Mammalian spinal biomechanics: postural support in seated macaques
School of Applied Sciences, University of Glamorgan, Trefforest, Pontypridd CF37 1DL, Wales, UK
* e-mail: jgal{at}glam.ac.uk
Accepted 3 April 2002
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Summary |
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Key words: biomechanics, sitting, posture, spine, macaque, Macaca spp
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Introduction |
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Most primates frequently use a seated posture and, indeed, many species
have evolved specialised posterior pads, the ischial callosities, upon which
they sit. The prevalence of sitting was investigated recently by McGraw
(1998), who found that 60-90 %
of the total awake time of six sympatric species of Old World monkeys was
spent during seated activities (feeding, socialising and resting). While there
were some differences among species in terms of their activity-specific
preference for sitting, McGraw
(1998
) demonstrates the high
frequency of use of the sitting posture amongst primates.
If, in these animals, the seated posture is maintained exclusively by active muscular contraction, then an individual may incur an appreciable energetic cost. If, however, the mechanical requirements for postural support were met at least in part by the passive mechanical properties of connective tissue, then metabolic energy would be saved. The aim of this report is to consider whether the ligamentous spine of a macaque (Macaca fascicularis) is capable of providing passive mechanical support for the combined weight of the head, upper body and forelimbs during sitting.
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Materials and methods |
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In this paper, an attempt is made to estimate the bending (flexion) moment required to alter the spinal curvature from the excised `unloaded' condition (e.g. Fig. 2, hyper-extended) to the seated `loaded' condition (e.g. Fig. 1, flexed). The corresponding force will then be calculated by using an estimate for the flexion moment arm. Finally, the calculated force will be compared with the likely proportional weight of the head, upper body and forelimbs.
The calculations are based upon a 2.34 kg macaque (M.
fascicularis) with the spinal dimensions of that shown in
Fig. 2 sitting with the flexed
spinal curve displayed by the `groomer' animal in
Fig. 1 (M. sylvana).
The body morphologies of macaques are highly conserved so that an
extrapolation of the spinal flexion curve from one species to another should
not present a serious problem (e.g. Napier
and Napier, 1967).
Gal (1993a) conducted cyclic
bending (extension and flexion) experiments with ligamentous
lumbarlumbar and lumbosacral intervertebral joints from M.
fascicularis. Negative exponential functions of the form:
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The negative exponential model parameters for M. fascicularis
lumbarlumbar intervertebral joints in flexion are shown in
Table 1 (adapted from
Table 2 in
Gal, 1993a). The mean values of
A and B for L1L2 to L5L6 are shown. These mean values were
used to construct a mean bending equation for macaque lumbarlumbar
intervertebral joints in flexion. The model parameters are also shown for the
M. fascicularis lumbosacral joint in flexion (L6S) for comparison.
While A is notably greater for the lumbosacral joint compared with
the lumbarlumbar intervetebral joints, the values of B were
similar across all macaque intervertebral joints relative to the magnitudes of
their respective standard errors. This would suggest that, mechanistically,
the lumbarlumbar intervertebral joints are similar and, therefore, that
generating a mean equation would seem to be reasonable. Therefore, the mean
lumbarlumbar flexion equation used in this study was:
![]() | (2) |
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The method for estimating the mean change in intervertebral angle from the
unloaded excised state to the loaded in vivo state (during sitting)
was as follows. The unloaded excised intervertebral angles were measured
directly, from a tracing of the X-radiograph shown in
Fig. 2, as the angles between
lines drawn parallel to the long axes of adjacent vertebral centra
(Gal, 1993a). The loaded in
vivo angles were estimated from the external dorsal curve of the
`groomer' animal shown in Fig.
1. Dissections have shown that the spine of M.
fascicularis lies very close to the dorsal surface and that spinous
processes can be palpated along the external dorsal curve
(Gal, 1993a
). It was therefore
assumed that the external dorsal curve was an accurate reflection of the
internal spinal curve, as derived from the sum of the intervertebral joint
angles along the length of the spine. Tangents were drawn to the external
dorsal curve in the approximate regions of L1 and L6. The angle between these
two tangents was estimated to be -20° (negative for flexion, as shown in
Fig. 3), and was subsequently
partitioned equally amongst all the lumbar intervertebral joints, giving
flexion angles of -4° for each of the five joints. The change in
intervertebral angle per joint was taken as the difference between the final
angular position (flexed) and the initial angular position (hyper-extended).
Since hyper-extended joint angles ranged from +3 to +7°, changes in angle
ranged from -7 to -11°, with a mean value of -8.6°
(Table 2). This mean value was
rounded up to the nearest degree, and thus -9° was substituted for
iv in equation 3, allowing the normalised net bending
moment (M/m) to be calculated.
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Results |
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![]() | (3) |
Moments can be generated by an infinite number of combinations of force and moment arm. In the seated posture, the head, upper body and forelimbs of the macaque are displaced ventrally, relative to the spine, and therefore exert a flexion moment about the spine (see Fig. 3). This flexion moment is the product of the collective `weight' of the ventrally displaced masses and the length of the moment arm. Since the lumbar column is oriented almost vertically, each lumbarlumbar intervertebral joint `sees' approximately the same moment arm because the line of action of the weight of the ventrally displaced head, upper body and forelimbs is approximately equidistant from each lumbar intervertebral joint centre. The length of the moment arm may be approximated by considering the location of the centre of the collective mass of the head, upper body and forelimbs, relative to the location of the intervertebral joint centres, in the sagittal plane. Thus, for a 2.34 kg animal with the vertebral dimensions shown in Fig. 2 (i.e. L1L6 is approximately 10 cm) sitting with the same posture as the `groomer' animal shown in Fig. 1, this flexion moment arm would also be approximately 0.10 m (see Fig. 3).
The net force associated with the net required bending moment to support
the observed seated vertebral curvature would be equal to 0.41/0.10 N, or 4.1
N. The total body weight of the 2.34 kg macaque is approximately 23 N; 4.1 N
constitutes approximately 18% of that total. The fraction of the total body
weight attributable to the head, forelimbs and upper body probably lies within
the range 30-40% [estimated from data published by Vilensky
(1979) and Preuschoft et al.
(1998
)]. This means that the
passive support afforded by the flexed ligamentous lumbar spine constitutes
approximately half the total support required to balance the spinal flexion
moment exerted by the head, upper body and forelimbs in the seated posture
exhibited by the `groomer' animal in Fig.
1.
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Discussion |
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The precise ventral bending moment that must be supported at any one time
during sitting is highly variable. Slight changes in the position of the head
and upper body, relative to the spine, can change the moment arm length of
their collective weight and, hence, alter the ventral or flexion moment that
must be supported. Perhaps more importantly, the instantaneous length of reach
of the forelimbs can also change the flexion moment, particularly when one
considers that primates tend to have elongated proximal limb segments
containing muscles with long fibres
(Alexander, 1985) and are
therefore likely to be relatively heavy. More recently, Preuschoft et al.
(1998
) commented that both
prosimian and simian species possessed relatively heavy hands and that there
was little difference between the masses of the upper arms and forearms. These
features give many primate species, including the macaques, relatively heavy
upper limbs which, when significantly displaced in the ventral direction
relative to the spine, would exacerbate the flexion moment requiring support
during sitting.
Thus, any amount of passive mechanical support from the ligamentous lumbar spine would be beneficial in terms of reducing the energetic cost of supporting the seated posture, particularly if the alternative was total support and control by selective activation of the axial musculature. However, it is possible that additional passive mechanisms may be invoked during sitting in these animals. For example, moments resisting excessive spinal flexion may be generated by abdominal compression. The present study was conducted to explore the potential for passive support by the ligamentous lumbar spine only, and comments on additional passive mechanisms at this time are purely speculative.
A passive spinal mechanism for the support of posture during sitting
represents a potentially important energy-saving mechanism for macaques and
possibly other primate species. They spend significant proportions of their
waking hours occupied in grooming and foraging activities, both of which are
performed primarily while seated (e.g.
McGraw, 1998). While connective
tissue structures, notably tendons, have been well documented with respect to
their contribution to locomotor energetics (e.g.
Alexander, 1988
), the
contribution of connective tissues to the energetics of posture have been less
well documented. Dimery et al.
(1985
) have suggested that the
nuchal ligament can function as a supporting spring for large bovids. Their
experiments have shown that the weight of the head could be supported by
strain in this robust, elastin-rich ligament, with a minimal requirement for
muscle activation. Given that grazing is arguably the main activity performed
by many bovids, passive head support must represent a significant
energy-saving mechanism for these animals. It is possible that the ligamentous
spine is working in a similar way in sitting macaques.
In a general sense, when the vertebral column is flexed, dorsal elements
become subjected to tension, while ventral structures become compressed. Gal
(1993b) demonstrated that, if
the ligamentum flavum (the relatively robust yellowish dorsal intervertebral
ligament connecting vertebral arches) was severed, the resistance to applied
flexion moments was almost completely eliminated from the macaque
lumbarlumbar and lumbosacral joints studied. Thus, the integrity of the
ligamentum flavum appeared to be of paramount importance to the function of
the macaque spine in supporting flexion moments. At the same time, the
relatively ventral intervertebral discs did not appear to offer any
significant compressive resistance to the applied flexion moments, at least
within the ranges of angular change evoked during the cyclic bending tests
performed. While the angular changes selected for the cyclic bending
experiments appeared to coincide with the maximum ranges of motion for each
macaque intervertebral joint tested, it is possible that, during sitting,
bending stresses occur in combination with additional compressive and/or
torsional stresses. Quantitative information on the mechanical behaviour of
non-human primate intervertebral joints subjected to combined stress protocols
is unavailable at this time for comparison.
Therefore, it would appear that support of spinal flexion moments is
manifest primarily by the collective strain in ligamenta flava throughout the
vertebral column of the macaque. The yellowish tinge and permitted extension
of these particular spinal ligaments suggest a relatively high elastin
content. To support prolonged static loads, it is important for the structural
material to be resistant to mechanical creep, that is, continued strain
deformation under the application of a fixed prolonged stress. Vertebrate
tendon, which is considered to be a near-pure source of collagen, has been
shown to suffer creep damage (Wang and
Ker, 1995). Elastin, however, is resistant to creep damage
(Wainwright et al., 1976
),
which makes it a more suitable material for such a suspension-type mechanism
of support. Elastin, however, is far less stiff and strong than collagen, so
this type of passive supporting mechanism may have physical limits in terms of
the absolute size of animal that can take advantage of a suspensory-type of
spinal design. The possible influence of scale, in terms of the functional
morphology of the primate spine, warrants further investigation.
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Acknowledgments |
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References |
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Alexander, R. McN. (1985). Body size and limb design in primates and other mammals. In Size and Scaling in Primate Biology (ed. W. L. Jungers), pp.337 -343. New York: Plenum Press.
Alexander, R. McN. (1988). Elastic Mechanisms in Animal Movement. Cambridge: Cambridge University Press.
Dimery, N. J., Alexander, R. McN. and Deyst, K. A. (1985). Mechanics of the ligamentum nuchae of some artiodactyls. J. Zool., Lond. 206,341 -351.
Gal, J. (1993a). Mammalian spinal biomechanics.
I. Static and dynamic mechanical properties of intact intervertebral joints.
J. Exp. Biol. 174,247
-280.
Gal, J. (1993b). Mammalian spinal biomechanics.
II. Intervertebral lesion experiments and mechanisms of bending resistance.
J. Exp. Biol. 174,281
-297.
McGraw, W. S. (1998). Posture and support use of Old World monkeys (Cercopithecidae): The influence of foraging strategies, activity patterns, and spatial distribution of preferred food items. Am. J. Primatol. 46,229 -250.[Medline]
Napier, J. R. and Napier, P. H. (1967). A Handbook of Living Primates, Morphology, Ecology and Behaviour of Nonhuman Primates. London: Academic Press.
Preuschoft, H., Gunther, M. M. and Christian, A. (1998). Size dependence in prosimian locomotion, and its implications for the distribution of body mass. Folia Primatol. 69 (Suppl. 1),60 -81.[Medline]
Vilensky, J. A. (1979). Masses, centres-of-gravity and moments-of-inertia of the body segments of the Rhesus monkey (Macaca mulatta). Am. J. Phys. Anthropol. 50,57 -66.
Wainwright, S. A., Biggs, W. D., Currey, J. D. and Gosline, J. M. (1976). Mechanical Design in Organisms. Princeton, NJ: Princeton University Press.
Wang, X. T. and Ker, R. F. (1995). Creep
rupture of wallaby tail tendons. J. Exp. Biol.
198,831
-845.
Woodward, J. and Hare, T. (1988). The Illustrated Encyclopaedia of Wildlife, vol.14 . London: Orbis Publishing Ltd.
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