Physiological basis of temperature-dependent biogeography: trade-offs in muscle design and performance in polar ectotherms

Abstract

Polar, especially Antarctic, oceans host ectothermic fish and invertebrates characterized by low-to-moderate levels of motor activity; maximum performance is reduced compared with that in warmer habitats. The present review attempts to identify the trade-offs involved in adaptation to cold in the light of progress in the physiology of thermal tolerance. Recent evidence suggests that oxygen limitations and a decrease in aerobic scope are the first indications of tolerance limits at both low and high temperature extremes. The cold-induced reduction in aerobic capacity is compensated for at the cellular level by elevated mitochondrial densities, accompanied by molecular and membrane adjustments for the maintenance of muscle function. Particularly in the muscle of pelagic Antarctic fish, among notothenioids, the mitochondrial volume densities are among the highest known for vertebrates and are associated with cold compensation of aerobic metabolic pathways, a reduction in anaerobic scope, rapid recovery from exhaustive exercise and enhanced lipid stores as well as a preference for lipid catabolism characterized by high energy efficiency at high levels of ambient oxygen supply. Significant anaerobic capacity is still found at the very low end of the activity spectrum, e.g. among benthic eelpout (Zoarcideae). In contrast to the cold-adapted eurytherms of the Arctic, polar (especially Antarctic) stenotherms minimize standard metabolic rate and, as a precondition, the aerobic capacity per milligram of mitochondrial protein, thereby minimizing oxygen demand. Cost reductions are supported by the downregulation of the cost and flexibility of acid-base regulation. At maintained factorial scopes, the reduction in standard metabolic rate will cause net aerobic scope to be lower than in temperate species. Loss of contractile myofilaments and, thereby, force results from space constraints due to excessive mitochondrial proliferation. On a continuum between low and moderately high levels of muscular activity, polar fish have developed characteristics of aerobic metabolism equivalent to those of high-performance swimmers in warmer waters. However, they only reach low performance levels despite taking aerobic design to an extreme.