Integrative and Comparative Biology
Integrative and Comparative Biology, volume 54, number 6, pp. 1148–1158
doi:10.1093/icb/icu110
Society for Integrative and Comparative Biology
SYMPOSIUM
Dynamics of Locomotor Transitions from Arboreal to Terrestrial
Substrates in Verreaux’s Sifaka (Propithecus verreauxi)
R. E. Wunderlich,1,* A. Tongen,† J. Gardiner,* C. E. Miller‡ and D. Schmitt§
*Department of Biology, James Madison University, Harrisonburg, VA 22807, USA; †Department of Mathematics, James
Madison University, Harrisonburg, VA 22807, USA; ‡Division of Biology, University of South Wales, Cardiff, UK;
§
Department of Evolutionary Anthropology, Duke University, Durham, NC 27710, USA
From the symposium ‘‘Terrestrial Locomotion: Where Do We Stand, Where Are We Going?’’ presented at the annual
meeting of the Society for Integrative and Comparative Biology, January 3–7, 2014 at Austin, Texas.
1
E-mail: [email protected]
Synopsis Most primates are able to move with equal facility on the ground and in trees, but most use the same
quadrupedal gaits in both environments. A few specialized primates, however, use a suspensory or leaping mode of
locomotion when in the trees but a bipedal gait while on the ground. This is a rare behavioral pattern among mammals,
and the extent to which the bipedal gaits of these primates converge and are constrained by the anatomical and neurological adaptations associated with arboreal locomotion is poorly understood. Sifakas (Propithecus), primates living only
in Madagascar, are highly committed vertical clingers and leapers that also spend a substantial amount of time on the
ground. When moving terrestrially sifakas use a unique bipedal galloping gait seen in no other mammals. Little research
has examined the mechanics of these gaits, and most of that research has been restricted to controlled captive conditions.
The energetic costs associated with leaping and bipedal galloping are unknown. This study begins to fill that gap using
triaxial accelerometry to characterize and compare the dynamics of sifakas’ leaping and bipedal galloping behavior. As
this is a relatively novel approach, the first goal of this article is to explore the feasibility of collecting such data on freeroaming animals and attempt to automate the identification of leaping and bipedal behavior within the output. The
second goal is to compare the overall accelerations of the body and to use that as an approximation of aspects of
energetic costs during leaping and bipedalism. To achieve this, a lightweight accelerometer was mounted on freely moving
sifakas. The resulting acceleration profiles were processed, and sequences of leaps (bouts) were automatically extracted
from the waveforms with 85% accuracy. Both vector dynamic body acceleration and overall dynamic body acceleration
(ODBA) were used to characterize locomotor patterns and energy expenditure during leaping and bipedalism. The
unique kinematics of the gait of sifakas, and the mechanics of bouts involving a string of successive leaps or gallops,
appear to minimize redirections of the center of mass as well as the number of acceleration peaks and ODBAs. These
results suggest that bipedal galloping is not only a reflection of the unique anatomical configuration of a leaping primate,
but it may also provide a musculoskeletal and an energetic advantage to sifakas. In that sense, bipedal galloping represents
an advantageous way for sifakas to move when transitioning from arboreal leaping to terrestrial locomotion.
Introduction
Managing energy expenditure and controlling daily
metabolic costs is an essential element of animals’
fitness, and costs of locomotion comprise a large
portion of the daily expenditure for an animal
(Leonard and Robertson 1997; Biewener 2006;
Shepard et al. 2008a, 2008b). Numerous studies
have examined specializations among animals that
reduce the energetic cost of locomotion, whether
this cost is measured physiologically as oxygen consumption (see Hoyt and Taylor 1981; Taylor et al.
1982; Frappell et al. 1989; Griffin and Kram 2000;
Griffin et al. 2004; Hanna et al. 2008) or estimated as
levels of recovery (see Cavagna et al. 1977; Ahn et al.
2004; Zani et al. 2005; Biewener 2006; Lammers and
Zurcher 2011; O’Neill and Schmitt 2012) or losses
due to redirection of the center of mass (collisions)
(Kuo et al. 2005; Ruina et al. 2005; Usherwood et al.
Advanced Access publication September 17, 2014
ß The Author 2014. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved.
For permissions please email: [email protected].
Arboreal and terrestrial locomotion in sifaka
2008; Lee et al. 2011, 2013). Similarly, musculoskeletal design further imposes constraints on locomotion, as animals must experience musculoskeletal
loading but resist overloading of the system to
the point of failure. Although many animals exhibit
locomotor strategies specialized for movement on
particular substrates (land, trees) or in particular
media (water, air), others are able to operate under
a variety of conditions, often having to perform locomotor tasks with a completely different orientation
of the body in space. Orientation of the body vertically or horizontally results in different effects of
gravitational acceleration and differently oriented
substrate reaction forces. Such changes in orientation
and substrate make conservation of energy and regulation of musculoskeletal load potentially
challenging.
Primates are particularly interesting in this regard.
As an order, they utilize a vast array of arboreal and
terrestrial substrates, and most members move in
both environments [see Fleagle (2013) for a
review]. Of particular interest is the frequent occurrence of bipedalism in the order Primates compared
with other mammals. This form of locomotion appears regularly in all apes including, of course
humans, who are obligate bipeds; frequently in
some New and Old World monkeys; and as the
main and obligate form of walking and running
while on the ground in one strepsirhine primate—
the sifaka (Propithecus). Yet it is intriguing that, despite its frequency as a locomotor mode among primates, the nature of bipedalism, when it occurs
either as an obligate or as a facultative mode of locomotion, is quite different across the order.
Although humans use an obligate upright striding
gait, chimpanzees (Pan), gibbons (Hylobates), and
siamangs (Symphanlagus) use a bent hip, bent knee
bipedal walking gait; with the former switching easily
among bipedalism, quadrupedalism, and suspensory
locomotion, and the latter using bipedal gaits when
not using suspensory locomotion. The orangutan
also often uses a bipedal gait, but does so most frequently while holding branches (Thorpe et al. 2007).
New and Old World monkeys often engage in bipedal walking, especially when carrying objects (Liu
et al. 2009; Fragaszy et al. 2010; Duarte et al. 2012;
Demes and O’Neill 2013). Monkeys and apes engage
in bipedalism to different degrees. Although all monkeys probably can walk bipedally, for most this represents a small percentage of their locomotor
behavior, relying on quadrupedalism in most contexts. Other than sifakas, the nonhuman primates
that spend the most time moving bipedally are
highly suspensory New World monkeys and the
1149
nonhuman apes, all of whom regularly engage in
suspensory locomotion. The frequency with which
bipedalism is used in these groups is generally believed to be related to forelimb loading—by moving
bipedally these animals avoid compressive loading in
limbs specialized to function in tension (Wood-Jones
1916; Stern 1976; Reynolds 1985a, 1985b; Schmitt
2003). When moving bipedally apes use a striding
sequenced gait, which rarely involves an aerial
phase (Kimura et al. 1985; Vereecke et al. 2006).
It is important from a dynamic locomotor perspective to stress the commitment to bipedalism
seen in sifakas moving on the ground, and how
this type of bipedalism compares with that seen in
other primates. Sifakas are indrid primates specialized for dynamic vertical clinging and leaping [see
Oxnard et al. (1990) for a more extensive review of
the locomotor ecology of Propithecus]. They cling to
vertical supports and leap long distances for their
body size, travelling using richochetal bouts (a locomotor bout is defined as a continuous series of locomotion that ends when punctuated with a change
in locomotor type or a posture) of leaping in which
animals within a group follow behind one another
using the same pathway through the forest. Unlike
apes and monkeys, on the ground sifakas use a
highly unusual form of bipedalism that has been described as a bipedal gallop (Wunderlich and Schaum
2007) with a whole-body aerial phase. The trunk of
the animal is oriented about 308 to the direction of
movement, and the two hind limbs contact the
ground in a rapidly sequenced pattern, with the
trail limb contacting before the lead limb (Fig. 1)
[Note that ‘‘lead’’ and ‘‘trail’’ during sifaka bipedal
galloping refers to the limb that is in front and
behind, respectively, spatially rather than temporally
in succession (Wunderlich and Schaum 2007)]. This
raises the question of why sifakas, the only lemuriform primate to engage regularly in obligate bipedalism, adopt this type of gait. The explanation for
this may lie in the broader aspects of locomotor
ecology for this species. The anatomical and energetic commitment to leaping may constrain the
form of bipedalism in this species. But without a
comparison of the dynamics of these two gaits
such conclusions remain speculative.
This method of locomotion is poorly understood
both from a mechanical and evolutionary perspective. Here we examine why sifakas use these unusual
bipedal galloping gaits upon transitioning from the
trees to the ground and to what extent this pair of
locomotor strategies—leaping in the trees and galloping on the ground—can inform our understanding, in general, of transitions from one gait to
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R. E. Wunderlich et al.
Fig. 1 Sifaka bipedal galloping on the ground from right to left. The body is oriented 308 to the path of movement. The trail limb
touchdown is followed by the lead limb touchdown as the center of mass descends, and the two limbs come off the ground in the same
order as the center of mass ascends.
Fig. 2 Illustration of the technique used to filter raw accelerometer data and identify peaks representing leaps. This diagram shows two
series of leaps; the first, a 4-leap series and the second, a 6-leap series. Dotted lines represent the raw data, solid lines represent the
smoothed data. The open circles are the smoothed data peaks that are identified as leaps when their magnitude exceeds 20 Hz. The
associated raw data peaks (closed circles) are then associated with these peaks.
another on different substrates. Three main hypotheses for why an animal might exhibit a particular gait
when it transitions from one substrate to the next
are: (1) efficiency—bipedal galloping is more energetically efficient than other forms of terrestrial locomotion or it takes advantages of morphological or
functional patterns in place for vertical clinging and
leaping to provide the most efficient landscape for
movement on the ground; (2) reduction of peak
musculoskeletal load—bipedal galloping fosters
lower peak musculoskeletal loads than those that
would be predicted for other forms of locomotion;
and (3) neuromuscular constraint—sifakas are specialized for locomotor patterns associated with vertical clinging and leaping and are constrained by these
patterns of limb-use to this method of terrestrial
movement.
Traditionally, energetics is measured using indirect
or direct techniques for the estimation of oxygen
consumption. Direct respirometry involves measuring the rate of oxygen consumption by measuring
gas exchange through a mask worn by an animal
or in an isolated chamber, a technique that is not
amenable to measures of energy expenditure in the
field. Indirect methods, including heart rate and
doubly labeled water, have been used somewhat
more successfully in field applications. However,
these methods have numerous other difficulties,
such as their need for calibration/validation with
direct measurements and the inability to collect
Arboreal and terrestrial locomotion in sifaka
1151
Fig. 3 Acceleration data from all three axes and the resultant acceleration (green/gray peaks that have highest peak magnitude). Note that
the Y accelerations exhibit a baseline close to gravitational acceleration, but all three components of the acceleration have some baseline
static acceleration. VeDBA is calculated as the vector sum of these three components (resultant) summed over the series of leaps.
data at fine temporal scales (Speakman 1998; Butler
et al. 2004).
It is difficult to examine energy expenditure by
sifakas on any substrate using any of these traditional
techniques. Sifaka locomotion covers large distances
in short, intermittent bursts, not lending itself to
laboratory measurement of metabolism, particularly
the time-averaging measurements of doubly labeled
water. However, recent studies have shown direct
relationships between overall dynamic body accelerations (ODBA) and locomotor costs (Wilson et al.
2006; Green et al. 2009; Gleiss et al. 2011; Qasem
et al. 2012). With these techniques available, Byrnes
et al. (2008, 2011a, 2011b) quantified gliding mechanics in colugos and estimated the energetic costs
of gliding, showing that gliding is not more efficient
than climbing but does save travel time. Several studies have also been conducted on the mechanics of
leaping in lemuriform primates (Sellers and
Crompton 2004; Sellers 2008) using accelerometry;
however, no studies have been performed to date
on a VCL species, and no studies have explicitly examined ODBA or vector dynamic body acceleration
(VeDBA) as a proxy for energy expenditure. To
begin to understand the center-of-mass mechanics,
and ultimately energetics, in sifakas across different
locomotor substrates and body orientations, we are
using accelerometry to characterize whole-body dynamic accelerations and to estimate differences in
energy expenditure between arboreal leaping and
terrestrial bipedal galloping in sifakas in order to
shed light on the adaptive mechanisms behind this
unusual gait.
Numerous studies have illustrated the utility of
accelerometry for the documentation of footfalls
(Pfau et al. 2005, 2006; Ren and Hutchinson 2008;
Preston 2012) and activity patterns (e.g., Erkert and
Kappeler 2004; Sellers and Crompton 2004), as well as
the use of ODBA and VeDBA to estimate energy expenditure both by terrestrial and aquatic animals
(Wilson et al. 2006; Shepard et al. 2008a, 2008b;
Green et al. 2009; Gleiss et al. 2011; Qasem et al.
2012). Sellers and Crompton (1994, 2004) collected
the only quantitative locomotor data on primates
using accelerometry and have demonstrated the utility
of this method for further study and for quantification of primate locomotor behavior. Here we build on
their work to demonstrate the potential of accelerometry for measuring whole-body dynamics in a specialized leaping primate. With datalogging capabilities
and the ability to collect triaxial acceleration at high
recording rates [measured in data units (Gs) recorded
per second (Hz)], accelerometry has many advantages
over traditional techniques for measuring locomotor
behavior and locomotor dynamics. Traditionally, locomotor behavior is documented by observation
(Altmann 1974; Fleagle 1977) or occasionally by
video and is subject to highly variable experimenter
reliability due to experience, difficult terrain, or the
difficulty of maintaining consistent sight of animals
1152
moving in an arboreal environment, often in dense
tree cover or high in the forest. Datalogging for 24 h
allows animals’ movement to be measured in all locations, whether or not the animal is out of sight of the
observer, and can be accomplished at all times of the
day. Studies have demonstrated that lemurs, in particular, are much more cathemeral (Andrews and
Birkinshaw 1998) than previously recognized, suggesting that it is essential to develop methods that can
document activity for 24 h a day (Sellers and
Crompton 1994). Furthermore, techniques that
allow long-term logging of the dynamics of the
whole body or of limbs permit measurements of parameters that were formerly confined to the controlled
captive settings (acceleration, force, and kinematics)
to be made in the field, such that locomotor biomechanics can be measured in a natural setting. Here we
have presented work that validates the feasibility of
measuring triaxial whole-body accelerations during
leaping and bipedal galloping in a field setting, as
long as animals can be captured and re-captured for
attachment of the device and download of data.
Methods
A single Verreaux’s sifaka (4.9 kg) at the Duke Lemur
Center (DLC), Durham, NC, was used for this study.
The goals were to establish the protocols for collecting such data and to provide the first data on these
animals. This project explores both the feasibility of
mounting such equipment on the animals and the
ability to extract data from the outputs. This article
serves to validate the use of accelerometers in this
population and over a relatively long time frame.
Following this work additional animals will be studied, a process currently underway at the Duke Lemur
Center.
All procedures were approved by the Duke
University IACUC. The sifaka was equipped with a
Humotion (Munster, Germany) datalogger that contained a tri-axial accelerometer collecting at 100 Hz.
The device is small and lightweight enough (60 17
6 mm; 6.3 g, plus a battery weighing 20.1 g) that it
could be attached to the middle of the back of the
animal and not cause any interference with the
normal motion of the animal.
Data were collected in two settings at the DLC.
The first is a caged setting where the animal leaped
between two poles spaced at 2.2 m from one another.
This was used to validate and test the accuracy of
our identification of leaping patterns using the accelerometer. Although using relatively short distances,
the leaps were clearly defined in the acceleration profiles. Detailed results of these validation experiments
R. E. Wunderlich et al.
are reported elsewhere (Gardiner et al. 2013, manuscript in preparation). Longer distance leaps were
collected in the phase described in this study and
are explored in the analysis that follows. The
second environment used for this study was the
Natural Habitat Enclosure at the Duke Lemur
Center where animals are allowed to free range in
large sections of forested enclosure simulating a wild
sifaka’s habitat. Simultaneous data on acceleration
and behavior were collected for 4 h while the
animal ranged freely. Longer distance leaps could
be achieved in this habitat, as well as leaping and
bipedal galloping bouts of greater length. This
study is based on data collected in this enclosure.
In order to validate the accelerometer as a way to
characterize locomotor patterns, behavioral data
from video records, and from notes on observations
were compared with over 4 h of data on acceleration
collected at 100 Hz. Although the ultimate goal of the
project is to collect in the field for 24 h or longer,
this study is limited to recording one animal over a
4-h period because of the limitations of the protocol.
At present the DLC will allow the animal to wear the
unit for that period. In addition, we wanted to be
able to observe all behaviors during the recording
period to be confident of our assessment. For two
people to follow and collect notes precisely, 4 h was a
reasonable time.
Time and acceleration in three directions were imported into a custom Matlab (Mathworks, Natick,
MA) program for analysis. Data were smoothed
using a 4th order Butterworth (5 Hz) filter. Peak acceleration values over 20 Hz were identified as leaps,
and all leaps were matched with locomotor behavior
data such that the frequency with which the program
counted or missed leaps could be quantified, thus
making comparisons between sequences of leaping
and bipedal galloping. Although all three components of the acceleration profile are available, in
this article we concentrate on the vertical profile because of the predictions of our ballistic model
(see ‘‘Results’’ section). Therefore these were analyzed first. Although we recognize the importance
of rotation (Dunbar 1988) we have less strong predictions about horizontal accelerations, and there are
greater filtering challenges to be met with these components. We wanted to see how effective vertical
patterns alone would be in identifying leaps and gallops and comparing costs using the models described
below.
Series of leaps or bipedal gallops were automatically identified by finding local maxima that were
‘‘close’’ to each other. This measure of closeness is
a free parameter but is associated with the length of
1153
Arboreal and terrestrial locomotion in sifaka
Fig. 4 Sample acceleration signal (left) that has been integrated to give velocity (middle) and integrated again to provide position
(right). The dark gray middle section represents the aerial phase and the light gray ends the takeoff and landing phase.
time between consecutive leaps or gallops in a
sequence.
ODBA was calculated as the sum of the absolute
values of the dynamic accelerations from each of the
three axes (Wilson et al. 2006; Shepard et al. 2008a,
2008b; Gleiss et al. 2011):
ODBA ¼ jAx j þ jAy j þ jAz j
Previous methods for calculation of ODBA isolate
the static acceleration from the dynamic accelerations
by first smoothing the accelerations in each axis to
approximate the static component (gravitational acceleration) and subtracting this from the total
acceleration to isolate the dynamic component. We
do not know the orientation of the animal or
changes in body position during the movements we
are analyzing, but we do know that the orientation of
the animal (and the accelerometer relative to the
movements measured) is similar during the locomotor behaviors we are comparing, so we did not
perform this step but rather made the assumption
that the gravitational contribution would be similar
in each condition. Because of this difficulty of insuring consistent placement and orientation of the accelerometer on the animal as it moves in three
dimensions, we also calculated VeDBA, as it has
been suggested that the VeDBA may be a more accurate predictor of activity in these situations
(McGregor et al. 2009, but also see Qasem et al.
2012):
r
ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
VeDBA ¼
A2x þ A2y þ A2z
Peak accelerations, number of peaks, ODBA, and
VeDBA were compared across bouts of single leaps,
multiple leaps, and bipedal gallops to assess the extent
to which these modes of locomotion in sifakas
involve similar levels of musculoskeletal load and
energy expenditure.
Results
Characterization of leaping using acceleration
A leap can be modeled as a mass (the animal’s center
of mass) following a projectile path, and the aerial
phase of the leaps we observed follow that path closely. The only portion of the leap that varies substantially from the path of a projectile is the middle
phase in which a small deviation is observed in the
acceleration signal (arrow in Fig. 4). This is the point
at which the animal pulls its legs up, raising the level
of the center of mass and providing extra air time
and distance in the air.
We were able to identify correctly over 85% of the
bouts of leaping and automatically quantify the
height of peaks, ODBA, and VeDBA for these
bouts. The most frequent mis-identification of locomotor behaviors is recording bipedal galloping as
leaping. Series of bipedal galloping exhibit high
peaks in rapid sequence that resembles the high, rapidly-sequenced peaks of leaping, thereby reinforcing
the dynamic similarity of these two behaviors
(Fig. 5).
We compared single leaps to the more typical
multiple-leap bouts, which from the perspective of
whole-body dynamics, are also quite similar to bipedalism. While single leaps exhibit two acceleration
peaks, multiple-leap bouts exhibit a slightly different
pattern. Rather than exhibiting two peaks per leap,
accelerations during landing and take-off of consecutive leaps combine to form single intermediate peak
acceleration, greater than either the take-off peak or
the landing peak. So for each series of leaps, the
number of peaks is one less than expected for independent take-off and landing, and the animal is redirecting its center of mass one less time than it
would if it took separate single leaps.
Leaping versus bipedalism
Quantification of the dynamics of leaping and bipedalism was performed by comparing peak
1154
R. E. Wunderlich et al.
Fig. 5 (A) Four leap series illustrating both raw (dotted) and smoothed (solid) vertical acceleration data with peaks used to identify
leaps. Peak resultant accelerations were calculated at these same peaks. (B) Series of five bipedal galloping strides illustrating the
similarity of vertical acceleration signals.
accelerations and dynamic body accelerations of 51
bouts of leaping (including single and multiple leaps)
and 81 bouts of bipedalism over the course of the
sampling period.
There was no significant difference in peak
accelerations between leaping and bipedalism (mean
leaping ¼ 68.7; mean bipedalism ¼ 63.1; P ¼ 0.08).
Estimation of the energetics of a particular movement
or of daily energy expenditure due to locomotion is
quantified as ODBA and VeDBA. There were also no
significant differences between ODBA or VeDBA between leaping and bipedalism, suggesting a similar
overall contribution of each type of locomotion to
energy expenditure due to locomotion.
When we divide ODBA by the number of leaps in
a multiple-leap series, we find that ODBA values are
Arboreal and terrestrial locomotion in sifaka
1155
Fig. 6 ODBA during leaping and bipedalism, demonstrating the relative reduction of ODBA during multiple leaps or gallops relative to
single leaps or gallops.
relatively high for single leaps, but that ODBA drops
dramatically for two-leap bouts and continues to
drop for multiple-leap bouts. In other words, for
series involving a larger number of leaps, the relative
contribution of a leap to energy expenditure is much
less, suggesting a possible energy-saving mechanism
for bouts of multiple leaps. A similar pattern is observed during bipedalism. It is clear that the major
reduction in energy-cost occurs between single leaps
and bouts of multiple leaps, and this likely occurs
because of the reduction in number of acceleration
peaks; whereas a single leap has two acceleration
peaks, a two-leap bout has three acceleration peaks,
the middle peak being the landing peak of the first
leap and the takeoff peak of the second.
Discussion
Energy expenditure and musculoskeletal load are essential components of an animal’s fitness, and the
importance of these factors to fitness in saltatory
species, despite their frequent use of inefficient
paths, is well accepted (Crompton et al. 1993). The
specialized vertical clinging and leaping of sifakas, as
well as their enigmatic bipedal galloping gait on the
ground, beg inquisition as to the relationship between these activities, as well as the energetic and
biomechanical advantages of each. Measurement of
peak accelerations as well as whole-body, dynamic
accelerations have provided preliminary insight into
each of these.
Previous work has demonstrated the kinematic
similarity of leaping and bipedal galloping in sifakas
(Wunderlich and Schaum 2007). Triaxial accelerometry demonstrates the kinematic similarity of
these two movements with their high vertical accelerations of similar magnitude, closely spaced in time,
such that these movements are consistently miscategorized using vertical accelerations alone.
Efforts are in progress to use the horizontal components of acceleration to distinguish these patterns of
movement, as they differ primarily in that sifakas
maintain trunk position through multiple bipedal
gallops while they twist their trunk in each leap
from one vertical support to the next.
ODBA and VeDBA have been consistently associated with energy expenditure both in mammals, including humans, and in birds (Wilson et al. 2006;
Green et al. 2009; Gleiss et al. 2011; Qasem et al.
2012). While a direct measure of metabolic rate requires calibration for the species and activity being
measured (Qasem et al. 2012), comparison within a
species of similar locomotor behaviors is justified
and should reflect the relative energetic cost of
these activities. In our analysis, ODBA and VeDBA
did not differ significantly between leaping and bipedal galloping, suggesting that these dynamically
similar activities involve expending a similar level
of energy. Behavioral data, however, demonstrate
that the strides of bipedal galloping tend to be limited to about 1.0–1.5 m, whereas leaps can be 2–3
times this long at similar accelerations, suggesting
that cost of transport for leaping is actually substantially less than that for bipedal galloping.
Accelerometry can be calibrated for measurement
of distances, and this information will be essential
for obtaining a complete understanding of daily
energy costs and locomotor ecology in leaping primates (Crompton et al. 1993; Sellers and Crompton
2004).
1156
The locomotor strategies defined here for the individual suggest that leaping is more cost effective than
bipedal galloping and that leaping and bipedal galloping with multiple events in series may minimize energetic cost compared with single leaps or single bipedal
strides. More details are needed, but preliminary studies suggest an explanation that connects to the efforts
required to redirect the center of mass. We suggest that
sifakas may be able use the energy from a landing to
generate a least portion of the energy needed for the
next takeoff. The evidence for this is the single intermediate peaks in multiple-leap bouts. These peaks are
similar in size to take-off and landing peaks in a single
leap bout. In other words, a single leap will have two
peaks, one for take-off and one for landing. However, a
leaping bout of two leaps will have only three peaks,
one for take-off, one for landing and the next take-off,
and one for the last landing. This reduces the work
done redirecting the center of mass in multiple leaps.
Bipedal galloping may similarly reduce the costs of redirecting the center of mass, the collisional costs described by Ruina et al. (2005), Biewener (2006), and
Lee et al. (2013). Those authors have shown that, in
theory, animals can reduce costs of locomotion by
minimizing the magnitude of collisions (redirections
of the center of mass), involving multiple limbs in the
collision, and utilizing path-tracking that allows the
collision to develop pseudoelastic properties.
Baumgartner et al. (2009; Gardiner et al. 2013, manuscript in preparation) have demonstrated that bipedal
galloping minimizes the number of redirections of the
center of mass and sequences footfalls to minimize the
work required to redirect the center of mass.
This study has demonstrated the ease of application of accelerometers in captive and free-roaming
settings and the ability to identify specific movement
patterns in the absence of direct observation.
Furthermore, although the sample is limited, the
data collected point to ways in which the unusual
locomotor patterns—especially bipedal galloping—of
sifakas reflect potential selective pressures on a highly
specialized leaping animal that often must also transition to the ground for locomotion. What appeared
at first to be a constraint (i.e., that the adaptations
associated with leaping forced the animal to adopt an
unusual bipedal gait) may, with further data, reflect a
sensible solution utilizing a form of bipedalism that
is highly effective on the ground.
Acknowledgments
Thank you to Dave Brewer, Erin Ehmke, Sarah Zehr
and the rest of the staff at the Duke Lemur Center
for their assistance with animal handling and support
R. E. Wunderlich et al.
in the project. Johannes Rosenmoeller and Andreas
Becker (HuMotion, GMBH) provided substantial
technical support and advice. Thank you to
Brittany Wilhelm and Sara Ischinger for their contributions to the collection and analysis of data in
the early stages of this project. Many thanks to Rick
Blob and Tim Higham for organizing this symposium and for providing the opportunity to
participate.
Funding
The Jeffress Memorial Trust, Sigma Xi, and the
National Science Foundation (NSF-UBM DMS0734284) have provided support for this research.
Support for participation in this symposium was
provided by the Company of Biologists, and the
Society for Integrative and Comparative Biology
(Divisions of Vertebrate Morphology, Comparative
Biomechanics, Neurobiology, and Animal Behavior).
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