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.

Integrative modelling reveals mechanisms linking productivity and plant species richness.

How ecosystem productivity and species richness are interrelated is one of the most debated subjects in the history of ecology. Decades of intensive study have yet to discern the actual mechanisms behind observed global patterns. Here, by integrating the predictions from multiple theories into a single model and using data from 1,126 grassland plots spanning five continents, we detect the clear signals of numerous underlying mechanisms linking productivity and richness. We find that an integrative model has substantially higher explanatory power than traditional bivariate analyses. In addition, the specific results unveil several surprising findings that conflict with classical models. These include the isolation of a strong and consistent enhancement of productivity by richness, an effect in striking contrast with superficial data patterns. Also revealed is a consistent importance of competition across the full range of productivity values, in direct conflict with some (but not all) proposed models. The promotion of local richness by macroecological gradients in climatic favourability, generally seen as a competing hypothesis, is also found to be important in our analysis. The results demonstrate that an integrative modelling approach leads to a major advance in our ability to discern the underlying processes operating in ecological systems.

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.

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.

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.

Increased grassland arthropod production with mammalian herbivory and eutrophication: a test of mediation pathways.

Increases in nutrient availability and alterations to mammalian herbivore communities are a hallmark of the Anthropocene, with consequences for the primary producer communities in many ecosystems. While progress has advanced understanding of plant community responses to these perturbations, the consequences for energy flow to higher trophic levels in the form of secondary production are less well understood. We quantified arthropod biomass after manipulating soil nutrient availability and wild mammalian herbivory, using identical methods across 13 temperate grasslands. Of experimental increases in nitrogen, phosphorus, and potassium, only treatments including nitrogen resulted in significantly increased arthropod biomass. Wild mammalian herbivore removal had a marginal, negative effect on arthropod biomass, with no interaction with nutrient availability. Path analysis including all sites implicated nutrient content of the primary producers as a driver of increased arthropod mean size, which we confirmed using 10 sites for which we had foliar nutrient data. Plant biomass and physical structure mediated the increase in arthropod abundance, while the nitrogen treatments accounted for additional variation not explained by our measured plant variables. The mean size of arthropod individuals was 2.5 times more influential on the plot-level total arthropod biomass than was the number of individuals. The eutrophication of grasslands through human activity, especially nitrogen deposition, thus may contribute to higher production of arthropod consumers through increases in nutrient availability across trophic levels.

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.

Trophic phylogenetics: evolutionary influences on body size, feeding, and species associations in grassland arthropods.

Contemporary animal-plant interactions such as herbivory are widely understood to be shaped by evolutionary history. Yet questions remain about the role of plant phylogenetic diversity in generating and maintaining herbivore diversity, and whether evolutionary relatedness of producers might predict the composition of consumer communities. We tested for evidence of evolutionary associations among arthropods and the plants on which they were found, using phylogenetic analysis of naturally occurring arthropod assemblages sampled from a plant-diversity manipulation experiment. Considering phylogenetic relationships among more than 900 arthropod consumer taxa and 29 plant species in the experiment, we addressed several interrelated questions. First, our results support the hypothesis that arthropod functional traits such as body size and trophic role are phylogenetically conserved in community ecological samples. Second, herbivores tended to cooccur with closer phylogenetic relatives than would be expected at random, whereas predators and parasitoids did not show phylogenetic association patterns. Consumer specialization, as measured by association through time with monocultures of particular host plant species, showed significant phylogenetic signal, although the. strength of this association varied among plant species. Polycultures of phylogenetically dissimilar plant species supported more phylogenetically dissimilar consumer communities than did phylogenetically similar polycultures. Finally, we separated the effects of plant species richness and relatedness in predicting the phylogenetic distribution of the arthropod assemblages in this experiment. The phylogenetic diversity of plant communities predicted the phylogenetic diversity of herbivore communities even after accounting for plant species richness. The phylogenetic diversity of secondary consumers differed by guild, with predator phylogenetic diversity responding to herbivore relatedness, while parasitoid phylogenetic diversity was driven by plant relatedness. Evolutionary associations between plants and their consumers are apparent in plots only meters apart in a single field, indicating a strong role for host-plant phylogenetic diversity in sustaining landscape consumer biodiversity.

Life-history constraints in grassland plant species: a growth-defence trade-off is the norm.

Plant growth can be limited by resource acquisition and defence against consumers, leading to contrasting trade-off possibilities. The competition-defence hypothesis posits a trade-off between competitive ability and defence against enemies (e.g. herbivores and pathogens). The growth-defence hypothesis suggests that strong competitors for nutrients are also defended against enemies, at a cost to growth rate. We tested these hypotheses using observations of 706 plant populations of over 500 species before and following identical fertilisation and fencing treatments at 39 grassland sites worldwide. Strong positive covariance in species responses to both treatments provided support for a growth-defence trade-off: populations that increased with the removal of nutrient limitation (poor competitors) also increased following removal of consumers. This result held globally across 4 years within plant life-history groups and within the majority of individual sites. Thus, a growth-defence trade-off appears to be the norm, and mechanisms maintaining grassland biodiversity may operate within this constraint.

Life history traits predict relative abundance in an assemblage of forest caterpillars.

Species in a given trophic level occur in vastly unequal abundance, a pattern commonly documented but poorly explained for most taxa. Theoretical predictions of species density such as those arising from the metabolic theory of ecology hold well at large spatial and temporal scales but are not supported in many communities sampled at a relatively small scale. At these scales ecological factors may be more important than the inherent limits to energy use set by allometric scaling of mass. These factors include the amount of resources available, and the ability of individuals to convert these resources successfully into population growth. While previous studies have demonstrated the limits of macroecological theory in explaining local abundance, few studies have tested alternative generalized mechanisms determining abundance at the community scale. Using an assemblage of forest moth species found co-occurring as caterpillars on a single host plant species, we tested whether species abundance on that plant could be explained by mass allometry, intrinsic population growth, diet breadth, or some combination of these traits. We parameterized life history traits of the caterpillars in association with the host plant in both field and laboratory settings, so that the population growth estimate was specific to the plant on which abundance was measured. Using a generalized least-squares regression method incorporating phylogenetic relatedness, we found no relationship between abundance and mass but found that abundance was best explained by both intrinsic population growth rate and diet breadth. Species population growth potential was most affected by survivorship and larval development time on the host plant. Metabolic constraints may determine upper limits to local abundance levels for species, but local community abundance is strongly predicted by the potential for population increase and the resources available to that species in the environment.

Local loss and spatial homogenization of plant diversity reduce ecosystem multifunctionality.

Biodiversity is declining in many local communities while also becoming increasingly homogenized across space. Experiments show that local plant species loss reduces ecosystem functioning and services, but the role of spatial homogenization of community composition and the potential interaction between diversity at different scales in maintaining ecosystem functioning remains unclear, especially when many functions are considered (ecosystem multifunctionality). We present an analysis of eight ecosystem functions measured in 65 grasslands worldwide. We find that more diverse grasslands-those with both species-rich local communities (α-diversity) and large compositional differences among localities (ß-diversity)-had higher levels of multifunctionality. Moreover, α- and ß-diversity synergistically affected multifunctionality, with higher levels of diversity at one scale amplifying the contribution to ecological functions at the other scale. The identity of species influencing ecosystem functioning differed among functions and across local communities, explaining why more diverse grasslands maintained greater functionality when more functions and localities were considered. These results were robust to variation in environmental drivers. Our findings reveal that plant diversity, at both local and landscape scales, contributes to the maintenance of multiple ecosystem services provided by grasslands. Preserving ecosystem functioning therefore requires conservation of biodiversity both within and among ecological communities.

Climate modifies response of non-native and native species richness to nutrient enrichment.

Ecosystem eutrophication often increases domination by non-natives and causes displacement of native taxa. However, variation in environmental conditions may affect the outcome of interactions between native and non-native taxa in environments where nutrient supply is elevated. We examined the interactive effects of eutrophication, climate variability and climate average conditions on the success of native and non-native plant species using experimental nutrient manipulations replicated at 32 grassland sites on four continents. We hypothesized that effects of nutrient addition would be greatest where climate was stable and benign, owing to reduced niche partitioning. We found that the abundance of non-native species increased with nutrient addition independent of climate; however, nutrient addition increased non-native species richness and decreased native species richness, with these effects dampened in warmer or wetter sites. Eutrophication also altered the time scale in which grassland invasion responded to climate, decreasing the importance of long-term climate and increasing that of annual climate. Thus, climatic conditions mediate the responses of native and non-native flora to nutrient enrichment. Our results suggest that the negative effect of nutrient addition on native abundance is decoupled from its effect on richness, and reduces the time scale of the links between climate and compositional change.

The influence of balanced and imbalanced resource supply on biodiversity-functioning relationship across ecosystems.

Numerous studies show that increasing species richness leads to higher ecosystem productivity. This effect is often attributed to more efficient portioning of multiple resources in communities with higher numbers of competing species, indicating the role of resource supply and stoichiometry for biodiversity-ecosystem functioning relationships. Here, we merged theory on ecological stoichiometry with a framework of biodiversity-ecosystem functioning to understand how resource use transfers into primary production. We applied a structural equation model to define patterns of diversity-productivity relationships with respect to available resources. Meta-analysis was used to summarize the findings across ecosystem types ranging from aquatic ecosystems to grasslands and forests. As hypothesized, resource supply increased realized productivity and richness, but we found significant differences between ecosystems and study types. Increased richness was associated with increased productivity, although this effect was not seen in experiments. More even communities had lower productivity, indicating that biomass production is often maintained by a few dominant species, and reduced dominance generally reduced ecosystem productivity. This synthesis, which integrates observational and experimental studies in a variety of ecosystems and geographical regions, exposes common patterns and differences in biodiversity-functioning relationships, and increases the mechanistic understanding of changes in ecosystems productivity.

Comment on "Worldwide evidence of a unimodal relationship between productivity and plant species richness".

Fraser et al. (Reports, 17 July 2015, p. 302) report a unimodal relationship between productivity and species richness at regional and global scales, which they contrast with the results of Adler et al. (Reports, 23 September 2011, p. 1750). However, both data sets, when analyzed correctly, show clearly and consistently that productivity is a poor predictor of local species richness.

Grassland productivity limited by multiple nutrients.

Terrestrial ecosystem productivity is widely accepted to be nutrient limited(1). Although nitrogen (N) is deemed a key determinant of aboveground net primary production (ANPP)(2,3), the prevalence of co-limitation by N and phosphorus (P) is increasingly recognized(4-8). However, the extent to which terrestrial productivity is co-limited by nutrients other than N and P has remained unclear. Here, we report results from a standardized factorial nutrient addition experiment, in which we added N, P and potassium (K) combined with a selection of micronutrients (K+µ), alone or in concert, to 42 grassland sites spanning five continents, and monitored ANPP. Nutrient availability limited productivity at 31 of the 42 grassland sites. And pairwise combinations of N, P, and K+µ co-limited ANPP at 29 of the sites. Nitrogen limitation peaked in cool, high latitude sites. Our findings highlight the importance of less studied nutrients, such as K and micronutrients, for grassland productivity, and point to significant variations in the type and degree of nutrient limitation. We suggest that multiple-nutrient constraints must be considered when assessing the ecosystem-scale consequences of nutrient enrichment.

Plant species' origin predicts dominance and response to nutrient enrichment and herbivores in global grasslands.

Exotic species dominate many communities; however the functional significance of species' biogeographic origin remains highly contentious. This debate is fuelled in part by the lack of globally replicated, systematic data assessing the relationship between species provenance, function and response to perturbations. We examined the abundance of native and exotic plant species at 64 grasslands in 13 countries, and at a subset of the sites we experimentally tested native and exotic species responses to two fundamental drivers of invasion, mineral nutrient supplies and vertebrate herbivory. Exotic species are six times more likely to dominate communities than native species. Furthermore, while experimental nutrient addition increases the cover and richness of exotic species, nutrients decrease native diversity and cover. Native and exotic species also differ in their response to vertebrate consumer exclusion. These results suggest that species origin has functional significance, and that eutrophication will lead to increased exotic dominance in grasslands.

White-tailed deer alter specialist and generalist insect herbivory through plant traits.

Within a plant species, leaf traits can vary across environmental, genetic, spatial, and temporal gradients, even showing drastic differences within individuals. Herbivory can also induce variation in leaf morphology, defensive structure, and chemistry including nutritional content. Indirect effects of prior insect herbivory on later herbivores have been well documented, but the induction of trait changes after vertebrate herbivory has been little explored. Here, we examined how browsing of spicebush (Lindera benzoin L.), a dominant understory shrub in eastern mesic forests, by white-tailed deer (Odocoileus virginianus L.) altered plant quality and subsequent foliar herbivory by insects. Browsing history explained ≈ 10% of overall leaf trait variation; regenerated leaves had greater water content and specific leaf area (P = 0.009), but were lower in nitrogen and greater in carbon (P < 0.001), than leaves on unbrowsed plants. However, browsing did not shift terpene chemistry as revealed by GC-MS. In the lab, caterpillars of the specialist spicebush swallowtail (Papilio troilus L.) preferred (P = 0.02) and grew 20% faster (P = 0.02) on foliage from browsed plants; whereas total herbivory in the field, including generalist insect herbivory, was twice as high on unbrowsed plants (P = 0.016). These results suggest that the ecological impacts of deer in forest understories can have cascading impacts on arthropod communities by changing the suitability of host-plants to insect herbivores.

Novel weapons testing: are invasive plants more chemically defended than native plants?

BACKGROUND: Exotic species have been hypothesized to successfully invade new habitats by virtue of possessing novel biochemistry that repels native enemies. Despite the pivotal long-term consequences of invasion for native food-webs, to date there are no experimental studies examining directly whether exotic plants are any more or less biochemically deterrent than native plants to native herbivores. METHODOLOGY/PRINCIPAL FINDINGS: In a direct test of this hypothesis using herbivore feeding assays with chemical extracts from 19 invasive plants and 21 co-occurring native plants, we show that invasive plant biochemistry is no more deterrent (on average) to a native generalist herbivore than extracts from native plants. There was no relationship between extract deterrence and length of time since introduction, suggesting that time has not mitigated putative biochemical novelty. Moreover, the least deterrent plant extracts were from the most abundant species in the field, a pattern that held for both native and exotic plants. Analysis of chemical deterrence in context with morphological defenses and growth-related traits showed that native and exotic plants had similar trade-offs among traits. CONCLUSIONS/SIGNIFICANCE: Overall, our results suggest that particular invasive species may possess deterrent secondary chemistry, but it does not appear to be a general pattern resulting from evolutionary mismatches between exotic plants and native herbivores. Thus, fundamentally similar processes may promote the ecological success of both native and exotic species.