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

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

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

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

Modulation of proximal muscle function during level versus incline hopping in tammar wallabies (Macropus eugenii)

Copyright © 2007 The Company of Biologists LtdWe examined the functional role of two major proximal leg extensor muscles of tammar wallabies during level and inclined hopping (12°, 21.3% grade). Previous in vivo studies of hopping wallabies have revealed that, unlike certain avian bipeds, distal hindlimb muscles do not alter their force–length behavior to contribute positive work during incline hopping. This suggests that proximal muscles produce the increased mechanical work associated with moving up an incline. Based on relative size and architectural anatomy, we hypothesized that the biceps femoris (BF), primarily a hip extensor, and the vastus lateralis (VL), the main knee extensor, would exhibit changes in muscle strain and activation patterns consistent with increased work production during incline versus level hopping. Our results clearly support this hypothesis. The BF experienced similar activation patterns during level and incline hopping but net fascicle shortening increased (–0.5% for level hopping versus –4.2% for incline hopping) during stance when the muscle likely generated force. Unlike the BF, the VL experienced active net lengthening during stance, indicating that it absorbs energy during both level and incline hopping. However, during incline hopping, net lengthening was reduced (8.3% for level hopping versus 3.9% for incline hopping), suggesting that the amount of energy absorbed by the VL was reduced. Consequently, the changes in contractile behavior of these two muscles are consistent with a net production of work by the whole limb. A subsidiary aim of our study was to explore possible regional variation within the VL. Although there was slightly higher fascicle strain in the proximal VL compared with the distal VL, regional differences in strain were not significant, suggesting that the overall pattern of in vivo strain is fairly uniform throughout the muscle. Estimates of muscle work based on inverse dynamics calculations support the conclusion that both the BF and VL contribute to the additional work required for incline hopping. However, on a muscle mass-specific basis, these two muscles appear to contribute less than their share. This indicates that other hindlimb muscles, or possibly trunk and back muscles, must contribute substantial work during incline hopping.C. P. McGowan, R. V. Baudinette and A. A. Biewene

Joint work and power associated with acceleration and deceleration in tammar wallabies (Macropus eugenii)

Copyright © 2005 The Company of BiologistsMeasurements of joint work and power were determined using inverse dynamics analysis based on ground reaction force and high-speed video recordings of tammar wallabies as they decelerated and accelerated while hopping over a force platform on level ground. Measurements were obtained over a range of accelerations ranging from -6 m s-2 to 8 m s-2. The goal of our study was to determine which joints are used to modulate mechanical power when tammar wallabies change speed. From these measurements, we also sought to determine which hind limb muscle groups are the most important for producing changes in mechanical work. Because our previous in vivo analyses of wallaby distal muscle function indicated that these muscle-tendon units favor elastic energy savings and perform little work during steady level and incline hopping, we hypothesized that proximal muscle groups operating at the hip and knee joint are most important for the modulation of mechanical work and power. Of the four hind limb joints examined, the ankle joint had the greatest influence on the total limb work, accounting for 89% of the variation observed with changing speed. The hip and metatarsophalageal (MP) joints also contributed to modulating whole limb work, but to a lesser degree than the ankle, accounting for 28% (energy production) and -24% (energy absorption) of the change in whole limb work versus acceleration, respectively. In contrast, the work produced at the knee joint was independent of acceleration. Based on the results of our previous in vivo studies and given that the magnitude of power produced at the ankle exceeds that which these muscles alone could produce, we conclude that the majority of power produced at the ankle joint is likely transferred from the hip and knee joints via proximal bi-articular muscles, operating in tandem with bi-articular ankle extensors, to power changes in hopping speed of tammar wallabies. Additionally, over the observed range of performance, peak joint moments at the ankle (and resulting tendon strains) did not increase significantly with acceleration, indicating that having thin tendons favoring elastic energy storage does not necessarily limit a tammar wallaby's ability to accelerate or decelerate.C.P. McGowan, R.V. Baudinette and A.A. Biewene

Asymmetrical Force Production in the Maneuvering Flight of Pigeons

Downstroke force produced by Rock Doves (Columba livia) as they negotiated an obstacle course was measured using in vivo recordings of delto-pectoral crest strain. During this slow $(\u3c6\ {\rm m}\ {\rm s}^{-1})$ , maneuvering flight, pigeons produced a series of four to six successive wingbeats in which the wing on the outside of the turn produced greater peak force than the wing on the inside of the turn, suggesting that the birds maneuvered in a saltatory manner during slow flight. This asymmetrical downstroke force may be used to increase or reestablish bank lost during upstroke, or it may be directed as thrust to compensate for adverse yaw or create excess yaw to alter the bird\u27s direction of flight. Continuous production of asymmetrical downstroke force through a turn differs from the traditional model of maneuvering flight, in which asymmetrical force is used only to initiate a bank, the forces are briefly reversed to arrest the momentum of the roll and then equalized to maintain the established bank, and the redirected lift of the wings then effects a turn. Although this traditional model probably describes most turns initiated during fast and gliding flight in birds, it underestimates the complexity of maneuvering during slow, flapping flight, where sophisticated kinematics and neuromuscular control are needed to change direction effectively