Ionoregulatory aspects of the hypoxia-induced osmorespiratory compromise in the euryhaline Atlantic killifish (Fundulus heteroclitus): the effects of salinity

Author:

Giacomin Marina1ORCID,Onukwufor John O.12ORCID,Schulte Patricia M.1ORCID,Wood Chris M.13ORCID

Affiliation:

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

2. Department of Anesthesiology and Perioperative Medicine, University of Rochester Medical Center, Rochester, NY, 14642, USA

3. Department of Biology, McMaster University, Hamilton, ON, L8S 4K1, Canada

Abstract

The osmorespiratory compromise is a physiological trade-off between the characteristics of the gill that promote respiratory gas-exchange and those that limit passive fluxes of ions and water with the environment. In hypoxia, changes in gill blood flow patterns and functional surface area that increase gas transfer can promote an exacerbation in ion and water fluxes. Our goal was to determine whether the osmorespiratory compromise is flexible, depending on environmental salinity (fresh, isosmotic and sea water) and oxygen levels (hypoxia) in euryhaline killifish, Fundulus heteroclitus. Plasma ion concentrations were minimally affected by hypoxia, indicating a maintenance of osmoregulatory homeostasis. In FW-killifish, hypoxia exposure reduced branchial Na+/K+-ATPase and NEM-sensitive-ATPase activities, as well as diffusive water flux rates. Unidirectional Na+ influx and Na+ efflux decreased during hypoxia in FW, but net Na+ flux remained unchanged. Net loss rates of Cl−, K+ and ammonia were also attenuated in hypoxia, suggesting both transcellular and paracellular reductions in permeability. These reductions appeared to be regulated phenomena as fluxes were restored immediately in normoxia. Na+ flux rates increased during hypoxia in 11 ppt, but decreased in 35 ppt, the latter suggesting a similar response to hypoxia as in FW. In summary, FW- and SW-killifish experience a reduction in gill permeability, as seen in other hypoxia-tolerant species. Fish acclimated to isosmotic salinity increased Na+ influx and efflux rates, as well as paracellular permeability in hypoxia, responses in accord with the predictions of the classic osmorespiratory compromise.

Funder

Natural Sciences and Engineering Research Council of Canada

Publisher

The Company of Biologists

Subject

Insect Science,Molecular Biology,Animal Science and Zoology,Aquatic Science,Physiology,Ecology, Evolution, Behavior and Systematics

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