Indirect evidence for elastic energy playing a role in limb recovery during toad hopping

Abstract

Elastic energy is critical for amplifying muscle power during the propulsive phase of anuran jumping. In this study, we use toads (Bufo marinus) to address whether elastic recoil is also involved after take-off to help flex the limbs before landing. The potential for such spring-like behaviour stems from the unusually flexed configuration of a toad's hindlimbs in a relaxed state. Manual extension of the knee beyond approximately 908 leads to the rapid development of passive tension in the limb as underlying elastic tissues become stretched. We hypothesized that during take-off, the knee regularly extends beyond this, allowing passive recoil to help drive limb flexion in mid-air. To test this, we used high-speed video and electromyography to record hindlimb kinematics and electrical activity in a hindlimb extensor (semimembranosus) and flexor (iliofibularis). We predicted that hops in which the knees extended further during take-off would require less knee flexor recruitment during recovery. Knees extended beyond 908 in over 80% of hops, and longer hops involved greater degrees of knee extension during take-off and more intense semimembranosus activity. However, knee flexion velocities during recovery were maintained despite a significant decrease in iliofibularis intensity in longer hops, results consistent with elastic recoil playing a role.

Reduce torques and stick the landing: limb posture during landing in toads

“…This observation is consistent with recent findings, which suggest that the rapid flexion of the hindlimb may be associated with elastic recoil of the limb after the hindlimbs are fully extended during takeoff (Schnyer et al, 2014). This interpretation is based on the fact that the intensity of muscle activation in hindlimb flexors decreases with hop distance despite an increase in the magnitude and rate of hindlimb flexion (Schnyer et al, 2014). In fact, we have also observed that the only hops where hindlimbs are somewhat extended at impact are extremely short hops.…”

“…However, a more likely explanation may be that hindlimb flexion is primarily due to the elastic recoil of the limb during the aerial phase (Schnyer et al, 2014). If the hindlimb passively recoils when extended during take-off, then the behavior is not going to be modulated by altered sensory information or changes in motor control strategies (Schnyer et al, 2014). Finally, as our analysis only included stable landings, we cannot rule out the possibility that the addition of extrinsic loads increased the likelihood of unstable landings or crashes, which were not recorded or included in our analysis.…”

“…Of these modalities, vision would be totally unaffected by our perturbation. However, a more likely explanation may be that hindlimb flexion is primarily due to the elastic recoil of the limb during the aerial phase (Schnyer et al, 2014). If the hindlimb passively recoils when extended during take-off, then the behavior is not going to be modulated by altered sensory information or changes in motor control strategies (Schnyer et al, 2014).…”

Contribution of elastic tissues to the mechanics and energetics of muscle function during movement

“…In hopping toads, measurements of limb kinematics and electromyographic activity suggest that passive muscle elasticity helps to reposition the hindlimb to a flexed position during aerial phase of a jump, in preparation for landing (Schnyer et al, 2014). A systematic study of joint torques in passive rat hindlimbs showed that passive muscle forces establish a joint neutral position, from which the joint deviates as individual muscle units are removed by dissection (Wu et al, 2012).…”

Sensory feedback and coordinating asymmetrical landing in toads

“…Elbow kinematics were analysed bilaterally as in Cox & Gillis [6]. EMG data were analysed as described in Schnyer et al [9]. Differences between left and right forelimbs in touchdown times, TD L-R , m. anconeus onset timing, AO L-R , and intensity, AI L-R , were calculated by subtracting the value for the right limb from that of the left.…”