Blood flow in guinea fowl Numida meleagris as an indicator of energy expenditure by individual muscles during walking and running

Abstract

Running and walking are mechanically complex activities. Leg muscles must exert forces to support weight and provide stability, do work to accelerate the limbs and body centre of mass, and absorb work to act as brakes. Current understanding of energy use during legged locomotion has been limited by the lack of measurements of energy use by individual muscles. Our study is based on the correlation between blood flow and aerobic energy expenditure in active skeletal muscle during locomotion. This correlation is strongly supported by the available evidence concerning control of blood flow to active muscle, and the relationship between blood flow and the rate of muscle oxygen consumption. We used injectable microspheres to measure the blood flow to the hind-limb muscles, and other body tissues, in guinea fowl (Numida meleagris) at rest, and across a range of walking and running speeds. Combined with data concerning the various mechanical functions of the leg muscles, this approach has enabled the first direct estimates of the energetic costs of some of these functions. Cardiac output increased from 350 ml min −1 at rest, to 1700 ml min −1 at a running speed (∼2.6 m s −1 ) eliciting aV O 2 of 90% ofV O 2 ,max . The increase in cardiac output was achieved via approximately equal factorial increases in heart rate and stroke volume. Approximately 90% of the increased cardiac output was directed to the active muscles of the hind limbs, without redistribution of blood flow from the viscera. Values of mass-specific blood flow to the ventricles, ∼15 ml min −1 g −1 , and one of the hind-limb muscles, ∼9 ml min −1 g −1 , were the highest yet recorded for blood flow to active muscle. The patterns of increasing blood flow with increasing speed varied greatly among different muscles. The increases in flow correlated with the likely fibre type distribution of the muscles. Muscles expected to have many high-oxidative fibres preferentially increased flow at low exercise intensities. We estimated substantial energetic costs associated with swinging the limbs, co-contraction to stabilize the knee and work production by the hind-limb muscles. Our data provide a basis for evaluating hypotheses relating the mechanics and energetics of legged locomotion.

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

“…The ILPO is a biarticular muscle with extensor actions at the hip and the knee (Fig.1). The changes of energy use with speed during level locomotion in guinea fowl, indicate that the ILPO is most important in running, because energy use by this muscle is very low during walking (Ellerby et al, 2005). Evidence from comparative anatomy also suggests that the evolution (or retention) of a large ILPO is specifically associated with fast running in ground dwelling birds.…”

“…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.…”