Universidade Estadual Paulista “Júlio de Mesquita Filho” - Campus de Botucatu Instituto de Biociências de Botucatu Programa de Pós-Graduação em Ciências Biológicas (Zoologia) TESE DE DOUTORADO Variação geográfica dos camarões Dendrobranchiata nas regiões Sudeste e Sul do Brasil: teste de hipóteses sobre o paradigma do efeito latitudinal Raphael Cezar Grabowski Orientador: Professor Dr. Antonio Leão Castilho Botucatu, São Paulo 2017 Universidade Estadual Paulista “Júlio de Mesquita Filho” - Campus de Botucatu Instituto de Biociências de Botucatu Programa de Pós-Graduação em Ciências Biológicas (Zoologia) Variação geográfica dos camarões Dendrobranchiata nas regiões Sudeste e Sul do Brasil: teste de hipóteses sobre o paradigma do efeito latitudinal Tese apresentada ao Programa de Pós- Graduação em Ciências Biológicas (Zoologia) da Universidade Estadual Paulista “Júlio de Mesquita Filho” (UNESP), Instituto de Biociências de Botucatu, como requisito parcial à obtenção do título de Doutor em Ciências Biológicas (Zoologia). Raphael Cezar Grabowski Orientador: Professor Dr. Antonio Leão Castilho Botucatu, São Paulo 2017 i “Muitas das verdades às quais nos apegamos dependem muito do nosso próprio ponto de vista”. Obi-Wan Kenobi “Nada existe de permanente, exceto a mudança”. Heráclito “Faça ou não faça. Tentativa não há”. Yoda ii Dedico esta tese aos meus familiares (pai, mãe, Ju e Nando), por nunca medirem esforços para que eu alcance meus objetivos; e à minha namorada, Ana Elisa, pelo apoio incondicional durante a construção deste estudo. Também, a todos os professores que já tive. Seria impossível obter este título sem o esforço (e muita paciência) de cada um de vocês. “Se vi mais longe, foi por estar em pé sobre ombros de gigantes” – Isaac Newton. iii Agradecimentos A Deus, Inteligência Suprema do universo e Causa Primária de todas as coisas. Ao meu orientador e amigo, professor Dr. Antonio Leão Castilho (Tony), pela confiança depositada ao longo dos dez anos em que trabalhamos juntos. Pelo tempo e esforço dedicados à minha orientação acadêmica, pela amizade, conselhos (os científicos e os nem tão científicos) e vasto conhecimento compartilhado. Por ter me cedido um quarto na saudosa “Rep do Tony” quando decidi tentar a Pós-Graduação, e por sempre ter acreditado na minha capacidade enquanto orientado. Muito obrigado por tudo, chefe! À Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), agência de fomento pela qual fui bolsista durante o doutorado. Às agências de fomento, das quais o apoio foi essencial à execução deste projeto: → Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, processos: #94∕4878-8; #98∕07090-3; #2009/54672-4; BIOTA #2010∕50188-8); → Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPQ, processos: #406006/2012-1; #PQ308653/2014-9); → Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES∕ Ciências do Mar, processo: #23038.004310/2014-85); → Fundação para o Desenvolvimento da UNESP (FUNDUNESP, Programa Primeiros Projetos, processo: #1214/2010 – DFP). Ao Professor Dr. Alexandre de Azevedo, pelo auxílio durante as coletas realizadas em Macaé, e ao Núcleo em Ecologia e Desenvolvimento Sócio-Ambiental de Macaé - NUPEM/UFRJ - pelo empréstimo das suas dependências para a realização das atividades de laboratório. Ao professor Dr. Fernando L. M. Mantelatto, coordenador do projeto BIOTA∕FAPESP (#2010∕50188-8), pelos auxílios durante coletas, disciplinas, congressos, bem como pelo conhecimento compartilhado. A todos os funcionários e diretores da Base de Pesquisa “Dr. João de Paiva Carvalho” (Instituto Oceanográfico da Universidade de São Paulo, Cananéia, SP), pela competência no serviço prestado e pela hospitalidade ao longo dos dois anos em que coletamos em Cananéia. Ao Programa Institucional de Bolsas de Doutorado Sanduiche no Exterior (PDSE) (processo: #99999.006696/2015-05), por viabilizar minha estadia em Lafayette Agradecimentos iv (Louisiana, Estados Unidos) por quatro meses, durante a análise dos resultados apresentados nesta tese. Ao professor Dr. Raymond Bauer, por ter me recebido gentilmente em seu laboratório. Por compartilhar seu imensurável conhecimento sobre a biologia de camarões e pelas sugestões na discussão dos resultados e redação dos manuscritos. A ele e a sua esposa, Lydia Bauer, por haverem me recebido na “Pousada Bauer”, além de me apresentarem ao estilo de vida sulista dos Estados Unidos, o que, para mim, foi uma experiência extraordinária. Muito obrigado! Aos professores fundadores do NEBECC (Núcleo de Estudos em Biologia, Ecologia e Cultivo de Crustáceos), Dr. Adilson Fransozo e Dra. Maria Lucia Negreiros Fransozo pela amizade e conhecimento compartilhado, conselhos e ensinamentos acadêmicos. Ao coordenador do Laboratório de Biologia de Camarões Marinhos e de Água Doce (LABCAM), professor Dr. Rogério Caetano da Costa (Cebola), pelas sugestões e conselhos no desenvolvimento do projeto que originou esta tese, e por todo o conhecimento compartilhado. Aos funcionários da Seção Técnica de Pós-Graduação e do Departamento de Zoologia, pela dedicação ao serviço prestado. Aos colegas de pós-graduação (Professores e alunos do NEBECC e LABCAM) que, em algum momento, nos auxiliaram nas coletas em Macaé, Ubatuba, Cananéia ou São Francisco do Sul. Sou muito grato a todos pelo esforço que todos tiveram na execução deste projeto. Aos desenvolvedores do site SCI-HUB, por fazerem a alegria de milhares de estudantes ao promover o acesso gratuito ao conhecimento. Aos pescadores que nos auxiliaram com as coletas em todas as regiões abordadas neste estudo, por entenderem a importância da pesquisa científica e, por isso, sempre nos ajudarem a encontrar a melhor forma de responder aos nossos objetivos. Aos colegas do NEBECC: Aline (Nonatinha), Augusto, Camila, Douglas, Eduardo (Frio), Gustavo (Gari), Israel, Luciana, Mariana (Magrela), Samara e Thiago (Cabelo) (Cabelo, valeu pela ajuda com o R!!), pelo conhecimento compartilhado, discussões (científicas ou não) e momentos de descontração. Aos colegas do Laboratório de Biologia de Camarões Marinhos e de Água Doce (LABCAM): Abner, Dalilla, Daphine, Emerson (Cotia), Gabriel (Woody), João (Nelito), Lizandra, Mateus, Régis (Tesouro), Sarah, Sabrina e Thiago (Chuck), pelo Agradecimentos v auxílio ao longo das coletas, troca de dados e parceria durante disciplinas, congressos e simpósios. Especialmente ao Woody e ao Chuck, por terem me ensinado muito do que eu sei sobre coletas de campo, e à Sabrina, por ter me ensinado a fazer a análise de crescimento populacional. Aos colegas do “Laborantonio”, ou “LabTony”: Ana Elisa, Ana (Foguete), Ana Karolyne, Alexandre (Dino), Geslaine, Gilson (Nérso), Giovanna (Uilsom), Isabela, João, Joyce, Laura, Mariana (Dona), Milena, Rafaela, Renan (Grégui) e Taimara (Chorão), pela colaboração direta ou indireta em coletas, análise de dados e discussões científicas. Pelos momentos de descontração em churrascos e congressos, e por tornarem os dias de trabalho e as pausas para um café mais divertidos. #VAITIME! À colega Joyce, pelas discussões (científicas e existenciais) cotidianas e pelo imenso auxílio durante a redação desta tese (os famosos “Jó, dá uma lida aqui?”). Também, por ter me ensinado (ou, ao menos, tentado ensinar) a encarar a vida com menos ansiedade. Aos grandes amigos que fiz durante a minha estadia em Lafayette: Amie (Amie Jo), Mohamed, Richard (Dick Delphin) e Tamela (Big Tam), por terem me acolhido tão bem desde que cheguei lá. Por terem me levado aos melhores restaurantes de fast- food e lojas outlet da cidade, pelas partidas de Uno, caronas, risadas e troca de experiências culturais. Muito obrigado! Aos colegas do Bloco II do Departamento de Zoologia do IBB, pelos empréstimos de livros, trocas de experiências, conhecimento compartilhado e pelos momentos de descontração. À família Castilho (Dr. Emanuel, dona Heloisa, Tony, Ricardo, Gustavo, Lucas e Vô) e agregados, por terem me recebido tão bem desde que decidi mudar para o estado de São Paulo. Pela consideração, pelos favores, abrigos e momentos de festa. Muito obrigado! Ao núcleo mineiro da família: Ana, Kiko, Kátia, Guto, Fer e Gio e agregados (avós, tios, primos, etc), pelo imenso carinho que recebi todas as vezes que fui para Uberaba. Por terem me recebido tão bem em sua família, e pelos churrascos, pizzas, viagens e momentos de descontração. Muito obrigado! Aos meus familiares (Pai, Mãe, Ju e Nando) e agregados (avó, tios, primos, etc), pelo imenso apoio que sempre me ofereceram, nas decisões pessoais e profissionais. Por Agradecimentos vi terem me injetado ânimo e persistência durante os momentos difíceis, e por sempre terem compartilhado dos meus objetivos. Muito obrigado! À minha namorada querida, Ana Elisa. Pelo apoio, compreensão e carinho incondicionais ao longo da realização deste estudo. Por ter aguentado firme todos os meus momentos de estresse e azedume (que não foram poucos: no trânsito, na preparação para o estágio no exterior, na qualificação, na redação da tese... entre tantos outros). Por sempre ter tido um abraço e um “calma, logo passa” quando eu precisei, e por sempre respeitar as minhas decisões e me apoiar de todas as maneiras. Enfim, por ser a minha companheira em todos os aspectos! Muito obrigado por tudo! Aos demais colegas que, em algum momento, tiveram algum grau de envolvimento na realização deste estudo, mas que a minha memória falha em lembrar. Muito obrigado! vii Sumário Considerações Iniciais .................................................................................................... 1 Os Dendrobranchiata e a fauna acompanhante ........................................................... 2 A variação latitudinal nos parâmetros populacionais de peneídeos ............................ 3 Sobre as espécies estudadas ......................................................................................... 5 Plano de estudo ............................................................................................................. 7 Referências ...................................................................................................................... 8 Capítulo 1: Local environmental conditions alter latitudinal patterns in population dynamics of Sicyonia dorsalis Kingsley, 1878 from southeastern Brazil Resumo .......................................................................................................................... 12 Abstract ......................................................................................................................... 13 Introduction .................................................................................................................. 14 Material and methods .................................................................................................. 17 Sampling ..................................................................................................................... 17 Environmental data ..................................................................................................... 18 Sex ratio and population structure ............................................................................. 18 Reproduction and recruitment .................................................................................... 19 Individual growth and longevity ................................................................................. 19 Results ............................................................................................................................ 20 Environmental data ..................................................................................................... 20 Population structure ................................................................................................... 23 Sex ratio ...................................................................................................................... 25 Individual growth and longevity ................................................................................. 25 Reproductive periodicity and juvenile recruitment..................................................... 29 Discussion ...................................................................................................................... 33 References...................................................................................................................... 38 Sumário viii Capítulo 2: Environmental singularities affect the population dynamics of the temperate-region shrimp species Pleoticus muelleri (Spence Bate, 1888) in the Atlantic upwelling zone, southeastern Brazil Resumo .......................................................................................................................... 48 Abstract ......................................................................................................................... 49 Introduction .................................................................................................................. 50 Material and methods .................................................................................................. 53 Sampling ..................................................................................................................... 53 Environmental data ..................................................................................................... 54 Population structure, growth and reproductive biology ............................................ 55 Data analysis .............................................................................................................. 56 Results ............................................................................................................................ 56 Population structure and growth ................................................................................ 56 Environmental factors ................................................................................................. 63 Sex ratio and reproductive biology ............................................................................. 66 The environmental influence over population dynamics ............................................ 67 Discussion ...................................................................................................................... 70 Environmental effects ................................................................................................. 70 Growth and reproductive aspects ............................................................................... 73 References...................................................................................................................... 76 Capítulo 3: Ecological evidences for the behavioral plasticity of Rimapenaeus constrictus (Stimpson, 1874): the responses of a tropical shrimp species to local environmental singularities in southeastern Brazil Resumo .......................................................................................................................... 85 Abstract ......................................................................................................................... 86 Introduction .................................................................................................................. 87 Material and methods .................................................................................................. 89 Biological sampling .................................................................................................... 89 Environmental data ..................................................................................................... 90 Sumário ix Population structure ................................................................................................... 91 Reproductive biology .................................................................................................. 91 Data analysis .............................................................................................................. 92 Results ............................................................................................................................ 92 Population structure ................................................................................................... 92 Environmental factors ................................................................................................. 95 The environmental influence over population dynamics ............................................ 97 Reproductive biology ................................................................................................ 100 Discussion .................................................................................................................... 101 The environmental influence over population structure ........................................... 101 Reproductive biology ................................................................................................ 105 References.................................................................................................................... 107 Considerações finais ................................................................................................... 114 Referências .................................................................................................................. 117 Considerações Iniciais Considerações iniciais 2 Os Dendrobranchiata e a fauna acompanhante Em uma recente revisão taxonômica, De Grave et al. (2009) apontaram que, atualmente, existem aproximadamente 15.000 espécies viventes pertencentes à ordem Decapoda Latreille, 1802. Os decápodes representam cerca de um terço de todos os crustáceos conhecidos, tendo como principal característica diagnóstica a presença de cinco pares de apêndices birremes, ou patas, os quais podem apresentar-se modificados, não sendo necessariamente utilizados apenas na locomoção (Kaestner 1970, Fransozo & Negreiros-Fransozo 2016). Esta ordem subdivide-se em duas subordens: Pleocyemata Burkenroad, 1963 (indivíduos que utilizam filobrânquias ou tricobrânquias para trocas gasosas, e desenvolvimento embrionário pleopodial) e Dendrobranchiata Spence Bate, 1888 (de modo geral, exclusiva a animais que apresentam dendrobrânquias como principal estrutura de trocas gasosas e desenvolvimento embrionário sem encubação pleopodial) (Fransozo & Negreiros-Fransozo 2016). À subordem Pleocyemata pertencem os caranguejos, siris, ermitões, tatuíras, lagostas e lagostins, enquanto que Dendrobranchiata inclui camarões marinhos, em sua maioria, peneídeos (superfamília Penaeoidea Rafinesque, 1815) e sergestídeos (superfamília Sergestoidea Dana, 1852) (Pérez-Farfante & Kensley 1997, Brusca & Brusca 2003, Fransozo & Negreiros- Fransozo 2016). Dentre os indivíduos inseridos em Dendrobranchiata, muitos apresentam considerável importância econômica na pesca de camarões no mundo inteiro, sendo que a maioria de tais espécies é atualmente explorada em níveis acima da sua sustentabilidade (Brusca & Brusca 2003). Dentre as espécies de camarão comercialmente exploradas, D’Incao et al. (2002) destacaram que ao longo da costa Sudeste do Brasil, são explorados principalmente os camarões-rosa Farfantepenaeus brasiliensis (Latreille, 1817) e F. paulensis (Pérez-Farfante, 1967), sete-barbas Xiphopenaeus kroyeri (Heller, 1862), barba-ruça Artemesia longinaris Spence Bate, 1888, santana Pleoticus muelleri (Spence Bate, 1888) e branco Litopenaeus schmitti (Burkenroad, 1936). Infelizmente, devido à baixa seletividade dos apetrechos de pesca comumente utilizados nesta atividade (Keunecke et al. 2007), não apenas as populações das espécies-alvo sofrem as consequências da atividade pesqueira, mas também todos os organismos que partilham do mesmo hábitat. De acordo com a Organização das Nações Unidas para Agricultura e Alimentação (FAO) (2015), a biomassa de organismos coletados acidentalmente e sem interesse comercial durante as pescas de camarão Considerações iniciais 3 (bycatch, ou fauna acompanhante) pode ser de 3 a 15 vezes maior que a de espécies de interesse comercial. Frente a esta situação, faz-se imprescindível que o subsídio intelectual utilizado na concepção de políticas de proteção dos estoques pesqueiros leve em consideração não apenas as espécies-alvo, mas também a fauna que compõe o bycatch. Apenas desta maneira torna-se possível evitar o colapso dos estoques de espécies que não possuem interesse comercial, todavia, representam um importante elo na cadeia trófica local. A variação latitudinal nos parâmetros populacionais de peneídeos Diversos autores (Bauer 1992, Clarke 1993, Boschi 1997, Castilho et al. 2007, Costa et al. 2010, entre outros) afirmam que parâmetros e recursos ambientais são fatores altamente influentes nos padrões observados na dinâmica populacional de uma espécie. Dentre os fatores que regem tais processos, é possível citar como exemplo a variação na temperatura e a consecutiva produtividade planctônica. Tais características, por sua vez, estão variavelmente condicionadas à latitude local, moldando a distribuição e ciclo de vida de tais organismos. Adicionalmente, Lenihan & Micheli (2001) apontam que tais diferenças em cada gradiente latitudinal estão atadas às mudanças adaptativas observadas em comunidades bentônicas, as quais são associadas ao movimento, transporte, isolamento e às inter-relações entre as espécies. Portanto, cada espécie possui uma amplitude geográfica específica, e sua distribuição se encontra mais ou menos limitada por condições ambientais e, assim, cercada por áreas que dificultam o estabelecimento satisfatório de uma população, por prejudicar sua sobrevivência ou reprodução. Dentro deste contexto, vale lembrar que cada fator ambiental apresenta um gradiente de variação específico, e que as espécies respondem de formas distintas quanto à tolerância apresentada aos mesmos, podendo ser consideradas euritópicas (ecologicamente tolerantes) ou estenotópicas (ecologicamente intolerantes). Independentemente do grau de tolerância apresentado, cada espécie só pode atingir a eficiência plena de suas funções em uma porção mais ou menos limitada de cada gradiente, e em direção a qualquer um dos seus limites, a espécie sofre um crescente estresse fisiológico. Assim, a amplitude e a localização de tais limites, junto da mudança dos padrões de abundância dentro desses limites refletem na dinâmica populacional e na influência dos fatores ambientais na sobrevivência, reprodução e dispersão dos indivíduos (Brown & Lomolino 2006, Cox & Moore 2009). Considerações iniciais 4 Considerando-se camarões peneóideos, há muito é sugerida a existência de um paradigma (= padrão) geográfico em parâmetros de sua dinâmica populacional (Bauer 1992, Boschi 1997, Costa & Fransozo 2004, Castilho et al. 2007, entre outros). Considerando este paradigma, supõe-se, por exemplo, que indivíduos de uma mesma espécie sejam aptos a atingir tamanho corpóreo maior e viver por mais tempo em latitudes maiores, quando comparados a camarões amostrados em regiões mais próximas ao equador (Bauer 1992). A razão para a ocorrência de tal padrão seria a variação nos fatores ambientais ao longo da distribuição das espécies (especialmente temperatura), somada à variação na disponibilidade de recursos alimentares, especialmente para as fases larvais iniciais. Sendo assim, a tendência à homogeneidade nas condições climáticas observadas em ambientes marinhos tropicais seria responsável pela continuidade na periodicidade reprodutiva nestes locais, enquanto que em regiões de maiores latitudes, a flutuação climática ao longo do ano levaria a uma maior sazonalidade reprodutiva, por exemplo (Orton 1920, Baker 1938, Thorson 1950). Porém, a região costeira do Brasil apresenta diversas singularidades, as quais apresentam potencial suficiente para influenciar, ou até mesmo alterar o padrão observado nos parâmetros populacionais em peneídeos. Nesta área, localizada em uma região subtropical conhecida como “zona de ressurgência do Atlântico”, a circulação oceânica é dominada pelos fluxos opostos das correntes do Brasil (subtropical) e das Malvinas (subantártica), as quais se encontram na latitude média de 36ºS. Dentre as massas de água que influenciam a região, estão a Água Central do Atlântico Sul (ACAS), a Água Costeira e a Água Tropical. A mistura de características de diferentes fontes pode resultar em um aumento na produção primária e, consecutivamente, de produção secundária e, dentre elas, a ACAS é a que surte mais efeitos em áreas rasas, ainda que seja formada em regiões distantes da costa (Acha et al. 2004). A ACAS aproxima-se da região costeira durante o fim da primavera, e traz consigo baixa salinidade e temperatura, como resultado da mistura das correntes do Brasil e das Malvinas, emergindo também em uma situação de ressurgência na região de Cabo Frio (Castro-Filho et al. 1987, Castro-Filho & Miranda 1998, Acha et al. 2004). Como consequência de tais singularidades, é possível observar, em regiões tropicais, temperaturas similares às de regiões temperadas, em uma situação contrária ao esperado onde, teoricamente, regiões com menores latitudes apresentariam médias de temperatura mais elevadas (Brown & Lomolino 2006, Cox & Moore 2009). Considerações iniciais 5 Sobre as espécies estudadas Partindo deste princípio, nesta tese, três espécies de camarões Dendrobranchiata pertencentes a famílias distintas foram analisadas quanto à variação latitudinal nos parâmetros de sua dinâmica populacional. Popularmente conhecido como “camarão santana”, P. muelleri (Penaeoidea: Solenoceridae) (Fig. 1) completa seu ciclo de vida inteiramente no ambiente marinho, sendo encontrado exclusivamente ao longo do Atlântico Ocidental, do estado do Rio de Janeiro (23ºS), Brasil, à província de Santa Cruz, na Argentina (50ºS) (Boschi 1997, Costa et al. 2003). Sicyonia dorsalis Kingsley, 1878 (Penaeoidea: Sicyoniidae) (Fig. 2), conhecida popularmente como “camarão pedra”, distribui-se do estado de Carolina do Norte (34ºN), Estados Unidos, até o estado de Santa Catarina (26ºS), no Brasil (Costa et al. 2003), habitando a região costeira durante todo seu ciclo de vida (Dall et al. 1990). Popularmente conhecido como “camarão ferrinho”, Rimapenaeus constrictus (Stimpson, 1874) (Penaeoidea: Penaeidae) (Fig. 3) distribui-se da província de Nova Escócia (43ºN) (Canadá) ao estado de Santa Catarina (26ºS) (Brasil), em profundidades de até 127 m, completando seu ciclo de vida inteiramente em ambiente oceânico (Dall et al. 1990, Costa et al. 2003). As espécies foram amostradas em quatro regiões distintas ao longo de sua distribuição na costa brasileira, dentro de uma variação latitudinal de aproximadamente cinco graus: Macaé, RJ (≈22ºS), Ubatuba, SP (≈23ºS), Cananéia, SP (≈25ºS) e São Francisco do Sul, SC (≈26ºS). Considerações iniciais 6 Figura 1: Pleoticus muelleri, vista lateral. Imagem: Castilho AL, 2010. Figura 2: Sicyonia dorsalis, vista lateral. Imagem: Castilho AL, 2010. Figura 3: Rimapenaeus constrictus, vista lateral. Imagem: Castilho AL, 2010. Considerações iniciais 7 Plano de estudo À sombra do cenário descrito acima, o esforço amostral foi realizado com o intuito de testar as seguintes hipóteses:  A periodicidade reprodutiva das espécies se altera conforme a posição latitudinal em que se encontram. Em latitudes menores, existe uma tendência de continuidade no período reprodutivo, e conforme há um aumento na latitude, este tende a apresentar uma maior sazonalidade, devido à variação nas condições ambientais que influenciam seu desenvolvimento gonadal e o desenvolvimento inicial da prole;  A estrutura populacional apresenta diferentes características quando analisada em localidades diferentes, podendo apresentar diferenças no que diz respeito ao tamanho do corpo quando são amostradas em latitudes distintas. Para locais de maior latitude, presume-se que os indivíduos alcancem maiores tamanhos, bem como maturidade sexual tardia, quando comparados àqueles observados em latitudes inferiores;  Os peneóideos atingem maiores constantes de crescimento quando em latitudes menores, resultando em comprimentos assintóticos e longevidades menores, quando comparados com estimativas realizadas para indivíduos coletados em latitudes maiores, resultado da variação climática ao longo do gradiente latitudinal;  As características ambientais singulares encontradas ao longo da costa Sudeste e Sul do Brasil apresentam força suficiente para alterar os padrões esperados na dinâmica populacional dos peneóideos, como resultado da história de vida de cada espécie, que pode responder de formas distintas a tal cenário. Para testar as hipóteses propostas acima, a presente tese conta com três capítulos, redigidos sob a forma de artigo científico. Vale lembrar que, através da oportunidade oferecida pelo Programa Institucional de Bolsas de Doutorado Sanduiche no Exterior (PDSE, processo #99999.006696/2015-05), foi possível analisar os dados aqui apresentados sob a supervisão do professor Dr. Raymond T. Bauer, na Universidade de Luisiana em Lafayette (Lafayette, LA, Estados Unidos). Este pesquisador trouxe valiosas sugestões na análise, redação e discussão dos resultados, motivo pelo qual os capítulos foram redigidos em inglês (facilitando assim o processo Considerações iniciais 8 de correção, no qual o professor Raymond teve participação efetiva). Também, a escrita dos capítulos em inglês certamente facilitará e encurtará o processo de publicação, realizadas as correções sugeridas pela banca examinadora da tese. O primeiro capítulo abordará a variação geográfica nos parâmetros populacionais (estrutura populacional, biologia reprodutiva e crescimento populacional) de S. dorsalis. Excepcionalmente neste capítulo, os parâmetros de crescimento populacional foram analisados sob uma óptica temporal, com dados provenientes de amostras obtidas com um intervalo de 10 anos. Esta singularidade foi adicionada ao esforço amostral com o objetivo de testar a influência da criação de uma área de proteção ambiental (APA) em Ubatuba, uma vez que as amostras foram realizadas em um período antes (2001-2003) e outro depois (2013-2014) da criação da APA (no ano de 2008). No segundo capítulo, a espécie P. muelleri foi analisada quanto aos parâmetros de sua dinâmica populacional (crescimento e estrutura populacional, e biologia reprodutiva) e, por fim, no terceiro capítulo, foram analisados os parâmetros de biologia reprodutiva e estrutura populacional de R. constrictus. Referências Acha EM, Mianzan HW, Guerrero RA, Favero M & Bava J, 2004. Marine fronts at the continental shelves of austral South America: Physical and ecological processes. Journal of Marine Systems, 44(1-2): 83-105. Baker JR, 1938. The evolution of breeding seasons. In: Evolution, Essays on Aspects of Evolutionary Biology presented to Professor Goodrich ES on his seventieth Birthday. De Beer GR (ed.), Oxford University Press, London and New York, pp. 161-177. Bauer RT, 1992. Testing generalizations about latitudinal variation in reproduction and recruitment patterns with sicyoniid and caridean shrimp species. Invertebrate Reproduction and Development, 22(1-3): 193-202. Boschi EE, 1997. Las pesquerías de crustáceos decápodos en el litoral de la República Argentina. Investigaciones Marinas 25: 19-40. Brown JH & Lomolino MV, 2006. Biogeografia - 2ª Edição. Ribeirão Preto; Funpec Editora. Brusca RC & Brusca GJ, 2003. Invertebrados. Segunda edição. Editora Guanabara- Koogan, Rio de Janeiro, Brasil, 968 p. Clarke A, 1993. Reproductive trade-offs in caridean shrimps. Functional Ecology, 7(4): 411-419. Considerações iniciais 9 Castilho AL, Gavio MA, Costa RC, Boschi EE, Bauer RT & Fransozo A, 2007. Latitudinal variation in population structure and reproductive pattern of the endemic South American shrimp Artemesia longinaris (Decapoda: Penaeoidea). Journal of Crustacean Biology, 27(4): 548-552. Castro-Filho BM, Miranda LB & Miyao SY, 1987. Condições hidrográficas na plataforma continental ao largo de Ubatuba: variações sazonais e em média escala. Boletim do Instituto Oceanográfico, 35(2): 135-151. Castro-Filho BM & Miranda LB, 1998. Physical oceanography of the western Atlantic continental shelf located between 4° N and 34° S coastal segment (4° W). In Robinson AR & Brink KH (eds.). The Sea. Wiley, New York: 209-251. Costa RC, Branco JO, Machado IF, Campos BR & Avilla MG, 2010. Population biology of shrimp Artemesia longinaris (Crustacea: Decapoda: Penaeidae) from the southern coast of Brazil. Journal of the Marine Biological Association of the United Kingdom, 90(4): 663-669. Costa RC & Fransozo A, 2004. Reproductive biology of the shrimp Rimapenaeus constrictus (Decapoda, Penaeidae) in the Ubatuba region of Brazil. Journal of Crustacean Biology, 24(2): 274-281. Costa RC, Fransozo A, Melo GAS & Freire FAM, 2003. Chave ilustrada para identificação dos camarões Dendrobranchiata do litoral norte do estado de São Paulo, Brasil. Biota Neotropica, 3(1): 1-12. Cox CB & Moore PD, 2009. Biogeografia – uma abordagem ecológica e evolucionária. Rio de Janeiro; LTC. Dall W, Hill BJ, Rothlisberg PC & Sharples DJ, 1990. The biology of the Penaeidae. In: Blaxter JHS & Southward AJ (Eds.). Advances in Marine Biology. Academic Press, San Diego, pp. 1-489. De grave S, Pentcheff ND, Ahyong ST, Chan TY, Crandall KA, Dworschak PC, Felder DL, Feldmann RM, Fransen CHJM, Goulding LYD, Lemaitre R, Low MEY, Martin JW, NG PKL, Schweitzer CE, Tan SH, Tshudy D & Wetzer R, 2009. A classification of living and fossil genera of decapod crustaceans. Raffles Bulletin of Zoology, 1: 1-109. D’Incao F, Valentini H & Rodrigues LF, 2002. Avaliação da pesca de camarões nas regiões sudeste e sul do Brasil. Atlântica, 24(2): 103-116. Food and agriculture organization of the United Nations (FAO), 2015. Transforming wasted resources for a sustainable future. The sustainable management of bycatch in Considerações iniciais 10 Latin America and Caribbean trawl fisheries. Fisheries and Aquaculture Department, 8pp. Fransozo A & Negreiros-Fransozo ML (eds.), 2016. Zoologia dos Invertebrados, primeira edição. Roca, Rio de Janeiro, Brasil, 661 p. Kaestner A, 1970. Invertebrate zoology, vol. 3. Interscience Publishers, New York, USA, 523 p. Keunecke KA, Vianna M, Fonseca DB & D’Incao F, 2007. The pink-shrimp trawling bycatch in the northern coast of São Paulo, Brazil, with emphasis on crustaceans. Nauplius, 15:49-55. Lenihan HS & Micheli F, 2001. Soft-sediment communities. In: Bertness MD, Gaines SM & Hixon ME (eds.), Marine Community Ecology. Sinauer Associates, Massachusetts, pp 253-287. Orton JH, 1920. Sea temperature, breeding and distribution of marine animals. Journal of the Marine Biological Association of the United Kingdom, 12(2): 339-366. Pérez-Farfante I & Kensley B, 1997. Penaeoid and sergestoid shrimps and prawns of the world. Keys and diagnoses for the families and genera. Éditions du Muséum national d’Histoire naturalle, Paris, France, 233 p. Thorson G, 1950. Reproductive and larval ecology of marine bottom invertebrates. Biological Reviews, 25(1): 1-45. Capítulo 1 Local environmental conditions alter latitudinal patterns in population dynamics of Sicyonia dorsalis Kingsley, 1878 from southeastern Brazil Capítulo 1 12 Local environmental conditions alter latitudinal patterns in population dynamics of Sicyonia dorsalis Kingsley, 1878 from southeastern Brazil Resumo O objetivo deste estudo foi testar a hipótese de gradientes latitudinais na influência ambiental sobre parâmetros populacionais de Sicyonia dorsalis na costa sudeste do Brasil. Também, comparamos o crescimento da espécie em um período de dez anos na região de Ubatuba, amostrando cinco anos antes e cinco anos depois do estabelecimento de uma área de proteção marinha (APM). Amostras mensais foram realizadas em quatro regiões (Macaé (≈22ºS), Ubatuba (≈23ºS), Cananéia (≈25ºS) e São Francisco do Sul (≈26ºS)), utilizando barcos de pesca artesanal, em diferentes períodos entre julho de 2010 e junho de 2014. Para determinar a influência do estabelecimento da APM em Ubatuba, os parâmetros de crescimento também foram estimados para dados obtidos de julho de 2001 a junho de 2003. A influência da salinidade e temperatura da água de fundo foi testada utilizando a análise de correlação cruzada (p ≤ 0,05), e os períodos reprodutivos e de recrutamento foram considerados como os períodos com maior frequência de fêmeas reprodutivas e jovens, respectivamente, para cada região. Os parâmetros de crescimento foram analisados utilizando o modelo de crescimento de Von Bertalanffy, e a longevidade foi calculada a partir do mesmo modelo, invertido, comparando as curvas médias de cada região utilizando o teste F (p ≤ 0,05). Foram analisados 3.038 indivíduos, e em todas as regiões, as fêmeas atingiram maiores tamanhos, uma provável influência de seu sistema de cópula, o qual desconsidera o tamanho de machos, ou então uma adaptação para aumentar a fecundidade de fêmeas. As fêmeas também foram mais abundantes, uma consequência de diferentes atividades migratórias e taxas de mortalidade entre os sexos. Foi possível observar uma tendência à diminuição do tamanho corpóreo à medida que aumentou a latitude, o oposto à tendência esperada de aumento no tamanho corpóreo com o aumento da latitude, indicando uma conexão migratória entre grupos que podem pertencer a uma mesma população. Adicionalmente, os resultados da análise de crescimento mostraram um efeito positivo do estabelecimento da APM em Ubatuba, com uma tendência de aumento em tamanho assintótico entre 2001-2003 e 2013-2014. A reprodução apresentou uma tendência à sazonalidade em maiores latitudes, possivelmente induzida pela sazonalidade na disponibilidade de alimento larval e na influência de massas de água na costa brasileira. Capítulo 1 13 Local environmental conditions alter latitudinal patterns in population dynamics of Sicyonia dorsalis Kingsley, 1878 from southeastern Brazil Abstract The aim of this study was to test the hypothesis of latitudinal gradients in environmental influence over growth and reproductive parameters in Sicyonia dorsalis along the southeastern Brazilian coast. We also tested the differences in growth of the species over a ten-year period in Ubatuba, where data was collected 5 years before and then 5 after the establishment of a marine protected area (MPA). Monthly samples were carried out in four different regions throughout the Brazilian coastal area (Macaé (≈22ºS), Ubatuba (≈23ºS), Cananéia (≈25ºS) and São Francisco do Sul (≈26ºS)), using artisanal fishing boats, in different periods from July 2010 through June 2014. To determine the influence of the establishment of the MPA in Ubatuba, we also estimated growth parameters for data sampled from July 2001 through June 2003. We tested the influence of bottom water temperature and salinity over the population dynamics using cross-correlation analyses (p ≤ 0.05). Reproductive and juvenile recruitment periodicity were considered as the periods with higher frequency of reproductive females and immature individuals, respectively, for each region separately. Growth parameters were analyzed using the Von Bertalanffy’s growth model, while longevity was calculated using its inverse formula, comparing the results for each region by the F test (p ≤ 0.05). We analyzed 3,038 individuals to its reproductive and growth aspects. In all regions, female were bigger than males, a likely evolutionary influence of their mating system, in which there is no selection for larger males, or an adaptation to increase females size and consequent fecundity. Females were also more abundant, a consequence of different migration activities and mortality rates between sexes. There was a decreasing trend in maximum body size and asymptotic length as latitude increased, the opposite of the expected trend of larger body size with increasing latitude, what can be considered as an evidence of the migratory connection between groups that are part of the same population. The estimated growth analyses’ results also showed a possible positive effect of the establishment of the MPA in Ubatuba, since we observed an increasing trend in asymptotic lengths estimated for 2001-2003 and 2013-2014. We observed a tendency towards seasonal reproduction in higher latitudes, possibly induced by the seasonality in larval food availability and the influence of water masses along the Brazilian coast. Capítulo 1 14 Introduction Environmental factors often show gradients with latitude and depth in marine habitats, and different species tend to respond differently to such gradients (Bauer 1992, Eckelbarger & Watling 1995). The location and amplitude of these gradients may cause variable effects on the population dynamics (abundance, mortality, growth, reproduction, etc.) on both ecologically and commercially important species (Brown & Lomolino 2006, Cox & Moore 2009). Generalizations about biological phenomena are useful in summarizing knowledge, serving as models or paradigms which stimulate proposal and testing of hypotheses on factors responsible for observed patterns. Quite often, however, such generalizations are oversimplifications, and do not hold up as further studies are conducted about them, often with the discovery of contradictory or unexpected results (Bauer 1992, Marquet et al. 2004, Fernández et al. 2009). Trends in growth rates and reproductive periodicity can be observed in marine animals that are correlated with gradients in environmental seasonality. Individuals of tropical populations tend to be smaller in size than those from higher latitudes, and continuous reproduction in the tropics becomes increasingly seasonal with the increase in latitude (Thorson 1950, Bauer 1992, Hartnoll 2001). According to Hartnoll (2001), the impact of basic environmental factors (e.g., temperature, salinity, nutrient concentrations, food for planktonic larvae) on growth and reproduction have been demonstrated under laboratory conditions and can vary spatially and temporally in the natural environment. In general, an increase in temperature accelerates growth in crustaceans by shortening the intermoult period, increasing moult increment, or both. This has an antagonistic effect on growth rate, because reducing time between moults also reduces the size increment at each moult. Nonetheless, the former effect is proportionately greater, and thus the almost universal outcome is an increase in growth rate. On the other hand, decreases in temperature increase intermoult interval, but it leads to an increased molt increment in size, as well as an increase in lifespan. Thus, at higher latitudes, the net effect on growth is positive, and marine organisms from higher latitudes often attain larger body size than conspecifics or congenerics from lower latitudes (e.g., Pandalus borealis Krøyer, 1838, Haynes & Wigley 1969; Sicyonia spp., Bauer 2004). Orton (1920) first hypothesized that temperature is responsible for reproductive periodicity of marine invertebrates. According to this author, a constant warm temperature condition in tropical seas is the main cause for their continuous Capítulo 1 15 reproduction. Seasonal variation in water temperature, which is generally associated with subtropical to polar latitudes, is an environmental factor affecting gametogenesis, thus imposing reproductive seasonality in these animals outside of the tropics. On the other hand, Thorson (1950) postulated that the major selective pressure on the timing of reproduction for species with planktotrophic larvae is the seasonal variation in larval food supply (primary and secondary productivity), which is correlated with seasonality of factors affecting productivity. The variation in food supply for planktotrophic larvae of crustaceans, molluscs, and other marine species may be considered the ultimate factor (“evolutionary” cause) selecting for different patterns of reproductive seasonality. Therefore, environmental variables such as temperature, photoperiod, and nutrient concentration can be considered as environmental cues, or “proximate factors”, acting on reproduction and growth, which are highly correlated with the ultimate factor, larval food supply (Baker 1938, Bauer 1992, Marshall et al. 2012). Castilho et al. (2007b) pointed out that such a latitudinal pattern is applicable for Artemesia longinaris Spence Bate, 1888, a penaeid shrimp. The authors compared populations from Ubatuba, southeastern Brazil (23ºS), and Mar del Plata, east-central Argentina (37ºS), and found that in the higher latitude location, individuals reached larger body sizes than those at the tropical location. Additionally, there was a delay in the size of sexual maturity, suggesting that environmental factors such as water temperature and primary productivity could be responsible for such a difference. However, such a pattern does not seem to be applicable to all shrimp species occurring along the Brazilian coast. Grabowski et al. (2014) estimated growth parameters for Xiphopenaeus kroyeri (Heller, 1862) in the adjacent area from Babitonga Bay, southern Brazil, and compared their results to other studies along the Brazilian coast within 10 degrees of latitude range (Santos & Ivo 2000, Campos et al. 2011, Heckler et al. 2013). No latitudinal patterns were found. Grabowski et al. (2014) stated that genetic variation among populations, methodological differences among the studies compared, and effects of fishing pressure might contribute to this lack of latitudinal pattern. Additionally, Acha et al. (2004) pointed out some local variation in currents and water masses in this region which might explain the deviation from an expected latitudinal pattern. They pointed out that the Brazilian coast is strongly influenced by marine fronts, i.e., transitional regions, created by combining features of water masses such as the South Atlantic Central Water (SACW), Coastal Water (CW) and Tropical Water (TW). The SACW is often formed in regions far from the coast; however, it can Capítulo 1 16 get closer in late spring and early summer, in depths of 10-15 m. The SACW brings lower salinity and temperature (temperature: < 18 ºC; salinity: < 36 psu) by mixing water from the warm Brazilian current (temperature: > 20 ºC; salinity: > 36 psu) and the cold Falklands current (temperature: < 15 ºC; salinity: < 34 psu), and emerges in the Cabo Frio region as an important upwelling area (Castro-Filho & Miranda 1998, Acha et al. 2004). According to Merino & Monreal-Gómez (2009), upwelling is the physical process that most influences marine organisms in the regions where it occurs. Some studies carried out in upwelling areas have shown dramatic effects on the genetic structure, distribution and reproductive biology of A. longinaris (Carvalho-Batista et al. 2014, Sancinetti et al. 2014, 2015), reproductive biology of X. kroyeri (Silva et al. 2015) and shrimp species diversity and distribution (Pantaleão et al. 2016). The approach of the SACW to the coastal region of Brazil and its upwelling in Cabo Frio region results in a decrease in bottom water temperature, which has a retarding effect on growth and reproduction of tropical species. However, upwelling leads to a transport of nutrients from the lower layers into the euphotic zone, which influences primary productivity and the subsequent larval food supply (Valentin 1984, Odebrecht & Castello 2001, Gaeta & Brandini 2006), so that the SACW is a water mass high in nutrient concentration. There is a considerable concern and effort to improve fisheries management of penaeoid species in Brazilian waters (Pitcher 2000). The current legislation concerning Brazilian fisheries imposes a closed season on shrimp fishing in southern and southeastern coastal waters from March through May (IBAMA, CEPSUL). In addition, the Brazilian Ministry of the Environment has established MPAs (Marine Protected Areas) in which commercial fishing is not allowed (Almeida et al. 2012). Investigation on growth and longevity in shrimp species is needed not only to understand their basic population biology, but as importantly, to provide basic information necessary for their conservation and management (Die 1992, Keunecke et al. 2008, Vogt 2012). The penaeoid shrimp Sicyonia dorsalis Kingsley, 1878 is not commercially fished, primarily because of its small size. However, this species makes up to 92% of all of the sicyoniid species captured as bycatch in Brazilian waters, and is the seventh most abundant penaeoid species taken. The lack of economic interest does not justify the exclusion of a given species from the current fishing management, and it is necessary to highlight their ecological importance as components in the food web (Severino-Rodriguez et al. 2002, 2007, Graça-Lopes et al. 2002, Costa et al. 2005, Castilho et al. 2008c). We consider it Capítulo 1 17 a good penaeoid species model, with which to study effects of MPAs on growth and other population parameters in shrimp fisheries in Brazilian waters. The aim of this study was to test the hypothesis of latitudinal gradients in growth and reproductive parameters in S. dorsalis over a relatively narrow range of latitude along the Brazilian coast. We also measured variation in basic abiotic factors in sample locations to determine if they might be responsible for any deviation from the expected latitudinal pattern. Additionally, we tested the null hypothesis of no differences in growth over a ten-year period at a location in which data was collected for 5 years before and then after the establishment of a marine protected area. Material and methods Sampling Samples were carried out in four different regions throughout the Brazilian coastal area, covering a 5-degrees range of latitude (Fig. 1). For all sampling locations, similar gear and methods were adopted to avoid sampling failures and consequent errors in estimation of parameters. Sampling was carried out using shrimp-fishing boats outfitted with double-rig nets the same size and mesh as used in in artisanal fishing (mesh size: ≅3 cm; mesh gap: ≅11.5 m; boat velocity during trawls: ≅1.5 knots; total distance traveled during trawls: ≅0.5 miles), with monthly 30-min trawling at each sampling station for each region. In the Macaé region (MA) (≈22ºS), in northern Rio de Janeiro state, six sampling stations were selected, covering 5-15 m depth from July 2010 through June 2011. In the Ubatuba region (UB I) (≈23ºS), northern São Paulo state, four sampling stations were adopted, covering a 5-15 m depth variation, from July 2013 through June 2014. For long-term comparison of growth parameters in this area, we also analyzed data sampled from July 2001 through June 2003 at Ubatuba (UB II) (sampling in Castilho et al. 2008b), comprising six sampling stations under a 5-35 m depth. In the Cananéia region (CA) (≈25ºS), southern São Paulo state, seven stations (5-15 m depths) were sampled from July 2012 through May 2014. In the São Francisco do Sul region (SFS) (≈26ºS), five sampling stations were sorted, covering a 5-17 m depth variation (Fig. 1), from July 2010 through June 2011. Capítulo 1 18 Figure 1: Map of the Brazilian coastal area, highlighting the southeastern littoral and the sampling locations. Environmental data Since S. dorsalis only inhabits the bottom, only temperature and salinity of bottom were included in analyses. Bottom water samples were taken for each month using a Van Dorn bottle. Temperature was measured with a mercury thermometer, and salinity was determined using an optical refractometer. To assess the influence of environmental factors on the abundances of reproductive females and adult males, and juveniles (new recruits) and their interaction, we performed cross-correlation analyses. In such analyses, two data series are compared as a function of time lag (n), measuring the relationships between values of one data series and another months earlier (negative lag) or months later (positive lags), using the Pearson correlation coefficient. A correlation coefficient value of lag 0 shows no lag (Statsoft 2011). We considered lag coefficient values higher than 0.5 (positive or negative) as biologically significant when the analysis was statistically significant (p ≤ 0.05). Sex ratio and population structure At all sampling locations, individuals were identified to species (Costa et al. 2003), carapace length (CL) measured with vernier calipers as the linear distance from the posterior border of the carapace to the orbital angle (to the nearest 0.1 mm) and sexed according to the presence of a thelycum in females, and petasma in males (Pérez- Farfante & Kensley 1997). Sex ratio was calculated as the quotient between the Capítulo 1 19 abundance of males and the total abundance of individuals per month. Deviations from 0.5 (a 1:1 sex ratio) were tested by a binomial test (p ≤ 0.05) (Wilson & Hardy 2002, Baeza et al. 2013). The length frequency distribution was evaluated separately for each sex using 1-mm CL intervals. Both were compared using Kolmogorov-Smirnov two- sample tests (p ≤ 0.05), for each location separately, in which the null hypothesis adopted was that size distribution among sexes did not differ (Zar 1999, Castilho et al. 2008c). Reproduction and recruitment The reproductive condition of females was assessed by macroscopic observation of the degree of ovarian development, according to its color and volume occupied in the cephalothorax, which is visible through the transparent exoskeleton (Castilho et al. 2007a, 2008a, c). Thus, ovaries were classified as immature (juveniles) (ovaries varying from thin transparent strands to thicker strands); spent (whitish colored ovaries, much larger and thicker than the ones observed for juveniles); and reproductive (thicker ovaries ranging from light to olive green). Reproductive intensity was given as the frequency (percentage) of reproductive females in the adult (spent and reproductive gonadal stages) population, monthly, for each region (Castilho et al. 2008a, c). In penaeid shrimps, male sexual maturity is, in general, assessed by observation of the degree of linking of the petasmal lobes. In this study, sexual condition in males was defined as mature when petasmal lobes (endopods of first pleopods) were linked and immature (juveniles) when not (Boschi 1989, Bauer & Rivera Vega 1992, Castilho et al. 2008a, c). Juvenile recruitment was estimated as the percentage of juveniles in the entire monthly population sample. Individual growth and longevity Growth and longevity were analyzed only for females since the abundance of males was not sufficient to distinguish monthly cohorts. Growth analysis was performed based on the Von Bertalanffy growth model (Von Bertalanffy 1938), following the methodology proposed by Simões et al. (2013) as follows: modal peaks (CL) were obtained with the software PeakFit (Automatic Peak Fitting Detection and Fitting, Method I-Residual, no Data Smoothing), using 0.5 mm size classes. The modal peaks were plotted on a scatter graph vs. age, in order to assess the cohort growth. The growth parameters (CL∞: asymptotic carapace length; k: growth coefficient (day-1); t0: Capítulo 1 20 theoretical age at size zero) were estimated using the Solver supplement in Microsoft Excel (v. 2013) for Windows 7, which applies the Von Bertalanffy growth model: CLt=CL∞[1-exp-k(t-t0)] (CLt: carapace length at age t). The validation of a cohort was evaluated based on its similarity to the maximum body sizes sampled for each area. Growth data were pooled and growth parameters were estimated. The average growth curves obtained for each region were compared to each other using the F test (p ≤ 0.05), in order to attest if they were different (one region from another) (Cerrato 1990). Longevity was estimated using the inverse Von Bertalanffy growth model, with a modification suggested by D’Incao & Fonseca (1999): longevity=0-(1/k)Ln[1- (CLt/CL∞)] (considering t0= 0, and CLt/CL∞= 0.99). Results Environmental data Monthly mean values of bottom water salinity varied from 35.7 to 38 psu in MA (average mean: 36.9 psu); from 34.3 to 37 psu in UB I (average mean: 35.5 psu); from 20.6 to 36.1 psu in CA (average mean: 31.5 psu); and from 31.4 to 35.6 psu in SFS (average mean: 33.4 psu) (Fig. 2). Bottom water temperature monthly means varied from 19.5 to 22.9 ºC in MA (average mean: 20.8 ºC); from 19.9 to 25.5 ºC in UB I (average mean: 22.5 ºC); from 17.5 to 29.3 ºC in CA (average mean: 23.3 ºC); and from 18.2 to 26.1 ºC in SFS (average mean: 22.3 ºC) (Fig. 3). Capítulo 1 21 Figure 2: Monthly mean values on bottom water salinity (psu) sampled from: A) July 2010 through June 2011 in the Macaé region; B) July 2013 through June 2014 in the Ubatuba region; C) July 2012 through May 2014 in the Cananéia region; and D) July 2010 through June 2011 in the São Francisco do Sul region. SE: standard error; Min: minimum values; Max: maximum values. Capítulo 1 22 Figure 3: Monthly mean values on bottom water temperature (ºC) sampled from: A) July 2010 through June 2011 in the Macaé region; B) July 2013 through June 2014 in the Ubatuba region; C) July 2012 through May 2014 in the Cananéia region; and D) July 2010 through June 2011 in the São Francisco do Sul region. SE: standard error; Min: minimum values; Max: maximum values. Capítulo 1 23 Population structure During the sampling period, 3,038 individuals were collected and used in analyses of population structure and reproductive parameters: 571 from MA, 1,034 from UB I, 1,131 from CA and 301 from SFS. In all regions, females were more abundant than males, and they predominated in the higher size classes, showing significantly bigger body sizes when compared to males (Kolmogorov-Smirnov, p < 0.05). Additionally, we could observe a tendency of decreasing average and maximum body size with increasing latitude (Fig. 4). In MA, 565 adults and 6 juveniles were sampled, from which the mean size of males CL (n= 118) was 7.6 mm (size range: 4.9-11.6 mm), and 9.9 mm for females (n= 453) (size range: 4.8-20.5 mm) (Fig. 4). In UB I, 996 adults and 38 juveniles were sampled, from which the mean size recorded for males CL (n= 104) was 7.3 mm (size range: 5.0-11.3 mm), and 9.8 mm for females (n= 930) (size range: 5.6 to 16.8 mm) (Fig. 4). In CA, 855 adults and 276 juveniles were sampled, from which the mean size of males CL (n= 85) was 6.9 mm (size range: 4.4-10.1 mm), and 9.1 mm for females (n= 1046) (size range: 4.4 to 14.5 mm) (Fig. 4). In SFS, we sampled 298 adults and 3 juveniles, from which the mean size of males CL (n= 03) was 6.0 mm (size range: 5.2- 7.3 mm), and 9.9 mm for females (n= 298) (size range: 4.5-13.9 mm) (Fig. 4). Capítulo 1 24 Figure 4: Sicyonia dorsalis: number of individuals per demographic group in each size class. Samples taken in southeastern Brazil from: A) July 2010 through June 2011 in the Macaé region; B) from July 2013 through June 2014 in the Ubatuba region; C) from July 2012 through May 2014 in the Cananéia region; and D) from July 2010 through June 2011 in the São Francisco do Sul region. Capítulo 1 25 Sex ratio During the studied period, we recorded a strongly female-biased sex ratio (Binomial test, p < 0.05) for all months and regions. Individual growth and longevity Throughout the regions, 3,258 females were analyzed to their estimate of individual growth parameters (MA: 453 individuals; UB I: 930 individuals; UB II: 829 individuals; CA: 1,046 individuals). As in the population structure (above), we observed that growth estimates also showed a decrease in asymptotic length as latitude increases, even though longevity estimates seems not to follow a clear pattern among the regions studied. Due to the low number of individuals in some sampled months, it was not possible to recognize growth cohorts for the SFS region, preventing us from estimating growth parameters in this area. Based on modal values, we recognized the cohorts from which we constructed overall mean growth curves grouping all of the cohorts with estimates for CL∞, k and longevity for each region sampled. For MA, 7 cohorts were distinguished, with estimates of CL∞= 15.69 mm, k= 0.010 and longevity= 458 days (1.26 year) (Fig. 5). For UB I, 6 cohorts were distinguished, with estimates of CL∞= 16.32 mm; k= 0.010 and longevity= 441 days (1.21 year) (Fig. 6). In UB II, 6 cohorts were distinguished, with estimates of CL∞= 13.75 mm, k= 0.009 and longevity= 485 days (1.33 year) (Fig. 7). Finally, we recognized 5 cohorts for CA, with estimates of CL∞= 13.14 mm, k= 0.009 and longevity= 489 days (1.34 year) (Fig. 8). Capítulo 1 26 Figure 5: Sicyonia dorsalis: growth cohorts observed for females sampled in the Macaé region, from July 2010 through June 2011, based on the Von Bertalanffy growth model. Capítulo 1 27 Figure 6: Sicyonia dorsalis: growth cohorts observed for females sampled in Ubatuba I region, from July 2013 through June 2014, based on the Von Bertalanffy growth model. Capítulo 1 28 Figure 7: Sicyonia dorsalis: growth cohorts observed for females sampled in Ubatuba II region, from July 2001 through June 2003, based on the Von Bertalanffy growth model. Figure 8: Sicyonia dorsalis: growth cohorts observed for females sampled in Cananéia region, from July 2012 through May 2014, based on the Von Bertalanffy growth model. Capítulo 1 29 Growth curves differed significantly among females from all the regions (F test, p < 0.05), indicating that one single curve cannot be applied to explain the growth rate for S. dorsalis populations sampled in different locations along the southeastern Brazilian coast. Reproductive periodicity and juvenile recruitment For all of the regions, we observed that reproductive period was discontinuous throughout the year (seasonal). Even though the percentage of reproductive females was high all year in MA and UB I, during some periods the overall abundance of adult females was very low, so it should not be considered as an effective reproductive period. Using these criteria, we observed a slight decrease in the number of months composing the reproductive period as latitude increased (7-8 months in MA, UB I and CA; 6 months in SFS). In MA, the reproductive period lasted for 7 months (from August 2010 through February 2011), comprising the winter-summer seasons (Fig. 9). In this area, salinity means negatively influenced the abundance of reproductive females with a +1 month lag (Crosscorrelation= -0.62; p < 0.05) and adult males with a +2 months lag (Crosscorrelation= -0.62; p < 0.05). The abundance of adult males showed positive correlation with the abundance of reproductive and spent females (Crosscorrelation= 0.96 and 0.82, respectively; p < 0.05), with no time lag; and the abundance of juveniles (= recruits) showed a positive association with the number of reproductive females (Crosscorrelation= 0.68; p < 0.05) and adult males (Crosscorrelation= 0.65; p < 0.05), both in a -2 months lag. However, due to the low number of juvenile individuals throughout the year, it was not possible to determine any recruitment periodicity for this region. Capítulo 1 30 Figure 9: Sicyonia dorsalis: reproductive periodicity for individuals sampled from July 2010 through June 2011 in the coastal area from Macaé Region, Rio de Janeiro State, Brazil. In UB I, the reproductive period lasted for 8 months (from July 2013 through February 2014), comprising the winter-summer season, although the abundances observed in March and April 2014 were not high enough to represent a reliable population sample (Fig. 10). In this area, the abundance of juveniles showed a positive association with that of reproductive females (Crosscorrelation= 0.86; p < 0.05) and adult males (Crosscorrelation= 0.73; p < 0.05), with a +1 month lag. The abundance of adult males showed positive association with that for reproductive females, with no time lag (Crosscorrelation= 0.85; p < 0.05) and with spent females with a 0 and -1 month time lag (Crosscorrelation= 0.63 and 0.69, respectively; p < 0.05). The abundance of adult males showed a negative association with temperature means, with a +2 months lag (Crosscorrelation= -0.63; p < 0.05), and a negative association with the salinity mean values, with a -3 month lag (Crosscorrelation= -0.75; p < 0.05). On the other hand, reproductive females showed a positive association with the salinity mean values, with a 0 and +1 month lag (Crosscorrelation= 0.71 and 0.69, respectively; p < 0.05). Recruitment seems to be highly seasonal, once we only obtained juveniles in November and an additional single individual in January. 0 10 20 30 40 50 60 70 80 90 100 0 20 40 60 80 100 120 140 Ju l A u g S ep O ct N o v D ec Ja n F eb M ar A p r M ay Ju n P er ce n ta g e o f re p ro d u ct iv e fe m a le s N u m b e r o f a d u lt f e m a le s Months Number Percentage 2010 2011 Capítulo 1 31 Figure 10: Sicyonia dorsalis: reproductive periodicity of individuals sampled from July 2013 through June 2014 in the coastal area from Ubatuba I region, São Paulo State, Brazil. In CA, the reproductive period lasted for 8 months (from June 2013 through January 2014), comprising the winter-spring season (Fig. 11). We observed a positive association between the abundances of adult males and reproductive females, with no time lag (Crosscorrelation= 0.75; p < 0.05), as well as with the abundance of spent females (Crosscorrelation= 0.60; p < 0.05). The abundance of juveniles showed a positive association with reproductive females (Crosscorrelation= 0.83; p < 0.05) and adult males (Crosscorrelation= 0.82; p < 0.05). The abundance of juvenile individuals showed a negative association to the monthly values of temperature (Crosscorrelation= - 0.43; p < 0.05). The recruitment period showed some similarity to the periods of higher abundance on the percentage of reproductive females (from June 2013 through January 2014), with a peak in November (excluding months in which the abundance of individuals was not satisfactory). 0 10 20 30 40 50 60 70 80 90 100 0 50 100 150 200 250 300 Ju l A u g S ep O ct N o v D ec Ja n F eb M ar A p r M ay Ju n P er ce n ta g e o f re p ru d u ct iv e fe m a le s N u m b er o f a d u lt f em a le s Months Number Percentage 2013 2014 Capítulo 1 32 Figure 11: Sicyonia dorsalis: reproductive periodicity of individuals sampled from July 2012 through May 2014 in the coastal area from Cananéia region, São Paulo state, Brazil. In SFS, the reproductive period lasted for 6 months (July-December), comprising winter and spring seasons (Fig. 12). We observed a positive association between the abundance of juveniles and the one observed for reproductive females (Crosscorrelation= 0.77; p < 0.05), and a negative association between juveniles and temperature means in a -1 month lag (Crosscorrelation= -0.68; p < 0.05). The abundance of reproductive females showed a negative association to the temperature means in a 0 and -1 month lag (Crosscorrelation= -0.77 and -0.80, respectively; p < 0.05). Unfortunately, the low abundance of juveniles (n= 3) was not satisfactory so that we could define a recruitment period in this area. 0 20 40 60 80 100 120 0 20 40 60 80 100 120 140 160 180 Ju l A u g S ep O ct N o v D ec Ja n F eb M ar A p r M ay Ju n Ju l A u g S ep O ct N o v D ec Ja n F eb M ar A p r M ay P er ce n ta g e o f re p ro d u ct iv e fe m a le s N u m b er o f a d u lt f em a le s Months Number Percentage 2012 2014 Capítulo 1 33 Figure 12: Sicyonia dorsalis: reproductive periodicity of individuals sampled from July 2010 through June 2011 in the coastal area from São Francisco do Sul region, Santa Catarina state, Brazil. Discussion In this study, we show how local environmental conditions affect growth and reproduction of the shrimp S. dorsalis from different locations, even in a narrow range of latitudes. Further, our results suggest that S. dorsalis completes its lifecycle in the inshore area in all of the locations studied, given that we sampled both reproductive adults and juvenile recruits (even though the last in a low abundance). Additionally, we could detect a possible effect of an area protected from fishing off Ubatuba, Brazil, over a ten-year period, since larger individuals were sampled in this region after the establishment of this area. Our results complement the current knowledge about shrimp populations, allowing and understanding how the population biology of this and other species have evolved in light of environmental variation in different geographic areas. In decapod crustaceans, males of some species can show bigger body sizes when compared to females of the same species, what can be considered as a selective pressure associated with their reproductive behavior. In such species, males displaying more robust bodies show a higher success defending females and their mating territory, as well as in agonisitic encounters with other males for other resources. However, the mating system of S. dorsalis is promiscuous (“pure search”), in which males do not defend or fight over females or mating territories (Bauer 1996). In such penaeoid 0 10 20 30 40 50 60 70 80 90 100 0 10 20 30 40 50 60 70 80 90 Ju l A u g S ep O ct N o v D ec Ja n F eb M ar A p r M ay Ju n P er ce n ta g e o f re p ro d u ct iv e fe m a le s N u m b er o f a d u lt f em a le s Months Number Percentage 2010 2011 Capítulo 1 34 species, as in caridean shrimps with similar mating systems, there is no selection for large male size or enhanced weaponry (Bauer 2004). Females of S. dorsalis from all studied regions showed larger sizes when compared to males, showing a strong sexual dimorphism in size in penaeoids from southern Brazil, as already noted also by Castilho et al. (2008c) in the UB region for this species. Sexual dimorphism in body size (female > male) is considered the rule in the biology of penaeid shrimps, since female shrimp fecundity increases with size (Boschi 1969, Gab-Alla et al. 1990, Castilho et al. 2008a, c, 2015b). The same pattern on sexual dimorphism was also observed in other penaeid species in the Brazilian coast, such as X. kroyeri (Grabowski et al. 2014, 2016, Castilho et al. 2015a), Rimapenaeus constrictus (Stimpson, 1874) (Costa & Fransozo 2004, Garcia et al. 2016, Lopes et al. in press) and A. longinaris (Castilho et al. 2007a, 2015b), among others. In this study, differences in size were observed in females from different locations by comparing maximum body sizes and estimates of growth parameters. There was a decrease in maximum female body size as latitude increased. The biggest female sizes were observed in MA (most northern investigated region), and the smallest, from samples taken in SFS (most southern studied region). Estimates of asymptotic size were higher in females from UB I and MA, followed by those from CA. Interestingly, this result is just the opposite of the expected trend in larger body size with increasing latitude in decapod shrimps (Bauer 1992). In that paradigm, the lower temperatures of higher latitudes lead to slower growth but increased longevity, allowing individuals to attain larger body sizes in their lifetime. Higher temperatures generally found in lower latitudes may induce an increase to growth coefficient through higher metabolism, with more frequent molting but with smaller size increases at each molt, leading to small lifetime body size in a species with a shorter lifespan (Bauer 1992, Castilho et al. 2015a). This was shown for A. longinaris on the eastern South American coast, in which larger female sizes (CL) were observed with increasing latitude, when comparing individuals from the Brazilian and the Argentinean populations (Castilho et al. 2007b). However, Grabowski et al. (2014) did not find the same pattern of latitudinal variation for asymptotic body size for X. kroyeri along the Brazilian coast. In this study, the authors compared data on the growth of this tropical species and found that the highest asymptotic length estimates were found by Santos & Ivo (2000) in the northeastern region, while the lowest ones were estimated by Heckler et al. (2013) in a Capítulo 1 35 southeastern area. Such results were associated with the disagreement in sampling and growth estimating methods along the coast (Fonseca 1998, Freire 2005), the species’ overfishing along the analyzed area (D’Incao et al. 2002, Vasconcellos et al. 2007) or the existence of two Xiphopenaeus cryptic species (Gusmão et al. 2006). In this study, however, growth coefficients seemed not to follow a clear pattern with latitude. This could be held as an evidence of a migratory connection between groups that are part of a same population (Castilho et al. 2015b). Carvalho-Batista et al. (2014) inferred population connectivity for A. longinaris along its distributional range, and found no genetic variability for this species at an intraspecific level. According to the authors, the high efficiency on larval dispersal is an important factor that may be responsible for the homogeneity in its distribution over a wide geographical range (Gopurenko & Hughes 2002, Carvalho-Batista et al. 2014). For P. muelleri, a colder water species, it was observed that larvae can travel along 120 to 300 nautical miles, transported by the coastal currents (Boschi 1989). Adult stage of Melicertus plebejus (Hess, 1865) was also observed to migrate, in distances up to 930 km (Ruello 1975) along the Australian coast. Castilho et al. (2008b) found that S. dorsalis could migrate, following movement of preferred environmental conditions, from southern regions toward northern ones during the spring. They associated this activity to the presence of the SACW. Additionally, Almeida et al. (2012) pointed out that similarities in reproductive biology among populations located thousands of kilometers apart could be considered evidences for the existence open metapopulations with extensive connectivity. Growth analyses’ results also showed a possible effect of the establishment of a marine protected area (MPA) in the UB region, in October 2008. Comparing maximum body sizes and asymptotic lengths from 2001-2003 to the ones sampled in 2013-2014, we observed an increased body size (13.75 mm CL and 16.3 mm, respectively), but on the other hand, a decrease in estimated longevity (485 days in 2001-2003, to 441 days in 2013-2014). Almeida et al. (2012) investigated the reproductive biology of X. kroyeri in Fortaleza Bay, which is also located inside this MPA. The authors highlighted the existence of a nursery ground for the species within the region, and stated the importance of long-term studies to investigate the effects of such protection to the recovery of stocks in areas which are heavily exploited. Even though S. dorsalis is not a commercially important species along the Brazilian coast due to its small size and carapace hardness, it comprises a great portion of the bycatch fauna, as pointed out in Capítulo 1 36 the introductive session of this research (for additional information, see Costa et al. 2005, Castilho et al. 2008b). Therefore, information on its biological requirements are of great value to the preservation of the species and to the effects of a marine protected for other ecologically and commercially important penaeoid shrimps. Dall et al. (1990) pointed out that penaeid shrimps have short life spans, from 1- 2 years. However, life span and other population parameters can vary intragenerically when populations from different geographical areas and latitudes are compared. Bauer (1992) suggested different environmental features that might be responsible for such variation in the genus Sicyonia Edwards, 1830. The author compared body size and longevity in species from different biogeographical areas: S. parri (Burkenroad, 1934) and S. laevigata Stimpson, 1871 (Western Atlantic tropical species) showed a size range of 3-9 cm CL and longevity of 6-8 months; S. brevirostris (Stimpson, 1874) (Western Atlantic subtropical species), 17-35 cm CL and 20-22 months; and S. ingentis (Burkenroad, 1938) (Eastern Pacific temperate species), 24-45 cm CL and ≥ 22 months. Higher latitude species showed a tendency towards to seasonal reproductive periodicity when compared to tropical species, possibly induced by a concomitant seasonality in larval food availability. Females live longer in higher latitudes, which gives them time enough to select a favorable period to reproduce, while the tropical females (which lives less than a year, at least in many caridean species; Bauer 2004) must establish and grow to the sexual maturity in any time of the year. There are many examples of increasing life span in higher latitudes, but it is important to remember that such feature is not a simple effect of lower temperatures or lower growth coefficient, but an adaptation of a whole life history in different environments (Vogt 2012). In this study, the estimated longevities did not show a clear pattern among the sampled regions, as the highest one was observed in CA, followed by MA and UB. The longevity estimates found in this study agree with those given for penaeid shrimps (1-2 years) (Dall et al. 1990). As pointed out by Grabowski et al. (2014), migratory activities and larval dispersion could increase gene flow among populations from the limited range of latitudes sampled in this study, perhaps making a latitudinal pattern impossible. The studied region is strongly influenced by three water masses, from which the most important is the SACW, which brings low temperature and salinity to the areas where it is recognized (Castro-Filho et al. 1987, Carvalho et al. 1998, Pedrosa et al. 2006). The SACW brings with it a high concentration of nutrients, which leads to an increase in primary productivity in waters that it intrudes into (Pires 1992, Silveira et al. Capítulo 1 37 2000, Odebrecht & Castello 2001, Castilho et al. 2008b, c). Considering that lower temperatures can exert a negative influence on growth, which in turn increases overall body size, it seems reasonable to identify higher carapace length values in UB and MA. Even though CA showed the marked decreases in temperature means (mainly in winter months), in MA and UB, it was lower in spring, but tended to be more homogeneous throughout the year. The connection between temperature, salinity (most altered environmental parameters with the presence of the SACW) and the abundance of individuals could be noted by their negative effect on growth coefficients and asymptotic body size. Temperature and salinity also influenced reproductive and recruitment periods. Reproduction occurred seasonally, with most of the reproductive females sampled in winter-spring months, and critical decreases in their abundance observed on summer- autumn. Even though the reproductive period was approximately the same for the regions, it was possible to note a slight increase in the number of months in which the higher percentage of reproductive females was observed in each region as latitude decreases (from 6 months in higher latitudes to 7-8 months in lower latitudes). The same pattern (increase in number of reproductive months associated with more favorable temperature levels (in this case, with higher temperatures)) was also found by Aragón-Noriega (2007). In that study, carried out in the Gulf of California, the reproduction occurred during periods of warmer water temperature, varying from 7 months in lower latitudes (higher mean temperatures) to 4 months in higher ones (lower temperatures). Vega-Pérez (1993) states that, due to the presence of SACW in the UB region, phytoplankton production is increased as shown by higher values on chlorophyll in the water column. Such an increase in primary production possibly stimulates increases in herbivorous zooplankton, as the highest density of planktonic organisms was observed in summer, and the lowest one, in winter. Other studies also pointed out the importance of SACW seasonal dynamics as an enrichment factor for marine communities off the southern Brazilian coast (Pires 1992, De Léo & Pires-Vanin 2006, Rocha et al. 2007, Castilho et al. 2008d). It is evident that high primary productivity is essential as a resource for larval shrimps, suggested by the match-mismatch hypothesis (Cushing 1975), which suggests that highest reproductive investment of marine planktotrophic species should coincide with seasonal highest abundance on phytoplankton. Capítulo 1 38 Molting frequency is shorter during reproductive months, as energy for growth is funneled into reproductive effort (Anderson et al. 1985, Bauer & Rivera Vega 1992). For certain penaeid species, mating and female molting are correlated processes (Bauer 1996). In Sicyonia spp., females can store sperm for long periods in seminal receptacles after a reproductive molt and mating (Bauer 1991, 1996). In the present study, we could observe a correlation in the abundances of adult males and spent females, as the latter may molt and mate after using up their sperm supply after various spawns. The same relation between males and spent females was also observed in the Brazilian coast for the seabob shrimp X. kroyeri in Southern (Grabowski et al. 2016) and Southeastern Brazil (Heckler et al. 2013). On the other hand, the low abundance of adult females during certain periods of the year could be an evidence of a migration of females toward greater depths for spawning. Dall et al. (1990) stated that after mating, females tend to migrate to greater depths where spawning would occur. Additionally, Juneau (1977) suggested that mating and spawning might occur in deeper waters along the Gulf of Mexico, although it might be possible that they disappeared from study areas by migrating to other areas of similar depth not sampled. 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