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      Herbivore benefits from vectoring plant virus through reduction of period of vulnerability to predation

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          Abstract

          Herbivores can profit from vectoring plant pathogens because the induced defence of plants against pathogens sometimes interferes with the induced defence of plants against herbivores. Plants can also defend themselves indirectly by the action of the natural enemies of the herbivores. It is unknown whether the defence against pathogens induced in the plant also interferes with the indirect defence against herbivores mediated via the third trophic level. We previously showed that infection of plants with Tomato spotted wilt virus (TSWV) increased the developmental rate of and juvenile survival of its vector, the thrips Frankliniella occidentalis. Here, we present the results of a study on the effects of TSWV infections of plants on the effectiveness of three species of natural enemies of F. occidentalis: the predatory mites Neoseiulus cucumeris and Iphiseius degenerans, and the predatory bug Orius laevigatus. The growth rate of thrips larvae was positively affected by the presence of virus in the host plant. Because large larvae are invulnerable to predation by the two species of predatory mites, this resulted in a shorter period of vulnerability to predation for thrips that developed on plants with virus than thrips developing on uninfected plants (4.4 vs. 7.9 days, respectively). Because large thrips larvae are not invulnerable to predation by the predatory bug Orius laevigatus, infection of the plant did not affect the predation risk of thrips larvae from this predator. This is the first demonstration of a negative effect of a plant pathogen on the predation risk of its vector.

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          Defensive function of herbivore-induced plant volatile emissions in nature.

          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.
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            The Myriad Plant Responses to Herbivores.

            Walling (2000)
            Plant responses to herbivores are complex. Genes activated on herbivore attack are strongly correlated with the mode of herbivore feeding and the degree of tissue damage at the feeding site. Phloem-feeding whiteflies and aphids that produce little injury to plant foliage are perceived as pathogens and activate the salicylic acid (SA)-dependent and jasmonic acid (JA)/ethylene-dependent signaling pathways. Differential expression of plant genes in response to closely related insect species suggest that some elicitors generated by phloem-feeding insects are species-specific and are dependent on the herbivore's developmental stage. Other elicitors for defense-gene activation are likely to be more ubiquitous. Analogies to the pathogen-incompatible reactions are found. Chewing insects such as caterpillars and beetles and cell-content feeders such as mites and thrips cause more extensive tissue damage and activate wound-signaling pathways. Herbivore feeding is not equivalent to mechanical wounding. Wound responses are a part of the induced responses that accompany herbivore feeding. Herbivores induce direct defenses that interfere with herbivore feeding, growth and development, fecundity, and fertility. In addition, herbivores induce an array of volatiles that creates an indirect mechanism of defense. Volatile blends provide specific cues to attract herbivore parasites and predators to infested plants. The nature of the elicitors for volatile production is discussed.
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              Parasitic manipulation: where are we and where should we go?

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                Author and article information

                Contributors
                +34-96-3424102 , +34-96-3424001 , belliure@ivia.es
                Journal
                Oecologia
                Oecologia
                Springer-Verlag (Berlin/Heidelberg )
                0029-8549
                1432-1939
                8 April 2008
                July 2008
                : 156
                : 4
                : 797-806
                Affiliations
                [1 ]Institute for Biodiversity and Ecosystem Dynamics, Section Population Biology, University of Amsterdam, PO Box 94084, 1090 GB Amsterdam, The Netherlands
                [2 ]Valencian Institute for Agricultural Research, Associated Entomology Unit IVIA/CIB-CSIC/UJI, Center for Plant Protection and Biotechnology, Apartado Oficial, 46113 Moncada, Valencia Spain
                Author notes

                Communicated by Julia Koricheva.

                Article
                1027
                10.1007/s00442-008-1027-9
                2469278
                18392858
                0181e93c-fee6-462d-ba06-f89db561494f
                © The Author(s) 2008
                History
                : 18 June 2007
                : 7 March 2008
                : 7 March 2008
                Categories
                Plant-Animal Interactions - Original Paper
                Custom metadata
                © Springer-Verlag 2008

                Ecology
                prey size,frankliniella occidentalis,tritrophic interactions,preference,tomato spotted wilt virus

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