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

Abstract

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.

Host diversity and trophic status as determinants of species richness and community composition of fungus gnats

“…The reasons for ectomycorrhizal and saprotrophic fungi hosting distinct fungus gnat communities likely stem from differences in their nutritional strategies. These apparently cause variation in fruitbodies chemical composition, formation period, duration and seasonal predictability (Sato et al 2012). The fruitbodies of ectomycorrhizal and saprotrophic fungi differ mostly in carbon (C) and nitrogen (N) isotope ratios, with higher C and lower N content in saprotrophs (Taylor et al 2003).…”

“…However, the lack of standardisation of sample sizes may conversely have led to some frequent species erroneously being considered polyphagous. Moreover, mushroom-forming fungi can further be divided into functional guilds with distinct ways of obtaining carbohydrates, suggested to affect fruiting phenology and community structure of fungus-associated organisms (Sato, Morimoto, & Hattori, 2012). Neither mushroom-fungivore community relationships nor the distinction of specialist and generalist fungivores have been investigated in any empirical study.…”

“…The effect could be weak if the extent of polyphagy suggested for unpredictable hosts holds true. However, as persisting spatial fruitbody patterns are known for many mushroom species (Worthen & McGuire 1990;Sato et al 2012), higher levels of host specialisation among fungus gnats cannot be excluded. The few ecological studies available that report varying fungus gnat richness or abundance between habitats, years and seasons (Økland 1994;Økland et al 2005;Yakovlev 1995), lack or do not extrapolate on host data.…”

Mushroom biomass and diversity are driven by different spatio-temporal scales along Mediterranean elevation gradients

“…Here, the greater fraction of variance for ectomycorrhizal fungi occurred between years (44% and 43% for biomass and richness, respectively), whereas for saprotrophic fungi the greater fraction occurred between plots (56% and 54% for biomass and richness, respectively). It is well known that ectomycorrhizal and saprotrophic fungi differ in methods for obtaining carbon and other nutrients which affects their fruiting39. Ectomycorrhizal fungi are root symbionts that rely on photosynthate carbon flux from host plants16.…”

“…sustaining leaf biomass and its turnover41, and reducing the amounts available for the mycorrhizal fungi42. Therefore, yearly seasonal variations in host plants photosynthetic rates determine the available carbohydrates which are accessible for ectomycorrhizal fungal fruiting39. In contrast, saprotrophic fungi are decomposers obtaining carbon directly from organic matter (leaf litter and coarse woody debris)43, which are clearly reliant on plot-level processes involved in wood debris and leaf litter production.…”