Morphomechanical Innovation Drives Explosive Seed Dispersal.

How mechanical and biological processes are coordinated across cells, tissues, and organs to produce complex traits is a key question in biology. Cardamine hirsuta, a relative of Arabidopsis thaliana, uses an explosive mechanism to disperse its seeds. We show that this trait evolved through morphomechanical innovations at different spatial scales. At the organ scale, tension within the fruit wall generates the elastic energy required for explosion. This tension is produced by differential contraction of fruit wall tissues through an active mechanism involving turgor pressure, cell geometry, and wall properties of the epidermis. Explosive release of this tension is controlled at the cellular scale by asymmetric lignin deposition within endocarp b cells-a striking pattern that is strictly associated with explosive pod shatter across the Brassicaceae plant family. By bridging these different scales, we present an integrated mechanism for explosive seed dispersal that links evolutionary novelty with complex trait innovation. VIDEO ABSTRACT.

Lessons from natural flight for aviation: then, now and tomorrow.

Powered flight was once a capability limited only to animals, but by identifying useful attributes of animal flight and building on these with technological advances, engineers have pushed the frontiers of flight beyond our predecessors' wildest imaginations. Yet, there remain many key characteristics of biological flight that elude current aircraft design, motivating a careful re-analysis of what we have learned from animals already, and how this has been revealed experimentally, as well as a specific focus on identifying what remains unknown. Here, we review the literature to identify key contributions that began in biology and have since been translated into aeronautical devices or capabilities. We identify central areas for future research and highlight the importance of maintaining an open line of two-way communication between biologists and engineers. Such interdisciplinary, bio-informed analyses continue to push forward the frontiers of aeronautics and experimental biology alike.

Smart wing rotation and trailing-edge vortices enable high frequency mosquito flight.

Mosquitoes exhibit unusual wing kinematics; their long, slender wings flap at remarkably high frequencies for their size (>800 Hz)and with lower stroke amplitudes than any other insect group. This shifts weight support away from the translation-dominated, aerodynamic mechanisms used by most insects, as well as by helicopters and aeroplanes, towards poorly understood rotational mechanisms that occur when pitching at the end of each half-stroke. Here we report free-flight mosquito wing kinematics, solve the full Navier-Stokes equations using computational fluid dynamics with overset grids, and validate our results with in vivo flow measurements. We show that, although mosquitoes use familiar separated flow patterns, much of the aerodynamic force that supports their weight is generated in a manner unlike any previously described for a flying animal. There are three key features: leading-edge vortices (a well-known mechanism that appears to be almost ubiquitous in insect flight), trailing-edge vortices caused by a form of wake capture at stroke reversal, and rotational drag. The two new elements are largely independent of the wing velocity, instead relying on rapid changes in the pitch angle (wing rotation) at the end of each half-stroke, and they are therefore relatively immune to the shallow flapping amplitude. Moreover, these mechanisms are particularly well suited to high aspect ratio mosquito wings.

Bird wings act as a suspension system that rejects gusts.

Musculoskeletal systems cope with many environmental perturbations without neurological control. These passive preflex responses aid animals to move swiftly through complex terrain. Whether preflexes play a substantial role in animal flight is uncertain. We investigated how birds cope with gusty environments and found that their wings can act as a suspension system, reducing the effects of vertical gusts by elevating rapidly about the shoulder. This preflex mechanism rejected the gust impulse through inertial effects, diminishing the predicted impulse to the torso and head by 32% over the first 80 ms, before aerodynamic mechanisms took effect. For each wing, the centre of aerodynamic loading aligns with the centre of percussion, consistent with enhancing passive inertial gust rejection. The reduced motion of the torso in demanding conditions simplifies crucial tasks, such as landing, prey capture and visual tracking. Implementing a similar preflex mechanism in future small-scale aircraft will help to mitigate the effects of gusts and turbulence without added computational burden.

High aerodynamic lift from the tail reduces drag in gliding raptors.

Many functions have been postulated for the aerodynamic role of the avian tail during steady-state flight. By analogy with conventional aircraft, the tail might provide passive pitch stability if it produced very low or negative lift. Alternatively, aeronautical principles might suggest strategies that allow the tail to reduce inviscid, induced drag: if the wings and tail act in different horizontal planes, they might benefit from biplane-like aerodynamics; if they act in the same plane, lift from the tail might compensate for lift lost over the fuselage (body), reducing induced drag with a more even downwash profile. However, textbook aeronautical principles should be applied with caution because birds have highly capable sensing and active control, presumably reducing the demand for passive aerodynamic stability, and, because of their small size and low flight speeds, operate at Reynolds numbers two orders of magnitude below those of light aircraft. Here, by tracking up to 20,000, 0.3 mm neutrally buoyant soap bubbles behind a gliding barn owl, tawny owl and goshawk, we found that downwash velocity due to the body/tail consistently exceeds that due to the wings. The downwash measured behind the centreline is quantitatively consistent with an alternative hypothesis: that of constant lift production per planform area, a requirement for minimizing viscous, profile drag. Gliding raptors use lift distributions that compromise both inviscid induced drag minimization and static pitch stability, instead adopting a strategy that reduces the viscous drag, which is of proportionately greater importance to lower Reynolds number fliers.

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.

Dynamics of hinged wings in strong upward gusts.

A bird's wings are articulated to its body via highly mobile shoulder joints. The joints confer an impressive range of motion, enabling the wings to make broad, sweeping movements that can modulate quite dramatically the production of aerodynamic load. This is enormously useful in challenging flight environments, especially the gusty, turbulent layers of the lower atmosphere. In this study, we develop a dynamics model to examine how a bird-scale gliding aircraft can use wing-root hinges (analogous to avian shoulder joints) to reject the initial impact of a strong upward gust. The idea requires that the spanwise centre of pressure and the centre of percussion of the hinged wing start, and stay, in good initial alignment (the centre of percussion here is related to the idea of a 'sweet spot' on a bat, as in cricket or baseball). We propose a method for achieving this rejection passively, for which the essential ingredients are (i) appropriate lift and mass distributions; (ii) hinges under constant initial torque; and (iii) a wing whose sections stall softly. When configured correctly, the gusted wings will first pivot on their hinges without disturbing the fuselage of the aircraft, affording time for other corrective actions to engage. We expect this system to enhance the control of aircraft that fly in gusty conditions.

Virtual manipulation of tail postures of a gliding barn owl (Tyto alba) demonstrates drag minimization when gliding.

Aerodynamic functions of the avian tail have been studied previously using observations of bird flight, physical models in wind tunnels, theoretical modelling and flow visualization. However, none of these approaches has provided rigorous, quantitative evidence concerning tail functions because (i) appropriate manipulation and controls cannot be achieved using live animals and (ii) the aerodynamic interplay between the wings and body challenges reductive theoretical or physical modelling approaches. Here, we have developed a comprehensive analytical drag model, calibrated by high-fidelity computational fluid dynamics (CFD), and used it to investigate the aerodynamic action of the tail by virtually manipulating its posture. The bird geometry used for CFD was reconstructed previously using stereo-photogrammetry of a freely gliding barn owl (Tyto alba) and we validated the CFD simulations against wake measurements. Using this CFD-calibrated drag model, we predicted the drag production for 16 gliding flights with a range of tail postures. These observed postures are set in the context of a wider parameter sweep of theoretical postures, where the tail spread and elevation angles were manipulated independently. The observed postures of our gliding bird corresponded to near minimal total drag.

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.

Auditory sensory range of male mosquitoes for the detection of female flight sound.

Male mosquitoes detect and localize conspecific females by their flight-tones using the Johnston's organ (JO), which detects antennal deflections under the influence of local particle motion. Acoustic behaviours of mosquitoes and their JO physiology have been investigated extensively within the frequency domain, yet the auditory sensory range and the behaviour of males at the initiation of phonotactic flights are not well known. In this study, we predict a maximum spatial sensory envelope for flying Culex quinquefasciatus by integrating the physiological tuning response of the male JO with female aeroacoustic signatures derived from numerical simulations. Our sensory envelope predictions were tested with a behavioural assay of free-flying males responding to a female-like artificial pure tone. The minimum detectable particle velocity observed during flight tests was in good agreement with our theoretical prediction formed by the peak JO sensitivity measured in previous studies. The iso-surface describing the minimal detectable particle velocity represents the quantitative auditory sensory range of males and is directional with respect to the female body orientation. Our results illuminate the intricacy of the mating behaviour and point to the importance of observing the body orientation of flying mosquitoes to understand fully the sensory ecology of conspecific communication.

Raptor wing morphing with flight speed.

In gliding flight, birds morph their wings and tails to control their flight trajectory and speed. Using high-resolution videogrammetry, we reconstructed accurate and detailed three-dimensional geometries of gliding flights for three raptors (barn owl, Tyto alba; tawny owl, Strix aluco, and goshawk, Accipiter gentilis). Wing shapes were highly repeatable and shoulder actuation was a key component of reconfiguring the overall planform and controlling angle of attack. The three birds shared common spanwise patterns of wing twist, an inverse relationship between twist and peak camber, and held their wings depressed below their shoulder in an anhedral configuration. With increased speed, all three birds tended to reduce camber throughout the wing, and their wings bent in a saddle-shape pattern. A number of morphing features suggest that the coordinated movements of the wing and tail support efficient flight, and that the tail may act to modulate wing camber through indirect aeroelastic control.

Aerodynamic imaging by mosquitoes inspires a surface detector for autonomous flying vehicles.

Some flying animals use active sensing to perceive and avoid obstacles. Nocturnal mosquitoes exhibit a behavioral response to divert away from surfaces when vision is unavailable, indicating a short-range, mechanosensory collision-avoidance mechanism. We suggest that this behavior is mediated by perceiving modulations of their self-induced airflow patterns as they enter a ground or wall effect. We used computational fluid dynamics simulations of low-altitude and near-wall flights based on in vivo high-speed kinematic measurements to quantify changes in the self-generated pressure and velocity cues at the sensitive mechanosensory antennae. We validated the principle that encoding aerodynamic information can enable collision avoidance by developing a quadcopter with a sensory system inspired by the mosquito. Such low-power sensing systems have major potential for future use in safer rotorcraft control systems.

Insect and insect-inspired aerodynamics: unsteadiness, structural mechanics and flight control.

Flying insects impress by their versatility and have been a recurrent source of inspiration for engineering devices. A large body of literature has focused on various aspects of insect flight, with an essential part dedicated to the dynamics of flapping wings and their intrinsically unsteady aerodynamic mechanisms. Insect wings flex during flight and a better understanding of structural mechanics and aeroelasticity is emerging. Most recently, insights from solid and fluid mechanics have been integrated with physiological measurements from visual and mechanosensors in the context of flight control in steady airs and through turbulent conditions. We review the key recent advances concerning flight in unsteady environments and how the multi-body mechanics of the insect structure-wings and body-are at the core of the flight control question. The issues herein should be considered when applying bio-informed design principles to robotic flapping wings.

Petiolate wings: effects on the leading-edge vortex in flapping flight.

The wings of many insect species including crane flies and damselflies are petiolate (on stalks), with the wing planform beginning some distance away from the wing hinge, rather than at the hinge. The aerodynamic impact of flapping petiolate wings is relatively unknown, particularly on the formation of the lift-augmenting leading-edge vortex (LEV): a key flow structure exploited by many insects, birds and bats to enhance their lift coefficient. We investigated the aerodynamic implications of petiolation P using particle image velocimetry flow field measurements on an array of rectangular wings of aspect ratio 3 and petiolation values of P = 1-3. The wings were driven using a mechanical device, the 'Flapperatus', to produce highly repeatable insect-like kinematics. The wings maintained a constant Reynolds number of 1400 and dimensionless stroke amplitude Λ* (number of chords traversed by the wingtip) of 6.5 across all test cases. Our results showed that for more petiolate wings the LEV is generally larger, stronger in circulation, and covers a greater area of the wing surface, particularly at the mid-span and inboard locations early in the wing stroke cycle. In each case, the LEV was initially arch-like in form with its outboard end terminating in a focus-sink on the wing surface, before transitioning to become continuous with the tip vortex thereafter. In the second half of the wing stroke, more petiolate wings exhibit a more detached LEV, with detachment initiating at approximately 70% and 50% span for P = 1 and 3, respectively. As a consequence, lift coefficients based on the LEV are higher in the first half of the wing stroke for petiolate wings, but more comparable in the second half. Time-averaged LEV lift coefficients show a general rise with petiolation over the range tested.

Digital particle image velocimetry measurements of the downwash distribution of a desert locust Schistocerca gregaria.

Actuator disc models of insect flight are concerned solely with the rate of momentum transfer to the air that passes through the disc. These simple models assume that an even pressure is applied across the disc, resulting in a uniform downwash distribution. However, a correction factor, k, is often included to correct for the difference in efficiency between the assumed even downwash distribution, and the real downwash distribution. In the absence of any empirical measurements of the downwash distribution behind a real insect, the values of k used in the literature have been necessarily speculative. Direct measurement of this efficiency factor is now possible, and could be used to compare the relative efficiencies of insect flight across the Class. Here, we use Digital Particle Image Velocimetry to measure the instantaneous downwash distribution, mid-downstroke, of a tethered desert locust (Schistocerca gregaria). By integrating the downwash distribution, we are thereby able to provide the first direct empirical measurement of k for an insect. The measured value of k = 1.12 corresponds reasonably well with that predicted by previous theoretical studies.

Enhanced flight performance by genetic manipulation of wing shape in Drosophila.

Insect wing shapes are remarkably diverse and the combination of shape and kinematics determines both aerial capabilities and power requirements. However, the contribution of any specific morphological feature to performance is not known. Using targeted RNA interference to modify wing shape far beyond the natural variation found within the population of a single species, we show a direct effect on flight performance that can be explained by physical modelling of the novel wing geometry. Our data show that altering the expression of a single gene can significantly enhance aerial agility and that the Drosophila wing shape is not, therefore, optimized for certain flight performance characteristics that are known to be important. Our technique points in a new direction for experiments on the evolution of performance specialities in animals.

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'.

A CFD-informed quasi-steady model of flapping wing aerodynamics.

Aerodynamic performance and agility during flapping flight are determined by the combination of wing shape and kinematics. The degree of morphological and kinematic optimisation is unknown and depends upon a large parameter space. Aimed at providing an accurate and computationally inexpensive modelling tool for flapping-wing aerodynamics, we propose a novel CFD (computational fluid dynamics)-informed quasi-steady model (CIQSM), which assumes that the aerodynamic forces on a flapping wing can be decomposed into the quasi-steady forces and parameterised based on CFD results. Using least-squares fitting, we determine a set of proportional coefficients for the quasi-steady model relating wing kinematics to instantaneous aerodynamic force and torque; we calculate power with the product of quasi-steady torques and angular velocity. With the quasi-steady model fully and independently parameterised on the basis of high-fidelity CFD modelling, it is capable of predicting flapping-wing aerodynamic forces and power more accurately than the conventional blade element model (BEM) does. The improvement can be attributed to, for instance, taking into account the effects of the induced downwash and the wing tip vortex on the force generation and power consumption. Our model is validated by comparing the aerodynamics of a CFD model and the present quasi-steady model using the example case of a hovering hawkmoth. It demonstrates that the CIQSM outperforms the conventional BEM while remaining computationally cheap, and hence can be an effective tool for revealing the mechanisms of optimization and control of kinematics and morphology in flapping-wing flight for both bio-flyers and unmanned air systems.

The effect of aspect ratio on the leading-edge vortex over an insect-like flapping wing.

Insect wing shapes are diverse and a renowned source of inspiration for the new generation of autonomous flapping vehicles, yet the aerodynamic consequences of varying geometry is not well understood. One of the most defining and aerodynamically significant measures of wing shape is the aspect ratio, defined as the ratio of wing length (R) to mean wing chord (c). We investigated the impact of aspect ratio, AR, on the induced flow field around a flapping wing using a robotic device. Rigid rectangular wings ranging from AR = 1.5 to 7.5 were flapped with insect-like kinematics in air with a constant Reynolds number (Re) of 1400, and a dimensionless stroke amplitude of 6.5c (number of chords traversed by the wingtip). Pseudo-volumetric, ensemble-averaged, flow fields around the wings were captured using particle image velocimetry at 11 instances throughout simulated downstrokes. Results confirmed the presence of a high-lift, separated flow field with a leading-edge vortex (LEV), and revealed that the conical, primary LEV grows in size and strength with increasing AR. In each case, the LEV had an arch-shaped axis with its outboard end originating from a focus-sink singularity on the wing surface near the tip. LEV detachment was observed for AR > 1.5 around mid-stroke at ~70% span, and initiated sooner over higher aspect ratio wings. At AR > 3 the larger, stronger vortex persisted under the wing surface well into the next half-stroke leading to a reduction in lift. Circulatory lift attributable to the LEV increased with AR up to AR = 6. Higher aspect ratios generated proportionally less lift distally because of LEV breakdown, and also less lift closer to the wing root due to the previous LEV's continuing presence under the wing. In nature, insect wings go no higher than AR ~ 5, likely in part due to architectural and physiological constraints but also because of the reducing aerodynamic benefits of high AR wings.