Addition of multiple limiting resources reduces grassland diversity.

Niche dimensionality provides a general theoretical explanation for biodiversity-more niches, defined by more limiting factors, allow for more ways that species can coexist. Because plant species compete for the same set of limiting resources, theory predicts that addition of a limiting resource eliminates potential trade-offs, reducing the number of species that can coexist. Multiple nutrient limitation of plant production is common and therefore fertilization may reduce diversity by reducing the number or dimensionality of belowground limiting factors. At the same time, nutrient addition, by increasing biomass, should ultimately shift competition from belowground nutrients towards a one-dimensional competitive trade-off for light. Here we show that plant species diversity decreased when a greater number of limiting nutrients were added across 45 grassland sites from a multi-continent experimental network. The number of added nutrients predicted diversity loss, even after controlling for effects of plant biomass, and even where biomass production was not nutrient-limited. We found that elevated resource supply reduced niche dimensionality and diversity and increased both productivity and compositional turnover. Our results point to the importance of understanding dimensionality in ecological systems that are undergoing diversity loss in response to multiple global change factors.

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.

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.

Spatial heterogeneity in species composition constrains plant community responses to herbivory and fertilisation.

Environmental change can result in substantial shifts in community composition. The associated immigration and extinction events are likely constrained by the spatial distribution of species. Still, studies on environmental change typically quantify biotic responses at single spatial (time series within a single plot) or temporal (spatial beta diversity at single time points) scales, ignoring their potential interdependence. Here, we use data from a global network of grassland experiments to determine how turnover responses to two major forms of environmental change - fertilisation and herbivore loss - are affected by species pool size and spatial compositional heterogeneity. Fertilisation led to higher rates of local extinction, whereas turnover in herbivore exclusion plots was driven by species replacement. Overall, sites with more spatially heterogeneous composition showed significantly higher rates of annual turnover, independent of species pool size and treatment. Taking into account spatial biodiversity aspects will therefore improve our understanding of consequences of global and anthropogenic change on community dynamics.

Plant diversity predicts beta but not alpha diversity of soil microbes across grasslands worldwide.

Aboveground-belowground interactions exert critical controls on the composition and function of terrestrial ecosystems, yet the fundamental relationships between plant diversity and soil microbial diversity remain elusive. Theory predicts predominantly positive associations but tests within single sites have shown variable relationships, and associations between plant and microbial diversity across broad spatial scales remain largely unexplored. We compared the diversity of plant, bacterial, archaeal and fungal communities in one hundred and forty-five 1 m(2) plots across 25 temperate grassland sites from four continents. Across sites, the plant alpha diversity patterns were poorly related to those observed for any soil microbial group. However, plant beta diversity (compositional dissimilarity between sites) was significantly correlated with the beta diversity of bacterial and fungal communities, even after controlling for environmental factors. Thus, across a global range of temperate grasslands, plant diversity can predict patterns in the composition of soil microbial communities, but not patterns in alpha diversity.

Biotic mechanisms of community stability shift along a precipitation gradient.

Understanding how biotic mechanisms confer stability in variable environments is a fundamental quest in ecology, and one that is becoming increasingly urgent with global change. Several mechanisms, notably a portfolio effect associated with species richness, compensatory dynamics generated by negative species covariance and selection for stable dominant species populations can increase the stability of the overall community. While the importance of these mechanisms is debated, few studies have contrasted their importance in an environmental context. We analyzed nine long-term data sets of grassland species composition to investigate how two key environmental factors, precipitation amount and variability, may directly influence community stability and how they may indirectly influence stability via biotic mechanisms. We found that the importance of stability mechanisms varied along the environmental gradient: strong negative species covariance occurred in sites characterized by high precipitation variability, whereas portfolio effects increased in sites with high mean annual precipitation. Instead of questioning whether compensatory dynamics are important in nature, our findings suggest that debate should widen to include several stability mechanisms and how these mechanisms vary in importance across environmental gradients.

Sensitivity of grassland plant community composition to spatial vs. temporal variation in precipitation.

Climate gradients shape spatial variation in the richness and composition of plant communities. Given future predicted changes in climate means and variability, and likely regional variation in the magnitudes of these changes, it is important to determine how temporal variation in climate influences temporal variation in plant community structure. Here, we evaluated how species richness, turnover, and composition of grassland plant communities responded to interannual variation in precipitation by synthesizing long-term data from grasslands across the United States. We found that mean annual precipitation,(MAP) was a positive predictor of species richness across sites, but a positive temporal relationship between annual precipitation and richness was only evident within two sites with low MAP. We also found higher average rates of species turnover in dry sites that in turn had a high proportion of annual species, although interannual rates of species turnover were surprisingly high across all locations. Annual species were less abundant than perennial species at nearly all sites, and our analysis showed that the probability of a species being lost or gained from one year to the next increased with decreasing species abundance. Bray-Curtis dissimilarity from one year to the next, a measure of species composition change that is influenced mainly by abundant species, was insensitive to precipitation at all sites. These results suggest that the richness and turnover patterns we observed were driven primarily by rare species, which comprise the majority of the local species pools at these grassland sites. These findings are consistent with the idea that short-lived and less abundant species are more sensitive to interannual climate variability than longer-lived and more abundant species. We conclude that, among grassland ecosystems, xeric grasslands are likely to exhibit the greatest responsiveness of community composition (richness and turnover) to predicted future increases in interannual precipitation variability. Over the long-term, species composition may shift to reflect spatial patterns of mean precipitation; however, perennial-dominated systems will be buffered against rising interannual variation, while systems that have a large number of rare, annual species will show the greatest temporal variability in species composition in response to rising interannual variability in precipitation.

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.

Temperature-dependent shifts in phenology contribute to the success of exotic species with climate change.

PREMISE OF THE STUDY: The study of how phenology may contribute to the assembly of plant communities has a long history in ecology. Climate change has brought renewed interest in this area, with many studies examining how phenology may contribute to the success of exotic species. In particular, there is increasing evidence that exotic species occupy unique phenological niches and track climate change more closely than native species. METHODS: Here, we use long-term records of species' first flowering dates from fi ve northern hemisphere temperate sites (Chinnor, UK and in the United States, Concord, Massachusetts; Fargo, North Dakota; Konza Prairie, Kansas; and Washington,D.C.) to examine whether invaders have distinct phenologies. Using a broad phylogenetic framework, we tested for differences between exotic and native species in mean annual flowering time, phenological changes in response to temperature and precipitation,and longer-term shifts in first flowering dates during recent pronounced climate change ("flowering time shifts"). KEY RESULTS: Across North American sites, exotic species have shifted flowering with climate change while native species, on average, have not. In the three mesic systems, exotic species exhibited higher tracking of interannual variation in temperature,such that flowering advances more with warming, than native species. Across the two grassland systems, however, exotic species differed from native species primarily in responses to precipitation and soil moisture, not temperature. CONCLUSIONS: Our findings provide cross-site support for the role of phenology and climate change in explaining species' invasions.Further, they support recent evidence that exotic species may be important drivers of extended growing seasons observed with climate change in North America.

When the neighborhood matters: contextual selection on seedling traits in native and non-native California grasses.

Plants interact extensively with their neighbors, but the evolutionary consequences of variation in neighbor identity are not well understood. Seedling traits are likely to experience selection that depends on the identity of neighbors because they influence competitive outcomes. To explore this, we evaluated selection on seed mass and emergence time in two California grasses, the native perennial Stipa pulchra, and the non-native annual Bromus diandrus, in the field with six other native and non-native neighbor grasses in single- and mixed-species treatments. We also quantified characteristics of each neighbor treatment to further investigate factors influencing their effects on fitness and phenotypic selection. Selection favored larger seeds in both focal species and this was largely independent of neighbor identity. Selection generally favored earlier emergence in both focal species, but neighbor identity influenced the strength and direction of selection on emergence time in S. pulchra, but not B. diandrus. Greater light interception, higher soil moisture, and greater productivity of neighbors were associated with more intense selection for earlier emergence and larger seeds. Our findings suggest that changes in plant community composition can alter patterns of selection in seedling traits, and that these effects can be associated with measurable characteristics of the community.

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.

Phenological tracking enables positive species responses to climate change.

Earlier spring phenology observed in many plant species in recent decades provides compelling evidence that species are already responding to the rising global temperatures associated with anthropogenic climate change. There is great variability among species, however, in their phenological sensitivity to temperature. Species that do not phenologically "track" climate change may be at a disadvantage if their growth becomes limited by missed interactions with mutualists, or a shorter growing season relative to earlier-active competitors. Here, we set out to test the hypothesis that phenological sensitivity could be used to predict species performance in a warming climate, by synthesizing results across terrestrial warming experiments. We assembled data for 57 species across 24 studies where flowering or vegetative phenology was matched with a measure of species performance. Performance metrics included biomass, percent cover, number of flowers, or individual growth. We found that species that advanced their phenology with warming also increased their performance, whereas those that did not advance tended to decline in performance with warming. This indicates that species that cannot phenologically "track" climate may be at increased risk with future climate change, and it suggests that phenological monitoring may provide an important tool for setting future conservation priorities.

Incorporating clonal growth form clarifies the role of plant height in response to nitrogen addition.

Nutrient addition to grasslands consistently causes species richness declines and productivity increases. Competition, particularly for light, is often assumed to produce this result. Using a long-term dataset from North American herbaceous plant communities, we tested whether height and clonal growth form together predict responses to fertilization because neither trait alone predicted species loss in a previous analysis. Species with a tall-runner growth form commonly increased in relative abundance in response to added nitrogen, while short species and those with a tall-clumped clonal growth form often decreased. The ability to increase in size via vegetative spread across space, while simultaneously occupying the canopy, conferred competitive advantage, although typically only the abundance of a single species within each height-clonal growth form significantly responded to fertilization in each experiment. Classifying species on the basis of two traits (height and clonal growth form) increases our ability to predict species responses to fertilization compared to either trait alone in predominantly herbaceous plant communities. Electronic supplementary material The online version of this article (doi:10.1007/s00442-012-2264-5) contains supplementary material, which is available to authorized users.

Nutrient co-limitation of primary producer communities.

Synergistic interactions between multiple limiting resources are common, highlighting the importance of co-limitation as a constraint on primary production. Our concept of resource limitation has shifted over the past two decades from an earlier paradigm of single-resource limitation towards concepts of co-limitation by multiple resources, which are predicted by various theories. Herein, we summarise multiple-resource limitation responses in plant communities using a dataset of 641 studies that applied factorial addition of nitrogen (N) and phosphorus (P) in freshwater, marine and terrestrial systems. We found that more than half of the studies displayed some type of synergistic response to N and P addition. We found support for strict definitions of co-limitation in 28% of the studies: i.e. community biomass responded to only combined N and P addition, or to both N and P when added separately. Our results highlight the importance of interactions between N and P in regulating primary producer community biomass and point to the need for future studies that address the multiple mechanisms that could lead to different types of co-limitation.

Abundance of introduced species at home predicts abundance away in herbaceous communities.

Many ecosystems worldwide are dominated by introduced plant species, leading to loss of biodiversity and ecosystem function. A common but rarely tested assumption is that these plants are more abundant in introduced vs. native communities, because ecological or evolutionary-based shifts in populations underlie invasion success. Here, data for 26 herbaceous species at 39 sites, within eight countries, revealed that species abundances were similar at native (home) and introduced (away) sites - grass species were generally abundant home and away, while forbs were low in abundance, but more abundant at home. Sites with six or more of these species had similar community abundance hierarchies, suggesting that suites of introduced species are assembling similarly on different continents. Overall, we found that substantial changes to populations are not necessarily a pre-condition for invasion success and that increases in species abundance are unusual. Instead, abundance at home predicts abundance away, a potentially useful additional criterion for biosecurity programmes.

Vertebrate herbivory weakens directional selection for earlier emergence in competition.

The timing of seedling emergence is strongly linked with fitness because it determines the biotic and abiotic environment experienced by plants in this vulnerable life stage. Experiments and observations consistently find that earlier-emerging plants have a competitive advantage over those emerging later. However, substantial genetic and phenotypic variation in emergence timing is harbored within and among plant populations, making it important to characterize the selective agents-including biotic interactions-that contribute to this variation. In seasonal herbaceous communities, we hypothesized that consumption of early-emerging individuals by vertebrates could weaken the strength of directional selection for earlier emergence in competitive environments. To investigate this, we carried out phenotypic selection analyses on emergence timing in two California grass species, the native Stipa pulchra and non-native Bromus diandrus, growing in intraspecific competitive neighborhoods with and without vertebrate herbivore exclusion. Vertebrate herbivores consistently weakened directional selection for earlier emergence. Our results demonstrate that vertebrate herbivores play an underappreciated selective role on phenology in plant populations, with implications for contemporary evolution, such as the potential of species to adapt to global environmental changes.

Trade-off drives Pareto optimality of within- and among-year emergence timing in response to increasing aridity.

Adaptation to current and future climates can be constrained by trade-offs between fitness-related traits. Early seedling emergence often enhances plant fitness in seasonal environments, but if earlier emergence in response to seasonal cues is genetically correlated with lower potential to spread emergence among years (i.e., bet-hedging), then this functional trade-off could constrain adaptive evolution. Consequently, selection favoring both earlier within-year emergence and greater spread of emergence among years-as is expected in more arid environments-may constrain adaptive responses to trait value combinations at which a performance gain in either function (i.e., evolving earlier within- or greater among-year emergence) generates a performance loss in the other. All such trait value combinations that cannot be improved for both functions simultaneously are described as Pareto optimal and together constitute the Pareto front. To investigate how this potential emergence timing trade-off might constrain adaptation to increasing aridity, we sourced seeds of two grasses, Stipa pulchra and Bromus diandrus, from multiple maternal lines within populations across an aridity gradient in California and examined their performance in a greenhouse experiment. We monitored emergence and assayed ungerminated seeds for viability to determine seed persistence, a metric of potential among-year emergence spread. In both species, maternal lines with larger fractions of persistent seeds emerged later, indicating a trade-off between within-year emergence speed and potential among-year emergence spread. In both species, populations on the Pareto front for both earlier emergence and larger seed persistence fraction occupied significantly more arid sites than populations off the Pareto front, consistent with the hypothesis that more arid sites impose the strongest selection for earlier within-year emergence and greater among-year emergence spread. Our results provide an example of how evaluating genetically based correlations within populations and applying Pareto optimality among populations can be used to detect evolutionary constraints and adaptation across environmental gradients.

Phylogenetic diversity metrics for ecological communities: integrating species richness, abundance and evolutionary history.

Phylogenetic information is increasingly being used to understand the assembly of biological communities and ecological processes. However, commonly used metrics of phylogenetic diversity (PD) do not incorporate information on the relative abundances of individuals within a community. In this study, we develop three indices of PD that explicitly consider species abundances. First, we present a metric of phylogenetic-abundance evenness that evaluates the relationship between the abundance and the distribution of terminal branch lengths. Second, we calculate an index of hierarchical imbalance of abundances at the clade level encapsulating the distribution of individuals across the nodes in the phylogeny. Third, we develop an index of abundance-weighted evolutionary distinctiveness and generate an entropic index of phylogenetic diversity that captures both information on evolutionary distances and phylogenetic tree topology, and also serves as a basis to evaluate species conservation value. These metrics offer measures of phylogenetic diversity incorporating different community attributes. We compare these new metrics to existing ones, and use them to explore diversity patterns in a typical California annual grassland plant community at the Jasper Ridge biological preserve.

Contrasting trait responses in plant communities to experimental and geographic variation in precipitation.

• Patterns of precipitation are likely to change significantly in the coming century, with important but poorly understood consequences for plant communities. Experimental and correlative studies may provide insight into expected changes, but little research has addressed the degree of concordance between these approaches. • We synthesized results from four experimental water addition studies with a correlative analysis of community changes across a large natural precipitation gradient in the United States. We investigated whether community composition, summarized with plant functional traits, responded similarly to increasing precipitation among studies and sites. • In field experiments, increased precipitation favored species with small seed size, short leaf life span and high leaf nitrogen (N) concentration. However, with increasing precipitation along the natural gradient, community composition shifted towards species with higher mean seed mass, longer leaf life span and lower leaf N concentrations. • The differences in temporal and spatial scale of experimental manipulations and natural gradients may explain these contrasting results. Our results highlight the complexity of responses to climate change, and suggest that transient dynamics may not reflect long-term shifts in functional diversity and community composition. We propose a model of community change that incorporates these differences between short- and long-term responses to climate change.

Consumer versus resource control of producer diversity depends on ecosystem type and producer community structure.

Consumer and resource control of diversity in plant communities have long been treated as alternative hypotheses. However, experimental and theoretical evidence suggests that herbivores and nutrient resources interactively regulate the number and relative abundance of coexisting plant species. Experiments have yielded divergent and often contradictory responses within and among ecosystems, and no effort has to date reconciled this empirical variation within a general framework. Using data from 274 experiments from marine, freshwater, and terrestrial ecosystems, we present a cross-system analysis of producer diversity responses to local manipulations of resource supply and/or herbivory. Effects of herbivory and fertilization on producer richness differed substantially between systems: (i) herbivores reduced species richness in freshwater but tended to increase richness in terrestrial systems; (ii) fertilization increased richness in freshwater systems but reduced richness on land. Fertilization consistently reduced evenness, whereas herbivores increased evenness only in marine and terrestrial ecosystems. Producer community evenness and ecosystem productivity mediated fertilization and herbivore effects on diversity across ecosystems. Herbivores increased producer richness in more productive habitats and in producer assemblages with low evenness. These same assemblages also showed the strongest reduction in richness with fertilization, whereas fertilization increased (and herbivory decreased) richness in producer assemblages with high evenness. Our study indicates that system productivity and producer evenness determine the direction and magnitude of top-down and bottom-up control of diversity and may reconcile divergent empirical results within and among ecosystems.