Phenological and elevational shifts of plants, animals and fungi under climate change in the <scp>E</scp>uropean <scp>A</scp>lps

Mountain areas are biodiversity hotspots and provide a multitude of ecosystem services of irreplaceable socio-economic value. In the European Alps, air temperature has increased at a rate of about 0.36°C decade^-1 since 1970, leading to glacier retreat and significant snowpack reduction. Due to these rapid environmental changes, this mountainous region is undergoing marked changes in spring phenology and elevational distribution of animals, plants and fungi. Long-term monitoring in the European Alps offers an excellent natural laboratory to synthetize climate-related changes in spring phenology and elevational distribution for a large array of taxonomic groups. This review assesses the climatic changes that have occurred across the European Alps during recent decades, spring phenological changes and upslope shifts of plants, animals and fungi from evidence in published papers and previously unpublished data. Our review provides evidence that spring phenology has been shifting earlier during the past four decades and distribution ranges show an upwards trend for most of the taxonomic groups for which there are sufficient data. The first observed activity of reptiles and terrestrial insects (e.g. butterflies) in spring has shifted significantly earlier, at an average rate of -5.7 and -6.0 days decade^-1 , respectively. By contrast, the first observed spring activity of semi-aquatic insects (e.g. dragonflies and damselflies) and amphibians, as well as the singing activity or laying dates of resident birds, show smaller non-significant trends ranging from -1.0 to +1.3 days decade^-1 . Leaf-out and flowering of woody and herbaceous plants showed intermediate trends with mean values of -2.4 and -2.8 days decade^-1 , respectively. Regarding species distribution, plants, animals and fungi (N = 2133 species) shifted the elevation of maximum abundance (optimum elevation) upslope at a similar pace (on average between +18 and +25 m decade^-1 ) but with substantial differences among taxa. For example, the optimum elevation shifted upward by +36.2 m decade^-1 for terrestrial insects and +32.7 m decade^-1 for woody plants, whereas it was estimated to range between -1.0 and +11 m decade^-1 for semi-aquatic insects, ferns, birds and wood-decaying fungi. The upper range limit (leading edge) of most species also shifted upslope with a rate clearly higher for animals (from +47 to +91 m decade^-1 ) than for plants (from +17 to +40 m decade^-1 ), except for semi-aquatic insects (-4.7 m decade^-1 ). Although regional land-use changes could partly explain some trends, the consistent upward shift found in almost all taxa all over the Alps is likely reflecting the strong warming and the receding of snow cover that has taken place across the European Alps over recent decades. However, with the possible exception of terrestrial insects, the upward shift of organisms seems currently too slow to track the pace of isotherm shifts induced by climate warming, estimated at about +62 to +71 m decade^-1 since 1970. In the light of these results, species interactions are likely to change over multiple trophic levels through phenological and spatial mismatches. This nascent research field deserves greater attention to allow us to anticipate structural and functional changes better at the ecosystem level.