Hand preference in unimanual and bimanual tasks and postural effect on manual laterality in captive red-capped mangabeys (Cercocebus torquatus torquatus).код для вставкиСкачать
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: email@example.com 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.  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  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  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  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. , 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  found no taskrelated specialization (19 subjects were right-handed and 20 were left-handed), but Spinozzi et al.  indicated that a majority of Cebus apella were righthanded. However, the tasks in Spinozzi et al.’s  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  suggested. These results can be compared with King and Landau’s  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  in cotton-top tamarins and Steklis and Marchant  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. REFERENCES Alonso J, Castellano MA, Rodriguez M. 1991. Behavioural lateralization in rats: prenatal stress effects on sex differences. Brain Res 539:45–50. Altmann J. 1974. Observational study of behaviour: sampling methods. Behaviour 49: 227–267. Anderson JR, Degiorgio C, Lamarque C, Fagot J. 1996. A multi-task assessment of hand lateralization in capuchin monkeys (Cebus apella). Primates 37:97–103. Bisazza A, Cantalupo C, Robins A, Rogers L, Vallortigara G. 1996. Right-pawedness in toads. Nature 379:408. Bradshaw JL. 1991. Animal asymmetry and human heredity: dextrality, tool use and language in evolution–10 years after Walker (1980). Br J Psychol 82:39–59. Brinkman C. 1984. Determinants of hand preference in Macaca fascicularis. Int J Primatol 5:325. Brocca P. 1877. Perte de la parole. Ramollissement chronique et partiel du lobe antérieur gauche du cerveau. Bull Soc Anthropol 2: 235–237. Colell M, Segarra MD, Sabatier-Pi J. 1995. Manual laterality in chimpanzees (Pan troglodytes) in complex tasks. J Comp Psychol 109:298–307. Am. J. Primatol. DOI 10.1002/ajp Corbetta D. 2003. Right-handedness may have come first: evidence from studies in human infants and nonhuman primates. Behav. Br Sc 26:217–218. de Vleeschouwer K, Van Elsacker L,Verheyen RF. 1995. Effect of posture on hand preferences during experimental food reaching in bononbos (Pan paniscus). J Comp Psychol 109:203–207. Dhall U, Singh I. 1977. Anatomical evidence of one-sided forelimb dominance in the rhesus monkey. Anat Anzeiger 141:420–425. Diamond AC, McGrew WC. 1994. True handedness in the cotton-top tamarin (Sanguinus oedipus)? Primates 35:69–78. Fagot J, Vauclair J. 1988. Handedness and bimanual coordination in lowland gorilla. Brain Behav Evol 32:89–95. Fagot J, Vauclair J. 1991. Asymmetrical hand use in rhesus monkeys (Macaca mulatta) in tactually and visually regulated tasks. J Comp Psychol 105:260–268. Falk D, Pyne L, Helmkamp RC, DeRousseau CJ. 1988. Directional asymmetry in the forelimbs of Macaca mulatta. Am J Phys Anthropol 77:1–6. Forsythe C, Ward JP. 1988. Black lemur (Lemur macao) hand preference in food reaching. Primates 29:369–374. Laterality in Red-Capped Mangabey / 443 Fragaszy DM, Adams-Curtis LE. 1993. An exploration of manual preference and performance in crab eating macaques. In: Ward JP, Hopkins WD, editors. Primate laterality: current behavioral evidence of primate asymmetries. New York: Springer-Verlag. p 43–75. Gautier-Hion A, Colyn M, Gautier JP. 1999. Histoire naturelle des primates d’Afrique Centrale. Libreville, Gabon: ECOFAC. p 162. Hall KRD, Mayer B. 1966. Hand preferences and dexterities of captive patas monkeys. Folia Primatol 4:169–185. Harris LJ. 1989. Footedness in parrots: three centuries of research, theory and mere surmise. Can J Psychol 43:369–396. Harrison KE, Byrne RW. 2000. Hand preferences in unimanual and bimanual feeding by wild vervet monkeys (Cercopithecus aethiops). J Comp Psychol 114:13–21. Healey JM, Liederman J, Geschwind N. 1986. Handedness is not a unidimensional trait. Cortex 22:33–53. Hopkins WD. 1993. Posture and reaching in chimpanzees (Pan) and orangutans (Pongo). J Comp Psychol 107:162–168. Hopkins WD, Bard KA. 1993. Hemispheric specialization in infant chimpanzees (Pan troglodytes): evidence for a relation with gender and arousal? Dev Psychobiol 26: 219–235. Hopkins WD, Bennett AJ, Bales SL, Lee J, Ward JP. 1993. Behavioural laterality in captive bonoboos (Pan paniscus). J Comp Psychol 107:403–410. Hopkins WD, de Waal FBM. 1995. Behavioural laterality in captive bonobos (Pan paniscus): replication and extension. Int J Primatol 16: 261–276. King JE, Landau VI. 1993. Manual preference in varieties of reaching in squirrel monkeys. In: Ward JP, Hopkins WD, editors. Primate laterality: current behavioural evidence of primate asymmetries. New York: SpringerVerlag. p 107–124. Kubota K. 1990. Preferred hand use in Japanese macaque troop, Arashiyama-R, during visually guided reaching for food pellets. Primates 31:393–406. Larson CF, Dodson DL, Ward JP. 1989. Hand preferences and whole-body turning biases of lesser bush babies (Galago senegalensis). Brain Behav Evol 33:261–267. Lehman RWA. 1993. Manual preference in prosimians, monkeys, and apes. In: Ward JP, Hopkins WD, editors. Primate laterality: current behavioural evidence of primate asymmetries. New York: Springer-Verlag. p 127–134. MacNeilage PF, Studdert-Kennedy M, Lindblom B. 1987. Primate handedness reconsidered. Behav Brain Sci 10:247–303. Marchant LF, McGrew WC. 1991. Laterality of function in apes: a meta-analysis of methods. J Hum Evol 21:425–438. Masataka N. 1990. Handedness of capuchin monkeys. Folia Primatol 55:189–192. McGrew WC, Marchant LF. 1997. On the other hand: current issues in and metaanalysis of the behavioral laterality of hand function in nonhuman primates. Yearb Phys Anthropol 40:201–232. Miller CT, Paciulli LM. 2002. Patterns of lateralized hand use in an arboreal primate Simias concolor. Am J Primatol 56: 231–236. Morris RD, Hopkins WD, Bolser-Gilmore L. 1993. Assessment of hand preference in two language-trained chimpanzees (Pan troglodytes): a multimethod analysis. J Clin Exp Neuropsychol 15:487–502. Olson DA, Ellis JE, Nadler RD. 1990. Hand preferences in captive gorillas, orangutans and gibbons. Am J Primatol 20:83–94. Rawlins RG. 1986. Distribution of manual asymmetry among Cayo Santiago macaques (M. mulatto). Primates Rep 14:173–174. Robins A, Lippolis G, Bisazza A, Vallortigara G, Rogers LJ. 1998. Lateralized agonistic responses and hind-limb use in toads. Anim Behav 56:875–881. Roth ED. 2003. ‘Handedness’ in snakes? Lateralization of coiling behaviour in a cottonmouth, Agkistrodon piscivorus leucostoma, population. Anim Behav 66: 337–341. Sanford C, Guin C, Ward JP. 1984. Postural laterality in the bushbaby (Galago senegalensis). Brain Behav Evol 25:217–224. Spinozzi G, Castorina MG, Truppa V. 1998. Hand preference in unimanual and coordinated-bimanual tasks by tufted capuchin monkeys (Cebus paella). J Comp Psychol 112: 183–191. Spinozzi G, Truppa V. 1999. Hand preference in different tasks by tufted capuchins. Int J Primatol 20:827–849. Stafford DK, Milliken GW, Ward JP. 1990. Lateral bias in feeding and brachiation in Hylobates. Primates 31:407–414. Steklis HD, Marchant LF. 1987. Primate handedness: reaching and grasping for straws? Behav Brain Sci 10:284–286. Tomassello M. 1987. Why the left hand? Behav Brain Sci 10:286–287. Trouillard E, Blois-Heulin C. 2005. Manual laterality and task complexity in De Brazza’s monkey (Cercopithecus neglectus). Laterality 10:7–27. Vallortigara G, Bisazza A. 2002. How ancient is brain lateralization? In: Rogers LJ, Andrew JR, editors. Comparative vertebrate lateralization. Cambridge: Cambridge University Press. p 9–69. Am. J. Primatol. DOI 10.1002/ajp 444 / Blois-Heulin et al. Vauclair J, Fagot J. 1987. Spontaneous hand usage and handedness in a troop of baboons. Cortex 23:265–274. Warren JM. 1977. Handedness and cerebral dominance in monkeys. In: Hanard S, Doty RW, Jaynes J, Goldstein L, Krauthamer G, editors. Lateralization in the nervous system. New York: Academic Press. p 151–172. Watanabe K, Kaway M. 1993. Lateralized hand use in the precultural behaviour of the Koshima monkeys (Macaca fuscata). In: Ward JP, Hopkins WD, editors. Primate laterality: current behavioural evidence of Am. J. Primatol. DOI 10.1002/ajp primate asymmetries. New York: SpringerVerlag. p 183–192. Westergaard GC, Suomi SJ. 1996. Hand preference for a bimanual task in tufted capuchins (Cebus apella) and rhesus macaque (Macaca mulatta). J Comp Psychol 110:406–411. Westergaard GC, Kuhn HE, Lundquist AL, Suomi SJ. 1997. Posture and reaching in tufted capuchins (Cebus apella). Laterality 2:65–74. Westergaard GC, Kuhn HE, Suomi SJ. 1998. Bipedal posture and hand preference in humans and other primates. J Comp Psychol 112:55–64.