In vivo and in vitro aging of common carp Cyprinus carpio sperm after multiple hormonal application and stripping of males

Alavi SMH, Cosson J, Kazemi R (2006) Semen characteristics in Acipenser persicus in relation to sequential stripping. J Appl Ichthyol 22:400–405. https://doi.org/10.1111/j.1439-0426.2007.00994.x Alavi SMH, Linhart O, Coward K, Rodina M (2008) Fish spermatology: implication for aquaculture management. In: Alavi SMH, Cosson JJ, Coward K, Rafiee R (eds) Fish Spermatology. Alpha Science Ltd, Oxford, pp 397–460 Alavi SMH, Cosson J, Bondarenko O, Linhart O (2019) Sperm motility in fishes: (III) diversity of regulatory signals from membrane to the axoneme. Theriogenology 136:143–165. https://doi.org/10.1016/j.theriogenology.2019.06.038 Aramli MS, Kalbassi MR, Nazari RM, Aramli S (2013) Effects of short-term storage on the motility, oxidative stress, and ATP content of Persian sturgeon (Acipenser persicus) sperm. Anim Reprod Sci 143:112–117. https://doi.org/10.1016/j.anireprosci.2013.10.010 Aramli MS, Kalbassi MR, Gharibi MR (2015) Retracted: Effects of multiple collections on spermatozoa quality of Persian sturgeon, Acipenser persicus: motility, density and seminal plasma composition. J Anim Physiol Anim Nutr 99:66–72. https://doi.org/10.1111/jpn.12212 Babiak I, Ottesen O, Rudolfsen G, Johnsen S (2006) Quantitative characteristics of Atlantic halibut, Hippoglossus hippoglossus L, semen throughout the reproductive season. Theriogenology 65:1587–1604. https://doi.org/10.1016/j.theriogenology.2005.09.004 Beirão J, Soares F, Pousão-Ferreira P, Diogo P, Dias J, Dinis MT, Herráez MP, Cabrita E (2015) The effect of enriched diets on Solea senegalensis sperm quality. Aquaculture 435:187–194. https://doi.org/10.1016/j.aquaculture.2014.09.025 Billard R, Weil C, Bienarz K, Mikolajczyk T, Breton B, Epler P, Bougoussa M (1992) Testicular and some hormonal changes during the first four years of life in the mirror carp, Cyprinus curpio L. J Fish Biol 41:473–487. https://doi.org/10.1111/j.1095-8649.1992.tb02675.x Billard R, Cosson J, Perchec G, Linhart O (1995) Biology of sperm and artificial reproduction in carp. Aquaculture 129:95–112. https://doi.org/10.1016/0044-8486(94)00231-C Bokor Z, Żarski D, Palińska-Żarska K, Krejszeff S, Król J, Radóczi JI, Horváth Á, Várkonyi L, Urbányi B, Bernáth G (2021) Standardization of sperm management for laboratory assessment of sperm quality and in vitro fertilization in Eurasian perch (Perca fluviatilis). Aquacult Int 29:2021–2033. https://doi.org/10.1007/s10499-021-00731-4 Boryshpolets S, Kowalski RK, Dietrich GJ, Dzyuba B, Ciereszko A (2013) Different computer-assisted sperm analysis (CASA) systems highly influence sperm motility parameters. Theriogenology 80:758–765. https://doi.org/10.1016/j.theriogenology.2013.06.019 Butts IAE, Litvak MK, Trippel EA (2010) Seasonal variations in seminal plasma and sperm characteristics of wild-caught and cultivated Atlantic cod, Gadus morhua. Theriogenology 73:873–885. https://doi.org/10.1016/j.theriogenology.2009.11.011 Büyükhatipoglu S, Holtz W (1984) Sperm output in rainbow trout (Salmo gairdneri) effect of age, timing and frequency of stripping and presence of females. Aquaculture 37:63–71. https://doi.org/10.1016/0044-8486(84)90044-9 Cabrita E, Martínez-Páramo S, Gavaia PJ, Riesco MF, Valcarce DG, Sarasquete C, Herráez MP, Roblesbc V (2014) Factors enhancing fish sperm quality and emerging tools for sperm analysis. Aquaculture 432:389–401. https://doi.org/10.1016/j.aquaculture.2014.04.034 Caille N, Rodina M, Kocour M, Gela D, Flajšhans M, Linhart O (2006) Quantity, motility and fertility of tench Tinca tinca (L.) sperm in relation to LHRH analogue and carp pituitary treatments. Aquacult Int 14:75–87. https://doi.org/10.1007/s10499-005-9015-0 Cejko BI, Kowalski RK, Kucharczyk D, Zarski D, Targonska K, Glogowski J (2011) Effect of time after hormonal stimulation on semen quality indicators of common carp, Cyprinus carpio (Actinopterygii: Cypriniformes: Cyprinidae). Acta Ichthyol Piscatoria 41:75–80. https://doi.org/10.3750/AIP2011.41.2.01 Cejko BI, Horváth Á, Kollár T, Kása E, Lujić J, Marinović Z, Urbányi B, Kowalski RK (2018a) Optimisation of sodium and potassium concentrations and pH in the artificial seminal plasma of common carp Cyprinus carpio L. Fish Physiol Biochem 44:1435–1442. https://doi.org/10.1007/s10695-018-0491-3 Cejko BI, Sarosiek B, Krejszeff S, Kowalski RK (2018b) Multiple collections of common carp Cyprinus carpio L. semen during the reproductive period and its effects on sperm quality. Anim Reprod Sci 188:178–188. https://doi.org/10.1016/j.anireprosci.2017.12.002 Cheng Y, Franěk R, Rodina M, Xin MM, Cosson J, Zhang SP, Linhart O (2021a) Optimization of sperm management and fertilization in Zebrafish (Danio rerio (Hamilton)). Animals 11:1558. https://doi.org/10.3390/ani11061558 Cheng Y, Vechtova P, Fussy Z, Sterba J, Linhartová Z, Rodina M, Tučková V, Gela D, Samarin AM, Lebeda I, Xin MM, Zhang SP, Rahi D, Linhart O (2021b) Changes in phenotypes and DNA methylation of in vitro aging sperm in common carp Cyprinus carpio. Int J Mol Sci 22:5925. https://doi.org/10.3390/ijms22115925 Cheng Y, Zhang SP, Linhartová Z, Shazada NE, Linhart O (2022) Common carp (Cyprinus carpio) sperm reduction during short-term in vitro storage at 4 °C. Anim Reprod Sci 243:107017 Contreras P, Ulloa P, Merino O, Valdebenito I, Figueroa E, Farıas J, Risopatrón J (2017) Effect of short-term storage on sperm function in Patagonian blenny (Eleginops maclovinus) sperm. Aquaculture 481:58–63. https://doi.org/10.1016/j.aquaculture.2017.08.022 Contreras P, Dumorne K, Ulloa-Rodríguez P, Merino O, Figueroa E, Farias JG, Valdebenito I, Risopatrón J (2020) Effects of short-term storage on sperm function in fish semen: a review. Rev Aquac 12:1373–1389. https://doi.org/10.1111/raq.12387 Core R Team (2019) A language and environment for statistical computing; R Foundation for Statistical Computing: Vienna, Austria, Available online: https://www.R-project.org. Courtois F, Takashima F, Billard R (1986) Stimulation of spermiation following repeated injection of carp pituitary homogenates in the carp. B Jpn Soc Sci Fish 52:995–997. https://doi.org/10.2331/suisan.52.995 Cruea DD (1969) Some chemical and physical characteristics of fish sperm. Trans Am Fish Sot 98:785–788. https://doi.org/10.1577/1548-8659(1969)98[785:SCAPCO]2.0.CO;2 Dietrich MA, Judycka S, Słowińska M, Kodzik N, Ciereszko A (2021) Short-term storage-induced changes in the proteome of carp (Cyprinus carpio L.) spermatozoa. Aquaculture 530:735784. https://doi.org/10.1016/j.aquaculture.2020.735784. Dreanno C, Suquet M, Fauvel C, Le Coz JR, Dorange G, Quemener L, Billard R (1999) Effect of the aging process on the quality of sea bass (Dicentrarchus labrax) semen. J Appl Ichthyol 15:176–180 Gage MJG, Macfarlance CP, Yeates S, Ward RG, Searle JB, Parker GA (2004) Spermatozoal traits and sperm competition in Atlantic salmon: relative sperm velocity is the primary determinant of fertilization success. Curr Biol 14:44–47. https://doi.org/10.1016/j.cub.2003.12.028 Gallego V, Pérez L, Asturiano JF, Yoshida M (2013) Relationship between spermatozoa motility parameters, sperm/egg ratio, and fertilization and hatching rates in pufferfish (Takifugu niphobles). Aquaculture 416:238–243. https://doi.org/10.1016/j.aquaculture.2013.08.035 Gallego V, Cavalcante SS, Fujimoto RY, Carneiro PCF, Azevedo HC, Maria AN (2017) Fish sperm subpopulations: changes after cryopreservation process and relationship with fertilization success in tambaqui (Colossoma macropomum). Theriogenology 87:16–24. https://doi.org/10.1016/j.theriogenology.2016.08.001 Gu NH, Zhao WL, Wang GS, Sun F (2019) Comparative analysis of mammalian sperm ultrastructure reveals relationships between sperm morphology, mitochondrial functions and motility. Reprod Biol Endocrinol 17:1–12. https://doi.org/10.1186/s12958-019-0510-y Hassan MM, Nahiduzzaman M, Al Mamun SN, Taher MA, Hossain MAR (2013) Fertilization by refrigerator stored sperm of the Indian major carp, Labeo calbasu (Hamilton, 1822). Aquac Res 45:150–158. https://doi.org/10.1111/j.1365-2109.2012.03214.x Horokhovatskyi Y, Dietrich MA, Lebeda I, Fedorov P, Rodina M, Dzyuba B (2018) Cryopreservation effects on a viable sperm sterlet (Acipenser ruthenus) subpopulation obtained by a Percoll density gradient method. PLoS ONE 13:e0202514. https://doi.org/10.1371/journal.pone.0202514 Hulata G, Rothbard S (1979) Cold storage of carp semen for short periods. Aquaculture 16:267–269. https://doi.org/10.1016/0044-8486(79)90116-9 Kołdras M, Bieniarz K, Kime DE (1990) Sperm production and steroidogenesis in testes of the common carp, Cyprinus carpio L, at different stages of maturation. J Fish Biol 37:635–645. https://doi.org/10.1111/j.1095-8649.1990.tb05897.x Kowalski RK, Cejko BI (2019) Sperm quality in fish: determinants and affecting factors. Theriogenology 135:94–108 Lahnsteiner F, Mansour N, Plaetzer K (2010) Antioxidant systems of brown trout (Salmo trutta f. fario) semen. Anim Reprod Sci 119:314–321. https://doi.org/10.1016/j.anireprosci.2010.01.010 Lemaître JF, Gaillard JM, Ramm SA (2020) The hidden ageing costs of sperm competition. Ecol Lett 23:1573–1588. https://doi.org/10.1111/ele.13593 Linhart O, Mims SD, Gomelsky B, Hiott AE, Shelton WL, Cosson J, Rodina M, Gela D (2000) Spermiation of paddlefish (Polyodon spathula, Acipenseriformes) stimulated with injection of LHRH analogue and carp pituitary powder. Aquat Living Resour 13:455–460. https://doi.org/10.1016/S0990-7440(00)01068-8 Linhart O, Gela D, Rodina M, Kocour M (2004) Optimization of artificial propagation in European catfish, Silurus glanis L. Aquaculture 235:619–632. https://doi.org/10.1016/j.aquaculture.2003.11.031 Linhart O, Rodina M, Gela D, Kocour M, Vandeputte M (2005) Spermatozoal competition in common carp (Cyprinus carpio): what is the primary determinant of competition success? Reproduction 130:705–711. https://doi.org/10.1530/rep.1.00541 Linhart O, Cheng Y, Xin MM, Rodina M, Tučková V, Shelton WL, Kašpar V (2020b) Standardization of egg activation and fertilization in sterlet (Acipenser ruthenus). Aquac Rep 17:100381. https://doi.org/10.1016/j.aqrep.2020.100381 Linhart O, Cheng Y, Rodina M, Tučková V, Shelton WL, Tinkir M, Memiş D, Xin MM (2020a) Sperm management of European catfish (Silurus glanis L.) for effective reproduction and genetic conservation. Aquaculture 529, 735620. https://doi.org/10.1016/j.aquaculture.2020a.735620 Maklakov AA, Chapman T (2019) Evolution of ageing as a tangle of trade-offs: energy versus function. Proc R Soc B 286:20191604. https://doi.org/10.1098/rspb.2019.1604 Malinovskyi O, Policar T, Rahimnejad S, Křišťan J, Dzyuba B, Blecha M, Boryshpolets S (2021) Multiple sperm collection as an effective solution for gamete management in pikeperch (Sander lucioperca). Aquaculture 530:735870. https://doi.org/10.1016/j.aquaculture.2020.735870 Mylonas CC, Duncan NJ, Asturiano JF (2016) Hormonal manipulations for the enhancement of sperm production in cultured fish and evaluation of sperm quality. Aquaculture 472:21–44. https://doi.org/10.1016/j.aquaculture.2016.04.021 Park C, Chapman FA (2005) An extender solution for the short-term storage of sturgeon semen. N Am J Aqualcult 67:52–57. https://doi.org/10.1577/FA03-068.1 Perchec G, Jeulin C, Cosson J, André F, Billard R (1995) Relationship between sperm ATP content and motility of carp spermatozoa. J Cell Sci 108:747–753. https://doi.org/10.1242/jcs.108.2.747 Perchec G, Cosson MP, Cosson J, Jeulin C, Billard R (1996) Morphological and kinetic changes of carp (Cyprinus carpio) spermatozoa after initiation of motility in distilled water. Cell Motil Cytoskeleton 35:113–120. https://doi.org/10.1002/(SICI)1097-0169(1996)35:2%3c113::AID-CM4%3e3.0.CO;2-B Reinhardt K, Siva-Jothy MT (2005) An advantage for young sperm in the house cricket Acheta domesticus. Am Nat 165:718–723. https://doi.org/10.1086/430010 Risopatrón J, Merino O, Cheuquemán C, Figueroa E, Sánchez R, Farías JG, Valdebenito I (2018) Effect of the age of brood-stock males on sperm function during cold storage in the trout (Oncorhynchus mykiss). Andrologia 50:e12857. https://doi.org/10.1111/and.12857 Rodina M, Cosson J, Gela D, Linhart O (2004) Kurokura solution as immobilizing medium for spermatozoa of tench (Tinca tinca L.). Aquac Int 12:119–131. https://doi.org/10.1023/B:AQUI.0000017192.75993.e3 Rurangwa E, Volckaert FAM, Huyskens G, Kime DE, Ollevier F (2001) A concerted strategy for the quality control of refrigerated and cryopreserved semen using computer-assisted sperm analysis (CASA), viable staining and standardized fertilization: application to preservation of sperm of African catfish (Clarias gariepinus). Theriogenology 55:751–769. https://doi.org/10.1016/S0093-691X(01)00441-1 Rurangwa E, Kime DE, Ollevier F, Nash JP (2004) The measurement of sperm motility and factors affecting sperm quality in cultured fish. Aquaculture 234:1–28. https://doi.org/10.1016/j.aquaculture.2003.12.006 Saad A, Billard R (1987) Spermatozoa production and volume of semen collected after hormonal stimulation in the carp, Cyprinus carpio. Aquaculture 65:67–77. https://doi.org/10.1016/0044-8486(87)90271-7 Saad A, Billard R, Theron MC (1988) Hollebecq MG. Short-term preservation of carp (Cyprinbs carpio) semen. Aquaculture 71:133–150. https://doi.org/10.1016/0044-8486(88)90280-3 Sanocka D, Kurpisz M (2004) Reactive oxygen species and sperm cells. Reprod Biol Endocrinol 2:1–7. https://doi.org/10.1186/1477-7827-2-12 Sarosiek B, Dryl K, Kucharczyk D, Żarski D, Kowalski RK (2014) Motility parameters of perch spermatozoa (Perca fluviatilis L.) during short-term storage with antioxidants addition. Aquacult Int 22:159–165. https://doi.org/10.1007/s10499-013-9679-9 Shaliutina A, Dzyuba B, Hulak M, Boryshpolets S, Li P, Linhart O (2012) Evaluation of spermiation indices with multiple sperm collections in endangered sterlet (Acipenser ruthenus). Reprod Domest Anim 47:479–484. https://doi.org/10.1111/j.1439-0531.2011.01907.x Shaliutina A, Hulak M, Gazo I, Linhartova P, Linhart O (2013) Effect of short-term storage on quality parameters, DNA integrity, and oxidative stress in Russian (Acipenser gueldenstaedtii) and Siberian (Acipenser baerii) sturgeon sperm. Anim Reprod Sci 139:127–135. https://doi.org/10.1016/j.anireprosci.2013.03.006 Stoss J, Refstie T (1983) Short-term storage and cryopreservation of milt from Atlantic salmon and sea trout. Aquaculture 30:229–236. https://doi.org/10.1016/0044-8486(83)90165-5 Trigo P, Merino O, Figueroa E, Valdebenito I, Sánchez R, Risopatrón J (2015) Effect of short-term semen storage in salmon (Oncorhynchus mykiss) on sperm functional parameters evaluated by flow cytometry. Andrologia 47:407–411. https://doi.org/10.1111/and.12276 Ulloa-Rodríguez P, Contreras P, Dumorné K, Lee-Estevez M, Díaz R, Figueroa E, Valdebenito I, Risopatrón J, Farías JG (2018) Patagonian blenny (Eleginops maclovinus) spermatozoa quality after storage at 4 ºC in Cortland medium. Anim Reprod Sci 197:117–125. https://doi.org/10.1016/j.anireprosci.2018.08.019 Vandeputte M, Launey S (2004) The genetic management of fish domestication. Prod Anim 17:237–242 Zi JM, Pan XF, MacIsaac HJ, Yang JX, Xu RB, Chen SY, Chang XX (2018) Cyanobacteria blooms induce embryonic heart failure in an endangered fish species. Aquat Toxicol 194:78–85. https://doi.org/10.1016/j.aquatox.2017.11.007