Swimming in a school shelters fish from turbulence.

Much has been written about the energetic effects of animals moving in schools or flocks, but experimental results are few and often ambiguous. A new study in PLOS Biology shows that schooling greatly reduces the cost of transport for fish in turbulent flow.

It pays to follow the leader: Metabolic cost of flight is lower for trailing birds in small groups.

Many bird species commonly aggregate in flocks for reasons ranging from predator defense to navigation. Available evidence suggests that certain types of flocks-the V and echelon formations of large birds-may provide a benefit that reduces the aerodynamic cost of flight, whereas cluster flocks typical of smaller birds may increase flight costs. However, metabolic flight costs have not been directly measured in any of these group flight contexts [Zhang and Lauder, J. Exp. Biol. 226, jeb245617 (2023)]. Here, we measured the energetic benefits of flight in small groups of two or three birds and the requirements for realizing those benefits, using metabolic energy expenditure and flight position measurements from European Starlings flying in a wind tunnel. The starlings continuously varied their relative position during flights but adopted a V formation motif on average, with a modal spanwise and streamwise spacing of [0.81, 0.91] wingspans. As measured via CO2 production, flight costs for follower birds were significantly reduced compared to their individual solo flight benchmarks. However, followers with more positional variability with respect to leaders did less well, even increasing their costs above solo flight. Thus, we directly demonstrate energetic costs and benefits for group flight followers in an experimental context amenable to further investigation of the underlying aerodynamics, wake interactions, and bird characteristics that produce these metabolic effects.

The science and technology of kinematic measurements in a century of Journal of Experimental Biology.

Kinematic measurements have been essential to the study of comparative biomechanics and offer insight into relationships between technological development and scientific progress. Here, we review the 100 year history of kinematic measurements in Journal of Experimental Biology (JEB) through eras that used film, analog video and digital video, and approaches that have circumvented the use of image capture. This history originated with the career of Sir James Gray and has since evolved over the generations of investigators that have followed. Although some JEB studies have featured technological developments that were ahead of their time, the vast majority of research adopted equipment that was broadly available through the consumer or industrial markets. We found that across eras, an emphasis on high-speed phenomena outpaced the growth of the number of articles published by JEB and the size of datasets increased significantly. Despite these advances, the number of species studied within individual reports has not differed significantly over time. Therefore, we find that advances in technology have helped to enable a growth in the number of JEB studies that have included kinematic measurements, contributed to an emphasis on high-speed phenomena, and yielded biomechanical studies that are more data rich, but are no more comparative now than in previous decades.

Drink safely: common swifts (Apus apus) dissipate mechanical energy to decrease flight speed before touch-and-go drinking.

Flight is an efficient way of transport over a unit of distance, but it can be very costly over each unit of time, and reducing flight energy expenditure is a major selective pressure in birds. The common swift (Apus apus) is one of the most aerial bird species, performing most behaviours in flight: foraging, sleeping and also drinking by regularly descending to various waterbodies and skimming over the surface. An energy-saving way to perform such touch-and-go drinking would be to strive to conserve mechanical energy, by transforming potential energy to kinetic energy during the gliding descent, touching water at high speed, and regaining height with minimal muscular work. Using 3D optical tracking, we recorded 163 swift drinking trajectories, over three waterbodies near Rennes, France. Contrary to the energy conservation hypothesis, we show that swifts approaching a waterbody with a higher mechanical energy (higher height and/or speed 5 s before contact) do not reach the water at higher speeds, but do brake, i.e. dissipate mechanical energy to lose both height and speed. Braking seems to be linked with sharp turns and the use of headwind to some extent, but finer turns and postural adjustments, beyond the resolving power of our tracking data, could also be involved. We hypothesize that this surprisingly costly behaviour results from a trade-off between energy expenditure and safety, because approaching a water surface requires fine motor control, and high speed increases the risk of falling into the water, which would have serious energetic and survival costs for a swift.

Musculoskeletal wing-actuation model of hummingbirds predicts diverse effects of primary flight muscles in hovering flight.

Hummingbirds have evolved to hover and manoeuvre with exceptional flight control. This is enabled by their musculoskeletal system that successfully exploits the agile motion of flapping wings. Here, we synthesize existing empirical and modelling data to generate novel hypotheses for principles of hummingbird wing actuation. These may help guide future experimental work and provide insights into the evolution and robotic emulation of hummingbird flight. We develop a functional model of the hummingbird musculoskeletal system, which predicts instantaneous, three-dimensional torque produced by primary (pectoralis and supracoracoideus) and combined secondary muscles. The model also predicts primary muscle contractile behaviour, including stress, strain, elasticity and work. Results suggest that the primary muscles (i.e. the flight 'engine') function as diverse effectors, as they do not simply power the stroke, but also actively deviate and pitch the wing with comparable actuation torque. The results also suggest that the secondary muscles produce controlled-tightening effects by acting against primary muscles in deviation and pitching. The diverse effects of the pectoralis are associated with the evolution of a comparatively enormous bicipital crest on the humerus.

How biomechanics, path planning and sensing enable gliding flight in a natural environment.

Gliding animals traverse cluttered aerial environments when performing ecologically relevant behaviours. However, it is unknown how gliders execute collision-free flight over varying distances to reach their intended target. We quantified complete glide trajectories amid obstacles in a naturally behaving population of gliding lizards inhabiting a rainforest reserve. In this cluttered habitat, the lizards used glide paths with fewer obstacles than alternatives of similar distance. Their takeoff direction oriented them away from obstacles in their path and they subsequently made mid-air turns with accelerations of up to 0.5 g to reorient towards the target tree. These manoeuvres agreed well with a vision-based steering model which maximized their bearing angle with the obstacle while minimizing it with the target tree. Nonetheless, negotiating obstacles reduced mid-glide shallowing rates, implying greater loss of altitude. Finally, the lizards initiated a pitch-up landing manoeuvre consistent with a visual trigger model, suggesting that the landing decision was based on the optical size and speed of the target. They subsequently followed a controlled-collision approach towards the target, ending with variable impact speeds. Overall, the visually guided path planning strategy that enabled collision-free gliding required continuous changes in the gliding kinematics such that the lizards never attained theoretically ideal steady-state glide dynamics.

Dragonflies use underdamped pursuit to chase conspecifics.

Pursuit is a common behavior exhibited by animals chasing prey, competitors and potential mates. Because of their speed and maneuverability, dragonflies are frequently studied as a model system for biological pursuit. Most quantitative studies have focused on prey pursuits in captive environments. To determine whether a different pursuit strategy is used when chasing conspecifics of nearly equal speed and agility, we recorded 3D flight trajectories from nine territorial chases between male Erythemis simplicicollis dragonflies in natural field conditions. During chases, dragonflies used an interception strategy with an unusually high-magnitude gain (k=-10.03 s-1 horizontal; -8.86 s-1 vertical) and short time delay (τ=50 ms). The product kτ determines how aggressively a pursuer corrects course to achieve interception. Previous studies of prey pursuit have found kτ values close to -1/e (-0.37), the time-optimal value for achieving pursuit without overshooting. However, we found that dragonflies chasing conspecifics use more negative kτ (-0.50 horizontal; -0.44 vertical), resulting in pursuits with a high degree of overshooting (i.e. moving past the target and alternating position from side to side). We confirmed via simulation that the observed gain and delay produce overshooting. We propose that overshooting is an adaptive feature of conspecific chases that can be achieved with only slight modification of the strategy used for intercepting prey. Overshooting might help avoid potentially damaging collisions while exhibiting the pursuing animal's flight performance and competitive ability. Repeated close approaches might also evoke evasive responses from the other dragonfly, effectively herding the competitor out of the territory.

Gliding for a free lunch: biomechanics of foraging flight in common swifts (Apus apus).

Although the biomechanics of animal flight have been well studied in laboratory apparatus such as wind tunnels for many years, the applicability of these data to natural flight behaviour has been examined in few instances and mostly in the context of long-distance migration. Here, we used rotational stereo-videography to record the free-flight trajectories of foraging common swifts. We found that, despite their exquisite manoeuvring capabilities, the swifts only rarely performed high-acceleration turns. More surprisingly, we also found that despite feeding on tiny insects probably moving with ambient flow, the birds adjust their air speed to optimize cost of transport over distance. Finally, swifts spent only 25% of their time flapping; the majority of their time (71%) was spent in extended wing gliding, during which the average power expended for changes in speed or elevation was 0.84 W kg-1 and not significantly different from 0. Thus, gliding swifts extracted sufficient environmental energy to pay the cost of flight during foraging.

Three-dimensional trajectories and network analyses of group behaviour within chimney swift flocks during approaches to the roost.

Chimney swifts (Chaetura pelagica) are highly manoeuvrable birds notable for roosting overnight in chimneys, in groups of hundreds or thousands of birds, before and during their autumn migration. At dusk, birds gather in large numbers from surrounding areas near a roost site. The whole flock then employs an orderly, but dynamic, circling approach pattern before rapidly entering a small aperture en masse We recorded the three-dimensional trajectories of ≈1 800 individual birds during a 30 min period encompassing flock formation, circling, and landing, and used these trajectories to test several hypotheses relating to flock or group behaviour. Specifically, we investigated whether the swifts use local interaction rules based on topological distance (e.g. the n nearest neighbours, regardless of their distance) rather than physical distance (e.g. neighbours within x m, regardless of number) to guide interactions, whether the chimney entry zone is more or less cooperative than the surrounding flock, and whether the characteristic subgroup size is constant or varies with flock density. We found that the swift flock is structured around local rules based on physical distance, that subgroup size increases with density, and that there exist regions of the flock that are less cooperative than others, in particular the chimney entry zone.

Asymmetry costs: effects of wing damage on hovering flight performance in the hawkmoth Manduca sexta.

Flight performance is fundamental to the fitness of flying organisms. Whilst airborne, flying organisms face unavoidable wing wear and wing area loss. Many studies have tried to quantify the consequences of wing area loss to flight performance with varied results, suggesting that not all types of damage are equal and different species may have different means to compensate for some forms of wing damage with little to no cost. Here, we investigated the cost of control during hovering flight with damaged wings, specifically wings with asymmetric and symmetric reductions in area, by measuring maximum load lifting capacity and the metabolic power of hovering flight in hawkmoths (Manduca sexta). We found that while asymmetric and symmetric reductions are both costly in terms of maximum load lifting and hovering efficiency, asymmetric reductions are approximately twice as costly in terms of wing area lost. The moths also did not modulate flapping frequency and amplitude as predicted by a hovering flight model, suggesting that the ability to do so, possibly tied to asynchronous versus synchronous flight muscles, underlies the varied responses found in different wing clipping experiments.

Bristles reduce the force required to 'fling' wings apart in the smallest insects.

The smallest flying insects commonly possess wings with long bristles. Little quantitative information is available on the morphology of these bristles, and their functional importance remains a mystery. In this study, we (1) collected morphological data on the bristles of 23 species of Mymaridae by analyzing high-resolution photographs and (2) used the immersed boundary method to determine via numerical simulation whether bristled wings reduced the force required to fling the wings apart while still maintaining lift. The effects of Reynolds number, angle of attack, bristle spacing and wing-wing interactions were investigated. In the morphological study, we found that as the body length of Mymaridae decreases, the diameter and gap between bristles decreases and the percentage of the wing area covered by bristles increases. In the numerical study, we found that a bristled wing experiences less force than a solid wing. The decrease in force with increasing gap to diameter ratio is greater at higher angles of attack than at lower angles of attack, suggesting that bristled wings may act more like solid wings at lower angles of attack than they do at higher angles of attack. In wing-wing interactions, bristled wings significantly decrease the drag required to fling two wings apart compared with solid wings, especially at lower Reynolds numbers. These results support the idea that bristles may offer an aerodynamic benefit during clap and fling in tiny insects.

Flight mechanics and control of escape manoeuvres in hummingbirds. II. Aerodynamic force production, flight control and performance limitations.

The superior manoeuvrability of hummingbirds emerges from complex interactions of specialized neural and physiological processes with the unique flight dynamics of flapping wings. Escape manoeuvring is an ecologically relevant, natural behaviour of hummingbirds, from which we can gain understanding into the functional limits of vertebrate locomotor capacity. Here, we extend our kinematic analysis of escape manoeuvres from a companion paper to assess two potential limiting factors of the manoeuvring performance of hummingbirds: (1) muscle mechanical power output and (2) delays in the neural sensing and control system. We focused on the magnificent hummingbird (Eugenes fulgens, 7.8 g) and the black-chinned hummingbird (Archilochus alexandri, 3.1 g), which represent large and small species, respectively. We first estimated the aerodynamic forces, moments and the mechanical power of escape manoeuvres using measured wing kinematics. Comparing active-manoeuvring and passive-damping aerodynamic moments, we found that pitch dynamics were lightly damped and dominated by the effect of inertia, while roll dynamics were highly damped. To achieve observed closed-loop performance, pitch manoeuvres required faster sensorimotor transduction, as hummingbirds can only tolerate half the delay allowed in roll manoeuvres. Accordingly, our results suggested that pitch control may require a more sophisticated control strategy, such as those based on prediction. For the magnificent hummingbird, we estimated that escape manoeuvres required muscle mass-specific power 4.5 times that during hovering. Therefore, in addition to the limitation imposed by sensorimotor delays, muscle power could also limit the performance of escape manoeuvres.

Flight mechanics and control of escape manoeuvres in hummingbirds. I. Flight kinematics.

Hummingbirds are nature's masters of aerobatic manoeuvres. Previous research shows that hummingbirds and insects converged evolutionarily upon similar aerodynamic mechanisms and kinematics in hovering. Herein, we use three-dimensional kinematic data to begin to test for similar convergence of kinematics used for escape flight and to explore the effects of body size upon manoeuvring. We studied four hummingbird species in North America including two large species (magnificent hummingbird, Eugenes fulgens, 7.8 g, and blue-throated hummingbird, Lampornis clemenciae, 8.0 g) and two smaller species (broad-billed hummingbird, Cynanthus latirostris, 3.4 g, and black-chinned hummingbirds Archilochus alexandri, 3.1 g). Starting from a steady hover, hummingbirds consistently manoeuvred away from perceived threats using a drastic escape response that featured body pitch and roll rotations coupled with a large linear acceleration. Hummingbirds changed their flapping frequency and wing trajectory in all three degrees of freedom on a stroke-by-stroke basis, likely causing rapid and significant alteration of the magnitude and direction of aerodynamic forces. Thus it appears that the flight control of hummingbirds does not obey the 'helicopter model' that is valid for similar escape manoeuvres in fruit flies. Except for broad-billed hummingbirds, the hummingbirds had faster reaction times than those reported for visual feedback control in insects. The two larger hummingbird species performed pitch rotations and global-yaw turns with considerably larger magnitude than the smaller species, but roll rates and cumulative roll angles were similar among the four species.

Western and Clark's grebes use novel strategies for running on water.

Few vertebrates run on water. The largest animals to accomplish this feat are western and Clark's grebes (Aechmophorus occidentalis and Aechmophorus clarkii). These birds use water running to secure a mate during a display called rushing. Grebes weigh an order of magnitude more than the next largest water runners, basilisk lizards (Basilicus basiliscus), and therefore face a greater challenge to support their body weight. How do these birds produce the hydrodynamic forces necessary to overcome gravity and sustain rushing? We present the first quantitative study of water running by grebes. High-speed video recordings elucidate the hindlimb movements of grebes rushing in the wild. We complement these findings with laboratory experiments using physical models and a preserved grebe foot to estimate how slapping the water surface contributes to weight support. Our results indicate that grebes use three novel tactics to successfully run on water. First, rushing grebes use exceptionally high stride rates, reaching 10 Hz. Second, grebe foot size and high water impact speed allow grebes to generate up to 30-55% of the required weight support through water slap alone. Finally, flattened foot bones reduce downward drag, permitting grebes to retract each foot from the water laterally. Together, these mechanisms outline a water-running strategy qualitatively different from that of the only previously studied water runner, the basilisk lizard. The hydrodynamic specializations of rushing grebes could inform the design of biomimetic appendages. Furthermore, the mechanisms underlying this impressive display demonstrate that evolution can dramatically alter performance under sexual selection.

The mechanics and behavior of cliff swallows during tandem flights.

Cliff swallows (Petrochelidon pyrrhonota) are highly maneuverable social birds that often forage and fly in large open spaces. Here we used multi-camera videography to measure the three-dimensional kinematics of their natural flight maneuvers in the field. Specifically, we collected data on tandem flights, defined as two birds maneuvering together. These data permit us to evaluate several hypotheses on the high-speed maneuvering flight performance of birds. We found that high-speed turns are roll-based, but that the magnitude of the centripetal force created in typical maneuvers varied only slightly with flight speed, typically reaching a peak of ~2 body weights. Turning maneuvers typically involved active flapping rather than gliding. In tandem flights the following bird copied the flight path and wingbeat frequency (~12.3 Hz) of the lead bird while maintaining position slightly above the leader. The lead bird turned in a direction away from the lateral position of the following bird 65% of the time on average. Tandem flights vary widely in instantaneous speed (1.0 to 15.6 m s(-1)) and duration (0.72 to 4.71 s), and no single tracking strategy appeared to explain the course taken by the following bird.

A protocol and calibration method for accurate multi-camera field videography.

Stereo videography is a powerful technique for quantifying the kinematics and behavior of animals, but it can be challenging to use in an outdoor field setting. We here present a workflow and associated software for performing calibration of cameras placed in a field setting and estimating the accuracy of the resulting stereoscopic reconstructions. We demonstrate the workflow through example stereoscopic reconstructions of bat and bird flight. We provide software tools for planning experiments and processing the resulting calibrations that other researchers may use to calibrate their own cameras. Our field protocol can be deployed in a single afternoon, requiring only short video clips of light, portable calibration objects.

Clap and fling mechanism with interacting porous wings in tiny insect flight.

The aerodynamics of flapping flight for the smallest insects such as thrips is often characterized by a 'clap and fling' of the wings at the end of the upstroke and the beginning of the downstroke. These insects fly at Reynolds numbers (Re) of the order of 10 or less where viscous effects are significant. Although this wing motion is known to augment the lift generated during flight, the drag required to fling the wings apart at this scale is an order of magnitude larger than the corresponding force acting on a single wing. As the opposing forces acting normal to each wing nearly cancel during the fling, these large forces do not have a clear aerodynamic benefit. If flight efficiency is defined as the ratio of lift to drag, the clap and fling motion dramatically reduces efficiency relative to the case of wings that do not aerodynamically interact. In this paper, the effect of a bristled wing characteristic of many of these insects was investigated using computational fluid dynamics. We performed 2D numerical simulations using a porous version of the immersed boundary method. Given the computational complexity involved in modeling flow through exact descriptions of bristled wings, the wing was modeled as a homogeneous porous layer as a first approximation. High-speed video recordings of free-flying thrips in take-off flight were captured in the laboratory, and an analysis of the wing kinematics was performed. This information was used for the estimation of input parameters for the simulations. Compared with a solid wing (without bristles), the results of the study show that the porous nature of the wings contributes largely to drag reduction across the Re range explored. The aerodynamic efficiency, calculated as the ratio of lift to drag coefficients, was larger for some porosities when compared with solid wings.

Feeding rate in adult Manduca sexta is unaffected by proboscis submersion depth.

Adult moths from framily Spingidae (i.e. hawkmoths or sphinx moths) commonly feed on flower nectar through an extended proboscis, often several centimeters in length and longer than the body of the moth. Feeding on a viscous liquid (nectar) through a long and narrow tube is a challenging fluid dynamic problem and the subject of long-running scientific investigation. Here we characterized the relationship between proboscis submergence depth and nectar drinking rate in Manduca sexta hawkmoths. Video recordings of moth feeding bouts were collected and neural networks were used to extract data by object localization, tracking the location of the nectar meniscus and moths' proboscis tips. We found that although feeding rates vary among bouts, the variation was not associated with proboscis submergence depth. These results show that despite the theoretical possibility of fluid uptake through the walls of the proboscis, such effects do not have a substantial effect on nectar uptake rate, and suggest that nectar must traverse the full length of the proboscis.

Biomechanics of insect flight stability and perturbation response.

Insects must fly in highly variable natural environments filled with gusts, vortices, and other transient aerodynamic phenomena that challenge flight stability. Furthermore, the aerodynamic forces that support insect flight are produced from rapidly oscillating wings of time-varying orientation and configuration. The instantaneous flight forces produced by these wings are large relative to the average forces supporting body weight. The magnitude of these forces and their time-varying direction add another challenge to flight stability, because even proportionally small asymmetries in timing or magnitude between the left and right wings may be sufficient to produce large changes in body orientation. However, these same large magnitude oscillating forces also offer an opportunity for unexpected flight stability through non-linear interactions between body orientation, body oscillation in response to time varying inertial and aerodynamic forces, and the oscillating wings themselves. Understanding the emergent stability properties of flying insects is a crucial step toward understanding the requirements for evolution of flapping flight and decoding the role of sensory feedback in flight control. Here we provide a brief review of insect flight stability, with some emphasis stability effects brought about by oscillating wings, and present some preliminary experimental data probing some aspects of flight stability in free-flying insects.

Aerodynamic response of a red-tailed hawk to discrete transverse gusts.

A limiting factor in the design of smaller size uncrewed aerial vehicles is their inability to navigate through gust-laden environments. As a result, engineers have turned towards bio-inspired engineering approaches for gust mitigation techniques. In this study, the aerodynamics of a red-tailed hawk's response to variable-magnitude discrete transverse gusts was investigated. The hawk was flown in an indoor flight arena instrumented by multiple high-speed cameras to quantify the 3D motion of the bird as it navigated through the gust. The hawk maintained its flapping motion across the gust in all runs; however, it encountered the gust at different points in the flapping pattern depending on the run and gust magnitude. The hawk responded with a downwards pitching motion of the wing, decreasing the wing pitch angle to between -20∘and -5∘, and remained in this configuration until gust exit. The wing pitch data was then applied to a lower-order aerodynamic model that estimated lift coefficients across the wing. In gusts slower than the forward flight velocity (low gust ratio), the lift coefficient increases at a low-rate, to a maximum of around 2-2.5. In gusts faster than the forward flight velocity (high gust ratio), the lift coefficient initially increased rapidly, before increasing at a low-rate to a value around 4-5. In both regimes, the hawk's observed height change due to gust interaction was similar (and small), despite larger estimated lift coefficients over the high gust regime. This suggests another mitigation factor apart from the wing response is present. One potential factor is the tail pitching response observed here, which prior work has shown serves to mitigate pitch disturbances from gusts.