Honeybees can recognise images of complex natural scenes for use as potential landmarks

Journal of Experimental Biology

Volumn 211, Issue 8, 2008, Pages 1180-1186

  Dyer, Adrian G ^a,b   Rosa, Marcello G P ^a   Reser, David H ^a  

^a MONASH UNIVERSITY   (Australia)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

Differential conditioning; Foraging; Landmark; Navigation; Spatial vision

Indexed keywords

ANIMAL; ARTICLE; ASSOCIATION; BEE; DECISION MAKING; DISCRIMINATION LEARNING; INSTRUMENTAL CONDITIONING; PATTERN RECOGNITION; PHOTOSTIMULATION; PHYSIOLOGY; VIDEORECORDING;

ANIMALS; BEES; CONDITIONING, OPERANT; CUES; DECISION MAKING; DISCRIMINATION LEARNING; PATTERN RECOGNITION, VISUAL; PHOTIC STIMULATION; VIDEO RECORDING;

APIS MELLIFERA; APOIDEA;

EID: 44349145090     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.016683     Document Type: Article

References (63)

1. Bernard, J., Stach, S. and Giurfa, M. (2007). Categorization of visual stimuli in the honeybee Apis mellifera. Anim. Cogn. 9, 257-270.
2. Blough, D. S. (1967). Stimulus generalisation as signal detection in pigeons. Science 158, 940-941.
3. Capaldi, E. A. and Dyer, F. C. (1995). Landmarks and dance orientation in the honeybee Apis mellifera. Naturwissenschaften 82, 245-247.
4. Cartwright, B. A. and Collett, T. S. (1983). Landmark learning in bees-experiments and models. J. Comp. Physiol. 151, 521-543.
5. Chen, L., Zhang, S. and Srinivasan, M. V. (2003). Global perception in smalll brains: topological pattern recognition in honey bees. Proc. Natl. Acad. Sci. USA 100, 6884-6889.
6. Chittka, L. and Geiger, K. (1995a). Can honeybees count landmarks? Anim. Behav. 49, 159-164.
7. Chittka, L. and Geiger, K. (1995b). Honeybee long-distance orientation in a controlled environment. Ethology 99, 117-126.
8. Chittka, L. and Tautz, J. (2003). The spectral input to honeybee visual odometry. J. Exp. Biol. 206, 2393-2397.
9. Chittka, L., Bonn, A., Geiger, K., Hellstern, F., Klein, J., Knoll, P., Koch, G., Meuser, S. and Menzel, R. (1992). Do bees navigate by means of snapshot memory pictures? In Rhythmogenesis in Neurons and Networks: Proceedings of the 20th Göttingen Neurobiology Conference (ed. N. Eisner and D. W. Richter), p. 694. Stuttgart: Georg Thieme Verlag.
10. Chittka, L., Kunze, J. and Geiger, K. (1995a). The influences of landmarks on distance estimation of honeybees. Anim. Behav. 50, 23-31.
11. Chittka, L., Kunze, J., Shipman, C. and Buchmann, S. L. (1995b). The significance of landmarks for path integration of homing honey bee foragers. Naturwissenschaften 82, 341-343.
12. Chittka, L., Dyer, A. G., Bock, F. and Dornhaus, A. (2003). Bees trade off foraging speed for accuracy. Nature 424, 388-388.
13. Collett, T. S. (1992). Landmark learning and guidance in insects. Philos. Trans. R. Soc. Lond. B Biol. Sci. 337, 295-303.
14. Collett, T. S. and Collett, M. (2002). Memory use in insect visual navigation. Nat. Rev. Neurosci. 3, 542-552.
15. Collett, T. S. and Zeil, J. (1997). The selection and use of landmarks by insects. In Orientation and Communication in Arthropods (ed. M. Lehrer), pp. 41-65. Basel: Birkhäuser Verlag.
16. Collishaw, S. M. and Hole, G. J. (2000). Featural and configural processes in the recognition of faces if different familiarity. Perception 29, 893-909.
17. de Brito Sanchez, M. G., Giurfa, M., de Paula Mota, T. R. and Gauthier, M. (2005). Electrophysiological and behavioural characterization of gustatory responses to antennal 'bitter' taste in honeybees. Eur. J. Neurosci. 22, 3161-3170.
18. Dill, M., Wolf, R. and Heisenberg, M. (1993). Visual pattern recognition in Drosophila involves retinotopic matching. Nature 365, 751-753.
19. Dyer, A. G. (2007). Windy condition affected colour discrimination in bumblebees (Hymenopteran: Apidea: Bombus). Entomol. Gen. 30, 165-166.
20. Dyer, A. G. and Chittka, L. (2004a). Bumblebees (Bombus terrestris) sacrifice foraging speed to solve difficult colour discrimination tasks. J. Comp. Physiol. A 190, 759-763.
21. Dyer, A. G. and Chittka, L. (2004b). Fine colour discrimination requires differential conditioning in bumblebees. Naturwissenschaften 91, 224-227.
22. Dyer, A. G. and Williams, S. K. (2005). Mechano-optical lens array to simulate insect vision photographically. Imag. Sci. J. 53, 209-213.
23. Dyer, A. G., Neumeyer, C. and Chittka, L. (2005). Honeybee (Apis mellifera) vision can discriminate between and recognise images of human faces. J. Exp. Biol. 208, 4709-4714.
24. Efler, D. and Ronacher, B. (2000). Evidence against retinoptic-template matching in honeybees pattern recognition. Vis. Res. 40, 3391-3403.
25. Franceschini, N., Ruffier, F. and Serres, J. (2007). A bio-inspired flying robot sheds light on insect piloting abilities. Curr. Biol. 17, 329-335.
26. Frisch, K. v. (1967). The Dance Language and Orientation of Bees. Cambridge, MA: Harvard University Press.
27. Giger, A. D. and Srinivasan, M. V. (1995). Pattern recognition in honeybees: eidetic imagery and orientation discrimination. J. Comp. Physiol. A 176, 791-795.
28. Giurfa, M. (2004). Conditioning procedure and color discrimination in the honeybee Apis mellifera. Naturwissenschaften 91, 228-231.
29. Giurfa, M., Eichmann, B. and Menzel, R. (1996). Symmetry perception in an insect. Nature 382, 458-461.
30. Giurfa, M., Hammer, M., Stach, S., Stollhoff, N., Müller-Delsig, N. and Mizyrycki, C. (1999). Pattern learning by honeybees: conditioning procedure and recognition strategy. Anim. Behav. 57, 315-324.
31. Giurfa, M., Zhang, S., Jenett, A., Menzel, R. and Srinivasan, M. V. (2001). The concepts of 'sameness' and 'difference' in an insect. Nature 410, 930-933.
32. Gould, J. L. and Gould, C. G. (1988). The Honey Bee. New York: Scientific American Library.
33. Graham, P., Durler, V. and Collett, T. (2007). The co-activation of snapshot memories in wood ants. J. Exp. Biol. 210, 2128-2136.
34. Green, D. H. and Swets, J. A. (1966). Signal Detection Theory and Psychophysics. New York: Wiley.
35. Horridge, A. (2005a). Recognition of a familiar place by the honeybee (Apis mellifera). J. Comp. Physiol. A 191, 301-316.
36. Land, M. F. (1997a). The resolution of insect compound eyes. Isr. J. Plant Sci. 45, 79-91.
37. Land, M. F. (1997b). Visual acuity in insects. Annu. Rev. Entomol. 42, 147-177.
38. Lehrer, M. (1991). Bees which turn back and look. Naturwissenschaften 78, 274-276.
39. Lehrer, M. (1993). Why do bees turn back and look? J. Comp. Physiol. A 172, 549-563.
40. Lynn, S. K., Cnaani, J. and Papaj, D. R. (2005). Peak shift discrimination learning as a mechanism of signal evolution. Evolution 59, 1300-1305.
41. Marston, H. M. (1996). Analysis of cognitive function in animals, the value of SDT. Brain Res. Cogn. Brain Res. 3, 269-277.
42. Menzel, R., Geiger, K., Chittka, L., Joerges, J., Kunze, J. and Müller, U. (1996). The knowledge base of bee navigation. J. Exp. Biol. 199, 141-146.
43. Miller, J. (1996). The sampling distribution of d. Percept. Psychophys. 58, 65-72.
44. Peng, Y., Xi, W., Zhang, W., Zhang, K. and Guo, A. (2007). Experience improves feature extraction in Drosophila. J. Neurosci. 27, 5139-5145.
45. Reinhard, J., Srinivasan, M. V., Guez, D. and Zhang, S. W. (2004). Floral scents induce recall of navigational and visual memories in honeybees. J. Exp. Biol. 207, 4371-4381.
46. Si, A., Srinivasan, M. V. and Zhang, S. (2003). Honeybee navigation: properties of the visually driven 'odometer'. J. Exp. Biol. 206, 1265-1273.
47. Sole, L. M., Shettleworth, S. J. and Bennett, P. J. (2003). Uncertainty in pigeons. Psychon. Bull. Rev. 10, 738-745.
48. Srinivasan, M. V. and Lehrer, M. (1988). Spatial acuity of honeybee vision and its spectral properties. J. Comp. Physiol. A 162, 159-172.
49. Srinivasan, M. V., Zhang, S. W. and Bidwell, N. J. (1997). Visually mediated odometry in honeybees. J. Exp. Biol. 200, 2513-2522.
50. Srinivasan, M. V., Zhang, S., Altwein, M. and Tautz, J. (2000). Honeybee navigation: nature and calibration of the 'odometer'. Science 287, 851-853.
51. Stach, S. and Giurfa, M. (2005). The influence of training length on generalization of visual feature assemblies in honeybees. Behav. Brain Res. 161, 8-17.
52. Stach, S., Bernard, J. and Giurfa, M. (2004). Local-feature assembling in the visual pattern recognition and generalization in honeybees. Nature 429, 758-761.
53. Steckler, T. (2001). Using signal detection theory for analysis of operant performance in mice. Behav. Brain Res. 125, 237-248.
54. Steffan-Dewenter, I. and Kuhn, A. (2003). Honeybee foraging in differentially structured landscapes. Proc. R. Soc. Lond. B Biol. Sci. 270, 569-575.
55. Thompson, K. G. and Schall, J. D. (2000). Antecedents and correlates of visual attention and awareness in macaque prefrontal cortex. Vis. Res. 40, 1523-1538.
56. Vladusich, T., Hemmi, J. M., Srinivasan, M. V. and Zeil, J. (2005). Interactions of visual odometry and landmark guidance during food search in honeybees. J. Exp. Biol. 208, 4123-4135.
57. von der Emde, G. and Fetz, S. (2007). Distance, shape and more: recognition of object features during active electrolocation in a weakly electric fish. J. Exp. Biol. 210, 3082-3095.
58. Winston, M. (1987). The Biology of the Honeybee. Cambridge: Harvard University Press.
59. Zeil, J. and Wittmann, D. (1993). Landmark orientation during the approach to the nest in the stingless bee Trigona (Tetragonisca) angustula (Apidae, Meliponinae). Insectes Soc. 40, 381-389.
60. Zhang, S. W. and Srinivasan, M. V. (2004). Exploration of cognitive capacity in honeybees: higher functions emerge from a small brain. In Complex Worlds from Simpler Nervous Systems (ed. F. R. Prete), pp. 41-74. Cambridge: The MIT Press.
61. Zhang, S. W., Bartsch, K. and Srinivasan, M. V. (1996). Maze learning by honeybees. Neurobiol. Learn. Mem. 66, 267-282.
62. Zhang, S. W., Mizutani, A. and Srinivasan, M. V. (2000). Maze navigation by honeybees: learning path regularity. Learn. Mem. 7, 364-374.
63. Zhang, S. W., Srinivasan, M. V., Zhu, H. and Wong, J. (2004). Grouping of visual objects by honeybees. J. Exp. Biol. 207, 3289-3298.