Small deviations in kinematics and body form dictate muscle performances in the finely tuned avian downstroke.

Avian takeoff requires peak pectoralis muscle power to generate sufficient aerodynamic force during the downstroke. Subsequently, the much smaller supracoracoideus recovers the wing during the upstroke. How the pectoralis work loop is tuned to power flight is unclear. We integrate wingbeat-resolved muscle, kinematic, and aerodynamic recordings in vivo with a new mathematical model to disentangle how the pectoralis muscle overcomes wing inertia and generates aerodynamic force during takeoff in doves. Doves reduce the angle of attack of their wing mid-downstroke to efficiently generate aerodynamic force, resulting in an aerodynamic power dip, that allows transferring excess pectoralis power into tensioning the supracoracoideus tendon to assist the upstroke-improving the pectoralis work loop efficiency simultaneously. Integrating extant bird data, our model shows how the pectoralis of birds with faster wingtip speed need to generate proportionally more power. Finally, birds with disproportionally larger wing inertia need to activate the pectoralis earlier to tune their downstroke.

Birds both avoid and control collisions by harnessing visually guided force vectoring.

Birds frequently manoeuvre around plant clutter in complex-structured habitats. To understand how they rapidly negotiate obstacles while flying between branches, we measured how foraging Pacific parrotlets avoid horizontal strings obstructing their preferred flight path. Informed by visual cues, the birds redirect forces with their legs and wings to manoeuvre around the obstacle and make a controlled collision with the goal perch. The birds accomplish aerodynamic force vectoring by adjusting their body pitch, stroke plane angle and lift-to-drag ratios beat-by-beat, resulting in a range of about 100° relative to the horizontal plane. The key role of drag in force vectoring revises earlier ideas on how the avian stroke plane and body angle correspond to aerodynamic force direction-providing new mechanistic insight into avian manoeuvring-and how the evolution of flight may have relied on harnessing drag.

Lepidoptera demonstrate the relevance of Murray's Law to circulatory systems with tidal flow.

BACKGROUND: Murray's Law, which describes the branching architecture of bifurcating tubes, predicts the morphology of vessels in many amniotes and plants. Here, we use insects to explore the universality of Murray's Law and to evaluate its predictive power for the wing venation of Lepidoptera, one of the most diverse insect orders. Lepidoptera are particularly relevant to the universality of Murray's Law because their wing veins have tidal, or oscillatory, flow of air and hemolymph. We examined over one thousand wings representing 667 species of Lepidoptera. RESULTS: We found that veins with a diameter above approximately 50 microns conform to Murray's Law, with veins below 50 microns in diameter becoming less and less likely to conform to Murray's Law as they narrow. The minute veins that are most likely to deviate from Murray's Law are also the most likely to have atrophied, which prevents efficient fluid transport regardless of branching architecture. However, the veins of many taxa continue to branch distally to the areas where they atrophied, and these too conform to Murray's Law at larger diameters (e.g., Sesiidae). CONCLUSIONS: This finding suggests that conformity to Murray's Law in larger taxa may reflect requirements for structural support as much as fluid transport, or may indicate that selective pressures for fluid transport are stronger during the pupal stage-during wing development prior to vein atrophy-than the adult stage. Our results increase the taxonomic scope of Murray's Law and provide greater clarity about the relevance of body size.

How oscillating aerodynamic forces explain the timbre of the hummingbird's hum and other animals in flapping flight.

How hummingbirds hum is not fully understood, but its biophysical origin is encoded in the acoustic nearfield. Hence, we studied six freely hovering Anna's hummingbirds, performing acoustic nearfield holography using a 2176 microphone array in vivo, while also directly measuring the 3D aerodynamic forces using a new aerodynamic force platform. We corroborate the acoustic measurements by developing an idealized acoustic model that integrates the aerodynamic forces with wing kinematics, which shows how the timbre of the hummingbird's hum arises from the oscillating lift and drag forces on each wing. Comparing birds and insects, we find that the characteristic humming timbre and radiated power of their flapping wings originates from the higher harmonics in the aerodynamic forces that support their bodyweight. Our model analysis across insects and birds shows that allometric deviation makes larger birds quieter and elongated flies louder, while also clarifying complex bioacoustic behavior.

Anyone walking outdoors has heard the whooshing sound of birdwings flapping overhead, the buzzing sound of bees flying by, or the whining of mosquitos seeking blood. All animals with flapping wings make these sounds, but the hummingbird makes perhaps the most delightful sound of all: their namesake hum. Yet, how hummingbirds hum is poorly understood. Bird wings generate large vortices of air to boost their lift and hover in the air that can generate tones. Further, the airflow over bird wings can be highly turbulent, meaning it can generate loud sounds, like the jets of air coming out of the engines of aircraft. Given all the sound-generating mechanisms at hand, it is difficult to determine why some wings buzz whereas others whoosh or hum. Hightower, Wijnings et al. wanted to understand the physical mechanism that causes animal wings to whine, buzz, hum or whoosh in flight. They hypothesized that the aerodynamic forces generated by animal wings are the main source of their characteristic wing sounds. Hummingbird wings have the most features in common with different animals' wings, while also featuring acoustically complex feathers. This makes them ideal models for deciphering how birds, bats and even insects make wing sounds. To learn more about wing sounds, Hightower, Wijnings et al. studied how a species of hummingbird called Anna's hummingbird hums while drinking nectar from a flower. A three-dimensional 'acoustic hologram' was generated using 2,176 microphones to measure the humming sound from all directions. In a follow-up experiment, the aerodynamic forces the hummingbird wings generate to hover were also measured. Their wingbeat was filmed simultaneously in slow-motion in both experiments. Hightower, Wijnings et al. then used a mathematical model that governs the wing's aeroacoustics to confirm that the aerodynamic forces generated by the hummingbirds' wings cause the humming sound heard when they hover in front of a flower. The model shows that the oscillating aerodynamic forces generate harmonics, which give the wings' hum the acoustic quality of a musical instrument. Using this model Hightower, Wijnings et al. found that the differences in the aerodynamic forces generated by bird and insect wings cause the characteristic timbres of their whines, buzzes, hums, or whooshes. They also determined how these sounds scale with body mass and flapping frequency across 170 insect species and 80 bird species. This showed that mosquitos are unusually loud for their body size due to the unusual unsteadiness of the aerodynamic forces they generate in flight. These results explain why flying animals' wings sound the way they do ­ for example, why larger birds are quieter and mosquitos louder. Better understanding of how the complex forces generated by animal wings create sound can advance the study of how animals change their wingbeat to communicate. Further, the model that explains how complex aerodynamic forces cause sound can help make the sounds of aerial robots, drones, and fans not only more silent, but perhaps more pleasing, like the hum of a hummingbird.

Soft biohybrid morphing wings with feathers underactuated by wrist and finger motion.

Since the Wright Flyer, engineers have strived to develop flying machines with morphing wings that can control flight as deftly as birds. Birds morph their wing planform parameters simultaneously-including sweep, span, and area-in a way that has proven to be particularly challenging to embody robotically. Previous solutions have primarily centered around the classical aerospace paradigm of controlling every degree of freedom to ensure predictable performance, but underperform compared with birds. To understand how birds accomplish wing morphing, we measured the kinematics of wing flexion and extension in common pigeons, Columba livia The skeletal and feather kinematics show that the 20 primary and 20 secondary feathers are coordinated via approximately linear transfer functions controlled by wrist and finger motion. To replicate this control principle in a robot, we developed a biohybrid morphing wing with real feathers to understand the underlying design principles. The outcome, PigeonBot, embodies 42 degrees of freedom that control the position of 40 elastically connected feathers via four servo-actuated wrist and finger joints. Our flight tests demonstrate that the soft feathered wings morph rapidly and robustly under aerodynamic loading. They not only enable wing morphing but also make robot interactions safer, the wing more robust to crashing, and the wing reparable via "preening." In flight tests, we found that both asymmetric wrist and finger motion can initiate turn maneuvers-evidence that birds may use their fingers to steer in flight.

The aerodynamic force platform as an ergometer.

Animal flight requires aerodynamic power, which is challenging to determine accurately in vivo Existing methods rely on approximate calculations based on wake flow field measurements, inverse dynamics approaches, or invasive muscle physiological recordings. In contrast, the external mechanical work required for terrestrial locomotion can be determined more directly by using a force platform as an ergometer. Based on an extension of the recent invention of the aerodynamic force platform, we now present a more direct method to determine the in vivo aerodynamic power by taking the dot product of the aerodynamic force vector on the wing with the representative wing velocity vector based on kinematics and morphology. We demonstrate this new method by studying a slowly flying dove, but it can be applied more generally across flying and swimming animals as well as animals that locomote over water surfaces. Finally, our mathematical framework also works for power analyses based on flow field measurements.

How flight feathers stick together to form a continuous morphing wing.

Variable feather overlap enables birds to morph their wings, unlike aircraft. They accomplish this feat by means of elastic compliance of connective tissue, which passively redistributes the overlapping flight feathers when the skeleton moves to morph the wing planform. Distinctive microstructures form "directional Velcro," such that when adjacent feathers slide apart during extension, thousands of lobate cilia on the underlapping feathers lock probabilistically with hooked rami of overlapping feathers to prevent gaps. These structures unlock automatically during flexion. Using a feathered biohybrid aerial robot, we demonstrate how both passive mechanisms make morphing wings robust to turbulence. We found that the hooked microstructures fasten feathers across bird species except silent fliers, whose feathers also lack the associated Velcro-like noise. These findings could inspire innovative directional fasteners and morphing aircraft.

Birds repurpose the role of drag and lift to take off and land.

The lift that animal wings generate to fly is typically considered a vertical force that supports weight, while drag is considered a horizontal force that opposes thrust. To determine how birds use lift and drag, here we report aerodynamic forces and kinematics of Pacific parrotlets (Forpus coelestis) during short, foraging flights. At takeoff they incline their wing stroke plane, which orients lift forward to accelerate and drag upward to support nearly half of their bodyweight. Upon landing, lift is oriented backward to contribute a quarter of the braking force, which reduces the aerodynamic power required to land. Wingbeat power requirements are dominated by downstrokes, while relatively inactive upstrokes cost almost no aerodynamic power. The parrotlets repurpose lift and drag during these flights with lift-to-drag ratios below two. Such low ratios are within range of proto-wings, showing how avian precursors may have relied on drag to take off with flapping wings.

Birds land reliably on complex surfaces by adapting their foot-surface interactions upon contact.

Birds land on a wide range of complex surfaces, yet it is unclear how they grasp a perch reliably. Here, we show how Pacific parrotlets exhibit stereotyped leg and wing dynamics regardless of perch diameter and texture, but foot, toe, and claw kinematics become surface-specific upon touchdown. A new dynamic grasping model, which integrates our detailed measurements, reveals how birds stabilize their grasp. They combine predictable toe pad friction with probabilistic friction from their claws, which they drag to find surface asperities-dragging further when they can squeeze less. Remarkably, parrotlet claws can undergo superfast movements, within 1-2 ms, on moderately slippery surfaces to find more secure asperities when necessary. With this strategy, they first ramp up safety margins by squeezing before relaxing their grasp. The model further shows it is advantageous to be small for stable perching when high friction relative to normal force is required because claws can find more usable surface, but this trend reverses when required friction shrinks. This explains how many animals and robots may grasp complex surfaces reliably.

How lovebirds maneuver through lateral gusts with minimal visual information.

Flying birds maneuver effectively through lateral gusts, even when gust speeds are as high as flight speeds. What information birds use to sense gusts and how they compensate is largely unknown. We found that lovebirds can maneuver through 45° lateral gusts similarly well in forest-, lake-, and cave-like visual environments. Despite being diurnal and raised in captivity, the birds fly to their goal perch with only a dim point light source as a beacon, showing that they do not need optic flow or a visual horizon to maneuver. To accomplish this feat, lovebirds primarily yaw their bodies into the gust while fixating their head on the goal using neck angles of up to 30°. Our corroborated model for proportional yaw reorientation and speed control shows how lovebirds can compensate for lateral gusts informed by muscle proprioceptive cues from neck twist. The neck muscles not only stabilize the lovebirds' visual and inertial head orientations by compensating low-frequency body maneuvers, but also attenuate faster 3D wingbeat-induced perturbations. This head stabilization enables the vestibular system to sense the direction of gravity. Apparently, the visual horizon can be replaced by a gravitational horizon to inform the observed horizontal gust compensation maneuvers in the dark. Our scaling analysis shows how this minimal sensorimotor solution scales favorably for bigger birds, offering local wind angle feedback within a wingbeat. The way lovebirds glean wind orientation may thus inform minimal control algorithms that enable aerial robots to maneuver in similar windy and dark environments.

A Bird's-Eye View of Regulatory, Animal Care, and Training Considerations Regarding Avian Flight Research.

A thorough understanding of how animals fly is a central goal of many scientific disciplines. Birds are a commonly used model organism for flight research. The success of this model requires studying healthy and naturally flying birds in a laboratory setting. This use of a nontraditional laboratory animal species presents unique challenges to animal care staff and researchers alike. Here we review regulatory, animal care, and training considerations associated with avian flight research.

How the hummingbird wingbeat is tuned for efficient hovering.

Both hummingbirds and insects flap their wings to hover. Some insects, like fruit flies, improve efficiency by lifting their body weight equally over the upstroke and downstroke, while utilizing elastic recoil during stroke reversal. It is unclear whether hummingbirds converged on a similar elastic storage solution, because of asymmetries in their lift generation and specialized flight muscle apparatus. The muscles are activated a quarter of a stroke earlier than in larger birds, and contract superfast, which cannot be explained by previous stroke-averaged analyses. We measured the aerodynamic force and kinematics of Anna's hummingbirds to resolve wing torque and power within the wingbeat. Comparing these wingbeat-resolved aerodynamic weight support measurements with those of fruit flies, hawk moths and a generalist bird, the parrotlet, we found that hummingbirds have about the same low induced power losses as the two insects, lower than that of the generalist bird in slow hovering flight. Previous analyses emphasized how bird flight muscles have to overcome wing drag midstroke. We found that high wing inertia revises this for hummingbirds - the pectoralis has to coordinate upstroke to downstroke reversal while the supracoracoideus coordinates downstroke to upstroke reversal. Our mechanistic analysis aligns with all previous muscle recordings and shows how early activation helps furnish elastic recoil through stroke reversal to stay within the physiological limits of muscles. Our findings thus support Weis-Fogh's hypothesis that flies and hummingbirds have converged on a mechanically efficient wingbeat to meet the high energetic demands of hovering flight. These insights can help improve the efficiency of flapping robots.

Biomechanics of hover performance in Neotropical hummingbirds versus bats.

Hummingbirds and nectar bats are the only vertebrates that are specialized for hovering in front of flowers to forage nectar. How their aerodynamic performance compares is, however, unclear. To hover, hummingbirds consistently generate about a quarter of the vertical aerodynamic force required to support their body weight during the upstroke. In contrast, generalist birds in slow hovering flight generate little upstroke weight support. We report that nectar bats also generate elevated weight support during the upstroke compared to generalist bats. Comparing 20 Neotropical species, we show how nectarivorous birds and bats converged on this ability by inverting their respective feathered and membrane wings more than species with other diets. However, while hummingbirds converged on an efficient horizontal wingbeat to mostly generate lift, bats rely on lift and drag during the downstroke to fully support their body weight. Furthermore, whereas the ability of nectar bats to aerodynamically support their body weight during the upstroke is elevated, it is much smaller than that of hummingbirds. Bats compensate by generating more aerodynamic weight support during their extended downstroke. Although, in principle, it requires more aerodynamic power to hover using this method, bats have adapted by evolving much larger wings for their body weight. Therefore, the net aerodynamic induced power required to hover is similar among hummingbirds and bats per unit body mass. This mechanistic insight into how feathered wings and membrane wings ultimately require similar aerodynamic power to hover may inform analogous design trade-offs in aerial robots.

Automated calibration of multi-camera-projector structured light systems for volumetric high-speed 3D surface reconstructions.

It is challenging to calibrate multiple camera-projector pairs for multi-view 3D surface reconstruction based on structured light. Here, we present a new automated calibration method for high-speed multi-camera-projector systems. The method uses printed and projected dot patterns on a planar calibration target, which is moved by hand in the calibration volume. Calibration is enabled by automated image processing and bundle-adjusted parameter optimization. We determined the performance of our method by 3D reconstructing a sphere. The accuracy is -0.03 ± 0.09 % as a percentage of the diameter of the calibration volume. Applications include quality control, autonomous systems, engineering measurements, and motion capture, such as the preliminary 3D reconstruction of a bird in flight we present here.

Adaptive control of turbulence intensity is accelerated by frugal flow sampling.

The aerodynamic performance of vehicles and animals, as well as the productivity of turbines and energy harvesters, depends on the turbulence intensity of the incoming flow. Previous studies have pointed at the potential benefits of active closed-loop turbulence control. However, it is unclear what the minimal sensory and algorithmic requirements are for realizing this control. Here we show that very low-bandwidth anemometers record sufficient information for an adaptive control algorithm to converge quickly. Our online Newton-Raphson algorithm tunes the turbulence in a recirculating wind tunnel by taking readings from an anemometer in the test section. After starting at 9% turbulence intensity, the algorithm converges on values ranging from 10% to 45% in less than 12 iterations within 1% accuracy. By down-sampling our measurements, we show that very-low-bandwidth anemometers record sufficient information for convergence. Furthermore, down-sampling accelerates convergence by smoothing gradients in turbulence intensity. Our results explain why low-bandwidth anemometers in engineering and mechanoreceptors in biology may be sufficient for adaptive control of turbulence intensity. Finally, our analysis suggests that, if certain turbulent eddy sizes are more important to control than others, frugal adaptive control schemes can be particularly computationally effective for improving performance.

The biomechanical origin of extreme wing allometry in hummingbirds.

Flying animals of different masses vary widely in body proportions, but the functional implications of this variation are often unclear. We address this ambiguity by developing an integrative allometric approach, which we apply here to hummingbirds to examine how the physical environment, wing morphology and stroke kinematics have contributed to the evolution of their highly specialised flight. Surprisingly, hummingbirds maintain constant wing velocity despite an order of magnitude variation in body weight; increased weight is supported solely through disproportionate increases in wing area. Conversely, wing velocity increases with body weight within species, compensating for lower relative wing area in larger individuals. By comparing inter- and intraspecific allometries, we find that the extreme wing area allometry of hummingbirds is likely an adaptation to maintain constant burst flight capacity and induced power requirements with increasing weight. Selection for relatively large wings simultaneously maximises aerial performance and minimises flight costs, which are essential elements of humming bird life history.

How pigeons couple three-dimensional elbow and wrist motion to morph their wings.

Birds change the shape and area of their wings to an exceptional degree, surpassing insects, bats and aircraft in their ability to morph their wings for a variety of tasks. This morphing is governed by a musculoskeletal system, which couples elbow and wrist motion. Since the discovery of this effect in 1839, the planar 'drawing parallels' mechanism has been used to explain the coupling. Remarkably, this mechanism has never been corroborated from quantitative motion data. Therefore, we measured how the wing skeleton of a pigeon (Columba livia) moves during morphing. Despite earlier planar assumptions, we found that the skeletal motion paths are highly three-dimensional and do not lie in the anatomical plane, ruling out the 'drawing parallels' mechanism. Furthermore, micro-computed tomography scans in seven consecutive poses show how the two wrist bones contribute to morphing, particularly the sliding ulnare. From these data, we infer the joint types for all six bones that form the wing morphing mechanism and corroborate the most parsimonious mechanism based on least-squares error minimization. Remarkably, the algorithm shows that all optimal four-bar mechanisms either lock, are unable to track the highly three-dimensional bone motion paths, or require the radius and ulna to cross for accuracy, which is anatomically unrealistic. In contrast, the algorithm finds that a six-bar mechanism recreates the measured motion accurately with a parallel radius and ulna and a sliding ulnare. This revises our mechanistic understanding of how birds morph their wings, and offers quantitative inspiration for engineering morphing wings.

Design and analysis of aerodynamic force platforms for free flight studies.

We describe and explain new advancements in the design of the aerodynamic force platform, a novel instrument that can directly measure the aerodynamic forces generated by freely flying animals and robots. Such in vivo recordings are essential to better understand the precise aerodynamic function of flapping wings in nature, which can critically inform the design of new bioinspired robots. By designing the aerodynamic force platform to be stiff yet lightweight, the natural frequencies of all structural components can be made over five times greater than the frequencies of interest. The associated high-frequency noise can then be filtered out during post-processing to obtain accurate and precise force recordings. We illustrate these abilities by measuring the aerodynamic forces generated by a freely flying bird. The design principles can also be translated to other fluid media. This offers an opportunity to perform high-throughput, real-time, non-intrusive, and in vivo comparative biomechanical measurements of force generation by locomoting animals and robots. These recordings can include complex bimodal terrestrial, aquatic, and aerial behaviors, which will help advance the fields of experimental biology and bioinspired design.

How birds direct impulse to minimize the energetic cost of foraging flight.

Birds frequently hop and fly between tree branches to forage. To determine the mechanical energy trade-offs of their bimodal locomotion, we rewarded four Pacific parrotlets with a seed for flying voluntarily between instrumented perches inside a new aerodynamic force platform. By integrating direct measurements of both leg and wing forces with kinematics in a bimodal long jump and flight model, we discovered that parrotlets direct their leg impulse to minimize the mechanical energy needed to forage over different distances and inclinations. The bimodal locomotion model further shows how even a small lift contribution from a single proto-wingbeat would have significantly lengthened the long jump of foraging arboreal dinosaurs. These avian bimodal locomotion strategies can also help robots traverse cluttered environments more effectively.