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Olfactory perception in honeybees: Concatenated and mixed odorant stimuli, concentration, and exposure effects

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Summary

Here we present results obtained from 7 different series of experiments, all employing odor conditioning of proboscis extension in worker honeybees and each designed to address a particular question involving olfactory perception. The questions relate to: temporal complexity of odor cues; effects of concentration, suppression, and/or potentiation in mixture perception; acquisition and extinction rates, as well as levels of generalization associated with aliphatic compounds that have the same functional groups or same alkyl radical length; and the effects of continuous exposure to odorants in the first several days of adult life on various learning and discrimination tasks involving olfactory perception. From the data obtained in these experiments we were able to conclude the following: First, worker honeybees have a limited ability to perceive complex temporal odor-quality patterns in olfactory stimuli — they learn to associate the quality of only the last part of the stimulus with a sucrose reward. Second, we confirm that citral is qualitatively different in several perceptual contexts involving odor learning and conditioning and our results help elucidate the nature of these differences as they relate to learning, discrimination, mixture perception, and continuous exposure to particular odorants. Third, we appear to have uncovered some important perceptual differences between functional groups attached to the first as opposed to the second carbon atom of alkyl radicals. Finally, we failed to uncover any significant effects relating to continuous exposure to odorants during the first several days of a worker's adult life, despite evidence that considerable sensory development takes place during this period. Thus ontogenetic changes to the peripheral system due to environmental effects appear to leave basic perceptual systems unaltered.

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References

  • Akers RP, O'Connell RJ (1988) The contribution of olfactory receptor neurons to the perception of pheromone component ratios in male red-banded leafroller moths. J Comp Physiol A 163:641–650

    Google Scholar 

  • Bitterman ME, Menzel R, Fietz A, Schäfer S (1983) Classical conditioning of proboscis extension in honeybees (Apis mellifera). J Comp Psychol 97:107–119

    Google Scholar 

  • Boeckh J, Ernst KD (1987) Contribution of single unit analysis in insects to an understanding of olfactory function. J Comp Physiol A 161:549–565

    Google Scholar 

  • Boeckh J, Ernst KD, Sass H, Waldow U (1984) Anatomical and physiological characteristics of individual neurones in the central antennal pathway of insects. J Insect Physiol 30:15–26

    Google Scholar 

  • Brandes Ch (1988) Estimation of heritability of learning behavior in honeybees Apis mellifera capensis. Behav Genet 18:119–132

    Google Scholar 

  • Brandes Ch, Menzel R (1990) Common mechanisms in proboscis extension conditioning and visual learning revealed by genetic selection in honeybees (Apis mellifera capensis). J Comp Physiol A 166:545–552

    Google Scholar 

  • Breed M (1983) Nestmate recognition in honeybees. Anim Behav 31:86–91

    Google Scholar 

  • Breed M, Bennett B (1987) Kin recognition in highly eusocial insects. In: Fletcher D, Michener CD (eds) Kin recognition in animals. Wiley, New York, pp 243–285

    Google Scholar 

  • Breed M, Butler L, Stiller TM (1985) Kin discrimination by worker honeybees in genetically mixed groups. Proc Natl Acad Sci USA 82:3058–3061

    Google Scholar 

  • Breed M, Williams KR, Fewell JH (1988) Comb wax mediates the acquisition of nestmate recognition cues in honey bees. Proc Natl Acad Sci USA 85:8766–8769

    Google Scholar 

  • Caprio J, Dudek J, Robinson JJ II (1989) Electro-olfactogram and multiunit olfactory receptor responses to binary and trinary mixtures of amino acids in the channel catfish, Ictalurus punctatus. J Gen Physiol 93:245–262

    Google Scholar 

  • Daniel PC, Derby CD (1987) Multiple interaction analysis: a polynomial model for multiple-receptor systems which incorporates the Beidler equation. Chemical Senses 12:417–423

    Google Scholar 

  • De Jong R, Visser JH (1988) Specificity-related suppression of responses to binary mixtures in olfactory receptors of the Colorado potato beetle. Brain Res 447:18–24

    Google Scholar 

  • Derby CD, Girardot M, Daniel PC, Fine-Levy JB (1989) Olfactory discrimination of mixtures: behavioral, electrophysiological and theoretical studies using the spiny lobster Panulirus argus. In: Laing DF (ed) Perception of complex smells and taste. Academic Press, Sydney, pp 65–82

    Google Scholar 

  • Flanagan D, Mercer AR (1989) Morphology and response characteristics of neurones in the deutocerebrum of the brain in the honeybee Apis mellifera. J Comp Physiol A 164:483–494

    Google Scholar 

  • Free JB (1987) Pheromones in social bees. Cornell University Press, Ithaca, New York

    Google Scholar 

  • Frings H (1944) The loci of olfactory end-organs in the honey bee Apis mellifera L. J Exp Zool 97:123–134

    Google Scholar 

  • Frisch K von (1967) The dance language and orientation of bees. Harvard University Press, Cambridge, Massachusetts

    Google Scholar 

  • Getz WM (1988) Kin recognition in the honeybee: a communications perspective. In: Page R, Needham G, Delfindo-Baker M (eds) Africanized honey bees and bee mites. Ellis Hoswood, Chichester, England, pp 159–166

    Google Scholar 

  • Getz WM (1991) A neural network for processing olfactory-like stimuli. Bull Math Biol 53: (in press)

  • Getz WM, Chapman RF (1987) An odor discrimination model with application to kin recognition in social insects. Int J Neurosci 32:963–967

    Google Scholar 

  • Getz WM, Page R (1991) Chemosensory kin communication systems and kin recognition in honey bees. Ethology (in press)

  • Getz WM, Smith KB (1986) Honeybee kin recognition: learning self and nestmate phenotypes. Anim Behav 34:1617–1626

    Google Scholar 

  • Getz WM, Smith KB (1987) Olfactory sensitivity and discrimination of mixtures in the honeybee Apis mellifera. J Comp Physiol A 160:239–246

    Google Scholar 

  • Getz WM, Smith KB (1990) Odorant moiety and odor mixture perception in free flying honey bees (Apis mellifera). Chemical Senses 15:111–128

    Google Scholar 

  • Getz WM, Brückner D, Smith KB (1986) Conditioning honeybees to discriminate between heritable odors from full and half sisters. J Comp Physiol A 159:251–256

    Google Scholar 

  • Getz WM, Brückner D, Smith KB (1988) Variability of chemosensory stimuli within honeybee (Apis mellifera) colonies: a differential conditioning assay for discrimination cues. J Chem Ecol 14:249–260

    Google Scholar 

  • Getz WM, Brückner D, Smith KB (1989) The ontogeny of cuticular chemosensory cues in worker honey bees Apis mellifera. Apidologie 20:105–113

    Google Scholar 

  • Hildebrand JG, Montague RA (1986) Functional organization of olfactory pathways in the central nervous system of Manduca sexta. In: Payne TL, Birch MC, Kennedy CEJ (eds) Mechanisms in insect olfaction. Oxford University Press, Oxford, pp 279–285

    Google Scholar 

  • Kaissling KE (1986) Chemo-electrical transduction in insect olfactory receptors. Annu Rev Neurosci 9:121–145

    Google Scholar 

  • Kaissling KE (1987) R.H. Wright lectures on insect olfaction. Colbow K (ed) Simon Fraser University, Burnaby, British Columbia, Canada

    Google Scholar 

  • Kuwabara M (1957) Bildung des bedingten Reflexes von Pavlovs Typus bei der Honigbiene, Apis mellifera. J Fac Sci Hokkaido Univ (Zool) 13:458–464

    CAS  PubMed  Google Scholar 

  • Marfaing P, Rouault J, Laffort P (1989) Effect of the concentration and nature of olfactory stimuli on the proboscis extension of conditioned honey bees Aois mellifica ligustica. J Insect Physiol 35:949–955

    Google Scholar 

  • Martin H (1964) Zur Nahorientierung der Biene im Duftfeld, zugleich ein Nachweis für die Osmotropotaxis bei Insekten. Z Vergl Physiol 48:481–553

    Google Scholar 

  • Masson C, Arnold GS (1984) Ontogeny, maturation and plasticity of the olfactory system in the workerbee. J Insect Physiol 30:7–14

    Google Scholar 

  • Menzel R (1985) Learning in honeybees in an ecological and behavioral context. Fortschr Zool 31:55–74

    Google Scholar 

  • Menzel R (1990) Learning, memory, and ‘cognition’ in honey bees. In: Kesner RP (ed) Neurobiology of comparative cognition. Lawrence Erlbaum Assoc, Hillsdale, New Jersey, pp 237–292

    Google Scholar 

  • Menzel R, Erber J, Masuhr T (1974) Learning and memory in the honeybee. In: Barton Browne L (ed) Experimental analysis of insect behaviour. Springer, New York, p 195–217

    Google Scholar 

  • Sachs L (1982) Applied statistics: a handbook of techniques. Springer, New York

    Google Scholar 

  • Sass H (1976) Zur nervösen Codierung von Geruchsreizen bei Periplaneta americana. J Comp Physiol 107:49–65

    CAS  PubMed  Google Scholar 

  • Sass H (1978) Olfactory receptors on the antenna of Periplaneta: response constellations that incode food odors. J Comp Physiol 128:227–233

    Google Scholar 

  • Selzer R (1984) On the specificities of antennal olfactory receptor cells of Periplaneta americana. Chemical Senses 8:375–395

    Google Scholar 

  • Smith BH (1991) The olfactory memory of honey bee, Apis mellifera: Odorant-specific modulation of recall and generalization. J Exp Biol (in press)

  • Smith BH, Menzel R (1989a) The use of electromyogram recordings to quantify odourant discrimination in the honey bee, Apis mellifera. J Insect Physiol 35:369–375

    Google Scholar 

  • Smith BH, Menzel R (1989b) An analysis of variability in the feeding motor program of the honey bee; the role of learning in releasing a modal action pattern. Ethology 82:68–81

    Google Scholar 

  • Vareschi E (1971) Duftunterscheidung bei der Honigbiene — Einzel-zell-Ableitungen und Verhaltensreaktionen. Z Vergl Physiol 75:143–173

    Google Scholar 

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Getz, W.M., Smith, K.B. Olfactory perception in honeybees: Concatenated and mixed odorant stimuli, concentration, and exposure effects. J Comp Physiol A 169, 215–230 (1991). https://doi.org/10.1007/BF00215869

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