Fairy rings caused by a killer fungus foster plant diversity in species‐rich grassland

Questions Does the fairy ring fungus Agaricus campestris affects spatial distribution of co‐existing plant species? Is ring development related to changes of soil physical, chemical, enzymatic and microbiological properties? What are the causes of weakening and subsequent luxuriance of vegetation during fairy ring dynamics in the soil? Location Species‐rich, mowed calcareous grassland, central Italy (43° 17′26″ N, 12° 51′29″ E). Methods Fairy rings were monitored for total plant biomass, species richness and composition in four zones: external grassland (OUT), fungal front (FF), area with flourishing vegetation (BELT) and internal grassland (IN). In each zone, 17 soil parameter were analysed: physical and chemical properties (water‐holding capacity, pH, electrical conductivity, organic C, Olsen P, total N, NH 4 + , NO 3 − , hydrophobicity and cyanide concentration), total enzyme activity (FDA) and microbiological features (community‐level physiological profile using BIOLOG EcoPlates ™ , microbial biomass, fungal mycelium, culturable actinomycetes, bacteria and fungi). A bioassay was performed to evaluate responses of three co‐existing species ( Bromus erectus , Cynosurus echinatus and Centaurea ambigua ) growing on soil collected from different fairy ring zones. Results Plant species composition dramatically changed in response to fairy ring development, with disappearance of most grassland species in the ring‐affected area. Plant biomass and species richness were higher in OUT and IN areas, and lowest in FF. Profound changes in soil properties occurred after fungal passage, with consistent reductions of C and N content and increases of FDA and microbial physiological profiles. Soil from the FF zone had remarkable increases of mineral N forms, electrical conductivity and hydrophobicity, with no trace of cyanide. The bioassay showed species‐specific responses to different soil types. Conclusions This study provides evidence that the spread of fairy ring fungi, coupled with a reduction of perennial plant cover, creates empty niches for many short‐lived species.