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.

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.

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.

In vivo recording of aerodynamic force with an aerodynamic force platform: from drones to birds.

Flapping wings enable flying animals and biomimetic robots to generate elevated aerodynamic forces. Measurements that demonstrate this capability are based on experiments with tethered robots and animals, and indirect force calculations based on measured kinematics or airflow during free flight. Remarkably, there exists no method to measure these forces directly during free flight. Such in vivo recordings in freely behaving animals are essential to better understand the precise aerodynamic function of their flapping wings, in particular during the downstroke versus upstroke. Here, we demonstrate a new aerodynamic force platform (AFP) for non-intrusive aerodynamic force measurement in freely flying animals and robots. The platform encloses the animal or object that generates fluid force with a physical control surface, which mechanically integrates the net aerodynamic force that is transferred to the earth. Using a straightforward analytical solution of the Navier-Stokes equation, we verified that the method is accurate. We subsequently validated the method with a quadcopter that is suspended in the AFP and generates unsteady thrust profiles. These independent measurements confirm that the AFP is indeed accurate. We demonstrate the effectiveness of the AFP by studying aerodynamic weight support of a freely flying bird in vivo. These measurements confirm earlier findings based on kinematics and flow measurements, which suggest that the avian downstroke, not the upstroke, is primarily responsible for body weight support during take-off and landing.