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Research Article
Reduced lactate dehydrogenase activity in the heart and suppressed sex hormone levels are associated with female-biased mortality during thermal stress in Pacific salmon
A. G. Little, E. Hardison, K. Kraskura, T. Dressler, T. S. Prystay, B. Hendriks, J. N. Pruitt, A. P. Farrell, S. J. Cooke, D. A. Patterson, S. G. Hinch, E. J. Eliason
Journal of Experimental Biology 2020 223: jeb214841 doi: 10.1242/jeb.214841 Published 28 July 2020
A. G. Little
1Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, Santa Barbara, CA 93106, USA
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  • ORCID record for A. G. Little
E. Hardison
1Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, Santa Barbara, CA 93106, USA
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K. Kraskura
1Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, Santa Barbara, CA 93106, USA
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T. Dressler
1Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, Santa Barbara, CA 93106, USA
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T. S. Prystay
2Fish Ecology and Conservation Physiology Laboratory, Department of Biology and Institute of Environmental and Interdisciplinary Science, Carleton University, Ottawa, ON K1S 5B6, Canada
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B. Hendriks
3Fisheries and Oceans Canada, Cooperative Resource Management Institute, School of Resource and Environmental Management, Simon Fraser University, Burnaby, BC, Canada V5A 1S6
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J. N. Pruitt
1Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, Santa Barbara, CA 93106, USA
4Department of Psychology, Neuroscience & Behaviour, McMaster University, Hamilton, Ontario, Canada L8S 4K1
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A. P. Farrell
5Department of Zoology, University of British Columbia, Vancouver, BC, Canada V6T 1Z4
6Department of Zoology and Faculty of Land and Food Systems, University of British Columbia, Vancouver, BC, Canada V6T 1Z4
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S. J. Cooke
2Fish Ecology and Conservation Physiology Laboratory, Department of Biology and Institute of Environmental and Interdisciplinary Science, Carleton University, Ottawa, ON K1S 5B6, Canada
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D. A. Patterson
3Fisheries and Oceans Canada, Cooperative Resource Management Institute, School of Resource and Environmental Management, Simon Fraser University, Burnaby, BC, Canada V5A 1S6
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S. G. Hinch
7Pacific Salmon Ecology and Conservation Laboratory, Department of Forest and Conservation Sciences, University of British Columbia, Vancouver, BC, Canada V6T 1Z4
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E. J. Eliason
1Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, Santa Barbara, CA 93106, USA
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  • For correspondence: eliason@ucsb.edu
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ABSTRACT

Female-biased mortality has been repeatedly reported in Pacific salmon during their upriver migration in both field studies and laboratory holding experiments, especially in the presence of multiple environmental stressors, including thermal stress. Here, we used coho salmon (Oncorhynchus kisutch) to test whether females exposed to elevated water temperatures (18°C) (i) suppress circulating sex hormones (testosterone, 11-ketotestosterone and estradiol), owing to elevated cortisol levels, (ii) have higher activities of enzymes supporting anaerobic metabolism (e.g. lactate dehydrogenase, LDH), (iii) have lower activities of enzymes driving oxidative metabolism (e.g. citrate synthase, CS) in skeletal and cardiac muscle, and (iv) have more oxidative stress damage and reduced capacity for antioxidant defense [lower catalase (CAT) activity]. We found no evidence that a higher susceptibility to oxidative stress contributes to female-biased mortality at warm temperatures. We did, however, find that females had significantly lower cardiac LDH and that 18°C significantly reduced plasma levels of testosterone and estradiol, especially in females. We also found that relative gonad size was significantly lower in the 18°C treatment regardless of sex, whereas relative liver size was significantly lower in females held at 18°C. Further, relative spleen size was significantly elevated in the 18°C treatments across both sexes, with larger warm-induced increases in females. Our results suggest that males may better tolerate bouts of cardiac hypoxia at high temperature, and that thermal stress may also disrupt testosterone- and estradiol-mediated protein catabolism, and the immune response (larger spleens), in migratory female salmon.

Footnotes

  • Competing interests

    The authors declare no competing or financial interests.

  • Funding

    This work was supported by a University of California Santa Barbara Faculty Research Award to E.J.E. A.P.F. and S.J.C. are funded by the Natural Sciences and Engineering Research Council of Canada (NSERC) and the Canada Research Chair program. Funding was also provided by NSERC Discovery and Strategic Grants to S.G.H., S.J.C. and A.P.F. Funded in part by DFO's Aquatic Climate Change Adaptation Services Program to D.A.P.

  • Author contributions

    Conceptualization: A.P.F., S.J.C., D.A.P., S.G.H., E.J.E.; Methodology: A.G.L., E.H., K.K., T.D., T.S.P., B.H., E.J.E.; Validation: E.J.E.; Formal analysis: A.G.L., K.K., E.J.E.; Investigation: A.G.L., E.H., K.K., T.D., T.S.P., B.H., E.J.E.; Resources: J.N.P., A.P.F., S.J.C., D.A.P., S.G.H., E.J.E.; Data curation: E.H.; Writing - original draft: A.G.L., E.J.E.; Writing - review & editing: A.G.L., E.H., K.K., T.D., T.S.P., B.H., J.N.P., A.P.F., S.J.C., D.A.P., S.G.H.; Supervision: A.G.L., J.N.P., A.P.F., S.J.C., D.A.P., S.G.H., E.J.E.; Project administration: E.J.E.; Funding acquisition: J.N.P., A.P.F., S.J.C., D.A.P., S.G.H., E.J.E.

  • Received September 16, 2019.
  • Accepted June 10, 2020.
  • © 2020. Published by The Company of Biologists Ltd
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Keywords

  • Fish
  • Salmon
  • Temperature
  • Thermal stress
  • Metabolism
  • Oxidative stress
  • Hormones

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Research Article
Reduced lactate dehydrogenase activity in the heart and suppressed sex hormone levels are associated with female-biased mortality during thermal stress in Pacific salmon
A. G. Little, E. Hardison, K. Kraskura, T. Dressler, T. S. Prystay, B. Hendriks, J. N. Pruitt, A. P. Farrell, S. J. Cooke, D. A. Patterson, S. G. Hinch, E. J. Eliason
Journal of Experimental Biology 2020 223: jeb214841 doi: 10.1242/jeb.214841 Published 28 July 2020
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Research Article
Reduced lactate dehydrogenase activity in the heart and suppressed sex hormone levels are associated with female-biased mortality during thermal stress in Pacific salmon
A. G. Little, E. Hardison, K. Kraskura, T. Dressler, T. S. Prystay, B. Hendriks, J. N. Pruitt, A. P. Farrell, S. J. Cooke, D. A. Patterson, S. G. Hinch, E. J. Eliason
Journal of Experimental Biology 2020 223: jeb214841 doi: 10.1242/jeb.214841 Published 28 July 2020

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