Advertisement

Journal of Comparative Physiology A

, Volume 171, Issue 2, pp 171–181 | Cite as

The evolutionary adaptation of flower colours and the insect pollinators' colour vision

  • Lars Chittka
  • Randolf Menzel
Article
Accepted:

Summary

The evolutionary tuning between floral colouration and the colour vision of flower-visiting Hymenoptera is quantified by evaluating the informational transfer from the signalling flower to the perceiving pollinator. The analysis of 180 spectral reflection spectra of angiosperm blossoms reveals that sharp steps occur precisely at those wavelengths where the pollinators are most sensitive to spectral differences. Straight-forward model calculations determine the optimal set of 3 spectral photoreceptor types for discrimination of floral colour signals on the basis of perceptual difference values. The results show good agreement with the sets of photoreceptors characterized electrophysiologically in 40 species of Hymenoptera.

Key words

Colour vision Flower colours Evolution Hymenoptera Pollination ecology 
This is a preview of subscription content, log in to check access.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Backhaus W (1991) Colour opponent coding in the visual system of the honeybee. Vision Res 31:1381–1397Google Scholar
  2. Backhaus W, Menzel R (1987) Color distance derived from a receptor model of color vision in the honeybee. Biol Cybern 55:321–331Google Scholar
  3. Backhaus W, Menzel R, Kreißl S (1987) Multidimensional scaling of color similarity in bees. Biol Cybern 56:293–304Google Scholar
  4. Burkhardt D (1983) Wavelength perception and color vision. In: Cosens DJ, Vince-Price D (eds) The biology of photoreception. Soc Exp Biol Symp 36:371–397Google Scholar
  5. Chittka L (1992) The colour hexagon: a chromaticity diagram based on photoreceptor excitations as a generalized representation of colour opponency. J Comp Physiol A 170:533–543Google Scholar
  6. Chittka L, Lunau K (1992) Colour coding and innate preferences for flower color patterns in bumblebees. In: Elsner N, Richter DW (ed) Rhythmogenesis in neurons and networks. Proc 20th Göttingen neurobiology conf 1992. Thieme, Stuttgart, p 298Google Scholar
  7. Chittka L, Beier W, Hertel H, Steinmann E, Menzel R (1992) Opponent colour coding is a universal strategy to evaluate the photoreceptor signals in Hymenoptera. J Comp Physiol A 170:545–563Google Scholar
  8. Clements FE, Long FL (1923) Experimental pollination: an outline of the ecology of flowers and insects. Carnegie Inst Wash Publ 336Google Scholar
  9. Darwin C (1876) On the effects of cross and self fertilization in the vegetable kingdom. Murray, LondonGoogle Scholar
  10. Daumer K (1956) Reizmetrische Untersuchungen des Farbensehens der Bienen. Z Vergl Physiol 38:413–478Google Scholar
  11. Dukas R, Real L (1991) Learning foraging tasks by bees: a comparison between social and solitary species. Anim Behav 42:269–276Google Scholar
  12. Dukas R, Shmida A (in press) Interactions of pollinating insects with flowers in a Mediterranean community. OecologiaGoogle Scholar
  13. Faegri K, van der Pijl L (1978) The principles of pollination ecology. Pergamon Press, OxfordGoogle Scholar
  14. Feinsinger P (1983) Co-evolution and pollination. In: Futuyma DJ, Slatkin M (eds) Co-evolution. Sinauer, Sunderland, Mass., pp 282–310Google Scholar
  15. Free JB (1963) The flower constancy of honeybees. J Anim Ecol 32:119–131Google Scholar
  16. Free JB (1966) The foraging behaviour of bees and its effect on the isolation and speciation of plants. In: Hawkes JG (ed) Reproductive biology and taxonomy of vascular plants. Pergamon, Oxford, pp 76–91Google Scholar
  17. Frisch K von (1914) Demonstration von Versuchen zum Nachweis des Farbensinnes bei angeblich total farbenblinden Tieren. Verh Dtsch Zool Ges in Freiburg. BerlinGoogle Scholar
  18. Frisch K von (1919) Über den Geruchssinn der Bienen und seine blütenbiologische Bedeutung. Zool Jb Physiol 37:1–238Google Scholar
  19. Frisch K von (1967) The dance language and orientation of bees. Cambridge: Harvard Univ PressGoogle Scholar
  20. Goldsmith TS (1991) The evolution of visual pigments and colour vision. In: Gouras P (ed) The perception of colour. London, MacMillan Press, pp 62–89Google Scholar
  21. Gottsberger G, Gottlieb OR (1980) Blue flowers and phylogeny. Revta Bras Bot 3:79–83Google Scholar
  22. Gottsberger G, Gottlieb OR (1981) Blue flower pigmentation and evolutionary advancement. Biochem Syst Ecol 9:13–18Google Scholar
  23. Grant V (1950) The flower constancy of bees. Bot Rev 16:379–398Google Scholar
  24. Gribakin FG (1988) Photoreceptor optics of the honeybee and its eye colour mutants: the effects of screening pigments on the long-wave subsystem of colour vision. J Comp Physiol A 164:123–140Google Scholar
  25. Heinrich B (1979) “Majoring” and “minoring” by foraging bumblebees, Bombus vagans: an experimental analysis. Ecology 60:245–255Google Scholar
  26. Helversen O von (1972) Zur spektralen Unterschiedlichkeitsempfindlichkeit der Honigbiene. J Comp Physiol 80:439–472Google Scholar
  27. Kamil AC, Roitblat HL (1985) The ecology of foraging behavior: implications for animal learning and memory. Annu Rev Psychol 36:141–169Google Scholar
  28. Kevan PG (1978) In: Richards AJ (ed) The pollination of flowers by insects. Linnean Soc Sympos Series 51Google Scholar
  29. Kevan PG, Baker HG (1983) Insects as flower visitors and pollinators. Annu Rev Entomol 28:407–453Google Scholar
  30. Koehler DL, Davenport D (1983) Ultraviolet mimicry by Bulbophyllum lepidum? Am Orchid Soc Bul 52:359–363Google Scholar
  31. Kries J von (1905) Die Gesichtsempfindungen. In: Nagel W (ed) Handbuch der Physiologie des Menschen, Vol. 3. Braunschweig, Vieweg, pp 109–282Google Scholar
  32. Laughlin SB (1981) Neural principles in the peripheral visual system of invertebrates. In: Autrum HJ (ed) Invertebrate visual centers and behaviour 1 (Handbook of sensory physiology, Vol VII/6B) Springer, Berlin Heidelberg New York, pp 133–280Google Scholar
  33. Lipetz LE (1971) The relation of physiological and psychological aspects of sensory intensity. In: Loewenstein WR (ed) Principles of receptor physiology (Handbook of sensory physiology, vol I) Springer, Berlin Heidelberg New York, pp 191–225Google Scholar
  34. Lythgoe JN (1972) The adaptation of visual pigments to the photic environment. In: Dartnall HJ (ed) Photochemistry of vision (Handbook of sensory physiology, vol VII/1). Springer, Berlin Heidelberg New York, pp 567–624Google Scholar
  35. Lythgoe JN (1979) The ecology of vision. Oxford, Clarendon PressGoogle Scholar
  36. Lythgoe JN, Partridge JC (1989) Visual pigments and the acquisition of visual information. J Exp Biol 146:1–20Google Scholar
  37. Maximov VV (1988) An approximation of visual absorption spectra. Sensory systems (Sensornye systemy) 2:3–8Google Scholar
  38. Mazokhin-Porshniakov GA (1962) Farbmetrischer Beweis der Trichromasie des Farbensehens der Bienen (am Beispiel der Hummeln). Akad Nauk USSR Biofizika 7:221–227Google Scholar
  39. Menzel R (1967) Untersuchungen zum Erlernen von Spektralfarben durch die Honigbiene, Apis mellifica. Z Vergl Physiol 56:22–62Google Scholar
  40. Menzel R (1979) Spectral sensitivity and colour vision in invertebrates. In: Autrum H (ed) Invertebrate photoreceptors (Handbook of sensory physiology, vol. VII/6A). Springer, Berlin Heidelberg New York, pp 503–580Google Scholar
  41. Menzel R (1985) Learning in honeybees in an ecological and behavioural context. In: Hölldobler B, Lindauer M (eds) Experimental behavioural ecology. G Fischer, Stuttgart, pp 55–74Google Scholar
  42. Menzel R, Backhaus W (1991) Color vision in insects. In: Gouras P (ed) Vision and visual dysfunction, vol. VI. The perception of colour. Houndsmills: MacMillan Press, pp 262–293Google Scholar
  43. Menzel R, Shmida A (in press) The ecology of flower colours and the natural colour vision of insect pollinators. The Israeli flora as study case. Biol RevGoogle Scholar
  44. Menzel R, Ventura DF, Hertel H, de Souza J, Greggers U (1986) Spectral sensitivity of photoreceptors in insect compound eyes: comparison of species and methods. J Comp Physiol A 158:165–177Google Scholar
  45. Nilsson LA (1983) Mimesis of bellflower (Campanula) by the red helleborine orchid Cephalanthera rubra. Nature 305:799–800Google Scholar
  46. 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 170:23–40Google Scholar
  47. Plateau F (1901) Observacion sur le phénomène de la constance chez quelques hyménoptères. Ann Soc Entomol Belg 45:56–83Google Scholar
  48. Proctor M (1973) The pollination of flowers. Collins, LondonGoogle Scholar
  49. Pyke GH, Pulliam HR and Charnov EL (1977) Optimal foraging: A selective review of theory and tests. Q Rev Biol 52:137–154Google Scholar
  50. Rathke B (1983) Competition and facilitation among plants for pollination. In: Real LA (ed) Pollination biology. Academic Press, New York, pp 375–393Google Scholar
  51. Selten R, Shmida A (1988) Pollinator foraging and flower competition in a game equilibrium model. Game Theory Behav Sci 18:3–67Google Scholar
  52. Snyder AW, Menzel R, Laughlin SB (1973) Structure and function of the fused rhabdom. J Comp Physiol 87:99–135Google Scholar
  53. Sprengel CK (1793) Das entdeckte Geheimnis der Natur in Bau und Befruchtung der Blumen. Reprint: Verlag J. Cramer, Lehre 1972Google Scholar
  54. Stavenga DG (1989) Pigments in compound eyes. In: Stavenga DG, Hardie RC (eds) Facets of vision. Springer, Berlin Heidelberg New York, pp 152–172Google Scholar
  55. Stavenga DG, Schwemer J (1984) Visual pigments of invertebrates. In: Ali MA (ed) Photoreception and vision in invertebrates. Plenum, New York, pp 11–61Google Scholar
  56. Stephens WS, Krebs JR (1986) Foraging theory. Princeton University PressGoogle Scholar
  57. Waser NM (1983) The adaptive nature of floral traits: ideas and evidence. In: Real LA (ed) Pollination biology. Academic Press, New York, pp 241–285Google Scholar
  58. Waser NM (1986) Flower constancy: definition, cause, and measurement. Am Nat 127:593–603Google Scholar

Copyright information

© Springer-Verlag 1992

Authors and Affiliations

  • Lars Chittka
    • 1
  • Randolf Menzel
    • 1
  1. 1.Institut für Neurobiologie, Freie Universität BerlinBerlinGermany

Personalised recommendations

Cite article

Buy options