Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-14T17:29:18.633Z Has data issue: false hasContentIssue false
  • English
  • Français

Conditioned food aversions: principles and practices, with special reference to social facilitation

Published online by Cambridge University Press:  28 February 2007

Michael H. Ralphs  and
Frederick D. Provenza
Michael H. Ralphs*
Affiliation:
USDA/ARS Poisonous Plant Laboratory, Logan, Utah 84341, USA
Frederick D. Provenza
Affiliation:
Rangeland Resources Department, Utah State University, Logan, Utah 84322, USA
*
*Corresponding Author: Dr Michael H. Ralphs, fax +1 435 753 5681, email mralphs@cc.usu.edu
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Conditioned food aversion is a powerful experimental tool to modify animal diets. We have also investigated it as a potential management tool to prevent livestock from grazing poisonous plants such as tall larkspur (Delphinium barbeyi), white locoweed (Oxytropis sericea) and ponderosa pine (Pinus ponderosa) on western US rangelands. The following principles pertain to increasing the strength and longevity of aversions: mature animals retain aversions better than young animals; novelty of the plant is important, although aversions can be created to familiar plants; LiCl is the most effective emetic, and the optimum dose for cattle is 200 mg/kg body weight; averted animals should be grazed separately from non-averted animals to avoid the influence of social facilitation which can rapidly extinguish aversions. Social facilitation is the most important factor preventing widespread application of aversive conditioning. When averted animals see other animals eat the target food they will sample it, and if there is no adverse reaction they will continue eating and extinguish the aversion. However, if averted animals can be grazed separately, aversions will persist. Aversive conditioning may provide an effective management tool to prevent animals from eating palatable poisonous plants that cause major economic loss.

Keywords

Diet selectionConditioned food aversionSocial facilitationPoisonous plants
Type
Symposium on ‘Social and environmental influences on diet choice’
Information
Proceedings of the Nutrition Society , Volume 58 , Issue 4 , November 1999 , pp. 813 - 820
Copyright
The Nutrition Society

References

Andrews, EA & Braveman, NS (1975) The combined effects of dosage level and interstimulus interval in the formation of one trial poison-based aversions in rats. Animal Learning and Behavior 3, 287–289.CrossRefGoogle Scholar
Archer, T, Sjoden, PO & Nilsson, LG (1985) Contextual control of taste-aversion conditioning and extinction. In Context and Learning, pp. 225–271 [Balsam, PD and Tomie, A, editors]. Hillsdale, NJ: Lawrence Erlbaum Associates.Google Scholar
Balsam, PD (1985) The functions of context in learning and performance. In Context and Learning, pp. 1–21 [Balsam, PD and Tomie, A, editors]. Hillsdale, NJ: Lawrence Erlbaum Associates.Google Scholar
Best, MR & Barker, LM (1977) The nature of learned safety and its role in the delay of reinforcement gradient. In Learning Mechanisms in Food Selection, pp. 295–325 [Barker, LM, Best, MR and Domjan, M, editors]. Waco, TX: Baylor University Press.Google Scholar
Best, PJ, Best, MR & Henggeler, S (1977) The contribution of environmental non-ingestive cues in conditioning with aversive internal consequences. In Learning Mechanisms in Food Selection, pp. 371–389 [Barker, LM, Best, MR and Domjan, M, editors]. Waco, TX: Baylor University Press.Google Scholar
Braveman, NS & Bronstein, P (editors) (1985) Experimental assessments and clinical applications of conditioned food aversions. Annals of the New York Academy of Sciences 443, 441.Google Scholar
Braveman, NS & Crane, J (1977) Amount consumed and the formation of conditioned taste aversions. Behavioral Biology 21, 470–477.CrossRefGoogle ScholarPubMed
Burritt, EA & Provenza, FD (1989) Food aversion learning: conditioning lambs to avoid a palatable shrub (Cercocarpus montanus). Journal of Animal Science 67, 650–653.CrossRefGoogle Scholar
Burritt, EA & Provenza, FD (1991) Ability of lambs to learn with a delay between ingestion and consequences given meals containing novel and familiar foods. Applied Animal Behavior Science 32, 179–189.CrossRefGoogle Scholar
Burritt, EA & Provenza, FD (1992) Lambs form preferences for nonnutritive flavors paired with glucose. Journal of Animal Science 70, 1133–1136.CrossRefGoogle ScholarPubMed
Burritt, EA & Provenza, FD (1996) Amount of experience and prior illness affect the acquisition and persistence of conditioned food aversions in lambs. Applied Animal Behavior Science 48, 73–80.CrossRefGoogle Scholar
Burritt, EA & Provenza, FD (1997) Effect of an unfamiliar location on the consumption of novel and familiar foods by sheep. Applied Animal Behavior Science 54, 317–325.CrossRefGoogle Scholar
Clayton, DA (1978) Socially facilitated behavior. Quarterly Review of Biology 53, 373–391.Google Scholar
Dragoin, WB (1971) Conditioning and extinction of taste aversions with variations in intensity of the CS and UCS in two strains of rats. Psychonomic Science 22, 303–304.CrossRefGoogle Scholar
Duncan, AJ, Frutos, P & Kyriazakis, I (1998) Conditioned food aversions to oxalic acid in the food plants of sheep and goats. In Toxic Plants and Other Natural Toxicants, pp. 169–173 [Garland, T and Barr, AC, editors]. Wallingford, Oxon: CAB International.Google Scholar
du Toit, JT, Provenza, FD & Nastis, A (1991) Conditioned taste aversions: how sick must a ruminant get before it learns about toxicity in foods? Applied Animal Behavior Science 30, 35–40.CrossRefGoogle Scholar
Emmans, GC & Kyriazakis, I (1995) The idea of optimization in animals: uses and dangers. Livestock Production Science 44, 189–197.CrossRefGoogle Scholar
Fenwick, S, Miluka, PJ & Klein, SB (1975) The effect of different levels of preexposure to sucrose on the acquisition and extinction of a conditioned aversion. Behavioral Biology 14, 231–235.CrossRefGoogle ScholarPubMed
Fisher, DS, Burns, JC & Mayland, HF (1997) Variation in preference for morning or afternoon harvested hay in sheep, goats, and cattle. Journal of Animal Science 75, Suppl., 201.Google Scholar
Franchina, JJ & Horowitz, SW (1982) Effects of age and flavor preexposures on taste aversion performance. Bulletin of the Psychonomic Society 19, 41–44.Google Scholar
Freeland, WJ & Janzen, DH (1974) Strategies in herbivory by mammals; the role of plant secondary compounds. American Naturalist 108, 269–289.CrossRefGoogle Scholar
Galef BG, Jr (1986) Social interaction modifies learned aversions, sodium appetite, and both palatability and handling-time induced dietary preference in rats (Rattus norvegicus). Journal of Comparative Psychology 100, 432–439.CrossRefGoogle ScholarPubMed
Galef BG, Jr (1985) Socially induced diet preference can partially reverse a LiCl-induced diet aversion. Animal Learning and Behavior 13, 415–418.CrossRefGoogle Scholar
Galef BG, Jr, Kennett, DJ & Stein, M (1985) Demonstrator influence on observer diet preference: effects of simple exposure and the presence of a demonstrator. Animal Learning and Behavior 13, 25–30.CrossRefGoogle Scholar
Garcia, J (1989) Food for Tolman: cognition and cathexis in concert. In Aversion, Avoidance, and Anxiety, pp. 45–85 [Archer, T and Nilsson, L, editors]. Hillsdale, NJ: Lawrence Erlbaum Associates.Google Scholar
Garcia, J, Ervin, FR & Koelling, RA (1966) Learning with prolonged delay of reinforcement. Psychonomic Science 5, 121–122.CrossRefGoogle Scholar
Garcia, J & Holder, MD (1985) Time, space and value. Human Neurobiology 4, 81–89.Google ScholarPubMed
Grote, FW Jr & Brown, RT (1973) Deprivation level affects extinction of conditioned taste aversion. Learning and Motivation 4, 314–319.CrossRefGoogle Scholar
Guanowsky, V, Misanin, JR & Riccio, DC (1983) Retention of conditioned taste aversion in weanling, adult and old-age rats. Behavioral and Neural Biology 37, 173–178.CrossRefGoogle ScholarPubMed
Gustavson, CR & Gustavson, JC (1985) Predation control using conditioned food aversion methodology: theory, practice, and implications. Annals of the New York Academy of Sciences 443, 348–356.CrossRefGoogle ScholarPubMed
Johnson, JH, Crookshank, HR & Smolley, HE (1980) Lithium toxicity in cattle. Veterinary Human Toxicology 22, 248–251.Google ScholarPubMed
Kalat, JW & Rozin, P (1973) ‘Learned safety’ as a mechanism in long-delay taste-aversion learning in rats. Journal of Comparative and Physiological Psychology 83, 198–207.CrossRefGoogle ScholarPubMed
Kimball, BA (1997) Chemical ecology of vascular tissue foraging by black bears.PhD Thesis, Colorado State University, USA.Google Scholar
Kronberg, SL, Muntifering, RB, Ayers, EL & Marlow, CB (1993) Cattle avoidance of leafy spurge: a case of conditioned aversion. Journal of Range Management 46, 364–366.CrossRefGoogle Scholar
Kruz, EM & Levitsky, DA (1982) Novelty of contextual cues in taste aversion learning. Animal Learning Behavior 10, 229–232.CrossRefGoogle Scholar
Kyriazakis, I, Anderson, DH & Duncan, AJ (1998) Conditioned flavour aversions in sheep: the relationship between the dose rate of a secondary plant compound and the acquisition and persistence of aversions. British Journal of Nutrition 79, 55–62.CrossRefGoogle ScholarPubMed
Kyriazakis, I, Papachristou, TG, Duncan, AJ & Gordon, IJ (1997) Mild conditioned food aversions developed by sheep towards flavors associated with plant secondary compounds. Journal of Chemical Ecology 23, 727–746.CrossRefGoogle Scholar
Lane, MA, Ralphs, MH, Olsen, JD, Provenza, FD & Pfister, JA (1990) Conditioned taste aversion: potential for reducing cattle loss to larkspur. Journal of Range Management 43, 127–131.CrossRefGoogle Scholar
Launchbaugh, KL, Provenza, FD & Burritt, EA (1993) How herbivores track variable environments: response to variability of phytotoxins. Journal of Chemical Ecology 19, 1047–1056.CrossRefGoogle ScholarPubMed
Laycock, WA (1978) Coevolution of poisonous plants and large herbivores on rangelands. Journal of Range Management 31, 335–342.CrossRefGoogle Scholar
Logue, AW (1985) Conditioned food aversion learning in humans. Annals of the New York Academy of Sciences 443, 316–329.CrossRefGoogle ScholarPubMed
Lubow, RE, Bathsheva, R & Aick, M (1976) The context effect: the relationship between stimulus preexposure and environmental preexposure determines subsequent learning. Journal of Experimental Psychology 2, 38–47.Google Scholar
McArthur, C, Hagerman, AE & Robbins, CT (1991) Physiological strategies of mammalian herbivores against plant defenses. In Plant Defenses Against Mammalian Herbivory, pp. 103–114 [Palo, RT and Robins, CT, editors]. Boca Raton, FL: CRC Press.Google Scholar
Miller, RR & Schachtman, TR (1985) The several roles of context at time of retrieval. In Context and Learning, pp. 167–194 [Balsam, PD and Tomie, A, editors]. Hillsdale, NJ: Lawrence Erlbaum Associates.Google Scholar
Mitchell, D, Kirschbaum, EH & Perry, RL (1975) Effects of neophobia and habituation on the poison-induced avoidance of exteroceptive stimuli in the rat. Journal of Experimental Psychology 104, 47–55.Google Scholar
Nachman, M & Ashe, JA (1973) Learned taste aversion in rats as a function of dosage, concentration, and rate of administration of LiCl. Physiological Behavior 10, 73–77.CrossRefGoogle Scholar
Nachman, M, Rauschenberger, J & Ashe, JH (1977) Stimulus characteristics in food aversion learning. In Food Aversion Learning, pp. 105–131 [Milgram, NW, Krames, L and Alloway, TM, editors]. New York: Plenum Press.CrossRefGoogle Scholar
Nathan, PE (1985) Aversion therapy in the treatment of alcoholism: success and failure. Annals of the New York Academy of Sciences 443, 357–364.CrossRefGoogle ScholarPubMed
Pfister, JA, Provenza, FD, Manners, GD, Gardner, DR & Ralphs, MR (1997) Tall larkspur ingestion: can cattle regulate intake below toxic levels? Journal of Chemical Ecology 23, 759–777.CrossRefGoogle Scholar
Provenza, FD (1995) Postingestive feedback as an elementary determinant of food preference and intake in ruminants. Journal of Range Management 48, 2–17.CrossRefGoogle Scholar
Provenza, FD (1996) Acquired aversions as the basis for varied diets of ruminants foraging on rangelands. Journal of Animal Science 74, 2010–2020.CrossRefGoogle ScholarPubMed
Provenza, FD & Balph, DF (1988) Development of dietary choice in livestock on rangelands and its implications for management. Journal of Animal Science 66, 2356–2368.CrossRefGoogle Scholar
Provenza, FD, Burritt, EA, Clausen, TP, Bryant, JP, Reichardt, PB & Distel, RA (1990) Conditioned flavor aversion: a mechanism for goats to avoid condensed tannins in blackbrush. American Naturalist 136, 810–828.CrossRefGoogle Scholar
Provenza, FD, Lynch, JJ & Nolan, JV (1993) The relative importance of mother and toxicosis in the selection of foods by lambs. Journal of Chemical Ecology 19, 313–323.CrossRefGoogle ScholarPubMed
Provenza, FD, Ortega-Reyes, L, Scott, CB, Lynch, JJ & Burritt, EA (1994) Antiemetic drugs attenuate food aversions in sheep. Journal of Animal Science 72, 1989–1994.CrossRefGoogle ScholarPubMed
Provenza, FD, Villalba, JJ, Cheney, CD & Werner, SJ (1998) Self-organization of foraging behaviour: from simplicity to complexity without goals. Nutrition Research Reviews 11, 1–24.CrossRefGoogle ScholarPubMed
Ralphs, MH (1997) Persistence of aversions to larkspur in naive and native cattle. Journal of Range Management 50, 367–370.CrossRefGoogle Scholar
Ralphs, MH (1999) Lithium residue in milk from doses used to create food aversions: effect on nursing calves. Applied Animal Behaviour Science 61, 285–293.CrossRefGoogle Scholar
Ralphs, MH & Cheney, CD (1993) Influence of cattle age, lithium chloride dose level, and food type in the retention of food aversions. Journal of Animal Science 71, 373–379.CrossRefGoogle ScholarPubMed
Ralphs, MH, Graham, D, Galyean, ML & James, LF (1997) Creating aversions to locoweed in naive and familiar cattle. Journal of Range Management 50, 361–366.CrossRefGoogle Scholar
Ralphs, MH, Graham, D & James, LF (1994) Social facilitation influences cattle to graze locoweed. Journal of Range Management 47, 123–126.CrossRefGoogle Scholar
Ralphs, MH & Olsen, JD (1990) Adverse influence of social facilitation and learning context in training cattle to avoid eating larkspur. Journal of Animal Science 68, 1944–1952.CrossRefGoogle ScholarPubMed
Ralphs, MH & Olsen, JD (1992) Comparison of larkspur alkaloid extract and lithium chloride in maintaining cattle aversion to larkspur in the field. Journal of Animal Science 70, 1116–1120.CrossRefGoogle ScholarPubMed
Ralphs, MH & Stegelmeier, BE (1998) Comparison of apomorphine and lithium chloride in creating food aversions in cattle. Applied Animal Behavior Science 56, 129–137.Google Scholar
Revusky, S, Pohl, RW & Coombes, S (1980) Flavor aversions and deprivation state. Animal Learning and Behavior 8, 543–549.CrossRefGoogle Scholar
Riley, AL & Tuck, DL (1985) Conditioned taste aversion: a behavioral index to toxicity. Annals of the New York Academy of Sciences 443, 272–292.CrossRefGoogle ScholarPubMed
Rozin, P & Kalat, JW (1971) Specific hungers and poison avoidance as adaptive specializations of learning. Psychological Review 78, 459–485.CrossRefGoogle ScholarPubMed
Sclafani, A (1996) How food preferences are learned: laboratory animal models. Proceedings of the Nutrition Society 54, 419–427.CrossRefGoogle Scholar
Scott, TR (1990) Gustatory control of food selection. In Handbook of Behavioral Neurobiology, Vol. 10, pp. 243–263 [Stricker, EM, editor]. New York: Plenum Press.Google Scholar
Shumake, SA, Sterner, RT, Gaddis, SE & Crane, KA (1982) Conditioned taste aversion in Philippine rice rats (Ratus mindanensis): comparisons among drugs, dosages, modes of administration, and sexes. Animal Learning and Behavior 10, 499–504.CrossRefGoogle Scholar
Springer, AD & Fraley, SM (1981) Extinction of a conditioned taste aversion in young, mid-aged, and aged C57/BL6 mice. Behavior Neural Biology 32, 282–294.Google ScholarPubMed
Squibb, RC, Provenza, FD & Balph, DF (1990) Effect of age of exposure on consumption of a shrub by sheep. Journal of Animal Science 68, 987–997.CrossRefGoogle ScholarPubMed
Steinert, PA, Infurna, RN & Spear, NE (1980) Long-term retention of a conditioned taste aversion in preweanling and adult rats. Animal Learning and Behavior 8, 375–381.CrossRefGoogle Scholar
Testa, TJ & Ternes, JW (1977) Specificity of conditioning mechanisms in the modification of food preferences. In Learning Mechanisms in Food Selection, pp. 229–253 [Barker, LM, Best, MR and Domjan, M, editors]. Waco, TX: Baylor University Press.Google Scholar
Thorhallsdottir, AG, Provenza, FD & Balph, DF (1990) Social influences on conditioned food aversions in sheep. Applied Animal Behavioral Science 25, 45–50.CrossRefGoogle Scholar
Villalba, JJ & Provenza, FD (1996) Preference for flavored wheat straw by lambs conditioned with intraruminal administrations of sodium propionate. Journal of Animal Science 74, 2362–2368.CrossRefGoogle ScholarPubMed
Villalba, JJ & Provenza, FD (1997a) Preference for wheat straw by lambs conditioned with intraruminal infusions of starch. British Journal of Nutrition 77, 287–297.CrossRefGoogle ScholarPubMed
Villalba, JJ & Provenza, FD (1997b) Preference for flavoured foods by lambs conditioned with intraruminal administration of nitrogen. British Journal of Nutrition 78, 545–561.CrossRefGoogle ScholarPubMed
Villalba, JJ & Provenza, FD (1997c) Preference for flavored wheat straw by lambs conditioned with intraruminal infusions of acetate and propionate. Journal of Animal Science 75, 2905–2914.CrossRefGoogle ScholarPubMed
Villalba, JJ & Provenza, FD (1999) Effects of food structure and nutritional quality and animal nutritional state on intake behavior and food preferences in sheep. Applied Animal Behavior Science 61, 145–163.CrossRefGoogle Scholar
Wang, J & Provenza, FD (1996) Food deprivation affects preference of sheep for foods varying in nutrients and a toxin. Journal of Chemical Ecology 22, 2011–2021.CrossRefGoogle ScholarPubMed
Wang, J & Provenza, FD (1997) Dynamics of preference by sheep offered foods varying in flavors, nutrients, and a toxin. Journal of Chemical Ecology 23, 175–288.CrossRefGoogle Scholar
Wellman, PJ & Boissard, CG (1981) Influence of fluid deprivation level on the extinction of conditioned taste aversion induced by amphetamine in female rats. Physiological Psychology 9, 281–284.CrossRefGoogle Scholar
Zahorik, DM & Houpt, KA (1977) The concept of nutritional wisdom: applicability of laboratory learning models to large herbivores. In Learning Mechanisms in Food Selection, pp. 45–67 [Barker, LM, Best, MR and Domjan, M, editors]. Waco, TX: Baylor University Press.Google Scholar
Zahorik, DM & Houpt, KA (1981) Species differences in feeding strategies, food hazards, and the ability to learn food aversions. In Foraging Behavior, pp. 289–310 [Kamil, AC and Sargent, JD, editors]. New York: Garland.Google Scholar
Zajonc, RB (1968) Attitudinal effects of mere exposure. Journal of Personality and Social Psychology Monograph Suppl. 9, 1–27.Google Scholar