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.

Plant functional trait change across a warming tundra biome.

The tundra is warming more rapidly than any other biome on Earth, and the potential ramifications are far-reaching because of global feedback effects between vegetation and climate. A better understanding of how environmental factors shape plant structure and function is crucial for predicting the consequences of environmental change for ecosystem functioning. Here we explore the biome-wide relationships between temperature, moisture and seven key plant functional traits both across space and over three decades of warming at 117 tundra locations. Spatial temperature-trait relationships were generally strong but soil moisture had a marked influence on the strength and direction of these relationships, highlighting the potentially important influence of changes in water availability on future trait shifts in tundra plant communities. Community height increased with warming across all sites over the past three decades, but other traits lagged far behind predicted rates of change. Our findings highlight the challenge of using space-for-time substitution to predict the functional consequences of future warming and suggest that functions that are tied closely to plant height will experience the most rapid change. They also reveal the strength with which environmental factors shape biotic communities at the coldest extremes of the planet and will help to improve projections of functional changes in tundra ecosystems with climate warming.

When spring ephemerals fail to meet pollinators: mechanism of phenological mismatch and its impact on plant reproduction.

The flowering phenology of early-blooming plants is largely determined by snowmelt timing in high-latitude and high-altitude ecosystems. When the synchrony of flowering and pollinator emergence is disturbed by climate change, seed production may be restricted due to insufficient pollination success. We revealed the mechanism of phenological mismatch between a spring ephemeral ( Corydalis ambigua) and its pollinator (overwintered bumblebees), and its impact on plant reproduction, based on 19 years of monitoring and a snow removal experiment in a cool-temperate forest in northern Japan. Early snowmelt increased the risk of phenological mismatch under natural conditions. Seed production was limited by pollination success over the 3 years of the pollination experiment and decreased when flowering occurred prior to bee emergence. Similar trends were detected on modification of flowering phenology through snow removal. Following snowmelt, the length of the pre-flowering period strongly depended on the ambient surface temperature, ranging from 4 days (at greater than 7°C) to 26 days (at 2.5°C). Flowering onset was explained with an accumulated surface degree-day model. Bumblebees emerged when soil temperature reached 6°C, which was predictable by an accumulated soil degree-day model, although foraging activity after emergence might depend on air temperature. These results indicate that phenological mismatch tends to occur when snow melts early but subsequent soil warming progresses slowly. Thus, modification of the snowmelt regime could be a major driver disturbing spring phenology in northern ecosystems.

BioTIME: A database of biodiversity time series for the Anthropocene.

MOTIVATION: The BioTIME database contains raw data on species identities and abundances in ecological assemblages through time. These data enable users to calculate temporal trends in biodiversity within and amongst assemblages using a broad range of metrics. BioTIME is being developed as a community-led open-source database of biodiversity time series. Our goal is to accelerate and facilitate quantitative analysis of temporal patterns of biodiversity in the Anthropocene. MAIN TYPES OF VARIABLES INCLUDED: The database contains 8,777,413 species abundance records, from assemblages consistently sampled for a minimum of 2 years, which need not necessarily be consecutive. In addition, the database contains metadata relating to sampling methodology and contextual information about each record. SPATIAL LOCATION AND GRAIN: BioTIME is a global database of 547,161 unique sampling locations spanning the marine, freshwater and terrestrial realms. Grain size varies across datasets from 0.0000000158 km2 (158 cm2) to 100 km2 (1,000,000,000,000 cm2). TIME PERIOD AND GRAIN: BioTIME records span from 1874 to 2016. The minimal temporal grain across all datasets in BioTIME is a year. MAJOR TAXA AND LEVEL OF MEASUREMENT: BioTIME includes data from 44,440 species across the plant and animal kingdoms, ranging from plants, plankton and terrestrial invertebrates to small and large vertebrates. SOFTWARE FORMAT: .csv and .SQL.

Greater temperature sensitivity of plant phenology at colder sites: implications for convergence across northern latitudes.

Warmer temperatures are accelerating the phenology of organisms around the world. Temperature sensitivity of phenology might be greater in colder, higher latitude sites than in warmer regions, in part because small changes in temperature constitute greater relative changes in thermal balance at colder sites. To test this hypothesis, we examined up to 20 years of phenology data for 47 tundra plant species at 18 high-latitude sites along a climatic gradient. Across all species, the timing of leaf emergence and flowering was more sensitive to a given increase in summer temperature at colder than warmer high-latitude locations. A similar pattern was seen over time for the flowering phenology of a widespread species, Cassiope tetragona. These are among the first results highlighting differential phenological responses of plants across a climatic gradient and suggest the possibility of convergence in flowering times and therefore an increase in gene flow across latitudes as the climate warms.

Aphid-willow interactions in a high Arctic ecosystem: responses to raised temperature and goose disturbance.

Recently, there have been several studies using open top chambers (OTCs) or cloches to examine the response of Arctic plant communities to artificially elevated temperatures. Few, however, have investigated multitrophic systems, or the effects of both temperature and vertebrate grazing treatments on invertebrates. This study investigated trophic interactions between an herbivorous insect (Sitobion calvulum, Aphididae), a woody perennial host plant (Salix polaris) and a selective vertebrate grazer (barnacle geese, Branta leucopsis). In a factorial experiment, the responses of the insect and its host to elevated temperatures using open top chambers (OTCs) and to three levels of goose grazing pressure were assessed over two summer growing seasons (2004 and 2005). OTCs significantly enhanced the leaf phenology of Salix in both years and there was a significant OTC by goose presence interaction in 2004. Salix leaf number was unaffected by treatments in both years, but OTCs increased leaf size and mass in 2005. Salix reproduction and the phenology of flowers were unaffected by both treatments. Aphid densities were increased by OTCs but unaffected by goose presence in both years. While goose presence had little effect on aphid density or host plant phenology in this system, the OTC effects provide interesting insights into the possibility of phenological synchrony disruption. The advanced phenology of Salix effectively lengthens the growing season for the plant, but despite a close association with leaf maturity, the population dynamics of the aphid appeared to lack a similar phenological response, except for the increased population observed.

Global assessment of experimental climate warming on tundra vegetation: heterogeneity over space and time.

Understanding the sensitivity of tundra vegetation to climate warming is critical to forecasting future biodiversity and vegetation feedbacks to climate. In situ warming experiments accelerate climate change on a small scale to forecast responses of local plant communities. Limitations of this approach include the apparent site-specificity of results and uncertainty about the power of short-term studies to anticipate longer term change. We address these issues with a synthesis of 61 experimental warming studies, of up to 20 years duration, in tundra sites worldwide. The response of plant groups to warming often differed with ambient summer temperature, soil moisture and experimental duration. Shrubs increased with warming only where ambient temperature was high, whereas graminoids increased primarily in the coldest study sites. Linear increases in effect size over time were frequently observed. There was little indication of saturating or accelerating effects, as would be predicted if negative or positive vegetation feedbacks were common. These results indicate that tundra vegetation exhibits strong regional variation in response to warming, and that in vulnerable regions, cumulative effects of long-term warming on tundra vegetation - and associated ecosystem consequences - have the potential to be much greater than we have observed to date.

Experimentally increased snow depth affects high Arctic microarthropods inconsistently over two consecutive winters.

Climate change induced alterations to winter conditions may affect decomposer organisms controlling the vast carbon stores in northern soils. Soil microarthropods are particularly abundant decomposers in Arctic ecosystems. We studied whether increased snow depth affected microarthropods, and if effects were consistent over two consecutive winters. We sampled Collembola and soil mites from a snow accumulation experiment at Svalbard in early summer and used soil microclimatic data to explore to which aspects of winter climate microarthropods are most sensitive. Community densities differed substantially between years and increased snow depth had inconsistent effects. Deeper snow hardly affected microarthropods in 2015, but decreased densities and altered relative abundances of microarthropods and Collembola species after a milder winter in 2016. Although increased snow depth increased soil temperatures by 3.2 °C throughout the snow cover periods, the best microclimatic predictors of microarthropod density changes were spring soil temperature and snowmelt day. Our study shows that extrapolation of observations of decomposer responses to altered winter climate conditions to future scenarios should be avoided when communities are only sampled on a single occasion, since effects of longer-term gradual changes in winter climate may be obscured by inter-annual weather variability and natural variability in population sizes.

Experimental warming differentially affects vegetative and reproductive phenology of tundra plants.

Rapid climate warming is altering Arctic and alpine tundra ecosystem structure and function, including shifts in plant phenology. While the advancement of green up and flowering are well-documented, it remains unclear whether all phenophases, particularly those later in the season, will shift in unison or respond divergently to warming. Here, we present the largest synthesis to our knowledge of experimental warming effects on tundra plant phenology from the International Tundra Experiment. We examine the effect of warming on a suite of season-wide plant phenophases. Results challenge the expectation that all phenophases will advance in unison to warming. Instead, we find that experimental warming caused: (1) larger phenological shifts in reproductive versus vegetative phenophases and (2) advanced reproductive phenophases and green up but delayed leaf senescence which translated to a lengthening of the growing season by approximately 3%. Patterns were consistent across sites, plant species and over time. The advancement of reproductive seasons and lengthening of growing seasons may have significant consequences for trophic interactions and ecosystem function across the tundra.

Soil organic carbon depletion and degradation in surface soil after long-term non-growing season warming in High Arctic Svalbard.

Arctic tundra active-layer soils are at risk of soil organic carbon (SOC) depletion and degradation upon global climate warming because they are in a stage of relatively early decomposition. Non-growing season (NGS) warming is particularly pronounced, and observed increases of CO2 emissions during experimentally warmed NGSs give concern for great SOC losses to the atmosphere. Here, we used snow fences in Arctic Spitsbergen dwarf shrub tundra to simulate 1.86 °C NGS warming for 9 consecutive years, while growing season temperatures remained unchanged. In the snow fence treatment, the 4-11 cm thick A-horizon had a 2% lower SOC concentration and a 0.48 kg C m-2 smaller pool size than the controls, indicating SOC pool depletion. The snow fence treatment's A-horizon's alkyl/O-alkyl ratio was also significantly increased, indicating an advance of SOC degradation. The underlying 5 cm of B/C-horizon did not show these effects. Our results support the hypothesis that SOC depletion and degradation are connected to the long-term transience of observed ecosystem respiration (ER) increases upon soil warming. We suggest that the bulk of warming induced ER increases may originate from surface and not deep active layer or permafrost horizons. The observed losses of SOC might be significant for the ecosystem in question, but are in magnitude comparatively small relative to anthropogenic greenhouse gas enrichment of the atmosphere. We conclude that a positive feedback of carbon losses from surface soils of Arctic dwarf shrub tundra to anthropogenic forcing will be minor, but not negligible.

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.

Large loss of CO2 in winter observed across the northern permafrost region.

Recent warming in the Arctic, which has been amplified during the winter1-3, greatly enhances microbial decomposition of soil organic matter and subsequent release of carbon dioxide (CO2)4. However, the amount of CO2 released in winter is highly uncertain and has not been well represented by ecosystem models or by empirically-based estimates5,6. Here we synthesize regional in situ observations of CO2 flux from arctic and boreal soils to assess current and future winter carbon losses from the northern permafrost domain. We estimate a contemporary loss of 1662 Tg C yr-1 from the permafrost region during the winter season (October through April). This loss is greater than the average growing season carbon uptake for this region estimated from process models (-1032 Tg C yr-1). Extending model predictions to warmer conditions in 2100 indicates that winter CO2 emissions will increase 17% under a moderate mitigation scenario-Representative Concentration Pathway (RCP) 4.5-and 41% under business-as-usual emissions scenario-RCP 8.5. Our results provide a new baseline for winter CO2 emissions from northern terrestrial regions and indicate that enhanced soil CO2 loss due to winter warming may offset growing season carbon uptake under future climatic conditions.

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.

Dead or Alive; or Does It Really Matter? Level of Congruency Between Trophic Modes in Total and Active Fungal Communities in High Arctic Soil.

Describing dynamics of belowground organisms, such as fungi, can be challenging. Results of studies based on environmental DNA (eDNA) may be biased as the template does not discriminate between metabolically active cells and dead biomass. We analyzed ribosomal DNA (rDNA) and ribosomal RNA (rRNA) coextracted from 48 soil samples collected from a manipulated snow depth experiment in two distinct vegetation types in Svalbard, in the High Arctic. Our main goal was to compare if the rDNA and rRNA metabarcoding templates produced congruent results that would lead to consistent ecological interpretation. Data derived from both rDNA and rRNA clustered according to vegetation types. Different sets of environmental variables explained the community composition based on the metabarcoding template. rDNA and rRNA-derived community composition of symbiotrophs and saprotrophs, unlike pathotrophs, clustered together in a similar way as when the community composition was analyzed using all OTUs in the study. Mean OTU richness was higher for rRNA, especially in symbiotrophs. The metabarcoding template was more important than vegetation type in explaining differences in richness. The proportion of symbiotrophic, saprotrophic and functionally unassigned reads differed between rDNA and rRNA, but showed similar trends. There was no evidence for increased snow depth influence on fungal community composition or richness. Our findings suggest that template choice may be especially important for estimating biodiversity, such as richness and relative abundances, especially in Helotiales and Agaricales, but not for inferring community composition. Differences in study results originating from rDNA or rRNA may directly impact the ecological conclusions of one's study, which could potentially lead to false conclusions on the dynamics of microbial communities in a rapidly changing Arctic.

Ectomycorrhizal and saprotrophic fungi respond differently to long-term experimentally increased snow depth in the High Arctic.

Changing climate is expected to alter precipitation patterns in the Arctic, with consequences for subsurface temperature and moisture conditions, community structure, and nutrient mobilization through microbial belowground processes. Here, we address the effect of increased snow depth on the variation in species richness and community structure of ectomycorrhizal (ECM) and saprotrophic fungi. Soil samples were collected weekly from mid-July to mid-September in both control and deep snow plots. Richness of ECM fungi was lower, while saprotrophic fungi was higher in increased snow depth plots relative to controls. [Correction added on 23 September 2016 after first online publication: In the preceding sentence, the richness of ECM and saprotrophic fungi were wrongly interchanged and have been fixed in this current version.] ECM fungal richness was related to soil NO3 -N, NH4 -N, and K; and saprotrophic fungi to NO3 -N and pH. Small but significant changes in the composition of saprotrophic fungi could be attributed to snow treatment and sampling time, but not so for the ECM fungi. Delayed snow melt did not influence the temporal variation in fungal communities between the treatments. Results suggest that some fungal species are favored, while others are disfavored resulting in their local extinction due to long-term changes in snow amount. Shifts in species composition of fungal functional groups are likely to affect nutrient cycling, ecosystem respiration, and stored permafrost carbon.

Idiosyncratic responses of high Arctic plants to changing snow regimes.

The Arctic is one of the ecosystems most affected by climate change; in particular, winter temperatures and precipitation are predicted to increase with consequent changes to snow cover depth and duration. Whether the snow-free period will be shortened or prolonged depends on the extent and temporal patterns of the temperature and precipitation rise; resulting changes will likely affect plant growth with cascading effects throughout the ecosystem. We experimentally manipulated snow regimes using snow fences and shoveling and assessed aboveground size of eight common high arctic plant species weekly throughout the summer. We demonstrated that plant growth responded to snow regime, and that air temperature sum during the snow free period was the best predictor for plant size. The majority of our studied species showed periodic growth; increases in plant size stopped after certain cumulative temperatures were obtained. Plants in early snow-free treatments without additional spring warming were smaller than controls. Response to deeper snow with later melt-out varied between species and categorizing responses by growth forms or habitat associations did not reveal generic trends. We therefore stress the importance of examining responses at the species level, since generalized predictions of aboveground growth responses to changing snow regimes cannot be made.

Snow cover and extreme winter warming events control flower abundance of some, but not all species in high arctic Svalbard.

The High Arctic winter is expected to be altered through ongoing and future climate change. Winter precipitation and snow depth are projected to increase and melt out dates change accordingly. Also, snow cover and depth will play an important role in protecting plant canopy from increasingly more frequent extreme winter warming events. Flower production of many Arctic plants is dependent on melt out timing, since season length determines resource availability for flower preformation. We erected snow fences to increase snow depth and shorten growing season, and counted flowers of six species over 5 years, during which we experienced two extreme winter warming events. Most species were resistant to snow cover increase, but two species reduced flower abundance due to shortened growing seasons. Cassiope tetragona responded strongly with fewer flowers in deep snow regimes during years without extreme events, while Stellaria crassipes responded partly. Snow pack thickness determined whether winter warming events had an effect on flower abundance of some species. Warming events clearly reduced flower abundance in shallow but not in deep snow regimes of Cassiope tetragona, but only marginally for Dryas octopetala. However, the affected species were resilient and individuals did not experience any long term effects. In the case of short or cold summers, a subset of species suffered reduced reproductive success, which may affect future plant composition through possible cascading competition effects. Extreme winter warming events were shown to expose the canopy to cold winter air. The following summer most of the overwintering flower buds could not produce flowers. Thus reproductive success is reduced if this occurs in subsequent years. We conclude that snow depth influences flower abundance by altering season length and by protecting or exposing flower buds to cold winter air, but most species studied are resistant to changes. Winter warming events, often occurring together with rain, can substantially remove snow cover and thereby expose plants to cold winter air. Depending on morphology, different parts of the plant can be directly exposed. On this picture, we see Dryas octopetala seed heads from the previous growing season protrude through the remaining ice layer after a warming event in early 2010. The rest of the plant, including meristems and flower primordia, are still somewhat protected by the ice. In the background we can see a patch of Cassiope tetragona protruding through the ice; in this case, the whole plant including flower primordia is exposed, which might be one reason why this species experienced a loss of flowers the following season. Photograph by Philipp Semenchuk.

Variable temperature effects of Open Top Chambers at polar and alpine sites explained by irradiance and snow depth.

Environmental manipulation studies are integral to determining biological consequences of climate warming. Open Top Chambers (OTCs) have been widely used to assess summer warming effects on terrestrial biota, with their effects during other seasons normally being given less attention even though chambers are often deployed year-round. In addition, their effects on temperature extremes and freeze-thaw events are poorly documented. To provide robust documentation of the microclimatic influences of OTCs throughout the year, we analysed temperature data from 20 studies distributed across polar and alpine regions. The effects of OTCs on mean temperature showed a large range (-0.9 to 2.1 °C) throughout the year, but did not differ significantly between studies. Increases in mean monthly and diurnal temperature were strongly related (R(2)  = 0.70) with irradiance, indicating that PAR can be used to predict the mean warming effect of OTCs. Deeper snow trapped in OTCs also induced higher temperatures at soil/vegetation level. OTC-induced changes in the frequency of freeze-thaw events included an increase in autumn and decreases in spring and summer. Frequency of high-temperature events in OTCs increased in spring, summer and autumn compared with non-manipulated control plots. Frequency of low-temperature events was reduced by deeper snow accumulation and higher mean temperatures. The strong interactions identified between aspects of ambient environmental conditions and effects of OTCs suggest that a detailed knowledge of snow depth, temperature and irradiance levels enables us to predict how OTCs will modify the microclimate at a particular site and season. Such predictive power allows a better mechanistic understanding of observed biotic response to experimental warming studies and for more informed design of future experiments. However, a need remains to quantify OTC effects on water availability and wind speed (affecting, for example, drying rates and water stress) in combination with microclimate measurements at organism level.

Late snowmelt delays plant development and results in lower reproductive success in the High Arctic.

In tundra areas where the growing season is short, any delay in the start of summer may have a considerable effect on plant development, growth and reproductive success. Climate models suggest long-term changes in winter precipitation in the Arctic, which may lead to deeper snow cover and a resultant delay in date of snow melt. In this paper, we investigated the role of snow depth and melt out date on the phenological development and reproductive success of vascular plants in Adventdalen, Svalbard (78° 10'N, 16° 06'E). Effects of natural variations in snow accumulation were demonstrated using two vegetation types (snow depth: meadow 21 cm, heath 32 cm), and fences were used to experimentally increase snow depth by over 1m. Phenological delay was greatest directly after snowmelt in the earlier phenological phases, and had the largest effect on the early development of those species which normally green-up early (i.e. Dryas, Papaver, Salix, Saxifraga). Compressed growing seasons and length of the reproductive period led to a reduced reproductive success in some of the study species. There were fewer flowers, fewer plots with dispersing seeds, and lower germination rates. This can have consequences for plant establishment and community composition in the long-term.