Dynamics of testicular maturation during the reproductive cycle of Salminus hilarii (Teleostei, Characidae) in a natural habitat.
DOI:
https://doi.org/10.7594/revbio.19.01.04Keywords:
tabarana, reproduction, estradiol, testosterone, 11-ketotestosteroneAbstract
The objective was to describe the morphophysiological changes of Salminus hilarii testis during the annual reproductive cycle. The animals were collected in the Alto Tietê River Basin between Salesópolis and Biritiba Mirim cities (SP). Macro/microscopic analyzes of the testes allowed the classification of three stages (prespermatogenic, spermatogenic and regression) and six cell types (spermatogonia, spermatocytes, spermatids, spermatozoa, Sertoli and Leydig cells). The plasma concentration of estrogen/progestogen did not change during the reproductive cycle. However, androgens, testosterone and 11-ketotestosterone increased progressively with testicular maturation (continuous germ-to-discontinuous epithelial changes) and concomitantly with increased gonadosomatic index. These morphophysiological results suggest that the reproductive period occurs between the months of September to February.
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References
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Andrade DR, Godinho AL, Godinho HP, Shimoda E. 2006. Biologia reprodutiva da tabarana, Salminus hilarii (Osteichthyes, Characidae) na represa de três Marias, MG. Rev. Bras. Med. Vet. 28(1): 26-32. Doi: 10.4322/rbcv.2014.359.
Baldisserotto B, Gomes LC. 2005. Espécies nativas para piscicultura no Brasil. Santa Maria, Rio Grande do Sul, 1Ed. UFSM. 470p.
Behmer AO, Tolosa EMC, Neto AGF. 1976. Manual de técnicas para histologia normal e patológica. EDART. São Paulo. Livraria Editora Ltda. 239p.
Birba A, Ramallo MR, Lo Nostro FL, Moreira RG, Pandolfi M. 2015. Reproductive and parental care physiology of Cichlasoma dimerus males. Gen. Comp. Endocrinol. 221: 193-200. Doi: 10.1016/j.ygcen.2015.02.004.
Camargo C. 2007. Efeitos do bloqueio da migração reprodutiva nas reservas metabólicas da tabarana Salminus hilarii (Characiformes: Characidae). Dissertação. Universidade de Mogi das Cruzes. 65p.
Godoy MP. 1975. Peixes do Brasil – Sub-ordem Characoidei. Bacia do Rio Mogi-Guaçu, Piracicaba. Editora: Franciscana. 4vol. 398p.
Grier HJ. 1993. Comparative organization of Sertoli cells including the Sertoli barrier. In: Russel LD, Griswald MD (eds) The Sertoli Cell. Clearwater: Cache River Press. p703-739.
Honji RM, Mello PH, Araújo BC, Rodrigues-Filho JA, Hilsdorf AW, Moreira RG. 2011a. Influence of spawning procedure in fertilization success in Salminus hilarii Valenciennes, 1850 (Teleostei: Characidae): Implications for conservation this species. Neotropic. Ichthyol. 9: 363-370. Doi: 10.1590/S1679-62252011005000012.
Honji RM, Narcizo AM, Borella MI, Romagosa E, Moreira RG. 2009. Patterns of oocyte development in natural habitat and captive Salminus hilarii Valenciennes, 1850 (Teleostei: Characidae). Fish Physiol. Biochem. 35: 109-123. Doi: 10.1007/s10695-008-9239-9.
Honji RM, Caneppele D, Pandolfi M, Lo Nostro FL, Moreira RG. 2011b. The brain-pituitary axis structure in captivity reared females of Steindachneridion parahybae (Siluriformes). In: 9th International Symposium on Reproductive Physiology of Fish. Cochin, India. 4: 30-31.
Honji RM, Nóbrega RH, Pandolfi M, Shimizu A, Borella MI, Moreira RG. 2013. Immunohistochemical study of pituitary cells in wild and captive Salminus hilarii (Characiformes: Characidae) females during the annual reproductive cycle. SpringerPlus. 2: 460-474. Doi: 10.1186/2193-1801-2-460.
Lange IG, Hartel A, Meyer HHD. 2003. Evolution of oestrogen functions in vertebrates. J. Steroid Biochem. Mol. Biol. 83: 219-226. Doi: 10.1016/S0960-0760(02)00225-X.
Levavi-Sivan B, Bogerd J, Mañanós EL, Gómez A, Lareyre JJ. 2010. Perspectives on fish gonadotropins and their receptors. Gen. Comp. Endocrinol. 165: 412-437. Doi: 10.1016/j.ygcen.2009.07.019.
Lima FCT, Britski HA. 2007. Salminus fransciscanus, a new species from the Rio São Francisco Basin, Brazil (Ostariophysi: Characiformes: Characidae). Neotrop. Ichthyol. 5(3): 237-244. Doi: 10.1590/S1679-62252007000300001.
Marceniuk PA, Hilsdorf AWS. 2010. Peixes das cabeceiras do rio Tietê e Parque das Neblinas. 1. ed. Bauru: Canal 6. 157p.
Mennuet A, Adrio F, Kah O, Pakdel F. 2005. Regulation and function of estrogen receptors: comparative aspects. In: Melamed P, Sherwood N (eds) Hormones and their receptors in fish reproduction. Molecular aspects of fish and marine biology. vol 4. World Scientific. p.224-253.
Moreira RG, Honji RM, Melo RG, Narcizo AM, Amaral JS, Araújo RC, Hilsdorf AWS. 2015. The involvement of gonadotropins and gonadal steroids in the ovulatory dysfunction of the potamodromous Salminus hilarii (Teleostei: Characidae) in captivity. Fish Physiol. Biochem. 41(6): 1435-1447. Doi: 10.1007/s10695-015-0097-y.
Mylonas CC, Fostier A, Zanuy S. 2010. Broodstock management and hormonal manipulations of fish reproduction. Gen. Comp. Endocrinol. 165: 516-534. Doi: 10.1016/j.ygcen.2009.03.007.
Parenti LR, Grier HJ. 2004. Evolution and phylogeny of gonadal morphology in bony fishes. Int. Comp. Biol. 44: 333-348. Doi: 10.1093/icb/44.5.333.
Porto-Foresti F, Castilho-Almeida RB, Foresti F. 2005. Biologia e criação do lambari-do-rabo-amarelo (Astyanax altiparanae). In: Baldisserotto B, Gomes LC. (Org). Espécies nativas para piscicultura no Brasil. 1Editora UFSM. Santa Maria. p.105-120.
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.
Sato Y, Fenerich-Verani N, Nuñer APO, Godinho HP, Verani JR. 2003. Padrões reprodutivos de peixes da bacia do São Francisco. In: Godinho HP, Godinho AL. (Org). Águas, peixes e pescadores do São Francisco das Minas Gerais. Belo Horizonte. PUC-Minas. p.229-274.
Schulz RW, França LR, Lareyre J, LeGac F, Chiarini-Garcia H, Nóbrega RH, Miura T. 2010. Spermatogenesis in fish. Gen. Comp. Endocrinol. 165: 390-411. Doi: 10.1016/j.ygcen.2009.02.013.
Silva FSD, Deus JRM, Hilsdorf AWS. 2006. The upper reached ichthyofauna of the Tietê River, São Paulo, Brazil: aspects of their diversity and conservation. Biodivers. Conserv. 15: 3569-3577. Doi: 10.1007/s10531-004-1460-y.
Sink TD, Lockmann RT, Fecteau KA. 2008. Validation, use, and disadvantages of enzyme-linked immunosorbent assay kits for detection of cortisol in channel catfish, largemouth bass, red pacu, and golden shiners. Fish Physiol. Biochem. 34: 95–101. Doi: 10.1007/s10695-007-9150-9.
Takahashi ELH. 2006. Ciclo reprodutivo da tabarana Salminus hilarii (Valenciennes, 1849) (Characidae, Salmininae) na região do baixo Rio Sorocaba, SP. Dissertação. Universidade Estadual Paulista. Centro de Aquicultura. Jaboticabal. 58p.
Tubbs C, Thomas P. 2008. Functional characteristics of membrane progestin receptor alpha (mPRalpha) subtypes: a review with new data showing mPRalpha expression in seatrout sperm and its association with sperm motility. Steroids. 73: 935–941. Doi: 10.1016/j.steroids.2007.12.022.
Vazzoler AEAM. 1996. Biologia da reprodução de peixes teleósteos: teoria e prática. EDUEM, Maringá. 169p.
Villares-Junior GA, Goiten R. 2015. Variations of Salminus hilarii diet (Ostariophysi, Characidae): seasonal and ontogenetic effects. Braz. J. Biol. 75: 574-580. Doi: 10.1590/1519-6984.17213.
Villares-Junior GA, Goiten R. 2016. Morphological aspects in the ontogeny of Salminus hilarii Valenciennes, 1850 (Ostaryophysi: Characidae). Braz. J. Biol. 76: 905-911. Doi: 10.1590/1519-6984.04315.
Villares-Junior GA, Gomiero LM, Goiten R. 2007. Relação peso-comprimento e fator de condição de Salminus hilarii Valenciennes 1850 (Osteichthyes, Characidae) em um trecho da Bacia do Rio Sorocaba, Estado de São Paulo, Brasil. Acta Sci. Biol. Sci 29(4): 407-412. Doi: 10.4025/actascibiolsci.v29i4.884.
von Ihering R. 1929. Da vida dos peixes. Ensaios e scenas de pescarias. Companhia Melhoramentos de São Paulo. Editora Proprietária, 150p.
Weingartner M, Zaniboni-Filho E. 2005. Dourado. In: Baldiserotto B, Gomes LC. (Org). Espécies nativas para a piscicultura no Brasil. Editora UFSM. Santa Maria. p.257-281.
Young G, Kusakabe M, Nakamura I. 2005. Gonadal steroidogenesis in teleost fish. In: Melamed P, Sherwood N. (eds). Hormones and their receptors in fish reproduction. Molecular aspects of fish and marine biology. vol 4. World Scientific. p.155-233.
Yueh WS, Chang CF. 1997. 17,20,21-trihydroxy-4-pregnen-3-one and 17,20-dihydroxy-4-pregnen-3-one stimulated spermiation in protandrous black porgy, Acanthopagrus schlegeli. Fish Physiol. Biochem. 17: 187–193. Doi: 10.1023/A:100777462.
Zar JH. 2010. Biostatistical analysis. New Jersey. Prentice Hall. 718p.
Zohar Y, Muñoz-Cueto J, Elizur A, Kah O. 2010. Neuroendocrinology of reproduction in teleost fish. Gen. Comp. Endocrinol. 165: 438-455. Doi: 10.1016/j.ygcen.2009.04.017.
Andrade DR, Godinho AL, Godinho HP, Shimoda E. 2006. Biologia reprodutiva da tabarana, Salminus hilarii (Osteichthyes, Characidae) na represa de três Marias, MG. Rev. Bras. Med. Vet. 28(1): 26-32. Doi: 10.4322/rbcv.2014.359.
Baldisserotto B, Gomes LC. 2005. Espécies nativas para piscicultura no Brasil. Santa Maria, Rio Grande do Sul, 1Ed. UFSM. 470p.
Behmer AO, Tolosa EMC, Neto AGF. 1976. Manual de técnicas para histologia normal e patológica. EDART. São Paulo. Livraria Editora Ltda. 239p.
Birba A, Ramallo MR, Lo Nostro FL, Moreira RG, Pandolfi M. 2015. Reproductive and parental care physiology of Cichlasoma dimerus males. Gen. Comp. Endocrinol. 221: 193-200. Doi: 10.1016/j.ygcen.2015.02.004.
Camargo C. 2007. Efeitos do bloqueio da migração reprodutiva nas reservas metabólicas da tabarana Salminus hilarii (Characiformes: Characidae). Dissertação. Universidade de Mogi das Cruzes. 65p.
Godoy MP. 1975. Peixes do Brasil – Sub-ordem Characoidei. Bacia do Rio Mogi-Guaçu, Piracicaba. Editora: Franciscana. 4vol. 398p.
Grier HJ. 1993. Comparative organization of Sertoli cells including the Sertoli barrier. In: Russel LD, Griswald MD (eds) The Sertoli Cell. Clearwater: Cache River Press. p703-739.
Honji RM, Mello PH, Araújo BC, Rodrigues-Filho JA, Hilsdorf AW, Moreira RG. 2011a. Influence of spawning procedure in fertilization success in Salminus hilarii Valenciennes, 1850 (Teleostei: Characidae): Implications for conservation this species. Neotropic. Ichthyol. 9: 363-370. Doi: 10.1590/S1679-62252011005000012.
Honji RM, Narcizo AM, Borella MI, Romagosa E, Moreira RG. 2009. Patterns of oocyte development in natural habitat and captive Salminus hilarii Valenciennes, 1850 (Teleostei: Characidae). Fish Physiol. Biochem. 35: 109-123. Doi: 10.1007/s10695-008-9239-9.
Honji RM, Caneppele D, Pandolfi M, Lo Nostro FL, Moreira RG. 2011b. The brain-pituitary axis structure in captivity reared females of Steindachneridion parahybae (Siluriformes). In: 9th International Symposium on Reproductive Physiology of Fish. Cochin, India. 4: 30-31.
Honji RM, Nóbrega RH, Pandolfi M, Shimizu A, Borella MI, Moreira RG. 2013. Immunohistochemical study of pituitary cells in wild and captive Salminus hilarii (Characiformes: Characidae) females during the annual reproductive cycle. SpringerPlus. 2: 460-474. Doi: 10.1186/2193-1801-2-460.
Lange IG, Hartel A, Meyer HHD. 2003. Evolution of oestrogen functions in vertebrates. J. Steroid Biochem. Mol. Biol. 83: 219-226. Doi: 10.1016/S0960-0760(02)00225-X.
Levavi-Sivan B, Bogerd J, Mañanós EL, Gómez A, Lareyre JJ. 2010. Perspectives on fish gonadotropins and their receptors. Gen. Comp. Endocrinol. 165: 412-437. Doi: 10.1016/j.ygcen.2009.07.019.
Lima FCT, Britski HA. 2007. Salminus fransciscanus, a new species from the Rio São Francisco Basin, Brazil (Ostariophysi: Characiformes: Characidae). Neotrop. Ichthyol. 5(3): 237-244. Doi: 10.1590/S1679-62252007000300001.
Marceniuk PA, Hilsdorf AWS. 2010. Peixes das cabeceiras do rio Tietê e Parque das Neblinas. 1. ed. Bauru: Canal 6. 157p.
Mennuet A, Adrio F, Kah O, Pakdel F. 2005. Regulation and function of estrogen receptors: comparative aspects. In: Melamed P, Sherwood N (eds) Hormones and their receptors in fish reproduction. Molecular aspects of fish and marine biology. vol 4. World Scientific. p.224-253.
Moreira RG, Honji RM, Melo RG, Narcizo AM, Amaral JS, Araújo RC, Hilsdorf AWS. 2015. The involvement of gonadotropins and gonadal steroids in the ovulatory dysfunction of the potamodromous Salminus hilarii (Teleostei: Characidae) in captivity. Fish Physiol. Biochem. 41(6): 1435-1447. Doi: 10.1007/s10695-015-0097-y.
Mylonas CC, Fostier A, Zanuy S. 2010. Broodstock management and hormonal manipulations of fish reproduction. Gen. Comp. Endocrinol. 165: 516-534. Doi: 10.1016/j.ygcen.2009.03.007.
Parenti LR, Grier HJ. 2004. Evolution and phylogeny of gonadal morphology in bony fishes. Int. Comp. Biol. 44: 333-348. Doi: 10.1093/icb/44.5.333.
Porto-Foresti F, Castilho-Almeida RB, Foresti F. 2005. Biologia e criação do lambari-do-rabo-amarelo (Astyanax altiparanae). In: Baldisserotto B, Gomes LC. (Org). Espécies nativas para piscicultura no Brasil. 1Editora UFSM. Santa Maria. p.105-120.
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.
Sato Y, Fenerich-Verani N, Nuñer APO, Godinho HP, Verani JR. 2003. Padrões reprodutivos de peixes da bacia do São Francisco. In: Godinho HP, Godinho AL. (Org). Águas, peixes e pescadores do São Francisco das Minas Gerais. Belo Horizonte. PUC-Minas. p.229-274.
Schulz RW, França LR, Lareyre J, LeGac F, Chiarini-Garcia H, Nóbrega RH, Miura T. 2010. Spermatogenesis in fish. Gen. Comp. Endocrinol. 165: 390-411. Doi: 10.1016/j.ygcen.2009.02.013.
Silva FSD, Deus JRM, Hilsdorf AWS. 2006. The upper reached ichthyofauna of the Tietê River, São Paulo, Brazil: aspects of their diversity and conservation. Biodivers. Conserv. 15: 3569-3577. Doi: 10.1007/s10531-004-1460-y.
Sink TD, Lockmann RT, Fecteau KA. 2008. Validation, use, and disadvantages of enzyme-linked immunosorbent assay kits for detection of cortisol in channel catfish, largemouth bass, red pacu, and golden shiners. Fish Physiol. Biochem. 34: 95–101. Doi: 10.1007/s10695-007-9150-9.
Takahashi ELH. 2006. Ciclo reprodutivo da tabarana Salminus hilarii (Valenciennes, 1849) (Characidae, Salmininae) na região do baixo Rio Sorocaba, SP. Dissertação. Universidade Estadual Paulista. Centro de Aquicultura. Jaboticabal. 58p.
Tubbs C, Thomas P. 2008. Functional characteristics of membrane progestin receptor alpha (mPRalpha) subtypes: a review with new data showing mPRalpha expression in seatrout sperm and its association with sperm motility. Steroids. 73: 935–941. Doi: 10.1016/j.steroids.2007.12.022.
Vazzoler AEAM. 1996. Biologia da reprodução de peixes teleósteos: teoria e prática. EDUEM, Maringá. 169p.
Villares-Junior GA, Goiten R. 2015. Variations of Salminus hilarii diet (Ostariophysi, Characidae): seasonal and ontogenetic effects. Braz. J. Biol. 75: 574-580. Doi: 10.1590/1519-6984.17213.
Villares-Junior GA, Goiten R. 2016. Morphological aspects in the ontogeny of Salminus hilarii Valenciennes, 1850 (Ostaryophysi: Characidae). Braz. J. Biol. 76: 905-911. Doi: 10.1590/1519-6984.04315.
Villares-Junior GA, Gomiero LM, Goiten R. 2007. Relação peso-comprimento e fator de condição de Salminus hilarii Valenciennes 1850 (Osteichthyes, Characidae) em um trecho da Bacia do Rio Sorocaba, Estado de São Paulo, Brasil. Acta Sci. Biol. Sci 29(4): 407-412. Doi: 10.4025/actascibiolsci.v29i4.884.
von Ihering R. 1929. Da vida dos peixes. Ensaios e scenas de pescarias. Companhia Melhoramentos de São Paulo. Editora Proprietária, 150p.
Weingartner M, Zaniboni-Filho E. 2005. Dourado. In: Baldiserotto B, Gomes LC. (Org). Espécies nativas para a piscicultura no Brasil. Editora UFSM. Santa Maria. p.257-281.
Young G, Kusakabe M, Nakamura I. 2005. Gonadal steroidogenesis in teleost fish. In: Melamed P, Sherwood N. (eds). Hormones and their receptors in fish reproduction. Molecular aspects of fish and marine biology. vol 4. World Scientific. p.155-233.
Yueh WS, Chang CF. 1997. 17,20,21-trihydroxy-4-pregnen-3-one and 17,20-dihydroxy-4-pregnen-3-one stimulated spermiation in protandrous black porgy, Acanthopagrus schlegeli. Fish Physiol. Biochem. 17: 187–193. Doi: 10.1023/A:100777462.
Zar JH. 2010. Biostatistical analysis. New Jersey. Prentice Hall. 718p.
Zohar Y, Muñoz-Cueto J, Elizur A, Kah O. 2010. Neuroendocrinology of reproduction in teleost fish. Gen. Comp. Endocrinol. 165: 438-455. Doi: 10.1016/j.ygcen.2009.04.017.
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How to Cite
Honji, R. M. (2020). Dynamics of testicular maturation during the reproductive cycle of Salminus hilarii (Teleostei, Characidae) in a natural habitat. Revista Da Biologia, 19(1), 31-40. https://doi.org/10.7594/revbio.19.01.04
