Energetics of walking and running: insights from simulated reduced-gravity experiments CLAIRE

T. FARLEY

AND

THOMAS

A. McMAHON

Museum of Comparative Zoology, Concord Field Station; Harvard University, Cambridge, Mussachusetts 02138 FARLEY,CLAIRET.,

of walking

and running;

AND

THOMAS

A. MCMAHON.

insights from simulated

Energetics

reduced-gravity

J. Appl. Physiol. 73(6): 2709-2712, 1992.~On Earth, a person usesabout one-half as much energy to walk a mile as to run a mile. On another planet with lower gravity, would walking still be more economical than running? When people carry weights while they walk or run, energetic cost increasesin proportion to the addedload. It would seemto follow that if gravity were reduced, energetic cost would decrease in proportion to body weight in both gaits. However, we find that under simulated reduced gravity, the rate of energy consumption decreasesin proportion to body weight during running but not during walking. When gravity is reducedby 75%,the rate of energy consumptionis reducedby 72%during running but only by 33%during walking. Becausereducing gravity decreasesthe energetic cost much more fur running than for walking, walking is not the cheapest way to travel a mile at low levels of gravity. These results suggestthat the link between the mechanicsof locomotion and energetic cost is fundamentally different for walking and for running. experiments.

locomotion; low gravity; biomechanics animalscarryweights,the rate of energy consumption increases in proportion to the added load. For example, when a human carries weights equivalent to 40% of body weight, the rate of energy consumption during walking or running increases by -40% (14, 15). On the basis of this simple observation, it has been hypothesized that the metabolic rate during running is determined primarily by the cost of generating muscular force to support the weight of the body (11, 15). The load-carrying experiments suggest WHENWALKINGORRUNNING

that this hypothesis may also apply to walking, although this idea has not been closely examined. The purpose of this study is to use simulated reduced gravity to decrease the force that the muscles must generate to support the weight of the body. We predict, on the basis of the hypothesis, that the rate of energy consumption in both walking and running will decrease in proportion to body weight. METHODS

Proto& Four subjects (3 male and 1 female, average mass = 65 kg) who were familiar with treadmill running

and Division

of Applied Sciences,

volunteered to participate in the study. In the first part of the study, the rate of 0, consumption was measured as four subjects walked and ran over a range of speeds on a treadmill at 1.0 G (normal gravity) and 0.5 G (“G” means

“times normal gravity” throughout this paper). In the second part of the study, the rate of 0, consumption was measured as the subjects walked at 1 m/s and ran at 3 m/s at four different levels of gravity (1.0, 0.75, 0.5, and 0.25 G). This part was designed to investigate whether the rate of energy consumption changes as a regular function of gravity in walking and running. In both parts of the study, we checked that the subjects were using the correct gait by videotaping in lateral view at 60 fields per second and following the path of the hip during the stance phase. If the hip was at its highest point at the middle of the stance phase, the gait was defined as a walk, and if the hip was at its lowest point at the middle of the stance phase, the gait was defined as a run. Apparatus for simulating reduced gravity. A simple apparatus was used to simulate reduced gravity while humans walked and ran on a motorized treadmill (Fig. 1) (8). A series of steel springs applied a nearly constant upward force to the body through a bicycle saddle. The springs were the type that are normally used to balance the weight of garage doors (Door Depot, Irving, TX); they were enclosed in a polyvinylchloride tube as a safety precaution. The magnitude of the upward force applied to the body was adjusted by use of a winch to change the length of the springs. This adjustment was made as a subject stood quietly on a force platform mounted in the treadmill (“F” in Fig. 1). We measured the fluctuations in the upward force applied to the body by the springs during locomotion by inserting a force transducer (model 9203, Kistler, Amherst, NY) at point C in Fig. 1. In condi-

tions simulating 0.75, 0.5, and 0.25 G, the cable tension fluctuated by 4.2, 4.0, and 4.1%, respectively, during walking and by 9.5, 6.5, and 2.6% during running. This apparatus allowed a realistic simulation of reduced gravity in terms of the motions of the center of mass but not in terms of the motions of the swinging limbs. Thus the apparatus did not affect the mechanical energy fluctuations associated with accelerating or lifting the limbs during walking and running. However, to

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ENERGETICS

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FIG. 1. Apparatus for simulating reduced gravity, consisting of a series of springs (Sp), which applied a nearly constant upward force to the body through a bicycle saddle (S). Magnitude of for&was increased by stretching springs with a winch (Wj. Motorized treadmill included a strain gauge force platform (F) under the tread (10). [From He et al. (8) -1

test the hypothesis, this apparatus was ideal because it reduced the force that the muscles had to generate to support the weight of the body. Measurement of the metabolic cost of wulking und running. The rate of 0, consumption was measured by use of an open-flow system. Air was drawn through a-loosely fitting mask, and a small fraction of the mask air was continuously analyzed for 0, content by use of a paramagnetic 0, analyzer (Beckman F-3). The system was calibrated after each experiment by bleeding & into the mask at known rates, and the rate of 0, consumption was calculated with the N,-dilution technique, as described in detail by Fedak et al. (7). The rate of 0, consumption during quiet standing was subtracted from the rates for walking and running to calculate the extra 0, consumed for locomotion. The mass-specific metabolic rate (Emetab/Mb) was calculated by dividing the rate of 0, consumption by the mass of the subject (Mb) and using-an energetic equivalent of 20.1 J/ml 0, (3). The mass-specific metabolic rate was divided by the speed to give the net cost of transport (the energetic cost of moving a kilogram of body mass forward a meter). Measurement of the time offoot contact with the ground. The ground contact time (iC> during walking was measured from videotape at 60 fields/s in lateral view. During running, tc was measured using a strain gauge force platform (model OR6-5-1, Advanced Mechanical Technology, Newton, MA) mounted in the treadmill as shown in Fig. 1 (10). The cross talk from a horizontal force to the vertical was cl%, and the natural frequency of the force platform mounted in the treadmill was 160 Hz. The signal was sampled at I kHz. RESULTS

Reducing gravity by 50% (to 0.5 G) had a much larger effect on the metabolic rate during running than it did during walking (Fig. 2A). At both running speeds (2.0 and 3.0 m/s),_. the metabolic rate decreased bvd 40% -- - when -~---

WALKING

AND RUNNING

gravity was reduced to 0.5 G. In walking (0.5-2.0 m/s), metabolic rate decreased by only ~25%. At normal gravity (1.0 G), the net cost of transport (the mass-specific cost of moving a unit distance) was 40% less for walking (at 1 m/s) than for running (at 3 m/s; Fig. 2B). However, it was similar for both gaits when gravity was reduced to 0.5 G. At 1.0 G, the net cost of transport for walking was lower at the intermediate speeds (LO-l.5 m/s) than at the highest and lowest speeds. The existence of an “optimal” speed has been well documented for human walking (12). The optimal speed for walking was not substantially different when gravity was reduced to 0.5 G. When the subjects ran at 3 m/s over a range of gravities, metabolic rate decreased in direct proportion to gravity (Fig. 3A). During walking, the metabolic rate also decreased at lower gravities but much less dramatically than during running. When gravity was reduced by 75% (0.25 G), the metabolic rate was reduced by 72% for running but only by 33% for walking. Our findings about the energetics of walking under reduced gravity are similar to those of Wortz and Prescott (16), who measured the metabolic rate during walking at 1 and 0.25 G by use of a counterweight apparatus to simulate reduced gravity. We are not aware of any studies that have compared the metabolic rate for running at normal and low gravity. A

12-1

0

l.Og

1 2 Speed (m l 8)

3

FIG. 2. A: when gravity was reduced to 0.5 G, metabolic rat.e decreased proportionally during running [analysis of variance (ANOVA), F = 549, P < 0.011 but decreased much less dramatically (-25%) dZing walking (ANOVA, Fl 9 = 130, P < 0.01). Metabolic rate during quiet standing was subtractid to calculate extra energy used for locomotion. Standing metabolic rate was independent of gravity [I.47 t 0.112 (SE) W/kg at 1.0 G and 1.49 -t 0.113 W/kg at 0.5 G, P = 0.581. @, and A, walking at 0.5and 1.0 G, respectively; 0 and l , running at 0.5 and 1.0 G. Values are means t SE for 4 subjects. Lines are leastsquares regressions. B: at normal gravity, net cost of transport was -40% less for walking (at speed where it was minimized, 1 m/s) than for running (at 3 m/s). However, at 0.5 G, it was similar for running and walking. In addition, the minimum cost of transport during walking occurred at intermediate speeds at both levels of gravity. Cost of transport (mass-specific cost of moving a unit distance) was calculated by dividing Emetab/Mb by speed.

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ENERGETICS

OF LOW-GRAVITY

Because reducing gravity decreased the metabolic rate during running much more than during walking, walking was not the cheapest way to travel a unit distance at all levels of gravity (Fig. 3B). When gravity was higher than 0.5 G, the cost of transport was lower for walking than for running. The lines intersected at N0.5 G, where the cost of transport was similar for both gaits. At 0.25 G, the cost of transport was ~45% more for walking than for running, but the difference was not statistically significant at the 95% confidence level (P = 0.056). DISCUSSION

The difference between the energetics of running and walking under reduced gravity may be related to the energy-saving mechanisms associated with each of these gaits. Running humans and other animals literally bounce along the ground, using their muscles, tendons, and ligaments as springs that alternately store and return elastic energy (1,2,&g). Because these springs conserve mechanical energy during running, it makes sense that the metabolic energy consumption cannot be explained in terms of the mechanical energy changes of the body (9). For the body’s springs to operate, the muscles must be activated and generate sufficient force to sup-

0

]

I

0.25

i

I

I

0.50 0.75 1.oo Gravity (g) FIG. 3. A: metabolic rate during running decreased in direct proportion to gravity (Emetab/Mb = -0.005 + 9.88 G, R2 = 0.956, 95% confidence limits of slope = 8.66,11.1, P < 0.01). By contrast, metabolic rate during walking decreased only slightly when gravity was reduced (B m,,,,,/Mb = 1.19 + 0.93 G, R2 = 0.549, 95% confidence limits of slope = 0.45, 1.41, P < 0.01). A, walking at 1 m/s; l , running at 3 m/s. Values are means t SE for 4 subjects. B: walking a unit distance was not cheaper than running at all levels of gravity because reducing gravity had a much larger effect on energy consumption during running than during walking. Above 0.5 G, cost of transport was lower for walking at 1 m/s than for running at 3 m/s. Lines intersected at -0.5 G, where cost of transport was nearly the same for both gaits. At 0.25 G, cost transport was ~45% more for walking than for running, although difference was not statistically significant at 95% confidence level (P = 0.056). Lines are linear least-squares regressions (running: cost of transport = -0.002 + 3.29 G, R2 = 0.956, 95% confidence limits of slope = 2.89,3.70, P = 0.01; walking: cost of transport = 1.19 + 0.93 G, R2 = 0.549, 95% confidence limits of slope = 0.45, 1.41, P < 0.01). 0.00

WALKING

2711

AND RUNNING 1.0

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0.8

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Walk

c2 u aJ E .r(

3 0.6 z 3 0.4 Td s 0.2 -

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T

!I!

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El E3

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0.50 0.75 1.oo Gravity (g) FIG. 4. Time available to apply force to the ground (ground contact time, Q changed only slightly when gravity was reduced in both walking and running (walking: t, = 0.815 - 0.030 G, R2 = 0.017; running: t, = 0.208 + 0.064 G, R2 = 0.379). A, walking at 1 m/s; l , running at 3 m/s. Values are means t SF, for 4 subjects. 0.00

0.25

port the weight of the body. There is evidence that the metabolic cost of generating muscular force to support the weight of the body is the primary cost associated with running. In animals ranging in size from small rodents to horses, the metabolic rate during running simply depends on the weight of the body and the time available to apply force to the ground (the ground contact time) (11). At higher speeds and in smaller animals, the ground contact time is shorter, presumably requiring that force be generated by faster muscle fibers that have crossbridges that cycle and consume ATP at higher rates. In this study, when gravity was reduced, tcchanged only slightly (Fig. 4). Thus the observation that the metabolic rate during running decreased in proportion to gravity is consistent with the idea that the cost of running is determined by the cost of generating muscular force to support the weight of the body. In walking, an exchange of gravitational potential energy and forward kinetic energy has a role similar to the exchange between elastic energy and kinetic energy in running (4,6). Walking humans, as well as other animals, vault over their stance limbs like inverted pendulums, and as a result, there is an exchange between the gravitational potential energy and the forward kinetic energy of the center of mass. At the speed at which the cost of transport is minimized (m I m/s for humans), the fluctuations in potential and kinetic energy are similar in magnitude and nearly completely out of phase, resulting in maximal energy exchange by the pendulum mechanism (6). Margaria and Cavagna (13) predicted that at low gravity the exchange of potential and kinetic energy would be inhibited during moderate-speed walking because the magnitudes of their fluctuations would not be matched. If the displacement and velocity fluctuations of the center of mass are similar at low gravity and normal gravity, the potential energy fluctuations will be reduced in proportion to gravity but the forward kinetic energy fluctuations will be unchanged. As a result, at low gravity, the muscles may have to do more mechanical work to make up for ineffective pendulum exchange of mechanical energy. In addition, because the stance limb posture is straighter in walking than in running, the forces generated by the muscles of the stance limb may be lower in walking. Thus the cost of generating muscular force to support the weight of the body may be less important in

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ENERGETIC!3

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determining the whole body energy consumption in walking than in running. The results of these simulated reduced-gravity experiments suggest that the link between the mechanics of locomotion and energetic cost is fundamentally different fur running and for walking. For running, our results are consistent with the idea that the energetic cost is determined by the cost of generating muscular force to support the weight of the body. For walking, our results show that the energetic cost cannot be explained simply in terms of the cost of supporting the weight of the body. The authors are grateful to C. Richard Taylor, Rodger Kram, and Elizabeth Brainerd for their help with this project. This work was supported by National Institutes of Health Grant RO1 AR 18140 to C. R. Taylor and a Sloan Foundation (New York) grant to T. A. McMahon. Address for reprint requests: C. T. Farley, Dept. of Integrative Biology, University of California, Berkeley, CA 94720. Received 17 April 1992; accepted in final form 20 August 1992. REFERENCES R. McN. Elastic Mechanisms in Animal Movement. Cambridge, UK: Cambridge University Press, 1988, p. l-47. 2. ALEXANDER, R. McN., AND H. C. -BENNET-CLARK. Storage of elastic strain energy in muscle and other tissues. Nature Land. 265: 114-117,1977. 3. BLAXTER, K. Energy Metabolism in Animals and Man. Cambridge, UK: Cambridge University Press, 1989, p. 16-17. 4. CAVAGNA, G. A., N. C. HEGLUND, AND C. R. TAYLOR. Mechanical work in terrestrial locomotion: two basic mechanisms for minimiz-

WALKING

5.

6. 7. 8. 9.

10. 11. 12.

13. 14.

1. ALEXANDER,

15.

AND RUNNING

ing energy expenditure. Am. J. Physiol. 233 (Regulatory Integrative Camp. Physiol. 2): R243-R261, 1977. CAVAGNA, G. A., I?. P. SAIBENE, AND R. MARGARIA. Mechanical work in running. J. Apph Physiul. 19: 249-256, 1964. CAVAGNA, G, A., H. THYS, AND A. ZAMBONI. The sources of external work in level walking and running. J. Physiol. Lond. 262: 639657,1976. FEDAK, M. A., L, ROME, AND H. J. SEEHERMAN. One-step N,-dilution technique for calibrating open-circuit VO, systems. J. AppZ. Physiol. 51: 772-776, 1981. HE, J., R. KRAM, AND T. A. MCMAHON. Mechanics of running under simulated low gravity. J. Appl. Physiol. 71: 863-870, 1991. HEGLUND, N. C., M. A. FEDAK, C. R. TAYLOR, AND G. A. CAVAGNA. Energetics and mechanics of terrestrial locomotion. IV. Total mechanical energy changes as a function of speed and body size in birds and mammals. J. Exp. Biol. 79: 57-66, 1982. KRAM, R., AND A. J. POWELL. A treadmill-mounted force platform. J. Appl. Physiol. 67: 1692-1698, 1989. KRAM, R., AND C. R. TAYLOR. The energetics of running: a new perspective. Nature Lond. 346: 265-267, 1990. MARGARIA, R. Biomechanics and Energetics of Muscular Exercise. Oxford, UK: Oxford University Press, 1976, p. 67-73. MARGARIA, R., AND G. A. CAVAGNA. Human locomotion in subgravity. Aerospace Med. 35: 1140-1146, 1964. PANDOLF, K. B., B. GIVONI, AND R. F. GOLDMAN. Predicting energy expenditure with loads while standing or walking very slowly. J. Appl. Physiol. 43: 577-581, 1978. TAYLOR, C. R., N. C. HEGLUND, T. A. MCMAHON, AND T. R. LOONEY. Energetic cost of generating muscular force during running: a comparison of small and large animals. J. Exp. Biol. 86:

g-18,1980. 16. WORTZ,

E. C., AND E. J. PRESCOTT. Effects of subgravity traction simulation on the energy costs of walking. Aerospace Med. 37: f217-1222,

1966.

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Energetics of walking and running: insights from simulated reduced-gravity experiments.

On Earth, a person uses about one-half as much energy to walk a mile as to run a mile. On another planet with lower gravity, would walking still be mo...
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