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.

Geographic range of plants drives long-term climate change.

Long computation times in vegetation and climate models hamper our ability to evaluate the potentially powerful role of plants on weathering and carbon sequestration over the Phanerozoic Eon. Simulated vegetation over deep time is often homogenous, and disregards the spatial distribution of plants and the impact of local climatic variables on plant function. Here we couple a fast vegetation model (FLORA) to a spatially-resolved long-term climate-biogeochemical model (SCION), to assess links between plant geographical range, the long-term carbon cycle and climate. Model results show lower rates of carbon fixation and up to double the previously predicted atmospheric CO2 concentration due to a limited plant geographical range over the arid Pangea supercontinent. The Mesozoic dispersion of the continents increases modelled plant geographical range from 65% to > 90%, amplifying global CO2 removal, consistent with geological data. We demonstrate that plant geographical range likely exerted a major, under-explored control on long-term climate change.

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

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

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

Widespread herbivory cost in tropical nitrogen-fixing tree species.

Recent observations suggest that the large carbon sink in mature and recovering forests may be strongly limited by nitrogen1-3. Nitrogen-fixing trees (fixers) in symbiosis with bacteria provide the main natural source of new nitrogen to tropical forests3,4. However, abundances of fixers are tightly constrained5-7, highlighting the fundamental unanswered question of what limits new nitrogen entering tropical ecosystems. Here we examine whether herbivory by animals is responsible for limiting symbiotic nitrogen fixation in tropical forests. We evaluate whether nitrogen-fixing trees experience more herbivory than other trees, whether herbivory carries a substantial carbon cost, and whether high herbivory is a result of herbivores targeting the nitrogen-rich leaves of fixers8,9. We analysed 1,626 leaves from 350 seedlings of 43 tropical tree species in Panama and found that: (1) although herbivory reduces the growth and survival of all seedlings, nitrogen-fixing trees undergo 26% more herbivory than non-fixers; (2) fixers have 34% higher carbon opportunity costs owing to herbivory than non-fixers, exceeding the metabolic cost of fixing nitrogen; and (3) the high herbivory of fixers is not driven by high leaf nitrogen. Our findings reveal that herbivory may be sufficient to limit tropical symbiotic nitrogen fixation and could constrain its role in alleviating nitrogen limitation on the tropical carbon sink.

Climate windows of opportunity for plant expansion during the Phanerozoic.

Earth's long-term climate may have profoundly influenced plant evolution. Local climatic factors, including water availability, light, and temperature, play a key role in plant physiology and growth, and have fluctuated substantially over geological time. However, the impact of these key climate variables on global plant biomass across the Phanerozoic has not yet been established. Linking climate and dynamic vegetation modelling, we identify two key 'windows of opportunity' during the Ordovician and Jurassic-Paleogene capable of supporting dramatic expansions of potential plant biomass. These conditions are driven by continental dispersion, paleolatitude of continental area and a lack of glaciation, allowing for an intense hydrological cycle and greater water availability. These windows coincide with the initial expansion of land plants and the later angiosperm radiation. Our findings suggest that the timing and expansion of habitable space for plants played an important role in plant evolution and diversification.

Fire decreases soil enzyme activities and reorganizes microbially mediated nutrient cycles: A meta-analysis.

The biogeochemical signature of fire shapes the functioning of many ecosystems. Fire changes nutrient cycles not only by volatilizing plant material, but also by altering organic matter decomposition, a process regulated by soil extracellular enzyme activities (EEAs). However, our understanding of fire effects on EEAs and their feedbacks to nutrient cycles is incomplete. We conducted a meta-analysis with 301 field studies and found that fire significantly decreased EEAs by ~20%-40%. Fire decreased EEAs by reducing soil microbial biomass and organic matter substrates. Soil nitrogen-acquiring EEA declined alongside decreasing available nitrogen, likely from fire-driven volatilization of nitrogen and decreased microbial activity. Fire decreased soil phosphorus-acquiring EEA but increased available phosphorus, likely from pyro-mineralization of organic phosphorus. These findings suggest that fire suppresses soil microbes and consumes their substrates, thereby slowing microbially mediated nutrient cycles (especially phosphorus) via decreased EEAs. These changes can become increasingly important as fire frequency and severity in many ecosystems continue to shift in response to global change.

A starting guide to root ecology: strengthening ecological concepts and standardising root classification, sampling, processing and trait measurements.

In the context of a recent massive increase in research on plant root functions and their impact on the environment, root ecologists currently face many important challenges to keep on generating cutting-edge, meaningful and integrated knowledge. Consideration of the below-ground components in plant and ecosystem studies has been consistently called for in recent decades, but methodology is disparate and sometimes inappropriate. This handbook, based on the collective effort of a large team of experts, will improve trait comparisons across studies and integration of information across databases by providing standardised methods and controlled vocabularies. It is meant to be used not only as starting point by students and scientists who desire working on below-ground ecosystems, but also by experts for consolidating and broadening their views on multiple aspects of root ecology. Beyond the classical compilation of measurement protocols, we have synthesised recommendations from the literature to provide key background knowledge useful for: (1) defining below-ground plant entities and giving keys for their meaningful dissection, classification and naming beyond the classical fine-root vs coarse-root approach; (2) considering the specificity of root research to produce sound laboratory and field data; (3) describing typical, but overlooked steps for studying roots (e.g. root handling, cleaning and storage); and (4) gathering metadata necessary for the interpretation of results and their reuse. Most importantly, all root traits have been introduced with some degree of ecological context that will be a foundation for understanding their ecological meaning, their typical use and uncertainties, and some methodological and conceptual perspectives for future research. Considering all of this, we urge readers not to solely extract protocol recommendations for trait measurements from this work, but to take a moment to read and reflect on the extensive information contained in this broader guide to root ecology, including sections I-VII and the many introductions to each section and root trait description. Finally, it is critical to understand that a major aim of this guide is to help break down barriers between the many subdisciplines of root ecology and ecophysiology, broaden researchers' views on the multiple aspects of root study and create favourable conditions for the inception of comprehensive experiments on the role of roots in plant and ecosystem functioning.

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.

Long-term thermal sensitivity of Earth's tropical forests.

The sensitivity of tropical forest carbon to climate is a key uncertainty in predicting global climate change. Although short-term drying and warming are known to affect forests, it is unknown if such effects translate into long-term responses. Here, we analyze 590 permanent plots measured across the tropics to derive the equilibrium climate controls on forest carbon. Maximum temperature is the most important predictor of aboveground biomass (-9.1 megagrams of carbon per hectare per degree Celsius), primarily by reducing woody productivity, and has a greater impact per °C in the hottest forests (>32.2°C). Our results nevertheless reveal greater thermal resilience than observations of short-term variation imply. To realize the long-term climate adaptation potential of tropical forests requires both protecting them and stabilizing Earth's climate.

Tropical carbon sink accelerated by symbiotic dinitrogen fixation.

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.

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.

Have Synergies Between Nitrogen Deposition and Atmospheric CO2 Driven the Recent Enhancement of the Terrestrial Carbon Sink?

The terrestrial carbon sink has increased since the turn of this century at a time of increased fossil fuel burning, yet the mechanisms enhancing this sink are not fully understood. Here we assess the hypothesis that regional increases in nitrogen deposition since the early 2000s has alleviated nitrogen limitation and worked in tandem with enhanced CO2 fertilization to increase ecosystem productivity and carbon sequestration, providing a causal link between the parallel increases in emissions and the global land carbon sink. We use the Community Land Model (CLM4.5-BGC) to estimate the influence of changes in atmospheric CO2, nitrogen deposition, climate, and their interactions to changes in net primary production and net biome production. We focus on two periods, 1901-2016 and 1990-2016, to estimate changes in land carbon fluxes relative to historical and contemporary baselines, respectively. We find that over the historical period, nitrogen deposition (14%) and carbon-nitrogen synergy (14%) were significant contributors to the current terrestrial carbon sink, suggesting that long-term increases in nitrogen deposition led to a substantial increase in CO2 fertilization. However, relative to the contemporary baseline, changes in nitrogen deposition and carbon-nitrogen synergy had no substantial contribution to the 21st century increase in global carbon uptake. Nonetheless, we find that increased nitrogen deposition in East Asia since the early 1990s contributed 50% to the overall increase in net biome production over this region, highlighting the importance of carbon-nitrogen interactions. Therefore, potential large-scale changes in nitrogen deposition could have a significant impact on terrestrial carbon cycling and future climate.

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.

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.This article is part of a discussion meeting issue 'The Rhynie cherts: our earliest terrestrial ecosystem revisited'.

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.

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.

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.

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.

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.