Integrated global assessment of the natural forest carbon potential.

Forests are a substantial terrestrial carbon sink, but anthropogenic changes in land use and climate have considerably reduced the scale of this system1. Remote-sensing estimates to quantify carbon losses from global forests2-5 are characterized by considerable uncertainty and we lack a comprehensive ground-sourced evaluation to benchmark these estimates. Here we combine several ground-sourced6 and satellite-derived approaches2,7,8 to evaluate the scale of the global forest carbon potential outside agricultural and urban lands. Despite regional variation, the predictions demonstrated remarkable consistency at a global scale, with only a 12% difference between the ground-sourced and satellite-derived estimates. At present, global forest carbon storage is markedly under the natural potential, with a total deficit of 226 Gt (model range = 151-363 Gt) in areas with low human footprint. Most (61%, 139 Gt C) of this potential is in areas with existing forests, in which ecosystem protection can allow forests to recover to maturity. The remaining 39% (87 Gt C) of potential lies in regions in which forests have been removed or fragmented. Although forests cannot be a substitute for emissions reductions, our results support the idea2,3,9 that the conservation, restoration and sustainable management of diverse forests offer valuable contributions to meeting global climate and biodiversity targets.

Global imprint of mycorrhizal fungi on whole-plant nutrient economics.

Mycorrhizal fungi are critical members of the plant microbiome, forming a symbiosis with the roots of most plants on Earth. Most plant species partner with either arbuscular or ectomycorrhizal fungi, and these symbioses are thought to represent plant adaptations to fast and slow soil nutrient cycling rates. This generates a second hypothesis, that arbuscular and ectomycorrhizal plant species traits complement and reinforce these fungal strategies, resulting in nutrient acquisitive vs. conservative plant trait profiles. Here we analyzed 17,764 species level trait observations from 2,940 woody plant species to show that mycorrhizal plants differ systematically in nitrogen and phosphorus economic traits. Differences were clearest in temperate latitudes, where ectomycorrhizal plant species are more nitrogen use- and phosphorus use-conservative than arbuscular mycorrhizal species. This difference is reflected in both aboveground and belowground plant traits and is robust to controlling for evolutionary history, nitrogen fixation ability, deciduousness, latitude, and species climate niche. Furthermore, mycorrhizal effects are large and frequently similar to or greater in magnitude than the influence of plant nitrogen fixation ability or deciduous vs. evergreen leaf habit. Ectomycorrhizal plants are also more nitrogen conservative than arbuscular plants in boreal and tropical ecosystems, although differences in phosphorus use are less apparent outside temperate latitudes. Our findings bolster current theories of ecosystems rooted in mycorrhizal ecology and support the hypothesis that plant mycorrhizal association is linked to the evolution of plant nutrient economic strategies.

From pools to flow: The PROMISE framework for new insights on soil carbon cycling in a changing world.

Soils represent the largest terrestrial reservoir of organic carbon, and the balance between soil organic carbon (SOC) formation and loss will drive powerful carbon-climate feedbacks over the coming century. To date, efforts to predict SOC dynamics have rested on pool-based models, which assume classes of SOC with internally homogenous physicochemical properties. However, emerging evidence suggests that soil carbon turnover is not dominantly controlled by the chemistry of carbon inputs, but rather by restrictions on microbial access to organic matter in the spatially heterogeneous soil environment. The dynamic processes that control the physicochemical protection of carbon translate poorly to pool-based SOC models; as a result, we are challenged to mechanistically predict how environmental change will impact movement of carbon between soils and the atmosphere. Here, we propose a novel conceptual framework to explore controls on belowground carbon cycling: Probabilistic Representation of Organic Matter Interactions within the Soil Environment (PROMISE). In contrast to traditional model frameworks, PROMISE does not attempt to define carbon pools united by common thermodynamic or functional attributes. Rather, the PROMISE concept considers how SOC cycling rates are governed by the stochastic processes that influence the proximity between microbial decomposers and organic matter, with emphasis on their physical location in the soil matrix. We illustrate the applications of this framework with a new biogeochemical simulation model that traces the fate of individual carbon atoms as they interact with their environment, undergoing biochemical transformations and moving through the soil pore space. We also discuss how the PROMISE framework reshapes dialogue around issues related to SOC management in a changing world. We intend the PROMISE framework to spur the development of new hypotheses, analytical tools, and model structures across disciplines that will illuminate mechanistic controls on the flow of carbon between plant, soil, and atmospheric pools.

Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage.

Soil contains more carbon than the atmosphere and vegetation combined. Understanding the mechanisms controlling the accumulation and stability of soil carbon is critical to predicting the Earth's future climate. Recent studies suggest that decomposition of soil organic matter is often limited by nitrogen availability to microbes and that plants, via their fungal symbionts, compete directly with free-living decomposers for nitrogen. Ectomycorrhizal and ericoid mycorrhizal (EEM) fungi produce nitrogen-degrading enzymes, allowing them greater access to organic nitrogen sources than arbuscular mycorrhizal (AM) fungi. This leads to the theoretical prediction that soil carbon storage is greater in ecosystems dominated by EEM fungi than in those dominated by AM fungi. Using global data sets, we show that soil in ecosystems dominated by EEM-associated plants contains 70% more carbon per unit nitrogen than soil in ecosystems dominated by AM-associated plants. The effect of mycorrhizal type on soil carbon is independent of, and of far larger consequence than, the effects of net primary production, temperature, precipitation and soil clay content. Hence the effect of mycorrhizal type on soil carbon content holds at the global scale. This finding links the functional traits of mycorrhizal fungi to carbon storage at ecosystem-to-global scales, suggesting that plant-decomposer competition for nutrients exerts a fundamental control over the terrestrial carbon cycle.

Exploring the role of ectomycorrhizal fungi in soil carbon dynamics.

The extent to which ectomycorrhizal (ECM) fungi enable plants to access organic nitrogen (N) bound in soil organic matter (SOM) and transfer this growth-limiting nutrient to their plant host, has important implications for our understanding of plant-fungal interactions, and the cycling and storage of carbon (C) and N in terrestrial ecosystems. Empirical evidence currently supports a range of perspectives, suggesting that ECM vary in their ability to provide their host with N bound in SOM, and that this capacity can both positively and negatively influence soil C storage. To help resolve the multiplicity of observations, we gathered a group of researchers to explore the role of ECM fungi in soil C dynamics, and propose new directions that hold promise to resolve competing hypotheses and contrasting observations. In this Viewpoint, we summarize these deliberations and identify areas of inquiry that hold promise for increasing our understanding of these fundamental and widespread plant symbionts and their role in ecosystem-level biogeochemistry.

Nitrogen limitation of decomposition and decay: How can it occur?

The availability of nitrogen (N) is a critical control on the cycling and storage of soil carbon (C). Yet, there are conflicting conceptual models to explain how N availability influences the decomposition of organic matter by soil microbial communities. Several lines of evidence suggest that N availability limits decomposition; the earliest stages of leaf litter decay are associated with a net import of N from the soil environment, and both observations and models show that high N organic matter decomposes more rapidly. In direct contrast to these findings, experimental additions of inorganic N to soils broadly show a suppression of microbial activity, which is inconsistent with N limitation of decomposition. Resolving this apparent contradiction is critical to representing nutrient dynamics in predictive ecosystem models under a multitude of global change factors that alter soil N availability. Here, we propose a new conceptual framework, the Carbon, Acidity, and Mineral Protection hypothesis, to understand the effects of N availability on soil C cycling and storage and explore the predictions of this framework with a mathematical model. Our model simulations demonstrate that N addition can have opposing effects on separate soil C pools (particulate and mineral-protected carbon) because they are differentially affected by microbial biomass growth. Moreover, changes in N availability are frequently linked to shifts in soil pH or osmotic stress, which can independently affect microbial biomass dynamics and mask N stimulation of microbial activity. Thus, the net effect of N addition on soil C is dependent upon interactions among microbial physiology, soil mineralogy, and soil acidity. We believe that our synthesis provides a broadly applicable conceptual framework to understand and predict the effect of changes in soil N availability on ecosystem C cycling under global change.

Continental-scale nitrogen pollution is shifting forest mycorrhizal associations and soil carbon stocks.

Most tree roots on Earth form a symbiosis with either ecto- or arbuscular mycorrhizal fungi. Nitrogen fertilization is hypothesized to favor arbuscular mycorrhizal tree species at the expense of ectomycorrhizal species due to differences in fungal nitrogen acquisition strategies, and this may alter soil carbon balance, as differences in forest mycorrhizal associations are linked to differences in soil carbon pools. Combining nitrogen deposition data with continental-scale US forest data, we show that nitrogen pollution is spatially associated with a decline in ectomycorrhizal vs. arbuscular mycorrhizal trees. Furthermore, nitrogen deposition has contrasting effects on arbuscular vs. ectomycorrhizal demographic processes, favoring arbuscular mycorrhizal trees at the expense of ectomycorrhizal trees, and is spatially correlated with reduced soil carbon stocks. This implies future changes in nitrogen deposition may alter the capacity of forests to sequester carbon and offset climate change via interactions with the forest microbiome.

Interactions among plants, bacteria, and fungi reduce extracellular enzyme activities under long-term N fertilization.

Atmospheric nitrogen (N) deposition has enhanced soil carbon (C) stocks in temperate forests. Most research has posited that these soil C gains are driven primarily by shifts in fungal community composition with elevated N leading to declines in lignin degrading Basidiomycetes. Recent research, however, suggests that plants and soil microbes are dynamically intertwined, whereby plants send C subsidies to rhizosphere microbes to enhance enzyme production and the mobilization of N. Thus, under elevated N, trees may reduce belowground C allocation leading to cascading impacts on the ability of microbes to degrade soil organic matter through a shift in microbial species and/or a change in plant-microbe interactions. The objective of this study was to determine the extent to which couplings among plant, fungal, and bacterial responses to N fertilization alter the activity of enzymes that are the primary agents of soil decomposition. We measured fungal and bacterial community composition, root-microbial interactions, and extracellular enzyme activity in the rhizosphere, bulk, and organic horizon of soils sampled from a long-term (>25 years), whole-watershed, N fertilization experiment at the Fernow Experimental Forest in West Virginia, USA. We observed significant declines in plant C investment to fine root biomass (24.7%), root morphology, and arbuscular mycorrhizal (AM) colonization (55.9%). Moreover, we found that declines in extracellular enzyme activity were significantly correlated with a shift in bacterial community composition, but not fungal community composition. This bacterial community shift was also correlated with reduced AM fungal colonization indicating that declines in plant investment belowground drive the response of bacterial community structure and function to N fertilization. Collectively, we find that enzyme activity responses to N fertilization are not solely driven by fungi, but instead reflect a whole ecosystem response, whereby declines in the strength of belowground C investment to gain N cascade through the soil environment.

Ectomycorrhizal fungi slow soil carbon cycling.

Respiration of soil organic carbon is one of the largest fluxes of CO2 on earth. Understanding the processes that regulate soil respiration is critical for predicting future climate. Recent work has suggested that soil carbon respiration may be reduced by competition for nitrogen between symbiotic ectomycorrhizal fungi that associate with plant roots and free-living microbial decomposers, which is consistent with increased soil carbon storage in ectomycorrhizal ecosystems globally. However, experimental tests of the mycorrhizal competition hypothesis are lacking. Here we show that ectomycorrhizal roots and hyphae decrease soil carbon respiration rates by up to 67% under field conditions in two separate field exclusion experiments, and this likely occurs via competition for soil nitrogen, an effect larger than 2 °C soil warming. These findings support mycorrhizal competition for nitrogen as an independent driver of soil carbon balance and demonstrate the need to understand microbial community interactions to predict ecosystem feedbacks to global climate.

Historical precipitation predictably alters the shape and magnitude of microbial functional response to soil moisture.

Soil moisture constrains the activity of decomposer soil microorganisms, and in turn the rate at which soil carbon returns to the atmosphere. While increases in soil moisture are generally associated with increased microbial activity, historical climate may constrain current microbial responses to moisture. However, it is not known if variation in the shape and magnitude of microbial functional responses to soil moisture can be predicted from historical climate at regional scales. To address this problem, we measured soil enzyme activity at 12 sites across a broad climate gradient spanning 442-887 mm mean annual precipitation. Measurements were made eight times over 21 months to maximize sampling during different moisture conditions. We then fit saturating functions of enzyme activity to soil moisture and extracted half saturation and maximum activity parameter values from model fits. We found that 50% of the variation in maximum activity parameters across sites could be predicted by 30-year mean annual precipitation, an indicator of historical climate, and that the effect is independent of variation in temperature, soil texture, or soil carbon concentration. Based on this finding, we suggest that variation in the shape and magnitude of soil microbial response to soil moisture due to historical climate may be remarkably predictable at regional scales, and this approach may extend to other systems. If historical contingencies on microbial activities prove to be persistent in the face of environmental change, this approach also provides a framework for incorporating historical climate effects into biogeochemical models simulating future global change scenarios.

Divergence in plant and microbial allocation strategies explains continental patterns in microbial allocation and biogeochemical fluxes.

Allocation trade-offs shape ecological and biogeochemical phenomena at local to global scale. Plant allocation strategies drive major changes in ecosystem carbon cycling. Microbial allocation to enzymes that decompose carbon vs. organic nutrients may similarly affect ecosystem carbon cycling. Current solutions to this allocation problem prioritise stoichiometric tradeoffs implemented in plant ecology. These solutions may not maximise microbial growth and fitness under all conditions, because organic nutrients are also a significant carbon resource for microbes. I created multiple allocation frameworks and simulated microbial growth using a microbial explicit biogeochemical model. I demonstrate that prioritising stoichiometric trade-offs does not optimise microbial allocation, while exploiting organic nutrients as carbon resources does. Analysis of continental-scale enzyme data supports the allocation patterns predicted by this framework, and modelling suggests large deviations in soil C loss based on which strategy is implemented. Therefore, understanding microbial allocation strategies will likely improve our understanding of carbon cycling and climate.

Fungal community composition predicts forest carbon storage at a continental scale.

Forest soils harbor hyper-diverse microbial communities which fundamentally regulate carbon and nutrient cycling across the globe. Directly testing hypotheses on how microbiome diversity is linked to forest carbon storage has been difficult, due to a lack of paired data on microbiome diversity and in situ observations of forest carbon accumulation and storage. Here, we investigated the relationship between soil microbiomes and forest carbon across 238 forest inventory plots spanning 15 European countries. We show that the composition and diversity of fungal, but not bacterial, species is tightly coupled to both forest biotic conditions and a seven-fold variation in tree growth rates and biomass carbon stocks when controlling for the effects of dominant tree type, climate, and other environmental factors. This linkage is particularly strong for symbiotic endophytic and ectomycorrhizal fungi known to directly facilitate tree growth. Since tree growth rates in this system are closely and positively correlated with belowground soil carbon stocks, we conclude that fungal composition is a strong predictor of overall forest carbon storage across the European continent.

Positive feedbacks and alternative stable states in forest leaf types.

The emergence of alternative stable states in forest systems has significant implications for the functioning and structure of the terrestrial biosphere, yet empirical evidence remains scarce. Here, we combine global forest biodiversity observations and simulations to test for alternative stable states in the presence of evergreen and deciduous forest types. We reveal a bimodal distribution of forest leaf types across temperate regions of the Northern Hemisphere that cannot be explained by the environment alone, suggesting signatures of alternative forest states. Moreover, we empirically demonstrate the existence of positive feedbacks in tree growth, recruitment and mortality, with trees having 4-43% higher growth rates, 14-17% higher survival rates and 4-7 times higher recruitment rates when they are surrounded by trees of their own leaf type. Simulations show that the observed positive feedbacks are necessary and sufficient to generate alternative forest states, which also lead to dependency on history (hysteresis) during ecosystem transition from evergreen to deciduous forests and vice versa. We identify hotspots of bistable forest types in evergreen-deciduous ecotones, which are likely driven by soil-related positive feedbacks. These findings are integral to predicting the distribution of forest biomes, and aid to our understanding of biodiversity, carbon turnover, and terrestrial climate feedbacks.

Differences in fungal and bacterial physiology alter soil carbon and nitrogen cycling: insights from meta-analysis and theoretical models.

Since fungi and bacteria are the dominant decomposers in soil, their distinct physiologies are likely to differentially influence rates of ecosystem carbon (C) and nitrogen (N) cycling. We used meta-analysis and an enzyme-driven biogeochemical model to explore the drivers and biogeochemical consequences of changes in the fungal-to-bacterial ratio (F : B). In our meta-analysis data set, F : B increased with soil C : N ratio (R(2) = 0.224, P < 0.001), a relationship predicted by our model. We found that differences in biomass turnover rates influenced F : B under conditions of C limitation, while differences in biomass stoichiometry set the upper bounds on F : B once a nutrient limitation threshold was reached. Ecological interactions between the two groups shifted along a gradient of resource stoichiometry. At intermediate substrate C : N, fungal N mineralisation fuelled bacterial growth, increasing total microbial biomass and decreasing net N mineralisation. Therefore, we conclude that differences in bacterial and fungal physiology may have large consequences for ecosystem-scale C and N cycling.

Below-ground traits mediate tree survival in a tropical dry forest restoration.

Reforestation is one of our most promising natural climate solutions, and one that addresses the looming biodiversity crisis. Tree planting can catalyse forest community reassembly in degraded landscapes where natural regeneration is slow, however, tree survival rates vary remarkably across projects. Building a trait-based framework for tree survival could streamline species selection in a way that generalizes across ecosystems, thereby increasing the effectiveness of the global restoration movement. We investigated how traits mediated seedling survival in a tropical dry forest restoration, and how traits were coordinated across plant structures. We examined growth and survival of 14 species for 2 years and measured six below-ground and 22 above-ground traits. Species-level survival ranged widely from 7.8% to 90.1%, and a model including growth rate, below-ground traits and their interaction explained more than 73% of this variation. A strong interaction between below-ground traits and growth rate indicated that selecting species with fast growth rates can promote establishment, but this effect was most apparent for species that invest in thick fine roots and deep root structures. Overall, results emphasize the prominent role of below-ground traits in determining early restoration outcomes, and highlight little above- and below-ground trait coordination, providing a path forward for tropical dry forest restoration efforts. This article is part of the theme issue 'Understanding forest landscape restoration: reinforcing scientific foundations for the UN Decade on Ecosystem Restoration'.

Facilitating Reforestation Through the Plant Microbiome: Perspectives from the Phyllosphere.

Tree planting and natural regeneration contribute to the ongoing effort to restore Earth's forests. Our review addresses how the plant microbiome can enhance the survival of planted and naturally regenerating seedlings and serve in long-term forest carbon capture and the conservation of biodiversity. We focus on fungal leaf endophytes, ubiquitous defensive symbionts that protect against pathogens. We first show that fungal and oomycetous pathogen richness varies greatly for tree species native to the United States (n = 0-876 known pathogens per US tree species), with nearly half of tree species either without pathogens in these major groups or with unknown pathogens. Endophytes are insurance against the poorly known and changing threat of tree pathogens. Next, we review studies of plant phyllosphere feedback, but knowledge gaps prevent us from evaluating whether adding conspecific leaf litter to planted seedlings promotes defensive symbiosis, analogous to adding soil to promote positive feedback. Finally, we discuss research priorities for integrating the plant microbiome into efforts to expand Earth's forests.

Alternative stable states of the forest mycobiome are maintained through positive feedbacks.

Most trees on Earth form a symbiosis with either arbuscular mycorrhizal or ectomycorrhizal fungi. By forming common mycorrhizal networks, actively modifying the soil environment and other ecological mechanisms, these contrasting symbioses may generate positive feedbacks that favour their own mycorrhizal strategy (that is, the con-mycorrhizal strategy) at the expense of the alternative strategy. Positive con-mycorrhizal feedbacks set the stage for alternative stable states of forests and their fungi, where the presence of different forest mycorrhizal strategies is determined not only by external environmental conditions but also mycorrhiza-mediated feedbacks embedded within the forest ecosystem. Here, we test this hypothesis using thousands of US forest inventory sites to show that arbuscular and ectomycorrhizal tree recruitment and survival exhibit positive con-mycorrhizal density dependence. Data-driven simulations show that these positive feedbacks are sufficient in magnitude to generate and maintain alternative stable states of the forest mycobiome. Given the links between forest mycorrhizal strategy and carbon sequestration potential, the presence of mycorrhizal-mediated alternative stable states affects how we forecast forest composition, carbon sequestration and terrestrial climate feedbacks.