In vivo muscle force-length behavior during steady-speed hopping in tammar wallabies

Abstract

Moderate to large macropodids can increase their speed while hopping with little or no increase in energy expenditure. This has been interpreted by some workers as resulting from elastic energy savings in their hindlimb tendons. For this to occur, the muscle fibers must transmit force to their tendons with little or no length change. To test whether this is the case, we made in vivo measurements of muscle fiber length change and tendon force in the lateral gastrocnemius (LG) and plantaris (PL) muscles of tammar wallabies Macropus eugenii as they hopped at different speeds on a treadmill. Muscle fiber length changes were less than +/-0.5 mm in the plantaris and +/-2.2 mm in the lateral gastrocnemius, representing less than 2 % of total fiber length in the plantaris and less than 6 % in the lateral gastrocnemius, with respect to resting length. The length changes of the plantaris fibers suggest that this occurred by means of elastic extension of attached cross-bridges. Much of the length change in the lateral gastrocnemius fibers occurred at low force early in the stance phase, with generally isometric behavior at higher forces. Fiber length changes did not vary significantly with increased hopping speed in either muscle (P>0.05), despite a 1. 6-fold increase in muscle-tendon force between speeds of 2.5 and 6.0 m s-1. Length changes of the PL fibers were only 7+/-4 % and of the LG fibers 34+/-12 % (mean +/- S.D., N=170) of the stretch calculated for their tendons, resulting in little net work by either muscle (plantaris 0.01+/-0.03 J; gastrocnemius -0.04+/-0.30 J; mean +/- s.d. ). In contrast, elastic strain energy stored in the tendons increased with increasing speed and averaged 20-fold greater than the shortening work performed by the two muscles. These results show that an increasing amount of strain energy stored within the hindlimb tendons is usefully recovered at faster steady hopping speeds, without being dissipated by increased stretch of the muscles' fibers. This finding supports the view that tendon elastic saving of energy is an important mechanism by which this species is able to hop at faster speeds with little or no increase in metabolic energy expenditure.