Passive aeroelastic deflection of avian primary feathers.

Bird feathers are complex structures that passively deflect as they interact with air to produce aerodynamic force. Newtonian theory suggests that feathers should be stiff to effectively utilize this force. Observations of flying birds indicate that feathers respond to aerodynamic loading via spanwise bending, twisting, and sweeping. These deflections are hypothesized to optimize flight performance, but this has not yet been tested. We measured deflection of isolated feathers in a wind tunnel to explore how flexibility altered aerodynamic forces in emulated gliding flight. Using primary feathers from seven raptors and a rigid airfoil, we quantified bending, sweep, and twisting, as well as α (attack angle) and slip angle. We predicted that (1) feathers would deflect under aerodynamic load, (2) bending would result in lateral redirection of force, (3) twisting would alter spanwise α 'washout' and delay the onset of stall, and (4) flexural stiffness of feathers would exhibit positive allometry. The first three predictions were supported by our results, but not the fourth. We found that bending resulted in the redirection of lateral forces more toward the base of the feather on the order of ∼10% of total lift. In comparison to the airfoil which stalled at α = 13.5°, all feathers continued to increase lift production with increasing angle of attack to the limit of our range of measurements (α = 27.5°). We observed that feather stiffness exhibited positive allometry (∝ mass1.1±0.3), however this finding is not statistically different from other hypothesized scaling relationships such as geometric similarity (∝ mass1.67). These results demonstrate that feather flexibility may provide passive roll stability and delay stall by twisting to reduce local α at the feather tip. Our findings are the first to measure forces due to feather deflection under aerodynamic loading and can inform future models of avian flight as well as biomimetic morphing-wing technology.

Development of locomotion over inclined surfaces in laying hens.

The purpose of the present study was to evaluate locomotor strategies during development in domestic chickens (Gallus gallus domesticus); we were motivated, in part, by current efforts to improve the design of housing systems for laying hens which aim to reduce injury and over-exertion. Using four strains of laying hens (Lohmann Brown, Lohmann LSL lite, Dekalb White and Hyline Brown) throughout this longitudinal study, we investigated their locomotor style and climbing capacity in relation to the degree (0 to 70°) of incline, age (2 to 36 weeks) and the surface substrate (sandpaper or wire grid). Chicks and adult fowl performed only walking behavior to climb inclines ⩽40° and performed a combination of wing-assisted incline running (WAIR) or aerial ascent on steeper inclines. Fewer birds used their wings to aid their hind limbs when climbing 50° inclines on wire grid surface compared with sandpaper. The steepness of angle achieved during WAIR and the tendency to fly instead of using WAIR increased with increasing age and experience. White-feathered strains performed more wing-associated locomotor behavior compared with brown-feathered strains. A subset of birds was never able to climb incline angles >40° even when using WAIR. Therefore, we suggest that inclines of up to 40° should be provided for hens in three-dimensional housing systems, which are easily negotiated (without wing use) by chicks and adult fowl.

Neuromuscular control and kinematics of intermittent flight in the European starling (Sturnus vulgaris)

Electromyographic (EMG) and kinematic data were collected from European starlings (Sturnus vulgaris) flying at a range of speeds from 8 to 18 m s-1 in a variable-speed windtunnel. Their flight at all speeds consisted of alternating flapping and non-flapping phases. Wing postures during non-flapping phases included glides, partial-bounds and bounds. Glides were performed proportionally more often within each speed and were longer in duration than either of the other two non-flapping postures, but the percentage of bounds increased markedly with increasing flight speed. The shift from flap-gliding at slow speeds towards flap-bounding at fast speeds was consistent with reducing mean power output relative to continuous flapping. The starlings often combined more than one non-flapping posture within a single non-flapping period. Transitions between non-flapping postures, as well as transitions between bounds and subsequent flapping, were classified as 'pull-outs'. Pull-outs consisted of an increase in wingspan but no change in wingtip elevation. The pectoralis and supracoracoideus exhibited electrical activity during glides but not during bounds. The scapulohumeralis caudalis was not active during glides, but this muscle and the supracoracoideus were typically active during partial-bounds and pull-out phases. The scapulohumeralis caudalis occasionally showed activity during bounds, which may reflect its role as a humeral retractor. The frequency and duration of non-flapping intervals in starlings were less during EMG experiments than during non-implanted flights. During flapping phases, relative intensity and duration of EMG signal and wingbeat frequency increased with flight speed, whereas flapping or non-flapping cycle duration, the percentage of a cycle spent flapping and the number of wingbeats in a cycle were all greatest at 8 m s-1. Wingbeat amplitude was smaller at intermediate speeds, but differences among speeds were not significant. These variables allowed indirect estimates of power output and suggested that minimum power speed for starlings was near 12 m s-1 and that power output increased at both slower and faster speeds. Within windtunnel speeds, muscle activity changed in relation to wingspan at mid-upstroke, wingtip excursion, wingbeat frequency, acceleration, velocity, altitude and horizontal position.

NEUROMUSCULAR CONTROL AND KINEMATICS OF INTERMITTENT FLIGHT IN BUDGERIGARS (MELOPSITTACUS UNDULATUS)

Kinematic and electromyographic data were collected from budgerigars (parakeets), Melopsittacus undulatus, flying at different speeds in a variable-speed wind tunnel. Birds exhibited flap-gliding at low speeds and flap-bounding at high speeds. The percentage of time spent flapping generally decreased at intermediate speeds. These behavior patterns are consistent with minimizing energy expenditure according to aerodynamic theory. During intermittent glides, the pectoralis exhibited an isometric contraction while the supracoracoideus was inactive. During bounds, both muscles were inactive. Contrary to earlier work, our studies indicate that budgerigars do not exhibit simultaneous twitch contractions of the pectoralis during each wingbeat, but rather generate typical multiple-spike electromyographic bursts that represent motor unit action potential trains or asynchronous twitch contractions from different motor units. The relative intensity of electromyographic bursts from the primary flight muscles increased with flight speed. This may indicate an increase in force production. Our observations of isometric contractions during glides, along with patterns of variation in muscle activity and wingbeat frequency, do not support the hypothesis that small birds such as the budgerigar use flap-bounding as their only means of reducing power output during flight.

Flight kinematics of black-billed magpies and pigeons over a wide range of speeds

To investigate how birds that differ in morphology change their wing and body movements while flying at a range of speeds, we analyzed high-speed (60 Hz) video tapes of black-billed magpies (Pica pica) flying at speeds of 4-14 m s-1 and pigeons (Columba livia) flying at 6-20 m s-1 in a wind-tunnel. Pigeons had higher wing loading and higher-aspect-ratio wings compared with magpies. Both species alternated phases of steady-speed flight with phases of acceleration and deceleration, particularly at intermediate flight speeds. The birds modulated their wingbeat kinematics among these phases and frequently exhibited non-flapping phases while decelerating. Such modulation in kinematics during forward flight is typical of magpies but not of pigeons in the wild. The behavior of the pigeons may have been a response to the reduced power costs for flight in the closed wind-tunnel relative to those for free flight at similar speeds. During steady-speed flight, wingbeat frequency did not change appreciably with increasing flight speed. Body angle relative to the horizontal, the stroke-plane angles of the wingtip and wrist relative to the horizontal and the angle describing tail spread at mid-downstroke all decreased with increasing flight speed, thereby illustrating a shift in the dominant function of wing flapping from weight support at slow speeds to positive thrust at fast speeds. Using wingbeat kinematics to infer lift production, it appeared that magpies used a vortex-ring gait during steady-speed flight at all speeds whereas pigeons used a vortex-ring gait at 6 and 8 m s-1, a transitional vortex-ring gait at 10 m s-1, and a continuous-vortex gait at faster speeds. Both species used a vortex-ring gait for acceleration and a continuous-vortex gait or a non-flapping phase for deceleration during flight at intermediate wind-tunnel speeds. Pigeons progressively flexed their wings during glides as flight speed increased but never performed bounds. Wingspan during glides in magpies did not vary with flight speed, but the percentage of bounds among non-flapping intervals increased with speed from 10 to 14 m s-1. The use of non-flapping wing postures seemed to be related to the gaits used during flapping and to the aspect ratio of the wings. We develop an 'adverse-scaling' hypothesis in which it is proposed that the ability to reduce metabolic and mechanical power output using flap-bounding flight at fast flight speeds is scaled negatively with body mass. This represents an alternative to the 'fixed-gear' hypothesis previously suggested by other authors to explain the use of intermittent flight in birds. Future comparative studies in the field would be worthwhile, especially if instantaneous flight speeds and within-wingbeat kinematics were documented; new studies in the laboratory should involve simultaneous recording of wing kinematics and aerodynamic forces on the wing.

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.

Effects of body size on take-off flight performance in the Phasianidae (Aves).

To evaluate the mechanisms responsible for relationships between body mass and maximum take-off performance in birds, we studied four species in the Phasianidae: northern bobwhite (Colinus virginianus), chukar (Alectoris chukar), ring-necked pheasant (Phasianus colchicus) and wild turkey (Meleagris gallopavo). These species vary in body mass from 0.2 to 5.3 kg, and they use flight almost solely to escape predators. During take-off, all the species used a similar wingbeat style that appeared to be a vortex-ring gait with a tip reversal during the upstroke. The tip reversal is unusual for birds with rounded wings; it may offer an aerodynamic advantage during rapid acceleration. Flight anatomy generally scaled geometrically, except for average wing chord and wing area, which increased more than expected as body mass (m) increased. Pectoralis strain varied from 19.1 to 35.2 % and scaled in proportion to m(0.23). This positive scaling is not consistent with the widely held assumption that muscle strain is independent of body mass among geometrically similar species. The anatomy of the species precluded measurements of in vivo pectoralis force using the strain-gauge technique that has been employed successfully in other bird species, so we could not directly test in vivo pectoralis force-velocity relationships. However, whole-body kinematics revealed that take-off power (P(ta)), the excess power available for climbing and accelerating in flight, scaled in proportion to m(0.75) and that pectoralis mass-specific P(ta) decreased in proportion to m(-)(0.26) and was directly proportional to wingbeat frequency. These trends suggest that mass-specific pectoralis work did not vary with body mass and that pectoralis stress and strain were inversely proportional, as expected from classical force-velocity models for skeletal muscle. Our observations of P(ta) were consistent with evidence from other species engaged in escape flight and, therefore, appear to contradict evidence from studies of take-off or hovering with an added payload.

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.

Comparative power curves in bird flight.

The relationship between mechanical power output and forward velocity in bird flight is controversial, bearing on the comparative physiology and ecology of locomotion. Applied to flying birds, aerodynamic theory predicts that mechanical power should vary as a function of forward velocity in a U-shaped curve. The only empirical test of this theory, using the black-billed magpie (Pica pica), suggests that the mechanical power curve is relatively flat over intermediate velocities. Here, by integrating in vivo measurements of pectoralis force and length change with quasi-steady aerodynamic models developed using data on wing and body movement, we present mechanical power curves for cockatiels (Nymphicus hollandicus) and ringed turtle-doves (Streptopelia risoria). In contrast to the curve reported for magpies, the power curve for cockatiels is acutely concave, whereas that for doves is intermediate in shape and shows higher mass-specific power output at most speeds. We also find that wing-beat frequency and mechanical power output do not necessarily share minima in flying birds. Thus, aspects of morphology, wing kinematics and overall style of flight can greatly affect the magnitude and shape of a species' power curve.