Shifts in soil ammonia-oxidizing community maintain the nitrogen stimulation of nitrification across climatic conditions.

Anthropogenic nitrogen (N) loading alters soil ammonia-oxidizing archaea (AOA) and bacteria (AOB) abundances, likely leading to substantial changes in soil nitrification. However, the factors and mechanisms determining the responses of soil AOA:AOB and nitrification to N loading are still unclear, making it difficult to predict future changes in soil nitrification. Herein, we synthesize 68 field studies around the world to evaluate the impacts of N loading on soil ammonia oxidizers and nitrification. Across a wide range of biotic and abiotic factors, climate is the most important driver of the responses of AOA:AOB to N loading. Climate does not directly affect the N-stimulation of nitrification, but does so via climate-related shifts in AOA:AOB. Specifically, climate modulates the responses of AOA:AOB to N loading by affecting soil pH, N-availability and moisture. AOB play a dominant role in affecting nitrification in dry climates, while the impacts from AOA can exceed AOB in humid climates. Together, these results suggest that climate-related shifts in soil ammonia-oxidizing community maintain the N-stimulation of nitrification, highlighting the importance of microbial community composition in mediating the responses of the soil N cycle to N loading.

Functional rarity and evenness are key facets of biodiversity to boost multifunctionality.

The functional traits of organisms within multispecies assemblages regulate biodiversity effects on ecosystem functioning. Yet how traits should assemble to boost multiple ecosystem functions simultaneously (multifunctionality) remains poorly explored. In a multibiome litter experiment covering most of the global variation in leaf trait spectra, we showed that three dimensions of functional diversity (dispersion, rarity, and evenness) explained up to 66% of variations in multifunctionality, although the dominant species and their traits remained an important predictor. While high dispersion impeded multifunctionality, increasing the evenness among functionally dissimilar species was a key dimension to promote higher multifunctionality and to reduce the abundance of plant pathogens. Because too-dissimilar species could have negative effects on ecosystems, our results highlight the need for not only diverse but also functionally even assemblages to promote multifunctionality. The effect of functionally rare species strongly shifted from positive to negative depending on their trait differences with the dominant species. Simultaneously managing the dispersion, evenness, and rarity in multispecies assemblages could be used to design assemblages aimed at maximizing multifunctionality independently of the biome, the identity of dominant species, or the range of trait values considered. Functional evenness and rarity offer promise to improve the management of terrestrial ecosystems and to limit plant disease risks.

The impact of agricultural management on soil aggregation and carbon storage is regulated by climatic thresholds across a 3000 km European gradient.

Organic carbon and aggregate stability are key features of soil quality and are important to consider when evaluating the potential of agricultural soils as carbon sinks. However, we lack a comprehensive understanding of how soil organic carbon (SOC) and aggregate stability respond to agricultural management across wide environmental gradients. Here, we assessed the impact of climatic factors, soil properties and agricultural management (including land use, crop cover, crop diversity, organic fertilization, and management intensity) on SOC and the mean weight diameter of soil aggregates, commonly used as an indicator for soil aggregate stability, across a 3000 km European gradient. Soil aggregate stability (-56%) and SOC stocks (-35%) in the topsoil (20 cm) were lower in croplands compared with neighboring grassland sites (uncropped sites with perennial vegetation and little or no external inputs). Land use and aridity were strong drivers of soil aggregation explaining 33% and 20% of the variation, respectively. SOC stocks were best explained by calcium content (20% of explained variation) followed by aridity (15%) and mean annual temperature (10%). We also found a threshold-like pattern for SOC stocks and aggregate stability in response to aridity, with lower values at sites with higher aridity. The impact of crop management on aggregate stability and SOC stocks appeared to be regulated by these thresholds, with more pronounced positive effects of crop diversity and more severe negative effects of crop management intensity in nondryland compared with dryland regions. We link the higher sensitivity of SOC stocks and aggregate stability in nondryland regions to a higher climatic potential for aggregate-mediated SOC stabilization. The presented findings are relevant for improving predictions of management effects on soil structure and C storage and highlight the need for site-specific agri-environmental policies to improve soil quality and C sequestration.

Diversity of archaea and niche preferences among putative ammonia-oxidizing Nitrososphaeria dominating across European arable soils.

Archaeal communities in arable soils are dominated by Nitrososphaeria, a class within Thaumarchaeota comprising all known ammonia-oxidizing archaea (AOA). AOA are key players in the nitrogen cycle and defining their niche specialization can help predicting effects of environmental change on these communities. However, hierarchical effects of environmental filters on AOA and the delineation of niche preferences of nitrososphaerial lineages remain poorly understood. We used phylogenetic information at fine scale and machine learning approaches to identify climatic, edaphic and geomorphological drivers of Nitrososphaeria and other archaea along a 3000 km European gradient. Only limited insights into the ecology of the low-abundant archaeal classes could be inferred, but our analyses underlined the multifactorial nature of niche differentiation within Nitrososphaeria. Mean annual temperature, C:N ratio and pH were the best predictors of their diversity, evenness and distribution. Thresholds in the predictions could be defined for C:N ratio and cation exchange capacity. Furthermore, multiple, independent and recent specializations to soil pH were detected in the Nitrososphaeria phylogeny. The coexistence of widespread ecophysiological differences between closely related soil Nitrososphaeria highlights that their ecology is best studied at fine phylogenetic scale.

Stimulation of ammonia oxidizer and denitrifier abundances by nitrogen loading: Poor predictability for increased soil N2 O emission.

Unprecedented nitrogen (N) inputs into terrestrial ecosystems have profoundly altered soil N cycling. Ammonia oxidizers and denitrifiers are the main producers of nitrous oxide (N2 O), but it remains unclear how ammonia oxidizer and denitrifier abundances will respond to N loading and whether their responses can predict N-induced changes in soil N2 O emission. By synthesizing 101 field studies worldwide, we showed that N loading significantly increased ammonia oxidizer abundance by 107% and denitrifier abundance by 45%. The increases in both ammonia oxidizer and denitrifier abundances were primarily explained by N loading form, and more specifically, organic N loading had stronger effects on their abundances than mineral N loading. Nitrogen loading increased soil N2 O emission by 261%, whereas there was no clear relationship between changes in soil N2 O emission and shifts in ammonia oxidizer and denitrifier abundances. Our field-based results challenge the laboratory-based hypothesis that increased ammonia oxidizer and denitrifier abundances by N loading would directly cause higher soil N2 O emission. Instead, key abiotic factors (mean annual precipitation, soil pH, soil C:N ratio, and ecosystem type) explained N-induced changes in soil N2 O emission. Altogether, these findings highlight the need for considering the roles of key abiotic factors in regulating soil N transformations under N loading to better understand the microbially mediated soil N2 O emission.

Climate mediates the biodiversity-ecosystem stability relationship globally.

The insurance hypothesis, stating that biodiversity can increase ecosystem stability, has received wide research and political attention. Recent experiments suggest that climate change can impact how plant diversity influences ecosystem stability, but most evidence of the biodiversity-stability relationship obtained to date comes from local studies performed under a limited set of climatic conditions. Here, we investigate how climate mediates the relationships between plant (taxonomical and functional) diversity and ecosystem stability across the globe. To do so, we coupled 14 years of temporal remote sensing measurements of plant biomass with field surveys of diversity in 123 dryland ecosystems from all continents except Antarctica. Across a wide range of climatic and soil conditions, plant species pools, and locations, we were able to explain 73% of variation in ecosystem stability, measured as the ratio of the temporal mean biomass to the SD. The positive role of plant diversity on ecosystem stability was as important as that of climatic and soil factors. However, we also found a strong climate dependency of the biodiversity-ecosystem stability relationship across our global aridity gradient. Our findings suggest that the diversity of leaf traits may drive ecosystem stability at low aridity levels, whereas species richness may have a greater stabilizing role under the most arid conditions evaluated. Our study highlights that to minimize variations in the temporal delivery of ecosystem services related to plant biomass, functional and taxonomic plant diversity should be particularly promoted under low and high aridity conditions, respectively.

Contrasting mechanisms underlie short- and longer-term soil respiration responses to experimental warming in a dryland ecosystem.

Soil carbon losses to the atmosphere through soil respiration are expected to rise with ongoing temperature increases, but available evidence from mesic biomes suggests that such response disappears after a few years of experimental warming. However, there is lack of empirical basis for these temporal dynamics in soil respiration responses, and for the mechanisms underlying them, in drylands, which collectively form the largest biome on Earth and store 32% of the global soil organic carbon pool. We coupled data from a 10 year warming experiment in a biocrust-dominated dryland ecosystem with laboratory incubations to confront 0-2 years (short-term hereafter) versus 8-10 years (longer-term hereafter) soil respiration responses to warming. Our results showed that increased soil respiration rates with short-term warming observed in areas with high biocrust cover returned to control levels in the longer-term. Warming-induced increases in soil temperature were the main drivers of the short-term soil respiration responses, whereas longer-term soil respiration responses to warming were primarily driven by thermal acclimation and warming-induced reductions in biocrust cover. Our results highlight the importance of evaluating short- and longer-term soil respiration responses to warming as a mean to reduce the uncertainty in predicting the soil carbon-climate feedback in drylands.

Plant domestication disrupts biodiversity effects across major crop types.

Plant diversity fosters productivity in natural ecosystems. Biodiversity effects might increase agricultural yields at no cost in additional inputs. However, the effects of diversity on crop assemblages are inconsistent, probably because crops and wild plants differ in a range of traits relevant to plant-plant interactions. We tested whether domestication has changed the potential of crop mixtures to over-yield by comparing the performance and traits of major crop species and those of their wild progenitors under varying levels of diversity. We found stronger biodiversity effects in mixtures of wild progenitors, due to larger selection effects. Variation in selection effects was partly explained by within-mixture differences in leaf size. Our results indicate that domestication might disrupt the ability of crops to benefit from diverse neighbourhoods via reduced trait variance. These results highlight potential limitations of current crop mixtures to over-yield and the potential of breeding to re-establish variance and increase mixture performance.

Increasing microbial carbon use efficiency with warming predicts soil heterotrophic respiration globally.

The degree to which climate warming will stimulate soil organic carbon (SOC) losses via heterotrophic respiration remains uncertain, in part because different or even opposite microbial physiology and temperature relationships have been proposed in SOC models. We incorporated competing microbial carbon use efficiency (CUE)-mean annual temperature (MAT) and enzyme kinetic-MAT relationships into SOC models, and compared the simulated mass-specific soil heterotrophic respiration rates with multiple published datasets of measured respiration. The measured data included 110 dryland soils globally distributed and two continental to global-scale cross-biome datasets. Model-data comparisons suggested that a positive CUE-MAT relationship best predicts the measured mass-specific soil heterotrophic respiration rates in soils distributed globally. These results are robust when considering models of increasing complexity and competing mechanisms driving soil heterotrophic respiration-MAT relationships (e.g., carbon substrate availability). Our findings suggest that a warmer climate selects for microbial communities with higher CUE, as opposed to the often hypothesized reductions in CUE by warming based on soil laboratory assays. Our results help to build the impetus for, and confidence in, including microbial mechanisms in soil biogeochemical models used to forecast changes in global soil carbon stocks in response to warming.

Decoupling of soil nutrient cycles as a function of aridity in global drylands.

The biogeochemical cycles of carbon (C), nitrogen (N) and phosphorus (P) are interlinked by primary production, respiration and decomposition in terrestrial ecosystems. It has been suggested that the C, N and P cycles could become uncoupled under rapid climate change because of the different degrees of control exerted on the supply of these elements by biological and geochemical processes. Climatic controls on biogeochemical cycles are particularly relevant in arid, semi-arid and dry sub-humid ecosystems (drylands) because their biological activity is mainly driven by water availability. The increase in aridity predicted for the twenty-first century in many drylands worldwide may therefore threaten the balance between these cycles, differentially affecting the availability of essential nutrients. Here we evaluate how aridity affects the balance between C, N and P in soils collected from 224 dryland sites from all continents except Antarctica. We find a negative effect of aridity on the concentration of soil organic C and total N, but a positive effect on the concentration of inorganic P. Aridity is negatively related to plant cover, which may favour the dominance of physical processes such as rock weathering, a major source of P to ecosystems, over biological processes that provide more C and N, such as litter decomposition. Our findings suggest that any predicted increase in aridity with climate change will probably reduce the concentrations of N and C in global drylands, but increase that of P. These changes would uncouple the C, N and P cycles in drylands and could negatively affect the provision of key services provided by these ecosystems.

Pathways regulating decreased soil respiration with warming in a biocrust-dominated dryland.

A positive soil carbon (C)-climate feedback is embedded into the climatic models of the IPCC. However, recent global syntheses indicate that the temperature sensitivity of soil respiration (RS ) in drylands, the largest biome on Earth, is actually lower in warmed than in control plots. Consequently, soil C losses with future warming are expected to be low compared with other biomes. Nevertheless, the empirical basis for these global extrapolations is still poor in drylands, due to the low number of field experiments testing the pathways behind the long-term responses of soil respiration (RS ) to warming. Importantly, global drylands are covered with biocrusts (communities formed by bryophytes, lichens, cyanobacteria, fungi, and bacteria), and thus, RS responses to warming may be driven by both autotrophic and heterotrophic pathways. Here, we evaluated the effects of 8-year experimental warming on RS , and the different pathways involved, in a biocrust-dominated dryland in southern Spain. We also assessed the overall impacts on soil organic C (SOC) accumulation over time. Across the years and biocrust cover levels, warming reduced RS by 0.30 µmol CO2  m-2  s-1 (95% CI = -0.24 to 0.84), although the negative warming effects were only significant after 3 years of elevated temperatures in areas with low initial biocrust cover. We found support for different pathways regulating the warming-induced reduction in RS at areas with low (microbial thermal acclimation via reduced soil mass-specific respiration and ß-glucosidase enzymatic activity) vs. high (microbial thermal acclimation jointly with a reduction in autotrophic respiration from decreased lichen cover) initial biocrust cover. Our 8-year experimental study shows a reduction in soil respiration with warming and highlights that biocrusts should be explicitly included in modeling efforts aimed to quantify the soil C-climate feedback in drylands.

Differential responses of carbon-degrading enzyme activities to warming: Implications for soil respiration.

Extracellular enzymes catalyze rate-limiting steps in soil organic matter decomposition, and their activities (EEAs) play a key role in determining soil respiration (SR). Both EEAs and SR are highly sensitive to temperature, but their responses to climate warming remain poorly understood. Here, we present a meta-analysis on the response of soil cellulase and ligninase activities and SR to warming, synthesizing data from 56 studies. We found that warming significantly enhanced ligninase activity by 21.4% but had no effect on cellulase activity. Increases in ligninase activity were positively correlated with changes in SR, while no such relationship was found for cellulase. The warming response of ligninase activity was more closely related to the responses of SR than a wide range of environmental and experimental methodological factors. Furthermore, warming effects on ligninase activity increased with experiment duration. These results suggest that soil microorganisms sustain long-term increases in SR with warming by gradually increasing the degradation of the recalcitrant carbon pool.

Structure and functioning of dryland ecosystems in a changing world.

Understanding how drylands respond to ongoing environmental change is extremely important for global sustainability. Here we review how biotic attributes, climate, grazing pressure, land cover change and nitrogen deposition affect the functioning of drylands at multiple spatial scales. Our synthesis highlights the importance of biotic attributes (e.g. species richness) in maintaining fundamental ecosystem processes such as primary productivity, illustrate how N deposition and grazing pressure are impacting ecosystem functioning in drylands worldwide, and highlight the importance of the traits of woody species as drivers of their expansion in former grasslands. We also emphasize the role of attributes such as species richness and abundance in controlling the responses of ecosystem functioning to climate change. This knowledge is essential to guide conservation and restoration efforts in drylands, as biotic attributes can be actively managed at the local scale to increase ecosystem resilience to global change.

Asymmetric responses of primary productivity to precipitation extremes: A synthesis of grassland precipitation manipulation experiments.

Climatic changes are altering Earth's hydrological cycle, resulting in altered precipitation amounts, increased interannual variability of precipitation, and more frequent extreme precipitation events. These trends will likely continue into the future, having substantial impacts on net primary productivity (NPP) and associated ecosystem services such as food production and carbon sequestration. Frequently, experimental manipulations of precipitation have linked altered precipitation regimes to changes in NPP. Yet, findings have been diverse and substantial uncertainty still surrounds generalities describing patterns of ecosystem sensitivity to altered precipitation. Additionally, we do not know whether previously observed correlations between NPP and precipitation remain accurate when precipitation changes become extreme. We synthesized results from 83 case studies of experimental precipitation manipulations in grasslands worldwide. We used meta-analytical techniques to search for generalities and asymmetries of aboveground NPP (ANPP) and belowground NPP (BNPP) responses to both the direction and magnitude of precipitation change. Sensitivity (i.e., productivity response standardized by the amount of precipitation change) of BNPP was similar under precipitation additions and reductions, but ANPP was more sensitive to precipitation additions than reductions; this was especially evident in drier ecosystems. Additionally, overall relationships between the magnitude of productivity responses and the magnitude of precipitation change were saturating in form. The saturating form of this relationship was likely driven by ANPP responses to very extreme precipitation increases, although there were limited studies imposing extreme precipitation change, and there was considerable variation among experiments. This highlights the importance of incorporating gradients of manipulations, ranging from extreme drought to extreme precipitation increases into future climate change experiments. Additionally, policy and land management decisions related to global change scenarios should consider how ANPP and BNPP responses may differ, and that ecosystem responses to extreme events might not be predicted from relationships found under moderate environmental changes.

Biogeographic bases for a shift in crop C : N : P stoichiometries during domestication.

We lack both a theoretical framework and solid empirical data to understand domestication impacts on plant chemistry. We hypothesised that domestication increased leaf N and P to support high plant production rates, but biogeographic and climate patterns further influenced the magnitude and direction of changes in specific aspects of chemistry and stoichiometry. To test these hypotheses, we used a data set of leaf C, N and P from 21 herbaceous crops and their wild progenitors. Domestication increased leaf N and/or P for 57% of the crops. Moreover, the latitude of the domestication sites (negatively related to temperature) modulated the domestication effects on P (+), C (-), N : P (-) and C : P (-) ratios. Further results from a litter decomposition assay showed that domestication effects on litter chemistry affected the availability of soil N and P. Our findings draw attention to evolutionary effects of domestication legacies on plant and soil stoichiometry and related ecosystem services (e.g. plant yield and soil fertility).

Temporal dynamics of biotic and abiotic drivers of litter decomposition.

Climate, litter quality and decomposers drive litter decomposition. However, little is known about whether their relative contribution changes at different decomposition stages. To fill this gap, we evaluated the relative importance of leaf litter polyphenols, decomposer communities and soil moisture for litter C and N loss at different stages throughout the decomposition process. Although both microbial and nematode communities regulated litter C and N loss in the early decomposition stages, soil moisture and legacy effects of initial differences in litter quality played a major role in the late stages of the process. Our results provide strong evidence for substantial shifts in how biotic and abiotic factors control litter C and N dynamics during decomposition. Taking into account such temporal dynamics will increase the predictive power of decomposition models that are currently limited by a single-pool approach applying control variables uniformly to the entire decay process.

Are there links between responses of soil microbes and ecosystem functioning to elevated CO2, N deposition and warming? A global perspective.

In recent years, there has been an increase in research to understand how global changes' impacts on soil biota translate into altered ecosystem functioning. However, results vary between global change effects, soil taxa, and ecosystem processes studied, and a synthesis of relationships is lacking. Therefore, here we initiate such a synthesis to assess whether the effect size of global change drivers (elevated CO2, N deposition, and warming) on soil microbial abundance is related with the effect size of these drivers on ecosystem functioning (plant biomass, soil C cycle, and soil N cycle) using meta-analysis and structural equation modeling. For N deposition and warming, the global change effect size on soil microbes was positively associated with the global change effect size on ecosystem functioning, and these relationships were consistent across taxa and ecosystem processes. However, for elevated CO2, such links were more taxon and ecosystem process specific. For example, fungal abundance responses to elevated CO2 were positively correlated with those of plant biomass but negatively with those of the N cycle. Our results go beyond previous assessments of the sensitivity of soil microbes and ecosystem processes to global change, and demonstrate the existence of general links between the responses of soil microbial abundance and ecosystem functioning. Further we identify critical areas for future research, specifically altered precipitation, soil fauna, soil community composition, and litter decomposition, that are need to better quantify the ecosystem consequences of global change impacts on soil biodiversity.

Functional traits determine plant co-occurrence more than environment or evolutionary relatedness in global drylands.

Plant-plant interactions are driven by environmental conditions, evolutionary relationships (ER) and the functional traits of the plants involved. However, studies addressing the relative importance of these drivers are rare, but crucial to improve our predictions of the effects of plant-plant interactions on plant communities and of how they respond to differing environmental conditions. To analyze the relative importance of -and interrelationships among- these factors as drivers of plant-plant interactions, we analyzed perennial plant co-occurrence at 106 dryland plant communities established across rainfall gradients in nine countries. We used structural equation modeling to disentangle the relationships between environmental conditions (aridity and soil fertility), functional traits extracted from the literature, and ER, and to assess their relative importance as drivers of the 929 pairwise plant-plant co-occurrence levels measured. Functional traits, specifically facilitated plants' height and nurse growth form, were of primary importance, and modulated the effect of the environment and ER on plant-plant interactions. Environmental conditions and ER were important mainly for those interactions involving woody and graminoid nurses, respectively. The relative importance of different plant-plant interaction drivers (ER, functional traits, and the environment) varied depending on the region considered, illustrating the difficulty of predicting the outcome of plant-plant interactions at broader spatial scales. In our global-scale study on drylands, plant-plant interactions were more strongly related to functional traits of the species involved than to the environmental variables considered. Thus, moving to a trait-based facilitation/competition approach help to predict that: 1) positive plant-plant interactions are more likely to occur for taller facilitated species in drylands, and 2) plant-plant interactions within woody-dominated ecosystems might be more sensitive to changing environmental conditions than those within grasslands. By providing insights on which species are likely to better perform beneath a given neighbour, our results will also help to succeed in restoration practices involving the use of nurse plants.

Meta-analysis reveals that vertebrates enhance plant litter decomposition at the global scale.

Evidence is mounting that vertebrate defaunation greatly impacts global biogeochemical cycling. Yet, there is no comprehensive assessment of the potential vertebrate influence over plant decomposition, despite litter decay being one of the largest global carbon fluxes. We therefore conducted a global meta-analysis to evaluate vertebrate effects on litter mass loss and associated element release across terrestrial and aquatic ecosystems. Here we show that vertebrates affected litter decomposition by various direct and indirect pathways, increasing litter mass loss by 6.7% on average, and up to 34.4% via physical breakdown. This positive vertebrate impact on litter mass loss was consistent across contrasting litter types (woody and non-woody), climatic regions (boreal, temperate and tropical), ecosystem types (aquatic and terrestrial) and vertebrate taxa, but disappeared when evaluating litter nitrogen and phosphorus release. Moreover, we found evidence of interactive effects between vertebrates and non-vertebrate decomposers on litter mass loss, and a larger influence of vertebrates at mid-to-late decomposition stages, contrasting with the invertebrate effect known to be strongest at early decomposition stage. Our synthesis demonstrates a global vertebrate control over litter mass loss, and further stresses the need to account for vertebrates when assessing the impacts of biodiversity loss on biogeochemical cycles.

Biotic homogenization, lower soil fungal diversity and fewer rare taxa in arable soils across Europe.

Soil fungi are a key constituent of global biodiversity and play a pivotal role in agroecosystems. How arable farming affects soil fungal biogeography and whether it has a disproportional impact on rare taxa is poorly understood. Here, we used the high-resolution PacBio Sequel targeting the entire ITS region to investigate the distribution of soil fungi in 217 sites across a 3000 km gradient in Europe. We found a consistently lower diversity of fungi in arable lands than grasslands, with geographic locations significantly impacting fungal community structures. Prevalent fungal groups became even more abundant, whereas rare groups became fewer or absent in arable lands, suggesting a biotic homogenization due to arable farming. The rare fungal groups were narrowly distributed and more common in grasslands. Our findings suggest that rare soil fungi are disproportionally affected by arable farming, and sustainable farming practices should protect rare taxa and the ecosystem services they support.