Naturwissenschaften

, Volume 95, Issue 4, pp 325–331 | Cite as

Geophagy: soil consumption enhances the bioactivities of plants eaten by chimpanzees

  • Noémie Klein
  • François Fröhlich
  • Sabrina Krief
Original Paper

Abstract

Geophagy, the deliberate ingestion of soil, is a widespread practice among animals, including humans. Although some cases are well documented, motivations and consequences of this practice on the health status of the consumer remain unclear. In this paper, we focused our study on chimpanzees (Pan troglodytes schweinfurthii) of the Kibale National Park, Uganda, after observing they sometimes ingest soil shortly before or after consuming some plant parts such as leaves of Trichilia rubescens, which have in vitro anti-malarial properties. Chemical and mineralogical analyses of soil eaten by chimpanzees and soil used by the local healer to treat diarrhoea revealed similar composition, the clay mineralogy being dominated by kaolinite. We modelled the interaction between samples of the two types of soil and the leaves of T. rubescens in gastric and intestinal compartments and assayed the anti-malarial properties of these solutions. Results obtained for both soil samples are similar and support the hypothesis that soil enhances the pharmacological properties of the bio-available gastric fraction. The adaptive function of geophagy is likely to be multi-factorial. Nevertheless, the medical literature and most of occidental people usually consider geophagy in humans as an aberrant behaviour, symptomatic of metabolic dysfunction. Our results provide a new evidence to view geophagy as a practice for maintaining health, explaining its persistence through evolution.

Keywords

Geophagy Chimpanzee Human Plant secondary compounds Zoopharmacognosy 

Notes

Acknowledgements

We thank Makerere University Biological Field Station, Uganda Wildlife Authority and UNCST for permission to conduct this study in Kibale National Park, Uganda and Kibale Chimpanzee Project’s assistants, managers and directors, Richard Wrangham and Martin Muller for their collaboration in the field. We thank the Paleotropic team (IRD-Bondy) and especially S. Cacquineau and M. Garcia for X-ray and mineralogical analysis experiments and P. Grellier (MNHN), for anti-malarial bioassays. We are grateful to Bernard Bodo (MNHN), Marcel Hladik (MNHN) and Richard Wrangham (Harvard University) for their suggestions during the experiments and their comments on the manuscript. We deeply thank Tatyana Humle for useful comments to improve the manuscript. We are indebted to anonymous reviewers and the editorial board of the Journal who provided very helpful comments to improve this manuscript.

References

  1. Aufreiter S, Mahaney WC, Milner MW, Huffman MA, Hancock RGV, Wink M, Reich M (2001) Mineralogical and chemical interactions of soils eaten by chimpanzees of the Mahale mountains and Gombe stream National Parks, Tanzania. J Chem Ecol 27:285–311PubMedCrossRefGoogle Scholar
  2. Cogswell FB (2000) Malaria and piroplasms of non-human primates. In: Bowman DD (ed) Companion and exotic animal parasitology. International Veterinary Information Service, Ithaca, NY (A0304.0600, www.ivis.org)Google Scholar
  3. Desjardins RE, Canfield CJ, Haynes JD, Chulay JD (1979) Quantitative assessment of antimalarial activity in vitro by a semiautomated microdilution technique. Antimicrob Agents Chemother 16:710–718PubMedGoogle Scholar
  4. Farmer VC (1974) The infrared spectra of minerals. Monograph 4. Mineralogical Society, LondonGoogle Scholar
  5. Fröhlich F, Gendron-Badou A (2002) La spectroscopie infrarouge, un outil polyvalent. In: Miskovsky JC (ed) Géologie de la préhistoire. Géopré, Presses universitaires de Perpignan, PerpignanGoogle Scholar
  6. Geissler WP (2000) The significance of earth-eating: social and cultural aspects of geophagy among Luo children. Africa 70:653–682CrossRefGoogle Scholar
  7. Geissler PW, Princeb RJ, Levenec M, Podad C, Beckerlegc SE, Mutemid W, Shulmand CE (1999) Perceptions of soil-eating and anaemia among pregnant women on the Kenyan coast. Soc Sci Med 48(8):1069–1079PubMedCrossRefGoogle Scholar
  8. Gilardi JD, Duffey SS, Munn CA, Tell LA (1999) Biochemical functions of geophagy in parrots: detoxification of dietary toxins and cytoprotective effects. J Chem Ecol 25:897–922CrossRefGoogle Scholar
  9. Hladik CM, Gueguen L (1974) Géophagie et nutrition minérale chez les Primates sauvages. Compte Rendu de l’Académie des Sciences 279:1393–1396Google Scholar
  10. Hooda PS, Henry CJK, Seyoum TA, Armstrong LDM, Fowler MB (2004) The potential impact of soil ingestion on human mineral nutrition. Sci Total Environ 333:75–87PubMedCrossRefGoogle Scholar
  11. Houston DC, Gilardi JD, Hall AJ (2001) Soil consumption by elephants might help to minimize the toxic effects of plant secondary compounds in forest browse. Mamm Rev 31:249–254CrossRefGoogle Scholar
  12. Johns T (1986) Detoxification function of geophagy and domestication of the potato. J Chem Ecol 12:635–646CrossRefGoogle Scholar
  13. Johns T (1996) The origins of human diet and medicine. University of Arizona Press, Tucson, AZGoogle Scholar
  14. Johns T, Duquette M (1991) Detoxification and mineral supplementation as functions of geophagy. Am J Clin Nutr 53:448–456PubMedGoogle Scholar
  15. Ketch LA, Malloch D, Mahaney WC, Huffman MA (2001) Comparative microbial analysis and clay mineralogy of soils eaten by chimpanzees (Pan troglodytes schweinfurthii) in Tanzania. Soil Biol Biochem 33:199–203CrossRefGoogle Scholar
  16. Krief S, Martin M-T, Grellier P, Kasenene J, Sevenet T (2004) Novel antimalarial compounds isolated in a survey of self-medicative behavior of wild chimpanzees in Uganda. Antimicrob Agents Chemother 48:3196–3199PubMedCrossRefGoogle Scholar
  17. Krief S, Huffman MA, Sevenet T, Hladik CM, Grellier P, Loiseau PM, Wrangham RW (2006) Bioactive properties of plants species ingested by chimpanzees (Pan troglodytes schweinfurthii) in the Kibale National Park, Uganda. Am J Primatol 68:51–71PubMedCrossRefGoogle Scholar
  18. Krishnamani R, Mahaney WC (2000) Geophagy among primates: adaptive significance and ecological consequences. Anim Behav 59:899–915PubMedCrossRefGoogle Scholar
  19. Lambert JE (1998) Primate digestion: interactions among anatomy, physiology, and feeding ecology. Evol Anthropol 7:8–20CrossRefGoogle Scholar
  20. Laufer B (1930) Geophagy. Publication 280, Anthropological Series, vol. 18. Field Museum of Natural History, Chicago, pp 99–198Google Scholar
  21. Luoba AI (2005) Earth-eating and reinfection with intestinal helminths among pregnant and lactating women in Western Kenya. Trop Med Int Health 10:220–227PubMedCrossRefGoogle Scholar
  22. Mahaney WC, Hancock RGV, Inoue M (1993) Geochemistry and clay mineralogy of soils eaten by Japanese macaques. Primates 34:85–91CrossRefGoogle Scholar
  23. Mahaney WC, Aufreiter S, Hancock RGV (1995) Mountain gorilla geophagy: possible strategy for dealing with effects of dietary changes. Int J Primatol 16:475–488CrossRefGoogle Scholar
  24. Mahaney WC, Milner MW, Sanmugadas K, Hancock RGV, Aufreiter S, Wrangham RW, Pier HW (1997) Analysis of geophagy soils in Kibale Forest, Uganda. Primates 38:159–176CrossRefGoogle Scholar
  25. Mahaney WC, Milner MW, Aufreiter S, Hancock RGV, Wrangham R, Campbell S (2005) Soils consumed by chimpanzees of the Kanyawara community in the Kibale Forest, Uganda. Int J Primatol 26:1375–1398CrossRefGoogle Scholar
  26. Mnason T, Reynold V, Huffman MA, Pebsworth P, Mahaney WC, Milner M, Waddell A, Dirszowsky R, Hancock GV (2006) Geophagy in chimpanzees (Pan troglodytes schweinfurthii) of the Budongo forest reserve, Uganda. In: Notman H, Reynolds V, Paterson J (eds) Primates of Western Uganda. Springer, New York, pp 135–152Google Scholar
  27. Moore DM, Reynolds RC (1989) X-ray diffraction and the identification and analysis of clay minerals. Oxford University Press, OxfordGoogle Scholar
  28. National Research Council (1978) Nutrient requirements of non-human primates. National Academy, Washington, DCGoogle Scholar
  29. Nicolosi RJ, Hunt RD (1979) Dietary allowances for nutrients in nonhuman primates. In: Hayes KC (ed) Primates in nutritional research. Academic, New YorkGoogle Scholar
  30. Oates JF (1978) Water-plant and soil consumption by guereza monkeys (Colobus guereza): a relationship with mineral and toxins in the diet? Biotropica 10:241–253CrossRefGoogle Scholar
  31. Parkhurst RM, Thomas DW, Skinner WA, Cary LW (1973) Molluscicidal saponins of Phytolacca dodecandra: oleanoglycotoxin-A. Phytochemistry 12:1437–1442CrossRefGoogle Scholar
  32. Pharmacopée Européenne (2005) Direction Européenne de la Qualité du Médicament, 5th edn. Conseil de l’Europe, Strasbourg, FranceGoogle Scholar
  33. Reid RM (1992) Cultural and medical perspectives on geophagia. Med Anthropol 33:337–351Google Scholar
  34. Rode KD, Chapman CA, Chapman LJ, Mcdowell LR (2003) Mineral resource availability and consumption by colobus in Kibale National Park, Uganda. Int J Primatol 24:541–573CrossRefGoogle Scholar
  35. The United States Pharmacopeia-National Formulary (USP-NF) (2004) The Official compendia standards, 27th revision. Port City Press, BaltimoreGoogle Scholar
  36. Toft JD (1986) The pathoparasitology of non-human primates: a review. In: Benirshke K (ed) Primates: the road to self-sustaining population. Springer, New York, pp 571–679Google Scholar
  37. Vermeer DE (1971) Geophagy among the Ewe of Ghana. Ethnology 10:56–72CrossRefGoogle Scholar
  38. Vermeer DE, Ferrell RE Jr (1985) Nigerian geophagical clay: a traditional anti-diarrhoeal pharmaceutical. Science 227:634–636PubMedCrossRefGoogle Scholar
  39. Villalba J, Provenza FD, Shaw R (2006) Sheep self-medicate when challenged with illness-induced food. Anim Behav 71:1131–1139CrossRefGoogle Scholar
  40. Wakibara JV, Huffman MA, Wink M, Reich S, Aufreiter S, Hancock RGV, Sodhi R, Mahaney WC, Russel S (2001) The adaptive significance of geophagy for Japanese macaques (Macaca fuscata) at Arashiyama, Japan. Int J Primatol 22(3):495–520CrossRefGoogle Scholar
  41. Wiley AS, Katz SH (1998) Geophagy in pregnancy: a test of hypothesis. Curr Anthropol 39:532–545CrossRefGoogle Scholar
  42. Ziegler JL (1997) Geophagy: a vestige of palaeonutrition? Trop Med Int Health 2:609–611PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Noémie Klein
    • 1
  • François Fröhlich
    • 2
  • Sabrina Krief
    • 1
  1. 1.Département Hommes, Natures, Sociétés, Eco-anthropologie et Ethnobiologie, USM 0104Muséum National d’Histoire NaturelleParis Cedex 5France
  2. 2.Département de Préhistoire, CNRS UMR 5198, Centre de Spectroscopie Infrarouge, Musée de l’HommeMuséum National d’Histoire NaturelleParisFrance

Personalised recommendations