Sébastien Dugravot

Differences in volatile profiles of turnip plants subjected to single and dual herbivory above- and belowground.

Plants attacked by herbivorous insects emit volatile organic compounds that are used by natural enemies to locate their host or prey. The composition of the blend is often complex and specific. It may vary qualitatively and quantitatively according to plant and herbivore species, thus providing specific information for carnivorous arthropods. Most studies have focused on simple interactions that involve one species per trophic level, and typically have investigated the aboveground parts of plants. These investigations need to be extended to more complex networks that involve multiple herbivory above- and belowground. A previous study examined whether the presence of the leaf herbivore Pieris brassicae on turnip plants (Brassica rapa subsp. rapa) influences the response of Trybliographa rapae, a specialist parasitoid of the root feeder Delia radicum. It showed that the parasitoid was not attracted by volatiles emitted by plants under simultaneous attack. Here, we analyzed differences in the herbivore induced plant volatile (HIPV) mixtures that emanate from such infested plants by using Orthogonal Partial Least Squares-Discriminant Analysis (OPLS-DA). This multivariate model focuses on the differences between odor blends, and highlights the relative importance of each compound in an HIPV blend. Dual infestation resulted in several HIPVs that were present in both isolated infestation types. However, HIPVs collected from simultaneously infested plants were not the simple combination of volatiles from isolated forms of above- and belowground herbivory. Only a few specific compounds characterized the odor blend of each type of damaged plant. Indeed, some compounds were specifically induced by root herbivory (4-methyltridecane and salicylaldehyde) or shoot herbivory (methylsalicylate), whereas hexylacetate, a green leaf volatile, was specifically induced after dual herbivory. It remains to be determined whether or not these minor quantitative variations, within the background of more commonly induced odors, are involved in the reduced attraction of the root feeder’s parasitoid. The mechanisms involved in the specific modification of the odor blends emitted by dual infested turnip plants are discussed in the light of interferences between biosynthetic pathways linked to plant responses to shoot or root herbivory.

Identification of a Widespread Monomolecular Odor Differentially Attractive to Several Delia Radicum Ground-dwelling Predators in the Field

Dimethyl disulfide (DMDS) was identified as a major volatile constituent of Brassica napus roots heavily infested by Delia radicum, the cabbage root fly. Attractiveness of this widespread compound was tested in the field in a naturally complex odorous environment. By using an original setup especially designed for ground dwelling beetles, different concentrations of the pure molecule as well as attractiveness of the natural blend emitted by the rotten part of infested roots were tested simultaneously. The use of general linear model (GLM) statistics permitted us to finely discriminate the responses among the different treatments. The main predators of D. radicum (i.e., two staphylinids Aleochara bilineata and Aleochara bipustulata and carabid beetles of the genus Bembidion) were significantly attracted by DMDS, but responded in different ways to the natural blend and to the different concentrations tested. The dose–response curves were similar for the two staphylinids. However, whereas A. bilineata was more attracted by the natural volatile blend than by its preferred DMDS concentration, A. bipustulata was attracted as much by the natural blend as by its preferred DMDS concentration. Carabid beetles exhibited a different response. They were not attracted by the natural blend, but responded to a wider range of DMDS concentrations that included low concentrations that did not attract the staphylinid beetles. These results are discussed according to the potential resources searched by each taxon studied and their specificity for the resources. The possible use of DMDS for enhancing biological control of D. radicum is mentioned.

Aboveground herbivory affects indirect defences of brassicaceous plants against the root feeder Delia radicum Linnaeus: laboratory and field evidence

1. Belowground herbivory has recently been shown to disrupt the host location behaviour of aboveground parasitoids and thereby impact plants indirect defences. Reverse interactions, on the other hand, have received little attention so far.

Broccoli and turnip plants display contrasting responses to belowground induction by delia radicum infestation and phytohormone applications

Induced responses to insect herbivory are a common phenomenon in the plant kingdom. So far, induced responses have mostly investigated in aerial plant parts. Recently it was found that root herbivore may also elicit both local and systemic responses affecting aboveground herbivores and their natural enemies. Using broccoli (Brassica oleracea subsp. italica L.) and turnip (Brassica rapa subsp. rapa L.), two cultivated brassicaceaous plants differing in their chemistry and morphology, we analysed the local and systemic induced responses triggered by Delia radicum L. damage, JA and SA application. We also assessed whether the root induction treatments affected D. radicum larval performance. Both D. radicum damage and JA induced changes in glucosinolate and sugar content as well as affected D. radicum performance, while SA application did not. Despite the uniform chemical responses, the effect on larval performance on broccoli and turnip plants was very different. On broccoli, JA root treatment reduced herbivore performance, whereas in turnips the same treatment enhanced it. JA- and D. radicum-induced responses followed similar patterns, which suggests that the JA signalling pathway is involved in root-induced responses to larval feeding. Glucosinolate induction cannot fully explain the differences found in the performance of D. radicum on the different species. Changes in other resistance factors might significantly contribute to the induced resistance in these brassicaceaeous species as well.

Increased Sulfur Precursors and Volatiles Production by the Leek Allium porrum in Response to Specialist Insect Attack

To defend themselves against herbivory, plants use a variety of direct and indirect strategies involving induced increases in secondary substances. Species of the Allium genus (Alliaceae), such as the leek Allium porrum (L.), produce nonprotein sulfur amino acids derived from cysteine, i.e., alk(en)yl-cysteine sulfoxides that are precursors of volatile thiosulfinates and disulfides. These defend most species including the specialist leek moth, Acrolepiopsis assectella. We determined by measuring the increase in the sulfur precursor propyl-cysteine sulfoxide (PCSO) if production of this precursor is induced in response to moth attack and mechanical wounding. The concentration of PCSO was determined by HPLC in 2- or 6-mo-old leeks after attacks of various intensity either by the specialist leek moth or by a generalist moth, Agrotis ipsilon. Injury-induced release of sulfur volatiles was measured by GC/MS after the attacks. Results showed an increase in the production of sulfur compounds in both the precursor and volatile form, occurring only in association with intensive attacks by leek moths. The increase in sulfur precursors also led to an increase in the release of sulfur volatiles. This induced response may provide an effective defense strategy against the plant’s main natural enemy, both directly and indirectly by attracting entomophagous insects.

Characterizing Volatiles and Attractiveness of Five Brassicaceous Plants with Potential for a ‘Push-Pull’ Strategy Toward the Cabbage Root Fly, Delia radicum

Volatile Organic Compounds (VOCs) released by plants are involved in various orientation processes of herbivorous insects and consequently play a crucial role in their reproductive success. In the context of developing new strategies for crop protection, several studies have previously demonstrated the possibility to limit insect density on crops using either host or non-host plants that release attractive or repellent VOCs, respectively. The cabbage root fly, Delia radicum, is an important pest of brassicaceous crops for which control methods have to be implemented. Several studies have shown that plant odors influence cabbage root fly behavior, but only few VOCs have been identified so far. The present study aimed at selecting both plants and olfactory stimuli that could be used in the development of a “push-pull” strategy against the cabbage root fly. Olfactometer results revealed that plants belonging to the same family, even to the same species, may exhibit different levels of attractiveness toward D. radicum. Plants that were found attractive in behavioral observations were characterized by high release rates of distinct terpenes, such as linalool, β-caryophyllene, humulene, and α-farnesene. This study represents a first step to identify both attractive plants of agronomic interest, and additional volatiles that could be used in the context of trap crops to protect broccoli fields against the cabbage root fly.

Alkaloid concentration of the invasive plant species Ulex europaeus in relation to geographic origin and herbivory

In the study of plant defense evolution, invasive plant species can be very insightful because they are often introduced without their enemies, and traits linked to defense can be released from selective pressures and evolve. Further, studying plant defense evolution in invasive species is important for biological control and use of these species. In this study, we investigated the evolution of the defensive chemicals quinolizidine alkaloids (QAs) in the invasive species gorse, Ulex europaeus. Using a common garden experiment, our goals were to characterize the role of QAs relative to specialist enemies of gorse and to investigate if QA concentration evolved in invaded regions, where gorse was introduced without these enemies. Our results showed that pod infestation rate by the seed predator Exapion ulicis and infestation by the rust pathogen Uromyces genistae-tinctoriae were negatively correlated to concentration of the QA lupanine. Quinolizidine alkaloid concentration was very variable between individuals, both within and among populations, but it was not different between native and invaded regions, suggesting that no evolution of decreased resistance occurred after gorse lost its enemies. Our study also suggests that QA concentrations are traits integrated into seed predation avoidance strategies of gorse, with plants that mass-fruit in spring but do not escape pod infestation in time being richer in QAs.

Artificially applied plant volatile organic compounds modify the behavior of a pest with no adverse effect on its natural enemies in the field

Abstract The use of volatile organic compounds (VOCs) derived from plants to manipulate insect pest behavior can be applied in an integrated pest management strategy (IPM) using a combination of attractive and repulsive stimuli. The “push–pull” strategy was developed on this idea in order to disturb and modify the distribution and abundance of pests to protect crops and reduce the use of agrochemicals. This field experiment investigates, in a “push–pull” context using broccoli as a target crop and Chinese cabbage as a pull component, the stimulo-deterrent effect of five synthetic VOCs (dimethyl disulfide, linalool, geraniol, eucalyptol and citronellol) on the oviposition of the cabbage root fly Delia radicum. With the exception of linalool, all compounds tested had a significant effect in the field and eucalyptol showed the most promising results, reducing oviposition on broccoli by 45xa0%. Moreover, eucalyptol was the only VOC able to reduce the final infestation of D. radicum, i.e., the number of pupae. The other VOCs reduced oviposition by 20–30xa0%. No adverse effect of the treatments was found on major parasitoids (Trybliographa rapae and Aleochara bipustulata) and potential predators of D. radicum. This study highlights the potential of VOCs as deterrent stimuli against agricultural pests in the field.

Evolution of host acceptability and suitability in Callosobruchus maculatus (Coleoptera: Bruchidae) developing on an occasional host: importance for pest status prediction.

In West Africa, Callosobruchus maculatus Fabricius mainly develops on cowpea (Vigna unguiculata (L.) Walpers) and sometimes on Bambara groundnut (Vigna subterranea (L.) Verdcourt). A survey on the development of a C. maculatus strain selected on cowpea was undertaken during eight generations on two local varieties of Bambara to determine their level of acceptability and suitability for the pest and its evolution over time and successive generations. When C. maculatus females were in contact with seeds from both Bambara varieties for the first time, they laid fewer eggs on these hosts in comparison with cowpea. However, females that have developed inside Bambara cv. Local Beige seeds deposited more eggs on their hosts of origin from the first generation onwards. The same result was obtained on Bambara cv. Local Striped seeds from the F4 generation onwards. Egg viability was not affected by host variability. On the contrary, the larval survival was significantly reduced on Bambara seeds. Larval survival and intrinsic rates of natural increase were improved on both Bambara varieties with successive generations in comparison to cowpea. Our results demonstrate that in a non-choice situation, C. maculatus is able to develop on both Bambara cv. and even increase its reproduction potential over successive generations, regardless of the climatic variations. The results help to better understand why C. maculatus is becoming a serious concern on Bambara in West Africa where the pest is frequently in contact with this occasional host.

One more step toward a push-pull strategy combining both a trap crop and plant volatile organic compounds against the cabbage root fly Delia radicum

The “push-pull” strategy aims at manipulating insect pest behavior using a combination of attractive and repulsive stimuli using either plants derived volatile organic compounds or insect host plant preferences. In a field experiment using broccoli as a crop, we combined in a “push-pull” context the oviposition deterrent effect of dimethyl disulfide and the attractive effect of a Chinese cabbage strip enhanced with Z-3-hexenyl-acetate. The push component dimethyl disulfide reduced Delia radicum L. (Diptera: Anthomyiidae) oviposition on broccoli by nearly 30%, and applying Z-3-hexenyl-acetate in the pull component of Chinese cabbage increased it by 40%. Moreover, pest infestation was 40% higher in Chinese cabbage compared to broccoli and parasitism by Trybliographa rapae Westwood (Hymenoptera: Figitidae) was four times higher on this trap plant. In addition, lab experiments confirmed that Chinese cabbage is a more suitable host plant than broccoli for the cabbage root fly. Taken together, our results demonstrate the technical possibility of using a push-pull strategy to manipulate the egg-laying behavior of D. radicum in the field.