Roles of aphid honeydew associated bacteria in multitrophic interactions

The honeydew excreted by aphids serves as a carbohydrate source for several beneficial insects and various microorganisms. Microbial volatile organic compounds (mVOCs) have the potential to play diverse roles in herbivore-microbe-natural enemy multitrophic interactions, offering possibilities for further applications in integrated pest management (IPM). This thesis aims to utilize aphid honeydew-associated microorganisms and their mVOCs to enhance the efficacy of natural enemies, then developing alternative strategies for efficient and sustainable aphid biological control.The structure of this thesis encompasses a general introduction to honeydew and aphids (Chapter I), a comprehensive review summarizing interactions between aphids and microbiota from ecological perspectives to new opportunities for improving biological control efficacy (Chapter II). The core chapters (Chapter III-V) focus on selecting specific functional compounds from honeydew-associated bacteria, aiming to attract predators and parasitic wasps for aphid control. The thesis concludes with a discussion, an outlook on future research, and a general conclusion (Chapter VI). While existing studies have predominantly focused on honeydew microbial volatiles for host location by hoverflies, the function of chemical cues from aphid honeydew-associated microbes on predatory ladybirds remains largely unknown. In Chapter III, we present the first evidence of Asian ladybirds Harmonia axyridis using mVOCs, namely 4-methylpentan-2-ol and 6-methylhept-5-en-2-one emitted from Sitobion miscanthi honeydew bacteria Erwinia tasmaniensis MH4 and Klebsiella quasipneumoniae subsp. similipneumoniae MH6, to locate their preys. These bacteria and mVOCs hold potential for eco-friendly aphid pest control strategies, deepening our understanding of H. axyridis foraging behavior in response to honeydew-associated mVOCs. In Chapter IV, we found that S. miscanthi honeydew also can significantly attract the parasitic wasp Aphidius gifuensis. One bacterial strain, L. fusiformis MH1, was identified as the most attractive to A. gifuensis. Two compounds, namely 1-ethyl-2-methylbenzene and 2-butyl-1-octanol, emitted from L. fusiformis MH1, were attractive to A. gifuensis. Application of L. fusiformis MH1 and functional mVOC formulations in crop fields resulted in a significant decrease in aphid abundance, associated with higher ladybird and parasitoid abundance compared to the control (Chapter V). The relevance of this research project and the general context are discussed at the end of this thesis in Chapter VI. Taken as a whole, this thesis underlines the I importance of honeydew-associated microorganism for manipulating herbivore-natural enemy multitrophic interactions and have the potential to be developed as a novel environmentally friendly biological control method for aphids.