Dragondrop: a novel passive mechanism for aerial righting in the dragonfly.

Dragonflies perform dramatic aerial manoeuvres when chasing targets but glide for periods during cruising flights. This makes dragonflies a great system to explore the role of passive stabilizing mechanisms that do not compromise manoeuvrability. We challenged dragonflies by dropping them from selected inverted attitudes and collected 6-degrees-of-freedom aerial recovery kinematics via custom motion capture techniques. From these kinematic data, we performed rigid-body inverse dynamics to reconstruct the forces and torques involved in righting behaviour. We found that inverted dragonflies typically recover themselves with the shortest rotation from the initial body inclination. Additionally, they exhibited a strong tendency to pitch-up with their head leading out of the manoeuvre, despite the lower moment of inertia in the roll axis. Surprisingly, anaesthetized dragonflies could also complete aerial righting reliably. Such passive righting disappeared in recently dead dragonflies but could be partially recovered by waxing their wings to the anaesthetised posture. Our kinematics data, inverse dynamics model and wind-tunnel experiments suggest that the dragonfly's long abdomen and wing posture generate a rotational tendency and passive attitude recovery mechanism during falling. This work demonstrates an aerodynamically stable body configuration in a flying insect and raises new questions in sensorimotor control for small flying systems.

Internal models direct dragonfly interception steering.

Sensorimotor control in vertebrates relies on internal models. When extending an arm to reach for an object, the brain uses predictive models of both limb dynamics and target properties. Whether invertebrates use such models remains unclear. Here we examine to what extent prey interception by dragonflies (Plathemis lydia), a behaviour analogous to targeted reaching, requires internal models. By simultaneously tracking the position and orientation of a dragonfly's head and body during flight, we provide evidence that interception steering is driven by forward and inverse models of dragonfly body dynamics and by models of prey motion. Predictive rotations of the dragonfly's head continuously track the prey's angular position. The head-body angles established by prey tracking appear to guide systematic rotations of the dragonfly's body to align it with the prey's flight path. Model-driven control thus underlies the bulk of interception steering manoeuvres, while vision is used for reactions to unexpected prey movements. These findings illuminate the computational sophistication with which insects construct behaviour.

Caterpillar Climbing: Robust, Tension-Based Omni-Directional Locomotion.

Animals that must transition from horizontal to inclined or vertical surfaces typically change their locomotion strategy to compensate for the relative shift in gravitational forces. The species that have been studied have stiff articulated skeletons that allow them to redistribute ground reaction forces (GRFs) to control traction. Most also change their stepping patterns to maintain stability as they climb. In contrast, caterpillars, most of which are highly scansorial, soft-bodied, and lack rigid support or joints, can move with the same general kinematics in all orientations. In this study, we measure the GRFs exerted by the abdominal prolegs of Manduca sexta (Linnaeus) during locomotion. We show that, despite the orthogonal shift in gravitational forces, caterpillars use the same tension-based environmental skeleton strategy to crawl horizontally and to climb vertically. Furthermore, the transition from horizontal to vertical surfaces does not seem to require a change in gait; instead gravitational loading is used to help maintain a stance-phase body tension against which the muscles can pull the body upwards.

Flow sensing on dragonfly wings.

One feature of animal wings is their embedded mechanosensory system that can support flight control. Insect wings are particularly interesting as they are highly deformable yet the actuation is limited to the wing base. It is established that strain sensors on insect wings can directly mediate reflexive control; however, little is known about airflow sensing by insect wings. What information can flow sensors capture and how can flow sensing benefit flight control? Here, we use the dragonfly (Sympetrum striolatum) as a model to explore the function of wing sensory bristles in the context of flight control. Combining our detailed anatomical reconstructions of both the sensor microstructures and wing architecture, we used computational fluid dynamics simulations to ask the following questions. (1) Are there strategic locations on wings that sample flow for estimating aerodynamically relevant parameters such as the local effective angle of attack? (2) Is the sensory bristle distribution on dragonfly wings optimal for flow sensing? (3) What is the aerodynamic effect of microstructures found near the sensory bristles on dragonfly wings? We discuss the benefits of flow sensing for flexible wings and how the evolved sensor placement affects information encoding.

Why flying insects gather at artificial light.

Explanations of why nocturnal insects fly erratically around fires and lamps have included theories of "lunar navigation" and "escape to the light". However, without three-dimensional flight data to test them rigorously, the cause for this odd behaviour has remained unsolved. We employed high-resolution motion capture in the laboratory and stereo-videography in the field to reconstruct the 3D kinematics of insect flights around artificial lights. Contrary to the expectation of attraction, insects do not steer directly toward the light. Instead, insects turn their dorsum toward the light, generating flight bouts perpendicular to the source. Under natural sky light, tilting the dorsum towards the brightest visual hemisphere helps maintain proper flight attitude and control. Near artificial sources, however, this highly conserved dorsal-light-response can produce continuous steering around the light and trap an insect. Our guidance model demonstrates that this dorsal tilting is sufficient to create the seemingly erratic flight paths of insects near lights and is the most plausible model for why flying insects gather at artificial lights.

Systematic characterization of wing mechanosensors that monitor airflow and wing deformations.

Animal wings deform during flight in ways that can enhance lift, facilitate flight control, and mitigate damage. Monitoring the structural and aerodynamic state of the wing is challenging because deformations are passive, and the flow fields are unsteady; it requires distributed mechanosensors that respond to local airflow and strain on the wing. Without a complete map of the sensor arrays, it is impossible to model control strategies underpinned by them. Here, we present the first systematic characterization of mechanosensors on the dragonfly's wings: morphology, distribution, and wiring. By combining a cross-species survey of sensor distribution with quantitative neuroanatomy and a high-fidelity finite element analysis, we show that the mechanosensors are well placed to perceive features of the wing dynamics relevant to flight. This work describes the wing sensory apparatus in its entirety and advances our understanding of the sensorimotor loop that facilitates exquisite flight control in animals with highly deformable wings.

Scaling of caterpillar body properties and its biomechanical implications for the use of a hydrostatic skeleton.

Caterpillars can increase their body mass 10,000-fold in 2 weeks. It is therefore remarkable that most caterpillars appear to maintain the same locomotion kinematics throughout their entire larval stage. This study examined how the body properties of a caterpillar might change to accommodate such dramatic changes in body load. Using Manduca sexta as a model system, we measured changes in body volume, tissue density and baseline body pressure, and the dimensions of load-bearing tissues (the cuticle and muscles) over a body mass range from milligrams to several grams. All Manduca biometrics relevant to the hydrostatic skeleton scaled allometrically but close to the isometric predictions. Body density and pressure were almost constant. We next investigated the effects of scaling on the bending stiffness of the caterpillar hydrostatic skeleton. The anisotropic non-linear mechanical response of Manduca muscles and soft cuticle has previously been quantified and modeled with constitutive equations. Using biometric data and these material laws, we constructed finite element models to simulate a hydrostatic skeleton under different conditions. The results show that increasing the internal pressure leads to a non-linear increase in bending stiffness. Increasing the body size results in a decrease in the normalized bending stiffness. Muscle activation can double this stiffness in the physiological pressure range, but thickening the cuticle or increasing the muscle area reduces the structural stiffness. These non-linear effects may dictate the effectiveness of a hydrostatic skeleton at different sizes. Given the shared anatomy and size variation in Lepidoptera larvae, these mechanical scaling constraints may implicate the diverse locomotion strategies in different species.

The substrate as a skeleton: ground reaction forces from a soft-bodied legged animal.

The measurement of forces generated during locomotion is essential for the development of accurate mechanical models of animal movements. However, animals that lack a stiff skeleton tend to dissipate locomotor forces in large tissue deformation and most have complex or poorly defined substrate contacts. Under these conditions, measuring propulsive and supportive forces is very difficult. One group that is an exception to this problem is lepidopteran larvae which, despite lacking a rigid skeleton, have well-developed limbs (the prolegs) that can be used for climbing in complex branched structures and on a variety of surfaces. Caterpillars therefore are excellent for examining the relationship between soft body deformation and substrate reaction forces during locomotion. In this study, we devised a method to measure the ground reaction forces (GRFs) at multiple contact points during crawling by the tobacco hornworm (Manduca sexta). Most abdominal prolegs bear similar body weight during their stance phase. Interestingly, forward reaction forces did not come from pushing off the substrate. Instead, most positive reaction forces came from anterior abdominal prolegs loaded in tension while posterior legs produced drag in most instances. The counteracting GRFs effectively stretch the animal axially during the second stage of a crawl cycle. These findings help in understanding how a terrestrial soft-bodied animal can interact with its substrate to control deformation without hydraulic actuation. The results also provide insights into the behavioral and mechanistic constraints leading to the evolution of diverse proleg arrangements in different species of caterpillar.

Soft-cuticle biomechanics: a constitutive model of anisotropy for caterpillar integument.

The mechanical properties of soft tissues are important for the control of motion in many invertebrates. Pressurized cylindrical animals such as worms have circumferential reinforcement of the body wall; however, no experimental characterization of comparable anisotropy has been reported for climbing larvae such as caterpillars. Using uniaxial, real-time fluorescence extensometry on millimeter scale cuticle specimens we have quantified differences in the mechanical properties of cuticle to circumferentially and longitudinally applied forces. Based on these results and the composite matrix-fiber structure of cuticle, a pseudo-elastic transversely isotropic constitutive material model was constructed with circumferential reinforcement realized as a Horgan-Saccomandi strain energy function. This model was then used numerically to describe the anisotropic material properties of Manduca cuticle. The constitutive material model will be used in a detailed finite-element analysis to improve our understanding of the mechanics of caterpillar crawling.

Heuristic Rules Underlying Dragonfly Prey Selection and Interception.

Animals use rules to initiate behaviors. Such rules are often described as triggers that determine when behavior begins. However, although less explored, these selection rules are also an opportunity to establish sensorimotor constraints that influence how the behavior ends. These constraints may be particularly significant in influencing success in prey capture. Here we explore this in dragonfly prey interception. We found that in the moments leading up to takeoff, perched dragonflies employ a series of sensorimotor rules that determine the time of takeoff and increase the probability of successful capture. First, the dragonfly makes a head saccade followed by smooth pursuit movements to orient its direction-of-gaze at potential prey. Second, the dragonfly assesses whether the prey's angular size and speed co-vary within a privileged range. Finally, the dragonfly times the moment of its takeoff to a prediction of when the prey will cross the zenith. Each of these processes serves a purpose. The angular size-speed criteria biases interception flights to catchable prey, while the head movements and the predictive takeoff ensure flights begin with the prey visually fixated and directly overhead-the key parameters that underlie interception steering. Prey that do not elicit takeoff generally fail at least one of the criterion, and the loss of prey fixation or overhead positioning during flight is strongly correlated with terminated flights. Thus from an abundance of potential targets, the dragonfly selects a stereotyped set of takeoff conditions based on the prey and body states most likely to end in successful capture.

Rules to fly by: pigeons navigating horizontal obstacles limit steering by selecting gaps most aligned to their flight direction.

Flying animals must successfully contend with obstacles in their natural environments. Inspired by the robust manoeuvring 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 (VOs). Modelling VO flight guidance revealed that pigeons steer towards larger visual gaps when making fast steering decisions. In the present experiments, we recorded three-dimensional flight kinematics of pigeons as they flew through randomized arrays of horizontal obstacles (HOs). We found that pigeons still decelerated upon approach but flew faster through a denser array of HOs compared with the VO array previously tested. Pigeons exhibited limited steering and chose gaps between obstacles most aligned to their immediate flight direction, in contrast to VO navigation that favoured widest gap steering. In addition, pigeons navigated past the HOs 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 HO flight. Pigeons also exhibited pronounced head movements when negotiating HOs, 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 favours vertical manoeuvring, pigeons are able to navigate HOs using simple rules, with remarkable success.

Flight of the dragonflies and damselflies.

This work is a synthesis of our current understanding of the mechanics, aerodynamics and visually mediated control of dragonfly and damselfly flight, with the addition of new experimental and computational data in several key areas. These are: the diversity of dragonfly wing morphologies, the aerodynamics of gliding flight, force generation in flapping flight, aerodynamic efficiency, comparative flight performance and pursuit strategies during predatory and territorial flights. New data are set in context by brief reviews covering anatomy at several scales, insect aerodynamics, neuromechanics and behaviour. We achieve a new perspective by means of a diverse range of techniques, including laser-line mapping of wing topographies, computational fluid dynamics simulations of finely detailed wing geometries, quantitative imaging using particle image velocimetry of on-wing and wake flow patterns, classical aerodynamic theory, photography in the field, infrared motion capture and multi-camera optical tracking of free flight trajectories in laboratory environments. Our comprehensive approach enables a novel synthesis of datasets and subfields that integrates many aspects of flight from the neurobiology of the compound eye, through the aeromechanical interface with the surrounding fluid, to flight performance under cruising and higher-energy behavioural modes.This article is part of the themed issue 'Moving in a moving medium: new perspectives on flight'.

Bone-free: soft mechanics for adaptive locomotion.

Muscular hydrostats (such as mollusks), and fluid-filled animals (such as annelids), can exploit their constant-volume tissues to transfer forces and displacements in predictable ways, much as articulated animals use hinges and levers. Although larval insects contain pressurized fluids, they also have internal air tubes that are compressible and, as a result, they have more uncontrolled degrees of freedom. Therefore, the mechanisms by which larval insects control their movements are expected to reveal useful strategies for designing soft biomimetic robots. Using caterpillars as a tractable model system, it is now possible to identify the biomechanical and neural strategies for controlling movements in such highly deformable animals. For example, the tobacco hornworm, Manduca sexta, can stiffen its body by increasing muscular tension (and therefore body pressure) but the internal cavity (hemocoel) is not iso-barometric, nor is pressure used to directly control the movements of its limbs. Instead, fluid and tissues flow within the hemocoel and the body is soft and flexible to conform to the substrate. Even the gut contributes to the biomechanics of locomotion; it is decoupled from the movements of the body wall and slides forward within the body cavity at the start of each step. During crawling the body is kept in tension for part of the stride and compressive forces are exerted on the substrate along the axis of the caterpillar, thereby using the environment as a skeleton. The timing of muscular activity suggests that crawling is coordinated by proleg-retractor motoneurons and that the large segmental muscles produce anterograde waves of lifting that do not require precise timing. This strategy produces a robust form of locomotion in which the kinematics changes little with orientation. In different species of caterpillar, the presence of prolegs on particular body segments is related to alternative kinematics such as "inching." This suggests a mechanism for the evolution of different gaits through changes in the usage of prolegs, rather than, through extensive alterations in the motor program controlling the body wall. Some of these findings are being used to design and test novel control-strategies for highly deformable robots. These "softworm" devices are providing new insights into the challenges faced by any soft animal navigating in a terrestrial environment.

Through the eyes of a bird: modelling visually guided obstacle flight.

Various flight navigation strategies for birds have been identified at the large spatial scales of migratory and homing behaviours. However, relatively little is known about close-range obstacle negotiation through cluttered environments. To examine obstacle flight guidance, we tracked pigeons (Columba livia) flying through an artificial forest of vertical poles. Interestingly, pigeons adjusted their flight path only approximately 1.5 m 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 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 towards larger visual gaps when making fast steering decisions. The proposed behavioural modelling method converts the obstacle avoidance behaviour into a (piecewise) target-aiming behaviour, which is better defined and understood. This study demonstrates how such an approach decomposes open-loop free-flight behaviours into components that can be independently evaluated.

A new bi-axial cantilever beam design for biomechanics force measurements.

The demand for measuring forces exerted by animals during locomotion has increased dramatically as biomechanists strive to understand and implement biomechanical control strategies. In particular, multi-axial force transducers are often required to capture animal limb coordination patterns. Most existing force transducers employ strain gages arranged in a Wheatstone bridge on a cantilever beam. Bi-axial measurements require duplicating this arrangement in the transverse direction. In this paper, we reveal a method to embed a Wheatstone bridge inside another to allow bi-axial measurements without additional strain gages or additional second beams. This hybrid configuration resolves two force components from a single bridge circuit and simplifies fabrication for the simultaneous assessment of normal and transverse loads. This design can be implemented with two-dimensional fabrication techniques and can even be used to modify a common full bridge cantilever force transducer. As a demonstration of the new design, we built a simple beam which achieved bi-axial sensing capability that outperformed a conventional half-bridge-per-axis bi-axial strain gage design. We have used this design to measure the ground reaction forces of a crawling caterpillar and a caterpillar-mimicking soft robot. The simplicity and increased sensitivity of this method could facilitate bi-axial force measurements for experimental biologists.

GoQBot: a caterpillar-inspired soft-bodied rolling robot.

Rolling locomotion using an external force such as gravity has evolved many times. However, some caterpillars can curl into a wheel and generate their own rolling momentum as part of an escape repertoire. This change in body conformation occurs well within 100 ms and generates a linear velocity over 0.2 m s(-1), making it one of the fastest self-propelled wheeling behaviors in nature. Inspired by this behavior, we construct a soft-bodied robot to explore the dynamics and control issues of ballistic rolling. This robot, called GoQBot, closely mimics caterpillar rolling. Analyzing the whole body kinematics and 2D ground reaction forces at the robot ground anchor reveals about 1G of acceleration and more than 200 rpm of angular velocity. As a novel rolling robot, GoQBot demonstrates how morphing can produce new modes of locomotion. Furthermore, mechanical coupling of the actuators improves body coordination without sensory feedback. Such coupling is intrinsic to soft-bodied animals because there are no joints to isolate muscle-generated movements. Finally, GoQBot provides an estimate of the mechanical power for caterpillar rolling that is comparable to that of a locust jump. How caterpillar musculature produces such power in such a short time is yet to be discovered.

Caterpillars use the substrate as their external skeleton: A behavior confirmation.

Animals that lack rigid structures often employ pressurization to maintain body form and posture. Structural stability is then provided by incompressible fluids or tissues and the inflated morphology is called a hydrostatic skeleton. However, new ground reaction force data from the caterpillar, Manduca sexta suggest an alternate strategy for large soft animals moving in complex three dimensional structures. When crawling, Manduca can keep its body primarily in tension and transmit compressive deformation using the substrate. This effectively allows the caterpillar to minimize reliance on a hydrostatic skeleton and helps it conform to the environment. We call this alternative strategy an "environmental skeleton".