, Volume 95, Issue 7, pp 671–676 | Cite as

Autumn leaf colouration: a new hypothesis involving plant–ant mutualism via aphids

  • Kazuo YamazakiEmail author
Short Communication


Several recent hypotheses on the adaptive significance of autumn leaf colours have focused on specialist aphids. However, these hypotheses have overlooked several factors: the preferential investment by healthy vigorous trees in growth rather than defence against herbivores, variation among aphid species in their responses to bright autumn leaves and plant defences and the occurrence of tritrophic interactions in tree crowns. I incorporate these factors into a hypothesis that autumn leaf colours signal tree quality to myrmecophilous specialist aphids, with the aphids, in turn, attracting aphid-tending ants during the following spring, and the ants defending the trees from other aphids and herbivores. Therefore, bright autumn leaves may have adaptive significance, attracting myrmecophilous specialist aphids and their attending ants and, thus, reducing herbivory and competition among aphids.


Aphid–ant interactions Autumn colouration Indirect interactions Myrmecophilous specialist aphids Plant–ant mutualism 



I thank Shinji Sugiura and Hiroshi Sakata for helpful advice in shaping this hypothesis and Simcha Lev-Yadun, David M. Wilkinson and anonymous reviewers for suggestions and encouragement on manuscript revisions. This research complies with the current laws of Japan.


  1. Archetti M (2000) The origin of autumn colours by coevolution. J Theor Biol 205:625–630PubMedCrossRefGoogle Scholar
  2. Archetti M, Brown S (2004) The coevolution theory of autumn colours. Proc Roy Soc Lond B 271:1219–1223CrossRefGoogle Scholar
  3. Archetti M, Leather SR (2005) A test of the coevolution theory of autumn colours: colour preference of Rhopalosiphum padi on Prunus padus. Oikos 110:339–343CrossRefGoogle Scholar
  4. Beattie AJ (1985) Evolutionary ecology of ant–plant mutualisms. Cambridge University Press, CambridgeGoogle Scholar
  5. Blackman RL, Eastop VF (1994) Aphids on the world’s trees. CAB, WallingfordGoogle Scholar
  6. Bristow CM (1991) Why are so few aphids ant-tended? In: Huxley CR, Cutler DF (eds) Ant–plant interactions. Oxford University Press, Oxford, pp 104–119Google Scholar
  7. Buckley RC (1987a) Interactions involving plants, Homoptera, and ants. Annu Rev Ecol Syst 18:111–135CrossRefGoogle Scholar
  8. Buckley RC (1987b) Ant–plant–homopteran interactions. Adv Ecol Res 16:53–85CrossRefGoogle Scholar
  9. Carter W (1962) Insects in relation to plant disease, 2nd edn. Wiley, New YorkGoogle Scholar
  10. Crawley MJ (1985) Reduction of oak fecundity by low-density herbivore populations. Nature 314:163–164CrossRefGoogle Scholar
  11. Delabie JHC (2001) Trophobiosis between Formicidae and Hemiptera (Sternorrhyncha and Auchenorrhyncha): an overview. Neotrop Entomol 30:501–516CrossRefGoogle Scholar
  12. Dixon AFG (1971) The role of aphids in wood formation I. The effects of the sycamore aphid, Drepanosiphum platanoides (Schr.) (Aphididae), on the growth of sycamore, Acer pseudoplatanus (L.). J Appl Ecol 8:165–179CrossRefGoogle Scholar
  13. Dixon AFG (1998) Aphid ecology: an optimization approach, 2nd edn. Chapman and Hall, LondonGoogle Scholar
  14. Döring TM, Chittka L (2007) Visual ecology of aphids—a critical review on the role of colours in host finding. Arthropod–Plant Interactions 1:3–16CrossRefGoogle Scholar
  15. Fineblum WL, Rausher MD (1997) Do floral pigmentation and genes also influence resistance to enemies? The W locus in Ipomoea pupurea. Ecology 78:1646–1654Google Scholar
  16. Furuta K (1986) Host preference and population dynamics in an autumnal population of the maple aphid, Periphyllus californiensis Shinji (Homoptera, Aphididae). J Appl Entomol 102:93–100CrossRefGoogle Scholar
  17. Furuta K (1990) Early budding of Acer palmatum caused by the shade; intraspecific heterogeneity of the host for the maple aphid. Bull Tokyo Univ For 82:137–145Google Scholar
  18. Gayler S, Leser C, Priesack E, Treutter D (2004) Modelling the effect of environmental factors: the “trade-off” between growth and defensive compounds in young apple trees. Trees Struct Funct 18:363–371CrossRefGoogle Scholar
  19. Gotelli NJ, Ellison AM (2002) Biogeography at a regional scale: determinants of ant species diversity in New England bogs and forests. Ecology 83:1604–1609CrossRefGoogle Scholar
  20. Gould KS (2004) Nature’s Swiss army knife: the diverse protective roles of anthocyanins in leaves. J Biomed Biotechnol 2004:314–320PubMedCrossRefGoogle Scholar
  21. Gray SM, Rochon D (1999) Vector transmission of plant viruses. In: Granoff A, Webster RG (eds) Encyclopedia of virology. 2nd edn. Academic, London, pp 1899–1910Google Scholar
  22. Hagen SB, Debeausse S, Yoccoz NG, Folstad I (2004) Autumn coloration as a signal of tree condition. Proc Roy Soc Lond B 271:S184–S185 (Suppl)CrossRefGoogle Scholar
  23. Hamilton WD, Brown SP (2001) Autumn tree colours as a handicap signal. Proc Roy Soc Lond B 268:1489–1493CrossRefGoogle Scholar
  24. Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Quart Rev Biol 67:283–335CrossRefGoogle Scholar
  25. Holopainen JK, Peltonen P (2002) Bright autumn colours of deciduous trees attract aphids: nutrient retranslocation hypothesis. Oikos 99:184–188CrossRefGoogle Scholar
  26. Huang HT, Yang P (1987) The ancient cultured citrus ant: a tropical ant is used to control insect pests in southern China. BioScience 37:665–671CrossRefGoogle Scholar
  27. Ito F, Higashi S (1991) An indirect mutualism between oaks and wood ants via aphids. J Anim Ecol 60:463–470CrossRefGoogle Scholar
  28. Jeanne RL (1979) A latitudinal gradient in rates of ant predation. Ecology 60:1211–1224CrossRefGoogle Scholar
  29. Karban R (2007) Deciduous leaf drop reduces insect herbivory. Oecologia 153:81–88PubMedCrossRefGoogle Scholar
  30. Karban R, Baldin IT (1997) Induced response to herbivory. Univ Chicago Press, ChicagoGoogle Scholar
  31. Laine LJ, Niemelä P (1980) The influence of ants on the survival of mountain birches during an Oporinia autumnata (Lep., Geometridae) outbreak. Oecologia 47:39–42CrossRefGoogle Scholar
  32. Lee DW, Gould KS (2002a) Anthocyanins in leaves and other vegetative organs: an introduction. Adv Bot Res 37:1–16CrossRefGoogle Scholar
  33. Lee DW, Gould KS (2002b) Why leaves turn red. Amer Sci 90:524–531Google Scholar
  34. Leimu R, Koricheva J (2006) A meta-analysis of genetic correlations between plant resistances to multiple enemies. Amer Natur 168:E15–E37CrossRefGoogle Scholar
  35. Lev-Yadun S, Dafni A, Flaishman MA, Izhaki I, Katzir G, Ne’eman G (2004) Plant coloration undermines herbivorous insect camouflage. BioEssays 26:1126–1130PubMedCrossRefGoogle Scholar
  36. Lev-Yadun S, Gould KS (2007) What do red and yellow autumn leaves signal? Bot Rev 73:279–289Google Scholar
  37. Matile P (2000) Biochemistry of Indian summer: physiology of autumnal leaf coloration. Exp Gerontol 35:145–158PubMedCrossRefGoogle Scholar
  38. Merzlyak WN, Gitelson A (1995) Why and what for the leaves are yellow in autumn? On the interpretation of optical spectra of senescing leaves (Acer platanoides L.). J Plant Physiol 145:315–320Google Scholar
  39. Moritsu M (1982) Aphids of Japan in colour. Zenkoku-noson-kyoiku-kyokai, TokyoGoogle Scholar
  40. Ohgushi T (2005) Indirect interaction webs: herbivore-induced effects through trait change in plants. Annu Rev Ecol Evol Syst 36:81–105CrossRefGoogle Scholar
  41. Ougham HJ, Morris P, Thomas H (2005) The colors of autumn leaves as symptoms of cellular recycling and defences against environmental stresses. Curr Top Dev Biol 66:135–160PubMedCrossRefGoogle Scholar
  42. Price PW, Cobb N, Craig TP, Fernandes GW, Itami JK, Mopper S, Preszler RW (1990) Insect herbivore population dynamics on trees and shrubs: new approaches relevant to latent and eruptive species and life table development. In: Bernays EA (ed) Insect-plant interactions. vol. 2. CRC, Boca Raton, pp 1–38Google Scholar
  43. Rolshausen G, Schaefer HM (2007) Do aphids paint the tree red (or yellow)—can herbivore resistance or photoprotection explain colourful leaves in autumn? Plant Ecol 191:77–84CrossRefGoogle Scholar
  44. Sakata H (1994) How an ant decides to prey on or to attend aphids. Res Popul Ecol 36:45–51CrossRefGoogle Scholar
  45. Sakata H (1995) Density-dependent predation of the ant Lasius niger (Hymenoptera: Formicidae) on two attended aphids Lachnus tropicalis and Myzocallis kuricola (Homoptera: Aphididae). Res Popul Ecol 37:159–164CrossRefGoogle Scholar
  46. Schaefer HM, Wilkinson DM (2004) Red leaves, insects and coevolution: a red herring? Trend Ecol Evol 19:616–618CrossRefGoogle Scholar
  47. Schaefer HM, Rolshausen G (2006) Plants on red alert: do insects pay attention? BioEssays 28:65–71PubMedCrossRefGoogle Scholar
  48. Schmidt MH, Lauer A, Purtauf T, Thies C, Schaefer M, Tscharntke T (2003) Relative importance of predators and parasitoids for cereal aphid control. Proc Roy Soc Lond B 270:1905–1909CrossRefGoogle Scholar
  49. Schoonhoven LM, Jermy T, van Loon B (1997) Insect–plant biology: from physiology to evolution. Routledge, LondonGoogle Scholar
  50. Sinkkonen A (2006) Do autumn leaf colours serve as a reproductive insurance against sucking herbivores. Oikos 113:557–562CrossRefGoogle Scholar
  51. Skinner GJ, Whittaker JB (1981) An experimental investigation of inter-relationships between the wood-ant (Formica rufa) and some tree-canopy herbivores. J Anim Ecol 50:313–326CrossRefGoogle Scholar
  52. Stadler B, Dixon AFG (1999) Ant attendance in aphids: why different degrees of myrmecophily? Ecol Entomol 24:363–369CrossRefGoogle Scholar
  53. Stadler B, Dixon AFG (2005) Ecology and evolution of aphid-ant interactions. Annu Rev Ecol Evol Syst 36:345–372CrossRefGoogle Scholar
  54. Stiles EW (1982) Fruit flags: two hypotheses. Amer Natur 120:500–509CrossRefGoogle Scholar
  55. Strauss SY, Irwin RE (2004) Ecological and evolutionary consequences of multispecies plant–animal interactions. Annu Rev Ecol Evol Syst 35:435–466CrossRefGoogle Scholar
  56. Takabayashi J, Dicke M (1996) Plant–carnivore mutualism through herbivore-induced carnivore attractants. Trend Plant Sci 1:109–113CrossRefGoogle Scholar
  57. van Veen FJF, Morris RJ, Godfray HCJ (2006) Apparent competition, quantitative food webs, and the structure of phytophagous insect communities. Annu Rev Entomol 51:187–208PubMedCrossRefGoogle Scholar
  58. Way MJ (1963) Mutualism between ants and honeydew-producing Homoptera. Annu Rev Entomol 8:307–344CrossRefGoogle Scholar
  59. Wilkinson DM, Sherratt TN, Phillip DM, Wratten SD, Dixon AFG, Young AJ (2002) The adaptive significance of autumn leaf colours. Oikos 99:402–407CrossRefGoogle Scholar
  60. Wratten SD (1974) Aggregation in the birch aphid Euceraphis punctipennis (Zett.) in relation to food quality. J Anim Ecol 43:191–198CrossRefGoogle Scholar
  61. Yamamura N (2007) Conditions under which plants help herbivores and benefit from predators through apparent competition. Ecology 88:1593–1599PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  1. 1.Osaka City Institute of Public Health and Environmental SciencesOsakaJapan

Personalised recommendations