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Sex-related differences in the organismal and cellular stress response in juvenile salmon exposed to treated bleached kraft mill effluent

Fish Physiology and Biochemistry volume 29, pages 173–179 (2003)Cite this article

Abstract

Exposure of fish to stressors can elicit biochemical and organismal changes at multiple levels of biological organization collectively known as stress responses. The organismal (plasma glucose and cortisol levels) and cellular (hepatic hsp70) stress responses in fish have been studied in several species, but little is known about sex-related differences in these responses. In this study, we exposed sexually immature juvenile chinook salmon (Oncorhynchus tshawytscha) to bleached kraft mill effluent (BKME: 0%, 1%, and 10% v/v) for 30 days and then measured components of their organismal and cellular stress responses. Males exposed to 1% BKME had higher levels of plasma glucose than females. Plasma cortisol levels were unaffected in females exposed to BKME, but males exposed to 10% BKME had significantly higher levels of plasma cortisol relative to non-exposed males. While exposure to BKME did not affect hsp70 levels in males, females exposed to 1% BKME had higher levels of hsp70 relative to non-exposed and 10% BKME groups. Within any given treatment, females had higher levels of hsp70 relative to males. This study demonstrates that sex-related differences exist in commonly used indicators of stress in fish, and points out the importance of considering the sex of the fish in stress research.

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References

  • Aaltonen, T.M., Jokinen, E.I., Lappivaara, J., Markkula, S.E., Salo, H.M., Leppanen, H. and Lammi, R., 2000. Effects of primaryand secondary-treated bleached kraft mill effluents on the immune system and physiological parameters of roach. Aquat. Toxicol. 51: 55–67.

    Article  PubMed  CAS  Google Scholar 

  • Afonso, L.O.B., Smith, J.L., Ikonomou, M.G. and Devlin, R.H. 2002. Y-chromosomal DNA markers for discrimination of chemical substance and effluent effects on sexual differentiation in salmon. Env. Health Perspec. 110: 881–887.

    CAS  Google Scholar 

  • Barton, B.A. and Iwama, G.K. 1991. Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Ann. Rev. of Fish Diseases. 1: 3–26.

    Article  Google Scholar 

  • Basu, N., Nakano, T., Grau, E.G. and Iwama, G.K. 2001. The effects of cortisol on heat shock protein 70 levels in two fish species. Gen. Comp. Endocrinol. 124: 97–105.

    Article  PubMed  CAS  Google Scholar 

  • Basu, N., Todgham, A.E., Ackerman, P.A., Bibeau, M.R., Nakano, K., Schulte, P.M. and Iwama, G.K. 2002. Heat shock protein genes and their functional significance in fish. Gene 295: 173–183.

    Article  PubMed  CAS  Google Scholar 

  • Colborn, T., vom Saal, F.S. and Soto, A.M. 1993. Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environ. Health Perspect. 101: 378–384.

    PubMed  CAS  Google Scholar 

  • Dubeau, S.F., Pan, F., Tremblay, G.C. and Bradley, T.M. 1998. Thermal shock of salmon in vivoinduces the heat shock protein (Hsp70) and confers protection against osmotic shock. Aquaculture 168: 311–323.

    Article  CAS  Google Scholar 

  • Duffy, L.K., Scofield, E., Rodgers, T., Patton, M. and Bowyer, R.T. 1999. Comparative baseline levels of mercury, hsp70 and hsp60 in subsistence fish from the Yukon-Kuskokwim delta region of Alaska. Comp. Biochem. Physiol. Toxicol. Pharmacol. 124: 181–186.

    CAS  Google Scholar 

  • Feder, M.E. and Hofmann, G.E. 1999. Heat shock proteins, molecular chaperones and the stress response: Evolutionary and ecological physiology. Ann. Rev. Physiol. 61: 243–282.

    Article  CAS  Google Scholar 

  • Forsyth, R.B., Candido, E.P.M., Babich, S.L. and Iwama, G.K. 1997. Stress protein expression in coho salmon with bacterial kidney disease. J. Aquat. Anim. Health 9: 18–25.

    Article  Google Scholar 

  • Fournier, M., Lacroix, A., Voccia, I. and Brousseau, P. 1998. Phagocytic and metabolic activities of macrophages from mummichog naturally exposed to pulp mill effluents in the Miramichi River. Ecotoxicol. Environ. Saf. 40: 177–183.

    Article  PubMed  CAS  Google Scholar 

  • Hontela, A. 2000. Endocrine biomarkers: hormonal indicators of sublethal toxicity in fishes. In: Use of biomarkers for environmental quality assessment. pp. 187–204. Edited by L. Lagadic, Th. Caquet, J.C. Amiard and F. Ramade. Science Publishers Incorporated, USA.

    Google Scholar 

  • Hontela, A., Rasmussen, J.B., Audet, C. and Chevalier, G. 1992. Impaired cortisol stress response in fish from environments polluted by PAHs, PCBs, and mercury. Arch. Environ. Contam. Toxicol. 22: 278–283.

    Article  PubMed  CAS  Google Scholar 

  • Hontela, A., Daniel, C. and Rasmussen, J.B. 1997. Structural and functional impairment of the hypothalamo-pituitary-interrenal axis in fish exposed to bleached kraft mill effluent in the St Maurice River, Quebec. Ecotoxicol. 6: 1–12.

    Article  CAS  Google Scholar 

  • Iwama, G.K., Vijayan, M.M., Forsyth. R.B. and Ackerman, P.A. 1999. Heat shock proteins and physiological stress in fish. Am. Zool. 39: 901–909.

    CAS  Google Scholar 

  • Janz, D.M., McMaster, M.E., Munkittrick, K.R. and Van Der Kraak, G. 1997. Elevated ovarian follicular apoptosis and heat shock protein-70 expression in white sucker exposed to bleached kraft pulp mill effluent. Toxicol. Appl. Pharmacol. 147: 391–398.

    Article  PubMed  CAS  Google Scholar 

  • Jardine, J.J., Van der Kraak, G.J. and Munkittrick, K.R. 1996. Capture and confinement stress in white sucker exposed to bleached kraft pulp mill effluent. Ecotoxicol. Environ. Saf. 33: 287–298.

    Article  PubMed  CAS  Google Scholar 

  • Knowlton, A.A. and Sun, L. 2001. Heat-shock factor-1, steroid hormones, and regulation of heat-shock protein expression in the heart. Am. J Physiol. Heart Circ. Physiol. 280: H455–H464.

    PubMed  CAS  Google Scholar 

  • Kubokawa. K., Watanabe, T., Yoshioka. M. and Iwata, M. 1999. Effects of acute stress on plasma cortisol, sex steroid hormone and glucose levels in male and female sockeye salmon during the breeding season. Aquaculture 172: 335–349.

    Article  CAS  Google Scholar 

  • Laemmli, I.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680–685.

    Article  PubMed  CAS  Google Scholar 

  • Lappivaara, J. and Oikari. A. 1999. Altered challenge response in whitefish subchronically exposed in areas polluted by bleached kraft mill effluents. Ecotoxicol. Environ. Saf. 42: 212–222.

    Article  PubMed  CAS  Google Scholar 

  • Mommsen, T.P., Vijayan, M.M. and Moon, T.W. 1999. Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev. Fish Biol. Fisher. 9: 211–268.

    Article  Google Scholar 

  • Pankhurst, N.W. and Sharples, D.F. 1992. Effects of capture and confinement on plasma cortisol concentration in the snapper, Patrus auratus. Aust. J. Mar. Freshwater Res. 43: 345–356.

    Article  CAS  Google Scholar 

  • Pottinger. T.G., Balm, P.H.M. and Pickering, A.D. 1995. Sexual maturity modifies the responsiveness of the pituitary-interrenal axis to stress in male rainbow trout. Gen. Comp. Endocrinol. 98: 311–320.

    Article  PubMed  CAS  Google Scholar 

  • Pottinger, T.G., Carrick, T.R., Hughes, S.E. and Balm, P.H.M. 1996. Testosterone, 11-ketotestosterone, and estradiol-17βmodify baseline and stress-induced interrenal and corticotropic activity in trout. Gen. Comp. Endocrinol. 104: 284–295.

    Article  PubMed  CAS  Google Scholar 

  • Sanders, B.M. 1993. Stress proteins in aquatic organisms: an environmental perspective. Crit. Rev. Toxicol. 23: 49–75.

    PubMed  CAS  Google Scholar 

  • Stuart-Kregor, P.A.C., Sumpter, J.P. and Dodd, J.M. 1981. The involvement of gonadotrophin and sex steroids in the control of reproduction in the parr and adults of Atlantic salmon, Salmo salarL. J. Fish Biol. 18: 59–72.

    Article  CAS  Google Scholar 

  • Sunny, F., Jacob, A. and Oommen, O.V. 2002. Sex steroids regulate intermediary metabolism in Oreochromis mossambicus. Endoc. Res. 28: 175–188.

    Article  CAS  Google Scholar 

  • Swanson, P., Bernard, M., Nozaki, M., Suzuki, K., Kawauchi, H. and Dickhoff, W.W. 1989. Gonadotropin I and II in juvenile coho salmon. Fish Physiol. Biochem. 7: 169–176.

    CAS  Google Scholar 

  • Trinder, P. 1969. Determination of glucose in blood using glucose oxidase with an alternative oxygen acceptor. Annal. Clin. Biochem. 6: 24–27.

    CAS  Google Scholar 

  • Van Der Kraak, G.L., Munkittrick, K.R., McMaster, M.E. and MacLatchy, D.L. 1998. A comparison of bleached kraft mill effluent, 17β-estradiol, and β-sitosterol effects on reproductive function in fish. In: Principles and Processes for evaluating endocrine disruption in wildlife. pp. 249–285. Edited by R. Kendall, R. Dickerson, J. Giesy, and W. Suk. Setac Press, USA.

    Google Scholar 

  • Vijayan, M.M., Pereira, C., Forsyth, R.B., Kennedy, C.J. and Iwama, G.K. 1997. Handling stress does not affect the expression of hepatic heat shock protein 70 and conjugation enzymes in rainbow trout treated with β-naphthoflavone. Life Sci. 61: 117–127.

    Article  PubMed  CAS  Google Scholar 

  • Vijayan, M.M., Pereira, C., Kruzynski, G. and Iwama, G.K. 1998. Sublethal concentrations of contaminant induce the expression of hepatic heat shock protein 70 in two salmonids. Aquat. Toxicol. 40: 101–108.

    Article  CAS  Google Scholar 

  • Vijayan, M.M., Takemura, A. and Mommsen, T.P. 2001. Estradiol impairs hyposmoregulatory capacity in the euryhaline tilapia, Oreochromis mossambicus. Am. J. Physiol. Regul. Integr. Comp. Physiol. 281: 1161–1168.

    Google Scholar 

  • Washburn, B.S., Krantz, J.S., Avery, E.H. and Freeland, R.A. 1993. Effects of estrogen on gluconeogenesis and related parameters in male rainbow trout. Am. J. Physiol. 264: 720–725.

    Google Scholar 

  • Williams, J.H., Farag, A.M., Stansbury, M.A., Young, P.A., Bergman, H.L. and Petersen, N.S. 1996. Accumulation of hsp70 in juvenile and adult rainbow trout gill exposed to metalcontaminated water and/or diet. Environ. Toxicol. Chem. 15: 1324–1328.

    Article  CAS  Google Scholar 

  • Winzer, K. Winston, G.W., Becker, W., Van Noorden, C.J.F. and Köehler, A. 2001. Sex-related responses to oxidative stress in primary cultured hepatocytes of European flounder (Platichthys flesusL.). Aquat. Toxicol. 52: 143–155.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. National Research Council of Canada, Institute for Marine Biosciences, Halifax, Nova Scotia, B3S 3Z1, Canada

    L.O.B. Afonso & G.K. Iwama

  2. Department of Natural Resource Sciences, McGill University, Montreal, Quebec, B3S 3Z1, Canada

    N. Basu

  3. Faculty of Agricultural Sciences, The University of British Columbia, Vancouver, British Columbia, V6T 1Z4, Canada

    K. Nakano

  4. Fisheries and Oceans Canada, West Vancouver Laboratory, West Vancouver, British Columbia, V7V 1N6, Canada

    R.H. Devlin

Authors
  1. L.O.B. Afonso
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  2. N. Basu
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  3. K. Nakano
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  4. R.H. Devlin
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  5. G.K. Iwama
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Correspondence to L.O.B. Afonso.

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Afonso, L., Basu, N., Nakano, K. et al. Sex-related differences in the organismal and cellular stress response in juvenile salmon exposed to treated bleached kraft mill effluent. Fish Physiology and Biochemistry 29, 173–179 (2003). https://doi.org/10.1023/B:FISH.0000035939.81588.09

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  • Issue Date:

  • DOI: https://doi.org/10.1023/B:FISH.0000035939.81588.09

  • BKME
  • cortisol
  • environmental pollutants
  • hsp70
  • sex differences
  • stress response

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