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Spawning induction and embryonic development of Salminus hilarii (Characiformes: Characidae)

Published online by Cambridge University Press:  08 May 2020

Bruno Cavalheiro Araújo ,
Paulo Henrique Mello ,
Renata Guimarães Moreira ,
Alexandre Wagner Silva Hilsdorf ,
Victor Hugo Marques Open the ORCID record for Victor Hugo Marques [Opens in a new window]  and
Renato Massaaki Honji Open the ORCID record for Renato Massaaki Honji [Opens in a new window]
Bruno Cavalheiro Araújo
Affiliation:
Núcleo Integrado de Biotecnologia, Universidade de Mogi das Cruzes. Av. Dr. Cândido Xavier de Almeida Souza, 200, 08780-911, Mogi das Cruzes, SP, Brasil
Paulo Henrique Mello
Affiliation:
Centro de Aquicultura, Universidade Estadual Paulista ‘Júlio de Mesquita Filho’ (CAUNESP). Via de Acesso Prof. Paulo Donato Castellane, s/n, 14884-900, Jaboticabal, SP, Brasil
Renata Guimarães Moreira
Affiliation:
Departamento de Fisiologia, Instituto de Biociências, Universidade de São Paulo. Rua do Matão, Trav. 14, no. 321, 05508-090, São Paulo, SP, Brasil
Alexandre Wagner Silva Hilsdorf
Affiliation:
Núcleo Integrado de Biotecnologia, Universidade de Mogi das Cruzes. Av. Dr. Cândido Xavier de Almeida Souza, 200, 08780-911, Mogi das Cruzes, SP, Brasil
Victor Hugo Marques
Affiliation:
Departamento de Fisiologia, Instituto de Biociências, Universidade de São Paulo. Rua do Matão, Trav. 14, no. 321, 05508-090, São Paulo, SP, Brasil
Renato Massaaki Honji*
Affiliation:
Centro de Biologia Marinha, Universidade de São Paulo. Rodovia Manoel Hipólito do Rego, km. 131,5, 11612-109, São Sebastião, SP, Brasil
*
Author for correspondence: Renato Massaaki Honji. Centro de Biologia Marinha, Universidade de São Paulo. Rodovia Manoel Hipólito do Rego, km. 131,5, 11612-109, São Sebastião, SP, Brasil. E-mail: honjijp@usp.br
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Summary

The present study aimed to evaluate two different methods of artificial reproduction induction, and characterize the embryonic development of Salminus hilarii. Different than observed for other tropical fish species, artificial reproduction induction followed by hand-stripping of gametes was considered unfeasible for S. hilarii, as no gamete fertilization was observed. However, females that were induced and spawned naturally presented a fertilization rate of 65.64 ± 0.54%. With a mean temperature of 26.20 ± 0.90ºC it was possible to clearly distinguish a large perivitelline space at 14 min after fertilization (AF) and at 49 min AF more than 50% of the embryos presented two blastomeres, and these cleavages occurred until 1 h 54 min AF. The gastrula phase was characterized at 3 h 56 min AF, and blastopore closure was observed at 8 h 31 min AF. At 9 h 1 min, organogenesis started, with a clear distinction of the yolk mass, embryonic axis, cephalic and caudal regions; at 11 h 51 min AF the embryos already had advanced segmentation and a free tail. Total hatching occurred at 21 h 17 min and after opening the mouth, which occurred at 33 h 9 min, the larvae of S. hilarii presented a strong and characteristic cannibalism. This information can be considered fundamental to improving S. hilarii production in captivity and for collaboration with a conservation programme in the upper Tietê river basin.

Keywords

Artificial reproductionBrazilian riverEggsLarvaeTabarana
Type
Research Article
Information
Zygote , Volume 28 , Issue 5 , October 2020 , pp. 377 - 387
Copyright
© Cambridge University Press 2020

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References

Agostinho, AA, Gomes, LC, Suzuki, HI and Júlio, HF (2003). Migratory fish from the upper Paraná River Basin, Brazil. In Migratory fishes of South America: biology, fisheries and conservation status (eds Carolsfeld, J, Harvey, B, Ross, C and Baer, A), pp. 19–99. The World Bank and the International Development Research Center, Victoria: World Fisheries Trust.Google Scholar
Alexandre, JS, Ninhaus-Silveira, A, Veríssimo-Silveira, R, Buzollo, H, Senhorini, JA and Chaguri, MP (2009). Structural analysis of the embryonic development in Brycon cephalus (Günther, 1869). Zygote 18, 173–83.CrossRefGoogle Scholar
Andrade-Talmelli, EF, Kavamoto, ET, Romagosa, E and 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
Andrade-Talmelli, EF, Kavamoto, ET, Narahara, MY and Fenerich-Verani, N (2002). Reprodução induzida da piabanha, Brycon insignis (Steindachner, 1876), mantida em cativeiro. [Induced reproduction of the piabanha, Brycon insignis (Steindachner, 1876), kept in captivity.] Rev Bras Zootec 31, 803–11.CrossRefGoogle Scholar
Araújo, BC, Honji, RM, Mello, PH and Moreira, RG (2012). The influence of captive breeding on the fatty acid profiles of Salminus hilarii (Characiformes: Characidae) eggs and larvae. Aquac Int 20, 1161–81.CrossRefGoogle Scholar
Assembleia Legislativa do Estado de São Paulo (2008). Decreto estadual no. 53494–2008 de 02 de outubro de 2008. Diário Oficial do Estado de São Paulo. 118(187): Secretaria do Meio Ambiente. [State decree no. 53494–2008 of 2 October 2008. Official Gazette of the State of São Paulo. 118 (187): Secretariat for the Environment.]Google Scholar
Bagarinao, T (1986). Yolk resorption, onset of feeding and survival potential of larvae of three tropical marine fish species reared in the hatchery. Mar Biol 91, 449–59.CrossRefGoogle Scholar
Barón-Aguilar, CC, Rhody, NR, Brennan, NP, Main, KL, Peebles, EB and Muller-Karger, FE (2013). Influence of temperature on yolk resorption in common snook Centropomus undecimalis (Bloch, 1792) larvae. Aquac Res 46, 1679–87.CrossRefGoogle Scholar
Bonislawska, M, Formicki, K, Lorzelecka-Orkisz, A and Winnicki, A (2001). Fish egg size variability: biological significance. Electron J Pol Agric Univ 4, 1–12.Google Scholar
Bressan, PM, Kierulff, MCM and Sugieda, AM (2009). Fauna ameaçada de extinção no estado de São Paulo: Vertebrados. Governo do Estado de São Paulo, Fundação Parque Zoológico de São Paulo, Secretaria do Meio Ambiente, São Paulo. [Endangered fauna in the State of São Paulo: vertebrates. Government of São Paulo, Fundação Parque Zoológico and Secretariat of the Environment].Google Scholar
Buzollo, H, Veríssimo-Silveira, R, Oliveira-Almeida, IR, Alexandre, JS, Okuda, HT and Ninhaus-Silveira, A (2011). Structural analysis of the Pimelodus maculatus (Lacépèle, 1803) embryogenesis (Siluriformes: Pimelodidae). Neotrop Ichthyol 9, 601–16.CrossRefGoogle Scholar
Caneppele, D, Honji, RM, Hilsdorf, AWS and Moreira, RG (2009). Induced spawning of the endangered Neotropical species Steindachneridion parahybae (Siluriformes: Pimelodidae). Neotropic Ichthyol 7, 759–62.CrossRefGoogle Scholar
Cardoso, EL, Alves, MSD and Ferreira, RMA (1995). Embryogenesis of the neotropical freshwater Siluriformes Pseudoplatystoma corruscans. Aquat Living Resour 8, 343–6.CrossRefGoogle Scholar
Chalde, T, Fernández, DA, Cussac, VE and Somoza, GM (2011). The effect of rearing temperature in larval development of pejerrey, Odontesthes bonariensis – morphological indicators of development. Neotropic Ichthyol 9, 747–56.CrossRefGoogle Scholar
Coelho, GCZ, Costa, RS, Bashiyo-Silva, C, Souza, FMS, Ribeiro, DC, Senhorini, JA, Veríssimo-Silveira, R and Ninhaus-Silveira, A (2019). Characterization of the initial ontogeny of Leiarius marmoratus (Gill, 1870): larvae to juvenile. J Appl Ichthyol 35, 719–27.CrossRefGoogle Scholar
Faustino, F, Nakaghi, LSO and Neumann, E (2010a). Brycon gouldingi (Teleostei, Characidae): aspects of the embryonic development in a new fish species with aquaculture potential. Zygote 19, 351–63.CrossRefGoogle Scholar
Faustino, F, Nakaghi, LSO, Marques, C, Ganeco, LN and Makino, LC (2010b). Structural and ultrastructural characterization of the embryonic development of Pseudoplatystoma spp. hybrids. Int J Dev Biol 54, 723–30.CrossRefGoogle ScholarPubMed
Gilbert, SF (2003). Biologia do Desenvolvimento, Quinta edição. [Developmental Biology 5th edition.] Ribeirão Preto, FUNPEC.Google Scholar
Gomes, AD, Tolussi, CE, Boëchat, IG, Pompêo, MLM, Cortez, MPT, Honji, RM and Moreira, RG (2016). Fatty acid composition of tropical fish depends on reservoir trophic status and fish feeding habitat. Lipids 51, 1193–206.CrossRefGoogle Scholar
Honji, RM, Narcizo, AM, Borella, MI, Romagosa, E and Moreira, RG (2009). Patterns of oocyte development in natural habitat and captive Salminus hilarii Valenciennes, 1850 (Teleostei: Characidae). Fish Physiol Biochem 35, 109–23.CrossRefGoogle Scholar
Honji, RM, Mello, PH, Araújo, BC, Rodrigues-Filho, JA, Hilsdorf, AWS and Moreira, RG (2011). Influence of spawning procedure on gametes fertilization success in Salminus hilarii Valenciennes, 1850 (Teleostei: Characidae): implications for the conservation of this species. Neotropic Ichthyol 9, 363–70.CrossRefGoogle Scholar
Honji, RM, Tolussi, CE, Mello, PH, Caneppele, D and Moreira, RG (2012). Embryonic development and larval stages of Steindachneridion parahybae (Siluriformes: Pimelodidae) – implications for the conservation and rearing of this endangered neotropical species. Neotropic Ichthyiol 10, 313–27.CrossRefGoogle Scholar
Honji, RM, Nóbrega, RH, Pandolfi, M, Shimizu, A, Borella, MI and Moreira, RG (2013). Immunohistochemical study of pituitary cells in wild and captive Salminus hilarii (Characiformes: Characidae) females during the annual reproductive cycle. Springerplus. 2, 460–74.CrossRefGoogle ScholarPubMed
Ing, NS and Chew, HH (2015). Nutritional transition period in early larvae Clarias gariepinus. Malaysian J Anal Sci 19, 1120–30.Google Scholar
Jaroszewska, M and Dabrowski, K (2011). Utilization of yolk: transition from endogenous to exogenous nutrition in fish. In Larval Fish Nutrition (ed. Holt, GJ), pp. 183–218. John Wiley & Sons, Inc.CrossRefGoogle Scholar
Jaworski, A and Kamler, E (2002). Development of a bioenergetics model for fish embryos and larvae during the yolk feeding period. J Fish Biol 60, 785–809.CrossRefGoogle Scholar
Johns, DM and Howell, WH (1980). Yolk utilization in summer flounder (Paralichthys dentatus) embryos and larvae reared at two temperatures. Mar Ecol Prog Ser 2, 1–8.CrossRefGoogle Scholar
Kennedy, J, Geffen, AJ and Nash, RDM (2007). Maternal influences on egg and larval characteristics of plaice (Pleuronected platessa L.). J Sea Res 58, 65–77.CrossRefGoogle Scholar
Klimogianni, A, Kalanji, M, Pyrenis, G, Zouliote, A and Trakos, G (2011). Ontogeny of embryonic and yolk-sac larval stage of the sparid sharpsnout sea bream (Diplodus puntazzo Cetti, 1777). J Fish Aquat Sci 6, 62–73.Google Scholar
Korzelecka-Orkisz, AK, Szalast, Z, Pawlos, D, Smaruj, S, Tañski, A, Szulz, J and Formicki, K (2012). Early ontogenesis of the angelfish, Pterophyllum scalare Schultze, 1823 (Cichlidae). Neotropic Ichthyol 10, 567–76.CrossRefGoogle Scholar
Leal, E, Muñoz, X, Moyano, G, Bernal, C and Aranis, A (2017). A first experience of Patagonian sprat Sprattus fuegensis spawning in captivity: adult acclimation, egg and larval measurements. Rev Biol Mar Ocean 52, 641–5.CrossRefGoogle Scholar
Luz, RK, Reynalte-Tataje, DA, Ferreira, AA and Zaniboni-Filho, E (2001). Desenvolvimento embrionário e estágios larvais do Mandi-Amarelo Pimelodus maculatus. [Embryonic development and larval stages of the Yellow Mandi Pimelodus maculatus.] Bol Inst Pesca 27, 49–55.Google Scholar
Maria, AN, Ninhaus-Silveira, A, Orfão, LH and Viveiros, ATM (2017). Embryonic development and larval growth of Brycon nattereri Günther, 1864 (Characidae) and its implications for captive rearing. Zygote 25, 711–8.CrossRefGoogle ScholarPubMed
Marques, C, Nakaghi, LSO, Faustino, F, Ganeco, LN and Senhorini, JA (2008). Observation of the embryonic development in Pseudoplatystoma coruscans (Siluriformes: Pimelodidae) under light and scanning electron microscopy. Zygote 16, 333–42.CrossRefGoogle ScholarPubMed
Mello, PH, Araújo, BC, Campos, MF, Rodrigues-Filho, JA, Garcia, CEO and Moreira, RG (2018). Embryonic and larval development and fatty-acid profile of Epinephelus marginatus spawned in captivity: tools applied to captive rearing. J Fish Biol 92, 1126–48.CrossRefGoogle ScholarPubMed
Morrison, CM, Miyake, T and Wright, JR Jr (2001). Histological study of the development of the embryo and early larva of Oreochromis niloticus (Pisces; Cichlidae). J Morphol 247, 172–95.3.0.CO;2-H>CrossRefGoogle Scholar
Mylonas, CC, Fostier, A and Zanuy, S (2010). Broodstock management and hormonal manipulations of reproduction. Gen Comp Endocrinol 165, 516–34.CrossRefGoogle ScholarPubMed
Nakaghi, LSO, Marques, C, Faustino, F, Ganeco, LN and Senhorini, JA (2006). Desenvolvimento embrionário do dourado (Salminus brasiliensis) por meio de microscopia eletrônica de varredura. [Embryonic development of dorado (Salminus brasiliensis) by means of scanning electron microscopy.] Bol Tec CEPTA 19, 9–19.Google Scholar
Nakatani, K, Agostinho, AA, Baumgartner, G, Bialtzki, A, Sanches, PV, Makrakis, MC and Pavanelli, CS (2001). Ovos e larvas de peixes de água doce: desenvolvimento e identificação. [Freshwater fish eggs and larvae: development and identification.] Maringá, Paraná, EDUEM.Google Scholar
Nakauth, ACSS, Villacorta-Correa, MA, Figueiredo, MR, Bernardino, G and França, JM (2016). Embryonic and larval development of Brycon amazonicus (Spix & Agassiz, 1829). Braz J Biol 76, 109–66.CrossRefGoogle Scholar
Narahara, MY, Andrade-Talmelli, EF, Kavamoto, ET and Godinho, HM (2002). Reprodução induzida da pirapitinga-do-sul, Brycon opalinus (Cuvier, 1819), mantida em condições de confinamento. [Induced reproduction of the southern pirapitinga, Brycon opalinus (Cuvier, 1819), kept in confinement conditions.] Rev Bras Zootec 31, 1070–5.CrossRefGoogle Scholar
Ninhaus-Silveira, A, Foresti, F and Azevedo, A (2006). Structural and ultrastructural analysis of embryonic development of Prochilodus lineatus (Valenciennes, 1836) (Characiforme, Prochilodontidae). Zygote 14, 217–29.CrossRefGoogle Scholar
Reynalte-Tataje, D, Zaniboni-Filho, E and Esquivel, JR (2004). Embryonic and larvae development of piracanjuba, Brycon orbignyanus Valenciennes, 1849 (Pisces, Characidae). Acta Sci 26, 67–71.Google Scholar
Richards, WJ (2006). Early stages of Atlantic Fishes. An identification guide for the Western Central North Atlantic. Taylor & Francis.Google Scholar
Romagosa, E, Narahara, MY and Fenerich-Verani, N (2001). Stages of embryonic development of the ‘matrinxã’, Brycon cephalus (Pisces, Characidae). Bol Inst Pesca 27, 29–32.Google Scholar
Rønnestad, I, Finn, RN, Groot, EP and Fyhn, HJ (1992). Utilization of free amino acids related to energy metabolism of developing eggs and larvae of lemon sole Microstomus kitt reared in the laboratory. Mar Ecol Prog Ser 88, 195–205.CrossRefGoogle Scholar
Silva, FSD, Deus, JRM and Hilsdorf, AWS (2006). The upper reached ichthyofauna of the Tietê River, São Paulo, Brazil: aspects of their diversity and conservation. Biodivers Conserv 15, 3569–77.CrossRefGoogle Scholar
Silva, JVD, Hallerman, EM, Orfão, LH and Hilsdorf, AWS (2015). Genetic structuring of Salminus hilarii Valenciennes, 1850 (Teleostei: Characiformes) in the rio Paraná basin as revealed by microsatellite and mitochondrial DNA markers. Neotrop Ichthyol 13, 547–56.CrossRefGoogle Scholar
Sulaeman, and Fotedar, R (2017). Yolk utilization and growth during the early larval life of the Silver Perch, Bidyanus bidyanus (Mitchell, 1838). Int Aqua Res 9, 107–16.CrossRefGoogle Scholar
Vazzoler, AEAM (1981). Manual de métodos para estudos biológicos de populações de peixes: reprodução e crescimento. [Manual of methods for biological studies of fish populations: reproduction and growth.] Brasília, CNPq.Google Scholar
Vazzoler, AEAM (1996). Biologia da reprodução de peixes teleósteos: teoria e prática. [Biology of teleost fish reproduction: theory and practice.] Maringá, EDUEM.Google Scholar
Vega-Orellana, OM, Fracalossi, DM and Sugai, JK (2006). Dourado (Salminus brasiliensis) larviculture: weaning and ontogenetic development of digestive proteinases. Aquaculture 252, 484–93.CrossRefGoogle Scholar
Weingartner, M and Zaniboni-Filho, E (2005). Dourado. In Espécies Nativas para piscicultura no Brasil [Native species for fish farming in Brazil] (eds Baldisseroto, B and Gomes, LC), pp. 257–86. Santa Maria, Rio Grande do Sul, Ed. UFSM.Google Scholar
Yufera, M and Darias, MJ (2007). The onset of exogenous feeding in marine fish larvae. Aquaculture 268, 53–63.CrossRefGoogle Scholar
Zanandrea, ACV, Weingartner, M and Zaniboni-Filho, E (2016). Induced reproduction of dourado (Salminus brasiliensis): fertilization with sperm cryopreserved in ACP®-104. Acta Sci 38, 17–22.Google Scholar