Henry C. Astley

Evidence for a vertebrate catapult: elastic energy storage in the plantaris tendon during frog jumping

Anuran jumping is one of the most powerful accelerations in vertebrate locomotion. Several species are hypothesized to use a catapult-like mechanism to store and rapidly release elastic energy, producing power outputs far beyond the capability of muscle. Most evidence for this mechanism comes from measurements of whole-body power output; the decoupling of joint motion and muscle shortening expected in a catapult-like mechanism has not been demonstrated. We used high-speed marker-based biplanar X-ray cinefluoroscopy to quantify plantaris muscle fascicle strain and ankle joint motion in frogs in order to test for two hallmarks of a catapult mechanism: (i) shortening of fascicles prior to joint movement (during tendon stretch), and (ii) rapid joint movement during the jump without rapid muscle-shortening (during tendon recoil). During all jumps, muscle fascicles shortened by an average of 7.8 per cent (54% of total strain) prior to joint movement, stretching the tendon. The subsequent period of initial joint movement and high joint angular acceleration occurred with minimal muscle fascicle length change, consistent with the recoil of the elastic tendon. These data support the plantaris longus tendon as a site of elastic energy storage during frog jumping, and demonstrate that catapult mechanisms may be employed even in sub-maximal jumps.

Effects of perch diameter and incline on the kinematics, performance and modes of arboreal locomotion of corn snakes (Elaphe guttata).

SUMMARY Animals moving through arboreal habitats face several functional challenges, including fitting onto and moving on cylindrical branches with variable diameters and inclines. In contrast to lizards and primates, the arboreal locomotion of snakes is poorly understood, despite numerous snake species being arboreal. We quantified the kinematics and performance of corn snakes (Elaphe guttata) moving on seven cylinders (diameters 1.6–21 cm) with five inclines (horizontal, ±45° and± 90°) and through horizontal tunnels of corresponding widths. When perches were inclined at either 45° or 90°, snakes were unable to move uphill or downhill on the larger diameters. None of the locomotion on perches conformed to any previously described mode of limbless locomotion. On horizontal and uphill perches snakes performed a variant of concertina locomotion with periodic stopping and gripping. When moving downhill, snakes often slid continuously while grasping the perch to reduce their speed. Mean forward velocity decreased both with increased incline and with increased perch diameter, contrary to the beneficial effect of increased diameter on the speeds of lizards. Both tunnel width and perch diameter had widespread and similar effects on kinematics. When perches and tunnels were narrower, the snakes had more lateral bends at shallower angles. The numerous effects of perch diameter on kinematics and the similarity to tunnel concertina locomotion emphasize the importance of fit as a limitation in arboreal locomotion of snakes. However, the slower speeds on horizontal perches compared to tunnels also suggest that balance and grip may further limit locomotor performance.

The mechanics of elastic loading and recoil in anuran jumping

Many animals use catapult mechanisms to produce extremely rapid movements for escape or prey capture, resulting in power outputs far beyond the limits of muscle. In these catapults, muscle contraction loads elastic structures, which then recoil to release the stored energy extremely rapidly. Many arthropods employ anatomical ‘catch mechanisms’ to lock the joint in place during the loading period, which can then be released to allow joint motion via elastic recoil. Jumping vertebrates lack a clear anatomical catch, yet face the same requirement to load the elastic structure prior to movement. There are several potential mechanisms to allow loading of vertebrate elastic structures, including the gravitational load of the body, a variable mechanical advantage, and moments generated by the musculature of proximal joints. To test these hypothesized mechanisms, we collected simultaneous 3D kinematics via X-ray Reconstruction of Moving Morphology (XROMM) and single-foot forces during the jumps of three Rana pipiens. We calculated joint mechanical advantage, moment and power using inverse dynamics at the ankle, knee, hip and ilio-sacral joints. We found that the increasing proximal joint moments early in the jump allowed for high ankle muscle forces and elastic pre-loading, and the subsequent reduction in these moments allowed the ankle to extend using elastic recoil. Mechanical advantage also changed throughout the jump, with the muscle contracting against a poor mechanical advantage early in the jump during loading and a higher mechanical advantage late in the jump during recoil. These ‘dynamic catch mechanisms’ serve to resist joint motion during elastic loading, then allow it during elastic recoil, functioning as a catch mechanism based on the balance and orientation of forces throughout the limb rather than an anatomical catch.

Chasing maximal performance: a cautionary tale from the celebrated jumping frogs of Calaveras County

SUMMARY Maximal performance is an essential metric for understanding many aspects of an organisms biology, but it can be difficult to determine because a measured maximum may reflect only a peak level of effort, not a physiological limit. We used a unique opportunity provided by a frog jumping contest to evaluate the validity of existing laboratory estimates of maximum jumping performance in bullfrogs (Rana catesbeiana). We recorded video of 3124 bullfrog jumps over the course of the 4-day contest at the Calaveras County Jumping Frog Jubilee, and determined jump distance from these images and a calibration of the jump arena. Frogs were divided into two groups: ‘rental’ frogs collected by fair organizers and jumped by the general public, and frogs collected and jumped by experienced, ‘professional’ teams. A total of 58% of recorded jumps surpassed the maximum jump distance in the literature (1.295 m), and the longest jump was 2.2 m. Compared with rental frogs, professionally jumped frogs jumped farther, and the distribution of jump distances for this group was skewed towards long jumps. Calculated muscular work, historical records and the skewed distribution of jump distances all suggest that the longest jumps represent the true performance limit for this species. Using resampling, we estimated the probability of observing a given jump distance for various sample sizes, showing that large sample sizes are required to detect rare maximal jumps. These results show the importance of sample size, animal motivation and physiological conditions for accurate maximal performance estimates.

Getting around when you’re round: quantitative analysis of the locomotion of the blunt-spined brittle star, Ophiocoma echinata

SUMMARY Brittle stars (Ophiuroidea, Echinodermata) are pentaradially symmetrical echinoderms that use five multi-jointed limbs to locomote along the seafloor. Prior qualitative descriptions have claimed coordinated movements of the limbs in a manner similar to tetrapod vertebrates, but this has not been evaluated quantitatively. It is uncertain whether the ring-shaped nervous system, which lacks an anatomically defined anterior, is capable of generating rhythmic coordinated movements of multiple limbs. This study tested whether brittle stars possess distinct locomotor modes with strong inter-limb coordination as seen in limbed animals in other phyla (e.g. tetrapods and arthropods), or instead move each limb independently according to local sensory feedback. Limb tips and the body disk were digitized for 56 cycles from 13 individuals moving across sand. Despite their pentaradial anatomy, all individuals were functionally bilateral, moving along the axis of a central limb via synchronous motions of contralateral limbs (±∼13% phase lag). Two locomotor modes were observed, distinguishable mainly by whether the central limb was directed forwards or backwards. Turning was accomplished without rotation of the body disk by defining a different limb as the center limb and shifting other limb identities correspondingly, and then continuing locomotion in the direction of the newly defined anterior. These observations support the hypothesis that, in spite of their radial body plan, brittle stars employ coordinated, bilaterally symmetrical locomotion.

Arboreal habitat structure affects the performance and modes of locomotion of corn snakes (Elaphe guttata)

Arboreal environments pose many functional challenges for animal locomotion including fitting within narrow spaces, balancing on cylindrical surfaces, moving on inclines, and moving around branches that obstruct a straight path. Many species of snakes are arboreal and their elongate, flexible bodies appear well-suited to meet many of these demands, but the effects of arboreal habitat structure on the locomotion of snakes are not well understood. We examined the effects of 108 combinations of surface shape (cylinder vs. rectangular tunnel), surface width, incline, and a row of pegs on the locomotion of corn snakes (Elaphe guttata). Pegs allowed the snakes to move on the widest and steepest surfaces that were impassable without pegs. Tunnels allowed the snakes to move on steeper inclines than cylinders with similar widths. The mode of locomotion changed with habitat structure. On surfaces without pegs, most snakes used two variants of concertina locomotion but always moved downhill using a controlled slide. Snakes used lateral undulation on most surfaces with pegs. The detrimental effects of increased uphill incline were greater than those of increased surface width on maximal velocity. Snakes moved faster in tunnels than on cylinders regardless of whether pegs were present. Depending on the surface width, the addition of pegs to horizontal cylinders and tunnels resulted in 8-24-fold and 1.3-3.1-fold increases in speed, respectively. Thus, pegs considerably enhanced the locomotor performance of snakes, although similar structures such as secondary branches seem likely to impede the locomotion of limbed arboreal animals.

Tail use improves performance on soft substrates in models of early vertebrate land locomotors

Animal and robot experiments explore the use of a tail in aiding terrestrial locomotion. In the evolutionary transition from an aquatic to a terrestrial environment, early tetrapods faced the challenges of terrestrial locomotion on flowable substrates, such as sand and mud of variable stiffness and incline. The morphology and range of motion of appendages can be revealed in fossils; however, biological and robophysical studies of modern taxa have shown that movement on such substrates can be sensitive to small changes in appendage use. Using a biological model (the mudskipper), a physical robot model, granular drag measurements, and theoretical tools from geometric mechanics, we demonstrate how tail use can improve robustness to variable limb use and substrate conditions. We hypothesize that properly coordinated tail movements could have provided a substantial benefit for the earliest vertebrates to move on land.

Kinematic gait synthesis for snake robots

Snake robots are highly articulated mechanisms that can perform a variety of motions that conventional robots cannot. Despite many demonstrated successes of snake robots, these mechanisms have not been able to achieve the agility displayed by their biological counterparts. We suggest that studying how biological snakes coordinate whole-body motion to achieve agile behaviors can help improve the performance of snake robots. The foundation of this work is based on the hypothesis that, for snake locomotion that is approximately kinematic, replaying parameterized shape trajectory data collected from biological snakes can generate equivalent motions in snake robots. To test this hypothesis, we collected shape trajectory data from sidewinder rattlesnakes executing a variety of different behaviors. We then analyze the shape trajectory data in a concise and meaningful way by using a new algorithm, called conditioned basis array factorization, which projects high-dimensional data arrays onto a low-dimensional representation. The low-dimensional representation of the recorded snake motion is able to reproduce the essential features of the recorded biological snake motion on a snake robot, leading to improved agility and maneuverability, confirming our hypothesis. This parameterized representation allows us to search the low-dimensional parameter space to generate behaviors that further improve the performance of snake robots.

The diversity and evolution of locomotor muscle properties in anurans.

ABSTRACT Anuran jumping is a model system for linking muscle physiology to organismal performance. However, anuran species display substantial diversity in their locomotion, with some species performing powerful leaps from riverbanks or tree branches, while other species move predominantly via swimming, short hops or even diagonal-sequence gaits. Furthermore, many anurans with similar locomotion and morphology are actually convergent (e.g. multiple independent evolutions of ‘tree frogs’), while closely related species may differ drastically, as with the walking toad (Melanophryniscus stelzneri) and bullfrog-like river toad (Phrynoides aspera) compared with other Bufonid toads. These multiple independent evolutionary changes in locomotion allow us to test the hypothesis that evolutionary increases in locomotor performance will be linked to the evolution of faster, high-power muscles. I tested the jumping, swimming and walking (when applicable) performance of 14 species of anurans and one salamander, followed by measurement of the contractile properties of the semimembranosus and plantaris longus muscles and anatomical measurements, using phylogenetic comparative methods. I found that increased jumping performance correlated to muscle contractile properties associated with muscle speed (e.g. time to peak tetanus, maximum shortening speed, peak isotonic power), and was tightly linked to relevant anatomical traits (e.g. leg length, muscle mass). Swimming performance was not correlated to jumping, and was correlated with fewer anatomical and muscular variables. Thus, muscle properties evolve along with changes in anatomy to produce differences in overall locomotor performance. Summary: Frog muscle contractile properties (semimembranosus and plantaris) vary widely across taxa and show correlations to locomotor performance, particularly jumping performance.

Robust jumping performance and elastic energy recovery from compliant perches in tree frogs.

ABSTRACT Arboreal animals often move on compliant branches, which may deform substantially under loads, absorbing energy. Energy stored in a compliant substrate may be returned to the animal or it may be lost. In all cases studied so far, animals jumping from a static start lose all of the energy imparted to compliant substrates and performance is reduced. Cuban tree frogs (Osteopilus septentrionalis) are particularly capable arboreal jumpers, and we hypothesized that these animals would be able to recover energy from perches of varying compliance. In spite of large deflections of the perches and consequent substantial energy absorption, frogs were able to regain some of the energy lost to the perch during the recoil. Takeoff velocity was robust to changes in compliance, but was lower than when jumping from flat surfaces. This highlights the ability of animals to minimize energy loss and maintain dependable performance on challenging substrates via behavioral changes. Highlighted Article: Tree frogs can recover elastic energy lost to springy perches when jumping, allowing robust jumping performance across highly variable perch compliances.