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Carbon dioxide reversibly inhibits sperm motility and fertilizing ability in steelhead (Oncorhynchus mykiss)

Fish Physiology and Biochemistry volume 23, pages 275–281 (2000)Cite this article

Abstract

The effects of different carbon dioxide (CO2) levels on the short-term storage of semen samples from hatchery-produced steelhead (Oncorhynchus mykiss) were evaluated. Sperm motility and fertilizing ability were significantly reduced following 4 h incubation under a relatively modest (≥0.9 kPa = 1%) amount of CO2. The dose-dependent reductions, however, were not the result of cell death as sperm viability was unaltered even at the highest (5.2 kPa = 5.6%) CO2 exposures. Reductions in sperm motility and fertilizing ability were reversible. Although previous work has indicated a direct relationship between salmonid sperm motility and sperm ATP content, the inhibitory effects of CO2 on sperm motility were not the result of reduced sperm ATP levels. Decreasing the pH of the seminal fluid (to below ∼7.5) significantly reduced sperm motility. However, this effect was only observed after prolonged (4 h) exposure; short-term (1 min) exposure to this lowered pH did not alter sperm motility. Moreover, acetazolamide, a carbonic anhydrase inhibitor, attenuated the inhibitory effects of CO2 on sperm motility. These results suggest that CO2 inhibits steelhead sperm motility and therefore fertility in a dose-dependent manner, by reversibly lowering intracellular pH.

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References

  • Ballard, W.M. 1973. Normal embryonic stages for salmonid fishes, based on Salmo gairdneriRichardson and Salvelinus fontinalis(Mitchill). J. Exp. Zool. 184: 7-26.

    Google Scholar 

  • Bencic, D.C., Krisfalusi, M., Cloud, J.G. and Ingermann, R.L. 2000a. Short-term storage of salmonid sperm in air versus oxygen. N. Am. J. Aquaculture 62: 19-25.

    Google Scholar 

  • Bencic, D.C., Krisfalusi, M., Cloud, J.G., and Ingermann, R.L. 2000b. Erratum. Fish Physiol. Biochem. 22: 277-280.

    Google Scholar 

  • Bencic, D.C., Krisfalusi, M., Cloud, J.G. and Ingermann, R.L. 1999a. Maintenance of steelhead trout (Oncorhynchus mykiss) sperm at different in vitrooxygen tensions alters ATP levels and cell functional characteristics. Fish Physiol. Biochem. 21: 193-200.

    Google Scholar 

  • Bencic, D.C., Krisfalusi, M., Cloud, J.G. and Ingermann, R.L. 1999b. ATP levels of chinook salmon (Oncorhynchus tshawytscha) sperm following in vitroexposure to various oxygen tensions. Fish Physiol. Biochem. 20: 389-397.

    Google Scholar 

  • Bernier, N.J. and Randall, D.J. 1998. Carbon dioxide anaesthesia in rainbow trout: effects of hypercapnic level and stress on induction and recovery from anaesthetic treatment. J. Fish Biol. 52: 621-637.

    Google Scholar 

  • Billard, R., Petit, J., Jalabert, B. and Szollosi, D. 1974. Artificial insemination in trout using a sperm diluent. In: The Early Life History of Fish. pp. 715-723. Edited by J.H.S. Blaxter. Springer-Verlag, New York.

    Google Scholar 

  • Boitano, S. and Omoto, C.K. 1991. Membrane hyperpolarization activates trout sperm without an increase in intracellular pH. J. Cell Sci. 98: 343-349.

    Google Scholar 

  • Büyükhatipoglu, S. and Holtz, W. 1978. Preservation of trout sperm in liquid or frozen state. Aquaculture 14: 49-56.

    Google Scholar 

  • Dimberg, K. 1987. High blood CO2levels in rainbow trout exposed to hypercapnia in bicarbonate-rich hard fresh water-a methodological verification. J. Exp. Biol. 134: 463-466.

    Google Scholar 

  • Fish, F.F. 1943. The anesthesia of fish by high carbon dioxide concentrations. Trans. Am. Fish. Soc. 72: 25-29.

    Google Scholar 

  • Gatti, J.L., Billard, R. and Christen, R. 1990. Ionic regulation of the plasma membrane potential of rainbow trout Salmo gairdnerispermatozoa: role in the initiation of sperm motility. J. Cell Physiol. 143: 546-554.

    Google Scholar 

  • Gilderhus, P.A. and Marking, L.L. 1987. Comparative efficacy of 16 anesthetic chemicals on rainbow trout. N. Am. J. Fish. Management 7: 288-292.

    Google Scholar 

  • Gray, A.K., Evans, M.A. and Thorgaard, G.H. 1993. Viability and development of diploid and triploid salmonid hybrids. Aquaculture. 112: 125-142.

    Google Scholar 

  • Henry, R.P., Gilmour, K.M., Wood, C.M. and Perry, S.F. 1997. Extracellular carbonic anhydrase activity and carbonic anhydrase inhibitors in the cirulatory system of fish. Physiol. Zool. 70: 650-650.

    Google Scholar 

  • Holtz, W., Büyükhatipoglu, S., Stoss, J., Oldigs, B. and Langholz, H.-J. 1979. Preservation of trout spermatozoa for varying periods. In: Advances in Aquaculture. pp. 141-142. Edited by T.V.R. Pillay and W.A. Dill. Fishing New Books Ltd., Farnham, Surrey, England.

    Google Scholar 

  • Iwama, G.K., McGeer, J.C. and Pawluk, M.P. 1989. The effects of five fish anesthetics on acid-base balance, hematocrit, blood gases, cortisol and adrenaline in rainbow trout. Can. J. Zool. 67: 2065-2073.

    Google Scholar 

  • Johnson, C.H., Clapper, D.L., Winkler, M.M., Lee, H.C. and Epel, D. A volatile inhibitor immobilizes sea urchin sperm in semen by depressing the intracellular pH. Dev. Biol. 98: 493-501.

  • Lahnsteiner, F., Berger, B., Weismann, T. and Patzner, R.A. 1998. Determination of semen quality of the rainbow trout, Oncorhynchus mykiss, by sperm motility, seminal plasma parameters and spermatozoal metabolism. Aquaculture 163: 163-181.

    Google Scholar 

  • Lee, H.C., Johnson, C. and Epel, D. 1983. Changes in intracellular pH associated with initiation of motility and acrosome reaction of sea urchin sperm. Dev. Biol. 95: 31-45.

    Google Scholar 

  • Moccia, R.D. and Munkittrick, K.R. 1987. Relationship between the fertilization of rainbow trout (Salmo gairdneri) eggs and the motility of spermatozoa. Theriogenology 27: 679-688.

    Google Scholar 

  • Morisawa, S. and Morisawa, M. 1988. Induction of potential for sperm motility by bicarbonate and pH in rainbow trout and chum salmon. J. Exp. Biol. 136: 13-22.

    Google Scholar 

  • Munkittrick, K.R. and Moccia, R.D. 1987. Seasonal changes in the quality of rainbow trout (Salmo gairdneri) semen: effect of a delay in stripping on spermatocrit, motility, volume and seminal plasma constituents. Aquaculture 64: 147-156.

    Google Scholar 

  • Perry, S.F. 1985. Carbon dioxide excretion in fishes. Can. J. Zool. 64: 565-572.

    Google Scholar 

  • Prince, A.M., Low, S.E. and Lissimore, T.J. 1995. Sodium bicarbonate and acetic acid: an effective anaesthetic for field use. N. Am. J. Fish. Management 15: 170-172.

    Google Scholar 

  • Robitaille, P-M.L., Mumford, K.G. and Brown, G.G. 1987. 31P nuclear magnetic resonance study of trout spermatozoa at rest, after motility and during short-term storage. Biochem. Cell. Biol. 65: 474-485.

    Google Scholar 

  • Stevens, D.E. and Randall, D.J. 1967. Changes of gas concentrations in blood and water during moderate swimming activity in rainbow trout. J. Exp. Biol. 46: 329-337.

    Google Scholar 

  • Stoss, J. 1983. Fish gamete preservation and spermatozoan physiology. In: Fish Physiology. pp. 305-350. Edited by W. Hoar, D. Randall and E. Donaldson. Academic Press, NY.

    Google Scholar 

  • Stoss, J., Büyükhatipoglu, S. and Holtz, W. 1978. Short-term and cryopreservation of rainbow trout (Salmo gairdneriRichardson) sperm. Ann. Biol. Anim. Biochim. Biophys. 18: 1077-1082.

    Google Scholar 

  • Terner, C. 1986. Evaluation of salmonid sperm motility for cryopreservation. Prog. Fish-Cult. 48: 230-232.

    Google Scholar 

  • Wood, C.M., Walsh, P.J., Thomas, S. and Perry, S.F. 1990. Control of red blood cell metabolism in rainbow trout after exhaustive exercise. J. Exp. Biol. 154: 491-507.

    Google Scholar 

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Author notes

  1. D.C. Bencic

    Present address: Department of Cell Biology and Anatomy, University of North Carolina, Chapel Hill, NC, 27599-7090, USA

Authors and Affiliations

  1. Department of Biological Sciences and Center for Reproductive Biology, University of Idaho, P.O. Box 443051, Moscow, ID, 83844-3051, USA

    D.C. Bencic, J.G. Cloud & R.L. Ingermann

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  1. D.C. Bencic
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  2. J.G. Cloud
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  3. R.L. Ingermann
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Bencic, D., Cloud, J. & Ingermann, R. Carbon dioxide reversibly inhibits sperm motility and fertilizing ability in steelhead (Oncorhynchus mykiss). Fish Physiology and Biochemistry 23, 275–281 (2000). https://doi.org/10.1023/A:1011157329855

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  • DOI: https://doi.org/10.1023/A:1011157329855

  • acetazolamide
  • adenosine triphosphate
  • carbon dioxide
  • fertilization
  • motility
  • pH
  • sperm
  • trout

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