PerspectivePhysiology

Running a-Fowl of the Law

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Science  02 Jan 2004:
Vol. 303, Issue 5654, pp. 47-48
DOI: 10.1126/science.1093588

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I came across a colleague searching the grass in a circle of light under a street lamp. “What are you looking for?” I asked. “Keys,” he answered, at which point I started to help him in his search. But after a while it became apparent that we were not finding any keys, so I asked, “Are you sure they're here?” to which he replied “Oh, no, they're not here, they're out there someplace,” gesturing off into the darkness, “but the light's better here!”

Research is often like that. We know specifically what we are looking for, but for one reason or another we are unable to search for it directly. The paper by Marsh et al. (1) [HN1] on page 80 of this issue is a good example of approaching a scientific question indirectly. These authors wanted to measure the metabolic energy required to swing the legs during walking and running, and to compare it to the total metabolic energy requirement. But making this type of measurement in complex animals such as vertebrates is a daunting task. Moving the limbs involves many muscles [HN2]—some working together, some working against each other—with each muscle group showing activity during different phases of the stride cycle. Lacking the means to make direct measurements, Marsh et al. have found a clever substitute.

They used microspheres to measure the distribution of blood flow [HN3] to the hindlimb muscles of guinea fowl [HN4] while the birds were running. They injected a quantity of tiny spheres, each about twice the size of a red blood cell, into the arterial system of the birds, at the level of the heart. These spheres passed easily throughout the arterial system, but they became stuck in the capillaries (the concentration of spheres was low enough to ensure a negligible effect on blood flow). Because blood flow to muscle tissue is controlled locally according to oxygen demand, the density of spheres stuck in a capillary bed is proportional to the blood flow in that volume of muscle, and, by inference, to the oxygen consumption rate. Marsh and colleagues found that swinging the legs consumed a significant fraction of the total energy required for running.

CREDIT: JOE SUTLIFF

What is the interest in measuring the energy required to swing the legs? It is just one part of a long-standing mystery in comparative physiology. Since the late 1970s, we have known that the mass-specific cost of locomotion [HN5]—the metabolic cost (in joules) required to move 1 kg of body mass a distance of 1 m—generally increases with speed and decreases with increasing body size (2). By the early 1980s, we knew that the mass-specific work (in joules) done to move 1 kg of body mass a distance of 1 m also increases with speed even more rapidly than does the energy cost, but the work done appears to be independent of size. One consequence is that the efficiency—the work done divided by the metabolic energy consumed—has a maximum value of only about 5% in a mouse running at high speed; for comparison, this maximum is about 50% in a small pony running at high speed (3). The greater efficiency of locomotion in larger animals appears to be due to storage of energy in elastic structures [HN6] during one phase of the stride cycle, and recovery of that energy at a greatly reduced metabolic cost during a subsequent phase (4). But a peak efficiency of only 5% in small animals is more difficult to rationalize, particularly in light of subsequent isolated-muscle experiments showing that small animal muscle is no less efficient than large animal muscle (5).

Finding this speed and size dependence of whole animal efficiency very unsatisfying, Taylor (6), more than a decade ago, “switched street lamps” and started searching for what he hoped would be a unifying hypothesis to explain simply the energetic cost of locomotion. He came up with what is known as the “force hypothesis [HN7].” Basically, the force hypothesis states that the metabolic cost of walking or running is determined by the tension-time integral multiplied by a factor proportional to the rate of myosin cross-bridge cycling in muscle, independent of whether any work is done. Myosin cross-bridges, the structure that produce force and work in a muscle, undergo cyclic changes in conformation during a contraction [HN8], with each bridge consuming one unit of energy per cycle. Muscles with higher cross-bridge cycling rates are recruited as speed increases; homologous muscles in smaller animals have higher cycling rates than in larger animals. Unfortunately, in the original formulations of the hypothesis, Taylor and collaborators had to assume that the cost of swinging the limbs back and forth was negligible (7). It is this assumption that the Marsh et al. study demonstrates is incorrect, at least in guinea fowl.

The Marsh et al. work is not the first set of experiments to test the force hypothesis. Previous results either did not support the hypothesis or supported it only under such limiting conditions that the original goal of a simple unifying hypothesis was certainly lost. That does not mean that the general idea is totally wrong, but that the original formulation had such fundamental problems that it was undoubtedly incorrect.

The most fundamental problem with the force hypothesis is that energy transduction (for example, metabolic cost) cannot be explained by force—force is not work, force is not even energy. Although force is necessary to realize work, it is not sufficient. A positive force can result in negative work, no work, or positive work, which explains why tests of the force hypothesis that found a correlation between force and cost applied only when conditions were carefully restricted. Why not just ignore work, as stated in the force hypothesis? We cannot do this because the First Law of Thermodynamics requires us to take work into account [HN9]. If metabolic energy is consumed, that energy has to go somewhere. If the energy of a body segment increases, that energy comes from somewhere. If the energy of a body segment decreases, that energy has gone somewhere.

The explanation for the size and speed dependence of the cost of locomotion is still out there in the darkness. We know what we need to do—we need to follow the energy. But for the moment, the light is not shining on the keys. In the meantime, the running guinea fowl of Marsh et al. and the Laws of Thermodynamics are the best we can do.

HyperNotes Related Resources on the World Wide Web

General Hypernotes

Dictionaries and Glossaries

The On-line Medical Dictionary is available on CancerWEB.

A dictionary of biology is provided by Biology Online.

A glossary is provided by McGraw-Hill's Anatomy & Physiology Web site.

Web Collections, References, and Resource Lists

The Google Directory provides links to Internet physiology resources.

The WWW Virtual Library of Physiology and Biophysics is maintained by the Department of Physiology and Biophysics, Weill Medical College of Cornell University.

K. House's Biology Web References for Students and Teachers includes sections of Internet resources related to animal and human physiology.

The Physiological Society provides a collection of Internet links.

The American Physiological Society provides links to Internet resources.

The Harvey Project is a resource for Internet educational physiology materials and links.

Online Texts and Lecture Notes

J. Kimball maintains Kimball's Biology Pages, an online biology textbook and glossary.

The Muscle Physiology Home Page is provided by the Muscle Physiology Laboratory at the University of California, San Diego. An introduction to muscle physiology and design is included.

W. Sellers, Department of Human Sciences, Loughborough University, UK, makes available in PDF format a lecture presentation titled “Studying animal movement.”

A history of the study of locomotion is provided by the Clinical Gait Analysis Web site at the School of Physiotherapy, Curtin University of Technology, Bentley, Australia.

K. Prestwich, Department of Biology, Holy Cross College, Worcester, MA, provides lecture notes for a course on animal physiology.

J. Burns, Department of Biological Sciences, University of Alaska, Anchorage, provides lecture notes for a course on comparative animal physiology. Presentations on movement and biomechanics and animal energetics are included.

W. Wall, Department of Biological and Environmental Sciences, Georgia College and State University, Milledgeville, offers lecture slides for a course on vertebrate biomechanics.

General Reports and Articles

The introductory chapter of Principles of Animal Locomotion by R. M. Alexander is made available on the Web by Princeton University Press.

The Journal of Experimental Biology, a publication of the Company of Biologists, publishes research in comparative animal physiology; free access is available for articles prior to the current year.

The January-February 2002 issue of Harvard Magazine had an article by J. Shaw titled “Hop, skip, and soar: Studying animal locomotion at Harvard's Concord Field Station.”

The Journal of Prosthetics and Orthotics makes available two articles (from volume 9, 1997) by E. Ayyappa: issue 1 (“Normal human locomotion, Part 1: Basic concepts and terminology”) and issue 2 (“Normal human locomotion, Part 2: Motion, ground reaction force and muscle activity”).

The 7 April 2000 issue of Science (a special issue titled “Movement: Molecular to Robotic”) had a review by M. H. Dickinson et al. titled “How animals move: An integrative view.”

P. Frappell, Department of Zoology, La Trobe University, Melbourne, makes available in PDF format an article by D. F. Boggs and P. B. Frappell titled “Unifying principles of locomotion: Forward,” which was the introduction to a collection of symposium papers on locomotion that appeared in the November-December 2000 issue of Physiological and Biochemical Zoology.

Numbered Hypernotes

1. R. L. Marsh, D. J. Ellerby, J. A. Carr, and H. T. Henry are in the Department of Biology, Northeastern University, Boston. C. I. Buchanan is in the Department of Physical Therapy, Northeastern University.

2. Muscles. Kimball's Biology Pages includes a presentation on muscle. The BioMedia Center of the Department of Biology, Purdue University, provides a presentation on the properties of skeletal muscles. G. Ritchison, Department of Biological Sciences, Eastern Kentucky University, provides lecture notes on muscles for a human physiology course. J. Armbruster, Department of Biological Sciences, Auburn University, provides lecture notes on muscles for a course on vertebrate comparative anatomy. W. Wall offers lecture slides on muscles for a course on vertebrate biomechanics. The Department of Biological Sciences, University of California, Santa Cruz, makes available in PDF format lecture notes by C. L. Ortiz on animal muscles and movement for a course on the structure and function of organisms. For a course on functional anatomy, V. Kippers, Department of Anatomical Sciences, University of Queensland, makes available lecture notes on skeletal muscle mechanics. A. Baer, Department of Physiology, Queen's University, Kingston, Canada, offers a series of lecture notes on muscle physiology for a physiology course.

3. Measuring blood flow with microspheres. Triton Technology provides an introduction to their microsphere products and makes available a manual for using Dye-Trak colored microspheres for measurement of regional blood flow in experimental animals. Fluorescent Microsphere Resource Center, University of Washington, Division of Pulmonary and Critical Care Medicine, provides a tutorial on measuring regional organ blood flow with microspheres. The April 1999 issue of the American Journal of Physiology-Heart and Circulatory Physiology had an article by D. Hodeige et al. titled “On the validity of blood flow measurement using colored microspheres.”

4. Guinea fowl. An entry for guinea fowl is included in the Columbia Encyclopedia. Animal Diversity Web from the University of Michigan Museum of Zoology provides a photo of Numida meleagris (helmeted guinea fowl), which is the species used in the research by R. L. Marsh et al. An entry for the helmeted guinea fowl is included in the Wikipedia online encyclopedia. The Roger Williams Park Zoo, Providence, RI, offers an information page on the guinea fowl. The 1 September 2003 issue of the Journal of Experimental Biology had an “Inside JEB” article by K. Phillips about research on running guinea fowls. A video of Numida meleagris is available from the Internet Bird Collection.

5. Locomotion. W. Wall offers lecture slides on terrestrial locomotion for a course on vertebrate biomechanics. E. Schultz, Department of Ecology and Evolutionary Biology, University of Connecticut, provides lecture notes on the energetics of locomotion and terrestrial locomotion for a course on physiological ecology. W. Marshall, Department of Biology, St. Francis Xavier University, Antigonish, NS, Canada, offers a presentation on terrestrial locomotion. J. K. Shim, Department of Kinesiology, Pennsylvania State University, offers a presentation on the biomechanics of locomotion. P. Entin, Department of Exercise Science, Northern Arizona University, provides lecture notes on the biomechanics of animal movement for a course on exercise science. A. Minetti, Department of Exercise and Sport Science, Manchester Metropolitan University, UK, offers a presentation on locomotion research.

6. Energy storage in elastic structures. The Structure and Motion Laboratory at the Royal Veterinary College offers a presentation on elastic mechanisms in locomotion; an animation is provided. V. Kippers includes a section on stored elastic energy in lecture notes on muscle function in walking.

7. C. R. Taylor and the force hypothesis. The 15 July 1999 issue of the Harvard University Gazette included a “Memorial Minute” article about C. Richard Taylor (1939-1995). C. R. Taylor had been director of the Concord Field Station, a Harvard University research facility located in Bedford, MA, which is affiliated with the Museum of Comparative Zoology. The 12 January 1973 issue of Science had an article by C. R. Taylor and V. J. Rowntree titled “Running on two or on four legs: Which consumes more energy?” The 21 February 1997 issue of Science had a report by T. J. Roberts, R. L. Marsh, P. G. Weyand, and C. R. Taylor titled “Muscular force in running turkeys: The economy of minimizing work” and a related Research News article by E. Pennisi titled “A new view of how leg muscles operate on the run.” The 1 October 1998 issue of the Journal of Experimental Biology had an article (full text available in PDF format) by T. J. Roberts, R. Kram, P. G. Weyand, and C. R. Taylor titled “Energetics of bipedal running. I. Metabolic cost of generating force” and an article by T. J. Roberts, M. S. Chen, and C. R. Taylor titled “Energetics of bipedal running. II. Limb design and running mechanics.”

8. Myosin cross-bridge cycling and muscle contraction. The Columbia Encyclopedia has an entry for myosin. The Neuromuscular Disease Center at the University of Washington School of Medicine provides a resource page on myosin with a section on skeletal muscle contraction and relaxation. The BioMedia Center of the Department of Biology, Purdue University, provides an introduction to cross-bridge cycling in a presentation on the properties of skeletal muscles. The Muscle Physiology Home Page offers a presentation on the cross-bridge cycle. M. Ferenczi, Biomedical Sciences Division, Faculty of Medicine, Imperial College London, offers a presentation on muscle contraction. The Myosin Home Page, provided by the Myosin Group, Cambridge, UK, provides a review of the myosin superfamily and a presentation on the actomyosin cross-bridge cycle. K. C. Holmes, Max Planck Institute for Medical Research, Heidelberg offers a presentation on muscle contraction, as well as an animation of the cross-bridge cycle. M. Bárány, Department of Biochemistry and Molecular Biology, University of Illinois at Chicago, provides lecture notes for a course on the biochemistry of muscle contraction.

9. Thermodynamics. M. Farabee's Online Biology Book provides an introduction to the laws of thermodynamics. M. King's Medical Biochemistry Page provides an introduction to the First Law of Thermodynamics. C. R. Nave's HyperPhysics defines force, work, and energy and provides an introduction to the First Law of Thermodynamics. A. Crofts, Department of Biochemistry, University of Illinois, provides lecture notes on the biological applications of thermodynamics concepts for a biophysics course on biological energy conversion.

10. Norman C. Heglund is at the Unité de physiologie et de biomécanique de la locomotion, Université Catholique de Louvain, Belgium.

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