Beyond power limits: the kinetic energy capacity of skeletal muscle

Abstract

Muscle is the universal agent of animal movement, and limits to muscle performance are therefore an integral aspect of animal behaviour, ecology, and evolution. A mechanical perspective on movement makes it amenable to analysis from first principles, and so brings the seeming certainty of simple physical "laws" to the challenging comparative study of complex biological systems. Early work in biomechanics considered muscle energy output to be limited by muscle work capacity,Wmax; triggered by seminal work in the late 1960s, it is now held broadly that a complete analysis of muscle energy output during impulsive contractions is to also consider muscle power capacity, for no unit of work can be delivered in arbitrarily brief time. This work adopts a critical stance towards this paradigmatic notion of a "power-limit", and argues that the de facto alternative constraint to muscle energy output is imposed by a characteristic "kinetic energy capacity",Emax, dictated by the maximum speed with which the actuating muscle can shorten. The two critical energies can now be directly compared, and define the "physiological similarity index", Γ =Emax/Wmax. It is the explanatory power of this comparison that lends weight to a shift in perspective from muscle power to kinetic energy capacity, as is argued through a series of brief illustrative examples. Γ emerges as a key dimensionless number in musculoskeletal dynamics, and sparks novel hypotheses on functional adaptations in musculoskeletal "design" that depart from the default evolutionary null hypothesis of geometric similarity.

Dynamic similarity and the peculiar allometry of maximum running speed

“…14,18,28,[31][32][33][34] ]. We will discuss the concept of a power limit to speed in detail separately 35 , and note briefly that a finite power density cannot be linked to speed using only the moved mass-any limit to speed implies an explicit constraint on work output, and a variation in muscle power is thus neither necessary nor sufficient to alter the maximum possible speed. It has been argued that large animals cannot utilise the full work capacity of their muscles because they are limited by a supposed maximum anaerobic capacity 17 .…”