Search

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:P

A major uncertainty in the land carbon cycle is whether symbiotic nitrogen fixation acts to enhance the tropical forest carbon sink. Nitrogen-fixing trees can supply vital quantities of the growth-limiting nutrient nitrogen, but the extent to which the resulting carbon–nitrogen feedback safeguards ecosystem carbon sequestration remains unclear. We combine (i) field observations from 112 plots spanning 300 years of succession in Panamanian tropical forests, and (ii) a new model that resolves nitrogen and light competition at the scale of individual trees. Fixation doubled carbon accumulation in early succession and enhanced total carbon in mature forests by ~10% (~12MgC ha−1) through two mechanisms: (i) a direct fixation effect on tree growth, and (ii) an indirect effect on the successional sequence of non-fixing trees. We estimate that including nitrogen-fixing trees in Neotropical reforestation projects could safeguard the sequestration of 6.7 Gt CO2 over the next 20 years. Our results highlight the connection between functional diversity of plant communities and the critical ecosystem service of carbon sequestration for mitigating climate change., The contribution of symbiotic dinitrogen fixation to the forest carbon sink could change throughout forest succession. Here the authors model nitrogen cycling and light competition between trees based on data from Panamanian forest plots, showing that fixation contributes substantially to the carbon sink in early successional stages.

Our understanding of terrestrial nitrogen (N) cycling is changing as new processes are uncovered, including the sources, turnover and losses of N from ecosystems. We integrate recent insights into an updated N‐cycling framework and discuss how a new understanding integrates eco‐evolutionary dynamics with nutrient cycling. These insights include (a) the significance of rock weathering as a biologically meaningful N source to plants and microbes; (b) the lack of consistent N limitation of organic matter decomposition by soil microbes; (c) species‐specific variation in plant N limitation; and (d) how fire effects on soil N shift with ecosystem properties. Using an eco‐evolutionary framework and revised knowledge of N cycling, we describe how (a) rock N weathering could have contributed more strongly to gradients in soil N availability than previously recognized, (b) evolution and co‐evolution of plant and soil microbial resource‐use traits underlie whether decomposition and production are N‐limited, and (c) the effects of fire on soil N pools are mediated by composition of plant species and time‐scale. Our revised framework of N cycling provides a way forward for improving biogeochemical models to more accurately estimate rates of plant production and decomposition, and total soil N. A free Plain Language Summary can be found within the Supporting Information of this article.

Significance Symbiotic dinitrogen (N2)-fixing trees fulfill a critical function in tropical forests by bringing in new nitrogen, yet it remains unclear how they overcome constraints by highly weathered, nutrient-poor tropical soils. We advance forest biogeochemistry and microbial ecology with the discovery from field trials in Panama that fast-growing N2-fixing trees in tropical forests exhibit accelerated mineral weathering and distinctive soil metagenomes that improve their access to inorganic nutrients in nutrient-poor soils. Furthermore, we show that N2-fixing trees exert similar effects on non-N2–fixing trees nearby thus having previously overlooked community-wide effects on tropical forest nutrient cycling. These results offer insights into the role of N2-fixing trees and their associated microbiomes in safeguarding the function of tropical forests within the global biosphere., 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.

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.

Nitrogen fixation may be critical for supplying the nitrogen (N) needed to maintain the tropical carbon sink in a world of rising atmospheric CO2. However, we do not know whether increased CO2 acts to exacerbate nutrient limitation on the fixation process itself. We experimentally test this idea by growing N2-fixing plants in pre-Industrial (280 ppm), present-day (400 ppm), and doubled (800 ppm) atmospheric CO2. In a greenhouse experiment, we grew tree seedlings from N2-fixing species and a non-fixing species at three CO2 concentrations with control, +P (phosphorus), +Mo (molybdenum), and + P +Mo nutrient treatments. We found nutrient limitation to be minimal at pre-Industrial CO2, but with increasing CO2 fixer growth and fixation became increasingly limited by P and by a P-by-Mo interaction. At 400 ppm, plants with +P grew ~50% faster and fixed 10-15× more N2 based on nodule mass and nitrogenase activity. At 800 ppm, plants with +P +Mo grew 200% more, and fixed 25× more N2, suggesting Mo-P co-limitation at elevated CO2. Our findings imply that complex patterns of nutrient limitation can develop as CO2 rises, potentially suppressing tropical N2-fixation and the new inputs of N needed to sustain the tropical carbon sink.

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.

Potential variability in nutrient limitation among tree size classes, functional groups and species calls for an integrated community- and ecosystem-level perspective of lowland tropical rainforest nutrient limitation. In particular, canopy trees determine ecosystem nutrient conditions, but competitive success for nutrients and light during the sapling bottleneck determines canopy composition. We conducted an in situ multi-nutrient sapling fertilization experiment at La Selva Biological Station, Costa Rica, to determine how functional group identity, species identity and light availability can impact nutrient limitation of stem growth in three functional groups and nine species. Despite high soil fertility, we found nutrient-light limitation in two functional groups and four species. Unexpectedly, the nitrogen-fixing (“N2 fixers”) and shade-tolerant functional groups were significantly nutrient limited, while the light-demanding functional group was not. This was partially explained by species-level variation in nutrient limitation within these functional groups, with only some species conforming to the prediction of stronger nutrient limitation in light demanders compared to shade-tolerants. Most surprisingly, we found strong nutrient limitation at low-light levels in the N2 fixers (which were shade-tolerant), but not in the shade-tolerant non-fixers. We hypothesize that the N2 fixers were actually nitrogen limited at low-light levels because of their nitrogen-rich leaves and the high carbon cost of their symbionts. This finding suggests a highly shade-tolerant, N2 fixation strategy, in addition to the perception that N2 fixation is mostly advantageous in high-light environments during early and gap succession. The shade-tolerant, N2 fixation strategy may be part of a sapling and canopy tree feedback, where the canopy N2 fixers enrich the soil N, enhancing growth of their shade-tolerant saplings relative to non-fixing competitors, enabling further canopy domination by shade-tolerant N2 fixers, as seen at La Selva. Synthesis. The pervasiveness of functional group- and species-specific nutrient and light co-limitation in our saplings indicates that these interactions likely play an important role in the dynamics of lowland tropical rainforest nutrient limitation, potentially via other such sapling and canopy tree feedbacks as the one hypothesized.

Background: Although obesity is an increasing public health problem throughout the Arabian Peninsula, only a few comprehensive population-based studies have been published in Qatar. In particular, there is a dearth of published information on the increasing body mass index (BMI) of the most vulnerable Qatari sub-population – adolescents. This paper partially addresses this omission by documenting the BMI status of Qatari youth in 2008/2009; it also highlights the changes in BMI that occurred during the first decade of this century, when local risk factors were significantly increasing. Methods: Using a simple random sampling approach, adolescents were selected from a pool of Qatari children attending government schools in Qatar. This resulted in a comprehensive dataset of height and BMI for 705 boys and girls aged 12–17 years. Results: The overall prevalence of Qatari adolescents who were overweight/obese in 2008–2009 was 19.9%/26.7% (boys) and 23.2%/17.2% (girls). This represents a change in the prevalence of overweight/obesity of − 8.7%/+18.8 (boys) and +4.3%/+12.1% (girls) during the time between these studies. Conclusions: BMI increased substantially during the last decade, leading to a corresponding increase in the prevalence of adolescent obesity. These results demonstrate that regular monitoring of the BMI status of the Qatari adolescent population provides valuable predictors for adults.

Biological nitrogen fixation is critical for the nitrogen cycle of tropical forests, yet we know little about the factors that control the microbial nitrogen fixers that colonize the microbiome of leaves and branches that make up a forest canopy. Forest canopies are especially prone to nutrient limitation because they are (1) disconnected from soil nutrient pools and (2) often subject to leaching. Earlier studies have suggested a role of phosphorus and molybdenum in controlling biological N-fixation rates, but experimental confirmation has hitherto been unavailable. Here we present the results of a manipulation of canopy nutrient availability. Our findings demonstrate a primary role of phosphorus in constraining overall N fixation by canopy cyanobacteria, but also a secondary role of molybdenum in determining per-cell fixation rates. A conservative evaluation suggests that canopy fixation can contribute to significant N fluxes at the ecosystem level, especially as bursts following atmospheric inputs of nutrient-rich dust.

Elephants and fire are individually well-known disturbance agents within savanna ecosystems, but their interactive role in governing tree-cover dynamics and savanna-forest biome boundaries remain unresolved. Of central importance are the mechanisms by which elephants vs. fire affect tree biomass and cover, and how – over long time periods – both factors interact with rainfall and soils to govern tree biomass and carbon dynamics. Here, we evaluated the response of woody vegetation to 56 years of fire manipulation in South Africa's Kruger National Park, with three fire regimes (annual, triennial, and unburned) replicated across a productivity gradient and subject to two periods of contrasting elephant abundances (generated by the cessation of culling in 1994). Higher fire frequencies had a negative effect on woody biomass in the low-elephant period, but this effect was weak-to-negligible in the high-elephant period as the difference among fire treatments diminished. Moreover, elephants removed increasing amounts of woody biomass as productivity increased across study sites, but fire did not. We infer that elephant-induced tree mortality could overcome increases in woody-plant productivity, while fire-induced mortality alone could not. Elephants caused woody-plant carbon to shift from a sink to a source; this effect was independent of fire treatment, with highest rates of net carbon removal in the wettest and most productive site. Synthesis: Our results reveal a context-dependent interaction between fire and elephants as disturbance agents in savanna: the influence of fire on woody plants was sensitive to the abundance of elephants and diminished with increased plant productivity. In contrast, elephants were capable of shifting landscapes from relatively dense woodland to open savanna, even in unburned sites, and exerted strong impacts irrespective of site conditions and plant productivity. This article is protected by copyright. All rights reserved.

Fire is a critical force in structuring ecosystems, but it also removes substantial amounts of nitrogen (N), which can limit plant growth. Biological N fixation (BNF) may alleviate fire-induced N deficiencies that inhibit ecosystem recovery, yet if and how BNF achieves this under frequent fire is unclear. This problem is further complicated in the context of modern human influences (such as land-use history and atmospheric N deposition), which may confound the relationship between fire and fixation. Here, we investigate whether BNF supplies the N necessary to replace fire-induced N losses in restored longleaf pine savannas, and, if so, what factors control fixation. We established 54 1-ha plots of longleaf pine capturing 227 yr of forest recovery and a broad gradient of fire return interval (1.5-20 yr) at two sites in the southeastern United States. We quantified N fixation from three functional groups (herbaceous legumes, soil crusts, and asymbiotic N fixing bacteria), N losses from individual fire events and ecosystem dynamics of N supply and demand. We found that BNF rates were low but sustained over stand age but were substantially below estimated rates of atmospheric N deposition. While fire temporarily stimulated BNF from herbaceous legumes, neither BNF nor atmospheric N deposition were sufficient to balance N losses from fire and soil N stocks declined over stand age. However, rates of N mineralization were surprisingly high and tree productivity was unrelated to N availability, questioning the importance of N limitation in these temperate savannas. While it is possible that progressive N losses signal a decline in ecosystem resiliency, N enrichment from multiple land-use transitions and anthropogenic N deposition may suppress rates of BNF or diminish its importance as a long-term N balancing source in these pyrogenic ecosystems. In this case, fire may be acting as relief mechanism, critical for returning the modern longleaf pine landscape to its historical oligotrophic condition.

One of the most distinct but unresolved global patterns is the apparent variation in plant–symbiont nutrient strategies across biomes. This pattern is central to our understanding of plant–soil–nutrient feedbacks in the land biosphere, which, in turn, are essential for our ability to predict the future dynamics of the Earth system. Here, we present an evolution-based trait-modelling approach for resolving (1) the organization of plant–symbiont relationships across biomes worldwide and (2) the emergent consequences for plant community composition and land biogeochemical cycles. Using game theory, we allow plants to use different belowground strategies to acquire nutrients and compete within local plant–soil–nutrient cycles in boreal, temperate and tropical biomes. The evolutionarily stable strategies that emerge from this analysis allow us to predict the distribution of belowground symbioses worldwide, the sequence and timing of plant succession, the bistability of ecto- versus arbuscular mycorrhizae in temperate and tropical forests, and major differences in the land carbon and nutrient cycles across biomes. Our findings imply that belowground symbioses have been central to the evolutionary assembly of plant communities and plant–nutrient feedbacks at the scale of land biomes. We conclude that complex global patterns emerge from local between-organism interactions in the context of Darwinian natural selection and evolution, and that the underlying dynamics can be mechanistically probed by our low-dimensional modelling approach. Developing a modelling approach based on evolutionary game theory, the authors are able to successfully predict global patterns in belowground plant–symbiont distributions across biomes, as well as major patterns in nutrient cycling, succession and stability.

Previous studies investigating organic-rich tundra have reported that increasing biodegradation of Arctic tundra soil organic carbon (SOC) under warming climate regimes will cause increasing CO2 and CH4 emissions. Organic-poor, mineral cryosols, which comprise 87% of Arctic tundra, are not as well characterized. This study examined biogeochemical processes of 1 m long intact mineral cryosol cores (1–6% SOC) collected in the Canadian high Arctic. Vertical profiles of gaseous and aqueous chemistry and microbial composition were related to surface CO2 and CH4 fluxes during a simulated spring/summer thaw under light versus dark and in situ versus water saturated treatments. CO2 fluxes attained 0.8 ± 0.4 mmol CO2 m−2 h−1 for in situ treatments, of which 85 ± 11% was produced by aerobic SOC oxidation, consistent with field observations and metagenomic analyses indicating aerobic heterotrophs were the dominant phylotypes. The Q10 values of CO2 emissions ranged from 2 to 4 over the course of thawing. CH4 degassing occurred during initial thaw; however, all cores were CH4 sinks at atmospheric concentration CH4. Atmospheric CH4 uptake rates ranged from −126 ± 77 to −207 ± 7 nmol CH4 m−2 h−1 with CH4 consumed between 0 and 35 cm depth. Metagenomic and gas chemistry analyses revealed that high-affinity Type II methanotrophic sequence abundance and activity were highest between 0 and 35 cm depth. Microbial sulfate reduction dominated the anaerobic processes, outcompeting methanogenesis for H2 and acetate. Fluxes, microbial community composition, and biogeochemical rates indicate that mineral cryosols of Axel Heiberg Island act as net CO2 sources and atmospheric CH4 sinks during summertime thaw under both in situ and water saturated states.

We evaluated the effects of fire on ecosystem biogeochemistry by examining how 56 years of fire manipulations changed carbon and nutrients in soils and plants in an African savanna. Although fire treatment significantly changed carbon and nutrients in the soil, the stoichiometry of individual plants and the community composition of functional groups were remarkably resilient. We also evaluated the relative role of trees vs. grasses in driving changes in the soil pools and discussed possible implications behind shifts in physical vegetation structure for the sensitivity of carbon losses.

Plant roots have greatly diversified in form and function since the emergence of the first land plants1,2, but the global organization of functional traits in roots remains poorly understood3,4. 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 studies5,6 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.

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.

Summary Savanna vegetation is variable, and predicting how water, nutrients, and chronic disturbances interact to determine vegetation structure in savannas represents a challenge. Here, we examined in situ interactions among rainfall, soils, grasses, fire, and elephants that determine tree layer responses to resource gradients in Kruger National Park in South Africa, using 363 long-term monitoring sites throughout the park. Grass biomass increased with rainfall and on nutrient-rich clay soils. Fire frequency, too, increased with rainfall. Conversely, tree density was greater on sandier soils, where water infiltrates more readily, and in areas where the maximum interval between fires was longer, irrespective of average fire frequency. Elephant density responded positively to tree density, but did not contribute significantly to decreasing tree density. Savanna vegetation structure was reasonably predictable, via a combination of rainfall (favoring grasses), soil (sandy soils favoring trees), and fire (limiting trees until a longer interval between fires allows them to establish). Explicit consideration of bottom-up and top-down interactions may thus contribute to a predictive understanding of savanna vegetation heterogeneity.

Summary 1. Epiphytes have the potential to modify the canopy environments in which they grow. Accurately evaluating the impact of epiphytes can be challenging, since plants without epiphytes may also otherwise differ from host plants, and experimental removal is impractical and difficult to replicate in many forests. 2. We studied the impacts of epiphytes (primarily fruticose lichens and Tillandsia spp.) on host plants (Eulychnia saint-pieana and Caesalpinia spinosa) in two fog ecosystems in Chile (Pan de Azucar) and Peru (Atiquipa). These desert ecosystems sustain very high epiphyte loads and depend heavily on fog-water inputs. Using a combination of artificial substrates and epiphyte removals, we show significant impacts of epiphytes on their host plants. 3. The presence of epiphytes reduced throughfall volumes, reducing fog and rainfall inputs to the soil beneath host plant canopies. 4. Soil moisture loss rate was increased below cacti after removal of epiphytes from sun-facing but not shade-facing branches. This suggests epiphyte effects on hosts are microclimatic. 5. Epiphytes also buffered temperature fluctuations and reduced daytime vapour pressure deficit. 6. Epiphytes can have strong effects on host plant ecophysiology and forest ecosystem processes, making them an important component for models and studies of canopy environments.

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

[1] Our understanding of Earth's carbon climate system depends critically upon interactions between rising atmospheric CO2, changing land use, and nitrogen limitation on vegetation growth. Using a global land model, we show how these factors interact locally to generate the global land carbon sink over the past 200 years. Nitrogen constraints were alleviated by N2 fixation in the tropics and by atmospheric nitrogen deposition in extratropical regions. Nonlinear interactions between land use change and land carbon and nitrogen cycling originated from three major mechanisms: (i) a sink foregone that would have occurred without land use conversion; (ii) an accelerated response of secondary vegetation to CO2 and nitrogen, and (iii) a compounded clearance loss from deforestation. Over time, these nonlinear effects have become increasingly important and reduce the present-day net carbon sink by ~40% or 0.4 PgC yr−1.

Summary Symbiotic di-nitrogen (N2) fixation is a critical biogeochemical process in tropical forests, yet it remains unresolved how fixation is controlled by the availability of soil nitrogen and phosphorus, two nutrients often considered limiting in terrestrial ecosystems. We examine whether individual N2-fixing trees can overcome nitrogen and phosphorus constraints by employing different strategies of nutrient acquisition and use: N2 fixation, phosphatase exudation, mycorrhizal symbiosis and changes in root–shoot ratio or tissue stoichiometry. We grew a common and widespread N2 fixer, Inga punctata, in a full factorial nitrogen and phosphorus addition experiment (each nutrient at three levels) and evaluated whether trees adjusted their strategies of nutrient acquisition to overcome limitation. N2 fixation was controlled by nitrogen availability in phosphorus-sufficient soils, but both fixation and plant growth were constrained by phosphorus in the unamended native phosphorus-poor soils. Despite the investment in both extracellular phosphatases and mycorrhizal symbionts, plants were unable to overcome phosphorus limitation. Our findings support the hypotheses that: (i) N2 fixation is proximately controlled by nitrogen availability, consistent with a facultative fixation strategy, and (ii) N2 fixation and N2 fixer biomass growth are ultimately constrained by soil phosphorus. We found no support for the hypothesis that fixers can overcome phosphorus limitation by trading fixed N2 for soil phosphorus. Synthesis. This study provides new knowledge about how nitrogen and phosphorus interact to regulate tropical N2 fixation by examining a suite of strategies that plants may employ to overcome nutrient limitation. These findings, focused at the organismal level, have broader implications for biogeochemical controls at the ecosystem level in tropical forests.

Humid montane tropical forests are often thought to contain low levels of bioavailable nitrogen. An analysis of the concentration and isotopic signature of nitrate in tropical montane forest streams suggests that these ecosystems may be rich in nitrogen.

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.

Symbiotic dinitrogen (N(2)) fixation is often invoked to explain the N richness of tropical forests as ostensibly N(2)-fixing trees can be a major component of the community. Such arguments assume N(2) fixers are fixing N when present. However, in laboratory experiments, legumes consistently reduce N(2) fixation in response to increased soil N availability. These contrasting views of N(2) fixation as either obligate or facultative have drastically different implications for the N cycle of tropical forests. We tested these models by directly measuring N(2)-fixing root nodules and nitrogenase activity of individual canopy-dominant legume trees (Inga sp.) across several lowland forest types. Fixation was substantial in disturbed forests and some gaps but near zero in the high N soils of mature forest. Our findings suggest that canopy legumes closely regulate N(2) fixation, leading to large variations in N inputs across the landscape, and low symbiotic fixation in mature forests despite abundant legumes.

This corrects the article DOI: 10.1038/nature25783.

Observations of the tropical nitrogen (N) cycle over the past half century indicate that intact tropical forests tend to accumulate and recycle large quantities of N relative to temperate forests, as evidenced by plant and soil N to phosphorus (P) ratios, by P limitation of plant growth in some tropical forests, by an abundance of N-fixing plants, and by sustained export of bioavailable N at the ecosystem scale. However, this apparent up-regulation of the ecosystem N cycle introduces a biogeochemical paradox when considered from the perspective of physiology and evolution of individual plants: The putative source for tropical N richness—symbiotic N fixation—should, in theory, be physiologically down-regulated as internal pools of bioavailable N build. We review the evidence for tropical N richness and evaluate several hypotheses that may explain its emergence and maintenance. We propose a leaky nitrostat model that is capable of resolving the paradox at scales of both ecosystems and individual N-fixing organisms.

Biological nitrogen fixation limits plant growth and carbon exchange at local to global scales. Long-term nutrient manipulation experiments in forests and short-term manipulation experiments in microcosms suggest that the micronutrient molybdenum, a component of the nitrogen-fixing enzyme nitrogenase, limits nitrogen fixation by asymbiotic bacteria in tropical soils in Panama. Nitrogen fixation, the biological conversion of di-nitrogen to plant-available ammonium, is the primary natural input of nitrogen to ecosystems1, and influences plant growth and carbon exchange at local to global scales2,3,4,5,6. The role of this process in tropical forests is of particular concern, as these ecosystems harbour abundant nitrogen-fixing organisms1,4 and represent one third of terrestrial primary production4,7,8. Here we show that the micronutrient molybdenum, a cofactor in the nitrogen-fixing enzyme nitrogenase, limits nitrogen fixation by free-living heterotrophic bacteria in soils of lowland Panamanian forests. We measured the fixation response to long-term nutrient manipulations in intact forests, and to short-term manipulations in soil microcosms. Nitrogen fixation increased sharply in treatments of molybdenum alone, in micronutrient treatments that included molybdenum by design and in treatments with commercial phosphorus fertilizer, in which molybdenum was a ‘hidden’ contaminant. Fixation did not respond to additions of phosphorus that were not contaminated by molybdenum. Our findings show that molybdenum alone can limit asymbiotic nitrogen fixation in tropical forests and raise new questions about the role of molybdenum and phosphorus in the tropical nitrogen cycle. We suggest that molybdenum limitation may be common in highly weathered acidic soils, and may constrain the ability of some forests to acquire new nitrogen in response to CO2 fertilization9.

Inputs of available nitrogen (N) to ecosystems have grown over the recent past. There is limited general understanding of how increased N inputs affect the cycling and retention of other potentially limiting nutrients. Using a plant–soil nutrient model, and by explicitly coupling N and phosphorus (P) in plant biomass, we examine the impact of increasing N supply on the ecosystem cycling and retention of P, assuming that the main impact of N is to increase plant growth. We find divergent responses in the P cycle depending on the specific pathway by which nutrients are lost from the ecosystem. Retention of P is promoted if the relative propensity for loss of plant available P is greater than that for the loss of less readily available organic P. This is the first theoretical demonstration that the coupled response of ecosystem-scale nutrient cycles critically depends on the form of nutrient loss. P retention might be lessened, or reversed, depending on the kinetics and size of a buffering reactive P pool. These properties determine the reactive pool's ability to supply available P. Parameterization of the model across a range of forest ecosystems spanning various environmental and climatic conditions indicates that enhanced plant growth due to increased N should trigger increased P conservation within ecosystems while leading to more dissolved organic P loss. We discuss how the magnitude and direction of the effect of N may also depend on other processes.

The response of tropical forests to climate change will depend on individual plant species' nutritional strategies, which have not been defined in the case of the nitrogen nutrition that is critical to sustaining plant growth and photosynthesis. We used isotope natural abundances to show that a group of tropical plant species with diverse growth strategies (trees and ferns, canopy, and subcanopy) relied on a common pool of inorganic nitrogen, rather than specializing on different nitrogen pools. Moreover, the tropical species we examined changed their dominant nitrogen source abruptly, and in unison, in response to precipitation change. This threshold response indicates a coherent strategy among species to exploit the most available form of nitrogen in soils. The apparent community-wide flexibility in nitrogen uptake suggests that diverse species within tropical forests can physiologically track changes in nitrogen cycling caused by climate change.

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.

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.

The gastro-intestinal tract is an ecosystem containing trillions of commensal bacteria living in symbiosis with the host. These microbiota modulate a variety of our physiological processes, including production of vitamins, absorption of nutrients and development of the immune system. One of their major functions is to fortify the intestinal barrier, thereby helping to prevent pathogens and harmful substances from crossing into the general circulation. Recently, effects of these microbiota on other blood-tissue barriers have also been reported. Here, we review the evidence indicating that gut bacteria play a role in regulating the blood-brain and blood-testis barriers. The underlying mechanisms include control of the expression of tight junction proteins by fermentation products such as butyrate, which also influences the activity of histone deacetylase.

The gut microbiota contributes to postnatal development and maturation by influencing barrier functions of the intestinal wall, the development of the immune system, and the utilisation of nutrients. Recent studies have also implicated a role in the prenatal period since the maternal gut microbiota is altered during pregnancy with a potential role in the regulation of glucose homeostasis and protection against preterm birth. Using as a model system germ-free mice that have never encountered a live bacterium and pathogen-free mice that were reared in an environment free of monitored mouse pathogens, we demonstrated that lack of gut microbiota is associated with an altered hypothalamic-pituitary-adrenal axis (HPA) and impaired placental development. Germ-free (GF) mice displayed elevated serum glucocorticoids and reduced levels of glucocorticoid regulated insulin-like growth factor 2 (IGF2) and peroxisome proliferator-activated receptor (PPAR) β and γ compared to specific pathogen-free (SPF) dams, which correlated with an impairment of placenta development. Morphological analysis revealed reduced labyrinth size, inhibited vascularization and reduced expression of the tight junction proteins in the placenta from GF dams compared to SPF dams. Permeability test using a 1-kDa tracer showed an increased permeability in GF placental barrier. We conclude that the maternal microbiome can influence placental development and we propose that mammalian development, known to have the capacity to modulate placenta size and morphology to ensure the development of the growing offspring, is under the influence of the maternal microbiome, the forgotten This work was supported by grants from Qatar University, VR, Cancerfonden, EU-project TORNADO, and the Singapore Millennium Foundation.

We present a model of plant-nutrient interactions that extends classical resource competition theory to environments in which essential nutrients (resources) are recycled between plant and soil pools and dissolved nutrients are lost through plant-available (i.e., inorganic forms) or plant-unavailable (i.e., complex organic forms) pathways. Losses by dissolved organic pathways can alter ratios of nutrients that are recycled and supplied within the plant-soil system, thereby influencing competition and coexistence among plant species. In special cases, our extended model does not differ from classical models, but in more realistic cases our model introduces new dynamical behavior that influences competitive outcomes. At equilibrium, coexistence still depends on nutrient supply and consumption, but nutrient supply includes recycling and is highly sensitive to whether a species promotes more organic losses of the nutrient that limits its own growth than of nutrients that limit its competitors. Because recycling operates with a time delay compared with consumption, recycling-mediated effects on competition can, under certain conditions, lead to sustained population oscillations. Our findings have implications for how we understand nutrient competition, nutrient cycles, and plant evolutionary strategies.

Accelerated nitrogen (N) inputs can drive nonlinear changes in N cycling, retention, and loss in forest ecosystems. Nitrogen processing in soils is critical to understanding these changes, since soils typically are the largest N sink in forests. To elucidate soil mechanisms that underlie shifts in N cycling across a wide gradient of N supply, we added 15NH415NO3 at nine treatment levels ranging in geometric sequence from 0.2 kg to 640 kg N·ha−1·yr−1 to an unpolluted old-growth temperate forest in southern Chile. We recovered roughly half of 15N tracers in 0–25 cm of soil, primarily in the surface 10 cm. Low to moderate rates of N supply failed to stimulate N leaching, which suggests that most unrecovered 15N was transferred from soils to unmeasured sinks above ground. However, soil solution losses of nitrate increased sharply at inputs >160 kg N·ha−1·yr−1, corresponding to a threshold of elevated soil N availability and declining 15N retention in soil. Soil organic matter (

Inspired by the importance of globally well-constrained carbon:nitrogen: phosphorus (C:N:P) ratios in planktonic biomass to the understanding of nutrient cycles and biotic feedbacks in marine ecosystems, we looked for analogous patterns in forest ecosystems worldwide. We used data from the literature to examine the stoichiometry of C, N, and P in forest foliage and litter on both global and biome levels. Additionally, we examined the scaling of nutrient investments with biomass and production both globally and within biomes to determine if and when these ratios respond to macroscale ecosystem properties (such as nutrient availability). We found that, while global forest C:N:P ratios in both foliage and litter were more variable than those of marine particulate matter, biome level (temperate broadleaf, temperate coniferous, and tropical) ratios were as constrained as marine ratios and statistically distinct from one another. While we were more interested in the relative constancy of the C:N:P ratios than their numerical value we did note, as have others, that the atomic ratios calculated for foliage (1212:28:1) and litter (3007:45:1) reflect the increased proportion of C-rich structural material characteristic of terrestrial vegetation. Carbon : nutrient ratios in litter were consistently higher than in comparable foliar data sets, suggesting that resorption of nutrients is a globally important mechanism, particularly for P. Litter C:N ratios were globally constant despite biome-level differences in foliar C:N; we speculate that this strong coupling may be caused by the significant contribution of immobile cell wall bound proteins to the total foliar N pool. Most ratios scaled isometrically across the range of biomass stocks and production in all biomes sug- gesting that ratios arise directly from physiological constraints and are insensitive to factors leading to shifts in biomass and production. There were, however, important exceptions to this pattern: nutrient investment in broadleaf forest litter and coniferous forest foliage increased disproportionately relative to C with increasing biomass and production sug- gesting a systematic influence of macroscopic factors on ratios.

Biological, atmospheric, and geochemical processes interact to shape how element cycles and nutrient losses develop within newly formed landscapes. We examined losses of nitrogen (N), phosphorus (P), and base cations across a four-million-year substrate age gradient of Hawaiian montane tropical forests, with the goal of understanding how losses depend on changes in biotic demand, weathering, and atmospheric sources. We were particularly interested in whether losses of nutrients that are not subject to traditional mechanisms of biotic availability could influence ecosystem fertility and nutrient limitation over time. Over a three-year period we sampled nutrient outputs in soil solutions below the active plant-soil system and small streams, gaseous N losses (NO, N2O, and N2), and pools and transformations of N in soils. Weathering was the major determinant of ecosystem losses of P, of base cations and Si, and of ecosystem acid-base status. Sharp reductions in weathering inputs after 20 000 years of forest development caused dramatically lower outputs of P (;65% reduction), Ca 2 1 (;99%), and Si (;94%), to rates that matched inputs from dilute sea-salt and dust aerosols. Internal production of organic acids, in combination with low weathering, caused highly acidic soil waters (pH , 5.0) with elevated Al (up to 300 mg/L) and Ca:Al ratios (,0.3) below values considered critical thresholds for many plant species. Long-term N and P interactions were more complex than predicted by the Walker and Syers model, with important influences of N and P loss pathways that were not subject to direct biotic availability. While losses of available forms of dissolved N and P, and N gases followed (as predicted) ecosystem nutrient availability, significant dissolved organic N (DON) and dissolved organic P (DOP) losses occurred independent of ecosystem N or P status. DON losses were not sufficient (relative to external inputs) to sustain N limitation beyond 20 000 years, while dissolved P losses remained large enough to maintain P lim- itation in older forests. Forests developed high N:P loss ratios over time ( .300 on mass weight basis) due to efficient P recycling and unexpectedly high N throughputs (4-9 kg N·ha 21 ·yr 21 ) by either N fixation and/or N deposition.

The natural removal of NO3− by denitrification within riparian zones of streams and rivers is an area of considerable interest owing to its potential to minimize the impacts of excess anthropogenic loadings. In this study we utilize natural variations in stable N isotopic compositions of NO3− and NH4+ within a transect of shallow wells extending 4 m inland from Smith Creek, a southwestern Michigan stream, to provide insight into microbial processes and the extent of NO3− removal within a soil–stream interface. Within this region three water masses with unique biogeochemical characteristics intersect: a shallow flow rich in NH4+ and dissolved organic carbon (DOC), a deep groundwater mass rich in NO3− but depleted in DOC, and stream water low in NO3−, NH4+, and DOC. N isotope values for NO3− within the well transect were highly variable (−7.7–34.1‰) and reflected intense microbial activity within this narrow region. Isotopic variation was primarily controlled by upwelling of deep groundwater near the stream...

An experimental tracer addition of 84 Sr to an unpolluted temperate forest site in southern Chile, as well as the natural variation of 87 Sr/ 86 Sr within plants and soils, indicates that mechanisms in shallow soil organic horizons are of key importance for retaining and recycling atmospheric cation inputs at scales of decades or less. The dominant tree species Nothofagus nitida feeds nearly exclusively (>90%) on cations of atmospheric origin, despite strong variations in tree size and location in the forest landscape. Our results illustrate that ( i ) unpolluted temperate forests can become nutritionally decoupled from deeper weathering processes, virtually functioning as atmospherically fed ecosystems, and ( ii ) base cation turnover times are considerably more rapid than previously recognized in the plant available pool of soil. These results challenge the prevalent paradigm that plants largely feed on rock-derived cations and have important implications for understanding sensitivity of forests to air pollution.