In recent times the term `studies' in science has come to mean the testing of hypotheses through the collection of new data, at least when the science is done correctly. In the title of this classic article it describes something very different: the application of the mind to understanding aspects of the topic, in this case tetrapod mechanics, largely through reflection on the physical rules that the system works within. Such `reflection' is something that many of the luminaries of science had a talent for, and at which Sir James Gray was a master. A key feature of his brilliance, and consequently the longevity – read `continued relevance' – of his work was to sort the complex from the meaningful and cut directly to the relevant issues in spite of the confusion of the morphology he addressed. This reduction to the fundamental issues is a mainstay of many of the leaders of functional morphology and biomechanics and has led to substantial progress in the field over the last several decades; it certainly characterizes the work of such leaders as R. McNeil Alexander and Tom A. McMahon.
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.
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.
- © The Company of Biologists Limited 2007