Cultures in Chimpanzees

Nature, 399, 682-685 (1999)
Whiten, A. ‡1, Goodall, J. ‡2, McGrew, W.C. ‡3, Nishida, T. ‡4, Reynolds, V. ‡5, Sugiyama, Y. ‡6 Tutin, C. E. G. ‡7, Wrangham, R. W. ‡8 and Boesch, C. ‡9

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Oxford University. ‡6 Tutin. ‡5. Oxford OX2 6QS. Kigoma. ‡5 Institute of Biological Anthropology. Germany. Reynolds. From this perspective. 58 Banbury Road. are customary or habitual amongst some communities.Cultures in Chimpanzees Whiten. We therefore adopted a different strategy in our attempt to provide a definitive assessment of 2 . Kyoto University. Moreover. Inuyama 484-8506. a cultural behaviour is one that is transmitted repeatedly through social or observational learning. and Department of Biological Sciences. which. ‡2. to become a population-level characteristic17.. Scotland. C. these tabulations have been based upon published reports. 04301 Leipzig. We find that 39 different behaviour patterns. A. ______________________________________ As an increasing number of field studies of chimpanzees (Pan troglodytes) have achieved long-term status across Africa. ‡7 Centre Internationale de Recherche Medicales de Franceville. Amongst mammalian and avian species. a phenomenon characteristic of human cultures14 but previously unrecognised amongst non-human species. Well-documented examples include dialects in song-birds12-13 sweet-potato washing by Japanese macaques at Koshima19 and stone-handling by Japanese macaques at Arashiyama20. ‡8 and Boesch. C. However. each case refers to variation in only a single behaviour pattern. the combined repertoire of these behaviour patterns in each chimpanzee community is itself highly distinctive. and they do not systematically document the absence of behaviour patterns present elsewhere. Nishida. cultural variation has previously been identified only for single behaviour patterns. USA. The extensive. Culture is defined in very different ways in different academic disciplines15. Stirling. Tanzania. ‡9 ‡1 Scottish Primate Research Group. Y. V. MA 02138. Japan. some cultural anthropologists insist on linguistic mediation.C. ‡2 Gombe Stream Research Centre. Here we present a systematic synthesis of this information from the seven most long-term studies. Harvard University. Gabon. which together have accumulated 151 years of chimpanzee observation. a more inclusive definition is accepted. ‡1. so that culture is constrained to be a uniquely human phenomenon16. Tabulations of population differences amongst chimpanzees have indicated that multiple behavioural variants exist2-7. multiple variations now documented for chimpanzees are thus without parallel. ‡8 Department of Anthropology. KY16 9JU. However. McGrew. E. T. University of St Andrews. grooming and courtship behaviours. England. St Andrews. Japan. ‡6 Primate Research Institute. This comprehensive analysis reveals patterns of variation far more extensive than have previously been documented for any animal species except humans8-11. ‡7. ‡4 Laboratory of Human Evolution Studies. W. BP 769 Franceville. inter-generation transmission of behaviour may occur either genetically or through social learning. although they record the presence of behaviours. cultural differences (often known as ‘traditions’ in ethology) are well-established phenomena in the animal kingdom and are maintained through a variety of social transmission mechanisms18. Insellstrasse 22. Ohio 45056. In the biological sciences. ‡4. including tool usage. Wrangham. At one extreme. ‡9 Max-Planck Institute for Evolutionary Anthropology. R.O. ‡3. Cambridge. J. remain problematic in three respects: they are incomplete. in which the significance of cultural transmission is recognised as one of only two important processes that can generate evolutionary change. Oxford. W. Box 185. Kyoto 606-01. Gerontology and Anthropology. By this definition. Goodall. FK9 4LA. ‡3 Department of Zoology and Department of Sociology. Kyoto University. School of Psychology. University of Stirling. with processes of variation and selection shaping biological evolution in the first case and cultural evolution in the second. USA. differences in the behavioural repertoires described have become apparent that suggest there is significant cultural variation1-7. such as the local dialects of song-birds 12-13. they frequently do not clarify the extent to which each behaviour pattern is habitual in the community. yet are absent in others where ecological explanations have been discounted. Sugiyama. Miami University. P. G.

Three other classes of profile need to be recognised and discriminated from this. as applicable at their site: (1) customary. The only major difference between the western and eastern populations is that nutcracking occurs in the west. The remaining behaviours are absent at some sites but are customary or habitual at others (Band D in Table 1).. although the fact that this behaviour terminates abruptly at the 3 . Beginning with a list drawn from literature review by A. 1) are distinctively different. We arrive at a similar comparative conclusion when we examine the overall profiles of cultural variants in the different communities (Fig. Second. the profile of codings of particular interest with respect to cultural variation is that in which behaviours are recorded as customary or habitual in some communities. each with a pattern comprising many behavioural variants. These patterns vary as much between sites associated with the same sub-species (verus at Bossou vs. yet absent at others. but others are shared between two or more communities (Table 2). Use of an additional stone to balance an anvil (anvil-prop) occurs only at Bossou. and any absence of ground night-nesting by high predator risk. These studies bring together a total of 151 years of direct observation (range 8-38 years). The patterns were then split and lumped as appropriate. for which the behaviour occurs in all or most able-bodied members of at least one agesex class (e.what is now known of chimpanzee cultural variation. For any row in Table 1. the research directors of the major chimpanzee field projects (Table 1) added and defined unpublished candidate patterns. In phase 2. 1). Absence of algaefishing can be explained by the rarity of algae. but it is not expected elsewhere because stone anvils are either not used or (at Tai) embedded in the ground. We know of no comparable variation in other nonhuman species. which are behaviours suspected by research workers to be specific to particular chimpanzee populations. seven behaviours proposed as potential cultural variants in phase 1 were shown instead to be either customary or habitual in all communities (band A in Table 1). so the ‘unknown’ code seldom applicable (Table 1). This complex. adult males). and schweinfurthii at the four eastern sites) as between sub-species themselves.g. sixteen patterns failed to achieve habitual status in any community (band B in Table 1). The scope of this list. (4) absent. (3) present. These codings were cross-checked and confirmed by senior colleagues working at each site.W. so the clusters of variants that characterise each community are not mutually exclusive. First. for which absence is explicable because of a local ecological feature. for which the behaviour is not customary but has occurred repeatedly in several individuals. the profiles of each community (Fig. represents a unique record of the inventiveness of wild chimpanzees. Nevertheless. for which the behaviour has not been recorded and no ecological explanation is apparent.B. for which the behaviour has not been recorded. significantly more than previously suspected for chimpanzees 1-6. Phase 1 of the study established a comprehensive list of candidate cultural variants. (5) ecological explanation. We have found 39 such behavioural variants. Tai in the west. so our data summarize the enormous increase in our knowledge of chimpanzee behaviour achieved in the latter half of this century. Some customary and habitual patterns are unique to certain communities. and (6) unknown. for which the behaviour is neither customary nor habitual but is clearly identified. (2) habitual. differentiating 65 categories of behaviour. the research directors assigned to each of these behaviour categories one of the following six codes. but this may be because of inadequacy of relevant observational opportunities. and C. collaborative and iterative process produced a listing of candidate cultural variants that were fully and consensually defined (see Supplementary Information. The third class includes profiles in which all cases of absence are explicable by local conditions (band C in Table 1). consistent with some degree of social transmission. Table 1 gives abridged descriptions). just three cases were identified. Our results are for the seven chimpanzee groups with the most long-term observation record. although no systematic study of this kind appears to have been attempted before.

some of the differences between communities described here represent not only the contrast between habitual versus absent. are not found in animals. Experimental studies on the acquisition of tool-use and food-processing skills by both children and captive chimpanzees indicate that there is a complex mix of imitation.27-30 . with leaf-squash. items 39.40). ______________________________________ 4 . transmitted. or whether any other animal species. such as imitative learning and teaching. Our results show that chimpanzees. Unique refers to customary or habitual patterns unique to the sites. in which differences between cultures are constituted by a multiplicity of variations in technology and social customs14. the most commonly suggested alternative to which is stimulus enhancement26. shared refers to number of customary or habitual patterns shared with other sites. whereas in the second method a short stick is held in one hand and used to collect a smaller number of ants. Received 24 March. a long wand is held in one hand and a ball of ants is wiped off with the other. ______________________________________ Table 2 Number of unique versus shared patterns that are either customary or habitual. our closest sister-species. Examples include cases of tool use. such as the two different methods of ant-dip (Table 1. However. It is difficult to see how such behaviour patterns could be perpetuated by social learning processes simpler than imitation. It remains to be shown whether chimpanzees are unique in this respect. Site Bs Tai Go Ma Mk Kib Bd Unique 1 8 3 0 1 1 1 Shared 8 16 13 11 9 9 8 Sites are abbreviated as in Table 1. would reveal qualitatively similar patterns. although this study represent the definitive state of knowledge at present. have rich behavioural complexity. if studied in the same way. arguing that if processes of human cultural transmission. in the first of these. The patterns in Fig. leaf-inspect and index-hit occurring in different communities (Table 1. rather than genetically.Sassandra-N’Zo river within the range of the verus sub-species21 shows it is culturally. Other comparisons between human and nonhuman animal cultures have focused on the cognitive processes involved. other forms of social learning. But this does not mean that imitation is the only mechanism at work. accepted 11 May 1999. Other examples occur in social behaviour. and individual learning 24-25. then culture in animals is merely an analogue of that in humans. These experimental designs show differential copying of each of two quite different methods used to process the foods. 1 can thus be seen to resemble those in human societies. such as the variants used to deal with ectoparasites discovered during grooming. which are transferred directly to the mouth. in which the attention of an observer is merely drawn to a relevant item such as a stick. items 56-58). but also the contrast between different versions of an otherwise similar pattern. Every longterm study of wild chimpanzees has identified new behavioural variants. Frequencies exclude ‘universal’ behaviour patterns identified in band A of Table 1. Similarly. we must expect that more extended study will elaborate on this picture. Our data agree with experimental studies that have shown that chimpanzees copy the methods used by others to manipulate and open artificial ‘fruits’ designed as analogues of wild foods24-25. rather than homologous with it22-23.

Jr. M.1. Y.. B. & Galef. M. I. Cambridge MA. C.. Wilson for contributions to the database. 1988). T. C. Processes of social learning in the tool use of chimpanzees (Pan troglodytes) and children (Homo sapiens). The Chimpanzees of Gombe: Patterns of Behavior. 3-14 (1996).. Marchesi. Tokyo. 183223 (1980). Nishida. B. P. C. G. J. Huffman. K. Evidence for a social custom in wild chimpanzees? Man 13. 18. 1993). 16. Tomasello. 28. Heyes. Murdock. Man. 146. 5. Chicago 1987). & Bard. H. J.. 1. 34. Imitative learning of artificial fruitprocessing in children (Homo sapiens) and chimpanzees (Pan troglodytes). P. T. Primates 1. Correspondence and requests for materials should be addressed to A. N. C. J. Jr. Cheney. B. Marler. Marchesi.. Nishida. K. Collins. McGrew. Pittsburgh. On the nature of imitation in the animal kingdom: reappraisal of a century of research. Goodall. & Palameta. P. J. Imanishi. Teixidor. S. 175-183 (1987). Katongole. K. Collins. & Ratner. London. 1963) Bloch. H. 17. C. 183-198 (1991). 12. 168-181 (1985). Human Evolution 2. Supplementary information is available on Nature’s World-Wide Web site (http://www. L. 8. (Tokyo University Press. C. Nagell. P. B. (Cambridge University Press. Psych. de Waal. F. M. 16. M. Catchpole. 1. 25. Davis-Dasilva. Mkono. & Slater.. Sumita. Culture in non-human primates? Ann. Brain Sci. Wrangham. Whiten. Cambridge. 20. (Cambridge. A. Zentall. H. P. B.-C. S. (eds) Chimpanzee Cultures (Harvard University Press. C.. in Primate Societies (eds Smuts. Human Nature. 1-29 (1957). The acquisition of stone tool use in captive chimpanzees. Mass. 4. 239283 (1992).) 141-164 (Erlbaum.. Advances in the Study of Behaviour T. 806-850 (1937). & Chavaillon.. C. Mugurusi. R. Human Evolution 26. G. Boesch. Slater for advice on the manuscript. Kruger. Behav.M. Stokes. Newton-Fisher. J. D. Culture: A Critical Review of Concepts and Definitions. 1986). Boesch. M. B. A. 30. T.. Comp. Cambridge. G. Olguin. Ethol. W. (Cambridge University Press. 6. Imitation of the sequential structure of actions by chimpanzees (Pan troglodytes). 10. Ethnographic Atlas. & Tutin. 5 . 1996). in Social Learning: Psychological and Biological Perspectives (eds. 23. Muller. Fawcett. (Princeton University Press. Muhumuza. & Heltne. & Norikoshi. 27. M. Discovering and learning tool-use for fishing honey by captive chimpanzees. Primates 26. D. F. Kiwede. C. E. Kroeber. L.. Matama. B. I Salala. Psychol. J. Is nut cracking in wild chimpanzees a cultural behaviour? J. & Joulian. 157-178 (1992)..) 267-289 (Academic Press. Seyfarth. Princeton NJ. 1995). in The Use of Tools by Human and Non-human Primates (eds Berthelet. 234-251 (1978). Animal cultures and a general theory of cultural evolution. Perrett and P. 112. M. D. & Tomasello. 2. L. McGrew. R.: Harvard University Press. Mpongo. 495-552 (1993). W. 21.. K. Uehara. Song ‘dialects’ in three populations of white-crowned sparrows... Psychol. 88. W. Experimental studies of learning and the mental processes in infra-human primates. G. Chimpanzee Material Culture: Implications for Human Evolution. C. G. Cultural learning. K. Fruth. A. Camak. Wrangham. Proc. G. and M. K. 3. P. McGrew. Observational learning of tool-use by young chimpanzees. 325-338 (1994). D. J.. Arnold.. Psychol. Assersohn. W. Human Evolution 7. K. The Chimpanzees of the Mahale Mountains: Sexual and Life History Strategies. anthropology and cognitive science. 29. Z. 301-328 (1998). 1483-1486 (1964). M. 251-268 (1996). J.. A. 15. 13. A. 7. Kamenya. J. Pebsworth. G.A. An extended graphical database (unrefereed) of this material is also available (http://chimp. Boesch. K. K. A. H. Bird Song: Themes and Variations. and S. Arcadi. The question of animal culture. Rev. Anthropol. Tomasello. F. Identification: A process of enculturation in the subhuman society of Macaca fuscata. R. Yamakoshi. Huffman. & Tamura. N. E. Spence. 26. Whiten. Kitahara-Frisch. 24. C. C. Galef. J. (Random House. Kasagula. Acad. A. Oxford. 11. Bull. J. & Galef.nature. Paquette. Comp. & Kluckhohn. Kakura. G. & Bard. R. 19. T. Bonner. D. R. The emergence of cultures among wild chimpanzees.W. 26. Nyundo. Mundinger. K. 17-30 (1992). & Ham. Isabiriye-Basuta. Gomez. P. The Evolution of Culture in Animals. M. G. W. Hillsdale NJ.. 1992). Matsuzawa. 22. M. Smart for the graphics of Fig. Acknowledgements. A. Comp. 107. McGrew. E. Whiten..) 175-187 (Clarendon Press. 27. Brit. 1994). H. C. B. or as paper copy from the London editorial office of Nature. in Social Learning in Animals: The Roots of Culture (eds. W. Sociobiol. Tinka. J. K. B. Language. P. Sugiyama. 14. C.. 1967). L. D. M. 1990). Science. B. We thank T. W. & Struhsaker. M. (University of Pittsburgh Press. M. T. 9.) 462-474 (University of Chicago Press. Custance. 1980). New York. 270-281 (1998). Lefebvre. 174-186 (1993).

then probe) Sponge push-pull (stick and sponge tool) Algae-scoop (scoop algae using wand) Ground-night-nest (night-nests on ground) Anvil prop (rock used to level anvil) Food-pound onto wood (smash food) Food-pound onto other (e.Table 1. stone hammer on wood anvil Nut-hammer. on ground) Pestle-pound (mash palm crown with petiole) Club (strike forcefully with stick) Termite-fish using leaf midrib Termite-fish using non-leaf materials materialsmater(materials) Ant-fish (probe used to extract ants) Ant-dip-wipe (manually wipe ants off wand) Ant-dip-single (mouth ants off stick) Fluid-dip (use of probe to extract fluids) Bee-probe (disable bees. other (e.mouth (rip parts off leaf. wood hammer on stone anvil Nut-hammer. fingers (rip leaf with fingers) Leaf-strip (rip leaves off stem. groom) Bs H + H C H C C --+ + + -+ -----e? --+ C (--) H C ---+ C -C + + -+ + C -----+ --C ---C -+ ----Taï C H C C C C C -----e e -----+ --+ e e? e C H C C C C H -H e e --C C C C H C H H -C + + -C H ---C H Go C C C C C C C --------e e + + + + -+ e + e C C ------H -C + C + C e? -C H -+ H C C + C --H H + + -Ma H C C + C C C + --e? ----e? e? --e? --+ e e? e --e -e --e? + --C --H ---H -e? -C + -C C + + ? ? -C Mk H C C e C C C ---e? ----e? e? -+ e? --e e e? e --e -e --e? -C C C --H + --H -e? ----C C --? ? -C Kib + C H C C H C -----e e -e e -e ---e e e? e e? e? e? e? e? e? e? e? + e e ---H ----+ --+ C C C H H H ---C Bd (--) H H C C C C -+ ---e? e? -e e -e? ----e + e H -e e e e e e? -e? e? e? --------H -+ C -+ C C --C --- B C D 6 . examined) Leaf-groom (intense ‘grooming’ of leaves) Leaf-clip.g. with mouth) Leaf-clip. court) Buttress-beat (drum on buttress of tree) Nasal probe (clear nasal passage with stick) Comb (stem used to comb through hair) Insect-pound (probe used to mash insect) Resin-pound (extract resin by pounding) Branch-hook (branch used to hook branch) Perforate (stout stick perforates termite nest) Dig (stick used as spade to dig termite nest) Brush-stick (probing stick with brush end) Seat-stick (stick protection from thorns) Stepping-stick (walking on sticks over thorns) Container (object used as container) Leaf-mop (leaves used to mop up insects) Leaf-wipe (food wiped from skull etc. stone) Nut-hammer. groom) Branch-shake (to attract attention. Variation in occurrence of behaviour patterns across long-term study sites site: A 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 Investigatory probe (probe and sniff) Play start (invite play holding stem in mouth) Drag branch (drag large branch in display) Leaf-sponge (leaf mass used as sponge) Branch-clasp (clasp branch above. wood hammer on wood anvil Nut-hammer.g. as threat) Leaf-squash (squash ecto-parasite on leaf) Leaf-inspect (inspect ecto-parasite on hand) Index-hit (squash ecto-parasite on arm) Hand-clasp (clasp arms overhead.) Leaf-brush (leaf used to brush away bees) Open and probe (perforate. flick with probe) Marrow-pick (pick bone marrow out) Lever open (stick used to enlarge entrance) Expel/stir (stick expels or stirs insects) Seat-vegetation (large leaves as seat) Fly-whisk (leafy stick used to fan flies) Self-tickle (tickle self using objects) Aimed-throw (throw object directionally) Leaf-napkin ((leaves used to clean body) Leaf-dab (leaf dabbed on wound. stone hammer on stone anvil Nut-hammer.

ecological explanation suspected. behaviours are listed so that adjacent categories share broad functions.R. Gombe. Taï Forest. grooming. J. patterns not achieving habitual frequencies at any site. C. pounding actions. Y.). forcing. for attention) Stem pull-through (pull stems noisily) Shrub-bend (squash stems underfoot) Rain dance (slow display at start of rain) + -C C H -- C -C --H H e? -+ -C C -+ H C C C ----C -e? -H -C --C -C H A. exploitation of leaf properties. patterns for which any absence can be explained by local ecological factors.S. patterns absent at no site. answer uncertain (see text for full definitions). miscellaneous exploitation of vegetation properties. observation period in years by September 1998. D.E. 56-59. T. with no ecological explanation. present. Go. Sites (with sub-species.). absent possibly because of inadequate observation. site director): Bs. 50-57. 15-17 and 22 are allocated to band B because they have been recorded at shorter-term sites (see Supplementary Information). 41-43. Branch din (behaviour 61) is allocated to band D because it is known to be customary at Lope. 18. release saplings to warn) Branch-slap (slap branch. Tanzania (schweinfurthii. fishing. customary. Gabon (C. Uganda (schweinfurthii.). Ivory Coast (verus. in Band D these are 27-35.W. 23. e?. . Mk. Mahale K-group (schweinfurthii.).).N. (-). Budongo Forest. C.G. 36-40.T.). 7 . Kib. C. Tanzania (schweinfurthii. 48 and 49. ?.60 61 62 63 64 65 Knuckle-knock (knock to attract attention) Branch din (bend. 11. T. Bossou. Ma. patterns customary or habitual at some sites yet absent at others.W. habitual. B. comfort behaviour. attention-getting. Mahale M-group.). see Supplementary Information.. H. For full definitions of all behaviours.G.absent.). 8. Ta. e. 23. 44 and 45. absent with ecological explanation.N. V. behaviours 13. Guinea (verus. Bd.B. 38. R. probing. 30. 46 and 47. Kibale Forest. Uganda (schweinfurthii. 60-64. +. To facilitate comparison.

The secondary Mahale site (K) is omitted. horizontal bar. habitual. clear. absent. monochrome icons. answer uncertain. (available for download as hi-res tiff) Colour icons. 8 . circular icons. absent with ecological explanation. question mark. customary. with clusters for westerly sites on the left of the array and clusters for easterly sites on the right.Figure 1 Distribution of behaviour patterns from band D in Table 1 across 6 African study sites. present. Behaviours are arranged in the 5 x 8 arrays to cluster those behaviours customary or habitual at each site.

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