mean growth curve. The mean curves obtained for males and females were analyzed in a length-weight relationship (Y=a.X b ), and then, were apllied to the weight growth curve model proposed by Beverton (1954): Wt = W (1-exp -k(t-t0) ) b where Wt is the weight at time t, and b is the coefficient of the regression function between weight and shield length (Ricker 1973). The growth in weight was calculated for each sex, where W is the 39

48 Life-history traits of D. insignis Frameschi IF 2014 maximum weight. Longevity (in years) was estimated by the inverse equation of Bertalanffy as modified by D Incao & Fonseca (1999): Tmax = (0-(1/k)Ln(1- CSLt/CSL ), where Tmax is the longevity. The mean curves obtained for males and females were statistically analyzed to compare the growth in size and weight between the sexes. For these analyses, we used the F test (hypothesis test) with a significance level of 5% (Cerrato 1990). Results A total of 3169 hermit crabs were captured, including 1838 males and 1331 females. The gonad observations indicated that gonadal sexual maturity occurs between 3.8 and 5.5 mm (CSL) for both sexes (Fig. 1), since this interval comprises the transition of immature individuals to individuals with rudimentary gonads. Figure 1. Size-frequency distribution of Dardanus insignis, based on gonadal development stages (IM = immature, RU = rudimentary, ED = developing, DE = developed, OF = ovigerous females) Regarding the mean size of hermit crabs in each demographic group at different gonadal stages, males were larger than females when rudimentary (U = 35.0; p < 0.01), 40

49 Life-history traits of D. insignis Frameschi IF 2014 developing (U = 10.8; p < 0.00) and developed (U = 35.5; p < 0.00). Immature males and females did not differ in size (U = 34.2; p > 0.05) (Table 2). Table 2. Cephalothoracic shield length (mm) of males and females of Dardanus insignis in each stage of the gonadal cycle. (n = number of individuals; Min = minimum; Max = maximum; SD = standard deviation) Males Gonadal stages n Min Max Mean SD Immature Rudimentary Developing Developed Females Immature Rudimentary Developing Developed Ovigerous The logarithmic curve constructed based on the morphological data for maturity, based on cephalothoracic shield length (CSL), shows the size at which 50% of the individuals reach sexual maturity. This curve indicated adjustment and significance of estimated values of 4.4 mm CSL for males (Fig. 2a) and 4.1 mm CSL for females (Fig. 2b). Figure. 2. Adjustment of the logistic equation indicating the cephalothoracic shield length (CSL) for (a) males and (b) females of Dardanus insignis, where 50% of the hermit crabs are mature according to the analyses of gonadal development 41

50 Life-history traits of D. insignis Frameschi IF 2014 Males with developed gonads were recorded throughout the study period. Ovigerous females occurred from September to December, when they comprised approximately 85% of ovigerous females collected, and January to March in lower percentages, averaging approximately 15% in both study periods (Fig. 3). The increasing proportion of ovigerous females, preceded by a large number of females with developed gonads, revealed that the intense phase of the reproductive period begins in midwinter (August), i.e., is seasonal (Fig. 3). Juvenile recruitment was continuous, with a peak in February of the first year of study (Fig. 4); however there was no perceptible peak in the entrance of juveniles during the second period (Fig. 4). Regarding growth, seven cohorts of males and five cohorts of females coexisted during the two years (Fig. 4). Males reached a greater asymptotic length (CSL = mm) and weight (W = g), as well as a higher growth constant (k = /month) than the values found for females (CSL = mm, W = g; k = /month) (Fig. 5a). Males and females reached morphological sexual maturity, based on macroscopic analysis of the gonads and CSL50, at 160 and 250 days respectively. During the first year of life (12 months), the weight gain was the same for both sexes, although the males grew much larger (Fig. 5b). Females reached their asymptotic maximum length in a shorter time than males (51.20 and months, respectively). 42

51 Life-history traits of D. insignis Frameschi IF 2014 Figure. 3. Monthly variation in percentage of females of Dardanus insignis in each stage of gonad development for each year of the study: (a) first year, (b) second year. Number above each column indicates number of hermit crabs analyzed in each month. Percentages of immatures under solid (males) and dotted (females) lines are not added to the monthly stack columns, for better visualization of the reproductive dynamics 43

52 Life-history traits of D. insignis Frameschi IF 2014 Figure. 4. Frequency distribution of demographic groups of Dardanus insignis by month and size class (mm) (TJ = total juveniles, M = adult males, F = adult females, OF = ovigerous females). The circled numbers above the columns indicate temporal cohorts used in the analyses of growth for males (filled in white) and for females (filled in black) As regards weight gain, both sexes behaved similarly over time; however, after the first year of life, the males gained weight much more quickly than females. The longevity estimated for D. insignis was approximately 57 months (4.75 years) for males and 49 months (4.08 years) for females. The estimated growth curves for males and females showed significant differences in size (Fcalculated = > Fcritical 4.08, p < 0.05) and weight (Fcalculated = > Fcritical 2.90, p < 0.05). 44

53 Life-history traits of D. insignis Frameschi IF 2014 Figure. 5. Dardanus insignis. (a) Curves for increase in length for males (CSLt = 24.71*(1-e( *(t ))) and females (CSLt = 17.90*(1-e( *(t ))), (b) increase in weight for males (Wt = 70.83*(1 -exp( *(t ))) 5.54 and females (Wt = 26.19*(1-exp( *(t ))) 4.47 Discussion Combining the criteria for morphological and physiological maturity of the hermit crabs, it was possible to obtain an interval for the estimated population size at the beginning of the reproductive process. The reproduction of D. insignis begin after the coldest months of the year, peaking in mid-spring. However, juveniles entered the population during the entire study period, a strategy that may minimize competition for 45

54 Life-history traits of D. insignis Frameschi IF 2014 shells. The longevity of the species was estimated at between 49 and 57 months, with pronounced growth up to approximately 16 months. After this age was noticed a reduction in the abundance of the population. The size of the smallest ovigerous female has been used to establish the maximum size of juveniles (Fransozo & Mantelatto 1998; Garcia & Mantelatto 2001; Martinelli et al. 2002; Litulo 2005). Use of this criterion may overestimate the size at maturity, through excluding individuals that might not be juveniles. For the hermit D. insignis, males and females were estimated to mature at around 4.1 mm and 4.4 mm CSL, respectively; whereas the size of the smallest ovigerous female found was 5.0 mm. A similar effect was also observed for other hermits, such as Petrochirus diogenes and Loxopagurus loxochelis, in which the size of the smallest ovigerous females was much larger than that estimated for maturity based on gonadal development (Fransozo & Bertini 2002; Bertini et al. 2004). For majority of hermit crab populations a shortage of adequate shells may be a common problem. According Lancaster (1988) this limitation may be quantitative (insufficient shells to go around) or qualitative (plenty of shells, but of the wrong size, damaged or buried), or a mixture of both, but individuals forced to occupy sub-optimal shells will inevitably be at a disadvantage. When hermit crabs do not have access to new shells, which are necessary for growth, reproductive success is harmed, due to reducing the hermit crab size at sexual maturity and its potential clutch size (Bertness 1981b). This fact main explain the overlapping of individuals with different sexual characteristics (ie, immatures and ovigerous females) on the distribution in second size classes ( mm). Hermit crabs of subtropical regions may show two patterns of reproductive period: continuous with peaks in some months of the year and seasonal with potentially reproductive females occurring only part of the year (Table 3). Other studies, based on 46

55 Life-history traits of D. insignis Frameschi IF 2014 the presence of ovigerous females, showed that D. insignis reproduces from September to January (Table 3). Table 3. Reproductive patterns and peak months of ovigerous females of hermit crab species studied in the subtropical region of Brazil. Present study highlighted in bold Species Peak Reproduction Author Loxopagurus loxochelis Jul-Sep continuous Martinelli et al Jul-Sep continuous Bertini et al Clibanarius antillensis Feb-May continuous Turra & Leite 2000 Paguristes erythrops Oct-Dec continuous Garcia & Mantelatto 2001 Pagurus exilis Jul-Dec continuous Terossi et al Pagurus criniticornis Dez-Mar continuous Mantelatto et al Pagurus brevidactylus Jul-Dec continuous Mantelatto et al Petrochirus diogenes Sep-Apr seasonal Bertini & Fransozo 2002 Calcinus tibicen Nov-Mar seasonal Fransozo & Mantelatto 1998 Clibanarius sclopetarius Feb-May seasonal Turra & Leite 2000 Apr-Oct seasonal Clibanarius vittatus Oct-Dec seasonal Santa Anna et al Sep-Mar seasonal Branco et al Dardanus insignis Sep-Mar seasonal Fernandes-Goés et al Sep-Jan seasonal Miranda et al Sep-Mar seasonal Present study Isocheles sawayai Oct-Mar seasonal Fantucci et al Our data indicate that the reproductive period of females potentially begins in August, when females with developed gonads appear, with a gradual increase of ovigerous females until October, when they reach a peak of abundance. Temporal variations in the occurrence of ovigerous females and larval stages contribute to the reduction of inter and intraspecific megalopa competition for food and for the gastropod shells especially when they coexist with many other species of hermit crabs that use the same resource (Reese 1968). In the study region, nine species live in sympatry with D. insignis (Fransozo et al. 2008; 2012). According to Negreiros-Fransozo et al. (1992), the seasonal reproduction of Paguristes tortugae Schmitt, 1933, which occurs during the spring and summer, correlates with to increased plankton productivity and the high temperatures sped up the metamorphosis process, which in Ubatuba is caused by the influx of the South Atlantic Central Water (SACW). This statement is supported by the 47

56 Life-history traits of D. insignis Frameschi IF 2014 study of De Léo & Pires-Vanin (2006), who stated that food for zooplankton becomes more available during the spring and summer. In agreement with these statements, we observed larger numbers of juveniles during the summer of first year, even with continuous recruitment. The continuous influx of juveniles throughout the year in species of hermit crabs that breed seasonally can be attributed to the difficulty of finding new shells, which can slow the growth of these juveniles (Hazlett 1981); or through a supply of larvae from other regions, carried on ocean currents. Increases in hermit crab population densities can quickly follow local increases in gastropod shells numbers, and the value for the mean body size of an entire population can increase if the hermit crabs are given access to shells larger than those usually available to them (Drapkin, 1963). Studies of shell occupation by hermit crabs in Ubatuba have found that the local populations of hermit crabs compete more intensely for smaller shells, and are thus able eventually to reach their maximum individual size (Bertini & Fransozo 2000; Ayres- Peres et al. 2012). Besides the availability of shells, the different requirements of male and female crabs should be considered (Hazlett et al. 2005). Sexual dimorphism is a characteristic of hermit crabs in this region (Fransozo & Mantelatto 1998; Bertini & Fransozo 2002; Bertini et al. 2004; Mantellato et al. 2005), including D. insignis (Branco et al. 2002; Fernandes-Goés et al. 2005). Therefore, data for the sexes should not be combined in this type of analysis. For D. insignis, the growth constant (k) was different for each sex, as also in C. vittatus and P. brevidactylus studied by Sant Anna et al. (2008) and Mantellato et al. (2005), respectively. In addition, the maximum size and weight attained by each sex are also different (Table 4). 48

57 Life-history traits of D. insignis Frameschi IF 2014 Table 4. Parameters of the von Bertalanffy growth curve (CSL = asymptotic size (mm), W = asymptotic weight; k = growth constant, Long = longevity) used for hermit-crab populations. n.a. = not evaluated. Present study highlighted in bold Species Sex CSL (mm) W (g) k (annual) Life (months) Authors Cestopagurus timidus n.a 3.25 n.a Manjón-Cabeza & García-Raso 1994 Clibanarius antillensis n.a 7.39 n.a Clibanarius esclopetarius n.a n.a Turra & Leite 2000 Clibanarius vittatus n.a n.a Clibanarius vittatus n.a n.a Sant Anna et al Dardanus insignis n.a n.a Branco et al Dardanus insignis Present study n.a Diogenes pugilator Manjón-Cabeza & n.a García-Raso 1998 Pagurus brevidactylus Mantelatto et al The values of the constant k found for D. insignis indicate that this species grows faster than other species with known growth rates (Table 4). The difference between the growth constant reflects the time at which these animals reach their maximum size, since males allocate more energy to somatic growth throughout their lives, unlike females, which grow more rapidly until they reach sexual maturity and then invest more energy in reproduction (Lancaster 1988; Hartnoll 1982; 1985). The data for D. insignis indicate that even after these crabs reach their maximum size, both sexes continue to gain weight. Mantellato et al. (2005) found a similar pattern for the growth of P. brevidactylus. The estimated longevity of D. insignis also differed between the sexes. Similar differences have been reported for other decapods, such as brachyurans (Flores & Negreiros-Fransozo 1999; Pinheiro & Hattori 2006), other anomurans such as species of Aegla (Silva-Castiglioni et al. 2006; Boss Jr. et al. 2006) and porcellanid crabs (Baeza et al. 2013). Our data also indicated that the longevity of D. insignis increases with the 49

58 Life-history traits of D. insignis Frameschi IF 2014 largest asymptotic size reached by each sex, as also found for other hermit-crab species (Table 3). Most studies have found that males show greater longevity than females. The exception is the hermit C. vitattus, in which the shorter average life span of the males was attributed to their more-intense competition for shells (Sant Anna et al. 2008). This result can also be explained by the type of environment, considering that hermit crabs that inhabit intertidal areas are subject to greater environmental pressures compared to hermit crabs living on subtidal unconsolidated bottoms (Turra & Leite 2001; 2002). The longevity of D. insignis found here was greater than the span of 47 months estimated by Branco et al. (2002), for males and females combined. A similar difference in longevity estimated for the sexes together and separately was also recorded for the hermit crab C. vittatus: Sant Anna et al. (2008) analyzed the sexes separately and found greater longevity than did Turra & Leite (2000), who did not differentiate the sexes in their analyses. The coexistence with nine other hermit crab species might promote some interference in population characteristic (e.g. shell availability, recruitment, monthly distribution, and reproductive period), aiming to minimize inter-specific competition, and therefore influencing the life history of this population. This study showed that the high abundance of D. insignis relative to other hermit crabs (Fransozo et al. 2008; 2011; 2012) may be attributed to its seasonal reproductive strategy as well as to fundamental events for the establishment and maintenance of hermit crabs, such as sexual maturity at similar sizes for males and females, continuous recruitment and differential growth. Concluding that D. insignis is a specie highly adapted to the environment where it lives, which offers the necessary conditions to adults for its growth and reproduction. 50

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68 Capítulo III Traços da história de vida do ermitão endêmico do Atlântico Sul Loxopagurus loxochelis (Anomura: Paguroidea) em águas rasas da zona de transição tropical-subtropical na costa brasileira

69 Traços da história de vida de L. loxochelis Frameschi IF 2014 Resumo: Foram avaliadas as características da história de vida de Loxopagurus loxochelis provenientes de uma zona de transição tropical-subtropical com foco em sua distribuição espaço-temporal, estrutura populacional, maturidade sexual, período reprodutivo, razão sexual, crescimento, longevidade e relações com variáveis ambientais. Amostragens biológicas e ambientais foram realizadas mensalmente, por dois anos, em três ensedas. Quatro transectos paralelos à linha de costa (5, 10, 15 e 20 m de profundidade), um transecto protegido da ação de ondas e um em área mais exposta foram levados em consideração. Foram capturados 1823 indivíduos, 838 em Ubatuba, 704 em Mar Virado e 281 em Ubatumirim. A proporção entre os sexos favoreceu os machos. O período reprodutivo foi caracterizando como contínuo, com pico durante o inverno. A maturidade sexual foi estimada 3.1 mm para os machos e 3.0 mm para as fêmeas. As curvas de crescimento em comprimento e peso foram diferentes para machos e fêmeas, indicando uma longevidade de 38 meses para os machos e 26.8 meses para as fêmeas. Os locais de estudo diferiram em diversos fatores ambientais, e a análise de redundância revelou que tais características explicaram 87.4% da variação na abundância dos grupos demográficos de L. loxochelis. Composição do substrato e temperatura foram as variáveis determinantes para ocorrência da espécie, justificando a maior abundância durante o inverno, principalmente na profundidade dos 20 metros. Estes resultados permitem concluir que a abundância de L. loxochelis é decorrente de uma estratégia de vida diferenciada em relação aos demais ermitões coexistentes, abrangendo características que propiciam o estabelecimento e a continuidade das populações do ermitão endêmico do atlântico sul na região estudada. Palavras-chave: Diogenidae; Análises multivariadas; von Bertalanfy; População, Reprodução; Proporção sexual; Distribuição ecológica; 61

70 Traços da história de vida de L. loxochelis Frameschi IF 2014 Introdução A costa sul e sudeste do Brasil é uma área de transição hidrológica e faunística (Boschi, 2000) que abriga uma mistura de faunas provenientes de regiões tropicais, subtropicais e subantárticas (Sumida & Pires-Vanin, 1997). Dessa fauna, poucas espécies de crustáceos são endêmicas (Melo, 1999), sendo Loxopagurus loxochelis (Moreira, 1901) uma delas (Rieger, 1997; Nucci & Melo, 2007). Tal ermitão é um dos mais representativos na costa do Atlântico Sul, pertence a um gênero monotípico e ocorre no Brasil (da Bahia ao Rio Grande do Sul), Uruguai e Argentina (Melo, 1999). Na região sudeste do Brasil, seu limite norte de distribuição (Mantelatto et al. 2004), coexiste com mais 13 espécies de ermitões do sublitoral não-consolidado, e representa a segunda espécie mais abundante desse ambiente (Fransozo et al. 1998, 2008, 2011, 2012; Ayres- Peres et al. 2008). Em decorrência dessa expressiva abundância, diversos estudos ecológicos sobre ermitões tiveram como foco a espécie L. loxochelis (Martinelli & Mantelatto 1999; Mantelatto & Martinelli 2001; Martinelli et al. 2002; Bertini et al. 2004; Mantelatto et al. 2004; Biagi et al. 2006; Ayres-Peres & Mantelatto 2008a; Ayres-Peres et al. 2008; Carranza et al. 2008; Torati & Mantelatto 2008; Ayres-Peres et al. 2012; Frameschi et al. 2013). Tais estudos auxiliam de forma direta ou indireta na identificação de padrões que são modificados por estratégias que visam a obtenção do fitness populacional em regiões que são constantemente alteradas. Uma dessas alterações do ambiente pode ser decorrente da pesca camaroeira, que segundo Wassenberg & Hill (1989), promove alterações no sedimento que perturbam a comunidade bentônica, afetando principalmente os crustáceos, elasmobrânquios e cefalópodes. Além da intensa pesca de arrasto (FAO, 2012), o litoral do sudeste brasileiro também é fortemente afetado pelo turismo, urbanização e fisiografia da região, onde a intensa formação de 62

71 Traços da história de vida de L. loxochelis Frameschi IF 2014 enseadas limita a dispersão de elementos tóxicos em comparação ao mar aberto (Burone & Pires-Vanin, 2006), afetando diretamente espécies que habitam as águas rasas costeiras. Um estudo recente de Andrade et al. (2013) revelou uma plasticidade nos padrões reprodutivos do siri Arenaeus cribrarius (Lamarck, 1818) frente às modificações do ambiente que ocorreram na região sudeste do Brasil. Para afirmar tal modelagem, os autores supracitados utilizaram, além do período reprodutivo, uma análise das coortes de crescimento. Todavia, o modelo desenvolvido por von Bertalanffy (1938) é a técnica mais aceita para estimar a idade, o crescimento em tamanho e em peso, bem como a longevidade de crustáceos decápodos (Pauly et al., 1984; D Incao & Fonseca, 1999; Pinheiro et al., 2005; Leite Jr. & Petrere Jr., 2006; Diele & Koch, 2010). Tais informações, aliadas à estimativa do início da maturidade sexual, são importantes fatores na determinação da estratégia reprodutiva e permanência da espécie no ambiente (Andrade et al. 2013). Tomando como verdade que populações animais, principalmente às que apresentam endemismo, podem facilmente modificar seus padrões adaptativos para conservação da espécie (Stearns, 1989), este estudo objetivou investigar características da história de vida do ermitão L. loxochelis e suas relações com variáveis ambientais por meio de modelos matemáticos recentes e abordagens estatísticas multivariadas. Para tanto, foram avaliados: (a) variação espaço-temporal na abundância e razão sexual; (b) período reprodutivo e maturidade sexual; (c) crescimento em tamanho e peso; (d) longevidade; e (e) características ambientais de três enseadas do sudeste brasileiro em diferentes profundidades. 63

72 Traços da história de vida de L. loxochelis Frameschi IF 2014 Material e Métodos Área de estudo A porção tropical/subtropical da costa brasileira a Serra do Mar se estende para a frente sobre o Oceano Atlântico, abrangendo estreitas planícies costeiras em comparação com aqueles encontrados ao longo da costa sul do Estado de São Paulo. O litoral norte é marcadamente sinuoso, formando várias enseadas, que apresentam algumas características típicas de ambientes semi-confinados. A área de estudo compreendeu três enseadas (Ubatumirim, Ubatuba e Mar Virado), localizado no litoral norte do Estado de São Paulo. A desembocadura da enseada de Ubatumirim está voltada para o sudoeste com várias pequenas ilhas próximas à sua entrada; A enseada de Ubatuba está voltada para o leste e apresenta uma constrição em direção ao mar formado por projeções rochosas, e a enseada do Mar Virado que possui uma grande desembocadura voltada ao sudeste (Mahiques, 1995). Coletas Os ermitões foram coletados mensalmente durante 1998 (primeiro ano) e 1999 (segundo ano), nas enseadas de Ubatumirim, Ubatuba e Mar Virado, na região de Ubatuba, litoral norte do Estado de São Paulo, Brasil. Seis transectos foram estabelecidos em cada enseada: nas profundidades de 5, 10, 15 e 20 m (paralelas à linha de praia), bem como um transecto em uma área protegida (She) de ação das ondas, e outro em uma área mais expostas (Exp) (Fig.1). Um barco de pesca de camarão equipado com redes double-rig (tamanho de malha de 20 mm, 15 mm no saco da rede) foi usado para a pesca de arrasto. Em cada arrasto, foi amostrado por dois quilômetros, ao longo de um período de 30 minutos, cobrindo uma área de aproximadamente m 2. 64

73 Traços da história de vida de L. loxochelis Frameschi IF 2014 Variáveis ambientais Mensurações mensais em cada transecto, registraram as temperaturas de fundo e de superfície e salinidade de fundo usando um termômetro de mercúrio ligado a uma garrafa de Nansen e um refractómetro óptico. Um ecobatímetro acoplado com um GPS foi usado para registrar as profundidades nos locais de amostragem. As amostras de sedimento foram coletadas em cada estação, com uma garra Van Veen, a amostragem de uma área de fundo de 0,06 m 2 foi realizada para medir o teor de matéria orgânica (%) e granulometria dos sedimentos. O sedimento foi seco a 70 C durante 72 horas em numa estufa. O teor de matéria orgânica do sedimento (%) foi obtido através da pesagem de cinzas: 3 partes alíquotas de 10 g cada, para cada estação, foram colocadas em cadinhos de porcelana e incinerados durante 3 horas a 500 o C em uma mufla. Depois disso, foram então novamente pesadas para o cálculo do teor de matéria orgânica. O sedimento remanescente após análise da matéria orgânica foi novamente seco e passada através de uma série de peneiras com tamanhos de malha de acordo com a escala Wentworth (1922). Todos os procedimentos para a análise do sedimento seguiram Hakanson e Jansson (1983) e Tucker (1988). Procedimentos laboratoriais Depois de cada arrasto, todo o material coletado foi triado, congelado, e transportado para o laboratório, onde foram mantidos até a análise. Os ermitões foram identificados de acordo com Melo (1999). Todos os indivíduos de L. loxochelis foram contados, removidos manualmente de suas conchas, sexados com base na posição dos gonóporos (na coxa do terceiro par de pereiópodos das fêmeas e no quinto para os machos), mensurados quanto ao comprimento do escudo cefalotorácico (CSL) com um 65

74 Traços da história de vida de L. loxochelis Frameschi IF 2014 paquímetro (0.10 mm), e quanto ao peso em uma balança de precisão (0.01 g). Em seguida, o abdômen mole foi dissecado para verificação dos estágios de desenvolvimento gonadal para ambos os sexos. A observação das gônadas foi realizada sob um microscópio estereoscópico, considerando o tamanho, forma e coloração, foram caracterizados quatro estágios de desenvolvimento gonadal, para machos e fêmeas: imaturo, rudimentar, em desenvolvimento e desenvolvida (modificado de Lancaster, 1988) Análises estatísticas Os dados de abundância foram avaliados quanto à normalidade por meio do teste de normalidade de Shapiro Wilk s (Shapiro & Wilk, 1965). A abundância total de cada grupo demográfico, para cada enseada e transecto, foi organizada em uma tabela de contingência de dois fatores, a fim de realizar uma análise de correspondência (CA). As associações observadas de ambas as variáveis (grupo demográfico e distribuição espacial) foram resumidas pela frequência de cada célula da tabela e, em seguida, colocado em um espaço dimensional geométrico. A significância estatística dos valores e proporção foi avaliada usando o teste do qui-quadrado (χ 2 ), com p-valor simulado (com base em 2000 permutações) (Nenadic & Greenacre, 2007). O teste de permutação baseada na análise de variância multivariada (PerMANOVA; Anderson, 2001) testou as diferenças na abundância entre as estações do ano (análise temporal) e entre os transectos (análise espacial), utilizando 999 permutações dos dados. Um modelo aninhado em dois níveis dentro dos locais foi escolhido juntamente com a distância de Sorensen (Bray & Curtis, 1957). O teste não paramétrico de Kruskal-Wallis foi utilizado para comparar o tamanho (CSL) dos indivíduos em cada grupo demográfico para cada enseada, seguido por um teste a 66

75 Traços da história de vida de L. loxochelis Frameschi IF 2014 posteriori de Dunn (Zar, 1996). As diferenças na proporção sexual, foram testadas quanto a diferença significativa da proporção esperada (1:1) por meio de um teste binomial (Wilson e Hardy, 2002). Na determinação da maturidade sexual, a frequência relativa (%) dos adultos nas distintas classes de tamanho, com base na medida padrão de ermitões (CSL) foi plotada em gráficos, sendo ajustada uma curva do tipo sigmoide, seguindo o resultado de 1 equação logística: Y r 50 na qual CSL CSL CSL50 = comprimento do escudo 1 e cefalotorácico em que 50% dos indivíduos atingiram a maturidade sexual e r = coeficiente angular. O ajuste de equação foi efetuado pelo método dos mínimos quadrados (Vazzoler, 1996; Bertini et al., 2010). O período reprodutivo foi verificado pela porcentagem de fêmeas maduras (gônadas desenvolvidas + fêmeas ovígeras) em relação às fêmeas adultas totais. O período de recrutamento foi avaliado por meio da frequência e número dos indivíduos imaturos (Martinelli et al. 2002; Bertini et al. 2004; Litulo, 2005). O crescimento dos indivíduos da população foi estimado para machos e fêmeas, separadamente, por meio do acompanhamento do deslocamento modal mensal (método do ajuste não linear usando-se modas), para estimar os parâmetros do modelo von Bertalanffy (1938): CSLt = CSL (1-exp -k(t-t0) ) onde, CSLt = comprimento total no tempo t, k= constante de crescimento, t0 = parâmetro de ajuste (representando a idade do indivíduo quando seu tamanho é igual a zero) Para a análise modal, os dados de comprimento foram agrupados em classes de tamanho de 0.6 mm (CSL). A detecção dos picos modais foi realizada através do software PeakFit 4.0 (Sea Solve Software Inc. ), utilizando procedimento automático de ajuste, baseado nos mínimos quadrados de acordo com o detalhado por Lee et al. (2007). Um resumo estatístico de cada um dos ajustes mensais foi analisado, constando 67

76 Traços da história de vida de L. loxochelis Frameschi IF 2014 o coeficiente de determinação (r 2 ), os graus de liberdade (GL) e o valor de F crítico calculado (Fonseca & D incao, 2003). Só foram aceitos ajustes no qual o valor de F observado foi maior que o F crítico calculado e que o coeficiente de determinação era maior que 0.9. Por eliminação manual, os resultados do ajuste reduzido foram comparados com o ajuste inicial (ajuste completo) verificando a aceitação dos picos modais pelo cálculo do F crítico. Em seguida, através de um gráfico de dispersão dos picos modais vs. Idade (tempo) foi observado o ritmo de crescimento das coortes. O valor da constante de crescimento (k) e a idade teórica (t0) foram testados em várias nuances por tentativa e erro para encontrar as possíveis coortes na população amostrada. Os parâmetros de crescimento de cada coorte encontrada foram calculados, através da ferramenta Solver no software Microsoft Excel pela rotina de ajuste não-linear GRG2 (Generalized Reduced Gradient Fylstra 1998), que minimiza as somas dos resíduos entre os comprimentos observados em campo e os calculados pelo modelo de von Bertalanffy (1938), variando os parâmetros (k e t0) da equação. As curvas médias obtidas para machos e fêmeas foram analisadas em uma relação peso-comprimento, que foi determinada através do modelo proposto por Beverton (1954): Wt = W (1-exp -k(t-t0) ) b onde, Wt é o peso no tempo t, e b é o coeficiente da função de regressão entre o peso e o comprimento do escudo cefalotorácico (Ricker, 1973). O crescimento em peso foi calculado para cada sexo, onde W é o peso máximo. A longevidade (em anos) foi estimada por meio da equação inversa de Bertalanffy modificada por D incao & Fonseca (1999): Tmax = (0- (1/k)Ln(1-CSLt/CSL ), onde Tmax = longevidade. As curvas médias obtidas para machos e fêmeas foram analisadas estatisticamente para comparação do crescimento em tamanho e peso entre os sexos. Para estas análises, utilizou-se o teste F (teste de hipótese) com significância de 5% (Cerrato, 1990). 68

77 Traços da história de vida de L. loxochelis Frameschi IF 2014 Análise de Componentes Principais (PCA) foi utilizada para extrair os padrões anuais subjacentes das variáveis ambientais para cada transecto, utilizando uma matriz de correlação com base nos valores médios dos dados. Para determinar quais os componentes principais seriam utilizados, foi usada a hipótese de aleatoriedade obtida a partir do modelo de Broken Stick (Peres-Neto et al. 2005). As variáveis ambientais com componente de carga 0.5 foram retidas na descrição dos componentes principais (McCune & Grace, 2002; Maliao et al. 2008). A Análise de Redundância (RDA) foi utilizada para detectar possíveis relações entre as variações na abundancia dos grupos demográficos e as variáveis ambientais mensuradas. A RDA produz escores finais de coordenação que resumem a relação linear entre as variáveis explicativas e de resposta (Jongman et al. 1995). O teste de permutação (teste de Monte Carlo, 999 permutações), forneceu os valores de p, verificando a validade dos eixos na PCA, e para verificar a relação linear entre a resposta e matrizes explicativas, e associação entre os escores da primeira e segunda matriz na análise de ordenação RDA (McArdle & Anderson, 2001). Os valores de p dos testes de permutação, indicam o nível de confiança nas previsões (Peck, 2010). As análises multivariadas foram realizadas usando PC-ORD (versão 6, McCune & Mefford, 2011). Resultados Abundância e proporção sexual: a variação espaço-temporal Foram capturados 1823 indivíduos, dentre estes, 769 no primeiro ano e 1054 no segundo ano, não sendo observada diferença significativa na abundância entre os períodos (Tab. 1). Em ambos os anos, a abundância de L. loxochelis foi maior (p < 0.01) 69

78 Traços da história de vida de L. loxochelis Frameschi IF 2014 na enseada de Ubatuba (1º ano = 388, 2º ano = 450) e em Mar Virado (1º ano = 258, 2º ano = 446), quando comparado com Ubatumirim (1º ano = 123, 2º ano = 158) (Tab. 1). Tabela 1. Os resultados da análise MANOVA baseada no teste de permutação não paramétrico (PerMANOVA) da abundância de L. loxochelis por ano, enseada, estações e transectos. Os números em negrito indicam que diferiram estatisticamente (p < 0.05) Fonte de variação g.l. Soma dos quadrados Média dos quadrados Pseudo-F Anos Estações Enseadas Transectos Anos vs. Estações Transectos vs. Enseadas Estações vs. Transectos p Os ermitões foram mais capturados (p < 0.05) no transecto de maior profundidade (20 m) das enseadas de Ubatuba e Mar Virado (Fig. 1). Em Ubatumirim, a maior abundância de indivíduos ocorreu aos 15 e 20m durante o primeiro ano, sendo que no segundo ano também foi observada grande quantidade de indivíduos no transecto exposto (Exp) (Fig. 1 e Tab. 2). A proporção sexual dentre os transectos, foi favorável aos machos, principalmente nos transectos de maior abundância (Tab. 2). A maior abundância de L. loxochelis foi registrada durante o inverno nas três enseadas, para ambos os sexos (Fig. 2). A variação temporal na proporção sexual foi sempre favorável aos machos nas três enseadas, porém, com um aumento considerável no número de fêmeas, principalmente durante o inverno (Fig. 2). 70

79 Traços da história de vida de L. loxochelis Frameschi IF 2014 Figura 1. Distribuição da abundância relativa de L. loxochelis nos transectos nas três enseadas, indicando a distribuição diferencial dos grupos demográficos. (a) mapa indicando os transectos de cada enseada, (b) abundancia total, (c) abundância dos juvenis, (d) abundância de machos adultos, (e) abundância de fêmeas adultas, (f) abundância de fêmeas ovígeras. Os valores de cada figura indicam a análise de correspondência resultados (CA), e a significância estatística das proporções 71

80 Traços da história de vida de L. loxochelis Frameschi IF 2014 Tabela 2. Número de indivíduos de cada grupo demográfico (TJ = total de juvenis; AM = machos adultos; AF = fêmeas adultas; OF = fêmeas ovígeras, N = total de indivíduos) e proporção sexual (machos: fêmeas) em cada enseada e transectos, no litoral norte do Estado de São Paulo, Brasil. Valores com pelo menos uma letra em comum na linha não diferiram estatisticamente (p < 0.05; resultados da comparação de pares da análise de PerMANOVA); números em negrito indicam que diferiram estatisticamente (p < 0.05, teste binomial) Primeiro ano Segundo ano 5 m 10 m 15 m 20 m She Exp 5 m 10 m 15 m 20 m She Exp Ubatumirim Ubatuba Mar Virado TJ AM AF OF N 1 c 19 b 31 a 51 a 4 c 17 b 10 b 57 a 14 b 6 c 71 a M:F 1:0 1:0.58 1:0.41 1:0.31 1:0 1:0 1:2 1:0.58 1:0.40 1:2 1:1.12 TJ AM AF OF N 4 c 4 c 27 b 185 a a 3 c 1 c 8 c 150 a 276 a 12 c M:F 1:0.33 1:1 1:1.70 1:0.46 1:0.30 1:0.76 1:0.50 1:0 1:0.60 1:0.40 1:1.02 1:0 TJ AM AF OF N 4 d 4 d 4 d 181 b 35 c 30 c 5 d 437 a 4 d M:F 1:1 1:1 1:1 1:0.63 1:0.21 1:0.20 1:0.25 1:0.90 1:1 Total 9 d 27 d 62 c 417 a 91 c 163 b 3 d 11 d 70 c 601 a 286 b 83 c 72

81 Traços da história de vida de L. loxochelis Frameschi IF 2014 Figura 2. Distribuição da frequência de L. loxochelis, com base nos estágios de desenvolvimento gonadal (IM = imaturo, RU = rudimentar, ED = em desenvolvimento, DE = desenvolvido, OF = fêmeas ovígeras), e a proporção sexual (machos: fêmeas) em cada enseada e as estações dos anos. Número a frente de cada coluna indica o número de ermitões em cada estação do ano. Os valores em negrito da proporção sexual indicam que diferiram estatisticamente (p < 0.05, teste binomial) 73

82 Traços da história de vida de L. loxochelis Frameschi IF 2014 Características reprodutivas Na avaliação do tamanho médio de L. loxochelis para cada grupo demográfico, os machos foram maiores do que as fêmeas. Ao comparar tamanhos dos grupos demográficos entre as enseadas, não foi verificada diferença (Fig. 3), sendo assim, uma única estimativa de maturidade sexual, bem como de crescimento, foram realizados para as três enseadas regiões. Figura 3. Valor médio, desvio padrão, e mínimo (Min) e máximo (Max) do comprimento do escudo cefalotóracico para os grupos demográficos de cada enseada (TJ = juvenis totais; AM = machos adultos; AF = fêmeas adultas; OF = fêmeas ovígeras). Valores com uma mesma letra em comum nos grupos demográficos de cada enseada não diferiram estatisticamente (teste de Kruskal-Wallis a posteriori Dunn, p < 0.05) A curva logística construída com base nos dados de maturidade morfológica, usando o comprimento do escudo cefalotorácico (CSL), demonstrou que o tamanho em que 50% dos indivíduos alcançam sua maturidade sexual é estimado em 3.1 mm (CSL) para os machos e 3.0 mm (CSL) para as fêmeas (Fig. 4). 74

83 Traços da história de vida de L. loxochelis Frameschi IF 2014 Figura 4. O ajuste da equação logística, indicando o comprimento do escudo cefalotorácico (CSL) para machos e fêmeas de L. loxochelis, onde 50% dos ermitões estão maduros, de acordo com as análises de desenvolvimento das gônadas Os ermitões machos com gônadas desenvolvidas foram registrados principalmente no inverno, nas três enseadas. As fêmeas apresentaram ocorrência de gônadas desenvolvidas ao longo de todo período de estudo nas enseadas de Ubatuba e Mar Virado (Fig. 2). Fêmeas ovígeras também ocorreram ao longo de todo estudo, com menor intensidade no verão e maiores picos no inverno. A crescente representatividade de fêmeas ovígeras, precedida de um alto número de fêmeas com gônadas desenvolvidas, para cada um dos anos, revela que o período reprodutivo ocorre de maneira semelhante nas três enseadas, sendo caracterizando como contínuo (Fig. 2). Da mesma maneira, o recrutamento juvenil também foi contínuo, com pico registrado no verão (Fig. 2). Crescimento e longevidade Sete coortes coexistiram durante os dois anos para machos e cinco coortes para fêmeas (Fig. 5). 75

84 Traços da história de vida de L. loxochelis Frameschi IF 2014 Figura 5. Frequência de distribuição do tamanho dos grupos demográficos de L. loxochelis por mês em classes de tamanho (mm) (TJ = total de juvenis, AM = machos adultos, AF = fêmeas adultas, OF = fêmeas ovígeras). Os números circulados acima das colunas indicam coortes temporais usada nas análises de crescimento para os homens (círculo preenchido de branco) e para o sexo feminino (círculo preenchido em preto) 76

85 Traços da história de vida de L. loxochelis Frameschi IF 2014 Os machos apresentaram maior comprimento assintótico (CSL = 8.70 mm) e peso (W = 6.54 g), bem como maior constante de crescimento (k = /mensal) que os valores encontrados para fêmeas (CSL = 7.30 mm, W = 3.29 g; k = /mensal) (Fig. 6a). Machos e fêmeas alcançaram a maturidade sexual morfológica, com base na análise CSL50, aos aproximadamente 138 e 183 dias respectivamente, sendo que até os dois primeiros meses de idade (120 dias), houve o mesmo ganho de peso para ambos sexos, com um posterior crescimento exacerbadamente maior para os machos (Fig. 6b). Figura 6. L. loxochelis. (a) Curvas para crescimento em comprimento para machos (CSLt = 8.70*(1-exp( *(t ))) e fêmeas (CSLt = 7.30*(1-exp( *(t ))), (b) incremento de peso para os machos (Wt = 6.54*(1 -exp( *(t ))) 4.13 e fêmeas (Wt = 3.29*(1-exp( *(t )))

86 Traços da história de vida de L. loxochelis Frameschi IF 2014 Quanto ao crescimento em peso, ambos os sexos se comportam de maneira semelhante ao longo do tempo; todavia, os machos incrementam seu peso muito mais rapidamente do que as fêmeas. A longevidade estimada para L. loxochelis foi de aproximadamente 1140 dias (38 meses; 3.17 anos) para os machos e 803 dias (26.8 meses; 2.23 anos) para as fêmeas. As curvas de crescimento estimadas para machos e fêmeas mostraram diferenças quanto ao sexo tanto para tamanho (Fcalculated = > Fcritical 7.11, p < 0.05) quanto para o crescimento em peso (Fcalculated = > Fcritical 4.55, p < 0.05) (Fig. 6) Variáveis ambientais O teste de permutação de Monte Carlo indicou que a variação capturada pelas regressões e eixos da PCA foi significativa (Tab. 3). As três enseadas analisadas possuem características geomorfológicas diferentes, apresentando variações dos fatores ambientais em escala temporal e espacial. A PCA explicou nos dois primeiros eixos 57.1% da variabilidade total dos dados, os quais foram retidos para interpretação. O tamanho médio do grão, silte+argila, teor de matéria orgânica e temperatura de fundo correlacionaram-se positivamente com o primeiro eixo, enquanto, frações do sedimento (areia fina, média, grossa e muito fina), correlacionaram-se negativamente com o mesmo eixo (Tab. 3). Em relação ao segundo eixo, relacionaram-se positivamente, a areia muito grossa, fragmentos biodetríticos e silte+argila. Areia muito fina e a temperatura de fundo apresentaram uma alta correlação positiva com o segundo eixo (Tab. 3). Analisando-se a ordenação gerada pela PCA (Fig. 7) é possível notar, no primeiro eixo, o estabelecimento de um gradiente de profundidade. Em tal gradiente, os transectos de maiores profundidades, bem como no abrigado e protegido de cada enseada, apresentaram-se dispersos perifericamente, mais distantes do centro, devido às maiores oscilações na salinidade, temperatura de fundo e composição do sedimento. 78

87 Traços da história de vida de L. loxochelis Frameschi IF 2014 Tabela 3. Resultado da Análise de Componentes Principais (PCA). Os coeficientes foram obtidos a partir de correlação de Pearson. Os números em negrito indicam as relações mais elevadas Variáveis ambientais Componentes PC 1 PC 2 % variação explicada Autovalores Teste de Monte Carlo (p-valor) Temperatura de superficie (ST) Temperatura de fundo (BT) Salinidade de fundo (BS) % Matéria orgânica (OM) Fragmentos biodetríticos (BDF) Areia muito fina (VFS) Areia fina (FS) Areia média (MS) Areia grossa (CS) Areia muito grossa (VCS) Silte e argila (S+C) Tamanho médio do grão (Phi) Relação entre os grupos demográficos e variáveis ambientais O teste de permutação da RDA revelou que os autovalores observados para a análise de redundância foram significativos, o que nos permite rejeitar a hipótese nula de nenhuma estrutura entre as matrizes, indicando que os padrões de associação foram identificados (Tab. 4). Os dois primeiros eixos de RDA representaram 87.4% da variação dos grupos demográficos de L. loxochelis (Fig. 8). As correlações entre as variáveis ambientais e os eixos da ordenação mostram que as frações do sedimento, como a areia fina e muito fina, fragmentos biodetríticos, areia média e grossa, apresentaram relação positiva com a distribuição dos grupos demográficos, e negativa com o eixo 1. Em contrapartida, o tamanho médio do grão, silte + argila, matéria orgânica e a temperatura de fundo influenciaram negativamente a distribuição das espécies, correlacionando-se positivamente com o eixo 1 (Fig. 6). Os 79

88 Traços da história de vida de L. loxochelis Frameschi IF 2014 juvenis apresentaram altas correlações com os dois eixos (ver Tab. 4), e foram associados positivamente às frações granulométricas que afetaram o eixo 1, e uma relação antagônica à areia muito fina e o silte+argila (Fig. 8). Machos e fêmeas adultos, bem como as fêmeas ovígeras relacionaram-se com maior importância ao eixo 1, com os machos e fêmeas adultos demonstrando uma preferência positiva à areia grossa e fina, e negativa ao tamanho médio do grão e teor da matéria orgânica (Fig. 8). As fêmeas ovígeras demonstraram uma preferência pelas frações mais grosseiras do sedimento, com os fragmentos biodetríticos e areia muita grossa, sendo negativamente influenciada pela temperatura de fundo e teor de matéria orgânica (Tab. 4; Fig. 8). Figura 7. Análise de Componentes Principais das variáveis ambientais de cada enseada. (Ubm), Ubatumirim, (Uba) Ubatuba, (Mv) Mar Virado. (I) indicam primeiro ano; (II) indicam segundo ano; Consulte a tabela 3, para os códigos de cada uma das variáveis ambientais 80

89 Traços da história de vida de L. loxochelis Frameschi IF 2014 Tabela 4. Resumo dos resultados da análise de redundância (RDA) para cada grupos demográficos de L. loxochelis na região tropical/subtropical do Brasil. Os valores são correlações entre as respectivas variáveis com os eixos da ordenação. Valores em negrito indicam as maiores correlações RDA1 RDA2 Monte Carlo teste (p-valor) Autovalor (inércia total = 0.822) % Cumulativa explicada Correlação de Pearson Juvenis totais (TJ) Machos adultos (AM) Fêmeas adultas (AF) Fêmeas ovígeras (OF) Temperatura de Fundo (BT) Areia muito fina (VFS) Areia fina (FS) Silte e argila (S+C) Areia média (MS) Areia grossa (CS) Areia muito grossa (VCS) Fragmentos biodetríticos (BDF) Tamanho médio do grão (Phi) % Matéria orgânica (OM) Discussão O dimorfismo sexual é uma característica dos ermitões da região subtropical do Brasil (Fransozo & Mantelatto, 1998; Bertini & Fransozo, 2002, Mantellato et al., 2005), sendo observado também em L. loxochelis, com o mesmo padrão nas três enseadas, corroborando com os resultados de Bertini et al. (2004). Estudos anteriores 81

90 Traços da história de vida de L. loxochelis Frameschi IF 2014 com L. loxochelis na enseda de Ubatuba (Martinelli et al. 2002) e regiões próximas (Ayres-Peres & Mantelatto, 2008a) também registraram machos maiores que fêmeas nesta espécie de ermitão. No estudo de Yoshino & Goshima (2002) com Pagurus filholi (de Man, 1887), os autores relataram que os fatores mais importantes na hierarquia competitiva dos sistemas de acasalamento dos ermitões são o tamanho do corpo, da quela e a qualidade da concha, respectivamente. Em experimentos de laboratório, machos maiores sempre venceram a competição por fêmeas maduras, e atacavam apenas quando tinham certeza de vencer, isto é, quando eles eram suficientemente maiores do que seus rivais, sempre atacando machos menores. Estes fatores reafirmam um padrão na seleção sexual para ermitões, que de acordo com Abrams (1988), seriam três: (1) o direcionamento diferencial de energia para o crescimento; (2) a seleção sexual, onde machos maiores apresentam maior sucesso na obtenção de fêmeas; (3) o dimorfismo sexual, o qual pode propiciar uma prioridade na escolha da concha mais adequada. Relaciona-se ainda que a proporção sexual, também é modulada pelos fatores supracitados, acarretando a maior proporção de machos de L. loxochelis, em relação às fêmeas (Martinelli et al. 2002, Bertini et al. 2004; presente study). De acordo com Bertini et al. (2004) a maturidade sexual fisiológica para machos e fêmeas de L. loxochelis ocorre em tamanhos similares (3.3 e 3.2 mm de CSL, respectivamente). Todavia, estudos de Mantelatto & Martinelli (2001) revelaram que por meio da análise do crescimento relativo, a maturidade sexual da mesma espécie ocorreria entre 4.5 e 6.0 mm de CSL. Os resultados do presente estudo diferem do estudo supracitado e são similares àqueles encontrados por Bertini et al (2004), revelando que a maturidade morfológica ocorre em dimensões menores de CSL. Tal discrepância deve-se à precipitada utilização do maior quelípodo (o esquerdo, no caso de L. loxochelis), que pode não crescer de acordo com a estrutura utilizada como 82

91 Traços da história de vida de L. loxochelis Frameschi IF 2014 medida padrão nos ermitões (cefalotoracic shield length). Esta afirmação pode ser sustentada com base nos relatos de Blackstone (1985, 1986), o qual atesta que as dimensões da concha ocupada exerce um efeito sobre a eventual forma e tamanho do ermitão, particularmente no que diz respeito ao crescimento dos apêndices. Assim, animais em conchas menores têm uma restrição sobre o seu crescimento corporal, mas podem desenvolver quelípodos maiores para melhorar suas chances no combate sexual (Blackstone, 1987). Figura 8. Diagrama de ordenação da análise de redundância (RDA) entre as variáveis ambientais (indicadas pelas setas sólidas) e grupos demográficos de L. loxochelis (indicado por setas pontilhadas). Consulte a tabela 4, para os códigos de cada grupo demográfico e variáveis ambientais 83

92 Traços da história de vida de L. loxochelis Frameschi IF 2014 A quantidade de conchas e suas diferenças morfológicas também podem influenciar o tamanho dos indivíduos e a frequência de reprodução de uma população (Bertness 1980). Mesmo quando ermitões ocupam conchas consideradas adequadas em sua maioria, como observado para a mesma população do presente estudo por Frameschi et al. (2013), ainda é possível encontrar um crescimento somático maior para os machos, alcançando os maiores tamanhos (Ayres Peres et al. 2012; Frameschi et al. 2013). Nossos resultados revelaram que após alcançar a maturidade, os machos apresentam uma constante de crescimento (k) maior do que as fêmeas, o que também eleva sua longevidade. Sant Anna et al. (2008) estimaram o crescimento de Clibanarius vittatus ao longo de dois anos e também encontraram uma constante de crescimento (k) maior para os machos, com o mesmo número de coortes para os sexos (seis coortes). Para L. loxochelis foram encontradas sete coortes para os machos e cinco para as fêmeas. Acreditamos que esta diferença ocorre devido ao dimorfismo sexual característico da espécie, uma vez que somente os machos atingem as maiores classes de tamanho, o que diminui a competição intraespecífica na disputa por conchas nos maiores tamanhos (Frameschi et al. 2013). Sant Anna et al. (2006) avaliaram a utilização de conchas pela população de C. vittatus, da qual Sant Anna et al. (2008) determinaram o crescimento, e reportaram uma intensa disputa entre machos e fêmeas pela concha do gastrópodo Stramonita haemastoma (Linnaeus, 1767) de mesmo tamanho, acarretando que apresentassem tamanho assintótico semelhante. Como o tamanho máximo é considerado para determinação da longevidade, esta acabou sendo similar para machos (66 meses) e fêmeas (60 meses), apresentando uma diferença de apenas 9% entre os sexos (Sant Anna et al. 2008). Já para a espécie do presente estudo, os machos revelaram ter uma longevidade 28% maior do que a das fêmeas. Tal discrepância já foi também 84

93 Traços da história de vida de L. loxochelis Frameschi IF 2014 registrada para o pequeno e abundante ermitão P. brevidactylus, onde machos atingiram uma longevidade 25% maior daquela alcançada pelas fêmeas (Mantelatto et al. 2005). Ao contrário da maioria das espécies de ermitões que coexistem no sublitoral não consolidado da região de transição entre o domínio tropical/subtropical, como Dardanus insignis (Saussure, 1858), Petrochirus diogenes (Linnaeus, 1758), Isocheles sawayai (Forest & Saint Laurent, 1967), Pagurus criniticornis (Dana, 1852) e P. brevidactylus (Stimpson, 1859) (see Fernandes-Goés et al. 2005; Bertini & Fransozo, 2002; Fantucci et al., 2009; Mantelatto et al e Mantelatto et al. 2005; respectivamente), que independentemente do tipo de período reprodutivo (contínuo ou sazonal) apresentam o pico da reprodução nos meses mais quentes do ano, L. loxochelis (presente estudo), Pagurus exilis (Benedict, 1892) e Paguristes tortugae (Schmitt, 1933) são os únicos ermitões que apresentam pico reprodutivo nos meses mais frios do ano na região de Ubatuba. Tais espécies possuem preferência por menores temperaturas (Ayres-Peres & Mantelatto, 2008b; Meireles et al. 2006; Negreiros-Fransozo et al. 1992; respectivamente), assim como registrado para Pagurus bernhardus (Linnaeus, 1758) para costa atlântica da Europa, na Inglaterra, onde fêmeas reprodutivas foram abundantes durante o inverno e desapareceram no verão (Lancaster, 1990). De acordo com Terossi et al. (2010) a diferença na temperatura é a responsável pela alteração do período reprodutivo de P. exilis observado entre populações do Brasil e da Argentina, reproduzindo-se sazonalmente em áreas temperadas, enquanto que em águas subtropicais, a reprodução é contínua. Assim como encontrado por Martinelli et al. (2002), Bertini et al. (2004), Ayres- Peres & Mantelatto (2008a) e no presente estudo, a reprodução de L. loxochelis é caracterizada como como contínua, com o maior número de fêmeas ovígeras ocorrendo durante o inverno. Ayres-Peres & Mantelatto (2008b), atribuiram a oscilação na 85

94 Traços da história de vida de L. loxochelis Frameschi IF 2014 ocorrência de fêmeas ovígeras à variação na temperatura, e inferiram que tais fêmeas poderiam ter migrado para áreas mais frias nos meses em que não foram encontradas no local amostrado. Este padrão também foi observado para o ermitão P. exilis, sendo que a abundância de fêmeas ovígeras dessa espécie está associada com a chegada da Água Central do Atlântico Sul, a qual ocasiona uma redução da temperatura e possibilita a migração dos indivíduos até para partes internas das enseadas (De Léo & Pires-Vanin 2006). A inferência do processo migratório citada por Ayres-Peres & Mantelatto (2008b) pode ser afirmada através da correlação negativa entre fêmeas ovígeras e temperatura de fundo, evidenciada no primeiro eixo da RDA. Esta migração também pode ser possível devido ao comportamento de cópulas múltiplas e constante dispersão larval, já que fêmeas ovígeras de L. loxochelis têm capacidade de incubar embriões em todos os estágios de desenvolvimento, o que sugere que o desenvolvimento embrionário da espécie é um processo contínuo (Torati & Mantelatto, 2008). Tais características podem ser indicativas de um grande esforço reprodutivo que maximiza o sucesso larval de uma espécie endêmica, como é o caso de L. loxochelis. A relação entre o ermitão L. loxochelis e as menores temperaturas também foi evidenciada quando levado em consideração sua distribuição no habitat, com todos os grupos demográficos concentrando-se principalmente nos transectos mais profundos de cada enseada. Mantelatto et al (2004) e Bertini et al (2004) também avaliaram a região de Ubatuba e não capturaram L. loxochelis com representatividade nas regiões internas da enseada. A partir dos 15 e 20 m de profundidade, a influência do mar aberto é notável, sem obstáculo físico para o agente dinâmico e pouca influência da costa e rios (Soares-Gomes & Pires-Vanin 2003). Esta situação é caracterizada por um grau mais elevado de heterogeneidade na textura do sedimento, com predominância de sedimentos 86

95 Traços da história de vida de L. loxochelis Frameschi IF 2014 grossos e uma redução no teor de matéria orgânica, além da diminuição da temperatura em relação às áreas mais próximas da costa (Pires-Vanin et al. 1993). A uniformidade do sedimento nos transectos de maior profundidade das enseadas de Ubatuba e Mar Virado, evidenciada pela PCA, parece ser a melhor justificativa para o relevante número de indivíduos coletados nesses locais. Além de possuir o hábito de se enterrar no sedimento, L. loxochelis como outros ermitões, pode se alimentar por meio de filtragem de partículas suspensas na água (Schembri, 1982), utilizando suas antenas, como o ermitão Diogenes brevirostris Stimpson, 1858 (see Boltt, 1961), justificando a relação positiva entre a espécie e as frações de areia do sedimento (areia fina, média, grossa e muito grossa). Este tipo de substrato facilita o processo de enterramento (Rebach, 1974), ao contrário daquele com predominância de fragmentos biodetríticos e silte + argila (os quais relacionaram-se negativamente com a espécie), como o encontrado em Ubatumirim e transectos mais internos de Ubatuba e Mar Virado. Segundo Pires (1992) as partículas de silte + argila se acumulam em condições mais abrigadas, enquanto as frações mais grosseiras do sedimento refletem um ambiente mais dinâmico e de alta energia, o que também provém maior quantidade de alimento em suspensão. Decapodos endêmicos parecem ser mais adaptados às regiões em que se encontram do que as espécies de ampla distribuição. Assim, grandes variações ambientais acabam por alterar o fitness populacional das espécies restritas de uma região, como o registrado para o camarão Artemesia longinaris Bate,1888 (Castilho et al. 2007) e para o ermitão P. exilis (Terossi et al. 2010), que devido às menores temperaturas, sofreram alterações quanto ao tamanho e estratégias reprodutivas. A avaliação do efeito exercido pelas características ambientais na distribuição do ermitão endêmico L. loxochelis, que apresentou uma especificidade quanto à composição do 87

96 Traços da história de vida de L. loxochelis Frameschi IF 2014 sedimento e preferência por baixas temperaturas, é de fundamental importância para a compreensão de sua biologia. Populações de L. loxochelis que habitam regiões mais frias alcançam tamanhos expressivamente maiores, podendo atingir mm de CSL (estudo realizado na costa Uruguaia, por Carranza et al. 2008), e têm período reprodutivo caracterizado como sazonal (como observado na Argentina, por Scelzo et al. 2004). No presente estudo o maior indivíduo apresentou apenas 8.90 mm de CSL e o período reprodutivo foi caracterizado como contínuo. Tais características são semelhantes aos resultados obtidos em pesquisas realizadas na mesma região (Martinelli et al. 2002; Bertini et al. 2004; Ayres-Peres et al. 2008), evidenciando que o paradigma do efeito latitudinal (Bauer, 1992) acompanhado de baixas temperaturas afetam a história de vida de L. loxochelis. Mesmo tendo sua distribuição restrita ao atlântico sul, L. loxochelis é a segunda espécie de ermitão mais abundante do sublitoral não consolidado de onde ocorre, coexistindo com nove espécies de ampla distribuição (Melo 1999), sendo D. insignis, P. diogenes e I. sawayai as mais abundantes (Ayres-Peres et al. 2008; Fransozo et al. 2008; 2011). Os resultados encontrados no presente estudo sugerem que a grande abundância da espécie é decorrente de uma estratégia reprodutiva diferenciada, no qual a reprodução contínua com picos no inverno garante um maior número de larvas presentes no plâncton durante a ACAS, que se inicia na primavera e propicia um aumento na disponibilidade de alimento para as larvas. O rápido desenvolvimento pósembrionário, com apenas três estágios de zoea (Bernardi, 1986) também garante uma redução na disputa interespecífica por conchas (Abrams, 1980), uma vez que as demais espécies que utilizam esse mesmo recurso iniciam o período reprodutivo na primavera. As características reprodutivas supracitadas incluindo uma estimativa de maturidade sexual em tamanhos similares para machos e fêmeas, maior abundância e 88

97 Traços da história de vida de L. loxochelis Frameschi IF 2014 crescimento diferencial dos machos, ocupação de conchas adequadas (Frameschi et al. 2013), e robustez na ocupação do habitat, permitem concluir que o ermitão endêmico L. loxochelis possui características que contribuem para um equilíbrio entre custo e benefício que maximiza esforços em produção de prole melhorando a aptidão de sobrevivência da população. Referências Abrams, P.A Resource partitioning and interspecific competition in a tropical hermit crab community. Oecologia, 46: Abrams, P.A Sexual difference in resource use in hermit crabs; consequences and causes. In: Chelazzi, G. & Vannini, M. (eds.). Behavioral adaptation to intertidal life. New York, Plenum. pp Anderson, M.J A new method for non parametric multivariate analysis of variance. Austral Ecology, 26(1): Andrade, L.S.; Fransozo, V.; Bertini, G.; Negreiros-Fransozo, M.L. & López-Greco, L.S Reproductive Plasticity in the Speckled Crab Arenaeus cribrarius (Decapoda, Brachyura, Portunidae) Associated with a Population Decline. Journal of Coastal Research. In press. doi: Ayres-Peres, L. & Mantelatto, F.L. 2008b. Patterns of distribution of the hermit crab Loxopagurus loxochelis (Moreira, 1901) (Decapoda, Diogenidae) in two coastal areas of southern Brazil. Revista de Biología Marina y Oceanografía, 43(2): Ayres-Peres, L. & Mantelatto, F.L. 2008a. Análise comparativa da estrutura populacional do ermitão endêmico do Atlântico Ocidental Loxopagurus loxochelis (Decapoda, Anomura) em duas regiões do Estado de São Paulo, Brasil. Iheringia, 98(1): Ayres-Peres, L.; Quadros, A.F. & Mantelatto, F.L Comparative analysis of shell occupation by two southern populations of the hermit crab Loxopagurus loxochelis (Decapoda, Diogenidae). Brazilian Journal of Oceanography, 60(3):

98 Traços da história de vida de L. loxochelis Frameschi IF 2014 Ayres-Peres, L.; Sokolowicz, C.C.; Kotzian, C.B.; Rieger, P.J.; Santos, S Ocupação de conchas de gastrópodes por ermitões (Decapoda, Anomura) no litoral de Rio Grande, Rio Grande do Sul, Brasil. Iheringia, 98(2): Bauer, R.T Testing generalizations about latitudinal variation in reproduction and recruitment patterns with sicyoniid and caridean shrimp species. Invertebrate Reproduction and Development, 22: Bernardi, J.V.E Desenvolvimento larval de Loxopugurus loxochelis (Moreira, 1901) (Crustacea, Decapoda, Diogenidae) em laboratório. Bachelor Thesis, Universidade Estadual Paulista (UNESP), Rio Claro, Brazil. pp (unpublished). Bertini, G. & Fransozo, A Breeding season of the hermit crab Petrochirus diogenes (Anomura, Diogenidae) in the north coast of São Paulo state, Brazil. In: Escobar-Briones E. & Alvarez, F. (eds). Modern Approaches to the Study of Crustacea. Kluwer Academic/Plenum Publishers, New York. pp Bertini, G.; Fransozo, A. & Braga, A.A Ecological distribution and reproductive period of the hermit crab Loxopagurus loxochelis (Anomura, Diogenidae) on the northern coast of São Paulo State, Brazil. Journal of Natural History, 38(18): Bertini, G.; Teixeira, G.M.; Fransozo, V., & Fransozo, A Reproductive period and size at the onset of sexual maturity of mottled purse crab, Persephona mediterranea (Herbst, 1794) (Brachyura, Leucosioidea) on the southeastern Brazilian coast. Invertebrate Reproduction and Development, 54(1): Bertness, M.D Shell preference and utilization patterns in littoral hermit crabs of the Bay of Panama. Journal of Experimental Marine Biology and Ecology, 48(1): Beverton, R.J.H Notes on the use of theoretical models in the study of the dynamics of exploited fish populations. Miscellaneous Contributions of the U.S. Fishery Laboratory, 63: Biagi, R.; Meireles, A.L.; Scelzo, M.A. & Mantelatto, F.L Comparative study of shell choice by the southern endemic hermit crab Loxopagurus loxochelis from Brazil and Argertina. Revista Chilena de Historia Natural, 79(4): Blackstone, N.W The effects of shell size and shape on growth and form in the hermit crab Pagurus longicarpus. The Biological Bulletin, 168(1): Blackstone, N.W Variation of cheliped allometry in a hermit crab: The role of introduced periwinkle shells. The Biological Bulletin, 171(2):

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106 Capítulo IV Shell occupation by the hermit crab Dardanus insignis (Decapoda, Diogenidae) in a subtropical region of Brazil

107 Shell occupation by D. insignis Frameschi IF 2014 Abstract: The pattern of shell occupation by the hermit crab Dardanus insignis (Saussure, 1858) from the subtropical region of southeastern coast of Brazil was investigated in the present study. The percentage of shell types that were occupied and the morphometric relationships between hermit crabs and occupied shells were analyzed from monthly collections conducted during two years (from January 1998 to December 1999). Individuals were categorized according to sex and gonadal maturation, weighed and measured with respect to their cephalothoracic shield length (CSL) and wet weight (CWW). Shells were measured regarding their aperture width (SAW), dry weight (SDW) and internal volume (SIV). A total of 1086 hermit crabs was collected, occupying shells of 11 gastropod species. Olivancillaria urceus (Roding, 1798) was most commonly used by the hermit crab D. insignis, followed by Buccinanops cochlidium (Dillwyn, 1817), and Stramonita haemastoma (Linnaeus, 1767). The highest determination coefficients (r 2 > 0.50, p < 0.01) were recorded particularly in the morphometric relationships between CSL vs. CWW and SAW vs. SIV, which are important indication that in this D. insignis population the great majority the animals occupied adequate shells during the two years analysed. The high number of used shell species and relative plasticity in pattern of shell utilization by smaller individuals of D. insignis indicated that occupation is influenced by the shell availability, while larger individuals demonstrated more specialized occupation in Tonna galea (Linnaeus, 1758) shell. Keywords: Associated species, Interspecific relationships, Gastropod shells, Anomura. 99

108 Shell occupation by D. insignis Frameschi IF 2014 Introduction Anomuran crustaceans are important members of the intertidal and sublittoral communities due to their fundamental role in marine trophic chains (Negreiros- Fransozo et al., 1997). The adaptation and association of hermit crab species to their substrates reveal a complex structure in their communities (Martínez-Iglesias and García-Raso, 1999) given that they need to occupy structures produced by other organisms, such as polychaete tubes (Gherardi and Cassidy, 1995) and gastropod shells (Hazlett, 1981). Hermit grabs usually protect their soft abdomens within these shells, which are selected according to the biology and morphology of the species. Despite the adaptations to search, encounter, and select shells (Rittschof, 1980; Mesce, 1982), the availability of these shells in the environment is limited (Childress, 1972; Bertness, 1980). Due to this fact, some authors (Spight, 1977; Wilber and Herrnkind, 1984) suggest that shell availability in the environment has a positive influence on hermit crab populations, given that this resource is indispensable for the growth and protection of these organisms. In addition, the characteristics of a given shell occupied by a hermit crab can differ according to its species, reflecting fine differences in the selection of this resource that, in addition to variation in habitat, act in different ways depending on the species of hermit crab (Bertness, 1981). Although the process of shell selection has been investigated exhaustively (e.g. Vance, 1972; Elwood et al., 1979; Bertness, 1980; Wilber, 1990; Hazlett, 1992; Ohmori et al., 1995; Wada et al., 1997; Bertini and Fransozo, 2000; Meireles and Mantelatto, 2005), the landscape of a given location can regulate the persistence (or lack thereof) of these anomurans, particularly due to their capacity to influence the community that provides shell resources, i.e. the abundance and diversity of gastropods (Meireles et al., 2003). 100

109 Shell occupation by D. insignis Frameschi IF 2014 The hermit crab Dardanus insignis (Saussure, 1858) is distributed across the western Atlantic, ranging from eastern United States to the Gulf of Mexico, Antilles, Brazil (from Rio de Janeiro to Rio Grande do Sul) to Uruguay and Argentina, being found from shallow waters up to 500 m in depth, and in different types of substrate, including mud, sand, shell, and rocky bottoms (Rieger, 1997). Being adapted to a variety of habitats, it is the most abundant species of the family Diogenidae in the sublittoral of southeastern Brazil (Fransozo et al., 1998; 2011). Despite the scarcity of studies on its biology, a few studies have been carried out on its larval development (Hebling and Mansur, 1995), population dynamics (Branco et al., 2002), and regarding the biological characteristics that determine the symbiotic association between D. insignis and the porcelanid Porcellana sayana (Leach, 1820) (Meireles and Mantelatto, 2008). Populations of D. insignis deserve particular attention regarding their stability, given that these populations or individuals experience constant perturbation caused by trawl nets. According to Costa et al. (2005) the constant shrimp fisheries in south and southeast Brazil, as well as the anthropic effect caused by tourism, are the main causes for the decrease in local fishery resources. Due to the nonselectivity of the nets, the benthic fauna is greatly impacted, leading to injuries or even the death of the organisms that inhabit the area as they are considered as bycatch of fishing (Wassenberg and Hill, 1989). When considering these impacts, it becomes relevant to investigate the use of shells by hermit crabs, given that an understanding of this relationship can be used for future comparisons in monitoring initiatives to assess the stability of the populations and communities in which they occur. Thus, the present study analyzed the occupation pattern of gastropod shells by the hermit crab D. insignis in a subtropical region on the 101

110 Shell occupation by D. insignis Frameschi IF 2014 Brazilian coast, considering the percentage of shell occupation and demonstrating the shell variables that best fit the hermit crabs. Materials and Methods Hermit crabs were collected monthly from January, 1998 to December, 1999 in three bays, namely Ubatumirim (UBM), Ubatuba (UBA), and Mar Virado (MV), all of which in the municipality of Ubatuba ( W S, W S, and W S, respectively). Each location was determined by GPS (Global Position System). A shrimp-fishing boat equipped with double-rig nets (mesh size 20 mm and 15 mm in the cod end) was used for trawling. At each transect was trawled for 2 km over a period of 30 min, covering an area of approximately 18,000 m 2. After each trawl, all collected material was inspected, frozen, and transported to the laboratory. Hermit crabs were identified according to Melo (1999). Individuals of D. insignis were counted, manually removed from their shells, sexed based on the position of the gonopores (on the coxa of either the third or the fifth pair of pereiopods in females and males, respectively), weighed (wet weight, CWW) in a precision balance (0.01 g) and had their cephalothoracic shield length (CSL) measured using a caliper (0.10 mm). The shells occupied by hermit crabs were identified according to Rios (1994) and their aperture widths were measured (SAW). After removing the hermit crab, each shell was measured with respect to its dry weight (SDW) and then kept in an oven for 24h at 60 o C. Internal volume was measured by filling the shell with water and later transferring it to a graduated pipette (Conover, 1978). Hermit crabs were grouped into the following demographic groups: males, non-ovigerous females, and ovigerous females. The determination of the distribution of crabs into CSL size classes used the Shapiro-Wilks test for normality. Differences in the percentage of species of shells 102

111 Shell occupation by D. insignis Frameschi IF 2014 occupied in each bay by each demographic group were assessed through the chi-square (χ2) test (test of independence). Data on the measured variables of both hermit crabs and shells were log-transformed to better approximate normal distributions (Sokal and Rohlf, 1995). The size and weight of shells occupied by different demographic groups were tested using a one-way ANOVA, followed by a Tukey test (Zar, 1996). Relationships between hermit crab dimensions and occupied shells were verified by linear regression analyses and determination coefficients (r 2 ) (Sokal and Rohlf, 1995). The significance level used in all tests was p < 0.05 (Zar, 1996). Results A total of 1086 hermit crabs of the species D. insignis was collected over the course of two years, occupying shells of 11 gastropod species (Tab. 1). Hermit crabs were grouped into 11 size classes, with 2.0 mm intervals, starting from a minimum size of 2 mm (CSL). The distribution of individuals into size classes showed non-normal patterns, with an unimodal distribution in each of the three bays (Shapiro-Wilks, UBM, W=0.93; UBA, W=0.91; MV, W=0.98, p<0.05 for all locations). Out of 348 individuals collected in the UBM bay occupying shells of nine gastropod species, 215 were males (61.8%), 116 were non-ovigerous females (33.3%), and 17 were ovigerous females (4.9%), In UBA, shells of 11 gastropod species were occupied by 570 specimens, of which 365 were males (64.04%), 148 were non-ovigerous females (26.03%) and 57 were ovigerous females (10.0%). In the MV bay, a total of 168 specimens were collected inhabiting shells of only four gastropod species, of which 101 were males (60.1%), 66 were non-ovigerous females (39.3%) and a single ovigerous female (0.6%). 103

112 Shell occupation by D. insignis Frameschi IF 2014 Table 1. D. insignis. Characterization of 1086 occupied gastropod shells, and results of ANOVA followed by Tukey test, where different letters indicate significant differences (OP = occurrence percentage) Gastropod species n Aperture Width Internal Volume Weight (g) (mm) (ml) Max. Min. Max. Min. Max. Min. OP Mean ± SD Mean ± SD Mean ± SD (%) Olivancillaria urceus (Ou) (Röding, 1798) 16.8 ± 7.78a 7.76 ± 1.76a 4.15 ± 1.69a Buccinanops cochlidium (Bc) (Dillwyn, 1817) 8.24 ± 3.45b ± 2.46b 6.46 ± 2.97b Stramonita haemastoma (Sh) (Linnaeus, 1767) ± 5.37b ± 2.95c 5.13 ± 3.35ad Siratus tenuivaricosus (St) (Dautzenberg, 1927) 8.33 ± 4.56b ± 2.03c 3.87 ± 2.57a Cymatium parthenopeum (Cp) (Von Salis, 1793) 9.79 ± 5.65b ± 2.16c 5.81 ± 4.05bd Semicassis granulata (Sg) (Born, 1778) ± 8.28b ± 2.55bd ± 6.80c Tonna galea (Tg) (Linnaeus, 1758) ± 10.64b ± 6.77e ± 45.00e Fusinus marmoratus (Fm) (Philippi, 1846) ± 7.00b ± 2.39bc 8.62 ± 6.30d Strombus pugilis (Sp) (Linnaeus, 1768) ± 12.43c 8.75 ± 1.53ac ± 1.79c Zidona dufresnei (Zd) (Donovan, 1823) ± 17.12c ± 5.33d ± 13.33e Polinices lacteus (Pl) (Guilding, 1834)

113 Shell occupation by D. insignis Frameschi IF 2014 Figure 1. D. insignis. Percentage occupancy of different gastropod species for each demographic group in each bay, Ubatumirim (a), Ubatuba (b) and Mar Virado (c). Number above each column indicates number of hermit crabs of each demographic group. Abbreviations as in Table 1 105

114 Shell occupation by D. insignis Frameschi IF 2014 Shells of Strombus pugilis (Linnaeus, 1768), Zidona dufresnei (Donovan, 1823), and Olivancillaria urceus (Röding, 1798) were significantly heavier than those of the remaining species (Tab.1). With respect to aperture width and shell internal volume, Tonna galea (Linnaeus, 1758) was the largest among the occupied species, whereas O. urceus was the smallest (Tab.1). These last shell, O. urceus, was most commonly used by the hermit crab D. insignis in all three bays (UBM: χ 2 = 273.9; UBA: χ 2 = 259.7; MV: χ 2 = 83.91; p<0.01 for all bays), followed by Buccinanops cochlidium (Dillwyn, 1817), and Stramonita haemastoma (Linnaeus, 1767). In the context of shell occupation by different demographic groups, the shell of O. urceus was significantly more used by males and non-ovigerous females in all three bays (UBM: χ 2 = 82.95, χ 2 = 104.7; UBA: χ 2 = 140.2; χ 2 = 94.96; MV: χ 2 =140.2; χ 2 = 94.96; p < 0.01 for all groups) (Fig. 1). Ovigerous females occupied mostly the shell of O. urceus in UBM (χ 2 = 7.12; p < 0.01) and UBA (χ 2 = 0.6; p = 1.05) (Fig. 1a, b), yet in MV only a single ovigerous female was captured, which nevertheless was also found in a shell of O. urceus (Fig. 1c). With respect to the occupation of shells of different size classes by D. insignis, shells of O. urceus were the most commonly used by the first three size classes (grouping by size of cephalothoracic shield length), both for males and females. There was more variety in the fourth size class ( mm) for both sexes, including shells of O. urceus, B. gradatus, S. haemastoma, Siratus tenuivaricosus (Dautzenberg, 1927), and Cymatium parthenopeum (Von Salis, 1793). Only males occurred in the 6 th size class ( mm), usually in of shells T. galea (Fig. 2). 106

115 Shell occupation by D. insignis Frameschi IF 2014 Figure 2. D. insignis. Percentage occupancy of different gastropod species in each size classes by males (a) and females (b). Number above each column indicates number of hermit crabs of each size classes. Abbreviations as in Table 1 107

116 Shell occupation by D. insignis Frameschi IF 2014 The relationship between the traits of the occupied shell and the corresponding hermit crab were tested separately for each sex and showed the highest coefficients of determination in the case of males (r 2 > 0.50; p < 0.01), such that shell weight (SDW) was the only variable that did not show significant association. On the other hand, aperture width (SAW) and shell internal volume (SIV) showed the highest coefficients of determination (Tab. 2). Correlating hermit crab dimensions to shell variables indicated that the cephalothoracic shield length (CSL) showed the highest correlation coefficients. In particular, CSL vs. SAW and SIV; CWW vs. SAW and SIV were the relationships that best described the association between hermit crabs and the occupied shells. Regression analyses of all nine shell species most commonly occupied by D. insignis indicated significant relationships for most of them (p < 0.01). Only one relationship (SDW vs. CWW) of the shell of the species S. pugilis showed a low determination coefficient (r 2 = 0.04) e and did not reach statistical significance (Tab. 3). Discussion According to Hazlett (1981) the use of shells of different gastropod species by different hermit crab species can be explained by size and environmental variation, including protection from factors to which they are exposed, such as osmotic stress, energetic expenditure, and the action of waves. Thus, individuals of different sizes and sexes seek shells that best fit their morphology, which would vary according to different crab demographic groups and to availability of shells in the environment. 108

117 Shell occupation by D. insignis Frameschi IF 2014 Table 2. D. insignis. Regression equations in relation to the sex of the hermit crabs. (N = number of individuals; r 2 = determination coefficient; CSL = shield length; CWW = wet weight of hermit crabs; SAW = aperture width; SDW = shell weight; SIV = shell internal volume). * = p < 0.01; ns = not significant Linear Equation Relationships Groups N Y = a X+b Males 681 SAW = CSL * CSL vs. SAW Non-ovigerous females 330 SAW = CSL * Ovigerous females 75 SAW = CSL * r 2 CSL vs. SDW Males 681 SDW = CSL ns Non-ovigerous females 330 SDW = CSL * Ovigerous females 75 SDW = CSL ns CSL vs. SIV Males 681 SIV = CSL * Non-ovigerous females 330 SIV = CSL * Ovigerous females 75 SIV = CSL * CWW vs. SAW Males 681 SAW = CWW * Non-ovigerous females 330 SAW = CWW * Ovigerous females 75 SAW = CWW * CWW vs. SDW Males 681 SDW = CWW ns Non-ovigerous females 330 SDW = CWW ns Ovigerous females 75 SDW = CWW ns CWW vs. SIV Males 681 SIV = CWW * Non-ovigerous females 330 SIV = CWW * Ovigerous females 75 SIV = CWW * 109

118 Shell occupation by D. insignis Frameschi IF 2014 Table 3. D. insignis. Regression equations of the studied relationships (CSL = shield length; CWW = wet weight of hermit crabs; SAW= aperture width of shells; SDW = shell weight; SIV = shell internal volume). * = p < 0.01; ns = not significant Gastropod species Relationships n Linear Equation Y = a x + b r 2 O. urceus CSL vs. SAW 583 SAW = CSL * CSL vs. SDW 583 SDW = CSL * CSL vs. SIV 583 SIV = CSL * CWW vs. SAW 583 SAW = CWW * CWW vs. SDW 583 SDW = CWW * CWW vs. SIV 583 SIV = CWW * B. cochlidium CSL vs. SAW 177 SAW = CSL * CSL vs. SDW 177 SDW = CSL * CSL vs. SIV 177 SIV = CSL * CWW vs. SAW 177 SAW = CWW * CWW vs. SDW 177 SDW = CWW * CWW vs. SIV 177 SIV = CWW * S. haemastoma CSL vs. SAW 92 SAW = CSL * CSL vs. SDW 92 SDW = CSL * CSL vs. SIV 92 SIV = CSL * CWW vs. SAW 92 SAW = CWW * CWW vs. SDW 92 SDW = CWW * CWW vs. SIV 92 SIV = CWW * S. tenuivaricosus CSL vs. SAW 58 SAW = CSL * CSL vs. SDW 58 SDW = CSL * CSL vs. SIV 58 SIV = CSL * CWW vs. SAW 58 SAW = CWW * CWW vs. SDW 58 SDW = CWW * CWW vs. SIV 58 SIV = CWW * C. parthenopeum CSL vs. SAW 53 SAW = CSL * CSL vs. SDW 53 SDW = CSL * CSL vs. SIV 53 SIV = CSL * CWW vs. SAW 53 SAW = CWW * CWW vs. SDW 53 SDW = CWW * CWW vs. SIV 53 SIV = CWW * S. granulata CSL vs. SAW 34 SAW = CSL * CSL vs. SDW 34 SDW = CSL * CSL vs. SIV 34 SIV = CSL * CWW vs. SAW 34 SAW = CWW * 110

119 Shell occupation by D. insignis Frameschi IF 2014 CWW vs. SDW 34 SDW = CWW * CWW vs. SIV 34 SIV = CWW * T. galea CSL vs. SAW 28 SAW = CSL * CSL vs. SDW 28 SDW = CSL * CSL vs. SIV 28 SIV = CSL * CWW vs. SAW 28 SAW = CWW * CWW vs. SDW 28 SDW = CWW * CWW vs. SIV 28 SIV = 0.01 CWW * F. marmoratus CSL vs. SAW 24 SAW = CSL * CSL vs. SDW 24 SDW = CSL * CSL vs. SIV 24 SIV = CSL * CWW vs. SAW 24 SAW = CWW * CWW vs. SDW 24 SDW = CWW * CWW vs. SIV 24 SIV = CWW * S. pugilis CSL vs. SAW 24 SAW = CSL * CSL vs. SDW 24 SDW = CSL * CSL vs. SIV 24 SIV = CSL * CWW vs. SAW 24 SAW = CWW ns CWW vs. SDW 24 SDW = CWW * CWW vs. SIV 24 SIV = CWW * The results of the present study indicate a smaller suite of shells occupied by hermit crabs than compared to those of Miranda et al. (2006), who noted the occupation by ovigerous females (and only ovigerous females) of shells of 15 gastropod species. Such differences can be justified by the shell diversity rather than by the abundance of gastropod species in the region, given that nine of the species recorded in the abovementioned study showed low occupation rates (> 3 %), whereas in the present study only the species Polinices lacteus (Guilding, 1834), used by a single individual, and Z. dufresnei, used by 12 individuals, showed low occupancy. Shells of the gastropod O. urceus were the most used by D. insignis in a region at higher latitude according to Ayres-Peres et al. (2008). When compared to the present study, which also recorded O. urceus as the most occupied shell in all three bays 111

120 Shell occupation by D. insignis Frameschi IF 2014 (>50%) and, given its high occupation rate, we can assume that there is both a occupation and a better adaptation of the hermit crab D. insignis to occupy this species. According to Abrams (1988) differential growth patterns among the sexes directly influence shell occupation, yet this was not recorded in the present study, which indicates a consistent pattern in the choice for the occupation species of shell. Hahn (1998) suggested that the occupation of the same shell species (in this case, O. urceus) decreases intraspecific competition, which has a positive influence at the population level. This fact might be associated with the competitive dominance of D. insignis in the sub-littoral region (see Fransozo et al., 2008, 2011; Ayres-Peres et al., 2008). Hazlett (2005) suggests that male hermit crabs that use for the most part a given species of shell are considered specialists and allow for a higher effectiveness in the mating process in comparison to hermit crabs with generalist occupation patterns, occupying shells of different species according to their availability in the environment. In this study, only males were recorded among the largest size classes, and also showed specialization, given that they occupied mostly the shells with the largest aperture width (T. galea). In the case of hermit crabs, males are usually larger than females (Manjón-Cabeza and García-Raso, 1998; Branco et al., 2002; Martinelli et al., 2002 ; Litulo, 2005) to reduce competition risks, which is a consequence of the evolution of male reproductive strategies given the advantages that an asymptotically larger size can provide (Asakura, 1995). Despite indicating a higher diversity of occupied shells, Miranda et al. (2006) also indicated that O. urceus was the most used shell by ovigerous females of D. insignis. The small number of shell species occupied by ovigerous females in the present study when compared to males and non-ovigerous females might have been due to their restriction to only two size classes. This reduced diversity of occupation by 112

121 Shell occupation by D. insignis Frameschi IF 2014 ovigerous females was similar to that reported for other diogenid species, such as Petrochirus diogenes (Linnaeus, 1758) and Calcinus tibicen (Herbst, 1791) (studied by Bertini and Fransozo, 2000 and Garcia and Mantelatto, 2000; respectively); as well as the pagurid Pagurus exilis (Benedict, 1892), studied by Terossi et al. (2006). This similarity implies the existence of a restriction in the choice of shells by ovigerous females. According to Hazlett et al. (2005) females of Clibanarius vittatus (Bosc, 1802) that occupied heavier shells - larger than their ideal size - tended not to be ovigerous, whereas ovigerous females were most commonly found in adequate shells. When analyzing egg production strategies in Paguristes tortugae (Schmitt, 1933), Mantelatto et al. (2002) reported that the occupation of some shells provided an increase in fecundity. The same was shown for Loxopagurus loxochelis (Moreira, 1901) by Torati and Mantelatto (2008), who also showed that this increase in fecundity takes place particularly when the shell is lighter. The difference in shell utilization patterns between juveniles, males, and females has already been observed in several hermit crab species (Blackstone and Jocslyn, 1984; Imazu and Asakura, 1994). Although the present study has not identified juveniles, Fernandes-Goés et al. (2005) investigated the population biology of D. insignis and considered as juveniles those individuals that would correspond in the present study as the first size class, i.e. 2.0 a 3.9 mm. Based on this assumption, the results of the present study suggest that, during juvenile growth, the morphology of the animal and the shell are not determining factors in the choice of the resource, given that hermit crabs categorized as juveniles (both males and females) are found in a shells with a variety of shapes. The variation of occupation in the smaller size classes was verified by Ayres- Peres et al. (2012) when they analyzed the utilization of shells by the hermit, L. loxochelis at the same site of the present study. This diverse exploration of shell species 113

122 Shell occupation by D. insignis Frameschi IF 2014 by D. insignis in the first four size classes is likely because of the presence of a larger availability of gastropod species with varied sizes in the environment (Mantelatto and Garcia, 2000). The size of commonly used shells is well correlated with the cephalothoracic shield size in hermit crabs (Hazlett, 1981). In morphometric analyzes carried out for males of D. insignis, high correlation coefficients were found in relation to those of females (ovigerous and non-ovigerous). This fact should be due to the capacity of larger males to win agonistic encounters for the possession of empty shells, which enables them to occupy the best shells in nature (Asakura, 1995). According to Abrams (1980) the size of the occupied shell is usually well correlated with the size of the hermit crab and therefore is considered as adequate. Regression analyses conducted to assess different shell species inhabited by D. insignis, considering CSL and CWW vs. SAW and SIV, showed the highest correlation coefficients. These relationships also resulted in high determination coefficients for the hermit crab P. diogenes (Bertini and Fransozo, 2000). On the other hand, the relationships between shell weight (SDW) and hermit size and weight (CSL and CWW) showed the smallest coefficients, probably because regressions calculated based on shell weight (SDW) do not reflect properly the fit between the hermit crab and the shell because encrusting epifauna can increase the weight of the shell considerably (e.g. Conover, 1978; Sandford, 2003). Nevertheless, one can conclude that, on the southeastern coast of Brazil, the species D. insignis occupies shells that are adequate to their morphology. The variation in shell use patterns demonstrates that its occupation by the specie investigated in the present study is strongly linked: (1) to the availability of this resource in nature, possibly including the presence for occupying the shell of the gastropod O. urceus; and (2) to the animal size. Thus, the smallest hermits occupied a greater variety of shells, 114

123 Shell occupation by D. insignis Frameschi IF 2014 taking into account that there is a greater availability of small gastropod s shells than large gastropod s shells, according with Bollay (1964) small individuals may not be considered so dependent on a determinate gastropod shell species as the big ones are. Consequently, the larger individuals (males) do not find many shells options, preferring to occupy the T. galea, due it has low weight comparing to others with similar size (Zidona dufresnei and Semicassis granulata). The specialized occupation of shells, especially by larger individuals, together with the reproductive strategies of D. insignis (see Miranda et al., 2006) are factors that determine the marked abundance of the species in the non-consolidated sublittoral of the subtropical region of the Brazilian coast. References ABRAMS, PA., Resource partitioning and interspecific competition in a tropical hermit crab community. Oecologia, vol. 46, p ABRAMS, PA., Sexual difference in resource use in hermit crabs; consequences and causes. In: CHELAZZI, G. and VANNINI, M. (Eds.). Behavioral adaptations to intertidal life. New York: Plenum Press. p ASAKURA, A., Sexual differences in life history and resource utilization by the hermit crab. Ecology, vol. 76, no. 7, p AYRES-PERES, L., SOKOLOWICZ CC., KOTZIAN, CB., RIEGER, PJ. and SANTOS, S., Ocupação de conchas de gastrópodes por ermitões (Decapoda, Anomura) no litoral de Rio Grande, Rio Grande do Sul, Brasil. Iheringia, vol.98, no. 2, p AYRES-PERES, L., QUADROS, AF. and MANTELATTO, FL., Comparative analysis of shell occupation by two southern populations of the hermit crab Loxopagurus loxochelis (Decapoda, Diogenidae). Brazilian Journal of Oceanography, vol. 60, no. 3, p BERTINI, G. and FRANSOZO, A., Patterns of utilization in Petrochirus diogenes (Decapoda, Anomura, Diogenidae) in the Ubatuba region, São Paulo, Brazil. Journal of Crustacean Biology, vol. 20, no. 3, p BERTNESS, MD., 1980.Shell preference and utilization patterns in littoral hermit crabs of the Bay of Panama. Journal of Experimental Marine Biology and Ecology, vol. 48, p. 1-16, BERTNESS, MD., The influence of shell-type on hermit crab growth rate and clutch size. Crustaceana, vol. 40, p BLACKSTONE, NW. and JOCSLYN, AR., Utilization and preference for the introduced gastropod Littorina littorea (L.) by the hermit crab Pagurus longicarpus (Say) at Guilford, Connecticut. Journal of Experimental Marine Biology and Ecology, vol. 80, p

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125 Shell occupation by D. insignis Frameschi IF 2014 HAZLETT, BA., RITTSCHOF, D. and BACH, CE., The effects of size and coil orientation on reproduction in female hermit crabs, Clibanarius vittatus. Journal of Experimental Marine Biology and Ecology, vol. 323, p HEBLING, NJ. and MANSUR, CB., Desenvolvimento larval de Dardanus insignis (Saussure) (Crustacea, Decapoda, Diogenidae) em laboratório. Zoologia, vol. 12, p IMAZU, M. and ASAKURA, A., Distribution, reproduction and shell utilization patterns in three species of intertidal hermit crabs on a rocky shore on the Pacific coast of Japan. Journal of Experimental Marine Biology and Ecology, vol. 184, p LITULO, C., Population structure and reproduction of the hermit crab Dardanus deformis (Anomura: Diogenidae) in the Indian Ocean.. Journal of the Marine Biological Association of the United Kingdom, vol. 85, no. 4, p MANJÓN-CABEZA, ME. and GARCÍA-RASO, JE., Population structure and growth of the hermit crab Diogenes pugilator (Decapoda: Anomura: Diogenidae) from the northeastern Atlantic. Journal of Crustacean Biology, vol. 18, no. 4, p MANTELATTO, FL. and GARCIA, RB., Shell utilization pattern of the hermit crab Calcinus tibicen (Diogenidae) from southern Brazil. Journal of Crustacean Biology, vol. 20, no. 3, p MANTELATTO, FLM., ALARCON, VF. and GARCIA, RB., Egg production strategies of the tropical hermit crab Paguristes tortugae from Brazil. Journal of Crustacean Biology, vol. 22, no. 2, p MARTINELLI, JM., MANTELATTO, FL. and FRANSOZO, A., Population structure and breeding season of the south Atlantic hermit crab, Loxopagurus loxochelis (Anomura, Diogenidae) from the Ubatuba region, Brazil. Crustaceana, vol. 75, no. 6, p MARTÍNEZ-IGLESIAS, JC. and GARCÍA-RASO, JE., The crustacean decapod communities of the coral reefs from southwestern Caribbean Sea of Cuba: species composition, abundance and structure of the communities. Bulletin of Marine Science, vol. 65, no. 2, p MEIRELES, AL., BIAGI, R. and MANTELATTO, FL., Gastropod shell availability as a potential resource for the hermit crab infralittoral fauna of Anchieta Island (SP), Brazil. Nauplius, vol. 11, no. 2, p MEIRELES, AL. and MANTELATTO, FL., Biological features of a puzzling symbiotic association between the hermit crab Dardanus insignis and the porcellanid crab Porcellana Sayana (Crustacea). Journal of Experimental Marine Biology and Ecology, vol. 362, p MEIRELES, AL. and MANTELATTO, FL., Shell use by Pagurus brevidactylus (Anomura, Paguridae): a comparison between laboratory and field conditions. Acta Zoologica Sinica, vol. 51, p MELO, GAS., Manual de identificação dos Crustacea Decapoda do litoral brasileiro: Anomura, Thalassinidea, Palinuridea, Astacidea. São Paulo: Plêiade. 551 p. MESCE, KA., Calcium-bearing objects elicit shell selection behavior in a hermit crab. Science, vol. 215, p MIRANDA, I., MEIRELES, AL., BIAGI, R. and MANTELATTO, FL., Is the abundance of the red brocade hermit crab Dardanus insignis (Decapoda: Anomura: Diogenidae) in the infralittoral region of southern Brazil determined by reproductive potential? Crustacean Research, vol. 6, p

126 Shell occupation by D. insignis Frameschi IF 2014 NEGREIROS-FRANSOZO, ML., FRANSOZO, A., MANTELATTO, FLM., PINHEIRO, MAA. and SANTOS, S., Anomuran species (Crustacea, Decapoda) in their ecological distribution at Fortaleza Bay sublittoral, Ubatuba, São Paulo, Brazil. Iheringia, vol. 83, p OHMORI, H.; WADA, S., GOSHIMA, S. and NAKAO, S., Effects of body size and shell availability on the shell utilization pattern of the hermit crab Pagurus filholi (Anomura: Paguridae). Crustacean Research, vol. 24, p RIEGER, P.J Os ermitões (Crustacea, Decapoda,Parapaguridae, Diogenidae e Paguridae) do litoral brasileiro. Nauplius, v. 5, p , RITTSCHOF, D., Chemical attraction of hermit crabs and other attendants to gastropod predation sites. Journal of Chemical Ecology, vol. 6, p SOKAL, RR. and ROHLF, FJ., Biometry: The principles and practice of biological research. New York: W. H. Freeman. 887 p. SPIGHT, TM., Availability and use of shells by intertidal hermit crabs. Biological Bulletin, vol. 152, p SANDFORD, F., Population dynamics and epibiont associations of hermit crabs (Crustacea: Decapoda: Paguroidea) on Dog Island, Florida. Memoirs of Museum Victoria, vol. 60, no. 1, p TEROSSI, M., ESPÓSITO, DLA., MEIRELES, AL., BIAGI, R. and MANTELATTO, FL., Pattern of shell occupation by the hermit crab Pagurus exilis (Anomura, Paguridae) on the northern coast of São Paulo state, Brazil. Journal of Natural History, vol. 40, no. 1-2, p TORATI, LS. and MANTELATTO, FL., Uncommon mechanism of egg incubation in the endemic Southern hermit crab Loxopagurus loxochelis: how is this phenomenon related to egg production? Acta Zoologica, vol. 89, p VANCE, RR., The role of shell adequacy in behavioral interactions involving hermit crabs. Ecology, vol. 53, p WADA, SH., OHMORI, S., GOSHIMA, S. and NAKAO, S., Shell size preference of hermit crabs depends on their growth rate. Animal Behaviour, vol. 54, p WASSENBERG, TJ. and HILL, BJ., The Effect of Trawling and Subsequent Handling on the Survival Rates of the By-catch of Prawn Trawlers in Moreton Bay, Australia. Fisheries Research, vol. 7, p WILBER, JR. TP., Influence of size, species and damage on shell selection by the hermit crab Pagurus longicarpus. Marine Biology, vol. 104, p WILBER, TPJ. and HERRNKIND, WF., Predaceous gastropods regulate new-shell supply to salt marsh hermit crabs. Marine Biology, vol. 79, p ZAR, JH., Biostatistical analysis. New Jersey: Prentice-Hall. 907 p 118

127 Capítulo V Shell occupation by the South Atlantic endemic hermit crab Loxopagurus loxochelis (Moreira, 1901) (Anomura: Diogenidae)

128 Shell occupation by L. loxochelis Frameschi et al

129 Shell occupation by L. loxochelis Frameschi et al

130 Shell occupation by L. loxochelis Frameschi et al

131 Shell occupation by L. loxochelis Frameschi et al

132 Shell occupation by L. loxochelis Frameschi et al

133 Shell occupation by L. loxochelis Frameschi et al

134 Shell occupation by L. loxochelis Frameschi et al

135 Shell occupation by L. loxochelis Frameschi et al

136 Shell occupation by L. loxochelis Frameschi et al

137 Shell occupation by L. loxochelis Frameschi et al

138 Shell occupation by L. loxochelis Frameschi et al

139 Shell occupation by L. loxochelis Frameschi et al