Hypoxia tolerance in elasmobranchs. I. Critical oxygen tension as a measure of blood oxygen transport during hypoxia exposure

Abstract

The critical O 2 tension of whole-animal O 2 consumption rate (MO 2), or P crit, is the water PO 2 (PwO 2) at which an animal transitions from an oxyregulator to an oxyconformer. Although P crit is a popular measure of hypoxia tolerance in fishes because it reflects the capacity for O 2 uptake from the environment at low PwO 2, little is known about the interrelationships between P crit and blood O 2 transport characteristics and increased use of anaerobic metabolism during hypoxia exposure in fishes, especially elasmobranchs. We addressed this knowledge gap using progressive hypoxia exposures of two elasmobranch species with differing hypoxia tolerance. The P crit of the hypoxia-tolerant epaulette shark (Hemiscyllium ocellatum, 5.10±0.37?kPa) was significantly lower than that of the comparatively hypoxia-sensitive shovelnose ray (Aptychotrema rostrata, 7.23±0.40?kPa). Plasma [lactate] was elevated above normoxic values at around P crit in epaulette sharks, but increased relative to normoxic values at PwO 2 below P crit in shovelnose rays, providing equivocal support for the hypothesis that P crit is associated with increased anaerobic metabolism. The MO 2, arterial PO 2 and arterial blood O 2 content (CaO 2) were similar between the two species under normoxia and decreased in both species with progressive hypoxia, but as PwO 2 declined, epaulette sharks had a consistently higher MO 2 and CaO 2 than shovelnose rays, probably due to their significantly greater in vivo haemoglobin (Hb)-O 2 binding affinity (in vivo Hb-O 2 P 50=4.27±0.57kPa for epaulette sharks vs 6.35±0.34kPa for shovelnose rays). However, at PwO 2 values representing the same percentage of each species' P crit (up to ̃175% of P crit), Hb-O 2 saturation and CaO 2 were similar between species. These data support the hypothesis that Hb-O 2 P50 is an important determinant of P crit and suggest that P crit can predict Hb-O 2 saturation and CaO 2 during hypoxia exposure, with a lower P crit being associated with greater O 2 supply at a given PwO 2 and consequently better hypoxia tolerance. Thus, P crit is a valuable predictor of environmental hypoxia tolerance and hypoxia exposures standardized at a given percentage of P crit will yield comparable levels of arterial hypoxaemia, facilitating cross-species comparisons of responses to hypoxia. © 2012. Published by The Company of Biologists Ltd.