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

Abstract

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.

<em>Ficus tikoua </em>Bur. May Have Resistance to Invasive Plant <em>Alternanthera philoxeroides</em>

“…Hu et al, (2023) conducted an experiment to investigate the latitudinal and longitudinal allelopathic patterns of A. philoxeroides in China, finding that the allelopathic effects increased with latitude and decreased with longitude, and were determined by soluble protein (SP), free amino acids (FAA), plant polyphenol (PP), phosphorus (P) and potassium (K) contents of leaf, suggesting potential control strategies for reducing the component contents in the plant tissues. Recently, Gao et al,(2023) proposed that aboveground herbivory can facilitate the invasion of A. philoxeroides via both intra-and interspecific aboveground-belowground interactions based on multiyear field surveys and a 2-years plant-soil feedbacks (PSF) experiment. However, the interaction between native plants and invasive plants was not given much attention.…”

Leaf litter presence in the non‐growing season prolongs plant legacy effects on soil fungal communities and succeeding plant growth

“…For instance, the poorer performance of plants in conspecific‐conditioned soils than in heterospecific‐conditioned soils, for example, due to the accumulation of host‐specific below‐ground enemies, may promote species coexistence (Bever et al, 1997; Kandlikar et al, 2019). On the contrary, the poorer performance of plants in heterospecific‐conditioned soils than in conspecific‐conditioned soils, for example, due to spillover of generalist enemies and the presence of non‐compatible mutualists, may promote species dominance and alien plant invasions (Callaway et al, 2004; Gao et al, 2023). Differences in such plant responses to conspecific‐ and heterospecific‐conditioned soils may also depend on the phylogenetic distance between the examined plant species.…”

“…Due to evolutionary novelty, some alien species develop distinct rhizosphere communities and, compared to native plants, are differently affected by soil biota. For instance, some alien species accumulate abundant soil‐borne enemies that asymmetrically suppress native, but not alien, plants (Callaway et al, 2004; Gao et al, 2023), or establish novel associations with resident soil mutualists (Callaway et al, 2011), likely promoting their invasion. In a meta‐analysis, Zhang et al (2019) found that alien plant species alter the biomass and abundance of resident soil biota (including bacteria, detritivores and microbivores) differently through rhizosphere and litter inputs.…”

Uncovering subtle mechanisms hindering the efficacy of biological control in plant invasions

“…An article published in this issue of New Phytologist by Gao et al . (2023; pp. 2347–2359) is unique because it meets all of these requirements.…”

“…Undertaking this work demands additional and sustained funding for long-term, complex and resource-intensive studies at different ecological scales. An article published in this issue of New Phytologist by Gao et al (2023;pp. 2347-2359) is unique because it meets all of these requirements.…”