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Ovarian cycle in Devario aequipinnatus with emphasis on oogenesis

Published online by Cambridge University Press:  02 April 2018

Laíza Maria de Jesus-Silva
Affiliation:
Programa de Pós-Graduação em Ciência e Tecnologia Animal – FEIS/UNESP – Universidade Estadual Paulista, Campus de Ilha Solteira, São Paulo, Brasil. Laboratório de Ictiologia Neotropical – L.I.NEO., Departamento de Biologia e Zootecnia, FEIS/UNESP – Universidade Estadual Paulista ‘Júlio de Mesquita Filho’, Rua Monção, 226 – Zona Norte, Ilha Solteira, São Paulo, 15385-000, Brasil.
Pricila Viana de Oliveira
Affiliation:
Programa de Pós-Graduação em Ciência e Tecnologia Animal – FEIS/UNESP – Universidade Estadual Paulista, Campus de Ilha Solteira, São Paulo, Brasil. Laboratório de Ictiologia Neotropical – L.I.NEO., Departamento de Biologia e Zootecnia, FEIS/UNESP – Universidade Estadual Paulista ‘Júlio de Mesquita Filho’, Rua Monção, 226 – Zona Norte, Ilha Solteira, São Paulo, 15385-000, Brasil.
Cristiéle da Silva Ribeiro
Affiliation:
Departamento de Biologia e Zootecnia, FEIS/UNESP – Universidade Estadual Paulista ‘Júlio de Mesquita Filho’, Rua Monção, 226, Zona Norte, Ilha Solteira, São Paulo, 15385-000, Brasil.
Alexandre Ninhaus-Silveira
Affiliation:
Laboratório de Ictiologia Neotropical – L.I.NEO., Departamento de Biologia e Zootecnia, FEIS/UNESP – Universidade Estadual Paulista ‘Júlio de Mesquita Filho’, Rua Monção, 226 – Zona Norte, Ilha Solteira, São Paulo, 15385-000, Brasil.
Rosicleire Veríssimo-Silveira*
Affiliation:
Departamento de Biologia e Zootecnia, FEIS/UNESP – Universidade Estadual Paulista ‘Júlio de Mesquita Filho’, Rua Monção, 226, Zona Norte, Ilha Solteira, São Paulo, 15385-000, Brasil. Programa de Pós-Graduação em Ciência e Tecnologia Animal – FEIS/UNESP – Universidade Estadual Paulista, Campus de Ilha Solteira, São Paulo, Brasil.
*
All correspondence to: Rosicleire Veríssimo-Silveira. Departamento de Biologia e Zootecnia, FEIS/UNESP – Universidade Estadual Paulista ‘Júlio de Mesquita Filho’, Rua Monção, 226, Zona Norte, Ilha Solteira, São Paulo, 15385-000, Brasil. Tel: +55 (18) 37431935. Fax: +55 (18) 37422140. E-mail: rosiverissimo@bio.feis.unesp.br

Summary

This study aimed to understand how germ cell development occurs in females of Devario aequipinnatus, by morphologically describing oogenesis and the reproductive phases. Sexually mature females of D. aequipinnatus (n = 70) were obtained from commercial fisheries and delivered to the Laboratório de Ictiologia Neotropical, UNESP, Ilha Solteira, SP, Brazil. The ovaries were removed, fragmented and fixed following the usual techniques for light microscopy. The stages of ovarian development in D. aequipinnatus begin with the oogonia, which proliferate into new cells or differentiate into prophasic oocytes that, at the end of this process, form the ovarian follicle and end folliculogenesis. In the previtellogenic stage, the oocytes were characterized mainly by the gradual loss of basophilia and an increase in oocyte diameter. Vitellogenesis was marked mainly by the incorporation of yolk granules. Mature oocytes were defined by their migration from the nucleus to the micropyle. Postovulatory follicles and atresic oocytes were also observed. The reproductive phases were classified as: immature, early and final developing, spawning capable, regressing and regenerating. Therefore, the development of an understanding of cell modifications that occurs up to oogenesis is a basic step that is essential for the description of the reproductive biology of D. aequipinnatus, given the lack of information about the reproductive aspects of this species.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2018 

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References

Abascal, F. & Medina, A. (2005). Ultrastructure of oogenesis in the bluefin tuna, Thunnus thynnus. J. Morphol, 264, 149–60.CrossRefGoogle ScholarPubMed
Amorim, J.P.A. (2007). Foliculogênese e caracterização celular das classes reprodutivas em Pimelodus maculatus (Siluriformes: Pimelodidae). [Dissertation]. Botucatu, Universidade Estadual Paulista.Google Scholar
Andrade, R.F., Bazzoli, N., Rizzo, E. & Sato, Y. (2001). Continuous gametogenesis in the neotropical freshwater teleost, Bryconops affinis (Pisces: Characidae). Tissue Cell 5, 524–32.CrossRefGoogle Scholar
Arunachalam, M., Manickam, R., Manickam, C., Malaiammal, P. & Mayden, R. (2013). Natural history of zebrafish (Danio rerio) in India. Zebrafish 1, 114.CrossRefGoogle Scholar
Brown-Peterson, N.J., Wyanski, D.M., Saborido-Rey, F., Macewicz, B.J. & Lowerre-Barbieri, S.K. (2011). A standardized terminology for describing reproductive development in fishes. Mar. Coast. Fish. 3, 5270.CrossRefGoogle Scholar
Cassel, M., Camargo, M.P., Jesus, L.W.O. & Borella, M.I. (2017a). Involution processes of follicular atresia and post-ovulatory complex in a characid fish ovary: a study of apoptosis and autophagy pathways. J. Mol. Histol. 98, 243–57.CrossRefGoogle Scholar
Cassel, M., Chehade, C., Souza, G.B., Caneppele, D., Romagosa, E. & Borella, M. (2017b). Ovarian development and the reproductive profile of Astyanax altiparanae (Teleostei, Characidae) over one year: applications in fish farming. Theriogenology 98, 115.CrossRefGoogle ScholarPubMed
Çakici, Ö. & Üçüncü, S.İ. (2007). Oocyte development in the zebrafish, Danio rerio (Teleostei: Cyprinidae). Eur. J. Fish Aquat. Sci. 1–2, 137–41.Google Scholar
Çek, S., Bromage, N., Randall, C. & Rana, K. (2001). Oogenesis, hepatosomatic and gonadosomatic indexes, and sex ratio in Rosy Barb (Puntius conchonius). Turk. J. Fish. Aquat. Sci. 1, 3341.Google Scholar
Celius, T. & Walther, B.T. (1998). Oogenesis in Atlantic salmon (Salmo salar L.) occurs by zonagenesis preceding vitellogenesis in vivo and in vitro. J. Endocrinol. 158, 259–66.CrossRefGoogle ScholarPubMed
Connolly, M.H., Dutkosky, R.M., Heah, T.P., Sayker, G.S. & Henry, T.B. (2014). Temporal dynamics of oocyte growth and vitellogenin gene expression in zebrafish (Danio rerio). Zebrafish 11, 107–14.CrossRefGoogle ScholarPubMed
Eschmeyer, W. & Fong, J. (2017). Catalog of Fishes. Available at: http://researcharchive.calacademy.org/research/ichthyology/catalog/SpeciesByFamily.asp. Accessed 28 January 2017.Google Scholar
Fu, C.Z., Wu, J.H., Chen, J.K., Qu, Q.H. & Lei, G.C. (2003). Freshwater fish diversity in the Yangtze River basin in China: patterns, threats and conservation. Biodivers. Conserv. 12, 1649–85.CrossRefGoogle Scholar
Ganeco, L.N., Nakaghi, L.S.O., Urbinati, E.C., Neto, R.D. & Vasques, S.L.H. (2001). Análise morfológica do desenvolvimento ovocitário de pirancajuba, Brycon orbignyanus, durante o ciclo reprodutivo. Boletim do Instituto de Pesca 2, 131–8.Google Scholar
Glasser, F., Cauty, C., Mourot, B. & Breton, B. (2003). Disrupted sexual cycles in female grass carp (Ctenopharyngodon idella) raised in tropical conditions. Aquaculture 220, 857–68.CrossRefGoogle Scholar
Gonçalves, T.L., Bazzoli, N. & Brito, M.F.G. (2006). Gametogenesis and reproduction of the matrinxã Brycon orthotaenia (GÜNTHER, 1864) (PISCES: CHARACIDAE) in the São Francisco River, Minas Gerais, Brazil. Brazil. J. Biol. 66, 513–22.CrossRefGoogle Scholar
Grier, H.J. (2000). Ovarian germinal epithelium and folliculogenesis in the common snook Centropomus undecimalis (Teleostei: Centropomidae). J. Morphol. 243, 265–81.3.0.CO;2-I>CrossRefGoogle ScholarPubMed
Grier, H.J. (2012) Development of the follicle complex and oocyte staging in red drum, Sciaenops ocellatus Linnaeus, 1776 (Perciformes, Sciaenidae). J Morphol. 273, 801–29.CrossRefGoogle ScholarPubMed
Grier, H.J., Uribe-Aranzabal, M.C. & Parenti, L.R. (2007). Germinal epithelium, folliculogenesis, and postovulatory follicles in ovaries of rainbow trout, Oncorhynchus mykiss (Walbaum, 1792) (Teleostei, Protacanthopterygii, Salmoniformes). J. Morphol. 268, 293310.CrossRefGoogle ScholarPubMed
Honji, R.M., Vaz-dos-Santos, A.M. & Rossi-Wongtschowski, C.L.D.B. (2006). Identification of the stages of ovary maturation of the Argentine hake Merluccius hubbisi Marini, 1933 (Teleostei: Merlucciidae): advantages and disadvantages of the use of the macroscopic and microscopic scales. Neotrop. Ichthyol. 3, 329–37.CrossRefGoogle Scholar
Lele, Z. & Krone, P.H. (1996). The zebrafish as a model system in developmental, toxicological and transgenic research. Biotechnol. Adv. 1, 5772.CrossRefGoogle Scholar
Lima, R.V.A., Bernardino, G., Val-Sella, M.V., Fava-de-Moraes, F., Schemy, R.A. & Borella, M.I. (1991). Tecido germinativo ovariano e ciclo reprodutivo de pacus (Piaractus mesopotamicus HOLMBERG, 1887) mantidos em cativeiro. Boletim técnico Cepta. 1, 146.Google Scholar
Marques, D.K. S., Rosa, I.L. & Gurgel, H.C.B. (2000). Descrição histológica de gônadas de traíra Hoplias malabaricus (Bloch) (Osteichthyes, Erythrinidae) da barragem do rio Gramame, Alhandra, Paraíba, Brasil. Revista Brasileira de Zoologia. 3, 573–82.CrossRefGoogle Scholar
Martins, Y.S., Moura, D.F., Santos, G.B., Rizzo, E. & Bazzoli, N. (2010). Comparative folliculogenesis and spermatogenesis of four teleost fish from a reservoir in south-eastern Brazil. Acta Zool. 91, 466–73.CrossRefGoogle Scholar
Mazzoni, T.S., Grier, H.J. & Quagio-Grassiotto, I. (2010). Germline cysts and the formation of the germinal epithelium during female morphogenesis in Cyprinus carpio (Teleostei: Ostariophysi: Cypriniformes). Anat. Rec. 293, 1581–606.CrossRefGoogle ScholarPubMed
Mayden, R.L. (1991). New World Cyprinids. In Biology of Cyprinids (eds Winfield, I.J. & Nelson, J.S.), pp. 240–63. London: Chapman and Hall Ltd.Google Scholar
Morais, R.D.V.S., Thomé, R.G., Santos, H.B., Bazzoli, N. & Rizzo, E. (2016). Relationship between bcl-2, bax, beclin-1, and cathepsin-D proteins during postovulatory follicular regression in fish ovary. Theriogenology 85, 1118–31.CrossRefGoogle ScholarPubMed
Muñoz, M., Sabat, M., Mallol, S. & Casadevall, M. (2002). Gonadal structure and gametogenesis of Triglia lyra (Pisces: Triglidae). Zool. Stud. 41, 412–20.Google Scholar
Nelson, J.S. (1994). Fishes of the World, 3rd edn. New York: John Wiley and Sons, Inc., 624 pp.Google Scholar
Nelson, J.S. (2006). Fishes of the World. Hoboken: John Wiley, 601 pp.Google Scholar
Ohta, T., Iwamatsu, M., Tanaka, Y. & Yoshimoto, Y. (1990). Cortical alveolus breakdown in the eggs of the freshwater teleost Rhodeus ocellatus ocellatus. Anat. Rec. 4, 486–96.CrossRefGoogle Scholar
Patiño, R. & Sullivan, C.V. (2002). Ovarian follicle growth, maturation, and ovulation in teleost fish. Fish Physiol. Biochem. 26, 5770.CrossRefGoogle Scholar
Quagio-Grassiotto, I., Grier, H., Mazzoni, T.S., Nobrega, R.H. & Amorim, J.P.A. (2011). Activity of the ovarian germinal epithelium in the freshwater cattfish, Pimelodus maculatus (Teleostei: Ostariophysi: Siluriformes): germline cysts, follicle formation and oocyte development. J. Morphol. 272, 1290–306.CrossRefGoogle ScholarPubMed
Quagio-Grassiotto, I., Wilder, D.D. & Ishiba, R. (2013). Gametogênese de peixes: aspectos relevantes para o manejo reprodutivo. Revista Brasileira de Reprodução Animal 2, 181–91.Google Scholar
Quagio-Grassiotto, I., Wildner, D.D. & Guimarães-Bassoli, A.C.D. (2014). A cytochemical approach to describe oocyte development in the freshwater ostariophysan, Serrasalmus maculatus (Characiformes). Micron 60, 1828.CrossRefGoogle ScholarPubMed
Rodrigues, L.P., Querol, E. & Braccini, M.C. (2005). Descrição morfo-histológica do ovário de Acestrorhynchus pantaneiro (Menezes, 1992) (Teleostei, Characidae), em seus diferentes estádios de desenvolvimento, na bacia do rio Uruguai médio, Uruguaiana, RS. Biodiversidade Pampeana 3, 11–8.Google Scholar
Santos, H.B., Thomé, R.G., Arantes, F.P., Sato, Y., Bazzoli, N. & Rizzo, E. (2008). Ovarian follicular atresia is mediated by heterophagy, autophagy, and apoptosis in Prochilodus argenteus and Leporinus taeniatus (Teleostei: Characiformes). Theriogenology 70, 1449–60.CrossRefGoogle ScholarPubMed
Santos-Silva, A., Siqueira-Silva, D., Silveira-Ninhaus, A. & Silveira-Veríssimo, R. (2015). Oogenesis in Laetacara araguaiae (Ottoni and Costa, 2009) (Labriformes: Cichlidae). Zygote 24, 19.Google ScholarPubMed
Selman, K. & Wallace, R.A. (1989). Cellular aspects of oocyte growth in teleosts. Zool. Sci. 6, 211–31.Google Scholar
Shabanipour, N. & Heidari, B. (2004). A histological study of the zona radiata during late oocyte developmental stages in the Caspian sea Mugilid, Liza aurata (Risso, 1810). Braz. J. Morphol. Sci. 21, 37.Google Scholar
Shabanipour, N. & Hossayni, S.N. (2010). Histological and ultrastructural study of zona radiata in oocyte of common carp Cyprinus carpio (Linnaeus 1758). Micron 41. 877–81.CrossRefGoogle ScholarPubMed
Thomé, R.G., Domingos, F.F.T., Santos, H.B., Martinelli, P.M., Sato, Y., Rizzo, E. & Bazzoli, N. (2012). Apoptosis, cell proliferation and vitellogenesis during the folliculogenesis and follicular growth in teleost fish. Tissue Cell 44, 5462.CrossRefGoogle ScholarPubMed
Tyler, C.R. & Sumpter, J.P. (1996). Oocyte growth and development in teleosts. Rev. Fish Biol. Fish. 6, 287318.CrossRefGoogle Scholar
Üçüncü, S.I. & Çakici, Ö. (2009). Atresia and apoptosis in preovulatory follicles in the ovary of Danio rerio (zebrafish). Turk. J. Fish. Aquat. Sci. 9, 215–21.CrossRefGoogle Scholar
Varela, M.L., Ferreira, M.F., Da Cuna, R.H., Lo Nostro, F.L., Genovese, G. & Meijide, F.J. (2017). Dynamics of ovarian maturation throughout the reproductive cycle of the Neotropical cichlid fish Cichlasoma dimerus (Teleostei, Cichliformes). Can. J. Zool. 95, 485–98.CrossRefGoogle Scholar
Wallace, R.A. & Selman, K. (1981). Cellular and dynamic aspects of oocyte growth in teleosts. Am. Zool. 2, 325–43.CrossRefGoogle Scholar
West, G. (1990). Methods of assessing ovarian development in fishes: a review. Mar. Freshw. Res. 41, 199222.CrossRefGoogle Scholar
Wildner, D.D., Grier, H.J. & Quagio-Grassiotto, I. (2013). Female germ cell renewal during the annual reproductive cycle in Ostariophysians fish. Theriogenology 79, 709–24.CrossRefGoogle ScholarPubMed
Yön, N.D.K., Aytekin, Y. & Yuce, R. (2008). Ovary maturation stages and histologycal investigation of ovary of zebrafish (Danio rerio). Brazil. Arch. Biol. Technol. 3, 513–22.Google Scholar