Skip to main content
SpringerLink
Log in

Bees’ subtle colour preferences: how bees respond to small changes in pigment concentration

  • Original Paper
  • Published:
Naturwissenschaften Aims and scope Submit manuscript

Abstract

Variability in flower colour of animal-pollinated plants is common and caused, inter alia, by inter-individual differences in pigment concentrations. If and how pollinators, especially bees, respond to these small differences in pigment concentration is not known, but it is likely that flower colour variability impacts the choice behaviour of all flower visitors that exhibit innate and learned colour preferences. In behavioural experiments, we simulated varying pigment concentrations and studied its impact on the colour choices of bumblebees and honeybees. Individual bees were trained to artificial flowers having a specific concentration of a pigment, i.e. Acridine Orange or Aniline Blue, and then given the simultaneous choice between three test colours including the training colour, one colour of lower and one colour of higher pigment concentration. For each pigment, two set-ups were provided, covering the range of low to middle and the range of middle to high pigment concentrations. Despite the small bee-subjective perceptual contrasts between the tested stimuli and regardless of training towards medium concentrations, bees preferred neither the training stimuli nor the stimuli offering the highest pigment concentration but more often chose those stimuli offering the highest spectral purity and the highest chromatic contrast against the background. Overall, this study suggests that bees choose an intermediate pigment concentration due to its optimal conspicuousness. It is concluded that the spontaneous preferences of bees for flower colours of high spectral purity might exert selective pressure on the evolution of floral colours and of flower pigmentation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Armbruster WS, Antonsen L, Pélabon C (2005) Phenotypic selection on Dalechampia blossoms: honest signaling affects pollination success. Ecology 86:3323–3333. doi:10.1890/04-1873

    Article  Google Scholar 

  • Asmussen CB (1993) Pollination biology of the Sea Pea, Lathyrus japonicus: floral characters and activity and flight patterns of bumblebees. Flora 188:227–237

    Google Scholar 

  • 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:e15370. doi:10.1371/journal.pone.0015370

    Article  PubMed  Google Scholar 

  • Backhaus W (1992) The Bezold–Brücke effect in the color vision system of the honeybee. Vision Res 32:1425–1431

    Article  PubMed  CAS  Google Scholar 

  • Belsare PV, Sriram B, Watve MG (2009) The co-optimization of floral display and nectar reward. J Biosci 34:963–967. doi:10.1007/s12038-009-0110-7

    Article  PubMed  Google Scholar 

  • Benard J, Giurfa M (2008) The cognitive implications of asymmetric color generalization in honeybees. Anim Cogn 11:283–293

    Article  PubMed  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B Met 57:289–300

    Google Scholar 

  • Brandt R, Vorobyev M (1997) Metric analysis of threshold spectral sensitivity in the honeybee. Vision Res 37:425–439

    Google Scholar 

  • Schemske DW, Bradshaw HD Jr (1999) Pollinator preference and the evolution of floral traits in monkeyflowers (Mimulus). Proc Natl Acad Sci USA 96:11910–11915. doi:10.1073/pnas.96.21.11910

    Article  PubMed  CAS  Google Scholar 

  • Chittka L (1992) The colour hexagon: a chromaticity diagram based on photoreceptor excitations as a generalized representation of colour opponency. J Comp Physiol A 170:533–545

    Google Scholar 

  • Chittka L, Thomson JD, Waser NM (1999) Flower constancy, insect psychology, and plant evolution. Naturwissenschaften 86:361–377

    Article  CAS  Google Scholar 

  • Cittka L, Kevan PG (2005) Advertisement in flowers. In: Dafni A, Kevan PG, Husband BC (eds) Practical pollination biology. Enviroquest Ltd., Cambridge, pp 147–230

    Google Scholar 

  • Dobson HEM, Danielson EM, Wesep IDV (1999) Pollen odor chemicals as modulators of bumble bee foraging on Rosa rugosa Thunb. (Rosaceae). Plant Spec Biol 14:153–166

    Article  Google Scholar 

  • Dyer AG, Chittka L (2004a) Fine colour discrimination requires differential conditioning in bumblebees. Naturwissenschaften 91:224–227

    Article  PubMed  CAS  Google Scholar 

  • Dyer AG, Chittka L (2004b) 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

    Article  CAS  Google Scholar 

  • Dyer AG, Neumeyer C (2005) Simultaneous and successive colour discrimination in the honeybee (Apis mellifera). J Comp Physiol A 191:547–557

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Endler JA (1990) On the measurement and classification of colour in studies of animal colour patterns. Biol J Linn Soc 41:315–352. doi:10.1111/j.1095-8312.1990.tb00839.x

    Article  Google Scholar 

  • Exner F, Exner S (1910) Die physikalischen Grundlagen der Blütenfärbungen. Sitz der Akad Wiss Wien math naturw. Klasse 119(Abt 1):1–55

    Google Scholar 

  • Giurfa M, Núñez J, Chittka L, Menzel R (1995) Colour preferences of flower-naive honeybees. J Comp Physiol A 177:247–259

    Article  Google Scholar 

  • Giurfa M, Vorobyev M, Kevan P, Menzel R (1996) Detection of coloured stimuli by honeybees: minimum visual angles and receptor specific contrast. J Comp Physiol A 178:699–709

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Giurfa M, Vorobyev M (1998) The angular range of achromatic target detection by honey bees. J Comp Physiol A 183:101–110

    Article  Google Scholar 

  • Giurfa M (2004) Conditioning procedure and color discrimination in the honeybee Apis mellifera. Naturwissenschaften 91:228–231

    Article  PubMed  CAS  Google Scholar 

  • Goulson D, Cruise JL, Sparrow KR, Harris AJ, Park KJ, Tinsley MC, Gilburn AS (2007) Choosing rewarding flowers; perceptual limitations and innate preferences influence decision making in bumblebees and honeybees. Behav Ecol Sociobiol 61:1523–1529

    Article  Google Scholar 

  • Gumbert A (2000) Color choices by bumble bees (Bombus terrestris) innate preferences and generalization after learning. Behav Ecol Sociobiol 48:36–43

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Hill PSM, Wells PH, Wells H (1997) Spontaneous flower constancy and learning in honey bees as a function of colour. Anim Behav 54:615–627

    Article  PubMed  Google Scholar 

  • Kay QON, Daoud HS, Stirton CH (1981) Pigment distribution, light reflection and cell structure in petals. Bot J Linn Soc 83:57–83. doi:10.1111/j.1095-8339.1981.tb00129.x

    Article  CAS  Google Scholar 

  • Kevan PG, Giurfa M, Chittka L (1996) Why are there so many and so few white flowers? Trends Plant Sci 1:280–284

    Article  Google Scholar 

  • Kugler H (1936) Blütenökologische Untersuchungen mit Hummeln VIII. Planta 25:346–363

    Article  Google Scholar 

  • Laughlin SB (1981) Neural principles in the peripheral visual systems of invertebrates. In: Autrum H (ed) Vision in invertebrates (Handbook of sensory physiology). Springer, Berlin, pp 133–280

    Chapter  Google Scholar 

  • Lunau K (1990) Color saturation triggers innate reactions to flower signals—flower dummy experiments with bumblebees. J Comp Physiol A 166:827–834

    Article  Google Scholar 

  • Lunau K (1996) Unidirectionality of floral colour change. Plant Syst Evol 200:125–140

    Article  Google Scholar 

  • Lunau K, Wacht S, Chittka L (1996) Colour choices of naive bumble bees and their implications for colour perception. J Comp Physiol A 178:477–489

    Article  Google Scholar 

  • Lunau K, Papiorek S, Eltz T, Sazima M (2011) Avoidance of achromatic colours by bees provides a private niche for hummingbirds. J Exp Biol 214:1607–1612. doi:10.1242/jeb.052688

    Article  PubMed  Google Scholar 

  • Matsumura S, Yokoyama J, Tateishi Y, Maki M (2006) Intraspecific variation of flower colour and its distribution within a sea lavender, Limonium wrightii (Plumbaginaceae), in the northwestern Pacific Islands. J Plant Res 119:625–632

    Article  PubMed  Google Scholar 

  • Meléndez-Ackerman E, Campbell DR, Waser NM (1997) Hummingbird behavior and mechanisms of selection on flower color in Ipomopsis. Ecology 78:2532–2541. doi:10.1890/0012-9658(1997) 078

    Google Scholar 

  • Menzel R, Backhaus W (1991) Color vision in insects. In: Gouras P (ed) Vision and visual dysfunction. VI. Perception of color. Macmillan, Houndmills, pp 262–293

    Google Scholar 

  • 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 68:81–120. doi:10.1111/j.1469-185X.1993.tb00732.x

    Article  Google Scholar 

  • Neumeyer C (1981) Chromatic adaptation in the honeybee: successive color contrast and color constancy. J Comp Physiol 144:543–553

    Article  Google Scholar 

  • Noda K-I, Glover BJ, Linstead P, Martin C (1994) Flower colour intensity depends on specialized cell shape controlled by a Myb-related transcription factor. Nature 369:661–664. doi:10.1038/369661a0

    Article  PubMed  CAS  Google Scholar 

  • R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, http://www.R-project.org. ISBN 3-900051-07-0

    Google Scholar 

  • Raine NE, Ings TC, Dornhaus A, Saleh N, Chittka L (2006) Adaptation, genetic drift, pleiotropy, and history in the evolution of bee foraging behavior. Adv Stud Behav 36:305–354

    Article  Google Scholar 

  • Rohde K, Papiorek S, Lunau K (2013) Bumblebees (Bombus terrestris) and honeybees (Apis mellifera) prefer similar colours of higher spectral purity over trained colours. J Comp Physiol A 199:197–210. doi:10.1007/s00359-012-0783-5

    Article  Google Scholar 

  • Schaefer HM, Schaefer V, Levey DJ (2004) How plant-animal interactions signal new insights in communication. Trends Ecol Evol 19:577–584

    Article  Google Scholar 

  • Schaefer HM, Spitzer K, Bairlein F (2008) Long-term effects of previous experience determine nutrient discrimination abilities in birds. Front Zool 5:4. doi:10.1186/1742-9994-5-4

    Article  PubMed  Google Scholar 

  • Shipunov A, Kosenko Y, Volkova P (2011) Floral polymorphism in common primrose (Primula vulgaris Huds., Primulaceae) of the Northeastern Black Sea coast. Plant Syst Evol 296:167–178

    Article  Google Scholar 

  • Skorupski P, Döring TF, Chittka L (2007) Photoreceptor spectral sensitivity in island and mainland populations of the bumblebee, Bombus terrestris. J Comp Physiol A 193:485–494

    Article  Google Scholar 

  • Skorupski P, Chittka L (2010) Photoreceptor spectral sensitivity in the bumblebee, Bombus impatiens (Hymenoptera: Apidae). PLoS One 5:e12049. doi:10.1371/journal.pone.0012049

    Article  PubMed  Google Scholar 

  • Sprengel CK (1793) Das entdeckte Geheimnis der Natur im Bau und in der Befruchtung der Blumen. Fascimile-Druck. Mayer & Müller, Berlin

    Book  Google Scholar 

  • Tastard E, Andalo C, Giurfa M, Burrus M, Thébaud C (2008) Flower colour variation across a hybrid zone in Antirrhinum as perceived by bumblebee pollinators. Arthropod-Plant Inter 2:237–246. doi:10.1007/s11829-008-9046-3

    Article  Google Scholar 

  • Tourjee KR, Harding J, Byrne TG (1993) Calorimetric analysis of Gerbera flowers. HortSci 28:735–737

    Google Scholar 

  • Vogel S (1949) Farbwechsel und Zeichnungsmuster bei Blüten. Plant Syst Evol 97:44–100

    Google Scholar 

  • Vorobyev M, Osorio D (1998) Receptor noise as a determinant of colour thresholds. Proc R Soc Lond B 265:351–358. doi:10.1098/rspb.1998.0302

  • Vorobyev M, Brandt R, Peitsch D, Laughlin SB, Menzel R (2001) Colour thresholds and receptor noise: behaviour and physiology compared. Vision Res 41:639–653

    Article  PubMed  CAS  Google Scholar 

  • Weiss MR (1991) Floral color changes as cues for pollinators. Acta Hort 288:294–298

    Google Scholar 

  • Whibley AC, Langlade NB, Andalo C, Hanna AI, Bangham A, Thebaud C, Coen E (2006) Evolutionary paths underlying flower color variation in Antirrhinum. Science 313:963–966

    Article  PubMed  CAS  Google Scholar 

  • Wyszecki G, Stiles WS (1982) Color science: concepts and methods, quantitative data and formulae. Wiley, New York

    Google Scholar 

Download references

Acknowledgements

We thank Robert Junker for critical comments on the manuscript and statistical improvement, Ann Thorson for linguistic improvement and the E-Norm graduate school for funding.

Author information

Author notes

  1. Katja Rohde

    Present address: Department of Biogeography, Trier University, Universitätsring 15, 54286, Trier, Germany

Authors and Affiliations

  1. Department of Biology, Institute for Sensory Ecology, Heinrich-Heine University Düsseldorf, Universitätsstr. 1, 40225, Düsseldorf, Germany

    Sarah Papiorek, Katja Rohde & Klaus Lunau

Authors
  1. Sarah Papiorek
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Katja Rohde
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Klaus Lunau
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sarah Papiorek.

Additional information

Communicated by: Sven Thatje

Rights and permissions

Reprints and permissions

About this article

Cite this article

Papiorek, S., Rohde, K. & Lunau, K. Bees’ subtle colour preferences: how bees respond to small changes in pigment concentration. Naturwissenschaften 100, 633–643 (2013). https://doi.org/10.1007/s00114-013-1060-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00114-013-1060-3

Keywords

Search

Navigation