Skip to main content

Floral Odor Bouquet Loses its Ant Repellent Properties After Inhibition of Terpene Biosynthesis

Abstract

In their natural environment, plants are synchronously confronted with mutualists and antagonists, and thus benefit from signals that contain messages for both functional groups of interaction partners. Floral scents are complex blends of volatiles of different chemical classes, including benzenoids and terpenoids. It has been hypothesized that benzenoids have evolved as pollinator attracting signals, while monoterpenoids serve as defensive compounds against antagonists. In order to test this hypothesis, we reduced terpene emission in flowers of Phlox paniculata with specific biosynthetic inhibitors and compared the responses of Lasius niger ants to natural and inhibited floral scent bouquets. While the natural odors were strongly repellent to ants, the bouquets with a reduced emission rate of terpenoids were not. The loss of the flowers’ ability to repel ants could be attributed predominantly to reduced amounts of linalool, a monoterpene alcohol. Flying flower visitors, mainly hoverflies, did not discriminate between the two types of flowers in an outdoor experiment. Since individual compounds appear to be capable of either attracting pollinators or defending the flower from enemies, the complexity of floral scent bouquets may have evolved to allow flowers to respond to both mutualists and antagonists simultaneously.

This is a preview of subscription content, access via your institution.

Fig. 1

References

  • Adams, R. P. 2007. Identification of Essential Oil Components by Gas Chromatography/Mass Spectrometry, 4th ed. Allured Publishing Corporation, Carol Stream, Illinois.

    Google Scholar 

  • Andersson, S., Nilsson, L. A., Groth, I., and Bergström, G. 2002. Floral scents in butterfly-pollinated plants: possible convergence in chemical composition. Bot. J. Linn. Soc. 140:129–153.

    Article  Google Scholar 

  • Berglund, A., Bisazza, A., and Pilastro, A. 1996. Armaments and ornaments: an evolutionary explanation of traits of dual utility. Biol. J. Linn. Soc. 58:385–399.

    Article  Google Scholar 

  • Bleil, R., Blüthgen, N., and Junker, R. R. 2011. Ant-plant mutualism in Hawaii? Invasive ants reduce flower parasitism but also exploit floral nectar of the endemic shrub Vaccinium reticulatum (Ericaceae). Pac. Sci. 65:291–300.

    Article  Google Scholar 

  • Breiman, L. 2001. Random forests. Mach. Learn 45:5–32.

    Article  Google Scholar 

  • Breiman, L. 2003. Manual--Setting Up, Using, And Understanding Random Forests V4.0. ftp://ftp.stat.berkeley.edu/pub/users/breiman//Using_random_forests_v4.0.pdf.

  • Cane, J. H. 1986. Predator deterrence by mandibular gland secretions of bees (Hymenoptera, Apoidea). J. Chem. Ecol. 12:1295–1309.

    Article  Google Scholar 

  • Cunningham, J. P., Moore, C. J., Zalucki, M. P., and West, S. A. 2004. Learning, odour preference and flower foraging in moths. J. Exp. Biol. 207:87–94.

    PubMed  Article  Google Scholar 

  • Dobson, H. E. M. 2006. Relationship between floral fragrance composition and type of pollinator. pp. 147-198 in Biology of Floral Scent (eds N. Dudareva and E. Pichersky). CRC Press, Boca Raton.

  • Dötterl, S., Jürgens, A., Seifert, K., Laube, T., Weissbecker, B., and Schütz, S. 2006. Nursery pollination by a moth in Silene latifolia: the role of odours in eliciting antennal and behavioural responses. New Phytol. 169:707–718.

    PubMed  Article  Google Scholar 

  • Dudareva, N., Andersson, S., Orlova, I., Gatto, N., Reichelt, M., Rhodes, D., Boland, W., and Gershenzon, J. 2005. The nonmevalonate pathway supports both monoterpene and sesquiterpene formation in snapdragon flowers. Proc. Natl. Acad. Sci. USA 102:933–938.

    PubMed  Article  CAS  Google Scholar 

  • DUDAREVA, N. and PICHERSKY, E. 2006. Biology of Floral Scent. CRC Press, Boca Raton, FL, USA.

    Google Scholar 

  • Galen, C. 1983. The effects of nectar thieving ants on seedset in floral scent morphs of Polemonium viscosum. Oikos 41:245–249.

    Article  Google Scholar 

  • Gershenzon, J. and Dudareva, N. 2007. The function of terpene natural products in the natural world. Nature Chem. Biol. 3:408–414.

    Article  CAS  Google Scholar 

  • Gomez, J. M. 2000. Effectiveness of ants as pollinators of Lobularia maritima: effects on main sequential fitness components of the host plant. Oecologia 122:90–97.

    Article  Google Scholar 

  • Gomez, J. M. and Zamora, R. 1992. Pollination by ants: consequences of quantitative effects on a mutualistic system. Oecologia 91:410–418.

    Article  Google Scholar 

  • Junker, R. R., Bleil, R., Daehler, C. C., and Blüthgen, N. 2010a. Intra-floral resource partitioning between endemic and invasive flower visitors: consequences for pollinator effectiveness. Ecol. Entomol. 35:760–767.

    Article  Google Scholar 

  • Junker, R. R. and Blüthgen, N. 2008. Floral scents repel potentially nectar-thieving ants. Evol. Ecol. Res. 10:295–308.

    Google Scholar 

  • Junker, R. R. and Blüthgen, N. 2010a. Dependency on floral resources determines the animals’ responses to floral scents. Plant Signal. Behav. 5:1014–1016.

    PubMed  Article  Google Scholar 

  • Junker, R. R. and Blüthgen, N. 2010b. Floral scents repel facultative flower visitors, but attract obligate ones. Ann. Bot. 105:777–782.

    PubMed  Article  Google Scholar 

  • Junker, R. R., Daehler, C. C., Dötterl, S., Keller, A., and Blüthgen, N. 2011a. Hawaiian ant-flower networks: nectar-thieving ants prefer undefended native over introduced plants with floral defenses. Ecol. Monogr. 81:295–311.

    Article  Google Scholar 

  • Junker, R. R., Höcherl, N., and Blüthgen, N. 2010b. Responses to olfactory signals reflect network structure of flower-visitor interactions. J. Anim. Ecol. 79:818–823.

    PubMed  Google Scholar 

  • Junker, R. R., Loewel, C., Gross, R., Dötterl, S., Keller, A., and Blüthgen, N. 2011b. Composition of epiphytic bacterial communities differs on petals and leaves. Plant Biol. 13:918–924.

  • Kessler, A. and Halitschke, R. 2009. Testing the potential for conflicting selection on floral chemical traits by pollinators and herbivores: predictions and case study. Funct. Ecol. 23:901–912.

    Article  Google Scholar 

  • Kessler, D. and Baldwin, I. T. 2007. Making sense of nectar scents: the effects of nectar secondary metabolites on floral visitors of Nicotiana attenuata. Plant J. 49:840–854.

    PubMed  Article  CAS  Google Scholar 

  • Kessler, D., Gase, K., and Baldwin, I. T. 2008. Field experiments with transformed plants reveal the sense of floral scents. Science 321:1200–1202.

    PubMed  Article  CAS  Google Scholar 

  • Kita, T., Brown, M. S., and Goldstein, J. L. 1980. Feedback-regulation of 3-hydroxy-3-methyglutaryl coenzyme a reductase in livers of mice treated with mevinolin, a competitive inhibitor of the reductase. J. Clin. Invest. 66:1094–1100.

    PubMed  Article  CAS  Google Scholar 

  • Knudsen, J. T., Eriksson, R., Gershenzon, J., and Stahl, B. 2006. Diversity and distribution of floral scent. Bot. Rev. 72:1–120.

    Article  Google Scholar 

  • Lach, L. 2005. Interference and exploitation competition of three nectar-thieving invasive ant species. Insect. Soc. 52:257–262.

    Article  Google Scholar 

  • Laloi, D., Bailez, O., Blight, M. M., Roger, B., Pham-Delegue, M.-H., and Wadhams, L. J. 2000. Recognition of complex odors by restrained and free-flying honeybees, Apis mellifera. J. Chem. Ecol. 26:2307–2319.

    Article  CAS  Google Scholar 

  • Mumm, R., Posthumus, M. A., and Dicke, M. 2008. Significance of terpenoids in induced indirect plant defence against herbivorous arthropods. Plant Cell Environ. 31:575–585.

    PubMed  Article  CAS  Google Scholar 

  • Pettersson, J. 1970. An aphid sex attractant. I. Biological studies. Entomol. Scand. 1:63–73.

    Article  Google Scholar 

  • Prasad, A. M., Iverson, L. R., and Liaw, A. 2006. Newer classification and regression tree techniques: Bagging and random forests for ecological prediction. Ecosystems 9:181–199.

    Article  Google Scholar 

  • R DEVELOPMENT CORE TEAM 2011. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.

    Google Scholar 

  • Raguso, R. A. 2008a. Start making scents: the challenge of integrating chemistry into pollination ecology. Entomol. Exp. Appl. 128:196–207.

    Article  CAS  Google Scholar 

  • Raguso, R. A. 2008b. Wake up and smell the roses: The ecology and evolution of floral scent. Annu. Rev. Ecol. Evol. Syst. 39:549–69.

    Article  Google Scholar 

  • Ranganathan, Y. and Borges, R. M. 2010. Reducing the babel in plant volatile communication: using the forest to see the trees. Plant Biol. 12:735–742.

    PubMed  Article  CAS  Google Scholar 

  • Reinhard, J., Sinclair, M., Srinivasan, M. V., and Claudianos, C. 2010. Honeybees learn odour mixtures via a selection of key odorants. PLoS One 5.

  • Riffell, J. A., Lei, H., Christensen, T. A., and Hildebrand, J. G. 2009. Characterization and coding of behaviorally significant odor mixtures. Curr. Biol. 19:335–340.

    PubMed  Article  CAS  Google Scholar 

  • Scanion, J. T. and Willis, D. E. 1985. Calculation of flame ionization detector relative response factors using the effective carbon number concept. J. Chromatogr. Sci. 23:333–340.

    Google Scholar 

  • Schie, C. C. N. V., Haring, M. A., and Schuurink, R. C. 2006. Regulation of terpenoid and benzenoid production in flowers. Curr. Opin. Plant Biol. 9:203–208.

    PubMed  Article  Google Scholar 

  • Schiestl, F. P. 2010. The evolution of floral scent and insect chemical communication. Ecol. Lett. 13:643–656.

    PubMed  Article  Google Scholar 

  • Schiestl, F. P., Huber, F. K., and Gomez, J. M. 2011. Phenotypic selection on floral scent: trade-off between attraction and deterrence? Evol. Ecol. 25:237–248.

    Article  Google Scholar 

  • Smith, B. H., Wright, G. A., and Daly, K. C. 2006. Learning-based recognition and discrimination of floral odors. pp. 263-296 in Biology of Floral Scent (eds N. Dudareva and E. Pichersky). CRC Press, Boca Raton.

  • Stringer, L. D., El-Sayed, A. M., Cole, L. M., Manning, L. A. M., and Suckling, D. M. 2008. Floral attractants for the female soybean looper, Thysanoplusia orichalcea (Lepidoptera: Noctuidae). Pest Manag. Sci. 64:1218–1221.

    PubMed  Article  CAS  Google Scholar 

  • Unsicker, S. B., Kunert, G., and Gershenzon, J. 2009. Protective perfumes: the role of vegetative volatiles in plant defense against herbivores. Curr. Opin. Plant Biol. 12:1–7.

    Article  Google Scholar 

  • Willmer, P. G., Nuttman, .C. V, Raine, N. E., Stone, G. N., Pattrick, J. G., Henson, K., Stillman, P., McIlroy, L., Potts, S. G., and Knudsen, J. T. 2009. Floral volatiles controlling ant behaviour. Funct. Ecol. 23:888–900.

    Article  Google Scholar 

  • Wright, G. A. and Schiestl, F. P. 2009. The evolution of floral scent: the influence of olfactory learning by insect pollinators on the honest signalling of floral rewards. Funct. Ecol. 23:841–851.

    Article  Google Scholar 

  • Yano, S. 1994. Flower nectar of an autogamous perennial Rorippa indica as an indirect defense-mechanism against herbivorous insects. Res. Popul. Ecol. 36:63–71.

    Article  Google Scholar 

Download references

Acknowledgement

We thank Michael Reichelt, Andrea Hilpert, Tamara Krügel, and Norbert Schneider for technical support and Klaus Lunau for helpful comments. The study was funded by the DFG and the Max-Planck Society.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Robert R. Junker.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Junker, R.R., Gershenzon, J. & Unsicker, S.B. Floral Odor Bouquet Loses its Ant Repellent Properties After Inhibition of Terpene Biosynthesis. J Chem Ecol 37, 1323–1331 (2011). https://doi.org/10.1007/s10886-011-0043-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-011-0043-0

Key Words

  • Biochemical pathways
  • Floral volatiles
  • Direct defense
  • Lasius niger
  • Olfactometer experiments
  • Phlox paniculata