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.