Soil microbes from herbivory-damaged native congener impair invasive plant tolerance to biocontrol

Abstract Classical biocontrol of invasive plants often fails due to their high tolerance to herbivore damage. While it directly affects plants, herbivory can also indirectly influence soil microbes. However, whether herbivory-induced shifts in the soil microbiome further modulate invasive plant tolerance and how these interactions differ from native plants remain unclear. We performed a plant-soil feedback experiment with invasive Alternanthera philoxeroides, its native congener Alternanthera sessilis, and the biocontrol beetle Agasicles hygrophila. In Phase I, plants of each species were exposed to herbivory or control, and soils were collected for fungal community analysis at the end of this phase. In Phase II, A. philoxeroides was grown in these conditioned soils under herbivory or control. Compared with the no-herbivory control, herbivory significantly increased the relative abundance of soil pathogens in A. sessilis-conditioned soils but had no effect on A. philoxeroides-conditioned soils. Consequently, A. philoxeroides exhibited significantly lower tolerance when grown in herbivory-conditioned A. sessilis soil than in soils conditioned by unexposed A. sessilis or herbivory-exposed/unexposed A. philoxeroides. Further analysis revealed that tolerance decreased significantly with increasing relative abundance of soil pathogens. Our findings demonstrate that herbivory on the native congener creates a pathogen-enriched soil legacy that is strongly associated with impaired invader tolerance. In contrast, herbivory on the invader itself leaves soil pathogens unchanged, a scenario which coincides with sustained compensatory growth. This highlights the critical role of plant-specific soil microbial legacies in mediating biocontrol outcomes and suggests that disrupting the stable soil microbiome of invaders could improve their management efficacy.