Aleksandra V. Birn-Jeffery

Birds achieve high robustness in uneven terrain through active control of landing conditions

SUMMARY We understand little about how animals adjust locomotor behaviour to negotiate uneven terrain. The mechanical demands and constraints of such behaviours likely differ from uniform terrain locomotion. Here we investigated how common pheasants negotiate visible obstacles with heights from 10 to 50% of leg length. Our goal was to determine the neuro-mechanical strategies used to achieve robust stability, and address whether strategies vary with obstacle height. We found that control of landing conditions was crucial for minimising fluctuations in stance leg loading and work in uneven terrain. Variation in touchdown leg angle (θTD) was correlated with the orientation of ground force during stance, and the angle between the leg and body velocity vector at touchdown (βTD) was correlated with net limb work. Pheasants actively targeted obstacles to control body velocity and leg posture at touchdown to achieve nearly steady dynamics on the obstacle step. In the approach step to an obstacle, the birds produced net positive limb work to launch themselves upward. On the obstacle, body dynamics were similar to uniform terrain. Pheasants also increased swing leg retraction velocity during obstacle negotiation, which we suggest is an active strategy to minimise fluctuations in peak force and leg posture in uneven terrain. Thus, pheasants appear to achieve robustly stable locomotion through a combination of path planning using visual feedback and active adjustment of leg swing dynamics to control landing conditions. We suggest that strategies for robust stability are context specific, depending on the quality of sensory feedback available, especially visual input.

Don't break a leg: running birds from quail to ostrich prioritise leg safety and economy on uneven terrain

Cursorial ground birds are paragons of bipedal running that span a 500-fold mass range from quail to ostrich. Here we investigate the task-level control priorities of cursorial birds by analysing how they negotiate single-step obstacles that create a conflict between body stability (attenuating deviations in body motion) and consistent leg force–length dynamics (for economy and leg safety). We also test the hypothesis that control priorities shift between body stability and leg safety with increasing body size, reflecting use of active control to overcome size-related challenges. Weight-support demands lead to a shift towards straighter legs and stiffer steady gait with increasing body size, but it remains unknown whether non-steady locomotor priorities diverge with size. We found that all measured species used a consistent obstacle negotiation strategy, involving unsteady body dynamics to minimise fluctuations in leg posture and loading across multiple steps, not directly prioritising body stability. Peak leg forces remained remarkably consistent across obstacle terrain, within 0.35 body weights of level running for obstacle heights from 0.1 to 0.5 times leg length. All species used similar stance leg actuation patterns, involving asymmetric force–length trajectories and posture-dependent actuation to add or remove energy depending on landing conditions. We present a simple stance leg model that explains key features of avian bipedal locomotion, and suggests economy as a key priority on both level and uneven terrain. We suggest that running ground birds target the closely coupled priorities of economy and leg safety as the direct imperatives of control, with adequate stability achieved through appropriately tuned intrinsic dynamics.

The Scaling of Uphill and Downhill Locomotion in Legged Animals

Animals must continually respond dynamically as they move through complex environments, and slopes are a common terrain on which legged animals must move. Despite this, non-level locomotion remains poorly understood. In this study, we first review the literature on locomotor mechanics, metabolic cost, and kinematic strategies on slopes. Using existing literature we then performed scaling analyses of kinematic variables, including speed, duty factor, and stride-length across a range of body sizes from ants to horses. The studies that examined locomotion on inclines vastly outnumbered those focusing on declines. On inclines, animals tend to reduce speed and increase duty factor, but a similar consensus could not be reached for declines. Remarkably, stride-length did not differ between locomotion on inclines and on level terrain, but this may have resulted from data only being available for low slopes (<30°). On declines there appears to be a shift in locomotor strategy that is size-dependent. At masses <1-10 kg, animals tended to use shorter strides than on level terrain, and the opposite occurred at larger body masses. Therefore, possibly due to stability issues, body mass plays a significant role in the locomotor strategy used when traveling downhill. Although we currently lack sufficient data, differential leg function is likely to be critical for locomotion on slopes, with mechanical demands differing on limbs during movement on level, inclined, and declined surfaces. Our scaling analysis not only highlights areas that require future work, but also suggests that body size is important for determining the mechanics and strategies animals use to negotiate non-level terrain. It is clear that selection has resulted in an incredible range of body size among animals, both extant and extinct, and it is likely that the ability to move up and down slopes has constrained or relaxed these mechanical pressures. Given the lack of integration of ecological data with laboratory experiments, future work should first determine which inclines animals actually use in nature, as this likely plays a key role in behaviors such as predator-prey interactions.

Adaptive simplification and the evolution of gecko locomotion: Morphological and biomechanical consequences of losing adhesion

Significance The gecko adhesive system has garnered considerable interest from scientists over the past several decades. Most research has focused on the function and microanatomy of the adhesive system. However, it is currently unclear what impact the secondary loss or simplification of the adhesive system might have on the evolutionary biomechanics of gecko locomotion, which is critical for pinpointing the constraints that accompany such an innovation, and ultimately the release from these constraints. We found that geckos exhibit elevated rates of morphological and kinematic evolution when their adhesive system is lost/simplified, providing evidence that the loss of an innovation can have profound evolutionary impacts on organismal structural and functional divergence Innovations permit the diversification of lineages, but they may also impose functional constraints on behaviors such as locomotion. Thus, it is not surprising that secondary simplification of novel locomotory traits has occurred several times among vertebrates and could potentially lead to exceptional divergence when constraints are relaxed. For example, the gecko adhesive system is a remarkable innovation that permits locomotion on surfaces unavailable to other animals, but has been lost or simplified in species that have reverted to a terrestrial lifestyle. We examined the functional and morphological consequences of this adaptive simplification in the Pachydactylus radiation of geckos, which exhibits multiple unambiguous losses or bouts of simplification of the adhesive system. We found that the rates of morphological and 3D locomotor kinematic evolution are elevated in those species that have simplified or lost adhesive capabilities. This finding suggests that the constraints associated with adhesion have been circumvented, permitting these species to either run faster or burrow. The association between a terrestrial lifestyle and the loss/reduction of adhesion suggests a direct link between morphology, biomechanics, and ecology.

Does a crouched leg posture enhance running stability and robustness

Humans and birds both walk and run bipedally on compliant legs. However, differences in leg architecture may result in species-specific leg control strategies as indicated by the observed gait patterns. In this work, control strategies for stable running are derived based on a conceptual model and compared with experimental data on running humans and pheasants (Phasianus colchicus). From a model perspective, running with compliant legs can be represented by the planar spring mass model and stabilized by applying swing leg control. Here, linear adaptations of the three leg parameters, leg angle, leg length and leg stiffness during late swing phase are assumed. Experimentally observed kinematic control parameters (leg rotation and leg length change) of human and avian running are compared, and interpreted within the context of this model, with specific focus on stability and robustness characteristics. The results suggest differences in stability characteristics and applied control strategies of human and avian running, which may relate to differences in leg posture (straight leg posture in humans, and crouched leg posture in birds). It has been suggested that crouched leg postures may improve stability. However, as the system of control strategies is overdetermined, our model findings suggest that a crouched leg posture does not necessarily enhance running stability. The model also predicts different leg stiffness adaptation rates for human and avian running, and suggests that a crouched avian leg posture, which is capable of both leg shortening and lengthening, allows for stable running without adjusting leg stiffness. In contrast, in straight-legged human running, the preparation of the ground contact seems to be more critical, requiring leg stiffness adjustment to remain stable. Finally, analysis of a simple robustness measure, the normalized maximum drop, suggests that the crouched leg posture may provide greater robustness to changes in terrain height.

Pedal Claw Curvature in Birds, Lizards and Mesozoic Dinosaurs – Complicated Categories and Compensating for Mass-Specific and Phylogenetic Control

Pedal claw geometry can be used to predict behaviour in extant tetrapods and has frequently been used as an indicator of lifestyle and ecology in Mesozoic birds and other fossil reptiles, sometimes without acknowledgement of the caveat that data from other aspects of morphology and proportions also need to be considered. Variation in styles of measurement (both inner and outer claw curvature angles) has made it difficult to compare results across studies, as have over-simplified ecological categories. We sought to increase sample size in a new analysis devised to test claw geometry against ecological niche. We found that taxa from different behavioural categories overlapped extensively in claw geometry. Whilst most taxa plotted as predicted, some fossil taxa were recovered in unexpected positions. Inner and outer claw curvatures were statistically correlated, and both correlated with relative claw robusticity (mid-point claw height). We corrected for mass and phylogeny, as both likely influence claw morphology. We conclude that there is no strong mass-specific effect on claw curvature; furthermore, correlations between claw geometry and behaviour are consistent across disparate clades. By using independent contrasts to correct for phylogeny, we found little significant relationship between claw geometry and behaviour. ‘Ground-dweller’ claws are less curved and relatively dorsoventrally deep relative to those of other behavioural categories; beyond this it is difficult to assign an explicit category to a claw based purely on geometry.

Geckos significantly alter foot orientation to facilitate adhesion during downhill locomotion

Geckos employ their adhesive system when moving up an incline, but the directionality of the system may limit function on downhill surfaces. Here, we use a generalist gecko to test whether limb modulation occurs on downhill slopes to allow geckos to take advantage of their adhesive system. We examined three-dimensional limb kinematics for geckos moving up and down a 45° slope. Remarkably, the hind limbs were rotated posteriorly on declines, resulting in digit III of the pes facing a more posterior direction (opposite to the direction of travel). No significant changes in limb orientation were found in any other condition. This pes rotation leads to a dramatic shift in foot function that facilitates the use of the adhesive system as a brake/stabilizer during downhill locomotion and, although this rotation is not unique to geckos, it is significant for the deployment of adhesion. Adhesion is not just advantageous for uphill locomotion but can be employed to help deal with the effects of gravity during downhill locomotion, highlighting the incredible multi-functionality of this key innovation.

Swing-Leg Trajectory of Running Guinea Fowl Suggests Task-Level Priority of Force Regulation Rather than Disturbance Rejection

To achieve robust and stable legged locomotion in uneven terrain, animals must effectively coordinate limb swing and stance phases, which involve distinct yet coupled dynamics. Recent theoretical studies have highlighted the critical influence of swing-leg trajectory on stability, disturbance rejection, leg loading and economy of walking and running. Yet, simulations suggest that not all these factors can be simultaneously optimized. A potential trade-off arises between the optimal swing-leg trajectory for disturbance rejection (to maintain steady gait) versus regulation of leg loading (for injury avoidance and economy). Here we investigate how running guinea fowl manage this potential trade-off by comparing experimental data to predictions of hypothesis-based simulations of running over a terrain drop perturbation. We use a simple model to predict swing-leg trajectory and running dynamics. In simulations, we generate optimized swing-leg trajectories based upon specific hypotheses for task-level control priorities. We optimized swing trajectories to achieve i) constant peak force, ii) constant axial impulse, or iii) perfect disturbance rejection (steady gait) in the stance following a terrain drop. We compare simulation predictions to experimental data on guinea fowl running over a visible step down. Swing and stance dynamics of running guinea fowl closely match simulations optimized to regulate leg loading (priorities i and ii), and do not match the simulations optimized for disturbance rejection (priority iii). The simulations reinforce previous findings that swing-leg trajectory targeting disturbance rejection demands large increases in stance leg force following a terrain drop. Guinea fowl negotiate a downward step using unsteady dynamics with forward acceleration, and recover to steady gait in subsequent steps. Our results suggest that guinea fowl use swing-leg trajectory consistent with priority for load regulation, and not for steadiness of gait. Swing-leg trajectory optimized for load regulation may facilitate economy and injury avoidance in uneven terrain.

Human and avian running on uneven ground: a model-based comparison

Birds and humans are successful bipedal runners, who have individually evolved bipedalism, but the extent of the similarities and differences of their bipedal locomotion is unknown. In turn, the anatomical differences of their locomotor systems complicate direct comparisons. However, a simplifying mechanical model, such as the conservative spring–mass model, can be used to describe both avian and human running and thus, provides a way to compare the locomotor strategies that birds and humans use when running on level and uneven ground. Although humans run with significantly steeper leg angles at touchdown and stiffer legs when compared with cursorial ground birds, swing-leg adaptations (leg angle and leg length kinematics) used by birds and humans while running appear similar across all types of uneven ground. Nevertheless, owing to morphological restrictions, the crouched avian leg has a greater range of leg angle and leg length adaptations when coping with drops and downward steps than the straight human leg. On the other hand, the straight human leg seems to use leg stiffness adaptation when coping with obstacles and upward steps unlike the crouched avian leg posture.

Geckos decouple fore- and hind limb kinematics in response to changes in incline.

BackgroundTerrestrial animals regularly move up and down surfaces in their natural habitat, and the impacts of moving uphill on locomotion are commonly examined. However, if an animal goes up, it must go down. Many morphological features enhance locomotion on inclined surfaces, including adhesive systems among geckos. Despite this, it is not known whether the employment of the adhesive system results in altered locomotor kinematics due to the stereotyped motions that are necessary to engage and disengage the system. Using a generalist pad-bearing gecko, Chondrodactylus bibronii, we determined whether changes in slope impact body and limb kinematics.ResultsDespite the change in demand, geckos did not change speed on any incline. This constant speed was achieved by adjusting stride frequency, step length and swing time. Hind limb, but not forelimb, kinematics were altered on steep downhill conditions, thus resulting in significant de-coupling of the limbs.ConclusionsUnlike other animals on non-level conditions, the geckos in our study only minimally alter the movements of distal limb elements, which is likely due to the constraints associated with the need for rapid attachment and detachment of the adhesive system. This suggests that geckos may experience a trade-off between successful adhesion and the ability to respond dynamically to locomotor perturbations.