The turnover of carbon pools contributing to soil CO2 and soil respiration in a temperate forest exposed to elevated CO2 concentration

Soil carbon is returned to the atmosphere through the process of soil respiration, which represents one of the largest fluxes in the terrestrial C cycle. The effects of climate change on the components of soil respiration can affect the sink or source capacity of ecosystems for atmospheric carbon, but no current techniques can unambiguously separate soil respiration into its components. Long‐term free air CO₂ enrichment (FACE) experiments provide a unique opportunity to study soil C dynamics because the CO₂ used for fumigation has a distinct isotopic signature and serves as a continuous label at the ecosystem level. We used the ¹³C tracer at the Duke Forest FACE site to follow the disappearance of C fixed before fumigation began in 1996 (pretreatment C) from soil CO₂ and soil‐respired CO₂, as an index of belowground C dynamics during the first 8 years of the experiment. The decay of pretreatment C as detected in the isotopic composition of soil‐respired CO₂ and soil CO₂ at 15, 30, 70, and 200 cm soil depth was best described by a model having one to three exponential pools within the soil system. The majority of soil‐respired CO₂ (71%) originated in soil C pools with a turnover time of about 35 days. About 55%, 50%, and 68% of soil CO₂ at 15, 30, and 70 cm, respectively, originated in soil pools with turnover times of less than 1 year. The rest of soil CO₂ and soil‐respired CO₂ originated in soil pools that turn over at decadal time scales. Our results suggest that a large fraction of the C returned to the atmosphere through soil respiration results from dynamic soil C pools that cannot be easily detected in traditionally defined soil organic matter standing stocks. Fast oxidation of labile C substrates may prevent increases in soil C accumulation in forests exposed to elevated [CO₂] and may consequently result in shorter ecosystem C residence times.     

Response of soil surface CO2 flux in a boreal forest to ecosystem warming

Soil surface carbon dioxide (CO₂) flux (R_S) was measured for 2 years at the Boreal Soil and Air Warming Experiment site near Thompson, MB, Canada. The experimental design was a complete random block design that consisted of four replicate blocks, with each block containing a 15 m × 15 m control and heated plot. Black spruce [Picea mariana (Mill.) BSP] was the overstory species and Epilobium angustifolium was the dominant understory. Soil temperature was maintained (～5 °C) above the control soil temperature using electric cables inside water filled polyethylene tubing for each heated plot. Air inside a 7.3‐m‐diameter chamber, centered in the soil warming plot, contained approximately nine black spruce trees was heated ～5 °C above control ambient air temperature allowing for the testing of soil‐only warming and soil+air warming. Soil surface CO₂ flux (R_S) was positively correlated (P < 0.0001) to soil temperature at 10 cm depth. Soil surface CO₂ flux (R_S) was 24% greater in the soil‐only warming than the control in 2004, but was only 11% greater in 2005, while R_S in the soil+air warming treatments was 31% less than the control in 2004 and 23% less in 2005. Live fine root mass (< 2 mm diameter) was less in the heated than control treatments in 2004 and statistically less (P < 0.01) in 2005. Similar root mass between the two heated treatments suggests that different heating methods (soil‐only vs. soil+air warming) can affect the rate of decomposition.     

The response of heterotrophic CO2 flux to soil warming

In a forest ecosystem at steady state, net carbon (C) assimilation by plants and C loss through soil and litter decomposition by heterotrophic organisms are balanced. However, a perturbation to the system, such as increased mean soil temperature, will lead to faster decay, enhancing CO₂ release from decomposers, and thus upsetting the balance. Recent in situ experiments have indicated that the stimulation of soil respiration following a step increase in annual average soil temperature declines over time. One possible explanation for this decline may be changes in substrate availability. This hypothesis is examined by using the ecosystem model G'DAY, which simulates C and nitrogen (N) dynamics in plants and soil. We applied the model to observations from a soil‐warming experiment in a Norway spruce (Picea abies (L.) Karst.) stand by simulating a step increase of soil temperature. The model provided a good qualitative reproduction of the observed reduction of heterotrophic respiration (R_h) under sustained warming. The simulations showed how the combined effects of faster turnover and reduced substrate availability lead to a transient increase of R_h. The simulated annual increase in R_h from soil was 60% in the first year after perturbation but decreased to 30% after a decade. One conclusion from the analysis of the simulations is that R_h can decrease even though the temperature response function for decomposition remains unchanged. G'DAY suggests that acclimation of R_h to soil warming is partly an effect of substrate depletion of labile C pools during the first decade of warming as a result of accelerated rates of mineralization. The response is attributed mainly to changing levels of C in pools with short time constants, reflecting the importance of high‐quality soil C fractions. Changes of the structure or physiology of the decomposer community were not invoked. Therefore, it becomes a question of definition whether the simulated dynamics of the declining response of CO₂ release to the warming should be named acclimation or seen as a natural part of the system dynamics.     

The temporal response of forest ecosystems to doubled atmospheric CO2 concentration

Vegetation responses to high [CO₂] include both direct photosynthetic effects and indirect effects associated with various plant and soil feedbacks. Synthesis of these direct and indirect effects requires ecosystem process models describing the cycling of carbon and essential mineral nutrients through plants and soils. Here we use the ecosystem model G'DAY to investigate responses to an instantaneous doubling of [CO₂]. The analysis indicates that the magnitude and even direction of the growth response to high [CO₂] can vary widely on different timescales, because responses on different timescales are determined by different ecosystem-level feedbacks and hence by different sets of key model parameters. Of particular importance are parameters describing the flexibility of plant and soil nitrogen to carbon (N:C) ratios; large responses occur if N:C ratios decline significantly at high [CO₂], with little or no response if N:C ratios are inflexible. According to G'DAY, the CO₂-response changes over time because responses on longer timescales are dictated by the N:C ratios of less rapidly cycled organic matter.     

Influence of atmospheric CO2 enrichment on methane consumption in a temperate forest soil

Rates of atmospheric CH₄ consumption of soils in temperate forest were compared in plots continuously enriched with CO₂ at 200 µL L^?1 above ambient and in control plots exposed to the ambient atmosphere of 360 µL CO₂ L^?1. The purpose was to determine if ecosystem atmospheric CO₂ enrichment would alter soil microbial CH₄ consumption at the forest floor and if the effect of CO₂ would change with time or with environmental conditions. Reduced CH₄ consumption was observed in CO₂‐enriched plots relative to control plots on 46 out of 48 sampling dates, such that CO₂‐enriched plots showed annual reductions in CH₄ consumption of 16% in 1998 and 30% in 1999. No significant differences were observed in soil moisture, temperature, pH, inorganic‐N or rates of N‐mineralization between CO₂‐enriched and control plots, indicating that differences in CH₄ consumption between treatments were likely the result of changes in the composition or size of the CH₄‐oxidizing microbial community. A repeated measures analysis of variance that included soil moisture, soil temperature (from 0 to 30 cm), and time as covariates indicated that the reduction of CH₄ consumption under elevated CO₂ was enhanced at higher soil temperatures. Additionally, the effect of elevated CO₂ on CH₄ consumption increased with time during the two‐year study. Overall, these data suggest that rising atmospheric CO₂ will reduce atmospheric CH₄ consumption in temperate forests and that the effect will be greater in warmer climates. A 30% reduction in atmospheric CH₄ consumption by temperate forest soils in response to rising atmospheric CO₂ will result in a 10% reduction in the sink strength of temperate forest soils in the atmospheric CH₄ budget and a positive feedback to the greenhouse effect.     

CO2 flux from soil in pastures and forests in southwestern Amazonia

Stocks of carbon in Amazonian forest biomass and soils have received considerable research attention because of their potential as sources and sinks of atmospheric CO₂. Fluxes of CO₂ from soil to the atmosphere, on the other hand, have not been addressed comprehensively in regard to temporal and spatial variations and to land cover change, and have been measured directly only in a few locations in Amazonia. Considerable variation exists across the Amazon Basin in soil properties, climate, and management practices in forests and cattle pastures that might affect soil CO₂ fluxes. Here we report soil CO₂ fluxes from an area of rapid deforestation in the southwestern Amazonian state of Acre. Specifically we addressed (1) the seasonal variation of soil CO₂ fluxes, soil moisture, and soil temperature; (2) the effects of land cover (pastures, mature, and secondary forests) on these fluxes; (3) annual estimates of soil respiration; and (4) the relative contributions of grass‐derived and forest‐derived C as indicated by δ¹³CO₂. Fluxes were greatest during the wet season and declined during the dry season in all land covers. Soil respiration was significantly correlated with soil water‐filled pore space but not correlated with temperature. Annual fluxes were higher in pastures compared with mature and secondary forests, and some of the pastures also had higher soil C stocks. The δ¹³C of CO₂ respired in pasture soils showed that high respiration rates in pastures were derived almost entirely from grass root respiration and decomposition of grass residues. These results indicate that the pastures are very productive and that the larger flux of C cycling through pasture soils compared with forest soils is probably due to greater allocation of C belowground. Secondary forests had soil respiration rates similar to mature forests, and there was no correlation between soil respiration and either forest age or forest biomass. Hence, belowground allocation of C does not appear to be directly related to the stature of vegetation in this region. Variation in seasonal and annual rates of soil respiration of these forests and pastures is more indicative of flux of C through the soil rather than major net changes in ecosystem C stocks.     

Net grassland carbon flux over a subambient to superambient CO2 gradient

Increasing atmospheric CO₂ concentrations may have a profound effect on the structure and function of plant communities. A previously grazed, central Texas grassland was exposed to a 200‐µmol mol^?1 to 550 µmol mol^?1 CO₂ gradient from March to mid‐December in 1998 and 1999 using two, 60‐m long, polyethylene‐ covered chambers built directly onto the site. One chamber was operated at subambient CO₂ concentrations (200–360 µmol mol^?1 daytime) and the other was regulated at superambient concentrations (360–550 µmol mol^?1). Continuous CO₂ gradients were maintained in each chamber by photosynthesis during the day and respiration at night. Net ecosystem CO₂ flux and end‐of‐year biomass were measured in each of 10, 5‐m long sections in each chamber. Net CO₂ fluxes were maximal in late May (c. day 150) in 1998 and in late August in 1999 (c. day 240). In both years, fluxes were near zero and similar in both chambers at the beginning and end of the growing season. Average daily CO₂ flux in 1998 was 13 g CO₂ m^?2 day^?1 in the subambient chamber and 20 g CO₂ m^?2 day^?1 in the superambient chamber; comparable averages were 15 and 26 g CO₂ m^?2 day^?1 in 1999. Flux was positively and linearly correlated with end‐of‐year above‐ground biomass but flux was not linearly correlated with CO₂ concentration; a finding likely to be explained by inherent differences in vegetation. Because C₃ plants were the dominant functional group, we adjusted average daily flux in each section by dividing the flux by the average percentage C₃ cover. Adjusted fluxes were better correlated with CO₂ concentration, although scatter remained. Our results indicate that after accounting for vegetation differences, CO₂ flux increased linearly with CO₂ concentration. This trend was more evident at subambient than superambient CO₂ concentrations.     

Simulated mechanisms of soil N feedback on the forest CO2 response

An improved understanding of the response of forest ecosystems to elevated levels of CO₂ in the atmosphere is crucial because atmospheric CO₂ concentration continues to increase at an accelerating rate and forests are an important sink in the global carbon cycle. Several CO₂‐enrichment experiments have now been running for more than 10 years, with highly variable short‐term results after the first decade. Responses to rising [CO₂] over the next few decades will depend on several plant and ecosystem feedbacks that are inadequately understood. In this study, we conduct a sensitivity analysis, within the context of the simulated CO₂ response, using a new version of the G'DAY ecosystem model, with an improved decomposition submodel, applied to a nitrogen‐limited Norway spruce forest site in the north of Sweden. The new decomposition model incorporates important modifications to soil processes, including some that constitute negative feedbacks on an ecosystem's growth response to elevated [CO₂]. The sensitivity analysis reveals key parameters and processes that are important for the simulated CO₂ response on the short term and others that are more important on the long term. A process that has a strong impact on the short‐term response is a change in decomposer composition, potentially in response to altered litter quality. Parameters that become increasingly important in the long term are carbon allocation to root exudates that are directly or indirectly associated with atmospheric N₂ fixation, and the rate of humification of soil organic matter. We identify factors intrinsic to species and site (microbes and resources) and ecosystem nutrient supply that determine the duration of the enhanced simulated growth response to elevated [CO₂].     

The impact of elevated CO2, increased nitrogen availability and biodiversity on plant tissue quality and decomposition

Elevated CO₂, increased nitrogen (N) deposition and increasing species richness can increase net primary productivity (NPP). However, unless there are comparable changes in decomposition, increases in productivity will most likely be unsustainable. Without comparable increases in decomposition nutrients would accumulate in dead organic matter leading to nutrient limitations that could eventually prohibit additional increases in productivity. To address this issue, we measured aboveground plant and litter quality and belowground root quality, as well as decomposition of aboveground litter for one and 2‐year periods using in situ litterbags in response to a three‐way factorial manipulation of CO₂ (ambient vs. 560 ppm), N deposition (ambient vs. the addition of 4 g N m⁻² yr⁻¹) and plant species richness (one, four, nine and 16 species) in experimental grassland plots. Litter chemistry responded to the CO₂, N and plant diversity treatments, but decomposition was much less responsive. Elevated CO₂ induced decreases in % N and % lignin in plant tissues. N addition led to increases in % N and decreases in % lignin. Increasing plant diversity led to decreases in % N and % lignin and an increase in % cellulose. In contrast to the litter chemistry changes, elevated CO₂ had a much lower impact on decomposition and resulted in only a 2.5% decrease in carbon (C) loss. Detectable responses were not observed either to N addition or to species richness. These results suggest that global change factors such as biodiversity loss, elevated CO₂ and N deposition lead to significant changes in tissue quality; however, the response of decomposition is modest. Thus, the observed increases in productivity at higher diversity levels and with elevated CO₂ and N fertilization are not matched by an increase in decomposition rates. This lack of coupled responses between production and decomposition is likely to result in an accumulation of nutrients in the litter pool which will dampen the response of NPP to these factors over time.     

Terrestrial higher-plant response to increasing atmospheric [CO2] in relation to the global carbon cycle

Terrestrial higher plants exchange large amounts of CO₂ with the atmosphere each year; c. 15% of the atmospheric pool of C is assimilated in terrestrial-plant photosynthesis each year, with an about equal amount returned to the atmosphere as CO₂ in plant respiration and the decomposition of soil organic matter and plant litter. Any global change in plant C metabolism can potentially affect atmospheric CO₂ content during the course of years to decades. In particular, plant responses to the presently increasing atmospheric CO₂ concentration might influence the rate of atmospheric CO₂ increase through various biotic feedbacks. Climatic changes caused by increasing atmospheric CO₂ concentration may modulate plant and ecosystem responses to CO₂ concentration. Climatic changes and increases in pollution associated with increasing atmospheric CO₂ concentration may be as significant to plant and ecosystem C balance as CO₂ concentration itself. Moreover, human activities such as deforestation and livestock grazing can have impacts on the C balance and structure of individual terrestrial ecosystems that far outweigh effects of increasing CO₂ concentration and climatic change. In short-term experiments, which in this case means on the order of 10 years or less, elevated atmospheric CO₂ concentration affects terrestrial higher plants in several ways. Elevated CO₂ can stimulate photosynthesis, but plants may acclimate and (or) adapt to a change in atmospheric CO₂ concentration. Acclimation and adaptation of photosynthesis to increasing CO₂ concentration is unlikely to be complete, however. Plant water use efficiency is positively related to CO₂ concentration, implying the potential for more plant growth per unit of precipitation or soil moisture with increasing atmospheric CO₂ concentration. Plant respiration may be inhibited by elevated CO₂ concentration, and although a naive C balance perspective would count this as a benefit to a plant, because respiration is essential for plant growth and health, an inhibition of respiration can be detrimental. The net effect on terrestrial plants of elevated atmospheric CO₂ concentration is generally an increase in growth and C accumulation in phytomass. Published estimations, and speculations about, the magnitude of global terrestrial-plant growth responses to increasing atmospheric CO₂ concentration range from negligible to fantastic. Well-reasoned analyses point to moderate global plant responses to CO₂ concentration. Transfer of C from plants to soils is likely to increase with elevated CO₂ concentrations because of greater plant growth, but quantitative effects of those increased inputs to soils on soil C pool sizes are unknown. Whether increases in leaf-level photosynthesis and short-term plant growth stimulations caused by elevated atmospheric CO₂ concentration will have, by themselves, significant long-term (tens to hundreds of years) effects on ecosystem C storage and atmospheric CO₂ concentration is a matter for speculation, not firm conclusion. Long-term field studies of plant responses to elevated atmospheric CO₂ are needed. These will be expensive, difficult, and by definition, results will not be forthcoming for at least decades. Analyses of plants and ecosystems surrounding natural geological CO₂ degassing vents may provide the best surrogates for long-term controlled experiments, and therefore the most relevant information pertaining to long-term terrestrial-plant responses to elevated CO₂ concentration, but pollutants associated with the vents are a concern in some cases, and quantitative knowledge of the history of atmospheric CO₂ concentrations near vents is limited. On the whole, terrestrial higher-plant responses to increasing atmospheric CO₂ concentration probably act as negative feedbacks on atmospheric CO₂ concentration increases, but they cannot by themselves stop the fossil-fuel-oxidation-driven increase in atmospheric CO₂ concentration. And, in the very long-term, atmospheric CO₂ concentration is controlled by atmosphere-ocean C equilibrium rather than by terrestrial plant and ecosystem responses to atmospheric CO₂ concentration.     

Soil CO2 efflux in a boreal pine forest under atmospheric CO2 enrichment and air warming

The response of forest soil CO₂ efflux to the elevation of two climatic factors, the atmospheric concentration of CO₂ (↑CO₂ of 700 μmol mol⁻¹) and air temperature (↑ T with average annual increase of 5°C), and their combination (↑CO₂+↑ T ) was investigated in a 4-year, full-factorial field experiment consisting of closed chambers built around 20-year-old Scots pines ( Pinus sylvestris L.) in the boreal zone of Finland. Mean soil CO₂ efflux in May–October increased with elevated CO₂ by 23–37%, with elevated temperature by 27–43%, and with the combined treatment by 35–59%. Temperature elevation was a significant factor in the combined 4-year efflux data, whereas the effect of elevated CO₂ was not as evident. Elevated temperature had the most pronounced impact early and late in the season, while the influence of elevated CO₂ alone was especially notable late in the season. Needle area was found to be a significant predictor of soil CO₂ efflux, particularly in August, a month of high root growth, thus supporting the assumption of a close link between whole-tree physiology and soil CO₂ emissions. The decrease in the temperature sensitivity of soil CO₂ efflux observed in the elevated temperature treatments in the second year nevertheless suggests the existence of soil response mechanisms that may be independent of the assimilating component of the forest ecosystem. In conclusion, elevated atmospheric CO₂ and air temperature consistently increased forest soil CO₂ efflux over the 4-year period, their combined effect being additive, with no apparent interaction.     

The stomatal response to CO2 is linked to changes in guard cell zeaxanthin*

The mechanisms mediating CO₂ sensing and light–CO₂ interactions in guard cells are unknown. In growth chamber-grown Vicia faba leaves kept under constant light (500 μ mol m^–2 s^–1) and temperature, guard cell zeaxanthin content tracked ambient [CO₂] and stomatal apertures. Increases in [CO₂] from 400 to 1200 cm³ m^–3 decreased zeaxanthin content from 180 to 80 mmol mol^–1 Chl and decreased stomatal apertures by 7·0 μ m. Changes in zeaxanthin and aperture were reversed when [CO₂] was lowered. Guard cell zeaxanthin content was linearly correlated with stomatal apertures. In the dark, the CO₂-induced changes in stomatal aperture were much smaller, and guard cell zeaxanthin content did not change with chamber [CO₂]. Guard cell zeaxanthin also tracked [CO₂] and stomatal aperture in illuminated stomata from epidermal peels. Dithiothreitol (DTT), an inhibitor of zeaxanthin formation, eliminated CO₂-induced zeaxanthin changes in guard cells from illuminated epidermal peels and reduced the stomatal CO₂ response to the level observed in the dark. These data suggest that CO₂-dependent changes in the zeaxanthin content of guard cells could modulate CO₂-dependent changes of stomatal apertures in the light while a zeaxanthin-independent CO₂ sensing mechanism would modulate the CO₂ response in the dark.     

Changes in net photosynthesis and growth of Pinus eldarica seedlings in response to atmospheric CO2 enrichment

Pinus eldarica L. trees, rooted in the natural soil of an agricultural field at Phoenix, Arizona, were grown from the seedling stage in clear-plastic-wall open-top enclosures maintained at four different atmospheric CO₂ concentrations for 15 months. Light response functions were determined for one tree from each treatment by means of whole-tree net CO₂ exchange measurements at the end of this period, after which rates of carbon assimilation of an ambient-treatment tree were measured across a range of atmospheric CO₂ concentrations. The first of these data sets incorporates the consequences of both the CO₂-induced enhancement of net photosynthesis per unit needle area and the CO₂-induced enhancement of needle area itself (due primarily to the production of more needles), whereas the second data set reflects only the first of these effects. Hence the division of the normalized results of the first data set by the normalized results of the second set yields a representation of the increase in whole-tree net photosynthesis due to enhanced needle production caused by atmospheric CO₂ enrichment. In the solitary trees we studied, the relative contribution of this effect increased rapidly with the CO₂ concentration of the air to increase whole-tree net photosynthesis by nearly 50% at a CO₂ concentration approximately 300 μmol mol⁻¹ above ambient.     

Carbon accumulation, distribution and water use of Danthonia richardsonii swards in response to CO2 and nitrogen supply over four years of growth

Microcosms of Danthonia richardsonii (Cashmore) accumulated more carbon when grown under CO₂ enrichment (719 μL L^–1 cf. 359 μL L^–1) over a four-year period, even when nitrogen availability severely restricted productivity (enhancement ratios for total microcosm C accumulation of 1.21, 1.14 and 1.29 for mineral N supplies of 2.2, 6.7 and 19.8 g N m^–2 y^–1, respectively). The effect of CO₂ enrichment on total system carbon content did not diminish with time. Increased carbon accumulation occurred despite the development over time of a lower leaf area index and less carbon in the green leaf fraction at high CO₂. The extra carbon accumulated at high CO₂ in the soil, senesced leaf and leaf litter fractions at all N levels, and in root at high-N, while at low-and mid-N less carbon accumulated in the root fraction at high CO₂. The rate of leaf turnover was increased under CO₂ enrichment, as indicated by increases in the carbon mass ratio of senesced to green leaf lamina. Microcosm evapotranspiration rates were lower at high CO₂ when water was in abundant supply, resulting in higher average soil water contents. The higher soil water contents at high CO₂ have important implications for microcosm function, and may have contributed significantly to the increased carbon accumulation at high CO₂. These results indicate that CO₂ enrichment can increase carbon accumulation by a simple soil–plant system, and that any increase in whole system carbon accumulation may not be evident from snapshot measurements of live plant carbon.