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Hand preference in unimanual and bimanual tasks and postural effect on manual laterality in captive red-capped mangabeys (Cercocebus torquatus torquatus).

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American Journal of Primatology 68:429–444 (2006)
RESEARCH ARTICLE
Hand Preference in Unimanual and Bimanual
Tasks and Postural Effect on Manual Laterality
in Captive Red-Capped Mangabeys
(Cercocebus torquatus torquatus)
C. BLOIS-HEULIN, J.S. GUITTON, D. NEDELLEC-BIENVENUE, L. ROPARS,
AND E. VALLET
UMR 6552, University of Rennes 1, CNRS, Paimpont, France
Hand preference in 11 captive red-capped mangabeys (Cercocebus
torquatus torquatus) was examined under different conditions: a free
situation during spontaneous food processing, three different postural
conditions (brachiating, and bipedal and tripedal standing), and a
situation involving bimanual processing. Generally, individual laterality was found regardless of the task and behavior involved. However, the
number of monkeys with hand preferences and the strength of the
preference increased with the complexity of the tasks. The monkeys
exhibited a significantly higher and positive mean manual preference
index (HI) when they were hanging than when they were quadrupedal
or sitting. The strength of manual preference (ABS-HI) was in turn
higher when the monkeys were hanging or bipedal than when they were
quadrupedal. The strength of manual preference was higher for both the
bimanual and experimental tasks than for unimanual tasks and
spontaneous activities. Although our sample was too small to allow us
to make any generalizations concerning lateral preferences in red-capped
mangabeys, we propose some hypotheses about the influence of posture
stability and task complexity. Am. J. Primatol. 68:429–444, 2006. c 2006
Wiley-Liss, Inc.
Key words: laterality; Cercocebus torquatus torquatus; posture; task
complexity
INTRODUCTION
In the past, studies on laterality focused solely on Homo sapiens; however,
in recent years many animal species have also been studied in this context
[Harris, 1989; Robins et al., 1998; Roth, 2003; Vallortigara & Bisazza, 2002].
Correspondence to: C. Blois-Heulin, UMR 6552, Université de Rennes 1, Station Biologique,
F-36380 Paimpont, France. E-mail: catherine.blois-heulin@univ-rennes1.fr
Received 2 November 2003; revised 13 August 2004; revision accepted 23 August 2004
DOI 10.1002/ajp.20239
Published online 15 March 2006 in Wiley InterScience (www.interscience.wiley.com).
r 2006 Wiley-Liss, Inc.
430 / Blois-Heulin et al.
Such studies contribute to a better understanding of the origins of human
brain asymmetry and its adaptive value [Vallortigara & Bisazza, 2002].
The functional specialization of human brain hemispheres was first revealed
by studies of the relationships between language disorders and brain
damage [Brocca, 1877]. Similarly, the link between cortical asymmetry
and manual asymmetry was established very early on in humans, and
appears to have been confirmed in other vertebrates [Bisazza et al., 1996;
Bradshaw, 1991].
The conclusions of various long-term studies on manual laterality in
nonhuman primates appear to be contradictory [MacNeilage et al., 1987; McGrew
& Marchant, 1997]. For a long time it was believed that no uniform laterality
direction existed, and that the observed laterality was due only to environmental
or experimental conditions [Warren, 1977]. However, recent reports have
revealed laterality biases at the population level, and theories have been
developed to explain these biases [Fagot & Vauclair, 1991; MacNeilage et al.,
1987]. MacNeilage et al. [1987] suggested that the primitive postures of arboreal
primates could explain their preference for using their left hand. The postural
asymmetry required for brachiating would have favored the use of the left
hand to obtain food. In a second step, ‘‘liberation’’ from the constraints of
brachiating in species that had become semiterrestrial and then terrestrial
would have allowed the development of bimanual activities and the preferential
use of the right hand for fine manipulations. However, nothing explains
why brachiating would favor the use of the left hand [Tomassello, 1987].
The influence of bipedal posture on the expression of laterality is well
documented in primates. Thus the right hand is favored by bonoboset al.,
1993], chimpanzees [Hopkins, 1993], gorillas [Olson et al., 1990], and tufted
capuchins [Westergaard et al., 1997], and the left hand is favored by galagos
[Sanford et al., 1984] and gibbons [Olson et al., 1990]. Fagot and Vauclair
[1991] estimated that only complex or new tasks could reveal a bias at the
population level. Task complexity can be defined by various criteria, including:
1) the use of one or two hands [Marchant & McGrew, 1991; Spinozzi & Truppa,
1999] that in turn can be used in similar ways or to complement each other
[Hopkins, 1995; MacNeilage et al., 1987]; 2) one or several stages required to
perform the task [Marchant & McGrew, 1991]; 3) the level of precision of motor
acts [Healey at al., 1993; Morris et al., 1993]; and 4) the use of visual guidance
[MacNeilage et al., 1987].
We tested manual preference in a semiterrestrial Old World monkey,
the red-capped mangabey (Cercocebus torquatus torquatus). The aim of this
study was to compare hand preference in different situations (experimental situation vs. spontaneous behavior, hanging vs. bipedal/quadrupedal
posture, and unimanual tasks vs. bimanual tasks). These tests involve
different types of motor demands [Healey et al., 1986; Morris et al., 1993] in
which both the type of muscles used (e.g., proximal or distal muscles)
and the precision of the movement varies. This is the first report on laterality
in C. t. torquatus. This species is particularly interesting because little is
known about its manual preferences [McGrew & Marchant, 1997]. Furthermore, mangabeys can stand and move in a bipedal posture when they are
on the ground. This behavioral trait makes them particularly interesting
subjects in which to examine the influence of bipedal/quadrupedal postures
on laterality.
Am. J. Primatol. DOI 10.1002/ajp
Laterality in Red-Capped Mangabey / 431
MATERIALS AND Methods
Subjects and Housing
The subjects were 11 red-capped mangabeys housed at the Biological Station,
Paimpont, France. The sample comprised six males and five females, ranging in
age from 3 to 20 years. All were captive-born. The monkeys were housed in three
social groups, except for two males that were housed temporarily in isolation. The
monkeys were housed in heated (221C) indoor cages (approximately 42 m3)
connected to large outdoor wire-net cages (approximately 63 m3). Both the indoor
and outdoor cages were provided with vertical and horizontal perches. Observations were conducted when the monkeys were in the indoor cages. The monkeys
were given fresh fruit and vegetables in the morning and food pellets in the
evening. Water was provided ad libitum.
Procedure
Four types of investigations were used to test hand preference. One was
based on direct observations under free conditions, and the others involved
experimental tests. The tests were performed successively. In the first situation
the monkeys were observed during their daily meals under free conditions. In the
second situation all of the monkeys, while sitting on the ground, had to open a box
to find food. In the third situation they had to stand up to take a food item.
Finally, in the fourth situation they had to hang by one hand to take a food
item with their other hand. One or two monkeys of the same group were tested
per day.
Observations Under Free Conditions
The observations made under free conditions yielded data on manual
laterality for simple, familiar daily activities. The monkeys were observed while
they were feeding in the morning. During the observations, fruit and vegetables
were distributed uniformly across the floor of the indoor cages. This spatial
distribution of food items forced the monkeys to change positions and postures
before they took another food item [Olson et al., 1990]. The animals were
observed for 12 consecutive days. Fifteen-minute focal samples were recorded for
each monkey [Altmann, 1974]. Each monkey was observed for 3 hr (15 min 12 days 5 3 hr). During the observations all behavioral items that were likely to
include laterality were recorded, but only activities that were recorded more than
10 times for an individual were retained (Table I).
For each behavioral pattern we recorded which hand was used and whether
the other hand was free or occupied. Some patterns were strictly unimanual,
whereas others could be bimanual (preliminary observations; Table I). For
bimanual activities, we recorded precisely the activities of both hands. The order
in which the monkeys were observed was changed daily so that depletion of food
items or satiety of the subjects did not influence the results.
Experimental Tasks
Box task
In the box task each monkey had to take a small slice of fruit out of a
metal box. A spring kept the lid closed (Fig. 1A). The box was placed inside
the cage and fixed to the wire-net 37 cm above ground (i.e., the distance
from the top of the box to the ground). The monkey had to open the box, keep
Am. J. Primatol. DOI 10.1002/ajp
432 / Blois-Heulin et al.
TABLE I. Characteristics of the Different Behaviors and Tasks
Task
Posture
Behavioral pattern
Other hand
One or two hand
required to take food
Free
condition
Sitting on
the ground
Take a food item
Eat with one hand
Search for food
Move with food in
one hand
Pull a bit off a fruit
Eat with two hands
Peel fruit
Free
Free
Free
On the
ground
Support
Support
Support
Box task
Sitting on
the ground
Open box
Take food
Free
Unimanual
Maintaining Coordinated bimanual
the lid
Tray task
Hanging on
wire-net
Take food
Grasping
wire-net
Uncoordinated
bimanual
Take food
Support or
free
Unimanual
Bipedal task Upright on
the ground
Unimanual
Unimanual
Unimanual
Uncoordinated
bimanual
Coordinated bimanual
Coordinated bimanual
Coordinated bimanual
it open with one hand, and take the food item with the other hand. This
task required the coordination of both hands. One or two days were sufficient
to familiarize all animals to the apparatus. For a response to be considered
valid, the monkeys could be sitting in front of the box, but they had to change
their position in relation to the box before each trial. As a monkey opened the
box and then kept the box open with the other hand or a foot, the hand used
to open the box and the hand used to take the food item out of the box were
recorded. Each monkey was tested approximately 100 times (except for the
juvenile male, whose access to the test box was restricted by the other monkeys)
at a rate of 10 trials a day.
Tray task
For the tray task each monkey had to take a small slice of fruit (apple,
banana, or orange) that was placed in the center of a tray fixed onto the wire-net
inside the cage, approximately 150 cm above ground (Fig. 1B). To solve this
task, the monkey had to be hanging with one arm. The monkey had to change
its position in relation to the tray before a new trial was started. Familiarization to the apparatus took 1 day. For the monkey’s response to be considered
valid, the monkey had to climb onto the wire netting and then climb down
before starting a new trial. Data were collected only when the monkeys were
directly in front of the tray. This requirement eliminated possible artifacts
due to the position of the monkey. The hand used to take the food item was noted.
Each monkey was tested more than 100 times, at the rate of about 10 trials a day
for 10 days.
Bipedal task
For the bipedal task the subjects had to take a sunflower seed placed at
a level corresponding to the shoulder height of a fully upright subject.
The sunflower seed was held by the experimenter. For the monkey’s response
Am. J. Primatol. DOI 10.1002/ajp
Laterality in Red-Capped Mangabey / 433
A : Box
90 mm
Spring
122 mm
160 mm
55 mm
25 mm
B: Tray
Wire -net
Slice of banana
245 mm
245 mm
Fig. 1. Experimental devices used to test manual preference.
to be considered valid, it had to stand upright and maintain both hind limbs on
the cage floor while reaching for the food. It had to change its position before the
start of a new trial. The monkeys could use their non-reaching hand for upright
support during the bipedal task. Each monkey was tested 100 times, at a rate
of about 25 trials a day.
Am. J. Primatol. DOI 10.1002/ajp
434 / Blois-Heulin et al.
Statistical Analyses
A manual preference index was calculated for each monkey and for each task
or activity as follows:
RL
RþL
where R represents the number of times the right hand was used, and L is the
number of times the left hand was used [Alonso et al., 1991; Hopkins & Bard,
1993; Spinozzi & Truppa, 1999]. This index was used for comparisons between
individuals when the number of occurrences differed between individuals and
between tasks. The HI reveals the direction of manual preference and varies
continuously from 1 (totally left-handed) to 11 (totally right-handed). Its
absolute value, ABS-HI, indicates the strength of preference without taking into
account the direction of preference.
Binomial tests were used to evaluate the significance of differences between
the use of the left or right hand. A population-level effect of handedness was
evaluated by one-sample t-tests. Task and posture effects were tested by
Friedman two-way analysis of variance (ANOVA) by ranks, and Wilcoxon
signed-rank tests for related data. To analyze posture effect, the data regarding
the box task (sitting posture, n 5 11), tray task (hanging posture, n 5 11), bipedal
task (bipedal posture, n 5 11), and spontaneous behavior take a food item (only
when animals were in quadrupedal posture, n 5 11) were compared. The effect
of setting (three experimental tasks (n 5 33) and seven spontaneous behaviors
(n 5 76)), the location of the subject (on the ground: seven spontaneous behaviors
and two experimental tasks (n 5 98); hanging: tray task (n 5 11)), and the
complexity of the task (unimanual: three spontaneous behaviors (n 5 43); bipedal
task/bimanual: four spontaneous behaviors and two experimental tasks (n 5 66))
were assessed by the Mann-Whitney test.
RESULTS
Observations Under Free Conditions
The number of monkeys that showed a hand preference varied with the
activity involved (Table II). Seven, six, and four monkeys, respectively, were
lateralized for the behavioral items ‘‘take a food item’’ (four left-handed), ‘‘eat
with one hand’’ (three left-handed), and ‘‘search for food’’ (three left-handed;
Table II). For bimanual activities, 10, seven, and six monkeys, respectively, were
lateralized for the behavioral patterns ‘‘pull a bit off a fruit’’ (four left-handed),
‘‘eat with two hands’’ (four left-handed), and ‘‘peel fruit’’ (five left-handed;
Table III). And seven individuals were lateralized for ‘‘move with a food in one
hand’’ (six left-handed; Table III). Thus, more monkeys were lateralized for
bimanual than for unimanual activities (binomial test, P 5 0.03). Moreover,
bimanual activities revealed stronger laterality than unimanual activities (MannWhitney, n1 5 32, n2 5 44, Z 5 3.73, P 5 0.0002; Tables II and III).
Box Task
Nine monkeys were lateralized (Table IV). Five monkeys opened the box with
the right hand and took the food with the left hand. Except for one adult and one
juvenile male, the monkeys that opened the box with one hand took the food
inside the box with the other hand. No significant population bias was revealed
Am. J. Primatol. DOI 10.1002/ajp
Laterality in Red-Capped Mangabey / 435
TABLE II. Manual and Strength (ABS HI, Mean1SE) Preference for Unimanual
Activities in Free Situations
Take a food item
Subject
Chipie
Crapule
Gofrette
Nancy
Zunie
Bandit
Filou
Karlo
Marti
Pirate
Rapide
AF
AF
AF
AF
AF
AM
AM
AM
JM
AM
AM
Eat with one hand
Search food
RH
LH
P
RH
LH
P
RH
LH
P
NB
41
93
54
80
14
203
116
42
41
68
40
19
185
78
96
24
114
172
53
55
33
68
0.006
0.0001
0.045
0.26
0.14
0.0001
0.0019
0.31
0.18
0.0006
0.009
19
96
74
128
25
271
148
40
52
101
45
14
241
72
77
54
135
145
32
48
60
154
0.49
0.0001
0.93
0.0004
0.002
0.0001
0.91
0.41
0.76
0.002
0.0001
6
49
12
51
10
58
24
102
0.46
0.44
0.065
0.0001
31
36
18
7
7
2
10
48
57
13
2
3
0.002
0.23
0.0001
0.26
0.18
1
1
2
1
2
1
4
1
1
0
2
2
3
7
4
3
6
3
1
4
2
N
NL
ABS HI
0.2310.03
0.2310.05
0.2910.06
Bold numbers indicate significant use of that hand.
RH, right-handed; LH, left-handed; N, number of right- or left-handers for each activity; NL, total number
of lateralized subjects; NB, number of lateralized activities; AF, adult female; AM, adult male; JM, juvenile male;
P, binomial test; SE, standard error.
TABLE III. Manual and Strength (ABS HI, Mean1SE) Preference for Bimanual
Behaviors in Free Situations
Move with food
in one hand
Subject
Chipie
Crapule
Gofrette
Nancy
Zunie
Bandit
Filou
Karlo
Marti
Pirate
Rapide
N
NT
ABS (HI)
RH LH
AF
7
AF 49
AF 19
AF
5
AF
4
AM 17
AM 5
AM 0
JM 8
MA 4
MA 8
15
14
22
46
25
18
69
11
42
28
3
1
7
6
Pull a bit
off a fruit
P
RH
LH
0.13
0.0001
0.76
0.0001
0.0001
1
0.0001
0.001
0.0001
0.0001
0.23
123
32
41
69
34
96
61
69
90
71
23
9
45
166
19
8
38
22
102
121
43
137
7
10
3
0.5710.1
Eat with
two hands
P
RH LH
P
0.0001 148
8 0.0001
0.17
17 17 1
0.0001
57 94 0.003
0.0001
51 23 0.001
0.0001
29 26 0.79
0.0001
79 45 0.003
0.0001
43 30 0.16
0.01
21 46 0.003
0.04
15
9 0.31
0.01
107 21 0.0001
0.0001
22 137 0.0001
0.4610.07 0.4410.04
4
7
3
0.3710.08
Peel fruit
RH LH
93
5
40
25
7
42
15
7
15
56
29
11
8
52
9
12
25
5
5
7
21
73
5
6
1
P
NB
0.0001
0.58
0.25
0.009
0.36
0.049
0.04
0.77
0.13
0.0001
0.0001
3
1
2
4
2
3
3
3
2
4
3
0.3710.06
Bold numbers indicate significant use of that hand.
RH, right-handed; LH, left-handed; N, number of right- or left-hander for each activity; NT, total number
of lateralized subjects; NB, number of lateralized activities; AF, adult female; AM, adult male; JM, juvenile male;
P, binomial test; SE, standard error.
Am. J. Primatol. DOI 10.1002/ajp
436 / Blois-Heulin et al.
(one-sampled t-test, t (11) 5 0.29, P 5 0.78). The strength of preference varied
from 0.12 to 0.92 (Table IV).
Tray Task
All 11 monkeys were lateralized. Ten were right-handed and one was lefthanded (Table V). A one-sample t-test on HI scores revealed significant righthandedness (one-sample t-test, t (10) 5 3.87, P 5 0.003). The strength of
preference varied from 0.41 to 0.98 (Table V).
Bipedal Task
Ten monkeys were lateralized (seven were right-handed and three were lefthanded; Table V). However, a one-sample t-test did not reveal right-handedness
TABLE IV. Manual and Strength of Preferences (ABS HI) for ‘‘Box Task’’
Chipie
Crapule
Gofrette
Nancy
Zunie
Bandit
Filou
Karlo
Marti
Pirate
Rapide
AF
AF
AF
AF
AF
AM
AM
AM
JM
AM
AM
TL
OR/TL
OL/TR
P
ABS HI
83
10
63
39
78
41
70
122
3
46
2
30
63
6
33
9
98
25
12
19
59
23
0.0001
0.0001
0.0001
0.56
0.0001
0.0001
0.0001
0.0001
0.0009
0.25
0.0001
0.47
0.73
0.83
0.08
0.79
0.41
0.47
0.82
0.73
0.12
0.84
5
4
Bold numbers indicate significant use of that hand.
OR/TL, open the box with the right hand/take food with left hand; OL/TR, open with the left hand/take with
the right hand; TL, number of lateralized subjects; AF, adult female; AM, adult male; JM, juvenile male;
P, binomial test.
TABLE V. Manual and Strength Preferences for Tray Task and Bipedal Task
Tray task
Subject
Chipie
Crapule
Gofrette
Nancy
Zunie
Bandit
Filou
Karlo
Marti
Pirate
Rapide
RH Total
AF
AF
AF
AF
AF
AM
AM
AM
JM
AM
AM
138
102
125
75
142
106
84
14
133
169
106
175
106
164
106
147
107
107
156
156
175
120
P
0.0001
0.0001
0.0001
0.0001
0.0001
0.0001
0.0001
0.0001
0.0001
0.0001
0.0001
Bipedal task
Direction Strength RH Total
R
R
R
R
R
R
R
L
R
R
R
0.58
0.92
0.52
0.41
0.93
0.98
0.57
0.82
0.71
0.93
0.77
89
97
56
99
62
27
75
67
38
97
13
100
100
100
100
100
100
100
100
100
100
100
P
0.0001
0.0001
0.27
0.0001
0.0001
0.0001
0.0001
0.0001
0.0001
0.0001
0.0001
Direction Strength
R
R
A
R
R
L
R
R
L
R
L
0.78
0.94
0.12
0.98
0.24
0.46
0.50
0.34
0.24
0.94
0.74
RH, right-hand; AF, adult female; AM, adult male; JM, juvenile male; R, right-handed; L, left-handed;
A, ambidextrous.
Am. J. Primatol. DOI 10.1002/ajp
Laterality in Red-Capped Mangabey / 437
(one-sample t (10) 5 1.72, P 5 0.12). The strength of preference varied from 0.12
to 0.98 (Table V).
Comparisons Between Tasks
No significant difference on strength of preference was found between leftand right-handedness (Mann-Whitney, n1 5 75, n2 5 64, Z 5 0.09, P 5 0.22).
Impact of Task Type on the Strength of Laterality
The type of task significantly influenced both the direction (Friedman, dl 5 9,
H 5 25.59, P 5 0.002) and the strength of manual preference (Friedman test,
dl 5 9, H 5 29.38; P 5 0.0006). In the tray task the monkeys were more righthanded than in other tasks or behaviors (Fig. 2A). Spontaneous and experimental
tasks were divided into three groups according to their strength of manual
preference (Wilcoxon test, Po0.05; Fig. 2B). Group A, with the lowest strength
of laterality indices, included ‘‘take a food item,’’ ‘‘eat with one hand,’’ ‘‘search for
food,’’ ‘‘eat with two hands,’’ and ‘‘peel fruit’’ (all of these activities were observed
under free conditions). Group B, with medium laterality indices, included
activities observed under the free conditions (e.g., ‘‘move with food in one hand,’’
‘‘eat with both hands,’’ and ‘‘peel’’), as well as activities observed under
experimental conditions (e.g., ‘‘take food out of box,’’ ‘‘open box,’’ and ‘‘take food
when upright’’). Group C included one activity with the highest index: ‘‘take food
from tray’’ (an activity observed under experimental conditions).
Effect of Different Factors Characterizing Tasks on Manual
and Strength Preference
Effect of posture on manual and strength preference
More monkeys were right-handed when they were hanging or bipedal than
when they were sitting or quadrupedal (Fig. 3A). Monkeys showed a stronger
preference for using their right hand when they were hanging or bipedal than
when they were sitting or quadrupedal (Fig. 3A). Moreover, monkeys exhibited
significantly higher and positive mean HI when they were hanging than when
they were quadrupedal (Wilcoxon test, n 5 11, Z 5 2.49, P 5 0.01) or sitting
(Wilcoxon test, n 5 11, Z 5 2.86, P 5 0.004), and when they were bipedal than
sitting (Wilcoxon, n 5 11, Z 5 2.31, P 5 0.02; Fig. 3B). The strength of the
preference (ABS HI) was higher when the monkeys were hanging (Wilcoxon
n 5 11, Z 5 2.93, P 5 0.003) or bipedal (Wilcoxon test, n 5 11, Z 5 2.48, P 5 0.013)
than when they were quadrupedal (Fig. 3A).
Experimental tasks/spontaneous behavior
The experimental/spontaneous context of an activity influenced the direction
of manual preference (Mann-Whitney test, n1 5 33, n2 5 76, Z 5 –3.11,
P 5 0.0019). Monkeys were more right-handed in experimental tasks. This
context influenced the level of manual laterality (Mann-Whitney, Z 5 3.58,
P 5 0.0001). The expression of laterality was stronger for experimental tasks
than for everyday activities.
On the ground/hanging tasks
The location of the subjects (i.e., on the ground or hanging) influenced the
direction of manual preference (Mann-Whitney test, n1 5 98, n2 5 11, Z 5 –3.82,
P 5 0.0001). The monkeys were more right-handed when they were hanging.
Am. J. Primatol. DOI 10.1002/ajp
438 / Blois-Heulin et al.
A
C
0.80
B
0.60
0.40
AB
AB
AB AB
0.00
AB
AB
take upright
take food on tray
eat with two hand
C
0.80
B
B
0.60
B
B
AB AB
A
A
A
Eat with one hand
0.40
Take a food item
take upright
Take food on tray
Take food out the box
Peel fruit
Eat with 2 hands
Pull a bit off a fruit
0.00
Move with food in one hand
0.20
Search for food
Strength of laterality (±s.e.)
1.00
take food ou of the box
B
AB
A
move with food in one hand
search for food
-0.60
eat with one hand
-0.40
pull a bit off a fruit
-0.20
pell fruit
0.20
take a food item
Mean manual preference index (±s.e.)
1.00
Fig. 2. Variation of (A) the mean of the manual preference index (7SE) and (B) the mean strength
laterality in relation to the tasks or behaviors. Letters: Results of Wilcoxon test. Same letters:
No significant difference. Different letters: Significant difference.
Am. J. Primatol. DOI 10.1002/ajp
2
1.00
10
C
C
0.80
B
8
2
0.60
6
0.40
A
4
1
1
0.20
2
Number of right handlers
A
Mean strength of laterality (±s.e.)
Laterality in Red-Capped Mangabey / 439
0
0.00
Quadrupedal
Sitting
Bipedal
Hanging
B
Mean manual preference index (±s.e.)
posture
A
0.8
AB
0.6
0.4
0.2
Quadrupedal
Sitting
0
Bipedal
-0.2
Hanging
BC
-0.4
C
Fig. 3. Variations of (A) the mean of strength of laterality (7SE) and the number of right-handed
individuals (dots), and (B) the mean of manual preference index (7SE) in relation to the posture.
Letters: Results of Mann-Whitney test. Different letters: Significant difference. Same letters:
No significant difference. Number: Result of Mann-Whitney test. Different number: Significant
number of right-handed individuals. Same number: No significant difference.
Moreover, localization generally influenced strength of manual preference
(Mann-Whitney Z 5 67.77; P 5 0.0009). When the monkeys were on the ground,
there was less of a manual preference.
Unimanual/bimanual tasks requiring coordination of both hands
Whether a task required the use of one or of two hands did not influence the
direction of laterality (Mann-Whitney test, n1 5 43, n2 5 66, Z 5 1.22, P 5 0.29).
However, whether the task was unimanual or bimanual had an impact on the
strength of manual preference (Z 5 4.78; P 5 0.0001). Bimanual tasks revealed
stronger laterality than unimanual tasks.
DISCUSSION
The data presented here provide evidence of a manual preference at an
individual level, even for simple tasks, in red-capped mangabeys. Thus
mangabeys do not use their left or right hand indifferently for a given task.
Am. J. Primatol. DOI 10.1002/ajp
440 / Blois-Heulin et al.
Laterality has already been reported for several prosimians (Galago senegalensis
[Larson et al., 1989], Lemur macao [Forsythe & Ward, 1988), New World monkeys
(Cebus apella and C. capucinus [Masataka, 1990], and Erythrocebus patas [Hall
& Mayer, 1966]); Old World monkeys (Papio papio [Vauclair & Fagot, 1987],
M. mulatta [Westergaard et al., 1997; Rawlins, 1986], M. fascicularis [Brinkman,
1984], M. fuscata [Kubota, 1990], Cercopithecus neglectus [Trouillard & BloisHeulin, 2005], and Simias concolor [Miller & Paciulli, 2002]); and apes (Hylobates
concolor [Stafford et al., 1990], Pongo pygmaeus [Olson et al., 1990], and Gorilla
gorilla gorilla [Fagot & Vauclair, 1988]). However, manual preference for a
simple task is not the rule for all individuals within a group. Whatever the species,
some individuals may show a preference for either their left or right hand,
whereas others may use either hand indifferently for the same
task [reviewed in McGrew & Marchant, 1997; Steklis & Marchant, 1987; Vauclair
& Fagot, 1987].
Manual specialization in daily activities (i.e., the same hand is used for
different tasks) was found only in a few subjects. Manual specialization does not
occur very frequently, whatever the phylogenetic level. Lehman [1993] analyzed
40 reports concerning laterality in many species of primates and found evidence
for manual specialization in only 27.5% of them.
Thus simple tasks do not yield much information on laterality. Task
complexity appears to be a crucial factor because the presence or absence of
handedness appears to be related to complexity [Fagot & Vauclair, 1991]. The
need for coordination between both hands produced an increase in the number of
lateralized individuals and the strength of laterality in red-capped mangabeys.
This was verified for daily tasks (for example, pulling off a piece of fruit) as well as
under experimental conditions. This effect has already been noted in other
primates (Cebus apella [Anderson et al., 1996; Fragaszy & Adams-Curtis, 1993;
Spinozzi & Truppa, 1999; Spinozzi et al., 1998; Westergaard & Suomi, 1996],
Cercopithecus neglectus [Trouillard & Blois-Heulin, 2005], Cercopithecus aethiops
[Harrison & Byrne, 2000], and Pan troglodytes [Colell et al., 1995]). In this study,
detailed analyses of daily tasks that required the use of both hands revealed that
for three of the four activities (pull off a piece of fruit, peel fruit, and eat with two
hands), the monkeys were righted-handed in 16 cases and left-handed in seven
other cases. The need to coordinate the movements of both hands revealed a
tendency to use the right hand predominantly. This result provides support for
MacNeilage et al.’s [1987] theory that the right hand would be specialized for
finer movements.
Most of the subjects (81%) in the box task, which was the most difficult task,
were lateralized. The subjects opened the box with one hand and took the food out
with their other hand. Only one subject opened the box with one hand, held the
lid with his other hand, and took the food with the hand that had opened the box.
This bimanual task did not reveal a population bias for right-handedness. No task
specialization emerged. This result agrees with previous findings on the same
subject (Cebus apella [Westergaard & Suomi, 1996] and Cecopithecus aethiops
[Harrison & Byrne, 2000]). If, as proposed by MacNeilage et al. [1987], the right
hand is specialized for finer movements, we should have observed the use of the
right hand to open the box, and then the use of the left hand to keep the lid open,
followed by the use of the right hand to take the food. This was hardly ever
observed. Sharing tasks between the right and left hands (i.e., one hand opens,
one hand takes) was previously reported for De Brazza’s monkeys [Trouillard &
Blois-Heulin, 2005]. Therefore, this finding suggests that both hands are able
to perform finer movements when an action requires coordination of both hands.
Am. J. Primatol. DOI 10.1002/ajp
Laterality in Red-Capped Mangabey / 441
The influence of bimanuality of tasks on manual preference has been
investigated, and the results vary with the species. Rhesus monkeys [Westergaard
& Suomi, 1996] show a bias toward the right hand in bimanual tasks, whereas
Cercopithecus aethiops [Harrison & Byrne, 2000] show no specialization. Data for
Cebus apella are contradictory: Westergaard and Suomi [1996] found no taskrelated specialization (19 subjects were right-handed and 20 were left-handed),
but Spinozzi et al. [1998] indicated that a majority of Cebus apella were righthanded. However, the tasks in Spinozzi et al.’s [1998] experiments required
bimanual coordination with both hands playing complementary but different
roles: one hand was used to stabilize the object (tube) with the food in it, while the
other hand performed a more precise activity (i.e., to search for and take food
from the tube).
The scores for the tray task agree with those for the box task. The mangabeys
used the right hand more often to seize a piece of fruit, while using the left arm
and hand to maintain their posture. Thus, level 4 [McGrew & Marchant, 1997]
was reached. This level appears to be reached in visually guided tasks, and not
only when a task requires touch, as McGrew and Marchant [1997] suggested.
These results can be compared with King and Landau’s [1993] data on Saimiris.
Twenty-four of the 31 lateralized monkeys used their right hand to take a candy
while they were hanging on the wire-net with their left hand and feet. The strong
laterality of individuals (numbers as well as strength of laterality) can be related
to the monkeys’ morphological (muscular) asymmetry [Dhall & Singh, 1977; Falk
et al., 1988]. This raises the question of whether the observed manual
specialization is the result of dominance of the right hand in coordinating fine
movements, or is due to greater muscular development in the left arm. However,
this appears to be a circular argument. If such a morphological asymmetry exists,
it could be related to preferential use of the left arm for brachiating, which would
liberate the right hand for tasks requiring finer movements.
The function of maintaining a posture also emerges from the analysis of the
scores of the mangabeys taking food in a bipedal posture. Most of the subjects in
this study (90.9%) were lateralized for taking food items in a bipedal posture.
Seven of the 10 subjects were right-handed. The influence of this postural
instability on hand preference was previously stressed for apes [Hopkins, 1993;
Hopkins et al., 1993; Olson et al., 1990; de Vleeschouwer et al., 1995], prosimians
[Sanford et al., 1984; Westergaard et al., 1997], and New World monkeys [Larson
et al., 1989; Spinozzi et al., 1998]. Even though the proportions of right-handed
and left-handed rhesus macaques (species closely related phylogenetically to
mangabeys) are similar (48% are left-handed), an increase in the tendency to use
the right hand to take food exists when they are bipedal [Westergaard et al.,
1998]. Bipedal monkeys must make a precise gripping movement with their
fingers to take a food item with the right hand, while using their other hand
to stabilize themselves by holding onto the wire-net or leaning on it. The left
hand is used for stabilization and serves a function similar to that described in
the tray task. This link between bipedal posture and laterality has been stressed
in Homo sapiens: humans are not definitively lateralized before they are 3 years
old, and as children gain better upright balance, stable laterality responses appear
[Corbetta, 2003].
Another activity revealed marked laterality in mangabeys. For moving while
holding a piece of food in one hand (moving on three limbs), eight of the 11
subjects were lateralized, and 87.5% of the lateralized subjects were left-handed.
We hypothesize that holding food in the left hand liberates the right hand
for possible use in an activity involving greater precision. The laterality of this
Am. J. Primatol. DOI 10.1002/ajp
442 / Blois-Heulin et al.
activity was previously noted by Diamond and McGrew [1994] in cotton-top
tamarins and Steklis and Marchant [1987] in chimpanzees. However, the
direction of laterality varied in those studies. The chimpanzees were left-handed
(but not significantly: seven were left-handed, four were right-handed, and 15
were ambidextrous) and the tamarins were right-handed. Nevertheless,
laterality of this activity does not appear to be the rule in primates (chimpanzees
[Hopkins et al., 1993; Hopkins & de Waal, 1995] and Macaca fuscata [Watanabe
& Kaway, 1993].
To conclude, although the size of our sample does not allow us to make any
generalizations about lateral preferences in red-capped mangabeys, it appears
that precise movements are performed mostly with the right hand. The
complexity of the task, and mainly the maintenance of a stable posture, are
factors that appear to be involved in the emergence of laterality. We hypothesize
that instability requiring the use of one hand, either to avoid swaying or to hold
an object firmly, may be a factor favoring the emergence of marked laterality
at the population level. This type of laterality related to instability, in particular
to postural instability, should be more evident in arboreal species that search
for food and feed (under natural conditions) in trees and in more or less
unstable postures.
ACKNOWLEDGMENTS
We thank M.A. Richard, A. Cloarec, M. Novak, and the two anonymous
referees for helpful comments on the manuscript, and A. Cloarec for translation.
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