Elevated [CO2] effects on crops: Advances in understanding acclimation,nitrogen dynamics and interactions with drought and other organisms

Future rapid increases in atmospheric CO₂ concentration [CO₂] are expected, with values likely to reach ~550 ppm by mid‐century. This implies that every terrestrial plant will be exposed to nearly 40% more of one of the key resources determining plant growth. In this review we highlight selected areas of plant interactions with elevated [CO₂] (e[CO₂]), where recently published experiments challenge long‐held, simplified views. Focusing on crops, especially in more extreme and variable growing conditions, we highlight uncertainties associated with four specific areas. (1) While it is long known that photosynthesis can acclimate to e[CO₂], such acclimation is not consistently observed in field experiments. The influence of sink–source relations and nitrogen (N) limitation on acclimation is investigated and current knowledge about whether stomatal function or mesophyll conductance (g_m) acclimate independently is summarised. (2) We show how the response of N uptake to e[CO₂] is highly variable, even for one cultivar grown within the same field site, and how decreases in N concentrations ([N]) are observed consistently. Potential mechanisms contributing to [N] decreases under e[CO₂] are discussed and proposed solutions are addressed. (3) Based on recent results from crop field experiments in highly variable, non‐irrigated, water‐limited environments, we challenge the previous opinion that the relative CO₂ effect is larger under drier environmental conditions. (4) Finally, we summarise how changes in growth and nutrient concentrations due to e[CO₂] will influence relationships between crops and weeds, herbivores and pathogens in agricultural systems.     

Dynamics of soil CO2 efflux under varying atmospheric CO2 concentrations reveal dominance of slow processes

We evaluated the effect on soil CO₂ efflux (F_CO2) of sudden changes in photosynthetic rates by altering CO₂ concentration in plots subjected to +200 ppmv for 15 years. Five‐day intervals of exposure to elevated CO₂ (eCO₂) ranging 1.0–1.8 times ambient did not affect F_CO2. F_CO2 did not decrease until 4 months after termination of the long‐term eCO₂ treatment, longer than the 10 days observed for decrease of F_CO2 after experimental blocking of C flow to belowground, but shorter than the ~13 months it took for increase of F_CO2 following the initiation of eCO₂. The reduction of F_CO2 upon termination of enrichment (~35%) cannot be explained by the reduction of leaf area (~15%) and associated carbohydrate production and allocation, suggesting a disproportionate contraction of the belowground ecosystem components; this was consistent with the reductions in base respiration and F_CO2‐temperature sensitivity. These asymmetric responses pose a tractable challenge to process‐based models attempting to isolate the effect of individual processes on F_CO2.     

施氮对湿地松(Pinus elliottii)林土壤呼吸和相关因子的影响

人类活动引起陆地生态系统氮输入水平持续升高,对全球碳循环产生影响。为探究氮素对土壤呼吸的影响,2010年6月至2012年1月,采用氮添加试验对亚热带湿地松林的土壤呼吸进行了研究。试验共设置4种氮添加水平:对照CK,0 g m~(-2)a~(-1);低氮LN,5g m~(-2)a~(-1);中氮MN,15 g m~(-2)a~(-1);高氮HN,30 g m~(-2)a~(-1);每月上、下旬采用Li-cor 8100测定土壤呼吸速率。结果表明:(1)氮添加对土壤呼吸有着显著的抑制作用,LN、MN和HN处理的土壤呼吸年累积量较CK处理分别降低了26.6%、23.7%和29.5%,而施氮处理间的土壤呼吸无显著差异;(2)林分生长期间(6-9月),施氮第1年的土壤呼吸所受抑制作用显著高于第2年同期的水平,显示施氮对土壤呼吸的影响随时间的推移而降低;(3)湿地松林土壤呼吸存在明显的季节动态,最大值出现在8月(356.32 mgCO_2 m~(-2)h~(-1)),最小值出现在1月(99.12 mg CO_2 m~(-2)h~(-1)),施氮处理并不改变土壤呼吸的季节性变化规律;(4)CK处理林分中,土壤呼吸与土壤温度间存在极显著的指数关系,而与土壤湿度无显著相关。施氮处理没有改变土壤呼吸与土壤温度之间的相互关系,但抑制了土壤呼吸的温度敏感性(Q_(10));(5)施氮处理显著减少了林分凋落物量、土壤微生物碳、氮量,并轻微抑制了细根生物量,这些改变导致了土壤呼吸的下降。上述结果表明施氮会显著抑制亚热带湿地松林的土壤呼吸速率,而这种抑制作用将随着时间的推移而降低。     

土壤温度和水分对油松林土壤呼吸的影响

用LI-COR 6400-09土壤呼吸测定系统,在太原天龙山自然保护区对油松林的土壤呼吸进行了4a测定.结果表明,土壤呼吸具有明显的季节变化特点,最大值出现在8月份,在6～10 μmol m~(-2) s~(-1) 之间,最小值出现在12月份和3月份,在0.5 μmol m~(-2) s~(-1)左右.2005、2006、2007和2008年土壤呼吸CO_2的年平均值分别为(4.71±3.74)、(3.08±2.91)、(2.96±2.58) μmol m~(-2) s~(-1)和(2.12±1.54) μmol m~(-2) s~(-1);4a的CO_2总平均值为(3.27±2.95) μmol m~(-2) s~(-1).4个测定年土壤呼吸的平均值总体差异显著.4个测定年土壤CO_2释放C量分别为1103.5、882.8、918.4 g m~(-2)和666.3 g m~(-2),总C平均值为892.8 g m~(-2),具有明显的年际差异.指数方程可以很好的表达土壤呼吸与10 cm深度土壤温度的关系,R~2值4a分别为0.39,0.60,0.68和0.71,Q_(10)值分别为3.10,4.41、4.05和5.18,用4a全部数据计算的Q_(10)值为4.31.土壤水分对土壤呼吸的作用较弱,R~2值4a分别仅为0.31、0.25、0.13和0.02,但是夏季土壤干旱对土壤呼吸的抑制作用非常明显,可使土壤呼吸下降50%以上.夏季土壤干旱是导致土壤呼吸年际变化的主要原因.4个包括土壤温度和水分的双变量模型均可以很好地模拟土壤呼吸的季节变化, 拟合方程的R~2值从0.58到0.79.     

Time-dependent responses of soil CO2 efflux components to elevated atmospheric [CO2] and temperature in experimental forest mesocosms

We previously used dual stable isotope techniques to partition soil CO₂ efflux into three source components (rhizosphere respiration, litter decomposition, and soil organic matter (SOM) oxidation) using experimental chambers planted with Douglas-fir [Pseudotsuga menziesii (Mirb.) Franco] seedlings. The components responded differently to elevated CO₂ (ambient + 200 mol mol^–1) and elevated temperature (ambient + 4 °C) treatments during the first year. Rhizosphere respiration increased most under elevated CO₂, and SOM oxidation increased most under elevated temperature. However, many studies show that plants and soil processes can respond to altered climates in a transient way. Herein, we extend our analysis to 2 years to evaluate the stability of the responses of the source components. Total soil CO₂ efflux increased significantly under elevated CO₂ and elevated temperature in both years (1994 and 1995), but the enhancement was much less in 1995. Rhizosphere respiration increased less under elevated temperature in 1995 compared with 1994. Litter decomposition also tended to increase comparatively less in 1995 under elevated CO₂, but was unresponsive to elevated temperature between years. In contrast, SOM oxidation was similar under elevated CO₂ in the 2 years. Less SOM oxidation occurred under elevated temperature in 1995 compared with 1994. Our results indicate that temporal variations can occur in CO₂ production by the sources. The variations likely involve responses to antecedent physical disruption of the soil and physiological processes.     

Constraints to nitrogen acquisition of terrestrial plants under elevated CO2

A key part of the uncertainty in terrestrial feedbacks on climate change is related to how and to what extent nitrogen (N) availability constrains the stimulation of terrestrial productivity by elevated CO₂ (eCO₂), and whether or not this constraint will become stronger over time. We explored the ecosystem‐scale relationship between responses of plant productivity and N acquisition to eCO₂ in free‐air CO₂ enrichment (FACE) experiments in grassland, cropland and forest ecosystems and found that: (i) in all three ecosystem types, this relationship was positive, linear and strong (r² = 0.68), but exhibited a negative intercept such that plant N acquisition was decreased by 10% when eCO₂ caused neutral or modest changes in productivity. As the ecosystems were markedly N limited, plants with minimal productivity responses to eCO₂ likely acquired less N than ambient CO₂‐grown counterparts because access was decreased, and not because demand was lower. (ii) Plant N concentration was lower under eCO₂, and this decrease was independent of the presence or magnitude of eCO₂‐induced productivity enhancement, refuting the long‐held hypothesis that this effect results from growth dilution. (iii) Effects of eCO₂ on productivity and N acquisition did not diminish over time, while the typical eCO₂‐induced decrease in plant N concentration did. Our results suggest that, at the decennial timescale covered by FACE studies, N limitation of eCO₂‐induced terrestrial productivity enhancement is associated with negative effects of eCO₂ on plant N acquisition rather than with growth dilution of plant N or processes leading to progressive N limitation.     

CO2 efflux from a Mediterranean semi-arid forest soil. I. Seasonality and effects of stoniness

We studied the seasonality of total soil CO₂efflux and labeled C-CO₂ released from ¹⁴Clabeled straw incubated in the H horizon of asemi-arid Mediterranean forest soil. Fieldmeasurements were carried out over 520 days in aseries of reconstructed soil profiles with and withouta gravel layer below the H horizon. We monitored soilclimate and related this to soil CO₂ efflux.Seasonal variations in soil CO₂ efflux in asemiarid Mediterranean forest were mainly related tochanges in soil temperature. In spite of drought, highrespiration rates were observed in mid summer. Highsoil CO₂ efflux in hot and dry episodes wasattributed to increases in soil biological activity.The minimum soil CO₂ efflux occurred in latesummer also under dry conditions, probably related toa decrease in soil biological activity in deephorizons. Biological activity in organic layers waslimited by water potential () in summer and bytemperature in winter. Rewetting a dry soil resultedin large increases in soil CO₂ efflux only at hightemperatures. These large increases represented asignificant contribution to the decomposition oforganic matter in the uppermost horizons. Soilbiological activity in the uppermost horizons was moresensitive to changes in soil and hence tosummer rainstorms than the bulk soil microbialactivity. The presence of a layer of gravel improvedboth moisture and temperature conditions for thedecomposition of organic matter. As a result, soilCO₂ efflux increased in soils containing rockfragments. These effects were especially large for theorganic layers.     

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 ¹³CO₂ 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.     

Contrasting effects of low and high nitrogen additions on soil CO2 flux components and ectomycorrhizal fungal sporocarp production in a boreal forest

Nitrogen (N) added through atmospheric deposition or as fertilizer to boreal and temperate forests reduces both soil decomposer activity (heterotrophic respiration) and the activity of roots and mycorrhizal fungi (autotrophic respiration). However, these negative effects have been found in studies that applied relatively high levels of N, whereas the responses to ambient atmospheric N deposition rates are still not clear. Here, we compared an unfertilized control boreal forest with a fertilized forest (100 kg N ha^?1 yr^?1) and a forest subject to N‐deposition rates comparable to those in Central Europe (20 kg N ha^?1 yr^?1) to investigate the effects of N addition rate on different components of forest floor respiration and the production of ectomycorrhizal fungal sporocarps. Soil collars were used to partition heterotrophic (R_h) and autotrophic (R_a) respiration, which was further separated into respiration by tree roots (R_tr) and mycorrhizal hyphae (R_m). Total forest floor respiration was twice as high in the low N plot compared to the control, whereas there were no differences between the control and high N plot. There were no differences in R_h respiration among plots. The enhanced forest floor respiration in the low N plot was, therefore, the result of increased R_a respiration, with an increase in R_tr respiration, and a doubling of R_m respiration. The latter was corroborated by a slightly greater ectomycorrhizal (EM) fungal sporocarp production in the low N plot as compared to the control plot. In contrast, EM fungal sporocarp production was nearly eliminated, and R_m respiration severely reduced, in the high N plot, which resulted in significantly lower R_a respiration. We thus found a nonlinear response of the R_a components to N addition rate, which calls for further studies of the quantitative relations among N addition rate, plant photosynthesis and carbon allocation, and the function of EM fungi.     

Legume species identity and soil nitrogen supply determine symbiotic nitrogen-fixation responses to elevated atmospheric [CO2

In nitrogen (N)-limited systems, the response of symbiotic N fixation to elevated atmospheric [CO2] may be an important determinant of ecosystem responses to this global change. Experimental tests of the effects of elevated [CO2] have not been consistent. Although rarely tested, differences among legume species and N supply may be important. In a field free-air CO2 enrichment (FACE) experiment, we determined, for four legume species, whether the effects of elevated atmospheric [CO2] on symbiotic N fixation depended on soil N availability or species identity. Natural abundance and pool-dilution 15N methods were used to estimate N fixation. Although N addition did, in general, decrease N fixation, contrary to theoretical predictions, elevated [CO2] did not universally increase N fixation. Rather, the effect of elevated [CO2] on N fixation was positive, neutral or negative, depending on the species and N addition. Our results suggest that legume species identity and N supply are critical factors in determining symbiotic N-fixation responses to increased atmospheric [CO2].     

No cumulative effect of 10 years of elevated [CO2] on perennial plant biomass components in the Mojave Desert

Elevated atmospheric CO₂ concentrations ([CO₂]) generally increase primary production of terrestrial ecosystems. Production responses to elevated [CO₂] may be particularly large in deserts, but information on their long‐term response is unknown. We evaluated the cumulative effects of elevated [CO₂] on primary production at the Nevada Desert FACE (free‐air carbon dioxide enrichment) Facility. Aboveground and belowground perennial plant biomass was harvested in an intact Mojave Desert ecosystem at the end of a 10‐year elevated [CO₂] experiment. We measured community standing biomass, biomass allocation, canopy cover, leaf area index (LAI), carbon and nitrogen content, and isotopic composition of plant tissues for five to eight dominant species. We provide the first long‐term results of elevated [CO₂] on biomass components of a desert ecosystem and offer information on understudied Mojave Desert species. In contrast to initial expectations, 10 years of elevated [CO₂] had no significant effect on standing biomass, biomass allocation, canopy cover, and C : N ratios of above‐ and belowground components. However, elevated [CO₂] increased short‐term responses, including leaf water‐use efficiency (WUE) as measured by carbon isotope discrimination and increased plot‐level LAI. Standing biomass, biomass allocation, canopy cover, and C : N ratios of above‐ and belowground pools significantly differed among dominant species, but responses to elevated [CO₂] did not vary among species, photosynthetic pathway (C₃ vs. C₄), or growth form (drought‐deciduous shrub vs. evergreen shrub vs. grass). Thus, even though previous and current results occasionally show increased leaf‐level photosynthetic rates, WUE, LAI, and plant growth under elevated [CO₂] during the 10‐year experiment, most responses were in wet years and did not lead to sustained increases in community biomass. We presume that the lack of sustained biomass responses to elevated [CO₂] is explained by inter‐annual differences in water availability. Therefore, the high frequency of low precipitation years may constrain cumulative biomass responses to elevated [CO₂] in desert environments.     

Using ecosystem CO2 measurements to estimate the timing and magnitude of greenhouse gas mitigation potential of forest bioenergy

Forest bioenergy opportunities may be hindered by a long greenhouse gas (GHG) payback time. Estimating this payback time requires the quantification of forest‐atmosphere carbon exchanges, usually through process‐based simulation models. Such models are prone to large uncertainties, especially over long‐term carbon fluxes from dead organic matter pools. We propose the use of whole ecosystem field‐measured CO₂ exchanges obtained from eddy covariance flux towers to assess the GHG mitigation potential of forest biomass projects as a way to implicitly integrate all field‐level CO₂ fluxes and the inter‐annual variability in these fluxes. As an example, we perform the evaluation of a theoretical bioenergy project that uses tree stems as bioenergy feedstock and include multi‐year measurements of net ecosystem exchange (NEE) from forest harvest chronosequences in the boreal forest of Canada to estimate the time dynamics of ecosystem CO₂ exchanges following harvesting. Results from this approach are consistent with previous results using process‐based models and suggest a multi‐decadal payback time for our project. The time for atmospheric carbon debt repayment of bioenergy projects is highly dependent on ecosystem‐level CO₂ exchanges. The use of empirical NEE measurements may provide a direct evaluation of, or at least constraints on, the GHG mitigation potential of forest bioenergy projects.     

Interactive effects of soil nitrogen and atmospheric carbon dioxide on root/rhizosphere carbon dioxide efflux from loblolly and ponderosa pine seedlings

We measured CO₂ efflux from intact root/rhizosphere systems of 155 day old loblolly (Pinus taeda L.) and ponderosa (Pinus ponderosa Dougl. ex Laws.) pine seedlings in order to study the effects of elevated atmospheric CO₂ on the below-ground carbon balance of coniferous tree seedlings. Seedlings were grown in sterilized sand culture, watered daily with either 1, 3.5 or 7 mt M NH ₄ ⁺ , and maintained in an atmosphere of either 35 or 70 Pa CO₂. Carbon dioxide efflux (mol CO₂ plant^–1 s^–1) from the root/rhizosphere system of both species significantly increased when seedlings were grown in elevated CO₂, primarily due to large increases in root mass. Specific CO₂ efflux (mol CO₂ g root^–1 s^–1) responded to CO₂ only under conditions of adequate soil nitrogen availability (3.5 mt M). Under these conditions, CO₂ efflux rates from loblolly pine increased 70% from 0.0089 to 0.0151 mol g^–1 s^–1 with elevated CO₂ while ponderosa pine responded with a 59% decrease, from 0.0187 to 0.0077 mol g^–1 s^–1. Although below ground CO₂ efflux from seedlings grown in either sub-optimal (1 mt M) or supra-optimal (7 mt M) nitrogen availability did not respond to CO₂, there was a significant nitrogen treatment effect. Seedlings grown in supra-optimal soil nitrogen had significantly increased specific CO₂ efflux rates, and significantly lower total biomass compared to either of the other two nitrogen treatments. These results indicate that carbon losses from the root/rhizosphere systems are responsive to environmental resource availability, that the magnitude and direction of these responses are species dependent, and may lead to significantly different effects on whole plant carbon balance of these two forest tree species.     

Leaf traits of two Mediterranean perennial tussock grass species in relation to soil nitrogen and phosphorus availability

Studying relationships of plant traits to ecosystem properties is an emerging approach aiming to understand plant's potential effect on ecosystem functioning. In the current study, we explored links between morphological and nutritional leaf traits of two Mediterranean perennial grass species Stipa tenacissima and Lygeum spartum, widely used to prevent desertification process by stabilizing sand dunes. We evaluated also relationships in terms of nitrogen (N) and phosphorus (P) availability between leaves of the investigated species and the corresponding soil. Our results showed that leaf P was very low in comparison with leaf N for the two investigated species. In fact, chlorophyll content, photosynthesis capacity and water conservation during photosynthesis are mainly linked to leaf nitrogen content. Our findings support previous studies showing that at the species levels, morphological and nutritional leaf traits were not related. On the other hand, significant relationships were obtained between soil N and leaf N for S. tenacissima (P = 0.011) and L. spartum (P = 0.033). However, leaf P was not significantly related to soil P availability for both species. We suggest that any decrease in soil N with the predicted increasing aridity may result in reduction in leaf N and thus in worst dysfunction of some biological processes levels.     

Elevated carbon dioxide increases soil nitrogen and phosphorus availability in a phosphorus‐limited Eucalyptus woodland

Free‐air CO₂ enrichment (FACE) experiments have demonstrated increased plant productivity in response to elevated (e)CO₂, with the magnitude of responses related to soil nutrient status. Whilst understanding nutrient constraints on productivity responses to eCO₂ is crucial for predicting carbon uptake and storage, very little is known about how eCO₂ affects nutrient cycling in phosphorus (P)‐limited ecosystems. Our study investigates eCO₂ effects on soil N and P dynamics at the EucFACE experiment in Western Sydney over an 18‐month period. Three ambient and three eCO₂ (+150 ppm) FACE rings were installed in a P‐limited, mature Cumberland Plain Eucalyptus woodland. Levels of plant accessible nutrients, evaluated using ion exchange resins, were increased under eCO₂, compared to ambient, for nitrate (+93%), ammonium (+12%) and phosphate (+54%). There was a strong seasonality to responses, particularly for phosphate, resulting in a relatively greater stimulation in available P, compared to N, under eCO₂ in spring and summer. eCO₂ was also associated with faster nutrient turnover rates in the first six months of the experiment, with higher N (+175%) and P (+211%) mineralization rates compared to ambient rings, although this difference did not persist. Seasonally dependant effects of eCO₂ were seen for concentrations of dissolved organic carbon in soil solution (+31%), and there was also a reduction in bulk soil pH (‐0.18 units) observed under eCO₂. These results demonstrate that CO₂ fertilization increases nutrient availability – particularly for phosphate – in P‐limited soils, likely via increased plant belowground investment in labile carbon and associated enhancement of microbial turnover of organic matter and mobilization of chemically bound P. Early evidence suggests that there is the potential for the observed increases in P availability to support increased ecosystem C‐accumulation under future predicted CO₂ concentrations.     

模拟氮沉降增加对寒温带针叶林土壤 CO2排放的初期影响

研究大气氮沉降增加情景下北方森林土壤CO2排放通量及其相关控制因子至关重要。在大兴安岭寒温带针叶林区建立了大气氮沉降模拟控制试验,利用静态箱-气相色谱法测定土壤CO2排放通量,同时测定土壤温度、水分、无机氮和可溶性碳含量等相关变量,分析寒温带针叶林土壤CO2排放特征及其主要驱动因子。结果表明:氮素输入没有显著改变森林土壤含水量,但降低了有机层土壤溶解性无机碳(DIC)含量,并增加有机层和矿质层土壤溶解性有机碳(DOC)含量。增氮短期内不影响土壤NH+4-N含量,但促进了土壤NO-3-N的累积。增氮倾向于增加北方森林土壤CO2排放。土壤CO2通量主要受土壤温度驱动,其次为土壤水分和DIC含量。虽然土壤温度整体上控制着土壤CO2通量的季节变化格局,但在生长旺季土壤含水量对其影响更为明显。在分析增氮对土壤CO2通量的净效应时,除了土壤温度和水分外,还要考虑土壤有效碳、氮动态的影响。