The fellowship of the ring: Species-associated effects of fairy ring fungi on soil, microbiota and vegetation in a managed ornamental grassland

Abstract

Fairy ring-forming fungi may alter soil physicochemical properties through mycelial decomposition of organic matter, with potential cascading effects on plants and soil microbiota. This study investigated fairy rings formed by three co-occurring fungal species, Marasmius oreades, Amanita vittadinii, and Clitocybe collina, in the ornamental grassland of the Royal Palace of Caserta. Along outer, active-front, and inner transect zones, we assessed fungal DNA distribution, vegetation, soil physicochemical properties, and soil microbial communities through metabarcoding. Reads assigned to the dominant fairy ring-forming fungi peaked at the active fungal front and remained detectable in inner soils, consistently with the persistence of fungal residues after mycelial passage and with a model of centrifugal ring development associated with self-DNA accumulation. Across the three species, the active front showed a common functional syndrome, including increased CO₂ flux, soil acidification and nutrient mobilization. However, the ecological consequences, in terms of impact on biological communities, differed among fungal species and were consistent with distinct decomposition-related strategies. M. oreades was associated with high soil hydrophobicity and showed the strongest effects on both vegetation and soil microbial communities, supporting its recognition as the only clear ecosystem engineer in this system. A. vittadinii mainly promoted nutrient release and soil biochemical changes, whereas C. collina was consistent with lower decomposition intensity and produced weak or negligible effects on the managed ornamental grassland biota. Overall, the co-occurrence of different fairy ring-forming fungi within the same field conditions revealed both shared front-related processes and species-associated differences in their impacts on grassland biota.