Tuned muscle and spring properties increase elastic energy storage

Abstract

Elastic recoil drives some of the fastest and most powerful biological movements. For effective use of elastic recoil, the tuning of muscle and spring force capacity is essential. While studies of invertebrate organisms that use elastic recoil show evidence of increased force capacity in their energy loading muscle, changes in the fundamental properties of such muscles have yet to be documented in vertebrates. Here we used three species of frogs (Cuban tree frogs, bullfrogs, and cane toads) that differ in jumping power to investigate functional shifts in muscle-spring tuning in systems using latch-mediated spring actuation (LaMSA). We hypothesized that variation in jumping performance would result from increased force capacity in muscles and relatively stiffer elastic structures resulting in greater energy storage. To test this, we characterized the force-length property of the plantaris longus muscle-tendon unit (MTU), and quantified the maximal amount of energy stored in elastic structures for each species. We found that the plantaris longus MTU of Cuban tree frogs produced higher mass-specific energy and mass-specific forces than the other two species. Moreover, we found that the plantaris longus MTU of Cuban tree frogs had higher pennation angles than the other species suggesting that muscle architecture was modified to increase force capacity through packing of more muscle fibers. Finally, we found that the elastic structures were relatively stiffer in Cuban tree frogs. These results provide a mechanistic link between the tuned properties of LaMSA components, energy storage capacity and whole system performance.

Ecology, sexual dimorphism, and jumping evolution in anurans

“…Despite our growing knowledge of anuran jumping performance, we still lack extensive interspecific data for potentially important anatomical variables involved in jumping, such as plantaris pinnation angle (Juarez et al, 2020; Mendoza & Azizi, 2021) and most aspects of muscle physiology (Astley, 2016). This might limit our ability to understand the relationship between form and function across the ecomorphological diversity of anurans.…”

Elastic pinch biomechanisms can yield consistent launch speeds regardless of projectile mass

“…Examining the other components involved in latch-mediated spring actuation can reveal additional methods of adjusting elastic potential energy storage and release. Besides the projectile and spring, other components of spring-actuated systems include the motor (which loads energy into the spring [45,46] and the latch (which mediates the transition of elastic potential energy to kinetic energy [30,47]). The tuning of muscles (the motor) to tendons (the spring) explains why some frog species had higher mass-specific elastic potential energy storage in their tendons than others [45].…”

“…Besides the projectile and spring, other components of spring-actuated systems include the motor (which loads energy into the spring [45,46] and the latch (which mediates the transition of elastic potential energy to kinetic energy [30,47]). The tuning of muscles (the motor) to tendons (the spring) explains why some frog species had higher mass-specific elastic potential energy storage in their tendons than others [45]. The species that stored the most mass-specific elastic potential energy had the stiffest springs and was able to deform these springs with muscles that generated greater forces due to improved pennation angles compared to the other species [45].…”

“…The tuning of muscles (the motor) to tendons (the spring) explains why some frog species had higher mass-specific elastic potential energy storage in their tendons than others [45]. The species that stored the most mass-specific elastic potential energy had the stiffest springs and was able to deform these springs with muscles that generated greater forces due to improved pennation angles compared to the other species [45]. In the three witch hazel species, the motor is hypothesized to be the desiccation of the endocarp [15,27].…”

“…While one might expect springs to be metal coils and sheets, they also include more complex geometry [50], materials such as rubbers or carbon fibre [49,52], and can exhibit dynamic loading and recoiling through the use of meta-materials [55]. Meanwhile, animals typically use muscles as motors and can vary pennation angle [45], cross sectional area, and sarcomere length [56] to adjust muscle outputs. Animal springs include tendons, apodemes, and exoskeletons and can vary greatly in morphology and material composition [30].…”