Skip to main content
Log in

Insect vision models under scrutiny: what bumblebees (Bombus terrestris terrestris L.) can still tell us

  • Original Paper
  • Published:
The Science of Nature Aims and scope Submit manuscript

Abstract

Three contending models address the ability of bees to detect and discriminate colours: the colour opponent coding (COC) model, the colour hexagon (CH) model and the receptor noise-limited (RN) model, but few studies attempt to determine which model fits experimental data best. To assess whether the models provide an accurate description of bumblebee colour space, we trained bees to discriminate four colour pairs. The perceptual distance between the colours of each pair was similar according to the CH model but varied widely according to the COC and RN models. The time that bees required to select a flower and the proportion of correct choices differed between groups: decision times decreased as achromatic contrast increased, and the proportion of correct choices increased with achromatic contrast and perceptual distance, as predicted by the COC and RN models. These results suggest that both chromatic and achromatic contrasts affected the discriminability of colour pairs. Since flower colour affects the foraging choices of bees and foraging choices affect the reproductive success of plants, a better understanding of which model is more accurate under each circumstance is required to predict bee behaviour and the ecological implications of flower choice and colour.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Akaike H (1973) Information theory and an extension of the maximum likelihood principle. In: Petrov BN, Csaki F (eds) Proc. Second Int. Symp. Inf. Theory. Akademiai Kiado, Budapest, pp 267–281

  • Arnold SEJ, Chittka L (2012) Illumination preference, illumination constancy and colour discrimination by bumblebees in an environment with patchy light. J Exp Biol 215:2173–2180. doi:10.1242/jeb.065565

    Article  PubMed  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 Central  PubMed  Google Scholar 

  • Backhaus W (1991) Color opponent coding in the visual system of the honeybee. Vis Res 31:1381–1397

    Article  CAS  PubMed  Google Scholar 

  • Backhaus W, Menzel R, Kreißl S (1987) Multidimensional scaling of color similarity in bees. Biol Cybern 56:293–304. doi:10.1007/BF00319510

    Article  Google Scholar 

  • Benard J, Giurfa M (2008) The cognitive implications of asymmetric color generalization in honeybees. Anim Cogn 11:283–293. doi:10.1007/s10071-007-0112-5

    Article  PubMed  Google Scholar 

  • Bobeth H (1979) Dressurversuche zum Farbensehen der Bienen: Die Sättigung von Spektralfarben. 67

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

    Article  CAS  PubMed  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd ed. 488

  • Chittka L (1996) Optimal sets of color receptors and color opponent systems for coding of natural objects in insect vision. J Theor Biol 181:179–196. doi:10.1006/jtbi.1996.0124

    Article  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 170:533–543. doi:10.1007/BF00199331

    Google Scholar 

  • Chittka L, Beier W, Hertel H et al (1992) Opponent colour coding is a universal strategy to evaluate the photoreceptor inputs in Hymenoptera. J Comp Physiol A 170:545–563

    CAS  PubMed  Google Scholar 

  • Chittka L, Dyer AG, Block F, Dornhaus A (2003) Bees trade off foraging speed accuracy. Nature 424:388

    Article  CAS  PubMed  Google Scholar 

  • Chittka L, Kevan PG (2005) Flower colour as advertisement. In: Dafni A, Kevan PG, Husband BC (eds) Pract. Pollinat. Biol. Enviroquest Ltd., Cambridge, Ontario, Canada, pp 157–196

  • Chittka L, Spaethe J (2007) Visual search and the importance of time in complex decision making by bees. Arthropod Plant Interact 1:37–44. doi:10.1007/s11829-007-9001-8

    Article  Google Scholar 

  • 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, Thomson JD (eds) Cogn. Ecol. Pollinat. Cambridge University Press, Cambridge, pp 106–126

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

    Article  CAS  Google Scholar 

  • Chittka L, Waser NM (1997) Why red flowers are not invisible to bees. Isr J Plant Sci 45:169–183

    Article  Google Scholar 

  • Dyer AG, Chittka L (2004a) Fine colour discrimination requires differential conditioning in bumblebees. Naturwissenschaften 91:224–227. doi:10.1007/s00114-004-0508-x

    Article  CAS  PubMed  Google Scholar 

  • Dyer AG, Chittka L (2004b) Bumblebees (Bombus terrestris) sacrifice foraging speed to solve difficult colour discrimination tasks. J Comp Physiol A 190:759–763. doi:10.1007/s00359-004-0547-y

    Google Scholar 

  • Dyer AG, Chittka L (2004c) 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. doi:10.1007/s00359-003-0475-2

    Article  CAS  Google Scholar 

  • Dyer AG, Griffiths DW (2012) Seeing near and seeing far; behavioural evidence for dual mechanisms of pattern vision in the honeybee (Apis mellifera). J Exp Biol 215:397–404. doi:10.1242/jeb.060954

    Article  PubMed  Google Scholar 

  • Dyer AG, Neumeyer C (2005) Simultaneous and successive colour discrimination in the honeybee (Apis mellifera). J Comp Physiol A 191:547–557. doi:10.1007/s00359-005-0622-z

    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. doi:10.1007/s00359-008-0335-1

    Article  Google Scholar 

  • Forrest J, Thomson JD (2009) Background complexity affects colour preference in bumblebees. Naturwissenschaften 96:921–925. doi:10.1007/s00114-009-0549-2

    Article  CAS  PubMed  Google Scholar 

  • Giurfa M (2004) Conditioning procedure and color discrimination in the honeybee Apis mellifera. Naturwissenschaften 91:228–231. doi:10.1007/s00114-004-0530-z

    Article  CAS  PubMed  Google Scholar 

  • Giurfa M, Núñez J, Chittka L, Menzel R (1995) Colour preferences of flower-naive honeybees. J Comp Physiol A 177:247–259. doi:10.1007/BF00192415

    Article  Google Scholar 

  • Giurfa M, Sandoz J-C (2012) Invertebrate learning and memory: fifty years of olfactory conditioning of the proboscis extension response in honeybees. Learn Mem 19:54–66. doi:10.1101/lm.024711.111

    Article  PubMed  Google Scholar 

  • Giurfa M, Vorobyev M (1998) The angular range of achromatic target detection by honey bees. J Comp Physiol A 183:101–110. doi:10.1007/s003590050238

    Article  Google Scholar 

  • Giurfa M, Vorobyev M (1997) Detection and recognition of color stimuli by Honeybees: performance and mechanisms. Isr J Plant Sci 45:129–140. doi:10.1080/07929978.1997.10676679

    Article  Google Scholar 

  • Giurfa M, Vorobyev M, Brandt R et al (1997) Discrimination of coloured stimuli by honeybees: alternative use of achromatic and chromatic signals. J Comp Physiol A 180:235–243. doi:10.1007/s003590050044

    Article  Google Scholar 

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

    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 

  • von Helversen O (1972) Zur spektralen Unterschiedsempfindlichkeit der Honigbiene. J Comp Physiol 80:439–472. doi:10.1007/BF00696438

    Article  Google Scholar 

  • 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. doi:10.1006/anbe.2003.2269

    Article  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. doi:10.1007/s00359-002-0322-x

    Article  CAS  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. doi:10.1007/s003590100192

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Hempel de Ibarra N, Vorobyev M, Menzel R (2014) Mechanisms, functions and ecology of colour vision in the honeybee. J Comp Physiol A 200:411–433. doi:10.1007/s00359-014-0915-1

    Article  CAS  Google Scholar 

  • Inouye DW (1980) The terminology of floral larceny. Ecology 61:1251–1253

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Lehrer M, Bischof S (1995) Detection of model flowers by honeybees: the role of chromatic and achromatic contrast. Naturwissenschaften 82:145–147

    Article  CAS  Google Scholar 

  • Lotto RB, Chittka L (2005) Seeing the light: illumination as a contextual cue to color choice behavior in bumblebees. Proc Natl Acad Sci U S A 102:3852–3856. doi:10.1073/pnas.0500681102

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Lunau K (1993) Interspecific diversity and uniformity of flower colour patterns as cues for learned discrimination and innate detection of flowers. Experientia 49:1002–1010

    Article  Google Scholar 

  • Lunau K, Fieselmann G, Heuschen B, van de Loo A (2006) Visual targeting of components of floral colour patterns in flower-naïve bumblebees (Bombus terrestris; Apidae). Naturwissenschaften 93:325–328. doi:10.1007/s00114-006-0105-2

    Article  CAS  PubMed  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 

  • Macuda T, Gegear RJ, Laverty TM, Timney B (2001) Behavioural assessment of visual acuity in bumblebees (Bombus impatiens). J Exp Biol 204:559–564

    CAS  PubMed  Google Scholar 

  • Martínez-Harms J, Márquez N, Menzel R, Vorobyev M (2014) Visual generalization in honeybees: evidence of peak shift in color discrimination. J Comp Physiol A 200:317–325. doi:10.1007/s00359-014-0887-1

    Article  Google Scholar 

  • Martínez-Harms J, Palacios a G, Márquez N et al (2010) Can red flowers be conspicuous to bees? Bombus dahlbomii and South American temperate forest flowers as a case in point. J Exp Biol 213:564–571. doi:10.1242/jeb.037622

    Article  PubMed  Google Scholar 

  • Morawetz L, Spaethe J (2012) Visual attention in a complex search task differs between honeybees and bumblebees. J Exp Biol 215:2515–2523. doi:10.1242/jeb.066399

    Article  PubMed  Google Scholar 

  • Mota T, Gronenberg W, Giurfa M, Sandoz J-C (2013) Chromatic processing in the anterior optic tubercle of the honey bee brain. J Neurosci 33:4–16. doi:10.1523/JNEUROSCI. 1412-12.2013

    Article  CAS  PubMed  Google Scholar 

  • Moya-Laraño J, Corcobado G (2008) Plotting partial correlation and regression in ecological studies. Web Ecol 8:35–46. doi:10.5194/we-8-35-2008

    Article  Google Scholar 

  • Naka KI, Rushton WAH (1966a) S-potentials from color units in the retina of the fish (Cyprinidae). J Physiol 185:536–555

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Naka KI, Rushton WAH (1966b) S-potentials from luminosity units in the retina of the fish (Cyprinidae). J Physiol 185:587–599

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Niggebrügge C, Hempel de Ibarra N (2003) Colour-dependent target detection by bees. J Comp Physiol A 189:915–918. doi:10.1007/s00359-003-0466-3

    Article  Google Scholar 

  • Niggebrügge C, Leboulle G, Menzel R et al (2009) Fast learning but coarse discrimination of colours in restrained honeybees. J Exp Biol 212:1344–1350. doi:10.1242/jeb.021881

    Article  PubMed  Google Scholar 

  • Nityananda V, Pattrick JG (2013) Bumblebee visual search for multiple learned target types. J Exp Biol 216:4154–4160. doi:10.1242/jeb.085456

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Paulk AC, Gronenberg W (2008) Higher order visual input to the mushroom bodies in the bee, Bombus impatiens. Arthropod Struct Dev 37:443–458. doi:10.1016/j.asd.2008.03.002, Higher

    Article  PubMed Central  PubMed  Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing

  • Raine NE, Chittka L (2007) The adaptive significance of sensory bias in a foraging context: floral colour preferences in the bumblebee Bombus terrestris. PLoS ONE 2:e556. doi:10.1371/journal.pone.0000556

    Article  PubMed Central  PubMed  Google Scholar 

  • Raven PH (1972) Why are bird-visited flowers predominantly red? Evolution (N Y) 26:674

    Google Scholar 

  • Reisenman CE, Giurfa M (2008) Chromatic and achromatic stimulus discrimination of long wavelength (red) visual stimuli by the honeybee Apis mellifera. Arthropod Plant Interact 2:137–146

    Article  Google Scholar 

  • Reser DH, Witharanage RW, Rosa MGP, Dyer AG (2012) Honeybees (Apis mellifera) learn color discriminations via differential conditioning independent of long wavelength (Green) photoreceptor modulation. PLoS ONE 7:e48577. doi:10.1371/journal.pone.0048577

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rodríguez-Gironés MA, Santamaría L (2005) Resource partitioning among flower visitors and evolution of nectar concealment in multi-species communities. Proc Biol Sci 272:187–192. doi:10.1098/rspb.2005.2936

    Article  PubMed Central  PubMed  Google Scholar 

  • Rodríguez-Gironés MA, Santamaría L (2004) Why are so many bird flowers red? PLoS Biol 2:e350. doi:10.1371/journal.pbio.0020350

    Article  PubMed Central  PubMed  Google Scholar 

  • Rodríguez-Gironés MA, Santamaría L (2010) How foraging behaviour and resource partitioning can drive the evolution of flowers and the structure of pollination networks. Open Ecol J 3:1–11

    Article  Google Scholar 

  • Rodríguez-Gironés MA, Trillo A, Corcobado G (2013) Long term effects of aversive reinforcement on colour discrimination learning in free-flying bumblebees. PLoS ONE 8:e71551. doi:10.1371/journal.pone.0071551

    Article  PubMed Central  PubMed  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 

  • Santamaría L, Rodríguez-Gironés MA (2007) Linkage rules for plant-pollinator networks: trait complementarity or exploitation barriers? PLoS Biol 5:e31. doi:10.1371/journal.pbio.0050031

    Article  PubMed Central  PubMed  Google Scholar 

  • Skorupski P, Chittka L (2010) Differences in photoreceptor processing speed for chromatic and achromatic vision in the bumblebee, Bombus terrestris. J Neurosci Off J Soc Neurosci 30:3896–3903. doi:10.1523/JNEUROSCI. 5700-09.2010

    Article  CAS  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. doi:10.1007/s00359-006-0206-6

    Article  Google Scholar 

  • Skorupski P, Spaethe J, Chittka L (2006) Visual search and decision making in bees: time, speed, and accuracy. Int J Comp Psychol 19:342–357

    Google Scholar 

  • Spaethe J, Chittka L (2003) Interindividual variation of eye optics and single object resolution in bumblebees. J Exp Biol 206:3447–3453. doi:10.1242/jeb.00570

    Article  PubMed  Google Scholar 

  • 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 U S A 98:3898–3903. doi:10.1073/pnas.071053098

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Stang M, Klinkhamer PGL, van der Meijden E (2006) Size constraints and flower abundance determine the number of interactions in a plant-flower visitor web. Oikos 112:111–121

    Article  Google Scholar 

  • Vorobyev M, Brandt R (1997) How do insect pollinators discriminate colors? Isr J Plant Sci 45:103–113

    Article  Google Scholar 

  • Vorobyev M, Brandt R, Peitsch D et al (2001) Colour thresholds and receptor noise: behaviour and physiology compared. Vis Res 41:639–653

    Article  CAS  PubMed  Google Scholar 

  • Vorobyev M, De Ibarra NH, Brandt R, Giurfa M (1999) Do “white” and “ green ” look the same to a bee? Naturwissenschaften 86:592–594

    Article  CAS  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang M-Y, Ings TC, Proulx MJ, Chittka L (2013) Can bees simultaneously engage in adaptive foraging behaviour and attend to cryptic predators? Anim Behav 86:859–866. doi:10.1016/j.anbehav.2013.07.029

    Article  Google Scholar 

  • Wertlen AM, Niggebrügge C, Vorobyev M, Hempel de Ibarra N (2008) Detection of patches of coloured discs by bees. J Exp Biol 211:2101–2104. doi:10.1242/jeb.014571

    Article  PubMed  Google Scholar 

  • Yang E-C, Lin H-C, Hung Y-S (2004) Patterns of chromatic information processing in the lobula of the honeybee, Apis mellifera L. J Insect Physiol 50:913–925. doi:10.1016/j.jinsphys.2004.06.010

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Alejandro Trillo Iglesias and Guadalupe Corcobado for their assistance running the experiments, Klaus Lunau for his help in the calculation of spectral purities, four anonymous reviewers for comments, and Agrobío (Almería, Spain), for kindly providing bumblebee colonies. This research was supported by the Spanish Ministerio de Ciencia e Innovación/FEDER (project CGL2010-16795 to M.A.R.G.) and a PhD studentship to F.J.T. from the Spanish National Research Council (CSIC), co-funded by the European Social Fund (JAE: JAEPre033).

Conflict of interest

The authors declare that Agrobío has no claim on the scientific procedures of this study.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Francismeire Jane Telles.

Additional information

Communicated by: Sven Thatje

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 374 kb)

ESM 2

(PDF 273 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Telles, F.J., Rodríguez-Gironés, M.A. Insect vision models under scrutiny: what bumblebees (Bombus terrestris terrestris L.) can still tell us. Sci Nat 102, 4 (2015). https://doi.org/10.1007/s00114-014-1256-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00114-014-1256-1

Keywords

Navigation