Biome-scale nitrogen fixation strategies selected by climatic constraints on nitrogen cycle

Dinitrogen fixation by plants (in symbiosis with root bacteria) is a major source of new nitrogen for land ecosystems 1. A long-standing puzzle 2 is that trees capable of nitrogen fixation are abundant in nitrogen-rich tropical forests, but absent or restricted to early successional stages in nitrogen-poor extra-tropical forests. This biome-scale pattern presents an evolutionary paradox 3, given that the physiological cost 4 of nitrogen fixation predicts the opposite pattern: fixers should be out-competed by non-fixers in nitrogen-rich conditions, but competitively superior in nitrogen-poor soils. Here we evaluate whether this paradox can be explained by the existence of different fixation strategies in tropical versus extra-tropical trees: facultative fixers (capable of downregulating fixation 5,6 by sanctioning mutualistic bacteria 7) are common in the tropics, whereas obligate fixers (less able to downregulate fixation) dominate at higher latitudes. Using a game-theoretic approach, we assess the ecological and evolutionary conditions under which these fixation strategies emerge, and examine their dependence on climate-driven differences in the nitrogen cycle. We show that in the tropics, transient soil nitrogen deficits following disturbance and rapid tree growth favour a facultative strategy and the coexistence of fixers and non-fixers. In contrast, sustained nitrogen deficits following disturbance in extra-tropical forests favour an obligate fixation strategy, and cause fixers to be excluded in late successional stages. We conclude that biome-scale differences in the abundance of nitrogen fixers can be explained by the interaction between individual plant strategies and climatic constraints on the nitrogen cycle over evolutionary time

Nutrient acquisition by symbiotic fungi governs Palaeozoic climate transition

Fossil evidence from the Rhynie chert indicates that early land plants, which evolved in a high-CO2 atmosphere during the Palaeozoic Era, hosted diverse fungal symbionts. It is hypothesized that the rise of early non-vascular land plants, and the later evolution of roots and vasculature, drove the long-term shift towards a high-oxygen, low CO2 climate that eventually permitted the evolution of mammals and, ultimately, humans. However, very little is known about the productivity of the early terrestrial biosphere, which depended on the acquisition of the limiting nutrient phosphorus via fungal symbiosis. Recent laboratory experiments have shown that plant–fungal symbiotic function is specific to fungal identity, with carbon-for-phosphorus exchange being either enhanced or suppressed under superambient CO2. By incorporating these experimental findings into a biogeochemical model, we show that the differences in these symbiotic nutrient acquisition strategies could greatly alter the plant-driven changes to climate, allowing drawdown of CO2 to glacial levels, and altering the nature of the rise of oxygen. We conclude that an accurate depiction of plant–fungal symbiotic systems, informed by high-CO2 experiments, is key to resolving the question of how the first terrestrial ecosystems altered our planet

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

Rapid nitrogen fixation by canopy microbiome in tropical forest determined by both phosphorus and molybdenum

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

Nitrogen-fixing tree abundance in higher-latitude North America is not constrained by diversity

The rarity of nitrogen (N)-fixing trees in frequently N-limited higher-latitude (here, > 35°) forests is a central biogeochemical paradox. One hypothesis for their rarity is that evolutionary constraints limit N-fixing tree diversity, preventing N-fixing species from filling available niches in higher-latitude forests. Here, we test this hypothesis using data from the USA and Mexico. N-fixing trees comprise only a slightly smaller fraction of taxa at higher vs. lower latitudes (8% vs. 11% of genera), despite 11-fold lower abundance (1.2% vs. 12.7% of basal area). Furthermore, N-fixing trees are abundant but belong to few species on tropical islands, suggesting that low absolute diversity does not limit their abundance. Rhizobial taxa dominate N-fixing tree richness at lower latitudes, whereas actinorhizal species do at higher latitudes. Our results suggest that low diversity does not explain N-fixing trees' rarity in higher-latitude forests. Therefore, N limitation in higher-latitude forests likely results from ecological constraints on N fixation

Nitrogen-fixing tree abundance in higher-latitude North America is not constrained by diversity

The rarity of nitrogen (N)-fixing trees in frequently N-limited higher-latitude (here, > 35°) forests is a central biogeochemical paradox. One hypothesis for their rarity is that evolutionary constraints limit N-fixing tree diversity, preventing N-fixing species from filling available niches in higher-latitude forests. Here, we test this hypothesis using data from the USA and Mexico. N-fixing trees comprise only a slightly smaller fraction of taxa at higher vs. lower latitudes (8% vs. 11% of genera), despite 11-fold lower abundance (1.2% vs. 12.7% of basal area). Furthermore, N-fixing trees are abundant but belong to few species on tropical islands, suggesting that low absolute diversity does not limit their abundance. Rhizobial taxa dominate N-fixing tree richness at lower latitudes, whereas actinorhizal species do at higher latitudes. Our results suggest that low diversity does not explain N-fixing trees' rarity in higher-latitude forests. Therefore, N limitation in higher-latitude forests likely results from ecological constraints on N fixation

Limited biomass recovery from gold mining in Amazonian forests

1. Gold mining has rapidly increased across the Amazon Basin in recent years, especially in the Guiana shield, where it is responsible for >90% of total deforestation. However, the ability of forests to recover from gold mining activities remains largely unquantified. 2. Forest inventory plots were installed on recently abandoned mines in two major mining regions in Guyana, and re‐censused 18 months later, to provide the first ground‐based quantification of gold mining impacts on Amazon forest biomass recovery. 3. We found that woody biomass recovery rates on abandoned mining pits and tailing ponds are among the lowest ever recorded for tropical forests, with close to no woody biomass recovery after 3–4 years. 4. On the overburden sites (i.e. areas not mined but where excavated soil is deposited), however, above‐ground biomass recovery rates (0.4–5.4 Mg ha−1 year−1) were within the range of those recorded in other secondary forests across the Neotropics following abandonment of pastures and agricultural lands. 5. Our results suggest that forest recovery is more strongly limited by severe mining‐induced depletion of soil nutrients, especially nitrogen, than by mercury contamination, due to slowing of growth in nutrient‐stripped soils. 6. We estimate that the slow recovery rates in mining pits and ponds currently reduce carbon sequestration across Amazonian secondary forests by ~21,000 t C/year, compared to the carbon that would have accumulated following more traditional land uses such as agriculture or pasture. 7. Synthesis and applications. To achieve large‐scale restoration targets, Guyana and other Amazonian countries will be challenged to remediate previously mined lands. The recovery process is highly dependent on nitrogen availability rather than mercury contamination, affecting woody biomass regrowth. The significant recovery in overburden zones indicates that one potential active remediation strategy to promote biomass recovery may be to backfill mining pits and ponds with excavated soil

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

Mapping tropical disturbed forests using multi-decadal 30 m optical satellite imagery

Tropical disturbed forests play an important role in global carbon sequestration due to their rapid post-disturbance biomass accumulation rates. However, the accurate estimation of the carbon sequestration capacity of disturbed forests is still challenging due to large uncertainties in their spatial distribution. Using Google Earth Engine (GEE), we developed a novel approach to map cumulative disturbed forest areas based on the 27-year time-series of Landsat surface reflectance imagery. This approach integrates single date features with temporal characteristics from six time-series trajectories (two Landsat shortwave infrared bands and four vegetation indices) using a random forest machine learning classification algorithm. We demonstrated the feasibility of this method to map disturbed forests in three different forest ecoregions (seasonal, moist and dry forest) in Mato Grosso, Brazil, and found that the overall mapping accuracy was high, ranging from 81.3% for moist forest to 86.1% for seasonal forest. According to our classification, dry forest ecoregion experienced the most severe disturbances with 41% of forests being disturbed by 2010, followed by seasonal forest and moist forest ecoregions. We further separated disturbed forests into degraded old-growth forests and post-deforestation regrowth forests based on an existing post-deforestation land use map (TerraClass) and found that the area of degraded old-growth forests was up to 62% larger than the extent of post-deforestation regrowth forests, with 18% of old-growth forests actually being degraded. Application of this new classification approach to other tropical areas will provide a better constraint on the spatial extent of disturbed forest areas in Tropics and ultimately towards a better understanding of their importance in the global carbon cycle

Asthma exacerbation and proximity of residence to major roads: a population-based matched case-control study among the pediatric Medicaid population in Detroit, Michigan

<p>Abstract</p> <p>Background</p> <p>The relationship between asthma and traffic-related pollutants has received considerable attention. The use of individual-level exposure measures, such as residence location or proximity to emission sources, may avoid ecological biases.</p> <p>Method</p> <p>This study focused on the pediatric Medicaid population in Detroit, MI, a high-risk population for asthma-related events. A population-based matched case-control analysis was used to investigate associations between acute asthma outcomes and proximity of residence to major roads, including freeways. Asthma cases were identified as all children who made at least one asthma claim, including inpatient and emergency department visits, during the three-year study period, 2004-06. Individually matched controls were randomly selected from the rest of the Medicaid population on the basis of non-respiratory related illness. We used conditional logistic regression with distance as both categorical and continuous variables, and examined non-linear relationships with distance using polynomial splines. The conditional logistic regression models were then extended by considering multiple asthma states (based on the frequency of acute asthma outcomes) using polychotomous conditional logistic regression.</p> <p>Results</p> <p>Asthma events were associated with proximity to primary roads with an odds ratio of 0.97 (95% CI: 0.94, 0.99) for a 1 km increase in distance using conditional logistic regression, implying that asthma events are less likely as the distance between the residence and a primary road increases. Similar relationships and effect sizes were found using polychotomous conditional logistic regression. Another plausible exposure metric, a reduced form response surface model that represents atmospheric dispersion of pollutants from roads, was not associated under that exposure model.</p> <p>Conclusions</p> <p>There is moderately strong evidence of elevated risk of asthma close to major roads based on the results obtained in this population-based matched case-control study.</p