Limits on phenological response to high temperature in the Arctic.

Tundra plants are widely considered to be constrained by cool growing conditions and short growing seasons. Furthermore, phenological development is generally predicted by daily heat sums calculated as growing degree days. Analyzing over a decade of seasonal flower counts of 23 plant species distributed across four plant communities, together with hourly canopy-temperature records, we show that the timing of flowering of many tundra plants are best predicted by a modified growing degree day model with a maximum temperature threshold. Threshold maximums are commonly employed in agriculture, but until recently have not been considered for natural ecosystems and to our knowledge have not been used for tundra plants. Estimated maximum temperature thresholds were found to be within the range of daily temperatures commonly experienced for many species, particularly for plants at the colder, high Arctic study site. These findings provide an explanation for why passive experimental warming-where moderate changes in mean daily temperatures are accompanied by larger changes in daily maximum temperatures-generally shifts plant phenology less than ambient warming. Our results also suggest that many plants adapted to extreme cold environments may have limits to their thermal responsiveness.

Global change re-structures alpine plant communities through interacting abiotic and biotic effects.

Global change is altering patterns of community assembly, with net outcomes dependent on species' responses to the abiotic environment, both directly and mediated through biotic interactions. Here, we assess alpine plant community responses in a 15-year factorial nitrogen addition, warming and snow manipulation experiment. We used a dynamic competition model to estimate the density-dependent and -independent processes underlying changes in species-group abundances over time. Density-dependent shifts in competitive interactions drove long-term changes in abundance of species-groups under global change while counteracting environmental drivers limited the growth response of the dominant species through density-independent mechanisms. Furthermore, competitive interactions shifted with the environment, primarily with nitrogen and drove non-linear abundance responses across environmental gradients. Our results highlight that global change can either reshuffle species hierarchies or further favour already-dominant species; predicting which outcome will occur requires incorporating both density-dependent and -independent mechanisms and how they interact across multiple global change factors.

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.

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.

Towards global data products of Essential Biodiversity Variables on species traits.

Essential Biodiversity Variables (EBVs) allow observation and reporting of global biodiversity change, but a detailed framework for the empirical derivation of specific EBVs has yet to be developed. Here, we re-examine and refine the previous candidate set of species traits EBVs and show how traits related to phenology, morphology, reproduction, physiology and movement can contribute to EBV operationalization. The selected EBVs express intra-specific trait variation and allow monitoring of how organisms respond to global change. We evaluate the societal relevance of species traits EBVs for policy targets and demonstrate how open, interoperable and machine-readable trait data enable the building of EBV data products. We outline collection methods, meta(data) standardization, reproducible workflows, semantic tools and licence requirements for producing species traits EBVs. An operationalization is critical for assessing progress towards biodiversity conservation and sustainable development goals and has wide implications for data-intensive science in ecology, biogeography, conservation and Earth observation.

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.

Increasing phenological asynchrony between spring green-up and arrival of migratory birds.

Consistent with a warming climate, birds are shifting the timing of their migrations, but it remains unclear to what extent these shifts have kept pace with the changing environment. Because bird migration is primarily cued by annually consistent physiological responses to photoperiod, but conditions at their breeding grounds depend on annually variable climate, bird arrival and climate-driven spring events would diverge. We combined satellite and citizen science data to estimate rates of change in phenological interval between spring green-up and migratory arrival for 48 breeding passerine species across North America. Both arrival and green-up changed over time, usually in the same direction (earlier or later). Although birds adjusted their arrival dates, 9 of 48 species did not keep pace with rapidly changing green-up and across all species the interval between arrival and green-up increased by over half a day per year. As green-up became earlier in the east, arrival of eastern breeding species increasingly lagged behind green-up, whereas in the west-where green-up typically became later-birds arrived increasingly earlier relative to green-up. Our results highlight that phenologies of species and trophic levels can shift at different rates, potentially leading to phenological mismatches with negative fitness consequences.

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.

Estimates of local biodiversity change over time stand up to scrutiny.

We present new data and analyses revealing fundamental flaws in a critique of two recent meta-analyses of local-scale temporal biodiversity change. First, the conclusion that short-term time series lead to biased estimates of long-term change was based on two errors in the simulations used to support it. Second, the conclusion of negative relationships between temporal biodiversity change and study duration was entirely dependent on unrealistic model assumptions, the use of a subset of data, and inclusion of one outlier data point in one study. Third, the finding of a decline in local biodiversity, after eliminating post-disturbance studies, is not robust to alternative analyses on the original data set, and is absent in a larger, updated data set. Finally, the undebatable point, noted in both original papers, that studies in the ecological literature are geographically biased, was used to cast doubt on the conclusion that, outside of areas converted to croplands or asphalt, the distribution of biodiversity trends is centered approximately on zero. Future studies may modify conclusions, but at present, alternative conclusions based on the geographic-bias argument rely on speculation. In sum, the critique raises points of uncertainty typical of all ecological studies, but does not provide an evidence-based alternative interpretation.

Contrasting effects of warming and increased snowfall on Arctic tundra plant phenology over the past two decades.

Recent changes in climate have led to significant shifts in phenology, with many studies demonstrating advanced phenology in response to warming temperatures. The rate of temperature change is especially high in the Arctic, but this is also where we have relatively little data on phenological changes and the processes driving these changes. In order to understand how Arctic plant species are likely to respond to future changes in climate, we monitored flowering phenology in response to both experimental and ambient warming for four widespread species in two habitat types over 21 years. We additionally used long-term environmental records to disentangle the effects of temperature increase and changes in snowmelt date on phenological patterns. While flowering occurred earlier in response to experimental warming, plants in unmanipulated plots showed no change or a delay in flowering over the 21-year period, despite more than 1 °C of ambient warming during that time. This counterintuitive result was likely due to significantly delayed snowmelt over the study period (0.05-0.2 days/yr) due to increased winter snowfall. The timing of snowmelt was a strong driver of flowering phenology for all species - especially for early-flowering species - while spring temperature was significantly related to flowering time only for later-flowering species. Despite significantly delayed flowering phenology, the timing of seed maturation showed no significant change over time, suggesting that warmer temperatures may promote more rapid seed development. The results of this study highlight the importance of understanding the specific environmental cues that drive species' phenological responses as well as the complex interactions between temperature and precipitation when forecasting phenology over the coming decades. As demonstrated here, the effects of altered snowmelt patterns can counter the effects of warmer temperatures, even to the point of generating phenological responses opposite to those predicted by warming alone.

Experiment, monitoring, and gradient methods used to infer climate change effects on plant communities yield consistent patterns.

Inference about future climate change impacts typically relies on one of three approaches: manipulative experiments, historical comparisons (broadly defined to include monitoring the response to ambient climate fluctuations using repeat sampling of plots, dendroecology, and paleoecology techniques), and space-for-time substitutions derived from sampling along environmental gradients. Potential limitations of all three approaches are recognized. Here we address the congruence among these three main approaches by comparing the degree to which tundra plant community composition changes (i) in response to in situ experimental warming, (ii) with interannual variability in summer temperature within sites, and (iii) over spatial gradients in summer temperature. We analyzed changes in plant community composition from repeat sampling (85 plant communities in 28 regions) and experimental warming studies (28 experiments in 14 regions) throughout arctic and alpine North America and Europe. Increases in the relative abundance of species with a warmer thermal niche were observed in response to warmer summer temperatures using all three methods; however, effect sizes were greater over broad-scale spatial gradients relative to either temporal variability in summer temperature within a site or summer temperature increases induced by experimental warming. The effect sizes for change over time within a site and with experimental warming were nearly identical. These results support the view that inferences based on space-for-time substitution overestimate the magnitude of responses to contemporary climate warming, because spatial gradients reflect long-term processes. In contrast, in situ experimental warming and monitoring approaches yield consistent estimates of the magnitude of response of plant communities to climate warming.

Global meta-analysis reveals no net change in local-scale plant biodiversity over time.

Global biodiversity is in decline. This is of concern for aesthetic and ethical reasons, but possibly also for practical reasons, as suggested by experimental studies, mostly with plants, showing that biodiversity reductions in small study plots can lead to compromised ecosystem function. However, inferring that ecosystem functions will decline due to biodiversity loss in the real world rests on the untested assumption that such loss is actually occurring at these small scales in nature. Using a global database of 168 published studies and >16,000 nonexperimental, local-scale vegetation plots, we show that mean temporal change in species diversity over periods of 5-261 y is not different from zero, with increases at least as likely as declines over time. Sites influenced primarily by plant species' invasions showed a tendency for declines in species richness, whereas sites undergoing postdisturbance succession showed increases in richness over time. Other distinctions among studies had little influence on temporal richness trends. Although maximizing diversity is likely important for maintaining ecosystem function in intensely managed systems such as restored grasslands or tree plantations, the clear lack of any general tendency for plant biodiversity to decline at small scales in nature directly contradicts the key assumption linking experimental results to ecosystem function as a motivation for biodiversity conservation in nature. How often real world changes in the diversity and composition of plant communities at the local scale cause ecosystem function to deteriorate, or actually to improve, remains unknown and is in critical need of further study.

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.

Can spatial isolation help predict dispersal-limited sites for native species restoration?

When the distribution of species is limited by propagule supply, new populations may be initiated by seed addition, but identifying suitable sites for efficiently targeted seed addition remains a major challenge for restoration. In addition to the biotic or abiotic variables typically used in species distribution models, spatial isolation from conspecifics could help predict the suitability of unoccupied sites. Site suitability might be expected to increase with spatial isolation after other factors are accounted for, since isolation increases the chance that a site is unoccupied only because of propagule limitation. For two native annual forbs in Californian grasslands, we combined experimental seeding and niche modeling to ask whether suitability of unoccupied sites could be predicted by spatial variables (either distances from, or densities of, conspecific populations), either by themselves or in combination with niche models. We also asked whether experimental tests of these predictions held up not only in the short term (one year), but also in the longer term (three years). For Lasthenia californica, seed additions were only successful relatively near existing populations. For Lupinus nanus, seeding success was low and was positively related to the number of conspecifics within 1 km. For both species, a few previously unoccupied sites remained occupied three years after seeding, but this subset was not predictable based on either spatial or niche variables. Seed addition alone may be a limited means of native forb restoration if suitable unoccupied sites are either rare or unpredictable, or if they tend to be close to where the species already occurs.

Is plant community richness regulated over time? Contrasting results from experiments and long-term observations.

There is considerable debate among ecologists as to whether or not communities are saturated. In saturated communities, species richness should remain relatively constant over time, despite compositional turnover, because richness is negatively correlated with colonization and positively correlated with local extinction. Few studies have tested for saturation using temporal observational data as well as diversity-perturbation experiments. We analyzed 10 years of data for plant species richness at 71 sites on contrasting serpentine and non-serpentine soils within Californian (USA) grasslands. We also manipulated local richness and measured its effects on immigration and extinction. Consistent with saturation, we observed that richness was positively correlated with extinction rates and negatively correlated with colonization rates, and randomization tests confirmed that diversity fluctuated less than expected by chance. However, experimental species additions and removals did not affect extinction or colonization, suggesting that richness is not regulated by local species interactions. Instead, we propose three reasons why richness may fluctuate within narrow limits causing the appearance of saturation in temporal observational data sets: negatively autocorrelated patterns of biotic response to yearly conditions, differential affinities of particular species for local conditions, or stochastic abundance-dependent colonization and extinction rates. We illustrate the latter using a metacommunity model.

Temporal variability and nestedness in California grassland species composition.

Nestedness occurs when species-poor assemblages contain a subset of the species that occur in more species-rich communities and is a commonly observed pattern in spatial data sets. Examination of nested distribution patterns across time rather than space are rarely conducted, even though they may have important implications for species coexistence. Nested temporal assemblages can occur when most species respond similarly to interannual variation in conditions. In contrast, assemblages might be non-nested when different sets of species occur in different years, either because of different resource requirements or as a result of competitive exclusion. Using eight years of plant occurrence data at 71 sites in California grasslands, we found strong signals of temporal nestedness with most species favored by similar conditions. High-quality years enabled the expansion of both grasses and forbs into locales where they were not found during poor-quality years. Native annual forb, exotic annual forb, and exotic annual grass species richness were all greatest in cool, wet years following hot, dry years. Together, these analyses support the hypothesis that, in the absence of community members that specialize on poor-quality years, interannual environmental variation can cause communities to form nested subsets across time much as they do across space.

Use of community-composition data to predict the fecundity and abundance of species.

Species distribution models are critical tools for the prediction of invasive species spread and conservation of biodiversity. The majority of species distribution models have been built with environmental data. Community ecology theory suggests that species co-occurrence data could also be used to predict current and potential distributions of species. Species assemblages are the products of biotic and environmental constraints on the distribution of individual species and as a result may contain valuable information for niche modeling. We compared the predictive ability of distribution models of annual grassland plants derived from either environmental or community-composition data. Composition-based models were built with the presence or absence of species at a site as predictors of site quality, whereas environment-based models were built with soil chemistry, moisture content, above-ground biomass, and solar radiation as predictors. The reproductive output of experimentally seeded individuals of 4 species and the abundance of 100 species were used to evaluate the resulting models. Community-composition data were the best predictors of both the site-specific reproductive output of sown individuals and the site-specific abundance of existing populations. Successful community-based models were robust to omission of data on the occurrence of rare species, which suggests that even very basic survey data on the occurrence of common species may be adequate for generating such models. Our results highlight the need for increased public availability of ecological survey data to facilitate community-based modeling at scales relevant to conservation.

Plant competition varies with community composition in an edaphically complex landscape.

There is currently no consensus on how physical and biological factors affect competitive intensity. Tests of whether competitive intensity varies along axes of environmental change have commonly been conducted in systems with a single strong environmental gradient, such as productivity, a soil resource, or an environmental stress. Frequently, these same axes are associated with changes in species composition, yet few studies have asked whether shifts in the identity of competitors affect competitive intensity. We ask whether resources (nutrients, water), stressors (heavy metals, Ca:Mg ratio), productivity (aboveground biomass), or species identity (an ordination axis of plant community composition) were the best predictors of the intensity of competition in a heterogeneous grassland landscape that included multiple independent environmental gradients. The reproductive fitness of six annual plant species was measured in the presence and absence of competitors and used to calculate relative interaction intensity (RII). We found that RII was best predicted by community composition. Nutrient availability was also important, and a post hoc test showed that competitive intensity was best explained by the combined effects of community composition and nutrient availability. We argue that community composition may be the most effective metric for predicting competitive intensity in many ecosystems because it includes both the competitive effects of the local community and information about covarying environmental characteristics.