Skip to main content
Log in

Elemental and non-elemental olfactory learning using PER conditioning in the bumblebee, Bombus terrestris

  • Original article
  • Published:
Apidologie Aims and scope Submit manuscript

Abstract

Learning olfactory stimuli and their implications is essential in bumblebees for orientation and recognition of nest sites and food sources. To evaluate associative learning abilities in bees under controlled environmental conditions, the proboscis extension response (PER) assay is a well-established method used in honeybees and has recently been successfully adapted to bumblebees. In this study, we examined the cognitive abilities of workers of the eusocial bumblebee, Bombus terrestris, by training individuals in different olfactory learning tasks using classical PER conditioning. We compared learning performance for four different floral odors. Individuals were able to solve absolute (A+) and differential (A+ vs. B−) conditioning tasks, and no differences were found between single odors and odor combinations, respectively. Furthermore, bumblebees performed well on a positive pattern discrimination task (A−, B− vs. AB+), but failed to solve the negative pattern discrimination (A+, B+ vs. AB−). Our results indicate that workers of B. terrestris possess elemental olfactory learning abilities, but, in contrast to previous findings in honeybees, fail in more complex tasks, such as negative pattern discrimination. We discuss possible ultimate causes that have led to the difference in learning capabilities between bumblebees and honeybees.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1.
Figure 2.
Figure 3.
Figure 4.

Similar content being viewed by others

References

  • Anfora, G., Rigosi, E., Frasnelli, E., Ruga, V., Trona, F., Vallortigara, G. (2011) Lateralization in the invertebrate brain: left-right asymmetry of olfaction in bumble bee, Bombus terrestris. PLoS One 6(4), e18903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhagavan, S., Smith, B.H. (1997) Olfactory conditioning in the honeybee, Apis mellifera: effects of odor intensity. Physiol. Behav. 61(1), 107–117

    Article  CAS  PubMed  Google Scholar 

  • Bitterman, M.E., Menzel, R., Fietz, A., Schäfer, S. (1983) Classical conditioning of proboscis extension in honeybees (Apis mellifera). J. Comp. Psychol. 97(2), 107–119

    Article  CAS  PubMed  Google Scholar 

  • Brill, M.F., Rosenbaum, T., Reus, I., Kleineidam, C.J., Nawrot, M.P., Rössler, W. (2013) Parallel processing via a dual olfactory pathway in the honeybee. J. Neurosci. 33(6), 2443–2456

    Article  CAS  PubMed  Google Scholar 

  • Couvillon, P.A., Bitterman, M.E. (1988) Compound-component and conditional discrimination of colors and odors by honeybees: Further tests of a continuity model. Anim. Learn. Behav. 16(1), 67–74

    Article  Google Scholar 

  • Dacher, M., Smith, B.H. (2008) Olfactory interference during inhibitory backward pairing in honeybees. PLoS One 3(10), e3513

    Article  PubMed  PubMed Central  Google Scholar 

  • Deisig, N., Lachnit, H., Giurfa, M. (2001) Configural olfactory learning in honeybees: negative and positive patterning discrimination. Learn. Mem. 8, 70–78

    Article  CAS  PubMed  Google Scholar 

  • Deisig, N., Lachnit, H., Giurfa, M. (2002) The effect of similarity between elemental stimuli and compounds in olfactory patterning discriminations. Learn. Mem. 9(3), 112–121

    Article  PubMed  Google Scholar 

  • Deisig, N., Lachnit, H., Sandoz, J.C., Lober, K., Giurfa, M. (2003) A modified version of the unique cue theory accounts for olfactory compound processing in honeybees. Learn. Mem. 10(3), 199–208

    Article  PubMed  Google Scholar 

  • Dukas, R. (2008) Evolutionary biology of insect learning. Annu. Rev. Entomol. 53, 145–160

    Article  CAS  PubMed  Google Scholar 

  • Fauria, K., Dale, K., Colborn, M., Collett, T. (2002) Learning speed and contextual isolation in bumblebees. J. Exp. Biol. 205, 1009–1018

    PubMed  Google Scholar 

  • Free, J.B. (1970) The flower constancy of bumblebees. J. Anim. Ecol. 39(2), 395–402

    Article  Google Scholar 

  • Giurfa, M. (2003) Cognitive neuroethology: dissecting non-elemental learning in a honeybee brain. Curr. Opin. Neurobiol. 13(6), 726–735

    Article  CAS  PubMed  Google Scholar 

  • Giurfa, M. (2007) Behavioral and neural analysis of associative learning in the honeybee: a taste from the magic well. J. Comp. Physiol. A .Neuroethol. Sens. Neural. Behav. Physiol. 193(8), 801–824

    Article  PubMed  Google Scholar 

  • Giurfa, M., Sandoz, J.C. (2012) Invertebrate learning and memory: fifty years of olfactory conditioning of the proboscis extension response in honeybees. Learn. Mem. 19(2), 54–66

    Article  PubMed  Google Scholar 

  • Grant, V. (1950) The flower constancy of bees. Bot. Rev. 16(7), 379–398

    Article  Google Scholar 

  • Gumbert, A. (2000) Color choices by bumble bees (Bombus terrestris): innate preferences and generalization after learning. Behav. Ecol. Sociobiol. 48, 36–43

    Article  Google Scholar 

  • Hussaini, S.A., Komischke, B., Menzel, R., Lachnit, H. (2007) Forward and backward second-order Pavlovian conditioning in honeybees. Learn. Mem. 14(10), 678–683

    Article  PubMed  Google Scholar 

  • Jakobsen, H.B., Kristjánsson, K., Rohde, B., Terkildsen, M., Olsen, C.E. (1995) Can social bees be influenced to choose a specific feeding station by adding the scent of the station to the hive air? J. Chem. Ecol. 21(11), 1635–1648

    Article  CAS  PubMed  Google Scholar 

  • Kapustjanskij, A., Streinzer, M., Paulus, H.F., Spaethe, J. (2007) Bigger is better: implications of body size for flight ability under different light conditions and the evolution of alloethism in bumblebees. Funct. Ecol. 21(6), 1130–1136

    Article  Google Scholar 

  • Knudsen, J.T., Tollsten, L., Bergström, L.G. (1993) Floral Scents—a checklist of volatile compounds isolated by head-space techniques. Phytochemistry 33(2), 253–280

    Article  CAS  Google Scholar 

  • Komischke, B., Sandoz, J.-C., Lachnit, H., Giurfa, M. (2003) Non-elemental processing in olfactory discrimination tasks needs bilateral input in honeybees. Behav. Brain Res. 145(1–2), 135–143

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Laloi, D., Bailez, O., Blight, M.M., Roger, B., Pham-Delègue, M.H., Wadhams, L.J. (2000) Recognition of complex odors by restrained and free-flying honeybees, Apis mellifera. J. Chem. Ecol. 26(10), 2307–2319

    Article  CAS  Google Scholar 

  • Laloi, D., Pham-Delègue, M.H. (2004) Bumblebees show asymmetrical discrimination between two odors in a classical conditioning procedure. J. Insect Behav. 17(3), 385–396

    Article  Google Scholar 

  • Laloi, D., Sandoz, J.C., Picard-Nizou, A.L., Marchesi, A., Pouvreau, A., Taséi, J.N., Poppy, G., Pham-Delègue, M.H. (1999) Olfactory conditioning of the proboscis extension in bumble bees. Entomol. Exper. Appl. 90, 123–129

    Article  Google Scholar 

  • Matsumoto, Y., Menzel, R., Sandoz, J.C., Giurfa, M. (2012) Revisiting olfactory classical conditioning of the proboscis extension response in honey bees: a step toward standardized procedures. J. Neurosci. Methods 211(1), 159–167

    Article  PubMed  Google Scholar 

  • Mc Cabe, S.I., Farina, W.M. (2010) Olfactory learning in the stingless bee Tetragonisca angustula (Hymenoptera, Apidae, Meliponini). J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 196(7), 481–490

    Article  CAS  PubMed  Google Scholar 

  • Menzel, R., Giurfa, M., Gerber, B., Hellstern, F. (1999) Elementary and configural forms of memory in an insect: the honeybee. In: Friederici, A.D., Menzel, R. (eds.) Learning: Rule Extraction and Representation, pp. 259–282. Walter de Gruyter, Berlin, New York

    Google Scholar 

  • Menzel, R., Müller, U. (1996) Learning and memory in honeybees: from behavior to neural substrates. Annu. Rev. Neurosci. 19, 379–404

    Article  CAS  PubMed  Google Scholar 

  • Morawetz, L., Spaethe, J. (2012) Visual attention in a complex search task differs between honeybees and bumblebees. J. Exp. Biol. 215(Pt 14), 2515–2523

    Article  PubMed  Google Scholar 

  • Pearce, J.M. (1987) A Model for stimulus generalization in Pavlovian conditioning. Psychol. Rev. 94(1), 61–73

    Article  CAS  PubMed  Google Scholar 

  • Pearce, J.M., Bouton, M.E. (2001) Theories of associative learning in animals. Annu. Rev. Psychol. 52, 111–139

    Article  CAS  PubMed  Google Scholar 

  • Pelz, C., Gerber, B., Menzel, R. (1996) Odorant intensity as a determinant for olfactory conditioning in honeybees: roles in discrimination, over-shadowing, and memory consolidation. J. Exp. Biol. 200, 837–847

    Google Scholar 

  • Raine, N.E., Chittka, L. (2007). Flower Constancy and memory dynamics in bumblebees (Hymenoptera: Apidae: Bombus). Entomol. Gen. 29(2–4), 179–199

    Google Scholar 

  • Raine, N.E., Chittka, L. (2008) The correlation of learning speed and natural foraging success in bumblebees. Proc. Biol. Sci. 275(1636), 803–808

    Article  PubMed  PubMed Central  Google Scholar 

  • Reinhard, J., Sinclair, M., Srinivasan, M.V., Claudianos, C. (2010) Honeybees learn odor mixtures via a selection of key odorants. PLoS One 5(2), e9110

    Article  PubMed  PubMed Central  Google Scholar 

  • Rescorla, R.A. (1972) "Configural" conditioning in discrete-trial bar pressing. J. Comp. Physiol. Psychol. 79(2), 307–317

    Article  CAS  PubMed  Google Scholar 

  • Rescorla, R.A., Wagner, A.R. (1972) A theory of Pavlovian conditioning: variations in the effectiveness of reinforcement and non-reinforcement. In: Black, A.H., Prokasy, W.F. (eds.) Classical Conditioning 2: Current research and theory, pp. 64–99. Appleton, New York

    Google Scholar 

  • Riveros, A.J., Gronenberg, W. (2009a) Learning from learning and memory in bumblebees. Commun. Integr. Biol. 2(5), 437–440

    Article  PubMed  Google Scholar 

  • Riveros, A.J., Gronenberg, W. (2009b) Olfactory learning and memory in the bumblebee Bombus occidentalis. Naturwissenschaften 96(7), 851–856

    Article  CAS  PubMed  Google Scholar 

  • Rudy, J.W., Sutherland, R.J. (1992) Configural and elemental associations and the memory coherence problem. J. Cogn. Neurosci. 4(3), 208–216

    Article  CAS  PubMed  Google Scholar 

  • Sandoz, J.C., Pham-Delègue, M.H., Renou, M., Wadhams, L.J. (2001) Asymmetrical generalization between pheromonal and floral odors in appetitive olfactory conditioning of the honeybee (Apis mellifera L.). J. Comp. Physiol. A 187, 559–568

    Article  CAS  PubMed  Google Scholar 

  • Spaethe, J., Brockmann, A., Halbig, C., Tautz, J. (2007) Size determines antennal sensitivity and behavioral threshold to odors in bumblebee workers. Naturwissenschaften 94(9), 733–739

    Article  CAS  PubMed  Google Scholar 

  • Spaethe, J., Chittka, L. (2003) Interindividual variation of eye optics and single object resolution in bumblebees. J. Exper. Biol. 206(19), 3447–3453

    Article  Google Scholar 

  • Toda, N.R., Song, J., Nieh, J.C. (2009) Bumblebees exhibit the memory spacing effect. Naturwissenschaften 96(10), 1185–1191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wagner, A.R., Rescorla, R.A. (1972) Inhibition in Pavlovian conditioning: application of a theory. In: Halliday, M.S., Boakes, R.A. (eds.) Inhibition and learning, pp. 301–336. Academic, London

    Google Scholar 

  • Worden, B.D., Skemp, A.K., Papaj, D.R. (2005) Learning in two contexts: the effects of interference and body size in bumblebees. J. Exp. Biol. 208(Pt 11), 2045–2053

    Article  PubMed  Google Scholar 

  • Wright, G.A., Carlton, M., Smith, B.H. (2009) A honeybee's ability to learn, recognize, and discriminate odors depends upon odor sampling time and concentration. Behav. Neurosci. 123(1), 36–43

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We would like to thank Karin Möller for rearing the bumblebees. We also thank two anonymous reviewers for their helpful comments on an earlier draft of this manuscript. This work was supported by a PhD research scholarship offered by the Free State of Bavaria (Elitenetzwerk Bayern) to FMJS.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Frank M. J. Sommerlandt.

Additional information

Manuscript editor: Bernd Grünewald

Apprentissage olfactif de base ou complexe par conditionnement du REP (réflexe d’extension du proboscis) chez le bourdon, Bombus terrestris

Apprentissage élémentaire / bourdon / REP / associations configurales

Elementares und nicht-elementares olfaktorisches Lernen bei der PER-Konditionierung der Hummel Bombus terrestris

Elementares Lernen / Bombus terrestris / Rüsselreflexkonditionierung / Hummel / konfigurale Assoziationen

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 178 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sommerlandt, F.M.J., Rössler, W. & Spaethe, J. Elemental and non-elemental olfactory learning using PER conditioning in the bumblebee, Bombus terrestris . Apidologie 45, 106–115 (2014). https://doi.org/10.1007/s13592-013-0227-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13592-013-0227-4

Keywords

Navigation