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      An herbivore-induced plant volatile reduces parasitoid attraction by changing the smell of caterpillars

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          Abstract

          A volatile emitted by attacked maize plants renders caterpillars less attractive and more resistant to parasitoids.

          Abstract

          Herbivore-induced plant volatiles (HIPVs) can mediate tritrophic interactions by attracting natural enemies of insect herbivores such as predators and parasitoids. Whether HIPVs can also mediate tritrophic interactions by influencing the attractiveness of the herbivores themselves remains unknown. We explored this question by studying the role of indole, a common HIPV in the plant kingdom. We found that herbivory-induced indole increases the recruitment of the solitary endoparasitoid Microplitis rufiventris to maize plants that are induced by Spodoptera littoralis caterpillars. Surprisingly, however, indole reduces parasitoid recruitment when the caterpillars themselves are present on the plants. Further experiments revealed that indole exposure renders S. littoralis caterpillars unattractive to M. rufiventris, leading to an overall reduction in attractiveness of plant-herbivore complexes. Furthermore, indole increases S. littoralis resistance and decreases M. rufiventris parasitization success. S. littoralis caterpillars are repelled by indole in the absence of M. rufiventris but specifically stop avoiding the volatile in the presence of the parasitoid. Our study shows how an HIPV can undermine tritrophic interactions by reducing the suitability and attractiveness of caterpillars to parasitoids.

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          Airborne signals prime plants against insect herbivore attack.

          Green leafy volatiles (GLV), six-carbon aldehydes, alcohols, and esters commonly emitted by plants in response to mechanical damage or herbivory, induced intact undamaged corn seedlings to rapidly produce jasmonic acid (JA) and emit sesquiterpenes. More importantly, corn seedlings previously exposed to GLV from neighboring plants produced significantly more JA and volatile sesquiterpenes when mechanically damaged and induced with caterpillar regurgitant than seedlings not exposed to GLV. The use of pure synthetic chemicals revealed that (Z)-3-hexenal, (Z)-3-hexen-1-ol, and (Z)-3-hexenyl acetate have nearly identical priming activity. Caterpillar-induced nocturnal volatiles, which are enriched in GLV, also exhibited a strong priming effect, inducing production of larger amounts of JA and release of greater quantities of volatile organic compounds after caterpillar regurgitant application. In contrast, GLV priming did not affect JA production induced by mechanical wounding alone. Thus, GLV specifically prime neighboring plants against impending herbivory by enhancing inducible chemical defense responses triggered during attack and may play a key role in plant-plant signaling and plant-insect interactions.
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            Caterpillar-induced nocturnal plant volatiles repel conspecific females.

            Plants respond to insect herbivory by synthesizing and releasing complex blends of volatile compounds, which provide important host-location cues for insects that are natural enemies of herbivores. The effects of these volatile blends on herbivore behaviour have been investigated to only a limited extent, in part because of the assumption that herbivore-induced volatile emissions occur mainly during the light phase of the photoperiod. Because many moths-whose larvae are some of the most important insect herbivores-are nocturnal, herbivore-induced plant volatiles have not hitherto been considered to be temporally available as host-location cues for ovipositing females. Here we present chemical and behavioural assays showing that tobacco plants (Nicotiana tabacum) release herbivore-induced volatiles during both night and day. Moreover, several volatile compounds are released exclusively at night and are highly repellent to female moths (Heliothis virescens). The demonstration that tobacco plants release temporally different volatile blends and that lepidopteran herbivores use induced plant signals released during the dark phase to choose sites for oviposition adds a new dimension to our understanding of the role of chemical cues in mediating tritrophic interactions.
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              Indirect defence via tritrophic interactions.

              Many plants interact with carnivores as an indirect defence against herbivores. The release of volatile organic compounds (VOCs) and the secretion of extrafloral nectar (EFN) are induced by insect feeding, a response that is mediated by the plant hormone, jasmonic acid. Although VOCs mainly attract predatory mites and parasitic wasps, while EFN mainly attracts ants, many more animal-plant interactions are influenced by these two traits. Other traits involved in defensive tritrophic interactions are cellular food bodies and domatia, which serve the nutrition and housing of predators. They are not known to respond to herbivory, while food body production can be induced by the presence of the mutualists. Interactions among the different defensive traits, and between them and other biotic and abiotic factors exist on the genetic, physiological, and ecological levels, but so far remain understudied. Indirect defences are increasingly being discussed as an environmentally-friendly crop protection strategy, but much more knowledge on their fitness effects under certain environmental conditions is required before we can understand their ecological and evolutionary relevance, and before tritrophic interactions can serve as a reliable tool in agronomy.
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                Author and article information

                Journal
                Sci Adv
                Sci Adv
                SciAdv
                advances
                Science Advances
                American Association for the Advancement of Science
                2375-2548
                May 2018
                16 May 2018
                : 4
                : 5
                : eaar4767
                Affiliations
                [1 ]Institute of Plant Sciences, University of Bern, Altenbergrain 21, 3013 Bern, Switzerland.
                [2 ]Laboratory for Fundamental and Advanced Research in Chemical Ecology, University of Neuchâtel, Rue Emile-Argand 11, 2009 Neuchâtel, Switzerland.
                Author notes
                [*]

                These authors contributed equally to this work.

                []Corresponding author. Email: matthias.erb@ 123456ips.unibe.ch (M.E.); ted.turlings@ 123456unine.ch (T.C.J.T.)
                Author information
                http://orcid.org/0000-0002-6785-0099
                http://orcid.org/0000-0002-7791-9440
                http://orcid.org/0000-0002-8315-785X
                http://orcid.org/0000-0002-4446-9834
                Article
                aar4767
                10.1126/sciadv.aar4767
                5955622
                29774237
                15724f20-b0d7-425b-ad2a-c5f47edc5399
                Copyright © 2018 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).

                This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license, which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.

                History
                : 13 November 2017
                : 03 April 2018
                Funding
                Funded by: doi http://dx.doi.org/10.13039/100010661, Horizon 2020 Framework Programme;
                Award ID: ERC-2016-STG 714239
                Funded by: doi http://dx.doi.org/10.13039/501100001711, Swiss National Science Foundation;
                Award ID: 155781
                Funded by: doi http://dx.doi.org/10.13039/501100001711, Swiss National Science Foundation;
                Award ID: 160786
                Funded by: doi http://dx.doi.org/10.13039/501100001711, Swiss National Science Foundation;
                Award ID: 160786
                Funded by: Sino-Swiss Science and Technology Cooperation;
                Award ID: EG 03-032016
                Categories
                Research Article
                Research Articles
                SciAdv r-articles
                Agriculture
                Ecology
                Ecology
                Custom metadata
                Eunice Ann Alesin

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