The energetic benefits of tendon springs in running: is the reduction of muscle work important?

Abstract

The distal muscle-tendon units of cursorial species are commonly composed of short muscle fibres and long, compliant tendons. It is assumed that the ability of these tendons to store and return mechanical energy over the course of a stride, thus avoiding the cyclic absorption and regeneration of mechanical energy by active muscle, offers some metabolic energy savings during running. However, this assumption has not been tested directly. We used muscle ergometry and myothermic measurements to determine the cost of force production in muscles acting isometrically, as they could if mechanical energy was stored and returned by tendon, and undergoing active stretch-shorten cycles, as they would if mechanical energy was absorbed and regenerated by muscle. We found no detectable difference in the cost of force production in isometric cycles compared with stretch-shorten cycles. This result suggests that replacing muscle stretch-shorten work with tendon elastic energy storage and recovery does not reduce the cost of force production. This calls into question the assumption that reduction of muscle work drove the evolution of long distal tendons. We propose that the energetic benefits of tendons are derived primarily from their effect on muscle and limb architecture rather than their ability to reduce the cyclic work of muscle.

Keywords: Economy; Elastic; Force; Metabolic; Myothermic.

© 2014. Published by The Company of Biologists Ltd.

Figures

Fig. 1.

Schematic representation of the trajectory of the centre of mass and the cycling of mechanical energy over the course of a running step. (A) Muscle (light grey) is operating in series with a long, compliant tendon (dark grey). Tendon stretches and recoils to absorb and return mechanical energy. (B) Muscle is operating in series with a rigid tendon. Muscle is actively stretched and then actively shortens to absorb and generate mechanical energy.

Fig. 2.

Imposed strain and stimulation pattern, stress generated and heat produced. Isometric (A), stretch–shorten (B), shorten (C) and stretch (D) cycles. The stimulation period is shown by the black bars superimposed on the strain trace. Stimulus duration was the same in all conditions. Any delays between the rise of force and heat production in cycles with active stretch were probably a result of the transient storage of mechanical energy in the preparation (Linari et al., 2003). Note that because of large differences in the heat produced in different cycles, the heat axes have different scales.

Fig. 3.

Example work loops for all four conditions. Isometric (A), stretch–shorten (B), shorten (C) and stretch (D) cycles. Net work is zero in both isometric and stretch–shorten conditions, but is achieved in different ways. Note that in order to visualize the work loops, the stress axes have different scales. Arrows indicate the direction of muscle length change.

Fig. 4.

Net work done (white bars), heat produced (black bars) and the cost of a cycle (grey bars) in all four conditions. The cost of a cycle is given by the sum of the net work and heat; hence, when net work is zero (isometric and stretch–shorten cycles), heat is equal to cost. N=11, 6, 7 and 6 for the four conditions, respectively. Results are means ± s.e.

Fig. 5.

The metabolic cost of force production in all four conditions.N=11, 6, 7 and 6 for the four conditions, respectively. There are significant differences between shorten and isometric and shorten and stretch conditions (P<0.05), but not between isometric and stretch–shorten conditions (P=0.86). Results are means ± s.e.