Hand preference during unimanual and bimanual reaching actions in Sichuan snub-nosed monkeys (Rhinopithecus roxellana).код для вставкиСкачать
American Journal of Primatology 70:500–504 (2008) BRIEF REPORT Hand Preference During Unimanual and Bimanual Reaching Actions in Sichuan Snub-Nosed Monkeys (Rhinopithecus roxellana) DA-PENG ZHAO1, WEI-HONG JI2, KUNIO WATANABE3, AND BAO-GUO LI1 1 College of Life Sciences, Northwest University, Xi’an, China 2 The Ecology and Conservation Group, Institute of Natural Resources, Massey University, Albany, Auckland, New Zealand 3 Field Research Center, Primate Research Institute, Kyoto University, Inuyama, Aichi, Japan Hand preferences were investigated during one unimanual action (food-reaching) and one bimanual action (mount-reaching) in a semi-free-ranging group of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in Zhouzhi National Nature Reserve, Qinling Mountains of China. Nine of 14 individuals tested on the unimanual food-reaching action and all six individuals tested on the bimanual mountreaching action exhibited a manual preference. Both significant right- and left-handed preferences were observed in the two actions. Sex did not affect either direction or strength of hand preference in the unimanual action. Hand preference for the bimanual action was stable over time, and the strength of hand preference was significantly stronger in the bimanual action than in the unimanual action. Am. J. c 2007 Wiley-Liss, Inc. Primatol. 70:500–504, 2008. Key words: Sichuan snub-nosed monkey (Rhinopithecus roxellana); hand preference; unimanual food-reaching; bimanual mount-reaching INTRODUCTION Lateralized behavior has been studied as an observable measure of cerebral functional asymmetry for many years, and interest in the evolutionary origins of lateralized behavior in humans has prompted recent research into the study of manual laterality in nonhuman primates [Bradshaw & Rogers, 1993; Porac & Coren, 1981]. Preference for using one hand over the other has been studied in a wide variety of primate species [see review, Papademetriou et al., 2005]. The majority of studies on lateralized hand use in Old World monkeys has been conducted on cercopithecines [e.g. Blois-Heulin et al., 2006; Harrison & Byrne, 2000; Hauser et al., 1991; Tokuda, 1969; Warren et al., 1967; Watanabe & Kawai, 1993]; much less is known about handedness in colobines [e.g. Mittra et al., 1997; Neves & Dolhinow, 1995; Wells, 2002]. Furthermore, although captive settings offer a more controlled environment for assessing hand preferences [e.g. Blois-Heulin et al., 2006; Wells, 2002], studies of natural or semifree-ranging primate groups can provide further important insights into the evolution of handedness. This study of a colobine species, Rhinopithecus roxellana, has three main aims. First, we explore the laterality of manual function in unimanual foodreaching in a semi-free-ranging setting, consider the influence of sex on hand preference, and compare results with data on the same species in captivity. Second, we investigate laterality during bimanual r 2007 Wiley-Liss, Inc. mount-reaching, i.e. an action in which the male reaches with both hands from behind the solicited female toward her hindquarters. Third, the degree of hand preference shown in these two actions is compared and discussed. MATERIALS AND METHODS Study Site and Species The study site is located in Zhouzhi National Nature Reserve (ZNNR) on the northern slopes of the Qinling Mountains, China. The east ridge troop and the west ridge troop of this species are present in the study area [Zhao et al., 2008]. The west ridge troop includes one all-male group and our focal group, consisting of several one-male units. A 15 30 m provisioning site is established at Contract grant sponsor: Natural Science Foundation of China; Contract grant number: 30770375; 30570312; 30630016; Contract grant sponsor: Cosmo Oil Eco Card Fund of Japan; Contract grant number: 2005-2010; Contract grant sponsor: Graduate Innovation Fund of Northwest University; Contract grant numbers: 07YYB06. Correspondence to: Baoguo Li, College of Life Sciences, Northwest University, Xi’an 710069, China. E-mail: firstname.lastname@example.org Received 9 May 2007; revised 30 October 2007; revision accepted 31 October 2007 DOI 10.1002/ajp.20509 Published online 13 December 2007 in Wiley InterScience (www. interscience.wiley.com). Hand Preference During Reaching Actions in R. roxellana / 501 Sanchakou (1,646 m above sea level), Gongnigou valley (331480 6800 N, 1081160 1800 E), in ZNNR [Li & Zhao, 2007]. The focal group was herded toward the provisioning site where the research was conducted at approximately 9:00 every day. Apples, radishes, and corn were provided three times per day (10:00, 12:00, and 14:00). Approximately 200 g of feed were provided per monkey per day. The data were collected from a distance of between 0.5 and 50 m from the target animal. All the monkeys have been individually identified since 2001 based on their prominent physical characteristics [Zhao et al., 2005, 2007]. During our observation period, we obtained permission from ZNNR to conduct this research. Our research complied strictly with animal care regulations and applicable national laws in China. used binomial z-scores to determine whether the frequency of left- or right-hand use exceeded that expected by chance (50% right-hand use). A z-score greater than 11.96 indicated significant left-handedness, whereas a z-score less than 1.96 indicates a significant right-handedness. A z-score between 11.96 and 1.96 indicates no preference. With respect to group-level handedness, we performed Wilcoxon Signed ranks tests on the paired percentages to evaluate whether this group is ambipreferent or lateralized in hand use. Furthermore, sexual differences in manual laterality were tested with a Mann–Whitney U-test and the strength difference of hand preference (i.e. ABS-HI score) with the paired samples test. All statistical tests were two tailed and Po0.05 was chosen as the level of significance. Data Collection Data were collected from July 8, 2003, to January 17, 2004, with a video camera, by means of focal animal behavioral sampling [Altmann, 1974; Martin & Bateson, 1993]. Data on food-reaching and mount-reaching were collected from 14 individuals (nine adult males, five adult females) and six adult males, respectively. Of these focal subjects, five adult males were included in both food- and mountreaching observations. Hand preferences in the unimanual reaching action were assessed by observing which hand was used first when reaching for food (corn, or radish/apple pieces were scattered over a wide area) in a quadrupedal posture. If the focal animal sat in front of the food and repeatedly picked it up without moving position, only the first reaching action was recorded for hand preference. Hand preferences in the bimanual reaching action were assessed by observing which hand was extended first when reaching for mounting, the second step of copulation behavior as described in detail by Zhao  and Li and Zhao . Following the method described by Fletcher , the videotapes, totaling 5,786 min, were analyzed by two observers, using careful cross-checking and obtaining complete agreement, to confirm the hand preference of each individual performing each action. Data Analysis Hand preference for each focal individual in each action was analyzed using two methods described by Hopkins . First, to identify the degree of individual lateral bias, we calculated a handedness index (HI) for each animal by subtracting the number of left-handed responses (L) from the number of right-handed responses (R) and dividing by the total number of responses, i.e. HI 5 (RL)/(R1L). The HI varied between 1.0 and 1.0, indicating left and right hand bias, respectively. The absolute value (ABS-HI) reflects the strength of the individual-level hand preference. Second, we RESULTS Unimanual Food-reaching A total of 1,314 unimanual food-reaching events were recorded from 14 R. roxellana (nine adult males and five adult females) for hand preference analysis (mean 5 94, SE 5 32). On the basis of individual z-scores, seven individuals were classified as lefthanded (50%), two as right-handed (14%), and five as ambiguous-handed (36%) (Table I). There was no hand preference for unimanual food-reaching at group level in adult R.roxellana (z 5 1.852, P 5 0.064, not significant). The mean HI and ABS-HI scores in the unimanual reaching action were 0.22 (SD 5 0.35) and 0.33 (SD 5 0.24), respectively. No difference was found for unimanual food-reaching action between sexes, either in direction of hand preference (U 5 20; N1 5 9; N2 5 5; P 5 0.739; the mean HI score per subject was 0.26, SD 5 0.27 for males and 0.14, SD 5 0.48 for females), or in the strength of hand preference (U 5 18; N1 5 9; N2 5 5; P 5 0.549; the mean ABS-HI score per subject was 0.30, SE 5 0.22 for males and 0.38, SE 5 0.28 for females). Bimanual Mount Reaching We recorded a total of 497 bimanual mountreaching events from six male individuals for hand preference analysis in R. roxellana (mean 5 83, SE 5 13). The mean HI and ABS-HI scores for all focal animals in the bimanual reaching action were 0.28 (SD 5 0.65) and 0.64 (SD 5 0.11), respectively. All subjects exhibited significant individual-level hand preference during mount-reaching based on the z-scores. Four animals showed a left-hand preference and the remainder showed a right-hand preference at the individual level (Table I). No group-level preference for mount reaching was found in male R. roxellana (z 5 1.363, P 5 0.173, not significant). For testing whether individual Am. J. Primatol. 502 / Zhao et al. TABLE I. Lateralized Hand Use During Unimanual and Bimanual Reaching Actions in Rhinopithecus roxellana The unimanual reaching action No. Animal ID Animal gender 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 BZT CM DB HR JB JT JZT LP PK XN BT HTP XC YL YZM Male Male Male Male Male Male Male Male Male Male Female Female Female Female Female L R HI 343 132 0.44 31 32 0.02 49 39 0.11 55 35 0.22 53 28 0.31 29 4 0.76 27 16 0.26 85 113 0.14 — — — 33 13 0.43 62 22 0.48 6 22 0.57 20 4 0.67 15 16 0.03 17 13 0.13 The bimanual reaching action ABS-HI z-score Preference L 0.44 0.02 0.11 0.22 0.31 0.76 0.26 0.14 — 0.43 0.48 0.57 0.67 0.03 0.13 9.59 0.16 1.03 2.09 2.79 4.37 1.70 1.98 — 2.91 4.40 3.02 3.28 0.17 0.71 Left Ambi Ambi Left Left Left Ambi Right — Left Left Right Left Ambi Ambi 58 — 82 — 79 — 75 34 5 — — — — — — R HI 14 — 15 — 10 — 13 89 23 — — — — — — 0.61 — 0.69 — 0.78 — 0.70 0.47 0.64 — — — — — — ABS-HI z-score Preference 0.61 — 0.69 — 0.78 — 0.70 0.47 0.64 — — — — — — 5.18 — 6.80 — 7.36 — 6.57 5.21 3.39 — — — — — — Left — Left — Left — Left Right Right — — — — — — L, left-handed responses; R, right-handed responses; HI 5 (#R#L)/(#R1#L); ABS-HI, absolute value. preferences are consistent across time, we calculated the Pearson correlation coefficient between HI scores in the first and second halves of the observation period. There was a significant positive correlation (r 5 0.771, P 5 0.072), meaning that hand preferences in this bimanual reaching action were stable over time in this species. Among those five subjects tested on both the unimanual and bimanual actions, all displayed the same direction of hand preference according to the HI score. The HI scores for the unimanual action (mean 5 0.18, SE 5 0.20) were not significantly different from the HI scores for the bimanual action (mean 5 0.46, SE 5 0.52) (t(4) 5 1.754, P 5 0.154). Three exhibited the same hand preference based on the z-score; the other two moved from ambiguous (slightly, but not significantly, left-handed) in the unimanual action to significantly left-handed in the bimanual action based on the z-score. Manual preference strength (i.e. the ABS-HI score) of these five individuals was significantly greater in the bimanual action (mean ABS-HI 5 0.65, SD 5 0.12) than the unimanual action (mean ABS-HI 5 0.23, SD 5 0.11) (t(4) 5 7.464, P 5 0.002). DISCUSSION To our knowledge, this is the first study of hand preference in both unimanual and bimanual reaching actions in Sichuan snub-nosed monkeys. Our results suggest that hand preference during unimanual food-reaching and bimanual mountreaching in R. roxellana is specific to the individual rather than the group. Sex did not affect the direction or strength of hand preference in the unimanual action. These results agree with earlier studies of handedness in other colobines [e.g. Am. J. Primatol. Harrison & Byrne, 2000; Mittra et al., 1997; Neves & Dolhinow, 1995; Warren et al., 1967; Wells, 2002] and some great apes [e.g. Rogers & Kaplan, 1996]. Under the lateralization model of McGrew and Marchant  on the presence, strength, and direction of lateralized primate hand use, we classify R. roxellana into level 2. For the unimanual reaching action, our results differed from those of earlier captive studies which showed that male monkeys exhibit only right-hand preference at the individual level [Liang & Zhang, 1998; Ma et al., 1988]. The discrepancy in the results may be related to two differences in methodology between the studies. First, the settings are different: it has been shown that housing conditions and environmental stress may influence manual laterality in primates [e.g. MacNeilage et al., 1987]. Second, different statistical procedures may influence results. In our study, z-scores were used, whereas in others, P-values [Ma et al., 1988] and w2 values [Liang & Zhang, 1998] were used. A combination of differences in study environments and methods used to analyze hand preferences may partly account for the discrepant results between our study and some earlier ones. Studies on arboreal primates are crucial for understanding the role of posture and postural instability on handedness. This notion is central to the postural origin hypothesis proposed by MacNeilage et al.  and MacNeilage  that arboreal primates should preferentially use their left hand for manual actions like grasping food; such a postural effect is observable both in prosimians and in Old World monkeys [Papademetriou et al., 2005]. Although only half of the individuals in our study were significantly left-handed according to the z-score value, based on the HI, 71% of focal Hand Preference During Reaching Actions in R. roxellana / 503 R. roxellana showed a trend for left-hand preference during unimanual food-reaching action; this is in partial agreement with the postural origin hypothesis. Even though the bimanual reaching action did not reveal a group-level preference for one hand, all subjects tested displayed manual laterality at the individual level, and hand preferences were stable over time. Furthermore, we found stronger hand preferences for this action compared to unimanual reaching. This reflects the postural effect on hand preference during reaching actions in R. roxellana, also found in other primates [Bradshaw & Rogers, 1993; Frost, 1980; Westergaard et al., 1998]. In conclusion, although the size of our sample does not allow us to make strong generalizations concerning lateral preferences in Sichuan snubnosed monkeys, the R. roxellana studied appeared lateralized in unimanual and bimanual actions. Furthermore, hand preferences were stronger for a bimanual action than a unimanual action, supporting the view that posture could be a crucial factor influencing manual laterality in this species. 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