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 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.

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.

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.

A global Fine-Root Ecology Database to address below-ground challenges in plant ecology.

Variation and tradeoffs within and among plant traits are increasingly being harnessed by empiricists and modelers to understand and predict ecosystem processes under changing environmental conditions. While fine roots play an important role in ecosystem functioning, fine-root traits are underrepresented in global trait databases. This has hindered efforts to analyze fine-root trait variation and link it with plant function and environmental conditions at a global scale. This Viewpoint addresses the need for a centralized fine-root trait database, and introduces the Fine-Root Ecology Database (FRED, http://roots.ornl.gov) which so far includes > 70 000 observations encompassing a broad range of root traits and also includes associated environmental data. FRED represents a critical step toward improving our understanding of below-ground plant ecology. For example, FRED facilitates the quantification of variation in fine-root traits across root orders, species, biomes, and environmental gradients while also providing a platform for assessments of covariation among root, leaf, and wood traits, the role of fine roots in ecosystem functioning, and the representation of fine roots in terrestrial biosphere models. Continued input of observations into FRED to fill gaps in trait coverage will improve our understanding of changes in fine-root traits across space and time.

Root structure-function relationships in 74 species: evidence of a root economics spectrum related to carbon economy.

Although fine roots are important components of the global carbon cycle, there is limited understanding of root structure-function relationships among species. We determined whether root respiration rate and decomposability, two key processes driving carbon cycling but always studied separately, varied with root morphological and chemical traits, in a coordinated way that would demonstrate the existence of a root economics spectrum (RES). Twelve traits were measured on fine roots (diameter ≤ 2 mm) of 74 species (31 graminoids and 43 herbaceous and dwarf shrub eudicots) collected in three biomes. The findings of this study support the existence of a RES representing an axis of trait variation in which root respiration was positively correlated to nitrogen concentration and specific root length and negatively correlated to the root dry matter content, lignin : nitrogen ratio and the remaining mass after decomposition. This pattern of traits was highly consistent within graminoids but less consistent within eudicots, as a result of an uncoupling between decomposability and morphology, and of heterogeneity of individual roots of eudicots within the fine-root pool. The positive relationship found between root respiration and decomposability is essential for a better understanding of vegetation-soil feedbacks and for improving terrestrial biosphere models predicting the consequences of plant community changes for carbon cycling.

Root biomass, turnover and net primary productivity of a coffee agroforestry system in Costa Rica: effects of soil depth, shade trees, distance to row and coffee age.

Background and Aims In Costa Rica, coffee (Coffea arabica) plants are often grown in agroforests. However, it is not known if shade-inducing trees reduce coffee plant biomass through root competition, and hence alter overall net primary productivity (NPP). We estimated biomass and NPP at the stand level, taking into account deep roots and the position of plants with regard to trees. Methods Stem growth and root biomass, turnover and decomposition were measured in mixed coffee/tree (Erythrina poeppigiana) plantations. Growth ring width and number at the stem base were estimated along with stem basal area on a range of plant sizes. Root biomass and fine root density were measured in trenches to a depth of 4 m. To take into account the below-ground heterogeneity of the agroforestry system, fine root turnover was measured by sequential soil coring (to a depth of 30 cm) over 1 year and at different locations (in full sun or under trees and in rows/inter-rows). Allometric relationships were used to calculate NPP of perennial components, which was then scaled up to the stand level. Key Results Annual ring width at the stem base increased up to 2·5 mm yr-1 with plant age (over a 44-year period). Nearly all (92 %) coffee root biomass was located in the top 1·5 m, and only 8 % from 1·5 m to a depth of 4 m. Perennial woody root biomass was 16 t ha-1 and NPP of perennial roots was 1·3 t ha-1 yr-1. Fine root biomass (0-30 cm) was two-fold higher in the row compared with between rows. Fine root biomass was 2·29 t ha-1 (12 % of total root biomass) and NPP of fine roots was 2·96 t ha-1 yr-1 (69 % of total root NPP). Fine root turnover was 1·3 yr-1 and lifespan was 0·8 years. Conclusions Coffee root systems comprised 49 % of the total plant biomass; such a high ratio is possibly a consequence of shoot pruning. There was no significant effect of trees on coffee fine root biomass, suggesting that coffee root systems are very competitive in the topsoil.

Plant traits and decomposition: are the relationships for roots comparable to those for leaves?

BACKGROUND AND AIMS: Fine root decomposition is an important determinant of nutrient and carbon cycling in grasslands; however, little is known about the factors controlling root decomposition among species. Our aim was to investigate whether interspecific variation in the potential decomposition rate of fine roots could be accounted for by root chemical and morphological traits, life history and taxonomic affiliation. We also investigated the co-ordinated variation in root and leaf traits and potential decomposition rates. METHODS: We analysed potential decomposition rates and the chemical and morphological traits of fine roots on 18 Mediterranean herbaceous species grown in controlled conditions. The results were compared with those obtained for leaves in a previous study conducted on similar species. KEY RESULTS: Differences in the potential decomposition rates of fine roots between species were accounted for by root chemical composition, but not by morphological traits. The root potential decomposition rate varied with taxonomy, but not with life history. Poaceae, with high cellulose concentration and low concentrations of soluble compounds and phosphorus, decomposed more slowly than Asteraceae and Fabaceae. Patterns of root traits, including decomposition rate, mirrored those of leaf traits, resulting in a similar species clustering. CONCLUSIONS: The highly co-ordinated variation of roots and leaves in terms of traits and potential decomposition rate suggests that changes in the functional composition of communities in response to anthropogenic changes will strongly affect biogeochemical cycles at the ecosystem level.

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 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.

The worldwide leaf economics spectrum.

Bringing together leaf trait data spanning 2,548 species and 175 sites we describe, for the first time at global scale, a universal spectrum of leaf economics consisting of key chemical, structural and physiological properties. The spectrum runs from quick to slow return on investments of nutrients and dry mass in leaves, and operates largely independently of growth form, plant functional type or biome. Categories along the spectrum would, in general, describe leaf economic variation at the global scale better than plant functional types, because functional types overlap substantially in their leaf traits. Overall, modulation of leaf traits and trait relationships by climate is surprisingly modest, although some striking and significant patterns can be seen. Reliable quantification of the leaf economics spectrum and its interaction with climate will prove valuable for modelling nutrient fluxes and vegetation boundaries under changing land-use and climate.

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.

Litter quality and decomposability of species from a Mediterranean succession depend on leaf traits but not on nitrogen supply.

BACKGROUND AND AIMS: The rate of plant decomposition depends on both the decomposition environment and the functional traits of the individual species (e.g. leaf and litter quality), but their relative importance in determining interspecific differences in litter decomposition remains unclear. The aims of this study were to: (a) determine if species from different successional stages grown on soils with low and high nitrogen levels produce leaf and litter traits that decompose differently under identical conditions; and (b) assess which trait of living leaves best relates to litter quality and litter decomposability METHODS: The study was conducted on 17 herbaceous species representative of three stages of a Mediterranean successional sere of Southern France. Plants were grown in monocultures in a common garden under two nitrogen levels. To elucidate how different leaf traits affected litter decomposition a microcosm experiment was conducted to determine decomposability under standard conditions. Tests were also carried out to determine how successional stage and nitrogen supply affected functional traits of living leaves and how these traits then modified litter quality and subsequent litter decomposability. KEY RESULTS: The results demonstrated that leaf traits and litter decomposability varied according to species and successional stage. It was also demonstrated that while nitrogen addition affected leaf and litter traits, it had no effect on decomposition rates. Finally, leaf dry matter content stood out as the leaf trait best related to litter quality and litter decomposability CONCLUSIONS: In this study, species litter decomposability was affected by some leaf and litter traits but not by soil nitrogen supply. The results demonstrated the strength of a trait-based approach to predict changes in ecosystem processes as a result of species shifts in ecosystems.

Competition, traits and resource depletion in plant communities.

Although of primary importance to explain plant community structure, general relationships between plant traits, resource depletion and competitive outcomes remain to be quantified across species. Here, we used a comparative approach to test whether instantaneous measurements of plant traits can capture both the amount of resources depleted under plant cover over time (competitive effect) and the way competitors perceived this resource depletion (competitive response). We performed a large competition experiment in which phytometers from a single grass species were transplanted within 18 different monocultures grown in a common-garden experiment, with a time-integrative quantification of light and water depletion over the phytometers' growing season. Resource-capturing traits were measured on both phytometers (competitive response traits) and monocultures (competitive effect traits). The total amounts of depleted light and water availabilities over the season strongly differed among monocultures; they were best estimated by instantaneous measurements of height and rooting depth, respectively, performed when either light or water became limiting. Specific leaf area and leaf water potential, two competitive response traits measured at the leaf level, were good predictors of changes in phytometer performance under competition, and reflected the amount of light and water, respectively, perceived by plants throughout their lifespan. Our results demonstrated the relevance of instantaneous measures of plant traits as indicators of resource depletion over time, validating the trait-based approach for competition ecology.

Leaf life span, dynamics and construction cost of species from Mediterranean old-fields differing in successional status.

• Variations in leaf life span (LLS), construction cost (CC) and dynamics patterns (periods of leaf production, tp , and loss, tL , time lag separating the end of leaf production and the beginning of leaf loss, t) were investigated in species differing in successional status and life forms. We tested how those traits varied along the succession and how these were interrelated. A new graphical framework is proposed to assess the influence of dynamics traits on LLS. • The study was conducted on 42 species of contrasted life forms, typical of various stages of secondary succession, under the Mediterranean climate of southern France. • LLS increased along the succession, tp was shorter and t longer in species from the later stage, without significant change in CC or tL . Herbaceous species, mostly of early successional status, had short-lived, low-CC leaves, produced and lost continuously. Woody species, of later successional status, had long-lived leaves, with slightly higher CC than herbs. LLS and CC or payback time were weakly correlated. • Variations in LLS and leaf dynamics along the succession were related to changes in plant stature and growth potential of species, captured by leaf traits. Whether this is the consequence of a decrease in frequency of disturbance or of a change in the level of resources remains an open question.

Genotypic variation in the response of two perennial grass species to elevated carbon dioxide.

Shoot and reproductive biomass of genotypes of Bromus erectus and Dactylis glomerata grown in competition at ambient and elevated CO2 were examined for 2 consecutive years in order to test whether genetic variation in those traits exists and whether it is maintained over time. At the species level, a positive CO2 response of shoot biomass of both species was only found in the first year of treatment. At the genotype level, no significant CO2×genotype interaction was found at any single harvest either for vegetative or reproductive biomass of either species. Analysis over time, however, indicated that there is a potential for evolutionary adaptation only for D. glomerata: (1) repeated measures ANOVA detected a marginally significant CO2×genotype×time interaction for shoot biomass, because the range of the genotypes CO2 response increased over time; (2) genotypes that displayed the highest response during the first year under elevated CO2 also showed the highest response the second year. Null (B. erectus) or weak (D. glomerata) selective potentials of elevated CO2 were detected in this experiment, but short time series could underestimate this potential with perennial species.

Relating root structure and anatomy to whole-plant functioning in 14 herbaceous Mediterranean species.

This study investigated the relationships between root structure and anatomy and whole-plant functioning in herbaceous species. Fourteen annual and perennial species representative of a Mediterranean old-field succession were grown in monocultures in a common-garden experiment. Whole-plant functioning was assessed by inherent relative growth rate (RGR(max)), measured in standardized conditions, and maximum height (H(max)). Root tissue density (TMD(r)), considered as a major component of root structure, was measured on roots harvested within in-growth cores. Anatomical characteristics were analysed on cross-sectional areas (CSA). TMD(r) was correlated positively with H(max) and negatively with RGR(max). Root CSA explained interspecific variation in H(max) but not that in TMD(r) and RGR(max). Root xylem CSA and xylem proportion in root CSA were positively correlated with TMD(r) and H(max) and negatively with RGR(max). Mean xylem vessel CSA did not account for variations in TMD(r), H(max) and RGR(max). These results suggested that RGR(max) and H(max) are constrained by opposite root structural and anatomical traits, which have potential links with hydraulic conductance, support and longevity.

Assessing the effects of land-use change on plant traits, communities and ecosystem functioning in grasslands: a standardized methodology and lessons from an application to 11 European sites.

BACKGROUND AND AIMS: A standardized methodology to assess the impacts of land-use changes on vegetation and ecosystem functioning is presented. It assumes that species traits are central to these impacts, and is designed to be applicable in different historical, climatic contexts and local settings. Preliminary results are presented to show its applicability. METHODS: Eleven sites, representative of various types of land-use changes occurring in marginal agro-ecosystems across Europe and Israel, were selected. Climatic data were obtained at the site level; soil data, disturbance and nutrition indices were described at the plot level within sites. Sixteen traits describing plant stature, leaf characteristics and reproductive phase were recorded on the most abundant species of each treatment. These data were combined with species abundance to calculate trait values weighed by the abundance of species in the communities. The ecosystem properties selected were components of above-ground net primary productivity and decomposition of litter. KEY RESULTS: The wide variety of land-use systems that characterize marginal landscapes across Europe was reflected by the different disturbance indices, and were also reflected in soil and/or nutrient availability gradients. The trait toolkit allowed us to describe adequately the functional response of vegetation to land-use changes, but we suggest that some traits (vegetative plant height, stem dry matter content) should be omitted in studies involving mainly herbaceous species. Using the example of the relationship between leaf dry matter content and above-ground dead material, we demonstrate how the data collected may be used to analyse direct effects of climate and land use on ecosystem properties vs. indirect effects via changes in plant traits. CONCLUSIONS: This work shows the applicability of a set of protocols that can be widely applied to assess the impacts of global change drivers on species, communities and ecosystems.