An evaluation of muscle maintenance costs during fiber hypertrophy in the lobster Homarus americanus: are larger muscle fibers cheaper to maintain?

Abstract

SUMMARY Large muscle fiber size imposes constraints on muscle function while imparting no obvious advantages, making it difficult to explain why muscle fibers are among the largest cell type. Johnston and colleagues proposed the ‘optimal fiber size’ hypothesis, which states that some fish have large fibers that balance the need for short diffusion distances against metabolic cost savings associated with large fibers. We tested this hypothesis in hypertrophically growing fibers in the lobster Homarus americanus. Mean fiber diameter was 316±11 μm in juveniles and 670±26 μm in adults, leading to a surface area to volume ratio (SA:V) that was 2-fold higher in juveniles. Na+/K+-ATPase activity was also 2-fold higher in smaller fibers. 31P-NMR was used with metabolic inhibitors to determine the cost of metabolic processes in muscle preparations. The cost of Na+/K+-ATPase function was also 2-fold higher in smaller than in larger diameter fibers. Extrapolation of the SA:V dependence of the Na+/K+-ATPase over a broad fiber size range showed that if fibers were much smaller than those observed, maintenance of the membrane potential would constitute a large fraction of whole-animal metabolic rate, suggesting that the fibers grow large to reduce maintenance costs. However, a reaction–diffusion model of aerobic metabolism indicated that fibers in adults could attain still larger sizes without diffusion limitation, although further growth would have a negligible effect on cost. Therefore, it appears that decreased fiber SA:V makes larger fibers in H. americanus less expensive to maintain, which is consistent with the optimal fiber size hypothesis.