Artículo

Garcia Bento, M.A.; López Greco, L.S.; Zara, F.J."Seminal fluid production and sperm packaging in dromiid crabs (Brachyura, Podotremata)" (2019) Zoology. 132:17-30
Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Reproductive anatomy, including sperm storage structures and sperm transfer, is an important feature used to analyze phylogenetic relationships among taxa. We describe the male reproductive anatomy, seminal fluid production and packaging of spermatozoa in the vas deferens of primitive crabs. In all species of Dromiidae, the testes were tubular type and the vas deferens is a tube with a simple epithelium. The spermatozoa are in a central mass immersed in type I secretion, forming a large spermatic cord. In Moreiradromia antillensis and Dromia erythropus the spermatic cord is surrounded by a more complex secretion layer composed by protein granules and polysaccharides that seem to be responsible to form the sperm plaque which was absent in Hypoconcha. The sperm plaque was found in all Dromiinae species, which may result from the mating and probably act as a barrier to subsequent copulations. These patterns of elongated coenospermic spermatophore found here are unique and different from the spermatophores of all true crabs and may be considered a plesiomorphic state to spermatophoric structure in Brachyura. Our results show a novel type of spermatozoa packaging and new insights into how sperm might be transferred in Podotremata. © 2018 Elsevier GmbH

Registro:

Documento: Artículo
Título:Seminal fluid production and sperm packaging in dromiid crabs (Brachyura, Podotremata)
Autor:Garcia Bento, M.A.; López Greco, L.S.; Zara, F.J.
Filiación:Universidade Estadual Paulista (UNESP), FCAV, Laboratório de Morfologia de Invertebrados (IML), Departamento de Biologia Aplicada à Agropecuária e Centro de Aquicultura da Unesp (CAUNESP), Via de Acesso Prof. Paulo Donato Castellane, s/n, Jaboticabal, São Paulo 14884-900, Brazil
Universidad de Buenos Aires, CONICET, Instituto de Biodiversidad y Biología Experimental y Aplicada (IBBEA), Facultad de Ciencias Exactas y Naturales, Departamento de Biodiversidad y Biología Experimental, Laboratorio de Biología de la Reproducción y el Crecimiento de Crustáceos Decápodos, Buenos Aires, C1428EGA, Argentina
Universidade Estadual Paulista (UNESP), IB, Avenida 24 A, 1515, Rio Claro, São Paulo 13506-900, Brazil
Palabras clave:anatomy; Hypoconcha; male reproductive system; spermatheca; ultrastructure; animal; Brachyura; male; physiology; sperm; spermatozoon; Animals; Brachyura; Male; Semen; Spermatozoa
Año:2019
Volumen:132
Página de inicio:17
Página de fin:30
DOI: http://dx.doi.org/10.1016/j.zool.2018.09.001
Handle:http://hdl.handle.net/20.500.12110/paper_09442006_v132_n_p17_GarciaBento
Título revista:Zoology
Título revista abreviado:Zoology
ISSN:09442006
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_09442006_v132_n_p17_GarciaBento

Referencias:

  • Ahyong, T.S., Lai, J.C.Y., Sharkey, D., Colgan, D.J., Ng, P.K.L., Phylogenetics of the brachyuran crabs (Crustacea: Decapoda): The status of Podotremata based on small subunit nuclear ribosomal RNA (2007) Mol. Phylogenetics Evol, 45, pp. 576-586
  • Aiken, D.E., Waddy, S.L., Mercer, S.M., Confirmation of external fertilization in the American lobster, Homarus americanus (2004) J. Crustacean Biol., 24, pp. 474-480
  • Amadio, L.M., Mantelatto, F.L., Description of the male reproductive system of the hermit crab Calcinus tibicen (Decapoda: Anomura: Diogenidae) (2009) J. Crustacean Biol., 29, pp. 466-475
  • Anilkumar, G., Sudha, K., Subramoniam, T., Spermatophore transfer and sperm structure in the brachyuran crab Metopograpsus messor (Decapoda: Grapsidae) (1999) J. Crustacean Biol., 19, pp. 361-370
  • Bauer, R.T., Phylogenetic trends in sperm transfer and storage complexity in decapod crustaceans (1986) J. Crustacean Biol., 6, pp. 313-325
  • Bauer, R.T., Remarkable Shrimps Adaptations and Natural History of the Carideans (2004), Columbia University of Oklahoma press. Normam. Marine Resources Library; Martin, J.W., Crustacean Sexual Biology (1990), Columbia University Press New York; Bauer, R.T., Min, L.J., 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 (1993) Biol. Bull., 185, pp. 174-185
  • Becker, C., Scholtz, G., Phylogenetic implications of sperm storage in Podotremata: Histology and 3D‐reconstructions of spermathecae and gonopores in female carrier crabs (Decapoda: Brachyura: Homoloidea) (2017) J. Morphol, 278, pp. 89-105
  • Benhalima, K., Moriyasu, M., Structure and function of the posterior vas deferens of the snow crab, Chionoecetes opilio (Brachyura, Majidae) (2000) Invertebr. Reprod. Dev., 37, pp. 11-23
  • Beninger, P.G., Elner, R.W., Foyle, T.P., Odense, P., Functional anatomy of the male reproductive system and the female spermatheca in the snow crab Chionoecetes opilio (O. Fabricius) (Decapoda: Majidae) and a hypothesis for fertilization (1988) J. Crustacean Biol., 8, pp. 322-332
  • Buranelli, R.C., Zara, F.J., Mantelatto, F.L., Male reproductive system of the red brocade hermit crab Dardanus insignis (Diogenidae) and its relationship to other family members (2014) Zoomorphology, 133, pp. 127-137
  • Castilho, G.G., Ostrensky, A., Pie, M.R., Boeger, W.A., Morphology and histology of the male reproductive system of the mangrove land crab Ucides cordatus (L.) (Crustacea, Brachyura, Ocypodidae) (2008) Acta Zool., 89, pp. 157-161
  • Chow, S., Dougherty, M.M., Dougherty, W.J., Sandifer, P.A., Spermatophore formation in the white shrimps Penaeus setiferus and P. vannamei (1991) J. Crustacean Biol., 11, pp. 201-216
  • Dudenhausen, E.E., Talbot, P., An ultrastructural comparison of soft and hardened spermatophores from the crayfish Pacifastacus leniusculus Dana (1983) Can. J. Zool., 61, pp. 182-194
  • El-Sherief, S.S., Fine structure of the sperm and spermatophores of Portunus pelagicus (L.) (Decapoda, Brachyura) (1991) Crustaceana, 61, pp. 271-279
  • Erkan, M., Tunali, Y., Balkis, H., Oliveria, E., Morphology of testis and vas deferens in the xanthoid crab, Eriphia verrucosa (Forskål, 1775) (Decapoda: Brachyura) (2009) J. Crustacean Biol., 29, pp. 458-465
  • Fantucci, M.Z., Mantelatto, F.L., Male reproductive apparatus and spermatophore morphology of the hermit crabs Pagurus brevidactylus and P. criniticornis (Anomura, Paguridae) (2011) J Morphol, 272, pp. 1271-1280
  • Garcia, T.M., Silva, J.R.F., Testis and vas deferens morphology of the red-clawed mangrove tree crab (Goniopsis cruentata) (Latreille, 1803) (2006) Braz. Arch. Biol. Technol., 49, pp. 339-345
  • Guinot, D., Quenette, G., The spermatheca in podotreme crabs (Crustacea, Decapoda, Brachyura, Podotremata) and its phylogenetic implication (2005) Zoosystema, 27, pp. 267-342
  • Guinot, D., Tavares, M., A new subfamilial arrangement for the Dromiidae de Haan, 1833, with diagnoses and descriptions of new genera and species (2003) Zoosystema, 25, pp. 43-129
  • Guinot, D., Jamieson, B.G.M., Tudge, C.C., Ultrastructure and relationships of spermatozoa of the freshwater crabs Potamon fluviatile and Potamon ibericum (Crustacea, Brachyura, Potamidae) (1997) J. Zool., 241, pp. 229-244
  • Guinot, D., Tavares, M., Castro, P., Significance of the sexual openings and supplementary structures on the phylogeny of brachyuran crabs (Crustacea, Decapoda, Brachyura), with new nomina for higher-ranked podotreme taxa (2013) Zootaxa, 3665, pp. 1-414
  • Hartnoll, R.G., The freshwater grapsid crabs of Jamaica (1964) Proc. Linn. Soc. Lond., 175, p. 145
  • Hartnoll, R.G., Mating in the Brachyura (1969) Crustaceana, 16, pp. 161-181
  • Hartnoll, R.G., Copulatory structure and function in the Dromiacea, and their bearing on the evolution of the Brachyura (1975) Pubbl. Staz. Zool. Napoli., 39, pp. 657-676
  • Hayer, S., Köhnk, S., Boretius, S., Brandis, D., Ever more complex: a new type of organization of reproductive organs in female Dorippe sinica Chen, 1980 (Decapoda: Brachyura: Dorippidae) (2016) Zoology, 119, pp. 455-463
  • Hinsch, G.W., Ultrastructure of the sperm and spermatophores of the anomuran crab Pleuroncodes planipes (1991) J. Crustacean Biol., 11, pp. 17-22
  • Hinsch, G.W., Walker, M.H., The vas deferens of the spider crab, Libinia emarginata (1974) J. Morphol., 143, pp. 1-19
  • Hobbs, H.H., Jr, Harvey, M.C., Hobbs, H.H., III, A Comparative Study of Functional Morphology of the Male Reproductive Systems in the Astacidea with Emphasis on the Freshwater Crayfishes (Crustacea: Decapoda) (2007), Smithsonian Institution Scholarly Press Washington, D. C; Johnson, P.T., Histology of the Blue Crab, Callinectes sapidus: A Model for the Decapoda (1980), Praeger New York; Junqueira, L.C.U., Junqueira, L.M.M.S., Técnicas Básicas de Citologia e Histologia (1983), 1. ed. Instituto de Ciências Biomédicas e Faculdade de Medicina, Universidade de São Paulo Editora Santos 123 p; Klaus, S., Brandis, D., Evolution of sperm morphology in potamid freshwater crabs (Crustacea: Brachyura: Potamoidea) (2011) Zool. J. Linn. Soc., 161, pp. 53-63
  • Klaus, S., Schubart, C.D., Brandis, D., Ultrastructure of spermatozoa and spermatophores of old world freshwater crabs (Brachyura: Potamoidea: Gecarcinucidae, Potamidae, and Potamonautidae) (2009) J. Morphol., 270, pp. 175-193
  • Kooda-Cisco, M.J., Talbot, P., A structural analysis of the freshly extruded spermatophore from the lobster, Homarus americanus (1982) J. Morphol., 172, pp. 193-207
  • Kooda-Cisco, M., Talbot, P., Ultrastructure and role of the lobster vas deferens in spermatophore formation: the proximal segment (1986) J. Morphol., 188, pp. 91-103
  • Krol, R.M., Hawkins, W.E., Overstreet, R.M., Reproductive components (1992) Microscopic Anatomy of Invertebrates. v. 10: Decapod Crustacea, pp. 295-343. , F.W. Harrison A.G. Humes Wiley-Liss Inc. New York
  • López Greco, L.S., Functional anatomy of the reproductive system (2013) Functional Morphology and Diversity, pp. 413-450. , Les Watling Martin Thiel Oxford University Press New York
  • López Greco, L.S., Vazquez, F., Rodríguez, E.M., Morphology of the male reproductive system and spermatophore formation in the freshwater ‘red claw'crayfish Cherax quadricarinatus (Von Martens, 1898) (Decapoda, Parastacidae) (2007) Acta Zool., 88, pp. 223-229
  • Mantelatto, F.L., Scelzo, M.A., Tudge, C.C., Morphological and morphometric appraisal of the spermatophore of the southern hermit crab Isocheles sawayai Forest and Saint Laurent, 1968 (Anomura: Diogenidae), with comments on gonopores of both sexes (2009) Zool. Anz., 248, pp. 1-8
  • McLay, C.L., The Dromiidae of French Polynesia and a new collection of crabs (Crustacea, Decapoda, Brachyura) from the Marquesas Islands (2001) Zoosystema-Paris-, 23, pp. 77-100
  • McLay, C.L., Becker, C., Reproduction in Brachyura (2015) Treatise on Zoology-Anatomy, Taxonomy, Biology. The Crustacea, 9, pp. 185-243. , Brill
  • McLay, C.L., López Greco, L.S., A hypothesis about the origin of sperm storage in the Eubrachyura, the effects of seminal receptacle structure on mating strategies and the evolution of crab diversity: how did a race to be first become a race to be last? (2011) Zool. Anz.-A Journal of Comparative Zoology, 4, pp. 378-406
  • Mello, M.S.L., Vidal, B.C., Práticas de Biologia Celular (1980), Edgar Blucher – FUNCAMP São Paulo; Minagawa, M., Gonopods of the red frog crab Ranina ranina Linnaeus (Decapoda: Raninidae) (1993) Crust. Res., 22, pp. 45-54
  • Minagawa, M., Chiu, J.R., Kudo, M., Takashima, F., Male reproductive biology of the red frog crab, Ranina ranina, off Hachijojima, Izu Islands, Japan (1994) Mar. Biol., 118, pp. 393-401
  • Montanaro, J., Gruber, D., Leisch, N., Improved ultrastructure of marine invertebrates using non-toxic buffers (2016) PeerJ, 4, p. e1860
  • Nagao, J., Munehara, H., Annual cycle of testicular maturation in the helmet crab Telmessus cheiragonus (2003) Fish. Sci., 69, pp. 1200-1208
  • Nascimento, F.A.D., Zara, F.J., Development of the male reproductive system in Callinectes ornatus Ordway, 1863 (Brachyura: Portunidae) (2013) Nauplius, 21, pp. 161-177
  • Nicolau, C.F., Nascimento, A.A., Machado-Santos, C., Sales, A., Oshiro, L.M.Y., Gonads of males and females of the mangrove tree crab Aratus pisonii (Grapsidae: Brachyura: Decapoda): a histological and histochemical view (2012) Acta Zool., 93, pp. 222-230
  • Ravi, R., Manisseri, M.K., Sanil, N.K., Structure of the male reproductive system of the blue swimmer crab Portunus pelagicus (Decapoda: Portunidae) (2014) Acta Zool., 95, pp. 176-185
  • Reynolds, E.S., The use of lead citrate at high ph as an electron-opaque stain in electron microscopy (1963) J. Cell Biol., 17, p. 208
  • Ro, S., Talbot, P., Trujillo, J.L., Lawrence, A.L., Structure and function of the vas deferens in the shrimp Penaeus setiferus: segments 1-3 (1990) J. Crustacean Biol., 10, pp. 455-468
  • Rotllant, G., Chiva, M., Durfort, M., Ribes, E., Internal anatomy and ultrastructure of the male reproductive system of the Norway lobster Nephrops norvegicus (Decapoda: Astacidea) (2012) J. Morphol., 273, pp. 572-585
  • Ryan, E.P., Structure and function of the reproductive system of the crab Portunus sanguinolentus Herbst (Brachyura: Portunidae). I. The male system (1967) Proceedings of the Symposium on Crustacea at Erkulan, Índia, 1965. Part II. Symposium Series, 2, pp. 522-544
  • Santos, C.M., Lima, G.V., Nascimento, A.A., Sales, A., Oshiro, L.M.Y., Histological and histochemical analysis of the gonadal development of males and females of Armases rubripes (Rathbun 1897) (Crustacea, Brachyura, Sesarmidae) (2009) Braz. J. Biol., 69, pp. 161-169
  • Scelzo, M.A., Mantelatto, F.L., Tudge, C.C., Spermatophore morphology of the endemic hermit crab Loxopagurus loxochelis (Anomura, Diogenidae) from the southwestern Atlantic - Brazil and Argentina (2004) Invertebr. Reprod. Dev., 46, pp. 1-9
  • Simeó, C.G., Ribes, E., Rotllant, G., Internal anatomy and ultrastructure of the male reproductive system of the spider crab Maja brachydactyla (Decapoda: Brachyura) (2009) Tiss. Cell., 41, pp. 345-361
  • Stewart, M.J., Stewart, P., Soonklang, N., Linthong, V., Hanna, P.G., Duan, W., Sobhon, P., Spermatogenesis in the blue swimming crab, Portunus pelagicus, and evidence for histones in mature sperm nuclei (2010) Tiss. Cell., 42, pp. 137-150
  • Subramoniam, T., Spermatophores and sperm transfer in marine crustaceans (1993) Adv. Mar. Biol., 29, pp. 129-214
  • Tavares, M., Franco, G.M.O., Why the spermathecal openings are so displaced forward in the Podotremata (Decapoda: Brachyura)? Ontogenetic changes and phylogenetic implications (2004) Nauplius, 12, pp. 127-134
  • Tavares, M.S., Secretan, S., La notion de thelycum et de spermathèque chez les Crustacés Décapodes (1993) C. r. Acad. Sci. Paris., 316, pp. 133-138
  • Tiseo, G.R., Mantelatto, F.L., Zara, F.J., Is cleistospermy and coenospermy related to sperm transfer? A comparative study of the male reproductive system of Pachygrapsus transversus and Pachygrapsus gracilis (Brachyura: Grapsidae) (2014) J. Crustacean Biol., 34, pp. 704-716
  • Tiseo, G.R., Mantelatto, F.L., Zara, F.J., Ultrastructure of spermatophores and spermatozoa of intertidal crabs Pachygrapsus transversus, Pachygrapsus gracilis and Geograpsus lividus (Decapoda: Grapsidae) (2017) Zool. Anz.- A Journal of Comparative Zoology, 269, pp. 166-176
  • Tsang, L.M., Schubart, C.D., Ahyong, S.T., Lai, J.C., Au, E.Y., Chan, T.Y., Ng, K.L.P., Chu, K.H., Evolutionary history of true crabs (Crustacea: Decapoda: Brachyura) and the origin of freshwater crabs (2014) Mol. Biol. Evol., 31, pp. 1173-1187
  • Tudge, C.C., Spermatophore diversity within and among the hermit crab families, Coenobitidae, Diogenidae, and Paguridae (Paguroidea, Anomura, Decapoda) (1991) Biol. Bull., 181, pp. 238-247
  • Vehof, J., Scholtz, G., Becker, C., Morphology of the female reproductive system of three dorippid crabs (Crustacea: Decapoda: Brachyura: Dorippidae) and the role of accessory cuticle structures associated with seminal receptacles (2017) Invertebr. Biol., 136, pp. 271-289
  • Vehof, J., Scholtz, G., Becker, C., Paradorippe granulata– A crab with external fertilization and a novel type of sperm storage organ challenges prevalent ideas on the evolution of reproduction in Eubrachyura (Crustacea: Brachyura: Dorippidae) (2018) Arthropod Struct. Dev., 47, pp. 82-90
  • Zara, F.J., Caetano, F.H., Ultrastructure of the salivary glands of Pachycondyla (= Neoponera) villosa (Fabricius)(Formicidae: Ponerinae): functional changes during the last larval instar (2002) Cytologia, 67, pp. 267-280
  • Zara, F.J., Toyama, M.H., Caetano, F.H., López Greco, L.S., Spermatogenesis, spermatophore, and seminal fluid production in the adult blue crab, Callinectes danae (Portunidae) (2012) J. Crustacean Biol., 32, pp. 249-262
  • Zara, F.J., Raggi Pereira, G.R., Sant'Anna, B.S., Morphological changes in the seminal receptacle during ovarian development in the speckled swimming crab Arenaeus cribrarius (2014) Biol. Bull., 227, pp. 19-32

Citas:

---------- APA ----------
Garcia Bento, M.A., López Greco, L.S. & Zara, F.J. (2019) . Seminal fluid production and sperm packaging in dromiid crabs (Brachyura, Podotremata). Zoology, 132, 17-30.
http://dx.doi.org/10.1016/j.zool.2018.09.001
---------- CHICAGO ----------
Garcia Bento, M.A., López Greco, L.S., Zara, F.J. "Seminal fluid production and sperm packaging in dromiid crabs (Brachyura, Podotremata)" . Zoology 132 (2019) : 17-30.
http://dx.doi.org/10.1016/j.zool.2018.09.001
---------- MLA ----------
Garcia Bento, M.A., López Greco, L.S., Zara, F.J. "Seminal fluid production and sperm packaging in dromiid crabs (Brachyura, Podotremata)" . Zoology, vol. 132, 2019, pp. 17-30.
http://dx.doi.org/10.1016/j.zool.2018.09.001
---------- VANCOUVER ----------
Garcia Bento, M.A., López Greco, L.S., Zara, F.J. Seminal fluid production and sperm packaging in dromiid crabs (Brachyura, Podotremata). Zoology. 2019;132:17-30.
http://dx.doi.org/10.1016/j.zool.2018.09.001