Remarkable muscles, remarkable locomotion in desert-dwelling wildebeest.

Large mammals that live in arid and/or desert environments can cope with seasonal and local variations in rainfall, food and climate1 by moving long distances, often without reliable water or food en route. The capacity of an animal for this long-distance travel is substantially dependent on the rate of energy utilization and thus heat production during locomotion-the cost of transport2-4. The terrestrial cost of transport is much higher than for flying (7.5 times) and swimming (20 times)4. Terrestrial migrants are usually large1-3 with anatomical specializations for economical locomotion5-9, because the cost of transport reduces with increasing size and limb length5-7. Here we used GPS-tracking collars10 with movement and environmental sensors to show that blue wildebeest (Connochaetes taurinus, 220 kg) that live in a hot arid environment in Northern Botswana walked up to 80 km over five days without drinking. They predominantly travelled during the day and locomotion appeared to be unaffected by temperature and humidity, although some behavioural thermoregulation was apparent. We measured power and efficiency of work production (mechanical work and heat production) during cyclic contractions of intact muscle biopsies from the forelimb flexor carpi ulnaris of wildebeest and domestic cows (Bos taurus, 760 kg), a comparable but relatively sedentary ruminant. The energetic costs of isometric contraction (activation and force generation) in wildebeest and cows were similar to published values for smaller mammals. Wildebeest muscle was substantially more efficient (62.6%) than the same muscle from much larger cows (41.8%) and comparable measurements that were obtained from smaller mammals (mouse (34%)11 and rabbit (27%)). We used the direct energetic measurements on intact muscle fibres to model the contribution of high working efficiency of wildebeest muscle to minimizing thermoregulatory challenges during their long migrations under hot arid conditions.

Biomechanics of predator-prey arms race in lion, zebra, cheetah and impala.

The fastest and most manoeuvrable terrestrial animals are found in savannah habitats, where predators chase and capture running prey. Hunt outcome and success rate are critical to survival, so both predator and prey should evolve to be faster and/or more manoeuvrable. Here we compare locomotor characteristics in two pursuit predator-prey pairs, lion-zebra and cheetah-impala, in their natural savannah habitat in Botswana. We show that although cheetahs and impalas were universally more athletic than lions and zebras in terms of speed, acceleration and turning, within each predator-prey pair, the predators had 20% higher muscle fibre power than prey, 37% greater acceleration and 72% greater deceleration capacity than their prey. We simulated hunt dynamics with these data and showed that hunts at lower speeds enable prey to use their maximum manoeuvring capacity and favour prey survival, and that the predator needs to be more athletic than its prey to sustain a viable success rate.

There and back again - a zebra's tale.

Animals need to navigate between resources such as water, food and shelter and how they achieve this is likely to vary with species. Here, using high accuracy GPS data, we study repeated journeys made by wild zebra (Equus quagga) through a naturally vegetated environment to explore whether they consistently follow the same route through the area or whether they use a range of routes to reach their goal. We use a model to distinguish and quantify these two possibilities and show that our observations are consistent with the use of multiple routes. Our model performs better than assuming uniform angular distribution of trajectories. The typical separation of the routes was found to be small (1.96 m), while the scale at which neighboring trajectories are informative to direction of travel was found to be large (with a confidence interval of (1.19, 26.4) m). Our observations are consistent with the hypothesis that zebra are able to navigate without having to return to previously used routes, instead using numerous different routes of similar trajectories.

There and back again - a zebra's tale.

Animals need to navigate between resources such as water, food and shelter, and how they achieve this is likely to vary with species. Here, using high-accuracy GPS data, we studied repeated journeys made by wild plains zebra (Equus quagga) through a naturally vegetated environment to explore whether they consistently follow the same route through the area or whether they use a range of routes to reach their goal. We used a model to distinguish and quantify these two possibilities and show that our observations are consistent with the use of multiple routes. Our model performs better than assuming a uniform angular distribution of trajectories. The typical separation of the routes was found to be small (1.96 m), while the scale at which neighbouring trajectories are informative to direction of travel was found to be large (with a confidence interval of 1.19-26.4 m). Our observations are consistent with the hypothesis that zebra are able to navigate without having to return to previously used routes, instead using numerous different routes of similar trajectories.

Artificial mass loading disrupts stable social order in pigeon dominance hierarchies.

Dominance hierarchies confer benefits to group members by decreasing the incidences of physical conflict, but may result in certain lower ranked individuals consistently missing out on access to resources. Here, we report a linear dominance hierarchy remaining stable over time in a closed population of birds. We show that this stability can be disrupted, however, by the artificial mass loading of birds that typically comprise the bottom 50% of the hierarchy. Mass loading causes these low-ranked birds to immediately become more aggressive and rise-up the dominance hierarchy; however, this effect was only evident in males and was absent in females. Removal of the artificial mass causes the hierarchy to return to its previous structure. This interruption of a stable hierarchy implies a strong direct link between body mass and social behaviour and suggests that an individual's personality can be altered by the artificial manipulation of body mass.

Upwash exploitation and downwash avoidance by flap phasing in ibis formation flight.

Many species travel in highly organized groups. The most quoted function of these configurations is to reduce energy expenditure and enhance locomotor performance of individuals in the assemblage. The distinctive V formation of bird flocks has long intrigued researchers and continues to attract both scientific and popular attention. The well-held belief is that such aggregations give an energetic benefit for those birds that are flying behind and to one side of another bird through using the regions of upwash generated by the wings of the preceding bird, although a definitive account of the aerodynamic implications of these formations has remained elusive. Here we show that individuals of northern bald ibises (Geronticus eremita) flying in a V flock position themselves in aerodynamically optimum positions, in that they agree with theoretical aerodynamic predictions. Furthermore, we demonstrate that birds show wingtip path coherence when flying in V positions, flapping spatially in phase and thus enabling upwash capture to be maximized throughout the entire flap cycle. In contrast, when birds fly immediately behind another bird--in a streamwise position--there is no wingtip path coherence; the wing-beats are in spatial anti-phase. This could potentially reduce the adverse effects of downwash for the following bird. These aerodynamic accomplishments were previously not thought possible for birds because of the complex flight dynamics and sensory feedback that would be required to perform such a feat. We conclude that the intricate mechanisms involved in V formation flight indicate awareness of the spatial wake structures of nearby flock-mates, and remarkable ability either to sense or predict it. We suggest that birds in V formation have phasing strategies to cope with the dynamic wakes produced by flapping wings.

Ground reaction forces of overground galloping in ridden Thoroughbred racehorses.

The horse has evolved to gallop economically at high speed. Limb force increases with speed but direct measures of limb ground reaction forces (GRFs) at gallop are sparse. This study reports GRFs for multiple limbs, using force plates, across seven Thoroughbred racehorses during ridden galloping. The results show peak vertical GRF values of 13.6 N kg-1 (non-lead hindlimb), 12.3 N kg-1 (lead hindlimb), 14.0 N kg-1 (non-lead forelimb) and 13.6 N kg-1 (lead forelimb) at 11.4 m s-1 and recorded values are consistent with those predicted from duty factor. The distribution of body weight between the forelimbs and hindlimbs is approximated to 50:50, and is variable with speed, unlike the 60:40 commonly stated for cursorial quadrupeds in the literature. An even distribution of load on all limbs may help minimise accumulation of fatigue and assist in injury avoidance. Cranio-caudal force data concur with the observation that horses apply a net accelerative impulse with the hindlimbs and a net decelerative impulse with the forelimbs. Capturing GRFs enhances our knowledge on the mechanics of galloping in fast-moving species and provides insight into injury risk and factors limiting athletic performance.

The locomotor kinematics and ground reaction forces of walking giraffes.

Giraffes (Giraffa camelopardalis) possess specialised anatomy. Their disproportionately elongate limbs and neck confer recognised feeding advantages, but little is known about how their morphology affects locomotor function. In this study, we examined the stride parameters and ground reaction forces from three adult giraffes in a zoological park, across a range of walking speeds. The patterns of GRFs during walking indicate that giraffes, similar to other mammalian quadrupeds, maintain a forelimb-biased weight distribution. The angular excursion of the neck has functional links with locomotor dynamics in giraffes, and was exaggerated at faster speeds. The horizontal accelerations of the neck and trunk were out of phase compared with the vertical accelerations, which were intermediate between in and out of phase. Despite possessing specialised morphology, giraffes' stride parameters were broadly predicted from dynamic similarity, facilitating the use of other quadrupedal locomotion models to generate testable hypotheses in giraffes.

Energy turnover in mammalian skeletal muscle in contractions mimicking locomotion: effects of stimulus pattern on work, impulse and energetic cost and efficiency.

Active muscle performs various mechanical functions during locomotion: work output during shortening, work absorption when resisting (but not preventing) lengthening, and impulse (force-time integral) whenever there is active force. The energetic costs of these functions are important components in the energy budget during locomotion. We investigated how the pattern of stimulation and movement affects the mechanics and energetics of muscle fibre bundles isolated from wild rabbits (Oryctolagus cuniculus). The fibres were from muscles consisting of mainly fast-twitch, type 2 fibres. Fibre length was held constant (isometric) or a sinusoidal pattern of movement was imposed at a frequency similar to the stride frequency of running wild rabbits. Duty cycle (stimulation duration×movement frequency) and phase (timing of stimulation relative to movement) were varied. Work and impulse were measured as well as energy produced as heat. The sum of net work (work output-work input) and heat was taken as a measure of energetic cost. Maximum work output was produced with a long duty cycle and stimulation starting slightly before shortening, and was produced quite efficiently. However, efficiency was even higher with other stimulation patterns that produced less work. The highest impulse (considerably higher than isometric impulse) was produced when stimulation started while the muscle fibres were being lengthened. High impulse was produced very economically because of the low cost of producing force during lengthening. Thus, locomotion demanding high work, high impulse or economical work output or impulse requires a distinct pattern of stimulation and movement.

Movement patterns and athletic performance of leopards in the Okavango Delta.

Although leopards are the most widespread of all the big cats and are known for their adaptability, they are elusive and little is known in detail about their movement and hunting energetics. We used high-resolution GPS/IMU (inertial measurement unit) collars to record position, activity and the first high-speed movement data on four male leopards in the Okavango Delta, an area with high habitat diversity and habitat fragmentation. Leopards in this study were generally active and conducted more runs during the night, with peaks in activity and number of runs in the morning and evening twilight. Runs were generally short (less than 100 m) and relatively slow (maximum speed 5.3 m s-1, mean of individual medians) compared to other large predators. Average daily travel distance was 11 km and maximum daily travel distance was 29 km. No direct correlation was found between average daily temperature and travel distance or between season and travel distance. Total daily energy requirements based on locomotor cost and basal metabolic rate varied little between individuals and over time. This study provides novel insights into movement patterns and athletic performance of leopards through quantitative high-resolution measurement of the locomotor, energetic, spatial and temporal movement characteristics. The results are unbiased by methodological and observational limitations characteristic of previous studies and demonstrate the utility of applying new technologies to field studies of elusive nocturnal species.

Matching times of leading and following suggest cooperation through direct reciprocity during V-formation flight in ibis.

One conspicuous feature of several larger bird species is their annual migration in V-shaped or echelon formation. When birds are flying in these formations, energy savings can be achieved by using the aerodynamic up-wash produced by the preceding bird. As the leading bird in a formation cannot profit from this up-wash, a social dilemma arises around the question of who is going to fly in front? To investigate how this dilemma is solved, we studied the flight behavior of a flock of juvenile Northern bald ibis (Geronticus eremita) during a human-guided autumn migration. We could show that the amount of time a bird is leading a formation is strongly correlated with the time it can itself profit from flying in the wake of another bird. On the dyadic level, birds match the time they spend in the wake of each other by frequent pairwise switches of the leading position. Taken together, these results suggest that bald ibis cooperate by directly taking turns in leading a formation. On the proximate level, we propose that it is mainly the high number of iterations and the immediacy of reciprocation opportunities that favor direct reciprocation. Finally, we found evidence that the animals' propensity to reciprocate in leading has a substantial influence on the size and cohesion of the flight formations.

An exploratory clustering approach for extracting stride parameters from tracking collars on free-ranging wild animals.

Changes in stride frequency and length with speed are key parameters in animal locomotion research. They are commonly measured in a laboratory on a treadmill or by filming trained captive animals. Here, we show that a clustering approach can be used to extract these variables from data collected by a tracking collar containing a GPS module and tri-axis accelerometers and gyroscopes. The method enables stride parameters to be measured during free-ranging locomotion in natural habitats. As it does not require labelled data, it is particularly suitable for use with difficult to observe animals. The method was tested on large data sets collected from collars on free-ranging lions and African wild dogs and validated using a domestic dog.

Flying in a flock comes at a cost in pigeons.

Flying birds often form flocks, with social, navigational and anti-predator implications. Further, flying in a flock can result in aerodynamic benefits, thus reducing power requirements, as demonstrated by a reduction in heart rate and wingbeat frequency in pelicans flying in a V-formation. But how general is an aerodynamic power reduction due to group-flight? V-formation flocks are limited to moderately steady flight in relatively large birds, and may represent a special case. What are the aerodynamic consequences of flying in the more usual 'cluster' flock? Here we use data from innovative back-mounted Global Positioning System (GPS) and 6-degrees-of-freedom inertial sensors to show that pigeons (1) maintain powered, banked turns like aircraft, imposing dorsal accelerations of up to 2g, effectively doubling body weight and quadrupling induced power requirements; (2) increase flap frequency with increases in all conventional aerodynamic power requirements; and (3) increase flap frequency when flying near, particularly behind, other birds. Therefore, unlike V-formation pelicans, pigeons do not gain an aerodynamic advantage from flying in a flock. Indeed, the increased flap frequency, whether due to direct aerodynamic interactions or requirements for increased stability or control, suggests a considerable energetic cost to flight in a tight cluster flock.

Determining position, velocity and acceleration of free-ranging animals with a low-cost unmanned aerial system.

Unmanned aerial systems (UASs), frequently referred to as 'drones', have become more common and affordable and are a promising tool for collecting data on free-ranging wild animals. We used a Phantom-2 UAS equipped with a gimbal-mounted camera to estimate position, velocity and acceleration of a subject on the ground moving through a grid of GPS surveyed ground control points (area ∼1200 m(2)). We validated the accuracy of the system against a dual frequency survey grade GPS system attached to the subject. When compared with GPS survey data, the estimations of position, velocity and acceleration had a root mean square error of 0.13 m, 0.11 m s(-1) and 2.31 m s(-2), respectively. The system can be used to collect locomotion and localisation data on multiple free-ranging animals simultaneously. It does not require specialist skills to operate, is easily transported to field locations, and is rapidly and easily deployed. It is therefore a useful addition to the range of methods available for field data collection on free-ranging animal locomotion.

Skinned fibres produce the same power and force as intact fibre bundles from muscle of wild rabbits.

Skinned fibres have advantages for comparing the muscle properties of different animal species because they can be prepared from a needle biopsy taken under field conditions. However, it is not clear how well the contractile properties of skinned fibres reflect the properties of the muscle fibres in vivo. Here, we compare the mechanical performance of intact fibre bundles and skinned fibres from muscle of the same animals. This is the first such direct comparison. Maximum power and isometric force were measured at 25 °C using peroneus longus (PL) and extensor digiti-V (ED-V) muscles from wild rabbits (Oryctolagus cuniculus). More than 90% of the fibres in these muscles are fast-twitch, type 2 fibres. Maximum power was measured in force-clamp experiments. We show that maximum power per volume was the same in intact (121.3 ± 16.1 W l(-1), mean ± s.e.m.; N=16) and skinned (122.6 ± 4.6 W l(-1); N=141) fibres. Maximum relative power (power/F(IM) Lo, where F(IM) is maximum isometric force and Lo is standard fibre length) was also similar in intact (0.645 ± 0.037; N=16) and skinned (0.589 ± 0.019; N=141) fibres. Relative power is independent of volume and thus not subject to errors in measurement of volume. Finally, maximum isometric force per cross-sectional area was also found to be the same for intact and skinned fibres (181.9 kPa ± 19.1; N=16; 207.8 kPa ± 4.8; N=141, respectively). These results contrast with previous measurements of performance at lower temperatures where skinned fibres produce much less power than intact fibres from both mammals and non-mammalian species.

Markerless 3D kinematics and force estimation in cheetahs.

The complex dynamics of animal manoeuvrability in the wild is extremely challenging to study. The cheetah (Acinonyx jubatus) is a perfect example: despite great interest in its unmatched speed and manoeuvrability, obtaining complete whole-body motion data from these animals remains an unsolved problem. This is especially difficult in wild cheetahs, where it is essential that the methods used are remote and do not constrain the animal's motion. In this work, we use data obtained from cheetahs in the wild to present a trajectory optimisation approach for estimating the 3D kinematics and joint torques of subjects remotely. We call this approach kinetic full trajectory estimation (K-FTE). We validate the method on a dataset comprising synchronised video and force plate data. We are able to reconstruct the 3D kinematics with an average reprojection error of 17.69 pixels (62.94% PCK using the nose-to-eye(s) length segment as a threshold), while the estimates produce an average root-mean-square error of 171.3N ( ≈ 17.16% of peak force during stride) for the estimated ground reaction force when compared against the force plate data. While the joint torques cannot be directly validated against ground truth data, as no such data is available for cheetahs, the estimated torques agree with previous studies of quadrupeds in controlled settings. These results will enable deeper insight into the study of animal locomotion in a more natural environment for both biologists and roboticists.

Proactive cursorial and ambush predation risk avoidance in four African herbivore species.

Most herbivores must balance demands to meet nutritional requirements, maintain stable thermoregulation and avoid predation. Species-specific predator and prey characteristics determine the ability of prey to avoid predation and the ability of predators to maximize hunting success. Using GPS collar data from African wild dogs, lions, impala, tsessebes, wildebeest and zebra in the Okavango Delta, Botswana, we studied proactive predation risk avoidance by herbivores. We considered predator activity level in relation to prey movement, predator and prey habitat selection, and preferential use of areas by prey. We compared herbivore behaviour to lion and wild dog activity patterns and determined the effect of seasonal resource availability and prey body mass on anti-predator behaviour. Herbivore movement patterns were more strongly correlated with lion than wild dog activity. Habitat selection by predators was not activity level dependent and, while prey and predators differed to some extent in their habitat selection, there were also overlaps, probably caused by predators seeking habitats with high prey abundance. Areas favoured by lions were used by herbivores more when lions were less active, whereas wild dog activity level was not correlated with prey use. Prey body mass was not a strong predictor of the strength of proactive predation avoidance behaviour. Herbivores showed stronger anti-predator behaviours during the rainy season when resources were abundant. Reducing movement when top predators are most active and avoiding areas with a high likelihood of predator use during the same periods appear to be common strategies to minimize predation risk. Such valuable insights into predator-prey dynamics are only possible when using similar data from multiple sympatric species of predator and prey, an approach that should become more prevalent given the ongoing integration of technological methods into ecological studies.

Mechanical and energetic scaling relationships of running gait through ontogeny in the ostrich (Struthio camelus).

It is unclear whether small animals, with their high stride frequency and crouched posture, or large animals, with more tendinous limbs, are more reliant on storage and return of elastic energy during locomotion. The ostrich has a limb structure that appears to be adapted for high-speed running with long tendons and short muscle fibres. Here we investigate biomechanics of ostrich gait through growth and, with consideration of anatomical data, identify scaling relationships with increasing body size, relating to forces acting on the musculoskeletal structures, effective mechanical advantage (EMA) and mechanical work. Kinematic and kinetic data were collected through growth from running ostriches. Joint moments scaled in a similar way to the pelvic limb segments as a result of consistent posture through growth, such that EMA was independent of body mass. Because no postural change was observed, relative loads applied to musculoskeletal tissues would be predicted to increase during growth, with greater muscle, and hence tendon, load allowing increased potential for elastic energy storage with increasing size. Mass-specific mechanical work per unit distance was independent of body mass, resulting in a small but significant increase in the contribution of elastic energy storage to locomotor economy in larger ostriches.

Power output of skinned skeletal muscle fibres from the cheetah (Acinonyx jubatus).

Muscle samples were taken from the gluteus, semitendinosus and longissimus muscles of a captive cheetah immediately after euthanasia. Fibres were 'skinned' to remove all membranes, leaving the contractile filament array intact and functional. Segments of skinned fibres from these cheetah muscles and from rabbit psoas muscle were activated at 20°C by a temperature-jump protocol. Step and ramp length changes were imposed after active stress had developed. The stiffness of the non-contractile ends of the fibres (series elastic component) was measured at two different stress values in each fibre; stiffness was strongly dependent on stress. Using these stiffness values, the speed of shortening of the contractile component was evaluated, and hence the power it was producing. Fibres were analysed for myosin heavy chain content using gel electrophoresis, and identified as either slow (type I) or fast (type II). The power output of cheetah type II fibre segments was 92.5±4.3 W kg(-1) (mean ± s.e., 14 fibres) during shortening at relative stress 0.15 (the stress during shortening/isometric stress). For rabbit psoas fibre segments (presumably type IIX) the corresponding value was significantly higher (P<0.001), 119.7±6.2 W kg(-1) (mean ± s.e., 7 fibres). These values are our best estimates of the maximum power output under the conditions used here. Thus, the contractile filament power from cheetah was less than that of rabbit when maximally activated at 20°C, and does not account for the superior locomotor performance of the cheetah.

High speed galloping in the cheetah (Acinonyx jubatus) and the racing greyhound (Canis familiaris): spatio-temporal and kinetic characteristics.

The cheetah and racing greyhound are of a similar size and gross morphology and yet the cheetah is able to achieve a far higher top speed. We compared the kinematics and kinetics of galloping in the cheetah and greyhound to investigate how the cheetah can attain such remarkable maximum speeds. This also presented an opportunity to investigate some of the potential limits to maximum running speed in quadrupeds, which remain poorly understood. By combining force plate and high speed video data of galloping cheetahs and greyhounds, we show how the cheetah uses a lower stride frequency/longer stride length than the greyhound at any given speed. In some trials, the cheetahs used swing times as low as those of the greyhounds (0.2 s) so the cheetah has scope to use higher stride frequencies (up to 4.0 Hz), which may contribute to it having a higher top speed that the greyhound. Weight distribution between the animal's limbs varied with increasing speed. At high speed, the hindlimbs support the majority of the animal's body weight, with the cheetah supporting 70% of its body weight on its hindlimbs at 18 m s(-1); however, the greyhound hindlimbs support just 62% of its body weight. Supporting a greater proportion of body weight on a particular limb is likely to reduce the risk of slipping during propulsive efforts. Our results demonstrate several features of galloping and highlight differences between the cheetah and greyhound that may account for the cheetah's faster maximum speeds.