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Laterality of limb function in wild chimpanzees of Gombe National Park: comprehensive study of spontaneous activities
L. F. Marchant Department of Sociology, Gerontology and Anthropology, Miami University, Oxford, Ohio 45056, U.S.A.
W. C. McGrew Department of Sociology, Gerontology and Anthropology, and Department of Zoology, Miami Univesity, Oxford, Ohio 45056, U.S.A. Received 18 May 1994 Revision received 23 August 1995 and accepted 15 October 1995 Keywords: laterality, handedness, chimpanzee, Pan troglodytes, ethology, Gombe.
Laterality of limb function in wild chimpanzees of Gombe National Park: comprehensive study of spontaneous activities Resurgence of interest in laterality of hand function in nonhuman primates requires baseline knowledge of spontaneous hand-use in nature, in order to make sense of experimental studies in captivity. We present ethological data on 43 categories of limb movements exhibited by one community of wild chimpanzees (Pan troglodytes schweinfurthii) in the Gombe National Park, Tanzania. By focal-subject sampling, 42 individuals were observed at close-range over 4 months during their everyday activities. Laterality of hand function was largely absent, as both pooled results for the group and individual results rarely departed from 50:50 (ambilaterality). Neither age nor sex differences emerged. Nor did it matter if the subject was arboreal or terrestrial, or if the non-active hand was idle or engaged in postural support. Laterality was equally absent for unimanual and bimanual tasks. Lack of lateralization for limb movement in this natural population contrasts with findings of apparent right-handedness in captive chimpanzees. Unnatural postures and biased selection of measures in captive studies may account for these differences. ? 1996 Academic Press Limited Journal of Human Evolution (1996) 30, 427–443
Introduction Comparative (e.g. Ward & Hopkins, 1993) and evolutionary (Bradshaw & Rogers, 1993) studies of laterality of hand function in primates have mushroomed since interest in the topic was rekindled by MacNeilage et al. (1987). The hypothesized connections between brain lateralization, language, and handedness have led to further scrutiny of the hand preferences of nonhuman primates (e.g. Corballis, 1991). Evidence of hominid handedness in tool manufacture as a potential indicator of neural asymmetry has been sought in the archeological record (e.g. Toth, 1985; Schick & Toth, 1993). MacNeilage et al.’s (1987) postural origins theory hypothesized that nonhuman primates may show true handedness like human primates, that is, population-level laterality in hand use. This contrasted with the received wisdom of the time (e.g. Warren, 1980) that all nonhuman species (at least of mammals) were unlateralized, either being ambidextrous or at best, habitually lateralized in either direction as individuals. Of special interest is the extent of manual lateralization in the other hominoids, the lesser (Hylobatidae) and great (Pongidae) apes. For example, in their consideration of published results on gorillas (Gorilla gorilla), MacNeilage et al. (1991) concluded that these African apes showed a significant human-like pattern of preferring the right hand for all acts (cf. Byrne & Byrne, 1991; McGrew & Marchant, 1993). However, scrutiny of the available data on apes has led to differing conclusions: in a meta-analysis of methods, Marchant & McGrew (1991) opined that existing data-sets were inadequate, being based on too few, simplistic measures in too few, young subjects studied in captivity by artificial means. In a review of findings, Hopkins & Morris (1993) concluded that some functional motor asymmetries exist in great apes. Both articles decried the lack of data. The most crucial data are those from our nearest living relations, the chimpanzee (Pan troglodytes) and the bonobo (P. paniscus). With few exceptions (Marchant, 1983), earlier 0047–2484/96/050427+17 $18.00/0
? 1996 Academic Press Limited
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studies of these species were absent (P. paniscus) or suffered from the shortcomings detailed above (P. troglodytes). Recently, more useful data have become available both from captivity (e.g. Aruguete et al., 1992; Hopkins, 1993, 1996; Hopkins et al., 1993a,b) and from nature (Boesch, 1991; McGrew & Marchant, 1992; Sugiyama et al., 1993). (For a synthesis of laterality in hand-use by great apes, see McGrew & Marchant, 1996). These recent studies typically employed multiple tasks done by more than ten subjects, using precise measures and stricter statistical considerations. The field studies have focused on chimpanzees performing tool-use tasks, either nut-cracking or termite-fishing, and have found no convincing evidence of hand specialization, or handedness at the population level, but instead have found varying degrees of task specialization at the individual level (for explanation of terms, see McGrew & Marchant, 1994, and Discussion). The captive studies have found varying degrees of task specialization, especially when subjects assumed an (assisted) bipedal posture. Differences between the two sets of results could be general ones related to content (nature vs. captivity) or specific ones related to tasks (tool-use vs. non tool-use) or methods (spontaneous vs. induced performance). What is missing altogether is the simplest baseline data-set of all: a comprehensive, ethological study of spontaneous, everyday hand-use as practiced by chimpanzees in nature. What is needed are norms of what a community of apes does with their hands in all aspects of daily life in their environment of adaptedness. This was the aim of the study described below, except that tool-use as a special case is dealt with elsewhere (McGrew & Marchant, in prep.).
Methods The study was done in the Gombe National Park, a small (52 km2), well-protected park on the eastern shore of Lake Tanganyika, in western Tanzania (Goodall, 1986; Bygott, 1992). Subjects The main community (Kasakela) of eastern or long-haired chimpanzees (P. troglodytes schweinfurthii) was studied. It numbered 45 at the start of the study, though three members were never seen and were presumed dead. Table 1 gives information on age, sex, age-class, matrilineal kinship and number of days observed. Procedures Over 4 months (September–December 1992) the authors collected 238 h of observational data, using focal-subject sampling. Subjects were chosen opportunistically, with the goal of maintaining parallel running records on all 42 available subjects. Thus focal-sampling switched frequently, as one individual with fewer cumulative data arrived and ‘‘displaced’’ another with more data. After noting 100 instances of a behavioral pattern (see definitions below) by a subject, we took no more such data, but no subject reached this ceiling on all behavioral patterns. Data were collected by following subjects for up to 7 h, at a distance of no less than 3 m on the ground. All individuals were habituated to being watched, but some immigre adult females and their offspring were skittish. After informal reliability testing at the outset, we took on subjects as encountered, so that each observer collected data on all individuals. Observations were roughly even between mornings and afternoons, but were less frequent at dawn and dusk
Table 1
429
Subjects of study: chimpanzees of Kasakela community
Name Males (n=21) Evered Goblin Atlas Beethoven Freud Prof Wilkie Frodo Tubi Gimble Pax Apollo Kris Sheldon Mel [Dharsi] Galahad Faustino Jackson Fax Ferdinand Females (n=24) Gigi Fifi Sparrow Patti [Kidevu] Spray Candy Skosha Gremlin [Dominie] Jiffy Sandi Fanni Trezia California Tita Darbie Flossi Dilly Tanga Sherehe Conoco Schweini Shani
Code
Year of birth
Age class
Mother
Days of observation
EV GB AL BE FD PF WL FR TB GL PX AO KS SL ME DH GD FO JK FX FE
?1952 1964 1967 ?1969 1971 1971 1972 1976 1977 1977 1977 1979 1982 1983 1984 1985 1988 1989 1989 1992 1992
Adult Adult Adult Adult Adult Adult Adult Adult Adolescent Adolescent Adolescent Adolescent Juvenile Juvenile Juvenile Juvenile Infant Infant Infant Infant Infant
OL ML AT ? FF PS WK FF LB ML PS AT KD SW MF DO GM FF JF FN FF
14 10 17 10 13 16 17 17 13 15 13 17 16 9 13 — 15 15 12 16 —
GG FF SW PI KD SY CD SS GM DM JF SA FN TZ CF TT DB FS DL TG SR CO SI SN
?1954 ?1958 ?1960 ?1966 1966 ?1969 ?1969 1970 1970 1972 ? 1973 1981 ? 1983 1984 1984 1985 1986 1989 1991 1991 1991 ?1992
Adult Adult Adult Adult Adult Adult Adult Adult Adult Adult Adult Adult Adult Adult Adolescent Adolescent Juvenile Juvenile Juvenile Infant Infant Infant Infant Infant
? FL ? ? ? ? ? NV ML DO ? SW FF ? CD PI LB FF DM PI SA CD SW SY
14 19 6 7 — 5 6 2 18 — 16 — 23 14 6 11 5 18 14 4 — 4 — 4
?, Estimated or unknown; [ ], long missing, presumed dead; —, insufficient data.
. . . .
430 Table 2
Categories of limb movements recorded
Arm-wrestle Back-reach Beg *Bipedal Carry Chin rest Cradle Cross Drum Eat Embrace Fend Groom ‘‘Hat’’ Hold *Idle *Lead *Nipple Nose wipe Offer Overhead Pat Pick-up Pincer Pluck Poke Pound Pull Reach *Recline Roll Scratch Self-groom Shade Shake *Show sole Slap Snatch *Stamp Suck Threat Throw Touch
Engage arm, hand, finger in motor play with another chimpanzee. Extend arm backwards to another, from quadrupedal stance. Extend arm with palm up to another. Support full body weight on legs. Grip and transport an object, without further acting on it. Support own chin on crossed arm, with hand gripping opposite shoulder or upper arm. Support infant’s weight on cradler’s torso and flexed arm. Rest flexed arm on other flexed arm (record uppermost arm); rest flexed leg on other thigh or knee (record uppermost leg). Rapid, forceful blow of palm on inanimate object (record leading arm if series of blows). Place object in mouth. Flex arm with palm or contact around torso of another. Abduct partly flexed limb to another, making physical contact. Manipulate body surface of another while visually fixating same location. Rest palm on top of own head. Grip object or another without further acting on it, while holder is stationary. Other limb inactive (not including postural support). Leg first extended forward in locomotion, from terrestrial, quadrupedal stance. Suck nipple (record whether left or right nipple). Rub side of hand once across nostrils, horizontally and momentarily. Extend limb with object held in hand or foot to another. Extend arm upward, vertical and unsupported. Slow, gentle blow of palm on another; lower arm motion. Extend limb and grasp detached object, then flex limb, in one continuous motion. Adduct two fingers to extract embedded object. Extend limb and grasp attached object, then flex limb, in one continuous motion. Insert extended digit as probe, then withdraw digit. Strike rapidly and forcefully with palm-held object. Flex arm forcefully, with torso extension, to bring object or another nearer. Extend limb with palm down or lateral to another. Rest body-weight on side of trunk and arm (not elbow); terrestrial. Propel object forward with palm on ground, while locomoting. Rake rigidly and partly flexed digits over own body surface. Groom own midline organ, e.g. genitals. Cover own eyes with palm. Grip attached vegetation and jerk horizontally, usually repeatedly. Partly flex one leg (so shin is horizontal), in tripedal stance. Rapid, forceful blow of palm to another; whole limb motion. Rapid grasp and retrieve of moving airborne object. Rapid, forceful leg extension to strike sole against object or another; whole leg motion. Insert digit or object into mouth, with lips pursed around it. (Excludes Nipple.) Rapid abduction of extended arm to another. Propel object through air by forceful arm extension. Extend limb to make soft physical contact with another.
*Non-manual activity.
(as it seemed unlikely that laterality varied with the circadian cycle, even if relative frequency of behavior patterns did). Data Data were written into note books or dictated onto cassette tape recorders, then later transcribed onto standardized check-sheets. Table 2 gives the 43 categories of limb movements and other behavioral patterns recorded. The repertoire was devised from published literature and from pilot observations, and was meant to be comprehensive of arm movements that
Table 3
431
Features of behavior patterns recorded
Arboreal Both Dominant Left Non-arboreal Other Right Subordinate
Body-weight wholly supported by vegetation above ground or by object resting on ground, e.g., boulder, fallen log. Two limbs act simultaneously and similarly on same object or with same function, e.g., two-handed drumming. Of two limbs engaged simultaneously and complementarily in a coordinated act, limb that performs more precise and skilled action. Left limb acts alone. Body-weight wholly or parly supported by ground. Non-left or non-right limb gives postural support, stays idle, or performs an act directed to another object or with another function. Right limb acts alone. Non-dominant hand performs less precise and skilled action.
occur often enough to be studied (but termite-fishing, a skilled type of tool-use, was scored separately). Table 3 defines the features of limb movement that were recorded. We recorded ‘‘one-handed’’ (or footed) acts as ‘‘left’’ or ‘‘right’’, and simultaneously we noted if the opposite hand was idle, provided postural support, or was engaged in another independent act. Thus, a chimpanzee might ‘‘pluck a fruit with left’’, while ‘‘holding another fruit with right’’. More often, however, the opposite hand was engaged in providing postural support, through contact with either the substrate (usually terrestrial) or woody vegetation (usually arboreal). Arboreality was recorded independently. For two-handed (or footed) acts, we distinguished between coordinated acts in which both limbs were ‘‘yoked’’ in doing the same thing, and acts in which the two limbs functioned complementarily. When complementary, the more precise hand was labelled as ‘‘dominant’’ and the other hand as ‘‘subordinate’’. An example of the former is ‘‘both’’ hands pulling together to bend a sapling; of the latter is one (‘‘dominant’’) hand poking out the contents of a fruit while the other (‘‘subordinate’’) hand holds the same fruit. In principle, all behavioral patterns (unless otherwise noted) might be performed with upper or lower limbs. Given that acts often occur in series, it is crucial for statistical analysis to distinguish between independent events that occur soon after the other (for a fuller discussion, see McGrew & Marchant, 1992 and Martin & Bateson, 1993). We counted as a new bout, only the first performance of a behavioral pattern after there had occurred an interviewing bout of another behavioral pattern. Thus, if a chimpanzee ‘‘plucked’’ six fruit in a row, then paused to ‘‘scratch’’ herself three times, then ‘‘plucked’’ another four fruit, we only scored ‘‘pluck’’ twice and ‘‘scratch’’ once. Thus we sought to avoid inflation of sample-size and compromising of statistical independence. All statistical tests are two-tailed, and the significance level ( ) was set at 0·05. Results Table 4 gives comprehensive results of 9689 bouts of hand-use by the wild chimpanzees of Kasakela community. These are pooled across all 36 categories of manual activity and across 39 subjects, thus it is an overall measure of handedness. (The other seven, non-manual categories are excluded here, as are three subjects, SA, SI, SR, who yielded no data.) Table 4 presents the ten most common categories, ranked in descending order of frequency, and lumps the remaining 26 patterns as Miscellaneous. Four categories were clearly more common: ‘‘scratch’’ (as self-maintenance), ‘‘groom’’ (as social behavior), ‘‘eat’’ and ‘‘pluck’’ (as
. . . .
432 Table 4
Overall hand use in wild chimpanzees of Kasakela community, Gombe, Tanzania (pooled data, n=39 Ss) Behavior pattern
Total
1. Scratch 2. Groom 3. Eat 4. Pluck 5. Pull 6. Nose wipe 7. Pincer 8. Pick-up 9. Hold 10. Cradle Miscellaneous (n=26 patterns) Total
2220 1888 1712 1297 426 339 273 174 134 127 1099 9689
Left (%) 1077 594 662 634 154 168 128 91 59 53 499 4119
(49) (47) (49) (51) (54) (50) (54) (52) (55) (42) (49) (49)
Right (%) 1141 659 679 615 129 171 108 83 49 74 523 4231
(51) (53) (51) (49) (46) (50) (46) (48) (45) (58) (51) (51)
Bimanual 2 635 371 48 143 0 37 0 26 0 77 1339
subsistence). For each category, the total number of bouts is split into unimanual left, unimanual right, and bimanual tasks. The latter varies markedly across tasks: no chimpanzee ever wiped its nose or picked up an object with both hands, but 34% of grooming bouts involved simultaneous activity by two hands. Overall, 14% (1339 of 9689) of bouts involved bimanual performances that will not be further considered here, unless specifically noted. Figures in parentheses in Table 4 give the proportions for one-handed tasks, and none departs from symmetrical randomness (50%:50%). Overall, 51% of bouts were right-sided and 49% were left-sided. None of the individual patterns departs from 50:50 by more than a few, nonsignificant percentage points, and these are not consistently skewed to one side or the other. However, pooled figures for a group may obscure individual differences, either in proportion of data-points contributed or in degree of lateralization. One subject might contribute most of the data, or a group that averaged 50:50 might comprise two subgroups, one 100% right-handed and the other 100% left-handed. Table 5 gives individual preferences, or lack of them, for the ten most common patterns; thus, for Groom, 14 subjects used the left hand more frequently, 18 used the right hand more frequently, two used each hand equally frequently, and five did not groom. (The most consistent non-performers were babes-in-arms. One subject, FE, the youngest infant, was dropped from individual analyses on grounds of too few bouts. All 38 other subjects had at least 20.) The pooled frequency column gives only one-handed bouts, and as these numbers decline, from 2218 to 127, the number of non-performers (no data) rises from 0 to 26. For only one pattern, ‘‘cradle’’, is non-performance the norm; 75% of cradles were by only two subjects, FF and FN, who were mothers of the group’s two youngest infants. None of the left-vs.-right comparisons in Table 5 departs from 50:50, and neither side consistently predominates across patterns. The apparently most skewed, ‘‘pull’’, with twice as many left-preferents as right-preferents (22 vs. 11) does not depart significantly from chance: Binomial test, n=33, chi square=11, z=1·74, P=0·08, two-tailed (Siegel, 1956, pp. 36–42). Figure 1 presents individual data on hand specialization, that is, pooled observations within a subject but across all categories of hand-use. This all-encompassing measure showed all subjects converging on 50% right-handed or chance. The most left-sided individual, CD, was only 40% right-preferent (73 of 184 total bouts), whereas the most right-sided subject, GD, was
Table 5
433
Individuals’ hand preferences for most common behavioral patterns (n=38 Ss) Behavioral pattern 1. 2. 3. 4. 5. 6. 7. 8. 9. 10.
Scratch Groom Eat Pluck Pull Nose wipe Pincer Pick-up Hold Cradle
Pooled frequency
Left
Right
Equal
No data
2218 1253 1341 1249 283 339 236 174 108 127
13 14 21 15 22 10 13 13 11 3
23 18 13 19 11 17 7 8 13 7
2 2 4 2 2 5 3 4 1 2
0 5 0 2 3 6 15 13 13 26
only 61% right-preferent. Most subjects were within a few percentage points of 50:50, but nine of the 38 showed weak but statistically significant hand specialization. GD, FN, WL, FS, and FF were right-handers, CD, TG, PF, and SS were left-handers, and the other 29 individuals were ambidextrous. The nine lateralized individuals were consistently so across categories of behavior; no single task biased their overall totals. Figure 2 presents pooled data taken from Finch (1941) on hand specialization across four tasks: string-pulling with fruit attached; picking up fruit; displacing an obstacle to reach fruit; picking up an individual piece of fruit. The study was done at Orange Park, Florida, the great ape research center founded by R. M. Yerkes. All but five subjects were strongly lateralized, about equally to left or right. Of these five, only one, Lita, was ambidextrous. Finch presented his data in pooled form, so it cannot be tested to look for differences across the four tasks. Sex Table 6 summarizes the results when the data-set is divided into two subsets by sex. There were equal numbers of females and males, and the 38 individuals showed similar distributions over four age categories. On average, females were observed on fewer days, and they showed wider variation across subjects in number of days of data collection. Females also contributed fewer data-points per individual, and both sexes showed wide variation across subjects. The lower numbers and greater variation for females reflect their more solitary ranging, and greater skittishness as immigrants in contrast to philopatric males, but this is likely irrelevant to any lateralization of function. The mean percentages of right-handed events for the 19 females vs. the 19 males for each subject’s pooled hand-use did not differ, either between sexes or from chance. Standard errors and ranges showed the same equivalence. Thus, there is no sign of sex differences in overall laterality of hand-use. Age Table 7 provides a similar comparison of the results for age. Nineteen adults were compared with 19 immature subjects (i.e., adolescents plus juveniles plus infants). The two subsets of subjects were observed for similar numbers of days, but adults provided more data points than
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434 Subject (n = 38)
R/(R + L)
Cd Tg PF Ss TB Cf Sn Sw GB Sy Pi AO Gg JK FD KS Tz SL FR ME FO Co Db EV PX Gm DL AL GL Jf BE FX Tt Ff Fs WL Fn GD 0%
50%
73/184 53/131 125/296 145/330 105/234 53/118 9/20 51/111 196/423 122/258 107/226 128/268 136/284 29/60 121/249 52/107 55/113 24/49 102/207 132/267 66/133 18/36 13/26 277/542 57/111 142/273 143/273 154/293 208/390 92/171 101/187 40/74 144/262 188/336 172/300 199/337 302/509 95/157 100%
z 2.75 2.10 2.62 2.14
2.13 2.48 3.26 4.17 2.56
Figure 1. Percentage of right-handed responses for all manual activities pooled for each subject (n=38). The z-scores given are statistically significantly different from 50:50 at P<0·01, two-tailed. Double upper-case codes are males; upper and lower-case codes are females.
did immature individuals. This difference reflects the more peripheral nature of adolescents and juveniles, and the more limited behavioral repertoires of infants, but neither of these age-related factors is likely to be relevant to degree of lateralization. As for sex above, the mean percentages of right- vs. left-handed performance did not differ by age, and both approximated chance at 50:50. The two measures of variance were also similar. Thus, there is no sign of age differences in laterality of hand-use. Leading leg Table 8 shows left vs. right preference for the only category of lower-limb behavior to occur frequently enough for analysis: ‘‘lead’’. For the 30 subjects providing data on the leg leading
435
Subject (n = 30) Lia Mona Nira May Frank Dita Nana Suzy Soda Cuba Kambi Wendy Bokar Jack Gamma Lita Fifi Bimba Beta Pati Bula Dina Pan Mamo Helene Alpha Josie Mimi Fin Bentia 0%
50%
R
z
5 5 5 10 15 20 30 35 40 85 90 105 120 150 355 410 485 520 540 685 710 735 740 750 760 775 785 790 795 800
27.90 27.90 27.90 27.55 27.19 26.84 26.13 25.78 25.42 22.24 21.98 20.83 19.77 17.64 3.15 5.98 8.45 9.87 20.12 21.89 23.66 24.01 24.72 25.42 26.49 27.19 27.55 27.90 28.25
100%
Figure 2. Percentage of right-handed responses for four manual tasks pooled for each subject at Orange Park (n=30), adapted from Finch [(1941) Science 94, 117–118]. Frequencies are estimated to nearest five responses by measuring Finch’s histogram bars. The z-scores given are statistically significantly different from 50:50 at P<0·01, two-tailed. R+L=800.
off bouts of quadrupedal locomotion, the pooled data showed no departure from 50:50, with 53% of bouts leading with the left leg, and 47% with the right. The lack of laterality was reflected in the totals for individual predominance, with 12 subjects being predominantly left-leaders and 14 right-leaders. The overall picture for laterality of limb function is one of little or no bias from the symmetrical distribution of equivalence of left and right. Idle hands Most of the time in wild chimpanzees, both hands are simultaneously active. On average, in only 10% of bouts of overall manual activity was one hand idle, across the 39 subjects. Furthermore, 58% (435 of 748) of the cases of an idle hand occurred during the performance of only one behavioral pattern, ‘‘groom’’. For other categories of behavior,
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436 Table 6
Sex differences in handedness
No. of subjects Adults Adolescents Juveniles Infants Days of observation Mean Standard error Range No. of data-points Mean Standard error Range % Right-handed events Mean Standard error Range
Table 7
Males
19 11 2 3 3
19 8 4 3 4
10·3 6·4 2–23
14·1 2·5 9–17
208·5 125·3 20–509
230·7 132·4 49–542
49·3 5·4 40–59
50·5 4·5 42–61
Age differences in handedness
No. of subjects Days of observation: Mean Standard error Range No. of data-points: Mean Standard error Range % Right-handed events: Mean Standard error Range
Table 8
Females
Adults
Immatures
19
19
12·8 5·6 2–23
11·6 4·8 4–18
280·5 117·1 111–542
158·7 109·4 20–390
49·7 5·3 40–59
50·1 4·8 40–61
Lateralization of leading leg in initiating quadrupedal locomotion (n=30 Ss)
Overall pooled Individuals
Left (%)
Right (%)
Equal
No data
Total (%)
362 (53) 12
317 (47) 14
— 4
— 8
679 (100) 38
Table 9
Overall laterality of Groom when other hand is idle vs. active (pooled data, n=34 Ss) Left (%) Idle Support Other activity Total
Table 10
437
202 381 11 583
Right (%)
(46) (48) (44) (47)
233 412 14 645
Total (%)
(54) (52) (56) (53)
435 793 25 1253
(100) (100) (100) (100)
Individual’s grooming as more or less lateralized when other hand is idle rather than when providing positional support
Idle
Less
More
Same
Total
13
17
4
34
bouts with an idle hand were rare: ‘‘eat’’, 6%; ‘‘pluck’’, 2%; ‘‘pull’’, 0·5%, etc. Thus, detailed, further analysis of the other hand being idle while the active hand showed laterality are limited to grooming. Table 9 shows the overall proportions of bouts of grooming in which the non-grooming hand was idle, provided postural support, or was engaged in another activity, usually holding an object. Neither in the overall totals, nor in any of the three subsets is there a departure from 50:50 randomness. (In the other 635 bouts of grooming, both hands were involved, i.e., it was a bimanual task.) Table 10 compares the grooming of individual subjects for two kinds of bouts: when the other hand was idle vs. when it provided postural support. Two expectations seem plausible: one is that an occupied other hand will enhance laterality effects, as priorities such as positional security, comfort, or retaining possession of objects may bias what the active hand does. The other expectation is that when one hand is idle, the other activity will be more lateralized, as the chimpanzee has more freedom of choice of hand to use than when the environment was more constraining. The results showed no difference: of the 34 subjects who groomed, 13 were less lateralized and 17 were more lateralized when the other hand was idle. Arboreality Behavioral patterns varied in the extent to which they were performed in the trees or on the ground. (See Table 11.) Some were mostly terrestrial: ‘‘scratch’’ while resting or interspersed with grooming or locomotion; ‘‘groom’’ while lounging in parties. Others were mostly arboreal: ‘‘eat’’ and ‘‘pluck’’ in feeding; ‘‘pull’’ in foraging or nest-building. Whatever the behavioral pattern, it is hypothesized that arboreal chimpanzees should be more lateralized than terrestrial ones, as their positional behavior is more constrained by a three-dimensionally structured environment. That is, apes up in the canopy typically must use one hand in support to keep from falling, while on the ground, both hands typically are free. [This assumes that above the ground a ripe fruit is on average just as likely to be hanging to the right as to the left, or that the next branch needed for support projects from the left side as often as from the right
. . . .
438 Table 11
Overall laterality of most common behavior patterns when arboreal vs. non-arboreal, pooled data Arboreal
Behavioral pattern
Left (%)
Scratch Groom Eat Pluck Pull
374 111 521 517 122
Table 12
Behavioral pattern Groom Eat
(48) (49) (50) (50) (53)
Non-arboreal
Right (%) 404 116 521 512 107
Left (%)
(52) (51) (50) (50) (47)
696 483 144 117 32
(48) (47) (47) (53) (59)
Right (%) 744 543 160 103 22
(52) (53) (53) (47) (41)
Total
Arboreal
2218 1253 1346 1249 283
23% 17% 73% 82% 70%
Overall laterality of bimanual activities of sufficient frequency, when subordinate hand is simultaneously active vs. idle; pooled data Active
Idle
Total
Both
Left (%)
Right (%)
Left (%)
Right (%)
644 515
529 215
58 (50) 147 (49)
57 (50) 153 (51)
202 (46) 52 (49)
233 (54) 57 (52)
side of the tree’s trunk. Similarly, on the ground, objects are likely to be arranged evenly in all directions, although the essentially flat substrate allows more freedom of action, especially from whence they can be approached (cf. Boesch, 1991, for reaching).] Table 11 shows the overall laterality for the five most common behavioral patterns, when performed arboreally or non-arboreally. (The table includes only the top five, as the total numbers of bouts when broken down four ways are low.) There is no difference between left and right predominance in either condition for any behavioral pattern. Notably, extent of lateralization is not more when the behavior is done arboreally; none of the comparisons differs significantly from 50:50. Bimanual Table 4 shows that only two categories, ‘‘groom’’ and ‘‘eat’’, occurred often enough for further analysis of the simultaneous use of two hands. We combine ‘‘subordinate’’ and ‘‘other’’ (but excluding idle and postural support) to provide data on what the non-dominant hand actively does at the same time as the dominant hand. (See Table 12.) For ‘‘groom’’, most bimanual activity (82%, 529 of 644 bouts) entails both hands being similarly engaged in manipulating another’s body surface, focused on the same point. Less commonly, especially when a mother grooms her infant, she grooms with the dominant hand and holds another part, typically a limb, with the subordinate hand. For ‘‘eat’’, the most common case (58%, 300 of 515) is for the diner to eat from an object in the dominant hand while holding another food-item in the subordinate hand (cf. Hopkins et al., 1993b). We hypothesized that these bimanual combinations of hand-use would be more lateralized than cases in which only one hand was used in grooming or eating while the other hand was idle. This was expected on the grounds that two-handed activities are more constrained by task requirements than are one-handed activities. Table 12 shows no difference in bimanual activity between these conditions for either category of behavior; neither departs from 50:50.
439
Summary Wild chimpanzees are notably unlateralized in their limb movements, whether at the level of individual preference or population-level handedness, or task or hand specialization. This symmetry holds for both one- and two-handed tasks, across potentially biasing conditions. Put another way, the only indications of asymmetry are that a few (nine of 38) individuals showed weak but statistically significant hand specialization (see Figure 1). Discussion The results of this study suggest that at least one population of wild chimpanzees is comprehensively unlateralized in hand-use, at least in tasks other than tool-use. (At Gombe, only one type of tool-use, termite-fishing, is common, and it is highly seasonal, being confined largely to the months of October–December, Goodall, 1968.) These apes show no handedness (i.e., laterality across tasks and across individuals, at population level), no task specialization (i.e., laterality within a task but across individuals), and only a few may show mild hand specialization (i.e., laterality across tasks but within an individual). Theirs is essentially a 50/50 world of manual activity. These results run counter to the recent conclusions of MacNeilage et al. (1987, 1988, 1991) and to recent syntheses from published data (Hopkins, 1996; Hopkins & Morris, 1993), who found functional asymmetry in apes. More precisely, it differs from recent empirical findings in captivity: Aruguete et al. (1992) found for 27 chimpanzees, statistically significant right-sided touching of the inanimate environment, but no laterality at group level for touching their own faces or bodies. Hopkins (1993) found, for 40 chimpanzees, a statistically significant right-sided bias for the group in reaching to pick up an object while standing bipedally. Hopkins et al. (1993a) found, for 36 chimpanzees, that throwing was lateralized to the right for the group, while for 12 mothers with infants, the former’s cradling was not lateralized. For 11 bonobos, Hopkins et al. (1993b) found statistically significant biases for carrying an object (left-sided), for leading limb in locomotion (right-sided), and for feeding (right-sided) while holding another food item with the left hand. All of these biases were consistent across the group, but another four patterns (face-touching, self-touching, gesture, reaching) did not differ in laterality. Thus, at least some task specialization seems to be the norm for captive chimpanzees. In contrast, studies in nature of wild chimpanzees doing non-tool-use activities show a lack of lateralization. At Tai, Boesch (1991) found that chimpanzees were unlateralized as a group for reaching to pick up fruit (n=20 Ss) and for grooming (n=15 Ss). At Bossou, Sugiyama et al. (1993) found no lateralization at group level for 19 chimpanzees in bouts of picking fruit from a branch and moving it to the mouth (feeding). Thus, our findings of lack of laterality resemble those of other field studies using more selected measures, and contrast with those from captive settings in laboratories or zoological parks. In the naturalistic setting of an island in a safari park with a free-ranging group of 27 chimpanzees, the results for hand-use resembled these from the wild. For none of seven behavioral categories (social reach, non-social reach, feed, carry, throw, hold, groom) did the pooled results depart from 50:50, thus there was an overall lack of laterality. For two categories, non-social reach and feed, most of the individuals showed significant lateralization to one side or the other, but there was no population-level task specialization to one side, much less handedness across all or even most activities. (See Marchant, 1983, Tables 2 and 3, for details.) What independent variables might explain these apparently conflicting results?
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A potential major difference between captivity and nature is in arboreality–terrestriality, although this variable rarely is addressed specifically. Most if not all captive data seem to come from subjects on the floor or ground, whereas at least some data in all field studies comes from individuals above the ground. This is likely to mean differences in posture or positional behaviour in the two conditions of verticality, as when they are arboreal, apes typically use one or more hands or feet to support or secure themselves, whereas when they are terrestrial, this is unnecessary. Time spent arboreal is notable: fully habituated chimpanzees at Gombe and Mahale spend on average 53% and 39% of their waking hours above ground (Hunt, 1992). Doran (1993b) produced similar figures for arboreal postural activity of 37% for males and 58% for females among chimpanzees at Tai. (No comparable data are yet available for incompletely habituated bonobos at Lomako, but it seems likely that P. paniscus is equally as arboreal as P. troglodytes.) Our data-set from Gombe is the only one to focus on this dimension, and it yields no apparent differences across conditions in major manual activities, but until captive studies take note of the variable, preferably by housing and testing subjects in settings with rich vertical opportunities, and until field studies specify this variable during observation, its importance remains obscure. A methodological difference between captive and field studies in print is that the former have paid more attention to the status of the ‘‘other’’ hand. Aruguete et al. (1992) recorded laterality data only when both hands were free and available to make the response, and thus excluded all cases when the other hand provided postural support, held an object, etc. This provided ‘‘unbiased’’ data but restricted data collection to an abnormal subset of activities, at least by natural standards. (For example, Table 9 shows that the other hand was idle in only 35%, 435 of 1253, bouts of one-handed grooming, which is the most extreme case.) Hopkins et al. (1993b) divided the other hand’s activity into eight categories that were noted while the favored hand was feeding, and these alternatives made a significant difference. When the other, left hand held food, the bonobos were lateralized as right-sided feeders, but no such laterality occurred if the other hand was inactive, providing support, etc. Previous field studies did not specifically record such data, though Sugiyama et al. (1993) stated that while picking food, a chimpanzee at Bossou usually employed the other hand in support. Similarly, Boesch (1991) noted that Tai chimpanzees reached to pick up fruit while sitting (with both hands free), while in grooming the other hand sometimes held a branch or rested on the ground, and so this task had some external constraints. Only detailed and comparable data from a variety of settings will clarify the issue, but it seems likely that apes in laboratory cages or zoo enclosures will spend more time with idle hands, and this may influence the extent of lateralization shown in their manual activities. Most studies of laterality in hand use have focused on one-handed tasks (e.g. Aruguete et al., 1992; Hopkins et al., 1993a; Sugiyama et al., 1993) or have recorded but not presented data on the relative contributions of the hands to two-handed tasks (e.g. Hopkins et al., 1993b; McGrew & Marchant, 1992). This emphasis on selective, unimanual measures applies equally to published findings from field and laboratory (including tool-use). We presented data, though for only two behavioral patterns, ‘‘groom’’ and ‘‘eat’’, suggesting that whether the other hand is idle or engaged in coordinated but subordinate activity makes little difference to the degree of laterality of the active or dominant hand. We suggest that a more ethological approach, incorporating more and complex categories such as food processing, in both captivity and nature, would clarify these issues (cf. Byrne & Byrne, 1991, 1993). Following MacNeilage et al.’s (1987) lead, recent studies of laterality in limb-use by captive apes have emphasized posture as an independent variable (e.g. Hopkins, 1993) while field
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studies have not. While MacNeilage (1993, p. 330) continues to espouse a ‘‘postural origins’’ theory that accounts for right-handedness in higher primates, based on freed limbs while sitting, empirical tests of posture as an influence have focused on upright bipedal postures while standing (Hopkins et al., 1993a,b). Two kinds of upright bipedal stance are noted: one in which both hands are freed of providing support, and another in which one hand provides postural support while the other is free (Hopkins, 1993). The latter is really a form of tripedalism, and is sometimes called ‘‘aided bipedalism’’ (Doran, 1993b). Both versions of bipedalism occur naturally in Pan spp., but they are rare. At Gombe and Mahale, chimpanzees spend an average of 0·25% of their time in bipedal standing and 0·1% in bipedal walking (Hunt, 1992). For bonobos, the most frequent form of bipedalism, during feeding by males, occupies only 2·8% of the time, and it is arboreal, not terrestrial (Doran, 1993a). No published field study of apes has focused on posture as an independent variable, and no such study in captivity has singled out sitting as a postural category, nor distinguished between free-standing and aided bipedalism. (Diamond & McGrew, 1994, studied laterality in cotton-top tamarins, Saguinus oedipus, in captivity, and found population-level right-handedness for six of seven categories of manual activity. The effect was more strongly right-sided when subjects were in postures that had both forelimbs free than when they were in aided bipedal postures.) The best candidate explanation for differences in laterality of hand-use between natural and captive settings appears to be postural. Individuals of Pan spp. that are tested in atypical, human-like bipedal postures display indications of human-like handedness, unlike their wild counterparts who eschew such postures. It is tempting to infer that this contrived ‘‘hominization’’ somehow mimics the selection pressures that produced hominid bipedalism from a hominoid ancestral form (Hunt, 1994). An obvious analogy is how exposure to artificial language systems via human tutelage may have enhanced the cognitive functioning of captive apes toward more human levels (Tomasello et al., 1993). It may be that settings conducive to bipedalism may somehow lateralize the ‘‘freed hands’’ of captive apes. This is empirically testable, but additional ethological studies also need to be done of both captive and wild apes performing their full repertoire of manual behavior in the full range of postures. At the more micro-level, differences between nature and captivity may stem from the measures or tasks chosen. Most previous studies recorded few tasks of apparent high reliability but of suspect validity. This raises questions of artifactual results in contrived unnatural settings. For example, although it is the commonest dependent variable in experimental studies of primate laterality, picking up a detached object off a horizontal surface is actually an uncommon activity in wild chimpanzees (see Table 4). The objects that chimpanzees in nature handle are usually food-items, and these are usually plucked or picked. Another commonly recorded category, self-touching (of the face, body, etc.) is so vague as to be of doubtful utility, as it lumps together self-grooming (maintenance), scratching (displacement), masturbation (sexual), chin-resting (comfort), nose-wiping (nervous habit), etc. It is a sobering discovery that of the ten most common hand uses shown by Gombe’s chimpanzees, only five have ever been recorded in major captive studies: groom (Marchant, 1983); eat (=feed, Marchant, 1983; Hopkins et al., 1993b); pick up (=reach, Marchant, 1983; Hopkins et al., 1993a,b); hold (Marchant, 1983); and cradle (Hopkins, 1993). If apes are naturally ambidextrous, and only artificially lateralized (again, setting tool-use aside), what does this say about the basic problem of why laterality of function at population or species level should ever evolve? It is clear that in everyday life, wild chimpanzees benefit from moment to moment by being ambilateral: if a fruit is suspended in space to their left side, it is convenient to pluck it with the left hand; if one’s right ankle itches, it is convenient to
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scratch it with the right hand; if the trail immediately ahead is clear and flat to the left, it is convenient to take the first step to the left; if the next highest branch on the tree projects to the right, it is convenient to ascend by grasping it with the right hand; etc. Even if there are tasks of skill or strength that are done more efficiently by habitual use of one hand, unless these are lateralized in the environment, why need the lateralization be any more than individual preference to right or left. Viewed in this way, handedness or task specialization to one side at population level seems to be a self-imposed limitation. Rather than ask whether or not other species are lateralized like ourselves, perhaps we should be asking why any species should disadvantage itself with the curse of laterality? Finding and clarifying the benefits that offset the costs of being lateralized are the most basic challenges of laterality research. Acknowledgements We are grateful to the Tanzania Commission for Science and Technology (UTAFITI), Serengeti Wildlife Research Institute, and Tanzania National Parks for granting permission to do the research; L. S. B. Leakey Foundation and Miami University for funding; J. Goodall and the staff of the Gombe Research Centre and S. Qolly and P. Msuya and the staff of the Gombe National Park for facilities and assistance; A. Collins, J. R. Dharsi, C. Packer, C. Stanford, C. Uhlenbroek, K. & J. Vaitha, W. Wallauer, and J. Wallis for companionship and manifold acts of kindness; R. Byrne, M. Holder, W. Hopkins, J. King, and three anonymous reviewers for critical comments on the manuscript. The work is dedicated to the memory of two venerable wazee: Evered and Gigi. References Aruguete, M. S., Ely, E. A. & King, J. E. (1992). Laterality in spontaneous motor activity of chimpanzees and squirrel monkeys. Am. J. Primatol. 27, 177–188. Boesch, C. (1991). Handedness in wild chimpanzees. Int. J. Primatol. 12, 541–558. Bradshaw, J. & Rogers, L. (1993). The Evolution of Lateral Asymmetries, Language, Tool Use, and Intellect. San Diego: Academic Press. Bygott, D. (1992). Gombe Stream National Park. Arusha: Tanzania National Parks. Byrne, R. W. & Byrne, J. M. (1991). Hand preferences in the skilled gathering tasks of mountain gorillas (Gorilla g. beringei). Cortex 27, 521–546. Byrne, R. W. & Byrne, J. M. (1993). Complex leaf-gathering skills of mountain gorillas (Gorilla g. beringei): variability and standardization. Am. J. Primatol. 31, 241–261. Corballis, M. C. (1991). The Lopsided Ape. New York: Oxford University Press. Diamond, A. C. & McGrew, W. C. (1994). True handedness in the cotton-top tamarin (Saguinus oedipus)? Primates 35, 69–77. Doran, D. M. (1993a). Comparative locomotor behavior of chimpanzees and bonobos: the influence of morphology on locomotion. Am. J. Phys. Anthropol. 91, 83–98. Doran, D. M. (1993b). Sex differences in adult chimpanzee positional behavior: the influence of body size on locomotion and posture. Am. J. Phys. Anthropol. 91, 99–115. Finch, G. (1941). Chimpanzee handedness. Science 94, 117–118. Goodall, J. v. L. (1968). The behaviour of free-ranging chimpanzees in the Gombe Stream Reserve. Animal Behav. Monographs 1, 161–311. Goodall, J. (1986). The Chimpanzees of Gombe. Cambridge: Harvard University Press. Hopkins, W. D. (1993). Posture and reaching in chimpanzees (Pan troglodytes) and orangutans (Pongo pygmaeus). J. Comparative Psychol. 107, 162–168. Hopkins, W. D. (1996). Chimpanzee handedness revisited: 55 years since Finch (1941). Psychonomic Bull. Rev. (in press). Hopkins, W. D., Bard, K. A., Jones, A. & Bales, S. L. (1993a). Chimpanzee hand preference in throwing and infant cradling: implications for the origin of human handedness. Curr. Anthropol. 34, 786–790. Hopkins, W. D., Bennett, A. J., Bales, S. L., Lee, J. & Ward, J. (1993b). Behavioral laterality in captive bonobos (Pan paniscus). J. Comparative Psychol. 107, 403–410. Hopkins, W. D. & Morris, R. D. (1993). Handedness in great apes: a review of findings. Int. J. Primatol. 14, 1–25.
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Hunt, K. D. (1992). Positional behavior of Pan troglodytes in the Mahale Mountains and Gombe Stream National Parks, Tanzania. Am. J. Phys. Anthropol. 87, 83–105. Hunt, K. D. (1994). The evolution of human bipedality: ecology and functional morphology. J. hum. Evol. 26, 183–202. MacNeilage, P. F. (1993). Implications of primate functional asymmetries for the evaluation of cerebral hemispheric specialization. In (J. P. Ward & W. D. Hopkins, Eds) Primate Laterality. Current Behavioral Evidence of Primate Asymmetries, pp. 319–341. New York: Springer. MacNeilage, P. F., Studdert-Kennedy, M. G. & Lindblom, B. (1987). Primate handedness reconsidered. Behav. Brain Sci. 10, 247–303. MacNeilage, P. F., Studdert-Kennedy, M. G. & Lindblom, B. (1988). Primate handedness: a foot in the door. Behav. Brain Sci. 11, 720–746. MacNeilage, P. F., Studdert-Kennedy, M. G. & Lindblom, B. (1991). Primate handedness: the other theory, the other hand and the other attitude. Behav. Brain Sci. 14, 338–349. Marchant, L. F. (1983). Hand Preference Among Captive Island Groups of Chimpanzees (Pan troglodytes). 106 pp. Ann Arbor: University Microfilms International. Marchant, L. F. & McGrew, W. C. (1991). Laterality of function in apes: a meta-analysis of methods. J. hum. Evol. 21, 425–438. Martin, P. & Bateson, P. (1993). Measuring Behaviour. 2nd edn. Cambridge: Cambridge University Press. McGrew, W. C. & Marchant, L. F. (1992). Chimpanzees, tools, and termites: hand preference or handedness? Curr. Anthropol. 33, 114–119. McGrew, W. C. & Marchant, L. F. (1993). Are gorillas right-handed or not? Hum. Evol. 8, 17–23. McGrew, W. C. & Marchant, L. F. (1994). Primate ethology: a perspective on human and nonhuman handedness. In (P. K. Bock, Ed.) Handbook of Psychological Anthropology, pp. 171–184. Westport, CT: Greenwood Press. McGrew, W. C. & Marchant, L. F. (1996). On which side of the apes? Ethological study of laterality of hand use. In (W. C. McGrew, L. F. Marchant & T. Nishida, Eds) Great Ape Societies, pp. 255–272. Cambridge: Cambridge University Press. Schick, K. & Toth, N. (1993). Making Silent Stones Speak. New York: Simon & Schuster. Siegel (1956). Nonparametric Statistics for the Behavioral Sciences. New York: McGraw-Hill. Sugiyama, Y., Fushimi, T., Sakura, O. & Matsuzawa, T. (1993). Hand preference and tool use in wild chimpanzees. Primates 34, 151–159. Tomasello, M., Krieger, A. C. & Ratner, H. H. (1993). Cultural learning. Behav. Brain Sci. 16, 495–552. Toth, N. (1985). Archaeological evidence for preferential right-handedness in the Lower and Middle Pleistocene, and its possible implications. J. hum. Evol. 14, 607–614. Ward, J. P. & Hopkins, W. D. (Eds) (1993). Primate Laterality. Current Behavioral Evidence of Primate Asymmetries. New York: Springer. Warren, J. M. (1980). Handedness and laterality in humans and other animals. Physiol. Psychol. 8, 351–359.
W. C. McGrew Department of Sociology, Gerontology and Anthropology, and Department of Zoology, Miami Univesity, Oxford, Ohio 45056, U.S.A. Received 18 May 1994 Revision received 23 August 1995 and accepted 15 October 1995 Keywords: laterality, handedness, chimpanzee, Pan troglodytes, ethology, Gombe.
Laterality of limb function in wild chimpanzees of Gombe National Park: comprehensive study of spontaneous activities Resurgence of interest in laterality of hand function in nonhuman primates requires baseline knowledge of spontaneous hand-use in nature, in order to make sense of experimental studies in captivity. We present ethological data on 43 categories of limb movements exhibited by one community of wild chimpanzees (Pan troglodytes schweinfurthii) in the Gombe National Park, Tanzania. By focal-subject sampling, 42 individuals were observed at close-range over 4 months during their everyday activities. Laterality of hand function was largely absent, as both pooled results for the group and individual results rarely departed from 50:50 (ambilaterality). Neither age nor sex differences emerged. Nor did it matter if the subject was arboreal or terrestrial, or if the non-active hand was idle or engaged in postural support. Laterality was equally absent for unimanual and bimanual tasks. Lack of lateralization for limb movement in this natural population contrasts with findings of apparent right-handedness in captive chimpanzees. Unnatural postures and biased selection of measures in captive studies may account for these differences. ? 1996 Academic Press Limited Journal of Human Evolution (1996) 30, 427–443
Introduction Comparative (e.g. Ward & Hopkins, 1993) and evolutionary (Bradshaw & Rogers, 1993) studies of laterality of hand function in primates have mushroomed since interest in the topic was rekindled by MacNeilage et al. (1987). The hypothesized connections between brain lateralization, language, and handedness have led to further scrutiny of the hand preferences of nonhuman primates (e.g. Corballis, 1991). Evidence of hominid handedness in tool manufacture as a potential indicator of neural asymmetry has been sought in the archeological record (e.g. Toth, 1985; Schick & Toth, 1993). MacNeilage et al.’s (1987) postural origins theory hypothesized that nonhuman primates may show true handedness like human primates, that is, population-level laterality in hand use. This contrasted with the received wisdom of the time (e.g. Warren, 1980) that all nonhuman species (at least of mammals) were unlateralized, either being ambidextrous or at best, habitually lateralized in either direction as individuals. Of special interest is the extent of manual lateralization in the other hominoids, the lesser (Hylobatidae) and great (Pongidae) apes. For example, in their consideration of published results on gorillas (Gorilla gorilla), MacNeilage et al. (1991) concluded that these African apes showed a significant human-like pattern of preferring the right hand for all acts (cf. Byrne & Byrne, 1991; McGrew & Marchant, 1993). However, scrutiny of the available data on apes has led to differing conclusions: in a meta-analysis of methods, Marchant & McGrew (1991) opined that existing data-sets were inadequate, being based on too few, simplistic measures in too few, young subjects studied in captivity by artificial means. In a review of findings, Hopkins & Morris (1993) concluded that some functional motor asymmetries exist in great apes. Both articles decried the lack of data. The most crucial data are those from our nearest living relations, the chimpanzee (Pan troglodytes) and the bonobo (P. paniscus). With few exceptions (Marchant, 1983), earlier 0047–2484/96/050427+17 $18.00/0
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studies of these species were absent (P. paniscus) or suffered from the shortcomings detailed above (P. troglodytes). Recently, more useful data have become available both from captivity (e.g. Aruguete et al., 1992; Hopkins, 1993, 1996; Hopkins et al., 1993a,b) and from nature (Boesch, 1991; McGrew & Marchant, 1992; Sugiyama et al., 1993). (For a synthesis of laterality in hand-use by great apes, see McGrew & Marchant, 1996). These recent studies typically employed multiple tasks done by more than ten subjects, using precise measures and stricter statistical considerations. The field studies have focused on chimpanzees performing tool-use tasks, either nut-cracking or termite-fishing, and have found no convincing evidence of hand specialization, or handedness at the population level, but instead have found varying degrees of task specialization at the individual level (for explanation of terms, see McGrew & Marchant, 1994, and Discussion). The captive studies have found varying degrees of task specialization, especially when subjects assumed an (assisted) bipedal posture. Differences between the two sets of results could be general ones related to content (nature vs. captivity) or specific ones related to tasks (tool-use vs. non tool-use) or methods (spontaneous vs. induced performance). What is missing altogether is the simplest baseline data-set of all: a comprehensive, ethological study of spontaneous, everyday hand-use as practiced by chimpanzees in nature. What is needed are norms of what a community of apes does with their hands in all aspects of daily life in their environment of adaptedness. This was the aim of the study described below, except that tool-use as a special case is dealt with elsewhere (McGrew & Marchant, in prep.).
Methods The study was done in the Gombe National Park, a small (52 km2), well-protected park on the eastern shore of Lake Tanganyika, in western Tanzania (Goodall, 1986; Bygott, 1992). Subjects The main community (Kasakela) of eastern or long-haired chimpanzees (P. troglodytes schweinfurthii) was studied. It numbered 45 at the start of the study, though three members were never seen and were presumed dead. Table 1 gives information on age, sex, age-class, matrilineal kinship and number of days observed. Procedures Over 4 months (September–December 1992) the authors collected 238 h of observational data, using focal-subject sampling. Subjects were chosen opportunistically, with the goal of maintaining parallel running records on all 42 available subjects. Thus focal-sampling switched frequently, as one individual with fewer cumulative data arrived and ‘‘displaced’’ another with more data. After noting 100 instances of a behavioral pattern (see definitions below) by a subject, we took no more such data, but no subject reached this ceiling on all behavioral patterns. Data were collected by following subjects for up to 7 h, at a distance of no less than 3 m on the ground. All individuals were habituated to being watched, but some immigre adult females and their offspring were skittish. After informal reliability testing at the outset, we took on subjects as encountered, so that each observer collected data on all individuals. Observations were roughly even between mornings and afternoons, but were less frequent at dawn and dusk
Table 1
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Subjects of study: chimpanzees of Kasakela community
Name Males (n=21) Evered Goblin Atlas Beethoven Freud Prof Wilkie Frodo Tubi Gimble Pax Apollo Kris Sheldon Mel [Dharsi] Galahad Faustino Jackson Fax Ferdinand Females (n=24) Gigi Fifi Sparrow Patti [Kidevu] Spray Candy Skosha Gremlin [Dominie] Jiffy Sandi Fanni Trezia California Tita Darbie Flossi Dilly Tanga Sherehe Conoco Schweini Shani
Code
Year of birth
Age class
Mother
Days of observation
EV GB AL BE FD PF WL FR TB GL PX AO KS SL ME DH GD FO JK FX FE
?1952 1964 1967 ?1969 1971 1971 1972 1976 1977 1977 1977 1979 1982 1983 1984 1985 1988 1989 1989 1992 1992
Adult Adult Adult Adult Adult Adult Adult Adult Adolescent Adolescent Adolescent Adolescent Juvenile Juvenile Juvenile Juvenile Infant Infant Infant Infant Infant
OL ML AT ? FF PS WK FF LB ML PS AT KD SW MF DO GM FF JF FN FF
14 10 17 10 13 16 17 17 13 15 13 17 16 9 13 — 15 15 12 16 —
GG FF SW PI KD SY CD SS GM DM JF SA FN TZ CF TT DB FS DL TG SR CO SI SN
?1954 ?1958 ?1960 ?1966 1966 ?1969 ?1969 1970 1970 1972 ? 1973 1981 ? 1983 1984 1984 1985 1986 1989 1991 1991 1991 ?1992
Adult Adult Adult Adult Adult Adult Adult Adult Adult Adult Adult Adult Adult Adult Adolescent Adolescent Juvenile Juvenile Juvenile Infant Infant Infant Infant Infant
? FL ? ? ? ? ? NV ML DO ? SW FF ? CD PI LB FF DM PI SA CD SW SY
14 19 6 7 — 5 6 2 18 — 16 — 23 14 6 11 5 18 14 4 — 4 — 4
?, Estimated or unknown; [ ], long missing, presumed dead; —, insufficient data.
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430 Table 2
Categories of limb movements recorded
Arm-wrestle Back-reach Beg *Bipedal Carry Chin rest Cradle Cross Drum Eat Embrace Fend Groom ‘‘Hat’’ Hold *Idle *Lead *Nipple Nose wipe Offer Overhead Pat Pick-up Pincer Pluck Poke Pound Pull Reach *Recline Roll Scratch Self-groom Shade Shake *Show sole Slap Snatch *Stamp Suck Threat Throw Touch
Engage arm, hand, finger in motor play with another chimpanzee. Extend arm backwards to another, from quadrupedal stance. Extend arm with palm up to another. Support full body weight on legs. Grip and transport an object, without further acting on it. Support own chin on crossed arm, with hand gripping opposite shoulder or upper arm. Support infant’s weight on cradler’s torso and flexed arm. Rest flexed arm on other flexed arm (record uppermost arm); rest flexed leg on other thigh or knee (record uppermost leg). Rapid, forceful blow of palm on inanimate object (record leading arm if series of blows). Place object in mouth. Flex arm with palm or contact around torso of another. Abduct partly flexed limb to another, making physical contact. Manipulate body surface of another while visually fixating same location. Rest palm on top of own head. Grip object or another without further acting on it, while holder is stationary. Other limb inactive (not including postural support). Leg first extended forward in locomotion, from terrestrial, quadrupedal stance. Suck nipple (record whether left or right nipple). Rub side of hand once across nostrils, horizontally and momentarily. Extend limb with object held in hand or foot to another. Extend arm upward, vertical and unsupported. Slow, gentle blow of palm on another; lower arm motion. Extend limb and grasp detached object, then flex limb, in one continuous motion. Adduct two fingers to extract embedded object. Extend limb and grasp attached object, then flex limb, in one continuous motion. Insert extended digit as probe, then withdraw digit. Strike rapidly and forcefully with palm-held object. Flex arm forcefully, with torso extension, to bring object or another nearer. Extend limb with palm down or lateral to another. Rest body-weight on side of trunk and arm (not elbow); terrestrial. Propel object forward with palm on ground, while locomoting. Rake rigidly and partly flexed digits over own body surface. Groom own midline organ, e.g. genitals. Cover own eyes with palm. Grip attached vegetation and jerk horizontally, usually repeatedly. Partly flex one leg (so shin is horizontal), in tripedal stance. Rapid, forceful blow of palm to another; whole limb motion. Rapid grasp and retrieve of moving airborne object. Rapid, forceful leg extension to strike sole against object or another; whole leg motion. Insert digit or object into mouth, with lips pursed around it. (Excludes Nipple.) Rapid abduction of extended arm to another. Propel object through air by forceful arm extension. Extend limb to make soft physical contact with another.
*Non-manual activity.
(as it seemed unlikely that laterality varied with the circadian cycle, even if relative frequency of behavior patterns did). Data Data were written into note books or dictated onto cassette tape recorders, then later transcribed onto standardized check-sheets. Table 2 gives the 43 categories of limb movements and other behavioral patterns recorded. The repertoire was devised from published literature and from pilot observations, and was meant to be comprehensive of arm movements that
Table 3
431
Features of behavior patterns recorded
Arboreal Both Dominant Left Non-arboreal Other Right Subordinate
Body-weight wholly supported by vegetation above ground or by object resting on ground, e.g., boulder, fallen log. Two limbs act simultaneously and similarly on same object or with same function, e.g., two-handed drumming. Of two limbs engaged simultaneously and complementarily in a coordinated act, limb that performs more precise and skilled action. Left limb acts alone. Body-weight wholly or parly supported by ground. Non-left or non-right limb gives postural support, stays idle, or performs an act directed to another object or with another function. Right limb acts alone. Non-dominant hand performs less precise and skilled action.
occur often enough to be studied (but termite-fishing, a skilled type of tool-use, was scored separately). Table 3 defines the features of limb movement that were recorded. We recorded ‘‘one-handed’’ (or footed) acts as ‘‘left’’ or ‘‘right’’, and simultaneously we noted if the opposite hand was idle, provided postural support, or was engaged in another independent act. Thus, a chimpanzee might ‘‘pluck a fruit with left’’, while ‘‘holding another fruit with right’’. More often, however, the opposite hand was engaged in providing postural support, through contact with either the substrate (usually terrestrial) or woody vegetation (usually arboreal). Arboreality was recorded independently. For two-handed (or footed) acts, we distinguished between coordinated acts in which both limbs were ‘‘yoked’’ in doing the same thing, and acts in which the two limbs functioned complementarily. When complementary, the more precise hand was labelled as ‘‘dominant’’ and the other hand as ‘‘subordinate’’. An example of the former is ‘‘both’’ hands pulling together to bend a sapling; of the latter is one (‘‘dominant’’) hand poking out the contents of a fruit while the other (‘‘subordinate’’) hand holds the same fruit. In principle, all behavioral patterns (unless otherwise noted) might be performed with upper or lower limbs. Given that acts often occur in series, it is crucial for statistical analysis to distinguish between independent events that occur soon after the other (for a fuller discussion, see McGrew & Marchant, 1992 and Martin & Bateson, 1993). We counted as a new bout, only the first performance of a behavioral pattern after there had occurred an interviewing bout of another behavioral pattern. Thus, if a chimpanzee ‘‘plucked’’ six fruit in a row, then paused to ‘‘scratch’’ herself three times, then ‘‘plucked’’ another four fruit, we only scored ‘‘pluck’’ twice and ‘‘scratch’’ once. Thus we sought to avoid inflation of sample-size and compromising of statistical independence. All statistical tests are two-tailed, and the significance level ( ) was set at 0·05. Results Table 4 gives comprehensive results of 9689 bouts of hand-use by the wild chimpanzees of Kasakela community. These are pooled across all 36 categories of manual activity and across 39 subjects, thus it is an overall measure of handedness. (The other seven, non-manual categories are excluded here, as are three subjects, SA, SI, SR, who yielded no data.) Table 4 presents the ten most common categories, ranked in descending order of frequency, and lumps the remaining 26 patterns as Miscellaneous. Four categories were clearly more common: ‘‘scratch’’ (as self-maintenance), ‘‘groom’’ (as social behavior), ‘‘eat’’ and ‘‘pluck’’ (as
. . . .
432 Table 4
Overall hand use in wild chimpanzees of Kasakela community, Gombe, Tanzania (pooled data, n=39 Ss) Behavior pattern
Total
1. Scratch 2. Groom 3. Eat 4. Pluck 5. Pull 6. Nose wipe 7. Pincer 8. Pick-up 9. Hold 10. Cradle Miscellaneous (n=26 patterns) Total
2220 1888 1712 1297 426 339 273 174 134 127 1099 9689
Left (%) 1077 594 662 634 154 168 128 91 59 53 499 4119
(49) (47) (49) (51) (54) (50) (54) (52) (55) (42) (49) (49)
Right (%) 1141 659 679 615 129 171 108 83 49 74 523 4231
(51) (53) (51) (49) (46) (50) (46) (48) (45) (58) (51) (51)
Bimanual 2 635 371 48 143 0 37 0 26 0 77 1339
subsistence). For each category, the total number of bouts is split into unimanual left, unimanual right, and bimanual tasks. The latter varies markedly across tasks: no chimpanzee ever wiped its nose or picked up an object with both hands, but 34% of grooming bouts involved simultaneous activity by two hands. Overall, 14% (1339 of 9689) of bouts involved bimanual performances that will not be further considered here, unless specifically noted. Figures in parentheses in Table 4 give the proportions for one-handed tasks, and none departs from symmetrical randomness (50%:50%). Overall, 51% of bouts were right-sided and 49% were left-sided. None of the individual patterns departs from 50:50 by more than a few, nonsignificant percentage points, and these are not consistently skewed to one side or the other. However, pooled figures for a group may obscure individual differences, either in proportion of data-points contributed or in degree of lateralization. One subject might contribute most of the data, or a group that averaged 50:50 might comprise two subgroups, one 100% right-handed and the other 100% left-handed. Table 5 gives individual preferences, or lack of them, for the ten most common patterns; thus, for Groom, 14 subjects used the left hand more frequently, 18 used the right hand more frequently, two used each hand equally frequently, and five did not groom. (The most consistent non-performers were babes-in-arms. One subject, FE, the youngest infant, was dropped from individual analyses on grounds of too few bouts. All 38 other subjects had at least 20.) The pooled frequency column gives only one-handed bouts, and as these numbers decline, from 2218 to 127, the number of non-performers (no data) rises from 0 to 26. For only one pattern, ‘‘cradle’’, is non-performance the norm; 75% of cradles were by only two subjects, FF and FN, who were mothers of the group’s two youngest infants. None of the left-vs.-right comparisons in Table 5 departs from 50:50, and neither side consistently predominates across patterns. The apparently most skewed, ‘‘pull’’, with twice as many left-preferents as right-preferents (22 vs. 11) does not depart significantly from chance: Binomial test, n=33, chi square=11, z=1·74, P=0·08, two-tailed (Siegel, 1956, pp. 36–42). Figure 1 presents individual data on hand specialization, that is, pooled observations within a subject but across all categories of hand-use. This all-encompassing measure showed all subjects converging on 50% right-handed or chance. The most left-sided individual, CD, was only 40% right-preferent (73 of 184 total bouts), whereas the most right-sided subject, GD, was
Table 5
433
Individuals’ hand preferences for most common behavioral patterns (n=38 Ss) Behavioral pattern 1. 2. 3. 4. 5. 6. 7. 8. 9. 10.
Scratch Groom Eat Pluck Pull Nose wipe Pincer Pick-up Hold Cradle
Pooled frequency
Left
Right
Equal
No data
2218 1253 1341 1249 283 339 236 174 108 127
13 14 21 15 22 10 13 13 11 3
23 18 13 19 11 17 7 8 13 7
2 2 4 2 2 5 3 4 1 2
0 5 0 2 3 6 15 13 13 26
only 61% right-preferent. Most subjects were within a few percentage points of 50:50, but nine of the 38 showed weak but statistically significant hand specialization. GD, FN, WL, FS, and FF were right-handers, CD, TG, PF, and SS were left-handers, and the other 29 individuals were ambidextrous. The nine lateralized individuals were consistently so across categories of behavior; no single task biased their overall totals. Figure 2 presents pooled data taken from Finch (1941) on hand specialization across four tasks: string-pulling with fruit attached; picking up fruit; displacing an obstacle to reach fruit; picking up an individual piece of fruit. The study was done at Orange Park, Florida, the great ape research center founded by R. M. Yerkes. All but five subjects were strongly lateralized, about equally to left or right. Of these five, only one, Lita, was ambidextrous. Finch presented his data in pooled form, so it cannot be tested to look for differences across the four tasks. Sex Table 6 summarizes the results when the data-set is divided into two subsets by sex. There were equal numbers of females and males, and the 38 individuals showed similar distributions over four age categories. On average, females were observed on fewer days, and they showed wider variation across subjects in number of days of data collection. Females also contributed fewer data-points per individual, and both sexes showed wide variation across subjects. The lower numbers and greater variation for females reflect their more solitary ranging, and greater skittishness as immigrants in contrast to philopatric males, but this is likely irrelevant to any lateralization of function. The mean percentages of right-handed events for the 19 females vs. the 19 males for each subject’s pooled hand-use did not differ, either between sexes or from chance. Standard errors and ranges showed the same equivalence. Thus, there is no sign of sex differences in overall laterality of hand-use. Age Table 7 provides a similar comparison of the results for age. Nineteen adults were compared with 19 immature subjects (i.e., adolescents plus juveniles plus infants). The two subsets of subjects were observed for similar numbers of days, but adults provided more data points than
. . . .
434 Subject (n = 38)
R/(R + L)
Cd Tg PF Ss TB Cf Sn Sw GB Sy Pi AO Gg JK FD KS Tz SL FR ME FO Co Db EV PX Gm DL AL GL Jf BE FX Tt Ff Fs WL Fn GD 0%
50%
73/184 53/131 125/296 145/330 105/234 53/118 9/20 51/111 196/423 122/258 107/226 128/268 136/284 29/60 121/249 52/107 55/113 24/49 102/207 132/267 66/133 18/36 13/26 277/542 57/111 142/273 143/273 154/293 208/390 92/171 101/187 40/74 144/262 188/336 172/300 199/337 302/509 95/157 100%
z 2.75 2.10 2.62 2.14
2.13 2.48 3.26 4.17 2.56
Figure 1. Percentage of right-handed responses for all manual activities pooled for each subject (n=38). The z-scores given are statistically significantly different from 50:50 at P<0·01, two-tailed. Double upper-case codes are males; upper and lower-case codes are females.
did immature individuals. This difference reflects the more peripheral nature of adolescents and juveniles, and the more limited behavioral repertoires of infants, but neither of these age-related factors is likely to be relevant to degree of lateralization. As for sex above, the mean percentages of right- vs. left-handed performance did not differ by age, and both approximated chance at 50:50. The two measures of variance were also similar. Thus, there is no sign of age differences in laterality of hand-use. Leading leg Table 8 shows left vs. right preference for the only category of lower-limb behavior to occur frequently enough for analysis: ‘‘lead’’. For the 30 subjects providing data on the leg leading
435
Subject (n = 30) Lia Mona Nira May Frank Dita Nana Suzy Soda Cuba Kambi Wendy Bokar Jack Gamma Lita Fifi Bimba Beta Pati Bula Dina Pan Mamo Helene Alpha Josie Mimi Fin Bentia 0%
50%
R
z
5 5 5 10 15 20 30 35 40 85 90 105 120 150 355 410 485 520 540 685 710 735 740 750 760 775 785 790 795 800
27.90 27.90 27.90 27.55 27.19 26.84 26.13 25.78 25.42 22.24 21.98 20.83 19.77 17.64 3.15 5.98 8.45 9.87 20.12 21.89 23.66 24.01 24.72 25.42 26.49 27.19 27.55 27.90 28.25
100%
Figure 2. Percentage of right-handed responses for four manual tasks pooled for each subject at Orange Park (n=30), adapted from Finch [(1941) Science 94, 117–118]. Frequencies are estimated to nearest five responses by measuring Finch’s histogram bars. The z-scores given are statistically significantly different from 50:50 at P<0·01, two-tailed. R+L=800.
off bouts of quadrupedal locomotion, the pooled data showed no departure from 50:50, with 53% of bouts leading with the left leg, and 47% with the right. The lack of laterality was reflected in the totals for individual predominance, with 12 subjects being predominantly left-leaders and 14 right-leaders. The overall picture for laterality of limb function is one of little or no bias from the symmetrical distribution of equivalence of left and right. Idle hands Most of the time in wild chimpanzees, both hands are simultaneously active. On average, in only 10% of bouts of overall manual activity was one hand idle, across the 39 subjects. Furthermore, 58% (435 of 748) of the cases of an idle hand occurred during the performance of only one behavioral pattern, ‘‘groom’’. For other categories of behavior,
. . . .
436 Table 6
Sex differences in handedness
No. of subjects Adults Adolescents Juveniles Infants Days of observation Mean Standard error Range No. of data-points Mean Standard error Range % Right-handed events Mean Standard error Range
Table 7
Males
19 11 2 3 3
19 8 4 3 4
10·3 6·4 2–23
14·1 2·5 9–17
208·5 125·3 20–509
230·7 132·4 49–542
49·3 5·4 40–59
50·5 4·5 42–61
Age differences in handedness
No. of subjects Days of observation: Mean Standard error Range No. of data-points: Mean Standard error Range % Right-handed events: Mean Standard error Range
Table 8
Females
Adults
Immatures
19
19
12·8 5·6 2–23
11·6 4·8 4–18
280·5 117·1 111–542
158·7 109·4 20–390
49·7 5·3 40–59
50·1 4·8 40–61
Lateralization of leading leg in initiating quadrupedal locomotion (n=30 Ss)
Overall pooled Individuals
Left (%)
Right (%)
Equal
No data
Total (%)
362 (53) 12
317 (47) 14
— 4
— 8
679 (100) 38
Table 9
Overall laterality of Groom when other hand is idle vs. active (pooled data, n=34 Ss) Left (%) Idle Support Other activity Total
Table 10
437
202 381 11 583
Right (%)
(46) (48) (44) (47)
233 412 14 645
Total (%)
(54) (52) (56) (53)
435 793 25 1253
(100) (100) (100) (100)
Individual’s grooming as more or less lateralized when other hand is idle rather than when providing positional support
Idle
Less
More
Same
Total
13
17
4
34
bouts with an idle hand were rare: ‘‘eat’’, 6%; ‘‘pluck’’, 2%; ‘‘pull’’, 0·5%, etc. Thus, detailed, further analysis of the other hand being idle while the active hand showed laterality are limited to grooming. Table 9 shows the overall proportions of bouts of grooming in which the non-grooming hand was idle, provided postural support, or was engaged in another activity, usually holding an object. Neither in the overall totals, nor in any of the three subsets is there a departure from 50:50 randomness. (In the other 635 bouts of grooming, both hands were involved, i.e., it was a bimanual task.) Table 10 compares the grooming of individual subjects for two kinds of bouts: when the other hand was idle vs. when it provided postural support. Two expectations seem plausible: one is that an occupied other hand will enhance laterality effects, as priorities such as positional security, comfort, or retaining possession of objects may bias what the active hand does. The other expectation is that when one hand is idle, the other activity will be more lateralized, as the chimpanzee has more freedom of choice of hand to use than when the environment was more constraining. The results showed no difference: of the 34 subjects who groomed, 13 were less lateralized and 17 were more lateralized when the other hand was idle. Arboreality Behavioral patterns varied in the extent to which they were performed in the trees or on the ground. (See Table 11.) Some were mostly terrestrial: ‘‘scratch’’ while resting or interspersed with grooming or locomotion; ‘‘groom’’ while lounging in parties. Others were mostly arboreal: ‘‘eat’’ and ‘‘pluck’’ in feeding; ‘‘pull’’ in foraging or nest-building. Whatever the behavioral pattern, it is hypothesized that arboreal chimpanzees should be more lateralized than terrestrial ones, as their positional behavior is more constrained by a three-dimensionally structured environment. That is, apes up in the canopy typically must use one hand in support to keep from falling, while on the ground, both hands typically are free. [This assumes that above the ground a ripe fruit is on average just as likely to be hanging to the right as to the left, or that the next branch needed for support projects from the left side as often as from the right
. . . .
438 Table 11
Overall laterality of most common behavior patterns when arboreal vs. non-arboreal, pooled data Arboreal
Behavioral pattern
Left (%)
Scratch Groom Eat Pluck Pull
374 111 521 517 122
Table 12
Behavioral pattern Groom Eat
(48) (49) (50) (50) (53)
Non-arboreal
Right (%) 404 116 521 512 107
Left (%)
(52) (51) (50) (50) (47)
696 483 144 117 32
(48) (47) (47) (53) (59)
Right (%) 744 543 160 103 22
(52) (53) (53) (47) (41)
Total
Arboreal
2218 1253 1346 1249 283
23% 17% 73% 82% 70%
Overall laterality of bimanual activities of sufficient frequency, when subordinate hand is simultaneously active vs. idle; pooled data Active
Idle
Total
Both
Left (%)
Right (%)
Left (%)
Right (%)
644 515
529 215
58 (50) 147 (49)
57 (50) 153 (51)
202 (46) 52 (49)
233 (54) 57 (52)
side of the tree’s trunk. Similarly, on the ground, objects are likely to be arranged evenly in all directions, although the essentially flat substrate allows more freedom of action, especially from whence they can be approached (cf. Boesch, 1991, for reaching).] Table 11 shows the overall laterality for the five most common behavioral patterns, when performed arboreally or non-arboreally. (The table includes only the top five, as the total numbers of bouts when broken down four ways are low.) There is no difference between left and right predominance in either condition for any behavioral pattern. Notably, extent of lateralization is not more when the behavior is done arboreally; none of the comparisons differs significantly from 50:50. Bimanual Table 4 shows that only two categories, ‘‘groom’’ and ‘‘eat’’, occurred often enough for further analysis of the simultaneous use of two hands. We combine ‘‘subordinate’’ and ‘‘other’’ (but excluding idle and postural support) to provide data on what the non-dominant hand actively does at the same time as the dominant hand. (See Table 12.) For ‘‘groom’’, most bimanual activity (82%, 529 of 644 bouts) entails both hands being similarly engaged in manipulating another’s body surface, focused on the same point. Less commonly, especially when a mother grooms her infant, she grooms with the dominant hand and holds another part, typically a limb, with the subordinate hand. For ‘‘eat’’, the most common case (58%, 300 of 515) is for the diner to eat from an object in the dominant hand while holding another food-item in the subordinate hand (cf. Hopkins et al., 1993b). We hypothesized that these bimanual combinations of hand-use would be more lateralized than cases in which only one hand was used in grooming or eating while the other hand was idle. This was expected on the grounds that two-handed activities are more constrained by task requirements than are one-handed activities. Table 12 shows no difference in bimanual activity between these conditions for either category of behavior; neither departs from 50:50.
439
Summary Wild chimpanzees are notably unlateralized in their limb movements, whether at the level of individual preference or population-level handedness, or task or hand specialization. This symmetry holds for both one- and two-handed tasks, across potentially biasing conditions. Put another way, the only indications of asymmetry are that a few (nine of 38) individuals showed weak but statistically significant hand specialization (see Figure 1). Discussion The results of this study suggest that at least one population of wild chimpanzees is comprehensively unlateralized in hand-use, at least in tasks other than tool-use. (At Gombe, only one type of tool-use, termite-fishing, is common, and it is highly seasonal, being confined largely to the months of October–December, Goodall, 1968.) These apes show no handedness (i.e., laterality across tasks and across individuals, at population level), no task specialization (i.e., laterality within a task but across individuals), and only a few may show mild hand specialization (i.e., laterality across tasks but within an individual). Theirs is essentially a 50/50 world of manual activity. These results run counter to the recent conclusions of MacNeilage et al. (1987, 1988, 1991) and to recent syntheses from published data (Hopkins, 1996; Hopkins & Morris, 1993), who found functional asymmetry in apes. More precisely, it differs from recent empirical findings in captivity: Aruguete et al. (1992) found for 27 chimpanzees, statistically significant right-sided touching of the inanimate environment, but no laterality at group level for touching their own faces or bodies. Hopkins (1993) found, for 40 chimpanzees, a statistically significant right-sided bias for the group in reaching to pick up an object while standing bipedally. Hopkins et al. (1993a) found, for 36 chimpanzees, that throwing was lateralized to the right for the group, while for 12 mothers with infants, the former’s cradling was not lateralized. For 11 bonobos, Hopkins et al. (1993b) found statistically significant biases for carrying an object (left-sided), for leading limb in locomotion (right-sided), and for feeding (right-sided) while holding another food item with the left hand. All of these biases were consistent across the group, but another four patterns (face-touching, self-touching, gesture, reaching) did not differ in laterality. Thus, at least some task specialization seems to be the norm for captive chimpanzees. In contrast, studies in nature of wild chimpanzees doing non-tool-use activities show a lack of lateralization. At Tai, Boesch (1991) found that chimpanzees were unlateralized as a group for reaching to pick up fruit (n=20 Ss) and for grooming (n=15 Ss). At Bossou, Sugiyama et al. (1993) found no lateralization at group level for 19 chimpanzees in bouts of picking fruit from a branch and moving it to the mouth (feeding). Thus, our findings of lack of laterality resemble those of other field studies using more selected measures, and contrast with those from captive settings in laboratories or zoological parks. In the naturalistic setting of an island in a safari park with a free-ranging group of 27 chimpanzees, the results for hand-use resembled these from the wild. For none of seven behavioral categories (social reach, non-social reach, feed, carry, throw, hold, groom) did the pooled results depart from 50:50, thus there was an overall lack of laterality. For two categories, non-social reach and feed, most of the individuals showed significant lateralization to one side or the other, but there was no population-level task specialization to one side, much less handedness across all or even most activities. (See Marchant, 1983, Tables 2 and 3, for details.) What independent variables might explain these apparently conflicting results?
440
. . . .
A potential major difference between captivity and nature is in arboreality–terrestriality, although this variable rarely is addressed specifically. Most if not all captive data seem to come from subjects on the floor or ground, whereas at least some data in all field studies comes from individuals above the ground. This is likely to mean differences in posture or positional behaviour in the two conditions of verticality, as when they are arboreal, apes typically use one or more hands or feet to support or secure themselves, whereas when they are terrestrial, this is unnecessary. Time spent arboreal is notable: fully habituated chimpanzees at Gombe and Mahale spend on average 53% and 39% of their waking hours above ground (Hunt, 1992). Doran (1993b) produced similar figures for arboreal postural activity of 37% for males and 58% for females among chimpanzees at Tai. (No comparable data are yet available for incompletely habituated bonobos at Lomako, but it seems likely that P. paniscus is equally as arboreal as P. troglodytes.) Our data-set from Gombe is the only one to focus on this dimension, and it yields no apparent differences across conditions in major manual activities, but until captive studies take note of the variable, preferably by housing and testing subjects in settings with rich vertical opportunities, and until field studies specify this variable during observation, its importance remains obscure. A methodological difference between captive and field studies in print is that the former have paid more attention to the status of the ‘‘other’’ hand. Aruguete et al. (1992) recorded laterality data only when both hands were free and available to make the response, and thus excluded all cases when the other hand provided postural support, held an object, etc. This provided ‘‘unbiased’’ data but restricted data collection to an abnormal subset of activities, at least by natural standards. (For example, Table 9 shows that the other hand was idle in only 35%, 435 of 1253, bouts of one-handed grooming, which is the most extreme case.) Hopkins et al. (1993b) divided the other hand’s activity into eight categories that were noted while the favored hand was feeding, and these alternatives made a significant difference. When the other, left hand held food, the bonobos were lateralized as right-sided feeders, but no such laterality occurred if the other hand was inactive, providing support, etc. Previous field studies did not specifically record such data, though Sugiyama et al. (1993) stated that while picking food, a chimpanzee at Bossou usually employed the other hand in support. Similarly, Boesch (1991) noted that Tai chimpanzees reached to pick up fruit while sitting (with both hands free), while in grooming the other hand sometimes held a branch or rested on the ground, and so this task had some external constraints. Only detailed and comparable data from a variety of settings will clarify the issue, but it seems likely that apes in laboratory cages or zoo enclosures will spend more time with idle hands, and this may influence the extent of lateralization shown in their manual activities. Most studies of laterality in hand use have focused on one-handed tasks (e.g. Aruguete et al., 1992; Hopkins et al., 1993a; Sugiyama et al., 1993) or have recorded but not presented data on the relative contributions of the hands to two-handed tasks (e.g. Hopkins et al., 1993b; McGrew & Marchant, 1992). This emphasis on selective, unimanual measures applies equally to published findings from field and laboratory (including tool-use). We presented data, though for only two behavioral patterns, ‘‘groom’’ and ‘‘eat’’, suggesting that whether the other hand is idle or engaged in coordinated but subordinate activity makes little difference to the degree of laterality of the active or dominant hand. We suggest that a more ethological approach, incorporating more and complex categories such as food processing, in both captivity and nature, would clarify these issues (cf. Byrne & Byrne, 1991, 1993). Following MacNeilage et al.’s (1987) lead, recent studies of laterality in limb-use by captive apes have emphasized posture as an independent variable (e.g. Hopkins, 1993) while field
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studies have not. While MacNeilage (1993, p. 330) continues to espouse a ‘‘postural origins’’ theory that accounts for right-handedness in higher primates, based on freed limbs while sitting, empirical tests of posture as an influence have focused on upright bipedal postures while standing (Hopkins et al., 1993a,b). Two kinds of upright bipedal stance are noted: one in which both hands are freed of providing support, and another in which one hand provides postural support while the other is free (Hopkins, 1993). The latter is really a form of tripedalism, and is sometimes called ‘‘aided bipedalism’’ (Doran, 1993b). Both versions of bipedalism occur naturally in Pan spp., but they are rare. At Gombe and Mahale, chimpanzees spend an average of 0·25% of their time in bipedal standing and 0·1% in bipedal walking (Hunt, 1992). For bonobos, the most frequent form of bipedalism, during feeding by males, occupies only 2·8% of the time, and it is arboreal, not terrestrial (Doran, 1993a). No published field study of apes has focused on posture as an independent variable, and no such study in captivity has singled out sitting as a postural category, nor distinguished between free-standing and aided bipedalism. (Diamond & McGrew, 1994, studied laterality in cotton-top tamarins, Saguinus oedipus, in captivity, and found population-level right-handedness for six of seven categories of manual activity. The effect was more strongly right-sided when subjects were in postures that had both forelimbs free than when they were in aided bipedal postures.) The best candidate explanation for differences in laterality of hand-use between natural and captive settings appears to be postural. Individuals of Pan spp. that are tested in atypical, human-like bipedal postures display indications of human-like handedness, unlike their wild counterparts who eschew such postures. It is tempting to infer that this contrived ‘‘hominization’’ somehow mimics the selection pressures that produced hominid bipedalism from a hominoid ancestral form (Hunt, 1994). An obvious analogy is how exposure to artificial language systems via human tutelage may have enhanced the cognitive functioning of captive apes toward more human levels (Tomasello et al., 1993). It may be that settings conducive to bipedalism may somehow lateralize the ‘‘freed hands’’ of captive apes. This is empirically testable, but additional ethological studies also need to be done of both captive and wild apes performing their full repertoire of manual behavior in the full range of postures. At the more micro-level, differences between nature and captivity may stem from the measures or tasks chosen. Most previous studies recorded few tasks of apparent high reliability but of suspect validity. This raises questions of artifactual results in contrived unnatural settings. For example, although it is the commonest dependent variable in experimental studies of primate laterality, picking up a detached object off a horizontal surface is actually an uncommon activity in wild chimpanzees (see Table 4). The objects that chimpanzees in nature handle are usually food-items, and these are usually plucked or picked. Another commonly recorded category, self-touching (of the face, body, etc.) is so vague as to be of doubtful utility, as it lumps together self-grooming (maintenance), scratching (displacement), masturbation (sexual), chin-resting (comfort), nose-wiping (nervous habit), etc. It is a sobering discovery that of the ten most common hand uses shown by Gombe’s chimpanzees, only five have ever been recorded in major captive studies: groom (Marchant, 1983); eat (=feed, Marchant, 1983; Hopkins et al., 1993b); pick up (=reach, Marchant, 1983; Hopkins et al., 1993a,b); hold (Marchant, 1983); and cradle (Hopkins, 1993). If apes are naturally ambidextrous, and only artificially lateralized (again, setting tool-use aside), what does this say about the basic problem of why laterality of function at population or species level should ever evolve? It is clear that in everyday life, wild chimpanzees benefit from moment to moment by being ambilateral: if a fruit is suspended in space to their left side, it is convenient to pluck it with the left hand; if one’s right ankle itches, it is convenient to
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scratch it with the right hand; if the trail immediately ahead is clear and flat to the left, it is convenient to take the first step to the left; if the next highest branch on the tree projects to the right, it is convenient to ascend by grasping it with the right hand; etc. Even if there are tasks of skill or strength that are done more efficiently by habitual use of one hand, unless these are lateralized in the environment, why need the lateralization be any more than individual preference to right or left. Viewed in this way, handedness or task specialization to one side at population level seems to be a self-imposed limitation. Rather than ask whether or not other species are lateralized like ourselves, perhaps we should be asking why any species should disadvantage itself with the curse of laterality? Finding and clarifying the benefits that offset the costs of being lateralized are the most basic challenges of laterality research. Acknowledgements We are grateful to the Tanzania Commission for Science and Technology (UTAFITI), Serengeti Wildlife Research Institute, and Tanzania National Parks for granting permission to do the research; L. S. B. Leakey Foundation and Miami University for funding; J. Goodall and the staff of the Gombe Research Centre and S. Qolly and P. Msuya and the staff of the Gombe National Park for facilities and assistance; A. Collins, J. R. Dharsi, C. Packer, C. Stanford, C. Uhlenbroek, K. & J. Vaitha, W. Wallauer, and J. Wallis for companionship and manifold acts of kindness; R. Byrne, M. Holder, W. Hopkins, J. King, and three anonymous reviewers for critical comments on the manuscript. The work is dedicated to the memory of two venerable wazee: Evered and Gigi. References Aruguete, M. S., Ely, E. A. & King, J. E. (1992). Laterality in spontaneous motor activity of chimpanzees and squirrel monkeys. Am. J. Primatol. 27, 177–188. Boesch, C. (1991). Handedness in wild chimpanzees. Int. J. Primatol. 12, 541–558. Bradshaw, J. & Rogers, L. (1993). The Evolution of Lateral Asymmetries, Language, Tool Use, and Intellect. San Diego: Academic Press. Bygott, D. (1992). Gombe Stream National Park. Arusha: Tanzania National Parks. Byrne, R. W. & Byrne, J. M. (1991). Hand preferences in the skilled gathering tasks of mountain gorillas (Gorilla g. beringei). Cortex 27, 521–546. Byrne, R. W. & Byrne, J. M. (1993). Complex leaf-gathering skills of mountain gorillas (Gorilla g. beringei): variability and standardization. Am. J. Primatol. 31, 241–261. Corballis, M. C. (1991). The Lopsided Ape. New York: Oxford University Press. Diamond, A. C. & McGrew, W. C. (1994). True handedness in the cotton-top tamarin (Saguinus oedipus)? Primates 35, 69–77. Doran, D. M. (1993a). Comparative locomotor behavior of chimpanzees and bonobos: the influence of morphology on locomotion. Am. J. Phys. Anthropol. 91, 83–98. Doran, D. M. (1993b). Sex differences in adult chimpanzee positional behavior: the influence of body size on locomotion and posture. Am. J. Phys. Anthropol. 91, 99–115. Finch, G. (1941). Chimpanzee handedness. Science 94, 117–118. Goodall, J. v. L. (1968). The behaviour of free-ranging chimpanzees in the Gombe Stream Reserve. Animal Behav. Monographs 1, 161–311. Goodall, J. (1986). The Chimpanzees of Gombe. Cambridge: Harvard University Press. Hopkins, W. D. (1993). Posture and reaching in chimpanzees (Pan troglodytes) and orangutans (Pongo pygmaeus). J. Comparative Psychol. 107, 162–168. Hopkins, W. D. (1996). Chimpanzee handedness revisited: 55 years since Finch (1941). Psychonomic Bull. Rev. (in press). Hopkins, W. D., Bard, K. A., Jones, A. & Bales, S. L. (1993a). Chimpanzee hand preference in throwing and infant cradling: implications for the origin of human handedness. Curr. Anthropol. 34, 786–790. Hopkins, W. D., Bennett, A. J., Bales, S. L., Lee, J. & Ward, J. (1993b). Behavioral laterality in captive bonobos (Pan paniscus). J. Comparative Psychol. 107, 403–410. Hopkins, W. D. & Morris, R. D. (1993). Handedness in great apes: a review of findings. Int. J. Primatol. 14, 1–25.
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