Why leaves of some trees turn red in autumn has puzzled biologists for decades, as just before leaf fall the pigments causing red coloration are newly synthesized. One idea to explain this apparently untimely investment is that red colour signals the tree's quality to herbivorous insects, particularly aphids. However, it is unclear whether red leaves are indeed less attractive to aphids than green leaves. Because aphids lack a red photoreceptor, it was conjectured that red leaves could even be indiscernable from green ones for these insects. Here we show, however, that the colour of autumnal tree leaves that appear red to humans are on average much less attractive to aphids than green leaves, whereas yellow leaves are much more attractive. We conclude that, while active avoidance of red leaves by aphids is unlikely, red coloration in autumn could still be a signal of the tree's quality, or alternatively serve to mask the over-attractive yellow that is unveiled when the green chlorophyll is recovered from senescing leaves. Our study shows that in sensory ecology, receiver physiology alone is not sufficient to reveal the whole picture. Instead, the combined analysis of behaviour and a large set of natural stimuli unexpectedly shows that animals lacking a red photoreceptor may be able to differentiate between red and green leaves.

References

Archetti M . 2000 The origin of autumn colours by coevolution. J. Theor. Biol. 205, 625–630.doi:10.1006/jtbi.2000.2089. . Crossref, PubMed, ISI, Google Scholar
Barbagallo S, Cocuzza G, Cravedi P& Komazaki S IPM case studies: deciduous fruit trees. Aphids as crop pests , Van Emden H.F& Harrington R . 2007pp. 651–661. Eds. Wallingford, UK:CAB International. Crossref, Google Scholar
Blommers L.H.M, Helsen H.H.M& Vaal F.W.N.M . 2004 Life history data of the rosy apple aphid Dysaphis plantaginea (Pass.) (Homopt., Aphididae) on plantain and as migrant to apple. J. Pest Sci. 77, 155–163.doi:10.1007/s10340-004-0046-5. . Crossref, ISI, Google Scholar
Briscoe A& Chittka L . 2001 Evolution of color vision in insects. Annu. Rev. Entomol. 46, 471–510.doi:10.1146/annurev.ento.46.1.471. . Crossref, PubMed, ISI, Google Scholar
Chittka L . 1996 Optimal sets of color receptors and opponent process for coding of natural objects in insect vision. J. Theor. Biol. 181, 179–196.doi:10.1006/jtbi.1996.0124. . Crossref, ISI, Google Scholar
Chittka L& Döring T.F . 2007 Are autumn foliage colors red signals to aphids?. PLoS Biol. 5, e187 doi:10.1371/journal.pbio.0050187. . Crossref, PubMed, ISI, Google Scholar
Crawley M.J The R book. 2007 Chichester, UK:Wiley. Google Scholar
Döring T.F& Chittka L . 2007 Visual ecology of aphids: a critical review on the role of colours in host finding. Arthropod Plant Interact. 1, 3–16.doi:10.1007/s11829-006-9000-1. . Crossref, ISI, Google Scholar
Döring T.F& Hardie J . 2007 Host finding in aphids and the handicap of trapping methods. Biol. Lett. 3, 150–151.doi:10.1098/rsbl.2006.0592. . Link, ISI, Google Scholar
Döring T.F& Kirchner S.M . 2007 Preliminary characterisation of the spectral sensitivity in the cabbage aphid (Hemiptera: Aphididae) with electroretinogram recordings. Entomol. Gen. 30, 233–234. Crossref, ISI, Google Scholar
Gimingham C.T, Massee A.M& Tattersfield F . 1926 A quantitative examination of the toxicity of 3 : 5-dinitro-O-cresol and other compounds to insect eggs, under laboratory and field conditions. Ann. Appl. Biol. 13, 446–465.doi:10.1111/j.1744-7348.1926.tb04288.x. . Crossref, Google Scholar
Graf B, Höpli H.U, Höhn H& Samietz J . 2006 Temperature effects on egg development of the rosy apple aphid and forecasting of egg hatch. Entomol. Exp. Appl. 119, 207–211.doi:10.1111/j.1570-7458.2006.00411.x. . Crossref, ISI, Google Scholar
Hamilton W.D& Brown S.P . 2001 Autumn tree colours as a handicap signal. Proc. R. Soc. B. 268, 1489–1493.doi:10.1098/rspb.2001.1672. . Link, ISI, Google Scholar
Kehrli P& Wyss E . 2001 Effects of augmentative releases of the coccinellid, Adalia bipunctata, and of insecticide treatments in autumn on the spring population of aphids of the genus Dysaphis in apple orchards. Entomol. Exp. Appl. 99, 245–252.doi:10.1023/A:1018945117119. . Crossref, ISI, Google Scholar
Kirchner S.M, Döring T.F& Saucke H . 2005 Evidence for trichromacy in the green peach aphid Myzus persicae (Homoptera: Aphididae). J. Insect. Physiol. 51, 1255–1260.doi:10.1016/j.jinsphys.2005.07.002. . Crossref, PubMed, ISI, Google Scholar
Lee D.W . 2002 Anthocyanins in autumn leaf senescence. Adv. Bot. Res. 37, 147–165.doi:10.1016/S0065-2296(02)37048-4. . Crossref, ISI, Google Scholar
Lin H, Luo M.R, MacDonald L.W& Tarrant A.W.S . 2001 A cross-cultural colour-naming study. Part III: a colour-naming model. Color Res. Appl. 26, 270–277.doi:10.1002/col.1033. . Crossref, ISI, Google Scholar
Manetas Y . 2006 Why some leaves are anthocyanic and why most anthocyanic leaves are red. Flora. 201, 163–177. Crossref, ISI, Google Scholar
Müller H.J . 1964 Über die Anflugdichte von Aphiden auf farbige Salatpflanzen. Entomol. Exp. Appl. 7, 85–104.doi:10.1007/BF00369171. . Crossref, Google Scholar
Ougham H, Thomas H& Archetti M . 2008 Origin and evolution of autumn colours: report of a meeting held at St John's College Oxford 14–15 March 2008. New Phytol. 179, 9–13.doi:10.1111/j.1469-8137.2008.02505.x. . Crossref, PubMed, ISI, Google Scholar
Peitsch D, Fietz A, Hertel H, de Souza J, Ventura D.F& Menzel R . 1992 The spectral input system of hymenopteran insects and their receptor-based colour vision. J. Comp. Physiol. A. 170, 23–40.doi:10.1007/BF00190398. . Crossref, PubMed, ISI, Google Scholar
Prokopy R.J& Owens E.D . 1983 Visual detection of plants by herbivorous insects. Annu. Rev. Entomol. 28, 337–364.doi:10.1146/annurev.en.28.010183.002005. . Crossref, ISI, Google Scholar
Prokopy R.J, Collier R.H& Finch S . 1983 Leaf color used by cabbage root flies to distinguish among host plants. Science. 221, 190–192.doi:10.1126/science.221.4606.190. . Crossref, PubMed, ISI, Google Scholar
R Development Core Team 2007 R, a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Google Scholar
Roberson D, Davidoff J, Davies I.R& Shapiro L.R . 2005 Color categories: evidence for the cultural relativity hypothesis. Cognit. Psychol. 50, 378–411.doi:10.1016/j.cogpsych.2004.10.001. . Crossref, PubMed, ISI, Google Scholar
Sanger J.E . 1971 Quantitative investigations of leaf pigments from their inception in buds through autumn coloration to decomposition in falling leaves. Ecology. 52, 1075–1089.doi:10.2307/1933816. . Crossref, ISI, Google Scholar
Sharma G& Trussell H.J . 1997 Digital color imaging. IEEE Trans. Image Process. 6, 901–932.doi:10.1109/83.597268. . Crossref, PubMed, ISI, Google Scholar
Skorupski, P. & Chittka, L. 2008 Towards a cognitive definition of colour vision. Nature Precedings, pp.1–6. (hdl:10101/npre.2008.1766.1). Google Scholar
Stavenga D.G, Smits R.P& Hoenders B.J . 1993 Simple exponential functions describing the absorbance bands of visual pigment spectra. Vision Res. 33, 1011–1017.doi:10.1016/0042-6989(93)90237-Q. . Crossref, PubMed, ISI, Google Scholar
Van Emden H.F& Harrington R Aphids as crop pests. 2007 Wallingford, UK:CAB International. Google Scholar
Way M.J, Cammell M.E, Taylor L.R& Woiwood I.P . 1981 The use of egg counts and suction trap samples to forecast the infestation of spring-sown field beans, Vicia faba, by the black bean aphid, Aphis fabae. Ann. Appl. Biol. 98, 21–34.doi:10.1111/j.1744-7348.1981.tb00419.x. . Crossref, ISI, Google Scholar
Wilkinson D.M, Sherrat T.N, Phillip D.M, Wratten S.D, Dixon A.F.G& Young A.J . 2002 The adaptive significance of autumn leaf colours. Oikos. 99, 402–407.doi:10.1034/j.1600-0706.2002.990223.x. . Crossref, ISI, Google Scholar