Adaptive and phylogenetic influences on musculoskeletal design in cercopithecine primates
Department of Anthropology, Harvard University, 11 Divinity Avenue, Cambridge, MA 02138, USA
e-mail: jpolk{at}fas.harvard.edu
Accepted 7 August 2002
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Summary |
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Key words: interspecific scaling, kinematics, limb proportions, effective mechanical advantage, cercopithecine, monkey
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Introduction |
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The majority of the data on size-related changes in locomotor postures and
bone strength are derived from broad interspecific allometric analyses. Such
studies can often serve to identify fundamental organizing principles that
explain much of the variation in biological phenomena. That body mass is an
important factor in explaining variation in terrestrial locomotion is well
established and follows from the need for all terrestrial animals to overcome
the ubiquitous force of gravity. However, the adaptive and phylogenetic
diversity included in such broad samples of mammals may obscure the functional
relationship between body mass and locomotor variables. For example, the
scaling relationships for joint surface areas for specific clades of mammals
differ from those for across-clade comparisons
(Godfrey et al., 1991).
Consequently, the need for phylogenetic control in comparative and scaling
analyses has been increasingly emphasized
(Harvey and Pagel, 1991
;
Felsenstein, 1985
;
Martins, 1996
). In addition,
species included in broad interspecific samples frequently vary widely in
their locomotor adaptations.
The anatomical specializations related to differences in locomotor behavior may also influence both the limb postures and the mechanical advantage of muscles required to maintain these postures. For instance, the moment arm of the GRF about any joint depends on the relative length of the segments distal to that joint (Fig. 1). Consequently, animals with longer limb segments are predicted to experience higher moments at that joint (compared with shorter-limbed animals) unless they alter their posture to moderate these increased moments.
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Limb proportion effects on bone loading and body posture are also implied
by the scaling of humeral and femoral cross-sectional properties in three
orders of mammal (Polk et al.,
2000). When regressed either on bone length or on the product of
body mass and bone length, the estimated resistance to bending and compression
in the humerus scaled isometrically in primates, carnivorans and rodents. This
isometric scaling implies either that safety factors are lower in animals with
longer forelimbs (with no changes in joint posture) or that behavioral changes
must occur to moderate the bending loads that their humeri experience. In
contrast, femoral cross-sectional properties scaled with positive allometry,
suggesting that the femora of longer-limbed primates may be able to resist
increased bending without the need for postural adjustments.
The goal of this study is to test for phylogenetic and adaptive influences
on locomotor postures and behavior in a closely related sample of mammals.
Adaptive influences on locomotor postures are tested by comparing joint
postures and moments among animals that have the same body mass but that
differ in their body proportions. Phylogenetic effects will be recognized if
the scaling of locomotor variables differs between a phylogenetically
restricted and a phylogenetically diverse sample of mammals (Biewener,
1983,
1989
). Two specific hypotheses
will be tested: (i) that, among animals of similar body mass, those with
longer limb segments will have more extended joint postures, lower (or equal)
joint moments and a greater effective mechanical advantage for the extensor
muscles; (ii) that body mass will have a similar effect on closely related and
phylogenetically diverse samples of mammals. That is, animals with a larger
body mass will have more extended joint postures, lower (or equal) joint
moments and a greater effective mechanical advantage for their extensor
muscles (Biewener, 1983
,
1989
).
Cercopithecine primates are an ideal group in which to examine the effects
of body mass and limb proportions. Primates have longer limbs relative to
their body mass than most other mammals; they also take longer strides and
have greater amounts of forelimb protraction and hindlimb retraction
(Alexander et al., 1979;
Alexander and Maloiy, 1984
;
Reynolds, 1987
;
Larson, 1998
;
Larson et al., 2000
). As a
consequence, primates may either experience relatively larger joint moments
than other mammals or they should be more likely than other mammals to show
limb-proportion-related changes in the mechanical advantage of their limb
extensor muscles. The Cercopithecinae is an extremely well supported clade in
both morphological and molecular phylogenies
(Strasser and Delson, 1987
;
Groves, 2000
;
Disotell, 2000
), and
cercopithecines show a remarkable degree of morphological similarity in their
postcranial anatomy (Schultz,
1970
). Furthermore, if mass and proportion-related differences in
posture are observed between these primate taxa, the results should assist in
making functional interpretations about the postures used by some hominin taxa
that also differ in both mass and limb proportions
(Jungers, 1982
;
McHenry, 1991
).
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Materials and methods |
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The sample size was limited to one male and one female of each species
because of the difficulties in housing and training cercopithecine primates as
well as the considerable time required to digitize video sequences.
Nevertheless, these data are significant because they constitute the first
three-dimensional study of locomotor kinematics in non-human primates and,
while the results reflect interindividual differences in locomotor posture,
the morphological differences among these individuals closely mirror the size
and body proportion differences observed between larger samples of these
species (Gebo and Sargis,
1993; Strasser,
1992
). Thus, the results described below should also reflect
interspecific differences in locomotor behavior.
Absolute lengths of the limb segments for each of the three 15 kg monkeys
are shown in Fig. 2B. As noted
above, the length of the limb segments distal to a particular joint is
predicted to be a major influence on the moments experienced at that joint
(Fig. 1), and the animals with
longer limb segments are predicted to have more extended joint postures
(including lower angular excursions and lower protraction and retraction
angles at the hip and shoulder), correspondingly lower or equivalent joint
moments and greater effective mechanical advantage for their extensor
musculature. The male patas has relatively longer hindlimbs and longer
segments distal to the knee than either baboon. The forelimbs, segments distal
to the elbow, and feet of the patas were similar in length to those of the
male baboon, but these segments were longer in the male monkeys than in the
female baboon. The hand segment was similar in length between the female
baboon and the patas, while the male baboon had longer hands. The differences
in body mass and proportions among these individuals closely reflect the
differences observed between larger samples of these taxa
(Gebo and Sargis, 1993;
Strasser, 1992
). A summary of
predicted differences between the three 15 kg individuals is given in
Table 2.
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Three-dimensional kinematic and ground reaction force data were collected as the animals moved through a Lexan and plywood tunnel (11 mx1.2 m) at the Primate Locomotion Laboratory at SUNY, Stony Brook, USA. A three-camera video-based motion-analysis system (Peak Performance Technologies, Inc., Englewood, CO, USA) was used to measure the three-dimensional positions of reflective markers attached to the shaved skin overlying several bony landmarks (Table 3). Limb segments were defined by connecting adjacent limb markers, and joint angles were measured between adjacent segments. Three-dimensional angles were measured at the wrist, elbow, shoulder, ankle, knee and hip at mid-stance (MS). Protraction and retraction angles were obtained for the arm, forelimb, thigh and hindlimb at touch-down (TD) and lift-off (LO), respectively. Protraction and retraction angles for the forelimb and hindlimb were measured relative to a transverse plane passing through the shoulder and hip, respectively. Angular excursions (AEs) for the arm, forelimb, thigh and hindlimb were calculated as the sum of protraction and retraction angles. Video cameras were shuttered at 1/1000 s or 1/2000 s to avoid motion blur, and cameras were operated at both 60 and 180 Hz for animals weighing more than 15 kg and exclusively at 180 Hz for animals weighing less than 15 kg.
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Three-dimensional ground reaction force (GRF) components were measured
using a Kistler 9281B force platform (Kistler Instruments, Winterthur,
Switzerland) and recorded digitally, at 2700 Hz, using National Instruments
hardware and Lab View software (National Instruments, Austin, TX, USA).
Kinematic and kinetic data were synchronized using an Event-Video Coordinating
Unit (EVCU) and Peak Motus software. Synchronization pulses were generated by
the EVCU and recorded both on kinematic video tapes and in kinetic data files.
The Peak Motus software unites these two data sources, thereby allowing the
alignment of a single video frame with the start of the synchronization pulse
located in the analog force data file. The absolute accuracy of this
synchronization is determined by the frequency of the kinematic data (i.e.
maximum alignment errors are less than the duration of one frame). The
three-dimensional GRF vector resultant was projected upwards from the distal
end of the metatarsal or metacarpal (for fore- and hindlimb measurements,
respectively). External joint moments were estimated in Peak Motus software,
following Biewener (1983), as
the product of the GRF magnitude and the (three-dimensional) perpendicular
distance between the GRF vector and each limb joint (GRF moment arm).
Anatomical moment arms were measured from lateral-view radiographs for the
elbow, knee and ankle as the maximum perpendicular distance between the line
of action of the muscle (assumed to be parallel to the long axis of the bone
proximal to the joint in question) and the joint center of rotation. Joint
centers of rotation for the elbow, knee and ankle were assumed to be the
center of the humeral trochlea, the point of contact between the femur and
tibia and the anteroposterior center of the tibia's distal articular surface,
respectively. Muscle insertion points on the ulna, patella, tibia and
calcaneus were confirmed by dissection of conspecific cadaver specimens.
Effective mechanical advantages (EMAs) for these extensor (and plantar flexor)
muscles were calculated as the ratio of the anatomical moment arm to the GRF
moment arm (Biewener, 1989) at
the time of mid-support (mid-support was identified when the hip was over the
metatarsal or the shoulder over the metacarpal marker for the hindlimb and
forelimb, respectively). EMA measurements were obtained for all adult monkeys,
but not for the subadult male baboon. In addition, EMA measurements were not
obtained for the shoulder, hip or wrist because of the difficulty in measuring
muscle moment arms at these joints.
A total of 528 strides at a range of walking speeds comprised the study sample. At least 60 strides were included for each individual monkey to characterize limb kinematics, and at least 30 of these strides included both kinematic and kinetic data (Table 4). Walking speeds are shown in Fig. 3. The male patas tended to use faster walking speeds than the other monkeys while the male baboon tended to use slower speeds. Only walking speeds were included in this analysis since the male baboon would not gallop.
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Two general types of comparisons are reported here. First, kinematic and
kinetic variables are compared among the three individuals with similar body
mass but different limb proportions. Second, kinematic and kinetic variables
are scaled across the entire sample of adult primates and compared with those
for a diverse sample of mammals. For the first comparison, kinematic and
kinetic variables were compared between individuals using either analyses of
variance (ANOVAs) or analyses of covariance (ANCOVAs) depending on whether the
variables were significantly correlated with speed. For variables not
correlated with speed, the significance of differences between individuals was
tested using ANOVAs with post-hoc comparisons conducted using the
least-significant-difference method (Sokal
and Rohlf, 1995). ANCOVAs, with speed as the covariate, were used
to evaluate differences between individuals when variables were significantly
correlated with speed. In the ANCOVA, least-squares means (LSMs) for each
individual were obtained at the mean walking speed, and significant
differences in LSMs indicated significant differences between individuals for
a particular variable (Green et al.,
2000
). In the event that a variable was correlated with speed for
one individual but not the other, ANCOVA was used to assess the significance
of interindividual differences. A Bonferroni correction,
'=
/k (where
is the type one error rate
and k is the number of comparisons), was applied to the
experiment-wise type-one error rate to make the statistical tests of each
variable more conservative (Sokal and
Rohlf, 1995
).
To evaluate how kinematic variables scaled with body mass across the entire
sample of adult primates, it was necessary to obtain values for each variable
at comparable speeds. Considerable literature has been devoted to the issue of
comparable speeds, and for most mammals comparisons have been made at the
trotgallop transition (Heglund et
al., 1974). Unfortunately, primates do not use a classical
trotting gait (Hildebrand,
1967
; Vilensky,
1989
; Larson,
1998
) and do not appear to change gait to a gallop for similar
mechanical reasons as do non-primates
(Demes et al., 1994
).
Alexander and colleagues (Alexander and
Jayes, 1983
; Alexander,
1989
) have suggested that geometrically similar animals should
move in a dynamically similar fashion if they are moving at the same relative
speeds (the same Froude numbers). Under such conditions, linear gait
parameters should differ by a constant value for animals that are
geometrically similar. Similarly, all speeds, frequencies or muscle powers
should also be proportional (but with different constants) for animals moving
at similar Froude numbers. Thus, to obtain values of kinematic parameters at
comparable speeds, ANCOVAs (using relative speed as the covariate) were
conducted to obtain the LSM for each variable at the mean relative speed.
These LSM values were plotted against body mass to evaluate how they scaled
and to compare them with Biewener's
(1989
) diverse sample of
mammals. Relative speed is measured as the square root of Froude number,
v/(gh)0.5, where v is
velocity, g is the gravitational constant and h is
hip height.
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Results |
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Body proportion effects
Joint angles
Fig. 4 illustrates whether
the observed differences in joint angles corresponded with predictions;
summary data for these comparisons are shown in
Table 6. In general, the joint
angles differ between the male patas and female baboon in the direction
predicted from differences in limb proportions. That is, the patas, with its
longer limb segments, uses more extended joint postures and lower angular
excursions than the female baboon. Exceptions are found at the elbow and
shoulder at mid-stance, the shoulder at touch-down, the hip at touch-down and
lift-off and for hip angular excursion, where no significant differences are
observed. Despite the non-significant differences, the direction of the
difference was the same as that predicted (except for the elbow angle at
mid-stance). For the comparison of the male baboon with the male patas,
predicted differences are most often found for the hindlimb joints, where the
patas has more extended knee posture and decreased angular excursions at the
hip. The male patas also has more extended forelimb joints and lower forelimb
and shoulder angular excursions even though no significant difference was
predicted. It should be noted, however, that the subadult male baboon has more
extended wrist postures (as predicted by hand length differences), so it is
not always the case that the patas has more extended limb postures than the
baboons. Where significant differences exist for the comparison between the
male and female baboons, they are usually in the direction predicted from limb
length differences (e.g. the male, having longer limbs distal to the elbow,
has correspondingly more extended elbows). The majority of these results
suggest that mid-stance joint angles differ predictably with differences in
limb proportions. Given the subtle differences in limb proportions in this
sample, many of the differences are not significant at the
'=0.017 level. However, the fact that several of the
non-significant results also differ in the predicted direction suggests that
greater differences in limb proportions could have a more substantial effect
on locomotor postures. Comparison of protraction and retraction angles and
angular excursions reveals a more mixed picture, with angles either not
differing (e.g. comparison of male with female baboon) or not differing in the
manner predicted (e.g. forelimb comparisons for male patas with male
baboon).
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Joint moments
The joint moment comparisons across the pairs of 15 kg monkeys show a
mixture of predicted and unpredicted results
(Fig. 5,
Table 7). Joint moments depend
on the magnitude of the GRF and the moment arm of the GRF about the joint in
question. Animals with longer limb segments were predicted to have similar or
lower joint moments than those with shorter limb segments. When moving at the
same speed, the subadult male baboon exerted significantly lower ground
reaction forces on its forelimb and hindlimb than either the adult female
baboon or the male patas monkey. The latter two monkeys do not differ in their
GRF magnitudes.
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Despite having longer limbs and higher GRF magnitudes, the patas experiences similar or lower joint moments than either baboon (except for comparisons at the ankle for both baboons and at the hip and elbow for the male baboon). The moderation of joint moments for the patas is attained by better alignment between the limb segments and the GRF. In the comparisons between the two baboons, the predicted differences were observed for all joints. The male baboon had lower moments than the female because the GRF magnitude was lower and the male frequently used more extended limb postures (Fig. 4).
Effective mechanical advantage
EMA (Table 7) was measured
for the knee, elbow and ankle for all adults but not for the subadult baboon
(radiographs were not obtained for the subadult male). The greatest difference
in limb proportions between these monkeys is found in the limb segments below
the knee, with the patas having longer legs and feet. The male patas has
correspondingly more extended knee postures and greater mechanical advantage
at the knee than the female baboon. This indicates that the patas requires
less muscle force to maintain its knee joint posture than does the female
baboon. At the elbow and ankle, however, the female baboon has greater
mechanical advantage than the patas.
Scaling of variables across adult primates
Joint angles
Many of the joint angles at mid-stance do not change significantly with
increasing body mass across the entire sample of adult primates
(Table 8). However, where
significant differences are observed, they are most frequently in the
direction predicted: larger animals have more extended elbow and shoulder
joints at mid-stance. Hip and shoulder angles at lift-off also decrease with
increasing body mass, as do the hip and shoulder angular excursions.
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Joint moments
Joint moments (Table 8)
scale with negative allometry across the sample of adult primates, as
predicted. The same pattern of negative allometry is obtained without
including data from the adult male baboon, which moved more slowly and had
lower GRF magnitudes.
Effective mechanical advantage
EMA for the extensor musculature at the knee and elbow increases with
increasing body mass, allowing larger animals to use relatively less muscular
effort to maintain knee and elbow postures in comparison with smaller animals.
The slopes for the knee EMA lines are remarkably similar for the
phylogenetically constrained group of primates and for the diverse sample of
non-primate mammals (Fig. 6),
while the elbow EMA increases with a larger slope in the primate sample than
in the non-primate sample. In contrast, the ankle EMA for the primate sample
did not change with increasing mass.
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Discussion |
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The observation that mid-stance joint moments were similar or lower in
longer-limbed animals also has implications for the magnitudes of muscle force
required to maintain limb posture. As Biewener
(1983,
1989
,
1990
) has shown, the product
of the ground reaction force and the inverse of the effective mechanical
advantage can be used to estimate the amount of muscle force necessary to
prevent the limb from collapsing into flexion during stance. Only in the knee
was the EMA of a longer-limbed monkey greater than that of the shorter-limbed
monkey (allowing the longer-limbed animal to exert less quadriceps muscle
force). The strongest body proportion signal was expected at the knee joint
since the segment distal to the knee is where the greatest difference in body
proportions exists. While the EMAs at the ankle and elbow were significantly
higher for the shorter-limbed female baboon than for the male patas (in
contrast to expectations), the percentage difference between the individuals
was rather small.
Limb and proximal segment protraction and retraction angles, and their
corresponding angular excursions, do not vary predictably with body
proportions. This may result from the fact that the limbs are already quite
extended at touch-down and lift-off (Polk,
2001), and the GRF magnitude is relatively low at these times. As
a result, joint moments at these times are quite low compared with those at
mid-stance (Schmitt, 1999
),
and joint posture does not need to be modified.
Does phylogeny affect how body size influences musculoskeletal
design?
The similarities observed between the phylogenetically constrained sample
of primates and the diverse sample of mammals suggest that locomotor variables
in both samples respond to the same functional signals. That is, larger
animals tend to adopt more extended limb postures and have lower angular
excursions than smaller animals. Larger animals also have lower joint moments
and correspondingly greater effective mechanical advantages for their elbow
and knee extensor muscles than smaller animals. These similarities demonstrate
that the pattern of how body size influences knee and elbow kinematics is
generally not influenced by the phylogenetic composition of the study
sample.
One important and illustrative exception to this similarity between closely
related and diverse groups is observed at the ankle, where the EMA did not
increase with increasing body mass for the primate sample, but did increase
with mass in the non-primate sample. This difference in slopes probably
reflects the diversity in foot morphology subsumed within the non-primate
sample. That is, because of the phylogenetic diversity of the sample, a wide
variety of foot morphology is represented, ranging from the elongated pes of
the artiodactyl and perissodactyl taxa to the shorter feet of the rodents.
These variations in foot morphology probably require differences in ankle
posture either because of mechanical constraints related to body mass or
because of the relative lengths of the limb segments; or the differences in
posture may simply result from historical events associated with the origin of
unguligrade posture in the artiodactyl and perissodactyl clades. If so, the
`mass'-related increase in ankle EMA observed by Biewener
(1983,
1989
) may be conflated with
similar effects resulting from phylogenetically correlated differences in foot
morphology.
In contrast, the cercopithecine monkeys are more uniform in their foot
morphology (Strasser, 1992).
Perhaps more importantly, in the wild, these cercopithecines are accustomed to
spending part of their lives in trees to feed, sleep and escape from predators
(Fleagle, 1999
), and their
feet all possess significant grasping ability. When moving on arboreal
supports, even the largest of the monkeys is frequently required to use a
semi-plantigrade foot postures (the heel does not contact the substratum) to
maintain its grip above branches and avoid falling
(Schmitt and Larson, 1995
). On
terrestrial substrata, monkey foot posture ranges from semi-plantigrade to
digitigrade, but ankle postures remains similar between the taxa in this
study. Thus, primates may not show a mass-related increase in ankle EMA
because their foot postures are constrained by their need to use arboreal
supports. Size-related increases in ankle EMA may still be apparent in taxa
that are not constrained to be plantigrade or semi-plantigrade, but this
question remains to be tested with a sample that demonstrates the appropriate
control of phylogenetic and adaptive influences.
Predicting alignment between GRF and limb segments from joint
posture
In most cases, more extended limb postures result in lower joint moments.
Exceptions to this pattern (in the body proportion comparisons) are found at
the shoulder and elbow, where moments at mid-stance are lower for the patas
despite the fact that the elbow and shoulder joint angles did not differ
between these monkeys (Figs 4,
5). In addition, the ankle and
hip moments are higher for the patas monkey than for the female baboon despite
the fact that the patas used more extended hindlimb joint posture (Figs
4,
5). These results show that
alignment between the limb segments and the GRF is difficult to predict from
joint posture alone. These apparent discrepancies between joint angles and
moments may be overcome through changes in limb rotation or abduction. For
example, decreased shoulder and elbow joint moments, with no change in joint
angles, could be accomplished by medial rotation or adduction of the limb.
This would decrease the mediolateral (ML) moment arm by bring the limb
segments closer to the ML component of the GRF. Similarly, the moments in the
hindlimb could be increased through external rotation or abduction. This
finding underscores the advantage of recording both three-dimensional
kinematic data as well as the ML component of GRFs for animals such as
primates that may have greater joint mobility and that are not constrained to
parasagittal limb movements during locomotion.
Determinants of joint posture in intra- and interspecific
comparisons
Joint posture is clearly influenced by a variety of factors including
speed, limb proportions, body mass, joint moments and substratum use
(Biewener, 1983; Inman et al.,
1980; Vilensky and Gankiewicz,
1990
; Schmitt,
1999
). Comparisons among individuals demonstrate that joint
postures become more extended as body mass or limb length increases, probably
to avoid high joint and midshaft bending moments (see above; see also
Biewener, 1983
,
1989
). Joint moments also
increase with speed for most individuals (within a walking gait), yet the
changes in posture that accompany speed increases within individuals are in
the opposite direction to those observed among individuals that differ in
mass. Joint flexion increases with speed in both bipedal and quadrupedal taxa
(Table 5; Inman et al., 1980;
Vilensky and Gankiewicz, 1990
;
Gatesy and Biewener, 1991
),
permitting both more efficient forward motion of the body's center of mass and
moderation of peak vertical forces. Smoothing the path of the center of mass
has the effect of reducing fluctuations in potential and kinetic energies; the
vertical accelerations of the center of mass are decreased, and more efficient
forward motion is permitted (Inman et al., 1980;
Andriacchi et al., 1982
;
Andriacchi and Strickland,
1983
). Mochon and McMahon (1981) have also shown that increasing
knee flexion at mid-stance helps to moderate peak vertical forces.
Increasing limb flexion with increasing speed in intra-individual
comparisons may also result from changes in momentum. As speed increases, so
does forward momentum; when the limb touches down, a braking impulse is
applied, but the limb is not rigid and the joints of the limb may be forced
into flexion. The amount of flexion is dependent on limb stiffness, which
Farley et al. (1993) have
shown to be nearly independent of speed for running gaits. If stiffness is
also independent of speed for walking, the limb will flex more at higher
speeds than at lower speeds.
Thus, joint posture and joint moments have different relationships in intra- and inter-individual comparisons. Within individuals, increasing limb flexion allows efficient forward motion of the center of mass with increasing speed, at the cost of increasing joint moments. In comparisons among individuals, the limbs are extended to avoid high joint and midshaft bending moments that result from increased body mass or limb length.
In summary, adaptive differences in limb proportions generally have
significant and predictable effects on limb design, while phylogenetic effects
are more limited. Among animals with similar body mass, longer-limbed monkeys
use more extended limb postures at mid-stance than do shorter-limbed
individuals. A more-extended posture permits a greater effective mechanical
advantage and allows longer-limbed animals to resist gravity with less
muscular effort than shorter-limbed animals. Joint postures also tend to
increase among closely related animals that differ in body mass, allowing
larger monkeys to have a greater EMA at the elbow and knee than smaller
monkeys. The increase in elbow and knee EMA in the closely related primate
sample is similar to that observed in a diverse sample of mammals
(Biewener, 1989), suggesting
that body mass is the predominant influence on posture at these joints. In
contrast to the general mammalian pattern, ankle EMAs did not increase with
body mass across the primate sample, perhaps because arboreal substrata impose
constraints on primate foot posture. The observation that ankle EMA did not
increase with body mass suggests that clade-specific adaptive differences may
obscure the ubiquitous effects of body mass and that both phylogeny and limb
proportions can have significant effects on musculoskeletal design.
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Acknowledgments |
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References |
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