Prairie restoration promotes the abundance and diversity of mutualistic arbuscular mycorrhizal fungi.

Predicting how biological communities assemble in restored ecosystems can assist in conservation efforts, but most research has focused on plants, with relatively little attention paid to soil microbial organisms that plants interact with. Arbuscular mycorrhizal (AM) fungi are an ecologically significant functional group of soil microbes that form mutualistic symbioses with plants and could therefore respond positively to plant community restoration. To evaluate the effects of plant community restoration on AM fungi, we compared AM fungal abundance, species richness, and community composition of five annually cultivated, conventionally managed agricultural fields with paired adjacent retired agricultural fields that had undergone prairie restoration 5-9 years prior to sampling. We hypothesized that restoration stimulates AM fungal abundance and species richness, particularly for disturbance-sensitive taxa, and that gains of new taxa would not displace AM fungal species present prior to restoration due to legacy effects. AM fungal abundance was quantified by measuring soil spore density and root colonization. AM fungal species richness and community composition were determined in soils and plant roots using DNA high-throughput sequencing. Soil spore density was 2.3 times higher in restored prairies compared to agricultural fields, but AM fungal root colonization did not differ between land use types. AM fungal species richness was 2.7 and 1.4 times higher in restored prairies versus agricultural fields for soil and roots, respectively. The abundance of Glomeraceae, a disturbance-tolerant family, decreased by 25% from agricultural to restored prairie soils but did not differ in plant roots. The abundance of Claroideoglomeraceae and Diversisporaceae, both disturbance-sensitive families, was 4.6 and 3.2 times higher in restored prairie versus agricultural soils, respectively. Species turnover was higher than expected relative to a null model, indicating that AM fungal species were gained by replacement. Our findings demonstrate that restoration can promote a relatively rapid increase in the abundance and diversity of soil microbial communities that had been degraded by decades of intensive land use, and community compositional change can be predicted by the disturbance tolerance of soil microbial taxonomic and functional groups.

Drivers of soil microbial and detritivore activity across global grasslands.

Covering approximately 40% of land surfaces, grasslands provide critical ecosystem services that rely on soil organisms. However, the global determinants of soil biodiversity and functioning remain underexplored. In this study, we investigate the drivers of soil microbial and detritivore activity in grasslands across a wide range of climatic conditions on five continents. We apply standardized treatments of nutrient addition and herbivore reduction, allowing us to disentangle the regional and local drivers of soil organism activity. We use structural equation modeling to assess the direct and indirect effects of local and regional drivers on soil biological activities. Microbial and detritivore activities are positively correlated across global grasslands. These correlations are shaped more by global climatic factors than by local treatments, with annual precipitation and soil water content explaining the majority of the variation. Nutrient addition tends to reduce microbial activity by enhancing plant growth, while herbivore reduction typically increases microbial and detritivore activity through increased soil moisture. Our findings emphasize soil moisture as a key driver of soil biological activity, highlighting the potential impacts of climate change, altered grazing pressure, and eutrophication on nutrient cycling and decomposition within grassland ecosystems.

Multidimensional responses of grassland stability to eutrophication.

Eutrophication usually impacts grassland biodiversity, community composition, and biomass production, but its impact on the stability of these community aspects is unclear. One challenge is that stability has many facets that can be tightly correlated (low dimensionality) or highly disparate (high dimensionality). Using standardized experiments in 55 grassland sites from a globally distributed experiment (NutNet), we quantify the effects of nutrient addition on five facets of stability (temporal invariability, resistance during dry and wet growing seasons, recovery after dry and wet growing seasons), measured on three community aspects (aboveground biomass, community composition, and species richness). Nutrient addition reduces the temporal invariability and resistance of species richness and community composition during dry and wet growing seasons, but does not affect those of biomass. Different stability measures are largely uncorrelated under both ambient and eutrophic conditions, indicating consistently high dimensionality. Harnessing the dimensionality of ecological stability provides insights for predicting grassland responses to global environmental change.

Globally consistent response of plant microbiome diversity across hosts and continents to soil nutrients and herbivores.

All multicellular organisms host a diverse microbiome composed of microbial pathogens, mutualists, and commensals, and changes in microbiome diversity or composition can alter host fitness and function. Nonetheless, we lack a general understanding of the drivers of microbiome diversity, in part because it is regulated by concurrent processes spanning scales from global to local. Global-scale environmental gradients can determine variation in microbiome diversity among sites, however an individual host's microbiome also may reflect its local micro-environment. We fill this knowledge gap by experimentally manipulating two potential mediators of plant microbiome diversity (soil nutrient supply and herbivore density) at 23 grassland sites spanning global-scale gradients in soil nutrients, climate, and plant biomass. Here we show that leaf-scale microbiome diversity in unmanipulated plots depended on the total microbiome diversity at each site, which was highest at sites with high soil nutrients and plant biomass. We also found that experimentally adding soil nutrients and excluding herbivores produced concordant results across sites, increasing microbiome diversity by increasing plant biomass, which created a shaded microclimate. This demonstration of consistent responses of microbiome diversity across a wide range of host species and environmental conditions suggests the possibility of a general, predictive understanding of microbiome diversity.

Environmental heterogeneity modulates the effect of plant diversity on the spatial variability of grassland biomass.

Plant productivity varies due to environmental heterogeneity, and theory suggests that plant diversity can reduce this variation. While there is strong evidence of diversity effects on temporal variability of productivity, whether this mechanism extends to variability across space remains elusive. Here we determine the relationship between plant diversity and spatial variability of productivity in 83 grasslands, and quantify the effect of experimentally increased spatial heterogeneity in environmental conditions on this relationship. We found that communities with higher plant species richness (alpha and gamma diversity) have lower spatial variability of productivity as reduced abundance of some species can be compensated for by increased abundance of other species. In contrast, high species dissimilarity among local communities (beta diversity) is positively associated with spatial variability of productivity, suggesting that changes in species composition can scale up to affect productivity. Experimentally increased spatial environmental heterogeneity weakens the effect of plant alpha and gamma diversity, and reveals that beta diversity can simultaneously decrease and increase spatial variability of productivity. Our findings unveil the generality of the diversity-stability theory across space, and suggest that reduced local diversity and biotic homogenization can affect the spatial reliability of key ecosystem functions.

Impacts of soil, climate, and phenology on retention of dissolved agricultural nutrients by permanent-cover buffers.

Nutrient losses from farms affects environmental and human health, but retention by riparian buffers can vary by nutrient identity, flow path, soil texture, seasonality, and buffer width. On conventional farms with corn, we test the relationships between levels of dissolved nitrogen (N) and phosphorus (P) in downslope surface-water, and flow paths relating to porewater in soils (to 40 cm deep), groundwater of the saturated zone (to 2.5 m deep), soil nutrient pools, and changes in plant biomass and tissue quality by season. We found that the major drivers of surface-water nutrients were multi-factor and nutrient-specific, variously relating to soil, climate, vegetation uptake, and tiling on clay soils. N retention was best explained by soil type, with 10 times more surface-water N in the sand versus clay setting, despite identical fertilization rates on corn. P retention was best explained by precipitation and time of year. Vegetation uptake was strongest for shallow-soil porewater, and was greatest in buffers where root biomass was 20 times greater by weight. We were unable to detect any impact of vegetative uptake on groundwater nutrients. Overall, peak nutrient inputs to surface-water were in early summer, fall, and winter - all times when plant uptake is low. Buffers appear to be a necessary component of nutrient capture on farms, but insufficient unless partnered with measures that reduce nutrient flows at times when plants are inactive.

Evolutionary history of grazing and resources determine herbivore exclusion effects on plant diversity.

Ecological models predict that the effects of mammalian herbivore exclusion on plant diversity depend on resource availability and plant exposure to ungulate grazing over evolutionary time. Using an experiment replicated in 57 grasslands on six continents, with contrasting evolutionary history of grazing, we tested how resources (mean annual precipitation and soil nutrients) determine herbivore exclusion effects on plant diversity, richness and evenness. Here we show that at sites with a long history of ungulate grazing, herbivore exclusion reduced plant diversity by reducing both richness and evenness and the responses of richness and diversity to herbivore exclusion decreased with mean annual precipitation. At sites with a short history of grazing, the effects of herbivore exclusion were not related to precipitation but differed for native and exotic plant richness. Thus, plant species' evolutionary history of grazing continues to shape the response of the world's grasslands to changing mammalian herbivory.

Global Grassland Diazotrophic Communities Are Structured by Combined Abiotic, Biotic, and Spatial Distance Factors but Resilient to Fertilization.

Grassland ecosystems cover around 37% of the ice-free land surface on Earth and have critical socioeconomic importance globally. As in many terrestrial ecosystems, biological dinitrogen (N2) fixation represents an essential natural source of nitrogen (N). The ability to fix atmospheric N2 is limited to diazotrophs, a diverse guild of bacteria and archaea. To elucidate the abiotic (climatic, edaphic), biotic (vegetation), and spatial factors that govern diazotrophic community composition in global grassland soils, amplicon sequencing of the dinitrogenase reductase gene-nifH-was performed on samples from a replicated standardized nutrient [N, phosphorus (P)] addition experiment in 23 grassland sites spanning four continents. Sites harbored distinct and diverse diazotrophic communities, with most of reads assigned to diazotrophic taxa within the Alphaproteobacteria (e.g., Rhizobiales), Cyanobacteria (e.g., Nostocales), and Deltaproteobacteria (e.g., Desulforomonadales) groups. Likely because of the wide range of climatic and edaphic conditions and spatial distance among sampling sites, only a few of the taxa were present at all sites. The best model describing the variation among soil diazotrophic communities at the OTU level combined climate seasonality (temperature in the wettest quarter and precipitation in the warmest quarter) with edaphic (C:N ratio, soil texture) and vegetation factors (various perennial plant covers). Additionally, spatial variables (geographic distance) correlated with diazotrophic community variation, suggesting an interplay of environmental variables and spatial distance. The diazotrophic communities appeared to be resilient to elevated nutrient levels, as 2-4 years of chronic N and P additions had little effect on the community composition. However, it remains to be seen, whether changes in the community composition occur after exposure to long-term, chronic fertilization regimes.

Nutrients and herbivores impact grassland stability across spatial scales through different pathways.

Nutrients and herbivores are well-known drivers of grassland diversity and stability in local communities. However, whether they interact to impact the stability of aboveground biomass and whether these effects depend on spatial scales remain unknown. It is also unclear whether nutrients and herbivores impact stability via different facets of plant diversity including species richness, evenness, and changes in community composition through time and space. We used a replicated experiment adding nutrients and excluding herbivores for 5 years in 34 global grasslands to explore these questions. We found that both nutrient addition and herbivore exclusion alone reduced stability at the larger spatial scale (aggregated local communities; gamma stability), but through different pathways. Nutrient addition reduced gamma stability primarily by increasing changes in local community composition over time, which was mainly driven by species replacement. Herbivore exclusion reduced gamma stability primarily by decreasing asynchronous dynamics among local communities (spatial asynchrony). Their interaction weakly increased gamma stability by increasing spatial asynchrony. Our findings indicate that disentangling the processes operating at different spatial scales may improve conservation and management aiming at maintaining the ability of ecosystems to reliably provide functions and services for humanity.

Nutrient identity modifies the destabilising effects of eutrophication in grasslands.

Nutrient enrichment can simultaneously increase and destabilise plant biomass production, with co-limitation by multiple nutrients potentially intensifying these effects. Here, we test how factorial additions of nitrogen (N), phosphorus (P) and potassium with essential nutrients (K+) affect the stability (mean/standard deviation) of aboveground biomass in 34 grasslands over 7 years. Destabilisation with fertilisation was prevalent but was driven by single nutrients, not synergistic nutrient interactions. On average, N-based treatments increased mean biomass production by 21-51% but increased its standard deviation by 40-68% and so consistently reduced stability. Adding P increased interannual variability and reduced stability without altering mean biomass, while K+ had no general effects. Declines in stability were largest in the most nutrient-limited grasslands, or where nutrients reduced species richness or intensified species synchrony. We show that nutrients can differentially impact the stability of biomass production, with N and P in particular disproportionately increasing its interannual variability.

Prospects for soil carbon storage on recently retired marginal farmland.

Soil organic carbon (SOC) is strongly affected by farm cropping, which covers >10% of the earth's surface. Land retirement of marginal fields, now a global initiative, can increase SOC storage but reported accumulation rates are variable. Here, we quantify SOC in crop fields and retired marginal land in an intensely farmed 10,000 km 2 region of central North America, testing nutrients, soil texture and management as drivers of SOC storage. Overwhelmingly, SOC was associated with farm management with among-farm differences varying >fourfold (17.4-81 t ha -1) in the top 15 cm. Total farm SOC averaged 502.2 t farm -1 but again ranged widely (216-1611 t farm -1). Farm-specific SOC was often, but not always, higher on farms with N-rich silt-clay soils, and lower on sandy soils with higher P relating to former tobacco production. In contrast, within-farm SOC between crop fields and retired land did not significantly differ with time. Low SOC on retired lands was associated with persistently high soil N and P and elevated microbial respiration. Retired soils did possess substantially larger pools of lignin-rich root biomass to depths of 60 cm, which may signify eventual SOC accumulation possibly as nutrient legacies diminish. Our work shows that management legacy, interacting with soil texture and nutrients, predicts SOC more than short-term retirement. Indeed, crop fields averaged 67% of farm SOC because they represented up to 94% of total farm area - SOC retention on cropland remains a management priority, above and beyond gains with retirement. Interestingly, the largest per-volume SOC levels were in remnant forest that contained 25% of farm SOC despite only averaging 11% of farm area. Maintaining SOC stocks in farm landscapes may be more quickly attained by protecting remnant forest, with retired lands needing time to re-build SOC stocks.

Soil properties as key predictors of global grassland production: Have we overlooked micronutrients?

Fertilisation experiments have demonstrated that nutrient availability is a key determinant of biomass production and carbon sequestration in grasslands. However, the influence of nutrients in explaining spatial variation in grassland biomass production has rarely been assessed. Using a global dataset comprising 72 sites on six continents, we investigated which of 16 soil factors that shape nutrient availability associate most strongly with variation in grassland aboveground biomass. Climate and N deposition were also considered. Based on theory-driven structural equation modelling, we found that soil micronutrients (particularly Zn and Fe) were important predictors of biomass and, together with soil physicochemical properties and C:N, they explained more unique variation (32%) than climate and N deposition (24%). However, the association between micronutrients and biomass was absent in grasslands limited by NP. These results highlight soil properties as key predictors of global grassland biomass production and point to serial co-limitation by NP and micronutrients.

Comparison of the distribution and phenology of Arctic Mountain plants between the early 20th and 21st centuries.

Arctic plants are adapted to climatic variability, but their long-term responses to warming remain unclear. Responses may occur by range shifts, phenological adjustments in growth and reproduction, or both. Here, we compare distribution and phenology of 83 arctic and boreal mountain species, sampled identically in the early 20th (1917-1919) and 21st centuries (2017-2018) from a region of northern Sweden that has warmed significantly. We test two compensatory hypotheses to high-latitude warming-upward shifts in distribution, and earlier or extended growth and reproduction. For distribution, we show dramatic upward migration by 69% of species, averaging 6.1 m per decade, especially boreal woodland taxa whose upward expansion has reduced arctic montane habitat by 30%. Twenty percent of summit species showed distributional shifts but downward, especially moisture-associated snowbed flora. For phenology, we detected wide inter-annual variability in the onset of leafing and flowering in both eras. However, there was no detectable change in growing-season length, relating to two mechanisms. First, plot-level snow melt data starting in 1917 demonstrated that melt date, rather than vernal temperatures, better predicts plant emergence, with snow melt influenced by warmer years having greater snowfall-warmer springs did not always result in earlier emergence because snowbeds can persist longer. Second, the onset of reproductive senescence between eras was similar, even when plant emergence was earlier by a month, possibly due to intensified summer heat stress or hard-wired 'canalization' where senescence occurs regardless of summer temperature. Migrations in this system have possibly buffered arctic species against displacement by boreal expansion and warming, but ongoing temperature increases, woody plant invasion, and a potential lack of flexibility in timing of senescence may foreshadow challenges.

Soil nutrients increase long-term soil carbon gains threefold on retired farmland.

Abandoned agricultural lands often accumulate soil carbon (C) following depletion of soil C by cultivation. The potential for this recovery to provide significant C storage benefits depends on the rate of soil C accumulation, which, in turn, may depend on nutrient supply rates. We tracked soil C for almost four decades following intensive agricultural soil disturbance along an experimentally imposed gradient in nitrogen (N) added annually in combination with other macro- and micro-nutrients. Soil %C accumulated over the course of the study in unfertilized control plots leading to a gain of 6.1 Mg C ha-1 in the top 20 cm of soil. Nutrient addition increased soil %C accumulation leading to a gain of 17.8 Mg C ha-1 in fertilized plots, nearly a threefold increase over the control plots. These results demonstrate that substantial increases in soil C in successional grasslands following agricultural abandonment occur over decadal timescales, and that C gain is increased by high supply rates of soil nutrients. In addition, soil %C continued to increase for decades under elevated nutrient supply, suggesting that short-term nutrient addition experiments underestimate the effects of soil nutrients on soil C accumulation.

Globally, plant-soil feedbacks are weak predictors of plant abundance.

Plant-soil feedbacks (PSFs) have been shown to strongly affect plant performance under controlled conditions, and PSFs are thought to have far reaching consequences for plant population dynamics and the structuring of plant communities. However, thus far the relationship between PSF and plant species abundance in the field is not consistent. Here, we synthesize PSF experiments from tropical forests to semiarid grasslands, and test for a positive relationship between plant abundance in the field and PSFs estimated from controlled bioassays. We meta-analyzed results from 22 PSF experiments and found an overall positive correlation (0.12 ≤  r ¯  ≤ 0.32) between plant abundance in the field and PSFs across plant functional types (herbaceous and woody plants) but also variation by plant functional type. Thus, our analysis provides quantitative support that plant abundance has a general albeit weak positive relationship with PSFs across ecosystems. Overall, our results suggest that harmful soil biota tend to accumulate around and disproportionately impact species that are rare. However, data for the herbaceous species, which are most common in the literature, had no significant abundance-PSFs relationship. Therefore, we conclude that further work is needed within and across biomes, succession stages and plant types, both under controlled and field conditions, while separating PSF effects from other drivers (e.g., herbivory, competition, disturbance) of plant abundance to tease apart the role of soil biota in causing patterns of plant rarity versus commonness.

Landscape modification and nutrient-driven instability at a distance.

Almost 50 years ago, Michael Rosenzweig pointed out that nutrient addition can destabilise food webs, leading to loss of species and reduced ecosystem function through the paradox of enrichment. Around the same time, David Tilman demonstrated that increased nutrient loading would also be expected to cause competitive exclusion leading to deleterious changes in food web diversity. While both concepts have greatly illuminated general diversity-stability theory, we currently lack a coherent framework to predict how nutrients influence food web stability across a landscape. This is a vitally important gap in our understanding, given mounting evidence of serious ecological disruption arising from anthropogenic displacement of resources and organisms. Here, we combine contemporary theory on food webs and meta-ecosystems to show that nutrient additions are indeed expected to drive loss in stability and function in human-impacted regions. Our models suggest that destabilisation is more likely to be caused by the complete loss of an equilibrium due to edible plant species being competitively excluded. In highly modified landscapes, spatial nutrient transport theory suggests that such instabilities can be amplified over vast distances from the sites of nutrient addition. Consistent with this theoretical synthesis, the empirical frequency of these distant propagating ecosystem imbalances appears to be growing. This synthesis of theory and empirical data suggests that human modification of the Earth is strongly connecting distantly separated ecosystems, causing rapid, expansive and costly nutrient-driven instabilities over vast areas of the planet. Similar to existing food web theory, the corollary to this spatial nutrient theory is that slowing down spatial nutrient pathways can be a potent means of stabilising degraded ecosystems.

General destabilizing effects of eutrophication on grassland productivity at multiple spatial scales.

Eutrophication is a widespread environmental change that usually reduces the stabilizing effect of plant diversity on productivity in local communities. Whether this effect is scale dependent remains to be elucidated. Here, we determine the relationship between plant diversity and temporal stability of productivity for 243 plant communities from 42 grasslands across the globe and quantify the effect of chronic fertilization on these relationships. Unfertilized local communities with more plant species exhibit greater asynchronous dynamics among species in response to natural environmental fluctuations, resulting in greater local stability (alpha stability). Moreover, neighborhood communities that have greater spatial variation in plant species composition within sites (higher beta diversity) have greater spatial asynchrony of productivity among communities, resulting in greater stability at the larger scale (gamma stability). Importantly, fertilization consistently weakens the contribution of plant diversity to both of these stabilizing mechanisms, thus diminishing the positive effect of biodiversity on stability at differing spatial scales. Our findings suggest that preserving grassland functional stability requires conservation of plant diversity within and among ecological communities.

Global impacts of fertilization and herbivore removal on soil net nitrogen mineralization are modulated by local climate and soil properties.

Soil nitrogen (N) availability is critical for grassland functioning. However, human activities have increased the supply of biologically limiting nutrients, and changed the density and identity of mammalian herbivores. These anthropogenic changes may alter net soil N mineralization (soil net Nmin ), that is, the net balance between N mineralization and immobilization, which could severely impact grassland structure and functioning. Yet, to date, little is known about how fertilization and herbivore removal individually, or jointly, affect soil net Nmin across a wide range of grasslands that vary in soil and climatic properties. Here we collected data from 22 grasslands on five continents, all part of a globally replicated experiment, to assess how fertilization and herbivore removal affected potential (laboratory-based) and realized (field-based) soil net Nmin . Herbivore removal in the absence of fertilization did not alter potential and realized soil net Nmin . However, fertilization alone and in combination with herbivore removal consistently increased potential soil net Nmin. Realized soil net Nmin , in contrast, significantly decreased in fertilized plots where herbivores were removed. Treatment effects on potential and realized soil net Nmin were contingent on site-specific soil and climatic properties. Fertilization effects on potential soil net Nmin were larger at sites with higher mean annual precipitation (MAP) and temperature of the wettest quarter (T.q.wet). Reciprocally, realized soil net Nmin declined most strongly with fertilization and herbivore removal at sites with lower MAP and higher T.q.wet. In summary, our findings show that anthropogenic nutrient enrichment, herbivore exclusion and alterations in future climatic conditions can negatively impact soil net Nmin across global grasslands under realistic field conditions. This is an important context-dependent knowledge for grassland management worldwide.

Nutrient availability controls the impact of mammalian herbivores on soil carbon and nitrogen pools in grasslands.

Grasslands are subject to considerable alteration due to human activities globally, including widespread changes in populations and composition of large mammalian herbivores and elevated supply of nutrients. Grassland soils remain important reservoirs of carbon (C) and nitrogen (N). Herbivores may affect both C and N pools and these changes likely interact with increases in soil nutrient availability. Given the scale of grassland soil fluxes, such changes can have striking consequences for atmospheric C concentrations and the climate. Here, we use the Nutrient Network experiment to examine the responses of soil C and N pools to mammalian herbivore exclusion across 22 grasslands, under ambient and elevated nutrient availabilities (fertilized with NPK + micronutrients). We show that the impact of herbivore exclusion on soil C and N pools depends on fertilization. Under ambient nutrient conditions, we observed no effect of herbivore exclusion, but under elevated nutrient supply, pools are smaller upon herbivore exclusion. The highest mean soil C and N pools were found in grazed and fertilized plots. The decrease in soil C and N upon herbivore exclusion in combination with fertilization correlated with a decrease in aboveground plant biomass and microbial activity, indicating a reduced storage of organic matter and microbial residues as soil C and N. The response of soil C and N pools to herbivore exclusion was contingent on temperature - herbivores likely cause losses of C and N in colder sites and increases in warmer sites. Additionally, grasslands that contain mammalian herbivores have the potential to sequester more N under increased temperature variability and nutrient enrichment than ungrazed grasslands. Our study highlights the importance of conserving mammalian herbivore populations in grasslands worldwide. We need to incorporate local-scale herbivory, and its interaction with nutrient enrichment and climate, within global-scale models to better predict land-atmosphere interactions under future climate change.