Our understanding of how floral visitors integrate visual and olfactory cues when seeking food, and how background complexity affects flower detection is limited. Here, we aimed to understand the use of visual and olfactory information for bumblebees (Bombus terrestris terrestris L.) when seeking flowers in a visually complex background. To explore this issue, we first evaluated the effect of flower colour (red and blue), size (8, 16 and 32 mm), scent (presence or absence) and the amount of training on the foraging strategy of bumblebees (accuracy, search time and flight behaviour), considering the visual complexity of our background, to later explore whether experienced bumblebees, previously trained in the presence of scent, can recall and make use of odour information when foraging in the presence of novel visual stimuli carrying a familiar scent. Of all the variables analysed, flower colour had the strongest effect on the foraging strategy. Bumblebees searching for blue flowers were more accurate, flew faster, followed more direct paths between flowers and needed less time to find them, than bumblebees searching for red flowers. In turn, training and the presence of odour helped bees to find inconspicuous (red) flowers. When bees foraged on red flowers, search time increased with flower size; but search time was independent of flower size when bees foraged on blue flowers. Previous experience with floral scent enhances the capacity of detection of a novel colour carrying a familiar scent, probably by elemental association influencing attention.

Department of Botany and Zoology Masaryk University Brno Czech Republic

Department of Functional and Evolutionary Ecology Estación Experimental de Zonas Áridas Almería Spain

Department of Integrative Ecology Doñana Biological Station Sevilla Spain

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Leonard AS, Papaj DR, Dornhaus A. Why are floral signals complex? An outline of functional hypotheses In: Patiny S, editor. Evolution of Plant-Pollinator Relationships. Cambridge: Cambridge University Press; 2011. pp. 261–282.

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

Katzenberger TD, Lunau K, Junker RR. Salience of multimodal flower cues manipulates initial responses and facilitates learning performance of bumblebees. Behav Ecol Sociobiol. 2013;67: 1587–1599. doi: 10.1007/s00265-013-1570-1 DOI

Forrest J, Thomson JD. Background complexity affects colour preference in bumblebees. Naturwissenschaften. 2009;96: 921–5. doi: 10.1007/s00114-009-0549-2 PubMed DOI

Spaethe J, Tautz J, Chittka L. Visual constraints in foraging bumblebees: flower size and color affect search time and flight behavior. Proc Natl Acad Sci U S A. 2001;98: 3898–903. doi: 10.1073/pnas.071053098 PubMed DOI PMC

Lehrer M, Horridge G a., Zhang SW, Gadagkar R. Shape Vision in Bees: Innate Preference for Flower-Like Patterns. Philos Trans R Soc B Biol Sci. 1995;347: 123–137. doi: 10.1098/rstb.1995.0017 DOI

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

Ne’eman G, Ne’eman R. Factors determining visual detection distance to real flowers by Bumble bees. J Pollinat Ecol. 2017;20: 1–12.

Rivest SA, Austen EJ, Forrest JRK. Foliage affects colour preference in bumblebees (Bombus impatiens): a test in a three-dimensional artificial environment. Evol Ecol. Springer International Publishing; 2017; 1–12. doi: 10.1007/s10682-017-9893-4 DOI

Bukovac Z, Dorin A, Finke V, Shrestha M, Garcia J, Avarguès-Weber A, et al. Assessing the ecological significance of bee visual detection and colour discrimination on the evolution of flower colours. Evol Ecol. 2016; 1–20. doi: 10.1007/s10682-016-9843-6 DOI

Wright GA, Schiestl FP. The evolution of floral scent: the influence of olfactory learning by insect pollinators on the honest signalling of floral rewards. Funct Ecol. 2009;23: 841–851. doi: 10.1111/j.1365-2435.2009.01627.x DOI

Martínez-Harms J, Palacios a G, Márquez N, Estay P, Arroyo MTK, Mpodozis J. Can red flowers be conspicuous to bees? Bombus dahlbomii and South American temperate forest flowers as a case in point. J Exp Biol. 2010;213: 564–71. doi: 10.1242/jeb.037622 PubMed DOI

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

Dafni A, Bernhardt P, Shmida A, Ivri BY, Greenbaum S, Losito L. Red bowl-shaped flowers : convergence for beetle pollination in the Mediterranean region. Isr J Bot. 1990;39: 81–92.

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

Bergamo PJ, Rech AR, Brito VLG, Sazima M. Flower colour and visitation rates of Costus arabicus support the “bee avoidance” hypothesis for red-reflecting hummingbird-pollinated flowers. Funct Ecol. 2016;30: 710–720. doi: 10.1111/1365-2435.12537 DOI

Gegear RJ, Burns R, Swoboda-Bhattarai KA. “Hummingbird” floral traits interact synergistically to discourage visitation by bumblebee foragers. Ecology. 2017;98: 489–499. doi: 10.1002/ecy.1661 PubMed DOI

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

Peitsch D, Fietz A, Hertel H, de Souza J, Ventura DF, Menzel R. The spectral input systems of hymenopteran insects and their receptor-based colour vision. J Comp Physiol A. 1992;170: 23–40. Available: http://www.ncbi.nlm.nih.gov/pubmed/1573568 PubMed

Chittka L, Shmida A, Troje N, Menzel R. Ultraviolet as a component of flower reflections, and the colour perception of Hymenoptera. Vision Res. 1994;34: 1489–508. Available: http://www.ncbi.nlm.nih.gov/pubmed/8023461 PubMed

Skorupski P, Döring TF, Chittka L. Photoreceptor spectral sensitivity in island and mainland populations of the bumblebee, Bombus terrestris. J Comp Physiol A. 2007;193: 485–94. doi: 10.1007/s00359-006-0206-6 PubMed DOI

Galizia CG, Kunze J, Gumbert A, Borg-Karlson AK, Sachse S, Markl C, et al. Relationship of visual and olfactory signal parameters in a food-deceptive flower mimicry system. Behav Ecol. 2005;16: 159–168. doi: 10.1093/beheco/arh147 DOI

Kunze J, Gumbert A. The combined effect of color and odor on flower choice behavior of bumble bees in flower mimicry systems. Behav Ecol. 2001;12: 447–456.

Sánchez D, Nieh JC, Vandame R. Visual and chemical cues provide redundant information in the multimodal recruitment system of the stingless bee Scaptotrigona mexicana (Apidae, Meliponini). Insectes Soc. 2011;58: 575–579. doi: 10.1007/s00040-011-0181-y DOI

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

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

Backhaus W. Color opponent coding in the visual system of the honeybee. Vision Res. 1991;31: 1381–1397. PubMed

Chittka L. The colour hexagon: a chromaticity diagram based on photoreceptor excitations as a generalized representation of colour opponency. J Comp Physiol A. 1992;170: 533–543. doi: 10.1007/BF00199331 DOI

Vorobyev M, Osorio D. Receptor noise as a determinant of colour thresholds. Proc Biol Sci. 1998;265: 351–8. doi: 10.1098/rspb.1998.0302 PubMed DOI PMC

Vorobyev M, Brandt R, Peitsch D, Laughlin SB, Menzel R. Colour thresholds and receptor noise: behaviour and physiology compared. Vision Res. 2001;41: 639–53. Available: http://www.ncbi.nlm.nih.gov/pubmed/11226508 PubMed

Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM. Mixed effects models and extensions in ecology with R. New York: Springer New York; 2009. doi: 10.1007/978-0-387-87458-6 DOI

Akaike H. Information theory and an extension of the maximum likelihood principle In: Petrov BN, Csaki F, editors. Proceedings of the Second International Symposium on Information Theory. Budapest: Akademiai Kiado; 1973. pp. 267–281.

R Core Team. R: A language and environment for statistical computing [Internet]. Vienna, Austria: R Foundation for Statistical Computing; 2013. http://www.r-project.org/

Bates D, Maechler M. lme4: linear mixed-effects models using Eigen and S4 [Internet]. 2013. http://cran.r-project.org/package=lme4

Giurfa M, Vorobyev M, Brandt R, Posner BB, Menzel R. Discrimination of coloured stimuli by honeybees: alternative use of achromatic and chromatic signals. J Comp Physiol A. 1997;180: 235–243. doi: 10.1007/s003590050044 DOI

Dyer AG, Spaethe J, Prack S. Comparative psychophysics of bumblebee and honeybee colour discrimination and object detection. J Comp Physiol A. 2008;194: 617–27. doi: 10.1007/s00359-008-0335-1 PubMed DOI

Hempel de Ibarra N, Vorobyev M, Brandt R, Giurfa M. Detection of bright and dim colours by honeybees. J Exp Biol. 2000;203: 3289–98. Available: http://www.ncbi.nlm.nih.gov/pubmed/11023849 PubMed

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

Telles FJ, Rodríguez-Gironés MA. Insect vision models under scrutiny: what bumblebees (Bombus terrestris terrestris L.) can still tell us. Sci Nat. 2015;102: 1–13. doi: 10.1007/s00114-014-1256-1 PubMed DOI

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

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

Chittka L, Skorupski P, Raine NE. Speed-accuracy tradeoffs in animal decision making. Trends Ecol Evol. 2009;24: 400–407. doi: 10.1016/j.tree.2009.02.010 PubMed DOI

Dyer AG, Chittka L. Bumblebees (Bombus terrestris) sacrifice foraging speed to solve difficult colour discrimination tasks. J Comp Physiol A. 2004;190: 759–63. doi: 10.1007/s00359-004-0547-y PubMed DOI

Rodríguez-Gironés MA, Trillo A, Corcobado G. Long term effects of aversive reinforcement on colour discrimination learning in free-flying bumblebees. PLoS One. 2013;8: e71551 doi: 10.1371/journal.pone.0071551 PubMed DOI PMC

Lunau K. Innate flower recognition in bumblebees (Bombus terrestris, B. lucorum; Apidae): optical signals from stamens as landing reaction releasers. Ethology. 1991;88: 203–214.

Lunau K. Innate recognition of flowers by bumble bees: orientation of antennae to visual stamen signals. Can J Zool. 1992;70: 2139–2144. doi: 10.1139/z92-288 DOI

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

Vereecken NJ, Schiestl FP. On the roles of colour and scent in a specialized floral mimicry system. Ann Bot. 2009;104: 1077–1084. doi: 10.1093/aob/mcp208 PubMed DOI PMC

Cronk Q, Ojeda I. Bird-pollinated flowers in an evolutionary and molecular context. J Exp Bot. 2008;59: 715–727. doi: 10.1093/jxb/ern009 PubMed DOI

Ballantyne G, Willmer P. Nectar Theft and Floral Ant-Repellence: A Link between Nectar Volume and Ant-Repellent Traits? PLoS One. 2012;7: 1–10. doi: 10.1371/journal.pone.0043869 PubMed DOI PMC

Farré-Armengol G, Filella I, Llusia J, Peñuelas J. Floral volatile organic compounds: Between attraction and deterrence of visitors under global change. Perspect Plant Ecol Evol Syst. 2013;15: 56–67. doi: 10.1016/j.ppees.2012.12.002 DOI

Carlsson MA, Hansson BS. Detection and Coding of Flower Volatiles in Nectar-Foraging Insects In: Pichersky E, Dudareva N, editors. Biology of Floral Scent. CRC Press; 2006. pp. 243–261. doi: 10.1201/9781420004007.ch11 DOI

Wright GA, Baker DD, Palmer MJ, Stabler D, Mustard JA, Power EF, et al. Caffeine in floral nectar enhances a pollinator’s memory of reward. Science. 2013;339: 1202–1204. doi: 10.1126/science.1228806 PubMed DOI PMC

Kulahci IG, Dornhaus A, Papaj DR. Multimodal signals enhance decision making in foraging bumble-bees. Proc Biol Sci. 2008;275: 797–802. doi: 10.1098/rspb.2007.1176 PubMed DOI PMC

Gegear RJ, Laverty TM. Flower constancy in bumblebees: a test of the trait variability hypothesis. Anim Behav. 2005;69: 939–949. doi: 10.1016/j.anbehav.2004.06.029 DOI

Junker RR, Parachnowitsch AL. Working Towards a Holistic View on Flower Traits—How Floral Scents Mediate Plant–Animal Interactions in Concert with Other Floral Characters. J Indian Inst Sci A Multidiscip Rev J. 2015;95: 1–13.

Leonard AS, Masek P. Multisensory integration of colors and scents: insights from bees and flowers. J Comp Physiol A Neuroethol Sensory, Neural, Behav Physiol. 2014;200: 463–474. doi: 10.1007/s00359-014-0904-4 PubMed DOI

Goodale E, Kim E, Nabors A, Henrichon S, Nieh JC. The innate responses of bumble bees to flower patterns: separating the nectar guide from the nectary changes bee movements and search time. Naturwissenschaften. 2014;101: 523–6. doi: 10.1007/s00114-014-1188-9 PubMed DOI

Orbán LL, Plowright CMS. Getting to the start line: how bumblebees and honeybees are visually guided towards their first floral contact. Insectes Soc. 2014;61: 325–336. doi: 10.1007/s00040-014-0366-2 PubMed DOI PMC

Lunau K, Fieselmann G, Heuschen B, van de Loo A. Visual targeting of components of floral colour patterns in flower-naïve bumblebees (Bombus terrestris; Apidae). Naturwissenschaften. 2006;93: 325–8. doi: 10.1007/s00114-006-0105-2 PubMed DOI

Knauer AC, Schiestl FP. Bees use honest floral signals as indicators of reward when visiting flowers. Ecol Lett. 2015;18: 135–143. doi: 10.1111/ele.12386 PubMed DOI

Odell E, Raguso RA, Jones KN. Bumblebee foraging responses to variation in floral scent and color in Snapdragons (Antirrhinum: Scrophulariaceae). Am Midl Nat. 1999;142: 257–265. doi: 10.1674/0003-0031(1999)142[0257:BFRTVI]2.0.CO;2 DOI

Raguso RA, Pichersky E. A day in the life of a linalool molecule: Chemical communication in a plant-pollinator system. Part 1: Linalool biosynthesis in ßowering plants. Plant Species Biol. 1999;14: 95–120.

Garbuzov M, Ratnieks FLW. Quantifying variation among garden plants in attractiveness to bees and other flower-visiting insects. Funct Ecol. 2014;28: 364–374. doi: 10.1111/1365-2435.12178 DOI

Nouvian M, Hotier L, Claudianos C, Giurfa M, Reinhard J. Appetitive floral odours prevent aggression in honeybees. Nat Commun. Nature Publishing Group; 2015;6: 1–10. doi: 10.1038/ncomms10247 PubMed DOI PMC

Dötterl S, Vereecken NJ. The chemical ecology and evolution of bee–flower interactions: a review and perspectives. Can J Zool. 2010;88: 668–697. doi: 10.1139/Z10-031 DOI

Knudsen JT, Eriksson R, Gershenzon J, Ståhl B. Diversity and Distribution of Floral Scent. Bot Rev. 2006;72: 1–120. doi: 10.1663/0006-8101(2006)72[1:DADOFS]2.0.CO;2 DOI

Parachnowitsch AL, Raguso RA, Kessler A. Phenotypic selection to increase floral scent emission, but not flower size or colour in bee-pollinated Penstemon digitalis. New Phytol. 2012;195: 667–675. doi: 10.1111/j.1469-8137.2012.04188.x PubMed DOI

Byers KJRP, Bradshaw HD, Riffell JA. Three floral volatiles contribute to differential pollinator attraction in monkeyflowers (Mimulus). J Exp Biol. 2014;217: 614–623. doi: 10.1242/jeb.092213 PubMed DOI PMC

Goulson D, Cruise JL, Sparrow KR, Harris AJ, Park KJ, Tinsley MC, et al. Choosing rewarding flowers; perceptual limitations and innate preferences influence decision making in bumblebees and honeybees. Behav Ecol Sociobiol. 2007;61: 1523–1529. doi: 10.1007/s00265-007-0384-4 DOI

Goyret J, Kelber A, Pfaff M, Raguso R a. Flexible responses to visual and olfactory stimuli by foraging Manduca sexta: larval nutrition affects adult behaviour. Proc R Soc London, B. 2009;276: 2739–45. doi: 10.1098/rspb.2009.0456 PubMed DOI PMC