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).

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.

Trees adjust nutrient acquisition strategies across tropical forest secondary succession.

Nutrient limitation may constrain the ability of recovering and mature tropical forests to serve as a carbon sink. However, it is unclear to what extent trees can utilize nutrient acquisition strategies - especially root phosphatase enzymes and mycorrhizal symbioses - to overcome low nutrient availability across secondary succession. Using a large-scale, full factorial nitrogen and phosphorus fertilization experiment of 76 plots along a secondary successional gradient in lowland wet tropical forests of Panama, we tested the extent to which root phosphatase enzyme activity and mycorrhizal colonization are flexible, and if investment shifts over succession, reflective of changing nutrient limitation. We also conducted a meta-analysis to test how tropical trees adjust these strategies in response to nutrient additions and across succession. We find that tropical trees are dynamic, adjusting investment in strategies - particularly root phosphatase - in response to changing nutrient conditions through succession. These changes reflect a shift from strong nitrogen to weak phosphorus limitation over succession. Our meta-analysis findings were consistent with our field study; we found more predictable responses of root phosphatase than mycorrhizal colonization to nutrient availability. Our findings suggest that nutrient acquisition strategies respond to nutrient availability and demand in tropical forests, likely critical for alleviating nutrient limitation.

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.

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

This corrects the article DOI: 10.1038/nature25783.

Legume-microbiome interactions unlock mineral nutrients in regrowing tropical forests.

Legume trees form an abundant and functionally important component of tropical forests worldwide with N2-fixing symbioses linked to enhanced growth and recruitment in early secondary succession. However, it remains unclear how N2-fixers meet the high demands for inorganic nutrients imposed by rapid biomass accumulation on nutrient-poor tropical soils. Here, we show that N2-fixing trees in secondary Neotropical forests triggered twofold higher in situ weathering of fresh primary silicates compared to non-N2-fixing trees and induced locally enhanced nutrient cycling by the soil microbiome community. Shotgun metagenomic data from weathered minerals support the role of enhanced nitrogen and carbon cycling in increasing acidity and weathering. Metagenomic and marker gene analyses further revealed increased microbial potential beneath N2-fixers for anaerobic iron reduction, a process regulating the pool of phosphorus bound to iron-bearing soil minerals. We find that the Fe(III)-reducing gene pool in soil is dominated by acidophilic Acidobacteria, including a highly abundant genus of previously undescribed bacteria, Candidatus Acidoferrum, genus novus. The resulting dependence of the Fe-cycling gene pool to pH determines the high iron-reducing potential encoded in the metagenome of the more acidic soils of N2-fixers and their nonfixing neighbors. We infer that by promoting the activities of a specialized local microbiome through changes in soil pH and C:N ratios, N2-fixing trees can influence the wider biogeochemical functioning of tropical forest ecosystems in a manner that enhances their ability to assimilate and store atmospheric carbon.

Key role of symbiotic dinitrogen fixation in tropical forest secondary succession.

Forests contribute a significant portion of the land carbon sink, but their ability to sequester CO2 may be constrained by nitrogen, a major plant-limiting nutrient. Many tropical forests possess tree species capable of fixing atmospheric dinitrogen (N2), but it is unclear whether this functional group can supply the nitrogen needed as forests recover from disturbance or previous land use, or expand in response to rising CO2 (refs 6, 8). Here we identify a powerful feedback mechanism in which N2 fixation can overcome ecosystem-scale deficiencies in nitrogen that emerge during periods of rapid biomass accumulation in tropical forests. Over a 300-year chronosequence in Panama, N2-fixing tree species accumulated carbon up to nine times faster per individual than their non-fixing neighbours (greatest difference in youngest forests), and showed species-specific differences in the amount and timing of fixation. As a result of fast growth and high fixation, fixers provided a large fraction of the nitrogen needed to support net forest growth (50,000 kg carbon per hectare) in the first 12 years. A key element of ecosystem functional diversity was ensured by the presence of different N2-fixing tree species across the entire forest age sequence. These findings show that symbiotic N2 fixation can have a central role in nitrogen cycling during tropical forest stand development, with potentially important implications for the ability of tropical forests to sequester CO2.

Phosphatase activity and nitrogen fixation reflect species differences, not nutrient trading or nutrient balance, across tropical rainforest trees.

A fundamental biogeochemical paradox is that nitrogen-rich tropical forests contain abundant nitrogen-fixing trees, which support a globally significant tropical carbon sink. One explanation for this pattern holds that nitrogen-fixing trees can overcome phosphorus limitation in tropical forests by synthesizing phosphatase enzymes to acquire soil organic phosphorus, but empirical evidence remains scarce. We evaluated whether nitrogen fixation and phosphatase activity are linked across 97 trees from seven species, and tested two hypotheses for explaining investment in nutrient strategies: trading nitrogen-for-phosphorus or balancing nutrient demand. Both strategies varied across species but were not explained by nitrogen-for-phosphorus trading or nutrient balance. This indicates that (1) studies of these nutrient strategies require broad sampling within and across species, (2) factors other than nutrient trading must be invoked to resolve the paradox of tropical nitrogen fixation, and (3) nitrogen-fixing trees cannot provide a positive nitrogen-phosphorus-carbon feedback to alleviate nutrient limitation of the tropical carbon sink.

Phosphorus and species regulate N2 fixation by herbaceous legumes in longleaf pine savannas.

Longleaf pine savannas house a diverse community of herbaceous N2-fixing legume species that have the potential to replenish nitrogen (N) losses from fire. Whether legumes fill this role depends on the factors that regulate symbiotic fixation, including soil nutrients such as phosphorus (P) and molybdenum (Mo) and the growth and fixation strategies of different species. In greenhouse experiments, we determined how these factors influence fixation for seven species of legumes grown in pure field soil from two different regions of the southeastern US longleaf pine ecosystem. We first added P and Mo individually and in combination, and found that P alone constrained fixation. Phosphorus primarily influenced fixation by regulating legume growth. Second, we added N to plants and found that species either downregulated fixation (facultative strategy) or maintained fixation at a constant rate (obligate strategy). Species varied nearly fourfold in fixation rate, reflecting differences in growth rate, taxonomy and fixation strategy. However, fixation responded strongly to P addition across all species in our study, suggesting that the P cycle regulates N inputs by herbaceous legumes.

N2-fixing tropical legume evolution: a contributor to enhanced weathering through the Cenozoic?

Fossil and phylogenetic evidence indicates legume-rich modern tropical forests replaced Late Cretaceous palm-dominated tropical forests across four continents during the early Cenozoic (58-42 Ma). Tropical legume trees can transform ecosystems via their ability to fix dinitrogen (N2) and higher leaf N compared with non-legumes (35-65%), but it is unclear how their evolutionary rise contributed to silicate weathering, the long-term sink for atmospheric carbon dioxide (CO2). Here we hypothesize that the increasing abundance of N2-fixing legumes in tropical forests amplified silicate weathering rates by increased input of fixed nitrogen (N) to terrestrial ecosystems via interrelated mechanisms including increasing microbial respiration and soil acidification, and stimulating forest net primary productivity. We suggest the high CO2 early Cenozoic atmosphere further amplified legume weathering. Evolution of legumes with high weathering rates was probably driven by their high demand for phosphorus and micronutrients required for N2-fixation and nodule formation.

Why are nitrogen-fixing trees rare at higher compared to lower latitudes?

Symbiotic nitrogen (N) fixation provides a dominant source of new N to the terrestrial biosphere, yet in many cases the abundance of N-fixing trees appears paradoxical. N-fixing trees, which should be favored when N is limiting, are rare in higher latitude forests where N limitation is common, but are abundant in many lower latitude forests where N limitation is rare. Here, we develop a graphical and mathematical model to resolve the paradox. We use the model to demonstrate that N fixation is not necessarily cost effective under all degrees of N limitation, as intuition suggests. Rather, N fixation is only cost effective when N limitation is sufficiently severe. This general finding, specific versions of which have also emerged from other models, would explain sustained moderate N limitation because N-fixing trees would either turn N fixation off or be outcompeted under moderate N limitation. From this finding, four general hypothesis classes emerge to resolve the apparent paradox of N limitation and N-fixing tree abundance across latitude. The first hypothesis is that N limitation is less common at higher latitudes. This hypothesis contradicts prevailing evidence, so is unlikely, but the following three hypotheses all seem likely. The second hypothesis, which is new, is that even if N limitation is more common at higher latitudes, more severe N limitation might be more common at lower latitudes because of the capacity for higher N demand. Third, N fixation might be cost effective under milder N limitation at lower latitudes but only under more severe N limitation at higher latitudes. This third hypothesis class generalizes previous hypotheses and suggests new specific hypotheses. For example, greater trade-offs between N fixation and N use efficiency, soil N uptake, or plant turnover at higher compared to lower latitudes would make N fixation cost effective only under more severe N limitation at higher latitudes. Fourth, N-fixing trees might adjust N fixation more at lower than at higher latitudes. This framework provides new hypotheses to explain the latitudinal abundance distribution of N-fixing trees, and also provides a new way to visualize them. Therefore, it can help explain the seemingly paradoxical persistence of N limitation in many higher latitude forests.

Taxonomic identity determines N2 fixation by canopy trees across lowland tropical forests.

Legumes capable of fixing atmospheric N2 are abundant and diverse in many tropical forests, but the factors determining ecological patterns in fixation are unresolved. A long-standing idea is that fixation depends on soil nutrients (N, P or Mo), but recent evidence shows that fixation may also differ among N2-fixing species. We sampled canopy-height trees across five species and one species group of N2-fixers along a landscape P gradient, and manipulated P and Mo to seedlings in a shadehouse. Our results identify taxonomy as the major determinant of fixation, with P (and possibly Mo) only influencing fixation following tree-fall disturbances. While 44% of trees did not fix N2, other trees fixed at high rates, with two species functioning as superfixers across the landscape. Our results raise the possibility that fixation is determined by biodiversity, evolutionary history and species-specific traits (tree growth rate, canopy stature and response to disturbance) in the tropical biome.

Aridity, not fire, favors nitrogen-fixing plants across tropical savanna and forest biomes.

Tropical savannas are hypothesized to be hot spots of nitrogen-fixer diversity and activity because of the high disturbance and low nitrogen characteristic of savanna landscapes. Here we compare the abundances of nitrogen-fixing and non-fixing trees in both tropical savannas and tropical forests under climatically equivalent conditions, using plant inventory studies across 566 plots in South America and Africa. A single factor, aridity, explained 19-54% of the variance in fixer abundance, and unexpectedly was more important than fire frequency, biome, and continent. Nitrogen fixers were more abundant in arid environments; as a result, African savannas, which tend to be drier, were richer in nitrogen fixers than South American savannas. Fixer abundance converged on similar levels in forests in both continents. We conclude that climate plays a greater role than fire in determining the distribution of nitrogen fixers across tropical savanna and forest biomes.

Fire alters ecosystem carbon and nutrients but not plant nutrient stoichiometry or composition in tropical savanna.

Fire and nutrients interact to influence the global distribution and dynamics of the savanna biome, but the results of these interactions are both complex and poorly known. A critical but unresolved question is whether short-term losses of carbon and nutrients caused by fire can trigger long-term and potentially compensatory responses in the nutrient stoichiometry of plants, or in the abundance of dinitrogen-fixing trees. There is disagreement in the literature about the potential role of fire on savanna nutrients, and, in turn, on plant stoichiometry and composition. A major limitation has been the lack of fire manipulations over time scales sufficiently long for these interactions to emerge. We use a 58-year, replicated, large-scale, fire manipulation experiment in Kruger National Park (South Africa) in savanna to quantify the effect of fire on (1) distributions of carbon, nitrogen, and phosphorus at the ecosystem scale; (2) carbon: nitrogen: phosphorus stoichiometry of above- and belowground tissues of plant species; and (3) abundance of plant functional groups including nitrogen fixers. Our results show dramatic effects of fire on the relative distribution of nutrients in soils, but that individual plant stoichiometry and plant community composition remained unexpectedly resilient. Moreover, measures of nutrients and carbon stable isotopes allowed us to discount the role of tree cover change in favor of the turnover of herbaceous biomass as the primary mechanism that mediates a transition from low to high 'soil carbon and nutrients in the absence of fire. We conclude that, in contrast to extra-tropical grasslands or closed-canopy forests, vegetation in the savanna biome may be uniquely adapted to nutrient losses caused by recurring fire.

Complex response of the forest nitrogen cycle to climate change.

Climate exerts a powerful influence on biological processes, but the effects of climate change on ecosystem nutrient flux and cycling are poorly resolved. Although rare, long-term records offer a unique opportunity to disentangle effects of climate from other anthropogenic influences. Here, we examine the longest and most complete record of watershed nutrient and climate dynamics available worldwide, which was collected at the Hubbard Brook Experimental Forest in the northeastern United States. We used empirical analyses and model calculations to distinguish between effects of climate change and past perturbations on the forest nitrogen (N) cycle. We find that climate alone cannot explain the occurrence of a dramatic >90% drop in watershed nitrate export over the past 46 y, despite longer growing seasons and higher soil temperatures. The strongest climate influence was an increase in soil temperature accompanied by a shift in paths of soil water flow within the watershed, but this effect explained, at best, only ∼40% of the nitrate decline. In contrast, at least 50-60% of the observed change in the N export could be explained by the long-lasting effect of forest cutting in the early 1900s on the N cycle of the soil and vegetation pools. Our analysis shows that historic events can obscure the influence of modern day stresses on the N cycle, even when analyses have the advantage of being informed by 0.5-century-long datasets. These findings raise fundamental questions about interpretations of long-term trends as a baseline for understanding how climate change influences complex ecosystems.

Ecosystem properties self-organize in response to a directional fog-vegetation interaction.

Feedbacks between vegetation and resource inputs can lead to the local, self-organization of ecosystem properties. In particular, feedbacks in response to directional resources (e.g., coastal fog, slope runoff) can create complex spatial patterns, such as vegetation banding. Although similar feedbacks are thought to be involved in the development of ecosystems, clear empirical examples are rare. We created a simple model of a fog-influenced, temperate rainforest in central Chile, which allows the comparison of natural banding patterns to simulations of various putative mechanisms. We show that only feedbacks between plants and fog were able to replicate the characteristic distributions of vegetation, soil water, and soil nutrients observed in field transects. Other processes, such as rainfall, were unable to match these diagnostic distributions. Furthermore, fog interception by windward trees leads to increased downwind mortality, leading to progressive extinction of the leeward edge. This pattern of ecosystem development and decay through self-organized processes illustrates, on a relatively small spatial and temporal scale, the patterns predicted for ecosystem evolution.

Large losses of inorganic nitrogen from tropical rainforests suggest a lack of nitrogen limitation.

Inorganic nitrogen losses from many unpolluted mature tropical forests are over an order of magnitude higher than losses from analogous temperate forests. This pattern could either reflect a lack of N limitation or accelerated plant-soil N cycling under tropical temperatures and moisture. We used a simple analytical framework of the N cycle and compared our predictions with data of N in stream waters of temperate and tropical rainforests. While the pattern could be explained by differences in N limitation, it could not be explained based on up-regulation of the internal N cycle without invoking the unlikely assumption that tropical plants are two to four times less efficient at taking up N than temperate plants. Our results contrast with the idea that a tropical climate promotes and sustains an up-regulated and leaky - but N-limited - internal N cycle. Instead, they are consistent with the notion that many tropical rainforests exist in a state of N saturation.

Leaf N:P ratio does not predict productivity trends across natural terrestrial ecosystems.

Nitrogen (N) and phosphorus (P) are crucial nutrients for regulating plant growth. The classic growth rate hypothesis (GRH) proposes that fast-growing organisms have lower N:P ratios, and it is promising to predict net primary productivity (NPP) using the leaf N:P ratio at the community level (N:PCom ). However, whether leaf N:P ratio can predict NPP in natural ecosystems on a large scale remains nebulous. Here, we systematically calculated leaf N:PCom (community biomass-weighted mean and species arithmetic mean) using the consistently measured data of 2192 plant species-site combinations and productivity (biomass-based aboveground NPP and flux-based NPP) in 66 natural ecosystems in China. Unexpectedly, leaf N:PCom hardly predicted productivity in natural ecosystems due to their weak correlation, although significantly negative or positive relationships across different ecosystems were observed. The ambiguous relationship between leaf N:P and species dominance reflected a luxury consumption of N and P in turnover and structure in natural communities, unlike what GRH suggests. Climate, soil, and leaf nutrients (rather than N:P) influenced productivity, which highlighted the importance of external environment and nutrient constrains. Our findings pose a major challenge for leaf N:PCom as a direct parameter in productivity models and further question the direct application of classic hypotheses in short-term experiments or model species to long-term and complex natural ecosystems.