Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-26T05:47:20.986Z Has data issue: false hasContentIssue false

The effect of temperature on the initial development of Brycon amazonicus Spix & Agassiz, 1829 as tool for micromanipulation of embryos

Published online by Cambridge University Press:  20 September 2017

Regiane Cristina da Silva*
Affiliation:
UNESP's Aquaculture Centre (CAUNESP), UNESP – São Paulo State University, Campus Jaboticabal-SP. Via de Acesso Prof. Paulo Donato Castellane s/n, CEP 14884-900, Jaboticabal, SPBrazil.
Matheus Pereira dos Santos
Affiliation:
UNESP's Aquaculture Centre (CAUNESP), UNESP – São Paulo State University, Campus Jaboticabal-SP. Via de Acesso Prof. Paulo Donato Castellane s/n, CEP 14884-900, Jaboticabal, SP, Brazil.
José Augusto Senhorini
Affiliation:
Fish Biotechnology Laboratory, National Centre for Research and Continental Fish Conservation, Chico Mendes Institute of Biodiversity Conservation (CEPTA/ICMBio), Rodovia Pref. Euberto Nemesio Pereira de Godoy, Km 6,5, CEP 13630-970. Pirassununga-SP, Brazil.
Maria do Carmo Faria Paes
Affiliation:
Laboratory Animal Histology and Embryology, Department of Animal Morphology and Physiology, UNESP- São Paulo State University, Campus Jaboticabal-SP. Via de Acesso Prof. Paulo Donato Castellane s/n, CEP 14884-900 Jaboticabal, SP, Brazil.
Fernanda Nogueira Valentin
Affiliation:
UNESP's Aquaculture Centre (CAUNESP), UNESP – São Paulo State University, Campus Jaboticabal-SP. Via de Acesso Prof. Paulo Donato Castellane s/n, CEP 14884-900, Jaboticabal, SP, Brazil.
Takafumi Fujimoto
Affiliation:
Faculty of Fisheries Sciences, Hokkaido University, 3-1-1 Minato-cho, 041-8611 Hakodate, Japan.
Nivaldo Ferreira do Nascimento
Affiliation:
UNESP's Aquaculture Centre (CAUNESP), UNESP – São Paulo State University, Campus Jaboticabal-SP. Via de Acesso Prof. Paulo Donato Castellane s/n, CEP 14884-900, Jaboticabal, SP, Brazil.
George Shigueki Yasui
Affiliation:
Fish Biotechnology Laboratory, National Centre for Research and Continental Fish Conservation, Chico Mendes Institute of Biodiversity Conservation (CEPTA/ICMBio), Rodovia Pref. Euberto Nemesio Pereira de Godoy, Km 6,5, CEP 13630-970. Pirassununga-SP, Brazil.
Laura Satiko Okada Nakaghi
Affiliation:
UNESP's Aquaculture Centre (CAUNESP), UNESP – São Paulo State University, Campus Jaboticabal-SP. Via de Acesso Prof. Paulo Donato Castellane s/n, CEP 14884-900, Jaboticabal, SP, Brazil. Laboratory Animal Histology and Embryology, Department of Animal Morphology and Physiology, UNESP- São Paulo State University, Campus Jaboticabal-SP. Via de Acesso Prof. Paulo Donato Castellane s/n, CEP 14884-900 Jaboticabal, SP, Brazil.
*
All correspondence to: Regiane Cristina da Silva. UNESP's Aquaculture Centre (CAUNESP), UNESP – São Paulo State University, Campus Jaboticabal-SP. Via de Acesso Prof. Paulo Donato Castellane s/n, CEP 14884-900, Jaboticabal, SPBrazil. E-mail: regianesilva_bio@yahoo.com.br

Summary

Primordial germ cell (PGC) transplant is a promising tool in aquaculture; however, successful use of this technique requires in depth knowledge of the early stages of embryo and larval development. The aim of this study was to analyse the effect of different temperatures (22, 26, and 30°C) on the early development of B. amazonicus. The newly fertilized eggs were distributed into tanks with controlled temperature and oxygenation. Samples were collected at pre-established times and analysed under light and fluorescence microscopy. Temperature influenced the speed and duration of each stage of early development, including hatching time. The highest pronuclei fusion rate was observed 8 min post-fertilization (mpf) at 22 and 26°C, and 6 mpf at 30°C. The duration of the 512–1000 blastomeres phase during in the blastocyst stage was 1 h 30 min at 22°C, and 25 min at 26 and 30°C. Hatching occurred at 24 h 30 mpf at 22°C, 16 h post-fertilization (hpf) at 26°C, and 11 h 30 mpf at 30°C. The rate of morphologically normal larvae was 88.34% at 22°C, 90.49% at 26°C, and 73% at 30°C. Malformations of the head, yolk sac, heart, and tail were observed in all temperatures. Nevertheless, B. amazonicus embryos were able to develop satisfactory in all three temperatures tested. These results enable embryo manipulation at different temperatures to optimize the micromanipulation time of embryos and larvae for biotechnological studies.

Type
Research Article
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

Abdel, I., Abellán, E., López-Albors, O., Valdés, P., Nortes, M. & García-Alcázar, A. (2004). Abnormalities in the juvenile stage of sea bass (Dicentrarchus labrax L.) reared at different temperatures: types, prevalence and effect on growth. Aquac. Int. 12, 523–38.Google Scholar
Alberts, B., Johnson, A., Lewis, J., Raff, M., Roberts, K. & Walter, P. (2004). Biologia Molecular da Célula, Artmed, Porto Alegre.Google Scholar
Alexandre, J. S., Ninhaus-Silveira, A., Veríssimo-Silveira, R., Buzollo, H., Senhorini, J.A. & Chaguri, M.P. (2009). Structural analysis of the embryonic development in Brycon cephalus (Gunther, 1869). Zygote 18, 173–83.CrossRefGoogle ScholarPubMed
Andéol, Y. (1994). Early transcription in different animal species: implication for transition from maternal to zygotic control in development. Roux Arch. Dev. Biol. 204, 310.Google 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). Boletim do Instituto de Pesca 27, 21–8.Google Scholar
Arakawa, T., Kanno, Y., Akiyama, N., Kitano, T., Nakatsuji, N. & Nakatsuji, T. (1999). Stages of embryonic development of the ice goby (shiro-uo), Leucopsarion petersii. Zoo. Sci. 16, 761–73.CrossRefGoogle Scholar
Bermudes, M. & Ritar, A.J. (1999). Effects of temperature on the embryonic development of the striped trumpeter (Latris lineata Bloch and Schneider, 1801). Aquaculture 176, 245–55.Google Scholar
Camargo, A.C. S., Zaiden, S.F. & Urbinati, E.C. (2008). Desenvolvimento gonadal de fêmeas de matrinxã, Brycon amazonicus, submetidas a restrição alimentar. Ciência Rural 38, 1105–10.Google Scholar
Faustino, F., Makino, L. C., Neumann, E. & Nakaghi, L.S.O. (2015). Morphological and morphometric aspects of early life stagesof piabanha Brycon gouldingi (Characidae). J. Fish Biol., 86, 1491–506.Google Scholar
Faustino, F., Nakaghi, L.S. O., Marques, C., Ganeco, L.N. & Makino, L.C. (2010). Structural and ultrastructural characterization of the embryonic development of Pseudoplatystoma spp. hybrids. Int. J. Dev. Biol., 54, 723–30.CrossRefGoogle ScholarPubMed
Faustino, F., Nakaghi, L.S.O. & Neumann, E. (2011). Brycon gouldingi (Teleostei, Characidae): aspects of the embryonic development in a new fish species with aquaculture potential. Zygote 19, 351–63.Google Scholar
Fraser, T.W. K., Fleming, M. S., Poppe, T. T., Hansen, T. & Fjelldal, P.G. (2014). The effect of ploidy and incubation temperature on survival and the prevalence of aplasia of the septum transversum in Atlantic salmon, Salmo salar L. J. Fish Dis. 37, 189200.CrossRefGoogle ScholarPubMed
Fujimoto, T., Kataoka, T., Otani, S., Saito, T., Aita, T., Yamaha, E. & Arai, K. (2004). Embryonic stages from cleavage to gastrula in the loach Misgurnus anguillicaudatus . Zoo. Sci. 21, 747–55.Google Scholar
Fujimoto, T., Kataoka, T., Sakao, S., Saito, T., Yamaha, E. & Arai, K. (2006). Dev. Stages and Germ Cell Lineage of the Loach (Misgurnus anguillicaudatus). Zoo. Sci. 23, 977–89.Google Scholar
Fukuda, Y., Akematsu, T., Attiq, R., Tada, C., Nakai, Y. & Pearlman, R.E. (2015). Role of the Cytosolic Heat Shock Protein 70 Ssa5 in the Ciliate Protozoan Tetrahymena thermophila . J. Eukaryot. Microbiol. 62, 481–93.Google Scholar
Gomes, L.C. & Urbinati, E.C. (2005). Matrinxã (Brycon amazonicus). In Espécies Nativas para Piscicultura no Brasil (ed. UFSM) Santa Maria, pp. 149–64.Google Scholar
Gomes, R. Z., Sato, Y., Rizzo, E. & Bazzoli, N. (2013). Early development of Brycon orthotaenia (Pisces: Characidae). Zygote 21, 1120.Google Scholar
Gomez, C. & Pourquié, O. (2009). Dev. control of segment numbers in vertebrates. J. Exp. Zool. B: Mol. Dev. Evol. 312, 533–44.Google Scholar
Hansen, T.K. & Falk‐Petersen, I.B. (2002). Growth and survival of first-feeding spotted wolffish (Anarhichas minor Olafsen) at various temperature regimes. Aquac Res. 33, 1119–27.Google Scholar
Howes, G. (1982). Review of the genus Brycon (Teleostei: Characoidei). Bull. Br. Mus. (Nat. Hist.) Zool. 43, 147.Google Scholar
Isaú, Z. A., Rizzo, E., Amaral, T. B., Mourad, N. & Viveiros, A. (2013). Structural analysis of oocytes, post-fertilization events and embryonic development of the Brazilian endangered teleost Brycon insignis (Characiformes). Zygote 21, 8594.CrossRefGoogle ScholarPubMed
Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B. & Schilling, T.F. (1995). Stages of embryonic development of the zebrafish. Dev. Dynam. 203, 253310.Google Scholar
Lima, F.C.T. & Castro, R.M.C. (2000). Brycon vermelha, a new species of characid fish from the Rio Mucuri, a coastal river of eastern Brazil (Ostariophysi: Characiformes). Ichthyol. Explor. Freshw. 11, 155–62.Google Scholar
Linhartova, Z., Saito, T. & Psenicka, M. (2014). Embryogenesis, visualization and migration of primordial germ cells in tench (Tinca tinca). J. Appl. Ichthyol. 30, 2939.Google Scholar
Martell, D. J., Kieffer, J.D. & Trippel, E.A. (2005). Effects of temperature during early life history on embryonic and larval development and growth in haddock. J. Fish Biol., 66, 1558–75.Google Scholar
Melamed, P., Gong, Z., Fletcher, G. & Hew, C.L. (2002). The potential effect of modern biotechnology on fish aquaculture. Aquaculture 204, 255–69.Google Scholar
Molina-Arias, A. (2006). Desarrollo larval de Brycon guatemalensis (Regan, 1908) (Pisces: Characidae). Brenesia 66, 31–6.Google Scholar
Nakagawa, M., Kobayashi, T. & Ueno, K. (2002). Production of germline chimera in loach (Misgurnus anguillicaudatus) and proposal of new method for preservation of endangered fish species. J. Exp. Zool., 293, 624–31.Google Scholar
Nakaghi, L.S. O., Neumann, E., Faustino, F., Mendes, J.M.R. & Braga, F.M. (2013). Moments of induced spawning and embryonic development of Brycon amazonicus (Teleostei, Characidae). Zygote 22, 549–57.Google Scholar
Nakatani, K., Agostinho, A. A., Baumgartner, G., Bialetzki, A., Sanches, P.V. & Cavicchioli, M. (2001). Ovos e larvas de Peixes de Água Doce: Desenvolvimento e Manual de identificação, Eduem/Nupélia, Maringá.Google Scholar
Nakauth, A.C.S. S., Villacorta-Correa, M. A., Chim Figueiredo, M.R. & Bernardino, G. (2015). Desenvolvimento Embrionário e larval do Brycon amazonicus (GUNTER, 1869). IGAPÓ-Revista de Educação Ciência e Tecnologia do IFAM, 5.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.Google Scholar
Nogueira, L. B., Godinho, A.L. & Godinho, H.P. (2014). Early development and allometric growth in hatchery-reared characin Brycon orbignyanus . Aquac Res., 45, 1004–11.Google Scholar
Oliveira, F. G., Bialetzki, A., Gomes, L. C., Santin, M. & Taguti, T.L. (2012). Larval development of Brycon hilarii (Characiformes, Characidae). Iheringia. Série Zoologia 102, 6270.Google Scholar
Pankhurst, N.W. & Munday, P.L. (2011). Effects of climate change on fish reproduction and early life history stages. Mar. Freshw. Res., 62, 1015–26.CrossRefGoogle Scholar
Pereira-Santos, M., Yasui, G. S., Xavier, P.L. P., Admov, N.S. M., Nascimento, N. F., Fujimoto, T., Senhorini, J.A. & Nakaghi, L.S.O. (2016). Morphology of gametes, post-fertilization events and the effect of temperature on the embryonic development of Astyanax altiparanae (Teleostei, Characidae). Zygote 1–3.Google Scholar
Reynalte-Tataje, D., Zaniboni-Filho, E. & Esquivel, J.R. (2004). Embryonic and larvae development of piracanjuba, Brycon orbignyanus Valenciennes, 1849 (Pisces, Characidae). Acta Scientiarum 26, 5.Google Scholar
Rodrigues-Galdino, A. M., Maiolino, C. V., Forgati, M., Donatti, L., Mikos, J. D., Carneiro, P.C.F. & Rios, F.S.A. (2009). Dev. of the neotropical catfish Rhamdia quelen (Siluriformes, Heptapteridae) incubated in different temperature regimes. Zygote 18, 131–44.Google Scholar
Romagosa, E., Narahara, M.Y. & Fenerich-Verani, N. (2001). Stages of embryonic development of the’ Matrinxã’, Brycon cephalus (Pisces, Characidae). Boletim do Instituto de Pesca, 27, 2732.Google Scholar
Uji, S., Suzuki, T., Iwasaki, T., Teruya, K., Hirasawa, K., Shirakashi, M., Onoue, S., Yamashita, Y., Tsuji, M. & Tsuchihashi, Y. (2014). Effect of temperature, hypoxia and disinfection with ozonated seawater during somatogenesis on muscular development of the trunk in larval seven-band grouper, Epinephelus septemfasciatus Aquac Res., 46, 19.Google Scholar
Zhang, J., Sun, M., Zhou, L., Li, Z., Liu, Z., Li, X.-Y., Liu, X.-L., Liu, W. & Gui, J.-F. (2015) Meiosis completion and various sperm responses lead to unisexual and sexual reproduction modes in one clone of polyploid Carassius gibelio . Sci Rep. 5, 114.Google Scholar