Honeydew microbial ecology: A neglected frontier in multitrophic networks

Honeydew, the sugary excretion produced by sap-feeding Hemiptera, is one of the most common carbohydrate resources in many plant-based food webs. Honeydew supports a wide range of organisms, including ants, pollinators, (hyper-)parasitoids wasps, predatory insects, and microbes. As a sugar-rich resource, honeydew is frequently colonized by specific microbes (i.e., bacteria and fungi), which consume its sugars and other nutritional constituents. Recent research suggests that microbes within honeydew may modify its traits. Thereby driving microbial succession and acting as important "hidden players" in multitrophic ecological interactions. Yet its role as a dynamic microbial habitat remains largely unexplored. Here, we synthesize current evidence on the microbial ecology of honeydew and propose that honeydew is a dynamic rapidly changing microbial habitat. We further propose a four-stage successional model to frame its temporal dynamics. We discuss how the honeydew microbiome alters nutritional composition. Further, we discuss how the honeydew microbiome may mediate multitrophic interactions through the emission of volatile organic compounds that attract natural enemies of honeydew-producing insects. We propose that this process may pose a trade-off between the microbial secondary metabolism and its dispersal capacity of some microbes. We aim to stimulate research that will establish honeydew microbial ecology as a new frontier in plant-insect-microbe interactions.