Skip to main content
Log in

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

  • Short Communication
  • Published:
Naturwissenschaften Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

References

  • Archetti M (2000) The origin of autumn colours by coevolution. J Theor Biol 205:625–630

    Article  PubMed  CAS  Google Scholar 

  • Archetti M, Brown S (2004) The coevolution theory of autumn colours. Proc Roy Soc Lond B 271:1219–1223

    Article  Google Scholar 

  • Archetti M, Leather SR (2005) A test of the coevolution theory of autumn colours: colour preference of Rhopalosiphum padi on Prunus padus. Oikos 110:339–343

    Article  Google Scholar 

  • Beattie AJ (1985) Evolutionary ecology of ant–plant mutualisms. Cambridge University Press, Cambridge

    Google Scholar 

  • Blackman RL, Eastop VF (1994) Aphids on the world’s trees. CAB, Wallingford

    Google Scholar 

  • Bristow CM (1991) Why are so few aphids ant-tended? In: Huxley CR, Cutler DF (eds) Ant–plant interactions. Oxford University Press, Oxford, pp 104–119

    Google Scholar 

  • Buckley RC (1987a) Interactions involving plants, Homoptera, and ants. Annu Rev Ecol Syst 18:111–135

    Article  Google Scholar 

  • Buckley RC (1987b) Ant–plant–homopteran interactions. Adv Ecol Res 16:53–85

    Article  Google Scholar 

  • Carter W (1962) Insects in relation to plant disease, 2nd edn. Wiley, New York

    Google Scholar 

  • Crawley MJ (1985) Reduction of oak fecundity by low-density herbivore populations. Nature 314:163–164

    Article  Google Scholar 

  • Delabie JHC (2001) Trophobiosis between Formicidae and Hemiptera (Sternorrhyncha and Auchenorrhyncha): an overview. Neotrop Entomol 30:501–516

    Article  Google Scholar 

  • 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 8:165–179

    Article  Google Scholar 

  • Dixon AFG (1998) Aphid ecology: an optimization approach, 2nd edn. Chapman and Hall, London

    Google Scholar 

  • Döring TM, Chittka L (2007) Visual ecology of aphids—a critical review on the role of colours in host finding. Arthropod–Plant Interactions 1:3–16

    Article  Google Scholar 

  • Fineblum WL, Rausher MD (1997) Do floral pigmentation and genes also influence resistance to enemies? The W locus in Ipomoea pupurea. Ecology 78:1646–1654

    Google Scholar 

  • Furuta K (1986) Host preference and population dynamics in an autumnal population of the maple aphid, Periphyllus californiensis Shinji (Homoptera, Aphididae). J Appl Entomol 102:93–100

    Article  Google Scholar 

  • 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 82:137–145

    Google Scholar 

  • 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 18:363–371

    Article  Google Scholar 

  • Gotelli NJ, Ellison AM (2002) Biogeography at a regional scale: determinants of ant species diversity in New England bogs and forests. Ecology 83:1604–1609

    Article  Google Scholar 

  • Gould KS (2004) Nature’s Swiss army knife: the diverse protective roles of anthocyanins in leaves. J Biomed Biotechnol 2004:314–320

    Article  PubMed  Google Scholar 

  • Gray SM, Rochon D (1999) Vector transmission of plant viruses. In: Granoff A, Webster RG (eds) Encyclopedia of virology. 2nd edn. Academic, London, pp 1899–1910

    Google Scholar 

  • 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)

    Article  Google Scholar 

  • Hamilton WD, Brown SP (2001) Autumn tree colours as a handicap signal. Proc Roy Soc Lond B 268:1489–1493

    Article  CAS  Google Scholar 

  • Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Quart Rev Biol 67:283–335

    Article  Google Scholar 

  • Holopainen JK, Peltonen P (2002) Bright autumn colours of deciduous trees attract aphids: nutrient retranslocation hypothesis. Oikos 99:184–188

    Article  Google Scholar 

  • Huang HT, Yang P (1987) The ancient cultured citrus ant: a tropical ant is used to control insect pests in southern China. BioScience 37:665–671

    Article  Google Scholar 

  • Ito F, Higashi S (1991) An indirect mutualism between oaks and wood ants via aphids. J Anim Ecol 60:463–470

    Article  Google Scholar 

  • Jeanne RL (1979) A latitudinal gradient in rates of ant predation. Ecology 60:1211–1224

    Article  Google Scholar 

  • Karban R (2007) Deciduous leaf drop reduces insect herbivory. Oecologia 153:81–88

    Article  PubMed  Google Scholar 

  • Karban R, Baldin IT (1997) Induced response to herbivory. Univ Chicago Press, Chicago

    Google Scholar 

  • Laine LJ, Niemelä P (1980) The influence of ants on the survival of mountain birches during an Oporinia autumnata (Lep., Geometridae) outbreak. Oecologia 47:39–42

    Article  Google Scholar 

  • Lee DW, Gould KS (2002a) Anthocyanins in leaves and other vegetative organs: an introduction. Adv Bot Res 37:1–16

    Article  CAS  Google Scholar 

  • Lee DW, Gould KS (2002b) Why leaves turn red. Amer Sci 90:524–531

    Google Scholar 

  • Leimu R, Koricheva J (2006) A meta-analysis of genetic correlations between plant resistances to multiple enemies. Amer Natur 168:E15–E37

    Article  Google Scholar 

  • Lev-Yadun S, Dafni A, Flaishman MA, Izhaki I, Katzir G, Ne’eman G (2004) Plant coloration undermines herbivorous insect camouflage. BioEssays 26:1126–1130

    Article  PubMed  Google Scholar 

  • Lev-Yadun S, Gould KS (2007) What do red and yellow autumn leaves signal? Bot Rev 73:279–289

    Google Scholar 

  • Matile P (2000) Biochemistry of Indian summer: physiology of autumnal leaf coloration. Exp Gerontol 35:145–158

    Article  PubMed  CAS  Google Scholar 

  • 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 145:315–320

    CAS  Google Scholar 

  • Moritsu M (1982) Aphids of Japan in colour. Zenkoku-noson-kyoiku-kyokai, Tokyo

    Google Scholar 

  • Ohgushi T (2005) Indirect interaction webs: herbivore-induced effects through trait change in plants. Annu Rev Ecol Evol Syst 36:81–105

    Article  Google Scholar 

  • 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 66:135–160

    Article  PubMed  CAS  Google Scholar 

  • 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 1–38

    Google Scholar 

  • 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 191:77–84

    Article  Google Scholar 

  • Sakata H (1994) How an ant decides to prey on or to attend aphids. Res Popul Ecol 36:45–51

    Article  Google Scholar 

  • 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 37:159–164

    Article  Google Scholar 

  • Schaefer HM, Wilkinson DM (2004) Red leaves, insects and coevolution: a red herring? Trend Ecol Evol 19:616–618

    Article  Google Scholar 

  • Schaefer HM, Rolshausen G (2006) Plants on red alert: do insects pay attention? BioEssays 28:65–71

    Article  PubMed  Google Scholar 

  • 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 270:1905–1909

    Article  Google Scholar 

  • Schoonhoven LM, Jermy T, van Loon B (1997) Insect–plant biology: from physiology to evolution. Routledge, London

    Google Scholar 

  • Sinkkonen A (2006) Do autumn leaf colours serve as a reproductive insurance against sucking herbivores. Oikos 113:557–562

    Article  Google Scholar 

  • 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 50:313–326

    Article  Google Scholar 

  • Stadler B, Dixon AFG (1999) Ant attendance in aphids: why different degrees of myrmecophily? Ecol Entomol 24:363–369

    Article  Google Scholar 

  • Stadler B, Dixon AFG (2005) Ecology and evolution of aphid-ant interactions. Annu Rev Ecol Evol Syst 36:345–372

    Article  Google Scholar 

  • Stiles EW (1982) Fruit flags: two hypotheses. Amer Natur 120:500–509

    Article  Google Scholar 

  • Strauss SY, Irwin RE (2004) Ecological and evolutionary consequences of multispecies plant–animal interactions. Annu Rev Ecol Evol Syst 35:435–466

    Article  Google Scholar 

  • Takabayashi J, Dicke M (1996) Plant–carnivore mutualism through herbivore-induced carnivore attractants. Trend Plant Sci 1:109–113

    Article  Google Scholar 

  • van Veen FJF, Morris RJ, Godfray HCJ (2006) Apparent competition, quantitative food webs, and the structure of phytophagous insect communities. Annu Rev Entomol 51:187–208

    Article  PubMed  CAS  Google Scholar 

  • Way MJ (1963) Mutualism between ants and honeydew-producing Homoptera. Annu Rev Entomol 8:307–344

    Article  Google Scholar 

  • Wilkinson DM, Sherratt TN, Phillip DM, Wratten SD, Dixon AFG, Young AJ (2002) The adaptive significance of autumn leaf colours. Oikos 99:402–407

    Article  Google Scholar 

  • Wratten SD (1974) Aggregation in the birch aphid Euceraphis punctipennis (Zett.) in relation to food quality. J Anim Ecol 43:191–198

    Article  Google Scholar 

  • Yamamura N (2007) Conditions under which plants help herbivores and benefit from predators through apparent competition. Ecology 88:1593–1599

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kazuo Yamazaki.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yamazaki, K. Autumn leaf colouration: a new hypothesis involving plant–ant mutualism via aphids. Naturwissenschaften 95, 671–676 (2008). https://doi.org/10.1007/s00114-008-0366-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00114-008-0366-z

Keywords

Navigation