Skip to main content
Log in

Why do many galls have conspicuous colors? A new hypothesis

  • Forum Paper
  • Published:
Arthropod-Plant Interactions Aims and scope Submit manuscript

Abstract

Galls are abnormal plant growth induced by various parasitic organisms, mainly insects. They serve as “incubators” for the developing insects in which they gain nutrition and protection from both abiotic factors and natural enemies. Galls are typically armed with high levels of defensive secondary metabolites. Conspicuousness by color, size and shape is a common gall trait. Many galls are colorful (red, yellow etc.) and therefore can be clearly distinguished from the surrounding host plant organs. Here we outlined a new hypothesis, suggesting that chemically protected galls which are also conspicuous are aposematic. We discuss predictions, alternative hypotheses and experimental tests of this hypothesis.

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.

Fig. 1

Similar content being viewed by others

References

  • Abrahamson WG, Sattler JF, McCrea KD, Weis AE (1989) Variation in selection pressures on the goldenrod gall fly and the competitive interactions of its natural enemies. Oecologia 79:15–22

    Article  Google Scholar 

  • Archetti M, Döring TF, Hagen SB, Hughes NM, Leather SR, Lee DW, Lev-Yadun S, Manetas Y, Ougham HJ, Schaberg PG et al (2009) Unraveling the evolution of autumn colours: an interdisciplinary approach. Trends Ecol Evol 24:166–173

    Article  PubMed  Google Scholar 

  • Atsatt PR, O’Dowd DJ (1976) Plant defense guilds. Science 193:24–29

    Article  PubMed  Google Scholar 

  • Blest AD (1963) Longevity, palatability and natural selection in five species of new world saturnid moth. Nature 197:1183–1186

    Article  Google Scholar 

  • Bowers DM (1993) Aposematic caterpillars: life-styles of the warningly colored and unpalatable. In: Stamp NE, Casey TM (eds) Caterpillars: ecological and evolutionary constraints on foraging. Chapman & Hall, New York, pp 331–371

    Google Scholar 

  • Briscoe AD, Chittka L (2001) The evolution of color vision in insects. Annu Rev Entomol 46:471–510

    Article  CAS  PubMed  Google Scholar 

  • Burstein M, Wool D (1992) Great tits exploit aphid galls as a source of food. Ornis Scand 23:107–109

    Article  Google Scholar 

  • Chittka L, Döring TF (2007) Are autumn foliage colors red signals to aphids? PLoS Biol 5(8):e187. doi:10.1371/journal.pbio.0050187

    Article  PubMed  Google Scholar 

  • Chittka L, Osorio DC (2007) Cognitive dimensions of predator responses to imperfect mimicry? PLoS Biol 5:e339. doi:10.1371/journal.pbio.0050339

    Article  PubMed  Google Scholar 

  • Chittka L, Raine NE (2006) Recognition of flowers by pollinators. Curr Opin Plant Biol 9:428–435

    Article  PubMed  Google Scholar 

  • Close DC, Beadle CL (2003) The ecophysiology of foliar anthocyanin. Bot Rev 69:149–161

    Article  Google Scholar 

  • Cornell HV (1983) The secondary chemistry and complex morphology of galls formed by the Cynipinae (Hymenoptera): why and how? Am Midl Nat 110:225–234

    Article  Google Scholar 

  • Cott HB (1940) Adaptive coloration in animals. Methuen, London

    Google Scholar 

  • Crespi B, Worobey M (1998) Comparative analysis of gall morphology in Australian gall thrips: the evolution of extended phenotypes. Evolution 52:1686–1696

    Article  Google Scholar 

  • Czeczuga B (1977) Carotenoids in leaves and their galls. Marcellia 40:177–180

    CAS  Google Scholar 

  • Dawkins R (1982) The extended phenotype. Oxford University Press, Oxford

    Google Scholar 

  • Dominy NJ, Lucas PE (2001) Ecological importance of trichromatic vision to primates. Nature 410:363–366

    Article  CAS  PubMed  Google Scholar 

  • Edmunds M (1974) Defences in animals. A survey of anti-predator defences. Longman, Harlow, Essex & NY

    Google Scholar 

  • Eisner T, Grant RP (1981) Toxicity, odor aversion, and “olfactory aposematism”. Science 213:476

    Article  CAS  PubMed  Google Scholar 

  • Fadzly N, Jack C, Schaefer HM, Burns KC (2009) Ontogenetic colour changes in an insular tree species: signalling to extinct browsing birds? New Phytol 184:495–501

    Article  PubMed  Google Scholar 

  • Gittleman JL, Harvey PH (1980) Why are distasteful prey not cryptic? Nature 286:149–150

    Article  Google Scholar 

  • Gould KS, Neill SO, Vogelmann TC (2002) A unified explanation for anthocyanins in leaves? Adv Bot Res 37:167–192

    Article  CAS  Google Scholar 

  • Guilford T, Nicol C, Rothschild M, Moore BP (1987) The biological roles of pyrazines: evidence for a warning odour function. Biol J Linn Soc 31:113–128

    Article  Google Scholar 

  • Hartley SE (1998) The chemical composition of plant galls: are levels of nutrients and secondary compounds controlled by the gall-former? Oecologia 113:492–501

    Article  Google Scholar 

  • Hill ME (2006) The effect of aposematic coloration on the food preference of Aphelocoma coerulescens, the Florida scrub jay. Bios J 77:97–106

    Article  Google Scholar 

  • Hill DA, Lucas PW, Cheng PY (1995) Bite forces by Japanese macaques (Macaca fuscata yakui) on Yakushima island, Japan to open aphid-induced galls on Distylium racemosum (Hamamelidaceae). J Zool 237:57–63

    Article  Google Scholar 

  • Hunter AF (2000) Gregariousness and repellent defences in the survival of phytophagous insects. Oikos 91:213–224

    Article  Google Scholar 

  • Inbar M, Eshel A, Wool D (1995) Interspecific competition among phloem-feeding insects mediated by induced host-plant sinks. Ecology 76:1506–1515

    Article  Google Scholar 

  • Inbar M, Wink M, Wool D (2004) The evolution of host plant manipulation by insects: molecular and ecological evidence from gall-forming aphids on Pistacia. Mol Phylogenet Evol 32:504–511

    Article  CAS  PubMed  Google Scholar 

  • Joel DM, Juniper BE, Dafni A (1985) Ultraviolet patterns in the traps of carnivorous plants. New Phytol 101:585–593

    Article  Google Scholar 

  • Knight RS, Siegfried WR (1983) Inter-relationships between type, size and color of fruits and dispersal in Southern African trees. Oecologia 56:405–412

    Article  Google Scholar 

  • Lee DW, Brammeler S, Smith AP (1987) The selective advantages of anthocyanins in developing leaves of mango and cacao. Biotropica 19:40–49

    Article  Google Scholar 

  • Lev-Yadun S (2001) Aposematic (warning) coloration associated with thorns in higher plants. J Theor Biol 210:385–388

    Article  CAS  PubMed  Google Scholar 

  • Lev-Yadun S (2003) Why do some thorny plants resemble green zebras? J Theor Biol 244:483–489

    Article  Google Scholar 

  • Lev-Yadun S (2009) Aposematic (warning) coloration in plants. In: Baluska F (ed) Plant-environment interactions. From sensory plant biology to active plant behavior. Springer-Verlag, Berlin, pp 167–202

    Google Scholar 

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

    Article  Google Scholar 

  • Lev-Yadun S, Dafni A, Flaishman MA, Inbar M, 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, Ne’eman G, Izhaki I (2009) Unripe red fruits may be aposematic. Plant Signaling Behav 4:836–841

    Google Scholar 

  • Mallet J, Joron M (1999) Evolution of diversity in warning color and mimicry: polymorphism, shifting balance, and speciation. Annu Rev Ecol Sys 30:201–233

    Article  Google Scholar 

  • Massei G, Cotterill JV, Coats JC, Bryning G, Cowan DP (2007) Can Batesian mimicry help plants to deter herbivory? Pest Manag Sci 63:559–563

    Article  CAS  PubMed  Google Scholar 

  • Nyman T, Julkunen-Titto RR (2000) Manipulation of the phenolic chemistry of willows by gall-inducing sawflies. Proc Natl Acad Sci USA 97:13184–13187

    Article  CAS  PubMed  Google Scholar 

  • Price PW, Fernandes WG, Waring GL (1987) Adaptive nature of insect galls. Environ Entomol 16:15–24

    Google Scholar 

  • Provenza FD, Kimball BA, Villalba JJ (2000) Roles of odor, taste, and toxicity in the food preferences of lambs: implications for mimicry in plants. Oikos 88:424–432

    Article  Google Scholar 

  • Raman A, Schaefer CA, Withers TM (2005) Biology, ecology, and evolution of gall-inducing arthropods. Science Publishers, USA

    Google Scholar 

  • Rothschild M (1986) The red smell of danger. New Sci 111:34–36

    Google Scholar 

  • Rubino DL, McCarthy BC (2004) Presence of aposematic (warning) coloration in vascular plants of southeastern Ohio. J Torrey Bot Soc 131:252–256

    Article  Google Scholar 

  • Russo RA (2007) Field guide to plant galls of California and other western states. University of California Press, Berkeley

    Google Scholar 

  • Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding attack: the evolutionary ecology of crypsis, warning signals and mimicry. Oxford University Press, Oxford

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Schaefer HM, Ruxton GD (2008) Fatal attraction: carnivorous plants roll out the red carpet to lure insects. Biol Lett 4:153–155

    Article  PubMed  Google Scholar 

  • Schaefer HM, Schmidt V (2004) Detectability and content as opposing signal characteristics in fruits. Proc Roy Soc Lond B 271(Suppl.):S370–S373

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Schonrogge K, Walker P, Crawely MJ (1999) Complex life cycles in Andricus kollari (Hymenoptera: Cynipidae) and their impact on associated parasitoids and inquilines species. Oikos 84:293–301

    Article  Google Scholar 

  • Shorthouse JD, Rohfritsch O (1992) The biology of insect-induced galls. Oxford University Press, Oxford

    Google Scholar 

  • Snow B, Snow D (1988) Birds and berries. A study of an ecological interaction. T. & A.D. Poyser, Calton

    Google Scholar 

  • Speed MP, Ruxton GD (2005) Warning displays in spiny animals: one (more) evolutionary route to aposematism. Evolution 59:2499–2508

    PubMed  Google Scholar 

  • Stone GN, Schonrogge K (2003) The adaptive significance of insect gall morphology. Trends Ecol Evol 18:512–522

    Article  Google Scholar 

  • Stone GN, Schonrogge K, Atkinson RJ, Bellido D, Pujade-Villar J (2002) The population biology of oak gall wasps (Hymenoptera: Cynipidae). Annu Rev Entomol 47:633–668

    Article  CAS  PubMed  Google Scholar 

  • Sumner P, Mollon JD (2000) Catarrhine photopigments are optimized for detecting targets against a foliage background. J Exp Biol 203:1963–1986

    CAS  PubMed  Google Scholar 

  • Vogel ER, Neitz M, Dominy NG (2006) Effect of color vision phenotype on the foraging of wild white-faced capuchins, Cebus capucinus. Behav Ecol 18:292–297

    Article  Google Scholar 

  • Weis AE, Walton R, Crego CL (1988) Reactive plant tissue sites and the population biology of gall makers. Annu Rev Entomol 33:467–486

    Article  Google Scholar 

  • Willson MF, Whelan CJ (1990) The evolution of fruit color in fleshy-fruited plants. Am Nat 136:790–809

    Article  Google Scholar 

  • Wool D (2004) Galling aphids: Specialization, biological complexity, and variation. Annu Rev Entomol 49:175–192

    Article  CAS  PubMed  Google Scholar 

  • Zamora R, Gómez JM (1993) Vertebrates herbivores as predators of insect herbivores: an asymmetrical interaction mediated by size differences. Oikos 66:223–228

    Article  Google Scholar 

Download references

Acknowledgments

We thank Martin Schaefer, Stig Larsson and anonymous referees for their critical suggestions and comments.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. Inbar.

Additional information

Handling Editor: Lars Chittka.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Inbar, M., Izhaki, I., Koplovich, A. et al. Why do many galls have conspicuous colors? A new hypothesis. Arthropod-Plant Interactions 4, 1–6 (2010). https://doi.org/10.1007/s11829-009-9082-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11829-009-9082-7

Keywords

Navigation