High exposure of global tree diversity to human pressure.

Safeguarding Earth's tree diversity is a conservation priority due to the importance of trees for biodiversity and ecosystem functions and services such as carbon sequestration. Here, we improve the foundation for effective conservation of global tree diversity by analyzing a recently developed database of tree species covering 46,752 species. We quantify range protection and anthropogenic pressures for each species and develop conservation priorities across taxonomic, phylogenetic, and functional diversity dimensions. We also assess the effectiveness of several influential proposed conservation prioritization frameworks to protect the top 17% and top 50% of tree priority areas. We find that an average of 50.2% of a tree species' range occurs in 110-km grid cells without any protected areas (PAs), with 6,377 small-range tree species fully unprotected, and that 83% of tree species experience nonnegligible human pressure across their range on average. Protecting high-priority areas for the top 17% and 50% priority thresholds would increase the average protected proportion of each tree species' range to 65.5% and 82.6%, respectively, leaving many fewer species (2,151 and 2,010) completely unprotected. The priority areas identified for trees match well to the Global 200 Ecoregions framework, revealing that priority areas for trees would in large part also optimize protection for terrestrial biodiversity overall. Based on range estimates for >46,000 tree species, our findings show that a large proportion of tree species receive limited protection by current PAs and are under substantial human pressure. Improved protection of biodiversity overall would also strongly benefit global tree diversity.

Structure and function of the global topsoil microbiome.

Soils harbour some of the most diverse microbiomes on Earth and are essential for both nutrient cycling and carbon storage. To understand soil functioning, it is necessary to model the global distribution patterns and functional gene repertoires of soil microorganisms, as well as the biotic and environmental associations between the diversity and structure of both bacterial and fungal soil communities1-4. Here we show, by leveraging metagenomics and metabarcoding of global topsoil samples (189 sites, 7,560 subsamples), that bacterial, but not fungal, genetic diversity is highest in temperate habitats and that microbial gene composition varies more strongly with environmental variables than with geographic distance. We demonstrate that fungi and bacteria show global niche differentiation that is associated with contrasting diversity responses to precipitation and soil pH. Furthermore, we provide evidence for strong bacterial-fungal antagonism, inferred from antibiotic-resistance genes, in topsoil and ocean habitats, indicating the substantial role of biotic interactions in shaping microbial communities. Our results suggest that both competition and environmental filtering affect the abundance, composition and encoded gene functions of bacterial and fungal communities, indicating that the relative contributions of these microorganisms to global nutrient cycling varies spatially.

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.

Root traits as drivers of plant and ecosystem functioning: current understanding, pitfalls and future research needs.

The effects of plants on the biosphere, atmosphere and geosphere are key determinants of terrestrial ecosystem functioning. However, despite substantial progress made regarding plant belowground components, we are still only beginning to explore the complex relationships between root traits and functions. Drawing on the literature in plant physiology, ecophysiology, ecology, agronomy and soil science, we reviewed 24 aspects of plant and ecosystem functioning and their relationships with a number of root system traits, including aspects of architecture, physiology, morphology, anatomy, chemistry, biomechanics and biotic interactions. Based on this assessment, we critically evaluated the current strengths and gaps in our knowledge, and identify future research challenges in the field of root ecology. Most importantly, we found that belowground traits with the broadest importance in plant and ecosystem functioning are not those most commonly measured. Also, the estimation of trait relative importance for functioning requires us to consider a more comprehensive range of functionally relevant traits from a diverse range of species, across environments and over time series. We also advocate that establishing causal hierarchical links among root traits will provide a hypothesis-based framework to identify the most parsimonious sets of traits with the strongest links on functions, and to link genotypes to plant and ecosystem functioning.

A starting guide to root ecology: strengthening ecological concepts and standardising root classification, sampling, processing and trait measurements.

In the context of a recent massive increase in research on plant root functions and their impact on the environment, root ecologists currently face many important challenges to keep on generating cutting-edge, meaningful and integrated knowledge. Consideration of the below-ground components in plant and ecosystem studies has been consistently called for in recent decades, but methodology is disparate and sometimes inappropriate. This handbook, based on the collective effort of a large team of experts, will improve trait comparisons across studies and integration of information across databases by providing standardised methods and controlled vocabularies. It is meant to be used not only as starting point by students and scientists who desire working on below-ground ecosystems, but also by experts for consolidating and broadening their views on multiple aspects of root ecology. Beyond the classical compilation of measurement protocols, we have synthesised recommendations from the literature to provide key background knowledge useful for: (1) defining below-ground plant entities and giving keys for their meaningful dissection, classification and naming beyond the classical fine-root vs coarse-root approach; (2) considering the specificity of root research to produce sound laboratory and field data; (3) describing typical, but overlooked steps for studying roots (e.g. root handling, cleaning and storage); and (4) gathering metadata necessary for the interpretation of results and their reuse. Most importantly, all root traits have been introduced with some degree of ecological context that will be a foundation for understanding their ecological meaning, their typical use and uncertainties, and some methodological and conceptual perspectives for future research. Considering all of this, we urge readers not to solely extract protocol recommendations for trait measurements from this work, but to take a moment to read and reflect on the extensive information contained in this broader guide to root ecology, including sections I-VII and the many introductions to each section and root trait description. Finally, it is critical to understand that a major aim of this guide is to help break down barriers between the many subdisciplines of root ecology and ecophysiology, broaden researchers' views on the multiple aspects of root study and create favourable conditions for the inception of comprehensive experiments on the role of roots in plant and ecosystem functioning.

Symbiont switching and alternative resource acquisition strategies drive mutualism breakdown.

Cooperative interactions among species, termed mutualisms, have played a crucial role in the evolution of life on Earth. However, despite key potential benefits to partners, there are many cases in which two species cease to cooperate and mutualisms break down. What factors drive the evolutionary breakdown of mutualism? We examined the pathways toward breakdowns of the mutualism between plants and arbuscular mycorrhizal fungi. By using a comparative approach, we identify ∼25 independent cases of complete mutualism breakdown across global seed plants. We found that breakdown of cooperation was only stable when host plants (i) partner with other root symbionts or (ii) evolve alternative resource acquisition strategies. Our results suggest that key mutualistic services are only permanently lost if hosts evolve alternative symbioses or adaptations.

FungalRoot: global online database of plant mycorrhizal associations.

Testing of ecological, biogeographical and phylogenetic hypotheses of mycorrhizal traits requires a comprehensive reference dataset about plant mycorrhizal associations. Here we present a database, FungalRoot, which summarizes publicly available data about vascular plant mycorrhizal type and intensity of root colonization by mycorrhizal fungi, accompanied with rich metadata. We compiled and digitized data about plant mycorrhizal colonization in nine widespread languages. The present version of the FungalRoot database contains 36 303 species-by-site observations for 14 870 plant species, tripling the previously available compiled information about plant mycorrhizal associations. Based on these data, we provide a recommended list of genus-level plant mycorrhizal associations, based on the majority of data for species and careful analysis of conflicting data. The majority of ectomycorrhizal and ericoid mycorrhizal plants are trees (92%) and shrubs (85%), respectively. The majority of arbuscular and nonmycorrhizal plant species are herbaceous (50% and 70%, respectively). Our publicly available database is a powerful resource for mycorrhizal scientists and ecologists. It features possibilities for dynamic updating and addition of data about plant mycorrhizal associations. The new database will promote research on plant and fungal biogeography and evolution, and on links between above- and belowground biodiversity and ecosystem functioning.

Assessing the reliability of predicted plant trait distributions at the global scale.

AIM: Predictions of plant traits over space and time are increasingly used to improve our understanding of plant community responses to global environmental change. A necessary step forward is to assess the reliability of global trait predictions. In this study, we predict community mean plant traits at the global scale and present a systematic evaluation of their reliability in terms of the accuracy of the models, ecological realism and various sources of uncertainty. LOCATION: Global. TIME PERIOD: Present. MAJOR TAXA STUDIED: Vascular plants. METHODS: We predicted global distributions of community mean specific leaf area, leaf nitrogen concentration, plant height and wood density with an ensemble modelling approach based on georeferenced, locally measured trait data representative of the plant community. We assessed the predictive performance of the models, the plausibility of predicted trait combinations, the influence of data quality, and the uncertainty across geographical space attributed to spatial extrapolation and diverging model predictions. RESULTS: Ensemble predictions of community mean plant height, specific leaf area and wood density resulted in ecologically plausible trait-environment relationships and trait-trait combinations. Leaf nitrogen concentration, however, could not be predicted reliably. The ensemble approach was better at predicting community trait means than any of the individual modelling techniques, which varied greatly in predictive performance and led to divergent predictions, mostly in African deserts and the Arctic, where predictions were also extrapolated. High data quality (i.e., including intraspecific variability and a representative species sample) increased model performance by 28%. MAIN CONCLUSIONS: Plant community traits can be predicted reliably at the global scale when using an ensemble approach and high-quality data for traits that mostly respond to large-scale environmental factors. We recommend applying ensemble forecasting to account for model uncertainty, using representative trait data, and more routinely assessing the reliability of trait predictions.

Does the leaf economic spectrum hold within plant functional types? A Bayesian multivariate trait meta-analysis.

The leaf economic spectrum is a widely studied axis of plant trait variability that defines a trade-off between leaf longevity and productivity. While this has been investigated at the global scale, where it is robust, and at local scales, where deviations from it are common, it has received less attention at the intermediate scale of plant functional types (PFTs). We investigated whether global leaf economic relationships are also present within the scale of plant functional types (PFTs) commonly used by Earth System models, and the extent to which this global-PFT hierarchy can be used to constrain trait estimates. We developed a hierarchical multivariate Bayesian model that assumes separate means and covariance structures within and across PFTs and fit this model to seven leaf traits from the TRY database related to leaf longevity, morphology, biochemistry, and photosynthetic metabolism. Although patterns of trait covariation were generally consistent with the leaf economic spectrum, we found three approximate tiers to this consistency. Relationships among morphological and biochemical traits (specific leaf area [SLA], N, P) were the most robust within and across PFTs, suggesting that covariation in these traits is driven by universal leaf construction trade-offs and stoichiometry. Relationships among metabolic traits (dark respiration [Rd ], maximum RuBisCo carboxylation rate [Vc,max ], maximum electron transport rate [Jmax ]) were slightly less consistent, reflecting in part their much sparser sampling (especially for high-latitude PFTs), but also pointing to more flexible plasticity in plant metabolistm. Finally, relationships involving leaf lifespan were the least consistent, indicating that leaf economic relationships related to leaf lifespan are dominated by across-PFT differences and that within-PFT variation in leaf lifespan is more complex and idiosyncratic. Across all traits, this covariance was an important source of information, as evidenced by the improved imputation accuracy and reduced predictive uncertainty in multivariate models compared to univariate models. Ultimately, our study reaffirms the value of studying not just individual traits but the multivariate trait space and the utility of hierarchical modeling for studying the scale dependence of trait relationships.

Mapping local and global variability in plant trait distributions.

Our ability to understand and predict the response of ecosystems to a changing environment depends on quantifying vegetation functional diversity. However, representing this diversity at the global scale is challenging. Typically, in Earth system models, characterization of plant diversity has been limited to grouping related species into plant functional types (PFTs), with all trait variation in a PFT collapsed into a single mean value that is applied globally. Using the largest global plant trait database and state of the art Bayesian modeling, we created fine-grained global maps of plant trait distributions that can be applied to Earth system models. Focusing on a set of plant traits closely coupled to photosynthesis and foliar respiration-specific leaf area (SLA) and dry mass-based concentrations of leaf nitrogen ([Formula: see text]) and phosphorus ([Formula: see text]), we characterize how traits vary within and among over 50,000 [Formula: see text]-km cells across the entire vegetated land surface. We do this in several ways-without defining the PFT of each grid cell and using 4 or 14 PFTs; each model's predictions are evaluated against out-of-sample data. This endeavor advances prior trait mapping by generating global maps that preserve variability across scales by using modern Bayesian spatial statistical modeling in combination with a database over three times larger than that in previous analyses. Our maps reveal that the most diverse grid cells possess trait variability close to the range of global PFT means.

Asynchrony among local communities stabilises ecosystem function of metacommunities.

Temporal stability of ecosystem functioning increases the predictability and reliability of ecosystem services, and understanding the drivers of stability across spatial scales is important for land management and policy decisions. We used species-level abundance data from 62 plant communities across five continents to assess mechanisms of temporal stability across spatial scales. We assessed how asynchrony (i.e. different units responding dissimilarly through time) of species and local communities stabilised metacommunity ecosystem function. Asynchrony of species increased stability of local communities, and asynchrony among local communities enhanced metacommunity stability by a wide range of magnitudes (1-315%); this range was positively correlated with the size of the metacommunity. Additionally, asynchronous responses among local communities were linked with species' populations fluctuating asynchronously across space, perhaps stemming from physical and/or competitive differences among local communities. Accordingly, we suggest spatial heterogeneity should be a major focus for maintaining the stability of ecosystem services at larger spatial scales.

A global Fine-Root Ecology Database to address below-ground challenges in plant ecology.

Variation and tradeoffs within and among plant traits are increasingly being harnessed by empiricists and modelers to understand and predict ecosystem processes under changing environmental conditions. While fine roots play an important role in ecosystem functioning, fine-root traits are underrepresented in global trait databases. This has hindered efforts to analyze fine-root trait variation and link it with plant function and environmental conditions at a global scale. This Viewpoint addresses the need for a centralized fine-root trait database, and introduces the Fine-Root Ecology Database (FRED, http://roots.ornl.gov) which so far includes > 70 000 observations encompassing a broad range of root traits and also includes associated environmental data. FRED represents a critical step toward improving our understanding of below-ground plant ecology. For example, FRED facilitates the quantification of variation in fine-root traits across root orders, species, biomes, and environmental gradients while also providing a platform for assessments of covariation among root, leaf, and wood traits, the role of fine roots in ecosystem functioning, and the representation of fine roots in terrestrial biosphere models. Continued input of observations into FRED to fill gaps in trait coverage will improve our understanding of changes in fine-root traits across space and time.

Functional traits predict relationship between plant abundance dynamic and long-term climate warming.

Predicting climate change impact on ecosystem structure and services is one of the most important challenges in ecology. Until now, plant species response to climate change has been described at the level of fixed plant functional types, an approach limited by its inflexibility as there is much interspecific functional variation within plant functional types. Considering a plant species as a set of functional traits greatly increases our possibilities for analysis of ecosystem functioning and carbon and nutrient fluxes associated therewith. Moreover, recently assembled large-scale databases hold comprehensive per-species data on plant functional traits, allowing a detailed functional description of many plant communities on Earth. Here, we show that plant functional traits can be used as predictors of vegetation response to climate warming, accounting in our test ecosystem (the species-rich alpine belt of Caucasus mountains, Russia) for 59% of variability in the per-species abundance relation to temperature. In this mountain belt, traits that promote conservative leaf water economy (higher leaf mass per area, thicker leaves) and large investments in belowground reserves to support next year's shoot buds (root carbon content) were the best predictors of the species increase in abundance along with temperature increase. This finding demonstrates that plant functional traits constitute a highly useful concept for forecasting changes in plant communities, and their associated ecosystem services, in response to climate change.

Quantitative assessment of the differential impacts of arbuscular and ectomycorrhiza on soil carbon cycling.

A significant fraction of carbon stored in the Earth's soil moves through arbuscular mycorrhiza (AM) and ectomycorrhiza (EM). The impacts of AM and EM on the soil carbon budget are poorly understood. We propose a method to quantify the mycorrhizal contribution to carbon cycling, explicitly accounting for the abundance of plant-associated and extraradical mycorrhizal mycelium. We discuss the need to acquire additional data to use our method, and present our new global database holding information on plant species-by-site intensity of root colonization by mycorrhizas. We demonstrate that the degree of mycorrhizal fungal colonization has globally consistent patterns across plant species. This suggests that the level of plant species-specific root colonization can be used as a plant trait. To exemplify our method, we assessed the differential impacts of AM : EM ratio and EM shrub encroachment on carbon stocks in sub-arctic tundra. AM and EM affect tundra carbon stocks at different magnitudes, and via partly distinct dominant pathways: via extraradical mycelium (both EM and AM) and via mycorrhizal impacts on above- and belowground biomass carbon (mostly AM). Our method provides a powerful tool for the quantitative assessment of mycorrhizal impact on local and global carbon cycling processes, paving the way towards an improved understanding of the role of mycorrhizas in the Earth's carbon cycle.

Fungal communities are passengers in community development of dune ecosystems, while bacteria are not.

An increasing number of studies of above-belowground interactions provide a fundamental basis for our understanding of the coexistence between plant and soil communities. However, we lack empirical evidence to understand the directionality of drivers of plant and soil communities under natural conditions: 'Are soil microorganisms driving plant community functioning or do they adapt to the plant community?' In a field experiment in an early successional dune ecosystem, we manipulated soil communities by adding living (i.e., natural microbial communities) and sterile soil inocula, originating from natural ecosystems, and examined the annual responses of soil and plant communities. The experimental manipulations had a persistent effect on the soil microbial community with divergent impacts for living and sterile soil inocula. The plant community was also affected by soil inoculation, but there was no difference between the impacts of living and sterile inocula. We also observed an increasing convergence of plant and soil microbial composition over time. Our results show that alterations in soil abiotic and biotic conditions have long-term effects on the composition of both plant and soil microbial communities. Importantly, our study provides direct evidence that soil microorganisms are not "drivers" of plant community dynamics. We found that soil fungi and bacteria manifest different community assemblies in response to treatments. Soil fungi act as "passengers," that is, soil microorganisms reflect plant community dynamics but do not alter it, whereas soil bacteria are neither "drivers" nor "passengers" of plant community dynamics in early successional ecosystems. These results are critical for understanding the community assembly of plant and soil microbial communities under natural conditions and are directly relevant for ecosystem management and restoration.

Limited effects of crop foliar Si fertilization on a marginal soil under a future climate scenario.

Growing crops on marginal lands is a promising solution to alleviate the increasing pressure on agricultural land in Europe. Such crops will however be at the same time exposed to increased drought and pathogen prevalence, on already challenging soil conditions. Some sustainable practices, such as Silicon (Si) foliar fertilization, have been proposed to alleviate these two stress factors, but have not been tested under controlled, future climate conditions. We hypothesized that Si foliar fertilization would be beneficial for crops under future climate, and would have cascading beneficial effects on ecosystem processes, as many of them are directly dependent on plant health. We tested this hypothesis by exposing spring barley growing on marginal soil macrocosms (three with, three without Si treatment) to 2070 climate projections in an ecotron facility. Using the high-capacity monitoring of the ecotron, we estimated C, water, and N budgets of every macrocosm. Additionally, we measured crop yield, the biomass of each plant organ, and characterized bacterial communities using metabarcoding. Despite being exposed to water stress conditions, plants did not produce more biomass with the foliar Si fertilization, whatever the organ considered. Evapotranspiration (ET) was unaffected, as well as water quality and bacterial communities. However, in the 10-day period following two of the three Si applications, we measured a significant increase in C sequestration, when climate conditions where significantly drier, while ET remained the same. We interpreted these results as a less significant effect of Si treatment than expected as compared with literature, which could be explained by the high CO2 levels under future climate, that reduces need for stomata opening, and therefore sensitivity to drought. We conclude that making marginal soils climate proof using foliar Si treatments may not be a sufficient strategy, at least in this type of nutrient-poor, dry, sandy soil.

Fine-resolution global maps of root biomass carbon colonized by arbuscular and ectomycorrhizal fungi.

Despite the recognized importance of mycorrhizal associations in ecosystem functioning, the actual abundance patterns of mycorrhizal fungi belowground are still unknown. This information is key for better quantification of mycorrhizal impacts on ecosystem processes and for incorporating mycorrhizal pathways into global biogeochemical models. Here we present the first high-resolution maps of fine root stocks colonized by arbuscular mycorrhizal (AM) and ectomycorrhizal (EcM) fungi (MgC ha-1). The maps were assembled by combining multiple open-source databases holding information on root biomass carbon, the proportion of AM and EcM tree biomass, plot-level relative abundance of plant species and intensity of AM and EcM root colonization. We calculated root-associated AM and EcM abundance in 881 spatial units, defined as the combination of ecoregions and land cover types across six continents. The highest AM abundances are observed in the (sub-)tropics, while the highest EcM abundances occur in the taiga regions. These maps serve as a basis for future research where continuous spatial estimates of root mycorrhizal stocks are needed.

Mycorrhizal mycelium as a global carbon pool.

For more than 400 million years, mycorrhizal fungi and plants have formed partnerships that are crucial to the emergence and functioning of global ecosystems. The importance of these symbiotic fungi for plant nutrition is well established. However, the role of mycorrhizal fungi in transporting carbon into soil systems on a global scale remains under-explored. This is surprising given that ∼75% of terrestrial carbon is stored belowground and mycorrhizal fungi are stationed at a key entry point of carbon into soil food webs. Here, we analyze nearly 200 datasets to provide the first global quantitative estimates of carbon allocation from plants to the mycelium of mycorrhizal fungi. We estimate that global plant communities allocate 3.93 Gt CO2e per year to arbuscular mycorrhizal fungi, 9.07 Gt CO2e per year to ectomycorrhizal fungi, and 0.12 Gt CO2e per year to ericoid mycorrhizal fungi. Based on this estimate, 13.12 Gt of CO2e fixed by terrestrial plants is, at least temporarily, allocated to the underground mycelium of mycorrhizal fungi per year, equating to ∼36% of current annual CO2 emissions from fossil fuels. We explore the mechanisms by which mycorrhizal fungi affect soil carbon pools and identify approaches to increase our understanding of global carbon fluxes via plant-fungal pathways. Our estimates, although based on the best available evidence, are imperfect and should be interpreted with caution. Nonetheless, our estimations are conservative, and we argue that this work confirms the significant contribution made by mycorrhizal associations to global carbon dynamics. Our findings should motivate their inclusion both within global climate and carbon cycling models, and within conservation policy and practice.