Veterinary Science Communications, 3 (1979) Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
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1 Veterinary Science Communications, 3 (1979) Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands 165 TASTE AVERSION LEARNING IN SUCKLING AND WEANLING PIGS K. A. HOUPT, D. M. ZAHORIK, S. M. ANIKA and T. R. HOUPT Department of Physiology, Biochemistry and Pharmacology and Department of Psychology, Cornell University, Ithaca, New York (U.S.A.) Supported by N.S.F. Grant BNS NIH Grant AM-1760l (Accepted 22 January 1979) ABSTRACT Houpt, K. A., Zahorik, D. M., Anika, S. M. and Houpt, T. R., Taste aversion learning in suckling and weanling pigs. Vet. Sci. Commun., 3: Pigs are able to learn to avoid a novel flavor that has previously been associated with gastrointestinal malaise. Suckling pigs were allowed to nurse from maple syrup coated teats and then were injected with 0.3 M LiCl i.p. Littermates controls were injected with 0.9% NaCl. Three days later the LiCl treated piglets did not ingest as much milk from maple syrup coated teats as their littermate controls. Weanling pigs were treated with 0.05 mg/kg apomorphine i.v. or 0.3 M LiCl 5 ml/kg intraduodenally immediately after their first meal of maple flavored feed. When maple flavored feed was offered to them again several days later they ate less than they did initi~lly and less than controls which had been treated with 0.9% NaCI after their first maple flavored meal. The implications of taste aversion learning in pigs for both research and swine production are discussed. INTRODUCTION The concept of nutritional wisdom has been widely accepted (Richter, 1943), but it has become apparent that much of that wisdom is learned rather than innate. In fact, only sodium hunger in mammals has been shown to be innate (Denton, 1967). In other deficiencies the animals learn to eat those things that increase their sense of well being and learn to avoid those foods that make them sick. The latter type of learning is called taste aversion learning and has been demonstrated in a wide variety of animals including rodents and carnivores (Garcia et al., 1974). Taste aversion learning has not been demonstrated in pigs, however, despite the practical and theoretical implications that the presence or absence of that particular learning ability in a large omnivorous ungulate would have. This study was a preliminary effort to demonstrate taste aversion learning in suckling and weanling pigs. ticular learning ability in a large omnivorous ungulate would have. This study
2 166 EXPERIMENT 1 Methods Six weanling Yorkshire pigs, 4-8 weeks of age and weighing kg, were individually housed in stainless steel dog cages. (Squealer, Agway Incorporated, Syracuse, New York). They were fed a pelleted pig feed The daily routine was to fast the pigs for 4 hours and then to give them a weighed amount of feed for a twenty minute feeding period. On injection days the feed pellets were mixed with maple flavored syrup (Log Cabin, General Foods Corporation, Mlite Plains, New York) a ratio of 50 ml of syrup/kg feed. Intake was measured for 5 minutes and then an agent was administered that produces gastrointestinal malaise for no longer than a few hours. After three additional days of feeding plain pellets, the pigs were again presented with the maple flavored pellets on the fourth or test day. minute food intake was again recorded. at Five The difference in intake between the injection day and the test day was used to determine whether the pigs formed an aversion. For the injection procedure silicone rubber catheters were implanted: catheters were placed in the jugular vein of 4 pigs and in the duodenum of 2 pigs (Pond and Houpt, 1978). Two of the pigs with jugular catheters were infused with 0.05 mg/kg apomorphine hydrochloride immediately after they had eaten the maple flavored pellets for the first time; the other 2 pigs were infused with an equivalent volume of 0.9% NaCl immediately after eating the flavored pellets. a duodenal catheter was infused with 5 ml/kg of 0.3 M LiCI One of the pigs with immediately after it had eaten maple flavored pellets for the first time; the other pig was infused with an equivalent volume of 0.9% NaCl immediately after it had eaten maple flavored pellets. Results The results of the pairing of either a toxic agent (apomorphine) or a neutral agent (0.9% NaCl) with a novel food are seen in Fig. 1. All the pigs ate a large quantity of the maple-flavored pellets on their first exposure to it (left column of each pair of columns), but, although the pigs that had been treated on the first or injection day with 0.9% NaCl again ate a large amount, 65.5 ± 4 g, on the test day four days after the injection day, the pigs that had been treated with apomorphine on their first -exposure to the novel food ate only 29.5 ± 4 g on their test day. The results following LiCl administration were similar. On the injection day, the pig ate 94 g of maple flavored pellets; on the test day it ate only 3 g. The control pig ate 114 g of maple flavored pellets on the injection day and 134 g on the test day. The results following LiCl administration were similar. On the injection day, the pig ate 94 ~ of maple flavored pellets: on the test day it ate only ~ g_ The
3 D, st day ~ 3 days later ±SEM OL..._-L--~~~---_..._~~~ %NaCI APOMORPHINE INTRAJUGULAR INJECTIONS Fig. 1. Taste aversion tests in suckling pigs. Clear columns: intake of feed with novel flavor just before injection of 0.9% NaCI or apomorphine. Cross-hatched columns: intake 3 days later of same flavored feed. EXPERIMENT 2 Methods Two litters of Yorkshire piglets (n = 20), 2-7 days old and nursing from their dams, were removed from the sows and fasted for three hours. They were placed in a pen adjacent to their dam's and provided with a heat lamp for the duration of the fast. Following the fast the piglets were weighed and then returned to the sows, the udders of which had been spread with maple syrup. As soon as the sow had permitted the piglets to nurse for 5 minutes, the litter was again removed. Half of each litter was injected with 10 ml/kg body weight 0.3 M LiCl; the other half was injected with an equivalent volume of 0.9% NaCl (0.15 M). Control and Liel treated littermates were carefully matched on a body weight basis. Three days later the pigs were again fasted. Following the fast they were weighed individually and returned to the sows the udders of which had again been spread with maple syrup. The piglets remained with the sow for 3 hours and then were reweighed to determine three hour milk intake. Results Piglets exposed to maple syrup flavored teats just before injection of LiCI.L _... --,- -_ "'......, J.I.'\J\"A..L ~...,I... u, \...11.""".11. " v.l vyy Il;;~o11~U to determine three hour milk intake.
4 168 gained only 50 ± 14 g (n = 10) when again exposed to maple flavored teats three days later after they had recovered from the effects of LiCl. Littermates exposed to the maple flavored teats just before being injected with 0.9% NaCl gained 79 ± 22 g. A paired t test of the weight matched control and experimental piglets indicated that the difference in intake was significant (p < 0.01). DISCUSSION Pigs, even suckling pigs, are able to learn to avoid a food that has previously been associated with illness. Pigs, therefore, are capable of forming a taste aversion. Formation of a taste aversion by pigs may account for instances of anorexia in pigs that may have been ill after eating that particular feed in the past. The illness may have been caused by some toxin, a mold in corn for example, or by an infectious agent, but, because the taste of the food is associated with the illness, the food itself is avoided. Formation of a taste aversion may also account for the failure of pigs to eat deficient or imbalanced diets in experimental situations (Robinson, 1975). The reason why taste aversion learning is very valuable to the research worker is that it can be used to demonstrate that a given procedure or drug causes illness. In some cases illness may be sub-clinical but still be sufficient to cause the formation of a taste aversion. For example, there were no overt signs of toxicosis with the low dose of apomorphine employed in this study, but the pigs formed a strong aversion for the food indicating that they did feel sick after the injection. Pigs have previously been shown to learn active avoidance tasks and mazes (Hammell et al., 1975), and they can also be operantly conditioned to press a panel with their snouts for food (Stephens and Baldwin, 1973) and for light (Baldwin and Meese, 1977). Kennedy and Baldwin (1972) reported that pigs ingesting large amounts of sucrose became ill, but did not form an aversion to sucrose. The failure of those pigs to form an aversion is probably due to their repeated exposure to sucrose before they became ill. They had learned that the sucrose was a safe food (Rozin, 1967). Animals learn most quickly to avoid a novel food that was associated with the illness on its very first presentation. The converse situation or "learned safety" may be taken advantage of to stimulate solid food intake of weanling pigs by flavoring the food with a flavor that had been present in their dam's milk (Campbell, 1976). CONCLUSION Pigs are able to learn to avoid a food that has previou~ly been associated with illness. The ability of pigs to form a taste aversion may explain some aspects of feeding behavior in farm and laboratory pigs. The ability can be used to differentiate pharmacological or toxicological effects from physiological ones. CONCLUSION
5 169 REFERENCES Baldwin, B. A. and Meese, G. B., Sensory reinforcement and illumination preference in the domestic pig. Animal Behavio~ 25: Campbell, R. G., A note on the use of a feed flavor to stimulate the feed intake of weaner pigs. Animal Production, 23: Denton, D. A., Salt Appetite. In: C. F. Code (Editor), Handbook of Physiology. Section 6. Alimentary Canal. Vol. 1 Food and Water Intake. American Physiological Society, Washington, D. C. pp Garcia, J., Hankins, W. G. and Rusiniak, K. W., Behavioral regulation of the milieu interne in man and rat. Science, 185: Hammell, D. L., Kratzer, D. D. and Bramble, W. J., Avoidance and maze learning in pigs. Journal of Animal Science, 40: Kennedy, J. M. and Baldwin, B. A., Taste preferences in pigs for nutritive and non-nutritive sweet solutions. Animal Behaviour, 20: Pond, W. G. and Houpt, K. A., The Biology of the Pig. Cornell University Press, Ithaca, PP 371. Richter, C. P., Total self-regulatory functions in animals and human beings. Harvey Lecture Series, 38: Robinson, E. W., Food intake regulation in pigs. IV. The influence of dietary threonine imbalance on food intake, dietary choice and plasma acid patterns. British Veterinary Journal, 131: Rozin, P., Thiamine specific hunger. In: C. F. Code (Editor), Handbook of Physiology. Section 6. Alimentary Canal. Vol. 1 Food and Water Intake. American Physiological Society, Washington, D. C. pp Stephens, D. B. and Baldwin, B. A., The lack of effect of intrajugular or intraportal injections of glucose or amino acids on feed intake in pigs. Physiology and Behavior, 12:
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