Aboveground herbivory can promote exotic plant invasion through intra‐ and interspecific aboveground–belowground interactions

• Published in: The New phytologist Vol. 237; no. 6; pp. 2347 - 2359
• Main Authors: Gao, Lunlun, Wei, Chunqiang, He, Yifan, Tang, Xuefei, Chen, Wei, Xu, Hao, Wu, Yuqing, Wilschut, Rutger A., Lu, Xinmin
• Format: Journal Article
• Language: English
• Published: England Wiley Subscription Services, Inc 01.03.2023
• Subjects: aboveground–belowground interactions; Agasicles hygrophila; Alternanthera philoxeroides; Alternanthera sessilis; Amaranthaceae; Animals; Beetles; Biological control; Biological invasions; Biota; China; Coleoptera; ecological invasion; herbivore; Herbivores; Herbivory; Introduced plants; Introduced Species; invasive plant; Invasive plants; invasive species; Larva; Larvae; Microbial activity; Microorganisms; plant invasions; Plants; plant–soil feedback; Soil; soil biota; Soil conditions; Soil microorganisms; Soils; China; aboveground-belowground interactions; soil biota; invasive plant; biological control; herbivore; plant-soil feedback; plant invasions
• ISSN: 0028-646X; 1469-8137; 1469-8137
• DOI: 10.1111/nph.18520

Summary Aboveground herbivores and soil biota profoundly affect plant invasions. However, how they interactively affect plant invasions through plant–soil feedbacks (PSFs) remains unclear. To explore how herbivory by the introduced beetle Agasicles hygrophila affects Alternanthera philoxeroides invasions in China, we integrated multiyear field surveys and a 2‐yr PSF experiment, in which we examined how herbivory affects PSFs on the performance of native and invasive plants and the introduced beetles. Despite increased herbivory from A. hygrophila, A. philoxeroides dominance over co‐occurring congeneric native Alternanthera sessilis remained constant from 2014 to 2019. While occurring at lower abundances, A. sessilis experienced similar herbivore damage, suggesting apparent competitive effects. Our experiments revealed that herbivory on A. philoxeroides altered soil microbial communities, prolonged its negative PSF on A. sessilis, and decreased A. hygrophila larvae performance on the next‐generation invasive plants. Consequently, A. hygrophila larvae performed better on leaves of natives than those of invasives when grown in soils conditioned by invasive plants defoliated by the introduced beetles. Our findings suggest that aboveground herbivory might promote rather than suppress A. philoxeroides invasion by enhancing its soil‐mediated self‐reinforcement, providing a novel mechanistic understanding of plant invasions. These findings highlight the need to incorporate an aboveground–belowground perspective during the assessment of potential biocontrol agents. See also the Commentary on this article by Antunes, 237: 1941–1942.