Fertilization of freshwater fish occurs in the environment which negatively affects a lifespan of gametes mostly due to the osmotic shock; therefore, male gametes should reach the female gamete, as soon as possible. The existence of mechanisms controlling the encounter of gametes would be highly expedient in this case. By analogy with other species for which guidance was demonstrated, it is likely that this control may be performed by ovarian fluid or substances released by eggs. The aim was to study the effect of ovarian fluid and egg-released substances on spermatozoa behavior in sterlet. It was found that the presence of a particular concentration of ovarian fluid (30% solution in water) had an inhibiting effect on spermatozoa motility initiation. Lower concentrations of the ovarian fluid improved the longevity of spermatozoa and did not affect their trajectories. Test of chemotactic response (using a microcapillary injection of fluids into the suspension of motile spermatozoa) showed no effect of ovarian fluid on spermatozoa behavior, while at the same time, the attracting effect of the egg-conditioned medium was evident (i.e., due to some substances released from the eggs during their contact with freshwater). The results of the fertilization test showed that the presence of ovarian fluid prevented the eggs from losing the fertilizing ability due to the contact with water, as well as promoted the spermatozoa to fertilize the eggs during a longer period of time. Thus, the combined physicochemical action of "female factors" affects sterlet gametes during fertilization and may be involved in the guidance and selection mechanisms.

Department of Engineering Mathematics University of Bristol Bristol BS8 1UB UK

University of South Bohemia in České Budějovice Faculty of Fisheries and Protection of Waters South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses Zátiší 728 2 389 25 Vodňany Czech Republic

Zobrazit více v PubMed

Alavi SMH, Cosson J, Karami M, Mojazi Amiri B, Akhoundzadeh MA (2004) Spermatozoa motility in the Persian sturgeon, Acipenser persicus: effects of pH, dilution rate, ions and osmolality. Reproduction 128:819–828. https://doi.org/10.1530/rep.1.00244 PubMed DOI

Alavi SMH, Gela D, Rodina M, Linhart O (2011) Roles of osmolality, calcium - potassium antagonist and calcium in activation and flagellar beating pattern of sturgeon sperm. Comp Biochem Physiol A Mol Integr Physiol 160:166–174. https://doi.org/10.1016/j.cbpa.2011.05.026 PubMed DOI

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

Amanze D, Iyengar A (1990) The micropyle - a sperm guidance-system in teleost fertilization. Development 109:495–500 DOI

Bondarenko O, Dzyuba B, Cosson J, Yamaner G, Prokopchuk G, Psenicka M, Linhart O (2013) Volume changes during the motility period of fish spermatozoa: interspecies differences. Theriogenology 79:872–881. https://doi.org/10.1016/J.THERIOGENOLOGY.2013.01.005 PubMed DOI

Cherr GN, Morisawa M, Vines CA, Yoshida K, Smith EH, Matsubara T, Pillai MC, Griffin FJ, Yanagimachi R (2008) Two egg-derived molecules in sperm motility initiation and fertilization in the Pacific herring (Clupea pallasi). Int J Dev Biol 52:743–752. https://doi.org/10.1387/ijdb.072566gc PubMed DOI

Cosson J, Billard R, Gibert C et al (1999) Ionic factors regulating the motility of fish sperm. In: Gagnon C (ed) The male gamete: from basic to clinical applications. Cache River Press, Vienna II, pp 161–186

Debus L, Winkler M, Billard R (2002) Structure of micropyle surface on oocytes and caviar grains in sturgeons. Int Rev Hydrobiol 87:585–603. https://doi.org/10.1002/1522-2632(200211)87:5/6<585::AID-IROH585>3.0.CO;2-8 DOI

Dettlaff TA, Ginsburg AS, Schmalhausen OI (1993) Sturgeon fishes: developmental biology and aquaculture. Springer Science & Business Media, Berlin Heidelberg DOI

Dietrich GJ, Wojtczak M, Dobosz S et al (2007) Characterization of whitefish (Coregonus lavaretus) sperm motility: Effects of pH, cations and ovarian fluid. Adv Limnol 60:159–170

Dietrich GJJ, Wojtczak M, Słowińska M et al (2008) Effects of ovarian fluid on motility characteristics of rainbow trout (Oncorhynchus mykiss Walbaum) spermatozoa. J Appl Ichthyol 24:503–507. https://doi.org/10.1111/j.1439-0426.2006.01130.x DOI

Diogo P, Soares F, Dinis MT, Cabrita E (2010) The influence of ovarian fluid on Solea senegalensis sperm motility. J Appl Ichthyol 26:690–695. https://doi.org/10.1111/j.1439-0426.2010.01554.x DOI

Dzyuba B, Cosson J, Boryshpolets S, Dzyuba V, Rodina M, Bondarenko O, A.Shaliutina, Linhart O (2013) Motility of sturgeon spermatozoa can sustain successive activations episodes. Anim Reprod Sci 138:305–313. https://doi.org/10.1016/j.anireprosci.2013.02.011 PubMed DOI

Dzyuba B, Cosson J, Boryshpolets S, Bondarenko O, Dzyuba V, Prokopchuk G, Gazo I, Rodina M, Linhart O (2014) In vitro sperm maturation in sterlet, Acipenser ruthenus. Reprod Biol 14:160–163. https://doi.org/10.1016/J.REPBIO.2014.01.003 PubMed DOI

Dzyuba V, Cosson J, Dzyuba B, Rodina M (2015) Oxidative stress and motility in tench Tinca tinca spermatozoa. Czech J Anim Sci 60:250–255. https://doi.org/10.17221/8238-CJAS DOI

Dzyuba V, Shelton WL, Kholodnyy V, Boryshpolets S, Cosson J, Dzyuba B (2019) Fish sperm biology in relation to urogenital system structure. Theriogenology 132:153–163. https://doi.org/10.1016/j.theriogenology.2019.04.020 PubMed DOI

Eisenbach M, Giojalas LC (2006) Sperm guidance in mammals — an unpaved road to the egg. Nat Rev Mol Cell Biol 7:276–285. https://doi.org/10.1038/nrm1893 PubMed DOI

Elofsson H, Mcallister BG, Kime DE, Mayer I, Borg B (2003a) Long lasting stickleback sperm; is ovarian fluid a key to success in fresh water? J Fish Biol 63:240–253. https://doi.org/10.1046/j.1095-8649.2003.00153.x DOI

Elofsson H, Van Look K, Borg B, Mayer I (2003b) Influence of salinity and ovarian fluid on sperm motility in the fifteen-spined stickleback. J Fish Biol 63:1429–1438. https://doi.org/10.1111/j.1095-8649.2003.00256.x DOI

Faramarzi M, Kiaalvandi S, Iranshahi F (2011) Influence of ceolomic fluid on sperm motility characteristics in angel fish (Pterophyllum scalare schultze) during spawning season and its chemical composition. Glob Vet 6:324–328

Firman RC, Gasparini C, Manier MK, Pizzari T (2017) Postmating female control: 20 years of cryptic female choice. Trends Ecol Evol 32:368–382. https://doi.org/10.1016/j.tree.2017.02.010 PubMed DOI PMC

Galvano PM, Johnson K, Wilson CC, Pitcher TE, Butts IAE (2013) Ovarian fluid influences sperm performance in lake trout, Salvelinus namaycush. Reprod Biol 13:172–175. doi: 10.1016/j.repbio.2013.02.001

Goetz FW, Coffman MA (2000) Storage of unfertilized eggs of rainbow trout (Oncorhynchus mykiss) in artificial media. Aquaculture 184:267–276. https://doi.org/10.1016/S0044-8486(99)00327-0 DOI

Golpour A, Esfandyari M, Dadras H (2015) The influence of ovarian fluid on the sperm physiology of Rutilus kutum. Iran J Fish Sci 14:818–825

Hart NH (1990) Fertilization in teleost fishes: mechanisms of sperm-egg interactions. Int Rev Cytol 121:1–66. https://doi.org/10.1016/S0074-7696(08)60658-0 PubMed DOI

Hatef A, Niksirat H, Alavi SMHSMH (2009) Composition of ovarian fluid in endangered Caspian brown trout, Salmo trutta caspius, and its effects on spermatozoa motility and fertilizing ability compared to freshwater and a saline medium. Fish Physiol Biochem 35:695–700. https://doi.org/10.1007/s10695-008-9302-6 PubMed DOI

Johnson SL, Villarroel M, Rosengrave P, Carne A, Kleffmann T, Lokman PM, Gemmell NJ (2014) Proteomic analysis of Chinook salmon (Oncorhynchus tshawytscha) ovarian fluid. PLoS One 9:e104155. https://doi.org/10.1371/journal.pone.0104155 PubMed DOI PMC

Kaupp UB (2012) 100 years of sperm chemotaxis. J Gen Physiol 140:583–586. https://doi.org/10.1085/jgp.201210902 PubMed DOI PMC

Kaupp UB, Kashikar ND, Weyand I (2008) Mechanisms of sperm chemotaxis. Annu Rev Physiol 70:93–117. https://doi.org/10.1146/annurev.physiol.70.113006.100654 PubMed DOI

Kekäläinen J, Evans JP (2018) Gamete-mediated mate choice: towards a more inclusive view of sexual selection. Proc R Soc B Biol Sci 285:20180836. https://doi.org/10.1098/rspb.2018.0836 DOI

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/10.1111/raq.12378

Lahnsteiner F (2002) The influence of ovarian fluid on the gamete physiology in the Salmonidae. Fish Physiol Biochem 27:49–59. https://doi.org/10.1023/B:FISH.0000021792.97913.2e DOI

Liao WB, Huang Y, Zeng Y, Zhong MJ, Luo Y, Lüpold S (2018) Ejaculate evolution in external fertilizers: influenced by sperm competition or sperm limitation? Evolution (N Y) 72:4–17. https://doi.org/10.1111/evo.13372 DOI

Liley NRR, Tamkee P, Tsai R, Hoysak DJJ (2002) Fertilization dynamics in rainbow trout (Oncorhynchus mykiss): effect of male age, social experience, and sperm concentration and motility on in vitro fertilization. Can J Fish Aquat Sci 59:144–152. https://doi.org/10.1139/f01-202 DOI

Lillie FR (1912) The production of sperm iso-agglutinins by ova. Science (80-) 36:527–530 DOI

Litvak MK, Trippel EA (1998) Sperm motility patterns of Atlantic cod (Gadus morhua) in relation to salinity: effects of ovarian fluid and egg presence. Can J Fish Aquat Sci 55:1871–1877. https://doi.org/10.1139/f98-093 DOI

Moorehead WR, Biggs HG (1974) 2 Amino 2 methyl 1 propanol as the alkalizing agent in an improved continuous flow cresolphthalein complexone procedure for calcium in serum. Clin Chem 20:1458–1460 DOI

Morisawa M (1985) Initiation mechanism of sperm motility at spawning in teleosts. Zool Sci 2:605–615

Morisawa M (1994) Cell signaling mechanisms for sperm motility. Zool Sci 11:647–662

Niksirat H, Andersson L, Golpour A, Chupani L, James P (2017) Quantification of egg proteome changes during fertilization in sterlet Acipenser ruthenus. Biochem Biophys Res Commun 490:189–193. https://doi.org/10.1016/j.bbrc.2017.06.019 PubMed DOI

Pillai MC, Shields TS, Yanagimachi R, Cherr GN (1993) Isolation and partial characterization of the sperm motility initiation factor from eggs of the pacific herring, Clupea pallasi. J Exp Zool 265:336–342. https://doi.org/10.1002/jez.1402650316 DOI

Prokopchuk G, Dzyuba B, Rodina M, Cosson J (2016) Control of sturgeon sperm motility: antagonism between K PubMed DOI

Psenicka M, Vancova M, Koubek P, Tesitel J, Linhart O (2009) Fine structure and morphology of sterlet (Acipenser ruthenus L. 1758) spermatozoa and acrosin localization. Anim Reprod Sci 111:3–16. https://doi.org/10.1016/j.anireprosci.2008.02.006 PubMed DOI

Purchase CF, Earle PT (2012) Modifications to the imagej computer assisted sperm analysis plugin greatly improve efficiency and fundamentally alter the scope of attainable data. J Appl Ichthyol 28:1013–1016. https://doi.org/10.1111/jai.12070 DOI

Ribeiro DC, Chagas JMA, Bashiyo-Silva C, Costa RS, Veríssimo-Silveira R, Ninhaus-Silveira A (2017) Oocyte viability and cortical activation under different salt solutions in Prochilodus lineatus (Teleostei: Prochilodontidae). Reprod Domest Anim 52:932–938. https://doi.org/10.1111/rda.12997 PubMed DOI

Riffell JA, Krug PJ, Zimmer RK (2002) Fertilization in the sea: the chemical identity of an abalone sperm attractant. J Exp Biol 205:1439–1450 DOI

Rosengrave P, Montgomerie R, Metcalf VJ, McBride K, Gemmell NJ (2009) Sperm traits in Chinook salmon depend upon activation medium: implications for studies of sperm competition in fishes. Can J Zool 87:920–927. https://doi.org/10.1139/Z09-081 DOI

Safarzadenia M, Yazdanparast T, Taati MM, Esfahani HK (2013) Storage of unfertilized eggs of grass carp, Ctenopharyngodon idella, in artificial media. Aquac Aquarium Conserv Legis - Int J Bioflux Soc (AACL Bioflux) 6:478–485

Turner E, Montgomerie R (2002) Ovarian fluid enhances sperm movement in Arctic charr. J Fish Biol 60:1570–1579. https://doi.org/10.1111/j.1095-8649.2002.tb02449.x DOI

Wilson-Leedy JG, Ingermann RL (2007) Development of a novel CASA system based on open source software for characterization of zebrafish sperm motility parameters. Theriogenology 67:672. https://doi.org/10.1016/j.theriogenology.2006.10.003 DOI

Wojtczak M, Dietrich GJ, Słowińska M, Dobosz S, Kuźmiński H, Ciereszko A (2007) Ovarian fluid pH enhances motility parameters of rainbow trout (Oncorhynchus mykiss) spermatozoa. Aquaculture 270:259–264. https://doi.org/10.1016/j.aquaculture.2007.03.010 DOI

Yanagimachi R, Harumi T, Matsubara H, Yan W, Yuan S, Hirohashi N, Iida T, Yamaha E, Arai K, Matsubara T, Andoh T, Vines C, Cherr GN (2017) Chemical and physical guidance of fish spermatozoa into the egg through the micropyle. Biol Reprod 96:780–799. https://doi.org/10.1093/biolre/iox015 PubMed DOI PMC

Yoshida M, Inaba K, Morisawa M (1993) Sperm chemotaxis during the process of fertilization in the ascidians ciona savignyi and ciona intestinalis. Dev Biol 157:497–506. https://doi.org/10.1006/dbio.1993.1152 PubMed DOI

Yoshida M, Murata M, Inaba K, Morisawa M (2002) A chemoattractant for ascidian spermatozoa is a sulfated steroid. Proc Natl Acad Sci U S A 99:14831–14836. https://doi.org/10.1073/pnas.242470599 PubMed DOI PMC

Zarski D, Horváth Á, Bernáth G et al (2014) Application of different activating solutions to in vitro fertilization of crucian carp, Carassius carassius (L.), eggs. Aquac Int 22:173–184. https://doi.org/10.1007/s10499-013-9692-z DOI