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First published online June 29, 2007
Journal of Experimental Biology 210, 2401-2402 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.000687
JEB Classics |
HOW ANIMALS MOVE: STUDIES IN THE MECHANICS OF THE TETRAPOD SKELETON
University of Calgary jbertram{at}ucalgary.ca
|
Gray's general approach is even more distinctive when considered in the
context of the era; much of his work was done when the majority of zoology
involved the meticulous cataloguing of physical form, largely to document
changes in characteristics between lineages, now known as character shifts
(Lissman, 1978
). Gray realized
another approach was necessary to `understand' the form that organisms take
and the behaviours utilized in their function: `We cannot hope to analyse
the physiological properties of a locomotory mechanism until we have a
complete and accurate picture of all the forces acting on the body during each
phase of its motion' (Gray,
1939).
Although a substantive contribution, `mechanics of the tetrapod skeleton'
(Gray, 1944) has been more
neglected than heralded. It did, however, have much influence as a precursor
of the terrestrial chapters of Gray's über-influential book Animal
Locomotion (Gray, 1968). As I
consider the impact of this paper my mind most often runs to mistakes that
have been made by not paying adequate attention to what was said by Gray, many
decades previously. The explanation for this neglect? I suspect that the times
and organized thoroughness of Gray's thinking did not conspire to make a
`saleable' presentation. The paper begins with a thorough, and to an extent
laborious, discussion of terrestrial support from the perspective of pure
statics, the branch of mechanics dealing with rigid bodies in equilibrium. The
subject is presented in a complete and logical discussion that should be
worked through by every student of functional morphology, to form a foundation
for considering the dynamic features involved with terrestrial locomotion
where the magnitude of force and fluctuations in momentum and energy become
critical. This paper likely documents Gray's own thought process as he shifted
from considering locomotion in the fluid environments in the previous decade
(Lauder and Tytell, 2004).
Statics can be considered a special case of dynamics and provides the basic
tools necessary to assess all other aspects of terrestrial locomotion. And
this is indeed how Gray used these sections of the paper, as foundations for
the dynamic discussions that followed in section VI, The Limbs as Propulsive
Units. The latter portions of the paper demonstrate Gray's skill at cutting
past complexity of the biological form to focus on the relevant mechanics of
the system. And it is in the latter portions of the paper that I find the
foundations of issues that are currently being investigated, if not always
`studied' in the manner that Gray himself did.
Bypassing the details of the complexity of the muscles, tendons, ligaments
and joints of the tetrapod limb, Gray begins this section by pointing out
that, in locomotion, limbs can function either as struts, providing force
along their long axis, or as levers, providing a moment of force to supply
torque around the attachment point (Gray,
1944; p. 109). Sixty plus years later this same concept is
providing insight into the source of cost in human walking, where it is seen
that properly timed propulsive strut function can have about 1/4 the apparent
cost in walking as using the lever alternative
(Kuo, 2002). Gray used the
multiple force platform data from J. T. Manter's 1938 paper describing the
forces and kinematics of walking in the cat
(Manter, 1938) to extend these
elegant data to a general discussion of locomotion in quadrupeds. Gray was
astute enough to recognize from these data that horizontal accelerations of
one limb could well cause turning moments about the animal's centre of mass,
thus affecting the measured vertical forces
(Gray, 1944; pp.
110–111). As force plate technology became readily available in the
1960s and 1970s, Gray's explanation of the consequences of acceleration became
an important caution and the standard technique was to severely restrict speed
changes in force platform analyses. Unfortunately, in the decades that
followed the reason for this restriction became obscured in the minds of many
who learned the `techniques' of force plate analysis from reports in the
literature. Eventually the speed restriction became interpreted more as an
`inconvenience' and the range considered `constant' was gradually expanded.
Numerous studies during the 1970s and 1980s suffer from not paying adequate
heed to this issue. Gray's assertions on this topic were eventually verified
using a multiple force platform system that was functionally identical to
Manter's, if somewhat technologically more advanced
(Lee et al., 1999).
Other portions of Gray's discussion anticipated a variety of issues that
are currently being actively investigated. Gray noted that static stability,
where the body is stable at every instant, is relevant only to quite slow
movement (Gray, 1944; p. 111)
and by this implies dynamic stability at higher speeds, where the body can be
unstable at any point but achieves overall stability by cycling through
motions that compensate for the instability. Recognizing the influence of
dynamic stability has been an insight into the functioning of fast moving
organisms (Jindrich and Full,
2002). Gray also recognized that the musculature of the axial
skeleton must be coordinated with that of the limbs
(Gray, 1944; p. 112) and his
discussion of this process is consistent with current studies
(Ritter et al., 2001).
Indicative of Gray's ability to focus on the most fundamental issue is his
observation that, neglecting air resistance and when moving on a level
surface, gravity is the only external force acting on the body `and
against this force the animal does no work'
(Gray, 1944; p. 112). Yet we
observe, as Gray did, that locomotion requires substantial metabolic
investment, thus the animal `uses the energy of its muscles almost
exclusively to overcome resistances internal to the body...'. Although
mechanical work `accounting' systems have been employed to study terrestrial
locomotion, none provide a compelling solution to the issue of mechanical work
in locomotion. As the penultimate sentence of the remarkably thorough analysis
of mechanical and metabolic cost of locomotion by the C.R. Taylor research
group at Harvard stated, `We have found that the rate at which muscles of
running animals perform mechanical work during locomotion does not provide a
simple explanation for either the linear increase in metabolic rate with
speed, or the regular change in cost of locomotion with body size'
(Heglund et al., 1982). This
statement sums the understanding in the early 1980s and holds true today. It
is unfortunate for those of us interested in such issues that Sir James Gray
is not available to continue `study' on this most fundamental of problems.
Footnotes
John Bertram writes about Sir James Gray's classic paper on tetrapod locomotion entitled `Studies in the mechanics of the tetrapod skeleton'. A copy of the paper can obtained at http://jeb.biologists.org/cgi/reprint/20/2/88.
References
Gray, J. (1939). Croonian lecture: aspects of animal locomotion. Proc. R. Soc. Lond. B 128, 28-62.
Gray, J. (1944). Studies in the mechanics of
the tetrapod skeleton. J. Exp. Biol.
20, 88-116.
Gray, J. (1968). Animal Locomotion. 479 pp. London: Weidenfield & Nicolson.
Heglund, N. C., Fedak, M. A., Taylor, C. R. and Cavagna, G.
A. (1982). 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.
97, 57-66.
Jindrich, D. L. and Full, R. J. (2002). Dynamic
stabilization of rapid hexapedal locomotion. J. Exp.
Biol. 205,2803
-2823.
Kuo, A. D. (2002). Energetics of actively powered locomotion using the simplest walking model. J. Biomech. Eng. 124,113 -120.[CrossRef][Medline]
Lauder, G. V. and Tytell, E. D. (2004). Three
Gray classics on the biomechanics of animal movement. J. Exp.
Biol. 207,1597
-1599.
Lee, D. V., Bertram, J. E. A. and Todhunter, R. J. (1999). Acceleration and balance in trotting dogs. J. Exp. Biol. 202,3565 -3573.[Abstract]
Lissman, H. W. (1978). James Gray.Biographical Memoirs of the Fellows of the Royal Society . Nov. 1978, 54-70.
Manter, J. T. (1938). Dynamics of quadrupedal walking. J. Exp. Biol. 15,523 -540.
Ritter, D. A., Nassar, P. N., Fife, M. and Carrier, D. R.
(2001). Epaxial muscle function in trotting dogs. J.
Exp. Biol. 204,3053
-3064.
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