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First published online May 18, 2006
Journal of Experimental Biology 209, 2042-2049 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02235
Adaptive value of ambling gaits in primates and other mammals
1 Department of Biological Anthropology and Anatomy, Duke University,
Durham, NC 27710, USA
2 Orthopaedic Bioengineering Laboratory, Department of Surgery, Duke
University Medical Center, Durham, NC 27710, USA
3 Division of Anatomy, Faculty of Medicine and Dentistry, University of
Alberta, Edmonton, Alberta, T6G 2H7, Canada
* Author for correspondence (e-mail: daniel_schmitt{at}baa.mc.duke.edu)
Accepted 22 March 2006
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Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
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Key words: primate, ambling, gait, locomotion, running, walking, mammal, evolution
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Gambaryan, 1974;
Hildebrand, 1976;
Hildebrand, 1985;
Howell, 1944;
Muybridge, 1957). At their
fastest speeds, quadrupedal mammals generally use an asymmetrical running gait
such as a gallop (Gambaryan,
1974; Hildebrand,
1985; Howell,
1944; Muybridge,
1957). However, at speeds between that of a walk and a gallop,
quadrupedal mammals often use symmetrical running gaits that have an aerial
phase and in which the feet strike down in diagonal pairs (trot) or unilateral
pairs (pace) (Cartmill et al.,
2002; Gambaryan,
1974; Hildebrand,
1985; Howell,
1944; Muybridge,
1957). Such symmetrical running gaits are faster than walking
gaits but still provide relatively longer periods of bipedal support by both a
forelimb and a hindlimb than does galloping
(Cartmill et al., 2002).
However, trots or paces also produce marked increases in vertical oscillations
of the body and high whole-body peak forces compared to either walking or
galloping (Biewener and Taylor,
1986; McMahon,
1985; Rubin and Lanyon,
1982).
Recently, several studies have reported on the mechanics of some unusual
symmetrical running gaits that do not involve a whole-body aerial phase
(Biknevicus et al., 2003; Biknevicus et al., 2004;
Hutchinson et al., 2003;
Robilliard, 2005). Hutchinson
and colleagues (Hutchinson et al.,
2003) showed that when elephants increase speed, they shift from a
walk to a symmetrical gait in which the forelimbs and hindlimbs undergo
separate, non-overlapping aerial phases, with the feet striking the ground
independently rather than in pairs (Fig.
1). This pattern of locomotion has previously been reported for
elephants (Gambaryan, 1974;
Howell, 1944) and horses
(Barrey, 2001;
Biknevicius et al., 2003;
Biknevicius et al., 2004;
Nicodemus and Clayton, 2003;
Muybridge, 1957;
Robilliard, 2005;
Zips et al., 2001). These
gaits have been called `ambles'
(Muybridge, 1957), `running
walks' or `the single foot' (Hildebrand,
1967), and `tölts' or `toelts'
(Barrey, 2001;
Biknevicius et al., 2003;
Biknevicius et al., 2004;
Nicodemus and Clayton, 2003;
Robilliard, 2005;
Zips et al., 2001). We here
adopt Muybridge's term `amble'.
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;
Hutchinson et al., 2003). This
same effect has been noted in connection with the use of the amble (or
`tölt') among certain breeds of horses
(Barrey, 2001;
Biknevicius et al., 2003;
Biknevicius et al., 2004). The
classification of ambling as a type of walking or running has been debated
since ambling shares characteristics with both symmetrical gait categories.
The lack of a whole-body aerial phase suggests that ambles are a type of walk,
and whole body mechanics collected by Robilliard support this idea
(Robilliard, 2005).
Biknevicius et al. argued that horses use similar spring-like limb and body
mechanics during ambling and trotting
(Biknevicius et al., 2003;
Biknevicius et al., 2004). In
this paper we refer to the amble as a `running' gait because of the forelimb
or hindlimb aerial phase and the single-peak shape of the ground reaction
forces (Biknevicius et al.,
2004). This categorization is not intended to imply anything about
the exchange of potential and kinetic energy during ambling.
Despite considerable interest in the mechanics of ambling, no clear functional explanation exists as to why these symmetrical running gaits are used by some mammals instead of a trot or pace. This is partly because so few data exist on ambling in mammals.
An examination of locomotion in primates provides a new opportunity to
explore the functional correlates of ambling. The quadrupedal locomotion of
primates is unusual among mammals in many ways
(Cartmill et al., 2002;
Cartmill et al., 2006;
Demes et al., 1994;
Hildebrand, 1967;
Kimura et al., 1979;
Larson, 1998;
Larson et al., 2000;
Larson et al., 2001;
Lemelin and Schmitt, 2006;
Lemelin et al., 2003;
Rollinson and Martin, 1981;
Schmitt, 1999;
Schmitt and Lemelin, 2002;
Vilensky, 1989;
Vilensky and Larson, 1989).
The features that distinguish the walking gaits of primates include the
prevalence of diagonal-sequence gaits (in which the contact of each hindfoot
is followed by that of the contralateral forefoot), the use of highly
protracted arm positions at forelimb touchdown, and relatively higher vertical
peak forces on the hindlimb compared to the forelimb. It has been argued that
these features are part of a suite of basal primate adaptations associated
with locomotion and foraging on terminal, flexible branches
(Cartmill et al., 2002;
Cartmill et al., 2006;
Larson, 1998;
Lemelin and Schmitt, 2006;
Lemelin et al., 2003;
Schmitt, 1999;
Schmitt and Lemelin,
2002).
In addition to those features described, it has also been reported that
primates almost never adopt a running trot or pace
(Demes et al., 1990;
Demes et al., 1994;
Hildebrand, 1967;
Preuschoft and Gunther, 1994;
Rollinson and Martin, 1981;
Schmitt, 1995;
Vilensky, 1989). Some have
argued that primates eschew these gaits in order to avoid abrupt changes in
vertical oscillations of the body and high peak ground reaction forces
(Demes et al., 1990;
Demes et al., 1994;
Schmitt, 1999).
Despite the widely accepted claim that primates rarely trot or pace, it
remains unclear whether primates shift directly from a walk to a gallop as
they increase speed or use a previously unidentified gait during this
transition. Limited qualitative observations suggest that primates may in fact
amble rather than trot (Hildebrand,
1967; Howell,
1944; Rollinson and Martin,
1981; Vilensky and Larson,
1989) (Fig. 1). For
example, ambling has been suggested to be the gait used between a walk and a
gallop in baboons (Howell,
1944), and it has also been argued that ambling is used by lemurs
(Hildebrand, 1967). To date,
no quantitative data exist on the distribution and details of this unusual
gait in a broad sample of primates.
The fact that ambling appears to be a common, naturally occurring locomotor
mode in primates provides an opportunity to explore the biomechanical and
adaptive significance of ambling. This project examines the locomotor behavior
of 12 primate species to test the hypothesis that primates adopt an amble
rather than a trot as their preferred symmetrical running gait. A second
hypothesis to be tested, based on the model of Cartmill et al., is that during
ambling, primates should time their footfalls in ways that maximize bipedal
support by contralateral limbs (i.e. achieve a diagonality close to the trot)
but prevent an aerial phase (Cartmill et
al., 2002). In addition to testing these two hypotheses, a model
was developed to explore the ways in which ambling influences vertical
oscillations of the center of mass. This model was used to develop new ideas
about why ambling may be preferred over trotting in some mammals. By studying
the frequency and mechanics of ambling in a large phylogenetically and
ecologically diverse group of primate species, it will be possible to draw
some general conclusions about the adaptive value of this unusual gait pattern
in primates and other mammals and better understand the origins of primate
locomotor patterns.
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Materials and methods |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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; Schmitt,
2003a; Schmitt,
2003b; Schmitt and Lemelin,
2004). The species studied included primates that vary widely in
body size and substrate preference. Table
1 provides information on species, body masses, numbers of
individuals used and the substrates the animals moved on. All locomotor bouts
were recorded by at least one lateral-view video camera (60 Hz; shutter at
1/1000 s). Animals were allowed to move freely within a Plexiglas enclosure (6
mx1 mx1 m) at the Primate Locomotion Laboratory at the State
University of New York at Stony Brook or in a Lexan enclosure (6 mx0.66
mx0.66 m) at the Animal Locomotion Laboratory at Duke University and at
the Duke University Primate Center. A total of 1800 min of videotape were
available for this study.
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The goal of the second phase of this analysis was to determine the relative frequency of ambling and other gaits in the sample. In this phase we scored the frequency of ambling as part of the overall locomotor behavior of the animals under study and ascertained the frequency of other gaits, including trots and paces, using the same video records. To determine the frequency of ambling, an even sampling across videotapes was necessary. Forty steps were analyzed for each species. Steps were analyzed only on the type of substrate commonly used by the animals in the wild. For example, data for patas monkeys (Erythrocebus patas) were collected from videos of an animal moving on the ground, whereas data for the fat-tailed dwarf lemur (Cheirogaleus medius) were collected from videos of subjects moving on a horizontal pole. To sample without bias, the total time of available videotape for a species (e.g. 120 min) was divided evenly to allow for collection of 40 strides (e.g. 3 min sample intervals). At each time interval, the gait being used by the animal was recorded. This approach provided a conservative estimate of the frequency of ambling in primates and as such it may have underestimated its frequency in species adopting the amble less commonly (i.e. ambling events may not be evenly distributed).
In the third analytical phase, we calculated the timing of the footfalls
following a published method (Cartmill et
al., 2002), which allows the calculation of the timing of contact
and lift-off for each limb for an entire stride. These values were used to
calculate duty factor (i.e. foot-ground contact time divided by stride time)
for any limb and diagonality (i.e. the percent phase difference between
ipsilateral fore- and hindlimb cycles). Data were then plotted on a bivariate
graph. To evaluate the symmetry of a gait cycle, we followed Cartmill et al.'s
convention (Cartmill et al.,
2002). If the time from the first hind footfall to the next
(contralateral) hind footfall was greater than 60% or less than 40% of the
total stride period (±10% deviation from symmetry), the gait cycle was
considered asymmetrical and rejected from further analysis. Symmetrical gaits
with a limb duty factor less than 50% were identified as running gaits. Those
with a diagonality value of 50±5% were identified as trots. Those with
a diagonality value of 100±5% were identified as paces. Ambles were
those symmetrical gaits with a duty factor less than 50% in at least one limb
and diagonality between 55% and 95% or 5% and 45% such that no whole-body
aerial phase occurred during the stride. The model
(Cartmill et al., 2002)
suggested that adjustments in footfall patterns as speed increased during
walking were governed in part by the value of maintaining relatively long
periods of bipedal support in which the body is supported by a forelimb and
hindlimb. A similar model was applied to the ambling data.
The goal of the fourth and last phase of the analysis was to model the way in which ambling gaits may influence vertical oscillations of the center of mass compared to trotting. A model, rather than empirical data, was used in this study because our primates trotted so rarely and on the few occasions that they did so we were unable to record force plate data. Ideally, we would have liked to compare substrate reaction forces and movements of the center of mass during trotting and ambling in the animals themselves, but we were unable to do so for this study.
The theoretical foundations of the model are as follows. During trotting, diagonal limb pairs strike the ground simultaneously, thus generating peak forces twice that of a single limb acting on the whole body. In contrast, ambling animals should generate much lower peak forces acting on the whole body because the periods of simultaneous forelimb and hindlimb support are brief, thereby distributing the peak limb forces more evenly throughout the stride. Lower whole-body peak forces would be expected to reduce the vertical oscillation of the center of mass.
Vertical oscillations of the center of mass for ambling and trotting gaits
were compared by mathematically modeling whole-body vertical ground reaction
force patterns. In order to make this model operational, we specified values
for the individual limb vertical ground reaction force, duty factor and
diagonality. Vertical ground reaction force patterns for individual limbs were
modeled following published methods
(McNeill Alexander and Jayes,
1978). This requires selecting a shape factor for the force curves
that will be used for modeling the vertical force pattern for trotting and
ambling. A shape factor value of 0.0 (i.e. one-half sine wave) was chosen
because it approximates the actual force patterns applied to the ground by
trotting mammals and ambling primates. It is also consistent with the shape of
single-limb peak force curves recorded by Biknevicius et al. for ambling
horses (Biknevicius et al.,
2004). We determined this relationship through data found in the
literature and from our laboratory. The actual empirical value for this shape
factor is -0.03±0.06 (mean ± s.d.), based on a sample of
representative steps from three dogs
(McNeill Alexander and Jayes,
1978), one horse (McGuigan and
Wilson, 2003), three Old World monkeys and two prosimians
(unpublished primate data from our laboratory). The data from our laboratory
were collected from several single footfalls for five individuals. The method
for force plate data collection is described in detail elsewhere
(Schmitt, 1999;
Schmitt, 2003a). All data were
collected as the animal crossed an isolated section of the force-plate.
Force-plate output was processed with Motus 2000 software and filtered with a
Butterworth 30 Hz filter. The shape factor was then calculated following the
mathematical model used (McNeill Alexander
and Jayes, 1978). These values were used to set the parameters for
the model. In addition, the empirical values for a single ambling step with
both forelimb and hindlimb contacts for one primate were used to compare the
output of the model with actual values.
Holding everything else equal, these modeled individual-limb forces were
used to reconstruct whole-body ground reaction force patterns for the complete
range of possible trotting and diagonal-sequence ambling combinations using a
custom-written program with LabVIEW software (v 4.0.1, National Instruments,
Austin, TX, USA). To do so, whole-body ground reaction force traces were
created for 36 diagonality-duty factor combinations, where diagonality varied
from 0.5 to 0.75 and duty factor varied from 0.25 to 0.5. These reconstructed,
whole-body ground reaction forces were used in turn to calculate the vertical
oscillations (i.e. displacements) of the center of mass, using Cavagna's
methods (Cavagna, 1975).
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Table 2 shows the absolute
number of each gait type observed from a random sample of 40 steps for each
species. It also includes the percentage of symmetrical running gaits that are
ambles and the percentage of asymmetrical running gaits that are canters.
These results show that ambling was considerably more common than trotting in
primates (17% vs 1% of all gaits observed). Ambling represents 94% of
all symmetrical running gaits observed
(Table 2). The canter, an
asymmetrical gait with no whole-body aerial phase
(Howell, 1944), was preferred
to galloping (18% vs 5% of all gaits observed). Canters represent 73%
of all asymmetrical running gaits observed
(Table 2). The amble and the
canter both are gaits that allow animals to maintain at least one foot in
contact with the substrate during a stride. As mentioned above, the sampling
method for this phase of the analysis may have underestimated the frequency of
ambling gaits relative to other gaits. Although several ambles were found for
the crab-eating macaque (Macaca fascicularis) in the first video
analysis phase (Table 1), the
systematic sampling yielded no ambles at all
(Table 2).
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), p. 408]. Those gaits that plot directly on this line will
maximize the duration of bipedal support phases in the cycle without
introducing a whole-body aerial phase. Gaits that plot below the line approach
more closely to the trot, with diagonally opposite limbs moving in
near-synchrony, thereby providing longer periods of bipedal support by a
contralateral forelimb and hindlimb but also introducing a whole-body aerial
phase. For gaits that plot above the line, bipedal support periods are reduced
but there is no whole-body aerial phase. Most of the sampled primate gaits
fall above the line, but close to it (Fig.
2).
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Cartmill et al. argued that during walking, footfall timing is governed by
the value of maintaining relatively long periods of support on maximized
support polygons (Cartmill et al.,
2002). Trotting maintains long periods of bipedal support by
contralateral forelimbs and hindlimbs, but also introduces a whole-body aerial
phase. In contrast, ambling eliminates the whole-body aerial phase, thus
allowing an animal to maintain continuous contact with the substrate, but can
also reduce the duration of bipedal support by contralateral limbs. The
primates we observed in this study generally fall above the line that
represents a maximized duration for contralateral bipedal support phases
without introducing a whole-body aerial phase
(Fig. 2). This pattern suggests
that eliminating the aerial phase takes precedence over the maintenance of
relatively long periods of bipedal support. However, the data on the primates
follow the trend of the line in Fig.
2, suggesting that maximizing bipedal support is still an
important secondary goal.
Diagonal-sequence walking gaits (i.e. contact of the right hindfoot
followed by that of the left forefoot) are typical for walking primates
(Cartmill et al., 2002;
Hildebrand, 1967;
Muybridge, 1957;
Vilensky, 1989;
Vilensky and Larson, 1989).
All ambles we observed in our primate sample (except for one cycle) were
diagonal-sequence as well (Fig.
2). This suggests that a diagonal sequence footfall pattern
typifies both the walking and running gaits of primates. In contrast, ambles
observed in elephants (Fig. 1)
and horses are uniformly lateral-sequence (i.e. contact of the right hindfoot
followed by that of the right forefoot)
(Biknevicius et al., 2004;
Hutchinson et al., 2003).
Diagonal-sequence walking gaits may provide a biomechanical advantage in
terms of stability and safety while foraging on terminal branches
(Cartmill et al., 2002;
Cartmill et al., 2006;
Larson, 1998;
Lemelin et al., 2003;
Lemelin and Schmitt, 2006;
Rollinson and Martin, 1981;
Schmitt and Lemelin, 2002;
Vilensky and Larson, 1989). It
has been argued that this arboreal milieu (i.e. thin and flexible branches)
was critical to the early evolution of primates
(Cartmill, 1974) and that
diagonal-sequence gaits, and other unique aspects of primate locomotion, are
part of an adaptive complex associated with this mileu
(Cartmill et al., 2002;
Cartmill et al., 2006;
Larson, 1998;
Lemelin et al., 2003;
Lemelin and Schmitt, 2006;
Schmitt and Lemelin, 2002). We
hypothesize that ambling represents another characteristic part of this
complex of locomotor traits that evolved very early in primate history to
facilitate movement on thin branches.
Why is ambling preferable to trotting in a fine-branch arboreal
environment? Our mathematical models show that adopting an amble rather than a
trot allows animals to maintain a flatter trajectory of the center of mass, as
suggested for elephants (Hutchinson et
al., 2003). By excluding a true aerial phase, maintaining contact
with the substrate with at least one limb at all times, and avoiding the
simultaneous contact of limb pairs (as in a trot), the amble allows animals to
avoid relatively high whole-body oscillations and to moderate whole-body peak
forces when increasing locomotor speed. This could be important to animals
that forage on flexible and unstable terminal branches and that may want to
avoid being seen or oscillating the support when moving fast. Biknevicius et
al. reported that peak single-limb forces are lower in horses during ambling
compared to trotting, possibly due to changes in duty factor or limb mechanics
(Biknevicius et al., 2004).
They found no abrupt peak force transition when horses shift from a walk to an
amble, a finding that is also consistent with preliminary force data collected
in primates walking and ambling (Hanna et
al., 2003).
The conclusions of this study apply to primates and primate evolution but also provide a better understanding of the use of ambling by nonprimate mammals. Although primates and elephants may have developed ambling in different contexts and for different functional reasons, the biomechanical advantages of ambling gaits appear to be the same for both, namely, continuous contact with the substrate and reduced whole-body forces and vertical oscillations of the center of mass.
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Acknowledgments |
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Footnotes |
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References |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Barrey, E. (2001). Inter-limb coordination. In Equine Locomotion (ed. W. Back and H. M. Clayton), pp.77 -94.London: W. B. Saunders.
Biewener, A. A. and Taylor, C. R. (1986). Bone strain: a determinant of gait and speed? J. Exp. Biol. 123,383 -400.[Medline]
Biknevicius, A. R., Mullineaux, D. R. and Clayton, H. M. (2003). Taking the walk for a run: locomotor mechanics of lateral sequence singlefoot gaits. Integr. Comp. Biol. 43, 988.
Biknevicius, A. R., Mullineaux, D. R. and Clayton, H. M. (2004). Ground reaction forces and limb function in tolting horses. Equine Vet. J. 36,743 -747.[Medline]
Cartmill, M. (1974). Rethinking primate
origins. Science 184,436
-443.
Cartmill, M., Lemelin, P. and Schmitt, D. (2002). Support polygons and symmetrical gaits in mammals. Zool. J. Linn. Soc. Lond. 136,401 -420.[CrossRef]
Cartmill, M., Lemelin, P. and Schmitt, D. (2006). Primate gaits and primate origins. In Primate Origins: Adaptations and Evolution (ed. M. J. Ravosa and M. Dagosto). New York: Kluwer Academic Publishers. In press.
Cavagna, A. (1975). Force plates as ergometers.
J. Appl. Physiol. 39,174
-179.
Demes, B., Jungers, W. L. and Nieschalk, U. (1990). Size- and speed-related aspects of quadrupedal walking in slender and slow lorises. In Gravity, Posture and Locomotion in Primates (ed. F. K. Jouffroy, M. H. Stack and C. Niemitz), pp.175 -198. Florence: Il Sedicesimo.
Demes, B., Larson, S. G., Stern, J. T., Jr, Jungers, W. L., Biknevicius, A. R. and Schmitt, D. (1994). The kinetics of primate quadrupedalism: `hindlimb drive' reconsidered. J. Hum. Evol. 26,353 -374.[CrossRef]
Fleagle, J. G. (1999). Primate Adaptation and Evolution, 2nd edn. San Diego: Academic Press.
Gambaryan, P. P. (1974). How Mammals Run. New York: Wiley.
Hanna, J., Schmitt, D. and Lemelin, P. (2003). The effect of speed and gait changes on vertical peak forces in primates. Am. J. Phys. Anthropol. 36, S108.[CrossRef]
Hildebrand, M. (1967). Symmetrical gaits of primates. Am. J. Phys. Anthropol. 26,119 -130.[CrossRef]
Hildebrand, M. (1976). Analysis of tetrapod gaits: general considerations and symmetrical gaits. In Neural Control of Locomotion (ed. R. M. Herman, S. Grillner, P. S. G. Stein and D. G. Stuart), pp. 203-236. New York: Plenum Press.
Hildebrand, M. (1985). Walking and running. In Functional Vertebrate Morphology (ed. M. Hildebrand, D. M. Bramble, K. F. Liem and D. B. Wake), pp. 38-57. Cambridge, MA: Harvard University Press.
Howell, A. B. (1944). Speed in Animals. Chicago: University of Chicago Press.
Hutchinson, J. R., Famini, D., Lair, R. and Kram, R. (2003). Are fast-moving elephants really running? Nature 422,493 -494.[CrossRef][Medline]
Kimura, T., Okada, M. and Ishida, H. (1979). Kinesiological characteristics of primate walking: its significance in nonhuman walking. In Environment, Behavior, and Morphology: Dynamic Interactions in Primates (ed. M. E. Morbeck, H. Preuschoft and N. Gomberg), pp. 297-311. New York: Gustav Fischer.
Larson, S. G. (1998). Unique aspects of quadrupedal locomotion in nonhuman primates. In Primate Locomotion: Recent Advances (ed. E. Strasser, J. Fleagle, A. Rosenberger and H. McHenry), pp. 157-173. New York: Plenum Press.
Larson, S. G., Schmitt, D., Lemelin, P. and Hamrick, M. K. (2000). Uniqueness of primate forelimb posture during quadrupedal locomotion. Am. J. Phys. Anthropol. 112,87 -101.[CrossRef][Medline]
Larson, S. G., Schmitt, D., Lemelin, P. and Hamrick, M. K. (2001). Limb excursion during quadrupedalism: how do primates compare to other mammals? J. Zool. Lond. 255,353 -365.
Lemelin, P. and Schmitt, D. (2004). Seasonal variation in body mass and locomotor kinetics of the fat-tailed dwarf lemur (Cheirogaleus medius). J. Morphol. 260, 65-71.[Medline]
Lemelin, P. and Schmitt, D. (2006). Origins of grasping and locomotor adaptations in primates: comparative and experimental approaches using an opossum model. In Primate Origins: Adaptations and Evolution (ed. M. J. Ravosa and M. Dagosto). New York: Kluwer Academic Publishers. In Press
Lemelin, P., Schmitt, D. and Cartmill, M. (2003). Footfall patterns and interlimb co-ordination in opossums (Family Didelphidae): evidence for the evolution of diagonal-sequence gaits in primates. J. Zool. Lond. 260,423 -429.
McGuigan, M. P. and Wilson, A. M. (2003). The
effect of gait and digital flexor muscle activation on limb compliance in the
forelimb of the horse Equus caballus. J. Exp. Biol.
206,1325
-1336.
McMahon, T. A. (1985). The role of compliance in mammalian running. J. Exp. Biol. 115,263 -282.[Medline]
McNeill Alexander, R. and Jayes, A. S. (1978). Vertical movements in walking and running. J. Zool. Lond. 185,27 -40.
Muybridge, E. (1957). Animals in Motion. New York: Dover.
Nicodemus, M. C. and Clayton, H. C. (2003). Temporal variables of four-beat, stepping gaits of gaited horses. Appl. Anim. Behav. Sci. 80,133 -142.[CrossRef]
Preuschoft, H. and Günther, M. M. (1994). Biomechanics and body shape in primates compared with horses. Z. Morph. Anthop. 80,149 -165.
Robilliard, J. (2005). Mechanical basis of locomotion with spring-like legs. PhD thesis, Royal Veterinary College, London, UK.
Rollinson, J. and Martin, R. D. (1981). Comparative aspects of primate locomotion with special reference to arboreal cercopithecines. Symp. Zool. Soc. Lond. 48,377 -427.
Rubin, C. T. and Lanyon, L. E. (1982). Limb mechanics as a function of speed and gait: a study of functional strains in the radius and tibia of horse and dog. J. Exp. Biol. 101,187 -211.[Medline]
Schmitt, D. (1995). A kinematic and kinetic analysis of forelimb use during arboreal and terrestrial quadrupedalism in Old World monkeys. PhD thesis, State University of New York at Stony Brook, USA.
Schmitt, D. (1999). Compliant walking in primates. J. Zool. 248,149 -160.[CrossRef]
Schmitt, D. (2003a). Evolutionary implications of the unusual walking mechanics of the common marmoset (C. jacchus). Am. J. Phys. Anthropol. 128, 28-37.
Schmitt, D. (2003b). Substrate size and primate forelimb mechanics: implications for understanding the evolution of primate locomotion. Int. J. Primatol. 24,1023 -1036.[CrossRef]
Schmitt, D. and Lemelin, P. (2002). Origins of primate locomotion: gait mechanics of the woolly opossum. Am. J. Phys. Anthropol. 118,231 -238.[CrossRef][Medline]
Schmitt, D. and Lemelin, P. (2004). Locomotor mechanics of the slender loris (Loris tardigradus). J. Hum. Evol. 47,85 -94.[CrossRef][Medline]
Vilensky, J. A. (1989). Primate quadrupedalism: how and why does it differ from that of typical quadrupeds? Brain Behav. Evol. 34,357 -364.[Medline]
Vilensky, J. A. and Larson, S. G. (1989). Primate locomotion: utilization and control of symmetrical gaits. Annu. Rev. Anthropol. 18, 17-35.[CrossRef]
Zips, S., Pelham, C., Scheidl, M., Licka, T. and Girtler, D. (2001). Motion patterns of the toelt of Icelandic horses at different speeds. Equine Vet. J. Suppl. 33,109 -115.
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