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Honeydew, a sugary excretion produced by sap‐feeding insects, plays a pivotal role in shaping intricate interactions between insects and plants. This review explains the multifaceted aspects of honeydew, beginning with an overview of its production mechanisms and factors influencing its variability across insect species and plant hosts. Exploring its composition, we examine the chemical components and nutritional aspects, highlighting variations based on insect species and plant sources. The impact of honeydew on microbial communities is explored, shedding light on its role in influencing the diversity and abundance of microorganisms. Furthermore, the review investigates how honeydew affects pest behaviour and population dynamics, elucidating plant responses to honeydew deposition. In the realm of biocontrol, we examine the intricate relationships between honeydew and natural enemies, considering potential implications for integrated pest management. Beyond these individual components, the paper discusses the broader ecological consequences of honeydew in ecosystems, emphasizing the interconnected relationships between insects, plants and microorganisms. The review concludes by identifying research gaps and suggesting future directions, recognizing the need for further investigation into areas with potential applications for agriculture and ecology. This review provides a comprehensive synthesis of the current understanding of honeydew's significance in insect–plant interactions, offering insights for both researchers and practitioners in the field. [ABSTRACT FROM AUTHOR]

Herbivore feeding often increases secondary metabolite production in plants. These herbivore‐induced plant proteins might end up in honeydew excreted by phloem‐feeding insects. This is important because honeydew is one of the most abundant and accessible carbohydrate sources for natural enemies in many agroecosystems and these proteins can thus mediate many tri‐trophic interactions. Here, we hypothesized that defensive metabolites induced in the phloem by herbivory accumulate in the honeydew excreted by phloem‐feeding insects and, consequently, affect the fitness of the herbivores' natural enemies that feed on it. We used a tri‐trophic system consisting of citrus plants, the mealybug Planococcus citri and its primary parasitoid Anagyrus vladimiri. First, we assessed A. vladimiri fitness when fed on P. citri honeydew. We then collected honeydew of seven phloem‐feeding insects, including P. citri, and analysed their protein content. Finally, we analysed the effect of superoxide dismutase (SOD), an antioxidant enzyme associated with plant defences that was commonly found in the analysed honeydews, on A. vladimiri fitness. The fitness of A. vladimiri increased when fed on honeydew compared to a sucrose‐based diet, demonstrating that honeydew can contain compounds that benefit natural enemies. Proteomic analyses showed that defence‐related plant proteins were present in honeydew of seven phloem‐feeding insects analysed. Among these, the enzyme SOD was present in honeydew of all of them. Moreover, the levels of SOD were 10‐fold higher in the phloem of plants infested by P. citri than in that of uninfested plants. SOD was also actively excreted in P. citri honeydew, and we proved that it increases the fecundity of the parasitoid A. vladimiri. We conclude that enzymatic proteins induced by herbivory in the phloem and involved in plant defence, accumulate in the honeydew excreted by phloem‐feeding insects and, contrary to the current paradigm, at least some of these can have positive effects on the third trophic level. Read the free Plain Language Summary for this article on the Journal blog. [ABSTRACT FROM AUTHOR]