Mechanoethology: The Physical Mechanisms of Behavior.

Research that integrates animal behavior theory with mechanics-including biomechanics, physiology, and functional morphology-can reveal how organisms accomplish tasks crucial to their fitness. Despite the insights that can be gained from this interdisciplinary approach, biomechanics commonly neglects a behavioral context and behavioral research generally does not consider mechanics. Here, we aim to encourage the study of "mechanoethology," an area of investigation intended to encompass integrative studies of mechanics and behavior. Using examples from the literature, including papers in this issue, we show how these fields can influence each other in three ways: (1) the energy required to execute behaviors is driven by the kinematics of movement, and mechanistic studies of movement can benefit from consideration of its behavioral context; (2) mechanics sets physical limits on what behaviors organisms execute, while behavior influences ecological and evolutionary limits on mechanical systems; and (3) sensory behavior is underlain by the mechanics of sensory structures, and sensory systems guide whole-organism movement. These core concepts offer a foundation for mechanoethology research. However, future studies focused on merging behavior and mechanics may reveal other ways by which these fields are linked, leading to further insights in integrative organismal biology.

The Strategy of Predator Evasion in Response to a Visual Looming Stimulus in Zebrafish (Danio rerio).

A diversity of animals survive encounters with predators by escaping from a looming visual stimulus. Despite the importance of this behavior, it is generally unclear how visual cues facilitate a prey's survival from predation. Therefore, the aim of this study was to understand how the visual angle subtended on the eye of the prey by the predator affects the distance of adult zebrafish (Danio rerio) from predators. We performed experiments to measure the threshold visual angle and mathematically modeled the kinematics of predator and prey. We analyzed the responses to the artificial stimulus with a novel approach that calculated relationships between hypothetical values for a threshold-stimulus angle and the latency between stimulus and response. These relationships were verified against the kinematic responses of zebrafish to a live fish predator (Herichthys cyanoguttatus). The predictions of our model suggest that the measured threshold visual angle facilitates escape when the predator's approach is slower than approximately twice the prey's escape speed. These results demonstrate the capacity and limits to how the visual angle provides a prey with the means to escape a predator.

Una diversidad de animales sobrevive a los encuentros con los depredadores al escapar de un inminente estímulo visual. A pesar de la importancia de este comportamiento, generalmente no está claro cómo las señales visuales facilitan la supervivencia de una presa de la depredación. Por lo tanto, el objetivo del presente estudio fue comprender cómo el ángulo visual que el depredador subtiende en el ojo de la presa afecta la distancia del pez cebra adulto (Danio rerio) de los depredadores. Realizamos experimentos para medir el ángulo visual del umbral y modelamos matemáticamente la cinemática del depredador y la presa. Analizamos las respuestas al estímulo artificial con un enfoque novedoso que calculaba las relaciones entre los valores hipotéticos para un ángulo umbral-estímulo y la latencia entre el estímulo y la respuesta. Estas relaciones se verificaron contra las respuestas cinemáticas del pez cebra a un depredador de peces vivos (Herichthys cyanoguttatus). Las predicciones de nuestro modelo sugieren que el ángulo visual del umbral medido facilita el escape cuando el enfoque del depredador es más lento que aproximadamente el doble de la velocidad de escape de la presa. Estos resultados demuestran la capacidad y los límites de cómo el ángulo visual proporciona a una presa los medios para escapar de un depredador.

Context-dependent scaling of kinematics and energetics during contests and feeding in mantis shrimp.

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.

The comparative hydrodynamics of rapid rotation by predatory appendages.

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.

Hydrodynamic sensing does not facilitate active drag reduction in the golden shiner (Notemigonus crysoleucas).

The lateral line system detects water flow, which allows fish to orient their swimming with respect to hydrodynamic cues. However, it is unclear whether this sense plays a role in the control of propulsion. Hydrodynamic theory suggests that fish could reduce drag by coordinating the motion of the head relative to detected flow signals. To test this hypothesis, we performed measurements of undulatory kinematics during steady swimming in the golden shiner (Notemigonus crysoleucas) at three speeds (4.5, 11.0 and 22.0 cm s(-1)). We found that the phase shift between yaw angle and lateral velocity (20.5+/-13.1 deg., N=5) was significantly greater than the theoretical optimum (0 deg.) and the amplitude of these variables created a hydrodynamic index (H=0.05+/-0.03, N=6) that was less than an order of magnitude below the theoretical prediction. Furthermore, we repeated these measurements after pharmacologically ablating the lateral line hair cells and found that drag reduction was not adversely influenced by disabling the lateral line system. Therefore, flow sensing does not facilitate active drag reduction. However, we discovered that ablating the lateral line causes the envelope of lateral displacement to nearly double at the envelope's most narrow point for swimming at 4.5 cm s(-1). Therefore, fish may use hydrodynamic sensing to modulate the lateral amplitude of slow undulatory swimming, which could allow rapid responses to changes in environmental flow.

Larval zebrafish rapidly sense the water flow of a predator's strike.

Larval fishes have a remarkable ability to sense and evade the feeding strike of a predator fish with a rapid escape manoeuvre. Although the neuromuscular control of this behaviour is well studied, it is not clear what stimulus allows a larva to sense a predator. Here we show that this escape response is triggered by the water flow created during a predator's strike. Using a novel device, the impulse chamber, zebrafish (Danio rerio) larvae were exposed to this accelerating flow with high repeatability. Larvae responded to this stimulus with an escape response having a latency (mode=13-15 ms) that was fast enough to respond to predators. This flow was detected by the lateral line system, which includes mechanosensory hair cells within the skin. Pharmacologically ablating these cells caused the escape response to diminish, but then recover as the hair cells regenerated. These findings demonstrate that the lateral line system plays a role in predator evasion at this vulnerable stage of growth in fishes.

Mechanisms of helical swimming: asymmetries in the morphology, movement and mechanics of larvae of the ascidian Distaplia occidentalis.

A great diversity of unicellular and invertebrate organisms swim along a helical path, but it is not well understood how asymmetries in the body shape or the movement of propulsive structures affect a swimmer's ability to perform the body rotation necessary to move helically. The present study found no significant asymmetries in the body shape of ascidian larvae (Distaplia occidentalis) that could operate to rotate the body during swimming. By recording the three-dimensional movement of free-swimming larvae, it was found that the tail possessed two bends, each with constant curvature along their length. As these bends traveled posteriorly, the amplitude of curvature changes was significantly greater in the concave-left direction than in the concave-right direction. In addition to this asymmetry, the tail oscillated at an oblique angle to the midline of the trunk. These asymmetries generated a yawing moment that rotated the body in the counterclockwise direction from a dorsal view, according to calculations from hydrodynamic theory. The tails of resting larvae were bent in the concave-left direction with a curvature statistically indistinguishable from the median value for tail curvature during swimming. The flexural stiffness of the tails of larvae, measured in three-point bending, may be great enough to allow the resting curvature of the tail to have an effect on the symmetry of kinematics. This work suggests that asymmetrical tail motion is an important mechanism for generating a yawing moment during swimming in ascidian larvae and that these asymmetries may be caused by the tail's bent shape. Since helical motion requires that moments also be generated in the pitching or rolling directions, other mechanisms are required to explain fully how ascidian larvae generate and control helical swimming.

Mechanical control of swimming speed: stiffness and axial wave form in undulating fish models

The purpose of this study was to investigate the mechanical control of speed in steady undulatory swimming. The roles of body flexural stiffness, driving frequency and driving amplitude were examined; these variables were chosen because of their importance in vibration theory and their hypothesized functions in undulatory swimming. Using a mold of a pumpkinseed sunfish Lepomis gibbosus, we cast three-dimensional vinyl models of four different flexural stiffnesses. We swam the models in a flow tank and powered them via the input of an oscillating sinusoidal bending couple in the horizontal plane at the posterior margin of the neurocranium. To simulate the hydrodynamic conditions of steady swimming, drag and thrust acting on the model were balanced by adjusting flow speed. Under these conditions, the actuated models generated traveling waves of bending. At steady speeds, the motions of the ventral and lateral surfaces of the model were video-taped and analyzed to yield the following response variables: tail-beat amplitude, propulsive wavelength, wave speed and depth of the trailing edge of the caudal fin. Experimental results showed that changes in body flexural stiffness can control propulsive wavelength, wave speed, Froude efficiency and, in consequence, swimming speed. Driving frequency can control tail-beat amplitude, propulsive wavelength, Froude efficiency, relative rate of working and, in consequence, swimming speed. Although there is no significant correlation between rostral amplitude and swimming speed, rostral amplitude can control swimming speed indirectly by controlling tail-beat amplitude and relative power. Compared with live sunfish using undulatory waves at the same speed, models have a lower Froude efficiency. On the basis of the mechanical control of swimming speed in model sunfish, we predict that, in order to swim at fast speeds, live sunfish increase the flexural stiffness of their bodies by a factor of two relative to their passive body stiffness.