Clites TR, Arnold AS, Singh NM, H.Chen, Tugman C, Billadeau B, Biewener AA, Herr HM. Goats decrease hindlimb stiffness when walking over compliant surfaces. Journal of Experimental Biology. 2019;222. Publisher's Version
Lai A, Biewener AA, Wakeling JM. Muscle-specific indices to characterise the functional behaviours of human lower limb muscles during locomotion. Journal of Biomechanics. 2019;89 :134-138.
Biewener AA. Animal Locomotion: Near-Ground Low-Cost Flights. Curr. Biol. 2018;28 (23) :R1348-R1349. Publisher's Version
Lai A, Biewener AA, Wakeling JM. Metabolic cost underlies task-dependent variations in motor unit recruitment. J. Roy. Soc. Interface. 2018;15 (148). Publisher's Version
Clifton GT, Biewener AA. Foot-propelled swimming kinematics and turning strategies in common loons. J. exp. Biol. 2018;221 :1-11. Publisher's Version
Ahn AN, Konow N, Tijs C, Biewener AA. Different segments within vertebrate muscles can operate on different regions of their force-length relationships. Int. Comp. Biol. 2018;58 :219-231. Publisher's Version
Biewener AA. Evolutionary race as predators hunt prey. Nature. 2018;554 :176-178. Publisher's Version
Lai PH, Biewener AA, Pierce SE. Three‐dimensional mobility and muscle attachments in the pectoral limb of the Triassic cynodont Massetognathus pascuali (Romer, 1967). Journal of Anatomy. 2018;232 (3) :383-406. Publisher's VersionAbstract
The musculoskeletal configuration of the mammalian pectoral limb has been heralded as a key anatomical feature leading to the adaptive radiation of mammals, but limb function in the non‐mammaliaform cynodont outgroup remains unresolved. Conflicting reconstructions of abducted and adducted posture are based on mutually incompatible interpretations of ambiguous osteology. We reconstruct the pectoral limb of the Triassic non‐mammaliaform cynodont Massetognathus pascuali in three dimensions, by combining skeletal morphology from micro‐computed tomography with muscle anatomy from an extended extant phylogenetic bracket. Conservative tests of maximum range of motion suggest a degree of girdle mobility, as well as substantial freedom at the shoulder and the elbow joints. The glenoid fossa supports a neutral pose in which the distal end of the humerus points 45° posterolaterally from the body wall, intermediate between classically ‘sprawling’ and ‘parasagittal’ limb postures. Massetognathus pascuali is reconstructed as having a near‐mammalian complement of shoulder muscles, including an incipient rotator cuff (m. subscapularis, m. infraspinatus, m. supraspinatus, and m. teres minor). Based on close inspection of the morphology of the glenoid fossa, we hypothesize a posture‐driven scenario for the evolution of the therian ball‐and‐socket shoulder joint. The musculoskeletal reconstruction presented here provides the anatomical scaffolding for more detailed examination of locomotor evolution in the precursors to mammals.
Lai A, Arnold A, Biewener AA, Dick T, Wakeling JM. Does a two-element muscle model offer advantages when estimating ankle plantar flexor forces during human cycling?. Journal of Biomechanics. 2018;68 :6-13. Publisher's VersionAbstract
Traditional Hill-type muscle models, parameterized using high-quality experimental data, are often “too weak” to reproduce the joint torques generated by healthy adults during rapid, high force tasks. This study investigated whether the failure of these models to account for different types of motor units contributes to this apparent weakness; if so, muscle-driven simulations may rely on excessively high muscle excitations to generate a given force. We ran a series of forward simulations that reproduced measured ankle mechanics during cycling at five cadences ranging from 60 to 140 RPM. We generated both “nominal” simulations, in which an abstract ankle model was actuated by a 1-element Hill-type plantar flexor with a single contractile element (CE), and “test” simulations, in which the same model was actuated by a 2-element plantar flexor with two CEs that accounted for the force-generating properties of slower and faster motor units. We varied the total excitation applied to the 2-element plantar flexor between 60 and 105% of the excitation from each nominal simulation, and we varied the amount distributed to each CE between 0 and 100% of the total. Within this test space, we identified the excitation level and distribution, at each cadence, that best reproduced the plantar flexor forces generated in the nominal simulations. Our comparisons revealed that the 2-element model required substantially less total excitation than the 1-element model to generate comparable forces, especially at higher cadences. For instance, at 140 RPM, the required excitation was reduced by 23%. These results suggest that a 2-element model, in which contractile properties are “tuned” to represent slower and faster motor units, can increase the apparent strength and perhaps improve the fidelity of simulations of tasks with varying mechanical demands.
Lai AKM, Arnold AS, Wakeling JM. Why are antagonist muscles co-activated in my simulation? A musculoskeletal model for analyzing human locomotor tasks. Annals of Biomedical Engineering. 2017;45 (12) :2762-2774. Publisher's VersionAbstract
Existing "off-the-shelf" musculoskeletal models are problematic when simulating movements that involve substantial hip and knee flexion, such as the upstroke of pedalling, because they tend to generate excessive passive fibre force. The goal of this study was to develop a refined musculoskeletal model capable of simulating pedalling and fast running, in addition to walking, which predicts the activation patterns of muscles better than existing models. Specifically, we tested whether the anomalous co-activation of antagonist muscles, commonly observed in simulations, could be resolved if the passive forces generated by the underlying model were diminished. We refined the OpenSim™ model published by Rajagopal et al. (IEEE Trans Biomed Eng 63:1-1, 2016) by increasing the model's range of knee flexion, updating the paths of the knee muscles, and modifying the force-generating properties of eleven muscles. Simulations of pedalling, running and walking based on this model reproduced measured EMG activity better than simulations based on the existing model-even when both models tracked the same subject-specific kinematics. Improvements in the predicted activations were associated with decreases in the net passive moments; for example, the net passive knee moment during the upstroke of pedalling decreased from 36.9 N m (existing model) to 6.3 N m (refined model), resulting in a dramatic decrease in the co-activation of knee flexors. The refined model is available from and is suitable for analysing movements with up to 120° of hip flexion and 140° of knee flexion.
Kambic RE, Biewener AA, Pierce SE. Experimental determination of three-dimensional cervical joint mobility in the avian neck. Frontiers in Zoology. 2017;14 (37) :1-15.Abstract


Birds have highly mobile necks, but neither the details of how they realize complex poses nor the evolution of this complex musculoskeletal system is well-understood. Most previous work on avian neck function has focused on dorsoventral flexion, with few studies quantifying lateroflexion or axial rotation. Such data are critical for understanding joint function, as musculoskeletal movements incorporate motion around multiple degrees of freedom simultaneously. Here we use biplanar X-rays on wild turkeys to quantify three-dimensional cervical joint range of motion in an avian neck to determine patterns of mobility along the cranial-caudal axis.


Range of motion can be generalized to a three-region model: cranial joints are ventroflexed with high axial and lateral mobility, caudal joints are dorsiflexed with little axial rotation but high lateroflexion, and middle joints show varying amounts axial rotation and a low degree of lateroflexion. Nonetheless, variation within and between regions is high. To attain complex poses, substantial axial rotation can occur at joints caudal to the atlas/axis complex and zygapophyseal joints can reduce their overlap almost to osteological disarticulation. Degrees of freedom interact at cervical joints; maximum lateroflexion occurs at different dorsoventral flexion angles at different joints, and axial rotation and lateroflexion are strongly coupled. Further, patterns of joint mobility are strongly predicted by cervical morphology.


Birds attain complex neck poses through a combination of mobile intervertebral joints, coupled rotations, and highly flexible zygapophyseal joints. Cranial-caudal patterns of joint mobility are tightly linked to cervical morphology, such that function can be predicted by form. The technique employed here provides a repeatable protocol for studying neck function in a broad array of taxa that will be directly comparable. It also serves as a foundation for future work on the evolution of neck mobility along the line from non-avian theropod dinosaurs to birds.

Electronic supplementary material

The online version of this article (doi:10.1186/s12983-017-0223-z) contains supplementary material, which is available to authorized users.

Keywords: Function, Mobility, XROMM, Avian, Bird, Anatomy, Cervical, Neck, X-ray, Motion, Morphology
Deetjen ME, Biewener AA, Lentink D. High-speed surface reconstruction of a flying bird using structured-light. J. Exp. Biol. 2017;220 :1956-1961.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 fps 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.
McHorse BK, Biewener AA, Pierce SE. Mechanics of evolutionary digit reduction in fossil horses . Proc. Roy. Soc. B. 2017;284 (20171174) :1-8.Abstract
Digit reduction is a major trend that characterizes horse evolution, but its causes and consequences have rarely been quantitatively tested. Using beam analysis on fossilized centre metapodials, we tested how locomotor bone stresses changed with digit reduction and increasing body size across the horse lineage. Internal bone geometry was captured from 13 fossil horse genera that covered the breadth of the equid phylogeny and the spectrum of digit reduction and body sizes, from Hyracotherium to Equus. To account for the load-bearing role of side digits, a novel, continuous measure of digit reduction was also established—toe reduction index (TRI). Our results show that without accounting for side digits, three-toed horses as late as Parahippus would have experienced physiologically untenable bone stresses. Conversely, when side digits are modelled as load-bearing, species at the base of the horse radiation through Equus probably maintained a similar safety factor to fracture stress. We conclude that the centre metapodial compensated for evolutionary digit reduction and body mass increases by becoming more resistant to bending through substantial positive allometry in internal geometry. These results lend support to two historical hypotheses: that increasing body mass selected for a single, robust metapodial rather than several smaller ones; and that, as horse limbs became elongated, the cost of inertia from the side toes outweighed their utility for stabilization or load-bearing.
Dick TJM, Biewener AA, Wakeling JM. Comparison of human gastrocnemius forces predicted by Hill-type muscle models and estimated from ultrasound images. Journal of Experimental Biology. 2017;220 :1643-1653.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 gastrocnemii forces predicted by Hill-type models to 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 % the time-varying gastrocnemii 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 gastrocnemii 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.
Ros IG, Bhagavatula PS, Lin HT, Biewener AA. Rules to fly by: pigeons navigating horizontal obstacles limit steering by selecting gaps most aligned to their bearing. Roy. Soc. Interface Focus. 2017;7 (20160093).Abstract
Flying animals must successfully contend with obstacles in their natural
environments. Inspired by the robust manoeuvring abilities of flying animals,
unmanned aerial systems are being developed and tested to improve flight
control through cluttered environments. We previously examined steering
strategies that pigeons adopt to fly through an array of vertical obstacles
(VOs). Modelling VO flight guidance revealed that pigeons steer towards
larger visual gaps when making fast steering decisions. In the present experiments,
we recorded three-dimensional flight kinematics of pigeons as they
flew through randomized arrays of horizontal obstacles (HOs). We found
that pigeons still decelerated upon approach but flew faster through a
denser array of HOs compared with the VO array previously tested. Pigeons
exhibited limited steering and chose gaps between obstacles most aligned to
their immediate flight direction, in contrast to VO navigation that favoured
widest gap steering. In addition, pigeons navigated past the HOs with more
variable and decreased wing stroke span and adjusted their wing stroke
plane to reduce contact with the obstacles. Variability in wing extension,
stroke plane and wing stroke path was greater during HO flight. Pigeons
also exhibited pronounced head movements when negotiating HOs, which
potentially serve a visual function. These head-bobbing-like movements
were most pronounced in the horizontal (flight direction) and vertical directions,
consistent with engaging motion vision mechanisms for obstacle
detection. These results show that pigeons exhibit a keen kinesthetic sense of
their body and wings in relation to obstacles. Together with aerodynamic flapping
flight mechanics that favours vertical manoeuvring, pigeons are able to
navigate HOs using simple rules, with remarkable success.
Moore TY, Rivera AM, Biewener AA. Vertical leaping mechanics of the Lesser Egyptian Jerboa reveal specialization for maneuverability rather than elastic energy storage. Frontiers in Zoology. 2017;14 (32) :1-12.Abstract


Numerous historical descriptions of the Lesser Egyptian jerboa, Jaculus jaculus, a small bipedal mammal with elongate hindlimbs, make special note of their extraordinary leaping ability. We observed jerboa locomotion in a laboratory setting and performed inverse dynamics analysis to understand how this small rodent generates such impressive leaps. We combined kinematic data from video, kinetic data from a force platform, and morphometric data from dissections to calculate the relative contributions of each hindlimb muscle and tendon to the total movement.


Jerboas leapt in excess of 10 times their hip height. At the maximum recorded leap height (not the maximum observed leap height), peak moments for metatarso-phalangeal, ankle, knee, and hip joints were 13.1, 58.4, 65.1, and 66.9 Nmm, respectively. Muscles acting at the ankle joint contributed the most work (mean 231.6 mJ / kg Body Mass) to produce the energy of vertical leaping, while muscles acting at the metatarso-phalangeal joint produced the most stress (peak 317.1 kPa). The plantaris, digital flexors, and gastrocnemius tendons encountered peak stresses of 25.6, 19.1, and 6.0 MPa, respectively, transmitting the forces of their corresponding muscles (peak force 3.3, 2.0, and 3.8 N, respectively). Notably, we found that the mean elastic energy recovered in the primary tendons of both hindlimbs comprised on average only 4.4% of the energy of the associated leap.


The limited use of tendon elastic energy storage in the jerboa parallels the morphologically similar heteromyid kangaroo rat, Dipodomys spectabilis. When compared to larger saltatory kangaroos and wallabies that sustain hopping over longer periods of time, these small saltatory rodents store and recover less elastic strain energy in their tendons. The large contribution of muscle work, rather than elastic strain energy, to the vertical leap suggests that the fitness benefit of rapid acceleration for predator avoidance dominated over the need to enhance locomotor economy in the evolutionary history of jerboas.

Electronic supplementary material

The online version of this article (doi:10.1186/s12983-017-0215-z) contains supplementary material, which is available to authorized users.

Keywords: Jerboa, Inverse dynamics, Muscle-tendon stresses, Ricochetal bipedal locomotion
Moore TY, Cooper KL, Biewener AA, Vasudevan R. Unpredictability of escape trajectory explains predator evasion ability and microhabitat preference of desert rodents. Nature Communications. 2017;8 (440) :1-9. Publisher's VersionAbstract
Mechanistically linking movement behaviors and ecology is key to understanding the adaptive evolution of locomotion. Predator evasion, a behavior that enhances fitness, may depend upon short bursts or complex patterns of locomotion. However, such movements are poorly characterized by existing biomechanical metrics. We present methods based on the entropy measure of randomness from Information Theory to quantitatively characterize the unpredictability of non-steady-state locomotion. We then apply the method by examining sympatric rodent species whose escape trajectories differ in dimensionality. Unlike the speed-regulated gait use of cursorial animals to enhance locomotor economy, bipedal jerboa (family Dipodidae) gait transitions likely enhance maneuverability. In field-based observations, jerboa trajectories are significantly less predictable than those of quadrupedal rodents, likely increasing predator evasion ability. Consistent with this hypothesis, jerboas exhibit lower anxiety in open fields than quadrupedal rodents, a behavior that varies inversely with predator evasion ability. Our unpredictability metric expands the scope of quantitative biomechanical studies to include non-steady-state locomotion in a variety of evolutionary and ecologically significant contexts.
Warrick DR, Hedrick TL, Biewener AA, Crandell KE, Tobalske BW. Foraging at the edge of the world: low-altitude, high-speed maneuvering in barn swallows. Phil. Trans. Roy. Soc. 2016;371 (20150391).Abstract
While prior studies of swallow manoeuvering have focused on slow-speed flight and obstacle avoidance in still air, swallows survive by foraging at high speeds in windy environments. Recent advances in field-portable, high-speed video systems, coupled with precise anemometry, permit measures of high-speed aerial performance of birds in a natural state. We undertook the present study to test: (i) the manner in which barn swallows (Hirundo rustica) may exploit wind dynamics and ground effect while foraging and (ii) the relative importance of flapping versus gliding for accomplishing high-speed manoeuvers. Using multi-camera videography synchronized with wind-velocity measurements, we tracked coursing manoeuvers in pursuit of prey. Wind speed averaged 1.3–2.0 m s−1 across the atmospheric boundary layer, exhibiting a shear gradient greater than expected, with instantaneous speeds of 0.02–6.1 m s−1. While barn swallows tended to flap throughout turns, they exhibited reduced wingbeat frequency, relying on glides and partial bounds during maximal manoeuvers. Further, the birds capitalized on the near-earth wind speed gradient to gain kinetic and potential energy during both flapping and gliding turns; providing evidence that such behaviour is not limited to large, fixed-wing soaring seabirds and that exploitation of wind gradients by small aerial insectivores may be a significant aspect of their aeroecology.
Ros IG, Biewener AA. Optic flow stabilizes flight in ruby-throated hummingbirds. J. Exp. Biol. 2016;219 :2443-2448.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.
Biewener AA. Locomotion as an emergent property of muscle contractile dynamics. J. Exp. Biol. 2016;219 :285-294.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.