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The first case of dental flossing by a Japanese macaque (Macaca fuscata): implications for the determinants of behavioral innovation and the constraints on social transmission

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Abstract

We report the first case of dental flossing behavior by a Japanese macaque. We used cross-sectional data to assess the presence of this novel tool-use behavior at the group-level. Although this behavior was performed frequently by a central middle-ranking middle-aged female during her grooming interactions, and appeared at least four years ago, it remained idiosyncratic to its innovator, and until now has not spread to other group members. We examined the factors that may have favored this innovation, including the environmental context, the individual characteristics of the innovator, and the structural and functional aspects of the behavior. Group size, kinship, and dominance are socio-demographic factors that are likely to limit the opportunities for any group member to observe the innovator, and thus constrain the diffusion of this potential candidate as a new behavioral tradition. This is one of the rare studies to document the spontaneous appearance of tool-use behavior in primates under natural conditions. Identifying the determinants of innovations and the constraints on their diffusion within social groups of non-human primates is of special interest to understanding cultural evolution.

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References

  • Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267

    Article  CAS  PubMed  Google Scholar 

  • Beck BB (1980) Animal tool behavior: the use and manufacture of tools by animals. Garland Press, New York

    Google Scholar 

  • Bonnie KE, de Waal FBM (2006) Affiliation promotes the transmission of a social custom: handclasp grooming among captive chimpanzees. Primates 47:27–34

    Article  PubMed  Google Scholar 

  • Cavalli-Sforza LL, Feldman MW (1981) Cultural transmission and evolution: a quantitative approach. Princeton University Press, Princeton

    Google Scholar 

  • de Vries H (1995) An improved test of linearity in dominance hierarchies containing unknown or tied relationships. Anim Behav 50:1375–1389

    Article  Google Scholar 

  • Fragaszy DM, Perry S (2003) Towards a biology of traditions. In: Fragaszy DM, Perry S (eds) The biology of traditions: models and evidence. Cambridge University Press, Cambridge, pp 1–32

    Google Scholar 

  • Gunst N (2008) The ontogeny of foraging skills in wild brown capuchins (Cebus apella): developmental perspective on the acquisition of ecological competence. PhD Dissertation, The University of Georgia, USA

  • Huffman MA (1984) Stone-play of Macaca fuscata in Arashiyama B troop: transmission of a non-adaptive behavior. J Hum Evol 13:725–735

    Article  Google Scholar 

  • Huffman MA (1991) History of Arashiyama Japanese macaques in Kyoto, Japan. In: Fedigan LM, Asquith PJ (eds) The monkeys of Arashiyama: thirty-five years of research in Japan and the West. SUNY Press, Albany, pp 21–53

    Google Scholar 

  • Huffman MA (1996) Acquisition of innovative cultural behaviors in non-human primates: a case study of stone handling, a socially transmitted behavior in Japanese macaques. In: Galef B, Heyes C Jr (eds) Social learning in animals: the roots of culture. Academic Press, Orlando, pp 267–289

    Chapter  Google Scholar 

  • Huffman MA (2007) Primate self-medication. In: Campbell CJ, Fuentes A, MacKinnon KC, Panger M, Bearder SK (eds) Primates in perspective. Oxford University Press, New York, pp 677–690

    Google Scholar 

  • Huffman MA, Hirata S (2003) Biological and ecological foundations of primate behavioral tradition. In: Fragaszy DM, Perry S (eds) The biology of tradition: models and evidence. Cambridge University Press, Cambridge, pp 267–296

    Google Scholar 

  • Huffman MA, Quiatt D (1986) Stone handling by Japanese macaques (Macaca fuscata): implications for tool use of stone. Primates 27:413–423

    Article  Google Scholar 

  • Ingmanson EJ (1996) Tool-using behavior in wild Pan paniscus: social and ecological considerations. In: Russon AE, Bard KA, Parker ST (eds) Reaching into thought: the minds of the great apes. Cambridge University Press, New York, pp 190–210

    Google Scholar 

  • Itani J, Nishimura A (1973) The study of infra-human culture in Japan. In: Menzel E (ed) Precultural primate behaviour. Karger, Basel, pp 26–50

    Google Scholar 

  • Kawai M (1965) Newly acquired pre-cultural behavior of a natural troop of Japanese monkeys on Koshima Island. Primates 6:1–30

    Article  Google Scholar 

  • Kawai M, Watanabe K, Mori A (1992) Pre-cultural behaviors observed in free-ranging Japanese monkeys on Koshima islet over the past 25 years. Primate Rep 32:143–153

    Google Scholar 

  • Koyama N (1991) Grooming relationships in the Arashiyama group of Japanese monkeys. In: Fedigan LM, Asquith PJ (eds) The monkeys of Arashiyama: thirty-five years of research in Japan and the West. State University of New York Press, Albany, pp 211–226

    Google Scholar 

  • Kummer H, Goodall J (1985) Conditions of innovative behaviour in primates. Philos Trans R Soc Lond B Biol Sci 308:203–214

    Article  Google Scholar 

  • Laland KN, Hoppitt W (2003) Do animals have culture? Evol Anthropol 12:150–159

    Article  Google Scholar 

  • Leca JB, Gunst N, Watanabe K, Huffman MA (2007a) A new case of fish-eating in Japanese macaques: implications for social constraints on the diffusion of feeding innovation. Am J Primatol 69:821–828

    Article  PubMed  Google Scholar 

  • Leca JB, Gunst N, Huffman MA (2007b) Age-related differences in the performance, diffusion, and maintenance of stone handling, a behavioral tradition in Japanese macaques. J Hum Evol 53:691–708

    Article  PubMed  Google Scholar 

  • Leca JB, Gunst N, Huffman MA (2007c) Japanese macaque cultures: inter- and intra-troop behavioural variability of stone handling patterns across 10 troops. Behaviour 144:251–281

    Article  Google Scholar 

  • Leca JB, Gunst N, Petit O (2007d) Social aspects of fur rubbing in Cebus capucinus and C. apella. Int J Primatol 28:801–817

    Article  Google Scholar 

  • Leca JB, Nahallage CAD, Gunst N, Huffman MA (2008a) Stone-throwing by Japanese macaques: form and functional aspects of a group-specific behavioral tradition. J Hum Evol 55:989–998

    Article  PubMed  Google Scholar 

  • Leca JB, Gunst N, Huffman MA (2008b) Variability of food provisioning regimes and stone handling tradition in Japanese macaques: a comparative study of ten troops. Am J Primatol 70:803–813

    Article  PubMed  Google Scholar 

  • Leca JB, Gunst N, Huffman MA (2008c) Of stones and monkeys: testing ecological constraints on stone handling, a behavioral tradition in Japanese macaques. Am J Phys Anthropol 135:233–244

    Article  PubMed  Google Scholar 

  • Lefebvre L, Giraldeau LA (1994) Cultural transmission in pigeons is affected by the number of tutors and bystanders present. Anim Behav 47:331–337

    Article  Google Scholar 

  • Lockman J (2000) A perception-action perspective on tool use development. Child Dev 71:137–144

    Article  CAS  PubMed  Google Scholar 

  • Malaivijitnond S, Lekprayoon C, Tandavanitj N, Panha S, Cheewatham C, Hamada Y (2007) Stone-tool usage by Thai long-tailed macaques (Macaca fascicularis). Am J Primatol 69:227–233

    Article  PubMed  Google Scholar 

  • Martin P, Bateson P (1993) Measuring behaviour: an introductory guide. Cambridge University Press, Cambridge

    Google Scholar 

  • Masataka N, Koda H, Urasopon N, Watanabe K (2009) Free-ranging macaque mothers exaggerate tool-using behavior when observed by offspring. PLoS ONE 4:e4768

    Article  PubMed  Google Scholar 

  • McGrew WC (1992) Chimpanzee material culture: Implications for human evolution. Cambridge University Press, Cambridge

    Google Scholar 

  • McGrew WC, Tutin CEG (1972) Chimpanzee dentistry. J Am Dent Assoc 85:1198–1204

    CAS  PubMed  Google Scholar 

  • McGrew WC, Tutin CEG (1973) Chimpanzee tool use in dental grooming. Nature 241:477–478

    Article  Google Scholar 

  • Nahallage CAD, Huffman MA (2007) Acquisition and development of stone handling behavior in infant Japanese macaques. Behaviour 144:1193–1215

    Google Scholar 

  • Nakamichi M, Shizawa Y (2003) Distribution of grooming among adult females in a large, free-ranging group of Japanese macaques. Int J Primatol 24:607–625

    Article  Google Scholar 

  • Nakamichi M, Kato E, Kojima Y, Itoigawa N (1998) Carrying and washing of grass roots by free-ranging Japanese macaques at Katsuyama. Folia Primatol 69:35–40

    Article  CAS  PubMed  Google Scholar 

  • Nishida T, Matsusaka T, McGrew WC (2009) Emergence, propagation or disappearance of novel behavioral patterns in the habituated chimpanzees of Mahale: a review. Primates 50:23–36

    Article  PubMed  Google Scholar 

  • Perry S, Panger M, Rose LM, Baker M, Gros-Louis J, Jack K, McKinnon KC, Manson J, Fedigan L, Pyle K (2003) Traditions in wild white-faced capuchins. In: Fragaszy DM, Perry S (eds) The biology of traditions: models and evidence. Cambridge University Press, Cambridge, pp 391–423

    Google Scholar 

  • Reader SM, Laland KN (2001) Primate innovation: sex, age and social rank differences. Int J Primatol 22:787–805

    Article  Google Scholar 

  • Reader S, Laland KN (2003) Animal innovation: an introduction. In: Reader S, Laland KN (eds) Animal innovation. Oxford University Press, Oxford, pp 3–35

    Google Scholar 

  • Russon AE, van Schaik CP, Kuncoro P, Ferisa A, Handayani DP, van Noordwijk MA (2009) Innovation and intelligence in orangutans. In: Wich SA, Utami Atmoko SS, Mitra Setia T (eds) Orangutans: geographic variation in behavioral ecology and conservation. Oxford University Press, New York, pp 279–298

    Google Scholar 

  • Sinha A (1997) Complex tool manufacture by a wild bonnet macaque. Folia Primatol 68:23–25

    Article  Google Scholar 

  • Sinha A (2005) Not in genes: phenotypic flexibility, behavioural traditions and cultural evolution in wild bonnet macaques. J Biosci 30:51–64

    Article  PubMed  Google Scholar 

  • Tanaka I (1998) Social diffusion of modified louse egg-handling techniques during grooming in free-ranging Japanese macaques. Anim Behav 56:1229–1236

    Article  PubMed  Google Scholar 

  • Tanaka I, Takefushi H (1993) Elimination of external parasites (lice) is the primary function of grooming in free-ranging Japanese macaques. Anthropol Sci 101:187–193

    Google Scholar 

  • van Schaik CP, Ancrenaz M, Borgen G, Galdikas B, Knott CD, Singleton I, Suzuki A, Utami SS, Merill M (2003) Orangutan cultures and the evolution of material culture. Science 299:102–105

    Article  PubMed  Google Scholar 

  • van Schaik CP, van Noordwijk MA, Wich SA (2006) Innovation in wild Bornean orangutans (Pongo pygmaeus wurmbii). Behaviour 143:839–876

    Article  Google Scholar 

  • Watanabe K (1989) Fish: a new addition to the diet of Koshima monkeys. Folia Primatol 52:124–131

    Article  CAS  PubMed  Google Scholar 

  • Watanabe K, Urasopon N, Malaivijitnond S (2007) Long-tailed macaques use human hair as dental floss. Am J Primatol 69:940–944

    Article  PubMed  Google Scholar 

  • Weinberg SM, Candland DK (1981) “Stone-grooming” in Macaca fuscata. Am J Primatol 1:465–468

    Article  Google Scholar 

  • Whiten A, Goodall J, McGrew WC, Nishida T, Reynolds V, Sugiyama Y, Tutin CEG, Wrangham RW, Boesch C (1999) Cultures in chimpanzees. Nature 399:682–685

    Article  CAS  PubMed  Google Scholar 

  • Zahavi A (1977) The testing of a bond. Anim Behav 25:246–247

    Article  Google Scholar 

Download references

Acknowledgments

The authors’ work was funded by a Grant-In-Aid for scientific research (no. 1907421 to M.A. Huffman) sponsored by Ministry of Education, Culture, Sports, Science and Technology, Japan, by a JSPS (Japan Society for the Promotion of Science) postdoctoral fellowship to J.-B. Leca (no. 07421), and by travel funds from the HOPE Project, a core-to-core program sponsored by JSPS. We thank S. Asaba, J. Hashiguchi, S. Kobatake, and S. Tamada from Iwatayama Monkey Park for helping us during the course of the study. For occasional assistance with data collection, we thank N. Tworoski. We thank P. Vasey for providing us with longitudinal data on the study group. We thank T. Nishida, W.C. McGrew, and two anonymous reviewers for fruitful comments on the manuscript.

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Correspondence to Jean-Baptiste Leca.

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Leca, JB., Gunst, N. & Huffman, M.A. The first case of dental flossing by a Japanese macaque (Macaca fuscata): implications for the determinants of behavioral innovation and the constraints on social transmission. Primates 51, 13–22 (2010). https://doi.org/10.1007/s10329-009-0159-9

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