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Osmorespiratory compromise in an elasmobranch: oxygen consumption, ventilation and nitrogen metabolism during recovery from exhaustive exercise in dogfish sharks (Squalus suckleyi)

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Abstract

The functional trade-off between respiratory gas exchange versus osmolyte and water balance that occurs at the thin, highly vascularized gills of fishes has been termed the osmorespiratory compromise. Increases in gas exchange capacity for meeting elevated oxygen demands can end up favoring the passive movement of osmolytes and water, potentially causing a disturbance in osmotic balance. This phenomenon has been studied only sparsely in marine elasmobranchs. Our goal was to evaluate the effects of exhaustive exercise (as a modulator of oxygen demand) on oxygen consumption (MO2), branchial losses of nitrogenous products (ammonia and urea-N), diffusive water exchange rates, and gill ventilation (frequency and amplitude), in the Pacific spiny dogfish (Squalus suckleyi). To that end, MO2, osmolyte fluxes, diffusive water exchange rate, and ventilation dynamics were first measured under resting control conditions, then sharks were exercised until exhaustion (20 min), and the same parameters were monitored for the subsequent 4 h of recovery. While MO2 nearly doubled immediately after exercise and remained elevated for 2 h, ventilation dynamics did not change, suggesting that fish were increasing oxygen extraction efficiency at the gills. Diffusive water flux rates (measured over 0–2 h of recovery) were not affected. Ammonia losses were elevated by 7.6-fold immediately after exercise and remained elevated for 3 h into recovery, while urea-N losses were elevated only 1.75-fold and returned to control levels after 1 h. These results are consistent with previous investigations using different challenges (hypoxia, high temperature) and point to a tighter regulation of urea-N conservation mechanisms at the gills, likely due to the use of urea as a prized osmolyte in elasmobranchs. Environmental hyperoxia offered no relief from the osmorespiratory compromise, as there were no effects on any of the parameters measured during recovery from exhaustive exercise.

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Acknowledgements

This study was supported by Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grants to CMW (RGPIN-2017-03843 and RGPIN/473-2012) and PMS (RGPIN-203189). M.G. was supported by a 4-year graduate fellowship from the University of British Columbia. We would like to thank Dr. Eric Clelland (Bamfield Marine Sciences Centre research coordinator at the time) and the BMSC research and animal care supporting staff for excellent and invaluable support. Also, a whole-hearted thanks to Dr. Junho Eom for training and assistance with the ventilation set up. Finally, the authors would like to acknowledge the incredible women who assisted with shark handling and support with experiments: Dr. Gudrun De Boeck, Dr. Lygia Nogueira, Dr. Roberta D. Klein and Olivia J.L. McMillan.

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Authors and Affiliations

  1. Department of Zoology, The University of British Columbia, Vancouver, BC, V6T 1Z4, Canada

    Marina Giacomin, Patricia M. Schulte & Chris M. Wood

  2. Department of Biology, University of Alberta, Edmonton, AB, T6G 2E9, Canada

    Marina Giacomin

  3. Bamfield Marine Sciences Centre, Bamfield, BC, Canada

    Marina Giacomin & Chris M. Wood

  4. Department of Biology, McMaster University, Hamilton, ON, Canada

    Chris M. Wood

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  1. Marina Giacomin
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Correspondence to Marina Giacomin.

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Communicated by B. Pelster.

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Giacomin, M., Schulte, P.M. & Wood, C.M. Osmorespiratory compromise in an elasmobranch: oxygen consumption, ventilation and nitrogen metabolism during recovery from exhaustive exercise in dogfish sharks (Squalus suckleyi). J Comp Physiol B 192, 647–657 (2022). https://doi.org/10.1007/s00360-022-01447-4

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