Turlings, Ted

2014, D'Alessandro, Marco, Erb, Matthias, Ton, Jurriaan, Brandenburg, Anna, Karlen, Danielle, Zopfi, Jakob, Turlings, Ted

Volatile organic compounds (VOCs) released by soil microorganisms influence plant growth and pathogen resistance. Yet, very little is known about their influence on herbivores and higher trophic levels. We studied the origin and role of a major bacterial VOC, 2,3-butanediol (2,3-BD), on plant growth, pathogen and herbivore resistance, and the attraction of natural enemies in maize. One of the major contributors to 2,3-BD in the headspace of soil-grown maize seedlings was identified as Enterobacter aerogenes, an endophytic bacterium that colonizes the plants. The production of 2,3-BD by E.?aerogenes rendered maize plants more resistant against the Northern corn leaf blight fungus Setosphaeria turcica. On the contrary, E.?aerogenes-inoculated plants were less resistant against the caterpillar Spodoptera littoralis. The effect of 2,3-BD on the attraction of the parasitoid Cotesia marginiventris was more variable: 2,3-BD application to the headspace of the plants had no effect on the parasitoids, but application to the soil increased parasitoid attraction. Furthermore, inoculation of seeds with E.?aerogenes decreased plant attractiveness, whereas inoculation of soil with a total extract of soil microbes increased parasitoid attraction, suggesting that the effect of 2,3-BD on the parasitoid is indirect and depends on the composition of the microbial community.

2010, Held, Matthias, D'Alessandro, Marco, Hiltpold, Ivan, Turlings, Ted

2006, D'Alessandro, Marco, Held, Matthias, Triponez, Yann, Turlings, Ted

After herbivore attack, plants release a plethora of different volatile organic compounds (VOCs), which results in odor blends that are attractive to predators and parasitoids of these herbivores. VOCs in the odor blends emitted by maize plants (Zea mays) infested by lepidopteran larvae are well characterized. They are derived from at least three different biochemical pathways, but the relative importance of each pathway for the production of VOCs that attract parasitic wasps is unknown. Here, we studied the importance of shikimic acid derived VOCs for the attraction of females of the parasitoids Cotesia marginiventris and Microplitis rufiventris. By incubating caterpillar-infested maize plants in glyphosate, an inhibitor of the 5-enolpyruvylshikimate-3-phospate (EPSP) synthase, we obtained induced odor blends with only minute amounts of shikimic acid derived VOCs. In olfactometer bioassays, the inhibited plants were as attractive to naive C. marginiventris females as control plants that released normal amounts of shikimic acid derived VOCs, whereas naive M. rufiventris females preferred inhibited plants to control plants. By adding back synthetic indole, the quantitatively most important shikimic acid derived VOC in induced maize odors, to inhibited plants, we showed that indole had no effect on the attraction of C. marginiventris and that M. rufiventris preferred blends without synthetic indole. Exposing C. marginiventris females either to odor blends of inhibited or control plants during oviposition experiences shifted their preference in subsequent olfactometer tests in favor of the experienced odor. Further learning experiments with synthetic indole showed that C. marginiventris can learn to respond to this compound, but that this does not affect its choices between natural induced blends with or without indole. We hypothesize that for naive wasps the attractiveness of an herbivore-induced odor blend is reduced due to masking by nonattractive compounds, and that during oviposition experiences in the presence of complex odor blends, parasitoids strongly associate some compounds, whereas others are largely ignored.

2013, D'Alessandro, Marco, Erb, Matthias, Ton, Jurriaan, Brandenburg, Anna, Karlen, Danielle, Zopfi, Jakob, Turlings, Ted

Volatile organic compounds (VOCs) released by soil microorganisms influence plant growth and pathogen resistance. Yet, very little is known about their influence on herbivores and higher trophic levels. We studied the origin and role of a major bacterial VOC, 2,3-butanediol (2,3-BD), on plant growth, pathogen and herbivore resistance, and the attraction of natural enemies in maize. One of the major contributors to 2,3-BD in the headspace of soil-grown maize seedlings was identified as Enterobacter aerogenes, an endophytic bacterium that colonizes the plants. The production of 2,3-BD by E.?aerogenes rendered maize plants more resistant against the Northern corn leaf blight fungus Setosphaeria turcica. On the contrary, E.?aerogenes-inoculated plants were less resistant against the caterpillar Spodoptera littoralis. The effect of 2,3-BD on the attraction of the parasitoid Cotesia marginiventris was more variable: 2,3-BD application to the headspace of the plants had no effect on the parasitoids, but application to the soil increased parasitoid attraction. Furthermore, inoculation of seeds with E.?aerogenes decreased plant attractiveness, whereas inoculation of soil with a total extract of soil microbes increased parasitoid attraction, suggesting that the effect of 2,3-BD on the parasitoid is indirect and depends on the composition of the microbial community.

2010, Held, Matthias, D'Alessandro, Marco, Hiltpold, Ivan, Turlings, Ted

2005, D'Alessandro, Marco, Turlings, Ted

Many parasitic wasps (parasitoids) exploit volatile organic compounds (VOCs) emitted by herbivore-infested plants in order to locate their hosts, but it remains largely unknown which specific compounds within the volatile blends elicit the attractiveness to parasitoids. One way of studying the importance of specific VOCs is to test the attractiveness of odor blends from which certain compounds have been emitted. We used this approach by testing the attraction of naive and experienced females of the two parasitoids Cotesia marginiventris and Microplitis rufiventris to partially altered volatile blends of maize seedlings (Zea mays var. Delprim) infested with Spodoptera littoralis larvae. Adsorbing filter tubes containing carbotrap-C or silica were installed in a four-arm olfactometer between the odor source vessels and the arms of the olfactometer. The blends breaking through were tested for chemical composition and attractiveness to the wasps. Carbotrap-C adsorbed most of the sesquiterpenes, but the breakthrough blend remained attractive to naive C. marginiventris females. Silica adsorbed only some of the more polar VOCs, but this essentially eliminated all attractiveness to naive C. marginiventris, implying that among the adsorbed compounds there are some that play key roles in the attraction. Unlike C. marginiventris, M. rufiventris was still attracted to the latter blend, showing that parasitoids with a comparable biology may employ different strategies in their use of plant-provided cues to locate hosts. Results from similar experiments with modified odor blends of caterpillar-infested cowpea (Vigna unguiculata) indicate that key VOCs in different plant species vary greatly in quality and/or quantity. Finally, experienced wasps were more strongly attracted to a specific blend after they perceived the blend while ovipositing in a host. Considering the high number of distinct adsorbing materials available today, this in situ modification of complex volatile blends provides a new and promising approach pinpointing on key attractants within these blends. Advantages and disadvantages compared to other approaches are discussed.

2013, von Mérey, Georg E., Veyrat, Nathalie, D'Alessandro, Marco, Turlings, Ted

Plants under herbivore attack emit volatile organic compounds (VOCs) that can serve as foraging cues for natural enemies. Adult females of Lepidoptera, when foraging for host plants to deposit eggs, are commonly repelled by herbivore-induced VOCs, probably to avoid competition and natural enemies. Their larval stages, on the other hand, have been shown to be attracted to inducible VOCs. We speculate that this contradicting behaviour of lepidopteran larvae is due to a need to quickly find a new suitable host plant if they have fallen to the ground. However, once they are on a plant they might avoid the sites with fresh damage to limit competition and risk of cannibalism by conspecifics, as well as exposure to natural enemies. To test this we studied the effect of herbivore-induced VOCs on the attraction of larvae of the moth Spodoptera littoralis and on their feeding behaviour. The experiments further considered the importance of previous feeding experience on the responses of the larvae. It was confirmed that herbivore-induced VOCs emitted by maize plants are attractive to the larvae, but exposure to the volatiles decreased the growth rate of caterpillars at early developmental stages. Larvae that had fed on maize previously were more attracted by VOCs of induced maize than larvae that had fed on artificial diet. At relatively high concentrations synthetic green leaf volatiles, indicative of fresh damage, also negatively affected the growth rate of caterpillars, but not at low concentrations. In all cases, feeding by the later stages of the larvae was not affected by the VOCs. The results are discussed in the context of larval foraging behaviour under natural conditions, where there may be a trade-off between using available host plant signals and avoiding competitors and natural enemies.

2009-9, D'Alessandro, Marco, Brunner, V., von Mérey, Georg E., Turlings, Ted

Plants infested with herbivorous arthropods emit complex blends of volatile compounds, which are used by several natural enemies as foraging cues. Despite detailed knowledge on the composition and amount of the emitted volatiles in many plant-herbivore systems, it remains largely unknown which compounds are essential for the attraction of natural enemies. In this study, we used a combination of different fractionation methods and olfactometer bioassays in order to examine the attractiveness of different compositions of volatile blends to females of the parasitoid Cotesia marginiventris. In a first step, we passed a volatile blend emitted by Spodoptera littoralis infested maize seedlings over a silica-containing filter tube and subsequently desorbed the volatiles that were retained by the silica filter (silica extract). The volatiles that broke through the silica filter were collected on and subsequently desorbed from a SuperQ filter (breakthrough). The silica extract was highly attractive to the wasps, whereas the breakthrough volatiles were not attractive. The silica extract was even more attractive than the extract that contained all herbivore-induced maize volatiles. Subsequently, we fractioned the silica extract by preparative gas-chromatography (GC) and by separating more polar from less polar compounds. In general, C. marginiventris preferred polar over non-polar compounds, but several fractions were attractive to the wasp, including one that contained compounds emitted in quantities below the detection threshold of the GC analysis. These results imply that the attractiveness of the volatile blend emitted by Spodoptera-infested maize seedlings to C. marginiventris females is determined by a specific combination of attractive and repellent/masking compounds, including some that are emitted in very small amounts. Manipulating the emission of such minor compounds has the potential to greatly improve the attraction of certain parasitoids and enhance biological control of specific insect pests.