Abstract
Colour signalling by flowers appears to be the main plant-pollinator communication system observed across many diverse species and locations worldwide. Bees are considered one of the most important insect pollinators; however, native non-eusocial bees are often understudied compared to managed eusocial species, such as honeybees and bumblebees. Here, we tested two species of native Australian non-eusocial halictid bees on their colour preferences for seven different broadband colours with bee-colour-space dominant wavelengths ranging from 385 to 560 nm and a neutral grey control. Lasioglossum (Chilalictus) lanarium demonstrated preferences for a UV-absorbing white (455 nm) and a yellow (560 nm) stimulus. Lasioglossum (Parasphecodes) sp. showed no colour preferences. Subsequent analyses showed that green contrast and spectral purity had a significant positive relationship with the number of visits by L. lanarium to stimuli. Colour preferences were consistent with other bee species and may be phylogenetically conserved and linked to how trichromatic bees processes visual information, although the relative dearth of empirical evidence on different bee species currently makes it difficult to dissect mechanisms. Past studies and our current results suggest that both innate and environmental factors might both be at play in mediating bee colour preferences.
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References
Backhaus W, Menzel R, Kreißl S (1987) Multidimensional scaling of color similarity in bees. Biol Cybern 56:293–304
Barth FG (1985) Insects and flowers. The biology of a partnership. Princeton University Press, Princeton
Batley M, Hogendoorn K (2009) Diversity and conservation status of native Australian bees. Apidologie 40:347–354
Bell MC, Spooner-Hart RN, Haigh AM (2006) Pollination of greenhouse tomatoes by the Australian bluebanded bee Amegilla (Zonamegilla) holmesi (Hymenoptera: Apidae). J Econ Entomol 99:437–442
Biesmeijer JC, Giurfa M, Koedam D, Potts SG, Joel DM, Dafni A (2005) Convergent evolution: floral guides, stingless bee nest entrances, and insectivorous pitchers. Naturwissenschaften 92:444–450
Bischoff M, Campbell DR, Lord JM, Robertson AW (2013a) The relative importance of solitary bees and syrphid flies as pollinators of two outcrossing plant species in the New Zealand alpine. Austral Ecol 38:169–176
Bischoff M, Lord JM, Robertson A, Dyer AG (2013b) Hymenopteran pollinators as agents of selection on flower colour in the New Zealand mountains: salient chromatic signals enhance flower discrimination. N Z J Bot 51:181–193
Briscoe AD, Chittka L (2001) The evolution of color vision in insects. Annu Rev Entomol 46:471–510
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
Chittka L, Menzel R (1992) The evolutionary adaptation of flower colours and the insect pollinators’ colour vision. J Comp Physiol A 171:171–181
Chittka L, Wells H (2004) Color vision in bees: mechanisms, ecology and evolution. In: Prete F (ed) Complex worlds from simpler nervous systems. MIT Press, Boston, pp 165–191
Chittka L, Beier W, Hertel H, Steinmann E, Menzel R (1992) Opponent colour coding is a universal strategy to evaluate the photoreceptor inputs in Hymenoptera. J Comp Physiol A 170:545–563
Chittka L, Shmida A, Troje N, Menzel R (1994) Ultraviolet as a component of flower reflections, and the colour perception of Hymenoptera. Vis Res 34:1489–1508
Chittka L, Thomson JD, Waser NM (1999) Flower constancy, insect psychology, and plant evolution. Naturwissenschaften 86:361–377
Chittka L, Faruq S, Skorupski P, Werner A (2014) Colour constancy in insects. J Comp Physiol A 200:435–448
Darwin C (1876) The effects of cross and self fertilisation in the vegetable kingdom. John Murray, London
Daumer K (1956) Reizmetrische Untersuchungen des Farbensehens der Bienen. Z Vergl Physiol 38:413–478
Daumer K (1958) Blumenfarben, wie sie die Bienen sehen. Z Vergl Physiol 41:49–110
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
Dyer AG, Paulk AC, Reser DH (2011) Colour processing in complex environments: insights from the visual system of bees. Proc R Soc B 278:952–959
Dyer AG, Boyd-Gerny S, McLoughlin S, Rosa MG, Simonov V, Wong BB (2012) Parallel evolution of angiosperm colour signals: common evolutionary pressures linked to hymenopteran vision. Proc R Soc B 279:3606–3615
Dyer AG, Boyd-Gerny S, Shrestha M, Lunau K, Garcia JE, Koethe S, Wong BB (2016a) Innate colour preferences of the Australian native stingless bee Tetragonula carbonaria Sm. J Comp Physiol A 202:603–613
Dyer AG, Streinzer M, Garcia J (2016b) Flower detection and acuity of the Australian native stingless bee Tetragonula carbonaria Sm. J Comp Physiol A 202:629–639
Dyer AG, Boyd-Gerny S, Shrestha M, Garcia JE, van der Kooi CJ, Wong BB (2019) Colour preferences of Tetragonula carbonaria Sm. stingless bees for colour morphs of the Australian native orchid Caladenia carnea. J Comp Physiol A 205:347–361
Dyer AG et al (2021) Fragmentary blue: Resolving the rarity paradox in flower colors. Front Plant Sci 11:2212
Frisch K (1914) Der Farbensinn und Formensinn der Biene. Zool. Jb., Abt. Allg. Zool. Physiol. 35
Giurfa M (2004) Conditioning procedure and color discrimination in the honeybee Apis mellifera. Naturwissenschaften 91:228–231
Giurfa M, Nunez 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 178:699–709
Gumbert A (2000) Color choices by bumble bees (Bombus terrestris): innate preferences and generalization after learning. Behav Ecol Sociobiol 48:36–43
Heard T (2016) The Australian native bee book: kee** stingless bee hives for pets, pollination and sugarbag honey. Sugarbag Bees, Australia.
Hogendoorn K, Steen Z, Schwarz MP (2000) Native Australian carpenter bees as a potential alternative to introducing bumble bees for tomato pollination in greenhouses. J Apic Res 39:67–74
Hogendoorn K, Gross CL, Sedgley M, Keller MA (2006) Increased tomato yield through pollination by native Australian Amegilla chlorocyanea (Hymenoptera: Anthophoridae). J Econ Entomol 99:828–833
Hogendoorn K, Coventry S, Keller MA (2007) Foraging behaviour of a blue banded bee, Amegilla chlorocyanea in greenhouses: implications for use as tomato pollinators. Apidologie 38:86–92
Hogendoorn K, Bartholomaeus F, Keller MA (2010) Chemical and sensory comparison of tomatoes pollinated by bees and by a pollination wand. J Econ Entomol 103:1286–1292
Houston T (2018) A guide to native bees of Australia. CSIRO Publishing, Australia
Howard SR (2021) Wild non-eusocial bees learn a colour discrimination task in response to simulated predation events. Sci Nat 108(4):28
Howard SR, Shrestha M, Schramme J, Garcia JE, Avarguès-Weber A, Greentree AD, Dyer AG (2018) Honeybees prefer novel insect-pollinated flower shapes over bird-pollinated flower shapes. Curr Zool 65:457–465
Howard SR, Avarguès-Weber A, Garcia JE, Greentree AD, Dyer AG (2019a) Numerical cognition in honeybees enables addition and subtraction. Sci Adv 5:easv0961
Howard SR, Avarguès-Weber A, Garcia JE, Greentree AD, Dyer AG (2019b) Surpassing the subitizing threshold: appetitive–aversive conditioning improves discrimination of numerosities in honeybees. J Exp Biol 222:jeb205658
Howard SR, Avarguès-Weber A, Garcia JE, Greentree AD, Dyer AG (2019c) Symbolic representation of numerosity by honeybees (Apis mellifera): Matching characters to small quantities. Proc R Soc B 286:20190238
Howard SR, Schramme J, Garcia JE, Ng L, Avarguès-Weber A, Greentree AD, Dyer AG (2020) Spontaneous quantity discrimination of artificial flowers by foraging honeybees. J Exp Biol 223:jeb223610
Judd DB, MacAdam DL, Wyszecki G, Budde H, Condit H, Henderson S, Simonds J (1964) Spectral distribution of typical daylight as a function of correlated color temperature. Josa 54:1031–1040
Kantsa A, Raguso RA, Dyer AG, Sgardelis SP, Olesen JM, Petanidou T (2017) Community-wide integration of floral colour and scent in a Mediterranean scrubland. Nat Ecol Evol 1:1502–1510
Kemp DJ et al (2015) An integrative framework for the appraisal of coloration in nature. Am Nat 185:705–724
Kevan P, Giurfa M, Chittka L (1996) Why are there so many and so few white flowers? Trends Plant Sci 1:252
Kjøhl M, Nielsen A, Stenseth NC (2011) Potential effects of climate change on crop pollination. Food and Agriculture Organization of the United Nations (FAO).
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 202:615–627
Lehrer M, Horridge G, Zhang S, Gadagkar R (1995) Shape vision in bees: innate preference for flower-like patterns. Philos Trans R Soc 347:123–137
Leijs R, Dorey J, Hogendoorn K (2018) Twenty six new species of Leioproctus (Colletellus): Australian Neopasiphaeinae, all but one with two submarginal cells (Hymenoptera, Colletidae, Leioproctus). ZooKeys 811:109–168
Leonard AS, Masek P (2014) Multisensory integration of colors and scents: insights from bees and flowers. J Comp Physiol A 200:463–474
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 (1993) Interspecific diversity and uniformity of flower colour patterns as cues for learned discrimination and innate detection of flowers. Experientia 49:1002–1010
Mayack C, Naug D (2015) Starving honeybees lose self-control. Biol Lett 11:20140820
Menzel R (1967) Untersuchungen zum Erlernen von Spektralfarben durch die Honigbiene (Apis mellifica). Z Vergl Physiol 56:22–62
Menzel R (1999) Memory dynamics in the honeybee. J Comp Physiol A 185:323–340
Mitchell RJ, Irwin RE, Flanagan RJ, Karron JD (2009) Ecology and evolution of plant–pollinator interactions. Ann Bot 103:1355–1363
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 199:817–827
Ng L, Garcia JE, Dyer AG (2018) Why colour is complex: Evidence that bees perceive neither brightness nor green contrast in colour signal processing. Facets 3:800–817
Papiorek S, Rohde K, Lunau K (2013) Bees’ subtle colour preferences: how bees respond to small changes in pigment concentration. Naturwissenschaften 100:633–643
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 170:23–40
Potts SG et al. (2016) Summary for policymakers of the assessment report of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES) on pollinators, pollination and food production.
R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria
Raine NE, Chittka L (2005) Colour preferences in relation to the foraging performance and fitness of the bumblebee Bombus terrestris. Uludag Bee J 5:145–150
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
Raine NE, Ings TC, Ramos-Rodriguez O, Chittka L (2006) Intercolony variation in learning performance of a wild British bumblebee population Hymenoptera: apidae: Bombus terrestris audax. Entomol Gen 28:241–256
Rodríguez I, Gumbert A, de Ibarra NH, Kunze J, Giurfa M (2004) Symmetry is in the eye of the ‘beeholder’: innate preference for bilateral symmetry in flower-naïve bumblebees. Naturwissenschaften 91:374–377
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
Sargent RD, Ackerly DD (2008) Plant–pollinator interactions and the assembly of plant communities. Trends Ecol Evol 23:123–130
Shrestha M, Dyer AG, Boyd-Gerny S, Wong B, Burd M (2013) Shades of red: bird-pollinated flowers target the specific colour discrimination abilities of avian vision. New Phytol 198:301–310
Shrestha M, Dyer AG, Bhattarai P, Burd M (2014) Flower colour and phylogeny along an altitudinal gradient in the Himalayas of Nepal. J Ecol 102:126–135
Shrestha M, Dyer AG, Garcia JE, Burd M (2019) Floral colour structure in two Australian herbaceous communities: it depends on who is looking. Ann Bot 124:221–232
Shrestha M, Garcia JE, Burd M, Dyer AG (2020) Australian native flower colours: does nectar reward drive bee pollinator flower preferences? PLoS ONE 15:e0226469
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 98:3898–3903
Spaethe J, Streinzer M, Eckert J, May S, Dyer AG (2014) Behavioural evidence of colour vision in free flying stingless bees. J Comp Physiol A 200:485–496
Stavenga DG, Smits RP, Hoenders BJ (1993) Simple exponential functions describing the absorbance bands of visual pigment spectra. Vis Res 33:1011–1017
Tai K-C, Shrestha M, Dyer AG, Yang E-C, Wang C-N (2020) Floral colour diversity: how are signals shaped by elevational gradient on the tropical-subtropical mountainous island of Taiwan? Front Plant Sci 11:2037
van der Kooi CJ, Dyer AG, Kevan PG, Lunau K (2018) Functional significance of the optical properties of flowers for visual signalling. Ann Bot 123:263–276
Von Helversen O (1972) Zur spektralen Unterschiedsempfindlichkeit der honigbiene. J Comp Physiol 80:439–472
Wehner R (1981) Spatial vision in arthropods. In: Autrum H (ed). Handbook of sensory physiology. Vol. VII/6C comparative physiology and evolution of vision in invertebrates, vol 4. Springer, Berlin, pp 287–616
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
Acknowledgements
We thank Kit Prendergast for previously identifying the species used in this study. Scarlett R Howard acknowledges the Alfred Deakin Postdoctoral Research Fellowship from Deakin University. Adrian G Dyer was supported by the Australian Research Council Discovery Project 160100161. All animal care was in accordance with institutional guidelines. Formal ethics approval was not required for invertebrate behavioural testing.
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SRH was funded by an Alfred Deakin Postdoctoral Research Fellowship from Deakin University. AGD was supported by the Australian Research Council Discovery Project 160100161.
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Howard, S.R., Garcia, J.E. & Dyer, A.G. Comparative psychophysics of colour preferences in two species of non-eusocial Australian native halictid bees. J Comp Physiol A 207, 657–666 (2021). https://doi.org/10.1007/s00359-021-01504-3
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DOI: https://doi.org/10.1007/s00359-021-01504-3