Advertisement

Environmental Geochemistry and Health

, Volume 41, Issue 6, pp 2911–2927 | Cite as

Geophagy among East African Chimpanzees: consumed soils provide protection from plant secondary compounds and bioavailable iron

  • Paula A. PebsworthEmail author
  • Stephen Hillier
  • Renate Wendler
  • Ray Glahn
  • Chieu Anh Kim Ta
  • John T. Arnason
  • Sera L. Young
Original Paper

Abstract

Geophagy, the intentional consumption of earth materials, has been recorded in humans and other animals. It has been hypothesized that geophagy is an adaptive behavior, and that clay minerals commonly found in eaten soil can provide protection from toxins and/or supplement micronutrients. To test these hypotheses, we monitored chimpanzee geophagy using camera traps in four permanent sites at the Budongo Forest Reserve, Uganda, from October 2015–October 2016. We also collected plants, and soil chimpanzees were observed eating. We analyzed 10 plant and 45 soil samples to characterize geophagic behavior and geophagic soil and determine (1) whether micronutrients are available from the soil under physiological conditions and if iron is bioavailable, (2) the concentration of phenolic compounds in plants, and (3) if consumed soils are able to adsorb these phenolics. Chimpanzees ate soil and drank clay-infused water containing 1:1 and 2:1 clay minerals and > 30% sand. Under physiological conditions, the soils released calcium, iron, and magnesium. In vitro Caco-2 experiments found that five times more iron was bioavailable from three of four soil samples found at the base of trees. Plant samples contained approximately 60 μg/mg gallic acid equivalent. Soil from one site contained 10 times more 2:1 clay minerals, which were better at removing phenolics present in their diet. We suggest that geophagy may provide bioavailable iron and protection from phenolics, which have increased in plants over the last 20 years. In summary, geophagy within the Sonso community is multifunctional and may be an important self-medicative behavior.

Keywords

Soil eating Detoxification Micronutrients Primates Simulated digestion 

Notes

Acknowledgements

PAP thanks the Budongo Conservation Field Station staff, field assistants, and in particular Vernon Reynolds, Fred Babweteera, Klaus Zuberbühler, Catherine Hobaiter, Jakob Villioth, Geoffrey Muhanguzi, Geresomu Muhumuza, Jacob Alio, and Michael Jurua for field and data assistance. We also thank the Royal Zoological Society of Scotland who provided core funding and the Uganda Wildlife Authority and the Ugandan Council of Science and Technology for the opportunity of conduct research in Uganda. We thank David Emerson, Rui Liu, Nia Gray, Mary Bodis, Pei–Pei Chang, Nimal De Silva, Jean Bjornson, Christopher Boddy, and Joseph Ndawula for assistance with laboratory analyses. We further thank Thad Bartlett, Josh Miller, Chris and Diane West for manuscript assistance and logistical support. SH and RW acknowledge support of the Scottish Government’s Rural and Environment Science and Analytical Services Division (RESAS). JTA acknowledges support from the Canadian Natural Science and Engineering Research Council. Finally, we thank Environmental Geochemistry and Health, Professor William Mahaney, and two anonymous reviewers for their valuable advice and helpful comments on a previous version of this article.

References

  1. Abrahams, P. W. (1997). Geophagy (soil consumption) and iron supplementation in Uganda. Tropical Medicine & International Health: TM & IH,2(7), 617–623.CrossRefGoogle Scholar
  2. Ampeng, A., Shukor, M. N., Sahibin, A. R., Idris, W. M. R., Ahmad, S., Mohammad, H., et al. (2016). Patterns of mineral lick use by Northwest Bornean orangutans (Pongo pygmaeus pygmaeus) in the Lanjak Entimau Wildlife Sanctuary, Sarawak, Malaysia. European Journal of Wildlife Research,62(1), 147–150.  https://doi.org/10.1007/s10344-015-0983-8.CrossRefGoogle Scholar
  3. Ariza-Nieto, M., Blair, M. W., Welch, R. M., & Glahn, R. P. (2007). Screening of iron bioavailability patterns in eight bean (Phaseolus vulgaris L.) genotypes using the Caco-2 cell in vitro model. Journal of Agricultural and Food Chemistry, 55(19), 7950–7956.  https://doi.org/10.1021/jf070023y.CrossRefGoogle Scholar
  4. Aufreiter, S., Mahaney, W. C., Milner, M. W., Huffman, M. A., Hancock, R. G., Wink, M., et al. (2001). Mineralogical and chemical interactions of soils eaten by chimpanzees of the Mahale Mountains and Gombe Stream National Parks, Tanzania. Journal of Chemical Ecology,27(2), 285–311.CrossRefGoogle Scholar
  5. Basabose, A. K. (2002). Diet composition of chimpanzees inhabiting the Montane forest of Kahuzi, Democratic Republic of Congo. American Journal of Primatology,58(1), 1–21.  https://doi.org/10.1002/ajp.10049.CrossRefGoogle Scholar
  6. Bicca-Marques, J. C., & Calegaro-Marques, C. (1994). A case of geophagy in the black howling monkey Alouatta caraya. Neotropical Primates,2, 7–9.Google Scholar
  7. Bouyoucos, G. J. (1962). Hydrometer method improved for making particle size analysis of soils. Agronomy Journal,54, 464–465.CrossRefGoogle Scholar
  8. DeGabriel, J. L., Moore, B. D., Foley, W. J., & Johnson, C. N. (2009). The effects of plant defensive chemistry on nutrient availability predict reproductive success in a mammal. Ecology,90(3), 711–719.CrossRefGoogle Scholar
  9. Dominy, N. J., Davoust, E., & Minekus, M. (2004). Adaptive function of soil consumption: An in vitro study modeling the human stomach and small intestine. The Journal of Experimental Biology,207(Pt 2), 319–324.CrossRefGoogle Scholar
  10. Eggeling, W. J. (1947). Observations on the ecology of the Budongo Rain Forest, Uganda. The Journal of Ecology,34(1), 20.  https://doi.org/10.2307/2256760.CrossRefGoogle Scholar
  11. Engle-Stone, R., Yeung, A., Welch, R., & Glahn, R. (2005). Meat and ascorbic acid can promote Fe availability from Fe-phytate but not from Fe-tannic acid complexes. Journal of Agricultural and Food Chemistry,53(26), 10276–10284.  https://doi.org/10.1021/jf0518453.CrossRefGoogle Scholar
  12. Farmer, V. C., Russell, J. D., & Smith, B. F. L. (1983). Extraction of inorganic forms of translocated Al, Fe and Si from a podzol Bs horizon. Journal of Soil Science,34(3), 571–576.  https://doi.org/10.1111/j.1365-2389.1983.tb01056.x.CrossRefGoogle Scholar
  13. Fawcett, K. A. (2000). Female relationships and food availability in a forest community of chimpanzees (Dissertation). Edinburgh: University of Edinburgh.Google Scholar
  14. Gašperšič, M., & Pruetz, J. D. (2011). Chimpanzees in Bandafassi Arrondissement, southeastern Senegal: Field surveys as a basis for the sustainable community-based conservation. Pan-Africanism News,18, 23–25.CrossRefGoogle Scholar
  15. Gilardi, J., Duffey, S., Munn, C., & Tell, L. (1999). Biochemical functions of geophagy in parrots: Detoxification of dietary toxins and cytoprotective effects. Journal of Chemical Ecology,25(4), 897–922.  https://doi.org/10.1023/A:1020857120217.CrossRefGoogle Scholar
  16. Glahn, R. P., Gangloff, M. B., van Campen, D. R., Miller, D. D., Wien, E. M., & Norvell, W. A. (1995). Bathophenanthrolene disulfonic acid and sodium dithionite effectively remove surface-bound iron from Caco-2 cell monolayers. The Journal of Nutrition,125(7), 1833–1840.  https://doi.org/10.1093/jn/125.7.1833.CrossRefGoogle Scholar
  17. Glahn, R. P., Lee, O. A., Yeung, A., Goldman, M. I., & Miller, D. D. (1998). Caco-2 cell ferritin formation predicts nonradiolabeled food iron availability in an in vitro digestion/Caco-2 cell culture model. The Journal of Nutrition,128(9), 1555–1561.CrossRefGoogle Scholar
  18. Glahn, R. P., Wortley, G. M., South, P. K., & Miller, D. D. (2002). Inhibition of iron uptake by phytic acid, tannic acid, and ZnCl2: Studies using an in vitro digestion/Caco-2 cell model. Journal of Agricultural and Food Chemistry,50(2), 390–395.  https://doi.org/10.1021/jf011046u.CrossRefGoogle Scholar
  19. González, R., de Medina, F. S., Martínez-Augustin, O., Nieto, A., Gálvez, J., Risco, S., et al. (2004). Anti-inflammatory effect of diosmectite in hapten-induced colitis in the rat. British Journal of Pharmacology,141(6), 951–960.  https://doi.org/10.1038/sj.bjp.0705710.CrossRefGoogle Scholar
  20. Goodall, J. (1963). Feeding behaviour of wild chimpanzees: A preliminary report. In Symposium of the zoological society of London (Vol. 10, pp. 39–47).Google Scholar
  21. Gruber, T., Muller, M. N., Strimling, P., Wrangham, R., & Zuberbühler, K. (2009). Wild chimpanzees rely on cultural knowledge to solve an experimental honey acquisition task. Current Biology,19(21), 1806–1810.  https://doi.org/10.1016/j.cub.2009.08.060.CrossRefGoogle Scholar
  22. Gurian, E., O’Neil, P. L., & Price, C. S. (1992). Geophagy and its relation to tannin ingestion in rhesus macaques (Macaca mulatta). AAZPA Regional Proceedings,59, 152–159.Google Scholar
  23. Hart, J. J., Tako, E., & Glahn, R. P. (2017). Characterization of polyphenol effects on inhibition and promotion of iron uptake by Caco-2 cells. Journal of Agricultural and Food Chemistry,65(16), 3285–3294.  https://doi.org/10.1021/acs.jafc.6b05755.CrossRefGoogle Scholar
  24. Hillier, S. (1999). Use of an air brush to spray dry samples for X-ray powder diffraction. Clay Minerals,34(1), 127–135.CrossRefGoogle Scholar
  25. Hladik, C. M. (1977). A comparative study of the feeding strategies of two sympatric species of leaf monkeys: Presbytis senex and Presbytis entellus. In T. H. Clutton-Brock (Ed.), Primate ecology: Studies of feeding and ranging behaviour in lemurs, monkeys and apes (pp. 324–353). London: Academic Press.Google Scholar
  26. Johns, T. (1986). Detoxification function of geophagy and domestication of the potato. Journal of Chemical Ecology,12(3), 635–646.  https://doi.org/10.1007/BF01012098.CrossRefGoogle Scholar
  27. Kano, T., & Mulavwa, M. (1984). Feeding ecology of the pygmy chimpanzees (Pan paniscus) of Wamba. In R. L. Susman (Ed.), The Pygmy Chimpanzee: Evolutionary biology and behavior (pp. 233–274). Boston: Springer.  https://doi.org/10.1007/978-1-4757-0082-4_10.CrossRefGoogle Scholar
  28. Ketch, L. A., Malloch, D., Mahaney, W. C., & Huffman, M. A. (2001). Comparative microbial analysis and clay mineralogy of soils eaten by chimpanzees (Pan troglodytes schweinfurthii) in Tanzania. Soil Biology and Biochemistry,33(2), 199–203.CrossRefGoogle Scholar
  29. Klein, N., Fröhlich, F., & Krief, S. (2008). Geophagy: soil consumption enhances the bioactivities of plants eaten by chimpanzees. Naturwissenschaften,95(4), 325–331.  https://doi.org/10.1007/s00114-007-0333-0.CrossRefGoogle Scholar
  30. Knezevich, M. (1998). Geophagy as a therapeutic mediator of endoparasitism in a free-ranging group of rhesus macaques (Macaca mulatta). American Journal of Primatology,44(1), 71–82.  https://doi.org/10.1002/(SICI)1098-2345(1998)44:1%3c71:AID-AJP6%3e3.0.CO;2-U.CrossRefGoogle Scholar
  31. Kobayashi, T., Nozoye, T., & Nishizawa, N. K. (2018). Iron transport and its regulation in plants. Free Radical Biology and Medicine,133, 11.  https://doi.org/10.1016/j.freeradbiomed.2018.10.439.CrossRefGoogle Scholar
  32. Kreulen, D. A. (1985). Lick use by large herbivores: A review of benefits and banes of soil consumption. Mammal Review,15(3), 107–123.CrossRefGoogle Scholar
  33. Mahaney, W. C., Hancock, R. G. V., Aufreiter, S., & Huffman, M. A. (1996). Geochemistry and clay mineralogy of termite mound soil and the role of geophagy in chimpanzees of the Mahale Mountains, Tanzania. Primates,37(2), 121–134.  https://doi.org/10.1007/BF02381400.CrossRefGoogle Scholar
  34. Mahaney, W. C., & Krishnamani, R. (2003). Understanding geophagy in animals: Standard procedures for sampling soils. Journal of Chemical Ecology,29(7), 1503–1523.CrossRefGoogle Scholar
  35. Mahaney, W. C., Milner, M. W., Aufreiter, S., Hancock, R. G. V., Wrangham, R., & Campbell, S. (2005). Soils consumed by chimpanzees of the Kanyawara community in the Kibale Forest, Uganda. International Journal of Primatology,26(6), 1375–1398.  https://doi.org/10.1007/s10764-005-8857-7.CrossRefGoogle Scholar
  36. Mahaney, W. C., Milner, M. W., Sanmugadas, K., Hancock, R. G. V., Aufreiter, S., Wrangham, R., et al. (1997). Analysis of geophagy soils in Kibale Forest, Uganda. Primates,38(2), 159–176.  https://doi.org/10.1007/BF02382006.CrossRefGoogle Scholar
  37. Marsh, L. K., Chapman, C. A., Arroyo-Rodríguez, V., Cobden, A. K., Dunn, J. C., Gabriel, D., et al. (2013). Primates in fragments 10 years later: Once and future goals. In L. K. Marsh & C. A. Chapman (Eds.), Primates in fragments (pp. 505–525). New York: Springer.  https://doi.org/10.1007/978-1-4614-8839-2_34. Accessed 9 September 2015.CrossRefGoogle Scholar
  38. Miller, J. D., Collins, S., Krumdieck, N. R., Wekesa, P., Onono, M., & Young, S. L. (2016). Pica is associated with lower hemoglobin concentration in a cohort of pregnant Kenyan women of mixed HIV status. The FASEB Journal,30(1_supplement), 1149.Google Scholar
  39. Newton-Fisher, N. E. (2003). The home range of the Sonso community of chimpanzees from the Budongo Forest, Uganda. African Journal of Ecology,41(2), 150–156.  https://doi.org/10.1046/j.1365-2028.2003.00408.x.CrossRefGoogle Scholar
  40. Nishida, T., & Uehara, S. (1983). Natural diet of chimpanzees (Pan troglodytes schweinfurthii): Long-term record from the Mahale Mountains, Tanzania. African Study Monographs,3, 109–130.Google Scholar
  41. Oates, J. F. (1978). Water-plant and soil consumption by guereza monkeys (Colobus guereza): A relationship with minerals and toxins in the diet? Biotropica,10(4), 241.  https://doi.org/10.2307/2387676.CrossRefGoogle Scholar
  42. Omotoso, O., McCarty, D. K., Hillier, S., & Kleeberg, R. (2006). Some successful approaches to quantitative mineral analysis as revealed by the 3rd Reynolds Cup contest. Clays and Clay Minerals,54(6), 748–760.  https://doi.org/10.1346/CCMN.2006.0540609.CrossRefGoogle Scholar
  43. Papaioannou, D., Katsoulos, P. D., Panousis, N., & Karatzias, H. (2005). The role of natural and synthetic zeolites as feed additives on the prevention and/or the treatment of certain farm animal diseases: A review. Microporous and Mesoporous Materials,84(1–3), 161–170.  https://doi.org/10.1016/j.micromeso.2005.05.030.CrossRefGoogle Scholar
  44. Pebsworth, P. A., Bardi, M., & Huffman, M. A. (2012). Geophagy in chacma baboons: Patterns of soil consumption by age class, sex, and reproductive state. American Journal of Primatology,74(1), 48–57.  https://doi.org/10.1002/ajp.21008.CrossRefGoogle Scholar
  45. Pebsworth, P. A., Huffman, M. A., Lambert, J. E., & Young, S. L. (2019). Geophagy among nonhuman primates: A systematic review of current knowledge and suggestions for future directions. American Journal of Physical Anthropology,1, 11.  https://doi.org/10.1002/ajpa.23724.CrossRefGoogle Scholar
  46. Pebsworth, P. A., Seim, G. L., Huffman, M. A., Glahn, R. P., Tako, E., & Young, S. L. (2013). Soil consumed by chacma baboons is low in bioavailable iron and high in clay. Journal of Chemical Ecology,39(3), 447–449.  https://doi.org/10.1007/s10886-013-0258-3.CrossRefGoogle Scholar
  47. Plumptre, A. J., & Reynolds, V. (1996). Censusing chimpanzees in the Budongo Forest, Uganda. International Journal of Primatology,17(1), 85–99.  https://doi.org/10.1007/BF02696160.CrossRefGoogle Scholar
  48. Reid, R. M. (1992). Cultural and medical perspectives on geophagia. Medical Anthropology,13(4), 337–351.  https://doi.org/10.1080/01459740.1992.9966056.CrossRefGoogle Scholar
  49. Reynolds, V. (2005). The chimpanzees of the Budongo forest: Ecology, behaviour, and conservation. Oxford: Oxford University Press.CrossRefGoogle Scholar
  50. Reynolds, V., Lloyd, A. W., English, C. J., Lyons, P., Dodd, H., Hobaiter, C., et al. (2015). Mineral acquisition from clay by Budongo Forest chimpanzees. PLoS ONE,10(7), e0134075.  https://doi.org/10.1371/journal.pone.0134075.CrossRefGoogle Scholar
  51. Reynolds, V., Plumptre, A. J., Greenham, J., & Harborne, J. (1998). Condensed tannins and sugars in the diet of chimpanzees (Pan troglodytes schweinfurthii) in the Budongo Forest, Uganda. Oecologia,115(3), 331–336.  https://doi.org/10.1007/s004420050524.CrossRefGoogle Scholar
  52. Riemer, J., Hoepken, H. H., Czerwinska, H., Robinson, S. R., & Dringen, R. (2004). Colorimetric ferrozine-based assay for the quantitation of iron in cultured cells. Analytical Biochemistry,331(2), 370–375.  https://doi.org/10.1016/j.ab.2004.03.049.CrossRefGoogle Scholar
  53. Rode, K. D., Chapman, C. A., Chapman, L. J., & McDowell, L. R. (2003). Mineral resource availability and consumption by colobus in Kibale National Park, Uganda. International Journal of Primatology,24(3), 541–573.  https://doi.org/10.1023/A:1023788330155.CrossRefGoogle Scholar
  54. Rothman, J. M., Chapman, C. A., Struhsaker, T. T., Raubenheimer, D., Twinomugisha, D., & Waterman, P. G. (2015). Long-term declines in nutritional quality of tropical leaves. Ecology,96(3), 873–878.  https://doi.org/10.1890/14-0391.1.CrossRefGoogle Scholar
  55. Ruby, M. V., Davis, A., Schoof, R., Eberle, S., & Sellstone, C. M. (1996). Estimation of lead and arsenic bioavailability using a physiologically based extraction test. Environmental Science and Technology,30(2), 422–430.CrossRefGoogle Scholar
  56. Said, S. A., Shibl, A. M., & Abdullah, M. E. (1980). Influence of various agents on adsorption capacity of kaolin for Pseudomonas aeruginosa toxin. Journal of Pharmaceutical Sciences,69(10), 1238–1239.CrossRefGoogle Scholar
  57. Seim, G. L., Ahn, C. I., Bodis, M. S., Luwedde, F., Miller, D. D., Hillier, S., et al. (2013). Bioavailability of iron in geophagic earths and clay minerals, and their effect on dietary iron absorption using an in vitro digestion/Caco-2 cell model. Food and Function,4(8), 1263.  https://doi.org/10.1039/c3fo30380b.CrossRefGoogle Scholar
  58. Severance, H. W., Holt, T., Patrone, N. A., & Chapman, L. (1988). Profound muscle weakness and hypokalemia due to clay ingestion. Southern Medical Journal,81(2), 272–274.CrossRefGoogle Scholar
  59. Spoor, D. C. A., Martineau, L. C., Leduc, C., Benhaddou-Andaloussi, A., Meddah, B., Harris, C., et al. (2006). Selected plant species from the Cree pharmacopoeia of northern Quebec possess anti-diabetic potential. Canadian Journal of Physiology and Pharmacology,84(8–9), 847–858.  https://doi.org/10.1139/y06-018.CrossRefGoogle Scholar
  60. Ta, C. A. K., Pebsworth, P. A., Liu, R., Hillier, S., Gray, N., Arnason, J. T., et al. (2018). Soil eaten by chacma baboons adsorbs polar plant secondary metabolites representative of those found in their diet. Environmental Geochemistry and Health,40(2), 803–813.  https://doi.org/10.1007/s10653-017-0025-4.CrossRefGoogle Scholar
  61. Tweheyo, M., Reynolds, V., Huffman, M. A., Pebsworth, P. A., Goto, S., Mahaney, W. C., et al. (2006). Geophagy in chimpanzees (Pan troglodytes schweinfurthii) of the Budongo Forest Reserve, Uganda. In N. E. Newton-Fisher (Ed.), Primates of western Uganda (pp. 135–152). New York: Springer.CrossRefGoogle Scholar
  62. US Pharmacopeia. (2017). http://www.pharmacopeia.cn/v29240/usp29nf24s0_ris1s126.html. Accessed 1 June 2017.
  63. Villioth, J. (2019). Foraging ecology in chimpanzeesA comparison of two communities from Budongo Forest (Doctoral dissertation). University of Kent, Canterbury.Google Scholar
  64. Wrangham, R. W., Machanda, Z. P., Weaver, C., & Muller, M. (2014). The toxin-reduction hypothesis for geophagy: Evidence from pregnant chimpanzees. Presented at the 83rd Annual American Association of physical anthropologists, Calgary (Vol. 153, pp. 277–277). Alberta: American Journal of Physical Anthropology.Google Scholar
  65. Young, S. L. (2010). Pica in pregnancy: New ideas about an old condition. Annual Review of Nutrition, 30(1), 403–422.  https://doi.org/10.1146/annurev.nutr.012809.104713.CrossRefGoogle Scholar
  66. Young, S. L., Sherman, P. W., Lucks, J. B., & Pelto, G. H. (2011). Why on earth?: Evaluating hypotheses about the physiological functions of human geophagy. The Quarterly Review of Biology,86(2), 97–120.  https://doi.org/10.1086/659884.CrossRefGoogle Scholar
  67. Young, S. L., Wilson, M. J., Miller, D., & Hillier, S. (2008). Toward a comprehensive approach to the collection and analysis of pica substances, with emphasis on geophagic materials. PLoS ONE,3(9), e3147.  https://doi.org/10.1371/journal.pone.0003147.CrossRefGoogle Scholar
  68. Zhao, D., Huffman, M. A., & Li, B. (2013). First evidence of geophagy by golden snub-nosed monkeys (Rhinopithecus roxellana). Acta Theriologica Sinica,33(3), 282–285.Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of AnthropologyThe University of TexasSan AntonioUSA
  2. 2.National Institute of Advanced StudiesIndian Institute of Science CampusBangaloreIndia
  3. 3.James Hutton InstituteCraigiebuckler, AberdeenScotland, UK
  4. 4.Department of Soil and EnvironmentSwedish University of Agricultural Sciences, SLUUppsalaSweden
  5. 5.Robert Holley Center for Agriculture and HealthIthacaUSA
  6. 6.Department of BiologyUniversity of OttawaOttawaCanada
  7. 7.Department of Anthropology and Institute for Policy ResearchNorthwestern UniversityEvanstonUSA

Personalised recommendations