, Volume 74, Issue 8, pp 1011–1019 | Cite as

The different depths gradients may affect the reproductive dynamics of Hepatus pudibundus (Herbst, 1785) (Decapoda: Aethridae) in the southeastern region of Brazil

  • Veronica Pereira BernardesEmail author
  • Francislene Karina Martins
  • Gabriel Fellipe Barros Rodrigues
  • Camila Hipolito Bernardo
  • Aline Nonato de Sousa
  • Giovana Bertini
  • Adilson Fransozo
Original Article


The aim of this study was to evaluate the spatio-temporal variation and influence of environmental factors on the reproduction of H. pudibundus, and to estimate the size at the onset of sexual maturity (CW50). Samples were taken monthly from January to December 2000 in nine transects ranging from 2 to 40 m of depth. Bottom temperature, salinity, and sediment texture were recorded at each transect. Crabs were separated according to sex, measured (carapace width; CW), and classified according to their gonadal development stage. In total, 1808 individuals were captured: 498 males, 1039 non-ovigerous females, 173 ovigerous females, and 98 juveniles (males and females). The average size at the onset of sexual maturity of males and females was similar, 32.1 mm and 32.0 mm, respectively. This was unexpected since larger males have an advantage in competitions for females and during intraspecific interactions. Reproduction occurred continuously year-round, with peaks in summer and spring. These peaks might be caused by a higher food availability during this period, which could provide better survival conditions for the larvae. Reproductive females were more abundant at depths of 10–25 and 40 m, probably due to their migratory behavior that facilitates larvae dispersal and survival.


Brachyura Ubatuba Reproductive period Sexual maturity Conservation 



We are grateful to the Fundacão de Amparo à Pesquisa do Estado de São Paulo (FAPESP) for providing financial support (# 97/12108-6 and 97/12106-3). We are also thankful to our NEBECC co-workers for their help during fieldwork. All samplings have been conducted complying with current state and federal laws.

Compliance with ethical standards

Ethical approval

All samplings were conducted in compliance with current applicable state and federal laws.

Conflicts of interest

The authors declare that they have no conflict of interest.


  1. Abelló P, Valladares FJ, Castellón A (1988) Analysis of the structure of decapod crustacean assemblages off the Catalan coast (North-West Mediterranean). Mar Biol 98(1):39–49CrossRefGoogle Scholar
  2. Aidar E, Gaeta SA, Gianesella-Galvão SMF, Kutner MBB, Teixeira C (1993) Ecossistema costeiro subtropical: nutrientes dissolvidos, fitoplâncton e clorofila-a e suas relações com as condições oceanográficas na região de Ubatuba, SP. Publ Esp Inst Oceanogr 10:9–43Google Scholar
  3. Alencar CERD, Lima-Filho PA, Molina WF, Freire FAM (2014) Sexual shape dimorphism of the mangrove crab Ucides cordatus (Linnaeus, 1763) (Decapoda, Ucididae) accessed through geometric morphometric. Sci World J 2014:1–8. CrossRefGoogle Scholar
  4. Almeida AA, Fransozo V, Monteiro Teixeira GM, Furlan M, Hiroki KAN, Fransozo A (2011) Population structure period of white belly prawn Nematopalaemon schmitti (Holthuis, 1850) (Decapoda: Palaemonidae) on the southern coast of Brazil. Invertebr Reprod Dev 55(1):30–39. CrossRefGoogle Scholar
  5. Andrade LS, Fransozo V, Cobo VJ, Castilho AL, Bertini G, Fransozo A (2013) Ontogenetic distribution of Callinectes ornatus (Decapoda, Portunoidea) in southeastern Brazil. Cienc Mar 39(4):371–385. CrossRefGoogle Scholar
  6. Andrade LS, Bertini G, Fransozo F, Teixeira GM, Barros-Alves SP, Fransozo A (2014) Differential occupation of habitat as a reproductive strategy of the blue crab Callinectes ornatus Ordway, 1968 (Crustacea: Decapoda). Mar Biodivers 44(1):27–36. CrossRefGoogle Scholar
  7. Andrade LS, Antunes M, Lima PA, Furlan M, Frameschi IF, Fransozo A (2015) Reproductive features of the swimming crab Callinectes danae (Crustacea, Portunoidea) on the subtropical coast of Brazil: a sampling outside the estuary. Braz J Biol 75(3):692–702. CrossRefGoogle Scholar
  8. Andrade LS, Costa RC, Castilho AL, Frameschi IF, Sancinetti GS, Fransozo A (2017) Reproductive and population traits of the swimming crab Achelous spinimanus (Crustacea: Decapoda) in an upwelling region in southeastern Brazil. Nauplius 25:e2017004. CrossRefGoogle Scholar
  9. Bauer RT, Lin J (1994) Temporal patterns of reproduction and recruitment in populations of the penaeid shrimps Trachypenaeus similis (Smith) and T. constrictus (Stimpson) (Crustacea: Decapoda) from the northcentral Gulf of Mexico. J Exp Mar Biol Ecol 182(2):205–222. CrossRefGoogle Scholar
  10. Bauer RT, Rivera Vega LW (1992) Pattern of reproduction and recruitment in two sicyoniid shrimp species (Decapoda: Penaeoidea) from a tropical seagrass habitat. J Exp Mar Biol Ecol 161(2):223–240. CrossRefGoogle Scholar
  11. Bertini G, Fransozo A (2004) Bathymetric distribution of brachyuran crab (Crustacea, Decapoda) communities on coastal soft bottoms off southeastern Brazil. Mar Ecol Prog Ser 279:193–200. CrossRefGoogle Scholar
  12. 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. Invertebr Reprod Dev 54(1):7–17. CrossRefGoogle Scholar
  13. Braga AA, Fransozo A, Bertini G, Fumis PB (2005) Composition and abundance of the crabs (Decapoda, Brachyura) off Ubatuba and Caraguatatuba, northern coast of São Paulo, Brazil. Biota Neotropica 5(2):1–34. CrossRefGoogle Scholar
  14. Braga AA, Fransozo A, Bertini G, Fumis PB (2007) Bathymetric distribution and recruitment of the spider crab Libinia spinosa H. Milne Edwards 1834 in the Ubatuba and Caraguatatuba regions, northern coast of São Paulo, Brazil (Crustacea, Brachyura, Majoidea, Pisidae). Senckenberg Biol 87(1):7–16Google Scholar
  15. Branco JO, Lunardon-Branco MJ, Souto FX (2002) Estrutura populacional de Portunus spinimanus Latreille, 1819 (Crustacea, Portunidae) na Armação do Itapocoroy, Penha, Santa Catarina, Brasil. Rev Bras Zool 19(3):731–738. CrossRefGoogle Scholar
  16. Cobo VJ, Fransozo A (2000) Fecundity and reproduction period of the red mangrove crab Goniopsis cruentata (Brachyura, Grapsidae), São Paulo State, Brazil. In: Vaupel Von Klein JC, Schram FR (eds) The Biodiversity crisis and Crustacea, vol 12. Proceedings of the Fourth International Crustacean Congress. A. A. Balkema Publishers, Rotterdam, pp 527–533Google Scholar
  17. Cobo VJ, Fransozo A (2005) Physiological maturity and relationship of growth and reproduction in the red mangrove crab Goniopsis cruentata (Latreille) (Brachyura, Grapsidae) on the coast of São Paulo, Brazil. Rev Bras Zool 22(1):219–223. CrossRefGoogle Scholar
  18. Costa RC, Fransozo A (2004) Abundance and ecologic distribution of the shrimp Rimapenaeus constrictus (Crustacea: Penaeidae) on the northern coast of São Paulo State, Brazil. J Nat Hist 38(7):901–912. CrossRefGoogle Scholar
  19. Costa TM, Negreiros-Fransozo ML (1998) The reproductive cycle of Callinectes danae Smith 1869 (Decapoda, Portunidae) in Ubatuba region, Brazil. Crustaceana 71(6):615–627. CrossRefGoogle Scholar
  20. De-Carli BP, Severino-Rodrigues E, Rotundo MM, Musiello-Fernandes J, Ancona MC (2016) Fecundidade e morfometria de Achelous spinimanus (Latreille, 1819) (Brachyura, Portunidae) capturado no litoral do estado de São Paulo, Brasil. Bol Inst Pesca 40(4):487–495Google Scholar
  21. Fracasso HAA, Branco JO (2005) Population structure of Hepatus pudibundus (Herbst) in the Armação do Itapocoroy, Santa Catarina, Brazil. Rev Bras Zool 22(2):342–348. CrossRefGoogle Scholar
  22. Fransozo A, Sousa AN, Rodrigues GFB, Telles JN, Fransozo V, Negreiros-Fransozo ML (2016) Decapod crustaceans captured along with the sea-bob shrimp fisheries on nonconsolidated sublitoral from northern coast of São Paulo, Brazil. Bol Inst Pesca 42(2):369–386CrossRefGoogle Scholar
  23. Furtado VV, Mahiques MM (1990) Distribuição de sedimentos em regiões costeiras e plataforma continental de São Paulo. In: Simpósio Sobre Ecossistemas Da Costa Sul E Sudeste Brasileira: Estrutura, Função e Manejo. Águas de Lindóia, Anais. ACIESP, São Paulo, pp 20–29Google Scholar
  24. Gherardi F, Cassidy PM (1995) Life history patterns of Discorsopagurus schmitti, a hermit crab inhabiting Polychaeta tubes. Biol Bull 188(1):68–77. CrossRefGoogle Scholar
  25. Goodbody I (1965) Continuous breeding in populations of two tropical crustaceans, Mysidium columbiae (Zimmer) and Emerita portoricensis Schmidt. Ecology 46(1–2):195–197. CrossRefGoogle Scholar
  26. Hartnoll RG (1982) Growth. In: Abele LG (ed.). The biology of Crustacea: 2. Embryology, morphology and genetics. Academic Press, New York, pp 111–196Google Scholar
  27. Hartnoll RG (1985) Growth, sexual maturity and reproductive output. In: Wenner A (ed) Crustacean issues, vol 3, Factors in adult growth. A. A. Balkema, Boston, pp 101–128Google Scholar
  28. Hartnoll RG (2006) Reproductive investment in Brachyura. Hydrobiologia 557:31–40.
  29. Hartnoll RG, Gould P (1988) Brachyuran life history strategies and the optimization of egg production. Symp Zool Soc Lond 59:1–9Google Scholar
  30. Keunecke KA, D’Incao F, Fonseca DB (2007) Growth and mortality of Hepatus pudibundus (Herbst 1785) (Crustacea: Calappidae) in South-Western Brazil. J Mar Biol Assoc UK 87(4):885–891. CrossRefGoogle Scholar
  31. Klôh AS, Di Beneditto APM (2010) Estrutura populacional do siri-baú, Hepatus pudibundus (Herbst 1785) no Norte do Estado do Rio de Janeiro, Sudeste do Brasil. Biota Neotropica 10(3):463–467. Accessed 17 May 2018
  32. Lancaster I (1990) Reproduction and life history strategy of the hermit crab Pagurus bernhardus. J Mar Biol Assoc UK 70(1):129–142. CrossRefGoogle Scholar
  33. Lima PA, Bertini G, Fransozo V, Gregati RA, Corrêa Fernandes-Góes L, Castilho AL (2014a) Reproductive biology of Hepatus pudibundus (Crustacea: Brachyura), the most abundant crab on the southeastern Brazilian coast. Biologia 69(2):219–227. Google Scholar
  34. Lima PA, Andrade LS, Alencar CERD, Pereira RT, Teixeira GM, Fransozo A (2014b) Two species of swimming crabs of the genus Achelous (Crustacea, Brachyura): environmental requirements determining the niche. Hydrobiologia 727(1):197–207.
  35. Lopes RM, Katsuragawa M, Dias JF, Montú MA, Muelbert JH, Gorri C, Brandini PF (2006) Zooplankton and ichthyoplankton distribution on the southern Brazilian shelf: an overview. Sci Mar 70(2):189–202CrossRefGoogle Scholar
  36. Mahiques MM (1995) Dinâmica sedimentar atual nas enseadas da região de Ubatuba, Estado de São Paulo. Bol Inst Oceanogr 43(2):111–122CrossRefGoogle Scholar
  37. Mantelatto FLM (2000) Allocation of the portunid crab Callinectes ornatus (Decapoda: Brachyura) in the Ubatuba Bay, northern coast of São Paulo State, Brazil. In: Von Vaupel Klein JC, Schram FR (eds) The Biodiversity Crisis and Crustacea -Proceedings of the 4th International Crustacean Congress, Balkema, Rotterdam, Brookfield, The Netherlands. Crustacean Issues, pp 431–443Google Scholar
  38. Mantelatto FLM, Fransozo A (1996) Size at sexual maturity in Callinectes ornatus (Brachyura, Portunidae) from the Ubatuba Region (SP), Brazil. Nauplius 4:29–38Google Scholar
  39. Mantelatto FLM, Fransozo A (1999) Reproductive biology and moulting cycle of the crab Callinectes ornatus (Decapoda, Portunidae) from the Ubatuba region, São Paulo, Brazil. Crustaceana 72(1):63–75. CrossRefGoogle Scholar
  40. Mantelatto FLM, Fransozo A, Negreiros-Fransozo ML (1995) Population structure of Hepatus pudibundus (Herbst, 1785) (Decapoda, Brachyura, Calappidae) in Fortaleza Bay, Ubatuba (SP), Brazil. Rev Biol Trop 43(1):259–264Google Scholar
  41. Marochi MZ, Trevisan A, Gomes FB, Masunari S (2016) Dimorfismo sexual em Hepatus pudibundus (Crustacea, Decapoda, Brachyura). Iheringia 106:1–6. CrossRefGoogle Scholar
  42. Melo GAS (1996) Manual de Identificação dos Brachyura (caranguejos e siris) do Litoral Brasileiro. Plêiade /FAPESP, São Paulo, Brasil, pp 1–604Google Scholar
  43. Moura NFO, Coelho PA (2004) Physiological sexual maturity of Goniopsis cruentata (Latreille) (Crustacea, Brachyura, Grapsidae) in the Paripe Estuary, Pernambuco State, Brazil. Rev Bras Zool 21(4):1011–1015. CrossRefGoogle Scholar
  44. Odebrecht C, Castello JP (2001) The convergence ecosystem in the Southwest Atlantic. In: Seeliger U, Kjerfve B (eds) Coastal marine ecosystems of Latin America, ecological studies. Springer, Berlin, pp 147–165CrossRefGoogle Scholar
  45. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'hara RB, Simpson GL, Solymos P, Henry M, Stevens H, Wagner H (2013) Vegan: community ecology package. R package version 2, pp 0–7. Accessed 05 Mar 2018
  46. Orton JH (1920) Sea-temperature, breeding and distribution in marine animals. J Mar Biol Assoc UK 12(2):39–336. CrossRefGoogle Scholar
  47. Pinheiro MAA, Fransozo A (1998) Sexual maturity of the speckled swimming crab Arenaeus cribrarius (Lamarck, 1818) (Decapoda, Brachyura, Portunidae), in the Ubatuba littoral, São Paulo State, Brazil. Crustaceana 71(4):434–452. CrossRefGoogle Scholar
  48. Pinheiro MAA, Fransozo A (1999) Reproductive behaviour of the swimming crab Arenaeus cribarius (Lamarck, 1818) (Crustacea, Brachyura, Portunidae) in captivity. Bull Mar Sci 64(2):243–253Google Scholar
  49. Pinheiro MAA, Fransozo A (2002) Reproduction of the speckled swimming crab Arenaeus cribrarius (Brachyura: Portunidae) on the Brazilian coast. J Crustac Biol 22(2):416–428. CrossRefGoogle Scholar
  50. Pires AMS (1992) Structure and dynamics of benthic megafauna on the continental shelf offshore of Ubatuba, southeastern, Brazil. Mar Ecol Prog Ser 86:63–76CrossRefGoogle Scholar
  51. Pires-Vanin MAS, Matsuura Y (1993) Estrutura e função do ecossistema de plataforma continental da região de Ubatuba, Estado de São Paulo: uma introdução. Publ Esp Inst Oceanogr 10:1–8Google Scholar
  52. Pires-Vanin AMS, Rossi-Wongtschowski CLDB, Aidar E, Mesquita HDS, Soares LSH, Katsuragawa M, Matsuura Y (1993) Estrutura e função do ecossistema de plataforma continental do Atlântico Sul brasileiro: síntese dos resultados. Publ Esp Inst Oceanogr 10:217–231Google Scholar
  53. R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Accessed 05 Mar 2018
  54. Rakocinski CF, Lyczkowski-Shultz J, Richardson SL (1996) Ichthyoplankton assemblage structure in Mississippi sound as revealed by canonical correspondence analysis. Estuar Coast Shelf Sci 43(2):237–257. CrossRefGoogle Scholar
  55. Reigada ALD, Negreiros-Fransozo ML (1995) Fecundidade do caranguejo Hepatus pudibundus (Herbst, 1785) (Crustacea, Decapoda, Calapidae) em Ubatuba (SP), Brasil. Arch Biol Technol 38(2):661–668Google Scholar
  56. Reigada ALD, Negreiros-Fransozo ML (1999) Maturidade sexual em Hepatus pudibundus (Decapoda, Brachyura, Calappidae). Iheringia Ser Zool 86:159–164Google Scholar
  57. Reigada ALD, Negreiros-Fransozo ML (2000) Reproductive cycle of Hepatus pudibundus (Herbst, 1758) (Crustacea, Decapoda, Calappidae) in Ubatuba, SP, Brazil. Rev Bras Biol 60(3):483–491. CrossRefGoogle Scholar
  58. Rodrigues PJB, Graça Lopes SER, Coelho JAP (1985) Levantamento da família Portunidae (Crustacea, Decapoda, Brachyura) no complexo Baía-Estuário de Santos, São Paulo, Brasil. Bol Inst Pesca 12(3):153–162Google Scholar
  59. Santos S, Negreiros-Fransozo ML (1999) Reproductive cycle of the swimming crab Portunus spinimanus Latreille (Crustacea, Decapoda, Brachyura) from Ubatuba, Sao Paulo, Brazil. Rev Bras Zool 16(4):1183–1193. CrossRefGoogle Scholar
  60. Sardá FO, Machado IF, Prata PFS, Dumont LFC (2013) Population biology of the box crab Hepatus pudibundus (Crustacea: Aethridae) off the coast of Santa Catarina State Southern Brazil. Pan-Am J Aquat Sci 8(2):126–138Google Scholar
  61. Silva TE, Franzoso V, Taddei FG, Costa RC, Almeida AC, Fransozo A (2017) Reproductive analyses of the swimming crab Achelous spinicarpus (Stimpson, 1871) (Crustacea: Decapoda: Portunoidea) on the northern coast of São Paulo, Brazil. Bol Inst Oceanogr Venezuela 55(2):3–16Google Scholar
  62. Soares-Gomes A, Pires-Vanin AMS (2003) Padrões de abundância, riqueza e diversidade de moluscos bivalves na plataforma continental ao largo de Ubatuba, São Paulo, Brasil: uma comparação metodológica. Rev Bras Zool 20(4):717–725.
  63. Terossi M, Torati LS, Miranda I, Scelzo MA, Mantelatto FL (2010) Comparative reproductive biology of two southwestern Atlantic populations of the hermit crab Pagurus exilis (Crustacea: Anomura: Paguridae). Mar Ecol 31(4):584–591. CrossRefGoogle Scholar
  64. Vazzoler AEAM (1996) Biologia da reprodução de peixes teleósteos: teorias e práticas. Eduem, Maringá, pp 1–169Google Scholar
  65. Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall, New Jersey, pp 1–663Google Scholar

Copyright information

© Institute of Zoology, Slovak Academy of Sciences 2019

Authors and Affiliations

  • Veronica Pereira Bernardes
    • 1
    Email author
  • Francislene Karina Martins
    • 1
  • Gabriel Fellipe Barros Rodrigues
    • 1
  • Camila Hipolito Bernardo
    • 1
  • Aline Nonato de Sousa
    • 1
  • Giovana Bertini
    • 2
  • Adilson Fransozo
    • 1
  1. 1.Group of Studies on Biology, Ecology and Culture of Crustaceans (NEBECC), Department of Zoology, Biosciences InstituteUniversidade Estadual Paulista UNESPBotucatuBrazil
  2. 2.Laboratório de Biologia e Cultivo de Crustáceos- LABCRUSTUniversidade Estadual Paulista, UNESPRegistroBrazil

Personalised recommendations