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Science 16 March 2001:
Vol. 291. no. 5511, pp. 2141 - 2144
DOI: 10.1126/science.291.5511.2141

Reports

Defensive Function of Herbivore-Induced Plant Volatile Emissions in Nature

André Kessler, Ian T. Baldwin*

Herbivore attack is known to increase the emission of volatiles, which attract predators to herbivore-damaged plants in the laboratory and agricultural systems. We quantified volatile emissions from Nicotiana attenuata plants growing in natural populations during attack by three species of leaf-feeding herbivores and mimicked the release of five commonly emitted volatiles individually. Three compounds (cis-3-hexen-1-ol, linalool, and cis-alpha -bergamotene) increased egg predation rates by a generalist predator; linalool and the complete blend decreased lepidopteran oviposition rates. As a consequence, a plant could reduce the number of herbivores by more than 90% by releasing volatiles. These results confirm that indirect defenses can operate in nature.

Department of Molecular Ecology, Max-Planck-Institute for Chemical Ecology, Jena 07745, Germany.
*   To whom correspondence should be addressed. E-mail: baldwin{at}ice.mpg.de


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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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