Enhanced shrub growth in a warming alpine climate has potential far-reaching implications, including soil nutrient cycling, carbon storage, or water and surface energy exchanges. Growth ring analysis can yield mid-to long-term, annually resolved records of shrub growth, and thereby offer valuable insights into how growth is driven by interannual climate variability. In the European Alps, dendroecological approaches have shown that dwarf shrub productivity is influenced by interannual variations of growing season temperature but results also point to a negative effect of winter precipitation on radial growth. However, as past work lacked snow cover data, links between snow cover duration, growing season length, energy availability and inter-annual shrub growth remain poorly understood. In this paper, we combined multi-decadal shrub-ring series from 49 individuals sampled at three sites along a 600-m elevational gradient in the Taillefer massif, located in the French Alps to assess growth sensitivity of long-lived and widespread Rhododendron ferrugineum shrubs to 2 both snow cover dynamics and temperature changes. To this end, we computed structural equation models to track the response of shrub radial growth to extending growing season at 1800, 2000 and 2400 m above sea level and for two time periods (i.e. 1959-1988 and 1989-2016). The second period is marked by a significant advance in snow melt-out resulting in a regime shift highlighted at the end of the 1980s by a breakpoint analysis. At the high-elevation site, our results demonstrate a positive effect of increasing growing season length on shrub growth, which is strongly dependent on snowpack depth and snow cover duration. Conversely, at lower elevations, earlier melt-out dates and associated late frost exposure are shown to lead to radial growth reduction. Moreover, the climate signal in ringwidth chronologies of R. ferrugineum portrays a weakening since 1988similar to a phenomenon observed in series from circumpolar and alpine tree-ring sites and referred to as "divergence". By analyzing long-term records of radial growth along an elevation gradient, our work provides novel insights into the complex responses of shrub growth to climate change in alpine environments. This paper demonstrates that R. ferrugineum, as a dominant alpine shrub species, behave as an ecological indicator of the response of alpine ecosystem to global warming.

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PREMISE:Mountain ecosystems are particularly sensitive to climate change. However, only a very small number of studies exist so far using annually resolved records of alpine plant growth spanning the past century. Here we aimed to identify the effects of heat waves and drought, driven by global warming, on annual radial growth of Rhododendron ferrugineum. METHODS:We constructed two century-long shrub ring-width chronologies from R. ferrugineum individuals on two adjacent, north-and west-facing slopes in the southern French Alps. We analyzed available meteorological data (temperature, precipitation and drought) over the period 1960-2016. Climate-growth relationships were evaluated using bootstrapped correlation functions and structural equation models to identify the effects of rising temperature on shrub growth. RESULTS: Analysis of meteorological variables during 1960-2016 revealed a shift in the late 1980s when heat waves and drought increased in intensity and frequency. In response to these extreme climate events, shrubs have experienced significant changes in their main limiting factors. Between 1960 and 1988, radial growth on both slopes was strongly controlled by the sum of growing degree days during the snow free period. Between 1989 and 2016, August temperature and drought have emerged as the most important. CONCLUSIONS: Increasing air temperatures have caused a shift in the growth response of shrubs to climate. The recently observed negative effect of high summer temperature and drought on shrub growth can, however, be buffered by topographic variability, supporting the macro-and microrefugia hypotheses.

In the European Alps, air temperature has increased almost twice as much as the global average over the last century and, as a corollary, snow cover duration has decreased substantially. In the Arctic, dendroecological studies have evidenced that shrub growth is highly sensitive to temperature—this phenomenon has often been linked to shrub expansion and ecosystem greening. Yet, the impacts of climate change on mountain shrub radial growth have not been studied with a comparable level of detail so far. Moreover, dendroecological studies performed in mountain environments did not account for the potential modulation and/or buffering of global warming impacts by topography, despite its possible crucial role in complex alpine environments. To fill this gap, we analyzed a network of eight sites dominated by the dwarf shrub Rhododendron ferrugineum. The sites selected for analysis represent the diversity of continentality, elevation and slope aspect that can be found across the French Alps. We quantified annual radial increment growth for 119 individuals, assembled meteorological reanalyzes specifically accounting for topographic effects (elevation, slope and aspect) and assessed climate-growth relations using a mixed modeling approach. In agreement with a vast majority of dendroecological work conducted in alpine and arctic environments, we find that the number of growing degree days during the snow-free period snow-free growing degree days (SFGDDs) is a strong and consistent driver of R. ferrugineum growth across all sites since 1960 until the late 1980s. We also document a marked loss of sensitivity of radial growth to increasing SFGDD since the 1990s, with this decoupling being more pronounced at the driest sites. Our observations of the spatial and temporal variability of shrub sensitivity to limiting factors can be compared to the ‘divergence’ problem observed in tree-ring series from circumpolar and alpine regions and, accordingly, sheds light on possible future trajectories of alpine shrub growth in response to ongoing climate change.

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IntroductionMean xylem vessel or tracheid area have been demonstrated to represent powerful proxies to better understand the response of woody plants to changing climatic conditions. Yet, to date, this approach has rarely been applied to shrubs.MethodsHere, we developed a multidecadal, annually-resolved chronology of vessel sizes for Rhododendron ferrugineum shrubs sampled at the upper shrubline (2,550 m asl) on a north-facing, inactive rock glacier in the Italian Alps.Results and DiscussionOver the 1960-1989 period, the vessel size chronology shares 64% of common variability with summer temperatures, thus confirming the potential of wood anatomical analyses on shrubs to track past climate variability in alpine environments above treeline. The strong winter precipitation signal recorded in the chronology also confirms the negative effect of long-lasting snow cover on shrub growth. By contrast, the loss of a climate-growth relation signal since the 1990s for both temperature and precipitation, significantly stronger than the one found in radial growth, contrasts with findings in other QWA studies according to which stable correlations between series of anatomical features and climatic parameters have been reported. In a context of global warming, we hypothesize that this signal loss might be induced by winter droughts, late frost, or complex relations between increasing air temperatures, permafrost degradation, and its impacts on shrub growth. We recommend future studies to validate these hypotheses on monitored rock glaciers.

Shrub dendrochronology is gaining increasing momentum in temperate high mountain regions to decipher climatic controls on current shrub expansion. Yet, a lack of consensus still persists in terms of sampling protocols, thus hampering comparability of results from different studies. For instance, serial sectioning, i.e. the sampling of multiple sections along the same shrub stem is recommended as it increases the detection of partial and missing rings, but has only been employed in few studies as it is time-consuming. Similarly, as a result of serial sectioning, chronologies frequently combine sections sampled at different positions along the stem and at the root collar which hinders the detection of climatic signals. Here, we used cross-sections sampled on 21 Rhododendron ferrugineum shrubs from the French Pyrenees to define a parsimonious protocol enabling detection of partial and missing rings while increasing the strength of the climate signal in the shrub ring chronology. We demonstrate that partial and missing rings are almost evenly distributed along Rhododendron ferrugineum stems and that they can be detected optimally using two sections on which growth rings are measured along three radii. Our results also evidence that chronologies which include only ring-width series from basal sections more strongly integrate summer temperature fluctuations than stem-based or mixed chronologies. Noteworthy, the snowpack signal is stronger in chronologies with individuals from the upper stem sections. Overall, our results confirm that sampling design - serial sectioning and caution in ring-width series aggregation - is key to ensure robustness of dendroecological studies on dwarf shrubs in alpine environments.