Bird flight takes various forms in nature from gliding to hovering. While flying, birds must be agile enough to maneuver around obstacles and avoid predators, yet stable enough to navigate along an controlled path. To better understand maneuvering in complex environments, I looked to an extreme—hummingbirds. Hummingbirds represent the pinnacle of avian maneuverability. In addition to being the only bird capable of continuous hovering, they also hold the fastest recorded length-specific speeds of any animal and can sustain accelerations of up to nine times the acceleration of gravity. Hummingbirds must maneuver with great accuracy to feed on the nectar of flowers, and they must navigate between trees and branches and into and out of dense vegetation as they pursue arthropods, nest, or evade predators. They also perform these tasks in changing and windy conditions, which can impose simultaneous demands on their flight system. In Chapter 1 of this thesis I investigate how hummingbirds maneuver through narrow constrictions, which represent the most difficult and constraining aspect of flight through vegetation. In Chapter 2 I report how they minimize the perturbing effects of wind gusts. Finally, in Chapter 3 I describe novel maneuvering strategies that hummingbirds display when simultaneously confronted with high winds and narrow constrictions.

Chapter 1:

Many birds routinely fly fast through dense vegetation characterized by variably sized structures and voids. I show that Anna's Hummingbirds (Calypte anna) can negotiate structural constrictions less than one wingspan in diameter using a previously undescribed sideways maneuver coupled with bilaterally asymmetric wing motions. Crucially, this maneuver allows hummingbirds to continue flapping as they negotiate the constriction. By contrast, much smaller openings are negotiated via a faster ballistic trajectory characterized by tucked and thus non-flapping wings, which reduces force production and increases descent rate relative to the asymmetric technique. Hummingbirds progressively shift to the symmetric method as they perform hundreds of consecutive transits, suggesting increased locomotor performance with task familiarity. Initial use of asymmetric transit may allow birds to better assess upcoming obstacles and voids, thereby reducing the likelihood of subsequent collisions. This switching strategy to aperture transit may determine the limits of flight performance within structurally complex environments and will inform design efforts for small aerial vehicles intended for flight within vegetation.

Chapter 2:

Airflows near Earth's surface are highly dynamic over many spatial and temporal scales. To successfully negotiate these environments, flying organisms must mitigate aerodynamic perturbations and quickly return to their desired flight trajectories. Airborne animals maintain body orientation either by altering aerodynamic forces or shifting angular momentum from the body to appendages and other structures, such as the tail, but how these techniques enable birds to reject aerodynamic perturbations has not been well characterized. To better understand how hummingbirds modify wing and tail motions in response to individual gusts, I recorded Anna's Hummingbirds as they negotiated an upward jet of fast moving air using high-speed video. Birds exhibited large variation in wing elevation, tail pitch, and tail fan angles among trials as they repeatedly negotiated the same gust, and exhibited a dramatic decrease in body angle (27 +- 16 degrees) post-transit. Birds reached a minimum body angle and began to pitch up from this nose dive about 55 ms after leaving the gust. After extracting three-dimensional kinematic features, I identified two distinct control strategies for gust transit, one involving continuous flapping and little disruption to body angle (20 +- 13 degrees downward pitch), and the other characterized by wing holding, tail fanning and 13% faster transit, albeit with greater changes in body angle (46 +- 6 degrees downward pitch). The use of a deflectable tail on a glider model transiting the same gust resulted in enhanced stability and could easily be implemented in design of aerial robots.

Chapter 3:

Hummingbirds face many environmental challenges during flight such as wind, rain, and constrictions formed by vegetation. Movement through the natural world often presents these challenges simultaneously. Whereas we know in part how hummingbirds confront individual challenges, we do not understand how they manage multiple constraints at once. In these situations, birds could use a combination of the same compensatory behaviors---such as adjustments to wing and body kinematics---that they use to overcome individual challenges. Alternatively, I hypothesized that novel behaviors would emerge when birds are confronted with simultaneous constraints for which compensatory behaviors are in conflict. To assess responses to multiple locomotor challenges, I measured behavior and kinematics of hummingbirds flying through a circular constriction in a wind tunnel with either a headwind or a tailwind. I compared these measurements with compensatory behaviors previously observed for wind or constrictions in isolation and determined that birds use a combination of pre-existing behaviors and also develop novel behaviors when faced with simultaneous aperture and wind constraints. One novel behavior I observed in upstream transits was a precisely timed longitudinal shift in the position of the stroke plane. This shift allowed the wings to continue flapping throughout transit and to produce enough forward thrust to offset drag. If implemented in flapping wing robots, such an additional degree of freedom could improve their ability to negotiate simultaneous challenges in complex environments. These novel behaviors suggest that hummingbirds do not have a prescribed set of responses to a known list of expected environments, but instead may adapt novel wing kinematics on-the-fly when encountering to complex environments.