Soft skeletons transmit force with variable gearing.

A hydrostatic skeleton allows a soft body to transmit muscular force via internal pressure. A human's tongue, an octopus' arm and a nematode's body illustrate the pervasive presence of hydrostatic skeletons among animals, which has inspired the design of soft engineered actuators. However, there is a need for a theoretical basis for understanding how hydrostatic skeletons apply mechanical work. We therefore modeled the shape change and mechanics of natural and engineered hydrostatic skeletons to determine their mechanical advantage (MA) and displacement advantage (DA). These models apply to a variety of biological structures, but we explicitly consider the tube feet of a sea star and the body segments of an earthworm, and contrast them with a hydraulic press and a McKibben actuator. A helical winding of stiff, elastic fibers around these soft actuators plays a critical role in their mechanics by maintaining a cylindrical shape, distributing forces throughout the structure and storing elastic energy. In contrast to a single-joint lever system, soft hydrostats exhibit variable gearing with changes in MA generated by deformation in the skeleton. We found that this gearing is affected by the transmission efficiency of mechanical work (MA×DA) or, equivalently, the ratio of output to input work. The transmission efficiency changes with the capacity to store elastic energy within helically wrapped fibers or associated musculature. This modeling offers a conceptual basis for understanding the relationship between the morphology of hydrostatic skeletons and their mechanical performance.

Cooperative transport in sea star locomotion.

It is unclear how animals with radial symmetry control locomotion without a brain. Using a combination of experiments, mathematical modeling, and robotics, we tested the extent to which this control emerges in sea stars (Protoreaster nodosus) from the local control of their hundreds of feet and their mechanical interactions with the body. We discovered that these animals compensate for an experimental increase in their submerged weight by recruiting more feet that synchronize in the power stroke of the locomotor cycle during their bouncing gait. Mathematical modeling of the mechanics of a sea star replicated this response to loading without a central controller. A robotic sea star was found to similarly recruit more actuators under higher loads through purely decentralized control. These results suggest that an array of biological or engineered actuators are capable of cooperative transport where the actuators are dynamically recruited by the mechanics of the body. In particular, the body's vertical oscillations serve to recruit feet in greater numbers to overcome the weight to propel the body forward. This form of distributed control contrasts the conventional view of animal locomotion as governed by the central nervous system and offers inspiration for the design of engineered devices with arrays of actuators.

Through the looking glass: attempting to predict future opportunities and challenges in experimental biology.

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.

A lionfish-inspired predation strategy in planar structured environments.

This paper investigates a pursuit-evasion game with a single pursuer and evader in a bounded environment, inspired by observations of predation attempts by lionfish (Pterois sp.). The pursuer tracks the evader with a pure pursuit strategy while using an additional bioinspired tactic to trap the evader, i.e. minimize the evader's escape routes. Specifically, the pursuer employs symmetric appendages inspired by the large pectoral fins of lionfish, but this expansion increases its drag and therefore its work to capture the evader. The evader employs a bioinspired randomly-directed escape strategy to avoid capture and collisions with the boundary. Here we investigate the trade-off between minimizing the work to capture the evader and minimizing the evader's escape routes. By using the pursuer's expected work to capture as a cost function, we determine when the pursuer should expand its appendages as a function of the relative distance to the evader and the evader's proximity to the boundary. Visualizing the pursuer's expected work to capture everywhere in the bounded domain, yields additional insights about optimal pursuit trajectories and illustrates the role of the boundary in predator-prey interactions.

Evaluating evasion strategies in zebrafish larvae.

An effective evasion strategy allows prey to survive encounters with predators. Prey are generally thought to escape in a direction that is either random or serves to maximize the minimum distance from the predator. Here, we introduce a comprehensive approach to determine the most likely evasion strategy among multiple hypotheses and the role of biomechanical constraints on the escape response of prey fish. Through a consideration of six strategies with sensorimotor noise and previous kinematic measurements, our analysis shows that zebrafish larvae generally escape in a direction orthogonal to the predator's heading. By sensing only the predator's heading, this orthogonal strategy maximizes the distance from fast-moving predators, and, when operating within the biomechanical constraints of the escape response, it provides the best predictions of prey behavior among all alternatives. This work demonstrates a framework for resolving the strategic basis of evasion in predator-prey interactions, which could be applied to a broad diversity of animals.

Evaluating Evasion Strategies in Zebrafish Larvae.

An effective evasion strategy allows prey to survive encounters with predators. Prey are generally thought to escape in a direction that is either random or serves to maximize the minimum distance from the predator. Here we introduce a comprehensive approach to determine the most likely evasion strategy among multiple hypotheses and the role of biomechanical constraints on the escape response of prey fish. Through a consideration of six strategies with sensorimotor noise and previous kinematic measurements, our analysis shows that zebrafish larvae generally escape in a direction orthogonal to the predator's heading. By sensing only the predator's heading, this orthogonal strategy maximizes the distance from fast-moving predators, and, when operating within the biomechanical constraints of the escape response, it provides the best predictions of prey behavior among all alternatives. This work demonstrates a framework for resolving the strategic basis of evastion in predator-prey interactions, which could be applied to a broad diversity of animals.

Evaluating Evasion Strategies in Zebrafish Larvae.

An effective evasion strategy allows prey to survive encounters with predators. Prey are generally thought to escape in a direction that is either random or serves to maximize the minimum distance from the predator. Here we introduce a comprehensive approach to determine the most likely evasion strategy among multiple hypotheses and the role of biomechanical constraints on the escape response of prey fish. Through a consideration of six strategies with sensorimotor noise and previous kinematic measurements, our analysis shows that zebrafish larvae generally escape in a direction orthogonal to the predator's heading. By sensing only the predator's heading, this orthogonal strategy maximizes the distance from fast-moving predators, and, when operating within the biomechanical constraints of the escape response, it provides the best predictions of prey behavior among all alternatives. This work demonstrates a framework for resolving the strategic basis of evastion in predator-prey interactions, which could be applied to a broad diversity of animals.

The science and technology of kinematic measurements in a century of Journal of Experimental Biology.

Kinematic measurements have been essential to the study of comparative biomechanics and offer insight into relationships between technological development and scientific progress. Here, we review the 100 year history of kinematic measurements in Journal of Experimental Biology (JEB) through eras that used film, analog video and digital video, and approaches that have circumvented the use of image capture. This history originated with the career of Sir James Gray and has since evolved over the generations of investigators that have followed. Although some JEB studies have featured technological developments that were ahead of their time, the vast majority of research adopted equipment that was broadly available through the consumer or industrial markets. We found that across eras, an emphasis on high-speed phenomena outpaced the growth of the number of articles published by JEB and the size of datasets increased significantly. Despite these advances, the number of species studied within individual reports has not differed significantly over time. Therefore, we find that advances in technology have helped to enable a growth in the number of JEB studies that have included kinematic measurements, contributed to an emphasis on high-speed phenomena, and yielded biomechanical studies that are more data rich, but are no more comparative now than in previous decades.

The persistent-predation strategy of the red lionfish (Pterois volitans).

The pursuit of prey is vital to the biology of a predator and many aspects of predatory behaviour are well-studied. However, it is unclear how a pursuit can be effective when the prey is faster than a non-cryptic predator. Using kinematic measurements, we considered the strategy of red lionfish (Pterois volitans) as they pursued a faster prey fish (Chromis viridis) under laboratory conditions. Despite swimming about half as fast as C. viridis, lionfish succeeded in capturing prey in 61% of our experiments. This successful pursuit behaviour was defined by three critical characteristics. First, lionfish targeted C. viridis with pure pursuit by adjusting their heading towards the prey's position and not the anticipated point of interception. Second, lionfish pursued prey with uninterrupted motion. By contrast, C. viridis moved intermittently with variation in speed that included slow swimming. Such periods allowed lionfish to close the distance to a prey and initiate a suction-feeding strike at a relatively close distance (less than 9 cm). Finally, lionfish exhibited a high rate of strike success, capturing prey in 74% of all strikes. These characteristics comprise a behaviour that we call the 'persistent-predation strategy', which may be exhibited by a diversity of predators with relatively slow locomotion.

Pursuit and Evasion Strategies in the Predator-Prey Interactions of Fishes.

Predator-prey interactions are critical to the biology of a diversity of animals. Although prey capture is determined by the direction, velocity, and timing of motion by both animals, it is generally unclear what strategies are employed by predators and prey to guide locomotion. Here we review our research on fishes that tests the pursuit strategy of predators and the evasion strategy of prey through kinematic measurements and agent-based models. This work demonstrates that fish predators track prey with variations on a deviated-pursuit strategy that is guided by visual cues. Fish prey employ a mixed strategy that varies with factors such as the direction of a predator's approach. Our models consider the stochastic nature of interactions by incorporating measured probability distributions to accurately predict measurements of survivorship. A sensitivity analysis of these models shows the importance of the response distance of prey to their survival. Collectively, this work demonstrates how strategy affects the outcome of predator-prey interactions and articulates the roles of sensing, control, and propulsion. The research program that we have developed has the potential to offer a framework for the study of strategy in the predator-prey interactions of a variety of animals.

Scaling and development of elastic mechanisms: the tiny strikes of larval mantis shrimp.

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.

Pursuit predation with intermittent locomotion in zebrafish.

The control of a predator's locomotion is critical to its ability to capture prey. Flying animals adjust their heading continuously with control similar to guided missiles. However, many animals do not move with rapid continuous motion, but rather interrupt their progress with frequent pauses. To understand how such intermittent locomotion may be controlled during predation, we examined the kinematics of zebrafish (Danio rerio) as they pursued larval prey of the same species. Like many fishes, zebrafish move with discrete burst-and-coast swimming. We found that the change in heading and tail excursion during the burst phase was linearly related to the prey's bearing. These results suggest a strategy, which we call intermittent pure pursuit, that offers advantages in sensing and control. This control strategy is similar to perception and path-planning algorithms required in the design of some autonomous robots and may be common to a diversity of animals.

The sensory basis of schooling by intermittent swimming in the rummy-nose tetra (Hemigrammus rhodostomus).

Schooling is a collective behaviour that enhances the ability of a fish to sense and respond to its environment. Although schooling is essential to the biology of a diversity of fishes, it is generally unclear how this behaviour is coordinated by different sensory modalities. We used experimental manipulation and kinematic measurements to test the role of vision and flow sensing in the rummy-nose tetra (Hemigrammus rhodostomus), which swims with intermittent phases of bursts and coasts. Groups of five fish required a minimum level of illuminance (greater than 1.5 lx) to achieve the necessary close nearest-neighbour distance and high polarization for schooling. Compromising the lateral line system with an antibiotic treatment caused tetras to swim with greater nearest-neighbour distance and lower polarization. Therefore, vision is both necessary and sufficient for schooling in H. rhodostomus, and both sensory modalities aid in attraction. These results can serve as a basis for understanding the individual roles of sensory modalities in schooling for some fish species.

Sea star inspired crawling and bouncing.

The oral surface of sea stars is lined with arrays of tube feet that enable them to achieve highly controlled locomotion on various terrains. The activity of the tube feet is orchestrated by a nervous system that is distributed throughout the body without a central brain. How such a distributed nervous system produces a coordinated locomotion is yet to be understood. We develop mathematical models of the biomechanics of the tube feet and the sea star body. In the model, the feet are coupled mechanically through their structural connection to a rigid body. We formulate hierarchical control laws that capture salient features of the sea star nervous system. Namely, at the tube foot level, the power and recovery strokes follow a state-dependent feedback controller. At the system level, a directionality command is communicated through the nervous system to all tube feet. We study the locomotion gaits afforded by this hierarchical control model. We find that these minimally coupled tube feet coordinate to generate robust forward locomotion, reminiscent of the crawling motion of sea stars, on various terrains and for heterogeneous tube feet parameters and initial conditions. Our model also predicts a transition from crawling to bouncing consistently with recent experiments. We conclude by commenting on the implications of these findings for understanding the neuromechanics of sea stars and their potential application to autonomous robotic systems.

Multichannel stroboscopic videography (MSV): a technique for visualizing multiple channels for behavioral measurements.

Biologists commonly visualize different features of an organism using distinct sources of illumination. Such multichannel imaging has largely not been applied to behavioral studies because of the challenges posed by a moving subject. We address this challenge with the technique of multichannel stroboscopic videography (MSV), which synchronizes multiple strobe lights with video exposures of a single camera. We illustrate the utility of this approach with kinematic measurements of a walking cockroach (Gromphadorhina portentosa) and calculations of the pressure field around a swimming fish (Danio rerio). In both, transmitted illumination generated high-contrast images of the animal's body in one channel. Other sources of illumination were used to visualize the points of contact for the feet of the cockroach and the water flow around the fish in separate channels. MSV provides an enhanced potential for high-throughput experimentation and the capacity to integrate changes in physiological or environmental conditions in freely-behaving animals.

Probabilistic analytical modelling of predator-prey interactions in fishes.

Predation is a fundamental interaction between species, yet it is largely unclear what tactics are successful for the survival or capture of prey. One challenge in this area comes with how to test theoretical ideas about strategy with experimental measurements of features such as speed, flush distance and escape angles. Tactics may be articulated with an analytical model that predicts the motion of predator or prey as they interact. However, it may be difficult to recognize how the predictions of such models relate to behavioural measurements that are inherently variable. Here, we present an alternative approach for modelling predator-prey interactions that uses deterministic dynamics, yet incorporates experimental kinematic measurements of natural variation to predict the outcome of biological events. This technique, called probabilistic analytical modelling (PAM), is illustrated by the interactions between predator and prey fish in two case studies that draw on recent experiments. In the first case, we use PAM to model the tactics of predatory bluefish ( Pomatomus saltatrix) as they prey upon smaller fish ( Fundulus heteroclitus). We find that bluefish perform deviated pure pursuit with a variable pursuit angle that is suboptimal for the time to capture. In the second case, we model the escape tactics of zebrafish larvae ( Danio rerio) when approached by adult predators of the same species. Our model successfully predicts the measured patterns of survivorship using measured probability density functions as parameters. As these results demonstrate, PAM is a data-driven modelling approach that can be predictive, offers analytical transparency, and does not require numerical simulations of system dynamics. Though predator-prey interactions demonstrate the use of this technique, PAM is not limited to studying biological systems and has broad utility that may be applied towards understanding a wide variety of natural and engineered dynamical systems where data-driven modelling is beneficial.

The pursuit strategy of predatory bluefish ( Pomatomus saltatrix).

A predator's ability to capture prey depends critically on how it coordinates its approach in response to a prey's motion. Flying insects, bats and raptors are capable of capturing prey with a strategy known as parallel navigation, which allows a predator to move directly towards the anticipated point of interception. It is unclear if predators using other modes of locomotion are employing this strategy when pursuing evasive prey. Using kinematic measurements and mathematical modelling, we tested whether bluefish ( Pomatomus saltatrix) pursue prey fish ( Fundulus heteroclitus) with parallel navigation. We found that the directional changes of bluefish were not consistent with this strategy, but rather were predicted by a strategy known as deviated pursuit. Although deviated pursuit requires few sensory cues and relatively modest motor coordination, a comparison of mathematical models suggested negligible differences in path length from parallel navigation, largely owing to the acceleration exhibited by bluefish near the end of a pursuit. Therefore, the strategy of bluefish is unlike flying predators, but offers comparable performance with potentially more robust control that may be well suited to the visual system and habitat of fishes. These findings offer a foundation for understanding the sensing and locomotor control of predatory fishes.

Canal neuromasts enhance foraging in zebrafish (Danio rerio).

Aquatic animals commonly sense flow using superficial neuromasts (SNs), which are receptors that extend from the body's surface. The lateral line of fishes is unique among these systems because it additionally possesses receptors, the canal neuromasts (CNs), that are recessed within a channel. The lateral line has inspired the development of engineered sensors and concepts in the analysis of flow fields for submersible navigation. The biophysics of CNs are known to be different from the SNs and thereby offer a distinct submodality. However, it is generally unclear whether CNs play a distinct role in behavior. We therefore tested whether CNs enhance foraging in the dark by zebrafish (Danio rerio), a behavior that we elicited with a vibrating rod. We found that juvenile fish, which have only SNs, bite at this rod at about one-third the rate and from as little as one-third the distance of adults for a high-frequency stimulus (50 < f  < 100 Hz). We used novel techniques for manipulating the lateral line in adults to find that CNs offered only a modest benefit at a lower frequency (20 Hz) and that foraging was mediated entirely by cranial neuromasts. Consistent with our behavioral results, biophysical models predicted CNs to be more than an order of magnitude more sensitive than SNs at high frequencies. This enhancement helps to overcome the rapid spatial decay in high-frequency components in the flow around the stimulus. These findings contrast what has been previously established for fishes that are at least ten-times the length of zebrafish, which use trunk CNs to localize prey. Therefore, CNs generally enhance foraging, but in a manner that varies with the size of the fish and its prey. These results have the potential to improve our understanding of flow sensing in aquatic animals and engineered systems.

Fish prey change strategy with the direction of a threat.

Predation is a fundamental interaction between species, yet it is unclear what escape strategies are effective for prey survival. Classical theory proposes that prey should either escape in a direction that conforms to a performance optimum or that is random and therefore unpredictable. Here, we show that larval zebrafish (Danio rerio) instead use a mixed strategy that may be either random or directed. This was determined by testing classic theory with measurements of the escape direction in response to a predator robot. We found that prey consistently escaped in a direction contralateral to the robot when approached from the side of the prey's body. At such an orientation, the predator appeared in the prey's central visual field and the contralateral response was consistent with a model of strategy that maximizes the distance from the predator. By contrast, when the robot approached the rostral or caudal ends of the body, and appeared in the prey's peripheral vision, the escape showed an equal probability of a contralateral or ipsilateral direction. At this orientation, a contralateral response offered little strategic advantage. Therefore, zebrafish larvae adopt an escape strategy that maximizes distance from the threat when strategically beneficial and that is otherwise random. This sensory-mediated mixed strategy may be employed by a diversity of animals and offers a new paradigm for understanding the factors that govern prey survival.

A faster escape does not enhance survival in zebrafish larvae.

An escape response is a rapid manoeuvre used by prey to evade predators. Performing this manoeuvre at greater speed, in a favourable direction, or from a longer distance have been hypothesized to enhance the survival of prey, but these ideas are difficult to test experimentally. We examined how prey survival depends on escape kinematics through a novel combination of experimentation and mathematical modelling. This approach focused on zebrafish (Danio rerio) larvae under predation by adults and juveniles of the same species. High-speed three-dimensional kinematics were used to track the body position of prey and predator and to determine the probability of behavioural actions by both fish. These measurements provided the basis for an agent-based probabilistic model that simulated the trajectories of the animals. Predictions of survivorship by this model were found by Monte Carlo simulations to agree with our observations and we examined how these predictions varied by changing individual model parameters. Contrary to expectation, we found that survival may not be improved by increasing the speed or altering the direction of the escape. Rather, zebrafish larvae operate with sufficiently high locomotor performance due to the relatively slow approach and limited range of suction feeding by fish predators. We did find that survival was enhanced when prey responded from a greater distance. This is an ability that depends on the capacity of the visual and lateral line systems to detect a looming threat. Therefore, performance in sensing, and not locomotion, is decisive for improving the survival of larval fish prey. These results offer a framework for understanding the evolution of predator-prey strategy that may inform prey survival in a broad diversity of animals.