Do southern seed or soil microbes mitigate the effects of warming on establishing prairie plant communities?

Restoration in this era of climate change comes with a new challenge: anticipating how best to restore populations to persist under future climate conditions. Specifically, it remains unknown whether locally adapted or warm-adapted seeds best promote native plant community restoration in the warmer conditions predicted in the future and whether local or warm-adapted soil microbial communities could mitigate plant responses to warming. This may be especially relevant for biomes spanning large climatic gradients, such as the North American tallgrass prairie. Here, we used a short-term mesocosm experiment to evaluate how seed provenances (Local Northern region, Non-local Northern region, Non-local Southern region) of 10 native tallgrass prairie plants (four forbs, two legumes, and four grasses) responded to warmer conditions predicted in the future and how soil microbial communities from those three regions influenced these responses. Warming and seed provenance affected plant community composition and warming decreased plant diversity for all three seed provenances. Plant species varied in their individual responses to warming, and across species, we detected no consistent differences among the three provenances in terms of biomass response to warming and few strong effects of soil provenance. Our work provides evidence that warming, in part, may reduce plant diversity and affect restored prairie composition. Because the southern provenance did not consistently outperform others under warming and we found little support for the "local is best" paradigm currently dominating restoration practice, identifying appropriate seed provenances to promote restoration success both now and in future warmer environments may be challenging. Due to the idiosyncratic responses across species, we recommend that land managers compare seeds from different regions for each species to determine which seed provenance performs best under warming and in restoration for tallgrass prairies.

Global change effects on plant communities are magnified by time and the number of global change factors imposed.

Global change drivers (GCDs) are expected to alter community structure and consequently, the services that ecosystems provide. Yet, few experimental investigations have examined effects of GCDs on plant community structure across multiple ecosystem types, and those that do exist present conflicting patterns. In an unprecedented global synthesis of over 100 experiments that manipulated factors linked to GCDs, we show that herbaceous plant community responses depend on experimental manipulation length and number of factors manipulated. We found that plant communities are fairly resistant to experimentally manipulated GCDs in the short term (<10 y). In contrast, long-term (≥10 y) experiments show increasing community divergence of treatments from control conditions. Surprisingly, these community responses occurred with similar frequency across the GCD types manipulated in our database. However, community responses were more common when 3 or more GCDs were simultaneously manipulated, suggesting the emergence of additive or synergistic effects of multiple drivers, particularly over long time periods. In half of the cases, GCD manipulations caused a difference in community composition without a corresponding species richness difference, indicating that species reordering or replacement is an important mechanism of community responses to GCDs and should be given greater consideration when examining consequences of GCDs for the biodiversity-ecosystem function relationship. Human activities are currently driving unparalleled global changes worldwide. Our analyses provide the most comprehensive evidence to date that these human activities may have widespread impacts on plant community composition globally, which will increase in frequency over time and be greater in areas where communities face multiple GCDs simultaneously.

Determinants of community compositional change are equally affected by global change.

Global change is impacting plant community composition, but the mechanisms underlying these changes are unclear. Using a dataset of 58 global change experiments, we tested the five fundamental mechanisms of community change: changes in evenness and richness, reordering, species gains and losses. We found 71% of communities were impacted by global change treatments, and 88% of communities that were exposed to two or more global change drivers were impacted. Further, all mechanisms of change were equally likely to be affected by global change treatments-species losses and changes in richness were just as common as species gains and reordering. We also found no evidence of a progression of community changes, for example, reordering and changes in evenness did not precede species gains and losses. We demonstrate that all processes underlying plant community composition changes are equally affected by treatments and often occur simultaneously, necessitating a wholistic approach to quantifying community changes.

Unfair trade underground revealed by integrating data with Nash bargaining models.

Mutually beneficial resource exchange is fundamental to global biogeochemical cycles and plant and animal nutrition. However, there is inherent potential conflict in mutualisms, as each organism benefits more when the exchange ratio ('price') minimizes its own costs and maximizes its benefits. Understanding the bargaining power that each partner has in these interactions is key to our ability to predict the exchange ratio and therefore the functionality of the cell, organism, community and ecosystem. We tested whether partners have symmetrical ('fair') or asymmetrical ('unfair') bargaining power in a legume-rhizobia nitrogen-fixing symbiosis using measurements of carbon and nitrogen dynamics in a mathematical modeling framework derived from economic theory. A model of symmetric bargaining power was not consistent with our data. Instead, our data indicate that the growth benefit to the plant (Medicago truncatula) has greater weight in determining trade dynamics than the benefit to the bacteria. Quantitative estimates of the relative power of the plant revealed that the plant's influence rises as soil nitrogen availability decreases and trade benefits to both partners increase. Our finding that M. truncatula legumes have more bargaining power than their rhizobial partner at lower nitrogen availabilities highlights the importance of context-dependence for the evolution of mutualism with increasing nutrient deposition.

Ecosystem multifunctionality increases with beta diversity in restored prairies.

The loss of biodiversity at local and larger scales has potentially dramatic effects on ecosystem functioning. Many studies have shown that ecosystem functioning depends on biodiversity, but the role of beta diversity, spatial variation in community composition, is less clear than that of local-scale (alpha) diversity. To test the hypothesis that beta diversity would increase ecosystem multifunctionality through variation in species functional traits, we gathered data on plant community composition, plant functional traits, and seven ecosystem functions across 29 restored prairies. We found that averaged multifunctionality (mean of seven ecosystem functions) increased with both taxonomic beta diversity and functional beta diversity. The abundance of the dominant species, big bluestem, played a more minor role, suggesting a limited role for the selection effect. Neither taxonomic nor functional alpha richness was associated with multifunctionality, though this finding may be sensitive to the identity of the functions included because alpha diversity was associated with some individual functions in opposing directions. These findings suggest that in systems structured largely by natural processes, beta diversity (a patchwork of functionally different plant communities) and dominant species abundance may be more important than alpha diversity in fostering ecosystem multifunctionality. These findings suggest the need for an increased focus on community heterogeneity to reestablish functional ecosystems during restoration.

Modelling nutritional mutualisms: challenges and opportunities for data integration.

Nutritional mutualisms are ancient, widespread, and profoundly influential in biological communities and ecosystems. Although much is known about these interactions, comprehensive answers to fundamental questions, such as how resource availability and structured interactions influence mutualism persistence, are still lacking. Mathematical modelling of nutritional mutualisms has great potential to facilitate the search for comprehensive answers to these and other fundamental questions by connecting the physiological and genomic underpinnings of mutualisms with ecological and evolutionary processes. In particular, when integrated with empirical data, models enable understanding of underlying mechanisms and generalisation of principles beyond the particulars of a given system. Here, we demonstrate how mathematical models can be integrated with data to address questions of mutualism persistence at four biological scales: cell, individual, population, and community. We highlight select studies where data has been or could be integrated with models to either inform model structure or test model predictions. We also point out opportunities to increase model rigour through tighter integration with data, and describe areas in which data is urgently needed. We focus on plant-microbe systems, for which a wealth of empirical data is available, but the principles and approaches can be generally applied to any nutritional mutualism.

Asynchrony among local communities stabilises ecosystem function of metacommunities.

Temporal stability of ecosystem functioning increases the predictability and reliability of ecosystem services, and understanding the drivers of stability across spatial scales is important for land management and policy decisions. We used species-level abundance data from 62 plant communities across five continents to assess mechanisms of temporal stability across spatial scales. We assessed how asynchrony (i.e. different units responding dissimilarly through time) of species and local communities stabilised metacommunity ecosystem function. Asynchrony of species increased stability of local communities, and asynchrony among local communities enhanced metacommunity stability by a wide range of magnitudes (1-315%); this range was positively correlated with the size of the metacommunity. Additionally, asynchronous responses among local communities were linked with species' populations fluctuating asynchronously across space, perhaps stemming from physical and/or competitive differences among local communities. Accordingly, we suggest spatial heterogeneity should be a major focus for maintaining the stability of ecosystem services at larger spatial scales.

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.

Resource availability and imbalance affect plant-mycorrhizal interactions: a field test of three hypotheses.

Ecological stoichiometry can explain major trends in how interactions among species change across fertility gradients, but important questions remain. For example, stoichiometry predicts that fertilization should cause plants to reduce carbon allocation to arbuscular mycorrhizal fungi and, consequently, reduce fungal abundance, but responses in the field are highly variable. In a field experiment, we tested three hypotheses that could drive this variation: (1) fungi are nitrogen limited in very nitrogen-poor soils, so fertilization increases their abundance; (2) the N:P ratio of fertilization affects plant carbon allocation to fungi; (3) plant species differences affect fungal response. Our results support all three hypotheses: stoichiometry and species idiosyncrasies jointly determined fungal response to fertilization. We provide field evidence in support of the hypothesis that nitrogen can limit fungal abundance in temperate grasslands. We also show that fungal abundance in soil (hyphal length) differed beneath two dominant plant species: big bluestem (Andropogon gerardii) and smooth brome (Bromus inermis). These grass species also differed in the degree to which they reduced root colonization with fertilization, but these differences in allocation did not lead to differential responses to fertilization in terms of fungal abundance in the soil. This study shows that, while ecological stoichiometry is a useful framework for understanding the effects of eutrophication on this important and widespread species interaction, including these subtleties can increase the predictive power of the theory.

Ecological specialization and trade affect the outcome of negotiations in mutualism.

By definition, mutualisms involve the exchange of goods or services between partners. It has been shown that mutualism can grade into parasitism, but even when exchange is mutually beneficial, a conflict of interest remains because each partner benefits from reaping more benefits at a lower cost. Metaphorically, the partners negotiate the conditions of trade, the outcome of which will determine the net benefit to each partner. Each partner can adjust its allocation to self-provisioning while negotiating the ratio at which benefits are exchanged. To understand how these two features of trade affect mutualisms, we used the example of the plant-arbuscular mycorrhizal mutualism and modeled uptake and trade of two resources, phosphorus and carbon. In most contexts, the fungus specialized on phosphorus uptake while the plant took up both phosphorus and carbon. However, when phosphorus was abundant and light was scarce, the plant specialized, taking up only carbon and relying on trade for phosphorus. Resource availability was the most important factor determining specialization and the outcome of negotiation and trade, but other aspects of the context were also important. These results suggest experiments to link these two key features of trade with environmental conditions to determine the outcome of mutualism.

Plant species differ in their ability to reduce allocation to non-beneficial arbuscular mycorrhizal fungi.

Theory suggests that cheaters threaten the persistence of mutualisms, but that sanctions to prevent cheating can stabilize mutualisms. In the arbuscular mycorrhizal symbiosis, reports of parasitism suggest that reductions in plant carbon allocation are not universally effective. I asked whether plant species differences in mycorrhizal responsiveness would affect both their susceptibility to parasitism and their reduction in allocation to non-beneficial arbuscular mycorrhizal fungi (AMF) in high-phosphorus soils. In a greenhouse experiment, I found that two C3 grasses, Bromus inermis and Elymus repens, effectively suppressed root colonization and AMF hyphal abundance. Increases in soil phosphorus did not reduce the degree to which AMF increased plant biomass. In contrast, two C4 grasses, Andropogon gerardii and Schizachyrium scoparium, more weakly reduced root colonization and failed to suppress AMF hyphal abundance. Consequently, they experienced strong declines in their response to AMF, and one species suffered parasitism. Thus, species differ in susceptibility to parasitism and their reduction in allocation to non-beneficial AMF. These differences may affect the distribution and abundance of plants and AMF, as well as the stability of the mutualism.

Do trade-offs govern plant species' responses to different global change treatments?

Plants are subject to trade-offs among growth strategies such that adaptations for optimal growth in one condition can preclude optimal growth in another. Thus, we predicted that a plant species that responds positively to one global change treatment would be less likely than average to respond positively to another treatment, particularly for pairs of treatments that favor distinct traits. We examined plant species' abundances in 39 global change experiments manipulating two or more of the following: CO2 , nitrogen, phosphorus, water, temperature, or disturbance. Overall, the directional response of a species to one treatment was 13% more likely than expected to oppose its response to a another single-factor treatment. This tendency was detectable across the global data set, but held little predictive power for individual treatment combinations or within individual experiments. Although trade-offs in the ability to respond to different global change treatments exert discernible global effects, other forces obscure their influence in local communities.

Species pool size alters species-area relationships during experimental community assembly.

The species pool concept has advanced our understanding for how biodiversity is coupled at local and regional scales. However, it remains unclear how species pool size, the number of species available to disperse to a site, influences community assembly across spatial scales. We provide one of the first studies that assesses diversity across scales after experimentally assembling grassland communities from species pools of different sizes. We show that species pool size causes scale-dependent effects on diversity in grasslands undergoing restoration by altering the shape of the species-area relationship (SAR). Specifically, larger species pools increased the slope of the SAR, but not the intercept, suggesting that dispersal from a larger pool causes species to be more spatially aggregated. This increased aggregation appears to be caused by sampling effects due to fewer individuals arriving per species, rather than stronger species sorting across variation in soil moisture. These scale-dependent effects suggest that studies evaluating species pools at a single, small scale may underestimate their effects, thereby contributing to uncertainty about the importance of regional processes for community assembly and their consequences for ecological restoration.

Mechanisms contributing to stability in ecosystem function depend on the environmental context.

Stability in ecosystem function is an important but poorly understood phenomenon. Anthropogenic perturbations alter communities, but how they change stability and the strength of stabilizing mechanisms is not clear. We examined temporal stability (invariability) in aboveground productivity in replicated 18-year time series of experimentally perturbed grassland plant communities. We found that disturbed annual-dominated communities were more stable than undisturbed perennial communities, coincident with increases in the stabilizing effect of mean-variance scaling. We also found that nitrogen-fertilized communities maintained stability despite losses in species richness, probably because of increased compensatory dynamics and increased dominance by particularly stable dominant species. Among our communities, slight variation in diversity was not the strongest mechanism driving differences in stability. Instead, our study suggests that decreases in individual species variabilities and increases in the relative abundance of stable dominant species may help maintain stability in the functioning of ecosystems confronted with eutrophication, disturbance, and other global changes.

Landscape context explains ecosystem multifunctionality in restored grasslands better than plant diversity.

There is strong evidence for a positive relationship between biodiversity and ecosystem functioning at local spatial scales. However, how different aspects of biodiversity relate to multiple ecosystem functions (multifunctionality) across heterogeneous landscapes, and how the magnitude of biodiversity, dominant species, and environmental effects on functioning compare, remain poorly understood. We compared relationships between plant phylogenetic, functional, and taxonomic diversity and ecosystem multifunctionality across 29 restored grasslands. Functional diversity was positively associated with multifunctionality, more strongly than other diversity measures; however, landscape composition explained nearly four times more variation in multifunctionality than did functional diversity, with plots within human-modified landscapes supporting lower multifunctionality. Individual functions were typically more strongly correlated with environmental variables than with diversity. We also found that abundance of the dominant species, Andropogon gerardii, was positively correlated with multifunctionality. Plant diversity, dominant species, and underlying environmental conditions underpin ecosystem multifunctionality in grasslands, but how biodiversity is measured matters for the strength and direction of biodiversity-ecosystem function relationships. Finally, in natural systems environmental variation unrelated to local biodiversity is important for determining ecosystem functioning.