Diminishing warming effects on plant phenology over time.

Plant phenology, the timing of recurrent biological events, shows key and complex response to climate warming, with consequences for ecosystem functions and services. A key challenge for predicting plant phenology under future climates is to determine whether the phenological changes will persist with more intensive and long-term warming. Here, we conducted a meta-analysis of 103 experimental warming studies around the globe to investigate the responses of four phenophases - leaf-out, first flowering, last flowering, and leaf coloring. We showed that warming advanced leaf-out and flowering but delayed leaf coloring across herbaceous and woody plants. As the magnitude of warming increased, the response of most plant phenophases gradually leveled off for herbaceous plants, while phenology responded in proportion to warming in woody plants. We also found that the experimental effects of warming on plant phenology diminished over time across all phenophases. Specifically, the rate of changes in first flowering for herbaceous species, as well as leaf-out and leaf coloring for woody species, decreased as the experimental duration extended. Together, these results suggest that the real-world impact of global warming on plant phenology will diminish over time as temperatures continue to increase.

Effects of 5-year experimental warming in the Alpine belt on soil Archaea: Multi-omics approaches and prospects.

We currently lack a predictive understanding of how soil archaeal communities may respond to climate change, particularly in Alpine areas where warming is far exceeding the global average. Here, we characterized the abundance, structure, and function of total (by metagenomics) and active soil archaea (by metatranscriptomics) after 5-year experimental field warming (+1°C) in Italian Alpine grasslands and snowbeds. Our multi-omics approach unveiled an increasing abundance of Archaea during warming in snowbeds, which was negatively correlated with the abundance of fungi (by qPCR) and micronutrients (Ca and Mg), but positively correlated with soil water content. In the snowbeds transcripts, warming resulted in the enrichment of abundances of transcription and nucleotide biosynthesis. Our study provides novel insights into possible changes in soil Archaea composition and function in the climate change scenario.

Fungal communities in European alpine soils are not affected by short-term in situ simulated warming than bacterial communities.

The impact of global warming on biological communities colonizing European alpine ecosystems was recently studied. Hexagonal open top chambers (OTCs) were used for simulating a short-term in situ warming (estimated around 1°C) in some alpine soils to predict the impact of ongoing climate change on resident microbial communities. Total microbial DNA was extracted from soils collected either inside or outside the OTCs over 3 years of study. Bacterial and fungal rRNA copies were quantified by qPCR. Metabarcoding sequencing of taxonomy target genes was performed (Illumina MiSeq) and processed by bioinformatic tools. Alpha- and beta-diversity were used to evaluate the structure of bacterial and fungal communities. qPCR suggests that, although fluctuations have been observed between soils collected either inside and outside the OTCs, the simulated warming induced a significant (p < 0.05) shift only for bacterial abundance. Likewise, significant (p < 0.05) changes in bacterial community structure were detected in soils collected inside the OTCs, with a clear increase of oligotrophic taxa. On the contrary, fungal diversity of soils collected either inside and outside the OTCs did not exhibit significant (p < 0.05) differences, suggesting that the temperature increase in OTCs compared to ambient conditions was not sufficient to change fungal communities.

Composition and functioning of the soil microbiome in the highest altitudes of the Italian Alps and potential effects of climate change.

As the European Alps are experiencing a strong climate warming, this study analyzed the soil microbiome at different altitudes and among different vegetation types at the Stelvio Pass (Italian Alps), aiming to (i) characterize the composition and functional potential of the microbiome of soils and their gene expression during the peak vegetative stage; (ii) explore the potential short-term (using open-top chambers) and long-term (space-for-time substitutions) effects of increasing temperature on the alpine soil microbiome. We found that the functional potential of the soil microbiome and its expression differed among vegetation types. Microbial α-diversity increased along the altitudinal gradient. At lower altitude, shrubland had the highest proportion of fungi, which was correlated with higher amounts of CAZymes, specific for degrading fungal biomass and recalcitrant plant biopolymers. Subalpine upward vegetation shift could lead a possible loss of species of alpine soils. Shrub encroachment may accelerate higher recalcitrant C decomposition and reduce total ecosystem C storage, increasing the efflux of CO2 to the atmosphere with a positive feedback to warming. A total of 5 years of warming had no effect on the composition and functioning of microbial communities, indicating that longer-term warming experiments are needed to investigate the effects of temperature increases on the soil microbiome.

Acceleration of climate warming and plant dynamics in Antarctica.

The strong air temperature warming between the 1950s and 2016 in the Antarctic Peninsula region1 exceeded the global average warming2,3 with evident impacts on terrestrial ecosystems and the two native Antarctic vascular plants Deschampsia antarctica Desv. and Colobanthus quitensis (Kunth) Bartl.4-10 Subsequently, a short but intense cooling occurred from the Antarctic Peninsula to the South Orkney Islands (1999-2016),1,11-13 impacting terrestrial ecosystems, with reduced lichen growth14 and no further expansion of D. antarctica in the Argentine Islands.5 The strong warming trend is predicted to resume15 with expansion of ice-free areas and continued impacts on the abiotic and biotic components of terrestrial ecosystems including the ingression of non-native species3,8,16,17 as recently recorded at Signy Island (South Orkney Islands).18-20 In this study we document acceleration in the expansion of D. antarctica and C. quitensis in the last decade (2009-2018) at Signy Island, where the air temperature warming trend resumed in summer after 2012. We hypothesize that the striking expansion of these plants is mainly triggered by summer air warming and release from the limitation of fur seal disturbance. We also hypothesize that the "pulse" climatic event of the strong air cooling detected in 2012 did not appear to influence the vegetation community dynamics on this island. This is the first evidence in Antarctica for accelerated ecosystem responses to climate warming, confirming similar observations in the Northern Hemisphere. Our findings support the hypothesis that future warming will trigger significant changes in these fragile Antarctic ecosystems.

Vessels in a Rhododendron ferrugineum (L.) population do not trace temperature anymore at the alpine shrubline.

Introduction: Mean 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. Methods: Here, 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 Discussion: Over 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.

Microbial activity in alpine soils under climate change.

Soil enzymatic activity was assessed in the Stelvio Pass area (Italian Central Alps) aiming to define the possible effects of climate change on microbial functioning. Two sites at two different elevations were chosen, a subalpine (2239 m) and an alpine belt (2604-2624 m), with mean annual air temperature differing by almost 3 °C, coherent with the worst future warming scenario (RCP 8.5) by 2100. The lower altitude site may represent a proxy of the potential future situation at higher altitude after the upward shift of subalpine vegetation due to climate change. Additionally, hexagonal open top chambers (OTCs) were installed at the upper site, to passively increase by about 2 °C the summer inner temperature to simulate short term effects of warming before the vegetation shift takes place. Soil physicochemical properties and the bacterial and fungal abundances of the above samples were also considered. The subalpine soils showed a higher microbial activity, especially for hydrolytic enzymes, higher carbon, ammonium and hydrogen (p < 0.001) contents, and a slightly higher PO4 content (p < 0.05) than alpine soils. Bacterial abundance was higher than fungal abundance, both for alpine and subalpine soils. On the other hand, the short term effect, which increased the mean soil temperature during the peak of the growing season in the OTC, showed to induce scarcely significant differences for edaphic parameters and microbial biomass content among the warmed and control plots. Using the manipulative warming experiments, we demonstrated that warming is able to change the enzyme activity starting from colder and higher altitude sites, known to be more vulnerable to the rising temperatures associated with climate change. Although five-years of experimental warming does not allow us to make bold conclusions, it appeared that warming-induced upwards vegetation shift might induce more substantial changes in enzymatic activities than the short-term effects, in the present vegetation context.

Multiple colonization and dispersal events hide the early origin and induce a lack of genetic structure of the moss Bryum argenteum in Antarctica.

The dispersal routes of taxa with transoceanic disjunctions remain poorly understood, with the potential roles of Antarctica not yet demonstrated. Mosses are suitable organisms to test direct intra-Antarctic dispersal, as major component of the extant Antarctic flora, with the cosmopolitan moss Bryum argenteum as ideal target species. We analyzed the genetic structure of B. argenteum to provide an evolutionary time frame for its radiation and shed light into its historical biogeography in the Antarctic region. We tested two alternative scenarios: (a) intra-Antarctic panmixia and (b) intra-Antarctic genetic differentiation. Furthermore, we tested for evidence of the existence of specific intra-Antarctic dispersal routes. Sixty-seven new samples (40 collected in Antarctica) were sequenced for ITS nrDNA and rps4 cpDNA regions, and phylogenetic trees of B. argenteum were constructed, with a focus on its Southern Hemisphere. Combining our new nrDNA dataset with previously published datasets, we estimated time-calibrated phylogenies based on two different substitution rates (derived from angiosperms and bryophytes) along with ancestral area estimations. Minimum spanning network and pairwise genetic distances were also calculated. B. argenteum was potentially distributed across Africa and Antarctica soon after its origin. Its earliest intra-Antarctic dispersal and diversification occurred during a warming period in the Pliocene. On the same timescale, a radiation took place involving a dispersal event from Antarctica to the sub-Antarctic islands. A more recent event of dispersal and diversification within Antarctica occurred during a warm period in the Pleistocene, creating favorable conditions also for its colonization outside the Antarctic continent worldwide. We provide evidence supporting the hypothesis that contemporary populations of B. argenteum in Antarctica integrate a history of both multiple long-range dispersal events and local persistence combined with in situ diversification. Our data support the hypothesis that B. argenteum has been characterized by strong connectivity within Antarctica, suggesting the existence of intra-Antarctic dispersal routes.

Belowground impacts of alpine woody encroachment are determined by plant traits, local climate, and soil conditions.

Global climate and land use change are causing woody plant encroachment in arctic, alpine, and arid/semi-arid ecosystems around the world, yet our understanding of the belowground impacts of this phenomenon is limited. We conducted a globally distributed field study of 13 alpine sites across four continents undergoing woody plant encroachment and sampled soils from both woody encroached and nearby herbaceous plant community types. We found that woody plant encroachment influenced soil microbial richness and community composition across sites based on multiple factors including woody plant traits, site level climate, and abiotic soil conditions. In particular, root symbiont type was a key determinant of belowground effects, as Nitrogen-fixing woody plants had higher soil fungal richness, while Ecto/Ericoid mycorrhizal species had higher soil bacterial richness and symbiont types had distinct soil microbial community composition. Woody plant leaf traits indirectly influenced soil microbes through their impact on soil abiotic conditions, primarily soil pH and C:N ratios. Finally, site-level climate affected the overall magnitude and direction of woody plant influence, as soil fungal and bacterial richness were either higher or lower in woody encroached versus herbaceous soils depending on mean annual temperature and precipitation. All together, these results document global impacts of woody plant encroachment on soil microbial communities, but highlight that multiple biotic and abiotic pathways must be considered to scale up globally from site- and species-level patterns. Considering both the aboveground and belowground effects of woody encroachment will be critical to predict future changes in alpine ecosystem structure and function and subsequent feedbacks to the global climate system.

Author Correction: Warming shortens flowering seasons of tundra plant communities.

In the version of this Article originally published, the following sentence was missing from the Acknowledgements: "This work was supported by the Norwegian Research Council SnoEco project, grant number 230970". This text has now been added.

Warming shortens flowering seasons of tundra plant communities.

Advancing phenology is one of the most visible effects of climate change on plant communities, and has been especially pronounced in temperature-limited tundra ecosystems. However, phenological responses have been shown to differ greatly between species, with some species shifting phenology more than others. We analysed a database of 42,689 tundra plant phenological observations to show that warmer temperatures are leading to a contraction of community-level flowering seasons in tundra ecosystems due to a greater advancement in the flowering times of late-flowering species than early-flowering species. Shorter flowering seasons with a changing climate have the potential to alter trophic interactions in tundra ecosystems. Interestingly, these findings differ from those of warmer ecosystems, where early-flowering species have been found to be more sensitive to temperature change, suggesting that community-level phenological responses to warming can vary greatly between biomes.

Accelerating climate change impacts on alpine glacier forefield ecosystems in the European Alps.

In the European Alps the increase in air temperature was more than twice the increase in global mean temperature over the last 50 years. The abiotic (glacial) and the biotic components (plants and vegetation) of the mountain environment are showing ample evidence of climate change impacts. In the Alps most small glaciers (80% of total glacial coverage and an important contribution to water resources) could disappear in the next decades. Recently climate change was demonstrated to affect higher levels of ecological systems, with vegetation exhibiting surface area changes, indicating that alpine and nival vegetation may be able to respond in a fast and flexible way in response to 1-2 degrees C warming. We analyzed the glacier evolution (terminus fluctuations, mass balances, surface area variations), local climate, and vegetation succession on the forefield of Sforzellina Glacier (Upper Valtellina, central Italian Alps) over the past three decades. We aimed to quantify the impacts of climate change on coupled biotic and abiotic components of high alpine ecosystems, to verify if an acceleration was occurring on them during the last decade (i.e., 1996-2006) and to assess whether new specific strategies were adopted for plant colonization and development. All the glaciological data indicate that a glacial retreat and shrinkage occurred and was much stronger after 2002 than during the last 35 years. Vegetation started to colonize surfaces deglaciated for only one year, with a rate at least four times greater than that reported in the literature for the establishment of scattered individuals and about two times greater for the well-established discontinuous early-successional community. The colonization strategy changed: the first colonizers are early-successional, scree slopes, and perennial clonal species with high phenotypic plasticity rather than pioneer and snowbed species. This impressive acceleration coincided with only slight local summer warming (approximately -0.5 degree C) and a poorly documented local decrease in the snow cover depth and duration. Are we facing accelerated ecological responses to climatic changes and/or did we go beyond a threshold over which major ecosystem changes may occur in response to even minor climatic variations?