UNIVERSIDADE ESTADUAL PAULISTA “JÚLIO DE MESQUITA FILHO” 

INSTITUTO DE BIOCIÊNCIAS – CAMPUS DE BOTUCATU 

PÓS-GRADUAÇÃO EM CIÊNCIAS BIOLÓGICAS – ZOOLOGIA 

 

 

 

 

DISSERTAÇÃO DE MESTRADO 

 

 

 

Biologia e ecologia de crustáceos decápodos 
(Caridea e Brachyura) do infralitoral não 

consolidado da costa sudeste do Brasil 
 

 

RAFAELA TORRES PEREIRA 

ORIENTADOR: PROF. DR. ADILSON FRANSOZO 

COORIENTADORA: PROF. DRA. ARIÁDINE CRISTINE DE ALMEIDA 

 

 

 

BOTUCATU – SP 

2014 



 

Biologia e ecologia de crustáceos decápodos (Caridea 
e Brachyura) do infralitoral não consolidado da costa 

sudeste do Brasil 

 

 

 

 

RAFAELA TORRES PEREIRA 

ORIENTADOR: PROF. DR. ADILSON FRANSOZO 

COORIENTADORA: PROF. DRA. ARIÁDINE CRISTINE DE ALMEIDA 

 

 

 

 

Dissertação apresentada ao curso de pós-
graduação 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



 

 

 

 

 

 

 

 

 

 

 

 

 
FICHA CATALOGRÁFICA ELABORADA PELA SEÇÃO TÉC. AQUIS. TRATAMENTO DA INFORM. 

DIVISÃO DE BIBLIOTECA E DOCUMENTAÇÃO - CAMPUS DE BOTUCATU - UNESP 
BIBLIOTECÁRIA RESPONSÁVEL: ROSEMEIRE APARECIDA VICENTE - CRB 8/5651 

Pereira, Rafaela Torres. 
Biologia e ecologia de crustáceos decápodos (Caridea e Brachyura) do 

infralitoral não consolidado da costa sudeste do Brasil / Rafaela Torres Pereira. – 
Botucatu, 2014 

 
Dissertação (mestrado) - Universidade Estadual Paulista, Instituto de 

Biociências de Botucatu 
Orientador: Adilson Fransozo 
Coorientador: Ariádine Cristine de Almeida 
Capes: 20400004 
 
1. Biodiversidade - Conservação. 2. Decapode (Crustáceo). 3. Distribuição 

geográfica. 4. Reprodução animal. 5. Zoologia – Pesquisa. 
 
 
Palavras-chave: Biodiversidade; Crustacea (Decapoda); Distribuição ecológica; 
Estratégia reprodutiva; Estrutura populacional. 



 

EPÍGRAFE 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

“Não são as espécies mais fortes que sobrevivem nem as mais 
inteligentes, e sim as mais suscetíveis a mudanças.” 

 
Charles Darwin 

 

 

 

 



 

DEDICATÓRIA 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

AOS MEUS PAIS CLÁUDIO E CIDA, AOS MEUS 

IRMÃOS BRUNO E FABIANA (IN MEMORIAN), E 

AOS MEUS QUERIDOS AVÓS JOÃO, EMERITA, 
JOSÉ (IN MEMORIAN) E TEREZINHA, EU 

DEDICO! 

 

 

 

 

 



 

AGRADECIMENTOS 

 

 

 Hoje, mais do que nunca, é momento de agradecer àqueles que contribuíram 

para que mais um objetivo em minha vida fosse atingido. Sem a colaboração destes essa 

etapa não estaria concluída. 

 Agradeço a Deus por estar sempre ao meu lado durante toda esta trajetória. 

 Sou grata ao professor doutor titular Adilson Fransozo, que além de orientador 

foi amigo. Obrigada pela oportunidade e confiança. Obrigada ainda pelos conselhos, 

sempre bem vindos, desde a época da graduação. Faltam-me palavras para expressar 

minha gratidão! 

 À minha coorientadora e amiga, Dra. Ariádine Cristine de Almeida, por toda 

ajuda e ensinamentos, desde a época da graduação, e por estar sempre disposta a me 

ajudar em tudo que precisei. Agradeço ainda por toda amizade e carinho. 

 À professora doutora titular Maria Lucia Negreiros Fransozo, carinhosamente 

chamada de “tia”, por todo carinho e conhecimento transmitido. Agradeço pela 

oportunidade de acompanhar suas aulas e pelas excelentes discussões em grupo, as 

quais foram fundamentais para meu crescimento profissional e pessoal. Você com 

certeza transmite um exemplo de profissionalismo a todos nós. Muito obrigada! 

 Aos professores Dr. Antônio L. Castilho, Dr. Rogério C. da Costa, pelos 

ensinamentos em suas disciplinas e pelas valiosas discussões nas mesmas. 

 Ao professor Dr. Válter Cobo, pelo conhecimento transmitido durante os cursos 

de extensão em Biologia Marinha. 

 Aos professores Dr. Adilson Fransozo e Dr. Juan A. Baeza, por me conceder 

permissão de utilizar fotos de sua autoria nesta dissertação. 

Agradeço ao Conselho Nacional de desenvolvimento científico e tecnológico 

(CNPq), por ter financiado minha bolsa de mestrado. 



 

 Ao Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis 

(IBAMA) e à Polícia Federal, concederem a licença para as coletas do material nas 

áreas estudadas. 

Agradeço à Universidade estadual Paulista “Júlio de Mesquita Filho”, ao 

Instituto de Biociências e ao Departamento de Zoologia, por terem proporcionado 

infraestrutura para que essa dissertação fosse realizada. Em especial, agradeço ao curso 

de pós-graduação em Ciências Biológicas - Zoologia e ao Departamento de Zoologia, 

incluindo seus atenciosos funcionários André Arruda, Carolina Lopes, Davi Müller, 

Flávio da Silva, Hamilton Rodrigues, Herivaldo Santos, Juliana Ramos, Luciana 

Campos e Silvio Almeida. 

 Sou grata às agências de fomento que financiaram os projetos de pesquisa, dos 

quais as coletas geraram os dados utilizados para execução dos trabalhos apresentados. 

 Agradeço aos pescadores da embarcação Progresso, Édson Ferreti (Dedinho) e 

Djalma Rosa (Passarinho), e aos membros do NEBECC, que participaram das coletas 

que deram origem aos dados utilizados nos trabalhos aqui apresentados. O esforço de 

vocês gerou e continua gerando uma série de publicações bem conceituadas. Muito 

obrigada. 

 Aos amigos do Núcleo de Estudos em Biologia, Ecologia e Cultivo de 

Crustáceos (NEBECC). Aos membros atuais e aos “antigos”, por terem me acolhido e 

contribuído para meu crescimento profissional. Em especial, gostaria de agradecer 

àqueles que me ensinaram muito, contribuindo nos trabalhos apresentados nesta 

dissertação. Agradeço aos professores Dra. Ariádine Almeida, Dr. Gustavo Teixeira, 

Dra. Vivian Fransozo, Dra. Giovana Bertini e Dr. Fúlvio Freire; aos colegas de trabalho 

Carlos Alencar, Paloma Lima, Eduardo Bolla Jr., Samara Alves, Mariana Antunes, 

Thiago Silva e por todas as discussões de cunho estatístico. Sou grata ainda aos demais 

colegas do NEBECC pela convivência e carinho. 

 É impossível deixar de agradecer àqueles que, além de colegas de trabalho se 

tornaram minha outra família em Botucatu. Obrigada Marciano Venâncio, Ariádine 

Almeida, Samara Alves, Douglas Alves, Eduardo Bolla Jr., Mariana Antunes, Thiago 

Silva, Kátia Hiroki, Bárbara Martins, Emanuelle Stopa, Gustavo Sancinetti, Augusto 



 

Silveira e Eduardo Degani. Quando eu mais precisava vocês sempre tinham uma 

palavra amiga e um gesto de carinho. 

 Agradeço ao meu querido Augusto Silveira, por todo carinho, amor e amizade. 

Obrigada pelo cuidado e dedicação. E, principalmente, obrigada por se dispor a ser meu 

companheiro. Eu te amo! 

 À toda minha família, em especial aos meus pais Cláudio Pereira e Maria 

Aparecida Torres Pereira, e avós, João Torres, Emerita Torres, José Pereira (in 

memorian) e Terezinha Pereira, que mesmo à distância se fizeram presentes a cada dia, 

em cada ligação, conversa por Skype e afins. Sem o apoio de vocês nada disso seria 

possível, obrigada por acreditarem no meu sonho, e principalmente por me incentivarem 

a busca-lo. Obrigada por cada palavra de carinho. Eu amo vocês! 

 Papai e mamãe, nós sabemos o quanto foi e é difícil conviver com a distância, 

mas isso é irrelevante para nós. Distância nenhuma interfere na nossa união! Obrigada 

pela educação que me deram e por acreditarem que eu conseguiria. Essa é mais uma 

vitória que alcançamos juntos. Bruno, meu querido irmão, agradeço pelas lindas 

palavras de incentivo e por se orgulhar de mim. 

 À minha eterna Ciça (in memorian), que continuará sempre em meus 

pensamentos, e à minha Lily, minhas queridas amigas caninas que fizeram com que 

meus dias fossem mais leves e felizes. Obrigada por serem tão amorosas. 

 A todos que torceram por mim, meus sinceros agradecimentos! 



 

SUMÁRIO 

CONSIDERAÇÕES INICIAIS ........................................................................................... 1 

CONSIDERAÇÕES INICIAIS ............................................................................................................. 2 
REFERÊNCIAS .............................................................................................................................. 10 

INFRAORDEM CARIDEA ............................................................................................. 13 

CAPÍTULO 1 ...................................................................................................................... 14 
REPRODUCTIVE STRATEGY OF THE SHRIMP NEMATOPALAEMON SCHMITTI (HOLTHUIS, 1950) 
(DECAPODA, CARIDEA, PALAEMONOIDEA) FROM THE SOUTHEASTERN BRAZILIAN COAST 14 
ABSTRACT ................................................................................................................................... 15 
INTRODUCTION ............................................................................................................................ 16 
MATERIAL AND METHODS .......................................................................................................... 19 
RESULTS ...................................................................................................................................... 22 
DISCUSSION ................................................................................................................................. 29 
REFERENCES ................................................................................................................................ 34 

INFRAORDEM BRACHYURA ....................................................................................... 39 

CAPÍTULO 2 ...................................................................................................................... 40 
ECOLOGICAL DISTRIBUTION AND POPULATION PARAMETERS OF PERSEPHONA 

MEDITERRANEA (HERBST, 1794) (BRACHYURA, LEUCOSIIDAE) IN A PROTECTED AREA ON 
THE SOUTHEASTERN BRAZILIAN COAST ............................................................................ 40 
ABSTRACT ................................................................................................................................... 41 
INTRODUCTION ............................................................................................................................ 42 
MATERIAL AND METHODS .......................................................................................................... 44 
RESULTS ...................................................................................................................................... 50 
DISCUSSION ................................................................................................................................. 59 
REFERENCES ................................................................................................................................ 62 
 
CAPÍTULO 3 ...................................................................................................................... 71 
ENVIRONMENTAL FACTORS INFLUENCING THE DISTRIBUTION OF THREE SPECIES WITHIN 
THE GENUS PERSEPHONA LEACH, 1817 (CRUSTACEA, DECAPODA, LEUCOSIIDAE) IN TWO 
REGIONS ON THE NORTHERN COAST OF SÃO PAULO STATE, BRAZIL ................................. 71 
ABSTRACT ................................................................................................................................... 72 
INTRODUCTION ............................................................................................................................ 73 
MATERIAL AND METHODS .......................................................................................................... 75 
RESULTS ...................................................................................................................................... 82 
DISCUSSION ................................................................................................................................. 96 
REFERENCES .............................................................................................................................. 100 
 
 



 

CAPÍTULO 4 .................................................................................................................... 105 
ENVIRONMENTAL FACTORS MODULATING THE ABUNDANCE AND DISTRIBUTION OF 

CALLINECTES DANAE SMITH, 1869 (DECAPODA, PORTUNIDAE) FROM TWO AREAS OF THE 
SOUTHEASTERN COAST OF BRAZIL .................................................................................. 105 
ABSTRACT ................................................................................................................................. 106 
INTRODUCTION .......................................................................................................................... 108 
MATERIAL AND METHODS ........................................................................................................ 110 
RESULTS .................................................................................................................................... 114 
DISCUSSION ............................................................................................................................... 123 
REFERENCES .............................................................................................................................. 126 

CONSIDERAÇÕES FINAIS .......................................................................................... 133 

CONSIDERAÇÕES FINAIS ............................................................................................................ 134 



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O subfilo Crustacea é, entre todos os organismos atuais, o grupo que apresenta a 

maior diversidade morfológica (Martin & Davis 2001). Essa variação de formas 

permitiu a esses organismos habitar os mais diferenciados ambientes, adquirindo, 

portanto uma expressiva distribuição no mundo todo (Ng et al. 2008). A ordem 

Decapoda é a mais diversa, sendo constituída de cerca de 14756 espécies descritas (De 

Grave et al. 2009) Essa ordem agrega organismos abundantes, com importância 

ecológica e apreciados na alimentação humana, como os camarões, lagostas, siris e 

caranguejos. 

A Infraordem Caridea é representada por aproximadamente 2500 espécies de 

camarões descritos. Estes são caracterizados por apresentarem filobrânquias, o primeiro 

ou os dois primeiros pares de pereópodos quelados e de tamanhos variados e a segunda 

pleura abdominal marcadamente mais expandida, recobrindo parcialmente a primeira e 

a terceira pleuras (Hendrickx 1995). Esta Infraordem é formada por 16 superfamílias e 

36 famílias (Martin & Davis 2001). A Família Palaemonidae, inserida dentro da 

Superfamília Palaemonoidea, é grande e diversa, com pelo menos 118 gêneros e 887 

espécies. Os camarões palaemonídeos são epibentônicos e ecologicamente importantes, 

atuando como detritívoros, predadores de pequenos invertebrados e presas para peixes 

(Bauer 2004). 

O camarão palaemonídeo utilizado nesse estudo foi o camarão barriga branca 

Nematopalaemon schmitti (Holthuis, 1950) (Figura 1). Esta espécie apresenta uma 

ampla distribuição geográfica, desde a Venezuela até o Brasil (do Amapá até São Paulo) 

(Holthuis 1980, Ramos-Porto & Coelho 1998). Esta espécie habita águas marinhas e 



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estuarinas, onde o substrato é composto por cascalho, areia e/ou silt + argila, e em 

profundidades de até 75 m (Holthuis 1980). 

 

 

Figura 1 - Nematopalaemon schmitti (Holthuis, 1950). Foto de JA, Baeza. 

 

Pertencente à subordem Pleocyemata, a Infraordem Brachyura é constituída por 

mais de 6700 espécies (Ng et al. 2008, De Grave et al. 2009), das quais mais de 300 são 

conhecidas na costa brasileira e 188 são descritas no litoral do Estado de São Paulo 

(Bertini et al. 2004). Esta Infraordem é composta por caranguejos e siris, os quais 

apresentam ampla distribuição, podendo ser encontrados em habitats diversificados 

(terrestre, marinho e dulcícola) (Ng et al. 2008). 



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As espécies de braquiúros utilizadas nesse estudo foram: Persephona 

mediterranea (Herbst, 1794), Persephona punctata (Linnaeus, 1758), Persephona 

lichtensteinii Leach, 1817 e Callinectes danae Smith, 1869. 

Os caranguejos P. mediterranea (Figura 2), P. punctata (Figura 3), e 

Persephona lichtensteinii (Figura 4) apresentam ampla distribuição no Atlântico 

Ocidental, habitando zonas bentônicas, em substratos compostos por lodo, areia, 

conchas, algas calcárias e corais. No Brasil, P. mediterranea e P. punctata possuem 

distribuição mais ampla quando comparadas à P. lichtensteinii. As duas primeiras 

ocorrem desde o Amapá ao Rio Grande do Sul, enquanto a outra espécie se distribui do 

Amapá à São Paulo (Melo 1996). 

 

 

Figura 2 - Persephona mediterranea (Herbst, 1794). Foto de A, Fransozo. 

 



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Figura 3 - Persephona punctata (Linnaeus, 1758). Foto de A, Fransozo. 

 

 

Figura 4 - Persephona lichtensteinii Leach, 1817. Foto de A, Fransozo. 



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O siri Callinectes danae (Figura 5) tem distribuição registrada para o Atlântico 

Ocidental, sendo encontrado em Bermuda, Flórida, Golfo do México, Antilhas, 

Colômbia, Venezuela e Brasil (da Paraíba ao Rio Grande do Sul). Essa espécie habita, 

preferencialmente, regiões de águas salobras até hipersalinas, sendo encontrada em 

manguezais e estuários lamosos, em praias arenosas e mar aberto, e na região intertidal 

até os 75m de profundidade (Melo 1996). 

 

 

Figura 5 - Callinectes danae Smith, 1869. Foto de A, Fransozo. 

 



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Conhecer a distribuição de organismos marinhos é de fundamental importância 

para inferir sobre preferência de habitat, seja espacial ou temporal. Além disso, pode-se 

prever com base nos fatores ambientais analisados, de que forma essa distribuição pode 

ser moldada por fatores ambientais. No entanto, é importante pensar que a distribuição 

não é regida apenas por relações entre os organismos e os agentes do ambiente, 

variações genéticas e até mesmo intra e interespecíficas podem alterar os padrões 

distribucionais de organismos marinhos (Haedrich et al. 1975, Hecker 1990, Pinheiro et 

al. 1996, Bertini et al. 2001, Bertini & Fransozo 2004). Compreender esses padrões de 

distribuição é importante para conhecermos a biologia e ecologia das populações, 

fornecendo resultados que sirvam de subsídio a futuros estudos e ainda informações que 

possam servir de fonte para que os órgãos competentes possam estabelecer medidas de 

mitigação de impacto sobre as espécies marinhas. 

Ao se estudar uma população, a biologia reprodutiva e todos os seus aspectos 

deve ser estudada a fim de estabelecer padrões reprodutivos para espécies. Isso pode 

auxiliar a determinação de regiões de reprodução, as quais são de fundamental 

importância para a conservação e manutenção das populações. Aspectos como o 

tamanho ao atingir a maturidade sexual e o período reprodutivo da espécie são 

utilizados como ferramenta para definir períodos de defeso para espécies de interesse 

comercial. O tamanho ao atingir a maturidade sexual representa o tamanho a partir do 

qual os indivíduos tornam-se aptos a reprodução e, portanto, manter o equilíbrio da 

população (Hines 1982). Esse tamanho pode variar diante de uma série de fatores 

ambientais, gradiente latitudinal, relações intra e interespecíficas (Sastry 1983, Hartnoll 

1982, 1985, 2006). Por isso, é importante conhecer o que, de fato, atua sobre a 

reprodução da população. Além disso, o período reprodutivo deve ser compreendido, 



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seja para dar suporte às inferências de regiões de reprodução, afirmando quando os 

organismos de uma população estão ativos reprodutivamente, ou então para dar suporte 

e informações básicas à biologia de espécies marinhas, podendo evidenciar padrões de 

reprodução contínua ou sazonal. 

A fim de fornecer informações complementares de populações, são ainda 

realizados estudos da estrutura populacional. Esses são fundamentais para se conhecer 

de que forma esses animais se distribuem em grupos demográficos (Jovens, Machos, 

Fêmeas e Fêmeas ovígeras), e como esses grupos flutuam em decorrência de eventos de 

natalidade e mortalidade. Ainda, esse tipo de estudo pode fornecer informações quanto 

ao equilíbrio populacional, quando se considera a razão sexual entre machos e fêmeas. 

Por fim, nesse tipo de estudo, pode-se ainda verificar a entrada de jovens na população 

ao avaliar o recrutamento da mesma, e assim obter informações que auxiliam tanto na 

compreensão da estrutura, e dos aspectos reprodutivos desses organismos (Bertini et al. 

2010, Almeida et al. 2013). 

De modo geral, a presente dissertação tem como título “Biologia e ecologia de 

crustáceos decápodos (Caridea e Brachyura) do infralitoral não consolidado da costa 

sudeste do Brasil”, sendo subdividida em duas seções, as quais estão subdivididas em 

capítulos. A primeira seção, Infraordem Caridea, é composta por um capítulo. A 

segunda seção, Infraordem Brachyura, é subdividida em três capítulos. O primeiro 

capítulo, “Reproductive strategy of the shrimp Nematopalaemon schmitti (Holthuis, 

1950) (Decapoda, Caridea, Palaemonoidea) from the Southeastern Brazilian coast” 

aborda as estratégias reprodutivas do camarão carídeo N. schmitti, focando no 

investimento reprodutivo, fecundidade, perda de ovos, e sincronia no desenvolvimento 

de ovos e ovários dessa espécie. Os dados utilizados nesse capítulo são provenientes de 



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coletas entre os anos de 2008 e 2011 na Enseada de Ubatuba. O segundo capítulo, 

“Ecological distribution and population parameters of Persephona mediterranea 

(Herbst, 1794) (Brachyura, Leucosiidae) in a protected área on the southeastern 

Brazilian coast” revela a distribuição ecológica de P. mediterranea, em diferentes 

profundidades e estações do ano, a estrutura populacional, a razão sexual e o tamanho 

ao atingir a maturidade sexual. Os caranguejos desse estudo foram coletados durante o 

ano 2000 na região de Ubatuba, na qual está incluída uma área marinha de proteção 

ambiental (APA marinha – Setor Cunhambebe). O terceiro capítulo, “Environmental 

factors influencing the distribution of three Species within the genus Persephona Leach, 

1817 (Crustacea, Decapoda, Leucosiidae) in two regions on the northern coast of São 

Paulo State, Brazil” aborda a influência dos fatores ambientais na distribuição 

batimétrica de três espécies do gênero Persephona, buscando padrões de distribuição 

para essas espécies. Neste capítulo, os dados utilizados são provenientes de coletas no 

período de julho/2001 a junho/2003 nas regiões de Ubatuba e Caraguatatuba. O quarto 

capítulo, “Environmental factors modulating the abundance and distribution of 

Callinectes danae Smith, 1869 (Decapoda, Portunidae) from two áreas of the 

Southeastern coast of Brazil” compreende a influência dos fatores ambientais sobre a 

abundância e distribuição do siri Callinectes danae, destacando a abundância e 

distribuição da espécie em escala espacial e temporal. Esses siris foram coletados 

durante o período de julho/2001 a junho/2003 nas regiões de Ubatuba e Caraguatatuba. 

Assim, esta dissertação pretende contribuir com informações relevantes sobre aspectos 

da biologia e ecologia de diferentes espécies de crustáceos que habitam a costa sudeste 

brasileira.



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Almeida AC, Hiyodo C, Cobo VJ, Bertini G, Fransozo V & Teixeira GM. 2013. 

Relative growth, sexual maturity, and breeding season of three species of the 

genus Persephona (Decapoda: Brachyura: Leucosiidae): a comparative study. 

Journal of the Marine Biological Association of the United Kingdom 01: 1-11. 

Bauer RT. 2004. Remarkable shrimps: Natural History and Adapatations of the 

Carideans. University of Oklahoma Press, Norman, 316p. 

Bertini G, Fransozo A & Costa RC. 2001. Ecological distribution of three species 

of Persephona (Brachyura: Leucosiidae) in the Ubatuba region, São Paulo, 

Brazil. Nauplius 9(2): 31-42. 

Bertini G & Fransozo A. 2004. Bathymetric distribution of brachyuran crab 

(Crustacea, Decapoda) communities on coastal soft bottoms off southeastern 

Brazil. Marine Ecology Progress Series 279: 193-200. 

Bertini G, Fransozo A & Melo GAS. 2004. Biodiversity of brachyuran crabs 

(Crustacea: Decapoda) from non-consolidated sublittoral bottom on the northern 

coast of São Paulo State, Brazil. Biodiversity and Conservation 13: 2185-2207. 

Bertini G, Teixeira GM, Fransozo V & Fransozo A. 2010. 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): 7-17. 



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Felder DL, Feldmann RM, Fransen CHJM, Goulding LYD, Lemaitre R, Low 

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2009. A classification of living and fossil genera of decapod crustaceans. Raffles 

Bulletin of Zoology 21: 1-109. 

Haedrich RL, Rowe GT & Polloni PT. 1975. Zonation and faunal composition of 

epibenthic populations on the continental slope south of New England. Journal 

of Marine Research 33: 955-960. 

Hartnoll RG. 1982. Growth. In: Bliss DE & Abele LG (eds.), The biology of 

Crustacea: embryology, morphology and genetics. Vol. 2, Academic Press, New 

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Hartnoll RG. 1985. Growth, sexual maturity and reproductive output. In: Wenner 

AM (ed.), Crustacean issues: factors in adult growth. Vol. 3, AA Balkema, 

Rotterdan, pp. 101-128. 

Hartnoll RG. 2006. Reproductive investment in Brachyura. Hydrobiologia 557: 31-

40. 

Hecker B. 1990. Variation in megafaunal assemblages on the continental margin 

south of New England. Deep-Sea Research 37 (1): 37-57. 

Hendrickx ME. 1995. Camarones. In: W. Fischer, F. Krupp, W. Schneider, C. 

Sommer, K.E. Carpenter y V.H. Niem. (eds.), Guía FAO para la identificación 

de especies para los fines de la pesca. Pacífico centro-oriental. Vol. 1. Plantas e 

Invertebrados, FAO, Roma, Italia, pp 417-537. 



CONSIDERAÇÕES INICIAIS 

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12 
 

Hines AH. 1982. Allometric constraints and variables of reproductive effort in 

brachyuran crabs. Marine Biology 69: 309-320. 

Holthuis LB. 1980. Shrimps and Prawns of the World: An annotated catalogue of 

species of interest to fisheries. In: FAO Species Catalogue. FAO Fisheries 

Synopsis, 1: 1-270. 

Martin JW & Davis GE. 2001. An updated classification of the Recent Crustacea. 

Natural History Museum of Los Angeles County Science Series 39: 1-124. 

Melo GAS. 1996. Manual de identificação dos Brachyura (caranguejos e siris) do 

litoral brasileiro. Plêiade/FAPESP, São Paulo, 603 p. 

Ng PKL, Guinot D & Davie PJF. 2008. Systema brachyurorum: Part I. An 

annotated checklist of extant brachyuran crabs of the world. The Raffles Bulletin 

of Zoology 17: 1-286. 

Pinheiro MAA, Fransozo A & Negreiros-Fransozo ML. 1996. Distribution patterns of 

Arenaeus cribrarius (Lamarck, 1818) (Crustacea, Portunidae) in Fortaleza Bay, 

Ubatuba (SP), Brazil. Revista Brasileira de Biologia 56: 705-716. 

Ramos-Porto M, Coelho PA. 1998. Malacostraca. Eucarida. Caridea (Alpheoidea 

excluded). In: Young PS (ed.). Catalogue of Crustacea of Brazil. Rio de Janeiro: 

Museu Nacional, pp. 325-350. 

Sastry AN. 1983. Ecological aspects of reproduction. In: Vernberg FJ & Vernberg WB 

(eds.), The biology of Crustacea: environmental adaptations. Academic Press, New 

York, pp. 179−270. 



 

13 
 

 
 
 
 
 
 

INFRAORDEM CARIDEA



 

14 
 

CAPÍTULO 1 

 

REPRODUCTIVE STRATEGY OF THE 
SHRIMP Nematopalaemon schmitti 
(HOLTHUIS, 1950) (DECAPODA, 
CARIDEA, PALAEMONOIDEA) FROM 
THE SOUTHEASTERN BRAZILIAN 
COAST



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ABSTRACT 
 

The specimens of Nematopalaemon schmitti were captured in southeastern Brazil from 

2008 to 2011, for reproductive output (RO) and fecundity analysis of species. Changes 

in the egg development associated to the ovary maturation of ovigerous female were 

also analyzed in order to verify possible synchronous relationship between them. 

Obtained ovigerous females were measured (carapace length [CL]) and analyzed as the 

stage of development of their ovaries and eggs. The RO was calculated based on dry 

weight of eggs and female masses. Fecundity was expressed by the equation obtained 

from regression between egg numbers and CL. A significant relationship was observed 

between the number of eggs and CL (p<0.001), showing that as higher is the female 

higher is its capacity to produce eggs. Comparing the mean number of eggs in stages I 

and II in N. schmitti, became evident a loss of 7% of eggs. Females with rudimentary 

ovaries showed, predominantly, eggs in stage I and females with developed ovaries 

showed only eggs in stage II, showing synchrony between the developing of both, thus 

supporting the hypothesis of a continuous reproductive cycle for N. schmitti in the study 

region. The RO and fecundity can be affected for biotic and abiotic factors, as parasites 

and variations in the latitudinal gradient. Informations of the reproductive output and its 

relations with the synchrony between the gonadal and embryonic development are rare 

for the palaemonoid shrimps, although they are crucial in understanding the 

reproductive biology of these animals, as well as other caridean shrimps. 

 

Keywords: Egg loss, egg production, reproductive biology.



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INTRODUCTION 

 

Reproductive characteristics of crustaceans may vary according to the individual 

intrinsic aspects such as the size and age of females, and also environmental factors 

(Sastry 1983). These variations that can be the number and size of eggs and the 

reproductive investment of individuals may reflect adaptive mechanisms of species to 

environmental conditions. All these reproductive aspects play an important role in the 

biology and ecology of the species (Yoshino et al. 2002). Changes in volume of eggs of 

species of crustaceans were verified by Sastry (1983) in latitudinal gradients, depth, 

thermal and salinity. Furthermore, significant differences in reproductive investment of 

freshwater and marine caridean were verified by Anger & Moreira (1998). Thus, to 

study newly fertilized eggs can help show responses to selective pressures that these 

eggs were submitted, which affect the reproductive investment and larval development 

of crustaceans (Bauer 1991). 

Among the several subjects addressed in the reproduction of caridean shrimp 

studies, the reproductive output (RO) and the fecundity have been considered as 

important quantifiable measures of the species reproductive effort (e.g., Clarke et al. 

1991, Clarke 1993, Anger & Moreira 1998, Wehrtmann & Lardies 1999, Kim & Hong 

2004, Oh & Hartnoll 2004, Chilari et al. 2005, Pavanelli et al. 2008, Echeverría-Sáenz 

& Wehrtmann 2011). Reproductive output is defined by the association between the dry 

weight of the brood and dry weight of the female (Hines 1982). In general, both 

fecundity and RO show a strong relationship with some body measures of each species, 

and its respective variations at spatial and temporal scales. While, the Fecundity is 

considered as the number of eggs released by a female during a single spawning event 



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or specific period of its life history, being frequently associated to the female width 

(Negreiros-Fransozo et al. 1992, Ramírez-Llodra 2002). 

The population of whitebelly shrimp Nematopalaemon schmitti (Holthuis, 1950) 

has been heavily impacted due to the fishing activity, which can cause imbalances in the 

food chain in which it is, since it presents fundamental ecological importance in their 

habitat, serving as a food source for other species as an important item of marine trophic 

web (Fransozo et al. 2009, Almeida et al. 2012). Nevertheless, the publications related 

to this species are restricted to spatial and temporal variations in abundance and 

association with abiotic factors (Fransozo et al. 2009, Almeida et al. 2012), population 

structure and reproductive period (Almeida et al. 2011). In the southeast coast of Brazil, 

N. schmitti occurs at temperatures around 23°C (usually recorded during autumn and 

winter), in areas where the sediment is composed of fine and very fine sand and silt and 

clay, and presence of algae and plant fragments (Fransozo et al. 2009, Almeida et al. 

2012). Concerning the population structure of the whitebelly shrimp, there is a sexual 

dimorphism in body size, with males attaining smaller sizes than females. In addition, 

the reproduction of N. schmitti is characterized by a continuous pattern along the 

northern coast of São Paulo State (Almeida et al. 2011). 

Therefore, additional investigations that contribute to the knowledge of the N. 

schmitti life history and reproductive aspects on the southeastern coast of Brazil are 

needed for the purpose of maintaining and preserving the natural stocks. 

The aim of this study is describing some features of the reproductive biology of 

N. schmitti on the Brazilian southeastern coast, such as reproductive output (RO), 



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18 
 

fecundity (F) and possible synchronous relationship between ovary maturation and egg 

development. 



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19 
 

MATERIAL AND METHODS 
 

Shrimp samples were collected from Ubatuba Bay (23º 30’ S, 45º 09’ W), São 

Paulo, during November 2008, January 2009, July 2010 and July 2011 using a fishing 

boat carrying two otter-trawl nets (4.5 m wide; 20 mm and 15 mm mesh diameter at the 

body and cod end of the net, respectively). 

 Females carrying embryos at different stages of development were immediately 

placed in an ice chest filled with ice, transported to the laboratory and stored frozen 

until analysis. Next, the carapace length (CL, the distance from the orbital angle to the 

posterior margin of the carapace) of each female was measured with a caliper (precision 

= 0.1 mm). After that, each female was examined under a stereomicroscope to 

determine the degree of embryonic and ovarian development. Two stages of embryonic 

development were recognized: (1) embryos just spawned with no visible eyes, no 

visible blastoderm and uniformly distributed yolk and (2) embryos near hatching with 

large developed eyes and no yolk (Corey 1981, Jewett et al. 1985). Similarly, based on 

the color and volume of the ovary, three stages of ovarian development were 

recognized: (1) rudimentary ovaries filling less than half of the space in the 

cephalothorax having a translucent white coloration, (2) developing ovaries with light 

orange coloration filling most of space in the cephalothorax, and (3) developed ovaries 

(near spawning) with dark orange coloration filling all the space in the cephalothorax 

and the first abdominal segment (modified from Bauer & Abdalla 2000). 

Females were measured and their embryos and ovarian development examined. 

The totality of the embryos attached to the pleopods of each female was carefully 

extracted using a dissecting needles and a fine brush. After that, they were counted 



CAPÍTULO 1. REPRODUCTIVE STRATEGY OF N. schmitti 

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20 
 

under the dissecting microscope. Each female and their embryo masses were dried for 

48 h at 60°C and then weighed with an analytical balance (precision = 0.001 g). The 

differences between the number of eggs in different stages of development were tested 

using a Student t–test. 

The RO and fecundity were analyzed based on measurements of weight and 

body size, respectively. In addition, the brood production of the whitebelly shrimp was 

characterized according to changes in the ovary maturation and egg development. 

Differences in the RO of N. schmitti were analyzed by size classes with interval 

of 0.5 mm CL using analysis of variance (One-way ANOVA, ɑ = 0.05), followed by a 

multiple comparison test (Tukey, ɑ = 0.05). 

The fecundity (F = n° embryos female−1) of each female were obtained from 

both stages 1 and 2 of embryonic development. Whereas the reproductive output (RO = 

brood dry weight / female body dry weight - Clarke et al. 1991) was analyzed based on 

females carrying initial embryos (Stage I). The isometry was tested for F vs. CL and 

brood dry weight (BDW) vs. female body dry weight (FBW). For this purpose, the 

relationship between F and CL, and brood weight and body weight of females was 

examined using the allometric model y = axb, converted to the linear form, lny = lna + 

blnx, by means of natural logarithm transformation (y = dependent variables [F or brood 

dry weight]; x = independent variable [CL or body dry weight]; a = intercept on the y-

axis of the line relating y to x; and b = allometric coefficient - Hartnoll 1978, 1982). The 

slope b of the ln–ln least squares linear regression represents the rate of exponential 

change of each reproductive parameter with an increase in CL or body weight of female 

shrimps. The relationship between F and CL was considered isometric when b was = 3, 



CAPÍTULO 1. REPRODUCTIVE STRATEGY OF N. schmitti 

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21 
 

positively allometric when b > 3 and negatively allometric when b < 3 (Somers 1991). 

In turn, the relationships between brood dry weight and female body dry weight were 

considered isometric when b was = 1, positively allometric when b > 1 and negatively 

allometric when b < 1. Departures from isometry were tested using a Student t–test (Zar 

2010). 

 We estimated embryo loss (%) during embryonic development and examined the 

hypothesis of successive spawning in N. schmitti. The hypothesis of no embryo loss 

during development was tested using a Student t-test (Zar 2010). In this test, embryo 

stage (I vs. II) was used as the factor to estimate differences between females carrying 

embryos in different stages of development in fecundity. 

Lastly, the hypothesis of successive spawning was examined as in Bauer & 

Newman (2004) and Baeza (2006) by determining the association between embryonic 

and ovarian development. For this purpose, the association between embryonic and 

ovarian development categories was tested with the Goodman’s test, which analyzes the 

contrasts between and within multinomial proportions (Goodman 1965, Curi & Moraes 

1981). If females spawn successively after every molt, then the degree of embryonic 

development should be positively correlated with the degree of ovarian development. 

In the different analyses above, tests for homocedasticity and normality of the 

contrasted data sets (after ln-ln transformation) were examined and found to be 

satisfactory (Zar 2010). 



CAPÍTULO 1. REPRODUCTIVE STRATEGY OF N. schmitti 

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22 
 

RESULTS 
 

A total of 107 females carrying embryos at different stages of development were 

collected. Carapace length of ovigerous females varied between 10.2 and 13.7 mm, with 

mean (± standard deviation) of 11.6 ± 0.7 mm (Table I). 



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CAPÍTULO 1. REPRODUCTIVE STRATEGY OF N. schmitti 

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24 
 

Differences between RO and size classes was not statistically detected 

(ANOVA: F= 0.59, df= 7, p = 0.76), while the ratio between the weight of female and 

the weight of the egg mass was positive statistically significant (linear regression: F= 

27.67, df= 1.73, p< 0. 0001). Obtained an isometric relation to brood dry weight and 

female body dry weight. The average RO of N. schmitti was 0.123 ± 0.041, rangind 

from 0.055 to 0.248. The reproductive output total estimado was de 12.31% (Figure 1). 



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25 
 

 

Figure 1 – Nematopalaemon schmitti (Holthuis, 1950). Reproductive output (RO) by 

carapace length (CL), size class and weight. 



CAPÍTULO 1. REPRODUCTIVE STRATEGY OF N. schmitti 

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26 
 

 Fecundity of females carrying initial (stage I – N = 75) and final (stage II – N = 

32) embryos varied, respectively, between 740 and 3293 (1542.03 ± 480.00 eggs) and 

between 708 and 2310 (1433.34 ± 406.26 eggs). No statistical difference was observed 

between the number of eggs at different stages of development (Student t-test, p = 0:30) 

with a loss of only 7% of embryos during development. Obtained an isometric relation 

to F and CL ratio. A positive statistically significant correlation between fecundity and 

CL was detected for females carrying both initial and final stage embryos (linear 

regression; stage I: R = 0.61, df = 1, p < 0.001; stage II: R =0.54, df = 1, p = 0.001) 

(Figure 2). 

 

 

Figure 2 – Nematopalaemon schmitti (Holthuis, 1950). Allometric relationship between 

ln number of eggs and ln carapace length (I = initial embryonic development, II = final 

embryonic development). 

 



CAPÍTULO 1. REPRODUCTIVE STRATEGY OF N. schmitti 

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27 
 

 Lastly, the association between ovarian and embryonic development was 

statistically significant (Goodman’s test: p< 0.05). It is possible to observe changes in 

the egg development associated to the ovary maturation of females analyzed in the 

present study (Figure 3). Considering the developmental stages of eggs, there was a 

predominance of eggs in stage I (67.80%), followed by stage II (32.20%). In relation to 

gonadal development, it was observed that most females had rudimentary ovaries 

(53.33%). While females with developing and developed ovaries accounted for 34.44% 

and 12.22% of the total abundance, respectively. Females with rudimentary ovaries 

exhibited predominantly eggs at stage I, and females with developed ovaries showed 

only eggs in stage II. However, females with developing ovaries showed eggs in both 

stage I and II. 

 

 

 

 



CAPÍTULO 1. REPRODUCTIVE STRATEGY OF N. schmitti 

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28 
 

 

Figure 3 – Nematopalaemon schmitti (Holthuis, 1950). Frequency of ovigerous females 

(N = 100) in each embryo development stage (I = initial, II = final) related to each 

gonad development stage (Rudimentary, Developing, Developed). 



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29 
 

DISCUSSION 
 

No association was observed between reproductive output and the carapace 

lenght for N. schmitti in this study. Echeverría-Sáenz & Wehrtmann (2011) obtained 

similar results for Heterocarpus vicarius Fazon, 1893, attributing the lack of association 

between the RO and CL to variations in egg size of species. According Wehrtmann & 

Lardies (1999), as observed for fertility, the RO would also be related to latitudinal 

differences. These authors compared the RO of Austropandalus grayi (Cunningham, 

1871) (collected in the Magellan Region, South America) with other species, and 

observed that A. grayi present lower values of RO compared to Pandalus borealis 

Kroyer, 1838 (collected in Western Bering Sea) and Pandalus montagui Leach, 1814 

(collected in Northumberland coast, England), but high value when compared to 

Heterocarpus reedi Bahamonde, 1955 (collected in Northern Chile), indicating RO 

increased by increasing latitude. Thus, the production of eggs in caridean can be 

associated to the latitude of the area in which the species is distributed, there is a 

tendency to reduce the number of eggs and increase in eggs volume for the species that 

inhabit regions of high latitudes (Clarke et al. 1991, Echeverría-Sáenz & Wehrtmann 

2011). It is possible that in southeastern Brazil the RO of N. schmitti is under latitudinal 

influence (23° 26’ S to 45° 02’ W), as observed by Clarke et al. (1991), Wehrtmann & 

Lardies (1999) and Echeverría-Sáenz & Wehrtmann (2011) for P. borealis species, A. 

grayi and H. vicarius, respectively, at different latitudes, for example 79° 10' N, 10° 40' 

E, 58° 47' N, 10° 55' E (Clarke et al. 1991.); 53° 42' 8'' S, 70° 57' 4'' N, 55° 09' 2'' S, 67° 

01' 6'' W (Wehrtmann & Lardies 1999). How different latitudes imply different 

environmental conditions, specimens of N. schmitti obtained in this study in a tropical 

region have higher RO compared to species of polar areas, probably due to high 



CAPÍTULO 1. REPRODUCTIVE STRATEGY OF N. schmitti 

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30 
 

temperature, food availability, among other factors. Thus, species of tropical regions 

may have higher RO and consequent increased production of eggs to ensure the survival 

of their offspring by abiotic and biotic conditions favorable to their establishment in 

these regions. 

Assuming that female size is closely linked to reproductive strategies (Hines 

1982), the positive relationship between carapace length and number of eggs observed 

in N. schmitti is corroborated with previous studies for other caridean shrimp as P. 

borealis (Clarke et al. 1991), Hippolyte zostericola (Smith, 1873) (Negreiros-Fransozo 

et al. 1996), A. grayi (Wehrtmann & Lardies 1999) Exhippolysmata oplophoroides 

(Holthuis, 1948) (Chacur & Negreiros-Fransozo 1999), Hippolyte obliquimanus Dana, 

1852 (Mantelatto et al. 1999) and Palaemon gravieri (Yu, 1930) (Kim & Hong 2004). 

This positive relationship suggests that larger females produce more eggs because they 

are more energy resource and ability to use it (Baeza 2006), and more space in the 

abdomen to accommodate them (Clarke 1993, Chacur & Negreiros-Fransozo 1999, 

Mantelatto et al. 1999). According to Calado & Dinis (2007), in some cases after the 

seeding of puberty the growth rate of individuals of Lysmata seticaudata (Risso, 1816) 

decreases and energy resources are directed to gonad maturation. In the present study 

we observed that smaller females produce fewer eggs than larger females. Probably due 

to the larger females have higher abdominal cavity to accommodate the embryos and 

greater available energy resource, investing more in reproduction than smaller females. 

Although it is clear that the number of eggs is larger in larger females, the reproductive 

output does not vary significantly. The variation is much greater within each class than 

between the averages of the different classes. 



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Studies show that the number of eggs tends to be higher in areas of low latitude, 

not associated only to the size of females (Clarke et al. 1991, Wehrtmann & Lardies 

1999), which may vary with the number of consecutive spawns in a same reproductive 

cycle (Sainte-Marie 1993) and by the loss of eggs during embryonic development 

(Mantelatto et al. 1999). 

The egg loss that occurs during the development of embryos was reported by 

different authors (Wehrtmann & Lardies 1999, Nazari et al. 2003, Kim & Hong 2004, 

Oh & Hartnoll 2004, Echeverría-Sáenz & Wehrtmann 2011), among them Nazari et al. 

(2003) emphasize that this loss may be favorable for the eggs which remain adhered to 

the female pleopods, since they will have more space to accommodate in the abdominal 

cavity, allowing a greater circulation of water between them and the consequent 

increase rate of oxygen around them. Some authors mention the loss of eggs can be 

influenced by specimens sampling, increased volume eggs, parasite action or 

mechanical stress (Wehrtmann & Lardies 1999, Kim & Hong 2004, Oh & Hartnoll 

2004, Echeverría-Sáenz & Wehrtmann 2011). In study conducted with the caridean A. 

grayi (Wehrtmann & Lardies 1999), it was verified the species loses 51.1% of the 

initially exteriorized eggs, being this loss related to the capture process and abrasions 

between embryos as for the caridean H. vicarius, a loss of 46.9% was observed 

(Echeverría-Sáenz & Wehrtmann 2011), which is associated with the end of embryonic 

development, when the incorporation of a large quantity of water occurs, which 

facilitates the larvae hatching. With the incorporation of large amounts of water, the 

eggs are larger and the space between them is reduced, which facilitates the abrasion 

between the embryos and the consequent loss to the environment. To N. schmitti a loss 

of less than the eggs of other species, with only 7% was observed. It was observed that 



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32 
 

the loss of eggs in N. schmitti and other caridean, Exopalaemon modestus (Heller, 1862) 

(Oh et al. 2002) were similar, both around 7%. However, E. modestus inhabits 

freshwater environment and is subject to different conditions of temperature and salinity 

compared to the species of the marine environment. Moreover, the collection 

methodology can influence this loss, varying according to the time and type of network 

used in the sampling of specimens. For E. modestus used a hand net, while for N. 

schmitti made use of trawl nets. It is believed that the drag is more stressful for the 

animals, since they require longer collection time. 

In the present study, comparing the abundance of females according to each 

stage of development of eggs and ovaries, it was possible to see, in general, synchrony 

between the development of both. Females with rudimentary ovaries showed mostly 

eggs in stage I, and females with developed ovaries showed only eggs in stage II. 

According to the results obtained in this study, along with the standard continuous 

reproduction of N. schmitti in the study region (Almeida et al. 2011), it is assumed that 

the reproductive cycle of females occurs as follows: females with ovaries in advanced 

stages of development suffer molt, called "parturial molt" are copulated and then 

externalize their eggs. After extrusion, the ovaries of these females are rudimentary, and 

eggs in early stages of development. During the incubation period, both the eggs as the 

ovaries develop almost in synchrony, and at larvae hatching, the ovaries of these 

females are at an advanced stage of development, beginning again with the reproductive 

cycle. With these results, we argue in support of the hypothesis of successive spawning 

as in Bauer & Newman (2004) and Baeza (2006). It was noted in this study that the 

number of eggs exteriorized by N. schmitti is correlated to carapace length, showing that 

larger specimens have higher space available to accommodate the eggs in the abdomen 



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33 
 

and greater potential as energy resources for production of the eggs. The loss of 7% in 

the number of eggs initially externalized can be linked to factors such as the increase in 

egg volume and the action of parasites, for example, may also have some influence on 

the loss. Although larger females have shown a greater number of eggs, the RO was not 

significantly associated to the size of females. Therefore, research on the reproductive 

biology of species that are widely distributed among different latitudes, help in 

understanding the influence of these species on the production of eggs. Through the 

wide geographic distribution of caridean N. schmitti, studies that address the RO along 

the Atlantic became critical for a better understanding of the reproductive biology of 

this species. The synchrony observed between the development of eggs and ovaries 

supports the standard cycle of continuous reproduction of N. schmitti in the study 

region. These results allow us a better understanding not only of the reproductive 

biology of N. schmitti, as well as other caridean which occur in the region of this study. 

Researches of this nature are essential for us to be able to propose effective conservation 

strategies, such as mitigation of impact on natural communities and important 

suggestion for conservation, and provide support for new research that addresses the 

biology and ecology of decapod crustaceans. 

 



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34 
 

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Zar JH. 2010. Biostatistical analysis. 5th ed, Prentice-Hall, Upper Saddle River, New 

Jersey, 944 p. 



 

39 
 

 
 
 
 
 
 

INFRAORDEM BRACHYURA



 

40 
 

CAPÍTULO 2 

 

ECOLOGICAL DISTRIBUTION AND 
POPULATION PARAMETERS OF 
Persephona mediterranea (HERBST, 
1794) (BRACHYURA, LEUCOSIIDAE) IN 
A PROTECTED AREA ON THE 
SOUTHEASTERN BRAZILIAN COAST



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41 
 

ABSTRACT 
 

The crab Persephona mediterranea is an abundant species in trawl fisheries in the 

Brazilian coast. As with other by catch species, it is subjected to similar impact as 

target species. In order to ascertain the life history of by catch species, 

investigations on their distribution and population parameters are needed. Such 

information becomes even more strategic when obtained from priority areas for 

conservation, for instance marine protected areas. In this study we aimed to 

describe the patterns of ecological distribution of P. mediterranea at different 

depths and seasons in the Ubatuba region, which is included in a marine protected 

area off the southeastern coast of Brazil (APA Navy - Sector Cunhambebe). 

According to our results, P. mediterranea is more abundant during the winter and at 

depths of 10 to 15 m. The type of sediment, salinity variations at the bottom of the 

water column and depth strongly affect the demographics of this species. With 

respect to the population parameters, the recruitment pattern and continuous 

reproduction are highlighted. Our results on population structure, sex ratio and 

sexual maturity are similar to literature records for the southeastern region of the 

continental shelf, suggesting that the distributional, structural and reproductive 

characterization of P. mediterranea seems to be conservative among species of the 

genus Persephona. Results of studies such as ours, therefore, are indispensable for 

future comparisons and to make decisions concerning the species in a newly 

established Marine Protected Area on the southeastern coast of Brazil. 

 

Keywords: Bathymetry, Brazilian littoral, purse crab, size at sexual maturity. 



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INTRODUCTION 
 

The zonation of the soft-bottom marine fauna is probably the result of the 

interaction among complex physical and biological factors, and the relative 

importance of each factor varies among the different areas (Hecker 1990). What 

exactly determines zonation in benthic marine communities is insufficiently 

understood. The traditional perception has been that changes in the fauna 

correspond with variables in the physical environment, for example temperature, 

sediment type, intensity of currents, and topography (Haedrich et al. 1975). 

As noted by Bertini & Fransozo (2004), the bathymetric distribution pattern 

of crabs is visible and, according to Pinheiro et al. (1996), it derives from the direct 

influence of environmental and biotic factors, which act on the benthic community. 

The distribution of decapods has been studied and associated with environmental 

factors such as bottom temperature, surface salinity, organic matter content, grain 

size and depth. The following publications on the subject are noteworthy: Santos et 

al. (1994), Negreiros-Fansozo & Fransozo (1995), Pinheiro et al. (1996), Atrill et 

al. (1999), Bertini et al. (2001), Martínez et al. (2009), Carvalho et al. (2010), 

Carvalho & Couto (2010). Environmental and biotic factors vary in space and time, 

and are especially influential in coastal areas when it comes to the population 

dynamics of crustaceans (Warwick & Uncles 1980, Bertini et al. 2001). 

The reproductive cycles observed in decapods are continuous or seasonal 

(Sastry 1983, Choy 1988, Emmerson 1994, Pinheiro & Fransozo 2002). Several 

authors have studied the reproductive cycle of brachyurans with respect to the 

presence reproductively mature individuals (with developed gonads) and presence 

of ovigerous females (Batoy et al. 1987; Mantelatto & Fransozo 1999, Reigada & 



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43 
 

Negreiros-Fransozo 1999, Mantelatto 2000, Pinheiro & Fransozo 2002, Bertini et 

al. 2010). Factors such as latitude, temperature and food availability can influence 

the reproductive season of brachyuran (Emmerson 1994). 

The crab Persephona mediterranea (Herbst, 1794) is widely distributed in 

the western Atlantic, with records of occurrence at the intertidal zone down to 60 m 

deep (Melo 1996). Although the species is not considered of economic importance, 

Bertini et al. (2010) pointed out that populations of this crab are subject to similar 

impacts as commercially harvested crabs and prawns in the southeastern coast of 

Brazil. Furthermore, the species plays an important ecological role as part of the 

trophic web (Martínez et al. 2009, Almeida et al. 2013). 



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MATERIAL AND METHODS 
 

1. Study area and sampling 

The Ubatuba region was established as a MPA (Marine Protected Area from 

north coast: Sector Cunhambebe) by Proclamation No. 53525, on 8 October 2008 

by the Brazilian Ministry of Environment, which aimed to prioritize the 

conservation, preservation and sustainable use of marine resources in the region. 

Under this MPA, fishing is only permitted in two circumstances: when it is 

necessary for the subsistence of traditional human communities, or for sports. 

Commercial fishing is not allowed. The idea is to protect, ensure and discipline the 

rational use of resources in the region, promoting sustainable development. 

This region is characterized by innumerable spurs of the Serra do Mar 

mountain chain that form an extremely indented coastline (Ab`Saber 1955). The 

exchange of water and sediments between the coastal region and the adjacent shelf 

is very limited (Mahiques 1995). This region is influenced by three water masses: 

coastal water (CW: temperature > 20oC, salinity < 36 PSU), tropical water (TW: > 

20oC, > 36 PSU) and South Atlantic central water (SACW: < 18oC, < 36 PSU) 

(Castro-Filho et al. 1987, Odebrecht & Castello 2001). During summer months, the 

SACW penetrates into the bottom layer of the coastal region and forms a 

thermocline over the inner shelf, which is located at depths of 10 to 15 m. In the 

winter, the SACW retreats to the shelf break and is replaced by the CW. As a result, 

no stratification is present over the inner shelf (Pires 1992, Pires-Vanin & Matsuura 

1993). The sediment is composed mainly of silt, clay, and fine and very fine sand, a 

result of the limited water movement within the bay and between the bay and the 

adjacent continental shelf (Mahiques et al. 1998). 



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Specimens of P. mediterranea were collected monthly in Ubatuba, São 

Paulo, from January to December 2000. Samples were taken with a commercial 

fishing boat equipped with "double rig" type nets (mesh size 20 mm, 15 mm in the 

cod end). Trawling was conducted at six different depths (10 m, 15 m, 20 m, 25 m, 

30 m and 35 m) in the Ubatuba region (Figure 1). 

 

 

Figure 1 - Study area and transect sampling in Ubatuba, north coast of São Paulo, 

Brazil. 

 

In each transect sampled we recorded bottom (BT) and surface (ST) 

temperatures, bottom (BS) and surface (SS) salinity, organic matter (OM) and 

sediment grain size (Phi). 

Salinity (PSU) and temperature (oC) were measured in samples of the 

bottom-water, obtained each month from each transect, using a Nansen bottle. 

Temperature was measured with a mercury thermometer and salinity was measured 

with an optic refractor. 

Sediment samples were collected seasonally with a 0.06 m2 Van Veen grab. 

In the laboratory, the sediment was oven-dried at 70oC for 72h. For analysis of 



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46 
 

grain size composition, two 50 g sub-samples were separated, treated with 250 ml 

of a 0.2 N NaOH solution and stirred for 5min to release silt and clay particles. 

Sub-samples were then rinsed on a 0.063 mm sieve. Sediments were sieved through 

2 mm (gravel); 2.0-1.0 mm (very coarse sand); 1.0-0.5 mm (coarse sand); 0.5-0.25 

mm (medium sand); 0.25-0.125 mm (fine sand); 0.125-0.063 mm (very fine sand); 

smaller particles were classified as silt-clay. Cumulative particle size curves were 

computer-plotted using the phi scale and phi values, corresponding to the 16th, 50th 

and 84th percentiles read from the curves to determine the mean diameter of the 

sediment. This was calculated using the formula Md = (φ15 + φ50 + φ84)/3. The value 

of phi was calculated using the formula φ = -log2d, where d = grain diameter (mm). 

The organic matter content of the sediment was calculated by the difference 

between the ash-free dry weights of three 10 g substrate subsamples incinerated in 

porcelain crucibles at 500oC for 3h. 

The three quantitatively most important sediments were defined according 

to Magliocca & Kutner (1965): class A corresponds to sediments in which medium 

sand (MS), coarse sand (CS), very coarse sand (VCS) and gravel (G) account for > 

70% of the total weight; in class B, fine sand (FS) and very fine sand (VFS) make 

up > 70% of total weight of sediment. More than 70% of sediments in class C are 

silt and clay (S+C). From these three categories, groups were established according 

to the combination of granulometric fractions in several proportions: PA = 

(MS+CS+VCS+G) > 70%; PAB = prevalence of A over B (FS+VFS); PAC = 

prevalence of A over C (S+C); PB = (FS+VFS) > 70%; PBA = prevalence of B 

over A; PBC = prevalence of B over C; PC = (S+C) > 70%; PCA = prevalence of C 

over A; PCB = prevalence of C over B. All procedures for sediment analysis 

followed Hakanson & Jansson (1983) and Tucker (1988). 



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Species identification was based on Melo (1996). The gender of the crabs 

was identified and specimens were dissected for the macroscopic observation of 

gonad development. The sex of the crabs was determined by scanning the shape of 

the abdomen and number of pleopods in each individual (abdomen of females 

approximately oval with four pairs of pleopods; males with abdomen elongated in a 

“T" with two pairs of pleopods). The gonads were classified into four stages of 

development according to their volume and color: immature (IM), rudimentary 

(RU), developing (DE) and advanced (AD) (adapted from Johnson 1980 and 

Bertini et al. 2010). From the classification of gonad groups the population 

structure (demographics) was defined for statistical analysis as IMM, IMF, RUM, 

RUF, DEM, DEF, ADM, ADF and OF (ovigerous females). The following 

abbreviation acronyms of gonad development were used, followed by M for male 

and F for female. Gonads were measured with a precision caliper (0.01mm), and 

the largest width of the carapace (CW) was measured. 

 

2. Statistical analyses 

Initially, we tested the data for univariate and multivariate analysis 

normality, respectively, sing the Shapiro-Wilk test (Shapiro & Wilk 1965) and 

symmetry and multivariate kurtosis (Mardia 1970, 1980) (with modifications 

proposed by Doornik & Hansen 2008 - omnibus test). In order to test for univariate 

and multivariate homogeneity (equivalence of covariance matrices) we used the 

Levene test (Levene 1960) and the M Box test (Anderson 1958), respectively. 

We analyzed crab size (CW) and population structure temporally (seasons) 

and spatially (depth) through the SDF, considering the demographic groups (males, 

females and ovigerous females). The number of size classes was estimated by the 



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48 
 

rule of (1926): K = 1+3.322 x logN, where K = number of classes, N = number of 

individuals captured. The range class was obtained by the equation A/K, where 

A=difference of the largest individual collected minus the smallest individual 

collected. As for the sex ratio, the subjects were analyzed for each sex, month and 

season using the multinomial proportions test proposed by Goodman (Goodman 

1964). This analysis compares the binomial proportion between and within 

multinomial populations (Curi & Moraes 1981). 

The gonad sexual maturity was evaluated by plotting a logistic curve for 

each sex. The relative frequency (%) of subjects considered from the standpoint of 

mature gonads was plotted on a graph with the respective data size classes 

(Vazzoler 1996). The data were fitted by the logistics equation curve: Y=1/1 + e r 

(LC-LC
50

) with r = slope of the line, and LC50 = width of shell in which 50% of 

individuals are mature. The fit of the logistic function was determined by the 

method of least squares using the routine "Solver" program Microsoft Excel 

(Microsoft 2010) and by the GRG2 algorithm (Fylstra 1998). We considered 

individuals to be mature when their gonads could be classified as RU, DE and AD. 

The relative abundance of crabs in groups of population structure (gonad 

stages) with respect to the environmental factors examined in each transect was 

assessed using redundancy analysis (RDA). Subsequently, we performed an 

adjustment of the RDA environmental vectors, a routine that draws the maximum 

correlation of environmental variables with the correlation data. The evaluation of 

the significance of the vectors adjustment was conducted through permutations (n = 

9999) using the goodness of fit statistics of the squared (r2) correlation coefficient. 

According to Oksanen et al. (2012), for the environmental variables it is defined as 



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49 
 

r2 = 1 – SSw/ SSt, where: SSw - sum of squares within groups and; SSt - total sum 

of squares. 

All analyzes were performed using the software R (R Development Core 

Team 2012), considering ɑ = 0:05 (Zar 2010). The RDA and the adjustment of the 

environmental vectors were made with the package "vegan" (Oksanen et al. 2012). 

Each analysis was conducted separately, in order to avoid computational conflicts. 



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RESULTS 
 

1. Population parameters 

We obtained a total of 194 specimens of P. mediterranea: 96 males, 24 non-

ovigerous and 74 ovigerous females. Males were more abundant in 15 m and 20 m 

depths; females, 15 m and 25 m (Table I). The abundance of individuals of both 

sexes was low in the 10 m and 35 m depths. The largest amount of ovigerous 

females was found in the 15 m transects and the smallest numbers in the 10 m, 20 

m and 25 m depths. Ovigerous females did not occur at depths of 30 m and 35 m 

(Figure 2). The smallest mature male measured 23 mm CW, the smallest non-

ovigerous female, 20.3 mm and the smallest ovigerous female, 25.7 mm CW. 

 

Table I - Persephona mediterranea (Herbst 1794). Abundance of demographic groups 

in Ubatuba during the sampling period, for bathymetry. M – Males, F – Non ovigerous 

females, OF – Ovigerous females. 

Depth M F OF Total 
10 2 0 4 6 
15 36 8 29 73 
20 30 4 25 59 
25 22 8 16 46 
30 2 1 0 3 
35 4 3 0 7 

Total per 
sex 96 24 74 194 

Percentage 49% 12% 38% 100% 
 



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51 
 

 

Figure 2 - Bathymetric distribution of demographic groups in Ubatuba during the 

sampling period. M – Males, F – Non ovigerous females, OF – Ovigerous female. 

A – 10 meters; B – 15 m; C – 20 m; D – 25 m; E – 30 m; F – 35 m. 

 

Ovigerous females occurred in all seasons; they were not very abundant in 

the spring and summer. The largest size class crabs were more abundant in autumn 

and winter, whereas summer and spring were characterized by the presence of crabs 

in the lower class sizes (Figure 3). 



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52 
 

Figure 3 - Seasonal distribution of demographic groups in Ubatuba during the 

sampling period. See Figure 2 for acronyms. A – Summer; B – Autumn; C – 

Winter; D – Spring. 

 

The multinomial analysis of Goodman indicated that there were seasonal 

(summer) and monthly (February) differences in the male/female ratio (Table II). 

When considering the variation in monthly multinomial proportions of each sex, we 

found different proportions of males in March, April, September, November and 

December and of females in January, March, April, June, August, September, 

November and December (Table II). Secondarily, with regards to the variation in 

seasonal multinomial proportions of each sex, differences were found between the 

summer and the other seasons for males, and between the summer and the winter 

for females (Table II). The size (CW) at which 50% of the crabs reached gonad 

maturity (CW50) was 29.98 mm for males and 28.80 mm for females (Figure 4). Of 

the 194 individuals collected, only 3 (1.55%) were immature (Table III).



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54 
 

Figure 4 - Gonad size at maturity (CW50) of males (full line) and females (dot line) 

of P. mediterranea from Ubatuba. 



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Table III - Persephona mediterranea (Herbst 1794). Abundance of immature and 

mature groups in Ubatuba during sampling period, by month. 

Month 

Absolute 
frequency 

of 
immatures 

Relative 
frequency 

of 
immature 

(%) 

Absolute 
frequency 
of mature 

forms 

Relative 
frequency 
of mature 

forms 
(%) 

Jan 0 0 18 9.28 
Feb 0 0 12 6.19 
Mar 0 0 3 1.55 
Apr 0 0 12 6.19 
May 2 1.03 14 7.22 
Jun 0 0 1 0.52 
Jul 0 0 43 22.16 
Aug 0 0 51 26.29 
Sep 0 0 8 4.12 
Oct 0 0 25 12.89 
Nov 0 0 2 1.03 
Dec 1 0.52 2 1.03 

Total 3 1.55 191 98.45 
 

 

2. Bathymetric distribution 

Redundancy Analysis (RDA) indicated that, in the first two axes generated, 

there was variation in the proportion of data in 95.18% (= 88.02% Axis 1 and Axis 

2 = 7.16%) (Figure 5). The adjustment algorithm of the environmental vectors of 

the RDA proved that the groups of population structure are associated with the 

three environmental variables (salinity in the bottom - BS, Depth and Phi) (Table 

IV). Of the three environmental variables with significant correlation, according to 

the adjustment vectors, the observed order of influence in structuring the 

community were Phi, BS and depth. The population structure groups in the early 

stages of gonad development (IMM, IMF, RUF, RUM) were in the center of origin 



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56 
 

of the RDA graph, indicating that these groups are the ones that are less associated 

with specific abiotic variables, whereas a gradient of gonad maturation for both 

sexes was observed in the negative direction of the axis 1 of the RDA. A direct 

association between the environmental variables Phi and BS with the gonad 

development gradient was observed, whereas depth was negatively associated with 

this gradient (Figure 5). The highest abundance was obtained in transects at 15 m 

and 20 m. The environmental factors checked in each transect were represented by 

their mean value and standard deviation (Figures 6, 7). 

 

Figure 5 - Redundancy Analysis (RDA) for P. mediterranea in the Ubatuba region. 

See Material & Methods for variables and population structure acronyms. 

*significant variables under the environmental fitting algorithm. 



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Table IV - Environmental fitting from analysis of redundancy (RDA) showing 

significant correlated variables. R2 – determination coefficient. See Material & 

Methods for variables acronyms. 

  Axis 1 Axis 2 R2 p-value 
BT 0.45 0.9 0.04 0.591 
BS -0.67 -0.74 0.39 0.002 

Depth 0.2 -0.98 0.25 0.029 
Phi -0.8 0.6 0.34 0.008 
OM -0.97 -0.23 0.15 0.126 

 

 

 

Figure 6 - Mean salinity, surface and bottom temperature variation of six transects 

from Ubatuba during 2000, by season. 

 



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Figure 7 - Granulometric fractions, Organic-matter content (% OM), and phi of 

each transect. Grain-size classes (%): Black = Class A; Striped = Class B; White = 

Class C (see Materials and methods for details). 

 

 



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DISCUSSION 
 

Persephona mediterranea was most abundant in the 15 m and 20 m 

transects, where 68 % of the individuals were captured. This result is consistent 

with the findings of Bertini & Fransozo (2004) and Bertini et al. (2010), who also 

collected more exemplars from transects at 15 m at 25 m. The preference for 

transects with similar sediment characteristics reflects the behavior of leucosids, 

which often get buried in fine sediment (Bertini et al. 2001, Carvalho et al. 2010). 

The seasonal distribution indicated that P. mediterranea was most abundant 

in the winter. Bertini et al. (2001) found that Persephona lichtensteinii Leach, 1817 

was more abundant in winter, whereas Persephona punctata (Linnaeus, 1758) was 

most abundant in the spring. Other authors observed a greater abundance of P. 

punctata and P. lichtensteinii in the autumn (Carvalho et al. 2010). Thus, we 

suggest that there is a reasonable variation in the abundance of species of the genus 

Persephona with respect to temporal variations. 

The CW50 was slightly greater in males (29.98 mm) than in females (28.80 

mm) in a manner similar to that found in the work Bertini et al. (2010), who studied 

the reproductive period and size of P. mediterranea at sexual maturity. Almeida et 

al. (2013) studied the relative growth, sexual maturity and reproductive period of 

three species of the genus Persephona Leach, 1817, including P. mediterranea. The 

same pattern was observed in other species of Persephona (Carvalho et al. 2010, 

Almeida et al. 2013), indicating that this is a conservative character in the genus. 

However, we emphasize that sexual maturity in decapods is subjected to spatial and 

latitudinal variations according to the different growth rates of individuals and 

changes in environmental factors that affect the organisms (Annala et al. 1980, 



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Hines 1982, 1989, Sampedro et al. 1999, Lestang et al. 2003). Significant 

differences in the size at which organisms reach sexual maturity may occur between 

sexes and congeneric species that have different reproductive strategies (Hartnoll 

1985, Ramírez-Llodra 2002). 

The sexual dimorphism found in our data, by which males had larger 

carapace compared to females, is a common pattern for Brachyura. After reaching 

sexual maturity, females grow slower, probably due to the energy requirements for 

egg production (Hartnoll 1982, 2006, Diaz & Conde 1989, Haefner & Spaargaren 

1993, Mantelatto & Martinelli 1999, Bertini et al. 2010). When studying sexual 

maturity, the trade-off between growth and reproduction, processes that compete 

for energy resources, must be considered (Hartnoll 1985, Haefner & Spaargen 

1993, Ramírez-Llodra 2002). Thus, in order for individuals to achieve reproductive 

success, resources must be properly allocated for it. 

The reproductive pattern of P. mediterranea is continuous, which can be 

verified by the presence of individuals in reproductive age and ovigerous females 

throughout the year. However, in certain months, the reproductive activity is 

reduced. A similar pattern was observed by Bertini et al. (2010) for P. 

mediterranea and Almeida et al. (2013) for P. mediterranea and P. punctata, which 

suggests that the reproductive activity is conservative for the genus Persephona. 

The pattern of continuous reproduction was also observed in other species 

on the northern coast of São Paulo, a subtropical region, for instance Callinectes 

danae Smith, 1869 studied by Costa & Negreiros-Fransozo (1998), Callinectes 

ornatus Ordway, 1863 by Mantelatto & Fransozo (1999) and Hepatus pudibundus 

(Herbst, 1785) by Reigada & Negreiros-Fransozo (1999). Subtropical and tropical 

regions provide favorable conditions for this pattern of continuous reproduction, 



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gonad and larval development and nutrition of individuals. However, temperate 

regions end up restricting the reproductive period of the species, which becomes 

seasonal following the availability seasonal of resources and variations in 

temperature (Sastry 1983). 

The presence of developed female gonads and ovigerous females throughout 

the year may be an indication that the study area is a region where reproduction 

takes place and should be protected. Two pieces of evidence support the hypothesis 

of continuous reproduction in the region: the benefits of the organic matter content 

of the substrate for the crustaceans, which results in the enrichment of the pelagic 

trophic system, impacting the benthic system (González-Gurriarán & Olaso 1987), 

and the position of the ovigerous females in areas under the influence of the 

dynamics of water bodies, which acts on larval dispersal, directing the larvae to 

locals that favor the development (Mantelatto 2000). 

The continuous recruitment pattern is characteristic of individuals with 

continuous reproduction. However, in this study we observed few numbers of 

immature individuals (1.55 %). The same was found by Almeida et al. (2013), and 

Bertini et al. (2010), who attributed the shortage of juveniles to the cryptic habits of 

P. mediterranea, recruitment in other areas, or ecological distribution. 

The results presented here may be similar for other species of the genus 

Persephona along the Brazilian coast, since distributional, structural and 

reproductive characterization seems conservative. Thus, this study provides 

practical data for future comparisons of the life history and distribution patterns of 

P. mediterranea in a newly established marine protected area. 



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