Separating root and soil microbial contributions to soil respiration: A review of methods and observations

Forest soil respiration is the sum of heterotrophic (microbes, soil fauna) and autotrophic (root) respiration. The contribution of each group needs to be understood to evaluate implications of environmental change on soil carbon cycling and sequestration. Three primary methods have been used to distinguish hetero- versus autotrophic soil respiration including: integration of components contributing to in situ forest soil CO₂ efflux (i.e., litter, roots, soil), comparison of soils with and without root exclusion, and application of stable or radioactive isotope methods. Each approach has advantages and disadvantages, but isotope based methods provide quantitative answers with the least amount of disturbance to the soil and roots. Published data from all methods indicate that root/rhizosphere respiration can account for as little as 10 percent to greater than 90 percent of total in situ soil respiration depending on vegetation type and season of the year. Studies which have integrated percent root contribution to total soil respiration throughout an entire year or growing season show mean values of 45.8 and 60.4 percent for forest and nonforest vegetation, respectively. Such average annual values must be extrapolated with caution, however, because the root contribution to total soil respiration is commonly higher during the growing season and lower during the dormant periods of the year.     

植物源和土壤有机质源土壤呼吸组分的拆分原理、方法与应用进展

区分土壤呼吸组分并揭示其与环境因素的相关关系,对于准确评估土壤碳过程及其环境影响机制至关重要。根据底物来源和作用机制的差异,土壤呼吸主要包括根系呼吸、根际微生物呼吸、凋落物分解、自然条件下和激发效应下土壤有机质（SOM）分解。现有土壤呼吸组分拆分方法可以分为基于植物源CO₂测定或土壤有机质源CO₂测定的差分拆分方法,以及基于土壤呼吸组分同位素信号差异的拆分方法。土壤呼吸组分拆分研究可以解决不同土壤呼吸组分对环境变化的响应机制、植物光合碳输入与地下土壤呼吸组分的交互作用、土壤呼吸组分变化对土壤碳库周转的影响机制等科学问题,但其理论假设、观测技术方法、潜在的误差来源等仍需要继续关注并系统研究。     

Partitioning the components of soil respiration: a research challenge

Little is known about the respiratory components of CO₂ emitted from soils and attaining a reliable quantification of the contribution of root respiration remains one of the major challenges facing ecosystem research. Resolving this would provide major advances in our ability to predict ecosystem responses to climate change. The merits and technical and theoretical difficulties associated with different approaches adopted for partitioning respiration components are discussed here. The way forward is suggested to be the development of non-invasive regression analysis validated by stable isotope approaches to increase the sensitivity of model functions to include components of rhizosphere microbial activity, changing root biomass and the dynamics of a wide range of soil C pools. Section Editor: A. Hodge     

On the assessment of root and soil respiration for soils of different textures: interactions with soil moisture contents and soil CO2 concentrations

Estimates of root and soil respiration are becoming increasingly important in agricultural and ecological research, but there is little understanding how soil texture and water content may affect these estimates. We examined the effects of soil texture on (i) estimated rates of root and soil respiration and (ii) soil CO₂ concentrations, during cycles of soil wetting and drying in the citrus rootstock, Volkamer lemon (Citrus volkameriana Tan. and Pasq.). Plants were grown in soil columns filled with three different soil mixtures varying in their sand, silt and clay content. Root and soil respiration rates, soil water content, plant water uptake and soil CO₂ concentrations were measured and dynamic relationships among these variables were developed for each soil texture treatment. We found that although the different soil textures differed in their plant-soil water relations characteristics, plant growth was only slightly affected. Root and soil respiration rates were similar under most soil moisture conditions for soils varying widely in percentages of sand, silt and clay. Only following irrigation did CO₂ efflux from the soil surface vary among soils. That is, efflux of CO₂ from the soil surface was much more restricted after watering (therefore rendering any respiration measurements inaccurate) in finer textured soils than in sandy soils because of reduced porosity in the finer textured soils. Accordingly, CO₂ reached and maintained the highest concentrations in finer textured soils (> 40 mmol CO₂ mol⁻¹). This study revealed that changes in soil moisture can affect interpretations of root and soil measurements based on CO₂ efflux, particularly in fine textured soils. The implications of the present findings for field soil CO₂ flux measurements are discussed. This revised version was published online in June 2006 with corrections to the Cover Date.     

A comparison of field methods for measuring soil carbon dioxide evolution: Experiments and simulation

Three widely used methods for measuring total soil CO₂ evolution are evaluated, including the dynamic CO₂ absorption method, the static CO₂ absorption method and the closed chamber method. The study covers laboratory experiments. numerical experiments with a simulation model and field measurements. The results are used to perform an error analysis. The aim of this error analysis is to indicate the impact of each method on the CO₂ dynamics during the measurement, and to select the most suitable method for frequent field usage.Laboratory experiments and simulation results show that the dynamic CO₂ absorption method has the potential to absorb all CO₂ evolving at the soil surface. The results also prove that the method has only a minor impact on the CO₂ concentration-depth gradient and the CO₂ efflux. The static CO₂ absorption method underestimates the soil CO₂ evolution, because the absorption velocity is too low, due to slow diffusion processes. Measurements with the closed-chamber method are based on an increasing concentration with time under a closed cover. However, the accumulation of gas alters the concentration gradient in the soil profile and thus causes a rapidly decreasing efflux during the measurement. A commonly used mathematical procedure, which corrects for the altered concentration gradient, does not yield the exact surface efflux, because the effect of increasing storage in the soil profile is not incorporated. Field measurements of CO₂ evolution, using the closed-chamber method and the dynamic CO₂ absorption method confirm the trends that have been predicted by the simulation model. The results of this study indicate that the dynamic CO₂ absorption method is accurate. As it is cheap and simple, it is suitable for the study of temporal and spatial dynamics of CO₂ evolution from the soil.     

Examination of the method for measuring soil respiration in cultivated land: Effect of carbon dioxide concentration on soil respiration

An acceleration of soil respiration with decreasing CO₂ concentration was suggested in the field measurements. The result supporrs that obtained in laboratory experiments in our previous study. The CO₂ concentrations in a chamber of the alkali absorption method (the AA-method) were about 150–250 parts/10⁶ lower than that in the atmosphere (about 350 parts/10⁶), while those observed in the open-flow IRGA method (the OF-method) were nearly equal to the soil surface CO₂ levels. The AA-method at such low CO₂ levels in the chamber appears to overestimate the soil respiration. Our results showed that the rates obtained by the AA-method were about twice as large as those by the OF-method in field and laboratory measurements. This finding has important consequences with respect to the validity of the existing data obtained by the AA-method and the estimation of changes in the terrestrial carbon flow with elevated CO₂     

Indirect partitioning of soil respiration in a series of evergreen forest ecosystems

A simple estimation of heterotrophic respiration can be obtained analytically as the y-intercept of the linear regression between soil-surface CO₂ efflux and root biomass. In the present study, a development of this indirect methodology is presented by taking into consideration both the temporal variation and the spatial heterogeneity of heterotrophic respiration. For this purpose, soil CO₂ efflux, soil carbon content and main stand characteristics were estimated in seven evergreen forest ecosystems along an elevation gradient ranging from 250 to 1740 m. For each site and for each sampling date the measured soil CO₂ efflux (R _S) was predicted with the model R _S = a × S _C + b × R _D ± ε, where S _C is soil carbon content per unit area to a depth of 30 cm and R _D is the root density of the 2–5 mm root class. Regressions with statistically significant a and b coefficients allowed the indirect separation of the two components of soil CO₂ efflux. Considering that the different sampling dates were characterized by different soil temperature, it was possible to investigate the temporal and thermal dependency of autotrophic and heterotrophic respiration. It was estimated that annual autotrophic respiration accounts for 16–58% of total soil CO₂ efflux in the seven different evergreen ecosystems. In addition, our observations show a decrease of annual autotrophic respiration at increasing availability of soil nitrogen. Section Editor: A. Hodge     

Estimating respiration of roots in soil: Interactions with soil CO2, soil temperature and soil water content

Little information is available on the variability of the dynamics of the actual and observed root respiration rate in relation to abiotic factors. In this study, we describe I) interactions between soil CO₂ concentration, temperature, soil water content and root respiration, and II) the effect of short-term fluctuations of these three environmental factors on the relation between actual and observed root respiration rates. We designed an automated, open, gas-exchange system that allows continuous measurements on 12 chambers with intact roots in soil. By using three distinct chamber designs with each a different path for the air flow, we were able to measure root respiration over a 50-fold range of soil CO₂ concentrations (400 to 25000 ppm) and to separate the effect of irrigation on observed vs. actual root respiration rate. All respiration measurements were made on one-year-old citrus seedlings in sterilized sandy soil with minimal organic material.Root respiration was strongly affected by diurnal fluctuations in temperature (Q₁₀ = 2), which agrees well with the literature. In contrast to earlier findings for Douglas-fir (Qi et al., 1994), root respiration rates of citrus were not affected by soil CO₂ concentrations (400 to 25000 ppm CO₂; pH around 6). Soil CO₂ was strongly affected by soil water content but not by respiration measurements, unless the air flow for root respiration measurements was directed through the soil. The latter method of measuring root respiration reduced soil CO₂ concentration to that of incoming air. Irrigation caused a temporary reduction in CO₂ diffusion, decreasing the observed respiration rates obtained by techniques that depended on diffusion. This apparent drop in respiration rate did not occur if the air flow was directed through the soil. Our dynamic data are used to indicate the optimal method of measuring root respiration in soil, in relation to the objectives and limitations of the experimental conditions.     

Evaluation of soil respiration and soil CO2 concentration in a lowland moist forest in Panama

Soil gas exchange was investigated in a lowland moist forest in Panama. Soil water table level and soil redox potentials indicate that the soils are not waterlogged. Substantial microspatial variation exists for soil respiration and soil CO₂ concentration. During the rainy season, soil CO₂ at 40 cm below the surface accumulates to 2.3%–4.6% and is correlated with rainfall during the previous two weeks. Temporal changes in soil CO₂ are rapid, large and share similar trends between sampling points. Possible effects of soil CO₂ changes on plant growth or phenology are discussed.     

Decomposition of tree leaf litters grown under elevated CO2: Effect of litter quality

Ash (Fraxinus excelsior L.), birch (Betula pubescens Ehrh.), sycamore (Acer pseudoplatanus L.) and Sitka spruce (Picea sitchensis (Bong.) Carr.) leaf litters were monitored for decomposition rates and nutrient release in a laboratory microcosm experiment. Litters were derived from solar domes where plants had been exposed to two different CO₂ regimes: ambient (350 L L^-1 CO₂) and enriched (600 L L^-1 CO₂).Elevated CO₂ significantly affected some of the major litter quality parameters, with lower N, higher lignin concentrations and higher ratios of C/N and lignin/N for litters derived from enriched CO₂. Respiration rates of the deciduous species were significantly decreased for litters grown under elevated CO₂, and reductions in mass loss at the end of the experiment were generally observed in litters derived from the 600 ppm CO₂ treatment. Nutrient mineralization, dissolved organic carbon, and pH in microcosm leachates did not differ significantly between the two CO₂ treatments for any of the species studied. Litter quality parameters were examined for correlations with cumulative respiration and decomposition rates: N concentration, C/N and lignin/N ratios showed the highest correlations, with differences between litter types. The results indicate that higher C storage will occur in soil as a consequence of litter quality changes resulting from higher atmospheric concentrations of CO₂.Abbreviations CHO soluble carbohydrates - DOC dissolved organic carbon - HCel holocellulose - WTREM weight remaining     

土壤CO2浓度的动态观测、模拟和应用

土壤CO₂浓度不仅是地上、地下生物活动的反映,其变化对未来大气CO₂浓度和气候变化也有重要影响.本文综述了国内外土壤CO₂浓度的原位测定方法及其优缺点,分析了不同时(昼夜、几天、季节、年际)空(剖面、立地、景观)尺度上土壤CO₂浓度的变化规律和影响因素,概括了现有土壤CO₂浓度的模拟模型和发展态势,并总结了土壤CO₂浓度梯度法在土壤呼吸研究中的应用和限制因素.最后展望了未来有待研究的4个领域：1)研发适于恶劣土壤环境(如淹水、石质土)的土壤CO₂气体采集、测定技术;2)探讨土壤CO₂浓度对天气变化的响应及其调控机理;3)加强土壤CO₂浓度空间异质性的研究;4)扩大通量梯度法在热带、亚热带土壤呼吸测定中的应用.     

大气CO2浓度升高对春玉米土壤呼吸的影响

为探讨春玉米不同生育期土壤呼吸速率对大气CO₂浓度升高的响应,以黄土高原旱作春玉米为研究对象,通过改进的开顶式气室（OTC）模拟大气CO₂浓度升高的环境,在田间条件下设置自然大气CO₂浓度（CK）、OTC对照（OTC,CO₂浓度同CK）与CO₂浓度升高（OTC+CO₂,OTC系统自动控制CO₂浓度700 μmol/mol）3种处理。研究了旱区覆膜高产栽培春玉米播前（V0）、六叶期（V6）、九叶期（V9）、吐丝期（R1）、乳熟期（R3）、蜡熟期（R5）及完熟期（R6）土壤呼吸速率对大气CO₂浓度升高的响应特征,以及大气CO₂浓度升高对土壤呼吸速率的温度与水分效应的影响。研究发现,OTC+CO₂处理土壤呼吸速率,与CK相比,在R3和R5期分别增加43%、104%（P<0.05）,与OTC相比,R3和R5期分别提升了63%、109%（P<0.05）;OTC处理与CK相比,在整个生育期对土壤呼吸影响不显著;3种处理条件下,土壤温度和水分随生育期变化趋势基本一致,土壤呼吸速率与土壤温度和水分分别呈指数相关和抛物线型相关;结果表明：大气CO₂浓度升高对土壤呼吸的影响因生育期而异,土壤温度和土壤水分是影响旱地农田土壤呼吸的重要因素,CO₂浓度升高会使土壤呼吸温度效应值（Q₁₀）降低,土壤呼吸对土壤水分响应的阈值提高。     

Non-phototrophic CO 2 fixation by soil microorganisms

Although soils are generally known to be a net source of CO₂ due to microbial respiration, CO₂ fixation may also be an important process. The non-phototrophic fixation of CO₂ was investigated in a tracer experiment with ¹⁴CO₂ in order to obtain information about the extent and the mechanisms of this process. Soils were incubated for up to 91 days in the dark. In three independent incubation experiments, a significant transfer of radioactivity from ¹⁴CO₂ to soil organic matter was observed. The process was related to microbial activity and could be enhanced by the addition of readily available substrates such as acetate. CO₂ fixation exhibited biphasic kinetics and was linearly related to respiration during the first phase of incubation (about 20–40 days). The fixation amounted to 3–5% of the net respiration. After this phase, the CO₂ fixation decreased to 1–2% of the respiration. The amount of carbon fixed by an agricultural soil corresponded to 0.05% of the organic carbon present in the soil at the beginning of the experiment, and virtually all of the fixed CO₂ was converted to organic compounds. Many autotrophic and heterotrophic biochemical processes result in the fixation of CO₂. However, the enhancement of the fixation by addition of readily available substrates and the linear correlation with respiration suggested that the process is mainly driven by aerobic heterotrophic microorganisms. We conclude that heterotrophic CO₂ fixation represents a significant factor of microbial activity in soils.     

The effect of plant material grown under elevated CO2 on soil respiratory activity

The biodegradability of aerial material from a C4 plant, sorghum grown under ambient (345 µmol mol^–1) and elevated (700 µmol mol^–1) atmospheric CO₂ concentrations were compared by measuring soil respiratory activity. Initial daily respiratory activity (measured over 10 h per day) increased four fold from 110 to 440 cm³ CO₂ 100g dry weight soil^–1 in soils amended with sorghum grown under either elevated or ambient CO₂. Although soil respiratory activity decreased over the following 30 days, respiration remained significantly higher (t-test;p>0.05) in soils amended with sorghum grown under elevated CO₂ concentrations. Analysis of the plant material revealed no significant differences in C:N ratios between sorghum grown under elevated or ambient CO₂. The reason for the differences in soil respiratory activity have yet to be elucidated. However if this trend is repeated in natural ecosystems, this may have important implications for C and N cycling.     

Changes in soil CO2 and O2 concentrations when radiata pine is grown in competition with pasture or weeds and possible feedbacks with radiata pine root growth and respiration

This study examined the reciprocal effects of growing ryegrass, lotus and other weed species in competition with radiata pine on soil CO₂ and O₂ concentrations and on the growth and root respiration of the radiata pine. Soil O₂ concentrations decreased and soil CO₂ concentrations increased with increasing soil depth. Radiata pine plus competing species slightly reduced soil O₂ concentrations and markedly increased soil CO₂ concentrations (up to 40 mmol mol⁻¹) compared with radiata pine alone. The dry weights of shoots and roots, and the root respiration rates of radiata pine grown with competing vegetation were much less than those for radiata pine alone. This probably was not solely caused by competition for nutrients water or light since adequate water and nutrients were supplied to all treatments and the radiata pine overtopped the competing vegetation. When radiata pine roots were raised in NaHCO₃ solutions equivalent to a range of CO₂ concentrations, succinate dehydrogenase activity (a metabolic indicator of mitochondrial respiration) and elongation rates of roots decreased as CO₂ concentrations increased from 0 to 40 mmol mol⁻¹. This suggests that the elevated CO₂ concentrations found in the experiments in soil was the cause, at least in part, of the reduced growth of radiata pine in competition with other species. This revised version was published online in June 2006 with corrections to the Cover Date.     

陆地生态系统土壤CO2排放对模拟增温的响应特征及影响因素

全球变暖已经成为不争的事实,陆地生态系统碳循环的研究受到了各界广泛关注,是当前全球变化研究中的重点。土壤CO₂排放是陆地生态系统与大气间二氧化碳交换的最大通量之一,当前陆地生态系统中土壤CO₂排放如何响应全球气候变暖及其影响因素仍不清楚,限制了对土壤碳循环过程及影响机制的深入认识。旨在明确全球变暖背景下陆地生态系统中土壤CO₂排放格局及影响因素。基于Web of Science、PubMed和中国知网等中英文期刊数据库,充分收集全球范围内的相关野外试验文献81篇,提取出65个研究位置和213组相关研究数据,采用Meta分析方法探讨陆地生态系统土壤CO₂排放对增温的响应特征,分析其与海拔、气候、土壤含水量、容重(BD)、pH、全氮(TN)和土壤有机碳(SOC)的相关关系。结果表明:陆地生态系统中土壤CO₂排放对增温整体有显著的正向响应,在农、林、草生态系统中,增温使土壤CO₂排放分别显著增加13.1%、18.0%、5.9% (P<0.05),森林生态系统对增温响应的正效应最强烈;增温能在短时期内促进土壤呼吸,但随着增温持续时间增加,土壤呼吸对温度的敏感性会降低,对温度变化产生适应性,从而使其对增温的响应能力减弱;响应特征受到环境因子、土壤特性以及其他试验条件等的影响,绝大多数条件下对增温表现出显著的正响应特征,不同影响因子之间共同作用、相互影响。增温通常能够改变植物生物量、土壤养分含量及微生物数量和活性,从而影响到植被根际呼吸和土壤呼吸速率。相关分析表明,海拔对土壤CO₂排放有显著负向影响,而年均气温、年均降水量、土壤含水量和仪器嵌入土壤深度则对土壤CO₂排放产生显著正向影响。这些结果对于理解全球土壤CO₂排放的时空变化格局有重要意义,也为准确评价全球变暖背景下土壤碳汇功能及其持续性提供理论依据。     

Diurnal cycle of carbon isotope ratio in soil CO2 in various ecosystems

Our investigations of diurnal variations of the ¹³C/¹²C ratio and CO₂ content in soil air were carried out in three environments during periods of high biosphere activity. It has been observed that diurnal variation of CO₂ concentration is negatively correlated ¹³. Particularly great variations occurred at shallow soil depths (10–30 cm) when the plant cover activity was high while the soil temperature was rather low. Under such conditions the ¹³ variations had the magnitude of 4, while the CO₂ concentration varied more than doubly. The maximum of the ¹³C/¹²C ratlo and the minimum of the CO₂ concentration in a cultivated field with winter wheat took place in the afternoon, whereas in deciduous forest similar patterns were observed at dawn. In these cases soil temperatures at 10 cm depths varied less than 2°C. Hence, under wheat the variation in root respiration rate seem to be the main reason of the recorded varations. In an uncultivated grass-field during the hottest period in summer we did not measure any distinct variations of CO₂ properties in spite of the fact that soil temperature varied up to 5°C. This might be due to dominant microbial respiration at the high soil temperature, which exceeded 20°C.     

杉木人工林不同深度土壤CO2通量

土壤CO₂通量具有明显的时间和空间变异性。土壤温度和含水量是影响土壤CO₂通量的重要因素,同时,不同深度的土壤CO₂通量对温度和含水量变化的响应差异较大,因此,研究土壤CO₂通量和影响因素随土壤深度的变化,对于准确评估土壤碳排放具有重要意义。选择福建三明杉木人工林(Cunninghamia lanceolata)作为研究对象,利用非散射红外CO₂浓度探头和Li-8100开路式土壤碳通量系统,并使用Fick扩散法计算了0-60cm深度土壤CO₂的通量,结果表明:(1)5种扩散模型计算的表层(5cm)CO₂通量与Li-8100测量结果均具有显著相关性(P<0.01),Moldrup气体扩散模型计算结果较好。(2)土壤CO₂浓度随深度的增加而升高,但60cm深度以下土壤CO₂浓度开始降低;不同深度土壤CO₂浓度的日变化均呈现单峰型;0-60cm土壤CO₂通量日通量均值变化范围为0.54-2.17μmol m^-2 s^-1;(3)指数拟合分析显示,5、10cm和60cm深度处土壤CO₂通量与温度具有显著相关性,Q₁₀值分别为1.35、2.01和4.95。不同深度土壤含水量与CO₂通量的相关性不显著。     

Effect of carbon dioxide concentration on microbial respiration in soil

In order to assess the validity of conventional methods for measuring CO₂ flux from soil, the relationship between soil microbial respiration and ambient CO₂ concentration was studied using an open-flow infra-red gas analyser (IRGA) method. Andosol from an upland field in central Japan was used as a soil sample. Soil microbial respiration activity was depressed with the increase of CO₂ concentration in ventilated air from 0 to 1000 ppmv. At 1000 ppmv, the respiration rate was less than half of that at 0 ppmv. Thus, it is likely that soil respiration rate is overestimated by the alkali absorption method, because CO₂ concentration in the absorption chamber is much lower than the normal level. Metabolic responses to CO₂ concentration were different among groups of soil microorganisms. The bacteria actinomycetes group cultivated on agar medium showed a more sensitive response to the CO₂ concentration than the filamentous fungi group.     

Effect of elevated atmospheric CO2 concentration on soil and root respiration in winter wheat by using a respiration partitioning chamber

Soil respiration in a cropland is the sum of heterotrophic (mainly microorganisms) and autotrophic (root) respiration. The contribution of both these types to soil respiration needs to be understood to evaluate the effects of environmental change on soil carbon cycling and sequestration. In this paper, the effects of free-air CO₂ enrichment (FACE) on hetero- and autotrophic respiration in a wheat field were differentiated and evaluated by a novel split-root growth and gas collection system. Elevated atmospheric pCO₂ of approximately 200 μmol mol⁻¹ above the ambient pCO₂ significantly increased soil respiration by 15.1 and 14.8% at high nitrogen (HN) and low nitrogen (LN) application rates, respectively. The effect of elevated atmospheric pCO₂ on root respiration was not consistent across the wheat growth stages. Elevated pCO₂ significantly increased and decreased root respiration at the booting-heading stage (middle stage) and the late-filling stage (late stage), respectively, in HN and LN treatments; however, no significant effect was found at the jointing stage (early stage). Thus, the effect of increased pCO₂ on cumulative root respiration for the entire wheat growing season was not significant. Cumulative root respiration accounted for approximately 25–30% of cumulative soil respiration in the entire wheat growing season. Consequently, cumulative microbial respiration (soil respiration minus root respiration) increased by 22.5 and 21.1% due to elevated pCO₂ in HN and LN, respectively. High nitrogen application significantly increased root respiration at the late stage under both elevated pCO₂ and ambient pCO₂; however, no significant effects were found on cumulative soil respiration, root respiration, and microbial respiration. These findings suggest that heterotrophic respiration, which is influenced by increased substrate supplies from the plant to the soil, is the key process to determine C emission from agro-ecosystems with regard to future scenarios of enriched pCO₂.