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The importance of phosphorus (P) in regulating ecosystem responses to climate change has fostered P-cycle implementation in land surface models, but their CO2 effects predictions have not been evaluated against measurements. Here, we perform a data-driven model evaluation where simulations of eight widely used P-enabled models were confronted with observations from a long-term free-air CO2 enrichment experiment in a mature, P-limited Eucalyptus forest. We show that most models predicted the correct sign and magnitude of the CO2 effect on ecosystem carbon (C) sequestration, but they generally overestimated the effects on plant C uptake and growth. We identify leaf-to-canopy scaling of photosynthesis, plant tissue stoichiometry, plant belowground C allocation, and the subsequent consequences for plant-microbial interaction as key areas in which models of ecosystem C-P interaction can be improved. Together, this data-model intercomparison reveals data-driven insights into the performance and functionality of P-enabled models and adds to the existing evidence that the global CO2-driven carbon sink is overestimated by models.

The capacity for terrestrial ecosystems to sequester additional carbon (C) with rising CO2 concentrations depends on soil nutrient availability1,2. Previous evidence suggested that mature forests growing on phosphorus (P)-deprived soils had limited capacity to sequester extra biomass under elevated CO2 (refs. 3,4,5,6), but uncertainty about ecosystem P cycling and its CO2 response represents a crucial bottleneck for mechanistic prediction of the land C sink under climate change7. Here, by compiling the first comprehensive P budget for a P-limited mature forest exposed to elevated CO2, we show a high likelihood that P captured by soil microorganisms constrains ecosystem P recycling and availability for plant uptake. Trees used P efficiently, but microbial pre-emption of mineralized soil P seemed to limit the capacity of trees for increased P uptake and assimilation under elevated CO2 and, therefore, their capacity to sequester extra C. Plant strategies to stimulate microbial P cycling and plant P uptake, such as increasing rhizosphere C release to soil, will probably be necessary for P-limited forests to increase C capture into new biomass. Our results identify the key mechanisms by which P availability limits CO2 fertilization of tree growth and will guide the development of Earth system models to predict future long-term C storage.

Human-induced disturbance has substantially influenced the structure and function of terrestrial ecosystems globally. However, the extent to which multiple ecosystem functions (multifunctionality) recover following anthropogenic disturbance (ecosystem recovery) remains poorly understood. We report on the first study examining the temporal dynamics in recovery of multifunctionality from 3 to 12 years after the commencement of rehabilitation following mining-induced disturbance, and relate this information to changes in biota. We examined changes in 57 biotic (plants, microbial) and functional (soil) attributes associated with biodiversity and ecosystem services at four open-cut coal mines in eastern Australia. Increasing time since commencement of rehabilitation was associated with increases in overall multifunctionality, soil microbial abundance, plant productivity, plant structure and soil stability, but not nutrient cycling, soil carbon sequestration nor soil nutrients. However, the temporal responses of individual ecosystem properties varied widely, from strongly positive (e.g. litter cover, fine and coarse frass, seed biomass, microbial and fungal biomass) to strongly negative (groundstorey foliage cover). We also show that sites with more developed biota tended to have greater ecosystem multifunctionality. Moreover, recovery of plant litter was closely associated with recovery of most microbial components, soil integrity and soil respiration. Overall, however, rehabilitated sites still differed from reference ecosystems a decade after commencement of rehabilitation. Synthesis and applications. The dominant role of plant and soil biota and litter cover in relation to functions associated with soil respiration, microbial function, soil integrity and C and N pools suggests that recovering biodiversity is a critically important priority in rehabilitation programs. Nonetheless, the slow recovery of most functions after a decade indicates that rehabilitation after op

Not only do soils provide 98.7% of the calories consumed by humans, they also provide numerous other functions upon which planetary survivability closely depends. However, our continuously increasing focus on soils for biomass provision (food, fiber, and energy) through intensive agriculture is rapidly degrading soils and diminishing their capacity to deliver other vital functions. These tradeoffs in soil functionality - the increased provision of one function at the expense of other critical planetary functions - are the focus of this review. We examine how land-use change for biomass provision has decreased the ability of soils to regulate the carbon pool and thereby contribute profoundly to climate change, to cycle the nutrients that sustain plant growth and ecosystem health, to protect the soil biodiversity upon which many other functions depend, and to cycle the Earth's freshwater supplies. We also examine how this decreasing ability of soil to provide these other functions can be halted and reversed. Despite the complexity and the interconnectedness of soil functions, we show that soil organic carbon plays a central role and is a master indicator for soil functioning and that we require a better understanding of the factors controlling the behavior and persistence of C in soils. Given the threats facing humanity and their economies, it is imperative that we recognize that Soil Security is itself an existential challenge and that we need to increase our focus on the multiple functions of soils for long-term human welfare and survivability of the planet.

Atmospheric CO2 concentration is increasing, largely due to anthropogenic activities. Previous studies of individual free-air CO2 enrichment (FACE) experimental sites have shown significant impacts of elevated CO2 (eCO2) on soil microbial communities; however, no common microbial response patterns have yet emerged, challenging our ability to predict ecosystem functioning and sustainability in the future eCO2 environment. Here we analyzed 66 soil microbial communities from five FACE sites, and showed common microbial response patterns to eCO2, especially for key functional genes involved in carbon and nitrogen fixation (e.g., pcc/acc for carbon fixation, nifH for nitrogen fixation), carbon decomposition (e.g., amyA and pulA for labile carbon decomposition, mnp and lcc for recalcitrant carbon decomposition), and greenhouse gas emissions (e.g., mcrA for methane production, norB for nitrous oxide production) across five FACE sites. Also, the relative abundance of those key genes was generally increased and directionally associated with increased biomass, soil carbon decomposition, and soil moisture. In addition, a further literature survey of more disparate FACE experimental sites indicated increased biomass, soil carbon decay, nitrogen fixation, methane and nitrous oxide emissions, plant and soil carbon and nitrogen under eCO2. A conceptual framework was developed to link commonly responsive functional genes with ecosystem processes, such as pcc/acc vs. soil carbon storage, amyA/pulA/mnp/lcc vs. soil carbon decomposition, and nifH vs. nitrogen availability, suggesting that such common responses of microbial functional genes may have the potential to predict ecosystem functioning and sustainability in the future eCO2 environment.

Atmospheric CO2 concentration is increasing, largely due to anthropogenic activities. Previous studies of individual free-air CO2 enrichment (FACE) experimental sites have shown significant impacts of elevated CO2 (eCO2) on soil microbial communities; however, no common microbial response patterns have yet emerged, challenging our ability to predict ecosystem functioning and sustainability in the future eCO2 environment. Here we analyzed 66 soil microbial communities from five FACE sites, and showed common microbial response patterns to eCO2, especially for key functional genes involved in carbon and nitrogen fixation (e.g., pcc/acc for carbon fixation, nifH for nitrogen fixation), carbon decomposition (e.g., amyA and pulA for labile carbon decomposition, mnp and lcc for recalcitrant carbon decomposition), and greenhouse gas emissions (e.g., mcrA for methane production, norB for nitrous oxide production) across five FACE sites. Also, the relative abundance of those key genes was generally increased and directionally associated with increased biomass, soil carbon decomposition, and soil moisture. In addition, a further literature survey of more disparate FACE experimental sites indicated increased biomass, soil carbon decay, nitrogen fixation, methane and nitrous oxide emissions, plant and soil carbon and nitrogen under eCO2. A conceptual framework was developed to link commonly responsive functional genes with ecosystem processes, such as pcc/acc vs. soil carbon storage, amyA/pulA/mnp/lcc vs. soil carbon decomposition, and nifH vs. nitrogen availability, suggesting that such common responses of microbial functional genes may have the potential to predict ecosystem functioning and sustainability in the future eCO2 environment.

Atmospheric carbon dioxide enrichment (eCO2) can enhance plant carbon uptake and growth1,2,3,4,5, thereby providing an important negative feedback to climate change by slowing the rate of increase of the atmospheric CO2 concentration6. Although evidence gathered from young aggrading forests has generally indicated a strong CO2 fertilization effect on biomass growth3,4,5, it is unclear whether mature forests respond to eCO2 in a similar way. In mature trees and forest stands7,8,9,10, photosynthetic uptake has been found to increase under eCO2 without any apparent accompanying growth response, leaving the fate of additional carbon fixed under eCO2 unclear4,5,7,8,9,10,11. Here using data from the first ecosystem-scale Free-Air CO2 Enrichment (FACE) experiment in a mature forest, we constructed a comprehensive ecosystem carbon budget to track the fate of carbon as the forest responded to four years of eCO2 exposure. We show that, although the eCO2 treatment of +150 parts per million (+38 per cent) above ambient levels induced a 12 per cent (+247 grams of carbon per square metre per year) increase in carbon uptake through gross primary production, this additional carbon uptake did not lead to increased carbon sequestration at the ecosystem level. Instead, the majority of the extra carbon was emitted back into the atmosphere via several respiratory fluxes, with increased soil respiration alone accounting for half of the total uptake surplus. Our results call into question the predominant thinking that the capacity of forests to act as carbon sinks will be generally enhanced under eCO2, and challenge the efficacy of climate mitigation strategies that rely on ubiquitous CO2 fertilization as a driver of increased carbon sinks in global forests.

Atmospheric carbon dioxide enrichment (eCO2) can enhance plant carbon uptake and growth1–5, thereby providing an important negative feedback to climate change by slowing the rate of increase of the atmospheric CO2 concentration6. Although evidence gathered from young aggrading forests has generally indicated a strong CO2 fertilization effect on biomass growth3–5, it is unclear whether mature forests respond to eCO2 in a similar way. In mature trees and forest stands7–10, photosynthetic uptake has been found to increase under eCO2 without any apparent accompanying growth response, leaving the fate of additional carbon fixed under eCO2 unclear4,5,7–11. Here using data from the first ecosystem-scale Free-Air CO2 Enrichment (FACE) experiment in a mature forest, we constructed a comprehensive ecosystem carbon budget to track the fate of carbon as the forest responded to four years of eCO2 exposure. We show that, although the eCO2 treatment of +150 parts per million (+38 per cent) above ambient levels induced a 12 per cent (+247 grams of carbon per square metre per year) increase in carbon uptake through gross primary production, this additional carbon uptake did not lead to increased carbon sequestration at the ecosystem level. Instead, the majority of the extra carbon was emitted back into the atmosphere via several respiratory fluxes, with increased soil respiration alone accounting for half of the total uptake surplus. Our results call into question the predominant thinking that the capacity of forests to act as carbon sinks will be generally enhanced under eCO2, and challenge the efficacy of climate mitigation strategies that rely on ubiquitous CO2 fertilization as a driver of increased carbon sinks in global forests.

Atmospheric carbon dioxide enrichment (eCO2) can enhance plant carbon uptake and growth1,2,3,4,5, thereby providing an important negative feedback to climate change by slowing the rate of increase of the atmospheric CO2 concentration6. Although evidence gathered from young aggrading forests has generally indicated a strong CO2 fertilization effect on biomass growth3,4,5, it is unclear whether mature forests respond to eCO2 in a similar way. In mature trees and forest stands7,8,9,10, photosynthetic uptake has been found to increase under eCO2 without any apparent accompanying growth response, leaving the fate of additional carbon fixed under eCO2 unclear4,5,7,8,9,10,11. Here using data from the first ecosystem-scale Free-Air CO2 Enrichment (FACE) experiment in a mature forest, we constructed a comprehensive ecosystem carbon budget to track the fate of carbon as the forest responded to four years of eCO2 exposure. We show that, although the eCO2 treatment of +150 parts per million (+38 per cent) above ambient levels induced a 12 per cent (+247 grams of carbon per square metre per year) increase in carbon uptake through gross primary production, this additional carbon uptake did not lead to increased carbon sequestration at the ecosystem level. Instead, the majority of the extra carbon was emitted back into the atmosphere via several respiratory fluxes, with increased soil respiration alone accounting for half of the total uptake surplus. Our results call into question the predominant thinking that the capacity of forests to act as carbon sinks will be generally enhanced under eCO2, and challenge the efficacy of climate mitigation strategies that rely on ubiquitous CO2 fertilization as a driver of increased carbon sinks in global forests.

Process-based models describing biogeochemical cycling are crucial tools to understanding long-term nutrient dynamics, especially in the context of perturbations, such as climate and land-use change. Such models must effectively synthesize ecological processes and properties. For example, in terrestrial ecosystems, plants are the primary source of bioavailable carbon, but turnover rates of essential nutrients are contingent on interactions between plants and soil biota. Yet, biogeochemical models have traditionally considered plant and soil communities in broad terms. The next generation of models must consider how shifts in their diversity and composition affect ecosystem processes. One promising approach to synthesize plant and soil biodiversity and their interactions into models is to consider their diversity from a functional trait perspective. Plant traits, which include heritable chemical, physical, morphological and phenological characteristics, are increasingly being used to predict ecosystem processes at a range of scales, and to interpret biodiversity?ecosystem functional relationships. There is also emerging evidence that the traits of soil microbial and faunal communities can be correlated with ecosystem functions such as decomposition, nutrient cycling, and greenhouse gas production. Here, we draw on recent advances in measuring and using traits of different biota to predict ecosystem processes, and provide a new perspective as to how biotic traits can be integrated into biogeochemical models. We first describe an explicit trait-based model framework that operates at small scales and uses direct measurements of ecosystem properties; second, an integrated approach that operates at medium scales and includes interactions between biogeochemical cycling and soil food webs; and third, an implicit trait-based model framework that associates soil microbial and faunal functional groups with plant functional groups, and operates at the Earth-system leve

Process-based models describing biogeochemical cycling are crucial tools to understanding long-term nutrient dynamics, especially in the context of perturbations, such as climate and land-use change. Such models must effectively synthesize ecological processes and properties. For example, in terrestrial ecosystems, plants are the primary source of bioavailable carbon, but turnover rates of essential nutrients are contingent on interactions between plants and soil biota. Yet, biogeochemical models have traditionally considered plant and soil communities in broad terms. The next generation of models must consider how shifts in their diversity and composition affect ecosystem processes. One promising approach to synthesize plant and soil biodiversity and their interactions into models is to consider their diversity from a functional trait perspective. Plant traits, which include heritable chemical, physical, morphological and phenological characteristics, are increasingly being used to predict ecosystem processes at a range of scales, and to interpret biodiversity?ecosystem functional relationships. There is also emerging evidence that the traits of soil microbial and faunal communities can be correlated with ecosystem functions such as decomposition, nutrient cycling, and greenhouse gas production. Here, we draw on recent advances in measuring and using traits of different biota to predict ecosystem processes, and provide a new perspective as to how biotic traits can be integrated into biogeochemical models. We first describe an explicit trait-based model framework that operates at small scales and uses direct measurements of ecosystem properties; second, an integrated approach that operates at medium scales and includes interactions between biogeochemical cycling and soil food webs; and third, an implicit trait-based model framework that associates soil microbial and faunal functional groups with plant functional groups, and operates at the Earth-system leve

The flux of CO2 from the soil to the atmosphere (soil respiration, Rsoil) is a major component of the global carbon cycle. Methods to measure and model Rsoil, or partition it into different components, often rely on the assumption that soil CO2 concentrations and fluxes are in steady state, implying that Rsoil is equal to the rate at which CO2 is produced by soil microbial and root respiration. Recent research, however, questions the validity of this assumption. Thus, the aim of this work was two-fold: (1) to describe a non-steady state (NSS) soil CO2 transport and production model, DETECT, and (2) to use this model to evaluate the environmental conditions under which Rsoil and CO2 production are likely in NSS. The backbone of DETECT is a non-homogeneous, partial differential equation (PDE) that describes production and transport of soil CO2, which we solve numerically at fine spatial and temporal resolution (e.g., 0.01 m increments to 1 m, every 6 hours). Production of soil CO2 is simulated for every depth and time increment as the sum of root respiration and microbial decomposition of soil organic matter, both of which can be driven by current and antecedent soil water content and temperature, which can also vary by time and depth. We also analytically solved the ordinary differential equation (ODE) corresponding to the steady-state (SS) solution to the PDE model. We applied the DETECT NSS and SS models to the 6-month growing season period representative of a native grassland in Wyoming. Simulation experiments were conducted with both model versions to evaluate factors that could affect departure from SS: (1) varying soil texture; (2) shifting the timing or frequency of precipitation; and (3) with and without the environmental antecedent drivers. For a coarse-textured soil, Rsoil from the SS model closely matched that of the NSS model. However, in a fine-textured (clay) soil, growing season Rsoil was ~3% higher under the assumption of NSS (versus SS). These differ

Multi-factor experiments are often advocated as important for advancing terrestrial biosphere models (TBMs), yet to date such models have only been tested against single-factor experiments. We applied 10 TBMs to the multi-factor Prairie Heating and CO2 Enrichment (PHACE) experiment in Wyoming, USA. Our goals were to investigate how multi-factor experiments can be used to constrain models, and to identify a road map for model improvement. We found models performed poorly in ambient conditions; there was a wide spread in simulated above-ground net primary productivity (range: 31-390 g C m-2 yr-1). Comparison with data highlighted model failures particularly in respect to carbon allocation, phenology, and the impact of water stress on phenology. Performance against single-factors was also relatively poor. In addition, similar responses were predicted for different reasons across models: there were large differences among models in sensitivity to water stress and, among the nitrogen cycle models, nitrogen availability during the experiment. Models were also unable to capture observed treatment effects on phenology: they over-estimated the effect of warming on leaf onset and did not allow CO2-induced water savings to extend growing season length. Observed interactive (CO2 x warming) treatment effects were subtle and contingent on water stress, phenology and species composition. Since the models did not correctly represent these processes under ambient and single-factor conditions, little extra information was gained by comparing model predictions against interactive responses. We outline a series of key areas in which this and future experiments could be used to improve model predictions of grassland responses to global change.

Multi-factor experiments are often advocated as important for advancing terrestrial biosphere models (TBMs), yet to date such models have only been tested against single-factor experiments. We applied 10 TBMs to the multi-factor Prairie Heating and CO2 Enrichment (PHACE) experiment in Wyoming, USA. Our goals were to investigate how multi-factor experiments can be used to constrain models, and to identify a road map for model improvement. We found models performed poorly in ambient conditions; there was a wide spread in simulated above-ground net primary productivity (range: 31-390 g C m-2 yr-1). Comparison with data highlighted model failures particularly in respect to carbon allocation, phenology, and the impact of water stress on phenology. Performance against single-factors was also relatively poor. In addition, similar responses were predicted for different reasons across models: there were large differences among models in sensitivity to water stress and, among the nitrogen cycle models, nitrogen availability during the experiment. Models were also unable to capture observed treatment effects on phenology: they over-estimated the effect of warming on leaf onset and did not allow CO2-induced water savings to extend growing season length. Observed interactive (CO2 x warming) treatment effects were subtle and contingent on water stress, phenology and species composition. Since the models did not correctly represent these processes under ambient and single-factor conditions, little extra information was gained by comparing model predictions against interactive responses. We outline a series of key areas in which this and future experiments could be used to improve model predictions of grassland responses to global change.

Climate change can alter soil communities and functions, but the consequences are uncertain for most ecosystems. We assessed the impacts of climate change on soil nematodes in a semiarid grassland using a 7-year, factorial manipulation of temperature and [CO2]. Elevated CO2 and warming decreased the abundance of plant-feeding nematodes and nematodes with intermediate to high values on the colonizer-persister scale (cp3-5), including predators and omnivores. Thus, under futuristic climate conditions, nematode communities were even more dominated by r-strategists (cp1-2) that feed on bacteria and fungi. These results indicate that climate change could alter soil functioning in semiarid grasslands. For example, the lower abundance of plant-feeding nematodes could facilitate positive effects of elevated CO2 and warming on plant productivity. The effects of elevated CO2 and warming on nematode functional composition were typically less than additive, highlighting the need for multi-factor studies.

Free amino acids (FAAs) in soil are an important N source for plants, and abundances are predicted to shift under altered atmospheric conditions such as elevated CO2. Composition, plant uptake capacity, and plant and microbial use of FAAs relative to inorganic N forms were investigated in a temperate semiarid grassland exposed to experimental warming and free-air CO2 enrichment. FAA uptake by two dominant grassland plants, Bouteloua gracilis and Artemesia frigida, was determined in hydroponic culture. B. gracilis and microbial N preferences were then investigated in experimental field plots using isotopically labeled FAA and inorganic N sources. Alanine and phenylalanine concentrations were the highest in the field, and B. gracilis and A. frigida rapidly consumed these FAAs in hydroponic experiments. However, B. gracilis assimilated little isotopically labeled alanine, ammonium and nitrate in the field. Rather, soil microbes immobilized the majority of all three N forms. Elevated CO2 and warming did not affect plant or microbial uptake. FAAs are not direct sources of N for B. gracilis, and soil microbes outcompete this grass for organic and inorganic N when N is at peak demand within temperate semiarid grasslands.

Future ecosystem properties of grasslands will be driven largely by belowground biomass responses to climate change, which are challenging to understand due to experimental and technical constraints. We used a multi-faceted approach to explore single and combined impacts of elevated CO2 and warming on root carbon (C) and nitrogen (N) dynamics in a temperate, semiarid, native grassland at the Prairie Heating and CO2 Enrichment experiment. To investigate the indirect, moisture mediated effects of elevated CO2, we included an irrigation treatment. We assessed root standing mass, morphology, residence time and seasonal appearance/disappearance of community-aggregated roots, as well as mass and N losses during decomposition of two dominant grass species (a C3 and a C4). In contrast to what is common in mesic grasslands, greater root standing mass under elevated CO2 resulted from increased production, unmatched by disappearance. Elevated CO2 plus warming produced roots that were longer, thinner and had greater surface area, which, together with greater standing biomass, could potentially alter root function and dynamics. Decomposition increased under environmental conditions generated by elevated CO2, but not those generated by warming, likely due to soil desiccation with warming. Elevated CO2, particularly under warming, slowed N release from C4—but not C3—roots, and consequently could indirectly affect N availability through treatment effects on species composition. Elevated CO2 and warming effects on root morphology and decomposition could offset increased C inputs from greater root biomass, thereby limiting future net C accrual in this semiarid grassland.

Nitrogen (N) and phosphorus (P) are essential nutrients for primary producers and decomposers in terrestrial ecosystems. Although climate change affects terrestrial N cycling with important feedbacks to plant productivity and carbon sequestration, the impacts of climate change on the relative availability of N with respect to P remain highly uncertain. In a semiarid grassland in Wyoming, USA, we studied the effects of atmospheric CO2 enrichment (to 600 ppmv) and warming (1.5/3.0°C above ambient temperature during the day/night) on plant, microbial and available soil pools of N and P. Elevated CO2 increased P availability to plants and microbes relative to that of N, whereas warming reduced P availability relative to N. Across years and treatments, plant N : Pratios varied between 5 and 18 and were inversely related to soil moisture. Our results indicate that soil moisture is important in controlling P supply from inorganic sources, causing reduced P relative to N availability during dry periods. Both wetter soil conditions under elevated CO2 and drier conditions with warming can further alter N : P. Although warming may alleviate N constraints under elevated CO2, warming and drought can exacerbate P constraints on plant growth and microbial activity in this semiarid grassland.