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Asymmetries in postural control and locomotion in chimpanzees (Pan troglodytes).

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American Journal of Primatology 68:802–811 (2006)
RESEARCH ARTICLE
Asymmetries in Postural Control and Locomotion
in Chimpanzees (Pan troglodytes)
ANA MORCILLO1, SAMUEL FERNANDEZ-CARRIBA2, AND ANGELA LOECHES1
1
Departamento de Psicologı´a Biológica y de la Salud, Facultad de Psicologı´a,
Universidad Autónoma de Madrid, Madrid, Spain
2
Emory Autism Center, Emory University, Atlanta, Georgia
Posture and locomotion are two of the most primitive and basic motor
manifestations of an organism’s behavior. Although the restrictions they
impose on other motor functions are evident, few studies have considered
the possibility of asymmetries in these behaviors in human and
nonhuman primates, and how they might impact other asymmetries at
higher functional levels. The aim of the current study was to explore in a
group of 10 chimpanzees at the Madrid Zoo-Aquarium the degree of
asymmetry in four behaviors related to locomotion (walking, ascending,
descending, and brachiating) and four behaviors associated with posture
(sitting, lying, hanging, and changing postures). Few subjects showed
individual preferences, but significant trends in the group for some of the
behaviors were found, including right-hand use when initiating quadruped walking, and left-hand use when descending and hanging. Some
significant correlations also emerged: a negative one between walking
and descending, and a positive one between walking and brachiating and
between sitting and changing postures. No correlations were found
between locomotor and postural modes. Although we cannot make
generalizations on the population level at this time, these findings
highlight the importance of considering postural and locomotion factors
when studying motor asymmetries in primates. Am. J. Primatol.
68:802–811, 2006. c 2006 Wiley-Liss, Inc.
Key words: laterality; hand preference; postural control; locomotion;
Pan troglodytes
INTRODUCTION
Postural control and locomotion are rudimentary manifestations of motor
systems in organisms. Because they are basic and necessary processes, their study
could be an adequate yet simple means of approaching the topic of functional
Contract grant sponsor: Universidad Autónoma de Madrid.
Preliminary data from this study were presented at the IV APE Conference, Madrid, 2001.
Correspondence to: Ana Morcillo, Departamento de Psicologı́a Biológica y de la Salud, Facultad de
Psicologı́a, Universidad Autónoma de Madrid, 28049 Madrid, Spain. E-mail: ana.morcillo@uam.es
Received 6 May 2005; revised 2 November 2005; revision accepted 2 November 2005
DOI 10.1002/ajp.20280
Published online in Wiley InterScience (www.interscience.wiley.com).
r 2006 Wiley-Liss, Inc.
Asymmetry in Posture in Chimpanzees / 803
motor asymmetries, and serve as a starting point for comparative studies on the
evolution of brain organization in human and nonhuman primates [Seltzer et al.,
1990]. Indeed, some authors have hypothesized that postural control is an
important factor in explaining the origin of manual laterality in nonhuman
primates [MacNeilage et al., 1987] and the early hominids [Calvin, 1983]. It has
also been argued that variation in cerebral dominance for language is more
strongly associated with postural asymmetries, such as footedness, than with
more traditional measures of motor dominance, such as handedness [Day &
MacNeilage, 1996; Elias et al., 1998; Maki, 1990]. However, few studies have
examined posture and locomotion asymmetries in primates.
Most of the research on lateralization of locomotor modes in nonhuman
primates has focused on quadruped walking. Studies in captivity with lemurs
(Varecia variegate) [Forsythe & Ward, 1987], orangutans (Pongo pigmaeus)
[Cunningham et al., 1989; Heestand, 1986], gorillas (Gorilla gorilla) [Heestand,
1986], chimpanzees (Pan troglodytes) [Heestand, 1986], and bonobos (Pan
paniscus) [Hopkins & de Waal, 1995], as well as human studies [Day &
MacNeilage, 1996; Seltzer et al., 1990], have provided evidence of group-level
right preferences in the upper limb when initiating quadruped locomotion in all
these species (except lemurs [Forsythe & Ward, 1987]). However, two studies in
wild chimpanzees [Marchant & McGrew, 1996; McGrew & Marchant, 2001] did
not report asymmetries in the leading limb. Interestingly, Hopkins and de Waal
[1995] found a significant negative correlation in bonobos between the preferred
hand to carry food and the preferred hand to initiate locomotion.
Regarding arboreal locomotion, Hook and Rogers [2002] reported no group
differences in marmosets for jumping and landing. However, the strength of the
preference was higher in these measures than in quadruped walking, with more
subjects using their right hand to break when landing compared to those that
showed a right preference when walking. In other studies of arboreal locomotion,
Stafford et al. [1990], and more recently Redmond and Lamperez [2004], reported
no preference in gibbons (Hylobates spp.) when brachiating, although strong
individual hand preferences were observed in both studies.
Most studies on postural modes have explored how postural requirements or
constrictions may influence the intensity or even the direction of the manual
preference exhibited by an individual when performing a specific task. The
rationale for these studies is that an atypical or unstable posture (such as
standing bipedally, in the case of most of nonhuman primates) may increase the
spatial-temporal requirements of the task [Fagot & Vauclair, 1991] or demand
more-integrated activity by the central nervous system in order to maintain
balance [Larson et al., 1989; Ward et al., 1993].
Visually guided reaching is probably the behavior that is most extensively
studied to explore postural effects on hand preference. Studies of great apes have
shown individual hand preferences when reaching from a quadruped position
[Annett & Annett, 1991; Hopkins & Pearson, 2000; McGrew & Marchant, 1992;
Stafford et al., 1990]. However, studies of gorillas [Olson et al., 1990], orangutans
[Hopkins, 1993; Olson et al., 1990], chimpanzees [Hopkins, 1993], and bonobos
[Collel et al., 1995; Hopkins & de Waal, 1995] have reported a right-hand
preference on the group level when reaching from a bipedal position. In
chimpanzees, a population-level right handedness was also found for quadrupedal
reaching [Hopkins et al., 2002; Hopkins et al., 2005]. Similarly, right-hand
preference in reaching for objects has been found at a population-level in humans,
in both bipedal and quadrupedal positions [Westergaard et al., 1998]. Other
unusual or restrictive postures that require different degrees of body adjustment
Am. J. Primatol. DOI 10.1002/ajp
804 / Morcillo et al.
(e.g., reaching for food or other objects while leaning over water) indicate a lefthand preference in black lemurs [Forsythe et al., 1988] and squirrel monkeys
(Saimiri sciureus) [King & Landau, 1993], and a right-hand preference in
chimpanzees [Collel et al., 1995].
Although these findings show that posture can influence manual laterality as
exhibited in unimanual tasks, there has been no thorough examination of a
possible hand preference in posture per se. The relevance of this is that hand
preference in a specific task clearly could be intensified or even changed by a
preexisting stable preference when one or another posture is adopted. In fact,
lower-limb preferences in purely postural behaviors have been observed in several
species of mammal, including bovines [Albright & Arave, 1997; Lane & Phillips,
2004; Phillips et al., 2003] and humans [Day & MacNeilage, 1996; Seltzer et al.,
1990]. For example, in humans Seltzer et al. [1990] found a group tendency in 100
individuals to distribute their body weight toward the left when standing, but
only individual differences when turning around.
Given the scarcity of data on motor asymmetries in locomotion and postural
control in nonhuman primates, the aim of this study was to explore whether a
group of chimpanzees (Pan troglodytes) showed any hand preference, on the
individual and/or group level, when initiating different spontaneous behaviors
related to locomotion and postural control. Walking, ascending, descending, and
brachiating were the behavioral categories considered for locomotion, and sitting,
lying, hanging, and changing postures were the ones associated with postural
control. Whereas right-hand preferences in great apes and humans were
previously reported for quadrupedal locomotion on a horizontal surface
[Cunningham et al., 1989; Day & MacNeilage, 1996; Forsythe & Ward, 1987;
Heestand, 1986; Hopkins & de Waal, 1995; Seltzer et al., 1990], one would expect
preferences to emerge in more individuals in the case of climbing or walking on an
incline (ascending and descending), as in other restrictive behaviors, since they
involve starting from a more unstable position, which requires more balance and
support control. Because going over an obstacle, descending to a lower level, and
simply walking horizontally may require very different forms of muscular
coordination, as they do in humans [Carpenter et al., 1998], the direction of the
asymmetry in ascending and descending would not necessarily be the same as in
walking. Brachiating is another unique type of locomotion (i.e., suspensory)
in which the upper limbs receive all the body weight. In this regard, individual
(but not group) preferences have been reported for gibbons [Stafford et al., 1990].
Finally, some level of asymmetry could be expected in posture alone, based on
findings about posture asymmetries in humans and the influence of complex
postures on the degree of manual asymmetry for certain tasks in human and
nonhuman primates.
MATERIALS AND METHODS
Subjects and Housing
Observations were conducted on a group of 10 chimpanzees (Pan troglodytes)
at the Madrid Zoo-Aquarium in Spain. The group included eight adults (six
females and two males, 415 years old), one juvenile male (Gost, o7 years old)
and one infant male (Gudu, o3 years old). With the exception of the two youngest
chimpanzees, which were born at the zoo, all of the individuals were wild-born
and captured when they were young. At the Madrid Zoo-Aquarium the
chimpanzees have access to an indoor enclosure that is used for feeding and
sleeping, and to an outdoor space of approximately 200 m2 that is enriched with
Am. J. Primatol. DOI 10.1002/ajp
Asymmetry in Posture in Chimpanzees / 805
different substrates and objects (several big rocks, areas with sawdust, plastic
toys, ropes, tires, etc.). On top of the outdoor enclosure is a heavy metal structure
made of bars that have different orientations and are attached together at
different angles, which the chimpanzees like to climb. Observations took place
only in the outdoor enclosure.
Procedure
Four observers received training for 3 months in observing and recording of
the focal behaviors of interest. Subsequently, an interrater reliability analysis was
conducted. Two adult chimpanzees and the infant male were each observed by the
four observers simultaneously during five 15-min-long focal periods. The level of
agreement among the observers was high and significant (Kendall’s coefficient
of concordance, W 5 0.97, n 5 4, Po0.01).
For the next 3 months the chimpanzees were observed by means of individual
focal sampling 3–4 days a week, four subjects a day, for 15 min each. The total
amount of observation time per subject was 9.5 hr. The order in which individuals
were observed and the time of the day when they were observed were randomized
across days. Hand use was recorded when the chimpanzees initiated the four
different locomotor behaviors described in Table I. These behaviors included
walking, ascending, descending, and brachiating. In the case of the postural
modes (sitting, lying, hanging, and changing postures), the hand used to sustain
TABLE I. Operational Definitions of Locomotor and Postural Behaviors
Locomotor modes: The leading upper limb initiating the following types of locomotion was
recorded when the animal was moving in an unbiased direction.
Walking: Quadruped locomotion on a horizontal plane. To record the hand that initiated
the walking the individual had to be in a motionless neutral position previously, i.e., a
quadruped position without any limb being forward. A new event was registered if any
walking stopped for at least 5 seconds, and the individual assumed a motionless neutral
position.
Ascending: Quadruped locomotion when going up or getting on an elevated object or
surface (445 degrees), or when climbing. The starting position had to be neutral and
motionless.
Descending: Quadruped locomotion when going down or getting off from an elevated
object or plane (445 degrees), or when climbing down. The starting position had to be
neutral and motionless.
Brachiating: Bimanual locomotion in a three-dimensional space. A new event was
registered if any brachiating stopped for at least 5 seconds, and the individual was
suspended hanging from both hands in a neutral motionless position.
Postural modes: Manual use in the following postures and postural adjustment was recorded.
Sitting: Being seated and motionless. The hand used to hold onto some surface or
structure, or to partially support the body was recorded. This hand alone did not
constitute the whole body support.
Lying: Reclining or stretching out motionless on a horizontal surface. The upper limb on
the side bearing the most amount of body weight was recorded.
Hanging: Assuming a vertical position while suspended totally or partially from one of
the upper limbs (only partially if the lower limbs might act as additional support). The
hand from which the individual was hanging was recorded.
Changing postures: Adjustment or shift in the body position, being this bipedal,
quadrupedal, sitting, or lying, without conveying locomotion. The hand supporting or
holding most of the body weight to change postures was recorded.
Am. J. Primatol. DOI 10.1002/ajp
806 / Morcillo et al.
the greater proportion of the body weight was recorded. These postural behaviors
are also described in Table I. The different postures were grouped according
to their different mechanical and kinematic attributes (i.e., how much weight
was borne by the upper limbs, and to what extent other supporting body areas
were used).
Data Analysis
Binomial z-scores were calculated for each subject and behavior to indicate
the directionality of the preferences. The subjects were categorized as righthanded (zZ1.96), left-handed (zr 1.96), or ambidextrous (z4 1.96 and
zo1.96). In addition, the percentage of right-hand use was calculated for each
subject and behavioral category (%R 5 (R/R1L) 100). Any possible group
tendencies in these percentages of right-hand use for each behavior were explored
using one sample t-tests. Finally, Pearson product-moment correlations were
calculated between all possible pairs of behavioral categories in order to examine
consistency across categories and individuals. All analyses were bilateral, with
a level of significance of Pr0.05.
RESULTS
Locomotion
Table II shows the total number of observations for each locomotor and
postural behavior in each subject, and the corresponding z-scores and percentages
of right-hand use. Based on the z-scores, three individuals showed a significant
(Pr0.05) hand preference in walking, and one in brachiating. All of these
individuals were right-handed (Fig. 1). The group average percentages for righthand use (7SD) in the locomotor modes were 57% (77) for walking, 49% (77)
for ascending, 40% (713) for descending, and 55% (79) for brachiating. A single
sample t-test demonstrated a significant deviation from a 50% right-hand use in
walking (t (9) 5 3.03, Po0.02) and descending (t (9) 5 2.42, Po0.04) with
a tendency toward using the right hand when beginning to walk, and using the
left hand to initiate descending.
Postural Control
Some individuals also showed hand preferences in postural modes (see
Table II). One subject significantly used his right hand as support when sitting;
two were classified as right-handed and one as left-handed when lying; another
subject significantly preferred to use the left hand while hanging; and one showed
a right preference and another a left preference when changing postures (Fig. 1).
As Table II shows, one adult male showed a significant right-hand preference in
three of the four postural modes (sitting, lying, and changing postures). The
group average percentages for right-hand use (7SD) in the postural modes were
54% (77) for sitting, 54% (714) for lying, 44% (78) for hanging, and 51% (714)
for changing postures. Only for hanging did a single sample t-test show a
significant group tendency (t (9) 5 2.39, Po0.05), with individuals preferring
to use their left hand.
Relations Between Measures
To explore a possible relation between different behaviors, we ran Pearson
product-moment correlations using the percentages of right-hand use. Within
Am. J. Primatol. DOI 10.1002/ajp
Asymmetry in Posture in Chimpanzees / 807
Fig. 1. Distribution of hand preferences among individuals for each behavior related to locomotion
and postural control. The filled circles () indicate the z-scores that were significant (Pr0.05),
and the open circles (J) indicate the z-scores that were nonsignificant.
locomotor modes a significant positive correlation was found between walking
and brachiating (r 5 0.63, Po0.05) and a significant negative correlation was
obtained between walking and descending (r 5 0.65, Po0.04), i.e., individuals
tended to use the same hand to start walking and brachiating, but opposite hands
when initiating walking on a horizontal surface and descending to a lower level.
Within postural modes, a significant positive correlation was found between
sitting and changing postures (r 5 0.68, Po0.03), which indicates that individuals
used the same hand to hold on when they were sitting and when they were
changing postures. The same tendency was found in the case of lying and
changing postures, with a positive and marginally significant correlation between
the two (r 5 0.62; P 5 0.06). Finally, no significant correlations were found
between any of the locomotor and postural modes.
DISCUSSION
This is the first study to explore hand preference in different spontaneous
behaviors related to locomotion and postural control in chimpanzees. The data
reveal some relevant findings. First, the chimpanzees at the Madrid ZooAquarium showed significant group trends to use either the right or the left upper
limb more often for some measures. Second, significant correlations emerged
between some locomotor behaviors on one hand, and between some postural
behaviors on the other hand. Nevertheless, no significant correlation was found
between locomotor and postural modes.
It is noteworthy that three of the 10 chimpanzees showed a significant
individual hand preference (being classified as right-handed) when initiating
Am. J. Primatol. DOI 10.1002/ajp
Am. J. Primatol. DOI 10.1002/ajp
n
c
b
Adult female.
Adult male.
Juvenile male.
d
Infant male.
Pr0.05.
Pr0.01.
a
73
Uskaa
Ulaa
129
138
Noea
Lindaa
117
Cheyena 127
Laraa
164
77
Utib
Luckib
130
Gostc
200
218
Gudud
Total
1373
Indiv
2.34
1.05
1.10
1.84
0.17
1.01
0.91
4.47
0.21
2.91
z
Walking
n
64.3 25
55
26
55
46
58.9 41
51.1 35
45.7 48
55.8 15
70
23
51
68
60
68
56.7 395
%R
–1.00
–0.19
1.32
–1.56
0.00
–0.14
0.00
0.41
0.00
–0.36
z
n
–0.51
–1.55
–0.23
–1.76
1.25
–0.17
–0.51
–0.89
–0.22
–1.11
z
n
z
60
52
51.1
55
46.1
41.1
71.4
60
49.5
66.6
55.3
%R
Branching
40
5 0.00
26.6 48 0.14
44.4 127 0.17
30.7 20 0.22
68.7 39 –0.16
47
34 –0.85
40
14 1.33
20
5 0.00
45 115 0.00
35
45 2.08
39.7 452
%R
Descending
40
15
46.1 15
60.8 18
36.5 26
51.4 16
47.9 34
53.3 15
56.5
5
50
20
47
20
49 184
%R
Ascending
52
95
128
87
77
119
69
64
134
111
936
n
0.69
1.43
–0.44
0.64
1.82
–0.73
3.37
–0.12
0.08
–0.19
z
Sitting
n
55.7 20
57.9 14
47.6 19
54
32
61
30
46.2 40
71
25
48.4 23
50.7 29
48.6
8
54.1 240
%R
0.22
–0.26
0.45
–2.29
0.54
2.68
2.4
0.00
1.11
–0.35
z
Lying
n
z
%R
n
1.70
–0.32
–0.32
–0.50
1.92
0.87
2.62
–2.24
–0.16
–1.60
z
67.8
45.9
45.9
44.4
66.6
57.4
74.1
33.3
47.3
31.5
51.2
%R
Changing postures
55
11 0.00 45.4 28
42.8 42 –2.62 28.5 37
57.9 53 1.09 58.5 37
28.1 10 0.00 50
36
56.6 45 –0.74 44.4 39
72.5 52 –1.80 36.5 47
76
15 0.00 46.6 42
52.1 11 –0.60 36.3 51
62 100 –1.50 042
38
37.5 87 –0.21 48.2 19
54 426
43.6 374
%R
Hanging
TABLE II. Number of Observations for Each Locomotor and Postural Behavior in Each Subject (n), and z-Scores and Average
Percentage of Right-Hand Use (%R)
808 / Morcillo et al.
Asymmetry in Posture in Chimpanzees / 809
walking, and that a significant group trend toward right-hand use was found for
this behavior. Such a tendency is consistent with the right upper limb preference
reported for the initiation of quadruped walking in the four species of great apes
[Cunningham et al., 1989; Heestand, 1986; Hopkins & de Waal, 1995] and in
humans [Day & MacNeilage, 1996; Seltzer et al., 1990]. As some of the above-cited
authors suggested, this could be a common trait in the great apes and humans
that would suggest a left hemisphere specialization in the control of locomotion.
Despite our prediction that there would be more asymmetries in ascending
and descending, no significant individual preferences were found when these
behaviors were initiated. Nevertheless, there was a significant group trend
toward the use of the left upper limb when the chimpanzees were walking down
or getting off an elevated surface or structure. Our results must be interpreted
carefully because of the limited number of recorded events in these behavioral
categories, although a connection could be made between the higher levels of
motor and visuospatial control required to descend [Hook & Rogers, 2002] and a
right hemisphere specialization for visuospatial tasks as reported in some species
of nonhuman primates [King & Landau, 1993; Vauclair & Fagot, 1993] and
humans [e.g., Wendt & Risberg, 1994].
No group tendency was found for brachiating, and only one individual, which
had also shown a significant right-hand preference in walking, was classified as
right-handed. Some authors have questioned the advantage of manual asymmetries in locomotion for arboreal primate species, which should be able to control
their movement well from both sides when traveling through branches that form
a discontinuous tridimensional pattern [Hook & Rogers, 2002]. The chimpanzee
is not strictly an arboreal species, and quadruped walking is the most frequent
type of locomotion in that species (although bipedal walking and brachiating
are also common) [Tuttle, 1986]. To our knowledge, the data in our study
constitute the first attempt to explore hand use in brachiating by chimpanzees,
and future studies should further explore this topic wherever an ‘‘arboreal’’
environment is available for the chimpanzees.
The fact that the chimpanzees in this study tended to use the same hand
when initiating quadruped walking and brachiating suggests that both behaviors
may be controlled or coordinated by the same or similar motor systems. That the
chimpanzees used opposite hands when initiating walking and descending is not
surprising, and may be explained by the different postural constraints found in
each behavior. The hand that initiates the move when walking, and probably
when brachiating, is the opposite of the hand that is actually bearing the body
weight and controlling the individual’s balance and posture. On the other hand,
descending could be understood as a shift of postures whereby support and
balance are momentarily transferred to another limb before the real locomotion is
initiated. This raises an interesting question about which hand is influencing
which–the hand that initiates locomotion or the hand that controls the overall
posture [Hopkins et al., 1997]. More data on postural control as an independent
measure are warranted in order to clarify this issue.
Our results show that one to three subjects demonstrated significant
individual preferences in each postural category. As a group, the chimpanzees
significantly showed a left-hand preference to hold their body while hanging.
Hanging is unique among the postural behaviors in this study because placing all
body weight on one hand while hanging from some structure could be considered
a difficult and unstable posture [Hopkins, 1993; Fagot & Vauclair, 1991] in which
asymmetrical behaviors may emerge or intensify [Collel et al., 1995]. Taking into
account the fact that the chimpanzees in this study were not engaged in any task
Am. J. Primatol. DOI 10.1002/ajp
810 / Morcillo et al.
with the unoccupied hand, and other results that point out a left-hand preference
for hanging in chimpanzees [Hopkins, 1996], one could argue that this postural
preference could be intensifying, complementing, or even influencing the righthand preference that has been reported for such complex unimanual tasks in
great apes.
Finally, a significant positive correlation and a borderline association were
found respectively between changing postures and sitting, and between changing
postures and lying, which means that the hand taking the lead shifting into a new
posture was often the one being used for postural support. On the other hand,
in agreement with findings by Seltzer et al. [1990] in humans, no significant
correlation was found in this study between locomotor and postural modes.
Accordingly, motor control for locomotion and motor control for a motionless
posture appear to be independent; however, it is unlikely that they do not interact
at some level, since posture coordination is essential for initiating locomotion.
In summary, the few significant group trends and correlations that emerged
even in individuals that did not show strong individual preferences demonstrate
how important it is to consider motor asymmetries in posture and locomotion, as
well as their possible interaction with other functional asymmetries in human
and nonhuman primates. Currently, we can only speculate that asymmetries
in postures or locomotion in an organism may be an adaptive solution to better
organize the different levels of motor coordination [Geschwind, 1985]. In any
case, the few studies conducted to date have pointed out that asymmetries do exist
at this primitive level, and thus it could be argued that locomotion and postural
asymmetries are ancestral precursors of other, more complex lateralized motor
functions that appeared later in mammalian evolution.
ACKNOWLEDGMENTS
We are grateful to the Madrid Zoo-Aquarium for allowing us to conduct this
study with the chimpanzees, and to the anonymous referees for their very
valuable comments and advice on the early version of the manuscript. We also
thank Rubén Gómez, Ivan Pérez, and Paloma Martı́n for their valuable help
in collecting data, and Dr. William D. Hopkins for helpful comments on the
manuscript. Support for this research was provided by a UAM Scholarship for
Graduate Studies to the first author.
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Am. J. Primatol. DOI 10.1002/ajp
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