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Ozone Degrades Common Herbivore-Induced Plant Volatiles: Does This Affect Herbivore Prey Location by Predators and Parasitoids?

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Abstract

Inducible terpenes and lipoxygenase pathway products, e.g., green-leaf volatiles (GLVs), are emitted by plants in response to herbivory. They are used by carnivorous arthropods to locate prey. These compounds are highly reactive with atmospheric pollutants. We hypothesized that elevated ozone (O3) may affect chemical communication between plants and natural enemies of herbivores by degrading signal compounds. In this study, we have used two tritrophic systems (Brassica oleraceaPlutella xylostellaCotesia plutellae and Phaseolus lunatusTetranychus urticaePhytoseiulus persimilis) to show that exposure of plants to moderately enhanced atmospheric O3 levels (60 and 120 nl l−1) results in complete degradation of most herbivore-induced terpenes and GLVs, which is congruent with our hypothesis. However, orientation behavior of natural enemies was not disrupted by O3 exposure in either tritrophic system. Other herbivore-induced volatiles, such as benzyl cyanide, a nitrile in cabbage, and methyl salicylate in lima bean, were not significantly reduced in reactions with O3. We suggest that more atmospherically stable herbivore-induced volatile compounds can provide important long-distance plant-carnivore signals and may be used by natural enemies of herbivores to orientate in O3-polluted environments.

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References

  • Agelopoulos, N. G. and Keller, M. A. 1994. Plant–natural enemy association in tritrophic system, Cotesia rubeculaPieris rapae–Brassicaceae (Cruciferae). III: Collection and identification of plant and frass volatiles. J. Chem. Ecol. 20:1955–1967.

    Article  CAS  Google Scholar 

  • Agrell, J., Kopper, B., Mc Donald, E. P., and Lindroth, R. L. 2005. CO2 and O3 effects on host plant preferences of the forest tent caterpillar (Malacosoma disstria). Glob. Change Biol. 11:588–599.

    Article  Google Scholar 

  • Atkinson, R. and Arey, J. 2003. Gas-phase tropospheric chemistry of biogenic volatile organic compounds: a review. Atmos. Environ. 37:S197–S219.

    Article  CAS  Google Scholar 

  • Baldwin, I. T., Halitschke, R., Paschold, A., Von Dahl, C. C., and Preston, C. A. 2006. Volatile signaling in plant–plant interactions: “Talking trees” in the genomics era. Science 311:812–815.

    Article  PubMed  CAS  Google Scholar 

  • Bruce, T. J. A., Wadhams, L. J., and Woodcock, C. M. 2005. Insect host location: a volatile situation. Trends Plant Sci. 10:269–274.

    Article  PubMed  CAS  Google Scholar 

  • Calogirou, A., Larsen, B. R., Brussol, C., Duane, M., and Kotzias, D. 1996. Decomposition of terpenes by ozone during sampling on Tenax. Anal. Chem. 68:1499–1506.

    Article  CAS  Google Scholar 

  • Calogirou, A., Larsen, B. R., and Kotzias, D. 1999. Gas-phase terpene oxidation products: a review. Atmos. Environ. 33:1423–1439.

    Article  CAS  Google Scholar 

  • Cameron, P. J. and Walker, G. P. 1997. Host specificity of Cotesia rubecula and Cotesia plutellae, parasitoids of white butterfly and diamondback moth. Proc. NZ Plant Prot Conf. 50:236–241.

    Google Scholar 

  • Canosa-Mas, C. E., Duffy, J. M., King, M. D., Thompson, K. C., and Wayne, R. P. 2002. The atmospheric chemistry of methyl salicylate—reactions with atomic chlorine and with ozone. Atmos. Environ. 36:2201–2205.

    Article  CAS  Google Scholar 

  • Coleman, J. S. and Jones, C. G. 1988. Plant stress and insect performance: cottonwood, ozone and a leaf beetle. Oecologia 76:57–61.

    Google Scholar 

  • De Boer, J. G. and Dicke, M. 2005. Information use by the predatory mite Phytoseiulus persimilis (Acari: Phytoseiidae), a specialised natural enemy of herbivorous spider mites. Appl. Entomol. Zool. 40:1–12.

    Article  Google Scholar 

  • De Boer, J. G., Posthumus, M. A., and Dicke, M. 2004. Identification of volatiles that are used in discrimination between plants infested with prey or nonprey herbivores by a predatory mite. J. Chem. Ecol. 30:2215–2230.

    Article  PubMed  Google Scholar 

  • Dicke, M. 1999. Evolution of induced indirect defence of plants, pp. 62–88, in R. Tollrian and C. D. Harvell (eds.). The Ecology and Evolution of Inducible Defenses. Princeton University Press, Princeton, New Jersey.

    Google Scholar 

  • Dicke, M. 2000. Chemical ecology of host–plant selection by herbivorous arthropods: a multitrophic perspective. Biochem. Syst. Ecol. 28:601–617.

    Article  PubMed  CAS  Google Scholar 

  • Dicke, M., Takabayashi, J., Posthumus, M. A., Schütte, C., and Krips, O. E. 1998. Plant–phytoseiid interactions mediated by herbivore-induced plant volatiles: variation in production of cues and in responses of predatory mites. Exp. Appl. Acarol. 22:311–333.

    Article  CAS  Google Scholar 

  • Gate, I. M., Mcneill, S., and Ashmore, M. R. 1995. Effects of air pollution on the searching behavior of an insect parasitoid. Water Air Soil Pollut. 85:1425–1430.

    Article  CAS  Google Scholar 

  • Holopainen, J. K. 2004. Multiple functions of inducible plant volatiles. Trends Plant Sci. 9:529–533.

    Article  PubMed  CAS  Google Scholar 

  • Holopainen, J. K., Kainulainen, P., and Oksanen, J. 1997. Growth and reproduction of aphids and levels of free amino acids in Scots pine and Norway spruce in an open-air fumigation with ozone. Glob. Change Biol. 3:139–147.

    Article  Google Scholar 

  • Holzinger, R., Lee, A., Paw, U. K. T., and Goldstein, A. H. 2005. Observations of oxidation products above a forest imply biogenic emissions of very reactive compounds. Atmos. Chem. Phys. 5:67–75.

    Article  CAS  Google Scholar 

  • Ibrahim, M. A., Nissinen, A., and Holopainen, J. K. 2005. The response of Plutella xylostella and its parasitoid Cotesia plutellae to volatile compounds. J. Chem. Ecol. 31:1969–1984.

    Article  PubMed  CAS  Google Scholar 

  • IPCC. 2001. Climate Change 2001: The Scientific Basis. Report of Working Group I of the Intergovernmental Panel on Climate Change, IPCC, Secretariat, Geneva, 2001). http://www.ipcc.ch/pub/spm22-01.pdf.

  • Jøndrup, P. M., Barnes, J. D., and Port, G. R. 2002. The effect of ozone fumigation and different Brassica rapa lines on the feeding behavior of Pieris brassicae larvae. Entomol. Exp. Appl. 104:143–151.

    Article  Google Scholar 

  • Joutsensaari, J., Loivamäki, M., Vuorinen, T., Miettinen, P., Nerg, A.-M., Holopainen, J. K., and Laaksonen, A. 2005. Nanoparticle formation by ozonloysis of inducible plant volatiles. Atmos. Chem. Phys. 5:1489–1495.

  • Kappers, I. F., Aharoni, A., Van Herpen, T. W. J. M., Luckerhoff, L. L. P., Dicke, M, and Bouwmeester, H. J. 2005. Genetic engineering of terpenoid metabolism attracts bodyguards to Arabidopsis. Science 309:2070–2072.

    Article  PubMed  CAS  Google Scholar 

  • Kesselmeier, J. and Staudt, M. 1999. Biogenic volatile organic compounds (VOC): an overview on emission, physiology and ecology. J. Atmos. Chem. 33:23–88.

    Article  CAS  Google Scholar 

  • Kopper, B. J. and Lindroth, R. L. 2003. Effects of elevated carbon dioxide and ozone on the phytochemistry of aspen and performance of an herbivore. Oecologia 134:95–103.

    Article  PubMed  Google Scholar 

  • Mattiacci, L., Dicke, M., and Posthumus, M. A. 1994. Induction of parasitoid attracting synomone in Brussels sprouts plants by feeding of Pieris brassicae larvae: role of mechanical damage and herbivore elicitor. J. Chem. Ecol. 20:2229–2247.

    Article  CAS  Google Scholar 

  • Owen, S. M. and Peñuelas, J. 2005. Opportunistic emissions of volatile isoprenoids. Trends Plant Sci. 10:420–426.

    Article  PubMed  CAS  Google Scholar 

  • Paré, P. W. and Tumlinson, J. H. 1999. Plant volatiles as a defense against insect herbivores. Plant Physiol. 121:325–331.

    Article  PubMed  Google Scholar 

  • Peñuelas, J. and Llusià, J. 2004. Plant VOC emissions: making use of the unavoidable. Trends Ecol. Evol. 19:402–404.

    Article  PubMed  Google Scholar 

  • Peñuelas, J., Filella, I., Stefanescu, C., and Llusià, J. 2005. Caterpillars of Euphydryas aurina (Lepidoptera: Nymphalidae) feeding on Succisa pratensis leaves induce large foliar emissions of methanol. New Phytol. 167:851–857.

    Article  PubMed  CAS  Google Scholar 

  • Potting, R. P. J., Poppy, G. M., and Schuler, T. H. 1999. The role of volatiles from cruciferous plants and pre-flight experience in the foraging behavior of the specialist parasitoid Cotesia plutellae. Entomol. Exp. Appl. 93:87–95.

    Article  CAS  Google Scholar 

  • Reddy, G. V. P., Holopainen, J. K., and Guerrero, A. 2002. Olfactory responses of Plutella xylostella natural enemies to host pheromone, larval frass, and green leaf cabbage volatiles. J. Chem. Ecol. 28:131–143.

    Article  PubMed  CAS  Google Scholar 

  • Scascighini, N., Mattiacci, L., D’Alessandro, M., Hern, A., Rott, A. S., and Dorn, S. 2005. New insights in analysing parasitoid attracting synomones: early volatile emission and use of stir bar sorptive extraction. Chemoecology 15:97–104.

    Article  Google Scholar 

  • Schnee, C., Köllner, T. G., Held, M., Turlings, T. C. J., Gershenzon, J., and Degenhardt, J. (2006). The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores. Proc. Natl. Acad. Sci. U S A 103:1129–1134.

    Article  PubMed  CAS  Google Scholar 

  • Schoonhoven, L., Van Loon, J. J. A., and Dicke, M. 2006. Insect–Plant Biology. Oxford University Press, UK.

    Google Scholar 

  • Shiojiri, K., Takabayashi, J., Yano, S., and Takafuji, A. 2001. Infochemically mediated tritrophic interaction webs on cabbage plants. Popul. Ecol. 43:23–29.

    Article  Google Scholar 

  • Smid, H. M., Van Loon, J. J. A., Posthumus, M. A., and Vet, L. E. M. 2002. GC-EAG-analysis of volatiles from Brussels sprouts plants damaged by two species of Pieris caterpillars: olfactory receptive range of a specialist and a generalist parasitoid wasp species. Chemoecology 12:169–176.

    Article  CAS  Google Scholar 

  • Tooker, J. F., Crumrin, A. L., and Hanks, L. M. 2005. Plant volatiles are behavioral cues for adult females of the gall wasp Antistrophus rufus. Chemoecology 15:85–88.

    Article  CAS  Google Scholar 

  • Turlings, T. C. J. and Wäckers, F. 2004. Recruitment of predators and parasitoids by herbivore-injured plants, pp. 21–75, in R. T. Cardé and J. G. Millar (eds.). Advances in Insect Chemical Ecology. Cambridge University Press, Cambridge.

    Google Scholar 

  • Ton, J., D’Alessandro, M., Jourdie, V., Jakab, G., Karlen, M., Held, M. Mauch-Mani, B., and Turlings, T. C. J. 2007. Priming by airborne signals boosts direct and indirect resistance in maize. Plant J. 49:16–26.

    Article  PubMed  CAS  Google Scholar 

  • Van Den Boom, C. E. M., Van Beek, T. A., Posthumus, M. A., De Groot, A., and Dicke, M. 2004. Qualitative and quantitative variation among volatile profiles induced by Tetranychus urticae feeding on plants from various families. J. Chem. Ecol. 3:69–89.

    Article  Google Scholar 

  • Von Dahl, C. C., Hävecker, M., Schlögl, R., and Baldwin, I. T. 2006. Caterpillar-elicited methanol emission: a new signal in plant–herbivore interactions? Plant J. 46:948–960.

    Article  CAS  Google Scholar 

  • Vuorinen, T., Nerg, A.-M., and Holopainen, J. K. 2004a. Ozone exposure triggers the emission of herbivore-induced plant volatiles, but does not disturb tritrophic signalling. Environ. Pollut. 131:305–311.

    Article  PubMed  CAS  Google Scholar 

  • Vuorinen, T., Nerg, A.-M., Ibrahim, M. A., Reddy, G. V. P., and Holopainen, J. K. 2004b. Emissions of Plutella xylostella-induced compounds from cabbage grown at elevated CO2 and orientation behavior of the natural enemies. Plant Physiol. 135:1–9.

    Article  Google Scholar 

  • Yu, J., Cocker III, D. R., Griffin, R. J., Flagan, R. C., and Seinfeld, J. H. 1999. Gas-phase ozone oxidation of monoterpenes: gaseous and particulate products. J. Atmos. Chem. 34:207–258.

    Article  CAS  Google Scholar 

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Acknowledgments

The authors thank Timo Oksanen for the assistance in the development of the setup used in the experiment. D.P., J.B., and J.K.H. are supported by ISONET, MRTN-CT-2003-504720, and J.K.H. and A-M.N. by the Academy of Finland (ESGEMO programme, decision no. 105209).

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Correspondence to Delia M. Pinto.

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Pinto, D.M., Blande, J.D., Nykänen, R. et al. Ozone Degrades Common Herbivore-Induced Plant Volatiles: Does This Affect Herbivore Prey Location by Predators and Parasitoids?. J Chem Ecol 33, 683–694 (2007). https://doi.org/10.1007/s10886-007-9255-8

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