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The role of bacterial volatiles in mediating the olfactory responses of aphid parasitoid wasps and their hyperparasitoids: Potential implications for biological control

Book - Dissertation

Plant pathogens, weeds, and insect pests pose significant threats to plants important for agriculture. Currently, approximately 10,000 herbivorous insects have been identified to be insect pests, which collectively cause an estimated 15.6% loss in crop yield across multiple crop species. Historically, insect pests have been controlled through the use of synthetic pesticides. However, the extensive use of such insecticidal compounds has led to several deleterious effects on the environment, non-target organisms and human health. Moreover, widespread usage of chemical pesticides has resulted in several insect species developing resistance against insecticidal compounds, which has resulted in a loss of their efficacy. To mitigate these drawbacks, biological control methods using arthropod natural enemies to control insect pests have become an important management strategy to complement or replace the use of synthetic pesticides. One of the most commonly employed arthropod natural enemies in the biological control of insect pests are parasitoids whose larvae develop at the expense of an arthropod host and eventually kill them. Nevertheless, despite the several benefits they offer, their biocontrol efficacy may still be enhanced, primarily due to two major limitations: a limited ability of the parasitoids to locate their hosts in a complex foraging environment with high levels of background noise, and the presence of secondary parasitoids attacking the primary, pest-killing parasitoids (further referred to as hyperparasitoids). In order for parasitoids to find their hosts in a complex environment, they largely rely on chemical cues, so-called "semiochemicals", released by host-infested plants and the host insects themselves. Additionally, recent research has shown that volatile compounds emitted by microorganisms (microbial volatile organic compounds (mVOCs)) may affect the olfactory behaviour of insects, thereby offering novel opportunities to manipulate the foraging behaviour of both parasitoids and hyperparasitoids. Nevertheless, the full potential of mVOCs in insect pest management is yet to be fully understood. The overall aim of this PhD research was to investigate the potential of mVOCs to improve parasitoid-based biological pest control through manipulation of the behaviour of primary parasitoids and their hyperparasitoids. Therefore, we used a study system based on the food web of aphids, parasitoids and their hyperparasitoids that are commonly found in the protected cultivation of sweet pepper and raspberry. Aphids are one of the most damaging phloem-feeding insect pests on Earth, responsible for yield losses between 30 and 100%. Although parasitoids contribute significantly in the management of aphid populations, their biocontrol efficacy is increasingly threatened by the presence of hyperparasitoids, but information on their temporal and spatial diversity is still scarce. In Chapter 1, we gave a comprehensive literature overview of the impact of insect pests on agricultural crops, presented different management strategies which are currently applied to control insect pests, and identified the major limitations of using parasitoids to manage insect pests. Additionally, we explained in detail the role of semiochemicals in the foraging behaviour of insects, as well as the potential of mVOCs to manipulate insect behaviour leading to increased pest control. Finally, we outlined the knowledge gaps and the objectives addressed in this PhD thesis. In Chapter 2, we investigated the presence and temporal dynamics of hyperparasitoids in the cultivation of sweet pepper and raspberry. This not only allowed us to obtain more insights into the population dynamics of hyperparasitoids and to assess potential differences among crops, it also enabled us to select relevant species for evaluating their olfactory response to microbial volatiles in the next chapter. Specifically, we surveyed the hyperparasitoid community using banker plants infested with the cereal aphid Sitobion avenae and parasitized by the primary parasitoid Aphidius ervi at five sweet pepper growers and five raspberry growers in the Flanders region of Belgium. Hyperparasitoids were sampled on a monthly basis from the start of the growing season (March) until the end of the growing season (October). Throughout the survey, hyperparasitoid species from six different genera were found. Hyperparasitoids were observed from the start of the survey until September in sweet pepper and until October in raspberry. The overall rate of hyperparasitism within the banker plants was higher in sweet pepper (42%) than in raspberry (10%). The most commonly identified genus differed between the two crops and depended on the sampling month. Dendrocerus was the most frequently identified hyperparasitoid in raspberry throughout the entire season. Conversely, while Dendrocerus was the only hyperparasitoid genus found in March and April in sweet pepper, it became replaced by individuals of the genera Alloxysta, Pachyneuron and Phaenoglyphis later in the growing season. In Chapter 3, we used Y-tube olfactometer experiments and chemical analysis of mVOCs to assess how volatile compounds emitted by bacteria affect the olfactory response of aphids, parasitoids and their hyperparasitoids. Experiments were performed using two aphid species (Amphorophora idaei and Myzus persicae var. nicotianae), three primary parasitoid species(Aphidius colemani, Aphidius ervi, and Aphidius matricariae) and two of their hyperparasitoid species which were commonly found in Chapter 2 (Asaphes suspensus and Dendrocerus aphidum). Olfactory responses were evaluated for three bacterial strains (Bacillus pumilus ST18.16/133, Curtobacterium sp. ST18.16/085, and Staphylococcus saprophyticus ST18.16/160) which were isolated from the habitat of the insects. We found that insects from all trophic levels investigated responded to bacterial volatiles, but that the olfactory responses varied between and within trophic levels. All bacteria produced the same set of volatile compounds, but often in different relative concentrations. For 11 of these volatiles, we identified significant contrasting correlations between the relative concentration of the compound and the olfactory response of the primary parasitoids and hyperparasitoids. Olfactometer experiments using A. colemani and D. aphidum on three of these compounds confirmed the contrasting olfactory responses between these two species. Furthermore, a mixture of 1 µg styrene and 10 ng benzaldehyde was found to be attractive for A. colemani and repellent for D. aphidum, making it a promising candidate to attract A. colemani parasitoids and keep their hyperparasitoids away. Next, in Chapter 4 we performed experiments at a semi-commercial sweet pepper greenhouse to investigate the potential of microbe-derived semiochemicals to attract parasitoids and enhance their biocontrol efficacy under greenhouse conditions. Therefore, experiments were performed with the styrene-benzaldehyde blend which was found to be promising under laboratory conditions in Chapter 3. We first performed experiments to determine an appropriate dispenser type (Omnilure® vs. low-density polyethylene (LDPE) bags) and the most suitable dose to attract A. colemani. Irrespective of the dispenser type, a mixture of 10 mg styrene and 100 µg benzaldehyde was the most attractive dose for A. colemani when provided at a distance of 0.5 m from the release spot of the parasitoids. Subsequently, we investigated the attractive range of this blend when released from Omnilure® dispensers, and found that the highest percentage of parasitoids was attracted when the parasitoids were released at a distance of 0.5 m from the Omnilure® dispensers. Nevertheless, compared to the solvent control the blend of styrene and benzaldehyde remained attractive over a distance of up to 5 m. Finally, we found that the application of the blend on aphid-infested plants increased the parasitism rate of A. colemani by a factor of 1.48× compared to aphid-infested plants without the blend, when parasitoids were released at a distance of 2.5 m from the infested plants. While the observed effects of microbe-derived semiochemicals on parasitoid attraction and performance were relatively limited under greenhouse conditions, further research could be conducted to enhance their activity to attract natural enemies and improve their biocontrol efficacy. This has been discussed in Chapter 5 and Chapter 6, alongside the main conclusions of this work and an outlook on the potential application of the obtained results.
Publication year:2024
Accessibility:Embargoed