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

Abstract

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.

Function of a large biarticular hip and knee extensor during walking and running in guinea fowl (Numida meleagris)

“…On balance it seems probable that positive work per stride increases above the value in level running when the birds run uphill. This conclusion is consistent with the substantial increase in energy use by the ILPO during uphill running (Rubenson et al, 2006).…”

“…Estimates of energy use by the ILPO are based on the rate of blood flow to the muscle during activity (Ellerby et al, 2005;Ellerby and Marsh, 2006;Rubenson et al, 2006). Marsh and Ellerby reviewed the use of muscle blood flow as an indicator of muscle energy use and concluded that for aerobically supported exercise the data from human and animal studies support a linear and proportional relationship between blood flow and energy use .…”

“…The speeds used in the blood flow studies are in some cases slightly different from those used here to measure the EMG activity, but are not expected to influence the comparisons. For three of the five birds this speed was 2.78ms , and for the fast running speed used by Ellerby et al we used data collected at 2.78ms -1 (Rubenson et al, 2006;Ellerby et al, 2005). Average EMG values reported in various publications represent either the integrated value divided by the duration of the burst or the integrated value divided by the entire cycle time.…”

“…This running condition was chosen as a reference because it was used in all the relevant studies of muscle blood flow in guinea fowl (Ellerby et al, 2005;Ellerby and Marsh, 2006;Rubenson et al, 2006).…”

“…The third was that changes in active muscle volume, as indicated by electromyographic (EMG) amplitude, would best correlate with changes in muscle energy use when the mechanical function was similar. To test this we examined the activity and mechanical function of the ILPO in relation to muscle energy use as measured by blood flow (Ellerby et al, 2005;Rubenson et al, 2006). We predicted that the relative magnitudes of the changes in volume and energy use would be different when the mechanical function of the muscle changes, e.g.…”