Light competition drives herbivore and nutrient effects on plant diversity.

Enrichment of nutrients and loss of herbivores are assumed to cause a loss of plant diversity in grassland ecosystems because they increase plant cover, which leads to a decrease of light in the understory1-3. Empirical tests of the role of competition for light in natural systems are based on indirect evidence, and have been a topic of debate for the last 40 years. Here we show that experimentally restoring light to understory plants in a natural grassland mitigates the loss of plant diversity that is caused by either nutrient enrichment or the absence of mammalian herbivores. The initial effect of light addition on restoring diversity under fertilization was transitory and outweighed by the greater effect of herbivory on light levels, indicating that herbivory is a major factor that controls diversity, partly through light. Our results provide direct experimental evidence, in a natural system, that competition for light is a key mechanism that contributes to the loss of biodiversity after cessation of mammalian herbivory. Our findings also show that the effects of herbivores can outpace the effects of fertilization on competition for light. Management practices that target maintaining grazing by native or domestic herbivores could therefore have applications in protecting biodiversity in grassland ecosystems, because they alleviate competition for light in the understory.

Within-individual leaf trait variation increases with phenotypic integration in a subtropical tree diversity experiment.

Covariation of plant functional traits, that is, phenotypic integration, might constrain their variability. This was observed for inter- and intraspecific variation, but there is no evidence of a relationship between phenotypic integration and the functional variation within single plants (within-individual trait variation; WTV), which could be key to understand the extent of WTV in contexts like plant-plant interactions. We studied the relationship between WTV and phenotypic integration in c. 500 trees of 21 species in planted forest patches varying in species richness in subtropical China. Using visible and near-infrared spectroscopy (Vis-NIRS), we measured nine leaf morphological and chemical traits. For each tree, we assessed metrics of single and multitrait variation to assess WTV, and we used plant trait network properties based on trait correlations to quantify phenotypic integration. Against expectations, strong phenotypic integration within a tree led to greater variation across leaves. Not only this was true for single traits, but also the dispersion in a tree's multitrait hypervolume was positively associated with tree's phenotypic integration. Surprisingly, we only detected weak influence of the surrounding tree-species diversity on these relationships. Our study suggests that integrated phenotypes allow the variability of leaf phenotypes within the organism and supports that phenotypic integration prevents maladaptive variation.

Linking changes in species composition and biomass in a globally distributed grassland experiment.

Global change drivers, such as anthropogenic nutrient inputs, are increasing globally. Nutrient deposition simultaneously alters plant biodiversity, species composition and ecosystem processes like aboveground biomass production. These changes are underpinned by species extinction, colonisation and shifting relative abundance. Here, we use the Price equation to quantify and link the contributions of species that are lost, gained or that persist to change in aboveground biomass in 59 experimental grassland sites. Under ambient (control) conditions, compositional and biomass turnover was high, and losses (i.e. local extinctions) were balanced by gains (i.e. colonisation). Under fertilisation, the decline in species richness resulted from increased species loss and decreases in species gained. Biomass increase under fertilisation resulted mostly from species that persist and to a lesser extent from species gained. Drivers of ecological change can interact relatively independently with diversity, composition and ecosystem processes and functions such as aboveground biomass due to the individual contributions of species lost, gained or persisting.

The potential of multispectral imaging flow cytometry for environmental monitoring.

Environmental monitoring involves the quantification of microscopic cells and particles such as algae, plant cells, pollen, or fungal spores. Traditional methods using conventional microscopy require expert knowledge, are time-intensive and not well-suited for automated high throughput. Multispectral imaging flow cytometry (MIFC) allows measurement of up to 5000 particles per second from a fluid suspension and can simultaneously capture up to 12 images of every single particle for brightfield and different spectral ranges, with up to 60x magnification. The high throughput of MIFC has high potential for increasing the amount and accuracy of environmental monitoring, such as for plant-pollinator interactions, fossil samples, air, water or food quality that currently rely on manual microscopic methods. Automated recognition of particles and cells is also possible, when MIFC is combined with deep-learning computational techniques. Furthermore, various fluorescence dyes can be used to stain specific parts of the cell to highlight physiological and chemical features including: vitality of pollen or algae, allergen content of individual pollen, surface chemical composition (carbohydrate coating) of cells, DNA- or enzyme-activity staining. Here, we outline the great potential for MIFC in environmental research for a variety of research fields and focal organisms. In addition, we provide best practice recommendations.

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.

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.

Beyond nitrogen: phosphorus - estimating the minimum niche dimensionality for resource competition between phytoplankton.

The niche dimensionality required for coexistence is often discussed in terms of the number of limiting resources. N and P limitation are benchmarks for studying phytoplankton interactions. However, it is generally agreed that limitation by small numbers of resources cannot explain the high phytoplankton diversity observed in nature. Here, we parameterised resource competition models using experimental data for six phytoplankton species grown in monoculture with nine potential limiting resources. We tested predicted species biomass from these models against observations in two-species experimental mixtures. Uptake rates were similar across species, following the classic Redfield ratio. Model accuracy levelled out at around three to five resources suggesting the minimum dimensionality of this system. The models included the resources Fe, Mg, Na and S. Models including only N and P always performed poorly. These results suggest that high-dimensional information about resource limitation despite stoichiometric constraints may be needed to accurately predict community assembly.

Understanding plant communities of the future requires filling knowledge gaps.

In their response to our letter, De Boek et al. (2019) and Muller, Ballhausen, Lakovic, and Rillig (2019) argue that our conclusion that we need more realistic climate change experiments is too "gloomy" and that we need a plurality of experiments including extremes and multifactorial approaches. We agree that a diversity of experimental approaches is required in order to anticipate the consequences for plant communities of alternative future environmental conditions. However, we argue that "realistic" experiments are underrepresented in the portfolio of previous experiments, and are urgently needed to understand how species communities of the future will look like and how they will function. This article is a response to Muller et al., 26, e4-e5 and De Boeck et al., 26, e6-e7.

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.

Scale Both Confounds and Informs Characterization of Species Coexistence in Empirical Systems.

Identifying stable coexistence in empirical systems is notoriously difficult. Here, we show how spatiotemporal structure and complex system dynamics can confound two commonly used stability metrics in empirical contexts: response to perturbation and invasion rate when rare. We use these metrics to characterize stable coexistence across a range of spatial and temporal scales for five simulated models in which the ability of species to coexist in the long term is known a priori and for an empirical old field successional time series. We term the resulting multivariate distribution of metrics a "stability fingerprint." In accordance with a wide range of classic and recent studies, our results demonstrate that no combination of empirically tractable metrics or measurements is guaranteed to "correctly" characterize coexistence. However, we also find that heuristic information from the stability fingerprint can be used to broadly characterize dynamic behavior and identify circumstances under which particular combinations of species are likely to persist. Moreover, stability fingerprints appear to be particularly well suited for matching potential theoretical models to observed dynamics. These findings suggest that it may be prudent to shift the focus of empirical stability analysis away from quantifying single measures of stability and toward more heuristic, multivariate characterizations of community dynamics.

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.

Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe.

Soil microorganisms are critical to ecosystem functioning and the maintenance of soil fertility. However, despite global increases in the inputs of nitrogen (N) and phosphorus (P) to ecosystems due to human activities, we lack a predictive understanding of how microbial communities respond to elevated nutrient inputs across environmental gradients. Here we used high-throughput sequencing of marker genes to elucidate the responses of soil fungal, archaeal, and bacterial communities using an N and P addition experiment replicated at 25 globally distributed grassland sites. We also sequenced metagenomes from a subset of the sites to determine how the functional attributes of bacterial communities change in response to elevated nutrients. Despite strong compositional differences across sites, microbial communities shifted in a consistent manner with N or P additions, and the magnitude of these shifts was related to the magnitude of plant community responses to nutrient inputs. Mycorrhizal fungi and methanogenic archaea decreased in relative abundance with nutrient additions, as did the relative abundances of oligotrophic bacterial taxa. The metagenomic data provided additional evidence for this shift in bacterial life history strategies because nutrient additions decreased the average genome sizes of the bacterial community members and elicited changes in the relative abundances of representative functional genes. Our results suggest that elevated N and P inputs lead to predictable shifts in the taxonomic and functional traits of soil microbial communities, including increases in the relative abundances of faster-growing, copiotrophic bacterial taxa, with these shifts likely to impact belowground ecosystems worldwide.

High plant diversity is needed to maintain ecosystem services.

Biodiversity is rapidly declining worldwide, and there is consensus that this can decrease ecosystem functioning and services. It remains unclear, though, whether few or many of the species in an ecosystem are needed to sustain the provisioning of ecosystem services. It has been hypothesized that most species would promote ecosystem services if many times, places, functions and environmental changes were considered; however, no previous study has considered all of these factors together. Here we show that 84% of the 147 grassland plant species studied in 17 biodiversity experiments promoted ecosystem functioning at least once. Different species promoted ecosystem functioning during different years, at different places, for different functions and under different environmental change scenarios. Furthermore, the species needed to provide one function during multiple years were not the same as those needed to provide multiple functions within one year. Our results indicate that even more species will be needed to maintain ecosystem functioning and services than previously suggested by studies that have either (1) considered only the number of species needed to promote one function under one set of environmental conditions, or (2) separately considered the importance of biodiversity for providing ecosystem functioning across multiple years, places, functions or environmental change scenarios. Therefore, although species may appear functionally redundant when one function is considered under one set of environmental conditions, many species are needed to maintain multiple functions at multiple times and places in a changing world.

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.

Cyanobacteria dominance influences resource use efficiency and community turnover in phytoplankton and zooplankton communities.

Freshwater biodiversity loss potentially disrupts ecosystem services related to water quality and may negatively impact ecosystem functioning and temporal community turnover. We analysed a data set containing phytoplankton and zooplankton community data from 131 lakes through 9 years in an agricultural region to test predictions that plankton communities with low biodiversity are less efficient in their use of limiting resources and display greater community turnover (measured as community dissimilarity). Phytoplankton resource use efficiency (RUE = biomass per unit resource) was negatively related to phytoplankton evenness (measured as Pielou's evenness), whereas zooplankton RUE was positively related to phytoplankton evenness. Phytoplankton and zooplankton RUE were high and low, respectively, when Cyanobacteria, especially Microcystis sp., dominated. Phytoplankton communities displayed slower community turnover rates when dominated by few genera. Our findings, which counter findings of many terrestrial studies, suggest that Cyanobacteria dominance may play important roles in ecosystem functioning and community turnover in nutrient-enriched lakes.

Sustainable land management enhances ecological and economic multifunctionality under ambient and future climate.

The currently dominant types of land management are threatening the multifunctionality of ecosystems, which is vital for human well-being. Here, we present a novel ecological-economic assessment of how multifunctionality of agroecosystems in Central Germany depends on land-use type and climate. Our analysis includes 14 ecosystem variables in a large-scale field experiment with five different land-use types under two different climate scenarios (ambient and future climate). We consider ecological multifunctionality measures using averaging approaches with different weights, reflecting preferences of four relevant stakeholders based on adapted survey data. Additionally, we propose an economic multifunctionality measure based on the aggregate economic value of ecosystem services. Results show that intensive management and future climate decrease ecological multifunctionality for most scenarios in both grassland and cropland. Only under a weighting based on farmers' preferences, intensively-managed grassland shows higher multifunctionality than sustainably-managed grassland. The economic multifunctionality measure is about ~1.7 to 1.9 times higher for sustainable, compared to intensive, management for both grassland and cropland. Soil biodiversity correlates positively with ecological multifunctionality and is expected to be one of its drivers. As the currently prevailing land management provides high multifunctionality for farmers, but not for society at large, we suggest to promote and economically incentivise sustainable land management that enhances both ecological and economic multifunctionality, also under future climatic conditions.

CoRRE Trait Data: A dataset of 17 categorical and continuous traits for 4079 grassland species worldwide.

In our changing world, understanding plant community responses to global change drivers is critical for predicting future ecosystem composition and function. Plant functional traits promise to be a key predictive tool for many ecosystems, including grasslands; however, their use requires both complete plant community and functional trait data. Yet, representation of these data in global databases is sparse, particularly beyond a handful of most used traits and common species. Here we present the CoRRE Trait Data, spanning 17 traits (9 categorical, 8 continuous) anticipated to predict species' responses to global change for 4,079 vascular plant species across 173 plant families present in 390 grassland experiments from around the world. The dataset contains complete categorical trait records for all 4,079 plant species obtained from a comprehensive literature search, as well as nearly complete coverage (99.97%) of imputed continuous trait values for a subset of 2,927 plant species. These data will shed light on mechanisms underlying population, community, and ecosystem responses to global change in grasslands worldwide.

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.