Rhizosphere priming effect increases the temperature sensitivity of soil organic matter decomposition

The temperature sensitivity of soil organic matter (SOM) decomposition has been a crucial topic in global change research, yet remains highly uncertain. One of the contributing factors to this uncertainty is the lack of understanding about the role of rhizosphere priming effect (RPE) in shaping the temperature sensitivity. Using a novel continuous ¹³C‐labeling method, we investigated the temperature sensitivity of RPE and its impact on the temperature sensitivity of SOM decomposition. We observed an overall positive RPE. The SOM decomposition rates in the planted treatments increased 17–163% above the unplanted treatments in three growth chamber experiments including two plant species, two growth stages, and two warming methods. More importantly, warming by 5 °C increased RPE up to threefold, hence, the overall temperature sensitivity of SOM decomposition was consistently enhanced (Q₁₀ values increased 0.3–0.9) by the presence of active rhizosphere. In addition, the proportional contribution of SOM decomposition to total soil respiration was increased by soil warming, implying a higher temperature sensitivity of SOM decomposition than that of autotrophic respiration. Our results, for the first time, clearly demonstrated that root–soil interactions play a crucial role in shaping the temperature sensitivity of SOM decomposition. Caution is required for interpretation of any previously determined temperature sensitivity of SOM decomposition that omitted rhizosphere effects using either soil incubation or field root‐exclusion. More attention should be paid to RPE in future experimental and modeling studies of SOM decomposition.     

The temperature dependence of organic matter decomposition: seasonal temperature variations turn a sharp short‐term temperature response into a more moderate annually averaged response

The temperature dependence of organic matter decomposition is a critically important determinant of any long‐term changes of soil‐carbon stocks in response to global warming. Because of practical experimental constraints, most knowledge of this temperature dependence is based on short‐term studies. These studies generally show a strong temperature dependence of organic matter decomposition. At the same time, many modelling studies, especially global studies, or studies that investigate the effects of climate change, use longer time steps, such as annual. It is investigated here to what extent the use of short‐term temperature dependencies are appropriate, or how they may need to be modified, for application over longer time steps. The work indicated that for global applications, it is critically important to explicitly consider seasonal temperature variations. Across the globe, observed annual mean temperature and the annual temperature range are negatively correlated. Inclusion of this correlation means that the strong short‐term temperature dependence becomes much weaker when data are expressed as annual averages for the temperatures experienced across the globe. For short‐term responses, the temperature dependence of organic matter decomposition is greater at low than high temperature and deviates strongly from an assumption of a constant Q₁₀ across temperature. For annually averaged values, this pattern also weakens, and temperature dependencies change only slightly with temperature. Using short time steps for simulations leads to the expectation of more positive changes (sequestration) in soil carbon especially for cold regions of the globe than would be predicted for simulations at annual time steps without explicit consideration of seasonal temperature variations. These considerations help to reconcile some of the apparent differences in temperature dependencies obtained by different workers using different approaches.     

Drought‐resistant fungi control soil organic matter decomposition and its response to temperature

Microbial‐mediated decomposition of soil organic matter (SOM) ultimately makes a considerable contribution to soil respiration, which is typically the main source of CO₂ arising from terrestrial ecosystems. Despite this central role in the decomposition of SOM, few studies have been conducted on how climate change may affect the soil microbial community and, furthermore, on how possible climate‐change induced alterations in the ecology of microbial communities may affect soil CO₂ emissions. Here we present the results of a seasonal study on soil microbial community structure, SOM decomposition and its temperature sensitivity in two representative Mediterranean ecosystems where precipitation/throughfall exclusion has taken place during the last 10 years. Bacterial and fungal diversity was estimated using the terminal restriction fragment length polymorphism technique. Our results show that fungal diversity was less sensitive to seasonal changes in moisture, temperature and plant activity than bacterial diversity. On the other hand, fungal communities showed the ability to dynamically adapt throughout the seasons. Fungi also coped better with the 10 years of precipitation/throughfall exclusion compared with bacteria. The high resistance of fungal diversity to changes with respect to bacteria may open the controversy as to whether future ‘drier conditions’ for Mediterranean regions might favor fungal dominated microbial communities. Finally, our results indicate that the fungal community exerted a strong influence over the temporal and spatial variability of SOM decomposition and its sensitivity to temperature. The results, therefore, highlight the important role of fungi in the decomposition of terrestrial SOM, especially under the harsh environmental conditions of Mediterranean ecosystems, for which models predict even drier conditions in the future.     

Effects of three years of soil warming and shading on the rate of soil respiration: substrate availability and not thermal acclimation mediates observed response

In a number of recent field studies, the positive response of soil respiration to warming has been shown to decline over time. The two main differing hypotheses proposed to explain these results are: (1) soil microbial respiration acclimates to the increased temperature, and (2) substrate availability within the soil decreases with warming so reducing the rate of soil respiration. To investigate the relative merits of these two hypotheses, soil samples (both intact cores and sieved samples) from a 3-year grassland soil-warming and shading experiment were incubated for 4 weeks at three different temperatures under constant laboratory conditions. We tested the hypothesis that sieving the soils would reduce differences in substrate availability between warmed and control plot samples and would therefore result in similar respiration rates if microbial activity had not acclimated to soil warming. In addition, to further test the effect of substrate availability, we compared the respiration rates of soils taken from shaded and unshaded plots. Both soil warming and shading significantly reduced respiration rates in the intact cores, especially under higher incubation temperatures. However, sieving the soil greatly reduced these differences suggesting that substrate availability, and not microbial acclimation to the higher temperatures, played the dominant role in determining the response of heterotrophic soil respiration to warming. The effect of shading appeared to be mediated by reduced plant productivity affecting substrate availability within the soil and hence microbial activity. Given the lack of evidence for thermal acclimation of microbial respiration, there remains the potential for prolonged carbon losses from soils in response to warming.     

Temperature sensitivity and substrate quality in soil organic matter decomposition: results of an incubation study with three substrates

Kinetic theory suggests that the temperature sensitivity of decomposition of soil organic matter should increase with increasing recalcitrance. This ‘temperature–quality hypothesis’ was tested in a laboratory experiment. Microcosms with wheat straw, spruce needle litter and mor humus were initially placed at 5, 15 and 25 °C until the same cumulative amount of CO₂ had been respired. Thereafter, microcosms from each single temperature were moved to a final set of incubation temperatures of 5, 15 and 25 °C. Straw decomposed faster than needle litter at 25 and 15 °C, but slower than needle litter at 5 °C, and showed a higher temperature sensitivity (expressed as Q₁₀) than needle litter at low temperatures. When moved to the same temperature, needle litter initially incubated at 5 and 15 °C had significantly higher respiration rates in the final incubation than litters initially placed at 25 °C. Mor humus placed at equal temperatures during the initial and final incubations had higher cumulative respiration during the final incubation than humus experiencing a shift in temperature, both up‐ and downwards. These results indicate that other factors than substrate quality are needed to fully explain the temperature dependence. In agreement with the hypothesis, Q₁₀ was always higher for the temperature step between 5 and 15 °C than between 15 and 25 °C. Also in agreement with the temperature–quality hypothesis, Q₁₀ significantly increased with increasing degree of decomposition in five out of the six constant temperature treatments with needle litter and mor humus. Q₁₀s for substrates moved between temperatures tended to be higher than for substrates remaining at the initial temperature and an upward shift in temperature increased Q₁₀ more than a downward shift. This study largely supports the temperature–quality hypothesis. However, other factors like acclimation and synthesis of recalcitrant compounds can modify the temperature response.     

Transplantation of organic surface horizons of boreal soils into warmer regions alters microbiology but not the temperature sensitivity of decomposition

Changes in soil carbon, the largest terrestrial carbon pool, are critical for the global carbon cycle, atmospheric CO₂ levels and climate. Climate warming is predicted to be most pronounced in the northern regions and therefore the large soil carbon pool residing in boreal forests will be subject to larger global warming impact than soil carbon pools in the temperate or the tropical forest. A major uncertainty in current estimates of the terrestrial carbon balance is related to decomposition of soil organic matter (SOM). We hypothesized that when soils are exposed to warmer climate the structure of the ground vegetation will change much more rapidly than the dominant tree species. This change will alter the quality and amount of litter input to the soil and induce changes in microbial communities, thus possibly altering the temperature sensitivity of SOM decomposition. We transferred organic surface soil sections from the northern borders of the boreal forest zone to corresponding forest sites in the southern borders of the boreal forest zone and studied the effects of warmer climate after an adaptation period of 2 years. The results showed that initially ground vegetation and soil microbial community structure and community functions were different in northern and southern forest sites and that 2 years of exposure to warmer climate was long enough to cause changes in these ecological indicators. The rate of SOM decomposition was approximately equally sensitive to temperature irrespective of changes in vegetation or microbial communities in the studied forest sites. However, as temperature sensitivity of the decomposition increases with decreasing temperature regime, the proportional increase in the decomposition rate in northern latitudes could lead to significant carbon losses from the soils.     

Effects of soil phosphorus availability,temperature and moisture on soil respiration in Eucalyptus pauciflora forest

Rates of soil respiration (CO₂ efflux) were measured for a year in a mature Eucalyptus pauciflora forest in unfertilized and phosphorus-fertilized plots. Soil CO₂ efflux showed a distinct seasonal trend, and average daily rates ranged from 124 to 574 mg CO₂ m^–2 hr^–1. Temperature and moisture are the main variables that cause variation in soil CO₂ efflux; hence their effects were investigated over a year so as to then differentiate the treatment effect of phosphorus (P) nutrition.Soil temperature had the greatest effect on CO₂ efflux and exhibited a highly significant logarithmic relationship (r² = 0.81). Periods of low soil and litter moisture occurred during summer when temperatures were greater than 10 °C, and this resulted in depression of soil CO₂ efflux. During winter, when temperatures were less than 10 °C, soil and litter moisture were consistently high and thus their variation had little effect on soil CO₂ efflux. A multiple regression model including soil temperature, and soil and litter moisture accounted for 97% of the variance in rates of CO₂ efflux, and thus can be used to predict soil CO₂ efflux at this site with high accuracy. Total annual efflux of carbon from soil was estimated to be 7.11 t C ha^–1 yr^–1. The model was used to predict changes in this annual flux if temperature and moisture conditions were altered. The extent to which coefficients of the model differ among sites and forest types requires testing.Increased soil P availability resulted in a large increase in stem growth of trees but a reduction in the rate of soil CO₂ efflux by approximately 8%. This reduction is suggested to be due to lower root activity resulting from reduced allocation of assimilate belowground. Root activity changed when P was added to microsites within plots, and via the whole tree root system at the plot level. These relationships of belowground carbon fluxes with temperature, moisture and nutrient availability provide essential information for understanding and predicting potential changes in forest ecosystems in response to land use management or climate change.     

土壤呼吸温度敏感性的影响因素和不确定性

土壤呼吸是陆地生态系统碳循环的重要环节之一, 其对温度升高的敏感程度在很大程度上决定着全球气候变化与碳循环之间的反馈关系。为了深刻理解地下生态过程对气候变化的响应和适应,本文综述了土壤呼吸温度敏感性（Q10）的影响因子及其内在机制,并分析了当前研究存在的不确定性。土壤生物、底物质量和底物供应显著调控着土壤呼吸的Q10值,但研究结论仍然有很大差异。温度和水分等环境因子则通过对土壤生物和底物的影响而作用于土壤呼吸的温度敏感性,一般情况下,随着温度的升高,土壤呼吸的Q10值下降;水分过高或过低时Q10值降低。另外本文从土壤温度测定深度、时空尺度、土壤呼吸不同组分温度敏感性差异、激发效应以及采用方法的不同等几方面分析了温度敏感性研究存在的不确定性。并在此基础上, 指出了未来拟重点加强的研究方向:（1）土壤呼吸不同组分温度敏感性差异的机理;（2）底物质量和底物供应对温度敏感性的交互影响;（3）生物因子对土壤呼吸温度敏感性的影响。     

Sensitivity of organic matter decomposition to warming varies with its quality

The relationship between organic matter (OM) lability and temperature sensitivity is disputed, with recent observations suggesting that responses of relatively more resistant OM to increased temperature could be greater than, equivalent to, or less than responses of relatively more labile OM. This lack of clear understanding limits the ability to forecast carbon (C) cycle responses to temperature changes. Here, we derive a novel approach (denoted Q_10?q) that accounts for changes in OM quality during decomposition and use it to analyze data from three independent sources. Results from new laboratory soil incubations (labile Q_10?q=2.1 ± 0.2; more resistant Q_10?q=3.8 ± 0.3) and reanalysis of data from other soil incubations reported in the literature (labile Q_10?q=2.3; more resistant Q_10?q=3.3) demonstrate that temperature sensitivity of soil OM decomposition increases with decreasing soil OM lability. Analysis of data from a cross‐site, field litter bag decomposition study (labile Q_10?q=3.3 ± 0.2; resistant Q_10?q=4.9 ± 0.2) shows that litter OM follows the same pattern, with greater temperature sensitivity for more resistant litter OM. Furthermore, the initial response of cultivated soils, presumably containing less labile soil OM (Q_10?q=2.4 ± 0.3) was greater than that for undisturbed grassland soils (Q_10?q=1.7 ± 0.1). Soil C losses estimated using this approach will differ from previous estimates as a function of the magnitude of the temperature increase and the proportion of whole soil OM comprised of compounds sensitive to temperature over that temperature range. It is likely that increased temperature has already prompted release of significant amounts of C to the atmosphere as CO₂. Our results indicate that future losses of litter and soil C may be even greater than previously supposed.     

The dependence of respiration on photosynthetic substrate supply and temperature: integrating leaf, soil and ecosystem measurements

Interactions between photosynthetic substrate supply and temperature in determining the rate of three respiration components (leaf, belowground and ecosystem respiration) were investigated within three environmentally controlled, Populus deltoides forest bays at Biosphere 2, Arizona. Over 2 months, the atmospheric CO₂ concentration and air temperature were manipulated to test the following hypotheses: (1) the responses of the three respiration components to changes in the rate of photosynthesis would differ both in speed and magnitude; (2) the temperature sensitivity of leaf and belowground respiration would increase in response to a rise in substrate availability; and, (3) at the ecosystem level, the ratio of respiration to photosynthesis would be conserved despite week‐to‐week changes in temperature. All three respiration rates responded to the CO₂ concentration‐induced changes in photosynthesis. However, the proportional change in the rate of leaf respiration was more than twice that of belowground respiration and, when photosynthesis was reduced, was also more rapid. The results suggest that aboveground respiration plays a key role in the overall response of ecosystem respiration to short‐term changes in canopy photosynthesis. The short‐term temperature sensitivity of leaf respiration, measured within a single night, was found to be affected more by developmental conditions than photosynthetic substrate availability, as the Q₁₀ was lower in leaves that developed at high CO₂, irrespective of substrate availability. However, the temperature sensitivity of belowground respiration, calculated between periods of differing air temperature, appeared to be positively correlated with photosynthetic substrate availability. At the ecosystem level, respiration and photosynthesis were positively correlated but the relationship was affected by temperature; for a given rate of daytime photosynthesis, the rate of respiration the following night was greater at 25 than 20°C. This result suggests that net ecosystem exchange did not acclimate to temperature changes lasting up to 3 weeks. Overall, the results of this study demonstrate that the three respiration terms differ in their dependence on photosynthesis and that, short‐ and medium‐term changes in temperature may affect net carbon storage in terrestrial ecosystems.     

土地利用方式对土壤有机质的影响

通过对地带性常绿阔叶林、杉木人工林、农田、竹林等不同土地利用方式下土壤有机质总量、活性有机质及其组分的研究,发现土地利用方式对土壤有机质和活性有机质各组分的影响差异显著,其中阔叶林含量最高,杉木人工林低于阔叶林,竹林和农田最低。这些差别主要是由于凋落物的数量、质量以及各种管理措施不同所致。     

Microbial soil respiration and its dependency on carbon inputs, soil temperature and moisture

This experiment was designed to study three determinant factors in decomposition patterns of soil organic matter (SOM): temperature, water and carbon (C) inputs. The study combined field measurements with soil lab incubations and ends with a modelling framework based on the results obtained. Soil respiration was periodically measured at an oak savanna woodland and a ponderosa pine plantation. Intact soils cores were collected at both ecosystems, including soils with most labile C burnt off, soils with some labile C gone and soils with fresh inputs of labile C. Two treatments, dry‐field condition and field capacity, were applied to an incubation that lasted 111 days. Short‐term temperature changes were applied to the soils periodically to quantify temperature responses. This was done to prevent confounding results associated with different pools of C that would result by exposing treatments chronically to different temperature regimes. This paper discusses the role of the above‐defined environmental factors on the variability of soil C dynamics. At the seasonal scale, temperature and water were, respectively, the main limiting factors controlling soil CO₂ efflux for the ponderosa pine and the oak savanna ecosystems. Spatial and seasonal variations in plant activity (root respiration and exudates production) exerted a strong influence over the seasonal and spatial variation of soil metabolic activity. Mean residence times of bulk SOM were significantly lower at the Nitrogen (N)‐rich deciduous savanna than at the N‐limited evergreen dominated pine ecosystem. At shorter time scales (daily), SOM decomposition was controlled primarily by temperature during wet periods and by the combined effect of water and temperature during dry periods. Secondary control was provided by the presence/absence of plant derived C inputs (exudation). Further analyses of SOM decomposition suggest that factors such as changes in the decomposer community, stress‐induced changes in the metabolic activity of decomposers or SOM stabilization patterns remain unresolved, but should also be considered in future SOM decomposition studies. Observations and confounding factors associated with SOM decomposition patterns and its temperature sensitivity are summarized in the modeling framework.     

Analysing temperature response of decomposition of organic matter

In order to analyse temperature effects on decomposition of organic matter, we tested the following hypothesis: Can an Arrhenius type of equation with constant parameter values for the temperature response of decomposer growth rate adequately describe decomposition of organic matter or must some additional properties be made functions of temperature? Possible temperature effects were analysed by aggregating data in different ways from an experiment with ¹⁴C‐labelled wheat material incubated in the laboratory at different temperatures and with soil materials collected from seven coniferous forest stands in Europe. Our analysis shows that it is possible to let all the temperature dependence reside in the decomposer growth rate. The analysis also supports the use of an Arrhenius type of equation for the temperature response of decomposer growth rate but with the parameters specific for each soil, or at least a distinction between organic and mineral horizons seems necessary.     

Experimental evidence for the attenuating effect of SOM protection on temperature sensitivity of SOM decomposition

The ability to predict C cycle responses to temperature changes depends on the accurate representation of temperature sensitivity (Q₁₀) of soil organic matter (SOM) decomposition in C models for different C pools and soil depths. Theoretically, Q₁₀ of SOM decomposition is determined by SOM quality and availability (referred to here as SOM protection). Here, we focus on the role of SOM protection in attenuating the intrinsic, SOM quality dependent Q₁₀. To assess the separate effects of SOM quality and protection, we incubated topsoil and subsoil samples characterized by differences in SOM protection under optimum moisture conditions at 25 °C and 35 °C. Although lower SOM quality in the subsoil should lead to a higher Q₁₀ according to kinetic theory, we observed a much lower overall temperature response in subsoil compared with the topsoil. Q₁₀ values determined for respired SOM fractions of decreasing lability within the topsoil increased from 1.9 for the most labile to 3.8 for the least labile respired SOM, whereas corresponding Q₁₀ values for the subsoil did not show this trend (Q₁₀ between 1.4 and 0.9). These results indicate the existence of a limiting factor that attenuates the intrinsic effect of SOM quality on Q₁₀ in the subsoil. A parallel incubation experiment of ¹³C‐labeled plant material added to top‐ and subsoil showed that decomposition of an unprotected C substrate of equal quality responds similarly to temperature changes in top‐ and subsoil. This further confirms that the attenuating effect on Q₁₀ in the subsoil originates from SOM protection rather than from microbial properties or other nutrient limitations. In conclusion, we found experimental evidence that SOM protection can attenuate the intrinsic Q₁₀ of SOM decomposition.     

Variable temperature sensitivity of soil organic carbon in North American forests

We investigated mean residence time (MRT) for soil organic carbon (SOC) sampled from paired hardwood and pine forests located along a 22 °C mean annual temperature (MAT) gradient in North America. We used acid hydrolysis fractionation, radiocarbon analyses, long-term laboratory incubations (525-d), and a three-pool model to describe the size and kinetics of the acid insoluble C (AIC), active and slow SOC fractions in soil. We found that active SOC was 2 ± 0.2% (mean ± SE) of total SOC, with an MRT of 33 ± 6 days that decreased strongly with increasing MAT. In contrast, MRT for slow SOC and AIC (70 ± 6% and 27 ± 6% of total SOC, respectively) ranged from decades to thousands of years, and neither was significantly related to MAT. The accumulation of AIC (as a percent of total SOC) was greater in hardwood than pine stands (36% and 21%, respectively) although the MRT for AIC was longer in pine stands. Based on these results, we suggest that the responsiveness of most SOC decomposition in upland forests to global warming will be less than currently modeled, but any shifts in vegetation from hardwood to pine may alter the size and MRT of SOC fractions.     

森林类型对土壤有机质、微生物生物量及酶活性的影响

以澳大利亚南昆士兰州典型森林类型——湿地松、南洋杉和贝壳杉林为对象,开展土壤可溶性有机碳和氮(SOC和SON)、微生物生物量碳和氮(MBC和MBN),以及土壤酶活性的研究,剖析森林类型对土壤质量的影响.结果表明:不同林型土壤SOC、SON含量分别在552 ～1154 mg·kg-1和20.11～57.32mg·kg-1;MBC、MBN分别在42～149 mg·kg-1和7～35 mg·kg-1.MBC、MBN之间呈显著相关.土壤几丁质酶、酸性磷酸酶、碱性磷酸酶和β-葡萄糖苷酶的活性分别为2.96 ～7.63、16.5 ～29.6、0.79 ～ 3.42和3.71 ～9.93 μg ·g-1·h-1,亮氨酸氨肽酶活性为0.18～0.46 μg·g-1·d-1.不同林型土壤SOC含量,以及土壤几丁质酶和亮氨酸氨肽酶活性为湿地松林、南洋杉林、贝壳杉林依次降低;而SON含量为南洋杉林＞贝壳杉林＞湿地松林,且南洋杉林的SON含量显著(P＜0.05)高于湿地松林;MBC和MBN以及碱性磷酸酶活性为贝壳杉林＞湿地松林＞南洋杉林;酸性磷酸酶和β-葡萄糖苷酶活性为湿地松林＞贝壳杉林＞南洋杉林.在土壤生物代谢因子中,MBC、MBN、SON和亮氨酸氨肽酶对不同森林类型土壤影响较大.     

华西雨屏区苦竹人工林土壤呼吸各组分特征及其温度敏感性

通过在华西雨屏区苦竹(Pleioblastus amarus)人工林内建立固定样地、定期监测等方法,研究该人工林生态系统土壤呼吸各组分特征及其温度敏感性.结果表明:2010年2月-2011年1月,苦竹林平均土壤呼吸速率为1.13 μmol·m-2·s-1,仲夏最高,深冬最低;凋落物层、无根土壤和植物根系对苦竹林土壤呼吸的贡献率分别为30.9％、20.8％和48.3％,各呼吸组分的季节动态均与土壤总呼吸类似,并与温度和凋落量等因素相关;苦竹林土壤总呼吸(RST)、凋落物层CO2排放(RSL)、无根土壤CO2排放(RSS)和植物根系呼吸(RSR)的年碳排放量分别为4.27、1.32、0.87和2.08 MgC· hm-2 ·a-1;土壤总呼吸及其各组分与凋落量呈显著正线性相关,与土壤10 cm温度和气温均呈显著正指数相关;基于土壤温度计算的RST、RSL、RSS和RSR的Q10值分别为2.90、2.28、3.09和3.19,凋落物层CO2排放的温度敏感性显著低于总呼吸和其他各组分.