Journal of Comparative Physiology A

, Volume 159, Issue 3, pp 281–295

Post-ingestive food-aversion learning to amino acid deficient diets by the terrestrial slugLimax maximus

  • K. Delaney
  • A. Gelperin
Article

Summary

An agar-based artificial diet containing carbohydrates, fats and twenty amino acids was constructed (Fig. 1). This diet is highly palatable and nutritionally complete forLimax maximus as demonstrated by significant ingestion on first encounter, consistent ingestion on subsequent days and good growth of young slugs fed this diet. Removing methionine, an essential amino acid, from the complete diet produces a food which is initially as palatable as the complete diet, but after one day's intake the amount of this deficient diet eaten is greatly reduced (Fig. 2). Removing alanine, a nonessential amino acid, does not produce any decrement in feeding relative to the complete diet (Fig. 5).

A single meal can be sufficient for establishing the aversion to the deficient diet (Fig. 5). Following seven days of feeding on the deficient diet the aversion is retained with little or no attenuation for at least 30 days (Fig. 3) and does not generalize to either a known ‘safe’ food (Fig. 3) or a novel food (Fig. 4). Evidence of a mild neophobia towards the artificial diet which attenuated after one or two meals was seen (Fig. 5).

The learned aversion to the deficient diet is reversible if slugs are repeatedly fed the complete diet following feeding on the deficient diet. Also, slugs initially fed the complete diet will develop an aversion to the methionine-deficient diet after sampling it (Fig. 7).

Slugs readily ate the artificial diets when these were offered 7 days post-hatch. The methionine-deficient diet however was not eaten in large amounts after the first meals and did not support growth (Fig. 9). Baby slugs fed the methionine-deficient diet for 10 days and then maintained on rat chow ate only small amounts when the deficient diet was presented again 126 days later, while baby slugs fed the complete diet or an alanine deficient diet for 10 days ate large amounts when these diets were presented 126 days later (Fig. 11 b).

Supplementing the methionine-deficient diet with an injection of methionine into the haemocoel one hour after the completion of a meal completely blocks the development of a learned aversion while injection ofLimax saline does not (Fig. 8).

These results are best explained by the hypothesis that the slugs acquire, post-ingestively, an aversion to the taste and probably the odor of the diet as the result of associative learning. The results of the experiments reported here indicate that there are substantial parallels at the behavioral level between mollusc and mammal with respect to post-ingestive feedback learning.

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References

  1. Altman PL, Dittmer DS (1968) Metabolism. Biological handbooks, Federation of American Societies for Experimental Biology, Bethesda MarylandGoogle Scholar
  2. Barker LM, Best MR, Domjan M (eds) (1977) Learning mechanisms in food selection. Baylor Univ Press, Waco TexasGoogle Scholar
  3. Booth DA, Simson PC (1974) Taste aversion induced by an histidine-free amino acid load. Physiol Psych 2:349–351Google Scholar
  4. Carefoot TH (1980) Studies on the nutrition and feeding preferences ofAplysia: Development of an artificial diet. J Exp Mar Biol Ecol 42:241–252Google Scholar
  5. Cates RG (1975) The interface between slugs and wild ginger: some evolutionary aspects. Ecology 56:391–400Google Scholar
  6. Cates RG, Orians GH (1975) Successional status and the palatability of plants to generalized herbivores. Ecology 56:410–418Google Scholar
  7. Cooke I, Delaney K, Gelperin A (1985) Complex computation in a small neural network. In: Weinberger NM, McGaugh JL, Lynch G (eds) Memory systems and the brain. The Guilford Press, New York, NY, pp 173–192Google Scholar
  8. Delaney K (1982) Post-ingestive modification of feeding on amino acid imbalanced or deficient artificial diets in the slugArion ater L. BSc Hon thesis Univ of British ColumbiaGoogle Scholar
  9. Denny M (1980) The cost of gastropod crawling. Science 208:1288–1290Google Scholar
  10. Domjan M (1977) Attenuation and enhancement of neophobia for edible substances. In: Barker LM, Best MR, Domjan M (eds) Learning mechanisms and food selection. Baylor Univ Press, Waco Texas, pp 151–179Google Scholar
  11. Domjan M (1980) Ingestional aversion learning: Unique and general processes. Adv Study Behavior 11:275–336Google Scholar
  12. Garcia J, Ervin FR, Koelling RA (1966) Learning with prolonged delay of reinforcement. Psychonomic Science 5:121–122Google Scholar
  13. Gelperin A (1974) Olfactory basis for homing behavior in the giant garden slug,Limax maximus. Proc Natl Acad Sei USA 71:966–970Google Scholar
  14. Gelperin A (1975) Rapid food aversion learning in a terrestrial mollusk. Science 189:567–570Google Scholar
  15. Gelperin A, Culligan N (1984) In vitro expression of in vivo learning in an isolated molluscan CNS. Brain Res 304:207–213Google Scholar
  16. Grouyon PH, Fort PH, Caraux G (1983) Selection of seedlings ofThymus uvlgaris by grazing slugs. J Ecol 71:299–306Google Scholar
  17. Harper AE, Benevenga NJ, Wohlheuter RM (1970) Effects of ingestion of disproportionate amounts of amino acids. Physiol Rev 50:428–557Google Scholar
  18. Jahan-Parwar B (1972) Behavioral and electrophysiological studies on chemoreception inAplysia. Am Zool 12:525–537Google Scholar
  19. Kalat JW, Rozin P (1973) ‘Learned safety’ as a mechanism in long-delay taste-aversion learning in rats. J Comp Physiol Psychol 83:198–207Google Scholar
  20. Kamil AC, Sargent TD (eds) Foraging behaviour. Ecological, ethological and psychological approaches. Garland STPM press, New YorkGoogle Scholar
  21. Maramatsu K, Odagiri, Morishitas H, Talreuchi H (1971) Effect of excess levels of individual amino acids on growth of rats fed casein diets. J Nutrition 101:1117–1126Google Scholar
  22. Mitchell D (1976) Experiments on neophobia in wild and laboratory rats: A re-evaluation. J Comp Physiol Psychol 90:190–197Google Scholar
  23. Rice RL, Lincoln DE, Langenheim JH (1978) Palatability of monoterpenoid compositional types ofSalveia douglasii to a generalist molluscan herbivore,Ariolimax dolichophallus. Bioch Syst Ecol 6:45–53Google Scholar
  24. Rogers QR, Harper AE (1970) Selection of a solution containing histidine by rats fed a histidine-imbalanced diet. J Comp Physiol Psychol 72:66–71Google Scholar
  25. Rogers QR, Leung PMB (1977) The control of food intake: When and how are amino acids involved. In: Kare MR, Maller O (eds) The chemical senses and nutrition, chapter 11, pp 213–249Google Scholar
  26. Rozin P (1976) The selection of foods by rats, humans, and other animals. Adv Study Behav 6:21–76Google Scholar
  27. Rozin P, Kalat JW (1971) Specific hungers and poison avoidance as adaptive specializations of learning. Psych Rev 78:459–486Google Scholar
  28. Sahley C, Gelperin A, Rudy JW (1981) One-trial associative learning modifies food odor preferences of a terrestrial mollusc. Proc Natl Acad Sci USA 78:640–642Google Scholar
  29. Sahley CL, Hardison P, Hsuan A, Gelperin A (1982) Appetitively reinforced odor-conditioning modulates feeding inLimax maximus, Soc Neurosci Abstr 8:823Google Scholar
  30. Sahley CL, Rudy JW, Gelperin A (1984) Associative learning in a mollusc: A comparative analysis. In: Alkon D, Farley J (eds) Primary neural substrates of learning and behavioral change. Cambridge Univ Press, New York, pp 243–258Google Scholar
  31. Simson PC, Booth DA (1973) Effects of CS-US interval on the conditioning of odor preferences by amino acid loads. Physiol Behav 11:801–808Google Scholar
  32. Stryer L (1975) Biochemistry. WH Freeman, San FranciscoGoogle Scholar
  33. Visek JW (1984) An update of concepts of essential amino acids. Annu Rev Nutr 4:135–155Google Scholar
  34. Whelan RJ (1982) Response of slugs to unacceptable food items. J Appl Ecol 19:79–87Google Scholar
  35. Zahler CL, Harper AE (1972) Effects of dietary amino acid pattern on food preference behavior of rats. J Comp Physiol Psychol 81:155–162Google Scholar
  36. Zahorik DM, Houpt KA (1977) The concept of nutritional wisdom: Applicability of laboratory learning models to large herbivores. In: Barker LM, Best MR, Domjan M (eds) Learning mechanisms in food selection. Baylor Univ Press, Waco Texas, pp 45–70Google Scholar
  37. Zahorik DM (1977) Associative and non-associative factors in learned food preferences. In: Barker LM, Best MR, Domjan M (eds) Learning mechanisms in food selection. Baylor Univ Press, Waco Texas, pp 181–200Google Scholar

Copyright information

© Springer-Verlag 1986

Authors and Affiliations

  • K. Delaney
    • 1
  • A. Gelperin
    • 2
  1. 1.Department of BiologyPrinceton UniversityPrincetonUSA
  2. 2.Department of Molecular BiophysicsAT&T Bell LaboratoriesMurray HillUSA

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