Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-11T00:44:26.421Z Has data issue: false hasContentIssue false

Structural analysis of oocytes, post-fertilization events and embryonic development of the Brazilian endangered teleost Brycon insignis (Characiformes)

Published online by Cambridge University Press:  15 August 2011

Ziara A. Isaú
Affiliation:
Dept of Animal Science (DZO), Federal University of Lavras (UFLA), MG, Brazil.
Elizete Rizzo
Affiliation:
Institute of Biological Science (ICB), Federal University of Minas Gerais (UFMG), MG, Brazil.
Thiciana B. Amaral
Affiliation:
Dept of Animal Science (DZO), Federal University of Lavras (UFLA), MG, Brazil.
Natália M.N. Mourad
Affiliation:
Dept of Animal Science (DZO), Federal University of Lavras (UFLA), MG, Brazil.
Ana T.M. Viveiros*
Affiliation:
Dept Zootecnia, Universidade Federal de Lavras (UFLA), caixa postal 3037, Lavras, MG, 37200–000, Brazil.
*
All correspondence to: Ana T M Viveiros. Dept Zootecnia, Universidade Federal de Lavras (UFLA), caixa postal 3037, Lavras, MG, 37200–000, Brazil. Tel/Fax: +55 35 38291231. e-mail: anatmviveiros@hotmail.com or ana.viveiros@dzo.ufla.br

Summary

The aim of this study was to evaluate the oocytes, post-fertilization events and embryonic development in Brycon insignis, under both scanning electron microscopy and stereomicroscopy. Oocytes and embryos were sampled from spawning up to hatching. Stripped oocytes were spherical, non-adhesive, greenish-brown, possessed a single micropyle, pore-canals and had a mean diameter of 1.46 mm. In 63% of oocytes the germinal vesicle was peripheric. The main post-fertilization events were the fertilization cone formation (20 s), micropyle closure (100–180 s) and agglutination of supernumerary spermatozoa (100–180 s). Embryonic development lasted 30 h at ~24 °C and was characterized by seven stages. Zygote, cleavage, blastula and gastrula stages were first observed at 0.25, 1, 3 and 6 h post-fertilization, respectively. Fertilization rate was determined at the moment of blastopore closure, 10–11 h post-fertilization. The segmentation stage began at 11 h post-fertilization and comprised the development of somites, notochord, optic, otic and Kupffer's vesicles, neural tube, primitive intestine, and development and release of the tail. The larval stage began 21 h post-fertilization and was characterized by the presence of somites, growth and elongation of the larvae. At the hatching stage, embryos presented vigorous contractions of the tail and body leading to chorion rupture (30 h). The morphological characteristics described for B. insignis were similar to that described for other teleost species, and such knowledge is important for a better understanding of reproductive features of a species and useful for ecological and conservational studies.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2011

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

Alexandre, J.S., Ninhaus-Silveira, A., Veríssimo-Silveira, R., Buzollo, H., Senhorini, J.A. & Chaguri, M.P. (2010). Structural analysis of the embryonic development in Brycon cephalus (Günther, 1869). Zygote 18, 173–83.CrossRefGoogle ScholarPubMed
Amorim, M.P., Gomes, B.V.C., Martins, Y.S., Sato, Y., Rizzo, E. & Bazzoli, N. (2009). Early development of the silver catfish Rhamdia quelen (Quoy & Gaimard, 1824) (Pisces: Heptapteridae) from the São Francisco River basin, Brazil. Aquac. Res. 40, 172–80.CrossRefGoogle Scholar
Andrade-Talmelli, E.F., Kavamoto, E.T., Romagosa, E. & Fenerich-Verani, N. (2001). Embryonic and larval development of the “piabanha,” Brycon insignis, Steindachner, 1876 (Pisces, Characidae). Bol. Inst. Pesca 27, 21–8.Google Scholar
Brasil, D.F., Nakaghi, L.S.O., Santos, H.S.L., Grassiotto, I.Q. & Foresti, F. (2002). Estudo morfológico dos primeiros momentos da fertilização em curimbatá Prochilodus lineatus (Valenciennes, 1836). CIVA 2002, 1 pp. 733747. Disponível em http://www.civa2002.org/Google Scholar
Cardoso, E.L., Alves, M.S.D., Ferreira, R.M.A. & Godinho, H.P. (1995). Embryogenesis of the neotropical freshwater siluriforme Pseudoplatystoma coruscans. Aquat. Living Resour. 8, 343–6.CrossRefGoogle Scholar
Castellani, L.R., Tse, H.G., Leme dos Santos, H.S. & Faria, R.H.S. (1994). Desenvolvimento embrionário do curimbatá, Prochilodus lineatus (Valenciennes, 1836) (Characiformes, Prochilodontidae). Rev. Bras. Ciênc. Morfol. 11, 99105.Google Scholar
Devlin, R.H. & Nagahama, Y. (2002). Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208, 191364.CrossRefGoogle Scholar
Eckmann, R. (1984). Induced reproduction in Brycon cf. erythropterus. Aquaculture 38, 379–82.CrossRefGoogle Scholar
Faustino, F., Nakaghi, L.S.O., Marques, C., Makino, L.C. & Senhorini, J.A. (2007). Fertilização e desenvolvimento embrionário: morfometria e análise estereomicroscópica dos ovos dos híbridos surubins (pintado, Pseudoplatystoma coruscans × cachara, Pseudoplatystoma fasciatum). Acta Sci. 29, 4955.Google Scholar
Flores, J.C.B., Araiza, M.A.F. & Valle, M.R.G. (2002). Desarrollo embrionario de Ctenopharyngodon idellus (Carpa herbívora). CIVA 2002 1, pp. 792797. Disponível em: http://www.civa2002.org/Google Scholar
Froese, R., Pauly, , Editors, D.. (2010). FishBase. World Wide Web electronic publication (http://www.fishbase.org), version (03/2010).Google Scholar
Ganeco, L.N. (2003). Análise dos ovos de piracanjuba, Brycon orbignyanus (Valenciennes, 1849), durante a fertilização e o desenvolvimento embrionário, sob condições de reprodução induzida. MSc Thesis, Universidade de Estadual Paulista, Jaboticabal, SP, Brazil.Google Scholar
Ganeco, L.N. & Nakaghi, L.S.O. (2003). Morfologia da superfície dos ovócitos e caracterização da micrópila de piracanjuba, Brycon orbignyanus, sob microscopia eletrônica de varredura. Acta Sci. 25, 227–31.Google Scholar
Ganeco, L.N., Franceschini-Vicentini, I.B. & Nakaghi, L.S.O. (2009). Structural analysis of fertilization in the fish Brycon orbignyanus. Zygote 17, 93–9.CrossRefGoogle ScholarPubMed
Gilbert, S.F. (1991). Developmental Biology. Sunderland, MA: Sinauer Associates.Google Scholar
Godinho, H.M., Fenerich, N., De, A. & Narahara, M.Y. (1978). Desenvolvimento embrionário e larval de Rhamdia hilarii (Valenciennes, 1840) (Siluriformes, Pimelodidae). Rev. Bras. Biol. 38, 151–6.Google Scholar
Gomes, B.V.C., Scarpelli, R.S., Arantes, F.P., Sato, Y., Bazzoli, N. & Rizzo, E. (2007). Comparative oocytes morphology and early development in three species of trahiras from the São Francisco River basin, Brazil. J. Fish Biol. 70, 1412–29.CrossRefGoogle Scholar
Hansen, T.K. & Falk-Petersen, I.B. (2002). Growth and survival of first-feeding spotted wolf fish (Anarhichas minor Olafsen) at various temperature regimes. Aquac. Res. 33, 1119–27.CrossRefGoogle Scholar
Hart, N.H. & Donovan, M. (1983). Fine structure of the chorion and site of sperm entry in the egg of Brachydanio. J. Exp. Zool. 227, 277–96.CrossRefGoogle Scholar
Hilsdorf, A.W.S. & Petrere, M. Jr (2002). Conservação de peixes na bacia do rio Paraíba do Sul. Ciência Hoje 30, 62–5.Google Scholar
Iwamatsu, T. & Ohta, T. (1981). Scanning electron microscopic observation on sperm penetration in teleostean fish. J. Exp. Zool. 218, 261–77.CrossRefGoogle Scholar
Iwamatsu, T., Onitake, K., Yoshimoto, Y. & Hiramoto, Y. (1991). Time sequence of early events in fertilization in the medaka egg. Dev. Growth Differ. 33, 479–90.CrossRefGoogle ScholarPubMed
Iwamatsu, T., Ishijima, S. & Nakashima, S. (1993). Movement of spermatozoa and changes in micropyles during fertilization in medaka eggs. J. Exp. Zool. 266, 5764.CrossRefGoogle Scholar
Kimmel, C.B. & Law, R.D. (1985). Cell lineage of zebrafish blastomeres: II Formation of the yolk syncytial layer. Dev. Biol. 108, 8693.CrossRefGoogle ScholarPubMed
Kimmel, C.B., Ballard, W.W., Kimmel, S.R. & Ullmann, B. (1995). Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253310.CrossRefGoogle ScholarPubMed
Kobayashi, W. & Yamamoto, T. (1981). Fine structure of the micropylar apparatus of the chum salmon egg, with a discussion of the mechanism for blocking polyspermy. J. Exp. Zool. 217, 265–75.CrossRefGoogle Scholar
Kudo, S. (1980). Sperm penetration and the formation of a fertilization cone in the common carp egg. Dev. Growth Differ. 22, 403–14.CrossRefGoogle ScholarPubMed
Kudo, S., Linhart, O. & Billard, R. (1994). Ultrastructural studies of sperm penetration in the egg of the European catfish, Silurus glanis. Aquat. Living Resour. 7, 93–8.CrossRefGoogle Scholar
Lagler, K.F., Bardach, J.E., Miller, R.R. & Passino, D.R.M. (1977). Ichthyology, 2nd edition. New York: John Wiley & Sons, Inc.Google Scholar
Leme dos Santos, H.S. & Azoubel, R. (1996). Embriologia comparada. Jaboticabal: FUNEP.Google Scholar
Lima, F.C.T., Albrecht, M.P., Pavanelli, C.S. & Vono, V. (2007). Threatened fishes of the world: Brycon nattereri Günther, 1864 (Characidae). Environ. Biol. Fishes 1, 12.Google Scholar
Linhart, O. & Kudo, S. (1997). Surface ultrastructure of paddlefish egg before and after fertilization. J. Fish Biol. 51, 573–82.Google Scholar
Lopes, R.N.M., Senhorini, J. A. & Soares, M.C.F. (1995). Desenvolvimento embrionário e larval do matrinxã Brycon cephalus Gunther, 1869, (PISCES, CHARACIDAE). Bol. Tec. Cepta 8, 2539.Google Scholar
Machado, C.E. & Abreu, H.C.F. (1952). Notas preliminares sobre a caça e a pesca no Estado de São Paulo–I. A pesca no vale do Paraíba. Bol. Ind. Animal 13, 145–60.Google Scholar
Maria, A.N. (2008). Caracterização ultra-estrutural dos gametas, aspectos da fertilização e desenvolvimento inicial de pirapitinga Brycon nattereri (Günther, 1864). PhD Thesis, Universidade Federal de Lavras, Lavras, MG, Brazil.Google Scholar
Maria, A.N., Viveiros, A.T.M., Freitas, R.T.F. & Oliveira, A.V. (2006). Extenders and cryoprotectants for cooling and freezing of piracanjuba (Brycon orbignyanus) semen, an endangered Brazilian teleost fish. Aquaculture 260, 298306.CrossRefGoogle Scholar
Marques, C., Nakaghi, L.S.O., Faustino, F., Ganeco, L.N., & Senhorini, J.A. (2008). Observation of the embryonic development in Pseudoplatystoma coruscans (Siluriformes: Pimelodidae) under light and scanning electron microscopy. Zygote 17, 110.Google Scholar
Moore, K.L. (2001). Embriologia Clínica. 4th edition. Rio de Janeiro: Guanabara Koogan S.A.Google Scholar
Morrison, C.M., Miyake, T. & Wright, J. Jr., (2001). Histological study of the development of the embryo and early larvae of Oreochromis niloticus (Pisces; Cichlidae). J. Morphol. 247, 172–95.3.0.CO;2-H>CrossRefGoogle ScholarPubMed
Murata, K. (2003). Blocks to polyspermy in fish: A brief review. In: Symposium on Aquaculture and Pathobiology of Crustacean and Other Species, 32, 2003, Santa Barbara. Anais Santa Barbara: UJNR. Aquaculture Panel Proceedings. 15 pp.Google Scholar
Nakaghi, L.S.O., Marques, C., Faustino, F., Ganeco, L.N. & Senhorini, J.A. (2006). Desenvolvimento embrionário do dourado (Salminus brasiliensis) por meio de microscopia eletrônica de varredura. Bol. Tec. Cepta 19, 919.Google Scholar
Neumann, E., Mendes, J.M.R. & Nakaghi, L.S.O. (2007). Momentos da fertilização induzida em jatuarana Brycon sp. (Teleostei, Characidae) em microscopia eletrônica de varredura. In: Congresso brasileiro de produção de peixes nativos de água doce, 1, Dourados. Anais ISSN 1809 9718; 87 Dourados: Painel Proceedings. 4 pp.Google Scholar
Ninhaus-Silveira, A., Foresti, F. & Azevedo, A. (2006). Structural and ultrastructural analysis of embryonic development of Prochilodus lineatus (Valenciennes, 1836) (Characiforme, Prochilodontidae). Zygote 14, 217–29.CrossRefGoogle ScholarPubMed
Perini, V.R., Sato, Y., Rizzo, E. & Bazzoli, N. (2010). Biology of eggs, embryos and larvae of Rhinelepis aspera (Spix & Agassiz, 1829) (Pisces: Siluriformes). Zygote 18, 159–71.CrossRefGoogle Scholar
Reynalte-Tataje, D., Zaniboni-Filho, E. & Esquivel, J.R. (2004). Embryonic and larvae development of piracanjuba, Brycon orbignyanus Valenciennes, 1849 (Pisces, Characidae). Acta Sci. 26, 6771.Google Scholar
Rizzo, E. & Bazzoli, N. (1993). Oogenesis, oocyte surface and micropylar apparatus of Prochilodus affinis Reinhardt, 1874 (Pisces Characiformes). Eur. Arch. Biol. 104, 16.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.CrossRefGoogle Scholar
Romagosa, E., Narahara, M.Y. & Fenerich-Verani, N. (2001). Stages of embryonic development of the ‘matrinxã,’ Brycon cephalus (Pisces, Characidae). Bol. Inst. Pesca 27, 2732.Google Scholar
Sato, Y., Fenerich-Verani, N., Verani, J.R., Vieira, L.J.S., & Godinho, H.P. (2000). Induced reproductive responses of the neotropical anostomids fish Leporinus elongatus Val. under captive breeding. Aquac. Res. 11, 189–93.CrossRefGoogle Scholar
Sato, Y., Fenerich-Verani, N., & Godinho, H.P. (2003). Reprodução induzida de peixes da bacia do São Francisco. In: Godinho, H.P. & Godinho, A.L. (Org.). Águas, peixes e pescadores do São Francisco da Minas Gerais. Belo Horizonte: PUC Minas, pp. 257–89.Google Scholar
Schatten, G. (1999). Fertilization. In: Encyclopedia of Reproduction vol. 2. (eds. Knobil, E. & Neill, J.D.) London: Academic Press. pp. 256–65.Google Scholar
Trinkaus, J.P. (1984). Mechanism of Fundulus epiboly: a current review. Am. Zool. 24, 673–88.CrossRefGoogle Scholar
Van Zutphen, L.F.M., Baumans, V. & Beynen, A.C. (1993). Principles of Laboratory Animal Science – A Contribution to the Humane Use and Care of Animals and to the Quality of Experimental Results. Elsevier, Amsterdam.Google Scholar
Vazzoler, A.E.A.M. (1996). Biologia da reprodução de peixes teleósteos: teoria e prática. Maringá: EDUEM. 169 pp.Google Scholar
Viveiros, A.T.M., Amaral, T.B., Orfão, L.H., Isau, Z.A., Caneppele, D. & Leal, M.C. (2011). Sperm cryopreservation of tiete tetra Brycon insignis (Characiformes): effects of cryoprotectants, extenders, thawing temperatures and activating agent on motility features. Aquac. Res. 42, 858–65.CrossRefGoogle Scholar