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.

Divergence of Arctic shrub growth associated with sea ice decline.

Arctic sea ice extent (SIE) is declining at an accelerating rate with a wide range of ecological consequences. However, determining sea ice effects on tundra vegetation remains a challenge. In this study, we examined the universality or lack thereof in tundra shrub growth responses to changes in SIE and summer climate across the Pan-Arctic, taking advantage of 23 tundra shrub-ring chronologies from 19 widely distributed sites (56°N to 83°N). We show a clear divergence in shrub growth responses to SIE that began in the mid-1990s, with 39% of the chronologies showing declines and 57% showing increases in radial growth (decreasers and increasers, respectively). Structural equation models revealed that declining SIE was associated with rising air temperature and precipitation for increasers and with increasingly dry conditions for decreasers. Decreasers tended to be from areas of the Arctic with lower summer precipitation and their growth decline was related to decreases in the standardized precipitation evapotranspiration index. Our findings suggest that moisture limitation, associated with declining SIE, might inhibit the positive effects of warming on shrub growth over a considerable part of the terrestrial Arctic, thereby complicating predictions of vegetation change and future tundra productivity.

Directional turnover towards larger-ranged plants over time and across habitats.

Species turnover is ubiquitous. However, it remains unknown whether certain types of species are consistently gained or lost across different habitats. Here, we analysed the trajectories of 1827 plant species over time intervals of up to 78 years at 141 sites across mountain summits, forests, and lowland grasslands in Europe. We found, albeit with relatively small effect sizes, displacements of smaller- by larger-ranged species across habitats. Communities shifted in parallel towards more nutrient-demanding species, with species from nutrient-rich habitats having larger ranges. Because these species are typically strong competitors, declines of smaller-ranged species could reflect not only abiotic drivers of global change, but also biotic pressure from increased competition. The ubiquitous component of turnover based on species range size we found here may partially reconcile findings of no net loss in local diversity with global species loss, and link community-scale turnover to macroecological processes such as biotic homogenisation.

Plant traits inform predictions of tundra responses to global change.

Contents Summary 1742 I. Introduction 1742 II. The global context of tundra trait variation 1743 III. The current state of knowledge on trait change in the tundra biome 1744 IV. The links between traits and ecosystem functions 1744 V. Future priorities for tundra trait research 1746 VI. Conclusions 1746 References 1747 SUMMARY: In the rapidly warming tundra biome, plant traits provide an essential link between ongoing vegetation change and feedbacks to key ecosystem functions. However, only recently have comprehensive trait data been compiled for tundra species and sites, allowing us to assess key elements of functional responses to global change. In this review, we summarize trait-based research in tundra ecosystems, with a focus on three components: plant trait variation and how it compares with global patterns; shifts in community-level traits in response to environmental change; and the use of traits to understand and predict ecosystem function. Quantifying patterns and trends in plant traits will allow us to better project the consequences of environmental change for the ecology and functioning of tundra ecosystems.

Local snow melt and temperature-but not regional sea ice-explain variation in spring phenology in coastal Arctic tundra.

The Arctic is undergoing dramatic environmental change with rapidly rising surface temperatures, accelerating sea ice decline and changing snow regimes, all of which influence tundra plant phenology. Despite these changes, no globally consistent direction of trends in spring phenology has been reported across the Arctic. While spring has advanced at some sites, spring has delayed or not changed at other sites, highlighting substantial unexplained variation. Here, we test the relative importance of local temperatures, local snow melt date and regional spring drop in sea ice extent as controls of variation in spring phenology across different sites and species. Trends in long-term time series of spring leaf-out and flowering (average span: 18 years) were highly variable for the 14 tundra species monitored at our four study sites on the Arctic coasts of Alaska, Canada and Greenland, ranging from advances of 10.06 days per decade to delays of 1.67 days per decade. Spring temperatures and the day of spring drop in sea ice extent advanced at all sites (average 1°C per decade and 21 days per decade, respectively), but only those sites with advances in snow melt (average 5 days advance per decade) also had advancing phenology. Variation in spring plant phenology was best explained by snow melt date (mean effect: 0.45 days advance in phenology per day advance snow melt) and, to a lesser extent, by mean spring temperature (mean effect: 2.39 days advance in phenology per °C). In contrast to previous studies examining sea ice and phenology at different spatial scales, regional spring drop in sea ice extent did not predict spring phenology for any species or site in our analysis. Our findings highlight that tundra vegetation responses to global change are more complex than a direct response to warming and emphasize the importance of snow melt as a local driver of tundra spring phenology.

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.

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.

Different parts, different stories: climate sensitivity of growth is stronger in root collars vs. stems in tundra shrubs.

Shrub densification has been widely reported across the circumpolar arctic and subarctic biomes in recent years. Long-term analyses based on dendrochronological techniques applied to shrubs have linked this phenomenon to climate change. However, the multi-stemmed structure of shrubs makes them difficult to sample and therefore leads to non-uniform sampling protocols among shrub ecologists, who will favor either root collars or stems to conduct dendrochronological analyses. Through a comparative study of the use of root collars and stems of Betula glandulosa, a common North American shrub species, we evaluated the relative sensitivity of each plant part to climate variables and assessed whether this sensitivity is consistent across three different types of environments in northwestern Québec, Canada (terrace, hilltop and snowbed). We found that root collars had greater sensitivity to climate than stems and that these differences were maintained across the three types of environments. Growth at the root collar was best explained by spring precipitation and summer temperature, whereas stem growth showed weak and inconsistent responses to climate variables. Moreover, sensitivity to climate was not consistent among plant parts, as individuals having climate-sensitive root collars did not tend to have climate-sensitive stems. These differences in sensitivity of shrub parts to climate highlight the complexity of resource allocation in multi-stemmed plants. Whereas stem initiation and growth are driven by microenvironmental variables such as light availability and competition, root collars integrate the growth of all plant parts instead, rendering them less affected by mechanisms such as competition and more responsive to signals of global change. Although further investigations are required to determine the degree to which these findings are generalizable across the tundra biome, our results indicate that consistency and caution in the choice of plant parts are a key consideration for the success of future dendroclimatological studies on shrubs.

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.

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.

A synthesis of methane emissions from 71 northern, temperate, and subtropical wetlands.

Wetlands are the largest natural source of atmospheric methane. Here, we assess controls on methane flux using a database of approximately 19 000 instantaneous measurements from 71 wetland sites located across subtropical, temperate, and northern high latitude regions. Our analyses confirm general controls on wetland methane emissions from soil temperature, water table, and vegetation, but also show that these relationships are modified depending on wetland type (bog, fen, or swamp), region (subarctic to temperate), and disturbance. Fen methane flux was more sensitive to vegetation and less sensitive to temperature than bog or swamp fluxes. The optimal water table for methane flux was consistently below the peat surface in bogs, close to the peat surface in poor fens, and above the peat surface in rich fens. However, the largest flux in bogs occurred when dry 30-day averaged antecedent conditions were followed by wet conditions, while in fens and swamps, the largest flux occurred when both 30-day averaged antecedent and current conditions were wet. Drained wetlands exhibited distinct characteristics, e.g. the absence of large flux following wet and warm conditions, suggesting that the same functional relationships between methane flux and environmental conditions cannot be used across pristine and disturbed wetlands. Together, our results suggest that water table and temperature are dominant controls on methane flux in pristine bogs and swamps, while other processes, such as vascular transport in pristine fens, have the potential to partially override the effect of these controls in other wetland types. Because wetland types vary in methane emissions and have distinct controls, these ecosystems need to be considered separately to yield reliable estimates of global wetland methane release.

Historical ecology: using unconventional data sources to test for effects of global environmental change.

Predicting the future ecological impact of global change drivers requires understanding how these same drivers have acted in the past to produce the plant populations and communities we see today. Historical ecological data sources have made contributions of central importance to global change biology, but remain outside the toolkit of most ecologists. Here we review the strengths and weaknesses of four unconventional sources of historical ecological data: land survey records, "legacy" vegetation data, historical maps and photographs, and herbarium specimens. We discuss recent contributions made using these data sources to understanding the impacts of habitat disturbance and climate change on plant populations and communities, and the duration of extinction-colonization time lags in response to landscape change. Historical data frequently support inferences made using conventional ecological studies (e.g., increases in warm-adapted species as temperature rises), but there are cases when the addition of different data sources leads to different conclusions (e.g., temporal vegetation change not as predicted by chronosequence studies). The explicit combination of historical and contemporary data sources is an especially powerful approach for unraveling long-term consequences of multiple drivers of global change. Despite the limitations of historical data, which include spotty and potentially biased spatial and temporal coverage, they often represent the only means of characterizing ecological phenomena in the past and have proven indispensable for characterizing the nature, magnitude, and generality of global change impacts on plant populations and communities.

Looking back on biodiversity change: lessons for the road ahead.

Estimating biodiversity change across the planet in the context of widespread human modification is a critical challenge. Here, we review how biodiversity has changed in recent decades across scales and taxonomic groups, focusing on four diversity metrics: species richness, temporal turnover, spatial beta-diversity and abundance. At local scales, change across all metrics includes many examples of both increases and declines and tends to be centred around zero, but with higher prevalence of declining trends in beta-diversity (increasing similarity in composition across space or biotic homogenization) and abundance. The exception to this pattern is temporal turnover, with changes in species composition through time observed in most local assemblages. Less is known about change at regional scales, although several studies suggest that increases in richness are more prevalent than declines. Change at the global scale is the hardest to estimate accurately, but most studies suggest extinction rates are probably outpacing speciation rates, although both are elevated. Recognizing this variability is essential to accurately portray how biodiversity change is unfolding, and highlights how much remains unknown about the magnitude and direction of multiple biodiversity metrics at different scales. Reducing these blind spots is essential to allow appropriate management actions to be deployed. This article is part of the theme issue 'Detecting and attributing the causes of biodiversity change: needs, gaps and solutions'.

Plant traits poorly predict winner and loser shrub species in a warming tundra biome.

Climate change is leading to species redistributions. In the tundra biome, shrubs are generally expanding, but not all tundra shrub species will benefit from warming. Winner and loser species, and the characteristics that may determine success or failure, have not yet been fully identified. Here, we investigate whether past abundance changes, current range sizes and projected range shifts derived from species distribution models are related to plant trait values and intraspecific trait variation. We combined 17,921 trait records with observed past and modelled future distributions from 62 tundra shrub species across three continents. We found that species with greater variation in seed mass and specific leaf area had larger projected range shifts, and projected winner species had greater seed mass values. However, trait values and variation were not consistently related to current and projected ranges, nor to past abundance change. Overall, our findings indicate that abundance change and range shifts will not lead to directional modifications in shrub trait composition, since winner and loser species share relatively similar trait spaces.

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.

Uniform female-biased sex ratios in alpine willows.

PREMISE OF THE STUDY: The development of biased sex ratios in dioecious plant species has been ascribed to either (1) factors influencing differential adult mortality of male and female plants or (2) factors acting at an early life stage that determine seed sex ratio or seedling survival. METHODS: To discriminate between these two competing hypotheses, we surveyed sex and age of 379 individuals from five species of the genus Salix across 11 alpine valleys in the southwest Yukon. KEY RESULTS: We observed uniformly female-biased sex ratios of approximately 2:1 across all adult age cohorts and patch sizes of the five willow species. No spatial variation in sex ratio occurred that could be associated with site-specific characteristics such as elevation or aspect. CONCLUSIONS: Our results indicate that the female-biased sex ratios in the alpine willow species investigated in this study are not a consequence of ecological processes acting on established adult plants. The sex ratio is instead determined at an early life stage by a mechanism that remains unknown.

Global application of an unoccupied aerial vehicle photogrammetry protocol for predicting aboveground biomass in non-forest ecosystems.

Non-forest ecosystems, dominated by shrubs, grasses and herbaceous plants, provide ecosystem services including carbon sequestration and forage for grazing, and are highly sensitive to climatic changes. Yet these ecosystems are poorly represented in remotely sensed biomass products and are undersampled by in situ monitoring. Current global change threats emphasize the need for new tools to capture biomass change in non-forest ecosystems at appropriate scales. Here we developed and deployed a new protocol for photogrammetric height using unoccupied aerial vehicle (UAV) images to test its capability for delivering standardized measurements of biomass across a globally distributed field experiment. We assessed whether canopy height inferred from UAV photogrammetry allows the prediction of aboveground biomass (AGB) across low-stature plant species by conducting 38 photogrammetric surveys over 741 harvested plots to sample 50 species. We found mean canopy height was strongly predictive of AGB across species, with a median adjusted R 2 of 0.87 (ranging from 0.46 to 0.99) and median prediction error from leave-one-out cross-validation of 3.9%. Biomass per-unit-of-height was similar within but different among, plant functional types. We found that photogrammetric reconstructions of canopy height were sensitive to wind speed but not sun elevation during surveys. We demonstrated that our photogrammetric approach produced generalizable measurements across growth forms and environmental settings and yielded accuracies as good as those obtained from in situ approaches. We demonstrate that using a standardized approach for UAV photogrammetry can deliver accurate AGB estimates across a wide range of dynamic and heterogeneous ecosystems. Many academic and land management institutions have the technical capacity to deploy these approaches over extents of 1-10 ha-1. Photogrammetric approaches could provide much-needed information required to calibrate and validate the vegetation models and satellite-derived biomass products that are essential to understand vulnerable and understudied non-forested ecosystems around the globe.

Expansion of canopy-forming willows over the twentieth century on Herschel Island, Yukon Territory, Canada.

Canopy-forming shrubs are reported to be increasing at sites around the circumpolar Arctic. Our results indicate expansion in canopy cover and height of willows on Herschel Island located at 70 degrees north on the western Arctic coast of the Yukon Territory. We examined historic photographs, repeated vegetation surveys, and conducted monitoring of long-term plots and found evidence of increases of each of the dominant canopy-forming willow species (Salix richardsonii, Salix glauca and Salix pulchra), during the twentieth century. A simple model of patch initiation indicates that the majority of willow patches for each of these species became established between 1910 and 1960, with stem ages and maximum growth rates indicating that some patches could have established as late as the 1980s. Collectively, these results suggest that willow species are increasing in canopy cover and height on Herschel Island. We did not find evidence that expansion of willow patches is currently limited by herbivory, disease, or growing conditions.

Multi-decadal changes in tundra environments and ecosystems: synthesis of the International Polar Year-Back to the Future project (IPY-BTF).

Understanding the responses of tundra systems to global change has global implications. Most tundra regions lack sustained environmental monitoring and one of the only ways to document multi-decadal change is to resample historic research sites. The International Polar Year (IPY) provided a unique opportunity for such research through the Back to the Future (BTF) project (IPY project #512). This article synthesizes the results from 13 papers within this Ambio Special Issue. Abiotic changes include glacial recession in the Altai Mountains, Russia; increased snow depth and hardness, permafrost warming, and increased growing season length in sub-arctic Sweden; drying of ponds in Greenland; increased nutrient availability in Alaskan tundra ponds, and warming at most locations studied. Biotic changes ranged from relatively minor plant community change at two sites in Greenland to moderate change in the Yukon, and to dramatic increases in shrub and tree density on Herschel Island, and in subarctic Sweden. The population of geese tripled at one site in northeast Greenland where biomass in non-grazed plots doubled. A model parameterized using results from a BTF study forecasts substantial declines in all snowbeds and increases in shrub tundra on Niwot Ridge, Colorado over the next century. In general, results support and provide improved capacities for validating experimental manipulation, remote sensing, and modeling studies.