Warming-induced shift in European mushroom fruiting phenology

Abstract

In terrestrial ecosystems, fungi are the major agents of decomposition processes and nutrient cycling and of plant nutrient uptake. Hence, they have a vital impact on ecosystem processes and the terrestrial carbon cycle. Changes in productivity and phenology of fungal fruit bodies can give clues to changes in fungal activity, but understanding these changes in relation to a changing climate is a pending challenge among ecologists. Here we report on phenological changes in fungal fruiting in Europe over the past four decades. Analyses of 746,297 dated and geo-referenced mushroom records of 486 autumnal fruiting species from Austria, Norway, Switzerland, and the United Kingdom revealed a widening of the annual fruiting season in all countries during the period 1970-2007. The mean annual day of fruiting has become later in all countries. However, the interspecific variation in phenological responses was high. Most species moved toward a later ending of their annual fruiting period, a trend that was particularly strong in the United Kingdom, which may reflect regional variation in climate change and its effects. Fruiting of both saprotrophic and mycorrhizal fungi now continues later in the year, but mycorrhizal fungi generally have a more compressed season than saprotrophs. This difference is probably due to the fruiting of mycorrhizal fungi partly depending on cues from the host plant. Extension of the European fungal fruiting season parallels an extended vegetation season in Europe. Changes in fruiting phenology imply changes in mycelia activity, with implications for ecosystem function.

Fig. 1.

Relationship between start of fruiting season and end of season for all species during the period 1970–2007. Changes in start and end of season are shown as the regression coefficients of the 2.5th and 97.5th percentiles as a function of year. Red circles indicate species with statistically significant changes. Upper left quadrants represent species with earlier start and later end dates, upper right quadrants have later start and later end dates, lower left quadrants have earlier start and earlier end, and lower right quadrants have later start and earlier end. The potential influence of varying sampling intensities (ln(N + 1)) is accounted for in these models.

Fig. 2.

The number of days of change in start, mean, and end of fruiting season during the period 1970–2007, averaged over all species and split according to countries and nutritional mode (saprotrophic or ECM). The 2.5th percentiles reflect changes in season start and the 97.5th percentiles changes in season end. The sampling intensities are accounted for within the model, and the plots here illustrate the expected trends at average intensities, ln(N + 1) = 2.2 ∼ 10 individuals per year. Abbreviations: AUT, Austria; ECM, ectomycorrhizal fungi; NOR, Norway; sapro, saprotrophic fungi; SWI, Switzerland.

Fig. 3.

Expected changes in start, mean, and end fruiting time for the period 1970–2010 in the four different countries plotted against the species-averaged fruiting day. The annual fruiting time is calculated for each species across the period 1970–2010. Cubic smooth spline functions describe the relationship between mean annual fruiting date (calculated for the period 1970–1985) and temporal changes in start, mean, and end of fruiting season in the four countries. The blue line represents the average smoothed trend, and the red lines correspond to 95% confidence intervals. The thin black line represents a linear trend using a classic least-squares procedure. The asterisks indicate the significance level of the linear models, where 0.05>*>0.001>**. The models here include a term for the sampling intensities, and the trends are all calculated assuming constant mean sampling intensities (ln(N + 1) = 2.2).

Fig. 4.

Summary of the estimated number of days of change in fruiting time for early-fruiting and late-fruiting species in the four countries during the period 1970–2010. We define early and late fruiters as mean normalized fruiting time of 30 d earlier or later than the overall mean normalized fruiting day. From the linear model of days of change vs. initial fruiting day (Fig. 3) we calculate the number of days changed for the early fruiters (−30) and late fruiters (+30). This calculation provides the direction and length of the arrows. To simplify visualization we calculate the range of fruiting period of those species considered earlier or later during the initial period (1970–1985). The black and red bars represent the calculated range of fruiting times at the start (1970, black) and end (2010, red) of the period. Black and red circles represent the estimated average fruiting times in the start (1970, black) and end (2010, red) of the period. The models behind the illustrations account for differentiated sampling strategies, and the illustrations are based on calculations from models assuming an average sampling intensity (ln(N + 1) = 2.2).