The ‘osmorespiratory compromise’ during hypoxia in freshwater fish

Abstract

To understand the ‘osmorespiratory compromise’ (the trade-off in gill function between ion and respiratory gas exchange) during hypoxia in freshwater fish, a species-specific approach was utilized where general ionoregulatory responses to hypoxia were compared in rainbow trout (Oncorhynchus mykiss, a hypoxia-intolerant freshwater fish), and in two hypoxia-tolerant species (the goldfish Carassius auratus and the Amazonian oscar Astronotus ocellatus). In the latter two species, the dual stress situation of hypoxia plus feeding was also explored. Measurements included unidirectional and net Na^+ flux rates, ammonia excretion rates, net K^+ loss rates, branchial Na^+/K^+- ATPase and H^+- ATPase activities, and branchial morphology by scanning electron microscopy (trout and oscar only). In trout, environmental hypoxia induced complex changes in gill ionoregulatory function, where the direction and magnitude varied with both the extent and duration of the hypoxia regime. The changes in ion-regulation observed in trout in response to hypoxia indicated that the osmorespiratory compromise in this hypoxia-intolerant species was different and more complex compared to its manifestation in oscar and goldfish. This could be attributed to the adaptive physiology of the trout to oxygen-rich environments and its intolerance to low environmental oxygen availability. In both of the hypoxia-tolerant species (oscar and goldfish), there was a general reduction in gill permeability in response to severe hypoxia regardless of feeding regime, rather different from the complex patterns seen in the hypoxia-intolerant trout. However, the effects of feeding on this phenomenon differed between these species. Fed goldfish had elevated branchial fluxes that were effectively turned down during hypoxia compared to baseline flux rates maintained by starved goldfish. In contrast, fed oscars had lower fluxes compared to starved fish. Although both fed and starved fish suppressed their branchial fluxes with severe hypoxia, fed oscars delayed the turning down of fluxes. Overall, our results indicate that feeding exerts opposite effects on gill ionoregulatory function in these two hypoxia-tolerant species, and thereby differentially modulates the responses to hypoxia. These differences may relate to differences in water chemistry. Furthermore, the manifestation of the osmorespiratory compromise during hypoxia appears to be rather different from the phenomenon during exercise.