Hummingbirds rapidly respond to the removal of visible light and control a sequence of rate-commanded escape manoeuvres in milliseconds

Hummingbirds routinely execute a variety of stunning aerobatic feats, which continue to challenge current notions of aerial agility and controlled stability in biological systems. Indeed, the control of these amazing manoeuvres is not well understood. Here, we examined how hummingbirds control a sequence of manoeuvres within milliseconds, and tested whether and when they use vision during this rapid process. We repeatedly elicited escape flights in calliope hummingbirds, removed visible light during each manoeuvre at various instants and quantified their flight kinematics and responses. We show that the escape manoeuvres were composed of rapidly controlled sequential modules including evasion, reorientation, nose-down dive, forward flight and nose-up to hover. The hummingbirds did not respond to the light removal during evasion and reorientation until a critical light-removal time; afterwards, they showed two categories of luminance-based responses that rapidly altered manoeuvring modules to terminate the escape. We also show that hummingbird manoeuvres were rate-commanded and required no active braking (i.e. their body angular velocities were proportional to the change of wing motion patterns, a trait that probably alleviates the computational demand on flight control). This work uncovers key traits of hummingbird agility, which can also inform and inspire designs for next-generation agile aerial systems.