How well do muscle biomechanics predict whole-animal locomotor performance? The role of Ca2+ handling

Abstract

SUMMARY It is important to determine the enabling mechanisms that underlie locomotor performance to explain the evolutionary patterns and ecological success of animals. Our aim was to determine the extent to which calcium (Ca2+) handling dynamics modulate the contractile properties of isolated skeletal muscle, and whether the effects of changing Ca2+ handling dynamics in skeletal muscle are paralleled by changes in whole-animal sprint and sustained swimming performance. Carp (Cyprinus carpio) increased swimming speed by concomitant increases in tail-beat amplitude and frequency. Reducing Ca2+ release from the sarcoplasmic reticulum (SR) by blocking ryanodine receptors with dantrolene decreased isolated peak muscle force and was paralleled by a decrease in tail-beat frequency and whole-animal sprint performance. An increase in fatigue resistance following dantrolene treatment may reflect the reduced depletion of Ca2+ stores in the SR associated with lower ryanodine receptor (RyR) activity. Blocking RyRs may be detrimental by reducing force production and beneficial by reducing SR Ca2+ depletion so that there was no net effect on critical sustained swimming speed (Ucrit). In isolated muscle, there was no negative effect on force production of blocking Ca2+ release via dihydropyridine receptors (DHPRs) with nifedipine. Nifedipine decreased fatigue resistance of isolated muscle, which was paralleled by decreases in tail-beat frequency and Ucrit. However, sprint performance also decreased with DHPR inhibition, which may indicate a role in muscle contraction of the Ca2+ released by DHPR into the myocyte. Inhibiting sarco(endo)plasmic reticulum Ca2+-ATPase (SERCA) activity with thapsigargin decreased fatigue resistance, suggesting that SERCA activity is important in avoiding Ca2+ store depletion and fatigue. We have shown that different molecular mechanisms modulate the same muscle and whole-animal traits, which provides an explanatory model for the observed variations in locomotor performance within and between species.