Hypoxia tolerance in elasmobranchs. II. Cardiovascular function and tissue metabolic responses during progressive and relative hypoxia exposures

Abstract

Cardiovascular function and metabolic responses of the heart and other tissues during hypoxia exposure were compared between the hypoxia-tolerant epaulette shark (Hemiscyllium ocellatum) and the hypoxia-sensitive shovelnose ray (Aptychotrema rostrata). In both species, progressive hypoxia exposure caused increases in stroke volume and decreases in heart rate, cardiac output, cardiac power output (CPO, an assessment of cardiac energy demand) and dorsal aortic blood pressure, all of which occurred at or below each species' critical P(O2) for whole-animal O(2) consumption rate, M(O2) (P(crit)). In epaulette sharks, which have a lower P(crit) than shovelnose rays, routine levels of cardiovascular function were maintained to lower water P(O2) levels and the changes from routine levels during hypoxia exposure were smaller compared with those for the shovelnose ray. The maintenance rather than depression of cardiovascular function during hypoxia exposure may contribute to the superior hypoxia tolerance of the epaulette shark, presumably by improving O(2) delivery and waste removal. Compared with shovelnose rays, epaulette sharks were also better able to maintain a stable cardiac high-energy phosphate pool and to minimize metabolic acidosis and lactate accumulation in the heart (despite higher CPO) and other tissues during a 4 h exposure to 40% of their respective P(crit) (referred to as a relative hypoxia exposure), which results in similar hypoxaemia in the two species (∼16% Hb-O(2) saturation). These different metabolic responses to relative hypoxia exposure suggest that variation in hypoxia tolerance among species is not solely dictated by differences in O(2) uptake and transport but also by tissue-specific metabolic responses. In particular, lower tissue [lactate] accumulation in epaulette sharks than in shovelnose rays during relative hypoxia exposure suggests that enhanced extra-cardiac metabolic depression occurs in the former species. This could facilitate strategic utilization of available O(2) for vital organs such as the heart, potentially explaining the greater hypoxic cardiovascular function of epaulette sharks.