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

Abstract

A widely held assumption is that metabolic rate (Ė(met)) 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, Ė(met) 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 (E(cot)). 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 Ė(met) and speed during walking, and both emus and ostriches demonstrated an abrupt change in the slope of Ė(met) versus speed at the gait transition with a linear increase during running. Similar to human locomotion, the minimum net E(cot) calculated after subtracting resting metabolism was lower in walking than in running in both species. However, the difference in net E(cot) between walking and running was less than is found in humans because of a greater change in the slope of Ė(met) 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 E(cot) 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.

Figure 1.

Mean mass-specific metabolic rate (Ė_met) of individual emus as a function of speed (v). Individuals that walked and ran over the full range of speeds (including the slowest speeds) and were used in the ANCOVA (see §3) are shown as black circles. Lines are regressions fitted separately to the walking and running data for all individuals: walking, Ė_met = 5.17 − 4.89v + 4.59v² (r² = 0.94); running, Ė_met = 7.19 + 2.36v (r² = 0.60). Shaded bands indicate the 95% confidence intervals of the predicted mean values from the regressions. The zero speed values represent the metabolic rates for animals standing quietly on the treadmill and are not included in the regression analysis.

Figure 2.

Mass-specific gross metabolic rate (Ė_met) as a function of speed (v) in large ratite birds and humans. The species mean values for emus (n = 6) from this study are shown as black circles. Data from the emu measured by Roberts et al. [30] are represented by white circles (original data provided by Thomas Roberts). Mean values for ostriches from this study are shown as black squares (new data collected in California, n = 5) and black triangles (data collected in Western Australia and used previously to calculate cost of transport by Rubenson et al. [23]; n = 4). Data from the ostrich studied by Fedak & Seeherman [29] are represented by white squares. Rhea data (n = 3) collected by Roberts et al. [30] are shown as white diamonds (original data provided by Thomas Roberts). Metabolic rates plotted for human walking (short-dashed line) and running (long-dashed line) data are regressions through the data from 33 publications, most of which are cited in Rubenson et al. [12]. Solid lines through the emu data from this study are regressions fitted separately to the walking and running data (see figure 1 for equations). Solid lines through the ostrich data are regressions fitted separately to the combined mean walking and running data from this study: walking, Ė_met = −0.50 + 4.10v (r² = 0.93); running, Ė_met = 2.95 + 2.11v (r² = 0.92). Values at zero speed are mean values from this study (emu value offset for clarity) for animals standing quietly on the treadmill and are not included in the regression analyses.

Figure 3.

(a) Mass-specific net cost of transport (J kg⁻¹ m⁻¹) plotted as a function of speed (m s⁻¹) for rheas, emus, ostriches and humans. Symbols are as defined in figure 2. (b) Bars show the number of trials (left axis) recorded at different speeds for emus moving freely through a passageway in a large pen. Solid and dashed curves show the total and net cost of transport, respectively (right axis), for emus calculated from the relations of metabolic rate versus speed for walking and running.

Figure 4.

Allometry of minimal cost of transport in running birds. Non-ratite values (galliform birds considered to be specialized for running) and the regression line for all birds and mammals are from Rubenson et al. [12]. Solid lines are regression lines fitted separately through the non-ratite (11.4M_b^−0.27, r² = 0.97) and ratite (27.7M_b^−0.57, r² = 0.89) data.