Volatiles of bacteria associated with parasitoid habitats elicit distinct olfactory responses in an aphid parasitoid and its hyperparasitoid

Abstract

1. To locate mating partners and essential resources such as food, oviposition sites and shelter, insects rely to a large extent on chemical cues. While most research has focused on cues derived from plants and insects, there is mounting evidence that indicates that micro-organisms emit volatile compounds that may play an important role in insect behaviour.2. In this study, we assessed how volatile compounds emitted by phylogenetically diverse bacteria affected the olfactory response of the primary parasitoid Aphidius colemani and one of its secondary parasitoids, Dendrocerus aphidum. Olfactory responses were evaluated for volatile blends emitted by bacteria isolated from diverse sources from the parasitoid's habitat, including aphids, aphid mummies and honeydew, and from the parasitoids themselves.3. Results revealed that A. colemani showed a wide variation in response to bacterial volatiles, ranging from significant attraction over no response to significant repellence. Our results further showed that the olfactory response of A. colemani to bacterial volatile emissions was different from that of D. aphidum. Gas chromatography-mass spectrometry analysis of the volatile blends revealed that bacterial strains repellent to A. colemani produced significantly higher amounts of esters, organic acids, aromatics and cycloalkanes than attractive strains. Strains repellent to D. aphidum produced significantly higher amounts of alcohols and ketones, whereas the strains attractive to D. aphidum produced higher amounts of the monoterpenes limonene, linalool and geraniol. 4. Overall, our results indicate that bacterial volatiles can have an important impact on insect olfactory responses, and should therefore be considered as an additional, so far often overlooked factor in studying multitrophic interactions between plants and insects. K E Y W O R D SAphidius colemani, chemical communication, Dendrocerus aphidum, microbial odour, multitrophic interactions, natural enemy, semiochemical, VOCs | 509 Functional Ecology GOELEN Et aL. Islam S. Sobhy https://orcid.org/0000-0003-4984-1823 Jetske G. de Boer https://orcid.org/0000-0002-3182-8543 Kevin J. Verstrepen https://orcid.org/0000-0002-3077-6219 Hans Jacquemyn https://orcid.org/0000-0001-9600-5794 Bart Lievens https://orcid.org/0000-0002-7698-6641 S U PP O RTI N G I N FO R M ATI O N Additional supporting information may be found online in the Supporting Information section. How to cite this article: Goelen T, Sobhy IS, Vanderaa C, et al. Volatiles of bacteria associated with parasitoid habitats elicit distinct olfactory responses in an aphid parasitoid and its hyperparasitoid. Funct Ecol. 2020;34:507-520. https ://doi.

Bacterial phylogeny predicts volatile organic compound composition and olfactory response of an aphid parasitoid

“…In this study, we have shown that phylogenetically related Bacillus strains tended to emit similar blends of mVOCs and elicited a comparable olfactory response in Aphidius colemani. The observed olfactory response was largely in agreement with results of a previous study where a smaller set of Bacillus strains was tested against the same parasitoid (Goelen et al 2020a), indicating the robustness of our bioassay and results. Furthermore, we identified the key mVOCs that significantly explained the phylogenetic signal.…”

“…An amount of 1.75 g NaCl was added to 5 ml of the samples and was kept at 60°C under constant agitation in a TriPlus RSH SMPE auto sampler. Volatile collection and separation conditions were as described previously (Goelen et al 2020a), and identification and quantification of the compounds was performed as in Reher et al (2019). Briefly, chromatograms were analysed using AMDIS ver.…”

“…Insect olfactory response was evaluated using the procedure described previously (Sobhy et al 2018, Goelen et al 2020a. A glass Y-tube olfactometer (base: 20 cm; arms:12 cm with a 60° angle at the Y-junction; inner diameter: 1.5 cm), connected to an air pump producing a unidirectional airflow of 400 ml min -1 from the arms to the base, was placed on a table that was homogeneously illuminated by four 24 W T5 TL-fluorescent tubes (16 × 549 mm, 1350 Lumen, 5500 K) at a height of 45 cm.…”

“…This chemical communication between insects and microorganisms is believed to drive a mutualistic relationship, in which not only the insects profit from the microorganisms, but also the microorganisms benefit from the insects by being dispersed to new niches where they can continue to develop or complete their life cycle (Um et al 2013, Christiaens et al 2014. Nevertheless, some mVOCs have been found to repel insects (Burkepile et al 2006, Stensmyr et al 2012, Goelen et al 2020a.…”

“…Recent Y-tube olfactometer bioassays have shown that olfactory responses of aphid parasitoids Aphidius colemani (Hymenoptera: Braconidae) to volatiles from bacteria occurring in the habitat of the parasitoids differed strongly between bacterial strains, ranging from significant attraction to repellence (Goelen et al 2020a). However, to what extent phylogenetic relationships between bacteria mediate mVOC composition and the olfactory response of parasitoids is less clear.…”