Abstract
Researchers have described apparently self-medicative behaviors for a variety of nonhuman species including birds and primates. Wild chimpanzees, bonobos, and gorillas have been observed to swallow rough leaves without chewing, a behavior proposed to be self-medicative and to aid control of intestinal parasites. Researchers have hypothesized that the presence of hairs on the leaf surface elicits the behavior. We investigated the acquisition and the underlying mechanisms of leaf swallowing. We provided 42 captive great apes (24 chimpanzees, six bonobos, six gorillas, and six orangutans) with both rough-surfaced and hairless plants. None of the subjects had previously been observed to engage in leaf swallowing behavior and were therefore assumed naïve. Two chimpanzees and one bonobo swallowed rough-surfaced leaves spontaneously without chewing them. In a social setup six more chimpanzees acquired the behavior. None of the gorillas or orangutans showed leaf swallowing. Because this behavior occurred in naïve individuals, we conclude that it is part of the behavioral repertoire of chimpanzees and bonobos. Social learning is thus not strictly required for the acquisition of leaf swallowing, but it may still facilitate its expression. The fact that apes always chewed leaves of hairless control plants before swallowing, i.e., normal feeding behavior, indicates that the surface structure of leaves is indeed a determinant for initiating leaf swallowing in apes where it occurs.
Similar content being viewed by others
References
Baker, M. (1996). Fur rubbing: use of medicinal plants by capuchin monkeys (Cebus capucinus). American Journal of Primatology, 38(3), 263–270.
Boesch, C. (1995). Innovation in wild chimpanzees (Pan troglodytes). International Journal of Primatology, 16(2), 1–16.
Clark, L., & Mason, J. R. (1985). Use of nest material as insecticidal and anti-pathogenic agents by the European starling. Oecologia, 67, 169–176.
Dupain, J., van Elsacker, L., Nell, C., Garcia, P., Ponce, F., & Huffman, M. A. (2002). New evidence for leaf swallowing and Oesophagostomum infection in bonobos (Pan paniscus). International Journal of Primatology, 23(5), 1053–1062.
Fowler, A., Koutsioni, Y., & Sommer, V. (2007). Leaf-swallowing in Nigerian chimpanzees: evidence for assumed self-medication. Primates, 48(1), 73–76.
Hart, B. L. (2005). The evolution of herbal medicine: behavioural perspectives. Animal Behaviour, 70(5), 975–989.
Huffman, M. A. (1997). Current evidence for self-medication in primates: a multidisciplinary perspective. American Journal of Physical Anthropology, 104(S25), 171–200.
Huffman, M. A. (2001). Self-medicative behavior in the African great apes: an evolutionary perspective into the origins of human traditional medicine. Bioscience, 51(8), 651–661.
Huffman, M. A. (2003). Animal self-medication and ethno-medicine: exploration and exploitation of the medicinal properties of plants. Proceedings of the Nutrition Society, 62, 371–381.
Huffman, M. A., & Caton, J. M. (2001). Self-induced increase of gut motility and the control of parasitic infections in wild chimpanzees. International Journal of Primatology, 22(3), 329–346.
Huffman, M. A., & Hirata, S. (2003). Biological and ecological foundations of primate behavioral tradition. In D. M. Fragaszy & S. Perry (Eds.), The biology of traditions (pp. 267–296). Cambridge: Cambridge University Press.
Huffman, M. A., & Hirata, S. (2004). An experimental study of leaf swallowing in captive chimpanzees: insights into the origin of a self-medicative behavior and the role of social learning. Primates, 45(2), 113–118.
Huffman, M. A., & Wrangham, R. W. (1994). Diversity of medicinal plant use by chimpanzees in the wild. In R. W. Wrangham, W. C. McGrew, F. B. M. De Waal, & P. G. Heltne (Eds.), Chimpanzee cultures (1st ed., pp. 129–148). Cambridge: Harvard University Press.
Huffman, M. A., Page, J., Sukhdeo, M., Gotoh, S., Kalunde, M., Chandrasiri, T., et al. (1996). Leaf-swallowing by chimpanzees: a behavioral adaptation for the control of strongyle nematode infections. International Journal of Primatology, 17(4), 475–503.
Huffman, M. A., Gotoh, S., Turner, L., Hamai, M., & Yoshida, K. (1997). Seasonal trends in intestinal nematode infection and medicinal plant use among chimpanzees in the Mahale Mountains, Tanzania. Primates, 38(2), 111–125.
Huffman, M., Spiezio, C., Sgaravatti, A., & Leca, J.-B. (2010). Leaf swallowing behavior in chimpanzees (Pan troglodytes): biased learning and the emergence of group level cultural differences. Animal Cognition, 13(6), 871–880.
Kawabata, M., & Nishida, T. (1991). A preliminary note on the intestinal parasites of wild chimpanzees in the Mahale Mountains, Tanzania. Primates, 32(2), 275–278.
Krief, S., Wrangham, R. W., & Lestel, D. (2006). Diversity of items of low nutritional value ingested by chimpanzees from Kanyawara, Kibale National Park, Uganda: an example of the etho-ethnology of chimpanzees. Social Science Information, 45(2), 227–263.
Messner, E., & Wrangham, R. (1996). In vitro testing of the biological activity of Rubia cordifolia leaves on primate Strongyloides species. Primates, 37(1), 105–108.
Morrogh-Bernard, H. C. (2008). Fur-rubbing as a form of self-medication in Pongo pygmaeus. International Journal of Primatology, 29(4), 1059–1064.
Newton, P. N., & Nishida, T. (1990). Possible buccal administration of herbal drugs by wild chimpanzees, Pan troglodytes. Animal Behaviour, 39(4), 798–801.
Nishida, T., Wrangham, R. W., Goodall, J., & Uehara, S. (1983). Local differences in plant-feeding habits of chimpanzees between the Mahale Mountains and Gombe National Park, Tanzania. Journal of Human Evolution, 12(5), 467–480.
Nishida, T., Kano, T., Goodall, J., McGrew, W. C., & Nakamura, M. (1999). Ethogram and ethnography of Mahale chimpanzees. Anthropological Science, 107(2), 141–188.
Ohigashi, H., Takagaki, T., Koshimizu, K., Watanabe, K., Kaji, M., Hoshino, J., et al. (1991). Biological activities of plant extracts from tropical Africa. African Study Monographs, 12(4), 201–210.
Page, J. E., Balza, F., Nishida, T., & Towers, G. H. N. (1992). Biologically active diterpenes from Aspilia mossambicensis, a chimpanzee medicinal plant. Phytochemistry, 31(10), 3437–3439.
Page, J. E., Huffman, M. A., Smith, V., & Towers, G. H. N. (1997). Chemical basis for Aspilia leaf-swallowing by chimpanzees: a reanalysis. Journal of Chemical Ecology, 23(9), 2211–2226.
Tennie, C., & Hedwig, D. (2009). How latent solution experiments can help to study differences between human culture and primate traditions. In E. Potocki & J. Krasiński (Eds.), Primatology: Theories, methods and research (pp. 95–112). New York: Nova Publishers.
Tennie, C., Call, J., & Tomasello, M. (2009). Ratcheting up the ratchet: on the evolution of cumulative culture. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 364(1528), 2405–2415.
Whiten, A., & Ham, R. (1992). On the nature and evolution of imitation in the animal kingdom reappraisal of a century of research. Advances in the Study of Behavior, 21, 239–283.
Whiten, A., Horner, V., Litchfield, C. A., & Marshall-Pescini, S. (2004). How do apes ape? Learning & Behavior, 32(1), 36–52.
Wrangham, R. W. (1977). Feeding behaviour of chimpanzees in Gombe National Park, Tanzania. In T. H. Clutton-Brock (Ed.), Primate ecology: Studies of feeding and ranging behaviour in lemurs, monkeys and apes (pp. 503–538). New York: Academic Press.
Wrangham, R. W. (1995). Relationship of chimpanzee leaf-swallowing to a tapeworm infection. American Journal of Primatology, 37(4), 297–303.
Wrangham, R. W., & Goodall, J. (1989). Chimpanzee use of medicinal leaves. In P. G. Heltne & L. A. Marquardt (Eds.), Understanding chimpanzees (pp. 22–37). Chicago: Chicago Academy of Science.
Wrangham, R., & Nishida, T. (1983). Aspilia spp. leaves: a puzzle in the feeding behavior of wild chimpanzees. Primates, 24(2), 276–282.
Yamagiwa, J., Basabose, A. K., Kaleme, K., & Yumoto, T. (2005). Diet of Grauer’s gorillas in the Montane Forest of Kahuzi, Democratic Republic of Congo. International Journal of Primatology, 26(6), 1345–1373.
Acknowledgments
We thank the Max Planck Society, the Department of Developmental and Comparative Psychology, and the Department of Primatology of the Max-Planck-Institute for Evolutionary Anthropology. We thank Joanna Setchell and three anonymous reviewers for their helpful comments. We also thank the staff of the Leipzig Zoo and Wolfgang Köhler Primate Research Center, especially the keepers, Charlotte Rahn, Daniel Hanus, Johannes Großmann, Matthias Allritz, Julia Löpelt, and Andreas Bernhard. Josefine Kalbitz, Hagen Knofe, and Julia Watzek were additional experimenters and we thank them for their support. Heike Heklau, Martin Freiberg, Ulf Schilling, and Helmut Eißner helped with selection and supply of plants. We are grateful for permission to collect plant parts in the city area of Leipzig and Halle/Saale, Germany. We thank Siobhan Loftus for reliability coding. We also thank Barbara Fruth and Gottfried Hohmann for their continued support during the study.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Online Resource 1
(JPEG 178 kb)
Appendix
Appendix
Rights and permissions
About this article
Cite this article
Menzel, C., Fowler, A., Tennie, C. et al. Leaf Surface Roughness Elicits Leaf Swallowing Behavior in Captive Chimpanzees (Pan troglodytes) and Bonobos (P. paniscus), but not in Gorillas (Gorilla gorilla) or Orangutans (Pongo abelii). Int J Primatol 34, 533–553 (2013). https://doi.org/10.1007/s10764-013-9679-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10764-013-9679-7