Abstract
Experiments were performed to test for nutrient-specific olfactory learning in the American cockroach, Periplaneta americana L. In a conditioning period, cockroaches were presented with two complementary foods, one of which contained protein and the other carbohydrate, this combination allowing them to select a nutritionally balanced diet. The foods were separated in space, and each was paired with one of two odors, citral or carvone. The cockroaches were then selectively deprived of one of the nutrients for 24 or 48 h. In the final (test) phase of the experiment the movement of the cockroaches toward the nutrient-associated odors was monitored. Associative learning was demonstrated with respect to protein, with protein-deprived cockroaches moving more frequently toward the protein-associated odor. No learned associations between carbohydrate and odor were demonstrated. These data are contrasted with similar experiments on an herbivorous insect, the locust Locusta migratoria.
Similar content being viewed by others
REFERENCES
Abisgold, J. D., and Simpson, S. J. (1988). The effect of dietary protein levels and haemolymph composition on the sensitivity of the maxillary palp chemoreceptors of locusts. J. Exp. Biol 135: 215-229.
Baker, B. J., Booth, D. A., Duggan, J. P., and Gibson, E. L. (1987). Protein appetite demonstrated: Learned specificity of protein-cue preference need in adult rats. Nutr. Res. 7: 481-487.
Beckers, R., Lachaud, J. P., and Fresneau, D. (1994). The influence of olfactory conditioning on food preferences in the ant Lasius niger (L.). Ethol. Ecol. Evol. 6: 159-167.
Bernays, E. A., and Chapman, R. F. (1994). Host-Plant Selection by Phytophagous Insects, Chapman & Hall, New York.
Bernays, E. A., and Raubenheimer, D. (1991). Dietary mixing in grasshoppers: Changes in acceptability of different plant secondary compounds associated with low levels of dietary protein (Orthoptera: Acrididae). J. Insect Behav. 4: 545-556.
Berteaux, D., Crete, M., Huot, J., Maltais, J., and Ouellet, J.-P. (1998). Food choice by white-tailed deer in relation to protein and energy content of the diet: A field experiment. Oecologia 115: 84-92.
Berthoud, H.-R., and Seeley, R. J. (eds.) (1999). Neural Control of Macronutrient Selection,CRC Press, Boca Raton, FL.
Boeckh, J., and Ernst, K. D. (1987). Contribution of single unit analysis in insects to an understanding of olfactory function. J. Comp. Physiol. A 161: 549-565.
Booth, D. A., and Baker, B. J. (1990). dl-Fenfluramine challenge to nutrient-specific textural preference conditioned by concurrent presentation of two diets. Behav. Neurosci. 104: 226-229.
Bowdish, T. I., and Bultman, T. L. (1993). Visual cues used by mantids in learning aversion to aposematically colored prey. Am. Midland Nat. 129: 215-222.
Clarebrough, C., Mira, A., and Raubenheimer, D. (2000). Sex-specific differences in nitrogen intake and investment by feral and laboratory-cultured cockroaches. J. Insect Physiol. 46: 677-684.
Cochran, D. G. (1985). Nitrogen excretion in cockroaches. Annu. Rev. Entomol. 30: 29-49.
Cohen, R.W., Heydon, S. L., Waldbauer, G. P., and Friedman, S. (1987). Nutrient self-selection by the omnivorous cockroach Supella longipalpa. J. Insect Physiol. 33: 77-82.
Corrigan, J. J., and Kearns, C. W. (1963). Amino acid metabolism in DDT-poisoned American cockroaches. J. Insect Physiol. 9: 1-12.
Dukas, R. (1995). Transfer and interference in bumblebee learning. Anim. Behav. 49: 1481-1490.
Geissler, T. G., and Rollo, C. D. (1987). The influence of nutritional history on the response to novel food by the cockroach Periplaneta americana (L.). Anim. Behav. 35: 1905-1907.
Gould, J. L. (1993). Ethological and comparative perspectives on honey bee learning. In Papaj, D. R., and Lewis, A. C. (eds.), Insect Learning, Chapman & Hall, New York, pp. 18-50.
Gould, J. L., and Marler, P. (1987). Learning by instinct. Sci. Am. 256: 62-73.
Gould, J. L., and Towne, W. F. (1988). Honey bee learning. Adv. Insect Physiol. 20: 55-86.
Guthrie, D. M., and Tindall, A. R. (1968). The Biology of the Cockroach, Edward Arnold, London.
Hammer, M., and Menzel, R. (1995). Learning and memory in the honeybee. J. Neurosci. 15: 1617-1630.
Healy, S. (1992). Optimal memory: Toward an evolutionary ecology of animal cognition. Trends Ecol. Evol. 7: 399-400.
Hoffmann, A. A. (1985). Effects of experience on oviposition and attraction in Drosophila: Comparing apples and oranges. Am. Nat. 126: 41-51.
Jermy, T. (1987).The role of experience in the host selection of phytophagous insects. In Chapman, R. F., Bernays, E. A., and Stoffonalo, J. G. (eds.), Perspectives in Chemoreception and Behavior, Springer-Verlag, New York, pp. 143-157.
Johnson, R. A. (1991). Learning, memory and foraging efficiency in two species of desert seedharvesterants. Ecology 72: 1408-1419.
Jones, S. A., and Raubenheimer, D. (1999). An integrated approach to baiting strategies for the German cockroach, Blattella germanica (L.) (Dictyoptera: Blattellidae). In Robinson, W H., Rettich, F., and Rambo, G.W. (eds.), Proceedings of the Third International Conference on Urban Pests, Prague, pp. 133-140.
Lee, J. C., and Bernays, E. A. (1990). Food tastes and toxic effects: Associative learning by the polyphagous grasshopper Schistocerca americana (Drury) (Orthoptera: Acrididae). Anim Behav. 39: 163-173.
McAllan, J. W., and Chefuka, W. (1961). Some physiological aspects of glutamate-aspartate transamination in insects. Comp. Biochem. Physiol. 2: 290-299.
Menzel, R. (1985). Learning in honey bees in an ecological and behavioral context. In Hölldobler, B., and Lindauer, M. (eds.), Experimental Behavioral Ecology and Sociobiology, Gustav Fischer Verlag, Stuttgart, New York, pp. 55-74.
Menzel, R., Greggers, U., and Hammer, M. (1993). Functional organization of appetitive learning and memory in a generalist pollinator, the honey bee. In Papaj, D. R., and Lewis, A. C (eds.), Insect Learning, Chapman & Hall, New York, pp. 18-50.
Mira, A. (1999). Nutritional and Evolutionary Studies of the Host-Endosymbiont Relationship in the Blattodea, D.Phil thesis, University of Oxford, Oxford.
Mullins, D. E., and Cochran, D. G. (1974). Nitrogen metabolism in the American cockroach: An examination of whole body and fat body regulation of cations in response to nitrogen balance. J. Exp. Biol. 61: 557-570.
Mullins, D. E., and Cochran, D. G. (1975a). Nitrogen metabolism in the American cockroach I. An examination of positive nitrogen balance with respect to uric acid stores. Comp Biochem. Physiol. A 50: 489-500.
Mullins, D. E., and Cochran, D. G. (1975b). Nitrogen metabolism in the American cockroach II. An examination of negative nitrogen balance with respect to mobilization of uric acid stores. Comp. Biochem. Physiol. A 50: 501-510.
Mullins, D. E., and Cochran, D. G. (1987). Nutritional ecology of cockroaches. In Slansky, F., and Rodriguez, J. G. (eds.), Nutritional Ecology of Insects, Mites, Spiders and Related Invertebrates,Wiley, New York, pp. 885-902.
Papaj, D. R., and Prokopy, R. J. (1989). Ecological and evolutionary aspects of learning in phytophagous insects. Annu. Rev. Entomol. 34: 315-350.
Papaj, D. R., Snellen, H., Swanns, K., and Vet, L. E. M. (1994). Unrewarding experiences and their effect on the foraging in the parasitic wasp Leptopilina heterotoma (Hymenoptera: Eucoilidae). J. Insect Behav. 7: 465-481.
Prokopy, R. J., Cooley, S. S., and Papaj, D. R. (1992). How well can relative specialist Rhagoletis flies learn to discriminate fruit for oviposition? J. Insect Behav. 6: 167-176.
Prokopy, R. J., Bergweiler, C., Galarza, L., and Schwerin, J. (1994). Prior experience affects the visual ability of Rhagoletis pomonella flies (Diptera: Tephritidae) to find host fruit. J. Insect Behav. 7: 663-677.
Raubenheimer, D. (1992). Tannic acid, protein, and digestible carbohydrate: Dietary imbalance and nutritional compensation in locusts. Ecology 73: 1012-1027.
Raubenheimer, D., and Blackshaw, J. (1994). Locusts learn to associate visual stimuli with drinking J. Insect Behav. 7: 569-575.
Raubenheimer, D., and Simpson, S. J. (1993). The geometry of compensatory feeding in the locust. Anim. Behav. 45: 953-964.
Raubenheimer, D., and Simpson, S. J. (1997). Integrative models of nutrient balancing: application to insects and vertebrates. Nutr. Res. Rev. 10: 151-179.
Raubenheimer, D., and Tucker, D. (1997). Associative learning by locusts: Pairing of visual cues with the separate consumption of protein and carbohydrate. Anim. Behav. 54: 1449-1459.
Rollo, C. D. (1984). Resource allocation and time budgeting in adults of the cockroach Periplaneta americana: The interaction of behaviour and metabolic reserves. Res. Pop. Ecol. 26: 150-187.
Schal, C., Gautier, J. Y., and Bell, W. J. (1984). Behavioural ecology of cockroaches. Biol. Rev 59: 209-254.
Sherry, D. F., Jacobs, L. F., and Gaulin, S. J.C. (1992). Spatial memory and adaptive specialization of the hippocampus. Trends Neurosci. 15: 298-303.
Simons, M. T. T. P., Suverkropp, B. P., Vet, L. E. M., and Demoed, G. (1992). Comparison of learning in related generalist and specialist eucoilid parasitoids. Entomol. Exp. Appl. 64: 117-124.
Simpson, S. J., and Abisgold, J. D. (1985). Compensation by locusts for changes in dietary nutrients: Behavioural mechanisms. Physiol. Entomol. 10: 443-452.
Simpson, S. J., and Raubenheimer, D. (1993). A multi-level analysis of feeding behaviour: The geometry of behavioural decisions. Philos. Trans. Roy. Soc. B 342: 381-402.
Simpson, S. J., and White, P. R. (1990). Associative learning and locust feeding: Evidence for a 'learned hunger' for protein. Anim. Behav. 40: 506-513.
Simpson, S. J., Simmonds, M. S. J., Blaney, W. M., and Jones, J. P. (1990). Compensatory dietary selection occurs in larval Locusta migratoria but not Spodoptera littoralis after a single deficient meal during ad libitum feeding. Physiol. Entomol. 15: 235-242.
Stephens, D.W., and Krebs, J.R. (1986). Foraging Theory, Princeton University Press, Princeton, NJ.
Traynier, R. M. M. (1984). Associative learning in the ovipositional behavior of the cabbage butterfly, Pieris rapae. Physiol. Entomol. 9: 465-472.
Westoby, M. (1974). An analysis of diet selection by large generalist herbivores. Am. Nat. 108: 290-304.
Wharton, D. R. A., Wharton, M. C., and Lola, J. E. (1965). Cellulase in the cockroach, with special reference to Periplaneta americana (L.). J. Insect Physiol. 11: 947-959.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Gadd, C.A., Raubenheimer, D. Nutrient-Specific Learning in an Omnivorous Insect: The American Cockroach Periplaneta americana L. Learns to Associate Dietary Protein with the Odors Citral and Carvone. Journal of Insect Behavior 13, 851–864 (2000). https://doi.org/10.1023/A:1007862501311
Issue Date:
DOI: https://doi.org/10.1023/A:1007862501311