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To celebrate its centenary year, Journal of Experimental Biology (JEB) commissioned a collection of articles examining the past, present and future of experimental biology. This Commentary closes the collection by considering the important research opportunities and challenges that await us in the future. We expect that researchers will harness the power of technological advances, such as '-omics' and gene editing, to probe resistance and resilience to environmental change as well as other organismal responses. The capacity to handle large data sets will allow high-resolution data to be collected for individual animals and to understand population, species and community responses. The availability of large data sets will also place greater emphasis on approaches such as modeling and simulations. Finally, the increasing sophistication of biologgers will allow more comprehensive data to be collected for individual animals in the wild. Collectively, these approaches will provide an unprecedented understanding of 'how animals work' as well as keys to safeguarding animals at a time when anthropogenic activities are degrading the natural environment., Competing Interests: Competing interests The authors declare no competing or financial interests., (© 2023. Published by The Company of Biologists Ltd.)

Energetic trade-offs are particularly pertinent to bio-ballistic systems which impart energy to projectiles exclusively during launch. We investigated such trade-offs in the spring-propelled seeds of Loropetalum chinense , Hamamelis virginiana and Fortunearia sinensis . Using similar seed-shooting mechanisms, fruits of these confamilial plants (Hamamelidaceae) span an order of magnitude in spring and seed mass. We expected that as seed mass increases, launch speed decreases. Instead, launch speed was relatively constant regardless of seed mass. We tested if fruits shoot larger seeds by storing more elastic potential energy (PE). Spring mass and PE increased as seed mass increased (in order of increasing seed mass: L. chinense , H. virginiana , F. sinensis ). As seed mass to spring mass ratio increased (ratios: H. virginiana = 0.50, F. sinensis = 0.65, L. chinense = 0.84), mass-specific PE storage increased. The conversion efficiency of PE to seed kinetic energy (KE) decreased with increasing fruit mass. Therefore, similar launch speeds across scales occurred because (i) larger fruits stored more PE and (ii) smaller fruits had higher mass-specific PE storage and improved PE to KE conversion. By examining integrated spring and projectile mechanics in our focal species, we revealed diverse, energetic scaling strategies relevant to spring-propelled systems navigating energetic trade-offs.

Across countless marine invertebrates, coordination of closely spaced swimming appendages is key to producing diverse locomotory behaviors. Using a widespread mechanism termed hybrid metachronal propulsion, mantis shrimp swim by moving five paddle-like pleopods along their abdomen in a posterior to anterior sequence during the power stroke and a near-synchronous motion during the recovery stroke. Despite the ubiquity of this mechanism, it is not clear how hybrid metachronal swimmers coordinate and modify individual appendage movements to achieve a range of swimming capabilities. Using high-speed imaging, we measured pleopod kinematics of mantis shrimp ( Neogonodactylus bredini ), while they performed two swimming behaviors: burst swimming and taking off from the substrate. By tracking each of the five pleopods, we tested how stroke kinematics vary across swimming speeds and the two swimming behaviors. We found that mantis shrimp achieve faster swimming speeds through a combination of higher beat frequencies, smaller stroke durations, and partially via larger stroke angles. The five pleopods exhibit non-uniform kinematics that contribute to the coordination and forward propulsion of the whole system. Micro-hook structures (retinacula) connect each of the five pleopod pairs and differ in their attachment across pleopods-possibly contributing to passive kinematic control. We compare our findings in N. bredini to previous studies to identify commonalities across hybrid metachronal swimmers at high Reynolds numbers and centimeter scales. Through our large experimental dataset and by tracking each pleopod's movements, our study reveals key parameters by which mantis shrimp adjust and control their swimming, yielding diverse locomotor abilities., (© The Author(s) 2023. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology.)

Evolutionary theory suggests that individuals should express costly traits at a magnitude that optimizes the trait bearer's cost-benefit difference. Trait expression varies across a species because costs and benefits vary among individuals. For example, if large individuals pay lower costs than small individuals, then larger individuals should reach optimal cost-benefit differences at greater trait magnitudes. Using the cavitation-shooting weapons found in the big claws of male and female snapping shrimp, we test whether size- and sex-dependent expenditures explain scaling and sex differences in weapon size. We found that males and females from three snapping shrimp species (Alpheus heterochaelis, Alpheus angulosus, and Alpheus estuariensis) show patterns consistent with tradeoffs between weapon and abdomen size. For male A. heterochaelis, the species for which we had the greatest statistical power, smaller individuals showed steeper tradeoffs. Our extensive dataset in A. heterochaelis also included data about pairing, breeding season, and egg clutch size. Therefore, we could test for reproductive tradeoffs and benefits in this species. Female A. heterochaelis exhibited tradeoffs between weapon size and egg count, average egg volume, and total egg mass volume. For average egg volume, smaller females exhibited steeper tradeoffs. Furthermore, in males but not females, large weapons were positively correlated with the probability of being paired and the relative size of their pair mates. In conclusion, we identified size-dependent tradeoffs that could underlie reliable scaling of costly traits. Furthermore, weapons are especially beneficial to males and burdensome to females, which could explain why males have larger weapons than females., Competing Interests: JD, SP No competing interests declared, (© 2023, Dinh and Patek.)

Across the tree of life - from fungi to frogs - organisms wield small amounts of energy to generate fast and potent movements. These movements are propelled with elastic structures, and their loading and release are mediated by latch-like opposing forces. They comprise a class of elastic mechanisms termed latch-mediated spring actuation (LaMSA). Energy flow through LaMSA begins when an energy source loads elastic element(s) in the form of elastic potential energy. Opposing forces, often termed latches, prevent movement during loading of elastic potential energy. As the opposing forces are shifted, reduced or removed, elastic potential energy is transformed into kinetic energy of the spring and propelled mass. Removal of the opposing forces can occur instantaneously or throughout the movement, resulting in dramatically different outcomes for consistency and control of the movement. Structures used for storing elastic potential energy are often distinct from mechanisms that propel the mass: elastic potential energy is often distributed across surfaces and then transformed into localized mechanisms for propulsion. Organisms have evolved cascading springs and opposing forces not only to serially reduce the duration of energy release, but often to localize the most energy-dense events outside of the body to sustain use without self-destruction. Principles of energy flow and control in LaMSA biomechanical systems are emerging at a rapid pace. New discoveries are catalyzing remarkable growth of the historic field of elastic mechanisms through experimental biomechanics, synthesis of novel materials and structures, and high-performance robotics systems., Competing Interests: Competing interests The author declares no competing or financial interests., (© 2023. Published by The Company of Biologists Ltd.)

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., Competing Interests: Competing interests The authors declare no competing or financial interests., (© 2023. Published by The Company of Biologists Ltd.)

The smallest, fastest, repeated-use movements are propelled by power-dense elastic mechanisms, yet the key to their energetic control may be found in the latch-like mechanisms that mediate transformation from elastic potential energy to kinetic energy. Here, we tested how geometric latches enable consistent or variable outputs in ultrafast, spring-propelled systems. We constructed a reduced-order mathematical model of a spring-propelled system that uses a torque reversal (over-center) geometric latch. The model was parameterized to match the scales and mechanisms of ultrafast systems, specifically snapping shrimp. We simulated geometric and energetic configurations that enabled or reduced variation of strike durations and dactyl rotations given variation of stored elastic energy and latch mediation. Then, we collected an experimental dataset of the energy storage mechanism and ultrafast snaps of live snapping shrimp (Alpheus heterochaelis) and compared our simulations with their configuration. We discovered that snapping shrimp deform the propodus exoskeleton prior to the strike, which may contribute to elastic energy storage. Regardless of the amount of variation in spring loading duration, strike durations were far less variable than spring loading durations. When we simulated this species' morphological configuration in our mathematical model, we found that the low variability of strike duration is consistent with their torque reversal geometry. Even so, our simulations indicate that torque reversal systems can achieve either variable or invariant outputs through small adjustments to geometry. Our combined experiments and mathematical simulations reveal the capacity of geometric latches to enable, reduce or enhance variation of ultrafast movements in biological and synthetic systems., Competing Interests: Competing interests The authors declare no competing or financial interests., (© 2023. Published by The Company of Biologists Ltd.)

Ultrafast movements propelled by springs and released by latches are thought limited to energetic adjustments prior to movement, and seemingly cannot adjust once movement begins. Even so, across the tree of life, ultrafast organisms navigate dynamic environments and generate a range of movements, suggesting unrecognized capabilities for control. We develop a framework of control pathways leveraging the non-linear dynamics of spring-propelled, latch-released systems. We analytically model spring dynamics and develop reduced-parameter models of latch dynamics to quantify how they can be tuned internally or through changing external environments. Using Lagrangian mechanics, we test feedforward and feedback control implementation via spring and latch dynamics. We establish through empirically-informed modeling that ultrafast movement can be controllably varied during latch release and spring propulsion. A deeper understanding of the interconnection between multiple control pathways, and the tunability of each control pathway, in ultrafast biomechanical systems presented here has the potential to expand the capabilities of synthetic ultra-fast systems and provides a new framework to understand the behaviors of fast organisms subject to perturbations and environmental non-idealities., (© 2023 IOP Publishing Ltd.)

Small organisms use propulsive springs rather than muscles to repeatedly actuate high acceleration movements, even when constrained to tiny displacements and limited by inertial forces. Through integration of a large kinematic dataset, measurements of elastic recoil, energetic math modeling and dynamic math modeling, we tested how trap-jaw ants (Odontomachus brunneus) utilize multiple elastic structures to develop ultrafast and precise mandible rotations at small scales. We found that O. brunneus develops torque on each mandible using an intriguing configuration of two springs: their elastic head capsule recoils to push and the recoiling muscle-apodeme unit tugs on each mandible. Mandibles achieved precise, planar, circular trajectories up to 49,100 rad s-1 (470,000 rpm) when powered by spring propulsion. Once spring propulsion ended, the mandibles moved with unconstrained and oscillatory rotation. We term this mechanism a 'dual spring force couple', meaning that two springs deliver energy at two locations to develop torque. Dynamic modeling revealed that dual spring force couples reduce the need for joint constraints and thereby reduce dissipative joint losses, which is essential to the repeated use of ultrafast, small systems. Dual spring force couples enable multifunctionality: trap-jaw ants use the same mechanical system to produce ultrafast, planar strikes driven by propulsive springs and for generating slow, multi-degrees of freedom mandible manipulations using muscles, rather than springs, to directly actuate the movement. Dual spring force couples are found in other systems and are likely widespread in biology. These principles can be incorporated into microrobotics to improve multifunctionality, precision and longevity of ultrafast systems., Competing Interests: Competing interests The authors declare no competing or financial interests., (© 2022. Published by The Company of Biologists Ltd.)

Numerous aquatic invertebrates use drag-based metachronal rowing for swimming, in which closely spaced appendages are oscillated starting from the posterior, with each appendage phase-shifted in time relative to its neighbor. Continuously swimming species such as Antarctic krill generally use "pure metachronal rowing" consisting of a metachronal power stroke and a metachronal recovery stroke, while burst swimming species such as many copepods and mantis shrimp typically use "hybrid metachronal rowing" consisting of a metachronal power stroke followed by a synchronous or nearly synchronous recovery stroke. Burst swimming organisms need to rapidly accelerate in order to capture prey and/or escape predation, and it is unknown whether hybrid metachronal rowing can augment acceleration and swimming speed compared to pure metachronal rowing. Simulations of rigid paddles undergoing simple harmonic motion showed that collisions between adjacent paddles restrict the maximum stroke amplitude for pure metachronal rowing. Hybrid metachronal rowing similar to that observed in mantis shrimp (Neogonodactylus bredini) permits oscillation at larger stroke amplitude while avoiding these collisions. We comparatively examined swimming speed, acceleration, and wake structure of pure and hybrid metachronal rowing strategies by using a self-propelling robot. Both swimming speed and peak acceleration of the robot increased with increasing stroke amplitude. Hybrid metachronal rowing permitted operation at larger stroke amplitude without collision of adjacent paddles on the robot, augmenting swimming speed and peak acceleration. Hybrid metachronal rowing generated a dispersed wake unlike narrower, downward-angled jets generated by pure metachronal rowing. Our findings suggest that burst swimming animals with small appendage spacing, such as copepods and mantis shrimp, can use hybrid metachronal rowing to generate large accelerations via increasing stroke amplitude without concern of appendage collision., (© The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology.)

Efficient and effective generation of high-acceleration movement in biology requires a process to control energy flow and amplify mechanical power from power density-limited muscle. Until recently, this ability was exclusive to ultrafast, small organisms, and this process was largely ascribed to the high mechanical power density of small elastic recoil mechanisms. In several ultrafast organisms, linkages suddenly initiate rotation when they overcenter and reverse torque; this process mediates the release of stored elastic energy and enhances the mechanical power output of extremely fast, spring-actuated systems. Here we report the discovery of linkage dynamics and geometric latching that reveals how organisms and synthetic systems generate extremely high-acceleration, short-duration movements. Through synergistic analyses of mantis shrimp strikes, a synthetic mantis shrimp robot, and a dynamic mathematical model, we discover that linkages can exhibit distinct dynamic phases that control energy transfer from stored elastic energy to ultrafast movement. These design principles are embodied in a 1.5-g mantis shrimp scale mechanism capable of striking velocities over 26 m [Formula: see text] in air and 5 m [Formula: see text] in water. The physical, mathematical, and biological datasets establish latching mechanics with four temporal phases and identify a nondimensional performance metric to analyze potential energy transfer. These temporal phases enable control of an extreme cascade of mechanical power amplification. Linkage dynamics and temporal phase characteristics are easily adjusted through linkage design in robotic and mathematical systems and provide a framework to understand the function of linkages and latches in biological systems., Competing Interests: The authors declare no competing interest.

Latch-mediated spring actuation (LaMSA) is used by small organisms to produce high acceleration movements. Mathematical models predict that acceleration increases as LaMSA systems decrease in size. Adult mantis shrimp use a LaMSA mechanism in their raptorial appendages to produce extremely fast strikes. Until now, however, it was unclear whether mantis shrimp at earlier life-history stages also strike using elastic recoil and latch mediation. We tested whether larval mantis shrimp (Gonodactylaceus falcatus) use LaMSA and, because of their smaller size, achieve higher strike accelerations than adults of other mantis shrimp species. Based on microscopy and kinematic analyses, we discovered that larval G. falcatus possess the components of, and actively use, LaMSA during their fourth larval stage, which is the stage of development when larvae begin feeding. Larvae performed strikes at high acceleration and speed (mean: 4.133×105 rad s-2, 292.7 rad s-1; 12 individuals, 25 strikes), which are of the same order of magnitude as for adults - even though adult appendages are up to two orders of magnitude longer. Larval strike speed (mean: 0.385 m s-1) exceeded the maximum swimming speed of similarly sized organisms from other species by several orders of magnitude. These findings establish the developmental timing and scaling of the mantis shrimp LaMSA mechanism and provide insights into the kinematic consequences of scaling limits in tiny elastic mechanisms., Competing Interests: Competing interests The authors declare no competing or financial interests., (© 2021. Published by The Company of Biologists Ltd.)

Small organisms can produce powerful, sub-millisecond impacts by moving tiny structures at high accelerations. We developed and validated a pendulum device to measure the impact energetics of microgram-sized trap-jaw ant mandibles accelerated against targets at 10 5  m s -2 Trap-jaw ants ( Odontomachus brunneus ; 19 individuals, 212 strikes) were suspended on one pendulum and struck swappable targets that were either attached to an opposing pendulum or fixed in place. Mean post-impact kinetic energy (energy from a strike converted to pendulum motion) was higher with a stiff target (21.0-21.5 µJ) than with a compliant target (6.4-6.5 µJ). Target mobility had relatively little influence on energy transfer. Mean contact duration of strikes against stiff targets was shorter (3.9-4.5 ms) than against compliant targets (6.2-7.9 ms). Shorter contact duration was correlated with higher post-impact kinetic energy. These findings contextualize and provide an energetic explanation for the diverse, natural uses of trap-jaw ant strikes such as impaling prey, launching away threats and performing mandible-powered jumps. The strong effect of target material on energetic exchange suggests material interactions as an avenue for tuning performance of small, high acceleration impacts. Our device offers a foundation for novel research into the ecomechanics and evolution of tiny biological impacts and their application in synthetic systems., Competing Interests: Competing interestsThe authors declare no competing or financial interests. Author contributionsConceptualization: J.F.J.; Methodology: J.F.J.; Validation: J.F.J., S.B., S.N.P.; Formal analysis: J.F.J., S.B., S.N.P.; Investigation: J.F.J.; Resources: S.N.P.; Writing - original draft: J.F.J.; Writing - review & editing: J.F.J., S.B., S.N.P.; Visualization: J.F.J.; Supervision: J.F.J., S.N.P.; Project administration: J.F.J., S.N.P.; Funding acquisition: S.N.P., (© 2021. Published by The Company of Biologists Ltd.)

The inherent force-velocity trade-off of muscles and motors can be overcome by instead loading and releasing energy in springs to power extreme movements. A key component of this paradigm is the latch that mediates the release of spring energy to power the motion. Latches have traditionally been considered as switches; they maintain spring compression in one state and allow the spring to release energy without constraint in the other. Using a mathematical model of a simplified contact latch, we reproduce this instantaneous release behaviour and also demonstrate that changing latch parameters (latch release velocity and radius) can reduce and delay the energy released by the spring. We identify a critical threshold between instantaneous and delayed release that depends on the latch, spring, and mass of the system. Systems with stiff springs and small mass can attain a wide range of output performance, including instantaneous behaviour, by changing latch release velocity. We validate this model in both a physical experiment as well as with data from the Dracula ant, Mystrium camillae , and propose that latch release velocity can be used in both engineering and biological systems to control energy output.

In the course of a single raptorial strike by a mantis shrimp (Stomatopoda), the stages of energy release span six to seven orders of magnitude of duration. To achieve their mechanical feats of striking at the outer limits of speeds, accelerations, and impacts among organisms, they use a mechanism that exemplifies a cascade of energy release-beginning with a slow and forceful, spring-loading muscle contraction that lasts for hundreds of milliseconds and ending with implosions of cavitation bubbles that occur in nanoseconds. Mantis shrimp use an elastic mechanism built of exoskeleton and controlled with a latching mechanism. Inspired by both their mechanical capabilities and evolutionary diversity, research on mantis shrimp strikes has provided interdisciplinary and fundamental insights to the fields of elastic mechanisms, fluid dynamics, evolutionary dynamics, contest dynamics, the physics of fast, small systems, and the rapidly-expanding field of bioinspired materials science. Even with these myriad connections, numerous discoveries await, especially in the arena of energy flow through materials actuating and controlling fast, impact fracture resistant systems., (© The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. For permissions please email: journals.permissions@oup.com.)

As animals get smaller, their ability to generate usable work from muscle contraction is decreased by the muscle's force-velocity properties, thereby reducing their effective jump height. Very small animals use a spring-actuated system, which prevents velocity effects from reducing available energy. Since force-velocity properties reduce the usable work in even larger animals, why don't larger animals use spring-actuated jumping systems as well? We will show that muscle length-tension properties limit spring-actuated systems to generating a maximum one-third of the possible work that a muscle could produce-greatly restricting the jumping height of spring-actuated jumpers. Thus a spring-actuated jumping animal has a jumping height that is one-third of the maximum possible jump height achievable were 100% of the possible muscle work available. Larger animals, which could theoretically use all of the available muscle energy, have a maximum jumping height that asymptotically approaches a value that is about three times higher than that of spring-actuated jumpers. Furthermore, a size related "crossover point" is evident for these two jumping mechanisms: animals smaller than this point can jump higher with a spring-actuated mechanism, while animals larger than this point can jump higher with a muscle-actuated mechanism. We demonstrate how this limit on energy storage is a consequence of the interaction between length-tension properties of muscles and spring stiffness. We indicate where this crossover point occurs based on modeling and then use jumping data from the literature to validate that larger jumping animals generate greater jump heights with muscle-actuated systems than spring-actuated systems., (© The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology.)

Elastically-driven motion has been used as a strategy to achieve high speeds in small organisms and engineered micro-robotic devices. We examine the size-scaling relations determining the limit of elastic energy release from elastomer bands that efficiently cycle mechanical energy with minimal loss. The maximum center-of-mass velocity of the elastomer bands was found to be size-scale independent, while smaller bands demonstrated larger accelerations and shorter durations of elastic energy release. Scaling relationships determined from these measurements are consistent with the performance of small organisms and engineered devices which utilize elastic elements to power motion.

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., Competing Interests: Competing interestsThe authors declare no competing or financial interests., (© 2019. Published by The Company of Biologists Ltd.)

Jumping is often achieved using propulsive legs, yet legless leaping has evolved multiple times. We examined the kinematics, energetics and morphology of long-distance jumps produced by the legless larvae of gall midges ( Asphondylia sp.). They store elastic energy by forming their body into a loop and pressurizing part of their body to form a transient 'leg'. They prevent movement during elastic loading by placing two regions covered with microstructures against each other, which likely serve as a newly described adhesive latch. Once the latch releases, the transient 'leg' launches the body into the air. Their average takeoff speeds (mean: 0.85 m s -1 ; range: 0.39-1.27 m s -1 ) and horizontal travel distances (up to 36 times body length or 121 mm) rival those of legged insect jumpers and their mass-specific power density (mean: 910 W kg -1 ; range: 150-2420 W kg -1 ) indicates the use of elastic energy storage to launch the jump. Based on the forces reported for other microscale adhesive structures, the adhesive latching surfaces are sufficient to oppose the loading forces prior to jumping. Energetic comparisons of insect larval crawling versus jumping indicate that these jumps are orders of magnitude more efficient than would be possible if the animals had crawled an equivalent distance. These discoveries integrate three vibrant areas in engineering and biology - soft robotics, small, high-acceleration systems, and adhesive systems - and point toward a rich, and as-yet untapped area of biological diversity of worm-like, small, legless jumpers., Competing Interests: Competing interestsThe authors declare no competing or financial interests., (© 2019. Published by The Company of Biologists Ltd.)

Measurements of energy use, and its scaling with size, are critical to understanding how organisms accomplish myriad tasks. For example, energy budgets are central to game theory models of assessment during contests and underlie patterns of feeding behavior. Clear tests connecting energy to behavioral theory require measurements of the energy use of single individuals for particular behaviors. Many species of mantis shrimp (Stomatopoda: Crustacea) use elastic energy storage to power high-speed strikes that they deliver to opponents during territorial contests and to hard-shelled prey while feeding. We compared the scaling of strike kinematics and energetics between feeding and contests in the mantis shrimp Neogonodactylus bredini We filmed strikes with high-speed video, measured strike velocity and used a mathematical model to calculate strike energy. During contests, strike velocity did not scale with body size but strike energy scaled positively with size. Conversely, while feeding, strike velocity decreased with increasing size and strike energy did not vary according to body size. Individuals most likely achieved this strike variation through differential compression of their exoskeletal spring prior to the strike. Post hoc analyses found that N. bredini used greater velocity and energy when striking larger opponents, yet variation in prey size was not accompanied by varying strike velocity or energetics. Our estimates of energetics inform prior tests of contest and feeding behavior in this species. More broadly, our findings elucidate the role behavioral context plays in measurements of animal performance., Competing Interests: Competing interestsThe authors declare no competing or financial interests., (© 2019. Published by The Company of Biologists Ltd.)

Many predators fracture strong mollusk shells, requiring specialized weaponry and behaviors. The current shell fracture paradigm is based on jaw- and claw-based predators that slowly apply forces (high impulse, low peak force). However, predators also strike shells with transient intense impacts (low impulse, high peak force). Toward the goal of incorporating impact fracture strategies into the prevailing paradigm, we measured how mantis shrimp ( Neogonodactylus bredini ) impact snail shells, tested whether they strike shells in different locations depending on prey shape ( Nerita spp., Cenchritis muricatus , Cerithium spp.) and deployed a physical model (Ninjabot) to test the effectiveness of strike locations. We found that, contrary to their formidable reputation, mantis shrimp struck shells tens to hundreds of times while targeting distinct shell locations. They consistently struck the aperture of globular shells and changed from the aperture to the apex of high-spired shells. Ninjabot tests revealed that mantis shrimp avoid strike locations that cause little damage and that reaching the threshold for eating soft tissue is increasingly difficult as fracture progresses. Their ballistic strategy requires feed-forward control, relying on extensive pre-strike set-up, unlike jaw- and claw-based strategies that can use real-time neural feedback when crushing. However, alongside this pre-processing cost to impact fracture comes the ability to circumvent gape limits and thus process larger prey. In sum, mantis shrimp target specific shell regions, alter their strategy depending on shell shape, and present a model system for studying the physics and materials of impact fracture in the context of the rich evolutionary history of predator-prey interactions., Competing Interests: Competing interestsThe authors declare no competing or financial interests., (© 2018. Published by The Company of Biologists Ltd.)

Mechanical power limitations emerge from the physical trade-off between force and velocity. Many biological systems incorporate power-enhancing mechanisms enabling extraordinary accelerations at small sizes. We establish how power enhancement emerges through the dynamic coupling of motors, springs, and latches and reveal how each displays its own force-velocity behavior. We mathematically demonstrate a tunable performance space for spring-actuated movement that is applicable to biological and synthetic systems. Incorporating nonideal spring behavior and parameterizing latch dynamics allows the identification of critical transitions in mass and trade-offs in spring scaling, both of which offer explanations for long-observed scaling patterns in biological systems. This analysis defines the cascading challenges of power enhancement, explores their emergent effects in biological and engineered systems, and charts a pathway for higher-level analysis and synthesis of power-amplified systems., (Copyright © 2018 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.)

The extraordinary snaps of snapping shrimp evolved through simple morphological transitions with remarkable mechanical results., (Copyright © 2017 Elsevier Ltd. All rights reserved.)

Safe and effective conflict resolution is critical for survival and reproduction. Theoretical models describe how animals resolve conflict by assessing their own and/or their opponent's ability (resource holding potential, RHP), yet experimental tests of these models are often inconclusive. Recent reviews have suggested this uncertainty could be alleviated by using multiple approaches to test assessment models. The mantis shrimp Neogonodactylus bredini presents visual displays and ritualistically exchanges high-force strikes during territorial contests. We tested how N. bredini contest dynamics were explained by any of three assessment models-pure self-assessment, cumulative assessment and mutual assessment-using correlations and a novel, network analysis-based sequential behavioural analysis. We staged dyadic contests over burrow access between competitors matched either randomly or based on body size. In both randomly and size-matched contests, the best metric of RHP was body mass. Burrow residency interacted with mass to predict outcome. Correlations between contest costs and RHP rejected pure self-assessment, but could not fully differentiate between cumulative and mutual assessment. The sequential behavioural analysis ruled out cumulative assessment and supported mutual assessment. Our results demonstrate how multiple analyses provide strong inference to tests of assessment models and illuminate how individual behaviours constitute an assessment strategy., (© 2018 The Author(s).)

Thousands of fungal species use surface energy to power the launch of their ballistospores. The surface energy is released when a spherical Buller's drop at the spore's hilar appendix merges with a flattened drop on the adaxial side of the spore. The launching mechanism is primarily understood in terms of energetic models, and crucial features such as launching directionality are unexplained. Integrating experiments and simulations, we advance a mechanistic model based on the capillary-inertial coalescence between the Buller's drop and the adaxial drop, a pair that is asymmetric in size, shape and relative position. The asymmetric coalescence is surprisingly effective and robust, producing a launching momentum governed by the Buller's drop and a launching direction along the adaxial plane of the spore. These key functions of momentum generation and directional control are elucidated by numerical simulations, demonstrated on spore-mimicking particles, and corroborated by published ballistospore kinematics. Our work places the morphological and kinematic diversity of ballistospores into a general mechanical framework, and points to a generic catapulting mechanism of colloidal particles with implications for both biology and engineering., (© 2017 The Author(s).)

Invertebrate biomechanics focuses on mechanical analyses of non-vertebrate animals, which at root is no different in aim and technique from vertebrate biomechanics, or for that matter the biomechanics of plants and fungi. But invertebrates are special - they are fabulously diverse in form, habitat, and ecology and manage this without the use of hard, internal skeletons. They are also numerous and, in many cases, tractable in an experimental and field setting. In this Primer, we will probe three axes of invertebrate diversity: worms (Phylum Annelida), spiders (Class Arachnida) and insects (Class Insecta); three habitats: subterranean, terrestrial and airborne; and three integrations with other fields: ecology, engineering and evolution. Our goal is to capture the field of invertebrate biomechanics, which has blossomed from having a primary focus on discoveries at the interface of physics and biology to being inextricably linked with integrative challenges that span biology, physics, mathematics and engineering., (Copyright © 2017 Elsevier Ltd. All rights reserved.)

The influence of biophysical relationships on rates of morphological evolution is a cornerstone of evolutionary theory. Mechanical sensitivity-the correlation strength between mechanical output and the system's underlying morphological components-is thought to impact the evolutionary dynamics of form-function relationships, yet has rarely been examined. Here, we compare the evolutionary rates of the mechanical components of the four-bar linkage system in the raptorial appendage of mantis shrimp (Order Stomatopoda). This system's mechanical output (kinematic transmission (KT)) is highly sensitive to variation in its output link, and less sensitive to its input and coupler links. We found that differential mechanical sensitivity is associated with variation in evolutionary rate: KT and the output link exhibit faster rates of evolution than the input and coupler links to which KT is less sensitive. Furthermore, for KT and, to a lesser extent, the output link, rates of evolution were faster in 'spearing' stomatopods than 'smashers', indicating that mechanical sensitivity may influence trait-dependent diversification. Our results suggest that mechanical sensitivity can impact morphological evolution and guide the process of phenotypic diversification. The connection between mechanical sensitivity and evolutionary rates provides a window into the interaction between physical rules and the evolutionary dynamics of morphological diversification., (© 2017 The Author(s).)

Countless aquatic animals rotate appendages through the water, yet fluid forces are typically modeled with translational motion. To elucidate the hydrodynamics of rotation, we analyzed the raptorial appendages of mantis shrimp (Stomatopoda) using a combination of flume experiments, mathematical modeling and phylogenetic comparative analyses. We found that computationally efficient blade-element models offered an accurate first-order approximation of drag, when compared with a more elaborate computational fluid-dynamic model. Taking advantage of this efficiency, we compared the hydrodynamics of the raptorial appendage in different species, including a newly measured spearing species, Coronis scolopendra The ultrafast appendages of a smasher species (Odontodactylus scyllarus) were an order of magnitude smaller, yet experienced values of drag-induced torque similar to those of a spearing species (Lysiosquillina maculata). The dactyl, a stabbing segment that can be opened at the distal end of the appendage, generated substantial additional drag in the smasher, but not in the spearer, which uses the segment to capture evasive prey. Phylogenetic comparative analyses revealed that larger mantis shrimp species strike more slowly, regardless of whether they smash or spear their prey. In summary, drag was minimally affected by shape, whereas size, speed and dactyl orientation dominated and differentiated the hydrodynamic forces across species and sizes. This study demonstrates the utility of simple mathematical modeling for comparative analyses and illustrates the multi-faceted consequences of drag during the evolutionary diversification of rotating appendages., (© 2016. Published by The Company of Biologists Ltd.)

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., (© 2016 The Author(s).)

Related species that share similar biomechanical systems and segmentation patterns may exhibit different patterns of morphological covariation. We examined morphological covariation of the potent prey capture appendage of two mantis shrimp (Stomatopoda) species-a spearer (Squilla empusa) and smasher (Gonodactylaceus falcatus). We assessed three frameworks for modularity, two based on the biomechanics of the appendage and one based on its segmentation as a proxy for shared developmental pathways. We collected morphometric data from S. empusa, and compared morphological covariation patterns across the raptorial appendage with patterns from a new analysis of previously published morphometric data from G. falcatus. The relative importance of the different hypothetical influences differed between the two species, and was dependent on whether specimens were analyzed all together or subdivided based on sex or sub-populations, including one particularly distinct population in the Gulf of Mexico. We also found an intriguing handedness pattern in which right-hand appendages had a variable number of spines, whereas the left had a constant number of spines. Overall, our findings highlight the importance of testing multiple, alternative frameworks for morphological covariation and suggest that mantis shrimp experience contrasting influences on covariation depending on their feeding mechanisms., (© 2016 Wiley Periodicals, Inc.)

To circumvent the limits of muscle, ultrafast movements achieve high power through the use of springs and latches. The time scale of these movements is too short for control through typical neuromuscular mechanisms, thus ultrafast movements are either invariant or controlled prior to movement. We tested whether mantis shrimp (Stomatopoda: Neogonodactylus bredini) vary their ultrafast smashing strikes and, if so, how this control is achieved prior to movement. We collected high-speed images of strike mechanics and electromyograms of the extensor and flexor muscles that control spring compression and latch release. During spring compression, lateral extensor and flexor units were co-activated. The strike initiated several milliseconds after the flexor units ceased, suggesting that flexor activity prevents spring release and determines the timing of strike initiation. We used linear mixed models and Akaike's information criterion to serially evaluate multiple hypotheses for control mechanisms. We found that variation in spring compression and strike angular velocity were statistically explained by spike activity of the extensor muscle. The results show that mantis shrimp can generate kinematically variable strikes and that their kinematics can be changed through adjustments to motor activity prior to the movement, thus supporting an upstream, central-nervous-system-based control of ultrafast movement. Based on these and other findings, we present a shishiodoshi model that illustrates alternative models of control in biological ballistic systems. The discovery of feed-forward control in mantis shrimp sets the stage for the assessment of targets, strategic variation in kinematics and the role of learning in ultrafast animals., (© 2016. Published by The Company of Biologists Ltd.)

Mantis shrimp strike with extreme impact forces that are deadly to prey. They also strike conspecifics during territorial contests, yet theoretical and empirical findings in aggressive behaviour research suggest competitors should resolve conflicts using signals before escalating to dangerous combat. We tested how Neogonodactylus bredini uses two ritualized behaviours to resolve size-matched contests: meral spread visual displays and telson (tailplate) strikes. We predicted that (i) most contests would be resolved by meral spreads, (ii) meral spreads would reliably signal strike force and (iii) strike force would predict contest success. The results were unexpected for each prediction. Contests were not resolved by meral spreads, instead escalating to striking in 33 of 34 experiments. The size of meral spread components did not strongly correlate with strike force. Strike force did not predict contest success; instead, winners delivered more strikes. Size-matched N. bredini avoid deadly combat not by visual displays, but by ritualistically and repeatedly striking each other's telsons until the loser retreats. We term this behaviour 'telson sparring', analogous to sparring in other weapon systems. We present an alternative framework for mantis shrimp contests in which the fight itself is the signal, serving as a non-lethal indicator of aggressive persistence or endurance., (© 2015 The Author(s).)

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., (© 2015 Wiley Periodicals, Inc.)

A classic question in evolutionary biology is how form-function relationships promote or limit diversification. Mechanical metrics, such as kinematic transmission (KT) in linkage systems, are useful tools for examining the evolution of form and function in a comparative context. The convergence of disparate systems on equivalent metric values (mechanical equivalence) has been highlighted as a source of potential morphological diversity under the assumption that morphology can evolve with minimal impact on function. However, this assumption does not account for mechanical sensitivity-the sensitivity of the metric to morphological changes in individual components of a structure. We examined the diversification of a four-bar linkage system in mantis shrimp (Stomatopoda), and found evidence for both mechanical equivalence and differential mechanical sensitivity. KT exhibited variable correlations with individual linkage components, highlighting the components that influence KT evolution, and the components that are free to evolve independently from KT and thereby contribute to the observed pattern of mechanical equivalence. Determining the mechanical sensitivity in a system leads to a deeper understanding of both functional convergence and morphological diversification. This study illustrates the importance of multi-level analyses in delineating the factors that limit and promote diversification in form-function systems., (© 2015 The Author(s) Published by the Royal Society. All rights reserved.)

Mechanical redundancy within a biomechanical system (e.g., many-to-one mapping) allows morphologically divergent organisms to maintain equivalent mechanical outputs. However, most organisms depend on the integration of more than one biomechanical system. Here, we test whether coupled mechanical systems follow a pattern of amplification (mechanical changes are congruent and evolve toward the same functional extreme) or independence (mechanisms evolve independently). We examined the correlated evolution and evolutionary pathways of the coupled four-bar linkage and lever systems in mantis shrimp (Stomatopoda) ultrafast raptorial appendages. We examined models of character evolution in the framework of two divergent groups of stomatopods-"smashers" (hammer-shaped appendages) and "spearers" (bladed appendages). Smashers tended to evolve toward force amplification, whereas spearers evolved toward displacement amplification. These findings show that coupled biomechanical systems can evolve synergistically, thereby resulting in functional amplification rather than mechanical redundancy., (© 2014 The Author(s). Evolution © 2014 The Society for the Study of Evolution.)

Should animals operating at great speeds and accelerations use fast or slow muscles? The answer hinges on a fundamental trade-off: muscles can be maximally fast or forceful, but not both. Direct lever systems offer a straightforward manifestation of this trade-off, yet the fastest organisms use power amplification, not direct lever action. Power-amplified systems typically use slow, forceful muscles to preload springs, which then rapidly release elastic potential energy to generate high speeds and accelerations. However, a fast response to a stimulus may necessitate fast spring-loading. Across 22 mantis shrimp species (Stomatopoda), this study examined how muscle anatomy correlates with spring mechanics and appendage type. We found that muscle force is maximized through physiological cross-sectional area, but not through sarcomere length. Sit-and-wait predators (spearers) had the shortest sarcomere lengths (fastest contractions) and the slowest strike speeds. The species that crush shells (smashers) had the fastest speeds, most forceful springs, and longest sarcomeres. The origin of the smasher clade yielded dazzlingly high accelerations, perhaps due to the release from fast spring-loading for evasive prey capture. This study offers a new window into the dynamics of force-speed trade-offs in muscles in the biomechanical, comparative evolutionary framework of power-amplified systems., (© 2014 The Author(s). Evolution © 2014 The Society for the Study of Evolution.)

To study the mechanical principles and fluid dynamics of ultrafast power-amplified systems, we built Ninjabot, a physical model of the extremely fast mantis shrimp (Stomatopoda). Ninjabot rotates a to-scale appendage within the environmental conditions and close to the kinematic range of mantis shrimp's rotating strike. Ninjabot is an adjustable mechanism that can repeatedly vary independent properties relevant to fast aquatic motions to help isolate their individual effects. Despite exceeding the kinematics of previously published biomimetic jumpers and reaching speeds in excess of 25 m s(-1) at accelerations of 3.2 × 10(4) m s(-2), Ninjabot can still be outstripped by the fastest mantis shrimp, Gonodactylus smithii, measured for the first time in this study. G. smithii reached 30 m s(-1) at accelerations of 1.5 × 10(5) m s(-2). While mantis shrimp produce cavitation upon impact with their prey, they do not cavitate during the forward portion of their strike despite their extreme speeds. In order to determine how closely to match Ninjabot and mantis shrimp kinematics to capture this cavitation behavior, we used Ninjabot to produce strikes of varying kinematics and to measure cavitation presence or absence. Using Akaike Information Criterion to compare statistical models that correlated cavitation with a variety of kinematic properties, we found that in rotating and accelerating biological conditions, cavitation inception is best explained only by maximum linear velocity.

The dynamic interplay among structure, function, and phylogeny form a classic triad of influences on the patterns and processes of biological diversification. Although these dynamics are widely recognized as important, quantitative analyses of their interactions have infrequently been applied to biomechanical systems. Here we analyze these factors using a fundamental biomechanical mechanism: power amplification. Power-amplified systems use springs and latches to generate extremely fast and powerful movements. This study focuses specifically on the power amplification mechanism in the fast raptorial appendages of mantis shrimp (Crustacea: Stomatopoda). Using geometric morphometric and phylogenetic comparative analyses, we measured evolutionary modularity and rates of morphological evolution of the raptorial appendage's biomechanical components. We found that "smashers" (hammer-shaped raptorial appendages) exhibit lower modularity and 10-fold slower rates of morphological change when compared to non-smashers (spear-shaped or undifferentiated appendages). The morphological and biomechanical integration of this system at a macroevolutionary scale and the presence of variable rates of evolution reveal a balance between structural constraints, functional variation, and the "roles of development and genetics" in evolutionary diversification., (© 2013 The Author(s). Evolution © 2013 The Society for the Study of Evolution.)

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.