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.

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.

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.

Higher biomass partitioning to absorptive roots improves needle nutrition but does not alleviate stomatal limitation of northern Scots pine.

Harsh environmental conditions affect both leaf structure and root traits. However, shoot growth in high-latitude systems is predominately under photoperiod control while root growth may occur for as long as thermal conditions are favorable. The different sensitivities of these organs may alter functional relationships above- and belowground along environmental gradients. We examined the relationship between absorptive root and foliar traits of Scots pine trees growing in situ along a temperate-boreal transect and in trees grown in a long-term common garden at a temperate latitude. We related changes in foliar nitrogen, phosphorus, specific leaf area, needle mass and 13 C signatures to geographic trends in absorptive root biomass to better understand patterns of altered tree nutrition and water balance. Increased allocation to absorptive fine roots was associated with greater uptake of soil nutrients and subsequently higher needle nutrient contents in the northern provenances compared with more southern provenances when grown together in a common garden setting. In contrast, the leaf δ13 C in northern and southern provenances were similar within the common garden suggesting that higher absorptive root biomass fractions could not adequately increase water supply in warmer climates. These results highlight the importance of allocation within the fine-root system and its impacts on needle nutrition while also suggesting increasing stomatal limitation of photosynthesis in the context of anticipated climatic changes.

Fine-root functional trait responses to experimental warming: a global meta-analysis.

Whether and how warming alters functional traits of absorptive plant roots remains to be answered across the globe. Tackling this question is crucial to better understanding terrestrial responses to climate change as fine-root traits drive many ecosystem processes. We carried out a detailed synthesis of fine-root trait responses to experimental warming by performing a meta-analysis of 964 paired observations from 177 publications. Warming increased fine-root biomass, production, respiration and nitrogen concentration as well as decreased root carbon : nitrogen ratio and nonstructural carbohydrates. Warming effects on fine-root biomass decreased with greater warming magnitude, especially in short-term experiments. Furthermore, the positive effect of warming on fine-root biomass was strongest in deeper soil horizons and in colder and drier regions. Total fine-root length, morphology, mortality, life span and turnover were unresponsive to warming. Our results highlight the significant changes in fine-root traits in response to warming as well as the importance of warming magnitude and duration in understanding fine-root responses. These changes have strong implications for global soil carbon stocks in a warmer world associated with increased root-derived carbon inputs into deeper soil horizons and increases in fine-root respiration.

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.

Climate and phylogenetic history structure morphological and architectural trait variation among fine-root orders.

Fine roots mediate below-ground resource acquisition, yet understanding of how fine-root functional traits vary along environmental gradients, within branching orders and across phylogenetic scales remains limited. Morphological and architectural fine-root traits were measured on individual root orders of 20 oak species (genus Quercus) from divergent climates of origin that were harvested after three growing seasons in a glasshouse. These were then compared with similar measurements obtained from a phylogenetically diverse dataset of woody species from the Fine-Root Ecology Database (FRED). For the oaks, only precipitation seasonality and growing season moisture availability were correlated to aspects of root diameter and branching. Strong correlations among root diameters and architecture of different branch orders were common, while correlations between diameter and length were weakly negative. By contrast, the FRED dataset showed strong positive correlations between diameter and length and fewer correlations between root diameter and architectural traits. Our findings suggest that seasonal patterns of water availability are more important drivers of root adaptation in oaks than annual averages in precipitation and temperature. Furthermore, contrasting patterns of trait relationships between the oak and FRED datasets suggest that branching patterns are differentially constrained at narrow vs broad phylogenetic scales.

Physical and Functional Constraints on Viable Belowground Acquisition Strategies.

Since their emergence onto land, terrestrial plants have developed diverse strategies to acquire soil resources. However, we lack a framework that adequately captures how these strategies vary among species. Observations from around the world now allow us to quantify the variation observed in commonly-measured fine-root traits but it is unclear how root traits are interrelated and whether they fall along an "economic" spectrum of acquisitive to conservative strategies. We assessed root trait variation and mycorrhizal colonization rates by leveraging the largest global database of fine-root traits (the Fine-Root Ecology Database; FRED). We also developed a heuristic model to explore the role of mycorrhizal fungi in defining belowground exploration efficiency across a gradient of thin- to thick-diameter roots. In support of the expectations of the "root economic spectrum," we found that root diameter was negatively related to specific root length (Pearson's r=-0.76). However, we found an unexpected negative relationship between root diameter and root tissue density (Pearson's r = -0.40), and we further observed that root nitrogen content was largely unrelated to other economic traits. Mycorrhizal colonization was most closely associated with root diameter (Pearson's r = 0.62) and was unrelated to root tissue density and root nitrogen. The heuristic model demonstrated that while thinner roots have inherently greater capacity to encounter soil resources based on higher surface area per unit mass, the potential for increased associations with mycorrhizal fungi in thicker roots, combined with greater hyphal growth, can result in equally acquisitive strategies for both thin- and thick roots. Taken together, our assessments of root trait variation, trade-offs with mycorrhizal fungi, and broader connections to root longevity allowed us to propose a series of fundamental constraints on belowground resource acquisition strategies. Physical tradeoffs based on root construction (i.e., economic traits) and functional limitations related to the capacity of a root to encounter and acquire soil resources combine to limit the two-dimensional belowground trait space. Within this trait space there remains a diversity of additional variation in root traits that facilitates a wide range of belowground resource acquisition strategies.

Intraspecific Fine-Root Trait-Environment Relationships across Interior Douglas-Fir Forests of Western Canada.

Variation in resource acquisition strategies enables plants to adapt to different environments and may partly determine their responses to climate change. However, little is known about how belowground plant traits vary across climate and soil gradients. Focusing on interior Douglas-fir (Pseudotsuga menziesii var. glauca) in western Canada, we tested whether fine-root traits relate to the environment at the intraspecific level. We quantified the variation in commonly measured functional root traits (morphological, chemical, and architectural traits) among the first three fine-root orders (i.e., absorptive fine roots) and across biogeographic gradients in climate and soil factors. Moderate but consistent trait-environment linkages occurred across populations of Douglas-fir, despite high levels of within-site variation. Shifts in morphological traits across regions were decoupled from those in chemical traits. Fine roots in colder/drier climates were characterized by a lower tissue density, higher specific area, larger diameter, and lower carbon-to-nitrogen ratio than those in warmer/wetter climates. Our results showed that Douglas-fir fine roots do not rely on adjustments in architectural traits to adapt rooting strategies in different environments. Intraspecific fine-root adjustments at the regional scale do not fit along a single axis of root economic strategy and are concordant with an increase in root acquisitive potential in colder/drier environments.

Author Correction: Evolutionary history resolves global organization of root functional traits.

We thank reader Joseph Craine for pointing out three inadvertent errors in this Letter. First, 4 of the 71 divergence dates extracted from ref. 1 of this Amendment and used in Fig. 1b of the original Letter were overestimated. The correct values are 45 million years ago (Ma) for Apocynaceae, 51 Ma for Anacardiaceae, 40 Ma for Primulaceae, and 53 Ma for Amaryllidaceae. These errors had little influence on the overall trend of Fig. 1b (r2 is now 0.48 rather than 0.54, with no change to P < 0.001) and do not change our conclusion and inferences. Second, we neglected to note that since refs. 1 and 2 of this Amendment considered only angiosperms, our Fig. 1b necessarily did not include gymnosperm taxa. The in-text reference to Fig. 1b should therefore read "all major angiosperm plant families in our dataset" rather than "all major vascular plant families in our dataset". Third, in Fig. 1c the trait value of mycorrhizal colonization for Machilus kwangtungensis was erroneously given the value 0.25 instead of 1.0. This error had little influence on the overall Fig. 1c trend, reducing r2 from 0.64 to 0.63 (with no change to P < 0.001).

How are nitrogen availability, fine-root mass, and nitrogen uptake related empirically? Implications for models and theory.

Understanding the effects of global change in terrestrial communities requires an understanding of how limiting resources interact with plant traits to affect productivity. Here, we focus on nitrogen and ask whether plant community nitrogen uptake rate is determined (a) by nitrogen availability alone or (b) by the product of nitrogen availability and fine-root mass. Surprisingly, this is not empirically resolved. We performed controlled microcosm experiments and reanalyzed published pot experiments and field data to determine the relationship between community-level nitrogen uptake rate, nitrogen availability, and fine-root mass for 46 unique combinations of species, nitrogen levels, and growing conditions. We found that plant community nitrogen uptake rate was unaffected by fine-root mass in 63% of cases and saturated with fine-root mass in 29% of cases (92% in total). In contrast, plant community nitrogen uptake rate was clearly affected by nitrogen availability. The results support the idea that although plants may over-proliferate fine roots for individual-level competition, it comes without an increase in community-level nitrogen uptake. The results have implications for the mechanisms included in coupled carbon-nitrogen terrestrial biosphere models (CN-TBMs) and are consistent with CN-TBMs that operate above the individual scale and omit fine-root mass in equations of nitrogen uptake rate but inconsistent with the majority of CN-TBMs, which operate above the individual scale and include fine-root mass in equations of nitrogen uptake rate. For the much smaller number of CN-TBMs that explicitly model individual-based belowground competition for nitrogen, the results suggest that the relative (not absolute) fine-root mass of competing individuals should be included in the equations that determine individual-level nitrogen uptake rates. By providing empirical data to support the assumptions used in CN-TBMs, we put their global climate change predictions on firmer ground.

Fine-root traits are linked to species dynamics in a successional plant community.

Despite the importance of fine roots for the acquisition of soil resources such as nitrogen and water, the study of linkages between traits and both population and community dynamics remains focused on aboveground traits. We address this gap by investigating associations between belowground traits and metrics of species dynamics. Our analysis included 85 species from a long-term data set on the transition from old field to forest in eastern North America (the Buell-Small Succession Study) and the new Fine-Root Ecology Database. Given the prominent roles of life form (woody vs. non-woody) and species origin (native vs. exotic) in defining functional relationships, we also assessed whether traits or their relationships with species dynamics differed for these groups. Species that reached their peak abundance early in succession had fine-root traits corresponding to resource acquisitive strategies (i.e., they were thinner, less dense, and had higher nitrogen concentrations) while species that peaked progressively later had increasingly conservative strategies. In addition to having more acquisitive root traits than native species, exotics diverged from the above successional trend, having consistently thinner fine roots regardless of the community context. Species with more acquisitive fine-root morphologies typically had faster rates of abundance increase and achieved their maximal rates in fewer years. Decreasing soil nutrient availability and increasing belowground competition may become increasingly strong filters in successional communities, acting on root traits to promote a transition from acquisitive to conservative foraging. However, disturbances that increase light and soil resource availability at local scales may allow acquisitive species, especially invasive exotics, to continue colonizing late into the community transition to forest.

Mechanical traits of fine roots as a function of topology and anatomy.

Background and Aims: Root mechanical traits, including tensile strength (Tr), tensile strain (εr) and modulus of elasticity (Er), are key functional traits that help characterize plant anchorage and the physical contribution of vegetation to landslides and erosion. The variability in these traits is high among tree fine roots and is poorly understood. Here, we explore the variation in root mechanical traits as well as their underlying links with morphological (diameter), architectural (topological order) and anatomical (stele and cortex sizes) traits. Methods: We investigated the four tropical tree species Pometia tomentosa, Barringtonia fusicarpa, Baccaurea ramiflora and Pittosporopsis kerrii in Xishuangbanna, Yunnan, China. For each species, we excavated intact, fresh, fine roots and measured mechanical and anatomical traits for each branching order. Key Results: Mechanical traits varied enormously among the four species within a narrow range of diameters (<2 mm): <0.1-65 MPa for Tr, 4-1135 MPa for Er and 0.4-37 % for εr. Across species, Tr and Er were strongly correlated with stele area ratio, which was also better correlated with topological order than with root diameter, especially at interspecific levels. Conclusions: Root topological order plays an important role in explaining variability in fine-root mechanical traits due to its reflection of root tissue development. Accounting for topological order when measuring fine-root traits therefore leads to greater empirical understanding of plant functions (e.g. anchorage) within and across species.

Erratum: Evolutionary history resolves global organization of root functional traits.

This corrects the article DOI: 10.1038/nature25783.