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Modulation of Flight Muscle Recruitment and Wing Rotation Enables Hummingbirds to Mitigate Aerial Roll Perturbations

21 Pages Posted: 18 May 2019 Sneak Peek Status: Review Complete

See all articles by Sridhar Ravi

Sridhar Ravi

University of New South Wales (UNSW) - School of Engineering and Information Technology; Australian Defense Force Academy

Ryusuke Noda

Kanto Gakuin University - Department of Mechanical Engineering

Susan Gagliardi

University of California, Davis - Department of Neurobiology, Physiology and Behavior

Dmitry Kolomenskiy

Japan Agency for Marine-Earth (JAMSTEC)Science and Technology

Stacey Combes

University of California, Davis - Department of Neurobiology, Physiology and Behavior

Hao Liu

Chiba University - Graduate School of Engineering

Andrew Biewener

Harvard University - Department of Organismic and Evolutionary Biology

Nicolai Konow

University of Massachusetts Lowell - Department of Biological Sciences

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Abstract

Both biological and artificial fliers must contend with aerial perturbations that are ubiquitous in the outdoor environment. Flapping fliers are generally least stable, but also the most maneuverable in roll, yet roll control in biological fliers remains less well understood. Hummingbirds are suitable models for linking aerodynamic perturbations to flight control strategies, as these small, powerful fliers are capable of remaining airborne even in adverse airflows. We challenged hummingbirds to fly within a longitudinally oriented vortex that imposed a continuous roll perturbation, measured wing kinematics and neuromotor activation of the major flight muscles with synchronized high-speed video and electromyography and used computational fluid dynamics (CFD) to estimate the aerodynamic forces generated by wing motions. Hummingbirds responded to the perturbation using bilaterally different activation of the main flight muscles and maintained symmetry in most major aspects of wing motion including stroke amplitude, stroke plane angle, and flapping frequency. However, hummingbirds also displayed consistent bilateral differences in subtle wing kinematics traits, including wing rotation and elevation. CFD modeling implicate asymmetric responses in wing rotation as important for generating the necessary stabilizing torques, suggesting that intrinsic wing muscles play a critical role in aerodynamic control. The birds also augment flight stabilization by adjusting body and tail posture to expose greater surface area to upwash than to the undesirable downwash. Our results provide insight into the remarkable capacity of hummingbirds to maintain flight control and bio-inspiration for simple yet effective control strategies for robotic fliers to contend with unfamiliar and challenging real-word aerial conditions.

Keywords: Hummingbird flight, flight control, flapping flight, wing kinematics, neuromotor control

Suggested Citation

Ravi, Sridhar and Noda, Ryusuke and Gagliardi, Susan and Kolomenskiy, Dmitry and Combes, Stacey and Liu, Hao and Biewener, Andrew and Konow, Nicolai, Modulation of Flight Muscle Recruitment and Wing Rotation Enables Hummingbirds to Mitigate Aerial Roll Perturbations (May 16, 2019). CURRENT-BIOLOGY-D-19-00783. Available at SSRN: https://ssrn.com/abstract=3389378 or http://dx.doi.org/10.2139/ssrn.3389378
This is a paper under consideration at Cell Press and has not been peer-reviewed.

Sridhar Ravi

University of New South Wales (UNSW) - School of Engineering and Information Technology ( email )

Canberra
Australia

Australian Defense Force Academy ( email )

Canberra
Australia

Ryusuke Noda

Kanto Gakuin University - Department of Mechanical Engineering ( email )

Yokohama
Japan

Susan Gagliardi

University of California, Davis - Department of Neurobiology, Physiology and Behavior ( email )

United States

Dmitry Kolomenskiy

Japan Agency for Marine-Earth (JAMSTEC)Science and Technology ( email )

2-15, Natsushima-cho
Kanagawa, 237-0061
Japan

Stacey Combes

University of California, Davis - Department of Neurobiology, Physiology and Behavior ( email )

United States

Hao Liu

Chiba University - Graduate School of Engineering

1- 33, Yayoi-cho
Chiba, 263-8522
Japan

Andrew Biewener

Harvard University - Department of Organismic and Evolutionary Biology ( email )

1875 Cambridge Street
Cambridge, MA 02138
United States

Nicolai Konow (Contact Author)

University of Massachusetts Lowell - Department of Biological Sciences ( email )

Lowell, MA
United States

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