Jonas Rubenson

Gait selection in the ostrich: mechanical and metabolic characteristics of walking and running with and without an aerial phase.

It has been argued that minimization of metabolic–energy costs is a primary determinant of gait selection in terrestrial animals. This view is based predominantly on data from humans and horses, which have been shown to choose the most economical gait (walking, running, galloping) for any given speed. It is not certain whether a minimization of metabolic costs is associated with the selection of other prevalent forms of terrestrial gaits, such as grounded running (a widespread gait in birds). Using biomechanical and metabolic measurements of four ostriches moving on a treadmill over a range of speeds from 0.8 to 6.7 m s−1, we reveal here that the selection of walking or grounded running at intermediate speeds also favours a reduction in the metabolic cost of locomotion. This gait transition is characterized by a shift in locomotor kinetics from an inverted–pendulum gait to a bouncing gait that lacks an aerial phase. By contrast, when the ostrich adopts an aerial–running gait at faster speeds, there are no abrupt transitions in mechanical parameters or in the metabolic cost of locomotion. These data suggest a continuum between grounded and aerial running, indicating that they belong to the same locomotor paradigm.

The energetic costs of trunk and distal-limb loading during walking and running in guinea fowl Numida meleagris: I. Organismal metabolism and biomechanics.

SUMMARY We examined the energetic cost of loading the trunk or distal portion of the leg in walking and running guinea fowl (Numida meleagris). These different loading regimes were designed to separately influence the energy use by muscles used during the stance and swing phases of the stride. Metabolic rate, estimated from oxygen consumption, was measured while birds locomoted on a motorized treadmill at speeds from 0.5 to 2.0 m s-1, either unloaded, or with a mass equivalent to 23% of their body mass carried on their backs, or with masses equal to approximately 2.5% of their body mass attached to each tarsometatarsal segment. In separate experiments, we also measured the duration of stance and swing in unloaded, trunk-loaded, or limb-loaded birds. In the unloaded and limb-loaded birds, we also calculated the mechanical energy of the tarsometatarsal segment throughout the stride. Trunk and limb loads caused similar increases in metabolic rate. During trunk loading, the net metabolic rate (gross metabolic rate - resting metabolic rate) increased by 17% above the unloaded value across all speeds. This percentage increase is less than has been found in most studies of humans and other mammals. The economical load carriage of guinea fowl is consistent with predictions based on the relative cost of the stance and swing phases of the stride in this species. However, the available comparative data and considerations of the factors that determine the cost of carrying extra mass lead us to the conclusion that the cost of load carrying is unlikely to be a reliable indicator of the distribution of energy use in stance and swing. Both loading regimes caused small changes in the swing and/or stance durations, but these changes were less than 10%. Loading the tarsometatarsal segment increased its segmental energy by 4.1 times and the segmental mechanical power averaged over the stride by 3.8 times. The increases in metabolism associated with limb loading appear to be linked to the increases in mechanical power. The delta efficiency (change in mechanical power divided by the change in metabolic power) of producing this power increased from 11% in walking to approximately 25% in running. Although tarsometatarsal loading was designed to increase the mechanical energy during swing phase, 40% of the increase in segmental energy occurred during late stance. Thus, the increased energy demand of distal limb loading in guinea fowl is predicted to cause increases in energy use by both stance- and swing-phase muscles.

Reappraisal of the comparative cost of human locomotion using gait-specific allometric analyses

SUMMARY The alleged high net energy cost of running and low net energy cost of walking in humans have played an important role in the interpretation of the evolution of human bipedalism and the biomechanical determinants of the metabolic cost of locomotion. This study re-explores how the net metabolic energy cost of running and walking (J kg–1 m–1) in humans compares to that of animals of similar mass using new allometric analyses of previously published data. Firstly, this study shows that the use of the slope of the regression between the rate of energy expenditure and speed to calculate the net energy cost of locomotion overestimates the net cost of human running. Also, the net energy cost of human running is only 17% higher than that predicted based on their mass. This value is not exceptional given that over a quarter of the previously examined mammals and birds have a net energy cost of running that is 17% or more above their allometrically predicted value. Using a new allometric equation for the net energy cost of walking, this study also shows that human walking is 20% less expensive than predicted for their mass. Of the animals used to generate this equation, 25% have a relatively lower net cost of walking compared with their allometrically predicted value. This new walking allometric analysis also indicates that the scaling of the net energy cost of locomotion with body mass is gait dependent. In conclusion, the net costs of running and walking in humans are moderately different from those predicted from allometry and are not remarkable for an animal of its size.

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

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.

On the ascent: the soleus operating length is conserved to the ascending limb of the force–length curve across gait mechanics in humans

SUMMARY The region over which skeletal muscles operate on their force–length (F–L) relationship is fundamental to the mechanics, control and economy of movement. Yet surprisingly little experimental data exist on normalized length operating ranges of muscle during human gait, or how they are modulated when mechanical demands (such as force output) change. Here we explored the soleus muscle (SOL) operating lengths experimentally in a group of healthy young adults by combining subject-specific F–L relationships with in vivo muscle imaging during gait. We tested whether modulation of operating lengths occurred between walking and running, two gaits that require different levels of force production and different muscle–tendon mechanics, and examined the relationship between optimal fascicle lengths (L0) and normalized operating lengths during these gaits. We found that the mean active muscle lengths reside predominantly on the ascending limbs of the F–L relationship in both gaits (walk, 0.70–0.94 L0; run, 0.65–0.99 L0). Furthermore, the mean normalized muscle length at the time of the peak activation of the muscle was the same between the two gaits (0.88 L0). The active operating lengths were conserved, despite a fundamentally different fascicle strain pattern between walking (stretch–shorten cycle) and running (near continuous shortening). Taken together, these findings indicate that the SOL operating length is highly conserved, despite gait-dependent differences in muscle–tendon dynamics, and appear to be preferentially selected for stable force production compared with optimal force output (although length-dependent force capacity is high when maximal forces are expected to occur). Individuals with shorter L0 undergo smaller absolute muscle excursions (P<0.05) so that the normalized length changes during walking and running remain independent of L0. The correlation between L0 and absolute length change was not explained on the basis of muscle moment arms or joint excursion, suggesting that regulation of muscle strain may occur via tendon stretch.

Joint kinetics in rearfoot versus forefoot running: Implications of switching technique

PURPOSE To better understand the mechanical factors differentiating forefoot and rearfoot strike (RFS) running, as well as the mechanical consequences of switching techniques, we assessed lower limb joint kinetics in habitual and imposed techniques in both groups. METHODS All participants performed both RFS and forefoot strike (FFS) techniques on an instrumented treadmill at 4.5 m·s while force and kinematic data were collected. RESULTS Total (sum of ankle, knee, and hip) lower limb work and average power did not differ between habitual RFS and FFS runners. However, moments, negative work and negative instantaneous and average power during stance were greater at the knee in RFS and at the ankle in FFS techniques. When habitual RFS runners switched to an imposed FFS, they were able to replicate the sagittal plane mechanics of a habitual FFS; however, the ankle internal rotation moment was increased by 33%, whereas the knee abduction moments were not reduced, remaining 48.5% higher than a habitual FFS. In addition, total positive and negative lower limb average power was increased by 17% and 9%, respectively. When habitual FFS runners switched to an imposed RFS, they were able to match the mechanics of habitual RFS runners with the exception of knee abduction moments, which remained 38% lower than a habitual RFS and, surprisingly, a reduction of total lower limb positive average power of 10.5%. CONCLUSIONS There appears to be no clear overall mechanical advantage of a habitual FFS or RFS. Switching techniques may have different injury implications given the altered distribution in loading between joints but should be weighed against the overall effects on limb mechanics; adopting an imposed RFS may prove the most beneficial given the absence of any clear mechanical performance decrements.

Gait-specific energetics contributes to economical walking and running in emus and ostriches

A widely held assumption is that metabolic rate (Ėmet) during legged locomotion is linked to the mechanics of different gaits and this linkage helps explain the preferred speeds of animals in nature. However, despite several prominent exceptions, Ėmet of walking and running vertebrates has been nearly uniformly characterized as increasing linearly with speed across all gaits. This description of locomotor energetics does not predict energetically optimal speeds for minimal cost of transport (Ecot). We tested whether large bipedal ratite birds (emus and ostriches) have gait-specific energetics during walking and running similar to those found in humans. We found that during locomotion, emus showed a curvilinear relationship between Ėmet and speed during walking, and both emus and ostriches demonstrated an abrupt change in the slope of Ėmet versus speed at the gait transition with a linear increase during running. Similar to human locomotion, the minimum net Ecot calculated after subtracting resting metabolism was lower in walking than in running in both species. However, the difference in net Ecot between walking and running was less than is found in humans because of a greater change in the slope of Ėmet versus speed at the gait transition, which lowers the cost of running for the avian bipeds. For emus, we also show that animals moving freely overground avoid a range of speeds surrounding the gait-transition speed within which the Ecot is large. These data suggest that deviations from a linear relation of metabolic rate and speed and variations in transport costs with speed are more widespread than is often assumed, and provide new evidence that locomotor energetics influences the choice of speed in bipedal animals. The low cost of transport for walking is probably ecologically important for emus and ostriches because they spend the majority of their active day walking, and thus the energy used for locomotion is a large part of their daily energy budget.

The cost of running uphill: linking organismal and muscle energy use in guinea fowl (Numida meleagris)

SUMMARY Uphill running requires more energy than level running at the same speed, largely due to the additional mechanical work of elevating the body weight. We explored the distribution of energy use among the leg muscles of guinea fowl running on the level and uphill using both organismal energy expenditure (oxygen consumption) and muscle blood flow measurements. We tested each bird under four conditions: (1) rest, (2) a moderate-speed level run at 1.5 m s–1, (3) an incline run at 1.5 m s–1 with a 15% gradient and (4) a fast level run at a speed eliciting the same metabolic rate as did running at a 15% gradient at 1.5 m s–1 (2.28–2.39 m s–1). The organismal energy expenditure increased by 30% between the moderate-speed level run and both the fast level run and the incline run, and was matched by a proportional increase in total blood flow to the leg muscles. We found that blood flow increased significantly to nearly all the leg muscles between the moderate-speed level run and the incline run. However, the increase in flow was distributed unevenly across the leg muscles, with just three muscles being responsible for over 50% of the total increase in blood flow during uphill running. Three muscles showed significant increases in blood flow with increased incline but not with an increase in speed. Increasing the volume of active muscle may explain why in a previous study a higher maximal rate of oxygen consumption was measured during uphill running. The majority of the increase in energy expenditure between level and incline running was used in stance-phase muscles. Proximal stance-phase extensor muscles with parallel fibers and short tendons, which have been considered particularly well suited for doing positive work on the center of mass, increased their mass-specific energy use during uphill running significantly more than pinnate stance-phase muscles. This finding provides some evidence for a division of labor among muscles used for mechanical work production based on their muscle–tendon architecture. Nevertheless, 33% of the total increase in energy use (40% of the increase in stance-phase energy use) during uphill running was provided by pinnate stance-phase muscles. Swing-phase muscles also increase their energy expenditure during uphill running, although to a lesser extent than that required by running faster on the level. These results suggest that neither muscle–tendon nor musculoskeletal architecture appear to greatly restrict the ability of muscles to do work during locomotor tasks such as uphill running, and that the added energy cost of running uphill is not solely due to lifting the body center of mass.

Programmable mechanical stimulation influences tendon homeostasis in a bioreactor system

Identification of functional programmable mechanical stimulation (PMS) on tendon not only provides the insight of the tendon homeostasis under physical/pathological condition, but also guides a better engineering strategy for tendon regeneration. The aims of the study are to design a bioreactor system with PMS to mimic the in vivo loading conditions, and to define the impact of different cyclic tensile strain on tendon. Rabbit Achilles tendons were loaded in the bioreactor with/without cyclic tensile loading (0.25 Hz for 8 h/day, 0–9% for 6 days). Tendons without loading lost its structure integrity as evidenced by disorientated collagen fiber, increased type III collagen expression, and increased cell apoptosis. Tendons with 3% of cyclic tensile loading had moderate matrix deterioration and elevated expression levels of MMP‐1, 3, and 12, whilst exceeded loading regime of 9% caused massive rupture of collagen bundle. However, 6% of cyclic tensile strain was able to maintain the structural integrity and cellular function. Our data indicated that an optimal PMS is required to maintain the tendon homeostasis and there is only a narrow range of tensile strain that can induce the anabolic action. The clinical impact of this study is that optimized eccentric training program is needed to achieve maximum beneficial effects on chronic tendinopathy management. Biotechnol. Bioeng. 2013; 110: 1495–1507.

Musculoskeletal modelling of an ostrich (Struthio camelus) pelvic limb: influence of limb orientation on muscular capacity during locomotion.

We developed a three-dimensional, biomechanical computer model of the 36 major pelvic limb muscle groups in an ostrich (Struthio camelus) to investigate muscle function in this, the largest of extant birds and model organism for many studies of locomotor mechanics, body size, anatomy and evolution. Combined with experimental data, we use this model to test two main hypotheses. We first query whether ostriches use limb orientations (joint angles) that optimize the moment-generating capacities of their muscles during walking or running. Next, we test whether ostriches use limb orientations at mid-stance that keep their extensor muscles near maximal, and flexor muscles near minimal, moment arms. Our two hypotheses relate to the control priorities that a large bipedal animal might evolve under biomechanical constraints to achieve more effective static weight support. We find that ostriches do not use limb orientations to optimize the moment-generating capacities or moment arms of their muscles. We infer that dynamic properties of muscles or tendons might be better candidates for locomotor optimization. Regardless, general principles explaining why species choose particular joint orientations during locomotion are lacking, raising the question of whether such general principles exist or if clades evolve different patterns (e.g., weighting of muscle force–length or force–velocity properties in selecting postures). This leaves theoretical studies of muscle moment arms estimated for extinct animals at an impasse until studies of extant taxa answer these questions. Finally, we compare our model’s results against those of two prior studies of ostrich limb muscle moment arms, finding general agreement for many muscles. Some flexor and extensor muscles exhibit self-stabilization patterns (posture-dependent switches between flexor/extensor action) that ostriches may use to coordinate their locomotion. However, some conspicuous areas of disagreement in our results illustrate some cautionary principles. Importantly, tendon-travel empirical measurements of muscle moment arms must be carefully designed to preserve 3D muscle geometry lest their accuracy suffer relative to that of anatomically realistic models. The dearth of accurate experimental measurements of 3D moment arms of muscles in birds leaves uncertainty regarding the relative accuracy of different modelling or experimental datasets such as in ostriches. Our model, however, provides a comprehensive set of 3D estimates of muscle actions in ostriches for the first time, emphasizing that avian limb mechanics are highly three-dimensional and complex, and how no muscles act purely in the sagittal plane. A comparative synthesis of experiments and models such as ours could provide powerful synthesis into how anatomy, mechanics and control interact during locomotion and how these interactions evolve. Such a framework could remove obstacles impeding the analysis of muscle function in extinct taxa.