WHY RED FLOWERS ARE NOT INVISIBLE TO BEES
In: Israel Journal of Plant SciencesA pervasive idea among pollination biologists is that bees cannot see red flowers. This idea has led many workers to assume that red coloration is an adaptation by which flowers exclude bees as visitors. However, recent empirical and theoretical evidence strongly supports the alternative view, that red flowers are visible to bees. Our purpose is to marshal this evidence from physiology, behavior, and ecology. First, we define the spectral boundary between orange and red, and show that the visual spectrum of all bee species studied to date extends enough into long wavelengths to provide sensitivity to red light. Such sensitivity differs from the ability to discriminate different monochromatic lights, and we argue that bees will be unable to discriminate such lights above about 550 nm. Second, we point out that flowers do not reflect monochromatic lights. Instead many of them, particularly those that appear red, orange, yellow, and white to humans, have reflectance patterns that are essentially step functions. We predict that bees should be able to discriminate such reflectance patterns over a range of 550–650 nm, since reflectance functions with steps at such wavelengths will occupy different loci in bee color space and thus be distinguishable. In this sense, bees should distinguish between green-, yellow-, orange-, and red-reflecting objects, even if these do not reflect in shorter wavelengths (including UV). A behavioral experiment shows that bumblebees can indeed perform this task. Third, we present information on the spectral reflectance of some typical “red” flowers, combined with field observations of bee visitation to such flowers. We end with a preliminary reassessment of the adaptive significance of red flower coloration, using North American “hummingbird” flowers as an example; we also stress some of the pitfalls facing evolutionary biologists who continue to assume that bees are blind to red objects.
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-
Arikawa K., Inokuma K., Eguchi E.Pantachromatic visual system in a butterfly. Naturwissenschaften 1987 74 297 298
-
Armbruster W.S.Estimating and testing the shapes of adaptive surfaces: the morphology and pollination of Dalechampia blossoms. Am. Nat. 1990 135 14 31
-
Backhaus W.Color opponent coding in the visual system of the honeybee. Vision Res. 1991 31 1381 1397
-
Béne F.Experiments on the color preference of black-chinned hummingbirds. Condor 1941 43 237 323
-
Bradshaw H.D. Jr., Wilbert S.M., Otto K.G., Schemske D.W.Genetic mapping of floral traits associated with reproductive isolation in monkeyflowers (Mimulus). Nature 1995 376 762 765
-
Campbell D.R., Waser N.M., Price M.V.Mechanisms of hummingbird-mediated selection for flower width in Ipomopsis aggregata Ecology 1996 77 1463 1472
-
Chen D.M., Goldsmith T.H.Four spectral classes of cone in the retinas of birds. J. Comp. Physiol. 1986 159 473 479
-
Chittka L.The color hexagon: a chromaticity diagram based on photoreceptor excitations as a generalized representation of colour opponency. J. Comp. Physiol. A 1992 170 533 543
-
Chittka L.Does bee color vision predate the evolution of flower color? Naturwissenschaften 1996 83 136 138
-
Chittka L., Menzel R.The evolutionary adaptation of flower colors and the insect pollinators' color vision systems. J. Comp. Physiol. A 1992 171 171 181
-
Chittka L., Beier W., Hertel H., Steinmann E., Menzel R.Opponent coding is a universal strategy to evaluate the photoreceptor inputs in Hymenopera. J. Comp. Physiol. A 1992 170 545 563
-
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 1508
-
Collias N.E., Collias E.C.Anna's hummingbird trained to select different colors in feeding. Condor 1968 70 273 274
-
Dafni A., Bernhardt P., Shmida A., Irvri Y., Greenbaum S., O'Toole C., Losito L.Red bowl-shaped flowers: convergence for beetle pollination in the Mediterranean region. Isr. J. Bot. 1990 39 81 92
-
Daumer K.Reizmetrische Untersuchung des Farbensehens der Bienen. Z. Vgl. Physiol. 1956 38 413 478
-
Daumer K.Blumenfarben, wie sie die Bienen sehen. Z. Vgl. Physiol. 1958 41 49 110
-
Elam D.R., Linhart Y.B.Pollination and seed production in Ipomopsis aggregata: differences among and within flower color morphs. Amer. J. Bot. 1978 75 1262 1274
-
Exner F., Exner S.Die physikalischen Grundlagen der Blütenfärbungen. 1910 I 119 191 245Sitzungsber. Kais. Akad. Wiss. Wien, Math.-nat. Kl
-
von Frisch K.Demonstration von Versuchen zum Nachweis des Farbensehens bei angeblich total farbenblinden Tieren. Verhandl. Deutsch. Zool. Ges. 1914 24 50 58
-
von Frisch K.Der Farbensinn und Formensinn der Bienen. Zool. Jahresber. (Physiol.) 1914/1915 35 1 188
-
von Frisch K.The dance language and orientation of bees. Harvard University Press Cambridge, MA. 1967
-
Giurfa M., Backhaus W., Menzel R.Colour and angular orientation in the discrimination of bilateral symmetric patterns in the honeybee. Naturwissenschaften 1995 82 198 201
-
Giurfa M., Vorobyev M., Kevan P., Menzel R.Detection of coloured stimuli by honeybees: minimum visual angles and receptor specific contrasts. J. Comp. Physiol. A 1996 178 699 709
-
Goldsmith T.H., Goldsmith K.M.Discrimination of colors by the black-chinned hummingbird, Archilochus alexandri J. Comp. Physiol. A 1979 130 209 220
-
Grant K.A., Grant V.Hummingbirds and their flowers. Columbia University Press New York 1968
-
Griffin D.R., Hubbard R., Wald G.The sensitivity of the human eye to infra-red radiation. J. Opt. Soc. Am. 1947 37 546 554
-
Hasselmann E.-M.Über die relative Empfindlichkeit von Käfer- und Schmetterlingsaugen bei verschiedenen Helligkeiten. Zool. J. Physiol. 1962 69 537 576
-
Harborne J.B., Biochemistry of plant pollination Introduction to ecological biochemistry. Harborne J.B.Academic Press London 1982 32 65
-
Hardie R.C.The photoreceptor array of the dipteran retina. Trends Neurosci. 1986 9 419 423
-
von Helversen O.Zur spektralen Unterschiedsempfindlichkeit der Honigbiene. J. Comp. Physiol. 1972 80 439 472
-
Hinton H.E.Possible significance of the red patches of the female crab spider, Misumena vatia J. Zool. 1976 180 35 37
-
Jacobs G.H.The distribution and nature of color vision among the mammals. Biol. Rev. 1993 68 413 471
-
Kelly D., Ladley J.J., Robertson A.W., Edwards J., Smith D.C.The birds and the flowers. Nature 1996 384615
-
Kevan P.O., Floral colors through the insect eye: what they are and what they mean Handbook of experimental pollination biology. Jones C.E., Little R.J.Van Nostrand Reinhold New York 1983 3 30
-
Kretz R.A behavioural analysis of colour vision in the ant Cataglyphis bicolor (Formicidae, Hymenoptera). J. Comp. Physiol. 1979 131 217 233
-
Kugler H.Hummeln als Blütenbesucher. Ergebn. Biol. 1943 19 143 323
-
Kühn A.Versuche über das Unterscheidungsvermögen der Bienen und Fische für Spektrallichter. Nachr. d. Ges. Wiss. Göttingen 1924 1 66 71
-
Laughlin S.B.The role of sensory adaptation in the retina. J. Exp. Biol. 1989 146 39 62
-
LeGrand Y.Light, colour and vision. Chapman and Hall London 1968
-
Lunau K., Wacht S., Chittka L.Colour choices of naive bumblebees and their implications for colour perception. J. Comp. Physiol. A 1996 178 477 489
-
Lythgoe J.N.The ecology of vision. Clarendon Press Oxford 1979
-
Macior L.W.Floral resource sharing by bumblebees and hummingbirds in Pedicularis (Scrophulariaceae) pollination. Bull. Torrey Bot. Club 1986 113 101 109
-
McNaughton I.H., Harper J.L.The comparative biology of closely related species living in the same area. I. External breeding barriers between Papaver species. New Phytol. 1960 59 15 26
-
Mazokhin-Porshniakov G.A.Insect vision. Plenum Press New York 1969
-
Meléndez-Ackerman E., Campbell D.R., Waser N.M.Hummingbird behavior and mechanisms of selection on flower color in Ipomopsis aggregata Ecology 1997in press
-
Menzel R., Backhaus W., Colour vision in insects Vision and visual dysfunction. The perception of colour. Gouras P.Macmillan Press London 1991 262 288
-
Miller R.S., Miller R.E.Feeding activity and color preference of ruby-throated hummingbirds. Condor 1971 73 309 313
-
Mitchell R.J.Is Penstemon centranthifolius truly hummingbird pollinated? Crossosoma 1989 15 1 9
-
Molitor A.Versuche betreffend die “Rotblindheit” solitärer Bienen. Verh. Zool.-bot. Ges. Wien 1937 86 125 139
-
Molitor A.Zum Farbensinn der Faltenwespen. Zool. Anz. 1939 126 259 264
-
Olesen J.M., Knudsen J.T.Scent profiles of flower colour morphs of Corydalis cava (Fumariaceae) in relation to foraging behaviour of bumblebee queens (Bombus terrestris). Biochem. Syst. Ecol. 1994 22 231 237
-
Paul R., Steiner A., Gemperlein R.Spectral sensitivities of Calliphora erythrocephala and other insect species studied with Fourier interferometric stimulation (FIS). J. Comp. Physiol. A 1986 158 669 680
-
Peitsch D., Fietz A., Hertel H., de Souza J., Ventura D.F., Menzel R.The spectral input systems of hymenopteran insects and their receptor-based colour vision. J. Comp. Physiol. A 1992 170 23 40
-
Plateau F.Nouvelles recherches sur les rapports entre les insectes et les fleurs. Mém. Soc. Zool. France 1899 12 336 370
-
Pleasants J.M., Waser N.M.Bumblebee foraging at a “hummingbird” flower: reward economics and floral choice. Am. Midl. Nat. 1985 114 283 291
-
Proctor M., Yeo P., Lack A.The natural history of pollination. Timber Press Portland, OR 1996
-
Raven P.H.Why are bird-visited flowers predominantly red? Evolution 1972 26674
-
Rosen D.Systematische und ökologische Aspekte der Ultraviolett-Reflexion von Blüten am Beispiel der Dilleniidae, Lamiidae und Asteridae. Ph.D. thesis, Friedrich-Wilhelms-Universität, Bonn, Germany 1991
-
Smith V.C., Pokorny J.Spectral sensitivities of human foveal cones between 400 and 500nm. Vision Res. 1975 15 161 171
-
Srinivasan M.V., Lehrer M., Horridge G.A.Visual figure-ground discrimination in the honeybee: the role of motion parallax at boundaries. Proc. R. Soc. London B 1990 238 331 350
-
Stout A.B.Daylillies, the wild species and garden clones of Hemerocallis. Macmillan New York 1934
-
Straw R.M.Floral isolation in Penstemon Am. Nat. 1956 90 47 53
-
Struwe G.Spectral sensitivity of single photoreceptors in the compound eye of a tropical butterfly. J. Comp. Physiol. 1972 79 197 201
-
Sutherland S.D., Vickery R.K. Jr.On the relative importance of floral color, shape, and nectar rewards in attracting pollinators to Mimulus Great Basin Nat. 1993 53 107 117
-
Temeles E.A new dimension to hummingbird-flower relationships. Oecologia 1996 105 517 523
-
Varela F.J, Palacios A.G., Goldsmith T.H., Color vision of birds Vision, brain, and behavior of birds. Zeigler H.P., Bischof H.J.MIT Press Cambridge, MA 1993 77 98
-
Vickery R.K. Jr.Pollinator preferences for yellow, orange, and red flowers of Mimulus verbenaceus, M. cardinalis Great Basin Nat. 1992 52 145 148
-
Vogel S., Christian Konrad Sprengel's theory of the flower: the cradle of floral ecology Floral ecology. Lloyd D.G., Barrett S.C.H.Chapman & Hall New York 1996 44 62
-
Waser N.M.Competition for hummingbird pollination and sequential flowering in two Colorado wildflowers. Ecology 1978 59 934 944
-
Waser N.M.Pollinator availability as a determinant of flowering time in ocotillo (Fouquieria splendens). Oecologia 1979 39 107 121
-
Waser N.M.A comparison of distances flown by different visitors to flowers of the same species. Oecologia 1982 55 251 257
-
Waser N.M., The adaptive nature of floral traits: ideas and evidence Pollination biology. Real L.A.Academic Press New York 1983 241 285
-
Waser N.M., Chittka L., Price M.V., Williams N., Ollerton J.Generalization in pollination systems, and why it matters. Ecology 1996 77 1043 1060
-
Wilson P.Selection for pollination success and the mechanical fit of Impatiens flowers around bumblebee bodies. Biol. J. Linn. Soc. 1995 55 355 383
-
Yang E., Osorio D.Spectral sensitivities of photoreceptors and lamina monopolar cells in the dragonfly, Hemicordulia tau. J. Comp. Physiol. A 1991 169 663 669
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WHY RED FLOWERS ARE NOT INVISIBLE TO BEES
In: Israel Journal of Plant SciencesA pervasive idea among pollination biologists is that bees cannot see red flowers. This idea has led many workers to assume that red coloration is an adaptation by which flowers exclude bees as visitors. However, recent empirical and theoretical evidence strongly supports the alternative view, that red flowers are visible to bees. Our purpose is to marshal this evidence from physiology, behavior, and ecology. First, we define the spectral boundary between orange and red, and show that the visual spectrum of all bee species studied to date extends enough into long wavelengths to provide sensitivity to red light. Such sensitivity differs from the ability to discriminate different monochromatic lights, and we argue that bees will be unable to discriminate such lights above about 550 nm. Second, we point out that flowers do not reflect monochromatic lights. Instead many of them, particularly those that appear red, orange, yellow, and white to humans, have reflectance patterns that are essentially step functions. We predict that bees should be able to discriminate such reflectance patterns over a range of 550–650 nm, since reflectance functions with steps at such wavelengths will occupy different loci in bee color space and thus be distinguishable. In this sense, bees should distinguish between green-, yellow-, orange-, and red-reflecting objects, even if these do not reflect in shorter wavelengths (including UV). A behavioral experiment shows that bumblebees can indeed perform this task. Third, we present information on the spectral reflectance of some typical “red” flowers, combined with field observations of bee visitation to such flowers. We end with a preliminary reassessment of the adaptive significance of red flower coloration, using North American “hummingbird” flowers as an example; we also stress some of the pitfalls facing evolutionary biologists who continue to assume that bees are blind to red objects.
| All Time | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 1483 | 650 | 136 |
| Full Text Views | 28 | 9 | 6 |
| PDF Views & Downloads | 23 | 4 | 0 |