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The role of indole and other shikimic acid derived maize volatiles in the attraction of two parasitic wasps

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.

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A comparison of naïve and conditioned responses of three generalist endoparasitoids of lepidopteran larvae to host-induced plant odours

2006, Tamò, Cristina, Ricard, Ingrid, Held, Matthias, Davison, A. C., Turlings, Ted

Many parasitic wasps that exploit herbivores as their hosts make use of herbivoreinduced plant odours to locate their victims and these wasps often exhibit an ability to learn to associate specific plant-produced odours with the presence of hosts. This associative learning is expected to allow generalist parasitoids to focus on cues that are most reliably associated with current host presence, but evidence supporting this hypothesis is ambiguous. Using a six-arm olfactometer we compared the responses of three generalist larval endoparasitoids, Cotesia marginiventris (Hymenoptera: Braconidae), Microplitis rufiventris (Hymenoptera: Braconidae) and Campoletis sonorensis (Hymenoptera: Ichneumonidae), to the induced odours of three plant species: maize (Zea mays), cowpea (Vigna unguiculata), and cotton (Gossypium hirsutum). We tested the responses of naïve females as well as of females that were first conditioned by parasitising host larvae feeding on one of the plant species. Despite similarities in biology and host range the three wasp species responded entirely differently. Naïve C. marginiventris and C. sonorensis chose equally among the induced odours of the three plants, whereas naïve M. rufiventris, which may have a somewhat more restricted host range, tended to prefer the odour of maize. After conditioning, most C. marginiventris females chose the odour of the plant species that they had experienced, but conditioned M. rufiventris showed an even stronger preference for maize odours, independently of the plant they had experienced. Cotesia sonorensis did not show any change in its preference after conditioning. We speculate that its extremely broad host range allows C. sonorensis females to use fixed responses to cues commonly associated with plants damaged by Lepidoptera. These results imply that different generalist parasitoids may employ different foraging strategies and that associative learning is not necessarily part of it.

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Evaluating the Induced-Odour Emission of a Bt Maize and its Attractiveness to Parasitic Wasps

2005, Turlings, Ted, Jeanbourquin, Philippe, Held, Matthias, Degen, Thomas

The current discussion on the safety of transgenic crops includes their effects on beneficial insects, such as parasitoids and predators of pest insects. One important plant trait to consider in this context is the emission of volatiles in response to herbivory. Natural enemies use the odours that result from these emissions as cues to locate their herbivorous prey and any significant change in these plant-provided signals may disrupt their search efficiency. There is a need for practical and reliable methods to evaluate transgenic crops for this and other important plant traits. Moreover, it is imperative that such evaluations are done in the context of variability for these traits among conventional genotypes of a crop. For maize and the induction of volatile emissions by caterpillar feeding this variability is known and realistic comparisons can therefore be made. Here we used a six-arm olfactometer that permits the simultaneous collection of volatiles emitted by multiple plants and testing of their attractiveness to insects. With this apparatus we measured the induced odour emissions of Bt maize (Bt11, N4640Bt) and its near-isogenic line (N4640) and the attractiveness of these odours to Cotesia marginiventris and Microplitis rufiventris, two important larval parasitoids of common lepidopteran pests. Both parasitoid species were strongly attracted to induced maize odour and neither wasp distinguished between the odours of the transgenic and the isogenic line. Also wasps that had previously experienced one of the odours during a successful oviposition divided their choices equally between the two odours. However, chemical analyses of collected odours revealed significant quantitative differences. The same 11 compounds dominated the blends of both genotypes, but the isogenic line released a larger amount of most of these. These differences may be due to altered resource allocation in the transgenic line, but it had no measurable effect on the wasps’ behaviour. All compounds identified here had been previously reported for maize and the differential quantities in which they were released fall well within the range of variability observed for other maize genotypes.