Compass gait mechanics account for top walking speeds in ducks and humans

Walking animals use immensely complex combinations of muscle and nerve actions to drive and control their limbs. However, the mechanical principles underlying walking may be simple and general. Walking – in humans at least – is a relatively stiff-limbed gait without aerial phases and is often described as acting as an `inverted pendulum', with kinetic energy E<sub>k</sub> at the beginning of each stance phase translating to gravitational potential energy E<sub>p</sub> as the centre of mass(CoM) rises to its highest point near mid-stance, and returning as E<sub>k</sub> as the body falls towards the end of stance. In its simplest form, walking as an inverted pendulum can be described by a `compass gait' model (McGeer, 1990; Alexander, 1995; Goswami et al., 1997; Garcia et al., 1998) (see also Saunders et al., 1953; Kuo, 2007). This model is planar, has completely rigid limbs, exactly one point-foot in contact with the ground at any time and instantaneous transition between legs. The mechanically-imposed speed limits to walking with compass gait are now well understood (Usherwood, 2005; Srinivasan and Ruina, 2006):at high speeds, especially at high step lengths, the acceleration due to gravity is insufficient to provide the centripetal acceleration requirements of vaulting in an arc over a stiff stance limb. But how generally can such an extremely simple model be useful? Does compass gait mechanics actually restrict walking speeds in humans? And is compass gait mechanics informative for unspecialized bipedal walkers with the relatively crouched limbs and`blurred' walk–run transition typical of many birds(Gatesy and Biewener, 1991; Hancock et al., 2007)? Birds are living bipedal dinosaurs and achieve walking and running gaits despite limb structures markedly different from the familiar mammalian bipeds –humans. Furthermore, some birds walk despite specialization for swimming,resulting in widely spaced hips and foot placements, and further deviation from the assumptions of the compass gait model. Ducks, therefore, present a fascinating comparison with humans: is the mechanical approximation of a compass gait relevant to walking in such a non-specialized walker?

In the present study, we report forceplate-derived measurements of waddling, walking and running in three breeds of duck. We use the term `energy recovery' (ER) (Cavagna et al.,1977) to describe the maximum potential for changes in CoM E<sub>k</sub> and E<sub>p</sub> to be passive, consistent with the inverted pendulum model of walking. We use ER to distinguish between `walking' (high ER) and `running' (low ER) gaits. The importance of lateral motions – `waddling' – to the potential passive qualities of walking is demonstrated by calculating ERs both including and excluding the E_k associated with lateral motions.

The three duck breeds, Aylesbury, Mallard and Indian Runner, are all derived from mallards Anas platyrhyncos (Linnaeus 1758) but have radically different forms (Fig. 1A). The Aylesbury is large, selected for the table. The Mallard used was close to wild-type, if overweight due to domestication. The Indian Runner or Penguin Duck has an upright form associated with highly reduced femora, and was bred for both egg-laying and a `peculiar' shape and carriage(Ashton and Ashton, 2002). Although Aylesbury ducks were clearly not bred for walking efficiency, they demonstrate a reasonable proficiency at walking; historically, they were walked from Aylesbury to London for market, a distance of approximately 70 km(>40 miles). The morphology of all ducks shows some degree of compromise between walking and swimming capability(Biewener and Corning, 2001). They were selected for this study precisely because they cannot be considered specialist cursors. Are these compromised, semi-aquatic animals capable of,and constrained by, the mechanics of inverted pendulum-like walking? And how do they contrast with relatively stiff-limbed humans that are presumably more specialized for effective walking?

The range of possible relative velocities V̂ and step angles swept from the vertical (see Materials and methods) while walking with a compass gait is dependent on the extent to which the vaulting of the body over the stiff stance limb can be considered passive. If the only condition is that sufficient gravity acts in line with the leg to provide enough centripetal acceleration to avoid a toe-drag or take-off(Fig. 2A, blue line), then step angles approaching 90 deg. are theoretically possible. As higher instantaneous speeds are possible near mid-stance (gravity acts directly in line with the leg), mechanical energy has to be applied to both raise and accelerate the body throughout the first half of stance and has to be removed throughout the second half (ER=0). By contrast, with completely passive vaulting mechanics (ER=1) lower maximum step angles are achievable. This is because the body moves most quickly (highest E_k) at the extremes of leg angle (lowest E_p). At this point, not only does a smaller component of gravity act in line with the leg but the requirement for centripetal acceleration of the body about the foot is also highest (Usherwood, 2005). Achieving both passive body mechanics and `take-off' avoidance results in a lower net horizontal velocity for a given leg angle than the constraints of take-off avoidance alone (Fig. 2A).

For perfectly passive vaulting of the body over the foot, there is also a low-speed/high step-angle boundary: very low speeds at high step angles (large step lengths) are impossible because there is insufficient E_k to allow the CoM to rise passively over mid-stance(boundary i in Fig. 2Band Fig. 3) – the body would simply rock upwards and fall back again without ever making it completely over the stance foot. This boundary is probably of more theoretical than applied interest as, with an infinitesimally small energy input to hold,control and release the body at the top of the vault, very slow walking is feasible with large step angles (Fig. 2A, the region in red) with very nearly passive body motions.

With each speed and step angle combination, a step frequency is explicit. This is indicated in a relative form f̂(Fig. 2B and Fig. 3), which gives the step frequency as a multiple of that expected for a swing leg acting as an ideal passive pendulum with mass focused at the foot (see Materials and methods).

It should be noted that this may differ from any true kinematic angle, as it assumes a compass-like gait with a single foot on the ground at any time and symmetry about the vertical.

Kinematic data from previous studies of humans walking(Bertram, 2005) or running(Gutmann et al., 2006) on treadmills were kindly provided by John Bertram. In these studies, the full range of speeds achievable during walking (N=11 subjects) and running(N=5 subjects) were measured. The highest walking speeds were moderately uncomfortable and slightly above the preferred walk–run transition speed. The low running speeds were certainly unnatural, extending well below the preferred run–walk transition speed.

At low speeds, ER (Fig. 1B) for Aylesbury and Mallard ducks is as high as 75%, close to that recorded in cursorial birds (Cavagna et al., 1977; Heglund et al.,1982), humans (Cavagna et al.,1977) and penguins (Griffin and Kram, 2000). At the lowest speeds, this ER is only achieved by the Aylesbury ducks if lateral, or `waddling', E<sub>k</sub> is included (Fig. 1C,D): ER<sub>planar</sub> indicates the ERwithout consideration of lateral motions and falls at the lowest speeds. This is not to suggest that waddling improves efficiency – side-to-side motions are presumably not the purpose of locomotion. A better view is that,at low speeds and, given widely splayed foot placement (presumably due to artificial selection for size or natural selection for swimming capability),lateral forces, displacements and movements are inevitable. However, these(inevitable but `pointless') motions have the potential to be achieved largely passively, though perhaps not without metabolic implications(Donelan et al., 2001).

At V̂>0.7 (or Fr>0.5), ER are universally low – above these speeds, no duck maintains passive, inverted pendulum-like energy interchanges. Low ERs may be interpreted as suggesting a `bouncing' or `running'gait; however, this terminology must be treated with caution. It appears most unlikely that ducks are specialized for elastic energy storage and recovery. They have relatively short legs and thick tendons, probably reflecting some of the compromises in form associated with evolutionary pressures for swimming performance. Therefore, low ERs should be taken as departure from inverted pendulum behaviour, perhaps as `pseudo-elastic' bouncing(Srinivasan and Ruina, 2006; Ruina et al., 2005) but not necessarily involving extensive elastic storage and recoil. Nonetheless, a running gait, even without elastic energy storage, may be a gait choice that minimizes mechanical work and energetic costs at higher speeds under the fundamental constraints of legged bipedal locomotion in gravity(Srinivasan and Ruina,2006).

Despite occasional slow trials, no steps of the Indian Runners displayed high ERs – `running' gaits were maintained at low speeds (see also Fig. 3B). The fact that this is mechanically possible is clear from observations of humans: it is perfectly possible to `run' at no net forward speed(Fig. 3C). Given the ability of all three duck breeds tested to achieve `running' mechanics (albeit predominantly `grounded running' without aerial phases) but the failure of Indian Runners to display inverted-pendulum walking mechanics (high ER), perhaps a better, if distinctly awkward, classification of Indian Runners might be as `Indian Not-Walkers'. Both the Mallards and Indian Runners did achieve aerial phases (`running' distinguished by the traditional kinematic definition) at their highest speeds (Movies 2 and 3 in supplementary material). This differs from the findings of Abourachid(Abourachid, 2001), presumably because the birds in the previous study achieved V̂ only up to 0.7. Running with an aerial phase was not observed by any of the Aylesbury ducks (Movie 1 in supplementary material shows a typical gait).

While discontinuities in kinematics with increasing speed suggest gait transition in some birds (Hayes and Alexander, 1983; Gatesy and Biewener, 1991; Gatesy,1999), the gait transition of ducks from a slow vaulting or`walking' gait (using a mechanical definition) to a faster `running' gait is blurred (Fig. 1B), typical of a number of bird species. In contrast to humans and most mammalian quadrupeds,there is no discontinuity in mechanics apparent with increasing speed. Although a discontinuity in stride parameters is reported in the relatively small and crouched painted quail between relative velocities of 0.6 and 0.8(Gatesy and Biewener, 1991),such a transition is difficult to determine for ducks. However, when step angle and ER are considered together, especially when viewed with the boundary determined by compass gait mechanics(Fig. 2B), a distinction between walking and running gaits can be perceived. Walking (high ER)is achieved with near-passive swing or step frequencies; running, with low ER and beyond the boundary determined by compass gait mechanics, is achieved with above-passive step frequencies. Taking any observed ERvalue as the sole distinguishing boundary between walking and running –especially in cases where ER varies without discontinuities with speed – is certainly arbitrary; however, in order to highlight the relationship between speed, step frequency and ER displayed in Fig. 2B, ER≥0.2 is used as an objective, quantitative condition for walking(Fig. 3A). For steps at ER≥0.2, the mean step frequency is 1.14 f̂. If the swing leg was passive, this would equate to an EPL of 0.78 (see Materials and methods)(Fig. 4A). Considering a real pendulum of even mass distribution results in a passive frequency of 1.22 f̂, swing leg mechanics in walking ducks can be considered near-passive. Therefore, ducks do not walk above a speed consistent with both compass gait and passive swing leg mechanics.

The fact that compass gait walking above V̂=1 is impossible has been understood for many years (e.g. Alexander,1989): above this speed, gravity cannot keep the CoM connected to the stance foot (in contact with the ground) with a stance limb in compression. More recently, similar constraints have been identified but for finite stance angles (Usherwood,2005; Srinivasan and Ruina,2006). Combined with some constraint on step frequency, this suggested an account for the observed walk–run transition speed of humans at approximately V̂=0.7(Fr=0.5) (Usherwood,2005). Since this, research on human swing-limb mechanics(Doke et al., 2005; Doke and Kuo, 2007) highlights that fast human walking is not actually achieved with passive swing-limb mechanics (see also Mochon and McMahon,1980). Indeed, if humans were constrained to walking with a passive (duck-like) swing leg, f̂ would be of the range from 1.2 [derived from Doke et al.(Doke et al., 2005)] to 1.3[from Doke and Kuo (Doke and Kuo,2007)] – close to that for a leg of even mass distribution of f̂=1.22 (see Fig. 4B,C). In order to achieve passive swing leg mechanics at observed step frequencies near top walking speeds (f̂≈2), EPL would have to be a quarter of the leg-length – most unlikely even with considerable leg flexion. If humans did walk with step frequencies determined by passive swing leg mechanics, and were constrained to walking with compass gait mechanics, they (like ducks) would be limited to maximum walking speeds of V̂=0.5 – only 3/4 the observed transition speed (Fig. 3C). Instead, humans increase the range of their walking speeds, while still complying with the constraints of compass gait CoM mechanics, by driving their swing-limbs at well above their natural pendular frequencies. High step frequencies (short step lengths or small step angles) have previously been identified as effective in reducing the energetic losses due to suddenly redirecting the CoM at the start of each step(Kuo, 2001; Kuo, 2002; Donelan et al., 2002); the increased potential walking speed with forced swing legs described here provides an alternative, though certainly not mutually exclusive, account for the relatively high step frequencies of walking humans.

The compass gait model predictions of constraints to step angle and speed presented in the current study are limited to the extreme cases of perfect,near-perfect and absent ER (Fig. 2A), and are based on the assumption of completely stiff stance limbs and consequently a duty factor of exactly 0.5. While this is an appealing and extremely reductionist abstraction allowing simple and intuitive predictions, real bipeds walk with intermediate ER and somewhat compliant limbs. In many cases, even the distinction between walking and running using ER can be obscure or arbitrary. The extent to which additional layers of realism – for instance, a certain degree of limb compliance – can be added to the model before its generality and predictive nature is lost remains to be determined.

Further forceplate measurements of walking bipeds are required to investigate whether it is the ducks or the humans (or both) that stand out as unusual. Also, the 4-legged analogue to the passive compass gait, a 4-bar linkage model (Usherwood et al.,2007) will be further developed to investigate whether similar constraints apply to quadrupeds.

The maximum speed of walking in both specialist (humans) and facultative(ducks) cursors appears constrained by compass gait mechanics. Humans increase their maximum walking speeds by driving their swing-limbs at above natural pendular frequencies. From the combination of the limitations imposed by compass gait mechanics and the cost of driving swing-limbs, predictions concerning maximum walking speeds can be made. Anything restricting the driving of the swing-limb – for instance massive boots or massive lower limb prosthetics – would be predicted to reduce maximum walking speed. Conversely, anything enhancing driving of the swing-limb, for instance spring-like torques about the hip or low-mass prosthetics, should permit higher walking speeds. Therefore, while the compass gait is an exceedingly reductionist model of bipedal walking, it is both effective in accounting for the walk–run transition speed in humans and ducks, and allows useful,intuitive predictions with application to prosthetic and orthotic designs.

We thank John Bertram for sharing his data on humans, and Bridget Brennan,the Van Hage Garden Company, and Sadie Rodgers for lending the ducks. J.R.U. was funded by The Wellcome Trust.