Bret W. Tobalske

Aerodynamics of the Hovering Hummingbird

Despite profound musculoskeletal differences, hummingbirds (Trochilidae) are widely thought to employ aerodynamic mechanisms similar to those used by insects. The kinematic symmetry of the hummingbird upstroke and downstroke has led to the assumption that these halves of the wingbeat cycle contribute equally to weight support during hovering, as exhibited by insects of similar size. This assumption has been applied, either explicitly or implicitly, in widely used aerodynamic models and in a variety of empirical tests. Here we provide measurements of the wake of hovering rufous hummingbirds (Selasphorus rufus) obtained with digital particle image velocimetry that show force asymmetry: hummingbirds produce 75% of their weight support during the downstroke and only 25% during the upstroke. Some of this asymmetry is probably due to inversion of their cambered wings during upstroke. The wake of hummingbird wings also reveals evidence of leading-edge vortices created during the downstroke, indicating that they may operate at Reynolds numbers sufficiently low to exploit a key mechanism typical of insect hovering. Hummingbird hovering approaches that of insects, yet remains distinct because of effects resulting from an inherently dissimilar—avian—body plan.

Biomechanics of bird flight

SUMMARY Power output is a unifying theme for bird flight and considerable progress has been accomplished recently in measuring muscular, metabolic and aerodynamic power in birds. The primary flight muscles of birds, the pectoralis and supracoracoideus, are designed for work and power output, with large stress (force per unit cross-sectional area) and strain (relative length change) per contraction. U-shaped curves describe how mechanical power output varies with flight speed, but the specific shapes and characteristic speeds of these curves differ according to morphology and flight style. New measures of induced, profile and parasite power should help to update existing mathematical models of flight. In turn, these improved models may serve to test behavioral and ecological processes. Unlike terrestrial locomotion that is generally characterized by discrete gaits, changes in wing kinematics and aerodynamics across flight speeds are gradual. Take-off flight performance scales with body size, but fully revealing the mechanisms responsible for this pattern awaits new study. Intermittent flight appears to reduce the power cost for flight, as some species flap–glide at slow speeds and flap–bound at fast speeds. It is vital to test the metabolic costs of intermittent flight to understand why some birds use intermittent bounds during slow flight. Maneuvering and stability are critical for flying birds, and design for maneuvering may impinge upon other aspects of flight performance. The tail contributes to lift and drag; it is also integral to maneuvering and stability. Recent studies have revealed that maneuvers are typically initiated during downstroke and involve bilateral asymmetry of force production in the pectoralis. Future study of maneuvering and stability should measure inertial and aerodynamic forces. It is critical for continued progress into the biomechanics of bird flight that experimental designs are developed in an ecological and evolutionary context.

Mechanical power output of bird flight

Aerodynamic theory predicts that the power required for an animal to fly over a range of speeds is represented by a ‘U’-shaped curve, with the greatest power required at the slowest and fastest speeds, and minimum power at an intermediate speed. Tests of these predictions, based on oxygen consumption measurements of metabolic power in birds and insects, support a different interpretation, generating either flat or ‘J’-shaped power profiles, implying little additional demand between hovering and intermediate flight speeds. However, respirometric techniques represent only an indirect assessment of the mechanical power requirements of flight and no previous avian study has investigated an animals full range of attainable level flight speeds. Here we present data from in vivo bone-strain measurements of pectoralis muscle force coupled with wing kinematics in black-billed magpies (Pica pica ), which we use to calculate mechanical power directly. As these birds flew over their full range of speeds, we offer a complete profile of mechanical power output during level flapping flight for this species. Values of mechanical power output are statistically indistinguishable (that is, the power curve is flat) over most forward-flight speeds but are significantly higher during hovering and flight at very low speeds.

Lift production in the hovering hummingbird

Aerodynamic theory and empirical observations of animals flying at similar Reynolds numbers (Re) predict that airflow over hummingbird wings will be dominated by a stable, attached leading edge vortex (LEV). In insects exhibiting similar kinematics, when the translational movement of the wing ceases (as at the end of the downstroke), the LEV is shed and lift production decreases until the energy of the LEV is re-captured in the subsequent half-cycle translation. We here show that while the hummingbird wing is strongly influenced by similar sharp-leading-edge aerodynamics, leading edge vorticity is inconsistent, varying from 0.7 to 26 per cent (mean 16%) of total lift production, is always generated within 3 mm of the dorsal surface of the wing, showing no retrograde (trailing to leading edge) flow, and does not increase from proximal to distal wing as would be expected with a conical vortex (class III LEV) described for hawkmoths. Further, the bound circulation is not shed as a vortex at the end of translation, but instead remains attached and persists after translation has ceased, augmented by the rotation (pronation, supination) of the wing that occurs between the wing-translation half-cycles. The result is a near-continuous lift production through wing turn-around, previously unknown in vertebrates, able to contribute to weight support as well as stability and control during hovering. Selection for a planform suited to creating this unique flow and nearly-uninterrupted lift production throughout the wingbeat cycle may help explain the relatively narrow hummingbird wing.

How cockatiels (Nymphicus hollandicus) modulate pectoralis power output across flight speeds.

SUMMARY The avian pectoralis muscle must produce a varying mechanical power output to achieve flight across a range of speeds (1-13 m s-1). We used the natural variation in the power requirements with flight speed to investigate the mechanisms employed by cockatiels (Nymphicus hollandicus) to modulate muscle power output. We found that pectoralis contractile function in cockatiels was generally conserved across speed and over a wide range of aerodynamic power requirements. Despite the 2-fold range of variation in muscle power output, many aspects of muscle performance varied little: duration of muscle shortening was invariant, and overall wingbeat frequency and muscle strain varied to a lesser degree (1.2-fold and 1.4-fold, respectively) than muscle power or work. Power output was primarily modulated by muscle force (accounting for 65% of the variation) rather than by muscle strain, cycle frequency or changes in the timing of force production relative to muscle strain. Strain rate and electromyogram (EMG) results suggest that the additional force was provided via increasing pectoralis recruitment. Due to their effect on the transformation of muscle work into useful aerodynamic work, changes in wing position and orientation during the downstroke probably also affect the magnitude of muscle force developed for a given level of motor recruitment. Analysis of the variation in muscle force and airflow over the wing suggests that the coefficients of lift and drag of the wing vary 4-fold over the speed range examined in this study.

Take-off mechanics in hummingbirds (Trochilidae).

SUMMARY Initiating flight is challenging, and considerable effort has focused on understanding the energetics and aerodynamics of take-off for both machines and animals. For animal flight, the available evidence suggests that birds maximize their initial flight velocity using leg thrust rather than wing flapping. The smallest birds, hummingbirds (Order Apodiformes), are unique in their ability to perform sustained hovering but have proportionally small hindlimbs that could hinder generation of high leg thrust. Understanding the take-off flight of hummingbirds can provide novel insight into the take-off mechanics that will be required for micro-air vehicles. During take-off by hummingbirds, we measured hindlimb forces on a perch mounted with strain gauges and filmed wingbeat kinematics with high-speed video. Whereas other birds obtain 80–90% of their initial flight velocity using leg thrust, the leg contribution in hummingbirds was 59% during autonomous take-off. Unlike other species, hummingbirds beat their wings several times as they thrust using their hindlimbs. In a phylogenetic context, our results show that reduced body and hindlimb size in hummingbirds limits their peak acceleration during leg thrust and, ultimately, their take-off velocity. Previously, the influence of motivational state on take-off flight performance has not been investigated for any one organism. We studied the full range of motivational states by testing performance as the birds took off: (1) to initiate flight autonomously, (2) to escape a startling stimulus or (3) to aggressively chase a conspecific away from a feeder. Motivation affected performance. Escape and aggressive take-off featured decreased hindlimb contribution (46% and 47%, respectively) and increased flight velocity. When escaping, hummingbirds foreshortened their body movement prior to onset of leg thrust and began beating their wings earlier and at higher frequency. Thus, hummingbirds are capable of modulating their leg and wingbeat kinetics to increase take-off velocity.

Aerodynamics of wing-assisted incline running in birds

SUMMARY Wing-assisted incline running (WAIR) is a form of locomotion in which a bird flaps its wings to aid its hindlimbs in climbing a slope. WAIR is used for escape in ground birds, and the ontogeny of this behavior in precocial birds has been suggested to represent a model analogous to transitional adaptive states during the evolution of powered avian flight. To begin to reveal the aerodynamics of flap-running, we used digital particle image velocimetry (DPIV) and measured air velocity, vorticity, circulation and added mass in the wake of chukar partridge Alectoris chukar as they engaged in WAIR (incline 65–85°; N=7 birds) and ascending flight (85°, N=2). To estimate lift and impulse, we coupled our DPIV data with three-dimensional wing kinematics from a companion study. The ontogeny of lift production was evaluated using three age classes: baby birds incapable of flight [6–8 days post hatching (d.p.h.)] and volant juveniles (25–28 days) and adults (45+ days). All three age classes of birds, including baby birds with partially emerged, symmetrical wing feathers, generated circulation with their wings and exhibited a wake structure that consisted of discrete vortex rings shed once per downstroke. Impulse of the vortex rings during WAIR was directed 45±5° relative to horizontal and 21±4° relative to the substrate. Absolute values of circulation in vortex cores and induced velocity increased with increasing age. Normalized circulation was similar among all ages in WAIR but 67% greater in adults during flight compared with flap-running. Estimated lift during WAIR was 6.6% of body weight in babies and between 63 and 86% of body weight in juveniles and adults. During flight, average lift was 110% of body weight. Our results reveal for the first time that lift from the wings, rather than wing inertia or profile drag, is primarily responsible for accelerating the body toward the substrate during WAIR, and that partially developed wings, not yet capable of flight, can produce useful lift during WAIR. We predict that neuromuscular control or power output, rather than external wing morphology, constrain the onset of flight ability during development in birds.

Flight style of the black-billed magpie: Variation in wing kinematics, neuromuscular control, and muscle composition

Black-billed magpies (Pica pica; Corvidae) exhibit an unusual flight style with pronounced, cyclic variation in wingbeat frequency and amplitude during level, cruising flight. In an effort to better understand the underlying internal mechanisms associated with this flight style, we studied muscle activity patterns, fiber composition of the pectoralis muscle, and wingbeat kinematics using both laboratory and field techniques. Over a wide range of speeds in a windtunnel (0-13.4 m s-1), wingbeat frequency, wingtip elevation, and relative intensity of electromyographic (EMG) signals s-1 from the flight muscles were least at intermediate speeds, and increased at both slower and faster speeds, in approximate agreement with theoretical models that predict a U-shaped curve of power output with flight speed. Considerable variation was evident in kinematic and electromyographic variables, but variation was continuous, and, thus, was not adequately described by the simple two-gait system which is currently accepted as describing gait selection during vertebrate flight. Indirect evidence suggests that magpies vary their flight style consistent with reducing average power costs in comparison to costs associated with continuous flapping at a fixed level of power per wingbeat. The range of variation for the kinematic variables was similar in the field and lab; however, in the field, proportionally fewer flights showed significant correlations between wingbeat frequency and the other variables. Average flight speed in the field was 8.0 m s-1. Average wingbeat frequency was less in the field than in the windtunnel, but mean values for wingtip elevation and wingspan at midupstroke were not significantly different. Histological study revealed that the pectoralis muscle of magpies contained only fast-twitch (acid-stable) muscle fibers, which were classified as red (R) and intermediate (I) based on oxidative and glycolytic capacities along with fiber diameter. This fiber composition may be related to variation in wingbeat kinematics, but such composition is found in the pectoralis of other bird species. This suggests that the muscle fibers commonly found in the pectoralis of small to medium sized birds are capable of a wider range of efficient contractile velocities than predicted by existing theory. Future studies should explore alternative explanations for variation in wingbeat kinematics, including the potential role of nonverbal communication among cospecifics.

Biomechanics and physiology of gait selection in flying birds.

Two wing‐beat gaits, distinguished by the presence or absence of lift production during the upstroke, are currently used to describe avian flight. Vortex‐visualization studies indicate that lift is produced only during the downstroke in the vortex‐ring gait and that lift is produced continuously in the continuous‐vortex gait. Tip‐reversal and feathered upstrokes represent different forms of vortex‐ring gait distinguished by wing kinematics. Useful aerodynamic forces may be produced during tip‐reversal upstroke in slow flight and during a feathered upstroke in fast flight, but it is probable that downstroke forces are much greater in magnitude. Uncertainty about the function of these types of upstroke may be resolved when more data are available on wake structure in different flight speeds and modes. Inferring from wing kinematics and available data on wake structure, birds with long wings or wings of high aspect ratio use a vortex‐ring gait with tip‐reversal upstroke at slow speeds, a vortex‐ring gait with a feathered upstroke at intermediate speeds, and a continuous‐vortex gait at fast speeds. Birds with short wings or wings of low aspect ratio use a vortex‐ring gait with a feathered upstroke at all speeds. Regardless of wing shape, species tend to use a vortex‐ring gait for acceleration and a continuous‐vortex gait for deceleration. Some correlations may exist between gait selection and the function of the muscular and respiratory system. However, overall variation in wing kinematics, muscle activity, and respiratory activity is continuous rather than categorical. To further our understanding of gait selection in flying birds, it is important to test whether upstroke function varies in a similar manner. Transitions between lifting and nonlifting upstrokes may be more subtle and gradual than implied by a binomial scheme of classification.

Morphological and kinematic basis of the hummingbird flight stroke: scaling of flight muscle transmission ratio

Hummingbirds (Trochilidae) are widely known for their insect-like flight strokes characterized by high wing beat frequency, small muscle strains and a highly supinated wing orientation during upstroke that allows for lift production in both halves of the stroke cycle. Here, we show that hummingbirds achieve these functional traits within the limits imposed by a vertebrate endoskeleton and muscle physiology by accentuating a wing inversion mechanism found in other birds and using long-axis rotational movement of the humerus. In hummingbirds, long-axis rotation of the humerus creates additional wing translational movement, supplementing that produced by the humeral elevation and depression movements of a typical avian flight stroke. This adaptation increases the wing-to-muscle-transmission ratio, and is emblematic of a widespread scaling trend among flying animals whereby wing-to-muscle-transmission ratio varies inversely with mass, allowing animals of vastly different sizes to accommodate aerodynamic, biomechanical and physiological constraints on muscle-powered flapping flight.