A Thirty-Year Survey Reveals That Ecosystem Function of Fungi Predicts Phenology of Mushroom Fruiting

Mushroom fruiting, the reproduction of fungi, has broad implications for forest health, terrestrial biomass turnover, and global carbon cycle. However, little is known about the difference in phenology and environmental drivers of mushroom fruiting between functional guilds, e.g., ectomycorrhizal (ECM) mutualists and saprotrophs (SAP). There is a remarkable difference between ECM and SAP fungi in their available carbon sources and lifecycles, and thus these fungal groups are likely to differ in fruiting phenology. We analyzed intra- and inter-annual phenological patterns of mushroom fruiting throughout the year using a long-term census dataset of mushroom-forming fungi in a Japanese oak forest in which a total of 11,923 mushroom counts (668 species) were recorded during monthly intervals from 1982 to 2011. ECM fungi showed a unimodal seasonal fruiting peak from mid-summer to early autumn; litter-decomposing fungi showed moderate fruiting peaks from early summer or early autumn, and the phenology of wood-decomposing fungi varied considerably among the genera. Each functional group was controlled by a different set of external factors; temperature and rainfall increased ECM fungal fruiting, but key factors substantially differed among the genera of litter- and wood-decomposing fungi in taxon-specific ways. Our results suggest that fungal fruiting phenology may be affected by the seasonality of carbohydrate availability. The highly scheduled reproduction of ECM fungi may reflect temperature-dependent increases and drought-induced decreases of photosynthetic activity in host plants rather than improved growth conditions for fungi during the summer. We argue that the way a fungus obtains carbohydrates may explain a substantial fraction of the fruiting phenology, which may make a differential contribution to the community structure of fungus-associated organisms and terrestrial biomass turnover based on fungal functional groups.