Development of the male reproductive system in Callinectes ornatus Ordway, 1863 (Brachyura: Portunidae)

Nascimento, Fabiana Aparecida do; Zara, Fernando José

Abstract

This study describes the histology and histochemistry of the male reproductive system in Callinectes ornatus, comparing juvenile and adult developmental stages. We also analyzed changes in the gonadosomatic (GSI) and hepatosomatic (HSI) indices, and the weights of the testis and vas deferens during the development. The results showed that all stages, beginning with the juvenile (JUV), through developing (DEV) and mature (MAT) adult males of C. ornatus produce sperm and spermatophores. During development, testicular lobes showed the same characteristics of production and release of sperm into the seminiferous duct. The vas deferens showed little histological and histochemical change in the epithelium in juvenile and adult males. The differences consisted of the larger amount of secretion in MAT males compared to JUV and DEV ones. The chemical composition of the seminal fluid was similar, but MAT males produced a more homogeneous secretion. Morphological and physiological maturation are not synchronized in C. ornatus, since JUV males produced spermatophores similar to those in DEV and MAT males. However, these JUV are not yet able to reproduce, since they still have the abdomen attached to the cephalothoracic sternum. The increase of the GSI during development was significant for MAT males, and is related to the production of sufficient volume of seminal fluid to form the sperm "plug" in the female seminal receptacle. The HSI decreased from DEV to MAT adult stages, indicating that reserves from the hepatopancreas are used to develop the reproductive system after the pubertal molt.

Gonadosomatic index; histochemistry; seminal fluid; spermatogenesis; spermatop

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Adiyodi, R.G. and Adiyodi, K.G. 1972. Hepatopancreas of Paratelphusa hydrodromous (Herbst): Histophysiology and the pattern of proteins in relation to reproduction and molt. Biological Bulletin, 142: 359-369.
Batoy, C.B.; Sarmago, J.F. and Pilapil, B.C. 1989. Breeding season, sexual maturity and fecundity of the blue crab Portunus pelagicus (L.) in selected coastal waters in Leyte and vicinity, Philippines. Annals of Tropical Research, 9: 157-177.
Bauer, R.T. and Min, L.J. 1993. Spermatophores and plug substance of the marine shrimp Trachypenaeus similis (Crustacea: Decapoda: Penaeidae): Formation in the male reproductive tract and disposition in the inseminated female. Biological Bulletin, 185: 174-185.
Benhalima, K. and Moriyasu, M. 2000. Structure and function of the posterior vas deferens of the snow crab, Chionoecetes opilio (Brachyura, Majidae). Invertebrate Reproduction and Development, 37: 1-23.
Beninger, P.G.; Elner, R.W.; Foyle, T.P. and Odense, P.H. 1988. Functional anatomy of the male reproductive system and the female spermathecae in the snow crab Chionoecetes opilio (O. Fabricius) (Decapoda: Majidae) and a hypothesis for fertilization. Journal of Crustacean Biology, 8: 322-332.
Branco, J.O. and Lunardon-Branco, M.J. 1993a. Aspectos da biologia de Callinectes ornatus Ordway, 1863 (Decapoda – Portunidae) da região de Matinhos, Paraná, Brasil. Arquivos de Biologia e Tecnologia, 36: 489-496.
Branco, J.O. and Lunardon-Branco, M.J. 1993b. Crescimento e tamanho de primeira maturação em Callinectes ornatus Ordway, 1863 (Decapoda – Portunidae) da região de Matinhos, Paraná, Brasil. Arquivos de Biologia e Tecnologia, 36: 497-503.
Castiglioni, D.S.; Oliveira, G.T. and Bond-Buckup, G. 2006. Dinâmica do desenvolvimento das gônadas de Parastacus varicosus (Crustacea, Decapoda, Parastacidae). Ilheringia, Série Zoologia, 96: 413-417.
Castilho, G.G.; Ostrensky, A.; Pie, M.R. and Boeger, W.A. 2008. Morphohistology of the male reproductive system of the mangrove land crab Ucides cordatus (L.) (Crustacea, Brachyura, Ocypodidae). Acta Zoologica, 89: 157-161.
Chu, K.H. 1999. Morphometric analysis and reproductive biology of the crab Charybdis affinis (Decapoda, Brachyura, Portunidae) from the Zhujiang Estuary, China. Crustaceana, 72: 647-658.
Costa, T.M. and Negreiros-Fransozo, M.L. 1998. The reproductive cycle of Callinectes danae Smith, 1869 (Decapoda, Portunidae) in the Ubatuba region, Brazil. Crustaceana, 71: 615-627.
Cronin, L.E. 1947. Anatomy and histology of the male reproductive system of Callinectes sapidus Rathbun. Journal of Morphology, 81: 209-239.
Diesel, R. 1989. Structure and function of the reproductive system of the symbiotic spider crab Inachus phalangium (Decapoda: Majidae): Observations on sperm transfer, sperm storage and spawning. Journal of Crustacean Biology, 9: 266-277.
Diesel, R. 1990. Sperm competition and reproductive success in the decapod Inachus phalangium (Majidae): A male ghost spider crab that seals off rivals' sperm. Journal of Zoology, 220: 213-223.
Erkan, M.; Tunali, Y.; Balkis, H. and Oliveria, E. 2009. Morphology of testis and vas deferens in the Xanthoid crab, Eriphia verrucosa (Forskål, 1775) (Decapoda: Brachyura). Journal of Crustacean Biology, 29: 458-465.
Fasten, N. 1918. Spermatogenesis of the Pacific Coast Edible Crab, Cancer magister Dana. Biological Bulletin, 34: 277-306.
Garcia, T.M. and Silva, J.R.F. 2006. Testis and vas deferens morphology of the red-clawed mangrove tree crab (Goniopsis cruentata) (Latreille, 1803). Brazilian Archives of Biology and Technology, 49: 339-345.
Hartnoll, R. G. 1969. Mating in Brachyura. Crustaceana, 16: 161-181.
Hinsch, G.W. and McKnight, C.E. 1988. The vas deferens of the Spanish lobster, Scyllarus chacei International Journal of Invertebrate Reproduction and Development, 13: 267-280.
Hinsch, G.W. and Walker, M.H. 1974. The vas deferens of the spider crab, Libinia emarginata. Journal of Morphology, 143: 1-20.
Jivoff, P. 1997. The relative roles of predation and sperm competition on the duration of the post-copulatory association between the sexes in the blue crab, Callinectes sapidus. Behavioral Ecology and Sociobiology, 40: 175-185.
Jivoff, P.; Hines, A.H. and Quackenbush, L.C. 2007. Reproductive Biology and Embryonic Development. p. 255-286. In: L.E. Cronin and V.S. Kennedy (eds), The Blue Crab Callinectes sapidus. Maryland Sea Grant College.
Johnson, P.T. 1980. Histology of the Blue Crab (Callinectes sapidus): A Model for the Decapoda. New York, Praeger Scientific, p. 440.
Junqueira, L.C.U. and Junqueira, L.M.M.S. 1983. Técnicas Básicas de Citologia e Histologia. Santos, São Paulo, p. 123.
Krol, R.M.; Hawkins, W.E. and Overstreet, R.M. 1992. Reproductive components, p. 295-343. In: F.W. Harrison and A.G. Humes (eds), Microscopic Anatomy of Invertebrates. Decapoda, Crustacea, Vol. 10. New York, Wiley-Liss Inc.
Kyomo, J. 1988. Analysis of the relationship between gonads and hepatopancreas in males and females of the crab Sesarma intermedia, with reference to resource use and reproduction. Marine Biology, 97: 87-93.
Lawrence, A.L. and Castille, F.L. 1989. Relationship between maturation and biochemical composition of the gonads and digestive glands of the shrimps Penaeus aztecus Ives and Penaeus setiferus (L.). Journal of Crustacean Biology, 9: 202-211.
López-Greco, L. S. and E. M. Rodríguez. 1999. Annual reproduction and growth of adult crabs Chasmagnathus granulata (Crustacea, Brachyura, Grapsidae). Cahiers Biologie Marine, 40: 155-164.
López-Greco, L.S.; López, G.C. and Rodríguez, E.M. 1999. Morphology of spermathecae in the estuarine crab Chasmagnathus granulata Dana, 1851 (Graspidae, Sesarminae). Journal of Zoology, 249: 490-493.
Mantelatto, F.L. 1995. Biologia Reprodutiva de Callinectes ornatus Ordway, 1863 (Decapoda, Brachyura, Portunidae) na região de Ubatuba (SP), Brasil. Universidade Estadual Paulista – UNESP, Botucatu, Brazil, Ph.D. Thesis.
Mantelatto, F.L. and Fransozo, A. 1996. Size at sexual maturity in Callinectes ornatus (Brachyura – Portunidae) from the Ubatuba region (SP), Brazil. Nauplius, 4: 29-38.
Mantelatto, F.L. and Fransozo, A. 1997. Fecundity of the crab Callinectes ornatus Ordway, 1863 (Decapoda, Brachyura, Portunidae) from the Ubatuba region, São Paulo, Brazil. Crustaceana, 70: 214-226.
Mantelatto, F.L. and Fransozo, A. 1999. Reproductive biology and moulting cycle of the crab Callinectes ornatus Ordway, 1863 (Decapoda – Brachyura – Portunidae) from the Ubatuba region, São Paulo, Brazil. Crustaceana, 72: 63-76.
Mello, M.L.S and Vidal, B.C. 1980. Práticas de Biologia Celular. São Paulo, ed. Edgar Blucher – FUNCAMP.
Moriyasu, M. and Benhalima, K. 1998. Snow crabs, Chionecetes opilio (O. Fabricius, 1978) (Crustacea: Majidae) have two types of spermatophore: hypotheses on the mechanism of fertilization and population reproductive dynamics in the southern Gulf of St. Lawrence, Canada. Journal of Natural History, 32: 1651-1665.
Moriyasu, M.; Benhalima, K.; Duggan, D.; Lawton, P. and Robichaud, D. 2002. Reproductive biology of male Jonah crab, Cancer borealis Stimpson, 1859 (Decapoda, Cancridae) on the Scotian Shelf, northwestern Atlantic. Crustaceana, 75: 891-913.
Negreiros-Fransozo, M.L.; Mantelatto, F.L. and Fransozo, A. 1999. Population biology of Callinectes ornatus Ordway, 1863 (Decapoda, Portunidae) from Ubatuba (SP), Brazil. Scientia Marina, 63: 157-163.
Ng, P.K.L.; Guinót, D. and Davie, P.J.F. 2008. Systema Brachyurorum: Part I. An Annotated Checklist of Extant Brachyuran Crabs of the World. The Raffles Bulletin of Zoology, 17: 1-286.
Pearse, A.G.E. 1985. Histochemistry: Theorical and applied, Vol. 2. Edinburgh, Churchill Livingstone, p. 998.
Pinheiro, M.A.A. and 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: 434-452.
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Publication Dates

Publication in this collection
27 Jan 2015
Date of issue
Dec 2013

History

Received
26 Sept 2013
Accepted
06 Dec 2013

This work is licensed under a Creative Commons Attribution 4.0 International License.

[1] Adiyodi, R.G. 1969. On the storage and mobilization of organic resources in the hepatopancreas of a crab (Paratelphusa hydrodromus). Experientia, 25: 43-44.

[2] Adiyodi, R.G. and Adiyodi, K.G. 1972. Hepatopancreas of Paratelphusa hydrodromous (Herbst): Histophysiology and the pattern of proteins in relation to reproduction and molt. Biological Bulletin, 142: 359-369.

[3] Batoy, C.B.; Sarmago, J.F. and Pilapil, B.C. 1989. Breeding season, sexual maturity and fecundity of the blue crab Portunus pelagicus (L.) in selected coastal waters in Leyte and vicinity, Philippines. Annals of Tropical Research, 9: 157-177.

[4] Bauer, R.T. and Min, L.J. 1993. Spermatophores and plug substance of the marine shrimp Trachypenaeus similis (Crustacea: Decapoda: Penaeidae): Formation in the male reproductive tract and disposition in the inseminated female. Biological Bulletin, 185: 174-185.

[5] Benhalima, K. and Moriyasu, M. 2000. Structure and function of the posterior vas deferens of the snow crab, Chionoecetes opilio (Brachyura, Majidae). Invertebrate Reproduction and Development, 37: 1-23.

[6] Beninger, P.G.; Elner, R.W.; Foyle, T.P. and Odense, P.H. 1988. Functional anatomy of the male reproductive system and the female spermathecae in the snow crab Chionoecetes opilio (O. Fabricius) (Decapoda: Majidae) and a hypothesis for fertilization. Journal of Crustacean Biology, 8: 322-332.

[7] Branco, J.O. and Lunardon-Branco, M.J. 1993a. Aspectos da biologia de Callinectes ornatus Ordway, 1863 (Decapoda – Portunidae) da região de Matinhos, Paraná, Brasil. Arquivos de Biologia e Tecnologia, 36: 489-496.

[8] Branco, J.O. and Lunardon-Branco, M.J. 1993b. Crescimento e tamanho de primeira maturação em Callinectes ornatus Ordway, 1863 (Decapoda – Portunidae) da região de Matinhos, Paraná, Brasil. Arquivos de Biologia e Tecnologia, 36: 497-503.

[9] Castiglioni, D.S.; Oliveira, G.T. and Bond-Buckup, G. 2006. Dinâmica do desenvolvimento das gônadas de Parastacus varicosus (Crustacea, Decapoda, Parastacidae). Ilheringia, Série Zoologia, 96: 413-417.

[10] Castilho, G.G.; Ostrensky, A.; Pie, M.R. and Boeger, W.A. 2008. Morphohistology of the male reproductive system of the mangrove land crab Ucides cordatus (L.) (Crustacea, Brachyura, Ocypodidae). Acta Zoologica, 89: 157-161.

[11] Chu, K.H. 1999. Morphometric analysis and reproductive biology of the crab Charybdis affinis (Decapoda, Brachyura, Portunidae) from the Zhujiang Estuary, China. Crustaceana, 72: 647-658.

[12] Costa, T.M. and Negreiros-Fransozo, M.L. 1998. The reproductive cycle of Callinectes danae Smith, 1869 (Decapoda, Portunidae) in the Ubatuba region, Brazil. Crustaceana, 71: 615-627.

[13] Cronin, L.E. 1947. Anatomy and histology of the male reproductive system of Callinectes sapidus Rathbun. Journal of Morphology, 81: 209-239.

[14] Diesel, R. 1989. Structure and function of the reproductive system of the symbiotic spider crab Inachus phalangium (Decapoda: Majidae): Observations on sperm transfer, sperm storage and spawning. Journal of Crustacean Biology, 9: 266-277.

[15] Diesel, R. 1990. Sperm competition and reproductive success in the decapod Inachus phalangium (Majidae): A male ghost spider crab that seals off rivals' sperm. Journal of Zoology, 220: 213-223.

[16] Erkan, M.; Tunali, Y.; Balkis, H. and Oliveria, E. 2009. Morphology of testis and vas deferens in the Xanthoid crab, Eriphia verrucosa (Forskål, 1775) (Decapoda: Brachyura). Journal of Crustacean Biology, 29: 458-465.

[17] Fasten, N. 1918. Spermatogenesis of the Pacific Coast Edible Crab, Cancer magister Dana. Biological Bulletin, 34: 277-306.

[18] Garcia, T.M. and Silva, J.R.F. 2006. Testis and vas deferens morphology of the red-clawed mangrove tree crab (Goniopsis cruentata) (Latreille, 1803). Brazilian Archives of Biology and Technology, 49: 339-345.

[19] Hartnoll, R. G. 1969. Mating in Brachyura. Crustaceana, 16: 161-181.

[20] Hinsch, G.W. and McKnight, C.E. 1988. The vas deferens of the Spanish lobster, Scyllarus chacei International Journal of Invertebrate Reproduction and Development, 13: 267-280.

[21] Hinsch, G.W. and Walker, M.H. 1974. The vas deferens of the spider crab, Libinia emarginata. Journal of Morphology, 143: 1-20.

[22] Jivoff, P. 1997. The relative roles of predation and sperm competition on the duration of the post-copulatory association between the sexes in the blue crab, Callinectes sapidus. Behavioral Ecology and Sociobiology, 40: 175-185.

[23] Jivoff, P.; Hines, A.H. and Quackenbush, L.C. 2007. Reproductive Biology and Embryonic Development. p. 255-286. In: L.E. Cronin and V.S. Kennedy (eds), The Blue Crab Callinectes sapidus. Maryland Sea Grant College.

[24] Johnson, P.T. 1980. Histology of the Blue Crab (Callinectes sapidus): A Model for the Decapoda. New York, Praeger Scientific, p. 440.

[25] Junqueira, L.C.U. and Junqueira, L.M.M.S. 1983. Técnicas Básicas de Citologia e Histologia. Santos, São Paulo, p. 123.

[26] Krol, R.M.; Hawkins, W.E. and Overstreet, R.M. 1992. Reproductive components, p. 295-343. In: F.W. Harrison and A.G. Humes (eds), Microscopic Anatomy of Invertebrates. Decapoda, Crustacea, Vol. 10. New York, Wiley-Liss Inc.

[27] Kyomo, J. 1988. Analysis of the relationship between gonads and hepatopancreas in males and females of the crab Sesarma intermedia, with reference to resource use and reproduction. Marine Biology, 97: 87-93.

[28] Lawrence, A.L. and Castille, F.L. 1989. Relationship between maturation and biochemical composition of the gonads and digestive glands of the shrimps Penaeus aztecus Ives and Penaeus setiferus (L.). Journal of Crustacean Biology, 9: 202-211.

[29] López-Greco, L. S. and E. M. Rodríguez. 1999. Annual reproduction and growth of adult crabs Chasmagnathus granulata (Crustacea, Brachyura, Grapsidae). Cahiers Biologie Marine, 40: 155-164.

[30] López-Greco, L.S.; López, G.C. and Rodríguez, E.M. 1999. Morphology of spermathecae in the estuarine crab Chasmagnathus granulata Dana, 1851 (Graspidae, Sesarminae). Journal of Zoology, 249: 490-493.

[31] Mantelatto, F.L. 1995. Biologia Reprodutiva de Callinectes ornatus Ordway, 1863 (Decapoda, Brachyura, Portunidae) na região de Ubatuba (SP), Brasil. Universidade Estadual Paulista – UNESP, Botucatu, Brazil, Ph.D. Thesis.

[32] Mantelatto, F.L. and Fransozo, A. 1996. Size at sexual maturity in Callinectes ornatus (Brachyura – Portunidae) from the Ubatuba region (SP), Brazil. Nauplius, 4: 29-38.

[33] Mantelatto, F.L. and Fransozo, A. 1997. Fecundity of the crab Callinectes ornatus Ordway, 1863 (Decapoda, Brachyura, Portunidae) from the Ubatuba region, São Paulo, Brazil. Crustaceana, 70: 214-226.

[34] Mantelatto, F.L. and Fransozo, A. 1999. Reproductive biology and moulting cycle of the crab Callinectes ornatus Ordway, 1863 (Decapoda – Brachyura – Portunidae) from the Ubatuba region, São Paulo, Brazil. Crustaceana, 72: 63-76.

[35] Mello, M.L.S and Vidal, B.C. 1980. Práticas de Biologia Celular. São Paulo, ed. Edgar Blucher – FUNCAMP.

[36] Moriyasu, M. and Benhalima, K. 1998. Snow crabs, Chionecetes opilio (O. Fabricius, 1978) (Crustacea: Majidae) have two types of spermatophore: hypotheses on the mechanism of fertilization and population reproductive dynamics in the southern Gulf of St. Lawrence, Canada. Journal of Natural History, 32: 1651-1665.

[37] Moriyasu, M.; Benhalima, K.; Duggan, D.; Lawton, P. and Robichaud, D. 2002. Reproductive biology of male Jonah crab, Cancer borealis Stimpson, 1859 (Decapoda, Cancridae) on the Scotian Shelf, northwestern Atlantic. Crustaceana, 75: 891-913.

[38] Negreiros-Fransozo, M.L.; Mantelatto, F.L. and Fransozo, A. 1999. Population biology of Callinectes ornatus Ordway, 1863 (Decapoda, Portunidae) from Ubatuba (SP), Brazil. Scientia Marina, 63: 157-163.

[39] Ng, P.K.L.; Guinót, D. and Davie, P.J.F. 2008. Systema Brachyurorum: Part I. An Annotated Checklist of Extant Brachyuran Crabs of the World. The Raffles Bulletin of Zoology, 17: 1-286.

[40] Pearse, A.G.E. 1985. Histochemistry: Theorical and applied, Vol. 2. Edinburgh, Churchill Livingstone, p. 998.

[41] Pinheiro, M.A.A. and 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: 434-452.

[42] Pochon-Masson, J. 1983. Arthropoda – Crustacea. In: R.G. Adiyodi and K.G. Adiyodi (eds), Reproductive Biology of Invertebrates: Spermatogenesis and Sperm Function, Vol. 2. Vatsyayana Centre of Invertebrate Reproduction, Calicut University, India.

[43] Ravi, R.; Manisseri, M.K. and Sanil, N.K. 2012. Structure of the male reproductive system of the blue swimmer crab Portunus pelagicus (Decapoda: Portunidae). Acta Zoologica (Stockholm). doi: 10.1111/azo.12017.

[44] Ryan, E.P. 1967. Structure and function of the reproductive system of the crab Portunus sanguinolentus Herbst (Brachyura: Portunidae). Part I. The male system. Proceedings of the Symposium on Crustacea at Erkulan, India, 1965. Part II. Symposium, Series 2, p. 522-544.

[45] Sainte-Marie, G. and Sainte-Marie, B. 1999. Reproductive products in the adult snow crab (Chionoecetes opilio). II. Multiple types of sperm cells and of spermatophores in the spermathecae of mated females. Canadian Journal of Zoology, 77(3): 451-462.

[46] Sal Moyano, M.P.; Gavio, M.A. and Cuartas, E.I. 2009. Morphology and function of the reproductive tract of the spider crab Libinia spinosa (Crustacea, Brachyura, Majoidea): Pattern of sperm storage. Helgoland Marine Research, 64: 213-221.

[47] Sant'Anna, B.S.; Turra, A. and Zara, F.J. 2010. Simultaneous activity of male and female gonads in intersex hermit crabs. Aquatic Biology, 10: 201-209.

[48] Santos, C.M.; Lima, G.V.; Nascimento, A.A.; Sales, A. and Oshiro, L.M.Y. 2009. Histological and histochemical analysis of the gonadal development of males and females of Armases rubripes (Rathbun, 1897) (Crustacea, Brachyura, Sesarmidae). Brazilian Journal of Biology, 69: 161-169.

[49] Santos, S. and Negreiros-Fransozo, M.L. 1999. Reproductive cycle of the swimming crab Portunus spinimanus Latreille (Crustacea, Decapoda, Brachyura) from Ubatuba, Sao Paulo, Brazil. Revista Brasileira de Zoologia, 16: 1183-1193.

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Development of the male reproductive system in Callinectes ornatus Ordway, 1863 (Brachyura: Portunidae)

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