Interindividual variation in maximum aerobic metabolism varies with gill morphology and myocardial bioenergetics

Abstract

This study asked whether interindividual variation in maximum and standard aerobic metabolic rates of the Gulf killifish, Fundulus grandis, held under common garden conditions correlate with gill morphology and cardiac mitochondrial bioenergetics, traits reflecting critical steps in the oxygen-supply cascade from the environment to the tissues. Maximum metabolic rate (MMR) was positively related to body mass, total gill filament length, and myocardial oxygen consumption during maximum oxidative phosphorylation (multiple R2 = 0.82). Standard metabolic rate (SMR) was positively related to body mass, total gill filament length, and myocardial oxygen consumption during maximum electron transport system activity (multiple R2 = 0.69). After controlling for body mass, individuals with longer gill filaments, summed over all filaments, or greater cardiac respiratory capacity had higher whole-animal metabolic rates. The overall model fit and the explanatory power of individual predictor variables were better for MMR than for SMR, suggesting that gill morphology and myocardial bioenergetics are more important in determining maximum rather than resting metabolism. Heart ventricle mass was not related to mass-independent variation in MMR or SMR, indicating that the quality of the heart (i.e., the capacity for mitochondrial metabolism) was more influential than heart size. Finally, myocardial oxygen consumption required to offset the dissipation of the transmembrane proton gradient in the absence of ATP synthesis was not correlated with either MMR or SMR. The results support the idea that interindividual variation in aerobic metabolism, particularly maximum metabolic rate, is explained, in part, by variation in specific steps in the oxygen-supply cascade.