Person:

Ros, Ivo

The analysis of terrestrial locomotion over the past half century has focused largely on strategies of mechanical energy recovery used during walking and running. In contrast, we describe the underlying mechanics of legged locomotion as a collision-like interaction that redirects the centre of mass (CoM). We introduce the collision angle, determined by the angle between the CoM force and velocity vectors, and show by computing the collision fraction, a ratio of actual to potential collision, that the quadrupedal walk and gallop employ collision-reduction strategies while the trot permits greater collisions. We provide the first experimental evidence that a collision-based approach can differentiate quadrupedal gaits and quantify interspecific differences. Furthermore, we show that this approach explains the physical basis of a commonly used locomotion metric, the mechanical cost of transport. Collision angle and collision fraction provide a unifying analysis of legged locomotion which can be applied broadly across animal size, leg number and gait.

Hummingbirds (Trochilidae) are widely known for their insect-like flight strokes characterized by high wing beat frequency, small muscle strains and a highly supinated wing orientation during upstroke that allows for lift production in both halves of the stroke cycle. Here, we show that hummingbirds achieve these functional traits within the limits imposed by a vertebrate endoskeleton and muscle physiology by accentuating a wing inversion mechanism found in other birds and using long-axis rotational movement of the humerus. In hummingbirds, long-axis rotation of the humerus creates additional wing translational movement, supplementing that produced by the humeral elevation and depression movements of a typical avian flight stroke. This adaptation increases the wing-to-muscle-transmission ratio, and is emblematic of a widespread scaling trend among flying animals whereby wing-to-muscle-transmission ratio varies inversely with mass, allowing animals of vastly different sizes to accommodate aerodynamic, biomechanical and physiological constraints on muscle-powered flapping flight.

Low speed avian maneuvering flight is an ecologically crucial behavior that has contributed to the explosive diversification of several avian taxa by allowing access to complex spatial environments. Negotiating a sharp aerial turn requires finely tuned interactions between an animal's sensory-motor system and its environment. My thesis work focuses on how aerodynamic forces, wing and body dynamics, and sensory feedback interact during aerial turning in the pigeon (Columba livea).

Turning is crucial for animals, particularly during predator–prey interactions and to avoid obstacles. For flying animals, turning consists of changes in (i) flight trajectory, or path of travel, and (ii) body orientation, or 3D angular position. Changes in flight trajectory can only be achieved by modulating aerodynamic forces relative to gravity. How birds coordinate aerodynamic force production relative to changes in body orientation during turns is key to understanding the control strategies used in avian maneuvering flight. We hypothesized that pigeons produce aerodynamic forces in a uniform direction relative to their bodies, requiring changes in body orientation to redirect those forces to turn. Using detailed 3D kinematics and body mass distributions, we examined net aerodynamic forces and body orientations in slowly flying pigeons (Columba livia) executing level 90° turns. The net aerodynamic force averaged over the downstroke was maintained in a fixed direction relative to the body throughout the turn, even though the body orientation of the birds varied substantially. Early in the turn, changes in body orientation primarily redirected the downstroke aerodynamic force, affecting the bird’s flight trajectory. Subsequently, the pigeon mainly reacquired the body orientation used in forward flight without affecting its flight trajectory. Surprisingly, the pigeon’s upstroke generated aerodynamic forces that were approximately 50% of those generated during the downstroke, nearly matching the relative upstroke forces produced by hummingbirds. Thus, pigeons achieve low speed turns much like helicopters, by using whole-body rotations to alter the direction of aerodynamic force production to change their flight trajectory.

The complexity of low speed maneuvering flight is apparent from the combination of two critical aspects of this behavior: high power and precise control. To understand how such control is achieved we examined the underlying kinematics and resulting aerodynamic mechanisms of low speed turning flight in the pigeon (Columba livia). Three birds were trained to perform 90-degree level turns in a stereotypical fashion and detailed three-dimensional (3D) kinematics were recorded at high speeds. Applying the angular momentum principle, we used mechanical modeling based on time-varying 3D inertia properties of individual sections of the pigeon’s body to separate angular accelerations of the torso based on aerodynamics from those based on inertial effects. Directly measured angular accelerations of the torso were predicted by aerodynamic torques, justifying inferences of aerodynamic torque generation based on inside wing versus outside wing kinematics. Surprisingly, contralateral asymmetries in wing speed did not appear to underlie the 90-degree aerial turns, nor did contralateral differences in wing area, angle of attack, wingbeat amplitude, or timing. Instead, torso angular accelerations into the turn were associated with the outside wing sweeping more anteriorly compared to a more laterally directed inside wing. In addition to moving through a relatively more retracted path, the inside wing was also more strongly pronated about its long axis compared with the outside wing, offsetting any difference in aerodynamic angle of attack that might arise from the observed asymmetry in wing trajectories. Therefore, to generate roll and pitch torques into the turn, pigeons simply reorient their wing trajectories toward the desired flight direction. As a result, by acting above the center of mass, the net aerodynamic force produced by the wings is directed inward, generating the necessary torques for turning.

Flying animals must successfully contend with obstacles in their natural environments. Inspired by the robust maneuvering abilities of flying animals, unmanned aerial systems are being developed and tested to improve flight control through cluttered environments. We previously examined steering strategies that pigeons adopt to fly through an array of vertical obstacles. Modeling vertical obstacle flight guidance revealed that pigeons steer toward larger visual gaps when making fast steering decisions. In the present experiments, we recorded 3D flight kinematics of pigeons as they flew through randomized arrays of horizontal obstacles. We found that pigeons still decelerated upon approach but flew faster through a denser array of horizontal obstacles compared with the vertical obstacle array previously tested. Pigeons exhibited limited steering and chose gaps between obstacles most aligned to their immediate flight direction, in contrast to vertical obstacle navigation that favored widest gap steering. In addition, pigeons navigated past the horizontal obstacles with more variable and decreased wing stroke span and adjusted their wing stroke plane to reduce contact with the obstacles. Variability in wing extension, stroke plane and wing stroke path was greater during horizontal obstacle flight. Pigeons also exhibited pronounced head movements when negotiating horizontal obstacles, which potentially serve a visual function. These head-bobbing-like movements were most pronounced in the horizontal (flight direction) and vertical directions, consistent with engaging motion vision mechanisms for obstacle detection. These results show that pigeons exhibit a keen kinesthetic sense of their body and wings in relation to obstacles. Together with aerodynamic flapping flight mechanics that favors vertical maneuvering, pigeons are able to navigate horizontal obstacles using simple rules with remarkable success.

Various flight navigation strategies for birds have been identified 9 at the large spatial scales of migratory and homing behaviors. However, relatively little is known about close range obstacle negotiation through cluttered environments. To examine obstacle flight guidance, we tracked pigeons (C. livea) flying through an artificial forest of vertical poles. Interestingly, pigeons adjusted their flight path only ~1.5m from the forest entry, suggesting a reactive mode of path planning. Combining flight trajectories with obstacle pole positions, we reconstructed the visual experience of the pigeons throughout obstacle flights. Assuming proportional-derivative (PD) control with a constant delay, we searched the relevant parameter space of steering gains and visuomotor delays that best explained the observed steering. We found that a pigeon’s steering resembles proportional control driven by the error angle between the flight direction and the desired opening, or gap, between obstacles. Using this pigeon steering controller, we simulated obstacle flights and showed that pigeons do not simply steer to the nearest opening in the direction of flight or destination. Pigeons bias their flight direction toward larger visual gaps when making fast steering decisions. The proposed behavioral modeling method converts the obstacle avoidance behavior into a (piece-wise) target-aiming behavior, which is better defined and understood. This study demonstrates how such an approach decomposes open-loop free-flight behaviors into components that can be independently evaluated.