Linking fine root lifespan to root chemical and morphological traits-A global analysis.

Fine root lifespan is a critical trait associated with contrasting root strategies of resource acquisition and protection. Yet, its position within the multidimensional "root economics space" synthesizing global root economics strategies is largely uncertain, and it is rarely represented in frameworks integrating plant trait variations. Here, we compiled the most comprehensive dataset of absorptive median root lifespan (MRL) data including 98 observations from 79 woody species using (mini-)rhizotrons across 40 sites and linked MRL to other plant traits to address questions of the regulators of MRL at large spatial scales. We demonstrate that MRL not only decreases with plant investment in root nitrogen (associated with more metabolically active tissues) but also increases with construction of larger diameter roots which is often associated with greater plant reliance on mycorrhizal symbionts. Although theories linking organ structure and function suggest that root traits should play a role in modulating MRL, we found no correlation between root traits associated with structural defense (root tissue density and specific root length) and MRL. Moreover, fine root and leaf lifespan were globally unrelated, except among evergreen species, suggesting contrasting evolutionary selection between leaves and roots facing contrasting environmental influences above vs. belowground. At large geographic scales, MRL was typically longer at sites with lower mean annual temperature and higher mean annual precipitation. Overall, this synthesis uncovered several key ecophysiological covariates and environmental drivers of MRL, highlighting broad avenues for accurate parametrization of global biogeochemical models and the understanding of ecosystem response to global climate change.

Coevolutionary legacies for plant decomposition.

Coevolution has driven speciation and evolutionary novelty in functional traits across the Tree of Life. Classic coevolutionary syndromes such as plant-pollinator, plant-herbivore, and host-parasite have focused strongly on the fitness consequences during the lifetime of the interacting partners. Less is known about the consequences of coevolved traits for ecosystem-level processes, in particular their 'afterlife' legacies for litter decomposition, nutrient cycling, and the functional ecology of decomposers. We review the mechanisms by which traits resulting from coevolution between plants and their consumers, microbial symbionts, or humans, and between microbial decomposers and invertebrates, drive plant litter decomposition pathways and rates. This supports the idea that much of current global variation in the decomposition of plant material is a legacy of coevolution.

Mycorrhizal symbiosis pathway and edaphic fertility frame root economics space among tree species.

The root economics space (RES) is multidimensional and largely shaped by belowground biotic and abiotic influences. However, how root-fungal symbioses and edaphic fertility drive this complexity remains unclear. Here, we measured absorptive root traits of 112 tree species in temperate and subtropical forests of China, including traits linked to functional differences between arbuscular mycorrhizal (AM) and ectomycorrhizal (ECM) hosts. Our data, from known mycorrhizal tree species, revealed a 'fungal-symbiosis' dimension distinguishing AM from ECM species. This divergence likely resulted from the contrasting mycorrhizal evolutionary development of AM vs ECM associations. Increased root tissue cortical space facilitates AM symbiosis, whereas increased root branching favours ECM symbiosis. Irrespective of mycorrhizal type, a 'root-lifespan' dimension reflecting aspects of root construction cost and defence was controlled by variation in specific root length and root tissue density, which was fully independent of root nitrogen content. Within this function-based RES, we observed a substantial covariation of axes with soil phosphorus and nitrate levels, highlighting the role played by these two axes in nutrient acquisition and conservation. Overall, our findings demonstrate the importance of evolved mycorrhizal symbiosis pathway and edaphic fertility in framing the RES, and provide theoretical and mechanistic insights into the complexity of root economics.

RhizoVision Explorer: open-source software for root image analysis and measurement standardization.

Roots are central to the function of natural and agricultural ecosystems by driving plant acquisition of soil resources and influencing the carbon cycle. Root characteristics like length, diameter and volume are critical to measure to understand plant and soil functions. RhizoVision Explorer is an open-source software designed to enable researchers interested in roots by providing an easy-to-use interface, fast image processing and reliable measurements. The default broken roots mode is intended for roots sampled from pots and soil cores, washed and typically scanned on a flatbed scanner, and provides measurements like length, diameter and volume. The optional whole root mode for complete root systems or root crowns provides additional measurements such as angles, root depth and convex hull. Both modes support providing measurements grouped by defined diameter ranges, the inclusion of multiple regions of interest and batch analysis. RhizoVision Explorer was successfully validated against ground truth data using a new copper wire image set. In comparison, the current reference software, the commercial WinRhizo™, drastically underestimated volume when wires of different diameters were in the same image. Additionally, measurements were compared with WinRhizo™ and IJ_Rhizo using a simulated root image set, showing general agreement in software measurements, except for root volume. Finally, scanned root image sets acquired in different labs for the crop, herbaceous and tree species were used to compare results from RhizoVision Explorer with WinRhizo™. The two software showed general agreement, except that WinRhizo™ substantially underestimated root volume relative to RhizoVision Explorer. In the current context of rapidly growing interest in root science, RhizoVision Explorer intends to become a reference software, improve the overall accuracy and replicability of root trait measurements and provide a foundation for collaborative improvement and reliable access to all.

A starting guide to root ecology: strengthening ecological concepts and standardising root classification, sampling, processing and trait measurements.

In the context of a recent massive increase in research on plant root functions and their impact on the environment, root ecologists currently face many important challenges to keep on generating cutting-edge, meaningful and integrated knowledge. Consideration of the below-ground components in plant and ecosystem studies has been consistently called for in recent decades, but methodology is disparate and sometimes inappropriate. This handbook, based on the collective effort of a large team of experts, will improve trait comparisons across studies and integration of information across databases by providing standardised methods and controlled vocabularies. It is meant to be used not only as starting point by students and scientists who desire working on below-ground ecosystems, but also by experts for consolidating and broadening their views on multiple aspects of root ecology. Beyond the classical compilation of measurement protocols, we have synthesised recommendations from the literature to provide key background knowledge useful for: (1) defining below-ground plant entities and giving keys for their meaningful dissection, classification and naming beyond the classical fine-root vs coarse-root approach; (2) considering the specificity of root research to produce sound laboratory and field data; (3) describing typical, but overlooked steps for studying roots (e.g. root handling, cleaning and storage); and (4) gathering metadata necessary for the interpretation of results and their reuse. Most importantly, all root traits have been introduced with some degree of ecological context that will be a foundation for understanding their ecological meaning, their typical use and uncertainties, and some methodological and conceptual perspectives for future research. Considering all of this, we urge readers not to solely extract protocol recommendations for trait measurements from this work, but to take a moment to read and reflect on the extensive information contained in this broader guide to root ecology, including sections I-VII and the many introductions to each section and root trait description. Finally, it is critical to understand that a major aim of this guide is to help break down barriers between the many subdisciplines of root ecology and ecophysiology, broaden researchers' views on the multiple aspects of root study and create favourable conditions for the inception of comprehensive experiments on the role of roots in plant and ecosystem functioning.

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.

Agroecosystem diversification with legumes or non-legumes improves differently soil fertility according to soil type.

Plant diversification through crop rotation or agroforestry is a promising way to improve sustainability of agroecosystems. Nonetheless, criteria to select the most suitable plant communities for agroecosystems diversification facing contrasting environmental constraints need to be refined. Here, we compared the impacts of 24 different plant communities on soil fertility across six tropical agroecosystems: either on highly weathered Ferralsols, with strong P limitation, or on partially weathered soils derived from volcanic material, with major N limitation. In each agroecosystem, we tested several plant communities for diversification, as compared to a matching low diversity management for their cropping system. Plant residue restitution, N, P and lignin contents were measured for each plant community. In parallel, the soil under each community was analyzed for organic C and N, inorganic N, Olsen P, soil pH and nematode community composition. Soil potential fertility was assessed with plant bioassays under greenhouse controlled climatic conditions. Overall, plant diversification had a positive effect on soil fertility across all sites, with contrasting effects depending on soil type and legumes presence in the community. Communities with legumes improved soil fertility indicators of volcanic soils, which was demonstrated through significantly higher plant biomass production in the bioassays (+18%) and soil inorganic N (+26%) compared to the low diversity management. Contrastingly, communities without legumes were the most beneficial in Ferralsols, with increases in plant biomass production in the bioassays (+39%), soil Olsen P (+46%), soil C (+26%), and pH (+5%). Piecewise structural equation models with Shipley's test revealed that plant diversification impacts on volcanic soil fertility were related to soil N availability, driven by litter N. Meanwhile, Ferralsols fertility was related to soil P availability, driven by litter P. These findings underline the importance of multifactorial and multi-sites experiments to inform trait-based frameworks used in designing optimal plant diversification in agroecological systems.

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.

Home-field advantage of litter decomposition: from the phyllosphere to the soil.

Plants often associate with specialized decomposer communities that increase plant litter breakdown, a phenomenon that is known as the 'home-field advantage' (HFA). Although the concept of HFA has long considered only the role of the soil microbial community, explicit consideration of the role of the microbial community on the foliage before litter fall (i.e. the phyllosphere community) may help us to better understand HFA. We investigated the occurrence of HFA in the presence vs absence of phyllosphere communities and found that HFA effects were smaller when phyllosphere communities were removed. We propose that priority effects and interactions between phyllosphere and soil organisms can help explain the positive effects of the phyllosphere at home, and suggest a path forward for further investigation.

Shifts in soil and plant functional diversity along an altitudinal gradient in the French Alps.

OBJECTIVES: Altitude integrates changes in environmental conditions that determine shifts in vegetation, including temperature, precipitation, solar radiation and edaphogenetic processes. In turn, vegetation alters soil biophysical properties through litter input, root growth, microbial and macrofaunal interactions. The belowground traits of plant communities modify soil processes in different ways, but it is not known how root traits influence soil biota at the community level. We collected data to investigate how elevation affects belowground community traits and soil microbial and faunal communities. This dataset comprises data from a temperate climate in France and a twin study was performed in a tropical zone in Mexico. DATA DESCRIPTION: The paper describes soil physical and chemical properties, climatic variables, plant community composition and species abundance, plant community traits, soil microbial functional diversity and macrofaunal abundance and diversity. Data are provided for six elevations (1400-2400 m) ranging from montane forest to alpine prairie. We focused on soil biophysical properties beneath three dominant plant species that structure local vegetation. These data are useful for understanding how shifts in vegetation communities affect belowground processes, such as water infiltration, soil aggregation and carbon storage. Data will also help researchers understand how plant communities adjust to a changing climate/environment.

Root traits as drivers of plant and ecosystem functioning: current understanding, pitfalls and future research needs.

The effects of plants on the biosphere, atmosphere and geosphere are key determinants of terrestrial ecosystem functioning. However, despite substantial progress made regarding plant belowground components, we are still only beginning to explore the complex relationships between root traits and functions. Drawing on the literature in plant physiology, ecophysiology, ecology, agronomy and soil science, we reviewed 24 aspects of plant and ecosystem functioning and their relationships with a number of root system traits, including aspects of architecture, physiology, morphology, anatomy, chemistry, biomechanics and biotic interactions. Based on this assessment, we critically evaluated the current strengths and gaps in our knowledge, and identify future research challenges in the field of root ecology. Most importantly, we found that belowground traits with the broadest importance in plant and ecosystem functioning are not those most commonly measured. Also, the estimation of trait relative importance for functioning requires us to consider a more comprehensive range of functionally relevant traits from a diverse range of species, across environments and over time series. We also advocate that establishing causal hierarchical links among root traits will provide a hypothesis-based framework to identify the most parsimonious sets of traits with the strongest links on functions, and to link genotypes to plant and ecosystem functioning.

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.

A multitrophic perspective on biodiversity-ecosystem functioning research.

Concern about the functional consequences of unprecedented loss in biodiversity has prompted biodiversity-ecosystem functioning (BEF) research to become one of the most active fields of ecological research in the past 25 years. Hundreds of experiments have manipulated biodiversity as an independent variable and found compelling support that the functioning of ecosystems increases with the diversity of their ecological communities. This research has also identified some of the mechanisms underlying BEF relationships, some context-dependencies of the strength of relationships, as well as implications for various ecosystem services that mankind depends upon. In this paper, we argue that a multitrophic perspective of biotic interactions in random and non-random biodiversity change scenarios is key to advance future BEF research and to address some of its most important remaining challenges. We discuss that the study and the quantification of multitrophic interactions in space and time facilitates scaling up from small-scale biodiversity manipulations and ecosystem function assessments to management-relevant spatial scales across ecosystem boundaries. We specifically consider multitrophic conceptual frameworks to understand and predict the context-dependency of BEF relationships. Moreover, we highlight the importance of the eco-evolutionary underpinnings of multitrophic BEF relationships. We outline that FAIR data (meeting the standards of findability, accessibility, interoperability, and reusability) and reproducible processing will be key to advance this field of research by making it more integrative. Finally, we show how these BEF insights may be implemented for ecosystem management, society, and policy. Given that human well-being critically depends on the multiple services provided by diverse, multitrophic communities, integrating the approaches of evolutionary ecology, community ecology, and ecosystem ecology in future BEF research will be key to refine conservation targets and develop sustainable management strategies.

Allocation, morphology, physiology, architecture: the multiple facets of plant above- and below-ground responses to resource stress.

Plants respond to resource stress by changing multiple aspects of their biomass allocation, morphology, physiology and architecture. To date, we lack an integrated view of the relative importance of these plastic responses in alleviating resource stress and of the consistency/variability of these responses among species. We subjected nine species (legumes, forbs and graminoids) to nitrogen and/or light shortages and measured 11 above-ground and below-ground trait adjustments critical in the alleviation of these stresses (plus several underlying traits). Nine traits out of 11 showed adjustments that improved plants' potential capacity to acquire the limiting resource at a given time. Above ground, aspects of plasticity in allocation, morphology, physiology and architecture all appeared important in improving light capture, whereas below ground, plasticity in allocation and physiology were most critical to improving nitrogen acquisition. Six traits out of 11 showed substantial heterogeneity in species plasticity, with little structuration of these differences within trait covariation syndromes. Such comprehensive assessment of the complex nature of phenotypic responses of plants to multiple stress factors, and the comparison of plant responses across multiple species, makes a clear case for the high (but largely overlooked) diversity of potential plastic responses of plants, and for the need to explore the potential rules structuring them.

Genotypic variability enhances the reproducibility of an ecological study.

Many scientific disciplines are currently experiencing a 'reproducibility crisis' because numerous scientific findings cannot be repeated consistently. A novel but controversial hypothesis postulates that stringent levels of environmental and biotic standardization in experimental studies reduce reproducibility by amplifying the impacts of laboratory-specific environmental factors not accounted for in study designs. A corollary to this hypothesis is that a deliberate introduction of controlled systematic variability (CSV) in experimental designs may lead to increased reproducibility. To test this hypothesis, we had 14 European laboratories run a simple microcosm experiment using grass (Brachypodium distachyon L.) monocultures and grass and legume (Medicago truncatula Gaertn.) mixtures. Each laboratory introduced environmental and genotypic CSV within and among replicated microcosms established in either growth chambers (with stringent control of environmental conditions) or glasshouses (with more variable environmental conditions). The introduction of genotypic CSV led to 18% lower among-laboratory variability in growth chambers, indicating increased reproducibility, but had no significant effect in glasshouses where reproducibility was generally lower. Environmental CSV had little effect on reproducibility. Although there are multiple causes for the 'reproducibility crisis', deliberately including genetic variability may be a simple solution for increasing the reproducibility of ecological studies performed under stringently controlled environmental conditions.

A test of the hierarchical model of litter decomposition.

Our basic understanding of plant litter decomposition informs the assumptions underlying widely applied soil biogeochemical models, including those embedded in Earth system models. Confidence in projected carbon cycle-climate feedbacks therefore depends on accurate knowledge about the controls regulating the rate at which plant biomass is decomposed into products such as CO2. Here we test underlying assumptions of the dominant conceptual model of litter decomposition. The model posits that a primary control on the rate of decomposition at regional to global scales is climate (temperature and moisture), with the controlling effects of decomposers negligible at such broad spatial scales. Using a regional-scale litter decomposition experiment at six sites spanning from northern Sweden to southern France-and capturing both within and among site variation in putative controls-we find that contrary to predictions from the hierarchical model, decomposer (microbial) biomass strongly regulates decomposition at regional scales. Furthermore, the size of the microbial biomass dictates the absolute change in decomposition rates with changing climate variables. Our findings suggest the need for revision of the hierarchical model, with decomposers acting as both local- and broad-scale controls on litter decomposition rates, necessitating their explicit consideration in global biogeochemical models.

A worldview of root traits: the influence of ancestry, growth form, climate and mycorrhizal association on the functional trait variation of fine-root tissues in seed plants.

Fine-root traits play key roles in ecosystem processes, but the drivers of fine-root trait diversity remain poorly understood. The plant economic spectrum (PES) hypothesis predicts that leaf and root traits evolved in coordination. Mycorrhizal association type, plant growth form and climate may also affect root traits. However, the extent to which these controls are confounded with phylogenetic structuring remains unclear. Here we compiled information about root and leaf traits for > 600 species. Using phylogenetic relatedness, climatic ranges, growth form and mycorrhizal associations, we quantified the importance of these factors in the global distribution of fine-root traits. Phylogenetic structuring accounts for most of the variation for all traits excepting root tissue density, with root diameter and nitrogen concentration showing the strongest phylogenetic signal and specific root length showing intermediate values. Climate was the second most important factor, whereas mycorrhizal type had little effect. Substantial trait coordination occurred between leaves and roots, but the strength varied between growth forms and clades. Our analyses provide evidence that the integration of roots and leaves in the PES requires better accounting of the variation in traits across phylogenetic clades. Inclusion of phylogenetic information provides a powerful framework for predictions of belowground functional traits at global scales.