Honeybees (Apis mellifera) Learn Color Discriminations via Differential Conditioning Independent of Long Wavelength (Green) Photoreceptor Modulation

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

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

^a MONASH UNIVERSITY   (Australia)

^b RMIT UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANALYSIS OF VARIANCE; ANIMAL BEHAVIOR; ARTICLE; AVERSIVE BEHAVIOR; COLOR DISCRIMINATION; COLORIMETRY; CONDITIONING; CONTROLLED STUDY; HONEYBEE; LEARNING; LIGHT EMITTING DIODE; NEUROMODULATION; NONHUMAN; PHOTORECEPTOR; VISUAL SYSTEM;

ANIMALS; BEES; BEHAVIOR, ANIMAL; COLOR PERCEPTION; COLOR VISION; CONDITIONING (PSYCHOLOGY); CUES; DISCRIMINATION (PSYCHOLOGY); PHOTIC STIMULATION; PHOTORECEPTOR CELLS, INVERTEBRATE;

APIS MELLIFERA; APOIDEA; HEXAPODA;

EID: 84869143742     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0048577     Document Type: Article

References (74)

1. Chittka L, Wells H (2004) Color vision in bees: mechanisms, ecology and evolution. In: Prete F, editor. How simple nervous systems create complex perceptual worlds. Boston: MIT Press. pp. 165-191.
2. Chiao C-C, Cronin TW, Osorio D, (2000) Color signals in natural scenes: characteristics of reflectance spectra and effects of natural illuminants. J Opt Soc Am A 17: 218-224.
3. Chittka L, Menzel R, (1992) The evolutionary adaptation of flower colors and the insect pollinators' color vision systems. J Comp Physiol A 171: 171-181.
4. Dyer AG, Boyd-Gerny S, McLoughlin S, Rosa MGP, Simonov V, et al. (2012) Parallel evolution of angiosperm colour signals: common evolutionary pressures linked to hymenopteran vision. Proc Royal Soc B In press. doi:10.1098/rspb.2012.0827.
5. Daumer K, (1956) Reizmetrische Untersuchung des Farbensehens der Bienen. Z Vergl Physiol 38: 413-478.
6. von Frisch K, (1914) Der Farbensinn und Formensinn der Biene. Zool Jb (Physiol) 37: 1-238.
7. Spaethe J, Tautz J, Chittka L, (2006) Do honeybees detect colour targets using serial or parallel visual search? Journal of Experimental Biology 209: 987-993.
8. Srinivasan M, Lehrer M, (1985) Temporal resolution of colour vision in the honeybee. J Comp Physiol A 157: 579-586.
9. Menzel R, Backhaus W (1991) Colour vision in insects. In: Gouras P, editor. The Perception of Colour. London: Macmillan Press. pp. 262-293.
10. Hempel de Ibarra N, Giurfa M, Vorobyev M, (2002) Discrimination of coloured patterns by honeybees through chromatic and achromatic cues. J Comp Physiol A 188: 503-512.
11. Neumeyer C, (1981) Chromatic adaption in the honeybee: successive color contrast and color constancy. J Comp Physiol 144: 543-553.
12. Dyer AG, Neumeyer C, (2005) Simultaneous and successive colour discrimination in the honeybee (Apis mellifera). J Comp Physiol A 191: 547-557.
13. Llandres AL, Rodriguez-Girones MA, (2011) Spider Movement, UV Reflectance and Size, but Not Spider Crypsis, Affect the Response of Honeybees to Australian Crab Spiders. PLoS ONE 6: e17136.
14. Heiling AM, Herberstein ME, Chittka L, (2003) Pollinator attraction- Crab-spiders manipulate flower signals. Nature 421: 334-334.
15. Chittka L, Thomson JD, Waser NM, (1999) Flower constancy, insect psychology, and plant evolution. Naturwiss 86: 361-377.
16. Peitsch D, Fietz A, Hertel H, de Souza J, Ventura DF, et al. (1992) The spectral input systems of hymenopteran insects and their receptor-based colour vision. J Comp Physiol A 170: 23-40.
17. Kulikowski JJ, Walsh V (1991) On the limits of colour detection and discrimination. In: Kulikowski JJ, Walsh V, Murray JJ, Cronly-Dillion JR, editors. Vision and visual dysfunction: Limits of vision. London: Macmillian. pp. 202-220.
18. Helversen Ov, (1972) Zur spektralen Unterschiedsempfindlichkeit der honigbiene. J Comp Physiol 80: 439-472.
19. Brandt R, Vorobyev M, (1997) Metric analysis of treshold spectral sensitivity in the honeybee. Vision Res 37: 425-439.
20. Dyer AG, Paulk AC, Reser DH, (2011) Colour processing in complex environments: insights from the visual system of bees. Proc Royal Soc B 278: 952-959.
21. Giurfa M, (2004) Conditioning procedure and color discrimination in the honeybee Apis mellifera. Naturwiss 91: 228-231.
22. Avarguès-Weber A, de Brito Sanchez MG, Giurfa M, Dyer AG, (2010) Aversive reinforcement improves visual discrimination learning in free flying honeybees. PLOS One pp. e15370.
23. Dyer AG, Murphy AH, (2009) Honeybees choose "incorrect" colors that are similar to target flowers in preference to novel colors. Isr J Plant Sci 57: 203-210.
24. Giurfa M, Vorobyev M, Kevan P, Menzel R, (1996) Detection of coloured stimuli by honeybees: minimum visual angles and receptor specific contrasts. J Comp Physiol A 178: 699-709.
25. Giurfa M, Vorobyev M, Brandt R, Posner B, Menzel R, (1997) Discrimination of coloured stimuli by honeybees: alternative use of achromatic and chromatic signals. J Comp Physiol A 180: 235-243.
26. Lehrer M (1993) Parallel processing of motion, shape and colour in the visual system of the bee. In: Wiese K, editor. Sensory Systems of Arthropods. Basel: Birkhäuser Verlag.
27. Ribi WA, Scheel M, (1981) The second and third optic ganglia of the worker bee. Golgi studies of the neuronal elements in the medulla and lobula. Cell Tissue Res 221: 17-43.
28. Paulk AC, Dacks AM, Gronenberg W, (2009) Color Processing in the Medulla of the Bumblebee (Apidae: Bombus impatiens). The Journal of Comparative Neurology 513: 441-456.
29. Menzel R, (1974) Spectral sensitivity of monopolar cells in the bee lamina. J Comp Physiol 93: 337-346.
30. Ribi WA, (1975) The first optic ganglion of the bee. I. Correlation between visual cell types and their terminals in the lamina and medulla. Cell Tiss Res 165: 103-111.
31. Ribi WA, (1975) The neurons in the first optic ganglion of the bee (Apis mellifera). Advan Anat Embryol and Cell Biol 50: 1-43.
32. Dyer AG, Spaethe J, Prack S, (2008) Comparative psychophysics of bumblebee and honeybee colour discrimination and object detection. J Comp Physiol A 194: 617-627.
33. Giurfa M, Lehrer M (2001) Honeybee vision and floral displays: from detection to close-up recognition. In: Chittka L, Thomson JD, editors. Cognitive Ecology of Pollination. Cambridge: University Press. pp. 61-82.
34. Kaiser W, Liske E, (1974) Die optomotorischen Reaktionen von fixiert fliegenden Bienen bei Reizung mit Spektrallichtern. J Comp Physiol 89: 391-408.
35. Srinivasan MV, Lehrer M, (1984) Temporal acuity of honeybee vision: behavioural studies using moving stimuli. J Comp Physiol A 155: 297-312.
36. Stojcev M, Radtke N, D'Amaro D, Dyer AG, Neumeyer C, (2011) General principles in motion vision: color-blindness of object motion depends on pattern velocity in honeybee and goldfish. Visual Neuroscience 28: 361-370.
37. Stach S, Bernard J, Giurfa M, (2004) Local-feature assembling in the visual pattern recognition and generalization in honeybees. Nature 429: 758-761.
38. Mota T, Yamagata N, Giurfa M, Gronenberg W, Sandoz JC, (2011) Neural organization and visual processing in the anterior optic tubercle of the honeybee brain. J Neurosci 31: 11443-11456.
39. von Frisch K (1967) The Dance Language and Orientation of Bees. Cambridge: Harvard Univ. Press.
40. Dyer AG, (2007) Windy conditions affected colour discrimination in bumblebees (Hymenopteran: Apidea: Bombus). Entomol Gen 30: 165-166.
41. Dyer AG, (1998) The colour of flowers in spectrally variable illumination and insect pollinator vision. J Comp Physiol A 183: 203-212.
42. Wyszecki G, Stiles WS (1982) Color science: Concepts and methods, quantitative data and formulae. New York: Wiley.
43. Hempel de Ibarra N, Giurfa M, Vorobyev M, (2001) Detection of coloured patterns by honeybees through chromatic and achromatic cues. J Comp Physiol A 187: 215-224.
44. Dyer AG, Chittka L, (2004) Biological significance of distinguishing between similar colours in spectrally variable illumination: bumblebees (Bombus terrestris) as a case study. J Comp Physiol A 190: 105-114.
45. Morawetz L, Spaethe J, (2012) Visual attention in a complex search task differs between honeybees and bumblebees. J Exp Biol 215: 2515-2523.
46. Dyer AG, (1999) Broad spectral sensitivities in the honeybee's photoreceptors limit colour constancy. J Comp Physiol A 185: 445-453.
47. Backhaus W, (1991) Color opponent coding in the visual system of the honeybee. Vision Res 31: 1381-1397.
48. Backhaus W, Menzel R, Kreissl S, (1987) Multidimensional scaling of color similarity in bees. Biol Cybern 56: 293-304.
49. Chittka L, Beier W, Hertel H, Steinmann E, Menzel R, (1992) Opponent colour coding is a universal strategy to evaluate the photoreceptor inputs in hymentoptera. J Comp Physiol A 170: 545-563.
50. Menzel R, (1967) Untersuchungen zum Erlernen von Spektralfarben durch die Honigbiene (Apis mellifica). Z Vergl Physiol 56: 22-62.
51. Lehrer M, Bischof S, (1995) Detection of model flowers by honeybees: the role of chromatic and achromatic contrast. Naturwiss 82: 145-147.
52. Hempel de Ibarra N, Giurfa M, (2003) Discrimination of closed coloured shapes by honeybees requires only contrast to the long wavelength receptor type. Anim Behav 66: 903-910.
53. Niggebrugge C, Hempel de Ibarra N, (2003) Colour-dependent target detection by bees. J Comp Physiol A 189: 915-918.
54. Kelber A, (2005) Alternative use of chromatic and achromatic cues in a hawkmoth. Proc R Soc B 272: 2143-2147.
55. Lehrer M, (1999) Dorsoventral asymmetry of colour discrimination in bees. J Comp Physiol A 184: 195-206.
56. Neumeyer C, (1980) Simultaneous color contrast in the honey bee. J Comp Physiol 139: 165-176.
57. Vorobyev M, Brandt R, (1997) How do insect pollinators discriminate colors? Isr J Plant Sci 45: 103-113.
58. Hempel de Ibarra N, Vorobyev M, Brandt R, Giurfa M, (2000) Detection of bright and dim colours by honeybees. J Exp Biol 203: 3289-3298.
59. Dyer AG, Chittka L, (2004) Fine colour discrimination requires differential conditioning in bumblebees. Naturwiss 91: 224-227.
60. Dyer AG, Chittka L, (2004) Bumblebees (Bombus terrestris) sacrifice foraging speed to solve difficult colour discrimination tasks. J Comp Physiol A 190: 759-763.
61. Stach S, Giurfa M, (2005) The influence of training length on generalization of visual feature assemblies in honeybees. Behav Brain Res 161: 8-17.
62. Whitney HM, Kolle M, Andrew L, Chittka L, Glover BJ, (2009) Floral iridescence, produced by diffractive optics, acts as a cue for animal pollinators. Science 323: 130-133.
63. Avarguès-Weber A, Portelli G, Benard J, Dyer A, Giurfa M, (2010) Configural processing enables discrimination and categorization of face-like stimuli in honeybees. J Exp Biol 213: 593-601.
64. Menzel R, Erber J, Masuhr T (1974) Learning and memory in the honeybee. In: Barton-Browne L, editor. Experimental analysis of insect behaviour. Berlin: Springer. pp. 195-217.
65. Burns JG, Dyer AG, (2008) Diversity of speed accuracy strategies benefits social insects. Curr Biol 18: R953-R954.
66. Kelber A, (2010) What a hawkmoth remembers after hibernation depends on innate preferences and conditioning situation. Behav Ecol 21: 1093-1097.
67. Camlitepe Y, Aksoy V, (2010) First evidence of fine colour discrimination ability in ants (Hymenoptera, Formicidae). J Exp Biol 213: 72-77.
68. Kelber A, Pfaff M, (1999) True colour vision in the orchard butterfly, Papilio aegeus. Naturwiss 86: 221-224.
69. Kunze J, Gumbert A, (2001) The combined effect of color and odor on flower choice behavior of bumble bees in flower mimicry systems. Behav Ecol 12: 447-456.
70. Jacobs GH, Williams GA, Cahill H, (2007) Emergence of Novel Color Vision in Mice Engineered to Express a Human Cone Pigment. Science 315: 1723-1725.
71. Mancuso K, Hauswirth WW, Li Q, Connor TB, Kuchenbecker JA, et al. (2009) Gene therapy for red-green colour blindness in adult primates. Nature 461: 784-787.
72. Paulk AC, Dacks AM, Phillips-Portillo J, Fellous JM, Gronenberg W, (2009) Visual Processing in the Central Bee Brain. J Neurosci 29: 9987-9999.
73. Paulk AC, Phillips-Portillo J, Dacks AM, Fellous J, Gronenberg W, (2008) The processing of colour, motion, and stimulus timing are anatomically segregated in the bumblebee brain. The Journal of Neuroscience 28: 6319-6332.
74. Paulk AC, Gronenberg W, (2008) Higher order visual input to the mushroom bodies in the bee, Bombus impatiens. Arthropod Structure and Development 37: 443-458.