Gait parameters in vertical climbing of captive, rehabilitant and wild Sumatran orang-utans (Pongo pygmaeus abelii)
1 Anthropologisches Institut und Museum, Universität
Zürich-Irchel, Winterthurerstr. 190, 8057 Zürich,
Switzerland
2 Dept of Human Biology, University of Cape Town, Observatory, 7925, South
Africa
* Author for correspondence (e-mail: kisler{at}aim.unizh.ch)
Accepted 6 August 2003
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Summary |
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Key words: kinematics, animal locomotion, vertical climbing, spatio-temporal gait parameters, primates, orang-utans, Pongo pygmaeus abelii
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Introduction |
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Orang-utans are the only extant great apes in Asia. They live in Sumatran
and Bornean rainforests and are seriously threatened by extinction through
habitat destruction. The two subspecies Pongo pygmaeus pygmaeus (from
Borneo) and Pongo pygmaeus abelii (from Sumatra) differ in general
appearance, behaviour and biochemistry (for an overview, see
Delgado and van Schaik, 2000).
No differences in postcranial morphology between the two subspecies have been
documented, but they may exist. Orang-utans exhibit pronounced sexual
dimorphism in body mass (adult females weighing 35 kg and males 78 kg on
average; Smith and Jungers,
1997
), which might be expected to influence vertical climbing
behaviour. They possess exceptionally long arms, whereas their hindlimbs are
relatively short (Jungers and Susman,
1984
). Both fore- and hindlimb joints are very flexible
(Morbeck and Zihlman, 1988
;
Tuttle and Cortright, 1988
).
Whilst their locomotor behaviour is best characterized as orthograde
suspension (after Hunt et al.,
1996
), which incorporates clamber, brachiation and orthograde
bridging behaviour (Cant, 1987
;
MacKinnon, 1974
;
Sugardjito, 1982
;
Sugardjito and van Hooff,
1986
), vertical climbing accounts for approximately a quarter of
all observed locomotion (Cant,
1987
; Thorpe et al., submitted), although note that Sugardjito and
van Hooff (1986
) recorded
smaller frequencies. Quadrupedal walking is less frequent, and leaping is
rarely performed. Vertical climbing has been observed to occur with
approximately the same frequency in adult females, adult males and adolescents
(Thorpe et al., submitted), ranging from 22% to 26% of total locomotor bouts.
These results reveal that classic predictions based on geometric scaling,
which imply that large animals should climb less than smaller ones, are not
borne out by orang-utan behaviour. However, it is possible that the lack of
size-related differences in climbing behaviour may be partly explained by the
presence of size-related, kinematically distinct, climbing strategies.
Consequently, to obtain valuable results for the kinematics of vertical
climbing in orang-utans that can be used for comparisons with the locomotion
of other species, it is necessary to start by investigating the extent of
intraspecific variation.
During human walking on level substrates, gait parameters such as cycle
duration, the duration of the support phase relative to cycle duration, stride
length or speed are correlated with the costs of locomotion relative to the
subject's physical ability or fitness (reviewed, for example, by
Whittle, 1996). For example,
walking gaits of very young or elderly humans are characterised by high duty
factors, short strides and slow speed
(Murray et al., 1969
;
Sutherland et al., 1988
). For
nonhuman primates, Isler
(2002a
) has identified key
differences in the climbing performance of gorillas and bonobos associated
with the age and sex of the individuals by comparing similar gait parameters.
She showed that the vertical climbing behaviour of an adult male gorilla was
characterised by higher duty factors, relatively shorter strides and more
variable footfall patterns compared with adult female or juvenile gorillas.
These results showed that the adult male climbed with apparent difficulty due
to his large body mass and indicate that heavier animals will, in general,
exhibit a prolonged support phase or higher duty factor, as well as a decrease
in stride length relative to leg length, reflecting the higher energy
expenditure relative to muscular strength that is predicted by theoretical
considerations (Cartmill, 1972
,
1974
;
Cartmill and Milton, 1977
;
Taylor et al., 1972
). In the
present study, we investigate whether differences in gait parameters can also
be observed between adult and juvenile orang-utans or between adult males and
females, which differ significantly in body mass, although their limb lengths
differ to a lesser extent than does body mass. In humans, carrying a child
also has a significant influence on locomotion costs
(Kramer, 1998
). Similarly, in
female orang-utans, the additional load of a clinging infant might be expected
to reduce climbing speed and increase the duty factor to compensate for the
increased mass. Thus, we compare the climbing performance of females with a
clinging infant with that of females without an infant.
The second focus of this study is to identify the influence of different
environments on vertical climbing performance of orang-utans. Due to their
large body size, arboreal lifestyle and extensive home range, the confined
living quarters of captive orang-utans present a strongly contrasting
environment to that of primary rainforest. Motivation to climb is also
reduced, as zoo animals are generally not dependent on locomotion for
foraging. Cage furniture, which is often rigid and of uniform type and
diameter, differs substantially from the compliant and complex nature of the
rainforest. This results in the captive habitat providing a less challenging
climbing environment than that experienced by wild individuals. Captive
animals become so familiar with their enclosure that one might expect climbing
performance to be characterised by increased speed and reduced duty factors in
comparison with their wild counterparts, who may be expected to move more
slowly due to the unknown or unstable nature of their substrates. On the other
hand, captive orang-utans generally exhibit a far larger proportion of
terrestrial locomotion than do their arboreal counterparts, which places very
different biomechanical demands on the musculo-skeletal system. During
terrestrial locomotion, compressive weight is distributed consistently between
the four limbs, and limited mobility is required at the joints. By contrast,
locomotion in an arboreal environment requires muscles capable of generating
greater stresses, both in compression and tension, in order to oppose gravity
during climbing and to cope with uneven and varied distribution of body mass
on the weight-bearing limbs. Forces also need to be exerted in a wide range of
joint positions, requiring full mobility at the joints. Sarmiento
(1985) has argued that this
results in the development of skeletal proportions of captive adult
orang-utans that are detrimental to climbing due to adaptations to terrestrial
quadrupedalism and consequently may result in less-confident climbing than
that exhibited by wild individuals and thus higher duty factors and/or reduced
speed. Rehabilitant orang-utans have also generally been kept in confined
living conditions (although often more restrictive than those of zoos) and may
not have received adequate nutrition, potentially hampering musculo-skeletal
development. After a period of rehabilitation they are reintroduced back into
a wild environment. Comparing the climbing performance of these animals with
those of wild and captive orang-utans will shed light on the ability of the
musculo-skeletal system to readapt to a locomotor repertoire that includes a
significant climbing component from one dominated by terrestriality.
Thus, in this study, we present data on vertical climbing obtained both
from captive individuals and from wild and rehabilitant orang-utans in
Sumatra, permitting a comparison of the gait parameters of wild, rehabilitant
and captive animals of all age and sex categories. To our knowledge, this is
the first quantitative comparison of locomotor kinematics in wild and captive
primates. Additionally, in an interspecific comparison with the vertical
climbing gait parameters of other hominoids (Isler,
2002a,2002b
,
2003
), we investigate the
influence of the specialised locomotor anatomy of orang-utans on their
climbing style.
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Materials and methods |
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Rehabilitant and wild orang-utans were observed at Bukit Lawang
rehabilitation centre and Ketambe Research Station, respectively, in the
Leuser Ecosystem, Sumatra, Indonesia. The Ketambe area is described in detail
by Rijksen (1978) and van
Schaik and Mirmanto (1985
). In
Bukit Lawang, all records were taken at a feeding platform at which
rehabilitants, who roamed freely through the forest, would congregate twice a
day for food supplements (bananas and milk). Consequently, calibration of the
locomotor sequences was possible. Records of wild orang-utans were obtained
throughout the Ketambe research area and, as a result, it was not possible to
calibrate these sequences.
Types of vertical climbing
In the literature, two types of vertical climbing are described
(Hunt et al., 1996): (1) when
climbing large-diameter substrates, such as tree trunks, the elbows are always
more or less extended (`extended-elbow vertical climbing'); (2) `flexed-elbow
vertical climbing' is used when the animal is climbing on a substrate of small
diameter, such as a rope, liana or thin tree, with flexion of the elbow
helping to elevate the body. The occurrence of these two types is influenced
by the animal's size, as flexed-elbow climbing requires the individual to grip
the substrate with one hand. In adult orang-utans, a substrate diameter larger
than 20 cm is likely to evoke extended-elbow climbing. In total, 47 sequences
of flexed-elbow vertical climbing in Sumatra were recorded: 42 in Bukit Lawang
(337 limb cycles) and five in Ketambe (47 limb cycles). Additionally, two
extended-elbow vertical climbing sequences on a large-diameter tree trunk were
recorded in Bukit Lawang (39 limb cycles). Five of the adult females in the
rehabilitant and wild groups had dependent infants, and these were generally
carried on the mother's hip whilst climbing. Subadult males do not exhibit the
characteristics of fully adult males (e.g. cheek flanges) and weigh about the
same as adult females (Delgado and van
Schaik, 2000
).
Analysis of gait parameters
Spatio-temporal gait parameters were analysed from the video sequences. The
footfall sequence and spatio-temporal gait parameters such as cycle duration,
duty factor and stride length were determined by reviewing the video sequences
frame-by-frame using NIH Image 1.62. Statistical analyses were carried out
with Statview 5 (SAS Institute Inc.). Cycle duration is defined as the time
between two initial contacts with the substrate (or `touchdowns') by the same
extremity. The relative support phase, or duty factor, is the fraction of the
cycle duration that a particular limb contacts the substrate. The cycles were
classified as symmetrical or asymmetrical according to the timing of the
footfalls, following Hildebrand
(1967). If the opposing limb's
touchdown occurred at between 40% and 60% of the cycle duration, the cycle was
considered symmetrical. Symmetrical cycles of the hindlimbs were further
classified as being either diagonal sequence or lateral sequence. In a
diagonal sequence gait, hindlimb touchdown is followed by the touchdown of the
opposite forelimb, whereas in a lateral sequence gait the ipsilateral forelimb
follows. The precise timing of the footfalls is expressed as the percentage of
the stride interval between the touchdown of the hindlimb and the following
touchdown of the ipsilateral forelimb. This yields a further subdivision of
the strides into the categories pace, diagonal couplets, single foot, lateral
couplets and trot (Hildebrand,
1967
). For statistical analysis, the laterality of a hindlimb
cycle was calculated as the interval between the touchdown of the hindlimb and
the following touchdown of the ipsilateral forelimb in percent of total cycle
duration minus 50%. Thus, a diagonal couplets gait results in a low value of
laterality, whereas a lateral couplets gait yields high values of
laterality.
All climbing sequences were further divided into strides of either the left
or the right hindlimb to analyse the type of limb support, according to the
scheme proposed by Vilensky and Gankiewicz
(1989). Stride length is
defined as the distance between two successive points of contact by the same
extremity; the reference point is the second joint of the middle finger or
toe. To compare the dynamics of climbing of the different-sized animals,
stride length and speed were normalised (following
Aerts et al., 2000
). As a size
determinant of the individual subject, and for calculating relative stride
length (sl), the lower leg length (l = distance
from knee to heel) was used. Stride length was measured relative to lower leg
length at the moment when this segment was held in parallel with, and close
to, the climbing substrate. This was usually the case at the end of the
support phase. Segment lengths were estimated from the video recordings for
the captive subjects and most of the rehabilitated subjects. They correspond
well with data on mean long bone lengths reported in the literature for the
corresponding sex and age groups (e.g.
Shea, 1981
), which were thus
used for all individuals (Table
1). Climbing speed (v) was then calculated by dividing
the stride length by the cycle duration (cd). The square root of the
Froude number (F) is used for normalising climbing speed to a
dimensionless parameter (see Alexander,
1992
):
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Statistics
For statistical comparison of the gait parameters in different sex/age
categories, the individuals were classified into the following groups:
carrying adult females (`mothers'), non-carrying adult females, adult males,
subadult males, adolescent males and juveniles. Being the only individual from
Ketambe (and therefore the only wild individual in a truly wild environment),
the results for adult mother Q are presented separately to those of the other
individuals. For comparisons between localities, results for juveniles and
adolescents were omitted from the captive and rehabilitant populations, as
they were not represented in the wild group. Significance of intraspecific
differences in the gait parameters was tested with factorial analysis of
variance (ANOVA) and Scheffé's post-hoc tests. Differences in
gait parameters between fore- and hindlimbs were tested with unpaired
Student's t-tests. Relationships between the relative stride length
and normalised speed were analysed with least-squares regressions on
log10-transformed data. Intraspecific differences of speed
modulation were tested using analysis of covariance (ANCOVA), with normalised
speed as a covariate.
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Results |
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Significant differences in gait parameters were also found between sex/age and locality (wild, rehabilitant, captive) categories. These are summarised in Table 3 and discussed below.
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Mean cycle duration and duty factor of fore- and hindlimbs during vertical climbing of Sumatran orang-utans are shown in Table 4 and Fig. 1A,B. In most individuals, neither the cycle duration nor the duty factor differed significantly between fore- and hindlimbs. The duty factor was not significantly different between sex/age or locality groups (ANOVA, Scheffé's post-hoc tests; Table 3). The cycle duration, however, is significantly shorter in juveniles than in all other groups. The wild adult female (Q) and wild adult male (O) exhibit similar cycle durations, and these are significantly longer than all other groups [except the adolescent male (M), who differs significantly from Q but not from O]. Accordingly, wild orangutans exhibit a significantly longer cycle duration than both captives or rehabilitants.
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In 78.4% of all hindlimb cycles, the footfalls of the hindlimbs were
symmetrical according to the definition of Hildebrand
(1967). Most individuals
preferred a diagonal sequence/diagonal couplets or single foot gait
(Table 5).Lateral sequence
gaits occurred very rarely, but, on occasion, lateral couplets were exhibited,
especially by juvenile D in Jersey Zoo and the wild mother (Q). Wild
individuals appear to exhibit a more diverse range of gaits than do
rehabilitants or captives, although this is largely influenced by the results
for wild mother Q.
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Table 6 shows the types of limb support that the orang-utans used during vertical climbing. The body was mostly supported by three limbs, although two-limb support phases were also observed relatively frequently, with diagonal pairs being the preferred support base in all subjects, except for the juvenile N and the adult female Q, who exhibited a greater percentage of lateral pairs. Thus, the index of laterality of limb support was higher in juveniles and the wild female (Q) than in the other groups (Fig. 1C). Support by only one limb, by both forelimbs or by both hindlimbs was extremely rare. The mean number of limbs used for support was also calculated for each subject (see Table 6). It was generally lower for juveniles than for adults, but this did not result in significant differences between the age and sex groups. In comparison to rehabilitants and captives, wild individuals had a slightly higher mean number of supporting limbs, but again this result was not significant.
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Mean relative hindlimb stride length and normalised speed of vertical climbing in orang-utans are shown in Table 7 and Fig. 1D,E. To account for body size differences between the animals studied, the gait parameters were normalised using lower leg length as an individual size determinant. Normalised speed of the wild mother (Q) is significantly lower than that of the other groups, while juveniles climb faster than adult females, mothers and the adult male (Factorial ANOVA, Scheffé's post-hoc test; see Table 3). Climbing speed is higher in captives than in rehabilitants, and higher in rehabilitants than in wild individuals, although the latter result is mainly caused by the very slow climbing speed of the wild adult mother (Q). The relative stride length is shorter in adult females than in juveniles, the adolescent male (M) and the subadult males (Table 3). Captive orang-utans exhibit significantly longer strides than rehabilitants.
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The relationships between log10-transformed hindlimb stride length and speed during vertical climbing are shown in Table 8 and Fig. 2. All gait parameters are normalised as described above. The slopes of the linear regression equations are significantly different from zero in most groups, with the exception of the wild mother (Q) and the adolescent male (M) (see Table 8). Intraspecific differences in the regression parameters are tested with an ANCOVA (Table 9), with normalised speed as a covariate. Adult females, the adolescent male and the juveniles do not differ significantly with respect to speed modulation in flexed-elbow vertical climbing. Subadult males take longer strides at the same dimensionless speed than adult females or juveniles. The wild adult male (O) takes even longer strides at the same dimensionless speed than subadult males. Between females that carry an infant and females that climb alone, there is no significant difference in speed modulation. The wild adult mother (Q), however, takes longer strides at the same dimensionless speed than other adult females.
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Extended-elbow vertical climbing
At Bukit Lawang, two sequences of extended-elbow vertical climbing on
large-diameter tree trunks were recorded, one of a mother carrying an infant
(H+) and one of an unaccompanied adult female (K). When compared with the
flexed-elbow vertical climbing sequences of adult females (both carrying an
infant and alone) at Bukit Lawang, the following results were apparent: the
cycle duration was not significantly different between flexed-elbow and
extended-elbow vertical climbing (unpaired t-test, P=0.240).
The duty factor, however, was higher in extended-elbow vertical climbing
(78.9±5.7% vs 71.4±8.7%; unpaired t-test,
P<0.001). Accordingly, the mean number of limbs used for support
was also higher for extended-elbow vertical climbing (see
Table 6). The preferred gait
pattern was diagonal sequence, as in flexed-elbow climbing. Trot did not
occur, but a single limb gait was used more often than diagonal couplets. The
laterality of the footfall patterns was therefore higher (unpaired
t-test, P=0.001), although lateral couplets gaits were
equally rare in both flexed- and extended-elbow vertical climbing.
The relative stride length, normalised speed and speed modulation were not significantly different between extended-elbow and flexed-elbow vertical climbing (ANCOVA; Table 9; Fig. 2B).
Infant-carrying
The flexed-elbow climbing characteristics of female Pongo p.
abelii carrying an infant at Bukit Lawang were compared with non-carrying
adult females at the same site. Cycle duration was not significantly different
between these two groups (unpaired t- test, P=0.899). Speed
modulation was also not different (ANCOVA;
Table 9). The duty factor was
even higher in adult females climbing alone than in carrying mothers
(73.8±6.6% vs 70.4±9.3%; unpaired t-test,
P=0.015). The other significant difference between carrying and
non-carrying females was the laterality of hindlimb cycles (unpaired
t-test, P=0.042). Both groups most often used a diagonal
sequence/diagonal couplets gait, but females that carried an infant used trot
more, whereas single females preferred a diagonal sequence/single limb
gait.
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Discussion |
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Differences in vertical climbing between wild, rehabilitant and
captive orang-utans
As a general rule, gait parameters of vertically climbing orang-utans are
remarkably similar between wild, rehabilitated and captive subjects from Bukit
Lawang, Ketambe and Jersey Zoo. Comparison is complicated by the limited
number of observations of wild individuals and the fact that the groups are
not balanced in terms of sex and age classes. However, some differences
between the climbing of zoo animals and that of orang-utans in Sumatra are
apparent: cycle duration is much longer, and normalised speed is lower, for
the wild orang-utans than for the rehabilitants, and even more so compared
with the zoo animals (Table 4).
Thus, no deficiencies in the ability to climb, which would be revealed by a
somewhat unstable or asymmetric gait or a higher duty factor, could be
detected in the rehabilitant orang-utans compared with wild animals. As our
study subjects were already rehabilitated to a certain extent, roaming freely
through the forest and only visiting feeding platforms, the differences in
locomotor fitness compared with wild individuals may not be substantial and
may indicate that orang-utans are able to adapt well to a locomotor repertoire
that includes a significant climbing component from one dominated by
terrestrial quadrupedalism. However, all observations of climbing in
rehabilitants were obtained at the feeding platform, on substrates that the
animals were very familiar with, and are thus not directly comparable to the
locomotion of wild animals on unknown substrates.
The studied zoo animals climb even faster and take longer strides than do rehabilitant orangutans, indicating that their confined living conditions did not significantly impair their climbing ability. This may be partly due to the fact that the captive subjects were not overweight. An influence of different motivations for climbing is less likely, as in all cases climbing was motivated mainly by the wish to gain access to food. Ultimately, it would be interesting to compare the locomotion of reintroduced ex-captives before and after their release or to study the locomotion of rehabilitant orang-utans at regular time intervals.
Another possible explanation for the differences in gait parameters observed between the animals of different locations would be that wild individuals climb more cautiously than do rehabilitant and captive orang-utans. A more cautious locomotion would show in slower speed, but, as the animals would physically be able to climb faster, the other gait parameters can be expected to remain unchanged (i.e. a steady, symmetrical gait with a similar duty factor, as in fact was observed in the wild subjects of this study). It seems likely that zoo animals are so familiar with the climbing structures in their enclosure that the need for caution is reduced. They simply know from experience that the ropes will not break. Wild orang-utans, on the other hand, inhabit large tracts of rainforest and may climb a specific tree or liana only once in their lifetime. Moreover, in the forest canopy, seemingly robust substrates may break under the animal's body weight, and orang-utans were frequently observed to test the strength of substrates before placing body weight on them. As a consequence, it is beneficial for wild individuals to move cautiously. Rehabilitant orang-utans are also familiar with their environment, particularly at the feeding platform, where the present observations were made. Accordingly, the gait parameters of rehabilitant orang-utans lie in-between those of wild and captive animals.
Captive orang-utans were found to have a larger degree of humeral head
torsion than wild animals (Sarmiento,
1985), which could be explained by the fact that the former devote
a considerable amount of time to quadrupedal walking on the ground
(Larson, 1988
). This
morphological feature may be related to the degree of humeral abduction during
climbing, which remains to be investigated in a three-dimensional analysis of
the joint angle kinematics. Such kinematic and musculoskeletal modifications
in captive animals compared with wild subjects indicate that studying the
locomotion of wild primates in undisturbed surroundings must remain the
ultimate aim of researchers if meaningful biomechanical data are required.
Extended-elbow versus flexed-elbow vertical
climbing
The characteristics of vertical climbing on different substrates by adult
female Pongo p. abelii at Bukit Lawang were compared. As only two
climbing sequences on large-diameter trees in Bukit Lawang were observed, the
following conclusions must be regarded as preliminary. A diagonal
sequence/single limb gait was preferred, and trot was not employed during
extended-elbow vertical climbing. The main difference between flexed- and
extended-elbow vertical climbing, however, was found in the relative duration
of the support phase, or duty factor, which was higher in extended-elbow
climbing. The mean number of supporting limbs was larger than three during
extended-elbow vertical climbing. At the same speed of locomotion, the duty
factor is an indicator of the effort that a subject exerts relative to its
physical ability or fitness (Murray et
al., 1969; Isler,
2002a
). It follows that extended-elbow vertical climbing is more
demanding than climbing a liana or a small-diameter tree and quantifies the
results of Thorpe et al. (submitted), who showed that wild individuals
revealed a strong preference for climbing single and multiple substrates of
less than 10 cm in diameter. Cant
(1992
) also noted this
preference when he observed wild orang-utans entering the crowns of large
fruiting trees, not by climbing the trunks with extended elbows but by
utilising adjacent, small, vertical lianas. The same pattern of a higher duty
factor can be observed in the vertical climbing of adult male gorillas
compared with adult females or juvenile gorillas
(Isler, 2002a
).
Nevertheless, mean cycle duration and relative stride length did not differ
between flexed-elbow and extended-elbow vertical climbing of female
orang-utans. Apart from the data presented here, gait parameters of
extended-elbow vertical climbing are available only for spider monkeys
(Ateles fusciceps robustus;
Isler, 2003). They belong to a
group of South American primates that exhibit adaptations to suspensory
locomotion and are convergent to hominoids in many morphological traits of the
postcranium, although their arms are not nearly as elongated as in
orang-utans. In spider monkeys, cycle duration was found to be shorter, i.e.
the step frequency was higher, and the stride length was shorter during
extended-elbow vertical climbing on a large-diameter tree than during
flexed-elbow vertical climbing on a rope or thin tree
(Isler, 2003
). Thus, it seems
that the differences between climbing on different substrates are more
pronounced in Ateles than in orang-utans, and this may suggest that
climbing a large-diameter vertical substrate is more demanding for spider
monkeys than for orang-utans. Thus, climbing on a large-diameter vertical
substrate may indeed be of adaptive significance for the evolution of
elongated arms, as biomechanical considerations suggest (e.g.
Cartmill, 1974
;
Fleagle et al., 1981
;
Preuschoft, 1990
;
Stern et al., 1977
). However,
to test this conclusion it would be necessary to investigate the 3-D
kinematics and kinetics of extended-elbow vertical climbing in the two
species.
Infant-carrying
Gait parameters of flexed-elbow climbing in adult female Pongo p.
abelii at Bukit Lawang were very similar between individuals carrying an
infant and those climbing alone. Thus, the climbing kinematics of female
orang-utans do not seem to be overly influenced by the additional load of a
clinging infant. This may be due to the small size of the observed infants and
may change later in development. A longitudinal study would be beneficial for
the understanding of the energetic costs of infant carrying in primates.
Age and sex differences
Sex differences in the gait parameters of vertically climbing Pongo p.
abelii are surprisingly small, given that the sexual dimorphism in body
mass of adult orang-utans is extreme
(Morbeck and Zihlman, 1988).
Duty factor, relative stride length, dimensionless speed and laterality of
limb cycles do not differ between the sexes. Only cycle duration is
significantly longer in the adult male than in adult females. However, as only
one adult male was observed, these results should be interpreted with caution.
Subadult males resemble adult females in all gait characteristics studied.
Thorpe et al. (submitted) conducted a log-linear analysis of the likely
influences on orang-utan locomotion. They also found that frequencies of
vertical climbing did not differ substantially between the sexes and, contrary
to classic geometric predictions, the age/sex category of the individual has
only limited influence on overall locomotor repertoire. They proposed that
this in part reflected the presence of arboreal pathways, which individuals of
all age/sex categories attempt to follow.
Juvenile orang-utans exhibit a shorter cycle duration than adults,
subadults or adolescents and a lower duty factor than adults and subadults
(see Fig. 1). The laterality of
hindlimb cycles is also higher in juveniles than in adults, although this is
largely due to an increased frequency of lateral couplets gait patterns in
juvenile male D from Jersey Zoo (Table
5). Stride length and speed do not differ between juvenile and
adult orang-utans if they are normalised against lower leg length. In a study
of 3-D joint angles during flexed-elbow vertical climbing in captive
orang-utans (Isler, 2003), it
was shown that the range of motion of all joints was reduced in the juvenile
individual: the shoulder and elbow joints were less flexed and the knee and
hip joints were less extended than in the adult orang-utans. This reduced
range of motion of the major limb joints in the juvenile orang-utan yields a
larger distance of the body centre of gravity from the substrate.
Consequently, whilst previous studies have shown that the frequency of
vertical climbing does not differ substantially between individuals of a
different age, the present study indicates that the kinematics of locomotion
do differ. This reflects the fact that, due to metabolic differences and the
allometric relationship of muscle dimensions to body mass, climbing is
energetically relatively more expensive for larger animals (Cartmill,
1972,
1974
;
Cartmill and Milton, 1977
;
Taylor et al., 1972
). Since
metabolic rates per unit body mass vary inversely with body mass, the increase
in oxygen consumption demanded by vertical locomotion represents a much larger
fraction of resting metabolism in large animals than in small ones
(Taylor et al., 1972
). Thus,
juveniles are expected to climb more easily than adult animals of the same
species, which is corroborated by the observed differences in gait parameters
during flexed-elbow vertical climbing.
However, as a considerable amount of variability between individuals as well as between different trials of the same individual was found in the present study, it must be emphasised that it is crucial to include a sufficient number of individuals and trials in studies on orang-utan locomotion, allowing extraction of reliable information through statistical analysis of the kinematic data. In particular, further analysis would indicate whether the results for the wild adult female (Q) are an outlier or truly representative of the vertical climbing of wild adult females.
Comparison with vertical climbing kinematics in other primates
Gait parameters of other hominoid primates are shown in
Table 10. Orang-utans are
peculiar in exhibiting an extremely long cycle duration and longer strides
during vertical climbing than other primates
(Hirasaki et al., 2000; Isler,
2002a
,
2003
). At any given
dimensionless speed, the relative stride length of orang-utans is the longest
of all primates studied by Isler
(2003
), i.e. gorillas
(Gorilla gorilla gorilla), bonobos (Pan paniscus), gibbons
(Hylobates concolor gabriellae and H. c. leucogenys), spider
monkeys (Ateles fusciceps robustus) and woolly monkeys (Lagothrix
lagotricha). Together with woolly monkeys and gorillas, orang-utans
exhibit the highest percentages of quadrupedal support, and thus also a large
mean number of supporting limbs and a high duty factor, when compared with
other apes. These characteristics can be explained by the peculiarities of
orang-utan locomotion and their corresponding morphological adaptations:
orang-utans are the largest extant canopy-dwelling animals
(Cant, 1987
), and adult males
sometimes crash to the ground when a substrate breaks
(Delgado and van Schaik, 2000
),
which explains why they aim to distribute their body weight on various
substrates and move slowly to test the strength of their holds. Their limb
joints are highly mobile due to the demands placed upon them by orthograde
scrambling and bridging (Morbeck and
Zihlman, 1988
; Tuttle and
Cortright, 1988
). Accordingly, the range of motion of the major
limb joints during vertical climbing was found to be larger in orang-utans
than in African apes (Isler,
2003
). Shoulder and elbow joints are more extended at hand
contact, and, in the hindlimb, the foot is more elevated relative to the
position of the hip joint than in African apes, thus further increasing stride
length. However, such mobility is achieved at a cost. Large strides require
forces to be exerted throughout a large range of joint positions. Thus,
muscles are primarily designed for mobility and velocity of shortening rather
than for the production of large forces, and joints are not robust enough to
withstand high impact forces at sudden speed changes. As a result, orang-utans
achieve only low climbing speeds. The same can be seen in other relatively
slow primates, such as slow and slender lorises (Loris tardigradus;
Demes and Jungers, 1989
;
Sellers, 1996
). Additionally,
the large body size of orang-utans disproportionately increases the forces
acting on the joints. Thus, the slow and cautious movements of orang-utans may
not be an expression of their character or purely a result of cautiousness but
rather a biomechanical necessity reflecting a compromise between large body
mass and enhanced joint mobility.
|
Conclusions
In conclusion, our results show that the gait parameters of wild,
rehabilitant and captive orang-utans are reasonably similar, despite very
different environments. Nevertheless, there are a few significant differences
between individuals from the different localities. Cycle duration is longer
and normalised speed is lower for the wild orang-utans than for the
rehabilitants and captives, reflecting the complexity of, and lack of an
individual's familiarity with, the wild environment in comparison with that of
the feeding platform and zoos. As a result, wild orang-utans climb more
cautiously than the other locality groups. However, as the wild sample
consisted of only three individuals, these results need to be corroborated by
further analysis. Sex/age differences in the gait parameters of climbing
orang-utans are small, although juveniles in general exhibited a shorter cycle
duration and lower duty factor than other groups, reflecting the advantage of
their lower body mass. Extended-elbow vertical climbing is primarily
characterised by a higher duty factor than flexed-elbow climbing, indicating
that the former is an energetically more demanding form of locomotion. No
significant differences were found in the spatio-temporal parameters of adult
females compared with mothers, indicating that clinging infants do not
influence climbing kinematics. In comparison with other primates, orang-utans
exhibit a longer cycle duration, longer strides but lower climbing speed,
reflecting a compromise between the demands of a large body mass and extreme
joint mobility.
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Acknowledgments |
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References |
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