Clapping in chimpanzees evidence of exclusive hand preference in a spontaneous bimanual gesture.код для вставкиСкачать
American Journal of Primatology 68:1081–1088 (2006) RESEARCH ARTICLE Clapping in Chimpanzees: Evidence of Exclusive Hand Preference in a Spontaneous, Bimanual Gesture ALISON W. FLETCHER1,2 1 Department of Biological Sciences, University of Chester, Chester, United Kingdom 2 Department of Zoology, Miami University, Oxford, Ohio An increased understanding of spontaneous bimanual tasks performed by chimpanzees would enhance the ongoing debate on population handedness in this species, and thus shed light on the evolution of hemispheric lateralization in humans. However, documentation of such bimanual activities has been largely absent in the literature because such behavior is infrequently observed in the natural repertoire of this species. This study presents data on a simple, spontaneous bimanual gesture– ‘‘clap’’–that was investigated in a naturalistic group of 26 chimpanzees (Pan troglodytes). Sixteen individuals exhibited a total of 657 bouts of clapping directed toward humans, usually in the context of food availability. Most individuals were exclusive in their dominant hand preference, but since there was no population bias to the right or the left, the population is placed at level 3 of McGrew and Marchant’s [Yearbbook of Physical Anthropology 40:201–232, 1997] laterality framework. This is the first reported evidence of level 3 laterality in a non-tool-using task. Clapping increased in frequency with age, being common in adults, present at lower rates in adolescents, and absent in infants and juveniles. There was no effect of rearing or sex. The lack of population bias to the left or right for this bimanual gesture has implications for the debate on the evolution of language. Am. J. Primatol. 68:1081–1088, 2006. c 2006 Wiley-Liss, Inc. Key words: laterality; chimpanzee; bimanual; gesture; clap INTRODUCTION The study of lateral bias in primates seeks to improve our understanding of left-hemispheric specialization and the emergence of language in humans. While studies of several primate species in this context have been conducted, investigations into chimpanzee (Pan troglodytes) handedness are by far the most numerous [McGrew & Marchant, 1997], reflecting the similarity to humans in the Correspondence to: Dr. Alison Fletcher, Dept. of Biological Sciences, University of Chester, Parkgate Rd., Chester, CH1 4BJ UK. E-mail: email@example.com Received 16 August 2005; revised 12 January 2006; revision accepted 30 January 2006 DOI 10.1002/ajp.20308 Published online in Wiley InterScience (www.interscience.wiley.com). r 2006 Wiley-Liss, Inc. 1082 / Fletcher physiological attributes of that species, as well as our common ancestry. Humans are usually considered to be significantly right-handed at the population level [Raymond & Pontier, 2004]; however, such assessments are usually based on measures of tool use, and observations of spontaneous, everyday activities do not show such a strong bias [Marchant et al., 1995; Murray & Fletcher, 2005]. The degree of hand preference observed in chimpanzees likely reflects several different factors, as evidenced by its apparent variability in different reports. It has been shown in simple, unimanual, spontaneous behaviors (i.e., involving a single continuous movement, such as ‘‘pick up’’ (extend limb and grasp detached object, then flex limb, in one continuous motion) and ‘‘eat’’ (place object in mouth)) that some individuals show hand preferences while others do not, and that there is variation among populations, whether wild or captive [Fletcher & Weghorst, 2005; McGrew & Marchant, 1997]. Overall, a lack of population laterality for simple unimanual tasks has been observed. What does seem to be apparent, however, is that hand preferences for bimanual tasks and tool use (e.g., termite fishing, which requires fine motor skills) are more likely. In consideration of bimanual non-tool tasks, in which both hands are active in a coordinated manner, captive experimental studies have reported population right-handedness [Hopkins, 1994, 1995; Hopkins et al., 2003]. The infrequent observation of spontaneous bimanual hand use in naturalistic and wild populations has hindered comparisons. However, Corp and Byrne  noted that in wild chimpanzees, bimanual, multistage processing of Saba and Citrus fruits provides clear evidence, at the individual level, of one hand specializing in a particular role. Hand preferences in tool use (whether unimanual, such as wadge-dipping, or bimanual, such as termite fishing or nut-cracking) have been observed more frequently in the wild [e.g., Boesch, 1991; Marchant & McGrew, 1996; McGrew & Marchant, 2001; Sugiyama et al., 1993]. Individuals in both wild and captive populations seem to exhibit some exclusivity of hand preference in tool-using behaviors, although frequently there is no resulting population bias. It was recently suggested by Corp and Byrne  that bimanual and toolusing tasks have important similarities that place them apart from simple, unimanual activities. They suggest that even when lateralized tool-using behaviors are unimanual, they require spatial and temporal coordination skills, which are also necessary for bimanual tasks. This raises the question of what should occur if the behavior is bimanual but relatively simple. This paper reports on the observation of chimpanzees in a naturalistic environment performing a simple and spontaneous bimanual gesture, ‘‘clap.’’ This behavior was exhibited by chimpanzees (Pan troglodytes) in Chester Zoo, apparently to attract the attention of zookeepers or visitors from a distance, and usually in the context of potential food availability. While ‘‘hand-clap’’ has been investigated in captive chimpanzees as a gesture exhibited during play (clapping of hand or wrist [Tomasello et al., 1994], and ‘‘clap’’ has been described as a means of getting attention from a human experimenter holding food by captive chimpanzees [Hostetter et al., 2001], the laterality of clapping in apes has been reported only within a composite measure of communicative gestures (including ‘‘beg’’ and ‘‘point,’’ e.g., in bonobos [Hopkins & de Waal, 1995]). MATERIALS AND METHODS Data were collected in 1997 during a comprehensive study of spontaneous behavior [Fletcher & Weghorst, 2005]. The subjects were 26 chimpanzees that ranged in age from just over 1 year to 50 years (Table I). They were observed as a Am. J. Primatol. DOI 10.1002/ajp Clapping in Chimpanzees / 1083 TABLE I. Number of Bouts of Clap for All Study Individuals in Ascending Order by Age, Indicating Hand Preference, Significance Level and Rearing Status Age at start of study (years: Age Individual months) class Rearing status No. of bouts No. of bouts with left hand with right hand uppermost uppermost Females CH HO LZ ZE WH AL 1:3 1:7 2 3 4 5 I I I I J a MR MR MR MR MR MR LA KA WA SL SA KK FL MY FA HP RO 6 6 9 9 10 13 17 19 21 22 24 a a A A A A A A A A A MR MR MR MR MR MR MR HR MR MR HR HE KT CL ME 25 26 26 50 A A A A HR – HR 70 Wild born 48 Wild born – Males DY FR NI WI BO 10 21 28 29 31 A A A A A MR HR HR HR Wild born – – – – – – – – – – – 2 7 – – – 1 20 – – 24 95 13 5 31 – – 8 – 14 19 61 – 46 – 4 – – – 100 – – – 1 45 – 17 26 Significance level – – – – – (less than 6 bouts) P 5 0.016 Po0.001 Po0.001 Po0.001 Po0.001 Po0.001 – Po0.001 Po0.001 Po0.001 (less than 6 bouts) Po0.001 Po0.001 Po0.001 – Po0.001 Po0.001 – n.s. (P 5 0.108) Po0.001 A=Adult, a=adolescent, J=Juvenile, I=Infant, MR=Mother-reared, HR=Hand-reared. naturalistic group in a spacious enclosure, which consisted of a conical, threedimensional indoor viewing area measuring 4.3 m wide and 13 m high, and an outdoor enclosure of approximately 0.2 ha. Data were collected by two observers, following informal cross-checking and complete agreement, by focal subject sampling from a distance of 1–40 m. The behavior reported here (‘‘clap’’) is defined as follows: One hand is brought forcefully downwards, palm facing down, to strike other hand, palm facing upwards; upper hand is recorded as dominant (Plate 1). This definition has been used in similar ethological studies of wild chimpanzees [Marchant & McGrew, 1996; McGrew & Marchant, 2001]. Only the first instance of this behavioral pattern was recorded when it happened in series, to ensure independence of data points. An intervening bout of another behavior had to be performed before ‘‘clap’’ was recorded again. Binomial analyses were used to establish handedness. Statistical tests were all two-tailed with the Am. J. Primatol. DOI 10.1002/ajp 1084 / Fletcher Plate. 1. ‘‘Clap’’ with the right hand dominant in adult female chimpanzee Heidi (HE). significance level set at Po0.05. For an individual to be included in statistical analyses, his/her clap frequency had to be at least six bouts. RESULTS In total, 657 bouts of ‘‘clap’’ were recorded. This bimanual gesture was always performed with either the left or right hand in the dominant, uppermost position, and was performed in a sitting or bipedal position. All but one of 16 individuals that performed this gesture above the criterion of six bouts needed for statistical analysis displayed a significant hand preference, and 12 of 16 individuals were always consistent in their preference of uppermost hand (Table I). In those that were not consistent, the inconsistencies were minor, and recorded as follows: SL 1/62 bouts, DY 1/32 bouts, and MY 4/28. The pattern of dominant hand preference was spread fairly equally, with eight showing a right preference and seven showing a left preference. There was no effect of sex (Z 5 0.356, n 5 26, n.s.) or rearing status (Z 5 1.408, n 5 26, n.s.). The majority of adults performed ‘‘clap,’’ and this behavior increased with age (rs 5 0.400, n 5 26, P 5 0.043; rs 5 0.524, n 5 25, P 5 0.007 after removal of ME, who was 50 years old and stiff, with reduced mobility). There was no Am. J. Primatol. DOI 10.1002/ajp Clapping in Chimpanzees / 1085 2.50 Bouts per day 2.00 1.50 1.00 0.50 0.00 0.0 10.0 20.0 30.0 40.0 50.0 60.0 Age (years) Fig. 1. Relationship between the mean frequency of ‘‘clap’’ and the age of the individual. evidence of this behavior in infants or juveniles, and fewer bouts were performed by adolescents than by most adults (Fig. 1). DISCUSSION The pattern of observed hand use represents exclusive hand preference in a significant majority of the individuals that engaged in clapping. In McGrew and Marchant’s  framework of lateralization in nonhuman primates, this represents level 3. Briefly, this framework categorizes populations of individuals as follows: At level 1, essentially all individuals are ambidextrous; at level 2 there is a significantly specialized proportion of individuals but the population is unbiased as a whole; level 3 exists when the population distribution remains unbiased to the left or right despite a significant proportion of exclusivelyspecialized individuals; at level 4 the majority of lateralized individuals are biased to either the left or right; and at level 5 most individuals are exclusivelyspecialized to the left or right. Level 3 lateralization has not previously been reported for spontaneous unimanual tasks in primates, although it has been observed in several studies of spontaneous tool use [Boesch, 1991; Goodall, 1968; McGrew et al., 1999; Sugiyama et al., 1993]. Thus, the handedness observed in chimpanzee clapping would seem to lend further support to Corp and Byrne’s  suggestion that bimanual tasks necessitate a degree of skill similar to that needed for tool use. Clapping in chimpanzees is also of note in terms of its gestural function. Manual gestural communication in chimpanzees is of particular interest in the debate on the evolution of language in humans, and several models have been proposed to explain the origins of left-hemispheric specialization for human language [Bradshaw & Rogers, 1993; Corballis, 2002]. Some studies in apes have reported a population right-hand bias in gesture use [e.g., Hopkins & Carriba, 2002], particularly when the gestures are accompanied by vocalizations [Hopkins et al., 2005; Hopkins & Cantero, 2003], and claim support for Corballis’s  proposal that hemispheric lateralization in humans evolved from a pre-existing manual communication system in ancestors we share with chimpanzees. However, data are lacking for hand preference in bimanual gestures of chimpanzees, such as drumming on objects, probably because these tend to occur at a low frequency [e.g., Fletcher & Weghorst, 2005] (McGrew and Am. J. Primatol. DOI 10.1002/ajp 1086 / Fletcher Marchant, unpublished data). However, bimanual clapping was seen daily in the Chester population and was observed in the majority of adults, with no apparent sex or rearing differences. The lack of population right-hand bias for this spontaneous gesture contrasts with the aforementioned captive studies of complex bimanual tasks and unimanual gestures, and thus does not provide support for Corballis , but is consistent with an overall lack of populationlevel handedness in spontaneous, unimanual (non-tool) behaviors observed in this population [Fletcher & Weghorst, 2005]. The audible nature of ‘‘clap’’ enables an individual to gain the attention of an observer without first establishing visual contact, unlike pointing and food begs. The fact that other simple bimanual gestures previously recorded for apes are also auditory (e.g., ‘‘clap,’’ ‘‘chest-beat,’’ and ‘‘slap ground’’ in bonobos [Pika et al., 2005]) suggests that a detailed investigation of lateral bias in these gestures may be worthwhile to test proposed models of the emergence of left-hemispheric specialization in human language. It has been suggested [McGrew & Marchant, 1997] that when humans interact regularly with chimpanzees, the hand preference of the humans may influence that of the chimpanzees. Since the Chester chimpanzees are regularly in visual contact with humans, it is not implausible that hand preference in humans may have had a subtle influence on these chimpanzees, given the interspecific nature of the gesture. However, without investigating hand preference for clapping within the general human population, and the frequency with which chimpanzees observe clapping in humans, it is impossible to make an informed judgment. There was a clear effect of age for ‘‘clap,’’ with the younger individuals failing to exhibit the behavior at all, and adolescents clapping infrequently. In Tomasello et al.’s  study, individuals as young as 1 year old engaged in ‘‘hand-clap’’ (clapping of one’s own hand or wrist) with their conspecifics during play, which suggests that the basic motor pattern is possible in this age group. The regular performance of ‘‘clap’’ by older individuals, and its frequent association with food suggest that intraspecific social learning is likely to be involved in the development of this behavior in the Chester individuals. However, there may well have been a human element in its original emergence, since some of these individuals were hand-reared. Indeed, in a group of bonobos, ‘‘clap’’ was performed only by individuals that were raised by humans [Ingmanson, 1987]. However, the lack of rearing effect and the late development of this behavior suggest that there are other factors at work. In a study of intentional communication, Leavens and Hopkins  found that juveniles were less likely to engage in face-to-face interactions with adult male, communicative humans, even though those that did gesture did not differ from older individuals in the type of gestures performed. The facts that ‘‘clap’’ was not seen in the context of play in the current study, and that only older individuals were observed to perform this behavior may support the notion that the emergence of intentionality as a cognitive ability is the key element that is necessary for the performance of this gesture during interaction with humans, rather than the physical capability to perform the motor action. Hand preference during the immature period, as observed during tool use and complex bimanual tasks, appears to be changeable [e.g., Boesch, 1991; Colell et al., 1995; Fletcher & Weghorst, 2005; Hopkins, 1995], and consistent hand preferences are not evident until adolescence or adulthood. This is likely to be due to the involved nature of such tasks, which may take some time to master fully (e.g., bimanual processing of Saba fruits [Corp & Byrne, 2002]). Changes in hand preference in an individual may represent development of the method used (e.g., Am. J. Primatol. DOI 10.1002/ajp Clapping in Chimpanzees / 1087 learning to crack nuts [Boesch, 1991]). Of note in the current study, for the three immature individuals that did perform ‘‘clap,’’ there was some evidence of exclusive hand use from the start, albeit from a small number of bouts. Although only a longitudinal study can confirm consistency of hand use for ‘‘clap’’ through immaturity and into adulthood, Hopkins and Leavens  found in an experimental study of gestures that a greater number of older chimpanzees gestured (food-begs and pointing) with the right hand than younger ones; however, that conclusion was based on only one observation on each individual. If it is assumed that all adult cohorts tested in this way are likely to be similar in exhibiting an overall hand preference for gestures (and a right-hand bias has been noted in several such experimental studies of gesture use [e.g., Hopkins & Cantero, 2003; Hopkins & Carriba, 2002], particularly for food-begs [Hopkins & Wesley, 2002]), a lack of bias in the immature group suggests that some maturation of hand preference for gestures may occur during the immature period, as it does for bimanual tasks and tool use. The later emergence of ‘‘clap,’’ and the apparently fully matured lateral bias that was observed even within younger individuals suggest a different course of development for ‘‘clap’’ compared to other gestures and bimanual activities, which may be linked to both its physical simplicity and its communicative, attention-seeking nature. ACKNOWLEDGMENTS I thank Chester Zoo for permission to conduct this study, J.A. Weghorst for joint data collection, and W.C. McGrew for advice on issues pertaining to these observations. I also thank the anonymous reviewers for helpful comments on the manuscript. REFERENCES Boesch C. 1991. Handedness in wild chimpanzees. Int J Primatol 12:541–558. Bradshaw JL, Rogers L. 1993. The evolution of lateral asymmetries, language, tool-use and intellect. San Diego, CA: Academic Press. 463p. Colell M, Segarra MD, Pi JS. 1995. Hand preferences in chimpanzees (Pan troglodytes), bonobos (Pan paniscus), and orangutans (Pongo pygmaeus) in food-reaching and other daily activities. Int J Primatol 16: 413–434. Corballis MC. 2002. From hand to mouth: the origins of language. Princeton, NJ: Princeton University Press. 257p. Corp N, Byrne RW. 2002. The ontogeny of manual skill in wild chimpanzees: evidence from feeding on the fruit of Saba florida. Behaviour 139:137–168. Corp N, Byrne RW. 2004. Sex differences in chimpanzee handedness. Am J Phys Anthropol 123:62–68. Fletcher AW, Weghorst JA. 2005. Laterality of hand function in naturalistic chimpanzees. Laterality 10:219–242. Goodall JVL. 1968. The behaviour of free-ranging chimpanzees in the Gombe Stream Reserve. Anim Behav Monogr 1: 161–311. Hopkins WD. 1994. Hand preferences for bimanual feeding in 140 captive chimpanzees (Pan troglodytes): rearing and ontogenetic determinants. Dev Psychobiol 27: 395–407. Hopkins WD. 1995. Hand preferences for a co-ordinated bimanual task in 110 chimpanzees (Pan troglodytes): cross-sectional analysis. J Comp Psychol 109:291–297. Hopkins WD, de Waal FBM. 1995. Behavioral laterality in captive bonobos (Pan paniscus): replication and extension. Int J Primatol 16: 261–276. Hopkins WD, Leavens DA. 1998. Hand use and gestural communication in chimpanzees (Pan troglodytes). J Comp Psychol 112: 95–99. Hopkins WD, Carriba SF. 2002. Laterality of communicative behaviours in nonhuman primates: a critical analysis. In: Rogers LJ, Andrew RJ, editors. Comparative vertebrate lateralization. New York: Cambridge University Press. p 445–479. Hopkins WD, Wesley MJ. 2002. Gestural communication in chimpanzees (Pan troglodytes): the influence of experimenter position on gesture type and hand preference. Laterality 7:19–30. Am. J. Primatol. DOI 10.1002/ajp 1088 / Fletcher Hopkins WD, Cantero M. 2003. From hand to mouth in the evolution of language: the influence of vocal behavior on lateralized hand use in manual gestures by chimpanzees (Pan troglodytes). Dev Sci 6:55–61. Hopkins WD, Hook M, Braccini S, Schapiro SJ. 2003. Population-level right handedness for a coordinated bimanual task in chimpanzees: replication and extension in a second colony of apes. Int J Primatol 24: 677–689. Hopkins WD, Russell J, Freeman H, Buehler N, Reynolds E, Schapiro SJ. 2005. The distribution and development of handedness for manual gestures in captive chimpanzees (Pan troglodytes). Psychol Sci 16:487–493. Hostetter AB, Cantero M, Hopkins WD. 2001. Differential use of vocal and gestural communication by chimpanzees (Pan troglodytes) in response to the attentional status of a human (Homo sapiens). J Comp Psychol 115:337–343. Ingmanson EJ. 1987. Clapping behavior: nonverbal communication during grooming in a group of captive pygmy chimpanzees. Am J Primatol 72:214. Leavens DA, Hopkins WD. 1998. Intentional communication by chimpanzees: a crosssectional study of the use of referential gestures. Dev Psychol 34:813–822. Marchant LF, McGrew WC, Eibl-Eibesfeldt I. 1995. Is human handedness universal–ethological analyses from 3 traditional cultures. Ethology 101:239–258. Marchant LF, McGrew WC. 1996. Laterality of limb function in wild chimpanzees of Am. J. Primatol. DOI 10.1002/ajp Gombe National Park: comprehensive study of spontaneous activities. J Hum Evol 30: 427–443. 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. McGrew WC, Marchant LF, Wrangham RW, Klein H. 1999. Manual laterality in anvil use: wild chimpanzees cracking Strychnos fruits. Laterality 4:79–87. McGrew WC, Marchant LF. 2001. Ethological study of manual laterality in the chimpanzees of the Mahale Mountains, Tanzania. Behaviour 138:329–358. Murray AL, Fletcher AW. 2005. Hand use in humans and chimpanzees–no tools, no laterality? [Abstract]. Primate Eye 86: 26–27. Pika S, Liebal K, Tomasello M. 2005. Gestural communication in subadult bonobos (Pan paniscus): repertoire and use. Am J Primatol 65:39–61. Raymond M, Pontier D. 2004. Is there geographical variation in human handedness? Laterality 9:35–51. Sugiyama Y, Fushimi T, Sakura O, Matsuzawa T. 1993. Hand preference and tool use in wild chimpanzees. Primates 34: 151–159. Tomasello M, Call J, Nagell K, Olguin R, Carpenter M. 1994. The learning and use of gestural signals by young chimpanzees: a trans-generational study. Primates 35: 137–154.