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.

Toward a coordinated understanding of hydro-biogeochemical root functions in tropical forests for application in vegetation models.

Tropical forest root characteristics and resource acquisition strategies are underrepresented in vegetation and global models, hampering the prediction of forest-climate feedbacks for these carbon-rich ecosystems. Lowland tropical forests often have globally unique combinations of high taxonomic and functional biodiversity, rainfall seasonality, and strongly weathered infertile soils, giving rise to distinct patterns in root traits and functions compared with higher latitude ecosystems. We provide a roadmap for integrating recent advances in our understanding of tropical forest belowground function into vegetation models, focusing on water and nutrient acquisition. We offer comparisons of recent advances in empirical and model understanding of root characteristics that represent important functional processes in tropical forests. We focus on: (1) fine-root strategies for soil resource exploration, (2) coupling and trade-offs in fine-root water vs nutrient acquisition, and (3) aboveground-belowground linkages in plant resource acquisition and use. We suggest avenues for representing these extremely diverse plant communities in computationally manageable and ecologically meaningful groups in models for linked aboveground-belowground hydro-nutrient functions. Tropical forests are undergoing warming, shifting rainfall regimes, and exacerbation of soil nutrient scarcity caused by elevated atmospheric CO2. The accurate model representation of tropical forest functions is crucial for understanding the interactions of this biome with the climate.

Las características de las raíces de los bosques tropicales y las estrategias de adquisición de recursos están subrepresentadas en modelos de vegetación, lo que dificulta la predicción del efecto de cambio de clima para estos ecosistemas ricos en carbono. Los bosques tropicales a menudo tienen combinaciones únicas a nivel mundial de alta biodiversidad taxonómica y funcional, estacionalidad de precipitación, y suelos infértiles, dando lugar a patrones distintos en los rasgos y funciones de las raíces en comparación con los ecosistemas de latitudes más altas. Integramos los avances recientes en nuestra comprensión de la función subterránea de los bosques tropicales en modelos de vegetación, centrándonos en la adquisición de agua y nutrientes. Ofrecemos comparaciones de avances recientes en la comprensión empírica y de modelos de las características de las raíces que representan procesos funcionales importantes en los bosques tropicales. Nos centramos en: (1) estrategias de raíces finas para adquisición de recursos del suelo, (2) acoplamiento y compensaciones entre adquisición del agua y de nutrientes, y (3) vínculos entre funciones sobre tierra y debajo del superficie en bosques tropicales. Sugerimos vías para representar estas comunidades de plantas extremadamente diversas en grupos computacionalmente manejables y ecológicamente significativos en modelos. Los bosques tropicales se están calentando, tienen cambios en los regímenes de lluvias, y tienen una exacerbación de la escasez de nutrientes del suelo causada por el elevado CO2 atmosférico. La representación precisa de las funciones de los bosques tropicales en modelos es crucial para comprender las interacciones de este bioma con el clima.

Root-associated fungal communities are influenced more by soils than by plant-host root traits in a Chinese tropical forest.

Forest fungal communities are shaped by the interactions between host tree root systems and the associated soil conditions. We investigated how the soil environment, root morphological traits, and root chemistry influence root-inhabiting fungal communities in three tropical forest sites of varying successional status in Xishuangbanna, China. For 150 trees of 66 species, we measured root morphology and tissue chemistry. Tree species identity was confirmed by sequencing rbcL, and root-associated fungal (RAF) communities were determined using high-throughput ITS2 sequencing. Using distance-based redundancy analysis and hierarchical variation partitioning, we quantified the relative importance of two soil variables (site average total phosphorus and available phosphorus), four root traits (dry matter content, tissue density, specific tip abundance, and forks), and three root tissue elemental concentrations (nitrogen, calcium, and manganese) on RAF community dissimilarity. The root and soil environment collectively explained 23% of RAF compositional variation. Soil phosphorus explained 76% of that variation. Twenty fungal taxa differentiated RAF communities among the three sites. Soil phosphorus most strongly affects RAF assemblages in this tropical forest. Variation in root calcium and manganese concentrations and root morphology among tree hosts, principally an architectural trade-off between dense, highly branched vs less-dense, herringbone-type root systems, are important secondary determinants.

Characterizing natural variability of lignin abundance and composition in fine roots across temperate trees: a comparison of analytical methods.

Lignin is an important root chemical component that is widely used in biogeochemical models to predict root decomposition. Across ecological studies, lignin abundance has been characterized using both proximate and lignin-specific methods, without much understanding of their comparability. This uncertainty in estimating lignin limits our ability to comprehend the mechanisms regulating root decomposition and to integrate lignin data for large-scale syntheses. We compared five methods of estimating lignin abundance and composition in fine roots across 34 phylogenetically diverse tree species. We also assessed the feasibility of high-throughput techniques for fast-screening of root lignin. Although acid-insoluble fraction (AIF) has been used to infer root lignin and decomposition, AIF-defined lignin content was disconnected from the lignin abundance estimated by techniques that specifically measure lignin-derived monomers. While lignin-specific techniques indicated lignin contents of 2-10% (w/w) in roots, AIF-defined lignin contents were c. 5-10-fold higher, and their interspecific variation was found to be largely unrelated to that determined using lignin-specific techniques. High-throughput pyrolysis-gas chromatography-mass spectrometry, when combined with quantitative modeling, accurately predicted lignin abundance and composition, highlighting its feasibility for quicker assessment of lignin in roots. We demonstrate that AIF should be interpreted separately from lignin in fine roots as its abundance is unrelated to that of lignin polymers. This study provides the basis for informed decision-making with respect to lignin methodology in ecology.

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.

Coordination between compound-specific chemistry and morphology in plant roots aligns with ancestral mycorrhizal association in woody angiosperms.

Recent studies on fine root functional traits proposed a root economics hypothesis where adaptations associated with mycorrhizal dependency strongly influence the organization of root traits, forming a dominant axis of trait covariation unique to roots. This conclusion, however, is based on tradeoffs of a few widely studied root traits. It is unknown how other functional traits fit into this mycorrhizal-collaboration gradient. Here, we provide a significant extension to the field of root ecology by examining how fine root secondary compounds coordinate with other root traits. We analyzed a dataset integrating compound-specific chemistry, morphology and anatomy of fine roots and leaves from 34 temperate tree species spanning major angiosperm lineages. Our data uncovered previously undocumented coordination where root chemistry, morphology and anatomy covary with each other. This coordination, aligned with mycorrhizal colonization, reflects tradeoffs between chemical protection and mycorrhizal dependency, and provides mechanistic support for the mycorrhizal-collaboration gradient. We also found remarkable phylogenetic structuring in root chemistry. These patterns were not mirrored by leaves. Furthermore, chemical protection was largely decoupled from the leaf economics spectrum. Our results unveil broad organization of root chemistry, demonstrate unique belowground adaptions, and suggest that root strategies and phylogeny could impact biogeochemical cycles through their links with root chemistry.

Limiting similarity shapes the functional and phylogenetic structure of root neighborhoods in a subtropical forest.

Environmental filtering and limiting similarity mechanisms can simultaneously structure community assemblages. However, how they shape the functional and phylogenetic structure of root neighborhoods remains unclear, hindering the understanding of belowground community assembly processes and diversity maintenance. In a 50-ha plot in a subtropical forest, China, we randomly sampled > 2700 root clusters from 625 soil samples. Focusing on 10 root functional traits measured on 76 woody species, we examined the functional and phylogenetic structure of root neighborhoods and linked their distributions with environmental cues. Functional overdispersion was pervasive among individual root traits (50% of the traits) and accentuated when different traits were combined. Functional clustering (20% of the traits) seemed to be associated with a soil nutrient gradient with thick roots dominating fertile areas whereas thin roots dominated infertile soils. Nevertheless, such traits also were sorted along other environmental cues, showing multidimensional adaptive trait syndromes. Species relatedness also was an important factor defining root neighborhoods, resulting in significant phylogenetic overdispersion. These results suggest that limiting similarity may drive niche differentiation of coexisting species to reduce competition, and that alternative root strategies could be crucial in promoting root neighborhood resource use and species coexistence.

Rapid responses of root traits and productivity to phosphorus and cation additions in a tropical lowland forest in Amazonia.

Soil nutrient availability can strongly affect root traits. In tropical forests, phosphorus (P) is often considered the main limiting nutrient for plants. However, support for the P paradigm is limited, and N and cations might also control tropical forests functioning. We used a large-scale experiment to determine how the factorial addition of nitrogen (N), P and cations affected root productivity and traits related to nutrient acquisition strategies (morphological traits, phosphatase activity, arbuscular mycorrhizal colonisation and nutrient contents) in a primary rainforest growing on low-fertility soils in Central Amazonia after 1 yr of fertilisation. Multiple root traits and productivity were affected. Phosphorus additions increased annual root productivity and root diameter, but decreased root phosphatase activity. Cation additions increased root productivity at certain times of year, also increasing root diameter and mycorrhizal colonisation. P and cation additions increased their element concentrations in root tissues. No responses were detected with N addition. Here we showed that rock-derived nutrients determined root functioning in low-fertility Amazonian soils, demonstrating not only the hypothesised importance of P, but also highlighting the role of cations. The changes in fine root traits and productivity indicated that even slow-growing tropical rainforests can respond rapidly to changes in resource availability.

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.

Root anatomy helps to reconcile observed root trait syndromes in tropical tree species.

PREMISE: Studying the organization of functional traits in plant leaves and stems has revealed notable patterns linking function and form; however, evidence of similarly robust organization in root tissues remains controversial. We posit that anatomical traits in roots can provide insight on the overall organization of the root system. We hypothesized that size variation in the tissue outside the stele is related in a nonlinear fashion with functional traits associated with direct resource uptake, including a negative relationship with root architectural traits, and that similar relationships detected in tropical areas also hold true in other biomes. METHODS: We addressed our hypotheses using empirical data from 24 tropical tree species in French Guiana, including anatomical measurements in first order roots and functional trait description for the entire fine root system. In addition, we compiled a global meta-analysis of root traits for 500+ forest species across tropical, subtropical, and temperate forests. RESULTS: Our results supported the expected nonlinear relationships between cortical size and morphological traits and a negative linear trend with architectural traits. We confirmed a global negative relationship among specific root length (SRL), diameter, and tissue density, suggesting similar anatomical constraints in root systems across woody plants. However, the importance of factors varies across biomes, possibly related to the unequal phylogenetic representation across latitudes. CONCLUSIONS: Our findings imply that the rhizocentric hypothesis can be a valuable approach to understand fine root trait syndromes and the evolution of absorptive roots in vascular plants.

Independent evolutionary changes in fine-root traits among main clades during the diversification of seed plants.

Changes in fine-root morphology are typically associated with transitions from the ancestral arbuscular mycorrhizal (AM) to the alternative ectomycorrhizal (ECM) or nonmycorrhizal (NM) associations. However, the modifications in root morphology may also coincide with new modifications in leaf hydraulics and growth habit during angiosperm diversification. These hypotheses have not been evaluated concurrently, and this limits our understanding of the causes of fine-root evolution. To explore the evolution of fine-root systems, we assembled a 600+ species database to reconstruct historical changes in seed plants over time. We utilise ancestral reconstruction approaches together with phylogenetically informed comparative analyses to test whether changes in fine-root traits were most strongly associated with mycorrhizal affiliation, leaf hydraulics or growth form. Our findings showed significant shifts in root diameter, specific root length and root tissue density as angiosperms diversified, largely independent from leaf changes or mycorrhizal affiliation. Growth form was the only factor associated with fine-root traits in statistical models including mycorrhizal association and leaf venation, suggesting substantial modifications in fine-root morphology during transitions from woody to nonwoody habits. Divergences in fine-root systems were crucial in the evolution of seed plant lineages, with important implications for ecological processes in terrestrial ecosystems.

Patterns in spatial distribution and root trait syndromes for ecto and arbuscular mycorrhizal temperate trees in a mixed broadleaf forest.

Functional differences between trees with arbuscular (AM) or ectomycorrhizal (ECM) partnerships influence important ecological processes including nutrient cycling, community assembly, and biomass allocation patterns. Although most broadleaf temperate forests show both mycorrhizal types, relatively few studies have addressed functional difference among coexisting mycorrhizal tree species. The maintenance of ECM associations usually requires higher C investment than AM, leading to (A) lower root biomass and (B) more conservative root trait syndromes in ECM tree species compared to AM species. Here we quantified the representation and trait syndromes of 14 canopy tree species associated with either AM or ECM fungi in a natural forest community. Our results showed that, whereas species root abundance was proportional to basal area, some ECM tree roots were largely under-represented (up to ~ 33%). Most of the under-representation was due to lower than expected root abundance of Quercus rubra and Fagus grandifolia. Functional root traits in tree species were similar, with the exception of higher tissue density in ECM species. Moreover, closely related AM and ECM exhibited similar traits, suggesting inherited trait syndrome from a common ancestor. Thus, we found little evidence of divergent functional root trait syndromes between mycorrhizal types. Cores dominated by ECM species influenced trait distribution at the community level, but not total biomass, suggesting that mycorrhizal affiliation may have a stronger effect on the spatial distribution of traits but not on biomass stocks. Our results present an important step toward relating belowground carbon dynamics to species traits, including mycorrhizal type, in broadleaf temperate forests.

Initial nitrogen enrichment conditions determines variations in nitrogen substrate utilization by heterotrophic bacterial isolates.

BACKGROUND: The nitrogen (N) cycle consists of complex microbe-mediated transformations driven by a variety of factors, including diversity and concentrations of N compounds. In this study, we examined taxonomic diversity and N substrate utilization by heterotrophic bacteria isolated from streams under complex and simple N-enrichment conditions. RESULTS: Diversity estimates differed among isolates from the enrichments, but no significant composition were detected. Substrate utilization and substrate range of bacterial assemblages differed within and among enrichments types, and not simply between simple and complex N-enrichments. CONCLUSIONS: N substrate use patterns differed between isolates from some complex and simple N-enrichments while others were unexpectedly similar. Taxonomic composition of isolates did not differ among enrichments and was unrelated to N use suggesting strong functional redundancy. Ultimately, our results imply that the available N pool influences physiology and selects for bacteria with various abilities that are unrelated to their taxonomic affiliation.

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.