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Sublethal effects of a carbamate pesticide on pheromonal mediated endocrine function in mature male Atlantic salmon (Salmo salar L.) parr

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Abstract

The sublethal effect of the carbamate pesticide carbofuran on the priming pheromonal system of Atlantic salmon (Salmo salar L.) was investigated. Previous studies have demonstrated that ovulated female salmon release a priming pheromone in their urine (considered to be an F-type prostaglandin) which is subsequently detected by mature male salmon and results in increased levels of plasma sex steroids and expressible milt. In the present study, electrophysiological recordings from the olfactory epithelium of mature male salmon parr indicated that the responses to prostaglandin F (PGF) were significantly reduced at nominal concentrations of carbofuran as low as 1.0 µg l-1, and the threshold of detection was reduced 10-fold. A 5 day exposure to carbofuran significantly reduced the ability of male parr to respond to PGF stimulation. The priming effect of PGF on milt and plasma 17,20β-dihydroxy-4-pregnen-3-one levels were abolished at water concentrations at and above 2.7 µg l-1. In addition, the priming effect of PGF on plasma testosterone and 11-ketotestosterone concentrations was abolished at water carbofuran concentrations above 6.5 µg l-1. Exposure to similar concentrations of carbofuran also resulted in a reduction in the levels of free and glucuronidated steroids in the bile of PGF primed male parr. The effect of carbofuran on the priming response did not appear to be due to a direct effect on the testes, since the ability of testes to respond to pituitary extract stimulation in vitro was not impaired in carbofuran-exposed males. Carbofuran appeared to reduce significantly or abolish the priming pheromonal system in mature male parr by directly affecting the ability of the olfactory system to detect PGF, although the toxicological mechanism involved is as yet unknown. The results are therefore discussed in relation to the possible sublethal effects of carbofuran on reproduction in the Atlantic salmon.

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References cited

  • Defraipont, M. and Sorenson, P.W. 1993. Exposure to the pheromone 17α,20ß-dihydroxy-4-pregnen-3-one enhances the behavioural spawning success, sperm production and sperm modility of male goldfish. Anim. Behav. 46: 245–256.

    Google Scholar 

  • Eisler, R. 1985. Carbofuran hazards to fish, wildlife, and invertebrates: a synaptic review. U.S. Fish Wildl. Serv. Biol. Rep. 85(1.3). 1–36.

    Google Scholar 

  • Evans, R.E. and Hara, T.J. 1985. The characteristics of the electro-olfactogram (EOG): its loss and recovery following olfactory nerve section in the rainbow trout (Oncorhynchus mykiss). Brain Res. 330: 65–75.

    Google Scholar 

  • Hidaka, H. and Tatsukawa, R. 1989. Avoidance by olfaction in a fish, medaka (Oryzias latipes), to aquatic contaminants. Environ. Poll. 56: 299–309.

    Google Scholar 

  • Honda, H. 1980. Female sex pheromone of rainbow trout, Salmo gairdneri, involved in courtship behaviour. Bull. Jap. Soc. Sci. Fish. 46: 1109–1112.

    Google Scholar 

  • Ishida, Y. and Kobayashi, H. 1995. Avoidance behavior of carp to pesticides and decrease of the avoidance threshold by addition of sodium lauryl sulfate. Fish. Sci. 61: 441–446.

    Google Scholar 

  • Liley, N.R., Olsén, K.H., Foote, C.J. and Van Der Kraak, G.J. 1993. Endocrine changes associated with spawning behavior in male kokanee salmon (Oncorhynchus nerka) and the effects of anosmia. Horm. Behav. 27: 470–487.

    Google Scholar 

  • Matthiessen, P., Sheahan, D., Harrison, R., Kirby, M., Rycroft, R., Turnbull, A., Volkner, C. and Williams, R. 1995. Use of a Gammarus pulex bioassay to measure the effects of transient carbofuran runoff from farmland. Ecotoxicol. Environ. Safetey 30: 111–119.

    Google Scholar 

  • Moore, A. 1994. An electrophysiological study on the effects of pH on olfaction in mature male Atlantic salmon (Salmo salar) parr. J. Fish Biol. 45: 493–502.

    Google Scholar 

  • Moore, A. and Scott, A.P. 1992. 17α,20ß-dihydroxy-4-pregnen-3-one 20-sulphate is a potent odorant in precocious male Atlantic salmon (Salmo salar L.) parr which have been preexposed to the urine of ovulated females. Proc. Roy. Soc. Lond. 249B: 205–209.

    Google Scholar 

  • Moore, A. and Waring, C.P. 1995. Seasonal changes in olfactory sensitivity of mature male Atlantic salmon (Salmo salar L.) parr to prostaglandins. In Proc. 5th Int. Symp. Reproductive Physiology Fish. p. 273. Edited by F.W. Goetz and P. Thomas. University of Texas Press, Austin.

    Google Scholar 

  • Moore, A. and Waring, C.P. 1996a. Sublethal effects of the pesticide Diazinon on olfactory function in mature male Atlantic salmon parr. J. Fish Biol. 48: 758–775.

    Google Scholar 

  • Moore, A. and Waring, C.P. 1996b. Electrophysiological and endocrinological evidence that F-series prostaglandins function as priming pheromones in mature male Atlantic salmon (Salmo salar L.) parr. J. Exp. Biol. 199: 2307–2316.

    Google Scholar 

  • Nagler, J.J., Scott, A.P., Tyler, C.R. and Sumpter, J.P. 1996. Gonadotropins I and II do not stimulate the in vitro secretion of 17α,20ß-dihydroxy-4-pregnen-3-one 20-sulphate by rainbow trout gonads during final sexual maturation. Fish Physiol. Biochem. 15: 149–156.

    Google Scholar 

  • Olsén, K.H. and Liley, N.R. 1993. The significance of olfaction and social cues in milt availability, sexual hormone status, and spawning behavior of male rainbow trout (Oncorhynchus mykiss). Gen. Comp. Endocrinol. 89: 107–118.

    Google Scholar 

  • Scott, A.P. and Liley, N.R. 1994. Dynamics of excretion of 17α,20ß-dihydroxy-4-pregnen-3-one 20-sulphate, and the glucuronides of testosterone and 17ß-Oestradiol, by urine of reproductively mature male and female rainbow trout (Oncorhynchus mykiss). J. Fish Biol. 44: 117–129.

    Google Scholar 

  • Scott, A.P., Sheldrick, E.L. and Flint, A.P.F. 1982. Measurement of 17α,20ß-dihydroxy-4-pregnen-3-one in plasma of trout (Salmo gairdneri Richardson): seasonal changes and response to salmon pituitary extract. Gen. Comp. Endocrinol. 46: 444–451.

    Google Scholar 

  • Scott, A.P., MacKenzie, D.S. and Stacey, N.E. 1984. Endocrine changes during natural spawning in the white sucker, Catostomus commersonii. II. Steroid hormones. Gen. Comp. Endocrinol. 56: 349–359.

    Google Scholar 

  • Verma, S.R., Bansal, S.K., Gupta, A.K., Pal, N., Tyagi, A.K., Bhatnagar, M.C., Kumar, V. and Dalela, R.C. 1982. Bioassay trials with twenty three pesticides to a freshwater teleost, Saccobranchus fossilis. Water Res. 16: 525–529.

    Google Scholar 

  • Waring, C.P. and Moore, A. 1995. F-series prostaglandins have a pheromonal priming effect on mature male Atlantic salmon (Salmo salar) parr. In Proc. 5th Int. Symp. Reproductive Physiology of Fish. pp. 255–257. Edited by F.W. Goetz and P. Thomas. University of Texas Press, Austin.

    Google Scholar 

  • Waring, C.P., Moore, A. and Scott, A.P. 1996. Milt and endocrine responses of mature male Atlantic salmon (Salmo salar L.) parr to water-borne testosterone, 17,20ß-dihydroxy-4-pregnen-3-one 20-sulfate, and the urines from adult female and male salmon. Gen. Comp. Endocrinol. 103: 142–149.

    Google Scholar 

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Waring, C., Moore, A. Sublethal effects of a carbamate pesticide on pheromonal mediated endocrine function in mature male Atlantic salmon (Salmo salar L.) parr. Fish Physiology and Biochemistry 17, 203–211 (1997). https://doi.org/10.1023/A:1007747316943

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  • DOI: https://doi.org/10.1023/A:1007747316943

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