Nitrogen deficiency accelerates soil organic carbon decomposition in temperate degraded grasslands.

The impacts of nitrogen (N) availability on soil organic carbon (SOC) decomposition were often explored based on N enrichment (N+) experiments. However, many natural and anthropogenic processes often reduce soil N availability. There is no direct evidence about how decreased N availability (N-) affects SOC decomposition, and the mechanisms of microbe-driven SOC decomposition in response to N availability remain unclear. Here, we used ion-exchange membranes to simulate N-. Soil samples from four temperate grassland sites, ranging from non-degradation to extreme degradation, were incubated with the N- and N+ treatments. We found that the total cumulative carbon (C) release was promoted by the N- treatment (8.60 to 87.30 mg C/g Cinital) but was inhibited by the N+ treatment (-129.81 to -16.49 mg C/g Cinital), regardless of the degradation status. N- dramatically increased recalcitrant C decomposition by increasing soil pH at all grassland sites; while did not affect or even decreased labile C decomposition by significantly increasing microbial C use efficiency and soil microbial biomass N. Interestingly, the effects of N- and N+ on SOC decomposition was asymmetric; with increased grassland degradation, the SOC decomposition was more sensitive to N- than to N+. Our results provide direct evidence for the different effects and mechanisms of N- on SOC decomposition and should be considered in soil process models to better predict the response of the nutrient cycle to global changes.

Leading nutrient foraging strategies shaping by root system characteristics along the elevations in rubber (Hevea brasiliensis) plantations.

When it comes to root and mycorrhizal associations that define resource acquisition strategy, there is a need to identify the leading dimension across root physiology, morphology, architecture and whole plant biomass allocation to better predict the plant's responses to multiple environmental constraints. Here, we developed a new framework for understanding the variation in roots and symbiotic fungi by quantifying multiple-scale characteristics, ranging from anatomy to the whole plant. We chose the rubber (Hevea brasiliensis) grown at three elevations to test our framework and to identify the key dimensions for resource acquisition. Results showed that the quantities of absorptive roots and root system architecture, rather than single root traits, played the leading role in belowground resource acquisition. As the elevation increased from the low to high elevation, root length growth, productivity and root mass fraction (RMF) increased by 2.9-, 2.3- and 13.8-fold, respectively. The contribution of RMF to the changes in total root length was 3.6-fold that of specific root length (SRL). Root architecture exhibited higher plasticity than anatomy and morphology. Further, mycorrhizal colonization was highly sensitive to rising elevations with a non-monotonic pattern. By contrast, both leaf biomass and specific leaf area (traits) co-varied with increasing elevation. In summary, rubber trees changed root system architecture by allocating more biomass and lowering the reliance on mycorrhizal fungi rather than improving single root efficiency in adapting to high elevation. Our framework is instructive for traits-based ecology; accurate assessments of forest carbon cycling in response to resource gradient should account for the leading dimension of root system architecture.

Niche partitioning in nitrogen uptake among subtropical tree species enhances biomass production.

Nitrogen (N) is a main nutrient limiting plant growth in most terrestrial ecosystems, but so far it remains unknown which role plant N uptake plays for the positive relationship between species richness and productivity. An in situ15N labeling experiment was carried out by planting four subtropical tree species (i.e., Koelreuteria bipinnata, Lithocarpus glaber, Cyclobalanopsis myrsinaefolia and Castanopsis eyrei) in pots, at richness levels 1, 2 and 4 species per pot. Plant N uptake preference for inorganic N form of NO3- to NH4+ and organic N form of glycine, as well as biomass and plant functional traits was evaluated under different tree species richness level. Overall, pot biomass productivity increased with tree species richness. Biomass of the most productive species, K. bipinnata increased, but not at the expense of a decreased growth of the other species. In mixtures, the species shifted their preference for the inorganic N form, from NO3- to NH4+ or vice versa. The uptake preference for glycine remained stable along the species richness gradient. Plant N uptake was well correlated with numerous functional traits, both aboveground, such as height and shoot diameter, and belowground, such as root diameter and root length. We conclude that increased ecosystem biomass production with tree species richness could be largely explained by niche partitioning in N uptake among tree species. Our findings highlight that niche partitioning for N uptake should be a possible important mechanism maintaining species diversity and ecosystem production in subtropical forests.

Biome boundary maintained by intense belowground resource competition in world's thinnest-rooted plant community.

Recent findings point to plant root traits as potentially important for shaping the boundaries of biomes and for maintaining the plant communities within. We examined two hypotheses: 1) Thin-rooted plant strategies might be favored in biomes with low soil resources; and 2) these strategies may act, along with fire, to maintain the sharp boundary between the Fynbos and Afrotemperate Forest biomes in South Africa. These biomes differ in biodiversity, plant traits, and physiognomy, yet exist as alternative stable states on the same geological substrate and in the same climate conditions. We conducted a 4-y field experiment to examine the ability of Forest species to invade the Fynbos as a function of growth-limiting nutrients and belowground plant-plant competition. Our results support both hypotheses: First, we found marked biome differences in root traits, with Fynbos species exhibiting the thinnest roots reported from any biome worldwide. Second, our field manipulation demonstrated that intense belowground competition inhibits the ability of Forest species to invade Fynbos. Nitrogen was unexpectedly the resource that determined competitive outcome, despite the long-standing expectation that Fynbos is severely phosphorus constrained. These findings identify a trait-by-resource feedback mechanism, in which most species possess adaptive traits that modify soil resources in favor of their own survival while deterring invading species. Our findings challenge the long-held notion that biome boundaries depend primarily on external abiotic constraints and, instead, identify an internal biotic mechanism-a selective feedback among traits, plant-plant competition, and ecosystem conditions-that, along with contrasting fire regime, can act to maintain biome boundaries.

Relationships Between Leaf Carbon and Macronutrients Across Woody Species and Forest Ecosystems Highlight How Carbon Is Allocated to Leaf Structural Function.

Stoichiometry of leaf macronutrients can provide insight into the tradeoffs between leaf structural and metabolic investments. Structural carbon (C) in cell walls is contained in lignin and polysaccharides (cellulose, hemicellulose, and pectins). Much of leaf calcium (Ca) and a fraction of magnesium (Mg) were further bounded with cell wall pectins. The macronutrients phosphorus (P), potassium (K), and nitrogen (N) are primarily involved in cell metabolic functions. There is limited information on the functional interrelations among leaf C and macronutrients, and the functional dimensions characterizing the leaf structural and metabolic tradeoffs are not widely appreciated. We investigated the relationships between leaf C and macronutrient (N, P, K, Ca, Mg) concentrations in two widespread broad-leaved deciduous woody species Quercus wutaishanica (90 individuals) and Betula platyphylla (47 individuals), and further tested the generality of the observed relationships in 222 woody eudicots from 15 forest ecosystems. In a subsample of 20 broad-leaved species, we also analyzed the relationships among C, Ca, lignin, and pectin concentrations in leaf cell walls. We found a significant leaf C-Ca tradeoff operating within and across species and across ecosystems. This basic relationship was explained by variations in the share of cell wall lignin and pectin investments at the cell scale. The C-Ca tradeoffs were mainly driven by soil pH and mean annual temperature and precipitation, suggesting that leaves were more economically built with less C and more Ca as soil pH increased and at lower temperature and lower precipitation. However, we did not detect consistent patterns among C-N, and C-Mg at different levels of biological organization, suggesting substantial plasticity in N and Mg distribution among cell organelles and cell protoplast and cell wall. We observed two major axes of macronutrient differentiation: the cell-wall structural axis consisting of protein-free C and Ca and the protoplasm metabolic axis consisting of P and K, underscoring the decoupling of structural and metabolic elements inherently linked with cell wall from protoplasm investment strategies. We conclude that the tradeoffs between leaf C and Ca highlight how carbon is allocated to leaf structural function and suggest that this might indicate biogeochemical niche differentiation of species.

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).

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

This corrects the article DOI: 10.1038/nature25783.

Evolutionary history resolves global organization of root functional traits.

Plant roots have greatly diversified in form and function since the emergence of the first land plants, but the global organization of functional traits in roots remains poorly understood. Here we analyse a global dataset of 10 functionally important root traits in metabolically active first-order roots, collected from 369 species distributed across the natural plant communities of 7 biomes. Our results identify a high degree of organization of root traits across species and biomes, and reveal a pattern that differs from expectations based on previous studies of leaf traits. Root diameter exerts the strongest influence on root trait variation across plant species, growth forms and biomes. Our analysis suggests that plants have evolved thinner roots since they first emerged in land ecosystems, which has enabled them to markedly improve their efficiency of soil exploration per unit of carbon invested and to reduce their dependence on symbiotic mycorrhizal fungi. We also found that diversity in root morphological traits is greatest in the tropics, where plant diversity is highest and many ancestral phylogenetic groups are preserved. Diversity in root morphology declines sharply across the sequence of tropical, temperate and desert biomes, presumably owing to changes in resource supply caused by seasonally inhospitable abiotic conditions. Our results suggest that root traits have evolved along a spectrum bounded by two contrasting strategies of root life: an ancestral 'conservative' strategy in which plants with thick roots depend on symbiosis with mycorrhizal fungi for soil resources and a more-derived 'opportunistic' strategy in which thin roots enable plants to more efficiently leverage photosynthetic carbon for soil exploration. These findings imply that innovations of belowground traits have had an important role in preparing plants to colonize new habitats, and in generating biodiversity within and across biomes.

Three Key Sub-leaf Modules and the Diversity of Leaf Designs.

Earth harbors a highly diverse array of plant leaf forms. A well-known pattern linking diverse leaf forms with their photosynthetic function across species is the global leaf economics spectrum (LES). However, within homogeneous plant functional groups such as tropical woody angiosperms or temperate deciduous woody angiosperms, many species can share a similar position in the LES but differ in other vital leaf traits, and thus function differently under the given suite of environmental drivers. How diverse leaves differentiate from each other has yet to be fully explained. Here, we propose a new perspective for linking leaf structure and function by arguing that a leaf may be divided into three key sub-modules, the light capture module, the water-nutrient flow module and the gas exchange module. Each module consists of a set of leaf tissues corresponding to a certain resource acquisition function, and the combination and configuration of different modules may differ depending on overall leaf functioning in a given environment. This modularized-leaf perspective differs from the whole-leaf perspective used in leaf economics theory and may serve as a valuable tool for tracing the evolution of leaf form and function. This perspective also implies that the evolutionary direction of various leaf designs is not to optimize a single critical trait, but to optimize the combination of different traits to better adapt to the historical and current environments. Future studies examining how different modules are synchronized for overall leaf functioning should offer critical insights into the diversity of leaf designs worldwide.

Diverse belowground resource strategies underlie plant species coexistence and spatial distribution in three grasslands along a precipitation gradient.

Functional traits and their variation mediate plant species coexistence and spatial distribution. Yet, how patterns of variation in belowground traits influence resource acquisition across species and plant communities remains obscure. To characterize diverse belowground strategies in relation to species coexistence and abundance, we assessed four key belowground traits - root diameter, root branching intensity, first-order root length and mycorrhizal colonization - in 27 coexisting species from three grassland communities along a precipitation gradient. Species with thinner roots had higher root branching intensity, but shorter first-order root length and consistently low mycorrhizal colonization, whereas species with thicker roots enhanced their capacity for resource acquisition by producing longer first-order roots and maintaining high mycorrhizal colonization. Plant species observed across multiple sites consistently decreased root branching and/or mycorrhizal colonization, but increased lateral root length with decreasing precipitation. Additionally, the degree of intraspecific trait variation was positively correlated with species abundance across the gradient, indicating that high intraspecific trait variation belowground may facilitate greater fitness and chances of survival across multiple habitats. These results suggest that a small set of critical belowground traits can effectively define diverse resource acquisition strategies in different environments and may forecast species survival and range shifts under climate change.

Building a better foundation: improving root-trait measurements to understand and model plant and ecosystem processes.

Trait-based approaches provide a useful framework to investigate plant strategies for resource acquisition, growth, and competition, as well as plant impacts on ecosystem processes. Despite significant progress capturing trait variation within and among stems and leaves, identification of trait syndromes within fine-root systems and between fine roots and other plant organs is limited. Here we discuss three underappreciated areas where focused measurements of fine-root traits can make significant contributions to ecosystem science. These include assessment of spatiotemporal variation in fine-root traits, integration of mycorrhizal fungi into fine-root-trait frameworks, and the need for improved scaling of traits measured on individual roots to ecosystem-level processes. Progress in each of these areas is providing opportunities to revisit how below-ground processes are represented in terrestrial biosphere models. Targeted measurements of fine-root traits with clear linkages to ecosystem processes and plant responses to environmental change are strongly needed to reduce empirical and model uncertainties. Further identifying how and when suites of root and whole-plant traits are coordinated or decoupled will ultimately provide a powerful tool for modeling plant form and function at local and global scales.

Fast-cycling unit of root turnover in perennial herbaceous plants in a cold temperate ecosystem.

Roots of perennial plants have both persistent portion and fast-cycling units represented by different levels of branching. In woody species, the distal nonwoody branch orders as a unit are born and die together relatively rapidly (within 1-2 years). However, whether the fast-cycling units also exist in perennial herbs is unknown. We monitored root demography of seven perennial herbs over two years in a cold temperate ecosystem and we classified the largest roots on the root collar or rhizome as basal roots, and associated finer laterals as secondary, tertiary and quaternary roots. Parallel to woody plants in which distal root orders form a fast-cycling module, basal root and its finer laterals also represent a fast-cycling module in herbaceous plants. Within this module, basal roots had a lifespan of 0.5-2 years and represented 62-87% of total root biomass, thus dominating annual root turnover (60%-81% of the total). Moreover, root traits including root length, tissue density, and biomass were useful predictors of root lifespan. We conclude that both herbaceous and woody plants have fast-cycling modular units and future studies identifying the fast-cycling module across plant species should allow better understanding of how root construction and turnover are linked to whole-plant strategies.

[Biomass of Quercus fabri population under different ecological restoration regimes in subtropical China].

In this paper, the tissue-specific biomass and above-ground biomass of Quercus fabri under different ecological restoration regimes in subtropical China were analyzed by establishing allometric models with different parameters. The best-fitted equations were adopted for estimating the biomass and its annual growth, and the below-ground biomass and its increment were estimated on the basis of its linear relationship with above-ground biomass. The results showed that the biomass of the branches and of the total above-ground tissues was best described by power-function models, and the best fitted independent variables were d2l and D2H, respectively. The tissue-specific biomass and total biomass of Q. fabri population were all greater in secondary forest than in Pinus elliottii plantation. The above-ground biomass and below-ground biomass of Q. fabri population in secondary forest were 3.592 and 1.723 t x hm(-2), respectively, in which, different tissue components were ranked in the order of stem > branch > leaf; while those in P. elliottii plantation were 0.666 and 0.462 t x hm(-2), respectively, in which, different tissue components were ranked in the order of stem > leaf > branch. From 2004 to 2006, the annual increments of above-ground, below-ground, and total biomass increased with time, and the increment of above-ground biomass had an ascent tendency, which was from 54.35% to 62.20% in P. elliottii plantation and from 67.27% to 68.94% in secondary forest. In comparing with that in secondary forest, the biomass increment of Q. fabri population in P. elliottii plantation was small, despite its relatively high growth rate.

[Estimation models of understory shrub biomass and their applications in red soil hilly region].

With 16 familiar species of understory shrub at Qianyezhou ecological experimental station in red soil hilly region under Chinese Academy of Sciences as test objects, crown area (A(c)) and projected volume (V(c)) were used as the variables for building quadratic and power allometric equations, respectively, to estimate the biomass of individual populations, and mixed-model was used to estimate the biomass of the 16 species. The best-fit models were applied to estimate the biomass of understory shrub in different forest types. The results showed that the biomass of shrub layer varied significantly among different stand types. With species-specific models, the biomass in deciduous, secondary, and coniferous forests was estimated as 4 773, 3 175 and 733 kg x hm(-2), respectively; while with mixed model, the estimation result was a little lower, being 3 946, 2 772 and 840 kg x hm(-2), respectively. Under the conditions of species-specific models being not established, mixed model was more convenient and practical in estimating the biomass of understory shrub.