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First published online July 20, 2006
Journal of Experimental Biology 209, 2829-2838 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02316
The dynamics of hylobatid bipedalism: evidence for an energy-saving mechanism?
1 Laboratorium for Functional Morphology, University of Antwerp,
Universiteitsplein 1, Wilrijk B-2610, Belgium
2 Department of Human Anatomy and Cell Biology, University of Liverpool L69
3GE, UK
3 Centre for Research and Conservation, Belgium
4 Department of Movement and Sports Sciences, University of Ghent,
Belgium
* Author for correspondence at address 2 (e-mail: evie.vereecke{at}liverpool.ac.uk)
Accepted 9 May 2006
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Summary |
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Key words: white-handed gibbon, Hylobates lar, primate locomotion, biomechanics, energy recovery
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Introduction |
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; Alexander,
1991a; Alexander,
1995) (Fig. 1).
Running exploits a `spring-mass' mechanism, which is based on the storage and
recoil of elastic energy in tendons, muscles and ligaments
(Blickhan, 1989;
Alexander, 1991a;
Alexander, 1991b;
Farley and Ferris, 1998)
(Fig. 1). An even more
effective mechanism is used during brachiation of gibbons. In this suspensory
gait there is a pendular exchange of potential and kinetic energy, like in the
IP mechanism, but the main feature of this gait is the minimization of
collisional energy loss (Bertram and Chang,
2001; Usherwood and Bertram,
2003; Bertram,
2004; Gomes and Ruina,
2005). Most arboreal travel is done using this fast and economical
progression mode, but from time to time gibbons also locomote bipedally (4-12%
of their locomotor activities) (Carpenter,
1964; Fleagle,
1976; Gittins,
1983; Cannon and Leighton,
1994). The question then arises whether an energy-saving mechanism
is also applicable during hylobatid bipedalism. Specifically, this paper
attempts to answer the following questions. (1) Do gibbons use an
energy-saving mechanism during bipedalism? And if so, (2) is this mechanism
used at all speeds or is there a speed-related gait transition during
hylobatid bipedalism?
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;
Kimura et al., 1977;
Okada et al., 1983;
Vereecke et al., 2005a).
Moreover, in a recent publication
(Schmitt, 1999), Schmitt
remarks that stiff-leg walking does not provide an advantage during arboreal
locomotion because it involves high impact forces at the hind limbs and
creates vertical oscillations of the substrates on which the animals walk.
Instead, arboreal primates will generally use a compliant gait in order to
flatten the path of the COM and to reduce impact velocity and force
(Schmitt, 1999). This makes us
expect that an inverted pendulum mechanism will be absent during hylobatid
bipedalism, but it does not cancel out the presence of a spring-mass
mechanism. In addition, the fact that all bipedal bouts investigated so far
have a similar vertical force pattern
(Vereecke et al., 2005a)
suggests that all bipedal bouts belong to the same locomotor mechanism and
that a gait transition is absent. This prediction is also supported by an
associated kinematic study, which found no abrupt speed-related change in
spatiotemporal and kinematic gait parameters over the entire speed range
tested (Vereecke et al.,
2006a; Vereecke et al.,
2006b).
These predictions are evaluated by calculating the centre of mass (COM) and associated energy fluctuations from the ground reaction forces during spontaneous hylobatid bipedalism. This should reveal if gibbons use an energy-saving gait mechanism during their bipedal locomotion and also clarify whether or not gait transitions are present in hylobatid bipedalism. In addition, we also calculated the external mechanical work to get an idea of the mechanical energy cost of the bipedal locomotion of gibbons.
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). We analyzed the ground reaction forces during one full
stride, i.e. from touchdown of one foot to the subsequent touchdown of the
same foot, for each sequence (N=43). The position of the hip was
digitized in the corresponding video recordings [using Kwon3D software (Kwon,
1994)] to calculate the average velocity of the bipedal bouts and to obtain
the average hip height of each individual. A detailed description of the
digitization process is given in a related paper on the kinematics of
hylobatid bipedalism (Vereecke et al.,
2006b). The average velocity was assessed from the linear
regression of the horizontal displacement of the hip against stride duration.
The hip height of each animal was calculated as the average vertical position
of the hip during the stance phase. As this measure showed some
stride-to-stride variation within each individual, hip height was averaged
over the selected sequences (±s.d. = 1 cm).
Centre of mass (COM) excursions
The ground reaction forces are used to calculate the fluctuations of the
centre of mass via the procedure first described in 1975
(Cavagna, 1975), and which has
been applied in a large number of recent publications
(Farley and Ko, 1997; Roberts
and Scales, 2002; Ahn et al.,
2004; Griffin et al.,
2004; Hallemans et al.,
2004; Parchman et al.,
2003). In this method, body mass is obtained by integration of the
total vertical force (of both hind limbs) over stride duration. Dividing the
lateral (Fx) and forward (Fy) forces
(of both hind limbs) by body mass yields the lateral (Ax)
and forward (Ay) acceleration. Subtracting body weight
from the vertical force (Fz), followed by subsequent
division by body mass, yields the vertical acceleration
(Az). Numerical integration of the 3D accelerations gives
the velocity components (Vx, Vy and
Vz). Integration constants are so defined that the average
3D velocities (Vx, Vy and
Vz) over a stride match the velocities as measured on the
video images. Subsequent integration of the 3D velocities yields the position
of the centre of mass (X, Y and Z), which is then plotted as
a function of stride duration to calculate the stride length and illustrate
the vertical oscillations of the COM.
Acceleration
The zoo protocol did not allow direct interaction with the animals, hence
we could not control for speed and animals were free to choose their own
locomotor speed. This resulted in a speed range of 0.79-3.53 m s-1,
of which the highest speeds presented substantial acceleration. As previous
research (Roberts and Scales, 2002; Roberts and Scales, 2004) has demonstrated
that acceleration can have a major effect on the dynamics of locomotion, we
have excluded the strides with substantial acceleration or deceleration
(Ay<-0.2 or Ay>0.2 m
s-2) from our statistical analyses, finally resulting in a speed
range of 0.79-2.08 m s-1 (N=26;
Fig. 2). The average
acceleration of each trial was calculated by dividing the average forward
force component (Fy) by body mass
(Mb). The remaining `unsteady' trials are shown in the
regression plots to illustrate the effect of velocity and/or acceleration, but
these relationships are not tested statistically.
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); see
Table 1]. Based on the
relationship between the fluctuations in PE and KE during a
stride, we can identify the applied gait mechanism
(Fig. 1). If the PE
and KE are out-of-phase, energy exchange via the `inverted
pendulum' (IP) mechanism is possible. If the PE and KE are
in-phase than a `spring-mass' mechanism might be active. We calculated the
following parameters to evaluate the energy exchange mechanism (the formulae
are shown in Table 1). The
relative amplitude (RA) gives the ratio between the PE and
KE amplitudes, the percentage congruity (%C) reflects the phase
relationship between the PE and (forward) KE fluctuations
(PE and KE are out-of-phase when %C=0 and in-phase when
%C=1), and the recovery (R) quantifies the amount of energy transfer between
PE and (forward) KE via the IP mechanism. Energy exchange
via the IP mechanism (or R=100%) is optimal when RA=1 and %C=0. To
estimate the potential amount of energy recovery via the spring-mass
mechanism, we calculated the power fluctuations during a stride by
differentiating energy change with respect to stride duration. At touchdown,
kinetic and potential energy are dissipated as heat or stored in elastic
structures (e.g. tendons), coinciding with a negative power peak (`absorption
phase'). During the second half of the stance phase, the muscles have to
generate mechanical work (`generation phase'), which is associated with a
positive power peak. Depending on the properties of the tendon (stiffness,
elastic modulus, hysteresis), a certain amount of energy can be stored in the
tendons during the `absorption phase' and recovered during the `generation
phase' (by recoil of the muscle-tendon units), thereby contributing to the
total mechanical work of the body during locomotion
(Biewener and Blickhan, 1988;
Ettema, 1996;
Lindstedt et al., 2002;
Lichtwark and Wilson, 2005).
By calculating the power ratio (PR), i.e. the ratio of positive to negative
power, we can evaluate the potential energy recovery via the
spring-mass mechanism during a stride. We also calculated the maximal power
output during a stride, i.e. the positive power peak, and plotted it as a
function of stride duration. The definitions of all calculated parameters are
given in Table 1.
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The sum of PE and KE gives the total mechanical energy, TE, and the sum of the positive time increments of TE over a complete stride gives us the total external mechanical energy, Wext. To allow comparison with humans and other animals, Wext is divided by body mass and stride length and expressed in J kg-1 m-1. The fluctuations in PE and KE over a stride are also expressed in J kg-1 m-1 (Table 1 and Fig. 1).
Data analysis
The animals varied in body mass (range=3.5-7.5 kg) and size (ankle to knee
distance; range=0.146-0.177 m), and to allow comparison of the different-sized
animals, we scaled the dynamic parameters to body mass
(FPE, FKE and
Wext, see Table
1) or hip height (for deltaZ, see
Table 1). Hip height is
obtained from digitization of the corresponding video images (see above). The
gait parameters are plotted as a function of dimensionless velocity (DV),
which is the square root of the Froude number
(Alexander and Jayes, 1983).
The DV is calculated as the average velocity over a complete stride,
as measured on the video images, normalized to hip height
(Alexander and Jayes,
1983):
DV = Velocity / (9.81 x hip height)1/2.
The relationship between dimensionless velocity and the dynamic gait
parameters was evaluated using a least-squares regression analysis. Different
regression curves were estimated, of which we selected the best-fitting curve
based on the highest R2 value (significance level:
P<0.05). Data for the four animals were pooled in the regression
analysis, because the effect of individual was not significant as determined
by a mixed linear model analysis in SAS software
(SAS Institute, 1999).
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Mechanical energy and effect of locomotor speed
The net external mechanical work (Wext) delivered
during a steady-state stride amounts on average to 0.72 J kg-1
m-1 (Table 2) for
hylobatid bipedalism. Wext increases almost linearly with
increasing dimensionless velocity (P<0.05,
Fig. 4I), and shows no
speed-related discontinuity within the observed speed range. The KE
fluctuations also increase with increasing dimensionless velocity
(P<0.05; Fig. 4H),
since KE is correlated with forward speed. There is, however, no
significant effect of dimensionless speed on the magnitude of the PE
fluctuations (FPE), due to the absence of increase in
vertical excursion of the COM (deltaZ) with increasing dimensionless
velocity. Yet, the small positive trend between the dimensionless speed and
deltaZ and FPE makes that the relative amplitude
(RA=PE/KE) does not increase with increasing dimensionless
velocity (Table 2).
The positive and negative power increase with increasing dimensionless velocity (P<0.001, Table 2), but since we are looking at steady-state locomotion, both increase proportionally, resulting in a similar power ratio at all speeds (P>0.05, Fig. 4H). The increase in positive power with increasing dimensionless speed is also reflected in the maximal power output, which increases sharply with dimensionless speed (P<0.0001, Fig. 4G). The %congruity increases with increasing dimensionless velocity (P<0.05), with PE and KE being more out-of-phase at lower velocities and more in-phase at higher velocities (Fig. 4E). This results in higher IP recovery rates at slower speeds, but even at these low velocities, the IP recovery rarely rises above 25%.
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Energy-saving mechanism
In most bipedal bouts, the PE and KE fluctuate largely
in-phase, being highest during double-support and lowest during midstance
(Fig. 3). This pattern is also
seen in human running and points to the use of a spring-mass mechanism
(Novacheck, 1998). In human
running, the Achilles tendon (and plantar aponeurosis) is stretched when the
ground reaction force increases (at touchdown) and energy is stored (negative
power). At the end of the stance phase, the force falls and the Achilles
tendon and plantar aponeurosis recoil, thereby releasing the stored elastic
energy, which can be re-utilized for forward propulsion (positive power).
However, the amount of energy that can be stored in the (Achilles) tendon and
the amount of stored energy that can be recovered varies with the tendon
properties (Ettema, 1996;
Lichtwark and Wilson, 2005).
The tendon should have a suitable stiffness and low hysteresis to allow
storage and recoil of elastic energy during bipedal locomotion. From detailed
dissections, we know that gibbons have a well-developed Achilles tendon
(Vereecke et al., 2005b), but
we have no information about the tendon properties so the energy-saving
capacity of the Achilles tendon remains unverified. The energy-saving role of
the plantar aponeurosis seems negligible during hylobatid bipedalism because
gibbons have a weak plantar aponeurosis and lack a longitudinal foot arch (but
see Alexander, 1991b)
(Fig. 2).
Apart from suitable material properties, we also need appropriate joint
motions and muscle activation patterns to effectuate an efficient spring-mass
mechanism. Therefore, we combined the power oscillation patterns with
corresponding kinematical data, which were presented in a related kinematic
study analyzing the same bipedal sequences
(Vereecke et al., 2006b). In
Fig. 5 the angular time
profiles of the hind limb joints and the corresponding oscillations of the
total power of a single bipedal stride are shown. During the initial stance
phase, the ankle dorsiflexes, herewith stretching the plantarflexor muscle
tendon unit (triceps surae and Achilles tendon) and enabling storage of
elastic energy. The ankle continues to dorsiflex until terminal stance when
the ankle finally starts to extend (or plantarflex). However, at that time the
power has already dropped to negative values, pointing to energy absorption.
This suggests that the Achilles tendon and ankle plantarflexors do not act as
effective elastic springs during hylobatid bipedalism. Still, muscle tendon
units at the knee and/or hip joint could behave like elastic springs. The
power/angular time profile of the knee joint shows knee flexion at initial
contact, enabling storage of elastic energy, and knee extension during
midstance when there is a positive power peak
(Fig. 5). At terminal stance,
the knee starts to flex, attaining a maximal flexed position during the swing
phase. Hence, the knee extensor group might act as an elastic spring, although
the small amount of knee flexion and extension during the stance phase
(compare ankle and knee flexion in Fig.
5) will probably limit its energy-saving capacity. The angular
time profile of the hip shows no hip flexion at touchdown, which excludes
storage of elastic energy in the hip extensors.
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In summary, the power/angular time profiles are compatible with storage and recoil of elastic energy in the knee extensors (the quadriceps), which suggests that a spring-mass mechanism might be active during hylobatid bipedalism. However, the energy-saving capacity of the system is probably limited compared to the efficiency of human running.
(Pseudo)-elastic springs
Detailed morphological data of the knee extensor muscle-tendon complex is
needed to confirm the energy-saving function of the quadriceps, but it seems
not unlikely that they behave like elastic springs during hylobatid
bipedalism. Energy storage and elastic recoil in the quadriceps has amongst
others been observed in human and galago jumping
(Prilutsky and Zatsiorsky,
1994; Aerts, 1998;
Novacheck, 1998), and it seems
compatible with the organization and structure of the quadriceps of gibbons.
Detailed dissections of gibbon hind limbs have shown that the external part of
the knee extensor tendon accounts for ca. 26% of the total knee extensor
muscle tendon length (Payne et al.,
2006) (E.E.V., personal observation). If we take the internal part
of the tendon into account, this ratio augments to approximately 70% (E.E.V.,
personal observation). In addition, a previous study of our group has shown
that both ankle and knee extensors are important for speed modulation during
hylobatid bipedalism (Vereecke et al.,
2006b), implying that the knee extensors contribute significantly
to propulsion generation at push-off.
Besides the potential energy-saving role of the knee extensors, both knee
and ankle joint might reduce the cost of locomotion by acting as
pseudo-elastic springs (Ruina et al.,
2005). In such structures, energy is stored during the initial
stance phase (absorption phase) but there is no recovery in the following
phase of the gait cycle (generation phase). Instead, all energy needed for
propulsion is actively generated by the muscles. Although this mechanism is
certainly not as efficient as a purely elastic spring [cf. human running
(Blickhan, 1989)], it is still
four times less costly than a mechanism without energy storage
(Ruina et al., 2005).
All things considered, it remains puzzling why gibbons have such a
well-developed Achilles tendon. In view of the broad locomotor repertoire of
gibbons, it might be possible that the Achilles tendon has an energy-saving
role during other, commonly used, locomotor modes. The stiffness of the tendon
might, for instance, be too high to function as an energy-saving mechanism
during bipedal locomotion but might be suitable for energy storage and recoil
during jumping [as is observed in humans
(Bobbert et al., 1986)], which
involves high take-off and landing forces
(Demes et al., 1999).
Alternatively, the relatively long Achilles tendon of gibbons might be an
adaptation for brachiation because it contributes to a reduction of the distal
hind limb mass (Payne et al.,
2006).
Gait transition
Most legged animals use two basic patterns of locomotion: a walk at low
speeds, corresponding to an inverted pendulum mechanism, and a run, trot, hop
or gallop at high speeds, corresponding to a spring-mass mechanism
(Farley and Ko, 1997). The
change from one locomotor pattern to another is called a gait transition and
goes along with abrupt changes in one or more determinants of the gait type
considered [spatiotemporal parameters, kinematic patterns, dynamic patterns
(Alexander, 1989;
Hreljac, 1995)]. This is, for
example, seen when humans change from walking to running
(Segers et al., 2006) or when
a trotting horse starts galloping (Farley
and Taylor, 1991). Such speed-related discontinuities in kinetic
(this study), spatiotemporal and kinematic parameters
(Vereecke et al., 2006a;
Vereecke et al., 2006b) are
not apparent, however, within the observed speed range of hylobatid
bipedalism. In addition, the ground reaction forces show a similar pattern
during all bipedal bouts, with a single-humped vertical force curve
(Vereecke et al., 2005a).
These observations suggest that all bipedal bouts belong to the same locomotor
mechanism, namely a spring-mass model, and that a clearcut gait transition is
absent in gibbon bipedalism. This is also supported by calculation of the net
mechanical work, averaging 0.72 J kg-1 m-1 in hylobatid
bipedalism [cf. other vertebrates: W=1.15±0.43 J
kg-1 m-1 (Heglund et
al., 1982; Full,
1989)], and which rises continuously with increasing speed. As the
mechanical work is correlated with the metabolic cost of locomotion
(Minetti et al., 1999;
Rubenson et al., 2004) and the
transition from one gait to another is generally associated with a
minimization of the metabolic cost of locomotion
(Hoyt and Taylor, 1981;
Rubenson et al., 2004), this
might indicate that (bipedal) gibbons do not change gaits, or alternatively,
that the gait transition is not triggered by metabolic cost.
However, if we look at the IP recovery rates, which reflect the applied
gait mechanism, we can observe a gradual change in IP recovery rates in the
lower speed range (Fig. 4B,E).
Below a dimensionless velocity of 0.7 or a Froude number of 0.5, which
coincides with the transitional speed at which most vertebrates generally
change gaits (Alexander, 1989;
Kram et al., 1997), the
variation in %congruity and IP recovery rates increases and the IP recovery
rate may rise up to 70% (Fig.
4B,E). High IP recovery rates are typically seen in slow
locomotion of large mammals, such as humans, dogs and horses, and point to the
use of a relatively stiff-legged gait
(Griffin et al., 2004;
Willems et al., 1995;
Minetti et al., 1999). In
contrast, small animals that generally adopt a compliant gait, such as frogs,
lizards (Ahn et al., 2004;
Farley and Ko, 1997), kangaroo
rats, opposums and most birds (Heglund et
al., 1982; Muir et al.,
1996; Parchman et al.,
2003, Rubenson et al.,
2004), have relatively low IP recovery rates. Gibbons fit in the
latter group, but unlike opposums and kangaroo rats which never use pendular
mechanics (Heglund et al.,
1982; Parchman et al.,
2003), gibbons occasionally adopt an IP-like gait at slow speeds.
This is very similar to the situation in lizards
(Farley and Ko, 1997) and in
some birds [e.g. quails and chicks
(Heglund et al., 1982;
Muir et al., 1996)], which
generally use spring mechanics, but are capable of using either pendular or
spring mechanics at low speeds. A large variation in IP recovery rates is also
typical for the transitional speed of quadrupedal mammals
(Hoyt and Taylor, 1981;
Farley and Taylor, 1991), but,
in contrast to the situation in mammals, we did not observe a range of very
low speeds at which gibbons only use pendular mechanics. Such slow bouts might
fall below the sampled speed range, but our personal observations make us
doubt that gibbons ever use such low locomotor speeds.
Thus, at moderate to high speeds, we observed no indication for the
presence of a gait transition, but a gradual change from a spring-mass to a
more IP-like in gait mechanism might be seen in the lower speed range. This is
unlike the clearcut gait transition seen in humans, but comparable to the
situation in birds. In avian locomotion, the transition from a (grounded) run
to a walk comes along with abrupt changes in recovery rate and %congruity, but
is not associated with any other speed-dependent kinematic discontinuities
(Gatesy and Biewener, 1991;
Muir et al., 1996;
Gatesy, 1999;
Rubenson et al., 2004). In
gibbons this `walk-run' transition is even less apparent as no sharp change in
IP recovery rate and %congruity is observed within the observed speed
range.
Grounded running, ambling and tölting
Although gibbons seem to use a bouncing gait at most speeds, aerial phases
are generally absent. Only at the highest speeds, might the duty factor drop
below 0.5 and an `aerial-running gait' be observed. Such a bouncing gait with
no aerial phase is also found in birds, where it is called a `grounded-running
gait' (Rubenson et al., 2004).
Both in birds and gibbons, the transition from a grounded to an aerial run
comes along with a gradual drop in duty factor with increasing speed, but is
not associated with any other discontinuities in kinematic or kinetic
parameters (Gatesy and Biewener,
1991; Rubenson et al.,
2004). Thus, according to duty factor the grounded and aerial runs
might be classified as distinct gait types, but according to the gait
dynamics, they belong to the same locomotor mechanism, namely a bouncing gait.
It has been suggested that such spring-mass or `running' gaits without aerial
phase are used by several vertebrates to ensure continuous contact with the
substrate and to reduce the vertical oscillations of the COM
(Schmitt et al., 2006).
Examples of such gaits are the amble of primates
(Schmitt et al., 2006) and
elephants (Hutchinson et al.,
2003), the walking run of frogs and lizards
(Ahn et al., 2004), the
tölt of Icelandic horses (Biknevicius
et al., 2004) or the Groucho run of humans
(McMahon et al., 1987).
This paper reinforces the concept that aerial phases are not a prerequisite
for spring-mass mechanics (Biknevicius et
al., 2004) and, in line with some previous publications
(McMahon et al., 1987;
Gatesy and Biewener, 1991), it
supports the claim that duty factor alone should not be used to distinguish a
walk from a run. In addition, the bipedal locomotion of gibbons clearly
demonstrates that the grounded-run is more than an `intermediate' or
`transitional' gait pattern and we suggest that it should be regarded as a
full-fledged gait.
Primate bipedalism
Finally, we can compare the results of hylobatid bipedalism to prevailing
kinetic data of bipedalism in other primates. This should give us an idea
about the different styles of bipedalism within the primates, which can be
helpful for the reconstruction of the locomotor behaviour of our hominin
ancestors. In gibbon bipedalism the vertical force curve is typically
single-humped during gibbon bipedalism, even during bipedal bouts with
relatively high %congruity and IP recovery rate. A similar pattern is observed
during bipedal locomotion of other primates, such as baboons, Japanese
monkeys, chimpanzees (Kimura et al.,
1977) and bonobos (personal observation). The vertical force curve
might have a broad peak or plateau phase during bonobo and (untrained)
chimpanzee bipedalism, but a clear double-humped pattern as seen in human
walking is rare (Li et al.,
1996). This single-humped vertical force pattern is linked to an
in-phase fluctuation of the kinetic and potential energy and to the adoption
of a bent-hip, bent-knee posture (Li et
al., 1996). The adoption of such compliant gait can be
advantageous in an arboreal setting because it enhances the maneuverability
and balance and reduces the magnitude of the peak vertical force
(McMahon et al., 1987;
Gatesy and Biewener, 1991;
Li et al., 1996;
Schmitt, 1999). Indeed,
arboreal primates generally use a compliant gait in order to flatten the path
of the COM and to reduce impact velocity and force
(Schmitt, 1999).
Gibbons also adopt a bent-hip, bent-knee posture during bipedal locomotion,
using long stride lengths (Vereecke et
al., 2005a; Vereecke et al.,
2006a) and large angular excursions of the hind limb
(Vereecke et al., et al.,
2006b). However, the in-phase fluctuation of PE and
KE during (overground) bipedalism of gibbons point to a
running gait, whereas most (quadrupedal) arboreal primates adopt a
compliant walk. Associated with this bouncing gait, the vertical
oscillations of the COM are also relatively high during gibbon bipedalism. The
average vertical excursion of the COM is 2.6 cm during gibbon bipedalism and 3
cm during human walking (Lee and Farley,
1998). Taking size differences into account, gibbons (with a hind
limb length of 0.37 m) seem to have relatively larger vertical oscillations of
the COM than during human walking (with an average human hind limb length of
0.85 m). Thus there is no evidence for a flattened path of the COM, or the
so-called `rope-walker' pattern (Tardieu
et al., 1993), during overground bipedalism of gibbons. It might,
however, be possible that gibbons adopt a modified compliant gait during
arboreal bipedalism, although there are no indications to suspect that gibbons
alter their gait dynamics to substrate type (see also
Alexander, 1991b;
Bonser, 1999). Observations of
wild gibbons indicate that gibbons select thick branches for bipedal
locomotion (Fleagle, 1976;
Gittins, 1983;
Sati and Alfred, 2002) (S.
Cheyne, K. Kakati, V. Nijman, personal communication), which leads us to
assume that a similar spring-mass mechanism is used during both terrestrial
and arboreal bipedalism.
Conclusion
This study suggests that gibbons make use of a spring-mass mechanism during
bipedal locomotion. A requisite for this is the presence of a suitable
muscle-tendon complex that allows storage and recoil of elastic energy during
bipedal locomotion. Although gibbons posses a well-developed Achilles tendon,
the kinematics of the ankle joint do not support an energy-saving role of the
ankle plantarflexor complex. A limited amount of elastic energy storage and
recoil seems, however, possible in the knee extensor muscle tendon unit of
gibbons, although this still needs to be confirmed by detailed anatomical
data. In conclusion, a spring-mass mechanism might be active during hylobatid
bipedalism, but the energy-saving capacities are probably limited.
In the lower speed range, gibbons either use a spring-mass or an inverted pendulum mechanism, but no speed range with an exclusive use of an inverted pendulum gait was observed. In contrast to the locomotor patterns of most mammals, there are no abrupt changes in the dynamics (current study) or in the kinematic, kinetic and spatiotemporal parameters (previous studies) within the observed speed range of hylobatid bipedalism. However, a more gradual change in gait pattern, as seen in some birds, might be observed.
Gibbons use a bouncing gait without an aerial phase at most speeds, probably as an adaptation for locomotion in an arboreal environment. In line with several other publications, this study shows that aerial phases are not a prerequisite for a spring-mass mechanism and it supports the claim that the distinction between walking and running should not solely be based on duty factor.
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