Journal of Chemical Ecology

, Volume 25, Issue 4, pp 897–922

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

  • James D. Gilardi
  • Sean S. Duffey
  • Charles A. Munn
  • Lisa A. Tell
Article

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.

Parrot macaw geophagy clay mineral detoxification secondary compounds dietary ecology cytoprotection 

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REFERENCES

  1. Abrahams, P. W., and Parsons, J. A. 1996. Geophagy in the tropics—a literature review. Geogr. J. 162:63–72.Google Scholar
  2. Acedo, V. 1992. Ecology of the Yellow-naped Amazon in Guatemala. AFA Watchbird 19:31–34.Google Scholar
  3. Arms, K., Feeney, P., and Lederhouse, R. C. 1974. Sodium: Stimulus for puddling behavior by tiger swallowtail butterflies, Papilo glaucus. Science 185:372–374.PubMedGoogle Scholar
  4. 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
  5. Best, L. B., and Gionfriddo, J. P. 1991. Characterization of grit use by cornfield birds. Wilson Bull. 103(1):68–82.Google Scholar
  6. 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.PubMedGoogle Scholar
  7. 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.PubMedGoogle Scholar
  8. 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
  9. 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
  10. 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
  11. Diamond, J., Bishop, K. D., and Gilardi, J. D. 1999. Geophagy in New Guinea birds. Ibis. 141(2).Google Scholar
  12. Dixon, W. J. 1992. BMDP Statistical Software Manual. BMDP Statistical Software, Inc., Los Angeles.Google Scholar
  13. 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
  14. 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
  15. 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.Google Scholar
  16. Emmons, L. H., and Stark, N. M. 1979. Elemental composition of a natural mineral lick in Amazonia. Biotropica 11(4):311–313.Google Scholar
  17. Fawcett, D. W. 1994. A Textbook of Histology, 12th ed. Chapman and Hall, New York.Google Scholar
  18. 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
  19. 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.PubMedGoogle Scholar
  20. 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
  21. 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.PubMedGoogle Scholar
  22. 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
  23. 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
  24. 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
  25. 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
  26. Heimenz, P. C. 1986. Principles of Colloid and Surface Chemistry, 2nd ed. Marcel Dekker, New York.Google Scholar
  27. 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
  28. 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
  29. Holliman, A. 1985. Acorn poisoning in ruminants. Vet. Rec. 116:546.Google Scholar
  30. Hunter, J. 1993. Macroterme geophagy and pregnancy clays in southern Africa. J. Cult. Geogr. 14(1):69–92.Google Scholar
  31. Hunter, J. M. 1973. Geophagy in Africa and the United States: A culture-nutrition hypothesis. Geogr. Rev. 63:170–195.Google Scholar
  32. Hunter, J. M., and De Kleine, R. 1984. Geophagy in Central America. Geogr. Rev. 74:157–169.PubMedGoogle Scholar
  33. 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
  34. 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
  35. Izawa, K. 1993. Soil-eating in Aouatta and Ateles. Int. J. Primatol. 14(2):229–242.Google Scholar
  36. Janitzky, P. 1986. Cation-exchange capacity. USGS Bull. 1648:21–23.Google Scholar
  37. Johns, T. 1986. Detoxification function of geophagy and domestication of the potato. J. Chem. Ecol. 12(3):635–646.Google Scholar
  38. 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
  39. Johns, T., and Duquette, M. 1991. Traditional detoxification of acorn bread with clay. Ecol. Food Nutr. 25(3):221–228.Google Scholar
  40. 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
  41. Kilham, L. 1960. Eating of sand by blue jays. Condor 62:295–296.Google Scholar
  42. 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
  43. Laufer, B. 1930. Geophagy. Field Mus. Nat. Hist. Anthropol. Ser. 28(2):1–198.Google Scholar
  44. 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.PubMedGoogle Scholar
  45. 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.PubMedGoogle Scholar
  46. 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.PubMedGoogle Scholar
  47. 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
  48. 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
  49. 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
  50. 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
  51. 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
  52. McIlhenny, E. A. 1932. The blue goose in its winter home. Auk 49:279–306.Google Scholar
  53. 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
  54. Mendel, V. E. 1971. Montmorillonite clay in feed lot rations. J. Anim. Sci. 33(4):891–894.Google Scholar
  55. 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.PubMedGoogle Scholar
  56. 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.PubMedGoogle Scholar
  57. 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
  58. 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.PubMedGoogle Scholar
  59. Munn, C. A. 1988. Macaw biology in Manu National Park, Peru. Parrotletter 1:18–21.Google Scholar
  60. 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
  61. 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
  62. 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
  63. 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.PubMedGoogle Scholar
  64. 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
  65. Pryce, E. 1994. Grey Iouries Corythaixoides concolor feeding on clay. Babbler 26–27:23–24.Google Scholar
  66. 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.PubMedGoogle Scholar
  67. Robinson, S. K. 1994. Habitat selection and foraging ecology of raptors in Amazonian Peru. Biotropica 26(4):443–458.Google Scholar
  68. Ronald, B. 1984. Comparison of quinidine assays on the TDx®, Optimate®, Cobas®, and Murtistat III®. Clin. Chem. 30(6):1020.Google Scholar
  69. Roth, P. 1984. Repartição do habitat entre psitacídeos simpátricos no del sul da Amazonica. Acta Amazon. 14(1–2):175–221.Google Scholar
  70. Sazima, I. 1989. Peach-fronted parakeet feeding on winged termites. Wilson Bull. 101(4):656–657.Google Scholar
  71. Sick, H. 1993. Birds in Brazil: A Natural History. Princeton University Press, Princeton, New Jersey.Google Scholar
  72. Smith, M. 1979. Behaviour of the koala, Phascolarctos cimereus Goldfuss, in captivity I. Non-social behaviour. Aust. Wildl. Res. 6:117–129.Google Scholar
  73. Sokol, O. M. 1971. Lithophagy and geophagy in reptiles. J. Herpetol. 5:69–71.Google Scholar
  74. 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.PubMedGoogle Scholar
  75. Stahl, A. B. 1984. Hominid dietary selection before fire. Curr. Anthrpol. 25(2):151–168.Google Scholar
  76. 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
  77. 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.PubMedGoogle Scholar
  78. Terborgh, J. 1983. Five New World primates: A Study in Comparative Ecology. Princeton University Press, Princeton, New Jersey.Google Scholar
  79. 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
  80. Verbeek, N. A. M. 1995. The use of grit in pipits, especially the American pipit. J. Field Ornithol. 65(4):498–503.Google Scholar
  81. Vermeer, D. E., and Ferrell, R. E. J. 1985. Nigerian geophagical clay: A traditional antidiarrheal pharmaceutical. Science 227:634–636.PubMedGoogle Scholar
  82. 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.PubMedGoogle Scholar
  83. 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
  84. 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
  85. 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
  86. Weisman, A., and Thompson, H. 1984. Acorn poisoning. Vet. Rec. 115:605.Google Scholar
  87. 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.Google Scholar

Copyright information

© Plenum Publishing Corporation 1999

Authors and Affiliations

  • James D. Gilardi
    • 1
    • 2
  • Sean S. Duffey
    • 2
  • Charles A. Munn
    • 3
  • Lisa A. Tell
    • 4
  1. 1.Section of Evolution and EcologyUniversity of CaliforniaDavis
  2. 2.Oceanic Society, Fort Mason CenterSan Francisco
  3. 3.Wildlife Conservation SocietyBronx
  4. 4.School of Veterinary MedicineUniversity of CaliforniaDavis

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