Skip to main content
Log in

Honeybees use a Lévy flight search strategy and odour-mediated anemotaxis to relocate food sources

  • Original Paper
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

The availability of food resources changes over time and space, and foraging animals are constantly faced with choices about how to respond when a resource becomes depleted. We hypothesise that flying insects like bees discover new food sources using an optimal Lévy flight searching strategy and odour-mediated anemotaxis, as well as visual cues. To study these searching patterns, foraging honeybees were trained to a scented feeder which was then removed. Two new unrewarding feeders, or ‘targets’, were then positioned up- and downwind of the original location of the training feeder. The subsequent flight patterns of the bees were recorded over several hundred metres using harmonic radar. We show that the flight patterns constitute an optimal Lévy flight searching strategy for the location of the training feeder, a strategy that is also optimal for the location of alternative food sources when patchily distributed. Scented targets that were positioned upwind of the original training feeder were investigated most with the numbers of investigations declining with increasing distance from the original feeder. Scented targets in downwind locations were rarely investigated and unscented targets were largely ignored, despite having the same visual appearance as the rewarding training feeder.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Baker TC, Vickers NJ (1997) Pheromone-mediated flight in moths. In: Cardé RT, Minks AK (eds) Insect pheromone research: new directions. Chapman and Hall, New York, pp 248–264

    Google Scholar 

  • Bartumeus F, Peters F, Pueyo S, Marrase C, Catalan J (2003) Helical Levy walks: adjusting searching statistics to resource availability in microzooplankton. Proc Natl Acad Sci 100:12771–12775

    Article  CAS  PubMed  Google Scholar 

  • Capaldi EA, Smith AD, Osborne JL, Fahrbach SE, Farris SM, Reynolds DR, Edwards AS, Martin A, Robinson GE, Poppy GM, Riley JR (2000) Ontogeny of orientation flight in the honeybee revealed by harmonic radar. Nature 403:537–540

    Article  CAS  PubMed  Google Scholar 

  • Cardé RT, Mafra-Neto A (1997) Mechanisms of flight of male moths to pheromone. In: Cardé RT, Minks AK (eds) Insect pheromone research: new directions. Chapman and Hall, New York, pp 275–290

    Google Scholar 

  • Cheng K (2000) How honeybees find a place: lessons from a simple mind. Anim Learn Behav 28:1–15

    Google Scholar 

  • Dobson HEM (1994) In: Bernays EA (ed) Floral volatiles in insect biology. In: Insect - Plant Interactions Volume V. CRC Press, Boca Raton, FL, pp. 47-81

  • Edwards AM (2008) Using likelihood to test for Lévy flight search patterns and for general power-law distributions in nature. J Ecol 77:1212–1222

    Article  Google Scholar 

  • Edwards AM, Phillips RA, Watkins NW, Freeman MP, Murphy EJ, Afanasyev V, Buldyrev SV, da Luz MGE, Raposo EP, Stanley HE, Viswanathan GM (2007) Revisiting Lévy flight search patterns of wandering albatrosses, bumblebees and deer. Nature 449:1044–1048

    Article  CAS  PubMed  Google Scholar 

  • Giurfa M, Menzel R (1997) Insect visual perception: complex abilities of simple nervous systems. Curr Opin Neurobiol 7:505–513

    Article  CAS  PubMed  Google Scholar 

  • Giurfa M, Nunez J, Backhaus W (1994) Odour and color information in the foraging choice behaviour of the honeybee. J Comp Physiol 175:773–779

    Article  Google Scholar 

  • Giurfa M, Vorobyev M, Kevan PG, Menzel R (1996) Detection of coloured stimuli by honeybees: minimum visual angles and receptor specific contrasts. J Comp Physiol 178:699–709

    Article  Google Scholar 

  • Kennedy JS (1983) Zigzagging and casting as a programme response to wind-borne odor—a review. Physiol Entomol 8:109–120

    Article  Google Scholar 

  • Kennedy JS (1986) Some current issues in orientation to odour sources. In: Payne TL, Birch MC, Kennedy CEJ (eds) Mechanisms in insect olfaction. Clarendon, Oxford, pp 11–25

    Google Scholar 

  • Mafra-Neto A, Cardé RT (1994) Fine-scale structure of pheromone plumes modulates upwind orientation of flying moths. Nature 369:142–144

    Article  CAS  Google Scholar 

  • McFrederick QS, Kathilankal JC, Fuentes JD (2008) Air pollution modifies floral scent trails. Atmos Environ 46:2336–2348

    Article  Google Scholar 

  • Murlis J, Elkinton JS, Cardé RT (1992) Odor plumes and how insects use them. Annu Rev Entomol 37:505–532

    Article  Google Scholar 

  • Peng CK, Hausdorff JM, Mietus JE, Havlin S, Stanley HE, Goldberger AL (1993) Long-range anticorrelations and non-Gaussian behaviour in the heartbeat. Phys Rev Lett 70:1343–1346

    Article  Google Scholar 

  • Reynolds AM (2008) Optimal random Lévy-loop searching: new insights into the searching behaviours of central place foragers. Europhysics Letters. 82, article 20001

    Google Scholar 

  • Reynolds AM (2009) Lévy flight patterns are an emergent property of a bumblebees’ foraging strategy. Behav Ecol Sociobiol . doi:10/1007/s00265-009-0813-7

    Google Scholar 

  • Reynolds AM, Frye MA (2007) Free-flight odor tracking in Drosophila is consistent with an optimal intermittent scale-free search. PLoS ONE 4:e354

    Article  Google Scholar 

  • Reynolds AM, Rhodes CJ (2009) The Lévy flight paradigm: random search patterns and mechanisms. Ecology 90:877–887

    Article  CAS  PubMed  Google Scholar 

  • Reynolds AM, Smith AD, Reynolds DR, Carreck NL, Osborne JL (2007a) Honeybees perform optimal scale-free searching flights when attempting to locate a food source. J Exp Biol 210:3763–3770

    Article  PubMed  Google Scholar 

  • Reynolds AM, Smith AD, Menzel R, Greggers U, Reynolds DR, Riley JR (2007b) Displaced honey bees perform optimal scale-free search flights. Ecology 88:1955–1961

    Article  PubMed  Google Scholar 

  • Riley JR, Smith AD (2002) Design considerations for an harmonic radar to investigate the flight of insects at low level. Comp Electron Agric 35:151–169

    Article  Google Scholar 

  • Riley JR, Smith AD, Reynolds DR, Edwards AS, Osborne JL, Williams IH, Carreck NL, Poppy GM (1996) Tracking bees with harmonic radar. Nature 379:29–30

    Article  CAS  Google Scholar 

  • Riley JR, Reynolds DR, Smith AD, Edwards AS, Osborne JL, Williams IH, McCartney HA (1999) Compensation for the wind by foraging bumble bees. Nature 400:126–127

    Article  CAS  Google Scholar 

  • Riley JR, Greggers U, Smith AD, Stach S, Reynolds DR, Stollhoff N, Brandt R, Schaupp F, Menzel R (2003) The automatic pilot of honeybees. Proc Roy Soc Lond B 270:2421–2424

    Article  CAS  Google Scholar 

  • Riley JR, Greggers U, Smith AD, Reynolds DR, Menzel R (2005) The flight paths of honeybees recruited by the waggle dance. Nature 435:205–207

    Article  CAS  PubMed  Google Scholar 

  • Vickers NJ, Baker TC (1994) Reiterative responses to single strands of odor promote sustained upwind flight and odor source location by moths. Proc Natl Acad Sci 91:5756–5760

    Article  CAS  PubMed  Google Scholar 

  • Viswanathan GM, Afanasyev V, Buldyrev SV, Murphy EJ, Prince PA, Stanley HE (1996) Lévy flight search patterns of wandering albatrosses. Nature 381:413–415

    Article  CAS  Google Scholar 

  • Viswanathan GM, Buldyrev SV, Havlin S, da Luz MGE, Raposo EP, Stanley HE (1999) Optimizing the success of random searches. Nature 401:911–914

    Article  CAS  PubMed  Google Scholar 

  • Viswanathan GM, Raposo EP, da Luz MGE (2008) Lévy flights and superdiffusion in the context of biological encounters and random searches. Physics of Life Reviews 5:133–150

    Article  Google Scholar 

  • Vladusich T, Hemmi JM, Zeil J (2006) Honeybee odometry and scent guidance. J Exp Biol 209:1367–1375

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Williams NH, Dodson CH (1972) Selective attraction of male euglossine bees to orchid floral fragrances and its importance in long distance pollen flow. Evolution 26:84–95

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the Biotechnology and Biological Sciences Research Council (Grant BB/E010695/1). Rothamsted Research receives grant-aided assistance from the Biotechnological and Biological Sciences Research Council of the United Kingdom. Thanks are also due to Shane Hatty, Richard Elsam and Amy McDougall.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Andrew M. Reynolds.

Additional information

Communicated by M. Giurfa

Rights and permissions

Reprints and permissions

About this article

Cite this article

Reynolds, A.M., Swain, J.L., Smith, A.D. et al. Honeybees use a Lévy flight search strategy and odour-mediated anemotaxis to relocate food sources. Behav Ecol Sociobiol 64, 115–123 (2009). https://doi.org/10.1007/s00265-009-0826-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-009-0826-2

Keywords

Navigation