Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-27T19:45:01.243Z Has data issue: false hasContentIssue false
  • English
  • Français

Grooves surrounding the micropyle decrease the inseminating dose in fish

Published online by Cambridge University Press:  01 December 2017

Matheus Pereira-Santos ,
Eduardo Shimoda ,
André Furugen Cesar de Andrade ,
Luciano Andrade Silva ,
Takafumi Fujimoto ,
José Augusto Senhorini ,
George Shigueki Yasui  and
Laura Satiko Okada Nakaghi
Matheus Pereira-Santos*
Affiliation:
Aquaculture Center, São Paulo State University, Via de Acesso Prof. Paulo Donato Castellane s/n, 14884–900, Jaboticabal-SP, Brazil.
Eduardo Shimoda
Affiliation:
Department of Pharmacy, Cândido Mendes University, Rua Anita Peçanha, 100, 28030–335, Campos dos Goytacazes-RJ, Brazil.
André Furugen Cesar de Andrade
Affiliation:
Department of Veterinary, University of São Paulo, Avenida Duque de Caxias Norte, 225, 13630-080, Pirassununga-SP, Brazil.
Luciano Andrade Silva
Affiliation:
Department of Veterinary, University of São Paulo, Avenida Duque de Caxias Norte, 225, 13630-080, Pirassununga-SP, Brazil.
Takafumi Fujimoto
Affiliation:
Faculty of Fisheries Sciences, Hokkaido University, 3–1-1 Minato-cho, 041–8611, Hakodate, Japan.
José Augusto Senhorini
Affiliation:
National Center for Research and Conservation of Continental Fish, Chico Mendes Institute of Biodiversity Conservation, Rodovia Pref. Euberto Nemésio Pereira de Godoy, Km 6, 5, CP 65, 13.630-970. Pirassununga, São Paulo, Brazil.
George Shigueki Yasui
Affiliation:
Department of Veterinary, University of São Paulo, Avenida Duque de Caxias Norte, 225, 13630-080, Pirassununga-SP, Brazil.
Laura Satiko Okada Nakaghi
Affiliation:
Aquaculture Center, São Paulo State University, Via de Acesso Prof. Paulo Donato Castellane s/n, 14884–900, Jaboticabal-SP, Brazil.
*
All correspondence to: Matheus Pereira-Santos. Aquaculture Center, São Paulo State University, Via de Acesso Prof. Paulo Donato Castellane s/n, 14884–900, Jaboticabal-SP, Brazil. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

In fish with external fertilization, sperm must reach the oocyte through the micropyle to enter the cytoplasm. Fertilization success is then influenced by characteristics of oocytes or sperm. In this study, we evaluated oocyte morphology and sperm motility parameters and their effects on the inseminating dose in a teleost fish Astyanax altiparanae. Interestingly, we found one of the lowest yet described inseminating doses in teleosts (2390 spermatozoa oocyte−1 ml−1). Such a fertilization efficacy may be explained by the long duration of sperm motility (>75 s), the small oocyte diameter (695.119 µm), large micropyle diameter (7.57 µm), and the presence of grooves on the oocyte surface that guides spermatozoon to the fertilization area. Additionally, we have described for the first time a structure that combines grooves on the chorion surface and a ridge in the micropylar area.

Keywords

FertilizationGametesMorphologySpermTeleosts
Type
Research Article
Information
Zygote , Volume 25 , Issue 6 , December 2017 , pp. 731 - 739
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Amanze, D. & Iyengar, A. (1990). The micropyle: a sperm guidance system in teleost fertilization. Development 109, 495–500.CrossRefGoogle ScholarPubMed
Bobe, J. & Labbé, C. (2010). Egg and sperm quality in fish. Gen. Comp. Endocrinol. 165, 535–48.Google Scholar
Casselman, S.J., Schulte-Hostedde, A.I. & Montgomerie, R. (2006). Sperm quality influences male fertilization success in walleye (Sander vitreus). Can. J. Fish. Aqua. Sci. 63, 2119–25.Google Scholar
Cosson, J. (2004). The ionic and osmotic factors controlling motility of fish spermatozoa. Aquacult. Int. 12, 69–85.Google Scholar
Coward, K., Bromage, N.R., Hibbitt, O. & Parrington, J. (2002). Gamete physiology, fertilization and egg activation in teleost fish. Rev. Fish Biol. Fish. 12, 33–58.Google Scholar
Gage, M.J.G., Macfarlane, C.P., Yeates, S., Ward, R.G., Searle, J.B. & Parker, G.A. (2004). Spermatozoal traits and sperm competition in Atlantic salmon: relative sperm velocity is the primary determinant of fertilization success. Curr. Biol. 14, 44–7.Google Scholar
Galego, V., Pérez, L., Asturiano, J.F. & Yoshida, M. (2013). Relationship between spermatozoa motility parameters, sperm/egg ratio, and fertilization and hatching rates in pufferfish (Takifugu niphobles). Aquaculture 416–417, 238–43.Google Scholar
Garutti, V. & Britski, H.A. (2000). Descrição de uma espécie nova de Astyanax (Teleostei: Characidae) da bacia do alto rio Paraná e considerações sobre as demais espécies do gênero na bacia. Comum. Mus. Ciênc. Tecnol. PUCRS. Sér. Zool. Porto Alegre, 13, 65–88.Google Scholar
Gasparini, C., Simmons, L.W., Beveridge, M. & Evans, J.P. (2010). Sperm swimming velocity predicts competitive fertilization success in the green swordtail Xiphophorus helleri . PLoS One 5, 1–5.Google Scholar
Ginsburg, A.S. (1961). The block to polyspermy in sturgeon and trout with special reference to the role of cortical granules (aleveoli). J. Embryo Exp. Morphol. 9, 173–90.Google Scholar
Ginsburg, A.S. (1963). Sperm-egg association and its relationship to the activation of the egg in Salmonid fishes. J. Embryo Exp. Morphol. 11, 13–33.Google Scholar
Giulianini, P.G. & Ferrero, E.A. (2000). Ultrastructural aspects of the ovarian follicle and egg envelope of the sea-grass goby Zosterisessor ophiocephalus (Osteichthyes, Gobiidae). Ital. J. Zool. 68, 29–37.Google Scholar
Gomendio, M. & Roldan, E.R.S. (2008). Implications of diversity in sperm size and function for sperm competition and fertility. Int. J. Dev. Biol. 52, 439–47.Google Scholar
Hart, N.Y. (1990). Fertilization in teleost fishes: Mechanisms of sperm–egg interactions. Int. Rev. Cyto. 121, 1–66.Google Scholar
Hirai, A. (1988). Fine structures of the micropyles of pelagic eggs of some marine fishes. Japan J. Ichthyol. 35, 351–7.Google Scholar
Hirohashi, N., Kamei, N., Kubo, H., Sawasa, H., Matsumoto, M. & Hoshi, M. (2008). Egg and sperm recognition systems during fertilization. Dev. Growth Diff. 50, S221–38.CrossRefGoogle ScholarPubMed
Hosken, D.J., Taylor, M.L., Hoyle, K., Higgins, S. & Wedell, N. (2008). Attractive males have greater success in sperm competition. Curr. Biol. 18, 553–4.Google Scholar
Hunter, F.M. & Birkhead, T.R. (2002). Sperm viability and sperm competition in insects. Curr. Biol. 12, 121–3.Google Scholar
Ishijima, S., Hamaguchi, Y. & Iwamatsu, T. (1993). Sperm behavior in the micropyle in the medaka egg. Zool. Sci. 10, 179–82.Google Scholar
Iwamatsu, T., Ishijima, S. & Nakashima, S. (2005). Movement of spermatozoa and changes in micropyles during fertilization in medaka eggs. J. Exp. Zool. 266, 57–64.CrossRefGoogle Scholar
Kime, D.E., Van Look, K.J.W., McAllister, B.G., Huyskens, G., Rurangwa, E. & Ollevier, F. (2001). Computer-assisted sperm analysis (CASA) as a tool for monitoring sperm quality in fish. Comp. Biochem. Physiol. 130, 425–33.Google ScholarPubMed
Kuchnow, K.P. & Scott, J.R. (2006). Ultrastructure of the chorion and its micropyle apparatus in the mature Fundulus heteroclitus (Walbaum) ovum. J. Fish Biol. 10, 197–201.CrossRefGoogle Scholar
Lillie, F.R. (1919). Problems of Fertilization. Chicago: Univ. of Chicago Press, pp. 98–99.Google Scholar
Linhart, O. & Kudo, S. (1997). Surface ultrastructure of paddlefish eggs before and after fertilization. J. Fish Biol. 51, 573–82.Google Scholar
Mansour, N., Lahnsteiner, F. & Patzner, R.A. (2002). The spermatozoon of the African catfish: fine structure, motility, viability and its behaviour in seminal vesicle secretion. J. Fish Biol. 60, 545–60.Google Scholar
Marciel, J. (1981). Contrôle de la reproduction et gestions dês gamètes de quelques espèces de poissons téléostéens. Lyons: École Pratique des hautes Études. 132 ff.Google Scholar
McMillan, D.B. (2007). Fish Histology: Female Reproductive Systems. University of Western Ontario, Canada. Springer.Google Scholar
Morisawa, S. & Morisawa, M. (1986). Acquisition of potential for sperm motility in rainbow trout and chum salmon. J. Exp. Biol. 126, 89–96.Google Scholar
Riehl, R. & Patzner, R.A. (1991). Breeding, structure, and larval morphology of the catfish Sturisoma aureum (Steindachner) (Teleostei, Loricariidae). J. Aquac. Aquat. Sci. 6, 1–6.Google Scholar
Rizzo, E., Sato, Y., Barreto, B.P. & Godinho, H.P. (2002). Adhesiveness and surface patterns of eggs in neotropical freshwater teleosts. J. Fish Biol. 61, 615–32.Google Scholar
Rudolfsen, G., Figenschou, L., Folstad, I. & Kleven, O. (2008). Sperm velocity influence paternity in the Atlantic cod (Gadus morhua L.). Aquacul. Res. 39, 212–6.Google Scholar
Rurangwa, E., Roelants, I., Huyskens, G., Ebrahimi, M., Kime, D.E. & Ollevier, F. (1998). The minimum effective spermatozoa: egg ratio for artificial inseminating and the effects of mercury on sperm motility and fertilization ability in Clarias gariepinus . J. Fish Biol. 53, 402–13.Google Scholar
Scott, A.P. & Baynes, S.M. (1980). A review of the biology, handling and storage of salmonid spermatozoa. J. Fish Biol. 17, 707–39.Google Scholar
Shimoda, E., Andrade, D.R., Vidal, Júnior, M.V., Godinho, H.P. & Yasui, G.S. (2007). Determinação da razão ótima de espermatozoides por ovócitos de piabanha Brycon insignis (Pisces: Characidae). Arq. Bras. de Med. Vet. Zootec. 59, 877–82.Google Scholar
Silveira, W.F., Kavamoto, E.T., Rigolino, M.G. & Tabata, Y.A. (1988). Fertilidade do sêmen da truta arco-íris, Salmo irideus Gibbons, em diferentes concentrações de espermatozoides por óvulo. Bol. Inst. Pesca 15, 51–7.Google Scholar
Stolz, J.A. & Neff, B.D. (2006). Sperm competition in a fish with external fertilization: the contribution of sperm number, speed and length. J. Evol. Biol. 19, 1873–81.Google Scholar
Suquet, M., Billard, R. & Cosson, J. (1995). Artificial inseminating in turbot (Scophthalmus maximus): determination of the optimal sperm to egg ratio and time of gamete contact. Aquaculture 133, 83–90.Google Scholar
Tuset, V.M., Dietrich, G.J., Wojtczak, M., Slowinska, M., Monserrat, J. & Ciereszko, A. (2008). Relationship between morphology, motility and fertilization capacity in rainbow trout (Oncorhynchus mykiss) spermatozoa. J. Appl. Ichthyol. 24, 393–7.Google Scholar
Viveiros, A.T.M. & Godinho, H.P. (2009). Sperm quality and cryopreservation of Brazilian freshwater fish species: a review. Fish. Physiol. Biochem. 35, 137–50.Google Scholar
Yanagimachi, R., Cherr, G.N., Pillai, M.C. & Baldwin, J.D. (1992). Factors controlling sperm entry into the micropyle of salmonid and herring eggs. Dev. Growth Diff. 34, 447–61.Google Scholar
Yanagimachi, R., Cherr, G., Matsubara, T., Andoh, T., Harumi, T., Vines, S, C., Pillai, M., Griffin, F, Matsubara, H., Weatherby, T. & Kenneth, K. (2013). Sperm attractant in the micropyle region of fish and insect eggs. Biol. Reprod. 88, 47.Google Scholar
Yasui, G.S., Arias-Rodrigues, L., Fujimoto, T. & Arai, K. (2009). A sperm cryopreservation protocol for the loach Misgurnus anguillicaudatus and its applicability for other related species. Anim. Repr. Sci. 116, 335–45.CrossRefGoogle ScholarPubMed
Yasui, G.S., Senhorini, J.A., Shimoda, E., Pereira-Santos, M., Nakaghi, L.S.O., Fujimoto, T., Arias-Rodrigues, L. & Silva, L.A. (2015). Improvement of gamete quality and its short-term storage: an approach for biotechnology in laboratory fish. Animal 9, 464–70.Google Scholar