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Environmental Geochemistry and Health

, Volume 40, Issue 2, pp 803–813 | Cite as

Soil eaten by chacma baboons adsorbs polar plant secondary metabolites representative of those found in their diet

  • Chieu Anh Kim Ta
  • Paula A. Pebsworth
  • Rui Liu
  • Stephen Hillier
  • Nia Gray
  • John T. Arnason
  • Sera L. Young
Original Paper
  • 115 Downloads

Abstract

Geophagy, the deliberate consumption of earth materials, is common among humans and animals. However, its etiology and function(s) remain poorly understood. The major hypotheses about its adaptive functions are the supplementation of essential elements and the protection against temporary and chronic gastrointestinal (GI) distress. Because much less work has been done on the protection hypothesis, we investigated whether soil eaten by baboons protected their GI tract from plant secondary metabolites (PSMs) and described best laboratory practices for doing so. We tested a soil that baboons eat/preferred, a soil that baboons never eat/non-preferred, and two clay minerals, montmorillonite a 2:1 clay and kaolinite a 1:1 clay. These were processed using a technique that simulated physiological digestion. The phytochemical concentration of 10 compounds representative of three biosynthetic classes of compounds found in the baboon diet was then assessed with and without earth materials using high-performance liquid chromatography with diode-array detection (HPLC–DAD). The preferred soil was white, contained 1% halite, 45% illite/mica, 14% kaolinite, and 0.8% sand; the non-preferred soil was pink, contained 1% goethite and 1% hematite but no halite, 40% illite/mica, 19% kaolinite, and 3% sand. Polar phenolics and alkaloids were generally adsorbed at levels 10× higher than less polar terpenes. In terms of PSM adsorption, the montmorillonite was more effective than the kaolinite, which was more effective than the non-preferred soil, which was more effective than the preferred soil. Our findings suggest that HPLC–DAD is best practice for the assessment of PSM adsorption of earth materials due to its reproducibility and accuracy. Further, soil selection was not based on adsorption of PSMs, but on other criteria such as color, mouth feel, and taste. However, the consumption of earth containing clay minerals could be an effective strategy for protecting the GI tract from PSMs.

Keywords

Plant toxin adsorption Simulated digestion HPLC–DAD Soil eating Detoxification Pica Methods 

Notes

Acknowledgements

This work was funded by a Natural Science and Engineering Research Council grant to JT Arnason. We thank Cape Nature and Jennifer Giddy for the opportunity to conduct research in South Africa and Nimal De Silva, Jean Bjornson, and Christopher N. Boddy for assistance with the analytical analyses. We also thank the EGH editor, Professor William Mahaney, and two anonymous reviewers for helpful comments on the previous version of the manuscript.

References

  1. Abrahams, P. W. (2013). Geophagy and the involuntary ingestion of soil. In Essentials of medical geology (pp. 433–454). Berlin: Springer.Google Scholar
  2. Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49(3), 227–266. doi: 10.1163/156853974X00534.CrossRefGoogle Scholar
  3. Arnason, J. T., & Bernards, M. A. (2010). Impact of constitutive plant natural products on herbivores and pathogens. Canadian Journal of Zoology, 88(7), 615–627. doi: 10.1139/Z10-038.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. Cornell, R. M., & Schwertmann, U. (2006). The iron oxides structure, properties, reactions, occurrences and uses. Weinheim: Wiley-VCH. http://nbn-resolving.de/urn:nbn:de:101:1-2014081514273. Accessed 1 June 2017.
  6. 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
  7. Dupont, C., & Vernisse, B. (2009). Anti-diarrheal effects of diosmectite in the treatment of acute diarrhea in children: A review. Paediatric Drugs, 11(2), 89–99.CrossRefGoogle Scholar
  8. Esaki, S., Kamiya, S., & Konishi, F. (1977). Structure and taste of some analogs of naringin. Agricultural and Biological Chemistry, 41(9), 1791–1792. doi: 10.1080/00021369.1977.10862757.Google Scholar
  9. Espinosa Gómez, F., Santiago García, J., Gómez Rosales, S., Wallis, I. R., Chapman, C. A., Morales Mávil, J., et al. (2015). Howler monkeys (Alouatta palliata mexicana) produce tannin-binding salivary proteins. International Journal of Primatology, 36(6), 1086–1100. doi: 10.1007/s10764-015-9879-4.CrossRefGoogle Scholar
  10. Ferrari, S. F., Veiga, L. M., & Urbani, B. (2008). Geophagy in new world monkeys (Platyrrhini): Ecological and geographic patterns. Folia Primatologica, 79(5), 402–415. doi: 10.1159/000141901.CrossRefGoogle Scholar
  11. 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. doi: 10.1023/A:1020857120217.CrossRefGoogle Scholar
  12. Gillman, G. P., & Sumpter, E. A. (1986). Modification to the compulsive exchange method for measuring exchange characteristics of soils. Australian Journal of Soil Research, 24(1), 61. doi: 10.1071/SR9860061.CrossRefGoogle Scholar
  13. 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. doi: 10.1038/sj.bjp.0705710.CrossRefGoogle Scholar
  14. Harris, C. S., Burt, A. J., Saleem, A., Le, P. M., Martineau, L. C., Haddad, P. S., et al. (2007). A single HPLC-PAD-APCI/MS method for the quantitative comparison of phenolic compounds found in leaf, stem, root and fruit extracts of Vaccinium angustifolium. Phytochemical Analysis, 18(2), 161–169. doi: 10.1002/pca.970.CrossRefGoogle Scholar
  15. Heister, K. (2014). The measurement of the specific surface area of soils by gas and polar liquid adsorption methods: Limitations and potentials. Geoderma, 216, 75–87. doi: 10.1016/j.geoderma.2013.10.015.CrossRefGoogle Scholar
  16. 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
  17. Horowitz, R. M., & Gentili, B. (1969). Taste and structure in phenolic glycosides. Journal of Agricultural and Food Chemistry, 17(4), 696–700. doi: 10.1021/jf60164a049.CrossRefGoogle Scholar
  18. Jeannoda, V., Rakotonirina, O., Randrianarivo, H., Rakoto, D., Wright, P. C., & Hladik, C. M. (2003). The toxic principle of the bamboo eaten by Hapalemur aureus is not neutralized by soil consumption. Revue d’Ecologie, 58, 151–153.Google Scholar
  19. Johns, T. (1986). Detoxification function of geophagy and domestication of the potato. Journal of Chemical Ecology, 12(3), 635–646. doi: 10.1007/BF01012098.CrossRefGoogle Scholar
  20. Johns, T., & Duquette, M. (1991). Traditional detoxification of acorn bread with clay. Ecology of Food and Nutrition, 25(3), 221–228.CrossRefGoogle Scholar
  21. Klaus, G., Klaus-Hugi, C., & Schmid, B. (1998). Geophagy by large mammals at natural licks in the rain forests of the Dzanga National Park, Central African Republic. Journal of Tropical Ecology, 14, 828–839.CrossRefGoogle Scholar
  22. Klein, N., Fröhlich, F., & Krief, S. (2008). Geophagy: Soil consumption enhances the bioactivities of plants eaten by chimpanzees. Naturwissenschaften, 95(4), 325–331. doi: 10.1007/s00114-007-0333-0.CrossRefGoogle Scholar
  23. 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
  24. Krishnamani, R., & Mahaney, W. C. (2000). Geophagy among primates: Adaptive significance and ecological consequences. Animal Behaviour, 59(5), 899–915. doi: 10.1006/anbe.1999.1376.CrossRefGoogle Scholar
  25. Kubota, T., & Kubo, I. (1969). Bitterness and chemical structure. Nature, 223(5201), 97–99. doi: 10.1038/223097a0.CrossRefGoogle Scholar
  26. Laska, M., & Hernandez Salazar, L. T. (2004). Gustatory responsiveness to monosodium glutamate and sodium chloride in four species of nonhuman primates. Journal of Experimental Zoology, 301A(11), 898–905. doi: 10.1002/jez.a.118.CrossRefGoogle Scholar
  27. Lounasmaa, M., & Tamminen, T. (1993). Chapter 1: The tropane Alkaloids. In The Alkaloids: Chemistry and pharmacology (vol. 44, pp. 1–114). Elsevier. doi: 10.1016/S0099-9598(08)60143-1.
  28. Mahaney, W. C., Hancock, R. G. V., & Inoue, M. (1993). Geochemistry and clay mineralogy of soils eaten by Japanese macaques. Primates, 34(1), 85–91.CrossRefGoogle Scholar
  29. 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. doi: 10.1007/BF02382006.CrossRefGoogle Scholar
  30. Mahaney, W. C., Zippin, J., Milner, M. W., Sanmugadas, K., Hancock, R. G. V., Aufreiter, S., et al. (1999). Chemistry, mineralogy and microbiology of termite mound soil eaten by the chimpanzees of the Mahale Mountains, Western Tanzania. Journal of Tropical Ecology, 15, 565–588.CrossRefGoogle Scholar
  31. Matsubayashi, H., Lagan, P., Majalap, N., Tangah, J., Sukor, J. R. A., & Kitayama, K. (2007). Importance of natural licks for the mammals in Bornean inland tropical rain forests. Ecological Research, 22(5), 742–748. doi: 10.1007/s11284-006-0313-4.CrossRefGoogle Scholar
  32. Mau, M., de Almeida, A. M., Coelho, A. V., & Südekum, K.-H. (2011). First identification of tannin-binding proteins in saliva of Papio hamadryas using MS/MS mass spectrometry. American Journal of Primatology, 73(9), 896–902. doi: 10.1002/ajp.20958.CrossRefGoogle Scholar
  33. Meyerhof, W., Batram, C., Kuhn, C., Brockhoff, A., Chudoba, E., Bufe, B., et al. (2010). The molecular receptive ranges of human TAS2R bitter taste receptors. Chemical Senses, 35(2), 157–170. doi: 10.1093/chemse/bjp092.CrossRefGoogle Scholar
  34. 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. doi: 10.1346/CCMN.2006.0540609.CrossRefGoogle Scholar
  35. Pebsworth, P. A., Bardi, M., & Huffman, M. A. (2012a). Geophagy in chacma baboons: Patterns of soil consumption by age class, sex, and reproductive state. American Journal of Primatology, 74(1), 48–57. doi: 10.1002/ajp.21008.CrossRefGoogle Scholar
  36. Pebsworth, P. A., MacIntosh, A. J. J., Morgan, H. R., & Huffman, M. A. (2012b). Factors influencing the ranging behavior of chacma baboons (Papio hamadryas ursinus) living in a human-modified habitat. International Journal of Primatology, 33(4), 872–887. doi: 10.1007/s10764-012-9620-5.CrossRefGoogle Scholar
  37. 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
  38. Schober, P. C., Bowers, P. W., & Smith, S. E. (1978). Low stereospecificity of quinine taste receptors. Journal of Pharmacy and Pharmacology, 30(1), 111–112. doi: 10.1111/j.2042-7158.1978.tb13173.x.CrossRefGoogle Scholar
  39. Setz, E., Enzweiler, J., Solferini, V., Amêndola, M., & Berton, R. (1999). Geophagy in the golden-faced saki monkey (Pithecia pithecia chrysocephala) in the Central Amazon. Journal of Zoology, 247(1), 91–103.CrossRefGoogle Scholar
  40. Song, M., Liu, Y., Soares, J. A., Che, T. M., Osuna, O., Maddox, C. W., et al. (2012). Dietary clays alleviate diarrhea of weaned pigs. Journal of Animal Science, 90(1), 345–360. doi: 10.2527/jas.2010-3662.CrossRefGoogle Scholar
  41. Strier, K. B. (2007). Primate behavioral ecology (3rd ed.). Boston: Pearson Allyn and Bacon.Google Scholar
  42. US Pharmacopeia. (2017). http://www.pharmacopeia.cn/v29240/usp29nf24s0_ris1s126.html. Accessed 1 June 2017.
  43. Vermeer, D., & Ferrell, R. (1985). Nigerian geophagical clay: A traditional antidiarrheal pharmaceutical. Science, 227(4687), 634–636. doi: 10.1126/science.3969552.CrossRefGoogle Scholar
  44. Vidal, S., Francis, L., Noble, A., Kwiatkowski, M., Cheynier, V., & Waters, E. (2004). Taste and mouth-feel properties of different types of tannin-like polyphenolic compounds and anthocyanins in wine. Analytica Chimica Acta, 513(1), 57–65. doi: 10.1016/j.aca.2003.10.017.CrossRefGoogle Scholar
  45. Wakibara, J. V., Huffman, M. A., Wink, M., Reich, S., Aufreiter, S., Hancock, R. G. V., et al. (2001). The Adaptive significance of geophagy for Japanese macaques (Macaca fuscata) at Arashiyama, Japan. International Journal of Primatology, 22(3), 495–520. doi: 10.1023/A:1010763930475.CrossRefGoogle Scholar
  46. Williams, L. B., Haydel, S. E., & Ferrell, R. E. (2009). Bentonite, bandaids, and borborygmi. Elements, 5(2), 99–104. doi: 10.2113/gselements.5.2.99.CrossRefGoogle Scholar
  47. Williams, L. B., & Hillier, S. (2014). Kaolins and health: From first grade to first aid. Elements, 10(3), 207–211. doi: 10.2113/gselements.10.3.207.CrossRefGoogle Scholar
  48. Young, S. L. (2012). Craving earth: understanding pica: The urge to eat clay, starch, ice, and chalk. New York: Columbia University Press.CrossRefGoogle Scholar
  49. 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. doi: 10.1086/659884.CrossRefGoogle Scholar
  50. Young, S. L., Wilson, M. J., Hillier, S., Delbos, E., Ali, S. M., & Stoltzfus, R. J. (2010). Differences and commonalities in physical, chemical and mineralogical properties of Zanzibari geophagic soils. Journal of Chemical Ecology, 36(1), 129–140. doi: 10.1007/s10886-009-9729-y.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  1. 1.Department of BiologyUniversity of OttawaOttawaCanada
  2. 2.Department of AnthropologyThe University of TexasSan AntonioUSA
  3. 3.James Hutton InstituteCraigiebuckler, AberdeenScotland, UK
  4. 4.Department of Soil and EnvironmentSwedish University of Agricultural Sciences, SLUUppsalaSweden
  5. 5.Department of Anthropology, Institute for Policy ResearchNorthwestern UniversityEvanstonUSA

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