The physiological ecology of myoglobin in scombrid fish

Tunas, members of the family Scombridae, possess the highest myoglobin concentrations in their slow-oxidative muscle outside of marine mammals and are unique among teleosts in their ability to maintain elevated temperatures in their axial muscle. This study investigates the unusually high myoglobin concentrations of tunas with reference to their thermal biology and examines the role of myoglobin in the physiological ecology of scombrid fish. By measuring in vivo physiological temperatures and depth movements of Pacific bluefin tuna using ultrasonic telemetry, the biochemical and physiological analysis of myoglobin is put into the context of whole animal physiology. The oxygen affinities of endothermic scombrids (bluefin and skipjack tuna) are demonstrated to be higher than those of ectothermic fish (bonito and mackerel), while the effect of temperature on oxygen affinity does not differ between the groups. The differences in oxygen affinities between endothermic and ectothermic animals are independent of phylogeny and suggest convergent evolution of oxygen affinities that are conserved at the physiological temperatures of the slow-oxidative muscles of the fish. The thermodynamics and kinetics of oxygen binding suggest that the myoglobins from the ectothermic fish are more flexible proteins. Analysis of the deduced amino acid sequences of myoglobins from several scombrids highlights substitutions in regions of the molecule lacking secondary structure that are consistent with the prediction of more flexible myoglobin proteins in mackerel and bonito. Sequence analysis also provides evidence for diversity of evolutionary rates in myoglobins within the Scombridae that are not correlated with endothermic ability or metabolic rate. Finally, a comparison of aerobic poise and myoglobin concentration of both the fast-twitch and slow-twitch muscle of bluefin tuna and bonito indicate that the high myoglobin concentrations of bluefin tuna are not explained by a higher aerobic capacity of their axial musculature. A role for myoglobin as a supplemental oxygen store to allow sustained locomotory performance when environmental variables limit cardiac output in tunas is proposed.