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Naturwissenschaften

, 95:1181 | Cite as

A bee in the corridor: centering and wall-following

  • Julien R. SerresEmail author
  • Guillaume P. Masson
  • Franck Ruffier
  • Nicolas Franceschini
Short Communication

Abstract

In an attempt to better understand the mechanism underlying lateral collision avoidance in flying insects, we trained honeybees (Apis mellifera) to fly through a large (95-cm wide) flight tunnel. We found that, depending on the entrance and feeder positions, honeybees would either center along the corridor midline or fly along one wall. Bees kept following one wall even when a major (150-cm long) part of the opposite wall was removed. These findings cannot be accounted for by the “optic flow balance” hypothesis that has been put forward to explain the typical bees’ “centering response” observed in narrower corridors. Both centering and wall-following behaviors are well accounted for, however, by a control scheme called the lateral optic flow regulator, i.e., a feedback system that strives to maintain the unilateral optic flow constant. The power of this control scheme is that it would allow the bee to guide itself visually in a corridor without having to measure its speed or distance from the walls.

Keywords

Insect flight Honeybee Apis mellifera Vision Optic flow Collision avoidance Image motion 

Abbreviation

OF

optic flow

Notes

Acknowledgments

We are grateful to Stéphane Viollet and Goeffrey Portelli for their fruitful comments and suggestions during this work, to Serge Dini (beekeeper) for his expert knowledge on honeybees’ behavior, to Marc Boyron (electronics engineer), Yannick Luparini, and Fabien Paganucci (mechanical engineers), and Robert Tollari (land surveyor) for their expert technical assistance, to Dominique de Vienne for his help with the statistical analysis. The three anonymous referees’ constructive comments have improved the paper considerably, and we are very grateful to them. This research was supported by CNRS (Life Science and Information & Engineering Science), by EU contract (IST/FET–1999-29043) and DGA contract (2005-0451037).

References

  1. Baird E, Srinivasan MV, Zhang SW, Cowling A (2005) Visual control of flight speed in honeybees. J Exp Biol 208:3895–3905PubMedCrossRefGoogle Scholar
  2. Buchner E (1984) Behavioral analysis of spatial vision in insects. In: Ali MA (ed) Photoreception and vision in invertebrates. New York, Plenum, pp 561–621Google Scholar
  3. Collett T, King AJ (1975) Vision during flight. In: Horridge GA (ed) The compound eye and vision of insects. Clarendon, Oxford, pp 437–466Google Scholar
  4. Collett TS, Nalbach H-O, Wagner H (1993) Visual stabilization in the arthropods. In: Miles FA, Wallman J (eds) Visual motion and its role in the stabilization of gaze, Chapter 11. Elsevier, Amsterdam, pp 239–263Google Scholar
  5. David CT (1978) The relationship between body angle and flight speed in free flying Drosophila. Physiol Entomol 3:191–195CrossRefGoogle Scholar
  6. Franceschini N, Ruffier F, Serres J (2007) A bio-inspired flying robot sheds light on insect piloting abilities. Current Biol 17:329–335CrossRefGoogle Scholar
  7. Gibson JJ (1950) The perception of the visual world. Boston, Houghton MifflinGoogle Scholar
  8. Heusser D, Wehner R (2002) The visual centering response in desert ants, Cataglyphis fortis. J Exp Biol 205:585–590PubMedGoogle Scholar
  9. Hrncir M, Jarau S, Zucchi R, Barth FG (2004) Thorax vibrations of the stingless bee (Melipona seminigra). I. No influence of visual flow. J Comp Physiol A 190:539–548Google Scholar
  10. Ibbotson MR (2001) Evidence for velocity-tuned motion sensitive descending neurons in the honeybee. Proc R Soc B 268:2195–2201PubMedCrossRefGoogle Scholar
  11. Kaiser W, Liske E (1974) Die optomotorischen Reaktionen von fixiert fliegenden Bienen bei Reizung mit Spektrallichtern. J Comp Physiol 89:391–408CrossRefGoogle Scholar
  12. Kennedy JS (1939) Visual responses of flying mosquitoes. Proc Zool Soc Lond 109:221–242Google Scholar
  13. Kirchner WH, Srinivasan MV (1989) Freely flying honeybees use image motion to estimate object distance. Naturwissenchaften 76:281–282CrossRefGoogle Scholar
  14. Lee DN (1980) The optic flow field: the foundation of vision. Phil Trans Roy Soc Lond B 290:169–179CrossRefGoogle Scholar
  15. Ruffier F, Franceschini N (2005) Optic flow regulation: the key to aircraft automatic guidance. Robot Auton Syst 50(4):177–194CrossRefGoogle Scholar
  16. Seidl R, Kaiser W (1981) Visual field size, binocular domain and the ommatidial array of the compound eyes in worker honey bees. J Comp Physiol A 143:17–26CrossRefGoogle Scholar
  17. Seidl R (1982) Die Sehfelder und Ommatidien-Divergenzwinkel von Arbeiterin, Konigin und Drohne der Honigbiene (Apis mellifica). PhD thesis, Darmstadt: Technische Hochschule Darmstadt, No. DO3046.Google Scholar
  18. Serres J, Dray D, Ruffier F, Franceschini, N (2008) A vision-based autopilot for a miniature air vehicle: joint speed control and lateral obstacle avoidance. Auton Robots 25:103–144CrossRefGoogle Scholar
  19. Shoemaker PA, O’Caroll DC, Straw AD (2005) Velocity constancy and models for wide-field visual motion detection in insects. Biol Cybern 93:275–287PubMedCrossRefGoogle Scholar
  20. Srinivasan MV, Lehrer M, Kirchner WH, Zhang SW (1991) Range perception through apparent image speed in freely flying honeybees. Vis Neurosci 6:519–535PubMedCrossRefGoogle Scholar
  21. Srinivasan MV, Zhang SW, Chandrashekara K (1993) Evidence for two distinct movement-detecting mechanisms in insect vision. Naturwissenschaften 80:38–41CrossRefGoogle Scholar
  22. Srinivasan MV, Zhang SW, Lehrer M, Collett TS (1996) Honeybee navigation en route to the goal: visual flight control and odometry. J Exp Biol 199:237–244PubMedGoogle Scholar
  23. Srinivasan MV, Zhang SW (2004) Visual motor computations in insects. Ann Rev Neurosci 27:679–696PubMedCrossRefGoogle Scholar
  24. Straw AD, Rainsford T, O’Carroll DC (2008) Contrast sensitivity of insect motion detectors to natural images. J Vision 8:1–9CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Julien R. Serres
    • 1
    Email author
  • Guillaume P. Masson
    • 1
  • Franck Ruffier
    • 1
  • Nicolas Franceschini
    • 1
  1. 1.Biorobotics Lab., Institute of Movement ScienceCNRS and University of the MediterraneanMarseille cedex 09France

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