Journal of Chemical Ecology

, Volume 21, Issue 7, pp 911–923 | Cite as

Tracking variable environments: There is more than one kind of memory

  • Frederick D. Provenza
Article

Abstract

Three kinds of memory help herbivores track changes in the environment. The first is the collective memory of the species with genetic instructions that have been shaped by the environment through millennia. This includes skin and gut defense systems. Auditory and visual stimuli and sensations of pain impinge upon the skin defense system that evolved in response to predation. The taste of food and the sensations of nausea and satiety are an integral part of the gut defense system that evolved in response to toxins and nutrients in plants. The second kind of memory in social mammals is represented by the mother, a source of transgenerational knowledge, who increases efficiency and reduces risk of learning about foods and environments. The third kind of memory is acquired by individual experience. Postingestive feedback from nutrients and toxins enables individuals to experience the consequences of food ingestion and to adjust food preference and selection commensurate with a food's utility. The three memories interact, each linking the past to the present, and collectively shape the present and future of every individual. Thus, the dynamics of foraging involves appreciating the uniqueness of individuals and subgroups of animals, each with their own genetic and behavioral history, and recognizing that foraging behaviors may not be stable, optimal, or even predictable in the conventional sense.

Key Words

Evolution ecology learning memory foraging habitat spotted owl 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Anderson, R. 1991. Habitat deterioration and the migratory behaviour of moose (Alces alces L.) in Norway.J. Appl. Ecol. 28:102–108.Google Scholar
  2. Bermudez-Rattoni, F., Forthman Quick, D.L., Sanchez, M.A., Perez, J.L., andGarcia, J. 1988. Odor and taste aversions conditioned in anesthetized rats.Behav. Neurosci. 102:726–732.PubMedGoogle Scholar
  3. Biquand, S., andBiquand-Guyot, V. 1992. The influence of peers, lineage and environment on food selection of the criollo goat (Capra hircus).Appl. Anim. Behav. Sci. 34:231–245.Google Scholar
  4. Brett, L.P., Hankins, W.G., andGarcia, J. 1976. Prey-lithium aversions III: Buteo hawks.Behav. Biol. 17:87–98.PubMedGoogle Scholar
  5. Buresova, O., andBures, J. 1973. Cortical and subcortical components of the conditioned saccharin aversion.Physiol. Behav. 11:435–439.PubMedGoogle Scholar
  6. Burritt, E.A., andProvenza, F.D. 1989. Food aversion learning: ability of lambs to distinguish safe from harmful foods.J. Anim. Sci. 67:1732–1739.PubMedGoogle Scholar
  7. Burritt, E.A., andProvenza, F.D. 1990. Food aversion learning in sheep: Persistence of conditioned taste aversions to palatable shrubs (Cercocarpus montanus andAmelanchier alnifolia).J. Anim. Sci. 68:1003–1007.PubMedGoogle Scholar
  8. Burritt, E.A., andProvenza, F.D. 1991. Ability of lambs to learn with a delay between food ingestion and consequences given meals containing novel and familiar foods.Appl. Anim. Behav. Sci. 32:179–189.Google Scholar
  9. Burritt, E.A. andF.D. Provenza. 1995. Effect of experience and prior illness on the acquisition and persistence of conditioned food aversions in lambs.Appl. Anim. Behav. Sci. in press.Google Scholar
  10. Cederlund, G., andOkama, H. 1988. Home range and habitat use of adult female moose.J. Wildl. Manage. 52:336–343.Google Scholar
  11. Cederlund, G., Sandegren, F., andLarsson, K. 1987. Summer movements of female moose and dispersal of their offspring.J. Wildl. Manage. 51:342–352.Google Scholar
  12. Chapple, R.S., andLynch, J.J. 1986. Behavioral factors modifying acceptance of supplementary foods by sheep.Res. Dev. Agric. 3:113–120.Google Scholar
  13. Chapple, R.S., Wodzicka-Tomaszewska, M., andLynch, J.J. 1987. The learning behavior of sheep when introduced to wheat. II. Social transmission of wheat feeding and the role of the senses.Appl. Anim. Behav. Sci. 18:163–172.Google Scholar
  14. Coil, J.D., Hankins, W.G., Jenden, D.J., andGarcia, J. 1978. The attenuation of a specific cue-to-consequence association by antiemetic agents.Psychopharmacology 56:21–25.PubMedGoogle Scholar
  15. Davis, J.L., andBures, J. 1972. Disruption of saccharin-aversion learning in rats by cortical spreading dispersion in the CS-US interval.J. Comp. Physiol. Psychol. 80:398–402.PubMedGoogle Scholar
  16. Easterbrook, G. 1994. The birds.The New Republic. March: 22–24.Google Scholar
  17. Festa-Bianchet, M. 1986a. Seasonal dispersion of overlapping mountain sheep ewe groups.J. Wildl. Manage. 50:325–330.Google Scholar
  18. Festa-Bianchet, M. 1986b. Site fidelity and seasonal range use by bighorn rams.Can. J. Zool. 64:2126–2132.Google Scholar
  19. Festa-Bianchet, M. 1988. Seasonal range selection in bighorn sheep: Conflicts between forage quality, forage quantity, and predator avoidance.Oecologia 75:580–586.Google Scholar
  20. Forthman Quick, D. 1984. Reduction of crop damage by olive baboons (Papio anubis): The feasibility of conditioned taste aversion. PhD thesis. University of California, Los Angeles.Google Scholar
  21. Galef, B.G., Jr. 1988. Imitation in animals: History, definition, and interpretation of data from the psychological laboratory, pp. 3–28,in T.R. Zentall and B.G. Galef, Jr. (eds.). Social Learning: Psychological and Biological Perspectives. Lawrence Erlbaum Associates, Hillsdale, New Jersey.Google Scholar
  22. Garcia, J. 1989. Food for Tolman: cognition and cathexis in concert, pp. 45–85,in T. Archer and L. Nilsson (Eds.). Aversion, Avoidance and Anxiety. Lawrence Erlbaum Associates, Hillsdale, New Jersey.Google Scholar
  23. Garcia, J., andKoelling, R.A. 1986. Relation of cue to consequence in avoidance learning.Psychon. Sci. 4:123–124.Google Scholar
  24. Garcia, J., andGarcia y Robertson, R. 1985. Evolution of learning mechanisms, pp. 191–242,in B.L. Hammonds (ed.). The Master Lecture Series, Psychology and Learning. American Psychological Association, Washington, D.C.Google Scholar
  25. Garcia, J., Lasiter, P.A., Bermudez-Rattoni, F., andDeems, D.A. 1985. A general theory of aversion learning. pp. 8–21,in N.S. Braveman and P. Bronstein (eds.). Experimental Assessments and Clinical Applications of Conditioned Food Aversions. New York Academy of Science, New York.Google Scholar
  26. Geist, V. 1971. Mountain Sheep: A Study in Behavior and Evolution. University of Chicago Press, Chicago.Google Scholar
  27. Green, G.C., Elwin, R.L., Mottershead, B.E., andLynch, J.J. 1984. Long-term effects of early experience to supplementary feeding in sheep.Proc. Aust. Soc. Anim. Prod. 15:373–375.Google Scholar
  28. Griffith, B., Scott, J.M., Carpenter, J.W., andReed, C. 1989. Translocation as a species conservation tool: status and strategy.Science 245:477–480.Google Scholar
  29. Gruell, G.E., andPapez, N.J. 1963. Movements of mule deer in northeastern Nevada.J. Wildl. Manage. 27:414–422.Google Scholar
  30. Hall, S.J.G. 1988. Chillingham Park and its herd of white cattle: relationships between vegetation classes and patterns of range use.J. Appl. Ecol. 25:777–789.Google Scholar
  31. Histol, T., andHjeljord, O. 1993. Winter feeding strategies of migrating and nonmigrating moose.Can. J. Zool. 71:1421–1428.Google Scholar
  32. Howery, L.D., Provenza, F.D., andBanner, R.E. 1995a. Intraspecific differences in distribution patterns among individuals in a cattle herd.Appl. Anim. Behav. Sci. Submitted.Google Scholar
  33. Howery, L.D., Provenza, F.D., andBanner, R.E. 1995b. The relative importance of mother and peers in perpetuating home range and habitat use patterns among individuals in a cattle herd.Appl. Anim. Behav. Sci. Submitted.Google Scholar
  34. Hunter, R.F., andMilner, C. 1963. The behavior of individual, related and groups of south country Cheviot hill sheep.Anim. Behav. 11:507–513.Google Scholar
  35. Kalat, J.W. 1974. Taste salience depends on novelty, not concentration, in taste-aversion learning in rats.J. Comp. Physiol. Psych. 86:47–50.Google Scholar
  36. Kalat, J.W., andRozin, P. 1970. “Salience”: A factor which can override temporal contiguity in taste-aversion learning.J. Comp. Physiol. Psychol. 71:192–197.Google Scholar
  37. Kalat, J.W., andRozin, P. 1971. Role of interference in taste-aversion learning.J. Comp. Physiol. Psychol. 77:53–58.PubMedGoogle Scholar
  38. Key, C., andMacIver, R.M. 1980. The effects of maternal influences on sheep: Breed differences in grazing, resting and courtship behavior.Appl. Anim. Ethol. 6:33–48.Google Scholar
  39. Lane, M.A., Ralphs, M.A., Olsen, J.D., Provenza, F.D., andPfister, J.A. 1990. Conditioned taste aversion: Potential for reducing cattle loss to larkspur.J. Range Manage. 43:127–131.Google Scholar
  40. Lawrence, A.B. 1990. Mother-daughter and peer relationships of Scottish hill sheep.Anim. Behav. 39:481–486.Google Scholar
  41. Launchbaugh, K.L., andProvenza, F.D. 1993. Can plants practice mimicry to avoid grazing by mammalian herbivores?Oikos 66:501–504.Google Scholar
  42. Launchbaugh, K.L., Provenza, F.D., andBurritt, E.A. 1993. How herbivores track variable environments: Response to variability of phytotoxins.J. Chem. Ecol. 19:1047–1056.Google Scholar
  43. LeDoux, J.E. 1992. Brain mechanisms of emotion and emotional learning.Curr. Opin. Neurobiol. 2:191–197.PubMedGoogle Scholar
  44. LeDoux, J.E. 1994. Emotion, memory and the brain.Sci. Am. 270:50–57.Google Scholar
  45. Lett, B.T. 1985. The pain-like effect of gallamine and naloxone differs from sickness induced by lithium chloride.Behav. Neurosci. 99:145–150.PubMedGoogle Scholar
  46. Lynch, J.J., Keogh, R.G., Elwin, R.L., Green, G.C., andMottershead, B.E. 1983. Effects of early experience on the post-weaning acceptance of whole grain wheat by fine-wool Merino lambs.Anim. Prod. 36:175–183.Google Scholar
  47. Martin, S.C., 1979. Evaluating the impacts of cattle grazing on riparian habitats in the national forests of Arizona and New Mexico, pp. 35–38,in Forum—Grazing and Riparian/Stream Ecosystems. Trout Unlimited, Denver.Google Scholar
  48. Mirza, S.N., andProvenza, F.D. 1990. Preference of the mother affects selection and avoidance of foods by lambs differing in age.Appl. Anim. Behav. Sci. 28:255–263.Google Scholar
  49. Mirza, S.N., andProvenza, F.D. 1992. Effects of age and conditions of exposure on maternally mediated food selection in lambs.Appl. Anim. Behav. Sci. 33:35–42.Google Scholar
  50. Mirza, S.N., andProvenza, F.D. 1994. Socially induced food avoidance in lambs: Direct or indirect maternal influence?J. Anim. Sci. 72:899–902.PubMedGoogle Scholar
  51. Nolte, D.L., Provenza, F.D., andBalph, D.F. 1990. The establishment and persistence of food preferences in lambs exposed to selected foods.J. Anim. Sci. 68:998–1002.PubMedGoogle Scholar
  52. O'Brien, P.H. 1984. Feral goat home range: Influence of social class and environmental variables.Appl. Anim. Behav. Sci. 12:373–385.Google Scholar
  53. Phy, T.S. andF.D. Provenza. 1995. Sheep acquire preferences for substances that rectify lactic acidosis.J. Anim. Sci., submitted.Google Scholar
  54. Porter, W.F. 1992. High fidelity deer.Nat. Hist. May:48–49.Google Scholar
  55. Provenza, F.D. 1994. Ontogeny and social transmission of food selection in domesticated ruminants, pp. 147–164,in B.G. Galef, Jr., M. Mainardi, and P. Valsecchi (eds.). Behavioral Aspects of Feeding: Basic and Applied Research in Mammals. Harwood Academic Publishers, Singapore.Google Scholar
  56. Provenza, F.D. 1995. Postingestive feedback as an elementary determinant of food preference and intake in ruminants.J. Range Manage. 48:2–17.Google Scholar
  57. Provenza, F.D., andBalph, D.F. 1990. Applicability of five diet-selection models to various foraging challenges ruminants encounters, pp. 423–459,in R.N. Hughes (ed.). Behavioural Mechanisms of Food Selection. NATO ASI Series G: Ecological Sciences, Vol. 20. Springer-Verlag, Berlin.Google Scholar
  58. Provenza, F.D., andCincotta, R.P. 1993. Foraging as a self-organizational learning process: Accepting adaptability at the expense of predictability, pp. 78–101,in R.N. Hughes (ed.). Diet Selection. Blackwell, London.Google Scholar
  59. Provenza, F.D., Burritt, E.A., Clausen, T.P., Bryant, J.P., Reichardt, P.B., andDistel, R.A. 1990. Conditioned flavor aversion: A mechanism for goats to avoid condensed tannins in blackbrush.Am. Nat. 136:810–828.Google Scholar
  60. Provenza, F.D., Lynch, J.J., andNolan, J.V. 1993a. The relative importance of mother and toxicosis in the selection of foods by lambs.J. Chem. Ecol. 19:313–323.Google Scholar
  61. Provenza, F.D., Lynch, J.J., andNolan, J.V. 1993b. Temporal contiguity between food ingestion and toxicosis affects the acquisition of food aversions in sheep.Appl. Anim. Behav. Sci. 38:269–281.Google Scholar
  62. Provenza, F.D., Lynch, J.J., andNolan, J.V. 1994a. Food aversion conditioned in anesthetized sheep.Physiol. Behav. 55:429–432.PubMedGoogle Scholar
  63. Provenza, F.D., Lynch, J.J., Burritt, E.A., andScott, C.B. 1994b. How goats learn to distinguish between novel foods that differ in postingestive consequences.J. Chem. Ecol. 20:609–624.Google Scholar
  64. Provenza, F.D., Lynch, J.J., andCheney, C.D. 1995. An experimental analysis of the effects of a flavor and food restriction on the response of sheep to novel foods. Appl. Anim. Behav. Sci. In press.Google Scholar
  65. Reinhardt, V., andReinhardt, A. 1981. Cohesive relationships in a cattle herd (Bos indicus).Behaviour 77:121–151.Google Scholar
  66. Revusky, S.H., andBedarf, E.W. 1967. Association of illness with prior ingestion of novel foods.Science 155:219–220.PubMedGoogle Scholar
  67. Roath, L.R., andKrueger, W.C. 1982. Cattle grazing and behavior on a forested range.J. Range Manage. 35:332–338.Google Scholar
  68. Roll, D.L., andSmith, J.C. 1972. Conditioned taste aversion in anesthetized rats, pp. 98–102,in M.E.P. Seligman and J.L. Hager (eds.). Biological Boundaries of Learning. Appleton-Century-Crofts, New York.Google Scholar
  69. Sacks, O. 1990. The Man Who Mistook His Wife for a Hat. Harper Collins, New York.Google Scholar
  70. Scott, C.B., Provenza, F.D., andBanner, R.E. 1995. Dietary habits and social interactions affect choice of foraging location by sheep.Appl. Anim. Behav. Sci. In press.Google Scholar
  71. Squibb, R.C., Provenza, F.D., andBalph, D.F. 1990. Effect of age of exposure on consumption of a shrub by sheep.J. Anim. Sci. 68:987–997.PubMedGoogle Scholar
  72. Thorhallsdottir, A.G., Provenza, F.D., andBalph, D.F. 1987. Food aversion learning in lambs with or without a mother: Discrimination, novelty and persistence.Appl. Anim. Behav. Sci. 18:327–340.Google Scholar
  73. Thorhallsdottir, A.G., Provenza, F.D., andBalph, D.F. 1990. Ability of lambs to learn about novel foods while observing or participating with social models.Appl. Anim. Behav. Sci. 25:25–33.Google Scholar
  74. Wilson, E.O. 1992. The Diversity of Life. Harvard Press, Cambridge, Massachusetts.Google Scholar
  75. Yeates, N.T.M., andSchmidt, P.J. 1974. Beef Cattle Production. Butterworth, Sidney, Australia.Google Scholar

Copyright information

© Plenum Publishing Corporation 1995

Authors and Affiliations

  • Frederick D. Provenza
    • 1
  1. 1.Department of Rangeland ResourcesUtah State UniversityLogan

Personalised recommendations