Muscle-spring dynamics in time-limited, elastic movements.

Muscle contractions that load in-series springs with slow speed over a long duration do maximal work and store the most elastic energy. However, time constraints, such as those experienced during escape and predation behaviours, may prevent animals from achieving maximal force capacity from their muscles during spring-loading. Here, we ask whether animals that have limited time for elastic energy storage operate with springs that are tuned to submaximal force production. To answer this question, we used a dynamic model of a muscle-spring system undergoing a fixed-end contraction, with parameters from a time-limited spring-loader (bullfrog: Lithobates catesbeiana) and a non-time-limited spring-loader (grasshopper: Schistocerca gregaria). We found that when muscles have less time to contract, stored elastic energy is maximized with lower spring stiffness (quantified as spring constant). The spring stiffness measured in bullfrog tendons permitted less elastic energy storage than was predicted by a modelled, maximal muscle contraction. However, when muscle contractions were modelled using biologically relevant loading times for bullfrog jumps (50 ms), tendon stiffness actually maximized elastic energy storage. In contrast, grasshoppers, which are not time limited, exhibited spring stiffness that maximized elastic energy storage when modelled with a maximal muscle contraction. These findings demonstrate the significance of evolutionary variation in tendon and apodeme properties to realistic jumping contexts as well as the importance of considering the effect of muscle dynamics and behavioural constraints on energy storage in muscle-spring systems.

Multilevel analysis of elastic morphology: The mantis shrimp's spring.

Spring systems, whether natural or engineered, are composed of compliant and rigid regions. Biological springs are often similar to monolithic structures that distribute compliance and rigidity across the whole system. For example, to confer different amounts of compliance in distinct regions within a single structure, biological systems typically vary regional morphology through thickening or elongation. Here, we analyze the monolithic spring in mantis shrimp (Stomatopoda) raptorial appendages to rapidly acquire or process prey. We quantified the shape of cross-sections of the merus segment of the raptorial appendage. We also examined specific regions of the merus that are hypothesized to either store elastic energy or provide structural support to permit energy storage in other regions of the system. We found that while all mantis shrimp contain thicker ventral bars in distal cross-sections, differences in thickness are more pronounced in high-impact "smasher" mantis shrimp than in the slower-striking "spearer" mantis shrimp. We also found that spearer cross-sections are more circular while those of smashers are more eccentric with elongation along the dorso-ventral axis. The results suggest that the regional thickening of ventral bars provides structural support for resisting spring compression and also reduces flexural stiffness along the system's long axis. This multilevel morphological analysis offers a foundation for understanding the evolution and mechanics of monolithic systems in biology.

Comparative spring mechanics in mantis shrimp.

Elastic mechanisms are fundamental to fast and efficient movements. Mantis shrimp power their fast raptorial appendages using a conserved network of exoskeletal springs, linkages and latches. Their appendages are fantastically diverse, ranging from spears to hammers. We measured the spring mechanics of 12 mantis shrimp species from five different families exhibiting hammer-shaped, spear-shaped and undifferentiated appendages. Across species, spring force and work increase with size of the appendage and spring constant is not correlated with size. Species that hammer their prey exhibit significantly greater spring resilience compared with species that impale evasive prey ('spearers'); mixed statistical results show that species that hammer prey also produce greater work relative to size during spring loading compared with spearers. Disabling part of the spring mechanism, the 'saddle', significantly decreases spring force and work in three smasher species; cross-species analyses show a greater effect of cutting the saddle on the spring force and spring constant in species without hammers compared with species with hammers. Overall, the study shows a more potent spring mechanism in the faster and more powerful hammering species compared with spearing species while also highlighting the challenges of reconciling within-species and cross-species mechanical analyses when different processes may be acting at these two different levels of analysis. The observed mechanical variation in spring mechanics provides insights into the evolutionary history, morphological components and mechanical behavior, which were not discernible in prior single-species studies. The results also suggest that, even with a conserved spring mechanism, spring behavior, potency and component structures can be varied within a clade with implications for the behavioral functions of power-amplified devices.

From bouncy legs to poisoned arrows: elastic movements in invertebrates.

Elastic mechanisms in the invertebrates are fantastically diverse, yet much of this diversity can be captured by examining just a few fundamental physical principles. Our goals for this commentary are threefold. First, we aim to synthesize and simplify the fundamental principles underlying elastic mechanisms and show how different configurations of basic building blocks can be used for different functions. Second, we compare single rapid movements and rhythmic movements across six invertebrate examples - ranging from poisonous cnidarians to high-jumping froghoppers - and identify remarkable functional properties arising from their underlying elastic systems. Finally, we look to the future of this field and find two prime areas for exciting new discoveries - the evolutionary dynamics of elastic mechanisms and biomimicry of invertebrate elastic materials and mechanics.