Fungal-based soil food webs, not local plant nor abiotic properties, are most affected by rhizome-derived secondary metabolites of Japanese knotweed (Reynoutria japonica)

Abstract

Plant invasions are a major threat to native biodiversity. Allelopathy often plays an important role in suppressing native plants and soil organisms. Effects of these secondary metabolites on plant and soil micro-organisms are rather well known. However, the effects of allelopathy on several soil biota components, either direct or indirectly through alterations of basal resources, are still unresolved. Japanese knotweed (Reynoutria japonica), an east-Asian species, contains allelopathic secondary compounds inhibiting native plants and microbial communities in Europe. We conducted a comprehensive study to unravel the role of allelopathic compounds released by this species in shaping above (germination and growth of 9 different local species) and belowground (soil microbiota and fauna) assemblages. The experiment was designed to include or exclude secondary metabolites through activated carbon filtration of Japanese knotweed rhizome extract. After a three-month garden trial, fungal biomass remained unaffected, whereas bacterial biomass, several nematode trophic groups: bacterivores, fungivores, omnivorous-predators, and Collembola density, all declined in response to the extract. These negative effects were directly attributable to the allelopathic secondary compounds. Structural equation modeling revealed major changes in soil food-web structure, with a positive correlation between bacteria and bacterivores but a clear negative effect of allelopathy on the fungal- and Collembola-based energy channels. Interestingly, Japanese knotweed rhizome extract had little influence on local plant biomass and germination rates, indicating a decoupling between plant performance and belowground biological responses. Our study highlights the need to account for soil biota when assessing the ecological risks of invasive plants and developing management and restoration practices.