Locomotor muscle fiber heterogeneity and metabolism in the fastest large-bodied rorqual: the fin whale (Balaenoptera physalus)

Abstract

From a terrestrial ancestry, fin whale (Balaenoptera physalus) is one of the largest animal on Earth with a sprinter antipredator strategy, and a characteristic feeding mode, lunge feeding, which involve bouts of high-intensity muscle activity demanding high metabolic output. We investigated the locomotor muscle morphology and metabolism of this cetacean to determine whether its muscle profile (1) explains this unique swimming performance and feeding behaviour, (2) is or is not homogeneous within the muscle, and (3) predicts allometric variations inherent to an extreme body size. A predominantly fast-glycolytic phenotype characterized the fin whale locomotor muscle, composed of abundant fast-twitch (type IIA) fibers with high glycolytic potential, low oxidative capacity, relatively small size, and reduced number of capillaries. Compared to superficial areas, deep regions of this muscle exhibited a slower and more oxidative profile, suggesting a division of labour between muscle strata. As expected, the fin whale locomotor muscle only expressed the two slowest myosin heavy chain isoforms (I and IIA). However, it displayed anaerobic (glycolytic) and aerobic (lipid-based metabolism) capabilities higher than would be predicted from the allometric perspective of its extreme body size. Relationships between muscle metabolism and body mass were fiber-type specific. The ‘sprinter’ profile of the fin whale swimming muscle, particularly of its superficial compartment, supports physiological demands during both high-speed swimming and the lunge, when energy expenditure reaches maximal or supramaximal levels. Comparatively, the slower and more oxidative profile of the deep compartment of this muscle seems to be well designed for sustained, low-intensity muscle activity during routine swimming.