Phenological and elevational shifts of plants, animals and fungi under climate change in the European Alps.

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phenological changes and upslope shifts of plants, animals and fungi from evidence in published papers and previously unpublished data.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.

Best environmental predictors of breeding phenology differ with elevation in a common woodland bird species.

Temperatures in mountain areas are increasing at a higher rate than the Northern Hemisphere land average, but how fauna may respond, in particular in terms of phenology, remains poorly understood. The aim of this study was to assess how elevation could modify the relationships between climate variability (air temperature and snow melt-out date), the timing of plant phenology and egg-laying date of the coal tit (Periparus ater). We collected 9 years (2011-2019) of data on egg-laying date, spring air temperature, snow melt-out date, and larch budburst date at two elevations (~1,300 m and ~1,900 m asl) on a slope located in the Mont-Blanc Massif in the French Alps. We found that at low elevation, larch budburst date had a direct influence on egg-laying date, while at high-altitude snow melt-out date was the limiting factor. At both elevations, air temperature had a similar effect on egg-laying date, but was a poorer predictor than larch budburst or snowmelt date. Our results shed light on proximate drivers of breeding phenology responses to interannual climate variability in mountain areas and suggest that factors directly influencing species phenology vary at different elevations. Predicting the future responses of species in a climate change context will require testing the transferability of models and accounting for nonstationary relationships between environmental predictors and the timing of phenological events.

Warm temperatures during cold season can negatively affect adult survival in an alpine bird.

Climate seasonality is a predominant constraint on the lifecycles of species in alpine and polar biomes. Assessing the response of these species to climate change thus requires taking into account seasonal constraints on populations. However, interactions between seasonality, weather fluctuations, and population parameters remain poorly explored as they require long-term studies with high sampling frequency. This study investigated the influence of environmental covariates on the demography of a corvid species, the alpine chough Pyrrhocorax graculus, in the highly seasonal environment of the Mont Blanc region. In two steps, we estimated: (1) the seasonal survival of categories of individuals based on their age, sex, etc., (2) the effect of environmental covariates on seasonal survival. We hypothesized that the cold season-and more specifically, the end of the cold season (spring)-would be a critical period for individuals, and we expected that weather and individual covariates would influence survival variation during critical periods. We found that while spring was a critical season for adult female survival, it was not for males. This is likely because females are dominated by males at feeding sites during snowy seasons (winter and spring), and additionally must invest energy in egg production. When conditions were not favorable, which seemed to happen when the cold season was warmer than usual, females probably reached their physiological limits. Surprisingly, adult survival was higher at the beginning of the cold season than in summer, which may result from adaptation to harsh weather in alpine and polar vertebrates. This hypothesis could be confirmed by testing it with larger sets of populations. This first seasonal analysis of individual survival over the full life cycle in a sedentary alpine bird shows that including seasonality in demographic investigations is crucial to better understand the potential impacts of climate change on cold ecosystems.

Elevation impacts the balance between growth and oxidative stress in coal tits.

The short favorable period of time available for the growth in seasonal environments could constrain the resources allocation between growth and other life-history traits, and the short-term fitness benefits of increased growth rate may prevail over other functions. Accelerated growth rates have been associated with long-term deleterious consequences (e.g., decreased lifespan), and recently oxidative stress (the imbalance between pro-oxidants generation and antioxidant defenses) has been suggested as a mediator of these effects. Here, we examined the impact of elevation on growth rate and self-maintenance parameters (resting metabolism, oxidative damage, and antioxidant defenses) of coal tit chicks (Periparus ater). We predicted that the shorter favorable season at the higher-elevation site could lead to a reallocation of resources towards growth at the expense of self-maintenance processes. We found that chicks at high elevation grew significantly faster in terms of body mass and body size. Chicks from the high-elevation site presented higher resting metabolism, higher oxidative damage level, but similar antioxidant defenses, compared to low-elevation chicks. Interestingly, the chicks exhibiting the better antioxidant defenses at 7 days were also those with the highest resting metabolic rate, and the chicks that grew at the faster rate within the high-elevation site were those with the highest levels of oxidative damage on DNA. Our study supports the idea that increasing elevation leads to a higher growth rate in coal tit chicks, possibly in response to a shorter favorable season. In accordance with life-history theory, a bigger investment in growth was done at the expense of body maintenance, at least in terms of oxidative stress.