The moth Macroglossum stellatarum can learn the color and sometimes the odor of a rewarding food source. We present data from 20 different experiments with different combinations of blue and yellow artificial flowers and the two odors, honeysuckle and lavender. The experiments show that learning about the odors depends on the color used. By training on different color—odor combinations and testing on others, it becomes possible to investigate the exact relation between the two modalities during learning. Three computational models were tested in the same experimental situations as the real moths and their predictions were compared with the experimental data. The average error over all experiments as well as the largest deviation from the experimental data were calculated. Neither the Rescorla—Wagner model nor a learning model with independent learning for each stimulus component were able to explain the experimental data. We present the new hawkmoth learning model, which assumes that the moth learns a template for the sensory attributes of the rewarding stimulus. This model produces behavior that closely matches that of the real moth in all 20 experiments.
Andersson, S. (2003). Foraging responses in the butterflies Inachis io, Aglais urticae (Nymphalidae), and Gonepteryx rhamni (Pieridae) to floral scents. Chemoecology, 13, 1- 11.
2.
Balkenius, A., & Kelber, A. (2004). Color constancy in diurnal and nocturnal hawkmoths . Journal of Experimental Biology, 207, 3307-3316.
3.
Balkenius, A., & Kelber, A. (2006). Color preferences influence odor learning in the hawkmoth, Macroglossum stellatarum. Naturwissenschaften, 93, 255-258.
4.
Balkenius, A., Kelber, A., & Balkenius, C. (2004). A model of selection between stimulus and place strategy in a hawkmoth. Adaptive Behavior, 12(1), 21-35.
5.
Balkenius, A., Rosén, W., & Kelber, A. (2006). The relative importance of olfaction and vision in a diurnal and a nocturnal hawkmoth. Journal of Comparative Physiology A: Sensory, Neural, and Behavioral Physiology, 192(4), 431-437.
6.
Borisyuk, A., & Smith, B.H. (2004). Odor interactions and learning in a model of the insect antennal lobe. Neurocomputing, 58-60, 1041-1047.
7.
Brantjes, N.B.M. (1978). Sensory responses to flowers in night-flying moths . In A. J. Richards (Ed.), The pollinaton of flowers by insects (pp. 13-19). Dorchester, UK: Dorset Press.
8.
Bush, R.R., & Mostellar, F. (1955). Stochastic models for learning. New York: Wiley.
9.
Couvillon, P.A., Arakaki, L., & Bitterman, M.E. (1997). Intramodal blocking in honeybees. Animal Learning and Behavior, 25, 277-282.
10.
Couvillon, P.A., Campos, A.C., Bass, T.D., & Bitterman, M.E. (2001). Intermodal blocking in honeybees. The Quarterly Journal of Experimental Psychology B, 54, 369-381.
11.
Couvillon, P.A., Mateo, E.T., & Bitterman, M.E. (1996). Reward and learning in honeybees: Analysis of an overshadowing effect. Animal Learning and Behavior, 24, 19- 27.
12.
Cunningham, J.P., Moore, C.J., Zalucki, M.P., & West, S.A. (2004). Learning, odour preference and flower foraging in moths. Journal of Experimental Biology, 207, 87-94.
13.
Funayama, E.S., Couvillon, P.A., & Bitterman, M.E. (1995). Compound conditioning in honeybees: Blocking tests of the independence assumption. Animal Learning and Behavior, 23, 429-437.
14.
Gallistel, R.C. (1990). The organization of learning. Cambridge, MA: MIT Press.
15.
Gerber, B., & Ullrich, J. (1999). No evidence for olfactory blocking in honeybee classical conditioning. Journal of Experimental Biology, 202, 1839-1854.
16.
Giurfa, M., Núñez, J., & Backhaus, W. (1994). Odour and colour information in the foraging choice behaviour of the honeybee. Journal of Comparative Physiology A, 175, 773-779.
17.
Giurfa, M., Núñez, J., Chittka, L., & Menzel, R. (1995). Colour preferences of flower-naïve honeybees. Journal of Comparative Physiology A, 177, 247-259.
18.
Goulson, D. (2000). Are insects flower constant because they use search images to find flowers? Oikos, 88(3), 547-552.
19.
Herrera, C.M. (1992). Activity pattern and thermal biology of a day-flying hawkmoth (Macroglossum stellatarum) under mediterranean summer conditions . Ecological Entomology, 17, 52-56.
20.
Kamin, L.J. (1969). Predictability, surprise, attention and conditioning . In B. A. Campbell & R. M. Church (Eds.), Punishment and aversive behavior (pp. 279-296). New York: Appleton-Century-Crofts .
21.
Kelber, A. (1997). Innate preferences for flower features in the hawkmoth Macroglossum stellatarum. Journal of Experimental Biology, 200, 826-835.
22.
Kelber, A., & Hénique, U. (1999). Trichromatic color vision in the hummingbird hawkmoth, Macroglossum stellatarum. Journal of Comparative Physiology A, 184, 535-541.
23.
Kelber, A., Vorobyev, M., & Osorio, D. (2003). Animal color vision-behavioral tests and physiological concepts. Biological Reviews, 78, 81-118.
24.
Kunze, J., & Gumbert, A. (2001). The combined effect of color and odor on flower choice behavior of bumble bees in flower mimicry systems. Behavioral Ecology, 12, 447- 456.
25.
Linster, C., & Smith, B. (1997). A computational model of the response of honey bee antennal lobe circuitry to odor mixtures: overshadowing, blocking and unblocking can arise from lateral inhibition. Behavioural Brain Research, 87(1), 1-14.
26.
Luo, R.C., & Kay, M.G. (1992). Data fusion and sensor integration: State-of-the-art 1990s. In M. A. Abidi & R. C. Gonzalez (Eds.), Data fusion in robotics and machine intelligence. Boston, MA: Academic Press.
27.
Mackintosh, N.J. (1974). The physiology of animal learning. London: Academic Press.
28.
Menzel, R. (1967). Untersuchungen zum erlernen von spektralfarben durch die honigbiene (Apis mellifica). Zeitschrift für vergleichende Physiologie, 56, 22-62.
29.
Pavlov, I.P. (1927). Conditioned reflexes. Oxford : Oxford University Press.
30.
Pearce, J.M. (1994). Similarity and discrimination: A selective review and a connectionist model. Psychological Review, 101(4), 587-607.
31.
Pelz, C., Gerber, B., & Menzel, R. (1997). Odorant intensity as a determinant for olfactory conditioning in honeybees: Roles in discrimination, overshadowing and memory consolidation. Journal of Experimental Biology, 200, 837- 847.
32.
Pfaff, M., & Kelber, A. (2003). Ein vielseitiger Futterspender für anthophile Insekten. Entomologische Zeitschrift, 113, 360-361.
33.
Raguso, R.A., & Willis, M.A. (2002). Synergy between visual and olfactory cues in nectar feeding by naïve hawkmoths, Manduca sexta. Animal Behaviour , 64, 685-695.
34.
Rescorla, R., & Wagner, A. (1972). A theory of pavlovian conditioning: variations in the effectiveness of reinforcement and non-reinforcement. In A. H. Black & W. F. Prokasy (Eds.), Classical conditioning II: Current research and theory (pp. 64-99). New York: Appleton-Century-Crofts .
35.
Rowe, C. (1999). Receiver psychology and the evolution of multicomponent signals. Animal Behaviour, 58, 921-931.
36.
Seligman, M.E.P. (1970). On the generality of the laws of learning. Psychological Review, 77, 406-418.
37.
Srinivasan, M.V., Zhang, S.W., & Zhu, H. (1998). Honeybees links sight to smell. Nature, 396, 637-638.
38.
Tinbergen, N. (1960). The natural control of insects in pine woods: Vol. I. Factors influencing the intensity of predation by songbirds. Archives Neelandaises de Zoologie, 13, 265-343.
39.
von Frisch, K. (1914). Der Farbensinn und Formensinn der Biene. Zoologisher Jahrbucher, Abteilung für Allgemeine Zoologie und Physiologie der Tierre, 15, 193-260.
40.
von Frisch, K. (1919). Über den Geruchssinn der Bienen und seine blütenbiologische Bedeutung. Zoologisher Jahrbucher, Abteilung für Allgemeine Zoologie und Physiologie der Tierre, 37, 2-238.
41.
Weiss, M. (1997). Innate colour preferences and flexible colour learning in the pipevine swallowtail. Animal Behaviour, 53, 1043-1052.
42.
Weiss, M. (2001). Vision and learning in some neglected pollinators: Beetles, flies, moths, and butterflies. In L. Chittka & J. D. Thomson (Eds.), Cognitive ecology of pollination (pp. 171-190). Cambridge: Cambridge University Press.
43.
Wessnitzer, J., Webb, B., & Smith, D. (2007). A model of non-elemental associative learning in the mushroom body neuropil of the insect brain. In Proceedings of the International Conference on Adaptive and Natural Computing Algorithms (LNCS Vol. 4431, pp. 488-497). Berlin: Springer-Verlag.
44.
Widrow, B., & Hoff, M.E. (1960). Adaptive switching circuits. In IRE WESCON convention record (pp. 96-104). New York: Institute of Radio Engineers.
45.
Zentall, T.R., & Riley, D.A. (2000). Selective attention in animal discrimination learning . Journal of General Psychology, 127, 45-66.
