Advertisement

Evolutionary Ecology

, Volume 31, Issue 2, pp 153–172 | Cite as

Assessing the ecological significance of bee visual detection and colour discrimination on the evolution of flower colours

  • Zoë Bukovac
  • Alan Dorin
  • Valerie Finke
  • Mani Shrestha
  • Jair Garcia
  • Aurore Avarguès-Weber
  • Martin Burd
  • Jürgen Schramme
  • Adrian Dyer
Article

Abstract

Bee pollinators interact with flowers in a complex signal-receiver system. Chromatic traits that allow reliable discrimination between rewarding and non-rewarding flowers have been proposed as an important feature of pollination syndromes: bee-pollinated flowers have spectral profiles that closely match the discrimination peaks of their pollinators across the visual spectrum. However, in the complexity of a natural environment, it may be hard for bees to even detect the presence of flowers. In particular, little is known about how discrimination and detection by bees may together contribute to pollinator-mediated selection on floral colour signals. We address here an unexplained feature of floral colour evolution: the extreme paucity of spectral patterns with pronounced changes in reflectance around 420–480 nm wavelength. We began by conducting experiments with honeybees in a Y-maze to determine their capacity to detect a stimulus rarely found in bee-pollinated flowers—one with a single sharp spectral reflectance change at 478 nm. We found bees to be poor at detecting this stimulus against a neutral background. We then conducted behaviourally-informed computer simulations that test how bee visual discrimination and detection interact, which yielded information about which flower colours most effectively facilitate cross-pollination. Finally, we identified from our previous work those bird-pollinated species whose floral colours had spectral characteristics similar to the stimulus used in the Y-maze experiment. These data demonstrate that plants can, and do, produce such spectra for pollinators other than bees. In combination, our results show that the interaction between colour discrimination and detection is important for understanding flower community assembly.

Keywords

Behaviour Computer simulation Plant phylogeny Vision Y-maze 

Notes

Acknowledgments

A.D. and A.G.D acknowledge ARC Grants DP130100015 and DP160100161. We thank Melbourne University, School of Biological Sciences, for access to bees to conduct experiments. We thank Adrian Ryan for plant identification.

Supplementary material

Supplementary material 1 (mp4 57275 KB)

References

  1. Arnold SEJ, Savolainen V, Chittka L (2009) Flower colours along an alpine altitude gradient, seen through the eyes of fly and bee pollinators. Arthropod Plant Interact 3(1):27–43CrossRefGoogle Scholar
  2. Avarguès-Weber A, Giurfa M (2014) Cognitive components of color vision in honey bees: how conditioning variables modulate color learning and discrimination. J Comp Physiol A 200(6):449–461CrossRefGoogle Scholar
  3. Avarguès-Weber A, de Brito Sanchez MG, Giurfa M, Dyer AG (2010) Aversive reinforcement improves visual discrimination learning in free-flying honeybees. PLoS One 5(10):e15,370CrossRefGoogle Scholar
  4. Backhaus W (1991) Color opponent coding in the visual system of the honeybee. Vis Res 31(7):1381–1397CrossRefPubMedGoogle Scholar
  5. Barth FG (1985) Insects and flowers. The biology of a partnership. George Allen and Unwin, Crows NestGoogle Scholar
  6. Becher MA, Grimm V, Thorbek P, Horn J, Kennedy PJ, Osborne JL (2014) Beehave: a systems model of honeybee colony dynamics and foraging to explore multifactorial causes of colony failure. J Appl Ecol 51(2):470–482CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bischoff M, Lord J, Robertson A, Dyer AG (2013) Hymenopteran pollinators as agents of selection on flower colour in the New Zealand mountains: salient chromatic signals enhance flower discrimination. N Z J Bot 51(3):181–193CrossRefGoogle Scholar
  8. Briscoe AD, Chittka L (2001) The evolution of colour vision in insects. Annu Rev Entomol 46(1):471–510CrossRefPubMedGoogle Scholar
  9. Brooker M, Kleinig D (1999) Field guide to eucalypts, vol 1. Inkata Press Pty Ltd, South-eastern AustraliaGoogle Scholar
  10. Bukovac Z, Dorin A, Dyer A (2013) A-Bees See: a simulation to assess social bee visual attention during complex search tasks. In: Liò P, Miglino O, Nicosia G, Nolfi S, Pavone M (eds) Advances in artificial life, ECAL 2013. Proceedings of the twelfth European conference on the synthesis and simulation of living systems, Taormina, September 2013. Complex Adaptive Systems, MIT Press, Cambridge, London, pp 276–283Google Scholar
  11. Burns JG, Dyer AG (2008) Diversity of speed accuracy strategies benefits social insects. Curr Biol 18:R953–R954CrossRefPubMedGoogle Scholar
  12. Chittka L (1992) The colour hexagon: a chromaticity diagram based on photoreceptor excitations as a generalized representation of colour opponency. J Comp Physiol A 170(5):533–543Google Scholar
  13. Chittka L, Menzel R (1992) The evolutionary adaptation of flower colours and the insect pollinators’ colour vision. J Comp Physiol A 171(2):171–181CrossRefGoogle Scholar
  14. Chittka L, Waser N (1997) Why red flowers are not invisible to bees. Isr J Plant Sci 45(2–3):169–183CrossRefGoogle Scholar
  15. Chittka L, Thomson JD (2001) Cognitive ecology of pollination: animal behaviour and floral evolution. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  16. Chittka L, Wells H (2004) Color vision in bees mechanims, ecology, and evolution. In: Prete FR (ed) Complex worlds from simpler nervous systems. The MIT Press, Cambridge, pp 165–191Google Scholar
  17. Chittka L, Kevan P (2005) Flower colour as advertisement. In: Dafni A, Kevan P, Husband B (eds) Practical pollination biology. Enviroquest Ltd, Cambridge, pp 157–196Google Scholar
  18. Chittka L, Osorio D (2007) Cognitive dimensions of predator responses to imperfect mimicry? PLoS Biol 5(12):2754–2758CrossRefGoogle Scholar
  19. Chittka L, Thomson JD, Waser NM (1999) Flower constancy, insect psychology, and plant evolution. Naturwissenschaften 86(8):361–377CrossRefGoogle Scholar
  20. Chittka L, Shmida A, Troje N, Menzel R (1994) Ultraviolet as a component of flower reflections, and the colour perception of Hymenoptera. Vis Res 34(11):1489–1508CrossRefPubMedGoogle Scholar
  21. Chittka L, Dyer AG, Bock F, Dornhaus A (2003) Psychophysics: bees trade off foraging speed for accuracy. Nature 424(6947):388–388CrossRefPubMedGoogle Scholar
  22. Daumer K (1956) Reizmetrische Untersuchung des Farbensehens der Bienen. Z Vergl Physiol 38(5):413–478Google Scholar
  23. Dyer AG (2006) Discrimination of flower colours in natural settings by the bumblebee species Bombus terrestris (Hymenoptera: Apidae). Entomol Gen 28(4):257–268CrossRefGoogle Scholar
  24. Dyer AG, Spaethe J, Prack S (2008) Comparative psychophysics of bumblebee and honeybee colour discrimination and object detection. J Comp Physiol A 194(7):617–627CrossRefGoogle Scholar
  25. Dyer AG, Paulk AC, Reser DH (2011) Colour processing in complex environments: insights from the visual system of bees. Proc R Soc Lond B Biol 278(1707):952–959CrossRefGoogle Scholar
  26. Dyer AG, Garcia JE, Shrestha M, Lunau K (2015) Seeing in colour: a hundred years of studies on bee vision since the work of the Nobel laureate Karl von Frisch. Proc R Soc Vic 127(1):66–72CrossRefGoogle Scholar
  27. Dyer AG, Whitney HM, Arnold SEJ, Glover BJ, Chittka L (2006) Behavioural ecology: bees associate warmth with floral colour. Nature 442(7102):525–525CrossRefPubMedGoogle Scholar
  28. Dyer AG, Whitney HM, Arnold SEJ, Glover BJ, Chittka L (2007) Mutations perturbing petal cell shape and anthocyanin synthesis influence bumblebee perception of Antirrhinum majus flower colour. Arthropod Plant Interact 1(1):45–55CrossRefGoogle Scholar
  29. Dyer AG, Dorin A, Reinhardt V, Garcia JE, Rosa M (2014) Bee reverse-learning behavior and intra-colony differences: simulations based on behavioral experiments reveal benefits of diversity. Ecol Model 277:119–131CrossRefGoogle Scholar
  30. Dyer AG, Boyd-Gerny S, McLoughlin S, Rosa MGP, Simonov V, Wong BBM (2012) Parallel evolution of angiosperm colour signals: common evolutionary pressures linked to hymenopteran vision. Proc R Soc Lond B Biol 279(1742):3606–3615CrossRefGoogle Scholar
  31. Evans LJ, Raine NE (2014) Foraging errors play a role in resource exploration by bumble bees (Bombus terrrestris). J Comp Physiol A 200(6):475–484CrossRefGoogle Scholar
  32. Ford HA, Paton DC (1976) Resource partitioning and competition in honeyeaters of the genus Meliphaga. Aust J Ecol 1(4):281–287CrossRefGoogle Scholar
  33. Ford HA, Paton DC, Forde N (1979) Birds as pollinators of Australian plants. N Z J Bot 17(4):509–519CrossRefGoogle Scholar
  34. Gallai N, Salles JM, Settele J, Vaissière BE (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol Econ 68(3):810–821CrossRefGoogle Scholar
  35. Giurfa M (2004) Conditioning procedure and color discrimination in the honeybee Apis mellifera. Naturwissenschaften 91:228–231CrossRefPubMedGoogle Scholar
  36. 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(5):699–709CrossRefGoogle Scholar
  37. Grimm V, Railsback SF (2005) Individual-based modeling and ecology. Princeton University Press, PrincetonCrossRefGoogle Scholar
  38. Grimm V, Revilla E, Berger U, Jeltsch F, Mooij WM, Railsback SF, Thulke H, Weiner J, Wiegand T, DeAngelis DL (2005) Pattern-oriented modeling of agent-based complex systems: lessons from ecology. Science 310(5750):987–991CrossRefPubMedGoogle Scholar
  39. Gumbert A (2000) Color choices by bumble bees (bombus terrestris): innate preferences and generalization after learning. Behav Ecol Sociobiol 48(1):36–43CrossRefGoogle Scholar
  40. Hempel de Ibarra N, Vorobyev M, Menzel R (2014) Mechanisms, functions and ecology of colour vision in the honeybee. J Comp Physiol A 200(6):411–433CrossRefGoogle Scholar
  41. Hertel H (1980) Chromatic properties of identified interneurons in the optic lobes of the bee. J Comp Physiol A 137(3):215–231CrossRefGoogle Scholar
  42. Hertel H, Maronde U (1987) The physiology and morphology of centrally projecting visual interneurones in the honeybee brain. J Exp Biol 133(1):301–315Google Scholar
  43. Judd DB, MacAdam DL, Wyszecki G, Budde H, Condit H, Henderson S, Simonds J (1964) Spectral distribution of typical daylight as a function of correlated color temperature. J Opt Soc Am 54(8):1031–1040CrossRefGoogle Scholar
  44. Kelber A, Vorobyev M, Osorio D (2003) Animal colour vision—behavioural tests and physiological concepts. Biol Rev 78(1):81–118CrossRefPubMedGoogle Scholar
  45. Kemp DJ, Herberstein ME, Fleishman LJ, Endler JA, Bennett AT, Dyer AG, Hart NS, Marshall J, Whiting MJ (2015) An integrative framework for the appraisal of coloration in nature. Am Nat 185(6):705–724CrossRefPubMedGoogle Scholar
  46. Kien J, Menzel R (1977a) Chromatic properties of interneurons in theoptic lobes of the bee. I. Broad band neurons. J Comp Physiol A 113(1):17–34CrossRefGoogle Scholar
  47. Kien J, Menzel R (1977b) Chromatic properties of interneurons in theoptic lobes of the bee. II. Narrow band and colour opponent neurons. J Comp Physiol A 113(1):35–53CrossRefGoogle Scholar
  48. Klein A, Vaissiere BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc Lond B Biol 274(1608):303–313CrossRefGoogle Scholar
  49. Land M, Chittka L (2013) Vision. In: Simpson SJ, Douglas AE (eds) The insects: structure and Function. Cambridge University Press, Cambridge, pp 708–737Google Scholar
  50. Lunau K, Papiorek S, Eltz T, Sazima M (2011) Avoidance of achromatic colours by bees provides a private niche for hummingbirds. J Exp Biol 214(9):1607–1612CrossRefPubMedGoogle Scholar
  51. Menzel R (1967) Untersuchungen zum Erlernen von Spektralfarben durch die Honigbiene (Apis mellifica). Z Vergl Physiol 56(1):22–62CrossRefGoogle Scholar
  52. Menzel R, Backhaus W (1991) Color vision in insects. In: Gouras P (ed) The perception of color. CRC press, Boca Raton, pp 262–293Google Scholar
  53. Mollon J, Jordan G (1997) On the nature of unique hues. In: Dickinson C, Murray I, Carden D (eds) John Dalton’s colour vision legacy: selected proceedings of the international conference. Taylor & Francis, Boca Raton, pp 381–392Google Scholar
  54. Morawetz L, Spaethe J (2012) Visual attention in a complex search task differs between honeybees and bumblebees. J Exp Biol 215(14):2515–2523CrossRefPubMedGoogle Scholar
  55. Morawetz L, Svoboda A, Spaethe J, Dyer AG (2013) Blue colour preference in honeybees distracts visual attention for learning closed shapes. J Comp Physiol A 19(10):817–827CrossRefGoogle Scholar
  56. Paulk AC, Dacks AM, Phillips-Portillo J, Fellous JM, Gronenberg W (2009) Visual processing in the central bee brain. J Neurosci 29(32):9987–9999CrossRefPubMedPubMedCentralGoogle Scholar
  57. Peitsch D, Fietz A, Hertel H, de Souza J, Ventura DF, Menzel R (1992) The spectral input systems of hymenopteran insects and their receptor-based colour vision. J Comp Physiol A 170(1):23–40CrossRefPubMedGoogle Scholar
  58. Pike TW (2012) Preserving perceptual distances in chromaticity diagrams. Behav Ecol 23(4):723–728CrossRefGoogle Scholar
  59. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25(6):345–353CrossRefPubMedGoogle Scholar
  60. Reser DH, Witharanage RW, Rosa MG, Dyer AG (2012) Honeybees (Apis mellifera) learn color discriminations via differential conditioning independent of long wavelength (green) photoreceptor modulation. PLoS One 7(11):e48,577CrossRefGoogle Scholar
  61. Rushton W (1972) Review lecture. Pigments and signals in colour vision. J Physiol 220(3):1–31CrossRefGoogle Scholar
  62. Schrödinger E (1920) Grundlinien einer Theorie der Farbenmetrik im Tagessehen. Ann Phys 368(22):481–520CrossRefGoogle Scholar
  63. Shrestha M, Dyer AG, Boyd-Gerny S, Wong BBM, Burd M (2013a) Shades of red: bird-pollinated flowers target the specific colour discrimination abilities of avian vision. New Phytol 198(1):301–310CrossRefPubMedGoogle Scholar
  64. Shrestha M, Dyer AG, Burd M (2013b) Evaluating the spectral discrimination capabilities of different pollinators and their effect on the evolution of flower colors. Commun Integr Biol 6(3):e24,000CrossRefGoogle Scholar
  65. Shrestha M, Dyer AG, Bhattarai P, Burd M (2014) Flower colour and phylogeny along an altitudinal gradient in the Himalayas of Nepal. J Ecol 102(1):126–135CrossRefGoogle Scholar
  66. Shrestha M, Lunau K, Dorin A, Schulze B, Bischoff M, Burd M, Dyer AG (2016) Floral colours in a world without birds and bees: the plants of macquarie island. Plant Biol. doi: 10.1111/plb.12456 Google Scholar
  67. Spaethe J, Tautz J, Chittka L (2001) Visual constraints in foraging bumblebees: flower size and color affect search time and flight behavior. P Natl Acad Sci USA 98(2):3898–3903CrossRefGoogle Scholar
  68. Stevens SS (1957) On the psychophysical law. Psychol Rev 64(3):153CrossRefPubMedGoogle Scholar
  69. Stillman RA, Railsback SF, Giske J, Berger U, Grimm V (2015) Making predictions in a changing world: the benefits of individual-based ecology. BioScience 65(2):140–150CrossRefPubMedGoogle Scholar
  70. Stoughton CM, Conway BR (2008) Neural basis for unique hues. Curr Biol 18(16):R698–R699CrossRefPubMedGoogle Scholar
  71. Streinzer M, Paulus HF, Spaethe J (2009) Floral colour signal increases short-range detectability of a sexually deceptive orchid to its bee pollinator. J Exp Biol 212(9):1365–1370CrossRefPubMedGoogle Scholar
  72. Troscianko T, Benton CP, Lovell PG, Tolhurst DJ, Pizlo Z (2009) Camouflage and visual perception. Philos Trans R Soc B 364(1516):449–461CrossRefGoogle Scholar
  73. Valberg A (2001) Unique hues: an old problem for a new generation. Vis Res 41(13):1645–1657CrossRefPubMedGoogle Scholar
  74. van der Kooi CJ, Elzenga JT, Staal M, Stavenga DG (2016) How to colour a flower: on the optical principles of flower coloration. Proc Biol Sci. doi: 10.1098/rspb.2016.0429
  75. von Frisch K (1914) Der Farbensinn und Formensinn der Biene. Zool Jb Physiol 37:1–238Google Scholar
  76. von Helversen O (1972) Zur spektralen Unterschiedsempfindlichkeit der Honigbiene. J Comp Physiol A 80(4):439–472CrossRefGoogle Scholar
  77. Vorobyev M, Brandt R (1997) How do insect pollinators discriminate colors? Isr J Plant Sci 45(2–3):103–113CrossRefGoogle Scholar
  78. Vorobyev M, Brandt R, Peitsch D, Laughlin SB, Menzel R (2001) Colour thresholds and receptor noise: behaviour and physiology compared. Vis Res 41(5):639–653CrossRefPubMedGoogle Scholar
  79. Wertlen AM, Niggebrugge C, Vorobyev M, Hempel de Ibarra N (2008) Detection of patches of coloured discs by bees. J Exp Biol 211(13):2101–2104CrossRefPubMedGoogle Scholar
  80. Yang E, Lin H, Hung Y (2004) Patterns of chromatic information processing in the lobula of the honeybee, Apis mellifera L. J Insect Physiol 50(10):913–925CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Zoë Bukovac
    • 1
  • Alan Dorin
    • 1
  • Valerie Finke
    • 2
  • Mani Shrestha
    • 1
    • 3
  • Jair Garcia
    • 3
  • Aurore Avarguès-Weber
    • 4
    • 5
  • Martin Burd
    • 6
  • Jürgen Schramme
    • 2
  • Adrian Dyer
    • 3
    • 7
  1. 1.Faculty of Information TechnologyMonash UniversityMelbourneAustralia
  2. 2.Institut für ZoologieJohannes Gutenberg UniversitätMainzGermany
  3. 3.School of Media and CommunicationRMIT UniversityMelbourneAustralia
  4. 4.Centre de Recherches sur la Cognition Animale, Université Toulouse III (UPS)ToulouseFrance
  5. 5.Centre National de la Recherche Scientifique (CNRS)Centre de Recherches sur la Cognition AnimaleToulouseFrance
  6. 6.School of Biological SciencesMonash UniversityMelbourneAustralia
  7. 7.Department of PhysiologyMonash UniversityMelbourneAustralia

Personalised recommendations