Abstract
Flowers are often viewed by bee pollinators against a variety of different backgrounds. On the Australian continent, backgrounds are very diverse and include surface examples of all major geological stages of the Earth’s history, which have been present during the entire evolutionary period of Angiosperms. Flower signals in Australia are also representative of typical worldwide evolutionary spectral adaptations that enable successful pollination. We measured the spectral properties of 581 natural surfaces, including rocks, sand, green leaves, and dry plant materials, sampled from tropical Cairns through to the southern tip of mainland Australia. We modelled in a hexagon colour space, how interactions between background spectra and flower-like colour stimuli affect reliable discrimination and detection in bee pollinators. We calculated the extent to which a given locus would be conflated with the loci of a different flower-colour stimulus using empirically determined colour discrimination regions for bee vision. Our results reveal that whilst colour signals are robust in homogeneous background viewing conditions, there could be significant pressure on plant flowers to evolve saliently-different colours to overcome background spectral noise. We thus show that perceptual noise has a large influence on how colour information can be used in natural conditions.
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References
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):449–461
Avarguès-Weber A, d’Amaro D, Metzler M, Dyer AG (2014) Conceptualization of relative size by honeybees. Front Behav Neurosci 8:80
Backhaus W (1991) Color opponent coding in the visual system of the honeybee. Vis Res 31(7):1381–1397
Barth FG (1985) Insects and flowers. Princeton University Press, Princeton, New Jersey, USA, The biology of a partnership
Briscoe AD, Chittka L (2001) The evolution of colour vision in insects. Ann Rev Entomol 46(1):471–510
Brito VL, Weynans K, Sazima M, Lunau K (2015) Trees as huge flowers and flowers as oversized floral guides: the role of floral color change and retention of old flowers in tibouchina pulchra. Front Plant Sci 6:362
Bukovac Z, Dorin A, Finke V, Shrestha M, Garcia J, Avarguès-Weber A, Burd M, Schramme J, Dyer AG (2016) Assessing the ecological significance of bee visual detection and colour discrimination on the evolution of flower colours. Evolutionary Ecology pp 1–20
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):533–543
Chittka L (1996) Does bee colour vision predate the evolution of flower colour? Naturwissenschaften 83:136–138
Chittka L, Menzel R (1992) The evolutionary adaptation of flower colours and the insect pollinators’ colour vision. J Comp Physiol A 171(2):171–181
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):1489–1508
Chittka L, Thomson JD, Waser NM (1999) Flower constancy, insect psychology, and plant evolution. Naturwissenschaften 86(8):361–377
Chittka L, Spaethe J, Schmidt A, Hickelsberger A (2001) Adaptation, constraint, and chance in the evolution of flower color and pollinator color vision. In: Chittka L, Thompson JD (eds) Cognitive ecology of pollination. Cambridge University Press, Cambridge, UK, pp 106–126
Dollin A (2010) Introduction to Australian native bees. Native bees of Australia series, Booklet 1, 1-14, North Richmond, Australia
Dollin A, Batley M, Robinson M, Faulkner B (2000) Native bees of the Sydney region: a field guide. Australian Native Bee Research Centre, Richmond
Dyer AG (1998) The colour of flowers in spectrally variable illumination and insect pollinator vision. J Comp Physiol A 183(2):203–212
Dyer AG (1999) Broad spectral sensitivities in the honeybee’s photoreceptors limit colour constancy. J Comp Physiol A 185:445–453
Dyer AG (2006) Discrimination of flower colours in natural settings by the bumblebee species Bombus terrestris (Hymenoptera: Apidae). Entomol Generalis 28(4):257–268
Dyer AG, Arikawa K (2014) A hundred years of color studies in insects: with thanks to Karl von Frisch and the workers he inspired. J Comp Physiol A 200(6):409
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(2):105–114
Dyer AG, Garcia JE (2014) Color difference and memory recall in free-flying honeybees: forget the hard problem. Insects 5:629–638
Dyer AG, Neumeyer C (2005) Simultaneous and successive colour discrimination in the honeybee ( Apis mellifera). J Comp Physiol A 191(6):547–557
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):45–55
Dyer AG, Spaethe J, Prack S (2008) Comparative psychophysics of bumblebee and honeybee colour discrimination and object detection. J Comp Physiol A 194(7):617–627
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 Sci 279(1742):3606–3615
Dyer AG, Dorin A, Reinhardt V, Garcia JE, Rosa MGP (2014) Bee reverse-learning behavior and intra-colony differences: simulations based on behavioral experiments reveal benefits of diversity. Ecol Model 277:119–131
Dyer AG, Streinzer M, Garcia J (2016) Flower detection and acuity of the australian native stingless bee Tetragonula carbonaria sm. J Comp Physiol A 1–11
Forrest J, Thomson JD (2009) Background complexity affects colour preference in bumblebees. Naturwissenschaften 96(8):921–925
Garcia JE, Dyer AG, Greentree AD, Spring G, Wilksch PA (2013) Linearisation of rgb camera responses for quantitative image analysis of visible and uv photography: a comparison of two techniques. PLOS One 8(11):e79,534
Giurfa M (1991) Colour generalization and choice behaviour of the honeybee Apis mellifera ligustica. J Insect Physiol 37(1):41–44
Giurfa M, Núñez J, Chittka L, Menzel R (1995) Colour preferences of flower-naive honeybees. J Comp Physiol A 177:247–259
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):699–709
Gumbert A (2000) Color choices by bumble bees ( Bombus terrestris): innate preferences and generalization after learning. Behav Ecol Sociobiol 48(1):36–43
Heard T (2016) The Australian Native Bee Book. Sugarbag Bees, Brisbane
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):411–433
Howard SR, Avarguès-Weber A, Garcia J, Dyer AG (2017) Free-flying honeybees extrapolate relational size rules to sort successively visited artificial flowers in a realistic foraging situation. Anim Cogn. doi:10.1007/s10071-017-1086-6
Hurvich LM (1981) Color vision. Sinauer Associates. Inc., Sunderland
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(3):215–224
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(7):503–512
Jarvis RA (1973) On the identification of the convex hull of a finite set of points in the plane. Inform Proc Lett 2(1):18–21
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):705–724
Kevan PG, Chittka L, Dyer AG (2001) Limits to the salience of ultraviolet: lessons from colour vision in bees and birds. J Exp Biol 204:2571–2580
Koethe S, Bossems J, Dyer AG, Lunau K (2016) Colour is more than hue: preferences for compiled colour traits in the stingless bees Melipona mondury and M. quadrifasciata. J Comp Physiol A 202(9):615–627
Kudo G, Ishii HS, Hirabayashi Y, Ida TY (2007) A test of the effect of floral color change on pollination effectiveness using artificial inflorescences visited by bumblebees. Oecologia 154(1):119–128
Laughlin SB (1989) The role of sensory adaptation in the retina. J Exp Biol 146(1):39–62
Lee HC (2005) Introduction to color imaging science. Cambridge University Press, Cambridge
Lehrer M, Bischof S (1995) Detection of model flowers by honeybees: the role of chromatic and achromatic contrast. Naturwissenschaften 82(3):145–147
Leonard AS, Masek P (2014) Multisensory integration of colors and scents: insights from bees and flowers. J Comp Physiol A 200(6):463–474
Leonard AS, Dornhaus A, Papaj DR (2011) Flowers help bees cope with uncertainty: signal detection and the function of floral complexity. J Exp Biol 214(1):113–121
Levin DA, Anderson WW (1970) Competition for pollinators between simultaneously flowering species. Am Nat 104:455–467
Lind O (2016) Colour vision and background adaptation in a passerine bird, the zebra finch (Taeniopygia guttata). R Soc Open Sci 3(9):160383
Lotto RB, Chittka L (2005) Seeing the light: illumination as a contextual cue to color choice behavior in bumblebees. Proc Natl Acad Sci USA 102(10):3852–3856
Lunau K, Wacht S, Chittka L (1996) Colour choices of naive bumble bees and their implications for colour perception. J Comp Physiol A 178(4):477–489
Maloney L, Yang JN (2003) The illuminant estimation hypothesis and surface colour perception. In: Mausfeld R, Heyer D (eds) Colour perception: Mind and the physical world. Oxford University Press, Oxford, pp 335–358
Maloney LT (2002) Illuminant estimation as cue combination. J Vis 2(6):6–6
Menzel R (1967) Untersuchungen zum Erlernen von Spektralfarben durch die Honigbiene ( Apis mellifica). Zeitschrift für vergleichende Physiologie 56(1):22–62
Menzel R, Shmida A (1993) The ecology of flower colours and the natural colour vision of insect pollinators: the Israeli flora as a study case. Biol Rev 68(1):81–120
Michener CD (2007) The bees of the world, 2nd edn. Johns Hopkins, Baltimore
Morawetz L, Spaethe J (2012) Visual attention in a complex search task differs between honeybees and bumblebees. J Exp Biol 215(14):2515–2523
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 199(10):817–827
Naka K, Rushton W (1966) S-potentials from colour units in the retina of fish (cyprinidae). J Physiol 185(3):536
Ne’eman G, Kevan PG (2001) The effect of shape parameters on maximal detection distance of model targets by honeybee workers. J Comp Physiol A 187(8):653–660
Ne’eman G, Ne’eman R (2016) Factors determining visual detection distance to real flowers by bumble bees. J Pollinat Ecol 20(1):1–12
Neumeyer C (1980) Simultaneous color contrast in the honeybee. J Comp Physiol A 139(3):165–176
Neumeyer C (1981) Chromatic adaptation in the honeybee: successive color contrast and color constancy. J Comp Physiol A 144(4):543–553
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):23–40
Rathcke B (1988) Flowering phenologies in a shrub community: Competition and constraints. J Ecol 76:975–994
Renoult JP, Kelber A, Schaefer HM (2015) Colour spaces in ecology and evolutionary biology. Biol Rev Camb Philos Soc 92(1):292–315
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):301–310
Shrestha M, Dyer AG, Burd M (2013b) Evaluating the spectral discrimination capabilities of different pollinators and their effect on the evolution of flower colors. Comm Integr Biol 6(3):e24,000
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):126–135
Sommerlandt FM, Spaethe J, Rössler W, Dyer AG (2016) Does fine color discrimination learning in free-flying honeybees change mushroom-body calyx neuroarchitecture? PLoS One 11(10):e0164386
Spaethe J, Tautz J, Chittka L (2001) Visual constraints in foraging bumblebees: flower size and color affect search time and flight behavior. Proc Natl Acad Sci USA 98(2):3898–3903
Spaethe J, Streinzer M, Eckert J, May S, Dyer A (2014) Behavioural evidence of colour vision in free flying stingless bees. J Comp Physiol A 200(6):485–496
Stavenga DG, Smits RP, Hoenders BJ (1993) Simple exponential functions describing the absorbance bands of visual pigment spectra. Vis Res 33(8):1011–1017
Taylor G (1994) Landscapes of australia: their nature and evolution. In: Hill R (ed) History of the Australian vegetation: Cretaceous to recent. Cambridge University Press, Cambridge, pp 60–79
Telles FJ, Rodríguez-Gironés MA (2015) Insect vision models under scrutiny: what bumblebees (Bombus terrestris L.) can still tell us. The Science of. Nature 102(1–2):1–13
van der Kooi CJ (2016) Plant biology: flower orientation, temperature regulation and pollinator attraction. Curr Biol 26(21):R1143–R1145
von Helversen O (1972) Zur spektralen Unterschiedsempfindlichkeit der Honigbiene. J Comp Physiol A 80(4):439–472
Vorobyev M, Menzel R (1999) Flower advertisement for insects: Bees, a case study. In: Archer SN, Djamgoz MBA, Loew ER, Partridge JC, Vallerga S (eds) Adaptive Mechanisms in the Ecology of Vision. Springer, Netherlands, Dordrecht, pp 537–553
Vorobyev M, Osorio D (1998) Receptor noise as a determinant of colour thresholds. Proc R Soc Lond B: Biol Sci 265(1394):351–358
Waser NM (1986) Flower constancy: definition, cause, and measurement. Am Nat 127(5):593–603
Waser NM, Chittka L, Price MV, Williams NM, Ollerton J (1996) Generalization in pollination systems, and why it matters. Ecology 77:1043–1060
Wertlen AM, Niggebrugge C, Vorobyev M, Hempel de Ibarra N (2008) Detection of patches of coloured discs by bees. J Exp Biol 211(13):2101–2104
Wyszecki G, Stiles WS (1982) Color science: concepts and methods, quantitative data and formulae, vol 8. Wiley, New York
Acknowledgements
We thank Elinya Dyer for assistance in collecting rocks and measuring spectra, as well as discussions about the project. We thank Chris Monteith for comments and discussions of the study design and mathematical style. MS thanks the School of Media and Communications RMIT for a postdoctoral fellowship to facilitate research. AGD thanks the ARC for QEII fellowship (project number DP0878968) to conduct the initial phases of the research. This research was supported under Australian Research Council’s Discovery Projects funding scheme (Project Numbers DP130100015, DP160100161).
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Bukovac, Z., Shrestha, M., Garcia, J.E. et al. Why background colour matters to bees and flowers. J Comp Physiol A 203, 369–380 (2017). https://doi.org/10.1007/s00359-017-1175-7
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DOI: https://doi.org/10.1007/s00359-017-1175-7