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Journal of Chemical Ecology

, 35:1349 | Cite as

Diversity of the Volatile Organic Compounds Emitted by 55 Species of Tropical Trees: a Survey in French Guiana

  • Elodie A. CourtoisEmail author
  • C. E. Timothy Paine
  • Pierre-Alain Blandinieres
  • Didier Stien
  • Jean-Marie Bessiere
  • Emeline Houel
  • Christopher Baraloto
  • Jerome Chave
Article

Abstract

Volatile organic compounds (VOCs) are produced by a broad range of organisms, from bacteria to mammals, and they represent a vast chemical diversity. In plants, one of the preeminent roles of VOCs is their repellent or cytotoxic activity, which helps the plant deter its predators. Most studies on VOCs emitted by vegetative parts have been conducted in model plant species, and little is known about patterns of VOC emissions in diverse plant communities. We conducted a survey of the VOCs released immediately after mechanical damage of the bark and the leaves of 195 individual trees belonging to 55 tropical tree species in a lowland rainforest of French Guiana. We discovered a remarkably high chemical diversity, with 264 distinct VOCs and a mean of 37 compounds per species. Two monoterpenes (α-pinene and limonene) and two sesquiterpenes (β-caryophyllene and α-copaene), which are known to have cytotoxic and deterrent effects, were the most frequent compounds in the sampled species. As has been established for floral scents, the blend of VOCs is largely species-specific and could be used to discriminate among 43 of the 55 sampled species. The species with the most diverse blends were found in the Sapindales, Laurales, and Magnoliales, indicating that VOC diversity is not uniformly distributed among tropical species. Interspecific variation in chemical diversity was caused mostly by variation in sesquiterpenes. This study emphasizes three aspects of VOC emission by tropical tree species: the species-specificity of the mixtures, the importance of sesquiterpenes, and the wide-ranging complexity of the mixtures.

Keywords

VOCs Chemical diversity Sesquiterpenes Tropical French Guiana 

Notes

Acknowledgements

We thank all participants of the BRIDGE project, Antoine Stevens and the Institut Pasteur of French Guiana in Cayenne for providing laboratory facilities, Pascal Petronelli for help in the field, Julien Engel for help in the validation of the protocol, Bruno Buatois for providing the alkane blend, and Martine Hossaert-McKey, Kyle G. Dexter, A. E. Hagerman and two anonymous reviewers for useful comments at several stages of the writing of this manuscript. This work is a contribution of the BRIDGE project, funded by the Agence Nationale pour la Recherche (ANR-Biodiversité program).

References

  1. AGRAWAL, A. A. and FISHBEIN, M. 2006. Plant defense syndromes. Ecology 87:132–149.CrossRefGoogle Scholar
  2. AKHTAR, Y. and ISMAN, M. B. 2003. Binary mixtures of feeding deterrents mitigate the decrease in feeding deterrent response to antifeedants following prolonged exposure in the cabbage looper, Trichoplusia ni (Lepidoptera: Noctuidae). Chemoecology 13:177–182.CrossRefGoogle Scholar
  3. BAKKALI, F., AVERBECK, S., AVERBECK, D., and IDAOMAR, M. 2008. Biological effects of essential oils: a review. Food Chem. Toxicol. 46:446–475.CrossRefPubMedGoogle Scholar
  4. BANCHIO, E., ZYGADLO, J., and VALLADARES, G. R. 2005. Effects of mechanical wounding on essential oil composition and emission of volatiles from Minthostachys mollis. J. Chem. Ecol. 31:719–727.CrossRefPubMedGoogle Scholar
  5. BARALOTO, C., PAINE, C. E. T., PATINÕ, S., BONAL, D., HÉRAULT, B., and CHAVE, J. 2009. Functional trait variation and sampling strategies in species-rich plant communities. Funct. Ecol. in press.Google Scholar
  6. BERENBAUM, M. and NEAL, J. J. 1985. Synergism between myristicin and xanthotoxin, a naturally cooccurring plant toxicant. J. Chem. Ecol. 11:1349–1358.CrossRefGoogle Scholar
  7. BORGES, R. M., BESSIÈRE, J.-M., and HOSSAERT-MCKEY, M. 2008. The chemical ecology of seed dispersal in monoecious and dioecious figs. Funct. Ecol. 22:484–493.CrossRefGoogle Scholar
  8. BOUVIER-BROWN, N. C., HOLZINGER, R., PALITZSCH, K., and GOLDSTEIN, A. H. 2007. Quantifying sesquiterpene and oxygenated terpene emissions from live vegetation using solid-phase microextraction fibers. J. Chrom. A 1161:113–120.CrossRefGoogle Scholar
  9. COLEY, P. D. and AIDE, M. T. 1991. Comparison of herbivory and plant defenses in temperate and tropical broad-leaved forests, pp. 25–49, in P. W. Price, T. M. Lewinsohn, G. W. Fernandes, and W. W. Benson (eds.). Plant–Animal Interactions: Evolutionary Ecology in Tropical and Temperate Regions. Wiley, New York.Google Scholar
  10. DE MORAES, C. M., MESCHER, M. C., and TUMLINSON, J. H. 2001. Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410:577–580.CrossRefPubMedGoogle Scholar
  11. DUDAREVA, N., NEGRE, F., NAGEGOWDA, D. A., and ORLOVA, I. 2006. Plant volatiles: Recent advances and future perspectives. Crit. Rev. Plant Sci. 25: 417–440.CrossRefGoogle Scholar
  12. FINE, P. V. A., MILLER, Z. J., MESONES, I., IRAZUZTA, S., APPEL, H. M., STEVENS, M. H. H., SÄÄKSJÄRVI, I., SCHULTZ, J. C., and COLEY, P. D. 2006. The growth-defense trade-off and habitat specialization by plants in amazonian forests. Ecology 87:150–162.CrossRefGoogle Scholar
  13. FIRN, R. D. and JONES, C. G. 2003. Natural products, a simple model to explain chemical diversity. Nat. Prod. Rep. 20:382–391.CrossRefPubMedGoogle Scholar
  14. FRAENKEL, G. S. 1959. The raison d’etre of secondary plant substances. Science 129:1466–1470.CrossRefPubMedGoogle Scholar
  15. GERSHENZON, J. and DUDAREVA, N. 2007. The function of terpene natural products in the natural world. Nat. Chem. Biol. 3:408–414.CrossRefPubMedGoogle Scholar
  16. GOLS, R., WITJES, L. M. A., VAN LOON, J. J. A., POSTHUMUS, M. A., DICKE, M., and HARVEY, J. A. 2008. The effect of direct and indirect defenses in two wild brassicaceous plant species on a specialist herbivore and its gregarious endoparasitoid. Entomol. Exp. Appl. 128:99–108.CrossRefGoogle Scholar
  17. GREENBERG, J. P., GUENTHER, A. B., PETRON, G., WIEDINMYER, C., VEGA, O., GATTI, L. V., TOTA, J., and FISCH, G. 2004. Biogenic VOC emissions from forested Amazonian landscapes. Global Change Biol. 10:651–662.CrossRefGoogle Scholar
  18. GUENTHER, A. 2002. The contribution of reactive carbon emissions from vegetation to the carbon balance of terrestrial ecosystems. Chemosphere 49:837–844.CrossRefPubMedGoogle Scholar
  19. GUO, F. Q., HUANG, L. F., ZHOU, S. Y., ZHANG, T. M., and LIANG, Y. Z. 2006. Comparison of the volatile compounds of Atractylodes medicinal plants by headspace solid-phase microextraction-gas chromatography-mass spectrometry. Anal. Chim. Acta 570: 73–78.CrossRefGoogle Scholar
  20. HARTMANN, T. 2007. From waste products to ecochemicals: Fifty years research of plant secondary metabolism. Phytochemistry 68:2831–2846.CrossRefPubMedGoogle Scholar
  21. HEIL, M. 2004. Direct defense or ecological costs: responses of herbivorous beetles to volatiles released by wild lima bean (Phaseolus lunatus). J. Chem. Ecol. 30:1289–1295.CrossRefPubMedGoogle Scholar
  22. HEIL, M. 2008. Indirect defence via tritrophic interactions. New Phytol. 178: 41–61.CrossRefPubMedGoogle Scholar
  23. JANZEN, D. H. 1970. Herbivores and the number of tree species in tropical forests. Am. Nat. 104:501–528.CrossRefGoogle Scholar
  24. JONES, C. G. and FIRN, R. D. 1991. On the evolution of plant secondary chemical diversity. Phil. Trans. R. Soc. Lond. B. 333:273–280.CrossRefGoogle Scholar
  25. KEELING, C. I. and BOHLMANN, J. 2006. Genes, enzymes and chemicals of terpenoid diversity in the constitutive and induced defence of conifers against insects and pathogens. New Phytol. 170:657–675.CrossRefPubMedGoogle Scholar
  26. KESSELMEIER, J. and STAUDT, M. 1999. Biogenic volatile organic compounds (VOC): An overview on emission, physiology and ecology. J. Atm. Chem. 33: 23–88.CrossRefGoogle Scholar
  27. KNUDSEN, J. T., ERIKSSON, R., GERSHENZON, J., and STAHL, B. 2006. Diversity and distribution of floral scent. Bot. Rev. 72, 1–120.CrossRefGoogle Scholar
  28. KÖLLNER, T. G., HELDB, M., LENK, C., HILTPOLD, I., TURLINGS, T. C. J., GERSHENZON, J., and DEGENHARDT, J. 2008. A maize (E)-b-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most American maize varieties. Plant Cell 20: 482–494.CrossRefPubMedGoogle Scholar
  29. KOVATS, E. 1958. Gas-chromatographische charakterisierung organischer verbindungen. teil 1: Retentionsindices aliphatischer halogenide, alkohole, aldehyde und ketone. Helv. Chim. Acta 41:1915–1932.CrossRefGoogle Scholar
  30. LEWINSOHN, T. M. and ROSLIN, T. 2008. Four ways towards tropical herbivore megadiversity. Ecology Lett. 11: 398–416.CrossRefGoogle Scholar
  31. LORD, H. and PAWLISZYN, J. 2000. Evolution of solid-phase microextraction technology. J. Chrom. A 885:153–193.CrossRefGoogle Scholar
  32. MATTIACCI, L., DICKE, M., and POSTHUMUS, M. A. 1995. B-Glucosidase: An elicitor of herbivore induced plant odor that attracts host-searching parasitic wasps. Proc. Natl. Acad. Sci. U.S.A. 92:2036–2040.CrossRefPubMedGoogle Scholar
  33. MAYER, V., SCHABER, D., and HADACEK, F. 2008. Volatiles of myrmecophytic Piper plants signal stem tissue damage to inhabiting Pheidole ant-partners. J. Ecol. 96:962–970.CrossRefGoogle Scholar
  34. MCKEY, D. 1979. The distribution of secondary compounds within plants, pp. 55–133, in G. A. Rosenthal and D. H. Janzen (eds.). Herbivores, Their Interactions with Secondary Plant Constituents. Academic, New York.Google Scholar
  35. MIRESMAILLI, S., BRADBURY, R., and ISMAN, M. B. 2006. Comparative toxicity of Rosmarinus officinalis L. essential oil and blends of its major constituents against Tetranychus urticae Koch (Acari: Tetranychidae) on two different host plants. Pest. Manag. Sci. 62:366–371.CrossRefPubMedGoogle Scholar
  36. MITHÖFER, A., WANNER, G., and BOLAND, W. 2005. Effects of feeding Spodoptera littoralis on lima bean leaves. II. Continuous mechanical wounding resembling insect feeding is sufficient to elicit herbivory-related volatile emission. Plant Physiol. 137: 1160–1168.CrossRefPubMedGoogle Scholar
  37. MUMM, R. and HILKER, M. 2006. Direct and indirect chemical defence of pine against folivorous insects. Trends Plant Sci. 11:351–358.CrossRefPubMedGoogle Scholar
  38. NOVOTNY, V., DROZD, P., MILLER, S. E., KULFAN, M., JANDA, M., BASSET, Y., and WEIBLEN, G. D. 2006. Why are there so many species of herbivorous insects in tropical rainforests? Science 313:1115–1118.CrossRefPubMedGoogle Scholar
  39. OZEKI, A., HITOTSUYANAGI, Y., HASHIMOTO, E., ITOKAWA, H., TAKEYA, K., and DE MELLO ALVES, S. 1998. Cytotoxic quassinoids from Simaba cedron. J. Nat. Prod. 61:776–780.CrossRefPubMedGoogle Scholar
  40. PICHERSKY, E. and GERSHENZON, J. 2002. The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Curr. Opin. Plant Biol. 5, 237–243. CrossRefPubMedGoogle Scholar
  41. RAGUSO, R. A. 2008. Wake Up and Smell the Roses: The ecology and evolution of floral scent. Annu. Rev. Ecol. Evol. Syst. 39:549–69.CrossRefGoogle Scholar
  42. ROUSSEEUW, P. J. 1987. Silhouettes: A graphical aid to the interpretation and validation of cluster analysis. J. Comput. Appl. Math. 20:53–65.CrossRefGoogle Scholar
  43. SUZUKI, R. and SHIMODAIRA, H. 2006. Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 22:1540–1542.CrossRefPubMedGoogle Scholar
  44. THOLL, D., BOLAND, W., HANSEL, A., LORETO, F., RÖSE, U. S. R., and SCHNITZLER, J. P. 2006. Practical approaches to plant volatile analysis. Plant J. 45: 540–560.CrossRefPubMedGoogle Scholar
  45. TURLINGS, T. C. J. and WÄCKERS, F. 2004. Recruitment of predators and parasitoids by herbivore-injured plants, pp 21–75, in R. T. Carde and J. G. Millar (eds.). Advances in Insect Chemical Ecology. Cambridge University.Google Scholar
  46. VICKERS, C. E., GERSHENZON, J., LERDAU, M. T., AND LORETO, F. 2009. A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Nat. Chem. Biol. 5:283–291.CrossRefPubMedGoogle Scholar
  47. WAJS, A., PRANOVICH, A., REUNANEN, M., WILLFÖR, S., and HOLMBOM, B. 2006. Characterisation of volatile organic compounds in stemwood using solid-phase microextraction. Phytochem. Anal. 17: 91–101.CrossRefPubMedGoogle Scholar
  48. WARD, J. H. 1963. Hierarchical grouping to optimize an objective function. J. Am. Stat. Assoc. 58: 236–244.CrossRefGoogle Scholar
  49. WINK, M. 2003. Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. Phytochemistry 64:3–19.CrossRefPubMedGoogle Scholar
  50. WINK, M. 2006. Importance of plant secondary metabolites for protection against insect and microbial infections, pp 251–268, in M. Rai and M. Carpinella (eds.). Naturally Occurring Bioactive Compounds. Elsevier, Amsterdam.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Elodie A. Courtois
    • 1
    • 2
    Email author
  • C. E. Timothy Paine
    • 5
  • Pierre-Alain Blandinieres
    • 2
  • Didier Stien
    • 2
  • Jean-Marie Bessiere
    • 4
  • Emeline Houel
    • 2
  • Christopher Baraloto
    • 3
  • Jerome Chave
    • 1
  1. 1.Laboratoire Evolution et Diversité BiologiqueUMR 5174 CNRS/Université Paul SabatierToulouseFrance
  2. 2.CNRSUMR EcofogCayenneFrance
  3. 3.INRAUMR EcofogKourou CedexFrance
  4. 4.UMR 5076École Nationale Supérieure de ChimieMontpellierFrance
  5. 5.ENGREFUMR EcofogKourou CedexFrance

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