Coronary blood flow influences tolerance to environmental extremes in fish

Abstract

ABSTRACT Approximately half of all fishes have, in addition to the luminal venous O2 supply, a coronary circulation supplying the heart with fully oxygenated blood. Yet, it is not fully understood how coronary O2 delivery affects tolerance to environmental extremes such as warming and hypoxia. Hypoxia reduces arterial oxygenation, while warming increases overall tissue O2 demand. Thus, as both stressors are associated with reduced venous O2 supply to the heart, we hypothesised that coronary flow benefits hypoxia and warming tolerance. To test this hypothesis, we blocked coronary blood flow (via surgical coronary ligation) in rainbow trout (Oncorhynchus mykiss) and assessed how in vivo cardiorespiratory performance and whole-animal tolerance to acute hypoxia and warming was affected. While coronary ligation reduced routine stroke volume relative to trout with intact coronaries, cardiac output was maintained by an increase in heart rate. However, in hypoxia, coronary-ligated trout were unable to increase stroke volume to maintain cardiac output when bradycardia developed, which was associated with a slightly reduced hypoxia tolerance. Moreover, during acute warming, coronary ligation caused cardiac function to collapse at lower temperatures and reduced overall heat tolerance relative to trout with intact coronary arteries. We also found a positive relationship between individual hypoxia and heat tolerance across treatment groups, and tolerance to both environmental stressors was positively correlated with cardiac performance. Collectively, our findings show that coronary perfusion improves cardiac O2 supply and therefore cardiovascular function at environmental extremes, which benefits tolerance to natural and anthropogenically induced environmental perturbations.