ABSTRACT Although cycling is a seemingly simple, reciprocal task, muscles must adapt their function to satisfy changes in mechanical demands induced by higher crank torques and faster pedalling cadences. We examined whether muscle function was sensitive to these changes in mechanical demands across a wide range of pedalling conditions. We collected experimental data of cycling where crank torque and pedalling cadence were independently varied from 13 to 44 N m and 60 to 140 rpm. These data were used in conjunction with musculoskeletal simulations and a recently developed functional index-based approach to characterise the role of human lower-limb muscles. We found that in muscles that generate most of the mechanical power and work during cycling, greater crank torque induced shifts towards greater muscle activation, greater positive muscle–tendon unit (MTU) work and a more motor-like function, particularly in the limb extensors. Conversely, with faster pedalling cadence, the same muscles exhibited a phase advance in muscle activity prior to crank top dead centre, which led to greater negative MTU power and work and shifted the muscles to contract with more spring-like behaviour. Our results illustrate the capacity for muscles to adapt their function to satisfy the mechanical demands of the task, even during highly constrained reciprocal tasks such as cycling. Understanding how muscles shift their contractile performance under varied mechanical and environmental demands may inform decisions on how to optimise pedalling performance and to design targeted cycling rehabilitation therapies for muscle-specific injuries or deficits.

ABSTRACT Most of what we know about whole muscle behaviour comes from experiments on single fibres or small muscles that are scaled up in size without considering the effects of the additional muscle mass. Previous modelling studies have shown that tissue inertia acts to slow the rate of force development and maximum velocity of muscle during shortening contractions and decreases the work and power per cycle during cyclic contractions; however, these results have not yet been confirmed by experiments on living tissue. Therefore, in this study we conducted in situ work-loop experiments on rat plantaris muscle to determine the effects of increasing the mass of muscle on mechanical work during cyclic contractions. We additionally simulated these experimental contractions using a mass-enhanced Hill-type model to validate our previous modelling work. We found that greater added mass resulted in lower mechanical work per cycle relative to the unloaded trials in which no mass was added to the muscle ( P =0.041 for both 85 and 123% increases in muscle mass). We additionally found that greater strain resulted in lower work per cycle relative to unloaded trials at the same strain to control for length change and velocity effects on the work output, possibly due to greater accelerations of the muscle mass at higher strains. These results confirm that tissue mass reduces muscle mechanical work at larger muscle sizes, and that this effect is likely amplified for lower activations.

ABSTRACT Mallard ducks are capable of performing a wide range of behaviors including nearly vertical takeoffs from both terrestrial and aquatic habitats. The hindlimb plays a key role during takeoffs from both media. However, because force generation differs in water versus on land, hindlimb kinematics and muscle function are likely modulated between these environments. Specifically, we hypothesize that hindlimb joint motion and muscle shortening are faster during aquatic takeoffs, but greater hindlimb muscle forces are generated during terrestrial takeoffs. In this study, we examined the hindlimb kinematics and in vivo contractile function of the lateral gastrocnemius (LG), a major ankle extensor and knee flexor, during takeoffs from water versus land in mallard ducks. In contrast to our hypothesis, we observed no change in ankle angular velocity between media. However, the hip and metatarsophalangeal joints underwent large excursions during terrestrial takeoffs but exhibited almost no motion during aquatic takeoffs. The knee extended during terrestrial takeoffs but flexed during aquatic takeoffs. Correspondingly, LG fascicle shortening strain, shortening velocity and pennation angle change were greater during aquatic takeoffs than during terrestrial takeoffs because of the differences in knee motion. Nevertheless, we observed no significant differences in LG stress or work, but did see an increase in muscle power output during aquatic takeoffs. Because differences in the physical properties of aquatic and terrestrial media require differing hindlimb kinematics and muscle function, animals such as mallards may be challenged to tune their muscle properties for movement across differing environments.

ABSTRACT Muscle function changes to meet the varying mechanical demands of locomotion across different gait and grade conditions. A muscle's work output is determined by time-varying patterns of neuromuscular activation, muscle force and muscle length change, but how these patterns change under different conditions in small animals is not well defined. Here, we report the first integrated in vivo force–length and activation patterns in rats, a commonly used small animal model, to evaluate the dynamics of two distal hindlimb muscles (medial gastrocnemius and plantaris) across a range of gait (walk, trot and gallop) and grade (level and incline) conditions. We use these data to explore how the pattern of force production, muscle activation and muscle length changes across conditions in a small quadrupedal mammal. As hypothesized, we found that the rat muscles show limited fascicle strains during active force generation in stance across gaits and grades, indicating that these distal rat muscles generate force economically but perform little work, similar to patterns observed in larger animals during level locomotion. Additionally, given differences in fiber type composition and variation in motor unit recruitment across the gait and grade conditions examined here for these muscles, the in vivo force–length behavior and neuromuscular activation data reported here can be used to validate improved two-element Hill-type muscle models.

ABSTRACT Leg stiffness, commonly estimated as the ‘compression’ of a defined leg element in response to a load, has long been used to characterize terrestrial locomotion. This study investigated how goats adjust the stiffness of their hindlimbs to accommodate surfaces of different stiffness. Goats provide a compelling animal model for studying leg stiffness modulation, because they skillfully ambulate over a range of substrates that vary in compliance. To investigate the adjustments that goats make when walking over such substrates, ground reaction forces and three-dimensional trajectories of hindlimb markers were recorded as goats walked on rigid, rubber and foam surfaces. Net joint moments, power and work at the hip, knee, ankle and metatarsophalangeal joints were estimated throughout stance via inverse dynamics. Hindlimb stiffness was estimated from plots of total leg force versus total leg length, and individual joint stiffness was estimated from plots of joint moment versus joint angle. Our results support the hypothesis that goats modulate hindlimb stiffness in response to surface stiffness; specifically, hindlimb stiffness decreased on the more compliant surfaces ( P <0.002). Estimates of joint stiffness identified hip and ankle muscles as the primary drivers of these adjustments. When humans run on compliant surfaces, they generally increase leg stiffness to preserve their center-of-mass mechanics. We did not estimate center-of-mass mechanics in this study; nevertheless, our estimates of hindlimb stiffness suggest that goats exhibit a different behavior. This study offers new insight into mechanisms that allow quadrupeds to modulate their gait mechanics when walking on surfaces of variable compliance.

ABSTRACT Loons (Gaviiformes) are arguably one of the most successful groups of swimming birds. As specialist foot-propelled swimmers, loons are capable of diving up to 70 m, remaining underwater for several minutes, and capturing fish. Despite the swimming prowess of loons, their undomesticated nature has prevented prior quantitative analysis. Our study used high-speed underwater cameras to film healthy common loons ( Gavia immer ) at the Tufts Wildlife Clinic in order to analyze their swimming and turning strategies. Loons swim by synchronously paddling their feet laterally at an average of 1.8 Hz. Combining flexion–extension of the ankle with rotation at the knee, loon swimming resembles grebe swimming and likely generates lift forces for propulsion. Loons modulate swimming speed by altering power stroke duration and use head bobbing to enhance underwater vision. We observed that loons execute tight but slow turns compared with other aquatic swimmers, potentially associated with hunting by flushing fish from refuges at short range. To execute turns, loons use several strategies. Loons increase the force produced on the outside of the turn by increasing the speed of the outboard foot, which also begins its power stroke before the inboard foot. During turns, loons bank their body away from the turn and alter the motion of the feet to maintain the turn. Our findings demonstrate that foot-propelled swimming has evolved convergently in loons and grebes, but divergently from cormorants. The swimming and turning strategies used by loons that allow them to capture fish could inspire robotic designs or novel paddling techniques.

ABSTRACT Birds fly effectively and maneuver nimbly by dynamically changing the shape of their wings during each wingbeat. These shape changes have yet to be quantified automatically at high temporal and spatial resolution. Therefore, we developed a custom 3D surface reconstruction method, which uses a high-speed camera to identify spatially encoded binary striped patterns that are projected on a flying bird. This non-invasive structured-light method allows automated 3D reconstruction of each stand-alone frame and can be extended to multiple views. We demonstrate this new technique by automatically reconstructing the dorsal surface of a parrotlet wing at 3200 frames s −1 during flapping flight. From this shape we analyze key parameters such as wing twist and angle of attack distribution. While our binary ‘single-shot’ algorithm is demonstrated by quantifying dynamic shape changes of a flying bird, it is generally applicable to moving animals, plants and deforming objects.

ABSTRACT Hill-type models are ubiquitous in the field of biomechanics, providing estimates of a muscle's force as a function of its activation state and its assumed force–length and force–velocity properties. However, despite their routine use, the accuracy with which Hill-type models predict the forces generated by muscles during submaximal, dynamic tasks remains largely unknown. This study compared human gastrocnemius forces predicted by Hill-type models with the forces estimated from ultrasound-based measures of tendon length changes and stiffness during cycling, over a range of loads and cadences. We tested both a traditional model, with one contractile element, and a differential model, with two contractile elements that accounted for independent contributions of slow and fast muscle fibres. Both models were driven by subject-specific, ultrasound-based measures of fascicle lengths, velocities and pennation angles and by activation patterns of slow and fast muscle fibres derived from surface electromyographic recordings. The models predicted, on average, 54% of the time-varying gastrocnemius forces estimated from the ultrasound-based methods. However, differences between predicted and estimated forces were smaller under low speed–high activation conditions, with models able to predict nearly 80% of the gastrocnemius force over a complete pedal cycle. Additionally, the predictions from the Hill-type muscle models tested here showed that a similar pattern of force production could be achieved for most conditions with and without accounting for the independent contributions of different muscle fibre types.

ABSTRACT 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.

ABSTRACT Skeletal muscles share many common, highly conserved features of organization at the molecular and myofilament levels, giving skeletal muscle fibers generally similar and characteristic mechanical and energetic properties; properties well described by classical studies of muscle mechanics and energetics. However, skeletal muscles can differ considerably in architectural design (fiber length, pinnation, and connective tissue organization), as well as fiber type, and how they contract in relation to the timing of neuromotor activation and in vivo length change. The in vivo dynamics of muscle contraction is, therefore, crucial to assessing muscle design and the roles that muscles play in animal movement. Architectural differences in muscle–tendon organization combined with differences in the phase of activation and resulting fiber length changes greatly affect the time-varying force and work that muscles produce, as well as the energetic cost of force generation. Intrinsic force–length and force–velocity properties of muscles, together with their architecture, also play important roles in the control of movement, facilitating rapid adjustments to changing motor demands. Such adjustments complement slower, reflex-mediated neural feedback control of motor recruitment. Understanding how individual fiber forces are integrated to whole-muscle forces, which are transmitted to the skeleton for producing and controlling locomotor movement, is therefore essential for assessing muscle design in relation to the dynamics of movement.

ABSTRACT This study examines whether the human iliotibial band (ITB) is specialized for elastic energy storage relative to the chimpanzee fascia lata (FL). To quantify the energy storage potential of these structures, we created computer models of human and chimpanzee lower limbs based on detailed anatomical dissections. We characterized the geometry and force–length properties of the FL, tensor fascia lata (TFL) and gluteus maximus (GMax) in four chimpanzee cadavers based on measurements of muscle architecture and moment arms about the hip and knee. We used the chimp model to estimate the forces and corresponding strains in the chimp FL during bipedal walking, and compared these data with analogous estimates from a model of the human ITB, accounting for differences in body mass and lower extremity posture. We estimate that the human ITB stores 15- to 20-times more elastic energy per unit body mass and stride than the chimp FL during bipedal walking. Because chimps walk with persistent hip flexion, the TFL and portions of GMax that insert on the FL undergo smaller excursions (origin to insertion) than muscles that insert on the human ITB. Also, because a smaller fraction of GMax inserts on the chimp FL than on the human ITB, and thus its mass-normalized physiological cross-sectional area is about three times less in chimps, the chimp FL probably transmits smaller muscle forces. These data provide new evidence that the human ITB is anatomically derived compared with the chimp FL and potentially contributes to locomotor economy during bipedal locomotion.

ABSTRACT Airflow conditions close to the Earth's surface are often complex, posing challenges to flight stability and control for volant taxa. Relatively little is known about how well flying animals can contend with complex, adverse air flows, or about the flight control mechanisms used by animals to mitigate wind disturbances. Several recent studies have examined flight in the unsteady von Kármán vortex streets that form behind cylinders, generating flow disturbances that are predictable in space and time; these structures are relatively rare in nature, because they occur only the immediate, downstream vicinity of an object. In contrast, freestream turbulence is characterized by rapid, unpredictable flow disturbances across a wide range of spatial and temporal scales, and is nearly ubiquitous in natural habitats. Hummingbirds are ideal organisms for studying the influence of freestream turbulence on flight, as they forage in a variety of aerial conditions and are powerful flyers. We filmed ruby-throated hummingbirds ( Archilochus colubris ) maintaining position at a feeder in laminar and strongly turbulent (intensity ∼15%) airflow environments within a wind tunnel and compared their mean kinematics of the head, body, tail and wing, as well as variability in these parameters. Hummingbirds exhibited remarkably stable head position and orientation in both smooth and turbulent flow while maintaining position at the feeder. However, the hummingbird's body was less stable in turbulent flow and appeared to be most sensitive to disturbances along the mediolateral axis, displaying large lateral accelerations, translations and rolling motions during flight. The hummingbirds mitigated these disturbances by increasing mean wing stroke amplitude and stroke plane angle, and by varying these parameters asymmetrically between the wings and from one stroke to the next. They also actively varied the orientation and fan angle of the tail, maintaining a larger mean fan angle when flying in turbulent flow; this may improve their passive stability, but probably incurs an energetic cost as a result of increased drag. Overall, we observed many of the same kinematic changes noted previously for hummingbirds flying in a von Kármán vortex street, but we also observed kinematic changes associated with high force production, similar to those seen during load-lifting or high-speed flight. These findings suggest that flight may be particularly costly in fully mixed, freestream turbulence, which is the flow condition that hummingbirds are likely to encounter most frequently in natural habitats.

ABSTRACT Few vertebrates run on water. The largest animals to accomplish this feat are western and Clark's grebes ( Aechmophorus occidentalis and Aechmophorus clarkii ). These birds use water running to secure a mate during a display called rushing. Grebes weigh an order of magnitude more than the next largest water runners, basilisk lizards ( Basilicus basiliscus ), and therefore face a greater challenge to support their body weight. How do these birds produce the hydrodynamic forces necessary to overcome gravity and sustain rushing? We present the first quantitative study of water running by grebes. High-speed video recordings elucidate the hindlimb movements of grebes rushing in the wild. We complement these findings with laboratory experiments using physical models and a preserved grebe foot to estimate how slapping the water surface contributes to weight support. Our results indicate that grebes use three novel tactics to successfully run on water. First, rushing grebes use exceptionally high stride rates, reaching 10 Hz. Second, grebe foot size and high water impact speed allow grebes to generate up to 30–55% of the required weight support through water slap alone. Finally, flattened foot bones reduce downward drag, permitting grebes to retract each foot from the water laterally. Together, these mechanisms outline a water-running strategy qualitatively different from that of the only previously studied water runner, the basilisk lizard. The hydrodynamic specializations of rushing grebes could inform the design of biomimetic appendages. Furthermore, the mechanisms underlying this impressive display demonstrate that evolution can dramatically alter performance under sexual selection.

The complexity of low speed maneuvering flight is apparent from the combination of two critical aspects of this behavior: high power and precise control. To understand how such control is achieved, we examined the underlying kinematics and resulting aerodynamic mechanisms of low speed turning flight in the pigeon ( Columba livia ). Three birds were trained to perform 90 deg level turns in a stereotypical fashion and detailed three-dimensional (3D) kinematics were recorded at high speeds. Applying the angular momentum principle, we used mechanical modeling based on time-varying 3D inertia properties of individual sections of the pigeon's body to separate angular accelerations of the torso based on aerodynamics from those based on inertial effects. Directly measured angular accelerations of the torso were predicted by aerodynamic torques, justifying inferences of aerodynamic torque generation based on inside wing versus outside wing kinematics. Surprisingly, contralateral asymmetries in wing speed did not appear to underlie the 90 deg aerial turns, nor did contralateral differences in wing area, angle of attack, wingbeat amplitude or timing. Instead, torso angular accelerations into the turn were associated with the outside wing sweeping more anteriorly compared with a more laterally directed inside wing. In addition to moving through a relatively more retracted path, the inside wing was also more strongly pronated about its long axis compared with the outside wing, offsetting any difference in aerodynamic angle of attack that might arise from the observed asymmetry in wing trajectories. Therefore, to generate roll and pitch torques into the turn, pigeons simply reorient their wing trajectories toward the desired flight direction. As a result, by acting above the center of mass, the net aerodynamic force produced by the wings is directed inward, generating the necessary torques for turning.

SUMMARY Goats and other quadrupeds must modulate the work output of their muscles to accommodate the changing mechanical demands associated with locomotion in their natural environments. This study examined which hindlimb joint moments goats use to generate and absorb mechanical energy on level and sloped surfaces over a range of locomotor speeds. Ground reaction forces and the three-dimensional locations of joint markers were recorded as goats walked, trotted and galloped over 0, +15 and −15 deg sloped surfaces. Net joint moments, powers and work were estimated at the goats' hip, knee, ankle and metatarsophalangeal joints throughout the stance phase via inverse dynamics calculations. Differences in locomotor speed on the level, inclined and declined surfaces were characterized and accounted for by fitting regression equations to the joint moment, power and work data plotted versus non-dimensionalized speed. During level locomotion, the net work generated by moments at each of the hindlimb joints was small (less than 0.1 J kg −1 body mass) and did not vary substantially with gait or locomotor speed. During uphill running, by contrast, mechanical energy was generated at the hip, knee and ankle, and the net work at each of these joints increased dramatically with speed ( P <0.05). The greatest increases in positive joint work occurred at the hip and ankle. During downhill running, mechanical energy was decreased in two main ways: goats generated larger knee extension moments in the first half of stance, absorbing energy as the knee flexed, and goats generated smaller ankle extension moments in the second half of stance, delivering less energy. The goats' hip extension moment in mid-stance was also diminished, contributing to the decrease in energy. These analyses offer new insight into quadrupedal locomotion, clarifying how the moments generated by hindlimb muscles modulate mechanical energy at different locomotor speeds and grades, as needed to accommodate the demands of variable terrain.

SUMMARY Animals modulate the power output needed for different locomotor tasks by changing muscle forces and fascicle strain rates. To generate the necessary forces, appropriate motor units must be recruited. Faster motor units have faster activation–deactivation rates than slower motor units, and they contract at higher strain rates; therefore, recruitment of faster motor units may be advantageous for tasks that involve rapid movements or high rates of work. This study identified motor unit recruitment patterns in the gastrocnemii muscles of goats and examined whether faster motor units are recruited when locomotor speed is increased. The study also examined whether locomotor tasks that elicit faster (or slower) motor units are associated with increased (or decreased) in vivo tendon forces, force rise and relaxation rates, fascicle strains and/or strain rates. Electromyography (EMG), sonomicrometry and muscle-tendon force data were collected from the lateral and medial gastrocnemius muscles of goats during level walking, trotting and galloping and during inclined walking and trotting. EMG signals were analyzed using wavelet and principal component analyses to quantify changes in the EMG frequency spectra across the different locomotor conditions. Fascicle strain and strain rate were calculated from the sonomicrometric data, and force rise and relaxation rates were determined from the tendon force data. The results of this study showed that faster motor units were recruited as goats increased their locomotor speeds from level walking to galloping. Slow inclined walking elicited EMG intensities similar to those of fast level galloping but different EMG frequency spectra, indicating that recruitment of the different motor unit types depended, in part, on characteristics of the task. For the locomotor tasks and muscles analyzed here, recruitment patterns were generally associated with in vivo fascicle strain rates, EMG intensity and tendon force. Together, these data provide new evidence that changes in motor unit recruitment have an underlying mechanical basis, at least for certain locomotor tasks.

SUMMARY 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.

SUMMARY Hummingbirds have the smallest body size and highest wingbeat frequencies of all flying vertebrates, so they represent one endpoint for evaluating the effects of body size on sustained muscle function and flight performance. Other bird species vary neuromuscular recruitment and contractile behavior to accomplish flight over a wide range of speeds, typically exhibiting a U-shaped curve with maxima at the slowest and fastest flight speeds. To test whether the high wingbeat frequencies and aerodynamically active upstroke of hummingbirds lead to different patterns, we flew rufous hummingbirds ( Selasphorus rufus , 3 g body mass, 42 Hz wingbeat frequency) in a variable-speed wind tunnel (0–10 m s −1 ). We measured neuromuscular activity in the pectoralis (PECT) and supracoracoideus (SUPRA) muscles using electromyography (EMG, N =4 birds), and we measured changes in PECT length using sonomicrometry ( N =1). Differing markedly from the pattern in other birds, PECT deactivation occurred before the start of downstroke and the SUPRA was deactivated before the start of upstroke. The relative amplitude of EMG signal in the PECT and SUPRA varied according to a U-shaped curve with flight speed; additionally, the onset of SUPRA activity became relatively later in the wingbeat at intermediate flight speeds (4 and 6 m s −1 ). Variation in the relative amplitude of EMG was comparable with that observed in other birds but the timing of muscle activity was different. These data indicate the high wingbeat frequency of hummingbirds limits the time available for flight muscle relaxation before the next half stroke of a wingbeat. Unlike in a previous study that reported single-twitch EMG signals in the PECT of hovering hummingbirds, across all flight speeds we observed 2.9±0.8 spikes per contraction in the PECT and 3.8±0.8 spikes per contraction in the SUPRA. Muscle strain in the PECT was 10.8±0.5%, the lowest reported for a flying bird, and average strain rate was 7.4±0.2 muscle lengths s −1 . Among species of birds, PECT strain scales proportional to body mass to the 0.2 power (∞ M b 0.2 ) using species data and ∞ M b 0.3 using independent contrasts. This positive scaling is probably a physiological response to an adverse scaling of mass-specific power available for flight.