Individual and interactive effects of warming and nitrogen supply on CO2 fluxes and carbon allocation in subarctic grassland.

Climate warming has been suggested to impact high latitude grasslands severely, potentially causing considerable carbon (C) losses from soil. Warming can also stimulate nitrogen (N) turnover, but it is largely unclear whether and how altered N availability impacts belowground C dynamics. Even less is known about the individual and interactive effects of warming and N availability on the fate of recently photosynthesized C in soil. On a 10-year geothermal warming gradient in Iceland, we studied the effects of soil warming and N addition on CO2 fluxes and the fate of recently photosynthesized C through CO2 flux measurements and a 13 CO2 pulse-labeling experiment. Under warming, ecosystem respiration exceeded maximum gross primary productivity, causing increased net CO2 emissions. N addition treatments revealed that, surprisingly, the plants in the warmed soil were N limited, which constrained primary productivity and decreased recently assimilated C in shoots and roots. In soil, microbes were increasingly C limited under warming and increased microbial uptake of recent C. Soil respiration was increased by warming and was fueled by increased belowground inputs and turnover of recently photosynthesized C. Our findings suggest that a decade of warming seemed to have induced a N limitation in plants and a C limitation by soil microbes. This caused a decrease in net ecosystem CO2 uptake and accelerated the respiratory release of photosynthesized C, which decreased the C sequestration potential of the grassland. Our study highlights the importance of belowground C allocation and C-N interactions in the C dynamics of subarctic ecosystems in a warmer world.

Conceptualizing soil organic matter into particulate and mineral-associated forms to address global change in the 21st century.

Managing soil organic matter (SOM) stocks to address global change challenges requires well-substantiated knowledge of SOM behavior that can be clearly communicated between scientists, management practitioners, and policy makers. However, SOM is incredibly complex and requires separation into multiple components with contrasting behavior in order to study and predict its dynamics. Numerous diverse SOM separation schemes are currently used, making cross-study comparisons difficult and hindering broad-scale generalizations. Here, we recommend separating SOM into particulate (POM) and mineral-associated (MAOM) forms, two SOM components that are fundamentally different in terms of their formation, persistence, and functioning. We provide evidence of their highly contrasting physical and chemical properties, mean residence times in soil, and responses to land use change, plant litter inputs, warming, CO2 enrichment, and N fertilization. Conceptualizing SOM into POM versus MAOM is a feasible, well-supported, and useful framework that will allow scientists to move beyond studies of bulk SOM, but also use a consistent separation scheme across studies. Ultimately, we propose the POM versus MAOM framework as the best way forward to understand and predict broad-scale SOM dynamics in the context of global change challenges and provide necessary recommendations to managers and policy makers.

Microbial carbon limitation: The need for integrating microorganisms into our understanding of ecosystem carbon cycling.

Numerous studies have demonstrated that fertilization with nutrients such as nitrogen, phosphorus, and potassium increases plant productivity in both natural and managed ecosystems, demonstrating that primary productivity is nutrient limited in most terrestrial ecosystems. In contrast, it has been demonstrated that heterotrophic microbial communities in soil are primarily limited by organic carbon or energy. While this concept of contrasting limitations, that is, microbial carbon and plant nutrient limitation, is based on strong evidence that we review in this paper, it is often ignored in discussions of ecosystem response to global environment changes. The plant-centric perspective has equated plant nutrient limitations with those of whole ecosystems, thereby ignoring the important role of the heterotrophs responsible for soil decomposition in driving ecosystem carbon storage. To truly integrate carbon and nutrient cycles in ecosystem science, we must account for the fact that while plant productivity may be nutrient limited, the secondary productivity by heterotrophic communities is inherently carbon limited. Ecosystem carbon cycling integrates the independent physiological responses of its individual components, as well as tightly coupled exchanges between autotrophs and heterotrophs. To the extent that the interacting autotrophic and heterotrophic processes are controlled by organisms that are limited by nutrient versus carbon accessibility, respectively, we propose that ecosystems by definition cannot be 'limited' by nutrients or carbon alone. Here, we outline how models aimed at predicting non-steady state ecosystem responses over time can benefit from dissecting ecosystems into the organismal components and their inherent limitations to better represent plant-microbe interactions in coupled carbon and nutrient models.

Impact of priming on global soil carbon stocks.

Fresh carbon input (above and belowground) contributes to soil carbon sequestration, but also accelerates decomposition of soil organic matter through biological priming mechanisms. Currently, poor understanding precludes the incorporation of these priming mechanisms into the global carbon models used for future projections. Here, we show that priming can be incorporated based on a simple equation calibrated from incubation and verified against independent litter manipulation experiments in the global land surface model, ORCHIDEE. When incorporated into ORCHIDEE, priming improved the model's representation of global soil carbon stocks and decreased soil carbon sequestration by 51% (12 ± 3 Pg C) during the period 1901-2010. Future projections with the same model across the range of CO2 and climate changes defined by the IPCC-RCP scenarios reveal that priming buffers the projected changes in soil carbon stocks - both the increases due to enhanced productivity and new input to the soil, and the decreases due to warming-induced accelerated decomposition. Including priming in Earth system models leads to different projections of soil carbon changes, which are challenging to verify at large spatial scales.

Annual burning of a tallgrass prairie inhibits C and N cycling in soil, increasing recalcitrant pyrogenic organic matter storage while reducing N availability.

Grassland ecosystems store an estimated 30% of the world's total soil C and are frequently disturbed by wildfires or fire management. Aboveground litter decomposition is one of the main processes that form soil organic matter (SOM). However, during a fire biomass is removed or partially combusted and litter inputs to the soil are substituted with inputs of pyrogenic organic matter (py-OM). Py-OM accounts for a more recalcitrant plant input to SOM than fresh litter, and the historical frequency of burning may alter C and N retention of both fresh litter and py-OM inputs to the soil. We compared the fate of these two forms of plant material by incubating (13) C- and (15) N-labeled Andropogon gerardii litter and py-OM at both an annually burned and an infrequently burned tallgrass prairie site for 11 months. We traced litter and py-OM C and N into uncomplexed and organo-mineral SOM fractions and CO2 fluxes and determined how fire history affects the fate of these two forms of aboveground biomass. Evidence from CO2 fluxes and SOM C:N ratios indicates that the litter was microbially transformed during decomposition while, besides an initial labile fraction, py-OM added to SOM largely untransformed by soil microbes. Additionally, at the N-limited annually burned site, litter N was tightly conserved. Together, these results demonstrate how, although py-OM may contribute to C and N sequestration in the soil due to its resistance to microbial degradation, a long history of annual removal of fresh litter and input of py-OM infers N limitation due to the inhibition of microbial decomposition of aboveground plant inputs to the soil. These results provide new insight into how fire may impact plant inputs to the soil, and the effects of py-OM on SOM formation and ecosystem C and N cycling.

Global stocks and capacity of mineral-associated soil organic carbon.

Soil is the largest terrestrial reservoir of organic carbon and is central for climate change mitigation and carbon-climate feedbacks. Chemical and physical associations of soil carbon with minerals play a critical role in carbon storage, but the amount and global capacity for storage in this form remain unquantified. Here, we produce spatially-resolved global estimates of mineral-associated organic carbon stocks and carbon-storage capacity by analyzing 1144 globally-distributed soil profiles. We show that current stocks total 899 Pg C to a depth of 1 m in non-permafrost mineral soils. Although this constitutes 66% and 70% of soil carbon in surface and deeper layers, respectively, it is only 42% and 21% of the mineralogical capacity. Regions under agricultural management and deeper soil layers show the largest undersaturation of mineral-associated carbon. Critically, the degree of undersaturation indicates sequestration efficiency over years to decades. We show that, across 103 carbon-accrual measurements spanning management interventions globally, soils furthest from their mineralogical capacity are more effective at accruing carbon; sequestration rates average 3-times higher in soils at one tenth of their capacity compared to soils at one half of their capacity. Our findings provide insights into the world's soils, their capacity to store carbon, and priority regions and actions for soil carbon management.

Five years of whole-soil warming led to loss of subsoil carbon stocks and increased CO2 efflux.

Subsoils below 20 cm are an important reservoir in the global carbon cycle, but little is known about their vulnerability under climate change. We measured a statistically significant loss of subsoil carbon (-33 ± 11%) in warmed plots of a conifer forest after 4.5 years of whole-soil warming (4°C). The loss of subsoil carbon was primarily from unprotected particulate organic matter. Warming also stimulated a sustained 30 ± 4% increase in soil CO2 efflux due to increased CO2 production through the whole-soil profile. The observed in situ decline in subsoil carbon stocks with warming is now definitive evidence of a positive soil carbon-climate feedback, which could not be concluded based on increases in CO2 effluxes alone. The high sensitivity of subsoil carbon and the different responses of soil organic matter pools suggest that models must represent these heterogeneous soil dynamics to accurately predict future feedbacks to warming.

High foliar K and P resorption efficiencies in old-growth tropical forests growing on nutrient-poor soils.

Resorption is the active withdrawal of nutrients before leaf abscission. This mechanism represents an important strategy to maintain efficient nutrient cycling; however, resorption is poorly characterized in old-growth tropical forests growing in nutrient-poor soils. We investigated nutrient resorption from leaves in 39 tree species in two tropical forests on the Guiana Shield, French Guiana, to investigate whether resorption efficiencies varied with soil nutrient, seasonality, and species traits. The stocks of P in leaves, litter, and soil were low at both sites, indicating potential P limitation of the forests. Accordingly, mean resorption efficiencies were higher for P (35.9%) and potassium (K; 44.6%) than for nitrogen (N; 10.3%). K resorption was higher in the wet (70.2%) than in the dry (41.7%) season. P resorption increased slightly with decreasing total soil P; and N and P resorptions were positively related to their foliar concentrations. We conclude that nutrient resorption is a key plant nutrition strategy in these old-growth tropical forests, that trees with high foliar nutrient concentration reabsorb more nutrient, and that nutrients resorption in leaves, except P, are quite decoupled from nutrients in the soil. Seasonality and biochemical limitation played a role in the resorption of nutrients in leaves, but species-specific requirements obscured general tendencies at stand and ecosystem level.

Soil properties explain tree growth and mortality, but not biomass, across phosphorus-depleted tropical forests.

We observed strong positive relationships between soil properties and forest dynamics of growth and mortality across twelve primary lowland tropical forests in a phosphorus-poor region of the Guiana Shield. Average tree growth (diameter at breast height) increased from 0.81 to 2.1 mm yr-1 along a soil texture gradient from 0 to 67% clay, and increasing metal-oxide content. Soil organic carbon stocks in the top 30 cm ranged from 30 to 118 tons C ha-1, phosphorus content ranged from 7 to 600 mg kg-1 soil, and the relative abundance of arbuscular mycorrhizal fungi ranged from 0 to 50%, all positively correlating with soil clay, and iron and aluminum oxide and hydroxide content. In contrast, already low extractable phosphorus (Bray P) content decreased from 4.4 to <0.02 mg kg-1 in soil with increasing clay content. A greater prevalence of arbuscular mycorrhizal fungi in more clayey forests that had higher tree growth and mortality, but not biomass, indicates that despite the greater investment in nutrient uptake required, soils with higher clay content may actually serve to sustain high tree growth in tropical forests by avoiding phosphorus losses from the ecosystem. Our study demonstrates how variation in soil properties that retain carbon and nutrients can help to explain variation in tropical forest growth and mortality, but not biomass, by requiring niche specialization and contributing to biogeochemical diversification across this region.

A systemic overreaction to years versus decades of warming in a subarctic grassland ecosystem.

Temperature governs most biotic processes, yet we know little about how warming affects whole ecosystems. Here we examined the responses of 128 components of a subarctic grassland to either 5-8 or >50 years of soil warming. Warming of >50 years drove the ecosystem to a new steady state possessing a distinct biotic composition and reduced species richness, biomass and soil organic matter. However, the warmed state was preceded by an overreaction to warming, which was related to organism physiology and was evident after 5-8 years. Ignoring this overreaction yielded errors of >100% for 83 variables when predicting their responses to a realistic warming scenario of 1 °C over 50 years, although some, including soil carbon content, remained stable after 5-8 years. This study challenges long-term ecosystem predictions made from short-term observations, and provides a framework for characterization of ecosystem responses to sustained climate change.

Design and operation of a continuous 13C and 15N labeling chamber for uniform or differential, metabolic and structural, plant isotope labeling.

Tracing rare stable isotopes from plant material through the ecosystem provides the most sensitive information about ecosystem processes; from CO2 fluxes and soil organic matter formation to small-scale stable-isotope biomarker probing. Coupling multiple stable isotopes such as (13)C with (15)N, (18)O or (2)H has the potential to reveal even more information about complex stoichiometric relationships during biogeochemical transformations. Isotope labeled plant material has been used in various studies of litter decomposition and soil organic matter formation(1-4). From these and other studies, however, it has become apparent that structural components of plant material behave differently than metabolic components (i.e. leachable low molecular weight compounds) in terms of microbial utilization and long-term carbon storage(5-7). The ability to study structural and metabolic components separately provides a powerful new tool for advancing the forefront of ecosystem biogeochemical studies. Here we describe a method for producing (13)C and (15)N labeled plant material that is either uniformly labeled throughout the plant or differentially labeled in structural and metabolic plant components. Here, we present the construction and operation of a continuous (13)C and (15)N labeling chamber that can be modified to meet various research needs. Uniformly labeled plant material is produced by continuous labeling from seedling to harvest, while differential labeling is achieved by removing the growing plants from the chamber weeks prior to harvest. Representative results from growing Andropogon gerardii Kaw demonstrate the system's ability to efficiently label plant material at the targeted levels. Through this method we have produced plant material with a 4.4 atom%(13)C and 6.7 atom%(15)N uniform plant label, or material that is differentially labeled by up to 1.29 atom%(13)C and 0.56 atom%(15)N in its metabolic and structural components (hot water extractable and hot water residual components, respectively). Challenges lie in maintaining proper temperature, humidity, CO2 concentration, and light levels in an airtight (13)C-CO2 atmosphere for successful plant production. This chamber description represents a useful research tool to effectively produce uniformly or differentially multi-isotope labeled plant material for use in experiments on ecosystem biogeochemical cycling.