Hydrogen sulphide toxicity and the importance of amphibious behaviour in a mangrove fish inhabiting sulphide-rich habitats

Abstract

We investigated amphibious behaviour, hydrogen sulphide (H2S) tolerance, and the mechanism of H2S toxicity in the amphibious mangrove rivulus (Kryptolebias marmoratus). We found that fish emersed (left water) in response to acutely elevated [H2S] (~ 130–200 µmol l−1). The emersion response to H2S may be influenced by prior acclimation history due to acclimation-induced alterations in gill morphology and/or the density and size of neuroepithelial cells (NECs) on the gills and skin. Thus, we acclimated fish to water (control), H2S-rich water, or air and tested the hypotheses that acclimation history influences H2S sensitivity due to acclimation-induced changes in (i) gill surface area and/or (ii) NEC density and/or size. Air-acclimated fish emersed at significantly lower [H2S] relative to fish acclimated to control or H2S-rich water, but exhibited no change in gill surface area or in NEC density or size in the gills or skin. Despite possessing exceptional H2S tolerance, all fish lost equilibrium when unable to emerse from environments containing extremely elevated [H2S] (2272 ± 46 µmol l−1). Consequently, we tested the hypothesis that impaired blood oxygen transport (i.e., sulphemoglobin formation) causes H2S toxicity in amphibious fishes. In vitro exposure of red blood cells to physiologically relevant [H2S] did not cause a substantial increase in sulphemoglobin formation. We found evidence, however, for an alternative hypothesis that H2S toxicity is caused by impaired oxidative phosphorylation (i.e., cytochrome c oxidase inhibition). Collectively, our results show that amphibious behaviour is critical for the survival of K. marmoratus in H2S-rich environments as fish experience impaired oxidative phosphorylation when unable to emerse.

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Acknowledgements

We thank Wen Pan for her help with confocal imaging as well as Matt Cornish, Mike Davies, Abiran Sritharan, and numerous undergraduate volunteers for assistance with animal care.

Funding

This work was supported by the National Sciences and Engineering Research Council of Canada (NSERC) Discovery grants to P.A.W (Grant number 120513).

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Correspondence to Patricia A. Wright.

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Communicated by H.V. Carey.

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Cochrane, P.V., Rossi, G.S., Tunnah, L. et al. Hydrogen sulphide toxicity and the importance of amphibious behaviour in a mangrove fish inhabiting sulphide-rich habitats. J Comp Physiol B 189, 223–235 (2019). https://doi.org/10.1007/s00360-019-01204-0

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Keywords

  • Hydrogen sulphide
  • Amphibious fish
  • Emersion
  • Sulphemoglobin
  • Cytochrome c oxidase