The present study was designed to evaluate sperm phenotypic variables during in vivo and in vitro storage following multiple sperm stripping in common carp (Cyprinus carpio L.). Each male was injected 3 times with carp pituitary 3 days apart. Sperm was stored in vivo in the body cavity for 0.5 days (Fresh sperm) and 3 days (Old sperm) after hormonal stimulation. Then sperm was collected and diluted with a carp extender at a ratio of 1:1, and stored in vitro on ice for 0, 3, and 6 days. The phenotypic parameters, including the number of total motile spermatozoa, number of fast motile spermatozoa, number of motile spermatozoa, percentage of fast motile spermatozoa, and percentage of spermatozoa motility were the major components of principal component analysis (PCA). In general, Fresh sperm from the first stripping showed slightly better quality than Old sperm from the second and third stripping, especially in the phenotypic parameters of a number of total spermatozoa and a number of total motile spermatozoa (P < 0.05). The highest kinetic and quantitative spermatozoa variables were obtained in Fresh and Old sperm just after sperm collection (0-day storage in vitro), and then they were decreased during the period of in vitro storage up to 6 days (P < 0.05). However, the fertilization, hatching, and malformation rates from Fresh sperm were similar compared with the Old sperm. Sperm could be stripped 0.5 days post hormonal treatment and stored in vitro up to 6 days with good fertilization performance (fertility, hatching, and malformation rates were 92.5%, 91.5%, and 1.3%, respectively). Therefore, our results suggested that multiple hormonal treatments with multiple stripping could be used in artificial reproduction in common carp.

College of Animal Science and Technology Sichuan Agricultural University Chengdu Sichuan Province China

Faculty of Fisheries and Protection of Waters South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses Research Institute of Fish Culture and Hydrobiology University of South Bohemia in Ceske Budejovice Zatisi 728 2 389 25 Vodnany Czech Republic

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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 DOI

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 PubMed DOI

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 PubMed DOI

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 DOI

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 PubMed DOI

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 DOI

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 DOI

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 DOI

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 DOI

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 PubMed DOI

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 PubMed DOI

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 DOI

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 DOI

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 DOI

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 DOI

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 PubMed DOI PMC

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 PubMed DOI

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 PubMed DOI PMC

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 PubMed DOI PMC

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 DOI

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 DOI

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 DOI

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 DOI

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 DOI

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 PubMed DOI

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 DOI

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 PubMed DOI

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 DOI

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 DOI

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 PubMed DOI PMC

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 DOI

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 DOI

Kowalski RK, Cejko BI (2019) Sperm quality in fish: determinants and affecting factors. Theriogenology 135:94–108 DOI

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 PubMed DOI

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 PubMed DOI

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 DOI

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 DOI

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 PubMed DOI

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 DOI

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 PubMed DOI PMC

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 DOI

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 DOI

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 DOI

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 PubMed DOI

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 PubMed DOI

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 PubMed DOI

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 DOI

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 DOI

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 PubMed DOI

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 DOI

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 DOI

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 DOI

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 DOI

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 DOI

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 PubMed DOI

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 PubMed DOI

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 DOI

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 PubMed DOI

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 PubMed DOI

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 PubMed DOI