1. Diets that maximise life span often differ from diets that maximise reproduction. Animals have therefore evolved advanced foraging strategies to acquire optimal nutrition and maximise their fitness. The free‐living adult females of parasitoid wasps (Hymenoptera) need to balance their search for hosts to reproduce and for carbohydrate resources to feed. 2. Honeydew, excreted by phloem‐feeding insects, presents a widely available carbohydrate source in nature that can benefit natural enemies of honeydew‐producing insects. However, the effects of variation in honeydew on organisms in the fourth trophic level, such as hyperparasitoids, are not yet understood. 3. This study examined how five different honeydew types influence longevity and fecundity of four hyperparasitoid taxa. Asaphes spp. (Pteromalidae) and Dendrocerus spp. (Megaspilidae) are secondary parasitoids of aphid parasitoids and are thus associated with honeydew‐producing insects. Gelis agilis and Acrolyta nens (both Ichneumonidae) are secondary parasitoids of species that do not use honeydew‐producing hosts. 4. Most honeydew types had a positive or neutral effect on life span and fecundity of hyperparasitoids compared with controls without honeydew, although negative effects were also found for both aphid hyperparasitoids. Honeydew produced by aphids feeding on sweet pepper plants was most beneficial for all hyperparasitoid taxa, which can partially be explained by the high amount of honeydew, but also by the composition of dietary sugars in these honeydew types. 5. The findings of this study underline the value of aphid honeydew as a carbohydrate resource for fourth‐trophic‐level organisms, not only those associated with honeydew‐producing insects but also ‘interlopers’ without such a natural association.
Insect communities consist of several trophic levels that have to forage for suitable resources among and within larger patches of non-resources. To locate their resources, insects use diverse stimuli, including olfactory, visual, acoustic, tactile and gustatory cues. While most research has focused on cues derived from plants and other insects, there is mounting evidence that insects also respond to volatile organic compounds (VOCs) emitted by microorganisms. However, to date only very little is known about the olfactory responses of insects to microbial VOCs within and across different trophic levels. In this study, using Y-tube bioassays and chemical analysis of VOCs we assessed how volatile compounds emitted by bacteria affect the olfactory response of insects of different trophic levels. Experiments were performed using two aphid species (Amphorophora idaei and Myzus persicae var. nicotianae), their most important primary parasitoid species (Aphidius colemani, A. ervi, and A. matricariae), and two of their hyperparasitoid species (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) isolated from the habitat of the insects. Results revealed that insects from all trophic levels responded to bacterial volatiles, but responses varied between and within trophic levels. All bacteria produced the same set of volatile compounds but often in different relative concentrations. For a number of these volatiles we found contrasting correlations between their concentration and the behaviour of the primary parasitoids and hyperparasitoids. Exploitation of such contrasting responses may lead to novel semiochemical-based strategies to improve biological aphid control.
There is increasing evidence that microorganisms, particularly fungi and bacteria, emit volatile compounds that mediate the foraging behaviour of insects and therefore have the potential to affect key ecological relationships. However, to what extent microbial volatiles affect the olfactory response of insects across different trophic levels remains unclear. Adult parasitoids use a variety of chemical stimuli to locate potential hosts, including those emitted by the host's habitat, the host itself and microorganisms associated with the host. Given the great capacity of parasitoids to utilize and learn odours to increase foraging success, parasitoids of eggs, larvae or pupae may respond to the same volatiles the adult stage of their hosts use when locating their resources, but compelling evidence is still scarce. In this study, using Saccharomyces cerevisiae we show that Trichopria drosophilae, a pupal parasitoid of Drosophila species, is attracted to the same yeast volatiles as their hosts in the adult stage, i.e. acetate esters. Parasitoids significantly preferred the odour of S. cerevisiae over the blank medium in a Y-tube olfactometer. Deletion of the yeast ATF1 gene, encoding a key acetate ester synthase, decreased attraction of T. drosophilae, while addition of synthetic acetate esters to the fermentation medium restored parasitoid attraction.Bioassays with individual compounds revealed that the esters alone were not as attractive as the volatile blend of S. cerevisiae, suggesting that other volatile compounds also contribute to the attraction of T. drosophilae. Altogether, our results indicate that pupal parasitoids respond to the same volatiles as the adult stage of their hosts, which may aid them in locating oviposition sites.
Insect communities consist of several trophic levels that have to forage for suitable resources among and within larger patches of non-resources. To locate their resources, insects use diverse stimuli, including olfactory, visual, acoustic, tactile and gustatory cues. While most research has focused on cues derived from plants and other insects, there is mounting evidence that insects also respond to volatile organic compounds (VOCs) emitted by microorganisms. However, to date only very little is known about the olfactory responses of insects to microbial VOCs within and across different trophic levels. In this study, using Y-tube bioassays and chemical analysis of VOCs we assessed how volatile compounds emitted by bacteria affect the olfactory response of insects of different trophic levels. Experiments were performed using two aphid species (Amphorophora idaei and Myzus persicae var. nicotianae), their most important primary parasitoid species (Aphidius colemani, A. ervi, and A. matricariae), and two of their hyperparasitoid species (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) isolated from the habitat of the insects. Results revealed that insects from all trophic levels responded to bacterial volatiles, but responses varied between and within trophic levels. All bacteria produced the same set of volatile compounds but often in different relative concentrations. For a number of these volatiles we found contrasting correlations between their concentration and the behaviour of the primary parasitoids and hyperparasitoids. Exploitation of such contrasting responses may lead to novel semiochemical-based strategies to improve biological aphid control.
Manipulation of insect foraging may provide the basis for effective insect pest control strategies. Recent laboratory and small‐scale greenhouse experiments have shown that a blend of styrene and benzaldehyde is attractive to some Aphidius parasitoids, making it a good candidate for attracting and retaining these natural enemies in cropping systems. However, an appropriate dispenser type and appropriate dose for field application and its attraction range have yet to be identified. In this study, we performed experiments to determine an appropriate dispenser type – Omnilure® vs. low‐density polyethylene (LDPE) bags – and the most suitable dose to attract Aphidius colemani Viereck (Hymenoptera: Braconidae) under commercial greenhouse conditions and to determine the maximum distance of attraction. A mixture of 10 mg styrene and 100 μg benzaldehyde was the most attractive dose for A. colemani when provided by the dispensers under greenhouse conditions. The highest percentage of parasitoids was attracted when insects 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. The potential application of these results in novel augmentation biocontrol strategies is discussed.
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