Optic flow stabilizes flight in ruby-throated hummingbirds

Flying birds rely on visual cues for retinal image stabilization by negating rotation-induced optic flow, the motion of the visual panorama across the retina, through corrective eye and head movements. In combination with vestibular and proprioceptive feedback, birds may also use visual cues to stabilize their body during flight. Here, we test whether artificially induced wide-field motion generated through projected visual patterns elicits maneuvers in body orientation and flight position, in addition to stabilizing vision. To test this hypothesis, we present hummingbirds flying freely within a 1.2 m cylindrical visual arena with a virtual surround rotated at different speeds about its vertical axis. The birds responded robustly to these visual perturbations by rotating their heads and bodies with the moving visual surround, and by adjusting their flight trajectories, following the surround. Thus, similar to insects, hummingbirds appear to use optic flow cues to control flight maneuvers as well as to stabilize their visual inputs

Fatigue Alters in Vivo Function Within and Between Limb Muscles During Locomotion

Muscle fatigue, a reduction in force as a consequence of exercise, is an important factor for any animal that moves, and can result from both peripheral and/or central mechanisms. Although much is known about whole-limb force generation and activation patterns in fatigued muscles under sustained isometric contractions, little is known about the in vivo dynamics of limb muscle function in relation to whole-body fatigue. Here we show that limb kinematics and contractile function in the lateral (LG) and medial (MG) gastrocnemius of helmeted guineafowl (Numida meleagris) are significantly altered following fatiguing exercise at 2 m sK1 on an inclined treadmill. The two most significant findings were that the variation in muscle force generation, measured directly from the muscles’ tendons, increased significantly with fatigue, and fascicle shortening in the proximal MG, but not the distal MG, decreased significantly with fatigue. We suggest that the former is a potential mechanism for decreased stability associated with fatigue. The region-specific alteration of fascicle behaviour within the MG as a result of fatigue suggests a complex response to fatigue that probably depends on muscle–aponeurosis and tendon architecture not previously explored. These findings highlight the importance of studying the integrative in vivo dynamics of muscle function in response to fatigue.Organismic and Evolutionary Biolog

Contractile properties of the pigeon supracoracoideus during different modes of flight

The supracoracoideus (SUPRA) is the primary upstroke muscle for avian flight and is the antagonist to the downstroke muscle, the pectoralis (PECT). We studied in vivo contractile properties and mechanical power output of both muscles during take-off, level and landing flight. We measured muscle length change and activation using sonomicrometry and electromyography, and muscle force development using strain recordings on the humerus. Our results support a hypothesis that the primary role of the SUPRA is to supinate the humerus. Antagonistic forces exerted by the SUPRA and PECT overlap during portions of the wingbeat cycle, thereby offering a potential mechanism for enhancing control of the wing. Among flight modes, muscle strain was approximately the same in the SUPRA (33–40%) and the PECT (35–42%), whereas peak muscle stress was higher in the SUPRA $(85–126 N m^{–2})$ than in the PECT $(50–58 N m^{–2})$. The SUPRA mainly shortened relative to resting length and the PECT mainly lengthened. We estimated that elastic energy storage in the tendon of the SUPRA contributed between 28 and 60% of the net work of the SUPRA and 6–10% of the total net mechanical work of both muscles. Mechanical power output in the SUPRA was congruent with the estimated inertial power required for upstroke, but power output from the PECT was only 42–46% of the estimated aerodynamic power requirements for flight. There was a significant effect of flight mode upon aspects of the contractile behavior of both muscles including strain, strain rate, peak stress, work and power.Organismic and Evolutionary BiologyOther Research Uni

Wing and Body Kinematics of Takeoff and Landing Flight in the Pigeon (Columba livia)

Takeoff and landing are critical phases in a flight. To better understand the functional importance of the kinematic adjustments birds use to execute these flight modes, we studied the wing and body movements of pigeons (Columba livia) during short-distance free-flights between two perches. The greatest accelerations were observed during the second wingbeat of takeoff. The wings were responsible for the majority of acceleration during takeoff and landing, with the legs contributing only one-quarter of the acceleration. Parameters relating to aerodynamic power output such as downstroke amplitude, wingbeat frequency and downstroke velocity were all greatest during takeoff flight and decreased with each successive takeoff wingbeat. This pattern indicates that downstroke velocity must be greater for accelerating flight to increase the amount of air accelerated by the wings. Pigeons used multiple mechanisms to adjust thrust and drag to accelerate during takeoff and decelerate during landing. Body angle, tail angle and wing plane angles all shifted from more horizontal orientations during takeoff to near-vertical orientations during landing, thereby reducing drag during takeoff and increasing drag during landing. The stroke plane was tilted steeply downward throughout takeoff (increasing from −60±5 deg. to −47±1 deg.), supporting our hypothesis that a downward-tilted stroke plane pushes more air rearward to accelerate the bird forward. Similarly, the stroke plane tilted upward during landing (increasing from −1±2 deg. to 17±7 deg.), implying that an upward-tilted stroke plane pushes more air forward to slow the bird down. Rotations of the stroke plane, wing planes and tail were all strongly correlated with rotation of the body angle, suggesting that pigeons are able to redirect aerodynamic force and shift between flight modes through modulation of body angle alone.Organismic and Evolutionary BiologyOther Research Uni

Muscle function during takeoff and landing flight in the pigeon (Columba livia)

This study explored the muscle strain and activation patterns of several key flight muscles of the pigeon (Columba livia) during takeoff and landing flight. Using electromyography (EMG) to measure muscle activation, and sonomicrometry to quantify muscle strain, we evaluated the muscle function patterns of the pectoralis, biceps, humerotriceps and scapulotriceps as pigeons flew between two perches. These recordings were analyzed in the context of three-dimensional wing kinematics. To understand the different requirements of takeoff, midflight and landing, we compared the activity and strain of these muscles among the three flight modes. The pectoralis and biceps exhibited greater fascicle strain rates during takeoff than during midflight or landing. However, the triceps muscles did not exhibit notable differences in strain among flight modes. All observed strain, activation and kinematics were consistent with hypothesized muscle functions. The biceps contracted to stabilize and flex the elbow during the downstroke. The humerotriceps contracted to extend the elbow at the upstroke-downstroke transition, followed by scapulotriceps contraction to maintain elbow extension during the downstroke. The scapulotriceps also appeared to contribute to humeral elevation. Greater muscle activation intensity was observed during takeoff, compared with mid-flight and landing, in all muscles except the scapulotriceps. The timing patterns of muscle activation and length change differed among flight modes, yet demonstrated that pigeons do not change the basic mechanical actions of key flight muscles as they shift from flight activities that demand energy production, such as takeoff and midflight, to maneuvers that require absorption of energy, such as landing. Similarly, joint kinematics were consistent among flight modes. The stereotypy of these neuromuscular and joint kinematic patterns is consistent with previously observed stereotypy of wing kinematics relative to the pigeon's body (in the local body frame) across these flight behaviors. Taken together, these observations suggest that the control of takeoff and landing flight primarily involves modulation of overall body pitch to effect changes in stroke plane angle and resulting wing aerodynamics.Organismic and Evolutionary Biolog

Muscle function in avian flight: achieving power and control

Flapping flight places strenuous requirements on the physiological performance of an animal. Bird flight muscles, particularly at smaller body sizes, generally contract at high frequencies and do substantial work in order to produce the aerodynamic power needed to support the animal's weight in the air and to overcome drag. This is in contrast to terrestrial locomotion, which offers mechanisms for minimizing energy losses associated with body movement combined with elastic energy savings to reduce the skeletal muscles' work requirements. Muscles also produce substantial power during swimming, but this is mainly to overcome body drag rather than to support the animal's weight. Here, I review the function and architecture of key flight muscles related to how these muscles contribute to producing the power required for flapping flight, how the muscles are recruited to control wing motion and how they are used in manoeuvring. An emergent property of the primary flight muscles, consistent with their need to produce considerable work by moving the wings through large excursions during each wing stroke, is that the pectoralis and supracoracoideus muscles shorten over a large fraction of their resting fibre length (33–42%). Both muscles are activated while being lengthened or undergoing nearly isometric force development, enhancing the work they perform during subsequent shortening. Two smaller muscles, the triceps and biceps, operate over a smaller range of contractile strains (12–23%), reflecting their role in controlling wing shape through elbow flexion and extension. Remarkably, pigeons adjust their wing stroke plane mainly via changes in whole-body pitch during take-off and landing, relative to level flight, allowing their wing muscles to operate with little change in activation timing, strain magnitude and pattern.Organismic and Evolutionary Biolog

Scaling of Terrestrial Support: Differing Solutions to Mechanical Constraints of Size

Terrestrial animals and plants span an enormous size range, and yet even distantly related groups are constructed of similar materials (e.g., bone, wood, muscle, and tendon). As with many physiological processes, evolutionary and ontogenetic changes in size impose constraints of scale on the mechanical design and function of skeletal support systems that are built of materials having similar properties. Adequate design requires that the capacity of skeletal elements (and muscles) for force transmission safely exceeds the levels required for biological support and movement. This is the case when the force transmitted per unit cross-sectional area of the material, defined as a mechanical stress (= F/,4, e.g., N/mm2), does not exceed the material's strength (the maximum stress that the material can withstand before faihrre). Clearly, larger structures can support larger forces more safely. The important design consideration, however, is whether changes in force requirements are matched by comparable changes in tissue cross-sectional area in order to keep maximal stresses and, thus, safety factors (defined as failure stress/peak functional stress) constant as size changes. Scale-invariant features (bone strength, timber strength, and peak muscle stress), therefore, require size-dependent changes in other features if the functional integrity of support systems is to be maintained over a broad size range (see also Li this volume). What are the features of terrestrial skeletal support systems that vary in a regular way with changes in size

Walking and Running in the Red-Legged Running Frog, Kassina Maculata

Although most frog species are specialized for jumping or swimming, Kassina maculata (red-legged running frog) primarily uses a third type of locomotion during which the hindlimbs alternate. In the present study, we examined Kassina\u27s distinct locomotory mode to determine whether these frogs walk or run and how their gait may change with speed. We used multiple methods to distinguish between terrestrial gaits: the existence or absence of an aerial phase, duty factor, relative footfall patterns and the mechanics of the animal\u27s center of mass (COM). To measure kinematic and kinetic variables, we recorded digital video as the animals moved over a miniature force platform (N=12 individuals). With respect to footfall patterns, the frogs used a single gait and walked at all speeds examined. Duty factor always exceeded 0.59. Based on COM mechanics, however, the frogs used both walking and running gaits. At slower speeds, the fluctuations in the horizontal kinetic energy (Ek) and gravitational potential energy (Ep) of the COM were largely out of phase, indicating a vaulting or walking gait. In most of the trials, Kassina used a combined gait at intermediate speeds, unlike cursorial animals with distinct gait transitions. This combined gait, much like a mammalian gallop, exhibited the mechanics of both vaulting and bouncing gaits. At faster speeds, the Ek and Ep of Kassina\u27s COM were more in phase, indicating the use of a bouncing or running gait. Depending on the definition used to distinguish between walking and running, Kassina either only used a walking gait at all speeds or used a walking gait at slower speeds but then switched to a running gait as speed increased

In Vivo muscle force-length behavior during steady-speed hopping in tammar wallabies

© The Company of BiologistsModerate to large macropodids can increase their speed while hopping with little or no increase in energy expenditure. This has been interpreted by some workers as resulting from elastic energy savings in their hindlimb tendons. For this to occur, the muscle fibers must transmit force to their tendons with little or no length change. To test whether this is the case, we made in vivo measurements of muscle fiber length change and tendon force in the lateral gastrocnemius (LG) and plantaris (PL) muscles of tammar wallabies Macropus eugenii as they hopped at different speeds on a treadmill. Muscle fiber length changes were less than +/-0.5 mm in the plantaris and +/-2.2 mm in the lateral gastrocnemius, representing less than 2 % of total fiber length in the plantaris and less than 6 % in the lateral gastrocnemius, with respect to resting length. The length changes of the plantaris fibers suggest that this occurred by means of elastic extension of attached cross-bridges. Much of the length change in the lateral gastrocnemius fibers occurred at low force early in the stance phase, with generally isometric behavior at higher forces. Fiber length changes did not vary significantly with increased hopping speed in either muscle (P>0.05), despite a 1. 6-fold increase in muscle-tendon force between speeds of 2.5 and 6.0 m s-1. Length changes of the PL fibers were only 7+/-4 % and of the LG fibers 34+/-12 % (mean +/- S.D., N=170) of the stretch calculated for their tendons, resulting in little net work by either muscle (plantaris 0.01+/-0.03 J; gastrocnemius -0.04+/-0.30 J; mean +/- s.d. ). In contrast, elastic strain energy stored in the tendons increased with increasing speed and averaged 20-fold greater than the shortening work performed by the two muscles. These results show that an increasing amount of strain energy stored within the hindlimb tendons is usefully recovered at faster steady hopping speeds, without being dissipated by increased stretch of the muscles' fibers. This finding supports the view that tendon elastic saving of energy is an important mechanism by which this species is able to hop at faster speeds with little or no increase in metabolic energy expenditure.Andrew A. Biewener, David D. Konieczynski and Russell V. Baudinett