Adaptations for economical bipedal running: the effect of limb structure on three-dimensional joint mechanics

Abstract

The purpose of this study was to examine the mechanical adaptations linked to economical locomotion in cursorial bipeds. We addressed this question by comparing mass-matched humans and avian bipeds (ostriches), which exhibit marked differences in limb structure and running economy. We hypothesized that the nearly 50 per cent lower energy cost of running in ostriches is a result of: (i) lower limb-swing mechanical power, (ii) greater stance-phase storage and release of elastic energy, and (iii) lower total muscle power output. To test these hypotheses, we used three-dimensional joint mechanical measurements and a simple model to estimate the elastic and muscle contributions to joint work and power. Contradictory to our first hypothesis, we found that ostriches and humans generate the same amounts of mechanical power to swing the limbs at a similar self-selected running speed, indicating that limb swing probably does not contribute to the difference in energy cost of running between these species. In contrast, we estimated that ostriches generate 120 per cent more stance-phase mechanical joint power via release of elastic energy compared with humans. This elastic mechanical power occurs nearly exclusively at the tarsometatarso-phalangeal joint, demonstrating a shift of mechanical power generation to distal joints compared with humans. We also estimated that positive muscle fibre power is 35 per cent lower in ostriches compared with humans, and is accounted for primarily by higher capacity for storage and release of elastic energy. Furthermore, our analysis revealed much larger frontal and internal/external rotation joint loads during ostrich running than in humans. Together, these findings support the hypothesis that a primary limb structure specialization linked to economical running in cursorial species is an elevated storage and release of elastic energy in tendon. In the ostrich, energy-saving specializations may also include passive frontal and internal/external rotation load-bearing mechanisms.

Figure 1.

Human and ostrich hind-limb postures during mid-stance of running: (a,b) sagittal plane; (c,d) frontal plane. Note: only the right limb is displayed for the ostrich. The vertical line represents the orientation of the ground reaction force vector. The circular mark represents the position of the combined centre of mass for all lower limb segments of the right limb (excluding pelvis). Differences between limb structures include: (i) a more distal limb-mass distribution in humans compared with ostriches, (ii) a plantigrade posture where the metatarsal bones of the foot are kept in contact with the ground in humans compared with a digitigrade posture in ostriches (walking/running on toes), resulting in a longer effective limb length and an additional joint for storing and releasing elastic energy (tarsometatarso-phalangeal (TMP) joint), and (iii) shorter tendons crossing the distal joints (ankle and TMP) in humans compared with ostriches; tendons crossing these joints originate from muscle–tendon junctions close to the knee joint (and mid-shank for the human soleus). Images developed from Vicon BodyBuilder software (Oxford Metrics, Oxford, UK) and bone images from OpenSim software at corresponding limb postures (SimTK; www.simtk.org). For motion files of ostrich and human running, see electronic supplementary material.

Figure 2.

A graphical representation of the calculation of the negative and positive elastic work and the positive muscle fibre work estimated at the joints during running. The power traces represent scenarios where either (a) all of the positive joint work (area under joint power curve) is provided by the recoil of stored elastic strain energy or (b) where only a fraction of the positive joint work is provided passively by the recoil of stored elastic strain energy with the remainder attributed to muscle fibres.

Figure 3.

Ground reaction force profiles for ostriches (solid lines) and a typical human trace (dotted line): (a) vertical, (b) fore–aft, and (c) medio-lateral directions. Red traces represent ostrich data from those trials used for full three-dimensional joint mechanical analyses (five traces per animal), and blue traces represent data from an additional three animals from which ground reaction forces were collected (five traces per animal).

Figure 4.

(a) Total positive body mass-specific joint mechanical work during limb swing and (b) the average positive body mass-specific mechanical power used to swing the limb during running in ostriches and humans.

Figure 5.

(a) Total positive body mass-specific joint mechanical work estimated to be generated via release of stored elastic energy during the stance phase (single limb), (b) the average positive body mass-specific mechanical power estimated to be generated by the release of elastic energy (both limbs), and (c) the percentage of the total positive mechanical power during the stance phase that is generated by the release of stored elastic energy in ostriches and humans. The asterisk denotes a significant difference between ostriches and humans (p < 0.05).

Figure 6.

The total average positive body mass-specific mechanical power during running in humans and ostriches and the average positive body mass-specific mechanical power estimated to be attributed to muscle fibres. The asterisk denotes a significant difference between ostriches and humans (p < 0.05). White bars, ostrich; black bars, human.

Figure 7.

The average (±s.d.; grey-shaded regions) net mass-specific joint moments in humans (dotted lines) and ostriches (solid lines) over the stride (mid-swing to mid-swing). Solid grey lines, ostrich (TMP). Toe/foot-down and toe-off are designated by the vertical bars (dotted, humans; solid, ostriches). Joint moments are the internal (i.e. muscle) net joint moment (negative values represent moments countering gravity).

Figure 8.

The average (±s.d.; grey shaded regions) mass-specific joint power in humans (dotted lines) and ostriches (solid lines) over the stride (mid-swing to mid-swing). Toe/foot-down and toe-off are designated by the vertical bars. (a,b) Dotted, humans; solid, ostriches. (c) Grey lines, ostrich (TMP).

Figure 9.

The distribution of (a) positive mechanical work and (b) negative mechanical work among the hind-limb joints during stance and swing in ostriches and humans.