Negative effects of nitrogen override positive effects of phosphorus on grassland legumes worldwide.

Anthropogenic nutrient enrichment is driving global biodiversity decline and modifying ecosystem functions. Theory suggests that plant functional types that fix atmospheric nitrogen have a competitive advantage in nitrogen-poor soils, but lose this advantage with increasing nitrogen supply. By contrast, the addition of phosphorus, potassium, and other nutrients may benefit such species in low-nutrient environments by enhancing their nitrogen-fixing capacity. We present a global-scale experiment confirming these predictions for nitrogen-fixing legumes (Fabaceae) across 45 grasslands on six continents. Nitrogen addition reduced legume cover, richness, and biomass, particularly in nitrogen-poor soils, while cover of non-nitrogen-fixing plants increased. The addition of phosphorous, potassium, and other nutrients enhanced legume abundance, but did not mitigate the negative effects of nitrogen addition. Increasing nitrogen supply thus has the potential to decrease the diversity and abundance of grassland legumes worldwide regardless of the availability of other nutrients, with consequences for biodiversity, food webs, ecosystem resilience, and genetic improvement of protein-rich agricultural plant species.

Species loss due to nutrient addition increases with spatial scale in global grasslands.

The effects of altered nutrient supplies and herbivore density on species diversity vary with spatial scale, because coexistence mechanisms are scale dependent. This scale dependence may alter the shape of the species-area relationship (SAR), which can be described by changes in species richness (S) as a power function of the sample area (A): S = cAz , where c and z are constants. We analysed the effects of experimental manipulations of nutrient supply and herbivore density on species richness across a range of scales (0.01-75 m2 ) at 30 grasslands in 10 countries. We found that nutrient addition reduced the number of species that could co-occur locally, indicated by the SAR intercepts (log c), but did not affect the SAR slopes (z). As a result, proportional species loss due to nutrient enrichment was largely unchanged across sampling scales, whereas total species loss increased over threefold across our range of sampling scales.

Microbial processing of plant remains is co-limited by multiple nutrients in global grasslands.

Microbial processing of aggregate-unprotected organic matter inputs is key for soil fertility, long-term ecosystem carbon and nutrient sequestration and sustainable agriculture. We investigated the effects of adding multiple nutrients (nitrogen, phosphorus and potassium plus nine essential macro- and micro-nutrients) on decomposition and biochemical transformation of standard plant materials buried in 21 grasslands from four continents. Addition of multiple nutrients weakly but consistently increased decomposition and biochemical transformation of plant remains during the peak-season, concurrent with changes in microbial exoenzymatic activity. Higher mean annual precipitation and lower mean annual temperature were the main climatic drivers of higher decomposition rates, while biochemical transformation of plant remains was negatively related to temperature of the wettest quarter. Nutrients enhanced decomposition most at cool, high rainfall sites, indicating that in a warmer and drier future fertilized grassland soils will have an even more limited potential for microbial processing of plant remains.

Eutrophication weakens stabilizing effects of diversity in natural grasslands.

Studies of experimental grassland communities have demonstrated that plant diversity can stabilize productivity through species asynchrony, in which decreases in the biomass of some species are compensated for by increases in others. However, it remains unknown whether these findings are relevant to natural ecosystems, especially those for which species diversity is threatened by anthropogenic global change. Here we analyse diversity-stability relationships from 41 grasslands on five continents and examine how these relationships are affected by chronic fertilization, one of the strongest drivers of species loss globally. Unmanipulated communities with more species had greater species asynchrony, resulting in more stable biomass production, generalizing a result from biodiversity experiments to real-world grasslands. However, fertilization weakened the positive effect of diversity on stability. Contrary to expectations, this was not due to species loss after eutrophication but rather to an increase in the temporal variation of productivity in combination with a decrease in species asynchrony in diverse communities. Our results demonstrate separate and synergistic effects of diversity and eutrophication on stability, emphasizing the need to understand how drivers of global change interactively affect the reliable provisioning of ecosystem services in real-world systems.

Herbivores and nutrients control grassland plant diversity via light limitation.

Human alterations to nutrient cycles and herbivore communities are affecting global biodiversity dramatically. Ecological theory predicts these changes should be strongly counteractive: nutrient addition drives plant species loss through intensified competition for light, whereas herbivores prevent competitive exclusion by increasing ground-level light, particularly in productive systems. Here we use experimental data spanning a globally relevant range of conditions to test the hypothesis that herbaceous plant species losses caused by eutrophication may be offset by increased light availability due to herbivory. This experiment, replicated in 40 grasslands on 6 continents, demonstrates that nutrients and herbivores can serve as counteracting forces to control local plant diversity through light limitation, independent of site productivity, soil nitrogen, herbivore type and climate. Nutrient addition consistently reduced local diversity through light limitation, and herbivory rescued diversity at sites where it alleviated light limitation. Thus, species loss from anthropogenic eutrophication can be ameliorated in grasslands where herbivory increases ground-level light.

Nitrogen enrichment suppresses other environmental drivers and homogenizes salt marsh leaf microbiome.

Microbial community assembly is affected by a combination of forces that act simultaneously, but the mechanisms underpinning their relative influences remain elusive. This gap strongly limits our ability to predict human impacts on microbial communities and the processes they regulate. Here, we experimentally demonstrate that increased salinity stress, food web alteration and nutrient loading interact to drive outcomes in salt marsh fungal leaf communities. Both salinity stress and food web alterations drove communities to deterministically diverge, resulting in distinct fungal communities. Increased nutrient loads, nevertheless, partially suppressed the influence of other factors as determinants of fungal assembly. Using a null model approach, we found that increased nutrient loads enhanced the relative importance of stochastic over deterministic divergent processes; without increased nutrient loads, samples from different treatments showed a relatively (deterministic) divergent community assembly whereas increased nutrient loads drove the system to more stochastic assemblies, suppressing the effect of other treatments. These results demonstrate that common anthropogenic modifications can interact to control fungal community assembly. Furthermore, our results suggest that when the environmental conditions are spatially heterogeneous (as in our case, caused by specific combinations of experimental treatments), increased stochasticity caused by greater nutrient inputs can reduce the importance of deterministic filters that otherwise caused divergence, thus driving to microbial community homogenization.

Herbivory and eutrophication mediate grassland plant nutrient responses across a global climatic gradient.

Plant stoichiometry, the relative concentration of elements, is a key regulator of ecosystem functioning and is also being altered by human activities. In this paper we sought to understand the global drivers of plant stoichiometry and compare the relative contribution of climatic vs. anthropogenic effects. We addressed this goal by measuring plant elemental (C, N, P and K) responses to eutrophication and vertebrate herbivore exclusion at eighteen sites on six continents. Across sites, climate and atmospheric N deposition emerged as strong predictors of plot-level tissue nutrients, mediated by biomass and plant chemistry. Within sites, fertilization increased total plant nutrient pools, but results were contingent on soil fertility and the proportion of grass biomass relative to other functional types. Total plant nutrient pools diverged strongly in response to herbivore exclusion when fertilized; responses were largest in ungrazed plots at low rainfall, whereas herbivore grazing dampened the plant community nutrient responses to fertilization. Our study highlights (1) the importance of climate in determining plant nutrient concentrations mediated through effects on plant biomass, (2) that eutrophication affects grassland nutrient pools via both soil and atmospheric pathways and (3) that interactions among soils, herbivores and eutrophication drive plant nutrient responses at small scales, especially at water-limited sites.

Physical stress modifies top-down and bottom-up forcing on plant growth and reproduction in a coastal ecosystem.

Bottom-up and top-down effects act together to exert strong control over plant growth and reproduction, but how physical stress modifies those interactive forces remains unclear. Even though empirical evidence is scarce, theory predicts that the importance of both top-down- and bottom-up forces may decrease as physical stress increases. Here, we experimentally evaluate in the field the separate and interactive effect of salinity, nutrient availability, and crab herbivory on plant above- and belowground biomass, as well as on sexual and clonal reproduction in the salt marsh plant Spartina densiflora. Results show that the outcome of the interaction between nutrient availability and herbivory is highly context dependent, not only varying with the abiotic context (i.e., with or without increased salinity stress), but also with the dependent variable considered. Contrary to theoretical predictions, our results show that, consistently across different measured variables, salinity stress did not cancel bottom-up (i.e., nutrients) or top-down (i.e., consumers) control, but has additive effects. Our results support emerging theory by highlighting that, under many conditions, physical stress can act additively with, or even stimulate, consumer control, especially in cases where the physical stress is only experienced by basal levels of the trophic chain. Abiotic stress, as well as bottom-up and top-down factors, can affect salt marsh structure and function not only by affecting biomass production but also by having other indirect effects, such as changing patterns in plant biomass allocation and reproduction.

Herbivory affects salt marsh succession dynamics by suppressing the recovery of dominant species.

Disturbance can generate heterogeneous environments and profoundly influence plant diversity by creating patches at different successional stages. Herbivores, in turn, can govern plant succession dynamics by determining the rate of species replacement, ultimately affecting plant community structure. In a south-western Atlantic salt marsh, we experimentally evaluated the role of herbivory in the recovery following disturbance of the plant community and assessed whether herbivory affects the relative importance of sexual and clonal reproduction on these dynamics. Our results show that herbivory strongly affects salt marsh secondary succession by suppressing seedlings and limiting clonal colonization of the dominant marsh grass, allowing subordinate species to dominate disturbed patches. These results demonstrate that herbivores can have an important role in salt marsh community structure and function, and can be a key force during succession dynamics.

Harnessing ecological theory to enhance ecosystem restoration.

Ecosystem restoration can increase the health and resilience of nature and humanity. As a result, the international community is championing habitat restoration as a primary solution to address the dual climate and biodiversity crises. Yet most ecosystem restoration efforts to date have underperformed, failed, or been burdened by high costs that prevent upscaling. To become a primary, scalable conservation strategy, restoration efficiency and success must increase dramatically. Here, we outline how integrating ten foundational ecological theories that have not previously received much attention - from hierarchical facilitation to macroecology - into ecosystem restoration planning and management can markedly enhance restoration success. We propose a simple, systematic approach to determining which theories best align with restoration goals and are most likely to bolster their success. Armed with a century of advances in ecological theory, restoration practitioners will be better positioned to more cost-efficiently and effectively rebuild the world's ecosystems and support the resilience of our natural resources.

Predicting invasion in grassland ecosystems: is exotic dominance the real embarrassment of richness?

Invasions have increased the size of regional species pools, but are typically assumed to reduce native diversity. However, global-scale tests of this assumption have been elusive because of the focus on exotic species richness, rather than relative abundance. This is problematic because low invader richness can indicate invasion resistance by the native community or, alternatively, dominance by a single exotic species. Here, we used a globally replicated study to quantify relationships between exotic richness and abundance in grass-dominated ecosystems in 13 countries on six continents, ranging from salt marshes to alpine tundra. We tested effects of human land use, native community diversity, herbivore pressure, and nutrient limitation on exotic plant dominance. Despite its widespread use, exotic richness was a poor proxy for exotic dominance at low exotic richness, because sites that contained few exotic species ranged from relatively pristine (low exotic richness and cover) to almost completely exotic-dominated ones (low exotic richness but high exotic cover). Both exotic cover and richness were predicted by native plant diversity (native grass richness) and land use (distance to cultivation). Although climate was important for predicting both exotic cover and richness, climatic factors predicting cover (precipitation variability) differed from those predicting richness (maximum temperature and mean temperature in the wettest quarter). Herbivory and nutrient limitation did not predict exotic richness or cover. Exotic dominance was greatest in areas with low native grass richness at the site- or regional-scale. Although this could reflect native grass displacement, a lack of biotic resistance is a more likely explanation, given that grasses comprise the most aggressive invaders. These findings underscore the need to move beyond richness as a surrogate for the extent of invasion, because this metric confounds monodominance with invasion resistance. Monitoring species' relative abundance will more rapidly advance our understanding of invasions.

Variable responses to top-down and bottom-up control on multiple traits in the foundational plant, Spartina alterniflora.

While the effects of top-down and bottom-up forces on aboveground plant growth have been extensively examined, less is known about the relative impacts of these factors on other aspects of plant life history. In a fully-factorial, field experiment in a salt marsh in Virginia, USA, we manipulated grazing intensity (top-down) and nutrient availability (bottom-up) and measured the response in a suite of traits for smooth cordgrass (Spartina alterniflora). The data presented within this manuscript are unpublished, original data that were collected from the same experiment presented in Silliman and Zieman 2001. Three categories of traits and characteristics were measured: belowground characteristics, litter production, and reproduction, encompassing nine total responses. Of the nine response variables measured, eight were affected by treatments. Six response variables showed main effects of grazing and/ or fertilization, while three showed interactive effects. In general, fertilization led to increased cordgrass belowground biomass and reproduction, the former of which conflicts with predictions based on resource competition theory. Higher grazing intensity had negative impacts on both belowground biomass and reproduction. This result contrasts with past studies in this system that concluded grazer impacts are likely relegated to aboveground plant growth. In addition, grazers and fertilization interacted to alter litter production so that litter production disproportionately increased with fertilization when grazers were present. Our results revealed both predicted and unexpected effects of grazing and nutrient availability on understudied traits in a foundational plant and that these results were not fully predictable from understanding the impacts on aboveground biomass alone. Since these diverse traits link to diverse ecosystem functions, such as carbon burial, nutrient cycling, and ecosystem expansion, developing future studies to explore multiple trait responses and synthesizing the ecological knowledge on top-down and bottom-up forces with trait-based methodologies may provide a promising path forward in predicting variability in ecosystem function.

Herbivory limits success of vegetation restoration globally.

Restoring vegetation in degraded ecosystems is an increasingly common practice for promoting biodiversity and ecological function, but successful implementation is hampered by an incomplete understanding of the processes that limit restoration success. By synthesizing terrestrial and aquatic studies globally (2594 experimental tests from 610 articles), we reveal substantial herbivore control of vegetation under restoration. Herbivores at restoration sites reduced vegetation abundance more strongly (by 89%, on average) than those at relatively undegraded sites and suppressed, rather than fostered, plant diversity. These effects were particularly pronounced in regions with higher temperatures and lower precipitation. Excluding targeted herbivores temporarily or introducing their predators improved restoration by magnitudes similar to or greater than those achieved by managing plant competition or facilitation. Thus, managing herbivory is a promising strategy for enhancing vegetation restoration efforts.

Top ten priorities for global saltmarsh restoration, conservation and ecosystem service research.

Coastal saltmarshes provide globally important ecosystem services including 'blue carbon' sequestration, flood protection, pollutant remediation, habitat provision and cultural value. Large portions of marshes have been lost or fragmented as a result of land reclamation, embankment construction, and pollution. Sea level rise threatens marsh survival by blocking landward migration where coastlines have been developed. Research-informed saltmarsh conservation and restoration efforts are helping to prevent further loss, yet significant knowledge gaps remain. Using a mixed methods approach, this paper identifies ten research priorities through an online questionnaire and a residential workshop attended by an international, multi-disciplinary network of 35 saltmarsh experts spanning natural, physical and social sciences across research, policy, and practitioner sectors. Priorities have been grouped under four thematic areas of research: Saltmarsh Area Extent, Change and Restoration Potential (including past, present, global variation), Spatio-social contexts of Ecosystem Service delivery (e.g. influences of environmental context, climate change, and stakeholder groups on service provisioning), Patterns and Processes in saltmarsh functioning (global drivers of saltmarsh ecosystem structure/function) and Management and Policy Needs (how management varies contextually; challenges/opportunities for management). Although not intended to be exhaustive, the challenges, opportunities, and strategies for addressing each research priority examined here, providing a blueprint of the work that needs to be done to protect saltmarshes for future generations.

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.

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.

Temporal rarity is a better predictor of local extinction risk than spatial rarity.

Spatial rarity is often used to predict extinction risk, but rarity can also occur temporally. Perhaps more relevant in the context of global change is whether a species is core to a community (persistent) or transient (intermittently present), with transient species often susceptible to human activities that reduce niche space. Using 5-12 yr of data on 1,447 plant species from 49 grasslands on five continents, we show that local abundance and species persistence under ambient conditions are both effective predictors of local extinction risk following experimental exclusion of grazers or addition of nutrients; persistence was a more powerful predictor than local abundance. While perturbations increased the risk of exclusion for low persistence and abundance species, transient but abundant species were also highly likely to be excluded from a perturbed plot relative to ambient conditions. Moreover, low persistence and low abundance species that were not excluded from perturbed plots tended to have a modest increase in abundance following perturbance. Last, even core species with high abundances had large decreases in persistence and increased losses in perturbed plots, threatening the long-term stability of these grasslands. Our results demonstrate that expanding the concept of rarity to include temporal dynamics, in addition to local abundance, more effectively predicts extinction risk in response to environmental change than either rarity axis predicts alone.

Density affects mating mode and large male mating advantage in a fiddler crab.

Fiddler crabs show two different mating modes: either females search and crabs mate underground in male burrows, or males search and crabs mate on the surface near female burrows. We explored the relationship between crab density, body size, the searching behavior of both sexes, and the occurrence of both mating modes in the fiddler crab Uca uruguayensis. We found that crabs change their mating mode depending on their size and crab density. Crabs mated mostly on the surface at low densities, and underground at high densities. The proportion of wandering receptive females but not courting males accounted for the variation in mating modes. This suggests that whether crabs mate underground (or on the surface) is determined by the presence (or absence) of searching females. We found that the change in the mating mode affected the level of assortative mating; males mating underground were bigger than those mating on the surface, suggesting active female choice. Given that fiddler crabs experience multiple reproductive cycles, they are prone to showing behavioral plasticity in their mating strategy whenever the payoffs of using different mating modes differ between reproductive events. Our results suggest that the incorporation of different levels of environmental variability may be important in theoretical models aimed at improving our understanding of the evolution of alternative mating tactics and strategies.

Abiotic stress mediates top-down and bottom-up control in a Southwestern Atlantic salt marsh.

Increasing evidence has shown that nutrients and consumers interact to control primary productivity in natural systems, but how abiotic stress affects this interaction is unclear. Moreover, while herbivores can strongly impact zonation patterns in a variety of systems, there are few examples of this in salt marshes. We evaluated the effect of nutrients and herbivores on the productivity and distribution of the cordgrass Spartina densiflora along an intertidal stress gradient, in a Southwestern Atlantic salt marsh. We characterized abiotic stresses (salinity, ammonium concentration, and anoxia) and manipulated nutrients and the presence of the herbivorous crab Neohelice (Chasmagnathus) granulata, at different tidal heights with a factorial experiment. Abiotic stress increased at both ends of the tidal gradient. Salinity and anoxia were highest at the upper and lower edge of the intertidal, respectively. Nutrients and herbivory interacted to control cordgrass biomass, but their relative importance varied with environmental context. Herbivory increased at lower tidal heights to the point that cordgrass transplants onto bare mud substrate were entirely consumed unless crabs were excluded, while nutrients were most important where abiotic stress was reduced. Our results show how the impact of herbivores and nutrients on plant productivity can be dependent on environmental conditions and that the lower intertidal limits of marsh plants can be controlled by herbivory.

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.