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      Mountain Pine Beetles Use Volatile Cues to Locate Host Limber Pine and Avoid Non-Host Great Basin Bristlecone Pine

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          Abstract

          The tree-killing mountain pine beetle ( Dendroctonus ponderosae Hopkins) is an important disturbance agent of western North American forests and recent outbreaks have affected tens of millions of hectares of trees. Most western North American pines ( Pinus spp.) are hosts and are successfully attacked by mountain pine beetles whereas a handful of pine species are not suitable hosts and are rarely attacked. How pioneering females locate host trees is not well understood, with prevailing theory involving random landings and/or visual cues. Here we show that female mountain pine beetles orient toward volatile organic compounds (VOCs) from host limber pine ( Pinus flexilis James) and away from VOCs of non-host Great Basin bristlecone pine ( Pinus longaeva Bailey) in a Y-tube olfactometer. When presented with VOCs of both trees, females overwhelmingly choose limber pine over Great Basin bristlecone pine. Analysis of VOCs collected from co-occurring limber and Great Basin bristlecone pine trees revealed only a few quantitative differences. Noticeable differences included the monoterpenes 3-carene and D-limonene which were produced in greater amounts by host limber pine. We found no evidence that 3-carene is important for beetles when selecting trees, it was not attractive alone and its addition to Great Basin bristlecone pine VOCs did not alter female selection. However, addition of D-limonene to Great Basin bristlecone pine VOCs disrupted the ability of beetles to distinguish between tree species. When presented alone, D-limonene did not affect behavior, suggesting that the response is mediated by multiple compounds. A better understanding of host selection by mountain pine beetles could improve strategies for managing this important forest insect. Moreover, elucidating how Great Basin bristlecone pine escapes attack by mountain pine beetles could provide insight into mechanisms underlying the incredible longevity of this tree species.

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          Perception of plant volatile blends by herbivorous insects--finding the right mix.

          Volatile plant secondary metabolites are detected by the highly sensitive olfactory system employed by insects to locate suitable plants as hosts and to avoid unsuitable hosts. Perception of these compounds depends on olfactory receptor neurones (ORNs) in sensillae, mostly on the insect antennae, which can recognise individual molecular structures. Perception of blends of plant volatiles plays a pivotal role in host recognition, non-host avoidance and ensuing behavioural responses as different responses can occur to a whole blend compared to individual components. There are emergent properties of blend perception because components of the host blend may not be recognised as host when perceived outside the context of that blend. Often there is redundancy in the composition of blends recognised as host because certain compounds can be substituted by others. Fine spatio-temporal resolution of the synchronous firing of ORNs tuned to specific compounds enables insects to pick out relevant host odour cues against high background noise and with ephemeral exposure to the volatiles at varying concentrations. This task is challenging as they usually rely on ubiquitous plant volatiles and not those taxonomically characteristic of host plants. However, such an odour coding system has the advantage of providing flexibility; it allows for adaptation to changing environments by alterations in signal processing while maintaining the same peripheral olfactory receptors. Copyright © 2011 Elsevier Ltd. All rights reserved.
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            Volatile chemical cues guide host location and host selection by parasitic plants.

            The importance of plant volatiles in mediating interactions between plant species is much debated. Here, we demonstrate that the parasitic plant Cuscuta pentagona (dodder) uses volatile cues for host location. Cuscuta pentagona seedlings exhibit directed growth toward nearby tomato plants (Lycopersicon esculentum) and toward extracted tomato-plant volatiles presented in the absence of other cues. Impatiens (Impatiens wallerana) and wheat plants (Triticum aestivum) also elicit directed growth. Moreover, seedlings can distinguish tomato and wheat volatiles and preferentially grow toward the former. Several individual compounds from tomato and wheat elicit directed growth by C. pentagona, whereas one compound from wheat is repellent. These findings provide compelling evidence that volatiles mediate important ecological interactions among plant species.
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              Naphthalene, an insect repellent, is produced by Muscodor vitigenus, a novel endophytic fungus.

              Muscodor vitigenus is a recently described endophytic fungus of Paullinia paullinioides, a liana growing in the understorey of the rainforests of the Peruvian Amazon. This fungus produces naphthalene under certain cultural conditions. Naphthalene produced by M. vitigenus was identified by gas chromatography/mass spectrometry. Its chromatographic and mass spectral properties were identical to authentic naphthalene. Agar plugs supporting growth of the fungus and producing known amounts of naphthalene effectively repelled the adult stage of the wheat stem sawfly, Cephus cinctus, in Y-tube bioassay tests. Authentic naphthalene, at comparable concentrations to those in tests involving the fungus itself, mimicked the insect repellency of the fungus. Although other Muscodor spp. produce volatile antimicrobials, M. vitigenus is unique in its ability to produce naphthalene almost exclusively. This report also describes the potential practical implications of M. vitigenus.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                2 September 2015
                2015
                : 10
                : 9
                : e0135752
                Affiliations
                [1 ]Department of Wildland Resources, Utah State University, 5230 Old Main Hill, Logan, UT, 84322, United States of America
                [2 ]USDA Forest Service, Rocky Mountain Research Station, Forestry Sciences Laboratory, Bozeman, Montana, United States of America
                University of Nevada Reno, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: CG JR MJ. Performed the experiments: CG JR AG. Analyzed the data: CG JR. Contributed reagents/materials/analysis tools: JR MJ. Wrote the paper: CG JR.

                Article
                PONE-D-15-16449
                10.1371/journal.pone.0135752
                4558103
                26332317
                7a37fd4a-bba4-40bb-bc90-acf5c0221d5c

                This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication

                History
                : 15 April 2015
                : 25 July 2015
                Page count
                Figures: 4, Tables: 1, Pages: 13
                Funding
                This project was supported by funding from USFS EM Project INT-EM-F-10-02, Utah Agricultural Experiment Station (UAES) UTA Project 1070, USDA National Needs Graduate Fellowship Competitive NIFA Grant, and PECASE (President’s Early Career Award in Science and Engineering) to Justin Runyon. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
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                All relevant data are within the paper and its Supporting Information files.

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