Rapid climate warming in the tundra biome has been linked to increasing shrub dominance 1-4 . Shrub expansion can modify climate by altering surface albedo, energy and water balance, and permafrost 2,5-8 , yet the drivers of shrub growth remain poorly understood. Dendroecological data consisting of multi-decadal time series of annual shrub growth provide an underused resource to explore climate-growth relationships. Here, we analyse circumpolar data from 37 Arctic and alpine sites in 9 countries, including 25 species, and ∼42,000 annual growth records from 1,821 individuals. Our analyses demonstrate that the sensitivity of shrub growth to climate was: (1) heterogeneous, with European sites showing greater summer temperature sensitivity than North American sites, and (2) higher at sites with greater soil moisture and for taller shrubs (for example, alders and willows) growing at their northern or upper elevational range edges. Across latitude, climate sensitivity of growth was greatest at the boundary between the Low and High Arctic, where permafrost is thawing 4 and most of the global permafrost soil carbon pool is stored 9 . The observed variation in climate-shrub growth relationships should be incorporated into Earth system models to improve future projections of climate change impacts across the tundra biome.The Arctic is warming more rapidly than lower latitudes owing to climate amplification involving temperature, water vapour, albedo and sea ice feedbacks 5,7 . Tundra ecosystems are thus predicted to respond more rapidly to climate change than other terrestrial ecosystems 4 . The tundra biome spans Arctic and alpine regions that have similar plant species pools and mean climates, yet vary in topography, seasonality, land cover and glaciation history. Concurrent with the recent high-latitude warming trend 7 , repeat photography and vegetation surveys have shown widespread expansion of shrubs 1-3 , characterized by increased canopy cover, height and abundance. However, climate warming 7 and shrub increase 2,10 have not occurred at all sites. Models predict that warming of 2-10 • C (ref. 11) could convert as much as half of current tundra to 'shrubland' by the end of the twenty-first century 8 , but the uniformity of the frequently cited relationship between climate
Alpine dwarf shrub communities are phenologically linked with snowmelt timing, so early spring exposure may increase risk of freezing damage during early development, and consequently reduce seasonal growth. We examined whether environmental factors (duration of snow cover, elevation) influenced size and the vulnerability of shrubs to spring freezing along elevational gradients and snow microhabitats by modelling the past frequency of spring freezing events. We sampled biomass and measured the size of Salix herbacea, Vaccinium myrtillus, Vaccinium uliginosum and Loiseleuria procumbens in late spring. Leaves were exposed to freezing temperatures to determine the temperature at which 50% of specimens are killed for each species and sampling site. By linking site snowmelt and temperatures to long-term climate measurements, we extrapolated the frequency of spring freezing events at each elevation, snow microhabitat and per species over 37 years. Snowmelt timing was significantly driven by microhabitat effects, but was independent of elevation. Shrub growth was neither enhanced nor reduced by earlier snowmelt, but decreased with elevation. Freezing resistance was strongly species dependent, and did not differ along the elevation or snowmelt gradient. Microclimate extrapolation suggested that potentially lethal freezing events (in May and June) occurred for three of the four species examined. Freezing events never occurred on late snow beds, and increased in frequency with earlier snowmelt and higher elevation. Extrapolated freezing events showed a slight, non-significant increase over the 37-year record. We suggest that earlier snowmelt does not enhance growth in four dominant alpine shrubs, but increases the risk of lethal spring freezing exposure for less freezing-resistant species.
Summary1. Current changes in shrub abundance in alpine and arctic tundra ecosystems are primarily driven by climate change. However, while taller shrub communities are expanding, dwarf shrub communities show reductions under climate warming, and the mechanisms driving the latter (such as warming temperatures or accelerated spring snowmelt) may be complex. 2. To determine and disentangle the response of a widespread arctic-alpine prostrate dwarf shrub to both climate warming and changes in snowmelt time, we investigated phenology, clonal and sexual reproduction, leaf size, wood tissue carbon balance and leaf damage in 480 patches of Salix herbacea, along its elevational and snowmelt microhabitat range over 3 years in a space-for-time substitution. 3. Earlier snowmelt was associated with longer phenological development periods, an increased likelihood of herbivory and fungal damage, lower stem density, smaller leaves and lower end-of-season wood reserve carbohydrates. Furthermore, while early snowmelt was associated with an increased proportion of flowering stems, the proportion of fruiting stems was not, as fruit set decreased significantly with earlier snowmelt. Warmer temperatures at lower elevations were associated with lower stem numbers and larger leaves. 4. Synthesis. Our study indicates that phenology, fitness proxies and fungal/insect damage of the dwarf shrub S. herbacea are strongly influenced by snowmelt timing, and that earlier spring snowmelt reduced performance in S. herbacea. The likely mechanisms for many of the observed patterns are related to adverse temperature conditions in the early growing season. Reductions in clonal (stem number) and sexual reproduction (reduced fruit set) under earlier snowmelt, in addition to increasing damage probability, will likely lead to lower fitness and poorer performance, particularly in shrubs growing in early-exposure microhabitats. Further, we saw few concurrent benefits of higher temperatures for S. herbacea, particularly as warming was associated with lower clonal growth. As growing seasons become warmer and longer in arctic and alpine tundra ecosystems, early snowmelt is a critical mechanism reducing fitness and performance in a widespread dwarf shrub and may ultimately reduce dwarf shrub communities in tundra biomes.
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