Skip to main content
Log in

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

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

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.

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.

Similar content being viewed by others

References

  • Anderson, R. 1991. Habitat deterioration and the migratory behaviour of moose (Alces alces L.) in Norway.J. Appl. Ecol. 28:102–108.

    Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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 

  • Brett, L.P., Hankins, W.G., andGarcia, J. 1976. Prey-lithium aversions III: Buteo hawks.Behav. Biol. 17:87–98.

    PubMed  Google Scholar 

  • Buresova, O., andBures, J. 1973. Cortical and subcortical components of the conditioned saccharin aversion.Physiol. Behav. 11:435–439.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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 

  • 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.

  • Cederlund, G., andOkama, H. 1988. Home range and habitat use of adult female moose.J. Wildl. Manage. 52:336–343.

    Google Scholar 

  • 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 

  • Chapple, R.S., andLynch, J.J. 1986. Behavioral factors modifying acceptance of supplementary foods by sheep.Res. Dev. Agric. 3:113–120.

    Google Scholar 

  • 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 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Easterbrook, G. 1994. The birds.The New Republic. March: 22–24.

  • Festa-Bianchet, M. 1986a. Seasonal dispersion of overlapping mountain sheep ewe groups.J. Wildl. Manage. 50:325–330.

    Google Scholar 

  • Festa-Bianchet, M. 1986b. Site fidelity and seasonal range use by bighorn rams.Can. J. Zool. 64:2126–2132.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

  • Garcia, J., andKoelling, R.A. 1986. Relation of cue to consequence in avoidance learning.Psychon. Sci. 4:123–124.

    Google Scholar 

  • 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 

  • 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 

  • Geist, V. 1971. Mountain Sheep: A Study in Behavior and Evolution. University of Chicago Press, Chicago.

    Google Scholar 

  • 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 

  • 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 

  • Gruell, G.E., andPapez, N.J. 1963. Movements of mule deer in northeastern Nevada.J. Wildl. Manage. 27:414–422.

    Google Scholar 

  • 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 

  • Histol, T., andHjeljord, O. 1993. Winter feeding strategies of migrating and nonmigrating moose.Can. J. Zool. 71:1421–1428.

    Google Scholar 

  • 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.

  • 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.

  • 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 

  • 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 

  • 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 

  • Kalat, J.W., andRozin, P. 1971. Role of interference in taste-aversion learning.J. Comp. Physiol. Psychol. 77:53–58.

    PubMed  Google Scholar 

  • 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 

  • 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 

  • Lawrence, A.B. 1990. Mother-daughter and peer relationships of Scottish hill sheep.Anim. Behav. 39:481–486.

    Google Scholar 

  • Launchbaugh, K.L., andProvenza, F.D. 1993. Can plants practice mimicry to avoid grazing by mammalian herbivores?Oikos 66:501–504.

    Google Scholar 

  • 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 

  • LeDoux, J.E. 1992. Brain mechanisms of emotion and emotional learning.Curr. Opin. Neurobiol. 2:191–197.

    PubMed  Google Scholar 

  • LeDoux, J.E. 1994. Emotion, memory and the brain.Sci. Am. 270:50–57.

    Google Scholar 

  • Lett, B.T. 1985. The pain-like effect of gallamine and naloxone differs from sickness induced by lithium chloride.Behav. Neurosci. 99:145–150.

    PubMed  Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

  • Mirza, S.N., andProvenza, F.D. 1994. Socially induced food avoidance in lambs: Direct or indirect maternal influence?J. Anim. Sci. 72:899–902.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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 

  • Phy, T.S. andF.D. Provenza. 1995. Sheep acquire preferences for substances that rectify lactic acidosis.J. Anim. Sci., submitted.

  • Porter, W.F. 1992. High fidelity deer.Nat. Hist. May:48–49.

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • Provenza, F.D., Lynch, J.J., andNolan, J.V. 1994a. Food aversion conditioned in anesthetized sheep.Physiol. Behav. 55:429–432.

    PubMed  Google Scholar 

  • 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 

  • 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.

  • Reinhardt, V., andReinhardt, A. 1981. Cohesive relationships in a cattle herd (Bos indicus).Behaviour 77:121–151.

    Google Scholar 

  • Revusky, S.H., andBedarf, E.W. 1967. Association of illness with prior ingestion of novel foods.Science 155:219–220.

    PubMed  Google Scholar 

  • Roath, L.R., andKrueger, W.C. 1982. Cattle grazing and behavior on a forested range.J. Range Manage. 35:332–338.

    Google Scholar 

  • 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 

  • Sacks, O. 1990. The Man Who Mistook His Wife for a Hat. Harper Collins, New York.

    Google Scholar 

  • 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.

  • 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.

    PubMed  Google Scholar 

  • 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 

  • 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 

  • Wilson, E.O. 1992. The Diversity of Life. Harvard Press, Cambridge, Massachusetts.

    Google Scholar 

  • Yeates, N.T.M., andSchmidt, P.J. 1974. Beef Cattle Production. Butterworth, Sidney, Australia.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Provenza, F.D. Tracking variable environments: There is more than one kind of memory. J Chem Ecol 21, 911–923 (1995). https://doi.org/10.1007/BF02033798

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02033798

Key Words

Navigation