Search

Changes in the nitrogen (N) status of forest ecosystems can directly and indirectly influence their carbon (C) sequestration potential by altering soil organic matter (SOM) decomposition, soil enzyme activity, and plant-soil interactions. However, model representation of linked C-N cycles and SOM decay are not well-validated against experimental data. Here, we use extensive data from the Fernow Experimental Forest long-term, whole-watershed N fertilization study to compare the response to N perturbations of two soil models that represent decomposition dynamics differently (first-order decay versus microbially-explicit reverse Michaelis-Menten kinetics). These two soil models were coupled to a common vegetation model which provided identical input data. Key responses to N additions measured at the study site included a shift in allocation to favor woody biomass over belowground carbon inputs, reductions in soil respiration, accumulation of particulate organic matter (POM), and an increase in soil C:N ratios. The vegetation model did not capture the often-observed shift in allocation with N additions, which resulted in poor predictions of the soil responses. We modified the plant C allocation scheme to favor wood production over fine root production with N additions, which significantly improved the vegetation and soil respiration responses. To elicit an increase in the soil C stocks and C:N ratios with N additions, as observed, we also modified the decay rates of the particulate organic matter (POM) in the soil models. With all of these modifications, only the microbially explicit model captured a positive soil C stock and C:N response in line with observations. Our results highlight the importance of accurately representing plant-soil interactions, such as rhizosphere priming, and their responses to environmental change.

Nitrogen (N) fertilization has enhanced the forest land carbon (C) sink by increasing the amount of C stored in soils, possibly through reductions in decomposition. Established differences in nutrient acquisition strategies between trees that associate with arbuscular mycorrhizal (AM) and ectomycorrhizal (ECM) fungi have been shown to influence the magnitude of this N effect on decomposition and soil C stocks. However, N deposition is declining across many temperate North American forests and little is known about how mycorrhizal-associated strategies in trees may impact short-term recovery. To examine divergent nutrient acquisition responses to N between AM and ECM systems, we developed a conceptual framework based on the idea that N fertilization reduces the C cost of N acquisition. In this framework, under N fertilization, ECM trees shift from N mining to N foraging and AM trees shift from mycorrhizal foraging to root foraging. We expanded on this framework by hypothesizing that initial recovery occurs across a spectrum, where nutrient foraging strategies either (1) persist in their N fertilized state, (2) return to the ambient state, or (3) shift to a new steady state. We tested this framework by examining fine root biomass and morphology, mycorrhizal colonization, and soil enzyme activities in organic horizon, bulk mineral, and rhizosphere mineral soils in AM and ECM dominated plots during the last year of a ~ 30 year N fertilization experiment and 1-year after fertilization ceased at Bear Brook Watershed, in Maine USA. Overall, our results indicate that N fertilization disrupted the organic N mining nutrient economy of ECM trees by reducing fine root biomass and mycorrhizal colonization and altering root morphology to improve N foraging. In contrast, AM trees appeared to shift from mycorrhizal foraging toward root foraging by reducing mycorrhizal colonization while maintaining root biomass. While AM and ECM mycorrhizal colonization in the fertilized plots remained lower than the ambient plots during the year after fertilization ceased, the rapid recovery of roots in fertilized ECM soils back to a level similar to those of the control soils was mirrored by ECM rhizosphere and organic horizon enzyme recovery. The ECM bulk mineral and all of the AM soil enzymes activities remained at their N fertilized levels. Although these are short-term recovery responses, our results suggest that the recovery of enzyme activities in the majority of ECM soil fractions, but not the AM soils may destabilize stored soil C in ECM stands that decades of N deposition have enhanced.

Microbial decomposition drives the transformation of plant-derived substrates into microbial products that form stable soil organic matter (SOM). Recent theories have posited that decomposition depends on an interaction between SOM chemistry with microbial diversity and resulting function (e.g., enzymatic capabilities, growth rates). Here, we explicitly test these theories by coupling quantitative stable isotope probing and metabolomics to track the fate of 13C enriched substrates that vary in chemical composition as they are assimilated by microbes and transformed into new metabolic products in soil. We found that differences in forest nutrient economies (e.g., nutrient cycling, microbial competition) led to arbuscular mycorrhizal (AM) soils harboring greater diversity of fungi and bacteria than ectomycorrhizal (ECM) soils. When incubated with 13C enriched substrates, substrate type drove shifts in which species were active decomposers and the abundance of metabolic products that were reduced or saturated in the highly diverse AM soils. The decomposition pathways were more static in the less diverse, ECM soil. Importantly, the majority of these shifts were driven by taxa only present in the AM soil suggesting a strong link between microbial identity and their ability to decompose and assimilate substrates. Collectively, these results highlight an important interaction between ecosystem-level processes and microbial diversity; whereby the identity and function of active decomposers impacts the composition of decomposition products that can form stable SOM.

Given that global change is predicted to increase the frequency and severity of drought in temperate forests, it is critical to understand the degree to which plant belowground responses cascade through the soil system to drive ecosystem responses to water stress. While most research has focused on plant and microbial responses independently of each other, a gap in our understanding lies in the integrated response of plant-microbial interactions to water stress. We investigated the extent to which divergent belowground responses to reduced precipitation between sugar maple trees (Acer saccharum) versus oak trees (Oak spp.) may influence microbial activity via throughfall exclusion in the field. Evidence that oak trees send carbon belowground to prime microbial activity more than maples under ambient conditions and in response to water stress suggests there is the potential for corresponding impacts of reduced precipitation on microbial activity. As such, we tested the hypothesis that differences in belowground C allocation between oaks and maples would stimulate microbial activity in the oak treatment soils and reduce microbial activity in in the sugar maple treatment soils compared to their respective controls. We found that the treatment led to declines in N mineralization, soil respiration, and oxidative enzyme activity in the sugar maple treatment plot. These declines may be due to sugar maple trees reducing root C transfers to the soil. By contrast, the reduced precipitation treatment enhanced soil respiration, as well as rates of N mineralization and peroxidase activity in the oak rhizosphere. This enhanced activity suggests that oak roots provided optimal rhizosphere conditions during water stress to prime microbial activity to support net primary production. With future changes in precipitation predicted for forests in the Eastern US, we show that the strength of plant-microbial interactions drives the degree to which reduced precipitation impacts soil C and nutrient cycling.

Roots promote the formation of slow-cycling soil carbon (C), yet we have a limited understanding of the magnitude and controls on this flux. We hypothesised arbuscular mycorrhizal (AM)- and ectomycorrhizal (ECM)-associated trees would exhibit differences in root-derived C accumulation in the soil, and that much of this C would be transferred into mineral-associated pools. We installed δ13 C-enriched ingrowth cores across mycorrhizal gradients in six Eastern U.S. forests (n = 54 plots). Overall, root-derived C was 54% greater in AM versus ECM-dominated plots. This resulted in nearly twice as much root-derived C in putatively slow-cycling mineral-associated pools in AM compared to ECM plots. Given that our estimates of root-derived inputs were often equal to or greater than leaf litter inputs, our results suggest that variation in root-derived soil C accumulation due to tree mycorrhizal dominance may be a key control of soil C dynamics in forests.

21st‐century modeling of greenhouse gas (GHG) emissions from bioenergy crops is necessary to quantify the extent to which bioenergy production can mitigate climate change. For over 30 years, the Century‐based biogeochemical models have provided the preeminent framework for belowground carbon and nitrogen cycling in ecosystem and earth system models. While monthly Century and the daily time‐step version of Century (DayCent) have advanced our ability to predict the sustainability of bioenergy crop production, new advances in feedstock generation, and our empirical understanding of sources and sinks of GHGs in soils call for a re‐visitation of DayCent's core model structures. Here, we evaluate current challenges with modeling soil carbon dynamics, trace gas fluxes, and drought and age‐related impacts on bioenergy crop productivity. We propose coupling a microbial process‐based soil organic carbon and nitrogen model with DayCent to improve soil carbon dynamics. We describe recent improvements to DayCent for simulating unique plant structural and physiological attributes of perennial bioenergy grasses. Finally, we propose a method for using machine learning to identify key parameters for simulating N2O emissions. Our efforts are focused on meeting the needs for modeling bioenergy crops; however, many updates reviewed and suggested to DayCent will be broadly applicable to other systems.

Conceptual and empirical advances in soil biogeochemistry have challenged long-held assumptions about the role of soil micro-organisms in soil organic carbon (SOC) dynamics; yet, rigorous tests of emerging concepts remain sparse. Recent hypotheses suggest that microbial necromass production links plant inputs to SOC accumulation, with high-quality (i.e., rapidly decomposing) plant litter promoting microbial carbon use efficiency, growth, and turnover leading to more mineral stabilization of necromass. We test this hypothesis experimentally and with observations across six eastern US forests, using stable isotopes to measure microbial traits and SOC dynamics. Here we show, in both studies, that microbial growth, efficiency, and turnover are negatively (not positively) related to mineral-associated SOC. In the experiment, stimulation of microbial growth by high-quality litter enhances SOC decomposition, offsetting the positive effect of litter quality on SOC stabilization. We suggest that microbial necromass production is not the primary driver of SOC persistence in temperate forests. Factors such as microbial necromass origin, alternative SOC formation pathways, priming effects, and soil abiotic properties can strongly decouple microbial growth, efficiency, and turnover from mineral-associated SOC.

Decades of atmospheric nitrogen (N) deposition in the northeastern USA have enhanced this globally important forest carbon (C) sink by relieving N limitation. While many N fertilization experiments found increased forest C storage, the mechanisms driving this response at the ecosystem scale remain uncertain. Following the optimal allocation theory, augmented N availability may reduce belowground C investment by trees to roots and soil symbionts. To test this prediction and its implications on soil biogeochemistry, we constructed C and N budgets for a long-term, whole-watershed N fertilization study at the Fernow Experimental Forest, WV, USA. Nitrogen fertilization increased C storage by shifting C partitioning away from belowground components and towards aboveground woody biomass production. Fertilization also reduced the C cost of N acquisition, allowing for greater C sequestration in vegetation. Despite equal fine litter inputs, the C and N stocks and C : N ratio of the upper mineral soil were greater in the fertilized watershed, likely due to reduced decomposition of plant litter. By combining aboveground and belowground data at the watershed scale, this study demonstrates how plant C allocation responses to N additions may result in greater C storage in both vegetation and soil.

Roots promote the formation of slow-cycling soil carbon (C), yet we have limited understanding of the magnitude and controls on this flux. We hypothesized that root-derived inputs from ectomycorrhizal (ECM)-associated trees would be greater than those from arbuscular mycorrhizal (AM)-associated trees, and that soils receiving the greatest inputs would promote greater root-derived C accumulation in mineral-associated pools. We installed δ13C-enriched ingrowth cores across mycorrhizal gradients in six Eastern U.S. forests (n = 54 plots). Counter to our hypothesis, root-derived C was 54% greater in AM versus ECM-dominated plots, resulting in 175% more root-derived C in mineral-associated, slow-cycling pools in AM compared to ECM plots. Notably, root-derived soil C was comparable in magnitude to leaf litter inputs and aboveground net primary production. Our results suggest that variation in root-derived C inputs due to tree mycorrhizal dominance may be a key control of soil C dynamics in forests.

The extent to which terrestrial ecosystems slow climate change by sequestering carbon hinges in part on nutrient limitation. We used a coupled carbon–climate model that accounts for the carbon cost to plants of supporting nitrogen-acquiring microbial symbionts to explore how nitrogen limitation affects global climate. To do this, we first calculated the reduction in net primary production due to the carbon cost of nitrogen acquisition. We then used a climate model to estimate the impacts of the resulting increase in atmospheric CO2 on temperature and precipitation regimes. The carbon costs of supporting symbiotic nitrogen uptake reduced net primary production by 8.1 Pg C yr−1, with the largest absolute effects occurring in tropical forest biomes and the largest relative changes occurring in boreal and alpine biomes. Globally, our model predicted relatively small changes in climate due to the carbon cost of nitrogen acquisition with temperature increasing by 0.1 ∘C and precipitation decreasing by 6 mm yr−1. However, there were strong regional impacts, with the largest impact occurring in boreal and alpine ecosystems, where such costs were estimated to increase temperature by 1.0 ∘C and precipitation by 9 mm yr−1. As such, our results suggest that carbon expenditures to support nitrogen-acquiring microbial symbionts have critical consequences for Earth's climate, and that carbon–climate models that omit these processes will overpredict the land carbon sink and underpredict climate change.

To classify trees along a spectrum of isohydric to anisohydric behavior is a promising new framework for identifying tree species' sensitivities to drought stress, directly related to the vulnerability of carbon uptake of terrestrial ecosystems with increased hydroclimate variability. Trees with isohydric strategies regulate stomatal conductance to maintain stationary leaf water potential, while trees with anisohydric strategies allow leaf water potential to fall, which in the absence of significant hydraulic cavitation will facilitate greater rates of carbon uptake. Despite the recognition of the gas exchange consequences of isohydric and anisohydric strategies for individual tree species, there have been few studies regarding whether isohydric trees produces distinct spectral signatures under drought stress that can be remotely sensed. Here, we examined the capability of four vegetation indices (PRI, NDVI, NDVI705, and EVI) to capture the differences in spectral responses between isohydric and anisohydric trees within a deciduous forest in central Indiana, USA. Both leaf-level spectral measurements and canopy-scale satellite observations were used to compare peak growing-season spectral signatures between a drought and a non-drought year. At the leaf scale, two vegetation indices (NDVI and NDVI705) failed to capture the drought signal or the divergent isohydric/anisohydric behavior. EVI successfully captured the drought signal at both leaf and canopy scales, but failed to capture the divergent behavior between isohydric and anisohydric tree species during the drought. PRI captured both drought signals and divergent isohydric/anisohydric behavior at both leaf and canopy scales once normalized between sunlit (backward direction images) and shaded (forward direction images) portions of canopy, which indicates drought stress and subsequent photosynthetic downregulation are greater in the sunlit portion of canopy. This study presents a significant step forward in our ability to directly mapping emergent isohydricity at different scales based on divergent spectral signatures between sunlit and shaded canopies.

Introductions and invasions by fungi, especially pathogens and mycorrhizal fungi, are widespread and potentially highly consequential for native ecosystems, but may also offer opportunities for linking microbial traits to their ecosystem functions. In particular, treating ectomycorrhizal (EM) invasions, i.e., co-invasions by EM fungi and their EM host plants, as natural experiments may offer a powerful approach for testing how microbial traits influence ecosystem functions. Forests dominated by EM symbiosis have unique biogeochemistry whereby the secretions of EM plants and fungi affect carbon (C) and nutrient cycling; moreover, particular lineages of EM fungi have unique functional traits. EM invasions may therefore alter the biogeochemistry of the native ecosystems they invade, especially nitrogen (N) and C cycling. By identifying “response traits” that favor the success of fungi in introductions and invasions (e.g., spore dispersal and germination) and their correlations with “effect traits” (e.g., nutrient-cycling enzymes) that can alter N and C cycling (and affect other coupled elemental cycles), one may be able to predict the functional consequences for ecosystems of fungal invasions using biogeochemistry models that incorporate fungal traits. Here, we review what is already known about how EM fungal community composition, traits, and ecosystem functions differ between native and exotic populations, focusing on the example of EM fungi associated with species of Pinus introduced from the Northern into the Southern Hemisphere. We develop hypotheses on how effects of introduced and invasive EM fungi may depend on interactions between soil N availability in the exotic range and EM fungal traits. We discuss how such hypotheses could be tested by utilizing Pinus introductions and invasions as a model system, especially when combined with controlled laboratory experiments. Finally, we illustrate how ecosystem modeling can be used to link fungal traits to their consequences for ecosystem N and C cycling in the context of biological invasions, and we highlight exciting avenues for future directions in understanding EM invasion., Frontiers in Forests and Global Change, 3, ISSN:2624-893X

Summary While it is well established that plants associating with arbuscular mycorrhizal (AM) and ectomycorrhizal (ECM) fungi cycle carbon (C) and nutrients in distinct ways, we have a limited understanding of whether varying abundance of ECM and AM plants in a stand can provide integrative proxies for key biogeochemical processes. We explored linkages between the relative abundance of AM and ECM trees and microbial functioning in three hardwood forests in southern Indiana, USA. Across each site's ‘mycorrhizal gradient’, we measured fungal biomass, fungal : bacterial (F : B) ratios, extracellular enzyme activities, soil carbon : nitrogen ratio, and soil pH over a growing season. We show that the percentage of AM or ECM trees in a plot promotes microbial communities that both reflect and determine the C to nutrient balance in soil. Soils dominated by ECM trees had higher F : B ratios and more standing fungal biomass than AM stands. Enzyme stoichiometry in ECM soils shifted to higher investment in extracellular enzymes needed for nitrogen and phosphorus acquisition than in C-acquisition enzymes, relative to AM soils. Our results suggest that knowledge of mycorrhizal dominance at the stand or landscape scale may provide a unifying framework for linking plant and microbial community dynamics, and predicting their effects on ecological function.

A central challenge in global ecology is the identification of key functional processes in ecosystems that scale, but do not require, data for individual species across landscapes. Given that nearly all tree species form symbiotic relationships with one of two types of mycorrhizal fungi - arbuscular mycorrhizal (AM) and ectomycorrhizal (ECM) fungi - and that AM- and ECM-dominated forests often have distinct nutrient economies, the detection and mapping of mycorrhizae over large areas could provide valuable insights about fundamental ecosystem processes such as nutrient cycling, species interactions, and overall forest productivity. We explored remotely sensed tree canopy spectral properties to detect underlying mycorrhizal association across a gradient of AM- and ECM-dominated forest plots. Statistical mining of reflectance and reflectance derivatives across moderate/high-resolution Landsat data revealed distinctly unique phenological signals that differentiated AM and ECM associations. This approach was trained and validated against measurements of tree species and mycorrhizal association across ~130 000 trees throughout the temperate United States. We were able to predict 77% of the variation in mycorrhizal association distribution within the forest plots (P

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 below-ground 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.

Summary While it is well established that leaf litter decomposition is controlled by climate and substrate quality at broad spatial scales, conceptual frameworks that consider how local-scale factors affect litter decay in heterogeneous landscapes are generally lacking. A critical challenge in disentangling the relative impacts of and interactions among local-scale factors is that these factors frequently covary due to feedbacks between plant and soil communities. For example, forest plots dominated by trees that associate with ectomycorrhizal (ECM) fungi often differ from those dominated by trees that associate with arbuscular mycorrhizal (AM) fungi in terms of their litter quality, microbial community structure and inorganic nutrient availability. Here, we evaluate the extent to which such factors alter leaf litter decomposition rates. To characterize variations in decomposition rates, we compared decay rates of high-quality litter (maple; AM) and low-quality litter (oak; ECM) across forest plots representing a gradient in litter matrix quality and nitrogen (N) availability driven by the relative proportions of AM and ECM trees in each plot. In experiment two, we added litter from two AM and three ECM tree species to forest plots with either a high-quality litter matrix and high N availability (i.e. AM-dominated plots) or a low-quality litter matrix and low N availability (i.e. ECM-dominated plots). In both experiments, we found that AM litter decomposed more rapidly than ECM litter, and this effect was enhanced in AM-dominated plots. Then, to separate the contributions of litter matrix effects from N availability effects, we added N fertilizer to a subset of plots from experiment two. Nitrogen addition increased decay rates of high-quality litter across all sites, but had no effect on low-quality litter, suggesting that low N availability, not litter matrix quality, constrains decomposition of high-quality litters. Hence, N availability appears to alter litter decomposition patterns independently of litter matrix properties. Synthesis. Our results indicate that shifts in the relative abundance of ECM- and AM-associated trees in a plot or stand have the potential to affect litter decay rates through both changes in litter quality as well as through alterations of the local-scale soil environment.

While there is an emerging view that roots and their associated microbes actively alter resource availability and soil organic matter (SOM) decomposition, the ecosystem consequences of such rhizosphere effects have rarely been quantified. Using a meta-analysis, we show that multiple indices of microbially mediated C and nitrogen (N) cycling, including SOM decomposition, are significantly enhanced in the rhizospheres of diverse vegetation types. Then, using a numerical model that combines rhizosphere effect sizes with fine root morphology and depth distributions, we show that root-accelerated mineralization and priming can account for up to one-third of the total C and N mineralized in temperate forest soils. Finally, using a stoichiometrically constrained microbial decomposition model, we show that these effects can be induced by relatively modest fluxes of root-derived C, on the order of 4% and 6% of gross and net primary production, respectively. Collectively, our results indicate that rhizosphere processes are a widespread, quantitatively important driver of SOM decomposition and nutrient release at the ecosystem scale, with potential consequences for global C stocks and vegetation feedbacks to climate.

Ecosystem carbon (C) balance is hypothesised to be sensitive to the mycorrhizal strategies that plants use to acquire nutrients. To test this idea, we coupled an optimality-based plant nitrogen (N) acquisition model with a microbe-focused soil organic matter (SOM) model. The model accurately predicted rhizosphere processes and C-N dynamics across a gradient of stands varying in their relative abundance of arbuscular mycorrhizal (AM) and ectomycorrhizal (ECM) trees. When mycorrhizal dominance was switched - ECM trees dominating plots previously occupied by AM trees, and vice versa - legacy effects were apparent, with consequences for both C and N stocks in soil. Under elevated productivity, ECM trees enhanced decomposition more than AM trees via microbial priming of unprotected SOM. Collectively, our results show that ecosystem responses to global change may hinge on the balance between rhizosphere priming and SOM protection, and highlight the importance of dynamically linking plants and microbes in terrestrial biosphere models.

Summary While multiple experiments have demonstrated that trees exposed to elevated CO2 can stimulate microbes to release nutrients from soil organic matter, the importance of root- versus mycorrhizal-induced changes in soil processes are presently unknown. We analyzed the contribution of roots and mycorrhizal activities to carbon (C) and nitrogen (N) turnover in a loblolly pine (Pinus taeda) forest exposed to elevated CO2 by measuring extracellular enzyme activities at soil microsites accessed via root windows. Specifically, we quantified enzyme activity from soil adjacent to root tips (rhizosphere), soil adjacent to hyphal tips (hyphosphere), and bulk soil. During the peak growing season, CO2 enrichment induced a greater increase of N-releasing enzymes in the rhizosphere (215% increase) than in the hyphosphere (36% increase), but a greater increase of recalcitrant C-degrading enzymes in the hyphosphere (118%) than in the rhizosphere (19%). Nitrogen fertilization influenced the magnitude of CO2 effects on enzyme activities in the rhizosphere only. At the ecosystem scale, the rhizosphere accounted for c. 50% and 40% of the total activity of N- and C-releasing enzymes, respectively. Collectively, our results suggest that root exudates may contribute more to accelerated N cycling under elevated CO2 at this site, while mycorrhizal fungi may contribute more to soil C degradation.

The biological responses to precipitation within the terrestrial components of Earth system models, or land surface models (LSMs), are mechanistically simple and poorly constrained, leaving projections of terrestrial ecosystem functioning and feedbacks to climate change uncertain. A number of field experiments have been conducted or are underway to test how changing precipitation will affect terrestrial ecosystems. Results from these experiments have the potential to vastly improve modeled processes. However, the transformation of experimental results into model improvements still represents a grand challenge. Here we review the current state of precipitation manipulation experiments and the precipitation responses of biological processes in LSMs to explore how these experiments can help improve model realism. First, we discuss contemporary precipitation projections and then review the structure and function of current-generation LSMs. We then examine different experimental designs and discuss basic variables that, if measured, would increase a field experiment's usefulness in a modeling context. Next, we compare biological processes commonly measured in the field with their model analogs and find that, in many cases, the way these processes are measured in the field is not compatible with the way they are represented in LSMs, an effect that hinders model development. We then discuss the challenge of scaling from the plot to the globe. Finally, we provide a series of recommendations aimed to improve the connectivity between experiments and LSMs and conclude that studies designed from the perspective of researchers in both communities will provide the greatest benefit to the broader global change community.

Accurate projections of the future land carbon (C) sink by terrestrial biosphere models depend on how nutrient constraints on net primary production are represented. While nutrient limitation is nearly universal, current models do not have a C cost for plant nutrient acquisition. Also missing are symbiotic mycorrhizal fungi, which can consume up to 20% of net primary production and supply up to 50% of a plant's nitrogen (N) uptake. Here we integrate simultaneous uptake and mycorrhizae into a cutting-edge plant N model—Fixation and Uptake of Nitrogen (FUN)—that can be coupled into terrestrial biosphere models. The C cost of N acquisition varies as a function of mycorrhizal type, with plants that support arbuscular mycorrhizae benefiting when N is relatively abundant and plants that support ectomycorrhizae benefiting when N is strongly limiting. Across six temperate forested sites (representing arbuscular mycorrhizal- and ectomycorrhizal-dominated stands and 176 site years), including multipath resistance improved the partitioning of N uptake between aboveground and belowground sources. Integrating mycorrhizae led to further improvements in predictions of N uptake from soil (R2 = 0.69 increased to R2 = 0.96) and from senescing leaves (R2 = 0.29 increased to R2 = 0.73) relative to the original model. On average, 5% and 9% of net primary production in arbuscular mycorrhizal- and ectomycorrhizal-dominated forests, respectively, was needed to support mycorrhizal-mediated acquisition of N. To the extent that resource constraints to net primary production are governed by similar trade-offs across all terrestrial ecosystems, integrating these improvements to FUN into terrestrial biosphere models should enhance predictions of the future land C sink.

The terrestrial biosphere sequesters up to a third of annual anthropogenic carbon dioxide emis- sions, offsetting a substantial portion of greenhouse gas forcing of the climate system. Although a number of factors are responsible for this terrestrial carbon sink, atmospheric nitrogen deposition contributes by enhancing tree productivity and promoting carbon storage in tree biomass. Forest soils also represent an important, but understudied carbon sink. Here, we examine the contribution of trees versus soil to total ecosystem carbon storage in a temperate forest and investigate the mechanisms by which soils accumulate carbon in response to two decades of elevated nitrogen inputs. We find that nitrogen-induced soil carbon accumulation is of equal or greater magnitude to carbon stored in trees, with the degree of response being dependent on stand type (hardwood versus pine) and level of N addition. Nitrogen enrichment resulted in a shift in organic matter chemistry and the microbial community such that unfertilized soils had a higher relative abundance of fungi and lipid, phenolic, and N-bearing compounds; whereas, N-amended plots were associated with reduced fungal biomass and activity and higher rates of lignin accumulation. We conclude that soil carbon accumulation in response to N enrichment was largely due to a suppression of organic matter decomposition rather than enhanced carbon inputs to soil via litter fall and root production.

Predicted decreases in water availability across the temperate forest biome have the potential to offset gains in carbon (C) uptake from phenology trends, rising atmospheric CO2, and nitrogen deposition. While it is well established that severe droughts reduce the C sink of forests by inducing tree mortality, the impacts of mild but chronic water stress on forest phenology and physiology are largely unknown. We quantified the C consequences of chronic water stress using a 13-year record of tree growth (n = 200 trees), soil moisture, and ecosystem C balance at the Morgan–Monroe State Forest (MMSF) in Indiana, and a regional 11-year record of tree growth (n > 300 000 trees) and water availability for the 20 most dominant deciduous broadleaf tree species across the eastern and midwestern USA. We show that despite ~26 more days of C assimilation by trees at the MMSF, increasing water stress decreased the number of days of wood production by ~42 days over the same period, reducing the annual accrual of C in woody biomass by 41%. Across the deciduous forest region, water stress induced similar declines in tree growth, particularly for waterdemanding ‘mesophytic’ tree species. Given the current replacement of water-stress adapted ‘xerophytic’ tree species by mesophytic tree species, we estimate that chronic water stress has the potential to decrease the C sink of deciduous forests by up to 17% (0.04 Pg C yr � 1 ) in the coming decades. This reduction in the C sink due to mesophication and chronic water stress is equivalent to an additional 1–3 days of global C emissions from fossil fuel burning each year. Collectively, our results indicate that regional declines in water availability may offset the growth-enhancing effects of other global changes and reduce the extent to which forests ameliorate climate warming.

Understanding the context dependence of ecosystem responses to global changes requires the development of new conceptual frameworks. Here we propose a framework for considering how tree species and their mycorrhizal associates differentially couple carbon (C) and nutrient cycles in temperate forests. Given that tree species predominantly associate with a single type of mycorrhizal fungi (arbuscular mycorrhizal (AM) fungi or ectomycorrhizal (ECM) fungi), and that the two types of fungi differ in their modes of nutrient acquisition, we hypothesize that the abundance of AM and ECM trees in a plot, stand, or region may provide an integrated index of biogeochemical transformations relevant to C cycling and nutrient retention. First, we describe how forest plots dominated by AM tree species have nutrient economies that differ in their C-nutrient couplings from those in plots dominated by ECM trees. Secondly, we demonstrate how the relative abundance of AM and ECM trees can be used to estimate nutrient dynamics across the landscape. Finally, we describe how our framework can be used to generate testable hypotheses about forest responses to global change factors, and how these dynamics can be used to develop better representations of plant-soil feedbacks and nutrient constraints on productivity in ecosystem and earth system models.

The exudation of carbon (C) by tree roots stimulates microbial activity and the production of extracellular enzymes in the rhizosphere. Here, we investigated whether the strength of rhizosphere processes differed between temperate forest trees that vary in soil organic matter (SOM) chemistry and associate with either ectomycorrhizal (ECM) or arbuscular mycorrhizal (AM) fungi. We measured rates of root exudation, microbial and extracellular enzyme activity, and nitrogen (N) availability in samples of rhizosphere and bulk soil influenced by four temperate forest tree species (i.e., to estimate a rhizosphere effect). Although not significantly different between species, root exudation ranged from 0.36 to 1.10 g C m−2 day−1, representing a small but important transfer of C to rhizosphere microbes. The magnitude of the rhizosphere effects could not be easily characterized by mycorrhizal associations or SOM chemistry. Ash had the lowest rhizosphere effects and beech had the highest rhizosphere effects, representing one AM and one ECM species, respectively. Hemlock and sugar maple had equivalent rhizosphere effects on enzyme activity. However, the form of N produced in the rhizosphere varied with mycorrhizal association. Enhanced enzyme activity primarily increased amino acid availability in ECM rhizospheres and increased inorganic N availability in AM rhizospheres. These results show that the exudation of C by roots can enhance extracellular enzyme activity and soil-N cycling. This work suggests that global changes that alter belowground C allocation have the potential to impact the form and amount of N to support primary production in ECM and AM stands.

Nitrogen regulates the Earth’s climate system by constraining the terrestrial sink for atmospheric CO2. Proteolytic enzymes are a principal driver of the within-system cycle of soil nitrogen, yet there is little to no understanding of their response to climate change. Here, we use a single methodology to investigate potential proteolytic enzyme activity in soils from 16 global change experiments. We show that regardless of geographical location or experimental manipulation (i.e., temperature, precipitation, or both), all sites plotted along a single line relating the response ratio of potential proteolytic activity to soil moisture deficit, the difference between precipitation and evapotranspiration. In particular, warming and reductions in precipitation stimulated potential proteolytic activity in mesic sites – temperate and boreal forests, arctic tundra – whereas these manipulations suppressed potential activity in dry grasslands. This study provides a foundation for a simple representation of the impacts of climate change on a central component of the nitrogen cycle.

Plants typically expend a significant portion of their available carbon (C) on nutrient acquisition - C that could otherwise support growth. However, given that most global terrestrial biosphere models (TBMs) do not include the C cost of nutrient acquisition, these models fail to represent current and future constraints to the land C sink. Here, we integrated a plant productivity-optimized nutrient acquisition model - the Fixation and Uptake of Nitrogen Model - into one of the most widely used TBMs, the Community Land Model. Global plant nitrogen (N) uptake is dynamically simulated in the coupled model based on the C costs of N acquisition from mycorrhizal roots, nonmycorrhizal roots, N-fixing microbes, and retranslocation (from senescing leaves). We find that at the global scale, plants spend 2.4 Pg C yr(-1) to acquire 1.0 Pg N yr(-1) , and that the C cost of N acquisition leads to a downregulation of global net primary production (NPP) by 13%. Mycorrhizal uptake represented the dominant pathway by which N is acquired, accounting for ~66% of the N uptake by plants. Notably, roots associating with arbuscular mycorrhizal (AM) fungi - generally considered for their role in phosphorus (P) acquisition - are estimated to be the primary source of global plant N uptake owing to the dominance of AM-associated plants in mid- and low-latitude biomes. Overall, our coupled model improves the representations of NPP downregulation globally and generates spatially explicit patterns of belowground C allocation, soil N uptake, and N retranslocation at the global scale. Such model improvements are critical for predicting how plant responses to altered N availability (owing to N deposition, rising atmospheric CO2 , and warming temperatures) may impact the land C sink.

Ongoing shifts in the species composition of Eastern US forests necessitate the development of frameworks to explore how species-specific water-use strategies influence ecosystem-scale carbon (C) cycling during drought. Here, we develop a diagnostic framework to classify plant drought-response strategies along a continuum of isohydric to anisohydric regulation of leaf water potential (Ψ L). The framework is applied to a 3-year record of weekly leaf-level gas exchange and Ψ measurements collected in the Morgan-Monroe State Forest (Indiana, USA), where continuous observations of the net ecosystem exchange of CO2 (NEE) have been ongoing since 1999. A severe drought that occurred in the middle of the study period reduced the absolute magnitude of NEE by 55 %, though species-specific responses to drought conditions varied. Oak species were characterized by anisohydric regulation of Ψ L that promoted static gas exchange throughout the study period. In contrast, Ψ L of the other canopy dominant species was more isohydric, which limited gas exchange during the drought. Ecosystem-scale estimates of NEE and gross ecosystem productivity derived by upscaling the leaf-level data agreed well with tower-based observations, and highlight how the fraction of isohydric and anisohydric species in forests can mediate net ecosystem C balance.

Summary Although it is increasingly being recognized that roots play a key role in soil carbon (C) dynamics, the magnitude and direction of these effects are unknown. Roots can accelerate soil C losses by provisioning microbes with energy to decompose organic matter or impede soil C losses by enhancing microbial competition for nutrients. We experimentally reduced belowground C supply to soils via tree girdling, and contrasted responses in control and girdled plots for three consecutive growing seasons. We hypothesized that decreases in belowground C supply would have stronger effects in plots dominated by ectomycorrhizal (ECM) trees rather than arbuscular mycorrhizal (AM) trees. In ECM-dominated plots, girdling decreased the activity of enzymes that break down soil organic matter (SOM) by c. 40%, indicating that, in control plots, C supply from ECM roots primes microbial decomposition. In AM-dominated plots, girdling had little effect on SOM-degrading enzymes, but increased the decomposition of AM leaf litter by c. 43%, suggesting that, in control plots, AM roots may intensify microbial competition for nutrients. Our findings indicate that root-induced changes in soil processes depend on forest composition, and that shifts in the distribution of AM and ECM trees owing to climate change may determine soil C gains and losses.

While multiple experiments have demonstrated that trees exposed to elevated CO₂ can stimulate microbes to release nutrients from soil organic matter, the importance of root- versus mycorrhizal-induced changes in soil processes are presently unknown. We analyzed the contribution of roots and mycorrhizal activities to carbon (C) and nitrogen (N) turnover in a loblolly pine (Pinus taeda) forest exposed to elevated CO₂ by measuring extracellular enzyme activities at soil microsites accessed via root windows. Specifically, we quantified enzyme activity from soil adjacent to root tips (rhizosphere), soil adjacent to hyphal tips (hyphosphere), and bulk soil. During the peak growing season, CO₂ enrichment induced a greater increase of N-releasing enzymes in the rhizosphere (215% increase) than in the hyphosphere (36% increase), but a greater increase of recalcitrant C-degrading enzymes in the hyphosphere (118%) than in the rhizosphere (19%). Nitrogen fertilization influenced the magnitude of CO₂ effects on enzyme activities in the rhizosphere only. At the ecosystem scale, the rhizosphere accounted for c. 50% and 40% of the total activity of N- and C-releasing enzymes, respectively. Collectively, our results suggest that root exudates may contribute more to accelerated N cycling under elevated CO₂ at this site, while mycorrhizal fungi may contribute more to soil C degradation.

Given that forests represent the primary terrestrial sink for atmospheric CO2 , projections of future carbon (C) storage hinge on forest responses to climate variation. Models of gross primary production (GPP) responses to water stress are commonly based on remotely sensed changes in canopy 'greenness' (e.g., normalized difference vegetation index; NDVI). However, many forests have low spectral sensitivity to water stress (SSWS) - defined here as drought-induced decline in GPP without a change in greenness. Current satellite-derived estimates of GPP use a vapor pressure deficit (VPD) scalar to account for the low SWSS of forests, but fail to capture their responses to water stress. Our objectives were to characterize differences in SSWS among forested and nonforested ecosystems, and to develop an improved framework for predicting the impacts of water stress on GPP in forests with low SSWS. First, we paired two independent drought indices with NDVI data for the conterminous US from 2000 to 2011, and examined the relationship between water stress and NDVI. We found that forests had lower SSWS than nonforests regardless of drought index or duration. We then compared satellite-derived estimates of GPP with eddy-covariance observations of GPP in two deciduous broadleaf forests with low SSWS: the Missouri Ozark (MO) and Morgan Monroe State Forest (MMSF) AmeriFlux sites. Model estimates of GPP that used VPD scalars were poorly correlated with observations of GPP at MO (r(2) = 0.09) and MMSF (r(2) = 0.38). When we included the NDVI responses to water stress of adjacent ecosystems with high SSWS into a model based solely on temperature and greenness, we substantially improved predictions of GPP at MO (r(2) = 0.83) and for a severe drought year at the MMSF (r(2) = 0.82). Collectively, our results suggest that large-scale estimates of GPP that capture variation in SSWS among ecosystems could improve predictions of C uptake by forests under drought.

[1] Increasing soil temperature has the potential to alter the activity of the extracellular enzymes that mobilize nitrogen (N) from soil organic matter (SOM) and ultimately the availability of N for primary production. Proteolytic enzymes depolymerize N from proteinaceous components of SOM into amino acids, and their activity is a principal driver of the within-system cycle of soil N. The objectives of this study were to investigate whether the soils of temperate forest tree species differ in the temperature sensitivity of proteolytic enzyme activity over the growing season and the role of substrate limitation in regulating temperature sensitivity. Across species and sampling dates, proteolytic enzyme activity had relatively low sensitivity to temperature with a mean activation energy (Ea) of 33.5 kJ mol−1. Ea declined in white ash, American beech, and eastern hemlock soils across the growing season as soils warmed. By contrast, Eain sugar maple soil increased across the growing season. We used these data to develop a species-specific empirical model of proteolytic enzyme activity for the 2009 calendar year and studied the interactive effects of soil temperature (ambient or +5°C) and substrate limitation (ambient or elevated protein) on enzyme activity. Declines in substrate limitation had a larger single-factor effect on proteolytic enzyme activity than temperature, particularly in the spring. There was, however, a large synergistic effect of increasing temperature and substrate supply on proteolytic enzyme activity. Our results suggest limited increases in N availability with climate warming unless there is a parallel increase in the availability of protein substrates.

Temperature and substrate availability constrain the activity of the extracellular enzymes that decompose and release nutrients from soil organic matter (SOM). Proteolytic enzymes are the primary class of enzymes involved in the depolymerization of nitrogen (N) from proteinaceous components of SOM, and their activity affects the rate of N cycling in forest soils. The objectives of this study were to determine whether and how temperature and substrate availability affect the activity of proteolytic enzymes in temperate forest soils, and whether the activity of proteolytic enzymes and other enzymes involved in the acquisition of N (i.e., chitinolytic and ligninolytic enzymes) differs between trees species that form associations with either ectomycorrhizal or arbuscular mycorrhizal fungi. Temperature limitation of proteolytic enzyme activity was observed only early in the growing season when soil temperatures in the field were near 4 degrees C. Substrate limitation to proteolytic activity persisted well into the growing season. Ligninolytic enzyme activity was higher in soils dominated by ectomycorrhizal associated tree species. In contrast, the activity of proteolytic and chitinolytic enzymes did not differ, but there were differences between mycorrhizal association in the control of roots on enzyme activity. Roots of ectomycorrhizal species but not those of arbuscular mycorrhizal species exerted significant control over proteolytic, chitinolytic, and ligninolytic enzyme activity; the absence of ectomycorrhizal fine roots reduced the activity of all three enzymes. These results suggest that climate warming in the absence of increases in substrate availability may have a modest effect on soil-N cycling, and that global changes that alter belowground carbon allocation by trees are likely to have a larger effect on nitrogen cycling in stands dominated by ectomycorrhizal fungi.

Empirical and modeling studies of the N cycle in temperate forests of eastern North America have focused on the mechanisms regulating the production of inorganic N, and assumed that only inorganic forms of N are available for plant growth. Recent isotope studies in field conditions suggest that amino acid capture is a widespread ecological phenomenon, although northern temperate forests have yet to be studied. We quantified fine root biomass and applied tracer-level quantities of U-(13)C(2)-(15)N-glycine, (15)NH(4) (+) and (15)NO(3) (-) in two stands, one dominated by sugar maple and white ash, the other dominated by red oak, beech, and hemlock, to assess the importance of amino acids to the N nutrition of northeastern US forests. Significant enrichment of (13)C in fine roots 2 and 5 h following tracer application indicated intact glycine uptake in both stands. Glycine accounted for up to 77% of total N uptake in the oak-beech-hemlock stand, a stand that produces recalcitrant litter, cycles N slowly and has a thick, amino acid-rich organic horizon. By contrast, glycine accounted for only 20% of total N uptake in the sugar maple and white ash stand, a stand characterized by labile litter and rapid rates of amino acid production and turnover resulting in high rates of mineralization and nitrification. This study shows that amino acid uptake is an important process occurring in two widespread, northeastern US temperate forest types with widely differing rates of N cycling.