Parámetros de calidad espermática en semen crioconservado de peces dulceacuícolas

Parámetros de calidad espermática en semen crioconservado de peces dulceacuícolas

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Resumen

La acuicultura a nivel mundial cada vez toma más relevancia y se ha convertido en una fuente de alimento e ingresos económicos de muchas comunidades alrededor del mundo. Sin embargo, actividades como la sobreexplotación del recurso hídrico y pesquero, el aumento de la población humana, la contaminación ambiental, el cambio climático, entre otros factores, están poniendo en riesgo no solo la seguridad alimentaria del planeta, sino también la biodiversidad de organismos, entre ellos los peces. Una de las herramientas para salvaguardar los recursos biológicos acuáticos, es la crioconservación, que en peces se enfoca principalmente en la conservación de semen en nitrógeno líquido y esta, pesar de ser una técnica muy útil, es susceptible a mejoramiento, ya que se ha reportado que las bajas temperaturas usadas en la crioconservación pueden causar efectos negativos en las células espermáticas, debido a esto es necesario establecer protocolos especie específicos para sacarle todo el potencial a esta forma de conservación. Por lo tanto, el objetivo de esta revisión es recopilar información sobre los principales parámetros de calidad espermática que se ven afectados en el momento de crioconservar el semen, haciendo énfasis en las especies dulceacuícolas.

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Biografía del autor/a (VER)

Owens J. Barros-Barrios, Universidad de los Llanos

MVZ, MSc (c), Grupo de Investigación sobre Reproducción y Toxicología de Organismos Acuáticos – GRITOX, Instituto de Acuicultura y Pesca de Los Llanos– IALL, Facultad de Ciencias Agropecuarias y Recursos Naturales, Universidad de los Llanos, Villavicencio, Colombia. Email: [email protected]

Víctor M. Medina-Robles, Universidad de los Llanos

MVZ, MSc, Dr, Grupo de Investigación sobre Reproducción y Toxicología de Organismos Acuáticos –GRITOX, Instituto de Acuicultura y Pesca de Los Llanos– IALL, Facultad de Ciencias Agropecuarias y Recursos Naturales, Universidad de los Llanos, Villavicencio, Colombia. Email:[email protected]

Referencias (VER)

Abd-Elmoaty M, Ramadan S, Rakesh S, Ashok A. Increased levels of oxidants and reduced antioxidants in semen of infertile men with varicocele. Fertil Steril, 2010;94(4): 1531–1534. https://doi.org/10.1016/j.fertnstert.2009.12.039

Agarwal A, Prabakaran SA. Mechanism, measurement, and prevention of oxidative stress in male reproductive physiology. Indian J. Exp. Biol, 2005;43:963–974.

Aitken R, De Iuliis G. Origins and consequences of DNA damage in male germ cells. Reprod. Biomed. Online, 2007;14:727–733. https://doi.org/https://doi.org/10.1016/S1472-6483(10)60676-1

Andrade Correa M. Estado del conocimiento de la biodiversidad en Colombia y sus amenazas. Consideraciones para fortalecer la interacción ciencia-política. Rev. la Acad. Colomb. ciencias exactas, físicas y Nat, 2011;35:491–508.

Andrade R, Bazzoli N, Rizzo E, Sato Y. Continuous gametogenesis in the neotropical freshwater teleost, Bryconops affinis (Pisces:Characidae). Tissue Cell, 2001;33;524–532. https://doi.org/https://doi.org/10.1054/tice.2001.0206

Aramli MS, Nazari RM. Motility and fertility of cryopreserved semen in Persian sturgeon, Acipenser persicus, stored for 30–60min after thawing. Cryobiology, 2014;69:500–502. https://doi.org/https://doi.org/10.1016/j.cryobiol.2014.10.006

Atencio-García V. (2016). Daños en el espermatozoide durante el proceso de crioconservación, in: Memorias Del VII Congreso Colombiano de Acuicultura. Revista de Investigación Pecuaria, San Juan de Pasto, Colombia, p. 8p.

Bennetts L, Aitken R. A comparative study of oxidative DNA damage in mammalian spermatozoa. Mol. Reprod. Dev, 2005;71:77–87. https://doi.org/https://doi.org/10.1002/mrd.20285

Bobe J, Labbé C. Egg and sperm quality in fish. Gen. Comp. Endocrinol, 2010;165:535–548. https://doi.org/https://doi.org/10.1016/j.ygcen.2009.02.011

Bonnet E, Fostier A, Bobe J. Characterization of rainbow trout egg quality: a case study using four different breeding protocols, with emphasis on the incidence of embryonic malformations. Theriogenology, 2007;67:786–94. https://doi.org/10.1016/j.theriogenology.2006.10.008

Boryshpolets S, Dzyuba B, Stejskal V, Linhart O. Dynamics of ATP and movement in Eurasian perch (Perca fluviatilis L.) sperm in conditions of decreasing osmolality. Theriogenology, 2009;72:851–859. https://doi.org/https://doi.org/10.1016/j.theriogenology.2009.06.005

Cabrita E, Martínez-Páramo S, Gavaia PJ, Riesco MF, Valcarce DG, Sarasquete C, Herráez MP, Robles V. Factors enhancing fish sperm quality and emerging tools for sperm analysis. Aquaculture, 2014;432:389–401. https://doi.org/https://doi.org/10.1016/j.aquaculture.2014.04.034

Cartón-García F, Riesco M, Cabrita E, Herráez M, Robles V. Quantification of lesions in nuclear and mitochondrial genes of Sparus aurata cryopreserved sperm. Aquaculture, 2013;402–403:106–112.https://doi.org/https://doi.org/10.1016/j.aquaculture.2013.03.034

Carvajal-Quintero JD, Januchowski-Hartley SR, Maldonado-Ocampo JA, Jézéquele C, Delgado J, Tedesco P. Damming fragments species’ ranges and heightens extinction risk. Conserv. Lett, 2017;10:708–716. https://doi.org/10.1111/conl.12336

Collazos-Lasso L, Arias-Castellanos J. Fundamentos de la tecnología biofloc (BFT). Una alternativa para la piscicultura en Colombia. Una revisión. Rev. ORINOQUIA, 2015;19(1):77–86.

Cosson J. Frenetic activation of fish spermatozoa flagella entails short-term motility, portending their precocious decadence. J. Fish Biol, 2010;76:240–79. https://doi.org/10.1111/j.1095-8649.2009.02504.x.

Cosson J. The Ionic and Osmotic Factors Controlling Motility of Fish Spermatozoa. Aquac. Int, 2004;12:69–85. https://doi.org/10.1023/B:AQUI.0000017189.44263.bc

da Costa B, de Oliveira D, Rodrigues R, Gomes I, Streit D. Morphological abnormalities in zebrafish cryopreserved sperm. Cryobiology, 2020;97:235–237. https://doi.org/https://doi.org/10.1016/j.cryobiol.2020.08.003

Dietrich GJ, Nynca J, Dobosz S, Zalewski T, Ciereszko A. Application of glucose-methanol extender to cryopreservation of semen of sex-reversed females rainbow trout results in high post-thaw sperm motility and fertilizing ability. Aquaculture, 2014;434:27–32. https://doi.org/10.1016/j.aquaculture.2014.07.015

Ding S, Ge J, Hao C, Zhang M, Yan W, Xu Z, Pan J, Chen S, Tian Y, Huang Y. Long-term cryopreservation of sperm from Mandarin fish Siniperca chuatsi. Anim. Reprod. Sci, 2009;113:229–235. https://doi.org/10.1016/j.anireprosci.2008.08.003

DoNascimiento C, Herrera-Collazos E, Herrera-R G, Ortega-Lara A, Villa-Navarro F, Usma-Oviedo J, Maldonado-Ocampo J. Checklist of the freshwater fishes of Colombia: a Darwin Core alternative to the updating problem. Zookeys, 2016;708:25–138.

DoNascimiento C, Herrera-Collazos E, Maldonado-Ocampo J, Herrera-Collazos E. (2020). Lista de especies de peces de agua dulce de Colombia / Checklist of the freshwater fishes of Colombia. https://doi.org/https://doi.org/10.15472/numrso accessed via GBIF.org on 2021-06-27

Duarte-Trujillo A, Ardila-Artunduaga M, Guaje-Ramírez D, Medina-Robles V. Efecto crioprotector de la yema de huevo en semen de Prochilodus mariae (Characiformes: Prochilodontidae). Biotecnol. en el Sect. Agropecu. y Agroindustrial, 2021;19:191–205. https://doi.org/https://doi.org/10.18684/bsaa(19)191-205

FAO, 2007. State of art in the management of animal genetic resource. Method for conservation, in: Nations, C. on G.R. for F. and A.F.y A.O. on the U. (Ed.), The State of the World’s Animal Genetic Resources for Food and Agriculture. Rome, pp. 443–475.

Fernández-Díez C, González-Rojo S, Lombó M, Herráez MP. Impact of sperm DNA damage and oocyte-repairing capacity on trout development. Reproduction, 2018;152: 57–67. https://doi.org/10.1530/REP-16-0077

Figueroa E, Lee-Estévez M, Valdebenito I, Farías J, Romero J. Potential biomarkers of DNA quality in cryopreserved fish sperm: impact on gene expression and embryonic development. Rev. Aquac. 2018;1–10. https://doi.org/10.1111/raq.12323

Figueroa E, Lee-Estevez M, Valdebenito I, Watanabe I, Oliveira RPS, Romero J, Castillo RL, Farías JG. Effects of cryopreservation on mitochondrial function and sperm quality in fish. Aquaculture, 2019;511:634190. https://doi.org/10.1016/j.aquaculture.2019.06.004

Figueroa E, Valdebenito I, Farias J. Technologies used in the study of sperm function in cryopreserved fish spermatozoa. Aquac. Res. 2016;47:1691–1705. https://doi.org/10.1111/are.12630

Figueroa E, Valdebenito I, Zepeda A, Figueroa C, Dumorné K, Castillo R, Farias J. Effects of cryopreservation on mitochondria of fish spermatozoa. Rev. Aquac, 2017;9:76–87. https://doi.org/https://doi.org/10.1111/raq.12105

Flesch F, Gadella M. Dynamics of the mammalian sperm plasma membrane in the process of fertilization. Biochim. Biophys. Acta - Rev. Biomembr, 2000;1469:197–235. https://doi.org/https://doi.org/10.1016/S0304-4157(00)00018-6

Gómez M, Trejo J. La bioenergética, las mitocondrias y la fosforilación oxidativa. Rev. Digit. Univ, [en línea] 2015;16:1–15.

González-Rojo S, Fernández-Díez C, Guerra S, Robles V, Herraez M. Differential Gene Susceptibility to Sperm DNA Damage: Analysis of Developmental Key Genes in Trout. PLoS One, 2014;9:e114161.

Holt WV. (2001). Aims of genetic resource bank progemmes, in: Watson, P., Holt, W. (Eds.), Cryobanking the Genetic Resources: Wildlife Conservation for the Future? Taylor y Francis, pp. 15–17.

Horváth Á, Urbányi B. The effect of cryoprotectants on the motility and fertilizing capacity of cryopreserved African catfish Clarias gariepinus (Burchell 1822) sperm. Aquac. Res, 2000;31:317–324. https://doi.org/https://doi.org/10.1046/j.1365-2109.2000.00444.x

Jimenez-Segura L, Galvis-Vergara G, Cala-Cala P, García-Alzate C, López-Casas S, Ríos-Pulgarín M, Arango G, Mancera-Rodríguez N, Gutiérrez F, Álvarez-León R. Freshwater fish faunas, habitats and conservation challenges in the Caribbean river basins of north-western South America: FRESHWATER FISHES OF NORTH-WEST SOUTH AMERICA. J. Fish Biol, 2016;89:65–101. https://doi.org/10.1111/jfb.13018.

Kefer JC, Agarwal A, Sabanegh E. Role of antioxidants in the treatment of male infertility. Int. J. Urol, 2009;16:449–457. https://doi.org/https://doi.org/10.1111/j.1442-2042.2009.02280.x

Kholodnyy V, Gadêlha H, Cosson, J., Boryshpolets, S. (2020). How do freshwater fish sperm find the egg? The physicochemical factors guiding the gamete encounters of externally fertilizing freshwater fish. Rev. Aquac, 12, 1165–1192. https://doi.org/https://doi.org/10.1111/raq.12378

Kommisrud E, Myromslien F, Stenseth E, Zeremichael T, Hofman N, Grevle I, Sunde J. Viability, motility, ATP content and fertilizing potential of sperm from Atlantic salmon (Salmo salar L.) in milt stored before cryopreservation. Theriogenology, 2020;151:58–65. https://doi.org/https://doi.org/10.1016/j.theriogenology.2020.04.008

Koppers AJ, Garg ML, Aitken RJ. Stimulation of mitochondrial reactive oxygen species production by unesterified, unsaturated fatty acids in defective human spermatozoa. Free Radic. Biol. Med, 2010;48:112–119. https://doi.org/https://doi.org/10.1016/j.freeradbiomed.2009.10.033

Křišťan J, Hatef A, Alavi S, Policar T. Sperm morphology, ultrastructure, and motility in pikeperch Sander lucioperca (Percidae, Teleostei) associated with various activation media. Czech J. Anim. Sci, 2014;59:1–10.

Labbe C, Martoriati A, Devaux A, Maisse G. Effect of sperm cryopreservation on sperm DNA stability and progeny development in rainbow trout. Mol. Reprod. Dev, 2001;60:397–404. https://doi.org/https://doi.org/10.1002/mrd.1102

Lahnsteiner F, Mansour N, Plaetzer K. Antioxidant systems of brown trout (Salmo trutta f. fario) semen. Anim. Reprod. Sci, 2010;119:314–321. https://doi.org/https://doi.org/10.1016/j.anireprosci.2010.01.010

Lasso C, Machado-Allison A, Taphorn D. Fishes and aquatic habitats of the Orinoco River Basin: Diversity and conservation. J. Fish Biol, 2016;89:1–18. https://doi.org/10.1111/jfb.13010

Li P, Wei Q, Liu L. DNA integrity of Polyodon spathula cryopreserved sperm. J. Appl. Ichthyol, 2008;24:121–125.

Liu Q, Li J, Zhang S, Xiao Z, Ding F, Yu D, Xu X. Flow cytometry and ultrastructure of cryopreserved red seabream (Pagrus major) sperm. Theriogenology, 2007;67:1168–1174. https://doi.org/https://doi.org/10.1016/j.theriogenology.2006.12.013

López-Hernández J, Pérez A, Jiménez-Félix S, Paramo S, Márquez-Couturier G, Yasui G, Arias-Rodriguez L. La calidad espermática en peces y los métodos de evaluación. Rev. Ciencias Mar. y Costeras, 2018;10:67. https://doi.org/10.15359/revmar10-1.5

Luberda Z. The role of glutathione in mammalian gametes. Reprod. Biol, 2005;5:5–17.

Lundberg J, Kottelat M, Smith G, Stiassny M, Gill A. So many fishes, so little time: an overview of recent ichthyological discovery in continental waters. Ann. Missouri Bot. Gard, 2000;87:26–62.

MADR. (2021). Acuicultura en Colombia.

Maria A, Azevedo H, Carneiro P. (2011). Protocolo para criopreservação do sêmen de tambaqui (Colossoma macropomum).

Maria A, Carvalho A, Araújo R, Santos J, Carneiro P, Azevedo H. Use of cryotubes for the cryopreservation of tambaqui fish semen (Colossoma macropomum). Cryobiology, 2015;70:109–114.

Márián T, Krasznai Z, Balkay L, Balázs M, Emri M, Bene L, Trón L. Hypo-osmotic shock induces an osmolality-dependent permeabilization and structural changes in the membrane of carp sperm. J Histochem Cytochem, 1993;41:291–7. https://doi.org/10.1177/41.2.8419464

Martínez-Páramo S, Horváth Á, Labbé C, Zhang T, Robles V, Herráez P, Suquet M, Adams S, Viveiros A, Tiersch TR, Cabrita E. Cryobanking of aquatic species. Aquaculture, 2017a;472:156–177. https://doi.org/10.1016/j.aquaculture.2016.05.042

Martínez-Páramo S, Horváth Á, Labbé C, Zhang T, Robles V, Herráez P, Suquet M, Adams S, Viveiros A, Tiersch TR, Cabrita E. Cryobanking of aquatic species. Aquaculture, 2017b;472:156–177. https://doi.org/10.1016/J.AQUACULTURE.2016.05.042

Martínez G, Atencio-García V, Pardo-Carrasco S. Efectos de la concentración de glucosa sobre la activación de la movilidad espermática en bocachico (Prochilodus magdalenae). Rev. MVZ Córdoba, 2011;16:2554–2563.

Martinez J, Pardo-Carrasco S. Effect of freezing and thawing rates on sperm motility in bocachico Prochilodus magdalenae (pisces, characiformes). Rev. MVZ Córdoba, 2013;8: 3295–3303.

Martínez J, Pardo-Carrasco S. CRIOCONSERVACIÓN DE SEMEN EN PECES: EFECTOS SOBRE LA MOVILIDAD ESPERMÁTICA Y LA FERTILIDAD. Acta Biológica Colomb, 2010;15:3–24.

Medina-Robles V. (2020). Evaluación de protocolos de crioconservación seminal en especies ícticas nativas como línea base para la conformación de un banco de semen de peces nativos con fines comerciales y de conservación. Universidad de Los Llanos.

Medina-Robles V, Duarte-Trujillo A, Cruz-Casallas P. Crioconservación seminal en peces de agua dulce: aspectos biotecnológicos, celulares y bioquímicos. Orinoquia, 2020;24(2):51–78. https://doi.org/https//doi.org/10.22579/20112629.630

Medina-Robles V, Guaje-Ramírez D, Marin-Cossio L, Sandoval-Vargas L, Cruz-Casallas P. Crioconservación seminal de Colossoma macropomum como estrategia de producción y conservación en la Orinoquia Colombiana. Orinoquia, 2019;23:16–24.

Medina-Robles VM, Sandoval-Vargas LY, Suárez-Martínez RO, Gómez-Ramírez E, Guaje-Ramírez DN, Cruz-Casallas PE. Cryostorage of white cachama (Piaractus orinoquensis) sperm: Effects on cellular, biochemical and ultrastructural parameters. Aquac. Reports, 2023a;29:101477. https://doi.org/https://doi.org/10.1016/j.aqrep.2023.101477

Medina-Robles VM, Suárez-Martínez RO, Baldisserotto B, Cruz-Casallas PE. CRYOPRESERVED SEMEN OF Piaractus orinoquensis (SERRASALMIDAE): POST-THAW STORAGE TIMES AND ACTIVATING SOLUTIONS. Acta Biológica Colomb, 2023b;28:86–94. https://doi.org/10.15446/abc.v28n1.95701

Medina‐Robles VM, Pahí‐Rosero AM, Sandoval‐Vargas LY, Cruz‐Casallas PE. Effect of Cryopreservation and Packaging System on Sperm Motility and Fertility of Striped Catfish. N. Am. J. Aquac, 2021;83:105–113. https://doi.org/10.1002/naaq.10177

Miliorini AB, Murgas-Solis LD, Rosa PV, Oberlender G, Pereira GJM, da Costa DV. A morphological classification proposal for curimba (Prochilodus lineatus) sperm damages after cryopreservation. Aquac. Res, 2011;42:177–187. https://doi.org/10.1111/j.1365-2109.2010.02575.x

Mójica J. (2012). Libro rojo de peces dulceacuícolas de Colombia, 1 ed. ed. Instituto de Investigación de Recursos Biológicos Alexander von Humboldt, Bogotá, Colombia.

Nelson J, Grande T, Wilson M. (2016). Fishes of the world, Quinta Edi. ed. Hoboken, EUA.

Ozkavukcu S, Erdemli E, Isik A, Oztuna D, Karahuseyinoglu S. Effects of cryopreservation on sperm parameters and ultrastructural morphology of human spermatozoa. J. Assist. Reprod. Genet, 2008;25:403–411. https://doi.org/10.1007/s10815-008-9232-3

Paniagua-Chávez CG, Ortiz-Gallarza SM, Aguilar-Juárez M. Subsistema Nacional de Recursos Genéticos Acuáticos: Uso de la criopreservación para la conservación de los recursos genéticos acuáticos en México. Hidrobiologica, 2011;21:415–429.

Pérez-Cerezales S, Gutiérrez-Adán A, Martínez-Páramo S, Beirão J, Herráez M. Altered gene transcription and telomere length in trout embryo and larvae obtained with DNA cryodamaged sperm. Theriogenology, 2011;76:1234–45. https://doi.org/10.1016/j.theriogenology.2011.05.028

Purdy P, Graham J. (2015). Membrane Modification Strategies for Cryopreservation, in: Wolkers, W., Oldenhof, H. (Eds.), Cryopreservation and Freeze-Drying Protocols. Humana Press, Hertfordshire, UK, pp. 352–357.

Quagio-Grassiotto I, Negrão J, Carvalho E, Foresti F. Ultrastructure of spermatogenic cells and spermatozoa in Hoplias malabaricus (Teleostei, Characiformes, Erythrinidae). J. Fish Biol, 2001;59:1494–1502. https://doi.org/https://doi.org/10.1111/j.1095-8649.2001.tb00214.x

Ramírez-Merlano J, Velasco-Santamaría Y, Medina-Robles V, Cruz-Casallas P. Cryopreservation effects on the sperm quality of cachama blanca Piaractus brachypomus (Cuvier 1818). Aquac. Res, 2011;42: https://doi.org/10.1111/j.1365-2109.2011.02835.x

Ramírez-Merlano JA, Medina-Robles VM, Cruz-Casallas PE. Crioconservación seminal de bagre rayado Pseudoplatystoma metaense (Teleostei, Pimelodidae), bajo diferentes protocolos de congelación . Arch. Med. Vet, 2011;43:135-144

Reis R, Albert J, Di Dario F, Mincarone M, Petry P, Rocha L. Fish biodiversity and conservation in South America. J. Fish Biol. 2016;89(1):12–47.

Rodao M, Montagne J, Clivio G, Papa N, Larrosa G. (2015). Sperm and Egg Envelope Ultrastructure and Some Considerations on Its Evolutionary Meaning, in: Berois, N., García, G., De Sá, R. (Eds.). Annual Fishes: Life History Strategy, Diversity and Evolution. CRC Press, Boca Ratón, USA, pp. 47–62. https://doi.org/10.1201/b19016-5

Rosamond L, Ronald W, Buschmann A, Bush S, Cao L, Klinger D, Little D, Lubchenco J, Shumway S, Troell M. A 20-year retrospective review of global aquaculture. Nature, 2021;591:551–563. https://doi.org/10.1038/s41586-021-03308-6

Sandoval-Vargas L, Dumorné K, Contreras P, Farías JG, Figueroa E, Risopatrón J, Valdebenito I. Cryopreservation of coho salmon sperm (Oncorhynchus kisutch): Effect on sperm function, oxidative stress and fertilizing capacity. Aquaculture, 2021;533: https://doi.org/10.1016/j.aquaculture.2020.736151

Sandoval‐Vargas LY, Silva-Jiménez M, Risopatrón-González J, Villalobos EF, Cabrita E, Valdebenito-Isler I. Oxidative stress and use of antioxidants in fish semen cryopreservation. Rev. Aquac, 2021;13:365–387. https://doi.org/10.1111/raq.12479

Słowińska M, Nynca J, Cejko B, Dietrich M, Horváth Á, Urbányi B, Kotrik L, Ciereszko A. Total antioxidant capacity of fish seminal plasma. Aquaculture, 2013;400–401:101–104. https://doi.org/https://doi.org/10.1016/j.aquaculture.2013.03.010

Słowińska M, Nynca J, Cejko BI, Dietrich MA, Horváth Á, Urbányi B, Kotrik L, Ciereszko A. Total antioxidant capacity of fish seminal plasma. Aquaculture, 2013;400–401:101–104. https://doi.org/10.1016/j.aquaculture.2013.03.010

Streit DP, Fornari DC, Povh JA, Godoy LC, De Mello F, Oliveira CAL, Kawakami E, Ribeiro RP. Germplasm banking and its role in the development of the fish genetic improvement programme in Brazil. Cryo-Letters, 2015;36:399–404.

Tabares C, Tarazona A, Olivera M. Fisiología de la activación del espermatozoide en peces de agua dulce. Rev. Colomb. Ciencias Pecu, 2005;18:149–161.

Tognelli M. (2016). Estado de conservación y distribución de la biodiversidad de agua dulce en los Andes Tropicales. UICN, Gland, Suiza, Cambridge, UK y Arlington, USA. https://doi.org/http://dx.doi.org/10.2305/IUCN.CH.2016.02.es

Tvrdá E, Kňažická Z, Bárdos L, Massányi P, Lukáč N. Impact of oxidative stress on male fertility - A review. Acta Vet. Hung, 2011;59(4):465–484. https://doi.org/https://doi.org/10.1556/AVet.2011.034

van Overveld F, Haenen GR, Rhemrev J, Vermeiden J, Bast A. Tyrosine as important contributor to the antioxidant capacity of seminal plasma. Chem. Biol. Interact, 2000;127: 151–161. https://doi.org/10.1016/S0009-2797(00)00179-4

Vermes I, Haanen C, Reutelingsperger C. Flow cytometry of apoptotic cell death. J. Immunol. Methods, 2000;243:167–190. https://doi.org/https://doi.org/10.1016/S0022-1759(00)00233-7

Viveiros A, Godinho H. Sperm quality and cryopreservation of Brazilian freshwater fish species: a review. Fish Physiol. Biochem, 2009;35:137–150.

Viveiros A, Nascimento A, Leal M, Antônio-Gonçalves C, Orfão L, Cosson J. Methyl glycol, methanol and DMSO effects on post-thaw motility, velocities, membrane integrity and mitocondrial function of Brycon orbignyanus and Prochilodus lineatus (Characiformes) sperm. Fish Physiol Biochem, 2015;41:193–201. https://doi.org/10.1007/s10695-014-0016-7

Volpedo A, Thompson G. Environmental changes on freshwater fish communities in South America in the last five decades: a case study in northeast Argentina. Sustain. Agri, Food Environ. Res, 2017;4(3):47–61.

Wathes C, Abayasekara R, Aitken R. Polyunsaturated fatty acids in male and female reproduction. Biol Reprod, 2007;77(2):190–201. https://doi.org/10.1095/biolreprod.107.060558

WHO, 2003. World Health Organization technical report.

WWF. (2021). Los peces de agua dulce son vitales para cientos de millones de personas, pero un tercio de ellos se enfrenta a la extinción [WWW Document]. WORLD’S Forgot. FISHES. URL https://www.wwf.org.co/?uNewsID=365976 (accessed 6.28.21).

Xin N, Liu T, Zhao H, Wang Z, Liu J, Zhang Q, Qi J. The impact of exogenous DNA on the structure of sperm of olive flounder (Paralichthys olivaceus). Anim. Reprod. Sci, 2014;149:305–310. https://doi.org/https://doi.org/10.1016/j.anireprosci.2014.06.029