Skip to main content
Log in

Biochemical Functions of Geophagy in Parrots: Detoxification of Dietary Toxins and Cytoprotective Effects

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

This study tests hypotheses on the biochemical functions of geophagy in parrots: mechanical enhancement of digestion, acid buffering capacity, mineral supplementation, adsorption of dietary toxins, and gastrointestinal cytoprotection. Parrots showed clear preferences for specific soil horizons. Comparisons of preferred and nonpreferred soils from several sites suggest that soils have little ability to enhance grinding and no measurable ability to buffer gastric pH. Soils offered insignificant mineral supplementation since most minerals occurred at similar levels in samples regardless of preference, and the minerals were generally more plentiful in the birds' diets. Sodium was available in moderate levels at some sites (>1000 ppm), but was well below sodium detection thresholds of parrots. X-ray diffraction, cation exchange capacity, and in vitro adsorptive trials showed that the preferred soils are capable of exchanging substantial quantities of cations and are capable of adsorbing low-molecular-weight secondary compounds. In captive Amazona parrots, orally administered clay reduced the bioavailability of the alkaloid quinidine by roughly 60%, demonstrating that in vivo adsorption of potentially toxic compounds may be a biologically important function of geophagy. Labeled clay remained in the lower gastrointestinal tract of captive parrots for >12 hr, which along with high adsorptive capacities, further suggests a potential role in protecting the gastrointestinal lining from various biological and chemical insults. Detoxification and cytoprotection are the most likely functions of geophagy for parrots and herbivores with similar ecologies. Given the variety of chemically defended seeds consumed by these herbivores, geophagy likely protects consumers from dietary toxins, allowing increased diet breadth and/or enhancing digestibility.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

REFERENCES

  • Abrahams, P. W., and Parsons, J. A. 1996. Geophagy in the tropics—a literature review. Geogr. J. 162:63–72.

    Google Scholar 

  • Acedo, V. 1992. Ecology of the Yellow-naped Amazon in Guatemala. AFA Watchbird 19:31–34.

    Google Scholar 

  • Arms, K., Feeney, P., and Lederhouse, R. C. 1974. Sodium: Stimulus for puddling behavior by tiger swallowtail butterflies, Papilo glaucus. Science 185:372–374.

    PubMed  Google Scholar 

  • Berenbaum, M. R., and Zangerl, A. R. 1994. Costs of inducible defense: Protein limitation, growth, and detoxification in parsnip webworms. Ecology 75(8):2311–2317.

    Google Scholar 

  • Best, L. B., and Gionfriddo, J. P. 1991. Characterization of grit use by cornfield birds. Wilson Bull. 103(1):68–82.

    Google Scholar 

  • Blair-West, J. R., Coghlan, J. P., Denton, D. A., Nelson, J. F., Orchard, E., Scoggins, B. A., Wright, R. D., Myers, K., and Junqueira, C. L. 1968. Physiological morphological and behavioural adaptation to a sodium deficient environment by wild native Australian and introduced species of animals. Nature 217:922–928.

    PubMed  Google Scholar 

  • Brouillard, M. Y., and Rateau, J. G. 1989. Pouvoir d'adsorption de deux argiles, la smectite et le kaolin sur des entérotoxines bactériennes. Gastroenterol. Clin. Biol. 13(1):18–24.

    PubMed  Google Scholar 

  • Burkitt, W. H. 1969. Sodium bentonite addition to high concentrate pelleted ratios self-fed to finishing yearling cattle. Feedstuffs 41(45):32, 39.

    Google Scholar 

  • Cade, T. J. 1964. Water and salt balance in granivorous birds, pp. 237–255, in M. J. Wayner (eds.). Thirst. Pergamon Press, New York.

    Google Scholar 

  • Cooper, M. 1957. Pica; a survey of the historical literature as well as reports from the fields of veterinary medicine and anthropology, the present study of pica in young children, and a discussion of its pediatric and psychological implications. Bannerstone House, Springfield, Illinois.

    Google Scholar 

  • Diamond, J., Bishop, K. D., and Gilardi, J. D. 1999. Geophagy in New Guinea birds. Ibis. 141(2).

  • Dixon, W. J. 1992. BMDP Statistical Software Manual. BMDP Statistical Software, Inc., Los Angeles.

    Google Scholar 

  • Droy-Lefaix, M. T., Drouet, Y., and Schatz, B. 1985. Sodium glycodeoxycholate and spinability of gastrointestinal mucus: protective effect of smectite. Gastroenterology 88:1369.

    Google Scholar 

  • Dukes, G. E. 1990. Over-the-counter antidiarrheal medications used for the self-treatment of acute nonspecific diarrhea. Symposium on the management of acute nonspecific diarrhea, Innisbrook, Florida, February 6, 1988. Am. J. Med. 88(6 Part A):6A24S-6A26S.

    Google Scholar 

  • Dumonceaux, G., and Harrison, G. J. 1994. Toxins, pp. 1030–1052, in B. W. Ritchie, G. J. Harrison, and L. R. Harrison (eds.). Avian Medicine: Principles and Application. Lake Worth, Florida.

  • Emmons, L. H., and Stark, N. M. 1979. Elemental composition of a natural mineral lick in Amazonia. Biotropica 11(4):311–313.

    Google Scholar 

  • Fawcett, D. W. 1994. A Textbook of Histology, 12th ed. Chapman and Hall, New York.

    Google Scholar 

  • Freeland, W. J., Calcott, P. H., and Geiss, D. P. 1985. Allelochemicals, minerals and herbivore population size. Biochem. Syst. Ecol. 13(2):195–206.

    Google Scholar 

  • Gardiner, K. R., Anderson, N. H., McCaigue, M. D., Erwin, P. J., Halliday, M. I., and Rowlands, B. J. 1993. Adsorbents as antiendotoxin agents in experimental colitis. Gut 34(1):51–55.

    PubMed  Google Scholar 

  • Gee, G. W., and Bauder, J. W. 1986. Particle size analysis, pp. 383–411, A. Klute (ed.). Methods of Soil Analysis, Part 1. Physical and Mineralogical Methods. Soil Science Society of America, Madison, Wisconsin.

    Google Scholar 

  • Gee, J. M., and Johnson, I. T. 1988. Interactions between hemolytic saponins, bile salts, and small intestinal mucosa in the rat. J. Nutr. 118:1391–1397.

    PubMed  Google Scholar 

  • Gilardi, J. D., and Munn, C. A. 1998. Patterns of activity, flocking, and habitat use in parrots of the Peruvian Amazon. Condor 100(4):641–653.

    Google Scholar 

  • Gionfriddo, J. P., and Best, L. B. 1995. Brit use by house sparrows: Effects of diet and grit size. Condor 97:57–67.

    Google Scholar 

  • Goodman, L. S., Gilman, A., and Gilman, A. G. 1990. Goodman and Gilman's The Pharmacological Basis of Therapeutics, 8th ed. Pergamon Press, New York.

    Google Scholar 

  • Grandjean, D., CrÉpin, F., and Paragon, B. M. 1992. Intérêt de la smectite dans les diarrhées aiguës du chien de traîneau. Rec. Méd. Vét. 168(5):323–329.

    Google Scholar 

  • Heimenz, P. C. 1986. Principles of Colloid and Surface Chemistry, 2nd ed. Marcel Dekker, New York.

    Google Scholar 

  • Heymann, E. W., and Hartman, G. 1991. Geophagy in moustached tamarins, Saguinus mystax (Platyrrhini: Callitrichidae), at the Río Blanco, Peruvian amazonia. Primates 32(4):533.

    Google Scholar 

  • Hladik, C. M., and Gueguen, L. 1974. Géophagie et nutrition minérale chez les primates sauvages. C. R. Acad. Sci. Ser. D. 279:1393–1396.

    Google Scholar 

  • Holliman, A. 1985. Acorn poisoning in ruminants. Vet. Rec. 116:546.

    Google Scholar 

  • Hunter, J. 1993. Macroterme geophagy and pregnancy clays in southern Africa. J. Cult. Geogr. 14(1):69–92.

    Google Scholar 

  • Hunter, J. M. 1973. Geophagy in Africa and the United States: A culture-nutrition hypothesis. Geogr. Rev. 63:170–195.

    Google Scholar 

  • Hunter, J. M., and De Kleine, R. 1984. Geophagy in Central America. Geogr. Rev. 74:157–169.

    PubMed  Google Scholar 

  • Huntington, G. B., Emerick, R. J., and Embry, L. B. 1977. Sodium bentonite or sodium bicarbonate as aids in feeding high-concentrate diets to lambs. J. Anim. Sci. 46(4):804–811.

    Google Scholar 

  • Hwang, E. K., Kwon, Y. B., Jean, Y. H., Im, H. U., Hyun, K. J., Kim, K. S., Yang, C. B., and Bak, Y. K. 1991. Experimental studies on blue Japanese oak (Quercus glauca) poisoning in mixed beef cattle: 2. Pathological changes of cattle being fed a blue Japanese oak. Res. Rep. Rural Dev. Admin. (Suweon) 33(2 VET):35–40.

    Google Scholar 

  • Izawa, K. 1993. Soil-eating in Aouatta and Ateles. Int. J. Primatol. 14(2):229–242.

    Google Scholar 

  • Janitzky, P. 1986. Cation-exchange capacity. USGS Bull. 1648:21–23.

    Google Scholar 

  • Johns, T. 1986. Detoxification function of geophagy and domestication of the potato. J. Chem. Ecol. 12(3):635–646.

    Google Scholar 

  • Johns, T. 1990. With Bitter Herbs They Shall Eat It: Chemical Ecology and the Origins of Human Diet and Medicine. University of Arizona Press, Tuscon.

    Google Scholar 

  • Johns, T., and Duquette, M. 1991. Traditional detoxification of acorn bread with clay. Ecol. Food Nutr. 25(3):221–228.

    Google Scholar 

  • Jones, R. L., and Hanson, H. C. 1985. Mineral Licks, Geophagy, and Biogeochemistry of North American Ungulates. The Iowa State University Press, Ames, Iowa.

    Google Scholar 

  • Kilham, L. 1960. Eating of sand by blue jays. Condor 62:295–296.

    Google Scholar 

  • Kreulen, D. A. 1985. Lick use by large herbivores: A review of benefits and banes of soil consumption. Mammal Rev. 15(3):107–123.

    Google Scholar 

  • Laufer, B. 1930. Geophagy. Field Mus. Nat. Hist. Anthropol. Ser. 28(2):1–198.

    Google Scholar 

  • Leber, W. 1988. A new suspension form of smectite (liquid “Diasorb”) for the treatment of acute diarrhoea: a randomized comparative study. Pharmatherapeutica 5(4):256–260.

    PubMed  Google Scholar 

  • Leonard, A., Droy-Lefaix, M. T., and Allen, A. 1994. Pepsin hydrolysis of the adherent mucus barrier and subsequent gastric mucosal damage in the rat: effect of diosmectite and 16,16 dimethyl prostaglandin E2. Gastroenterol. Clin. Biol. 18(6–7):609–616.

    PubMed  Google Scholar 

  • Lexomboon, U., Harikul, S., and Lortholary, O. 1994. Control randomized study of rehydration-rehydration with dioctahedral smectite in ambulatory Thai infants with acute diarrhea. Southeast Asian J. Trop. Med. Public Health 25(1):157–162.

    PubMed  Google Scholar 

  • Lumeij, J. T. 1994. Gastroenterology, pp. 482–521, in B. W. Ritchie, G. J. Harrison, and L. R. Harrison (eds.). Avian Medicine: Principles and Application. Wingers, Lake Worth, Florida.

    Google Scholar 

  • Mahaney, W. C., Hancock, R. G. V., Aufreiter, S., and Huffman, M. A. 1996. Geochemistry and clay mineralogy of termite mound soil and the role of geophagy in chimpanzees of the manhale mountains, Tanzania. Primates 37(2):121–134.

    Google Scholar 

  • MacRoberts, M. H., and MacRoberts, B. R. 1976. Social organization and behavior of the Acorn Woodpecker in central coastal California. Ornithol. Monogr. 21:1.

    Google Scholar 

  • Marlow, R. W., and Tollestrup, K. 1982. Mining and exploitation of natural mineral deposits by the desert tortoise, Gopherus agassizii. Anim. Behav. 30:475–478.

    Google Scholar 

  • Martuscelli, P. 1995. Ecology and conservation of the Red-tailed Amazon Amazona brasiliensis in south-eastern brazil. Bird Conserv. Int. 5(2–3):405–420.

    Google Scholar 

  • McIlhenny, E. A. 1932. The blue goose in its winter home. Auk 49:279–306.

    Google Scholar 

  • McInnes, R. S., and Carne, P. B. 1978. Predation of cossid moth larvae by yellow-tailed black cockatoos causing losses in plantations of Eucalyptus grandis in north coastal New South Wales. Austr. Wildl. Res. 5:101–121.

    Google Scholar 

  • Mendel, V. E. 1971. Montmorillonite clay in feed lot rations. J. Anim. Sci. 33(4):891–894.

    Google Scholar 

  • Mitchell, D., Wells, C., Hoch, N., Lind, K., Woods, S. C., and Mitchell, L. K. 1976. Poison induced pica in rats. Physiol. Behav. 17:691–697.

    PubMed  Google Scholar 

  • Mitjavila, S., Lacombe, C., Carrera, G., and Derache, R. 1977. Tannic acid and oxidized tannic acid on the functional state of rat intestinal epithelium. J. Nutr. 107:2113–2121.

    PubMed  Google Scholar 

  • Mole, S., and Waterman, P. G. 1986. Tannins as antifeedants to mammalian herbivores—still an open Question? pp. 572–587, in G. R. Waller (ed.). Allelochemicals: Role in Agriculture and Forestry. American Chemical Society, Washington, D.C.

    Google Scholar 

  • More, J., Penazet, F. Fioramonti, J., and Droy-Lefaix, M. T. 1987. Effects of treatment with smectite on gastric and intestinal glycoproteins in the rat a histochemical study. Histochem. J. 19(12):665–670.

    PubMed  Google Scholar 

  • Munn, C. A. 1988. Macaw biology in Manu National Park, Peru. Parrotletter 1:18–21.

    Google Scholar 

  • Munn, C. A. 1992. Macaw biology and ecotourism, or “when a bird in the bush is worth two in the hand,” pp. 47–72, in S. R. Beissinger and N. F. R. Snyder (eds.). New World Parrots in Crisis: Solutions from Conservation Biology. Smithsonian Institution Press, Washington, D.C.

    Google Scholar 

  • Norconk, M. A., Wertis, C., and Kinzey, W. G. 1997. Seed predation by monkeys and macaws in eastern Venezuela: Preliminary Findings. Primates 38(2):177–184.

    Google Scholar 

  • Oates, J. F. 1978. Water-plant and soil consumption by guerza mankeys (Colobus guereza): A relationship with minerals and toxins in the diet. Biotropica 10(4):241–253.

    Google Scholar 

  • Ortiz, L. T., Alzueta, C., TreviÑo, J., and CastaÑo, M. 1994. Effects of faba bean tannins on the growth and histological structure of the intestinal tract and liver of chicks and rats. Br. Poult. Sci. 35:743–754.

    PubMed  Google Scholar 

  • Pendergast, B. A., and Boag, D. A. 1970. Seasonal changes in diet of spruce grouse in central Alberta. J. Wildl. Manage. 34(3):605–611.

    Google Scholar 

  • Pryce, E. 1994. Grey Iouries Corythaixoides concolor feeding on clay. Babbler 26–27:23–24.

    Google Scholar 

  • Rateau, J. G., Margant, G., Droy-Priot, M. T., and Parier, J. L. 1982. A histological enzymatic and water-electrolyte study of the action of smectite, a mucoprotective clay, on experimental infectious diarrhoea in the rabbit. Curr. Med. Res. Opin. 8:233–241.

    PubMed  Google Scholar 

  • Robinson, S. K. 1994. Habitat selection and foraging ecology of raptors in Amazonian Peru. Biotropica 26(4):443–458.

    Google Scholar 

  • Ronald, B. 1984. Comparison of quinidine assays on the TDx®, Optimate®, Cobas®, and Murtistat III®. Clin. Chem. 30(6):1020.

    Google Scholar 

  • Roth, P. 1984. Repartição do habitat entre psitacídeos simpátricos no del sul da Amazonica. Acta Amazon. 14(1–2):175–221.

    Google Scholar 

  • Sazima, I. 1989. Peach-fronted parakeet feeding on winged termites. Wilson Bull. 101(4):656–657.

    Google Scholar 

  • Sick, H. 1993. Birds in Brazil: A Natural History. Princeton University Press, Princeton, New Jersey.

    Google Scholar 

  • Smith, M. 1979. Behaviour of the koala, Phascolarctos cimereus Goldfuss, in captivity I. Non-social behaviour. Aust. Wildl. Res. 6:117–129.

    Google Scholar 

  • Sokol, O. M. 1971. Lithophagy and geophagy in reptiles. J. Herpetol. 5:69–71.

    Google Scholar 

  • Solis, P. N., Wright, C. W., Anderson, M. M., Gupta, M. P., and Phillipson, J. D. 1993. A microwell cytotoxicity assay using Artemia-Salina brine shrimp. Planta Med. 59(3):250–252.

    PubMed  Google Scholar 

  • Stahl, A. B. 1984. Hominid dietary selection before fire. Curr. Anthrpol. 25(2):151–168.

    Google Scholar 

  • Struhsaker, T. T., Cooney, D. O., and Siex, K. S. 1997. Charcoal consumption by Zanzibar red colobus monkeys: Its function and its ecological and demographic consequences. Int. J. Primatol. 18(1):61–72.

    Google Scholar 

  • Takeda, N., Hasegawa, S., Morita, M., and Matsunaga, T. 1993. Pica in rats is analogous to emesis: An animal model in emesis research. Pharmacol. Biochem. Behav. 45(4):817–821.

    PubMed  Google Scholar 

  • Terborgh, J. 1983. Five New World primates: A Study in Comparative Ecology. Princeton University Press, Princeton, New Jersey.

    Google Scholar 

  • Terborgh, J. 1986. Community aspects of frugivory in tropical forests, pp. 371–384, in A. Estrada and T. H. Fleming (eds.). Frugivores and Seed Dispersal. Dr. W. Junk Publishers, Dordrecht.

    Google Scholar 

  • Verbeek, N. A. M. 1995. The use of grit in pipits, especially the American pipit. J. Field Ornithol. 65(4):498–503.

    Google Scholar 

  • Vermeer, D. E., and Ferrell, R. E. J. 1985. Nigerian geophagical clay: A traditional antidiarrheal pharmaceutical. Science 227:634–636.

    PubMed  Google Scholar 

  • Vivatvakin, B., Jongpipatvanich, S., Harikul, S., Eksaengri, P., and Lortholary, O. 1992. Control study of oral rehydration solution ors-ors plus dioctahedral smectite in hospitalized Thai infants with acute secretory diarrhea. Southeast Asian J. Trop. Med. Public Health 23(3):414–419.

    PubMed  Google Scholar 

  • Watts, D. W. 1994. In vitro buffering capacities of proprietary non-particulate antacids available in New Zealand. Anaesth. Intens. Care 22(2):184–186.

    Google Scholar 

  • Wang, X., LÁztity, A., VicziÁn, M., Isreal, Y., and Barnes, R. 1989. Inductively coupled plasma spectrometry in the study of childhood soil ingestion: part 1. methodology. J. Anal. Atom. Spectrom. 4:727–735.

    Google Scholar 

  • Whittig, L. D., and Allardice, W. R. 1986. X-ray diffraction techniques. In A. Klute (ed.). Methods of Soil Analysis, Part 1. Physical and Mineralogical Methods. Soil Science Society of America, Madison, Wisconsin.

    Google Scholar 

  • Weisman, A., and Thompson, H. 1984. Acorn poisoning. Vet. Rec. 115:605.

    Google Scholar 

  • Wyndham, E., and Cannon, C. E. 1985. Parrots of eastern Australian forests and woodlands: The genera Platycercus and Trichoglossus, pp. 141–150, in A. Keast, H. F. Recher, H. Ford, and D. A. Saunders (eds.). Birds of Eucalypt Forests and Woodlands: Ecology, Conservation and Management. Royal Australian Ornithologists Union and Surrey Beatty and Sons.

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gilardi, J.D., Duffey, S.S., Munn, C.A. et al. Biochemical Functions of Geophagy in Parrots: Detoxification of Dietary Toxins and Cytoprotective Effects. J Chem Ecol 25, 897–922 (1999). https://doi.org/10.1023/A:1020857120217

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1020857120217

Navigation