A power amplification dyad in seahorses.

Throughout evolution, organisms repeatedly developed elastic elements to power explosive body motions, overcoming ubiquitous limits on the power capacity of fast-contracting muscles. Seahorses evolved such a latch-mediated spring-actuated (LaMSA) mechanism; however, it is unclear how this mechanism powers the two complementary functions necessary for feeding: rapidly swinging the head towards the prey, and sucking water into the mouth to entrain it. Here, we combine flow visualization and hydrodynamic modelling to estimate the net power required for accelerating the suction feeding flows in 13 fish species. We show that the mass-specific power of suction feeding in seahorses is approximately three times higher than the maximum recorded from any vertebrate muscle, resulting in suction flows that are approximately eight times faster than similar-sized fishes. Using material testing, we reveal that the rapid contraction of the sternohyoideus tendons can release approximately 72% of the power needed to accelerate the water into the mouth. We conclude that the LaMSA system in seahorses is powered by two elastic elements, the sternohyoideus and epaxial tendons. These elements jointly actuate the coordinated acceleration of the head and the fluid in front of the mouth. These findings extend the known function, capacity and design of LaMSA systems.

The effects of temperature on elastic energy storage and release in a system with a dynamic mechanical advantage latch.

Changes in temperature alter muscle kinetics and in turn affect whole-organism performance. Some organisms use the elastic recoil of biological springs, structures which are far less temperature sensitive, to power thermally robust movements. For jumping frogs, the use of elastic energy in tendons is facilitated through a geometric latching mechanism that operates through dynamic changes in the mechanical advantage (MA) of the hindlimb. Despite the well-documented use of elastic energy storage, frog jumping is a locomotor behavior that is significantly affected by changes in temperature. Here, we used an in vitro muscle preparation interacting in real time with an in silico model of a legged jumper to understand how changes in temperature affect the flow of energy in a system using a MA latch. We used the plantaris longus muscle-tendon unit (MTU) to power a virtual limb with changing MA and a mass being accelerated through a real-time feedback controller. We quantified the amount of energy stored in and recovered from elastic structures and the additional contribution of direct muscle work after unlatching. We found that temperature altered the duration of the energy loading and recovery phase of the in vitro/in silico experiments. We found that the early phase of loading was insensitive to changes in temperature. However, an increase in temperature did increase the rate of force development, which in turn allowed for increased energy storage in the second phase of loading. We also found that the contribution of direct muscle work after unlatching was substantial and increased significantly with temperature. Our results show that the thermal robustness achieved by an elastic mechanism depends strongly on the nature of the latch that mediates energy flow, and that the relative contribution of elastic and direct muscle energy likely shapes the thermal sensitivity of locomotor systems.

Developing elastic mechanisms: ultrafast motion and cavitation emerge at the millimeter scale in juvenile snapping shrimp.

Organisms such as jumping froghopper insects and punching mantis shrimp use spring-based propulsion to achieve fast motion. Studies of elastic mechanisms have primarily focused on fully developed and functional mechanisms in adult organisms. However, the ontogeny and development of these mechanisms can provide important insights into the lower size limits of spring-based propulsion, the ecological or behavioral relevance of ultrafast movement, and the scaling of ultrafast movement. Here, we examined the development of the spring-latch mechanism in the bigclaw snapping shrimp, Alpheus heterochaelis (Alpheidae). Adult snapping shrimp use an enlarged claw to produce high-speed strikes that generate cavitation bubbles. However, until now, it was unclear when the elastic mechanism emerges during development and whether juvenile snapping shrimp can generate cavitation at this size. We reared A. heterochaelis from eggs, through their larval and postlarval stages. Starting 1 month after hatching, the snapping shrimp snapping claw gradually developed a spring-actuated mechanism and began snapping. We used high-speed videography (300,000 frames s-1) to measure juvenile snaps. We discovered that juvenile snapping shrimp generate the highest recorded accelerations (5.8×105±3.3×105 m s-2) for repeated-use, underwater motion and are capable of producing cavitation at the millimeter scale. The angular velocity of snaps did not change as juveniles grew; however, juvenile snapping shrimp with larger claws produced faster linear speeds and generated larger, longer-lasting cavitation bubbles. These findings establish the development of the elastic mechanism and cavitation in snapping shrimp and provide insights into early life-history transitions in spring-actuated mechanisms.

Elastic energy storage in seahorses leads to a unique suction flow dynamics compared with other actinopterygians.

Suction feeding is a dominant prey-capture strategy across actinopterygians, consisting of a rapid expansion of the mouth cavity that drives a flow of water containing the prey into the mouth. Suction feeding is a power-hungry behavior, involving the actuation of cranial muscles as well as the anterior third of the fish's swimming muscles. Seahorses, which have reduced swimming muscles, evolved a unique mechanism for elastic energy storage that powers their suction flows. This mechanism allows seahorses to achieve head rotation speeds that are 50 times faster than those of fish lacking such a mechanism. However, it is unclear how the dynamics of suction flows in seahorses differ from the conserved pattern observed across other actinopterygians, or how differences in snout length across seahorses affect these flows. Using flow visualization experiments, we show that seahorses generate suction flows that are 8 times faster than those of similar-sized fish, and that the temporal patterns of cranial kinematics and suction flows in seahorses differ from the conserved pattern observed across other actinopterygians. However, the spatial patterns retain the conserved actinopterygian characteristics, where suction flows impact a radially symmetric region of ∼1 gape diameter outside the mouth. Within seahorses, increases in snout length were associated with slower suction flows and faster head rotation speeds, resulting in a trade-off between pivot feeding and suction feeding. Overall, this study shows how the unique cranial kinematics in seahorses are manifested in their suction-feeding performance, and highlights the trade-offs associated with their unique morphology and mechanics.

Tuned muscle and spring properties increase elastic energy storage.

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. Although 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.

Morphology and performance of the 'trap-jaw' cheliceral strikes in spiders (Araneae, Mecysmaucheniidae).

Mecysmaucheniidae spiders have evolved ultra-fast cheliceral strikes 4 times independently. The mechanism for producing these high-speed strikes is likely due to a latch/spring system that allows for stored energy to be rapidly released. This study examined two different sister lineages: Zearchaea has ultra-fast cheliceral strikes and Aotearoa, based on external morphology of the clypeus, is hypothesized to have slower strikes. Using high-speed videography, I first gathered kinematic data on each taxon. Then, using histology and data from micro-computed tomography scanning, I examined internal cheliceral muscle morphology to test whether shifts in muscle anatomy correspond to performance differences in cheliceral strike. Results from high-speed video analysis revealed that Zearchaea achieves peak angular velocities of 25.0×103±4.8×103 rad s-1 (mean±s.d.) in durations of 0.0843±0.017 ms. The fastest recorded strike had a peak angular and linear velocity of 30.8×103 rad s-1 and 18.2 m s-1, respectively. The slower striking sister species, Aotearoa magna, was three orders of magnitude slower in velocity and longer in duration. Histology revealed sarcomere length differences, with some muscles optimized for force, and other muscles for speed. 3D printed models revealed structural differences that explain how the chelicerae hinge open and close. Combining all of this evidence, I put forth a hypothesis for the ultra-fast trap-jaw mechanism. This research documents the morphological shifts that accompany ultra-fast movements that result in increased rotation in joints and increased muscle specialization.

Beyond power amplification: latch-mediated spring actuation is an emerging framework for the study of diverse elastic systems.

Rapid biological movements, such as the extraordinary strikes of mantis shrimp and accelerations of jumping insects, have captivated generations of scientists and engineers. These organisms store energy in elastic structures (e.g. springs) and then rapidly release it using latches, such that movement is driven by the rapid conversion of stored elastic to kinetic energy using springs, with the dynamics of this conversion mediated by latches. Initially drawn to these systems by an interest in the muscle power limits of small jumping insects, biologists established the idea of power amplification, which refers both to a measurement technique and to a conceptual framework defined by the mechanical power output of a system exceeding muscle limits. However, the field of fast elastically driven movements has expanded to encompass diverse biological and synthetic systems that do not have muscles - such as the surface tension catapults of fungal spores and launches of plant seeds. Furthermore, while latches have been recognized as an essential part of many elastic systems, their role in mediating the storage and release of elastic energy from the spring is only now being elucidated. Here, we critically examine the metrics and concepts of power amplification and encourage a framework centered on latch-mediated spring actuation (LaMSA). We emphasize approaches and metrics of LaMSA systems that will forge a pathway toward a principled, interdisciplinary field.

The effect of muscle ultrastructure on the force, displacement and work capacity of skeletal muscle.

Skeletal muscle powers animal movement through interactions between the contractile proteins, actin and myosin. Structural variation contributes greatly to the variation in mechanical performance observed across muscles. In vertebrates, gross structural variation occurs in the form of changes in the muscle cross-sectional area : fibre length ratio. This results in a trade-off between force and displacement capacity, leaving work capacity unaltered. Consequently, the maximum work per unit volume-the work density-is considered constant. Invertebrate muscle also varies in muscle ultrastructure, i.e. actin and myosin filament lengths. Increasing actin and myosin filament lengths increases force capacity, but the effect on muscle fibre displacement, and thus work, capacity is unclear. We use a sliding-filament muscle model to predict the effect of actin and myosin filament lengths on these mechanical parameters for both idealized sarcomeres with fixed actin : myosin length ratios, and for real sarcomeres with known filament lengths. Increasing actin and myosin filament lengths increases stress without reducing strain capacity. A muscle with longer actin and myosin filaments can generate larger force over the same displacement and has a higher work density, so seemingly bypassing an established trade-off. However, real sarcomeres deviate from the idealized length ratio suggesting unidentified constraints or selective pressures.

Design and control of jumping microrobots with torque reversal latches.

Jumping microrobots and insects power their impressive leaps through systems of springs and latches. Using springs and latches, rather than motors or muscles, as actuators to power jumps imposes new challenges on controlling the performance of the jump. In this paper, we show how tuning the motor and spring relative to one another in a torque reversal latch can lead to an ability to control jump output, producing either tuneable (variable) or stereotyped jumps. We develop and utilize a simple mathematical model to explore the underlying design, dynamics, and control of a torque reversal mechanism, provides the opportunity to achieve different outcomes through the interaction between geometry, spring properties, and motor voltage. We relate system design and control parameters to performance to guide the design of torque reversal mechanisms for either variable or stereotyped jump performance. We then build a small (356 mg) microrobot and characterize the constituent components (e.g. motor and spring). Through tuning the actuator and spring relative to the geometry of the torque reversal mechanism, we demonstrate that we can achieve jumping microrobots that both jump with different take-off velocities given the actuator input (variable jumping), and those that jump with nearly the same take-off velocity with actuator input (stereotyped jumping). The coupling between spring characteristics and geometry in this system has benefits for resource-limited microrobots, and our work highlights design combinations that have synergistic impacts on output, compared to others that constrain it. This work will guide new design principles for enabling control in resource-limited jumping microrobots.

Controlling jumps through latches in small jumping robots.

Small jumping robots can use springs to maximize jump performance, but they are typically not able to control the height of each jump owing to design constraints. This study explores the use of the jumper's latch, the component that mediates the release of energy stored in the spring, as a tool for controlling jumps. A reduced-order model that considers the dynamics of the actuator pulling the latch and the effect of spring force on the latch is presented. This model is then validated using high speed video and ground reaction force measurements from a 4gjumper. Both the model and experimental results demonstrate that jump performance in small insect-inspired resource-constrained robots can be tuned to a range of outputs using latch mediation, despite starting with a fixed spring potential energy. For a fixed set of input voltages to the latch actuator, the results also show that a jumper with a larger latch radius has greater tunability. However, this greater tunability comes with a trade-off in maximum performance. Finally, we define a new metric, 'Tunability Range,' to capture the range of controllable jump behaviors that a jumper with a fixed spring compression can attain given a set of control inputs (i.e. latch actuation voltage) to choose from.

Control of high-speed jumps in muscle and spring actuated systems: a comparative study of take-off energetics in bush-crickets (Mecopoda elongata) and locusts (Schistocerca gregaria).

The Orthoptera are a diverse insect order well known for their locomotive capabilities. To jump, the bush-cricket uses a muscle actuated (MA) system in which leg extension is actuated by contraction of the femoral muscles of the hind legs. In comparison, the locust uses a latch mediated spring actuated (LaMSA) system, in which leg extension is actuated by the recoil of spring-like structure in the femur. The aim of this study was to describe the jumping kinematics of Mecopoda elongata (Tettigoniidae) and compare this to existing data in Schistocerca gregaria (Acrididae), to determine differences in control of rotation during take-off between similarly sized MA and LaMSA jumpers. 269 jumps from 67 individuals of M. elongata with masses from 0.014 g to 3.01 g were recorded with a high-speed camera setup. In M. elongata, linear velocity increased with mass0.18 and the angular velocity (pitch) decreased with mass-0.13. In S. gregaria, linear velocity is constant and angular velocity decreases with mass-0.24. Despite these differences in velocity scaling, the ratio of translational kinetic energy to rotational kinetic energy was similar for both species. On average, the energy distribution of M. elongata was distributed 98.8% to translational kinetic energy and 1.2% to rotational kinetic energy, whilst in S. gregaria it is 98.7% and 1.3%, respectively. This energy distribution was independent of size for both species. Despite having two different jump actuation mechanisms, the ratio of translational and rotational kinetic energy formed during take-off is fixed across these distantly related orthopterans.

Control of high-speed jumps: the rotation and energetics of the locust (Schistocerca gregaria).

Locusts (Schistocerca gregaria) jump using a latch mediated spring actuated system in the femur-tibia joint of their metathoracic legs. These jumps are exceptionally fast and display angular rotation immediately after take-off. In this study, we focus on the angular velocity, at take-off, of locusts ranging between 0.049 and 1.50 g to determine if and how rotation-rate scales with size. From 263 jumps recorded from 44 individuals, we found that angular velocity scales with mass-0.33, consistent with a hypothesis of locusts having a constant rotational kinetic energy density. Within the data from each locust, angular velocity increased proportionally with linear velocity, suggesting the two cannot be independently controlled and thus a fixed energy budget is formed at take-off. On average, the energy budget of a jump is distributed 98.7% to translational kinetic energy and gravitational potential energy, and 1.3% to rotational kinetic energy. The percentage of energy devoted to rotation was constant across all sizes of locusts and represents a very small proportion of the energy budget. This analysis suggests that smaller locusts find it harder to jump without body rotation.

A new species group of Strumigenys (Hymenoptera, Formicidae) from Ecuador, with a description of its mandible morphology.

Strumigenys is one of the most diverse ant genera in the world and arguably the most morphologically diverse, exhibiting an exceptional range of mandible shape and function. A new species, Strumigenys ayersthey sp. nov., discovered in the Chocó region of Ecuador is described. With two morphological characters, this species is shown to be a morphologically unique outlier among Strumigenys globally, having predominately smooth and shining cuticle surface sculpturing and long trap-jaw mandibles. Using µCT scans, we produced 3D images of the worker ant and static images to examine and compare mandible articular morphologies with most morphologically similar members of the mandibularis species group. Cuticular, pilosity, and articular mandible morphological differences supports placing the new species in its own new species group.