A novel proxy to examine interspecific phosphorus facilitation between plant species.

Resource complementarity can contribute to enhanced ecosystem functioning in diverse plant communities, but the role of facilitation in the enhanced complementarity is poorly understood. Here, we use leaf manganese concentration ([Mn]) as a proxy for rhizosheath carboxylate concentration to explore novel mechanisms of complementarity mediated by phosphorus (P) facilitation. In pot experiments, we showed that mixtures involving Carex korshinskyi, an efficient P-mobilizing species, exhibited greater biomass and relative complementarity effect than combinations without C. korshinskyi on P-deficient soils. Compared with monocultures, leaf [Mn] and [P] of species that are inefficient at P mobilization increased by 27% and 21% when grown with C. korshinskyi (i.e. interspecific P facilitation via carboxylates) rather than next to another inefficient P-mobilizing species. This experimental result was supported by a meta-analysis including a range of efficient P-mobilizing species. Phosphorus facilitation enhanced the relative complementarity effect in low-P environments, related to a greater change in several facilitated species of their root morphological traits relative to those in monoculture. Using leaf [Mn] as a proxy, we highlight a vital mechanism of interspecific P facilitation via belowground processes and provide evidence for the pivotal role of P facilitation mediated by the plasticity of root traits in biodiversity research.

The structure of root-associated fungal communities is related to the long-term effects of plant diversity on productivity.

Root-associated fungi could play a role in determining both the positive relationship between plant diversity and productivity in experimental grasslands, and its strengthening over time. This hypothesis assumes that specialized pathogenic and mutualistic fungal communities gradually assemble over time, enhancing plant growth more in species-rich than in species-poor plots. To test this hypothesis, we used high-throughput amplicon sequencing to characterize root-associated fungal communities in experimental grasslands of 1 and 15 years of age with varying levels of plant species richness. Specifically, we tested whether the relationship between fungal communities and plant richness and productivity becomes stronger with the age of the experimental plots. Our results showed that fungal diversity increased with plant diversity, but this relationship weakened rather than strengthened over the two time points. Contrastingly, fungal community composition showed increasing associations with plant diversity over time, suggesting a gradual build-up of specific fungal assemblages. Analyses of different fungal guilds showed that these changes were particularly marked in pathogenic fungi, whose shifts in relative abundance are consistent with the pathogen dilution hypothesis in diverse plant communities. Our results suggest that root-associated fungal pathogens play more specific roles in determining the diversity-productivity relationship than other root-associated plant symbionts.

Universal beta-diversity-functioning relationships are neither observed nor expected.

Widespread evidence shows that local species richness (α-diversity) loss hampers the biomass production and stability of ecosystems. ß-Diversity, namely the variation of species compositions among different ecological communities, represents another important biodiversity component, but studies on how it drives ecosystem functioning show mixed results. We argue that to better understand the importance of ß-diversity we need to consider it across contexts. We focus on three scenarios that cause gradients in ß-diversity: changes in (i) abiotic heterogeneity, (ii) habitat isolation, and (iii) species pool richness. We show that across these scenarios we should not expect universally positive relationships between ß-diversity, production, and ecosystem stability. Nevertheless, predictable relationships between ß-diversity and ecosystem functioning do exist in specific contexts, and can reconcile seemingly contrasting empirical relationships.

Plant neighbours can make or break the disease transmission chain of a fungal root pathogen.

Biodiversity can reduce or increase disease transmission. These divergent effects suggest that community composition rather than diversity per se determines disease transmission. In natural plant communities, little is known about the functional roles of neighbouring plant species in belowground disease transmission. Here, we experimentally investigated disease transmission of a fungal root pathogen (Rhizoctonia solani) in two focal plant species in combinations with four neighbour species of two ages. We developed stochastic models to test the relative importance of two transmission-modifying mechanisms: (1) infected hosts serve as nutrient supply to increase hyphal growth, so that successful disease transmission is self-reinforcing; and (2) plant resistance increases during plant development. Neighbouring plants either reduced or increased disease transmission in the focal plants. These effects depended on neighbour age, but could not be explained by a simple dichotomy between hosts and nonhost neighbours. Model selection revealed that both transmission-modifying mechanisms are relevant and that focal host-neighbour interactions changed which mechanisms steered disease transmission rate. Our work shows that neighbour-induced shifts in the importance of these mechanisms across root networks either make or break disease transmission chains. Understanding how diversity affects disease transmission thus requires integrating interactions between focal and neighbour species and their pathogens.

An integrated framework of plant form and function: the belowground perspective.

Plant trait variation drives plant function, community composition and ecosystem processes. However, our current understanding of trait variation disproportionately relies on aboveground observations. Here we integrate root traits into the global framework of plant form and function. We developed and tested an overarching conceptual framework that integrates two recently identified root trait gradients with a well-established aboveground plant trait framework. We confronted our novel framework with published relationships between above- and belowground trait analogues and with multivariate analyses of above- and belowground traits of 2510 species. Our traits represent the leaf and root conservation gradients (specific leaf area, leaf and root nitrogen concentration, and root tissue density), the root collaboration gradient (root diameter and specific root length) and the plant size gradient (plant height and rooting depth). We found that an integrated, whole-plant trait space required as much as four axes. The two main axes represented the fast-slow 'conservation' gradient on which leaf and fine-root traits were well aligned, and the 'collaboration' gradient in roots. The two additional axes were separate, orthogonal plant size axes for height and rooting depth. This perspective on the multidimensional nature of plant trait variation better encompasses plant function and influence on the surrounding environment.

Root traits explain plant species distributions along climatic gradients yet challenge the nature of ecological trade-offs.

Ecological theory is built on trade-offs, where trait differences among species evolved as adaptations to different environments. Trade-offs are often assumed to be bidirectional, where opposite ends of a gradient in trait values confer advantages in different environments. However, unidirectional benefits could be widespread if extreme trait values confer advantages at one end of an environmental gradient, whereas a wide range of trait values are equally beneficial at the other end. Here, we show that root traits explain species occurrences along broad gradients of temperature and water availability, but model predictions only resembled trade-offs in two out of 24 models. Forest species with low specific root length and high root tissue density (RTD) were more likely to occur in warm climates but species with high specific root length and low RTD were more likely to occur in cold climates. Unidirectional benefits were more prevalent than trade-offs: for example, species with large-diameter roots and high RTD were more commonly associated with dry climates, but species with the opposite trait values were not associated with wet climates. Directional selection for traits consistently occurred in cold or dry climates, whereas a diversity of root trait values were equally viable in warm or wet climates. Explicit integration of unidirectional benefits into ecological theory is needed to advance our understanding of the consequences of trait variation on species responses to environmental change.

Mycorrhizal associations change root functionality: a 3D modelling study on competitive interactions between plants for light and nutrients.

Recent studies show that the variation in root functional traits can be explained by a two-dimensional trait framework, containing a 'collaboration' axis in addition to the classical fast-slow 'conservation' axis. This collaboration axis spans from thin and highly branched roots that employ a 'do-it-yourself' strategy to thick and sparsely branched roots that 'outsource' nutrient uptake to symbiotic arbuscular mycorrhizal fungi (AMF). Here, we explore the functionality of this collaboration axis by quantifying how interactions with AMF change the impact of root traits on plant performance. To this end, we developed a novel functional-structural plant (FSP) modelling approach that simulates plants competing for light and nutrients in the presence or absence of AMF. Our simulation results support the notion that in the absence of AMF, plants rely on thin, highly branched roots for their nutrient uptake. The presence of AMF, however, promotes thick, unbranched roots as an alternative strategy for uptake of immobile phosphorus, but not for mobile nitrogen. This provides further support for a root trait framework that accommodates for the interactive effect of roots and AMF. Our modelling study offers unique opportunities to incorporate soil microbial interactions into root functionality as it integrates consequences of belowground trait expression.

Plant-Soil Feedbacks and Temporal Dynamics of Plant Diversity-Productivity Relationships.

Plant-soil feedback (PSF) and diversity-productivity relationships are important research fields to study drivers and consequences of changes in plant biodiversity. While studies suggest that positive plant diversity-productivity relationships can be explained by variation in PSF in diverse plant communities, key questions on their temporal relationships remain. Here, we discuss three processes that change PSF over time in diverse plant communities, and their effects on temporal dynamics of diversity-productivity relationships: spatial redistribution and changes in dominance of plant species; phenotypic shifts in plant traits; and dilution of soil pathogens and increase in soil mutualists. Disentangling these processes in plant diversity experiments will yield new insights into how plant diversity-productivity relationships change over time.

Biotic homogenization destabilizes ecosystem functioning by decreasing spatial asynchrony.

Our planet is facing significant changes of biodiversity across spatial scales. Although the negative effects of local biodiversity (α diversity) loss on ecosystem stability are well documented, the consequences of biodiversity changes at larger spatial scales, in particular biotic homogenization, that is, reduced species turnover across space (ß diversity), remain poorly known. Using data from 39 grassland biodiversity experiments, we examine the effects of ß diversity on the stability of simulated landscapes while controlling for potentially confounding biotic and abiotic factors. Our results show that higher ß diversity generates more asynchronous dynamics among local communities and thereby contributes to the stability of ecosystem productivity at larger spatial scales. We further quantify the relative contributions of α and ß diversity to ecosystem stability and find a relatively stronger effect of α diversity, possibly due to the limited spatial scale of our experiments. The stabilizing effects of both α and ß diversity lead to a positive diversity-stability relationship at the landscape scale. Our findings demonstrate the destabilizing effect of biotic homogenization and suggest that biodiversity should be conserved at multiple spatial scales to maintain the stability of ecosystem functions and services.

The fungal collaboration gradient dominates the root economics space in plants.

Plant economics run on carbon and nutrients instead of money. Leaf strategies aboveground span an economic spectrum from "live fast and die young" to "slow and steady," but the economy defined by root strategies belowground remains unclear. Here, we take a holistic view of the belowground economy and show that root-mycorrhizal collaboration can short circuit a one-dimensional economic spectrum, providing an entire space of economic possibilities. Root trait data from 1810 species across the globe confirm a classical fast-slow "conservation" gradient but show that most variation is explained by an orthogonal "collaboration" gradient, ranging from "do-it-yourself" resource uptake to "outsourcing" of resource uptake to mycorrhizal fungi. This broadened "root economics space" provides a solid foundation for predictive understanding of belowground responses to changing environmental conditions.

Limited evidence for spatial resource partitioning across temperate grassland biodiversity experiments.

Locally, plant species richness supports many ecosystem functions. Yet, the mechanisms driving these often-positive biodiversity-ecosystem functioning relationships are not well understood. Spatial resource partitioning across vertical resource gradients is one of the main hypothesized causes for enhanced ecosystem functioning in more biodiverse grasslands. Spatial resource partitioning occurs if species differ in where they acquire resources and can happen both above- and belowground. However, studies investigating spatial resource partitioning in grasslands provide inconsistent evidence. We present the results of a meta-analysis of 21 data sets from experimental species-richness gradients in grasslands. We test the hypothesis that increasing spatial resource partitioning along vertical resource gradients enhances ecosystem functioning in diverse grassland plant communities above- and belowground. To test this hypothesis, we asked three questions. (1) Does species richness enhance biomass production or community resource uptake across sites? (2) Is there evidence of spatial resource partitioning as indicated by resource tracer uptake and biomass allocation above- and belowground? (3) Is evidence of spatial resource partitioning correlated with increased biomass production or community resource uptake? Although plant species richness enhanced community nitrogen and potassium uptake and biomass production above- and belowground, we found that plant communities did not meet our criteria for spatial resource partitioning, though they did invest in significantly more aboveground biomass in higher canopy layers in mixture relative to monoculture. Furthermore, the extent of spatial resource partitioning across studies was not positively correlated with either biomass production or community resource uptake. Our results suggest that spatial resource partitioning across vertical resource gradients alone does not offer a general explanation for enhanced ecosystem functioning in more diverse temperate grasslands.

Author Correction: Diversity-dependent temporal divergence of ecosystem functioning in experimental ecosystems.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

The Future of Complementarity: Disentangling Causes from Consequences.

Evidence suggests that biodiversity supports ecosystem functioning. Yet, the mechanisms driving this relationship remain unclear. Complementarity is one common explanation for these positive biodiversity-ecosystem functioning relationships. Yet, complementarity is often indirectly quantified as overperformance in mixture relative to monoculture (e.g., 'complementarity effect'). This overperformance is then attributed to the intuitive idea of complementarity or, more specifically, to species resource partitioning. Locally, however, several unassociated causes may drive this overperformance. Here, we differentiate complementarity into three types of species differences that may cause enhanced ecosystem functioning in more diverse ecosystems: (i) resource partitioning, (ii) abiotic facilitation, and (iii) biotic feedbacks. We argue that disentangling these three causes is crucial for predicting the response of ecosystems to future biodiversity loss.

Multiple facets of biodiversity drive the diversity-stability relationship.

A substantial body of evidence has demonstrated that biodiversity stabilizes ecosystem functioning over time in grassland ecosystems. However, the relative importance of different facets of biodiversity underlying the diversity-stability relationship remains unclear. Here we use data from 39 grassland biodiversity experiments and structural equation modelling to investigate the roles of species richness, phylogenetic diversity and both the diversity and community-weighted mean of functional traits representing the 'fast-slow' leaf economics spectrum in driving the diversity-stability relationship. We found that high species richness and phylogenetic diversity stabilize biomass production via enhanced asynchrony in the performance of co-occurring species. Contrary to expectations, low phylogenetic diversity enhances ecosystem stability directly, albeit weakly. While the diversity of fast-slow functional traits has a weak effect on ecosystem stability, communities dominated by slow species enhance ecosystem stability by increasing mean biomass production relative to the standard deviation of biomass over time. Our in-depth, integrative assessment of factors influencing the diversity-stability relationship demonstrates a more multicausal relationship than has been previously acknowledged.

Lost in diversity: the interactions between soil-borne fungi, biodiversity and plant productivity.

There is consensus that plant species richness enhances plant productivity within natural grasslands, but the underlying drivers remain debated. Recently, differential accumulation of soil-borne fungal pathogens across the plant diversity gradient has been proposed as a cause of this pattern. However, the below-ground environment has generally been treated as a 'black box' in biodiversity experiments, leaving these fungi unidentified. Using next generation sequencing and pathogenicity assays, we analysed the community composition of root-associated fungi from a biodiversity experiment to examine if evidence exists for host specificity and negative density dependence in the interplay between soil-borne fungi, plant diversity and productivity. Plant species were colonised by distinct (pathogenic) fungal communities and isolated fungal species showed negative, species-specific effects on plant growth. Moreover, 57% of the pathogenic fungal operational taxonomic units (OTUs) recorded in plant monocultures were not detected in eight plant species plots, suggesting a loss of pathogenic OTUs with plant diversity. Our work provides strong evidence for host specificity and negative density-dependent effects of root-associated fungi on plant species in grasslands. Our work substantiates the hypothesis that fungal root pathogens are an important driver of biodiversity-ecosystem functioning relationships.

Diversity-dependent temporal divergence of ecosystem functioning in experimental ecosystems.

The effects of biodiversity on ecosystem functioning generally increase over time, but the underlying processes remain unclear. Using 26 long-term grassland and forest experimental ecosystems, we demonstrate that biodiversity-ecosystem functioning relationships strengthen mainly by greater increases in functioning in high-diversity communities in grasslands and forests. In grasslands, biodiversity effects also strengthen due to decreases in functioning in low-diversity communities. Contrasting trends across grasslands are associated with differences in soil characteristics.

Taxonomic and functional turnover are decoupled in European peat bogs.

In peatland ecosystems, plant communities mediate a globally significant carbon store. The effects of global environmental change on plant assemblages are expected to be a factor in determining how ecosystem functions such as carbon uptake will respond. Using vegetation data from 56 Sphagnum-dominated peat bogs across Europe, we show that in these ecosystems plant species aggregate into two major clusters that are each defined by shared response to environmental conditions. Across environmental gradients, we find significant taxonomic turnover in both clusters. However, functional identity and functional redundancy of the community as a whole remain unchanged. This strongly suggests that in peat bogs, species turnover across environmental gradients is restricted to functionally similar species. Our results demonstrate that plant taxonomic and functional turnover are decoupled, which may allow these peat bogs to maintain ecosystem functioning when subject to future environmental change.

Root chemistry and soil fauna, but not soil abiotic conditions explain the effects of plant diversity on root decomposition.

Plant diversity influences many ecosystem functions including root decomposition. However, due to the presence of multiple pathways via which plant diversity may affect root decomposition, our mechanistic understanding of their relationships is limited. In a grassland biodiversity experiment, we simultaneously assessed the effects of three pathways-root litter quality, soil biota, and soil abiotic conditions-on the relationships between plant diversity (in terms of species richness and the presence/absence of grasses and legumes) and root decomposition using structural equation modeling. Our final structural equation model explained 70% of the variation in root mass loss. However, different measures of plant diversity included in our model operated via different pathways to alter root mass loss. Plant species richness had a negative effect on root mass loss. This was partially due to increased Oribatida abundance, but was weakened by enhanced root potassium (K) concentration in more diverse mixtures. Equally, grass presence negatively affected root mass loss. This effect of grasses was mostly mediated via increased root lignin concentration and supported via increased Oribatida abundance and decreased root K concentration. In contrast, legume presence showed a net positive effect on root mass loss via decreased root lignin concentration and increased root magnesium concentration, both of which led to enhanced root mass loss. Overall, the different measures of plant diversity had contrasting effects on root decomposition. Furthermore, we found that root chemistry and soil biota but not root morphology or soil abiotic conditions mediated these effects of plant diversity on root decomposition.