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      Electrophysiological and Behavioral Responses of Male Fall Webworm Moths ( Hyphantria cunea) to Herbivory-Induced Mulberry ( Morus alba) Leaf Volatiles

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          Abstract

          Volatile organic compounds (VOCs) were collected from damaged and intact mulberry leaves ( Morus alba L., Moraceae) and from Hyphantria cunea larvae by headspace absorption with Super Q columns. We identified their constituents using gas chromatography-mass spectrometry, and evaluated the responses of male H. cunea antennae to the compounds using gas chromatography-flame ionization detection coupled with electroantennographic detection. Eleven VOC constituents were found to stimulate antennae of male H. cunea moths: β-ocimene, hexanal, cis-3-hexenal, limonene, trans-2-hexenal, cyclohexanone, cis-2-penten-1-ol, 6-methyl-5-hepten-2-one, 4-hydroxy-4-methyl-2-pentanone, trans-3-hexen-1-ol, and 2,4-dimethyl-3-pentanol. Nine of these chemicals were released by intact, mechanically-damaged, and herbivore-damaged leaves, while cis-2-penten-1-ol was released only by intact and mechanically-damaged leaves and β-ocimene was released only by herbivore-damaged leaves. Results from wind tunnel experiments conducted with volatile components indicated that male moths were significantly more attracted to herbivory-induced volatiles than the solvent control. Furthermore, male moths' attraction to a sex pheromone lure was increased by herbivory-induced compounds and β-ocimene, but reduced by cis-2-penten-1-ol. A proof long-range field trapping experiment showed that the efficiency of sex pheromone lures in trapping male moths was increased by β-ocimene and reduced by cis-2-penten-1-ol.

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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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            Ecological, behavioral, and biochemical aspects of insect hydrocarbons.

            This review covers selected literature from 1982 to the present on some of the ecological, behavioral, and biochemical aspects of hydrocarbon use by insects and other arthropods. Major ecological and behavioral topics are species- and gender-recognition, nestmate recognition, task-specific cues, dominance and fertility cues, chemical mimicry, and primer pheromones. Major biochemical topics include chain length regulation, mechanism of hydrocarbon formation, timing of hydrocarbon synthesis and transport, and biosynthesis of volatile hydrocarbon pheromones of Lepidoptera and Coleoptera. In addition, a section is devoted to future research needs in this rapidly growing area of science.
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              Highly selective tuning of a silkworm olfactory receptor to a key mulberry leaf volatile.

              The olfactory system plays an important role in the recognition of leaf volatiles during the search of folivore insects for a suitable plant host. For example, volatiles emitted by mulberry leaves trigger chemotaxis behavior in the silkworms Bombyx mori, and as a consequence, they preferentially reside on and consume mulberry leaves. Here, we aimed to identify natural chemoattractants and their corresponding olfactory receptors (Ors) involved in silkworm behavior to mulberry leaves. Chemotaxis behavioral assays for headspace volatiles detected by gas chromatography-mass spectroscopy analysis revealed that among the volatiles that were emitted by mulberry leaves, cis-jasmone was the most potent attractant for silkworms, working at a threshold of 30 pg from [corrected] 20 cm distance. Among a total of 66 Ors identified in the B. mori genome, we found that 23 were expressed in the olfactory organs during larval stages. Functional analysis of all the larvae-expressed Ors in Xenopus oocytes revealed that one Or, termed BmOr-56, showed a high sensitivity to cis-jasmone. In addition, the ligand-receptor activity of BmOr-56 reflected the chemotaxis behavioral response of silkworms. We identified cis-jasmone as a potent attractant in mulberry leaves for silkworms and provide evidence that a highly tuned receptor, BmOr-56, may mediate this behavioral attraction. The current study sheds light on the mechanism of the correlation between olfactory perception in folivore insects and chemotaxis behavior to a natural volatile emitted by green leaves.
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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, USA )
                1932-6203
                2012
                14 November 2012
                : 7
                : 11
                : e49256
                Affiliations
                [1 ]State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, People's Republic of China
                [2 ]Graduate University of the Chinese Academy of Sciences (GUCAS), Beijing, People's Republic of China
                Ghent University, Belgium
                Author notes

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

                Conceived and designed the experiments: RT JPZ ZNZ. Performed the experiments: RT. Analyzed the data: RT. Contributed reagents/materials/analysis tools: RT. Wrote the paper: RT ZNZ.

                Article
                PONE-D-12-19503
                10.1371/journal.pone.0049256
                3498160
                23166622
                d7b08b6d-981f-4625-824d-eb075f43ea17
                Copyright @ 2012

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 4 July 2012
                : 5 October 2012
                Page count
                Pages: 7
                Funding
                This study received financial support from the National Basic Research Program of China (973 program, no. 2009CB119204, supported by MOST of PRC). http://www.most.gov.cn/. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Agriculture
                Pest Control
                Integrated Control
                Biology
                Ecology
                Plant Ecology
                Plant-Environment Interactions
                Chemical Ecology
                Zoology
                Entomology
                Chemistry
                Chromatography
                Gas Chromatography

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                Uncategorized

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