Abstract
Bees have ultraviolet (UV), blue and green photoreceptor types in their compound eyes with which they locate food sources in landscapes that change continuously in cues emanating from plants and backgrounds against which they are perceived. The complexity of bee vision has been elucidated through studies examining individual species under laboratory conditions. Here, we used a bee-attractive fluorescent blue trap as a model for analyzing visual signals in operation outdoors, and across bee species. We manipulated trap color (appearance to humans under light with weak UV component) and UV-induced fluorescence emission, and aligned field capture results with bee vision models. Our studies show that the bees were attracted to traps that under solar illumination exhibited strong fluorescence emission exclusively in the blue spectral region. Through quantitative analysis, we established that strong spectral overlap of trap emittance with the photosensitivity characteristic of the blue receptor type and minimal overlap with those of the other two receptor types is the most critical property of attractive traps. A parameter has been identified which predicts the degree of attractiveness of the traps and which captures trends in the field data across wild bee species and for a diversity of backgrounds.
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Abbreviations
- BBF:
-
Blue blue fluorescent
- BF:
-
Blue fluorescent
- BN:
-
Blue non-fluorescent
- CBF:
-
Clear blue fluorescent
- CGF:
-
Clear green fluorescent
- CN:
-
Clear non-fluorescent
- CYF:
-
Clear yellow fluorescent
- JND:
-
Just-noticeable-difference
- RNL:
-
Receptor noise limited
- UV:
-
Ultraviolet
- YF:
-
Yellow fluorescent
References
Andrews K, Reed SM, Masta SE (2007) Spiders fluoresce variably across many taxa. Biol Lett 3:265–267
Campan R, Lehrer M (2002) Discrimination of closed shapes by two species of bee, Apis mellifera and Megachile rotundata. J Exp Biol 205:559–572
Chittka L (1997) Bee color vision is optimal for coding flower color, but flower colors are not optimal for being coded—Why? Isr J Plant Sci 45:115–127
Chittka L (1999) Bees, white flowers, and the color hexagon—a reassessment? No, not yet comments on the contribution by Vorobyev et al. Naturwissenschaften 86:595–597
Chittka L, Menzel R (1992) The evolutionary adaptation of flower colors and the insect pollinators color vision. J Comp Physiol A 171:171–181
Chittka L, Spaethe J (2007) Visual search and the importance of time in complex decision making by bees. Arthropod Plant Interact 1:37–44
Chittka L, Shmida A, Troje N, Menzel R (1994) Ultraviolet as a component of flower reflections, and the color perception of Hymenoptera. Vision Res 34:1489–1508
Dyer AG, Chittka L (2004) Biological significance of distinguishing between similar colors in spectrally variable illumination: bumblebees (Bombus terrestris) as a case study. J Comp Physiol A 190:105–114
Fasel A, Muller PA, Suppan P, Vauthey E (1997) Photoluminescence of the African scorpion “Pandinus imperator”. J Photochem Photobiol B 39:96–98
Gandia-Herrero F, Garcia-Carmona F, Escribano J (2005) Floral fluorescence effect. Nature 437:334
Giurfa M, Nunez J, Chittka L, Menzel R (1995) Color preferences of flower-naive honeybees. J Comp Physiol A 177:247
Goodale E, Kim E, Nabors A, Henrishon S, Nieh J (2014) The innate responses of bumble bees to flower patterns: separating the nectar guide from the nectary changes bee movements and search time. Naturwissenschaften 101:523–526
Gumbert A (2000) Color choice by bumble bees (Bombus terrestris): innate preferences and generalization after learning. Behav Ecol Sociobiol 48:36–43
Lunau K (1990) Color saturation triggers innate reactions to flower signals: flower dummy experiments with bumblebees. J Comp Physiol A 166:827–834
Lunau K (1991) Innate flower recognition in bumblebees (Bombus terrestris, B. lucorum; Apidae)—optical signals from stamens as landing reaction releasers. Ethology 88:203–214
Lunau K (1992) Innate recognition of flowers by bumble bees: orientation of antennae to visual stamen signals. Can J Zool 70:2139–2144
Lunau K, Maier EJ (1995) Innate color preferences of flower visitors. J Comp Physiol A 177:1–19
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
Lunau K, Fieselmann G, Heuschen B, van de Loo A (2006) Visual targeting of components of floral color patterns in flower-naive bumblebees (Bombus terrestris; Apidae). Naturwissenschaften 93:325–328
Milet-Pinheiro P, Ayasse M, Schlindwein C, Dobson H, Dotterl S (2012) Host location by visual and olfactory floral cues in an oligolectic bee: innate and learned behavior. Behav Ecol. doi:10.1093/beheco/arr219
Ostroverkhova O (ed) (2013) Handbook of organic materials for optical and (opto)electronic devices. Woodhead Publishing, Oxford
Papiorek S, Rohde K, Lunau K (2013) Bees’ subtle color preferences: how bees respond to small changes in pigment concentration. Naturwissenschaften 100:633–643
Paudel K, Johnson B, Thieme M, Haley M, Payne MM, Anthony JE, Ostroverkhova O (2014) Enhanced charge photogeneration promoted by crystallinity in small-molecule donor-acceptor bulk heterojunctions. Appl Phys Lett 105:043301
Pearn SM, Bennett ATD, Cuthill IC (2001) Ultraviolet vision, fluorescence, and mate choice in a parrot, the budgerigar Melopsittacus undulatus. Proc R Soc B 268:2273–2279
Peitsch D, Fietz A, Hertel H, de Souza J, Ventura D, Menzel R (1992) The spectral input systems of hymenopteran insects and their receptor-based color vision. J Comp Physiol A 170:23–40
Platt AD, Day J, Subramanian S, Anthony JE, Ostroverkhova O (2009) Optical, fluorescent, and (photo)conductive properties of high-performance functionalized pentacene and anthradithiophene derivatives. J Phys Chem C 113:14006–14014
Platt AD, Kendrick MJ, Loth M, Anthony JE, Ostroverkhova O (2011) Temperature dependence of exciton and charge carrier dynamics in organic thin films. Phys Rev B 84:235209
Rohde K, Papiorek S, Lunau K (2013) Bumblebees (Bombus terrestris) and honeybees (Apis mellifera) prefer similar colors of higher spectral purity over trained colors. J Comp Physiol A 199:197–210
Saikin SK, Eisfeld A, Valleau S, Aspuru-Guzik A (2013) Photonics meets excitonics: natural and artificial molecular aggregates. Nanophotonics 2:21–38
Skorupski P, Chittka L (2010) Differences in photoreceptor processing speed for chromatic and achromatic vision in the bumblebee Bombus terrestris. J Neurosci 30:3896–3903
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 98:3898–3903
Stephen WP, Rao S (2007) Sampling native bees in proximity to a highly competitive food resource (Hymenoptera : Apiformes). J Kans Entomol Soc 80:369–376
Valeur B (2002) Molecular fluorescence. Wiley-VCH, Weinheim
Vorobyev M, Osorio D (1998) Receptor noise as a determinant of color thresholds. Proc R Soc B 265:351–358
Whitney HM, Chittka L, Bruce TJA, Glover BJ (2009) Conical epidermal cells allow bees to grip flowers and increase foraging efficiency. Curr Biol 19:948–953
Acknowledgments
We thank the red clover farmers for permitting the study on their farms and Prof. W. Stephen and Dr. M. Bailey for help identifying the bees. Funding from Agricultural Research Foundation and Oregon State University is acknowledged.
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The authors declare that they have no conflict of interest.
Ethical standard
The ethical standards of the experiments comply with the current laws of the country in which they were performed.
Animal care
Animal care standards comply with the current laws of the country in which they were performed. Reports of animal experiments must state that the “Principles of laboratory animal care” (NIH publication no. 85-23 revised 1985) were followed as well as specific national laws (e.g., the current version of the German Law on the Protection of Animals) where applicable.
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Rao, S., Ostroverkhova, O. Visual outdoor response of multiple wild bee species: highly selective stimulation of a single photoreceptor type by sunlight-induced fluorescence. J Comp Physiol A 201, 705–716 (2015). https://doi.org/10.1007/s00359-015-0983-x
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DOI: https://doi.org/10.1007/s00359-015-0983-x