Hypoxia-seeking behaviour, metabolic depression, and skeletal muscle function in an amphibious fish out of water

Abstract

Several animals enter a state of dormancy to survive harsh environmental conditions. During dormancy, metabolic depression can be critical for economizing on limited endogenous energy reserves. We used two isogenic strains (Strain 1 and Strain 2) of a self-fertilizing amphibious fish (Kryptolebias marmoratus) to test the hypothesis that animals seek hypoxic microhabitats that, in turn, accentuate metabolic depression during dormancy. Using custom-built tunnels that maintained a longitudinal O2 gradient (hypoxic to normoxic), we assessed the O2 preference of K. marmoratus during prolonged air-exposure. In support of our hypothesis, we found that one isogenic strain (Strain 2) spent more time in hypoxia compared to normoxia after 21 days in air. Prolonged air-exposure in both strains resulted in lower O2 consumption rates compared to active fish (35% depression), which was accentuated (51% depression) when fish were exposed to aerial hypoxia acutely. We then tested the hypothesis that chronic aerial hypoxia acclimation would protect endogenous energy reserves and skeletal muscle integrity, thereby maintaining locomotor performance, possibly due to hypoxic hypometabolism. We found that air-acclimated fish from both strains were in poorer body condition relative to fish acclimated to aerial hypoxia. Furthermore, aerial hypoxia-acclimation minimized glycogen usage (Strain 1), lipid catabolism (Strain 2), and white muscle atrophy (Strain 2), as well as preserved terrestrial locomotor performance compared to fish in air (Strain 2). Overall, our findings suggest that some K. marmoratus strains seek microhabitats that accentuate metabolic depression during dormancy, and that microhabitat O2 availability may have significant implications for energy metabolism, and the structure and function of skeletal muscle. Furthermore, the differential responses between isogenic strains suggests that genetic factors also contribute to phenotypic differences in the emersion behaviour and physiology of this species.