The fastest biological movement are capable of generating high mechanical power efficiently and repeatably. Many of the fastest movements are achieved by using a common mechanistic framework know as latch-mediated spring actuation (LaMSA). While the fundamental mechanisms associated with LaMSA have been described over the last decade, such advances have not yet been able to pinpoint the mechanical or physiological features that explain biological variation in whole system performance. Furthermore, predicted scaling relationships suggest that there is a continuum between elastic recoil use and direct muscle actuation where elastic recoil is most prevalent at small masses and organisms transition to direct muscle actuation at large sizes. These predictions provide a framework that motivates experimental approaches aimed at understanding how animals at intermediate size range partition direct muscle and spring actuation to power fast movements. In this dissertation, I investigated factors that influenced energy storage and energy release in frogs who are believed to use both LaMSA and direct muscle actuation to power jumping. First, I examined interspecific variation in the plantaris longus muscle-tendon unit (MTU) of three species of frogs to investigate how tuned properties of the MTU affected their capacity to store energy. I found that high energy storage capacity was achieved when both muscle force capacity and relative spring stiffness increased. Second, I investigated how a dynamic mechanical advantage latch affected energy storage and energy release while varying environmental temperature. I found that the while spring actuation accounts for a significant portion of the energy of a jump, muscles continue to contribute energy during spring actuation. The ability to contribute this mechanical energy during the actuation phase required high muscle power and therefore explained the thermal sensitivity observed in these systems. Lastly, I examined the energy stored and returned during frog jumps. I discovered that the muscle stored energy in elastic structures prior to any substantial movement, and that it contributed work to the jump during limb extension. I found that 70% of the total muscle fascicle work was done during the loading phase and 30% was done during the unloading phase. Taken together, my dissertation work demonstrated that variation in elastic energy storage and release could be a consequence of evolutionary differences, latch mechanics, and real time control of energy flow.

Daily and seasonal fluctuations in the environmental temperature pose a challenge to ectotherms as they move through their environment. Their skeletal muscles must generate enough power to allow them to accelerate and move quickly enough to catch prey or escape predation, but muscle is highly temperature sensitive. Ectotherms circumvent these problems through behavioral modifications at low temperatures such as hiding and entering brumation, a hibernation-like state which can involve several months of inactivity without eating. A potential drawback to brumation is that long periods of inactivity can lead to skeletal muscle atrophy, which would lower muscle power upon the resumption of activity. Ectotherms have also evolved mechanisms to maintain locomotor performance at moderate temperatures, however the mechanisms used to maintain running performance are heretofore unknown. In my dissertation I use the western fence lizard, Sceloporus occidentalis, as a model running ectotherm. In chapter 1, I use in vitro muscle preparations and histology to find that the lowered metabolic rate conferred by a low body temperature is sufficient to mitigate muscle atrophy after long periods of muscle disuse. I then use inverse dynamics in chapter 2 to calculate hind-limb joint powers and determine that fence lizards amplify muscle power using tendons to maintain acceleration performance at moderate temperatures. In chapter 3, I measure EMG activity in an ankle extensor muscle of running fence lizards. I combine that data with an in silico muscle model to determine that lizards alter the timing of activation of their muscles to cycle energy through tendons rather than muscles while running, and that this helps them maintain speed at moderate temperatures.

Muscles act as motors that perform positive mechanical work when fibers, which are comprised of sarcomeres and are organized into bundles encased by connective tissue sheaths, shorten across a joint. Here, we examine the relationship between muscle structure and function in a fusiform muscle. We model the muscle as a constant volume barrel to predict regional strain patterns throughout the muscle, and test the model empirically with a fusiform muscle, palmaris longus (PL) in two species of frogs, Rana pipiens (R. pipiens) and Rana catesbeiana (R. catesbeiana). We allowed the muscle to contract against a servomotor at submaximal force conditions while filming with a high-speed camera, then analyzed the images taken at the extremes of the muscle length to measure strain in the inner and outer fibers. Both species of frogs exhibited significantly less strain in the outer muscle fibers compared to the innermost fibers, in broad agreement with predictions from our model. We then added an external constrain to the PL muscle of R. catesbeiana and measured force and length output under otherwise identical conditions. Adding this radial constraint reduced the length the muscle could contract by 50%, resulting in a decrease in the amount of mechanical work it could perform of 50%. We discuss how regional strain variations may similarly affect the positive work output and implications for these findings on natural constraints to radial expansion.

Moving effectively across a wide range of surface conditions is paramount to acquiring food and finding mates while simultaneously avoiding injury and predation. We used the cane toad, Rhinella marina, as a model organism to better understand how the environment shapes our locomotion because of toads’ jumping gait which pushes locomotor forces to relative extremes. Their amphibious nature also ensures they encounter a wide variety of surface conditions in their natural habitat. In Chapter 1, we used high speed videography and a moveable landing platform instrumented with a force transducer to measure landing kinematics and kinetics. We found that toads did not alter their landing behavior when landing on compliant surfaces. In Chapter 2, we examined the toad’s forelimb muscle activity by implanting electrodes in their pectoralis, deltoideus, anconeus, and palmaris longus muscles. Our results paralleled the findings from Chapter 1, were none of the muscle changed their intensity in preparation for or during landing. In Chapter 3, we tested the idea that hindlimb proprioception was informing forelimb landing behavior by performing sciatic nerve reinnervation which allowed motor control to recover while ablating the stretch reflex. We showed that the elbow joint was significantly affected even 6 months following surgery when hindlimb motor function recovered, suggesting the importance of hindlimb proprioception influencing forelimb landing behavior.

Most legged animals have evolved a suite of musculoskeletal adaptations to reduce the energetic cost of locomotion (e.g. upright limb posture, long tendons), but it remains unclear whether alligators and other sprawlers are capable of using similar energy saving mechanisms during locomotion. Through a combination of in situ muscle preparations, joint-level analyses, and in vivo muscle function measurements during walking we show that 1) alligator limb joint mechanics are similar to other legged animals during walking, 2) a representative ankle extensor, the gastrocnemius externus, is capable of storing significant elastic energy in its tendon during supramaximal contractions, 3) in vivo muscle work during locomotion is surprisingly low, suggesting tendon does significant work during locomotion, and 4) alligators modulate limb and limb muscle function to improve stability or work generation when walking across non-level terrain. This work adds to the body of work on muscle function during legged locomotion and shows that general strategies and energy saving mechanisms (e.g. elastic energy storage) during legged locomotion are likely more widespread than previously assumed.

The evolution of novel locomotor modes has played a crucial role in the evolution of vertebrates. A shift in an organisms’ primary mode of locomotion or changes in the mechanical properties of the external environment require adjustments to kinematic and motor patterns. These adaptations are often associated with distinct morphological changes. Such modifications are necessary for maintaining performance in response to variation in the external physical environment. This provides the foundation for the evolution of novel modes of locomotion. Understanding this adaptability, the mechanistic, and functional implications of novel gaits and the substrates that shape biological systems can provide further insights for design parameters in synthetic and engineered systems. My dissertation seeks to understand this adaptability and the functional implications of novel gaits and substrates that affect them. I examined how the evolution of novel locomotor modes shape variation in: (Chapter 1) limb morphology, (Chapter 2) motor control strategies, and (Chapter 3) muscle properties in frogs. I used morphological, biomechanical, and physiological approaches to understand modulation of organismal locomotor patterns and responses to varying external conditions.

First, we explore how quadrupedal walking gaits are achieved in four frog species that are ancestrally specialized for jumping. We examine how the prominence of this gait correlates with a shift in limb morphology and limb posture. We find frogs specialized for walking accommodate a quadrupedal gait with an increase in relative forelimb length compared to the average anuran body plan and maintain greater vertical retraction in the hindlimb compared to the forelimb during walking. Second, I investigate the effects of substrate compliance on limb kinematics and motor control patterns of jumping Cuban tree frogs. We found evidence Cuban tree frogs use a feedforward control program and compliance substrates potentially disrupt the inertial catch mechanism used to store elastic energy. Last, I explore the effects of substrate compliance on elastic energy storage at the muscle-tendon level. We develop a spring-loaded latch analogue model using an in vitro muscle preparation. We find slower rates of energy release, less optimal latches, allow for greater energy recovery from compliant substrates.